Breath Odors (Free)

Breath Odors

Nir Sterer • Mel Rosenberg
Breath Odors
Origin, Diagnosis, and Management
Authors
Dr. Nir Sterer, DMD, PhD
and
Prof. Mel Rosenberg, PhD
Department of Clinical
Microbiology and Immunology
Sackler Faculty of Medicine
Tel-Aviv University
Tel Aviv 69978
Israel
drsterer@gmail.com
dr.mel.rosenberg@gmail.com
melros@post.tau.ac.il
ISBN 978-3-642-19311-8 e-ISBN 978-3-642-19312-5

DOI 10.1007/978-3-642-19312-5
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Preface
Breath odors are a common and disturbing condition affecting some 25% of the adult
population. Caregivers (dentists, family practitioners, ENT specialists, gastroenterologists,
etc.) encounter patients with breath odor complaints in their daily practice. However, diag-
nosis and management of breath odors are barely taught in dental and medical faculties.
Academic research on breath odors dates back almost a century. During the 1960s,
Joseph Tonzetich (University of British Columbia) and colleagues introduced gas chroma-
tography techniques, and since then, continual growth has been seen in this field. The
wealth of scientific data that has accumulated warrants a concise textbook summarizing
the current status of breath research, and its implications for clinical diagnoses and man-
agement strategies. We hope that the current text will help fill this gap, that researchers,
students and clinicians will find it informative and helpful, and that the data presented here
will be shared in medical and dental curricula.
We are grateful to the many mentors, colleagues, students and technicians who have
contributed research and wisdom, and enriched us and the scientific community at large.
Specifically, we would like to thank Daniel van Steenberghe, the cofounder of the
International Society for Breath Odor Research (ISBOR), John Greenman and Walter
Loesche for their contribution to the understanding of the microbial aspects, Christopher
A.G. McCulloch and Avital Kozlovsky for their insight into the role of periodontal dis-
eases, Ilana Eli for her contribution to understanding the role of self-assessment, Israel
Kleinberg for his contribution on metabolic factors, Eugene Rosenberg for mentoring
(MR) and 30 years of fruitful scientific discussions, and Jacob Gabbay for his input into
sulfide testing and odor judge panels.
Tel Aviv, Israel N. Sterer and M. Rosenberg
v

Contents
1 Introduction............................................................................................................ 1
2 Breath Odors of Oral Origin (Oral Malodor)..................................................... 5

Oral Malodor and the Tongue................................................................................... 5
Oral Malodor, Gingival Health, and Periodontal Disease........................................ 10
Oral Malodor and Dental Restorations..................................................................... 14
Oral Malodor and Oral Dryness................................................................................ 14
References................................................................................................................. 15
3 Biochemical and Microbial Aspects of Oral Malodor Production.................... 19

The General Role of Bacteria in Breath Odors......................................................... 19
The Bacterial Origin of Oral Odors.......................................................................... 19
Metabolic Factors Affecting Malodor Production . ................................................. 20
Biochemical Aspects ............................................................................................... 21
Metabolism........................................................................................................... 21
Malodorous Volatile Organic Compounds (VOCs) in the Oral Cavity................ 24
Microbial Aspects..................................................................................................... 27
Malodor Producing Microorganisms.................................................................... 27
References................................................................................................................. 31
4 Odor Perception..................................................................................................... 35
Olfactory Psychophysics........................................................................................... 35
Odor Mixtures........................................................................................................... 36
Odor Perception and Odor Evaluation Panels.......................................................... 37
References................................................................................................................. 38
5 Breath Odors of Nasal and Pharyngeal Origin................................................... 41

Chronic Sinusitis....................................................................................................... 41
Chronic Caseous Tonsillitis...................................................................................... 42
Foreign Bodies.......................................................................................................... 43
Craniofacial Anomalies............................................................................................ 44
References................................................................................................................. 45
vii
viii Contents
6 Breath Odors and the Gastrointestinal Tract...................................................... 47

Gastroesophageal Reflux Disease (GERD).............................................................. 47
Helicobacter Pylori (Hp) Infection ......................................................................... 48
References................................................................................................................. 53
7 Other Sources of Breath Odors............................................................................ 55

References................................................................................................................. 57
8 Measurements of Breath Odors and Related Parameters................................. 59

Odor Judge Scoring.................................................................................................. 59
Instrumental Measuring of Malodor-Related Compounds....................................... 61
Gas Chromatography (GC)................................................................................... 61
Sulfide Monitor..................................................................................................... 62
Measuring Techniques of Malodor-Related Compounds......................................... 63
Biochemical Assays.................................................................................................. 63
BANA Test............................................................................................................ 63
b-Galactosidase Activity Assay............................................................................ 66
Cysteine Challenge................................................................................................... 67
Salivary Incubation Assays....................................................................................... 67
Microbial Assays...................................................................................................... 68
References................................................................................................................. 70
9 Breath Odor Diagnosis.......................................................................................... 73

Pre-appointment Instructions . ................................................................................. 73
Patient Interview....................................................................................................... 74
Examination.............................................................................................................. 74
Organoleptic Measurements................................................................................. 74
Oral VSC Quantification....................................................................................... 75
Examination of the Oral Cavity............................................................................ 75
Biochemical and Microbial Assays...................................................................... 76
References................................................................................................................. 76
10 Self-Assessment of Breath Odors......................................................................... 79

References................................................................................................................. 81
11 Breath Odors, Prevalence, Gender, and Age....................................................... 83

Prevalence................................................................................................................. 83
Gender ...................................................................................................................... 85
Age............................................................................................................................ 86
References................................................................................................................. 86
Contents ix
12 Psychological Aspects of Breath Odors................................................................ 89

Halitophobia.............................................................................................................. 89
Olfactory Reference Syndrome (ORS)..................................................................... 89
Back to Halitophobia................................................................................................ 90
References................................................................................................................. 93
13 Oral Malodor Management.................................................................................. 95

Mechanical Therapy................................................................................................. 95
Chemical Therapy..................................................................................................... 97
Professional Treatment............................................................................................. 102
References................................................................................................................. 105
14 History of Breath Odors........................................................................................ 109

Culture and Folklore................................................................................................. 109
Early Scientific and Medical Literature.................................................................... 111
Modern history.......................................................................................................... 112
References................................................................................................................. 114
15 Future Prospects.................................................................................................... 115

References................................................................................................................. 116
Index ............................................................................................................................ 117

Introduction
1
Breath odor is a common condition affecting those who have it, and those in their
proximity. Until the 1980s, most research was carried out at private companies (mainly
those producing mouthwash and those testing it), which tended to publish little and protect
as much of their “know how” as possible. There were only a few scientists working on this
subject in isolated university laboratories, often separated by thousands of kilometers.
However, the past two decades have seen this subject spawn a scientific community,
with a society (ISBOR, the International Society for Breath Odor Research), international
meetings (the ninth was recently held in Sau Paulo, Brazil) and a recently accredited inter-
national journal (The Journal of Breath Research, IOP Publishing). This growing body of
research has managed to shed light on some of the questions regarding this field while
other still remains open.
It is clear that the large majority (some 85–90%) of the cases of breath odors come from
the oral cavity itself. Other sources may include nasopharyngeal or upper respiratory con-
ditions, metabolic disorders, systemic diseases, and other external sources. In the oral cav-
ity, most of the odor is due to putrefactive microbial activity. It is not yet clear, however,
whether the bacteria responsible for the odor are a specific group of only a few species or
rather hundreds of types, and to what extent they vary from individual to individual. In
vitro, odor is not elaborated except under anaerobic conditions, yet it is not clear whether
the bacteria involved are obligate anaerobes. It is not known whether the odor is produced
independently by individual species, or due to cooperation (e.g., between Gram-positive
species producing glycosidases and Gram-negative anaerobes). Finally, is Solobacterium
moorei a causative bacterium in the odor process, or rather merely present in the mouths
of those with malodor?
There is a wide consensus that the posterior area of the tongue dorsum is the major site
of malodor production. Other sites in the oral cavity may be involved as well (e.g., inter-
dental plaque, and inflamed pockets). However, the typical odor from the back of the
tongue is quite different in quality as compared with interdental or subgingival odor,
as well as denture odor. This difference in odor character between the various sites is not
yet understood. Are these dissimilarities a function of different bacterial types involved at
the various sites, or rather the different substrates available for degradation? Further,
although many (but not all) studies link tongue coating with malodor, it is not clear to what
extent differences in tongue morphologies (e.g., fissured tongue) contribute to observed
differences in odor.
N. Sterer, M. Rosenberg, Breath Odors, 1

DOI: 10.1007/978-3-642-19312-5_1, Springer-Verlag Berlin Heidelberg 2011
2 1 Introduction
It is commonly held that during the day, odor is worst when our mouth dries out (espe-
cially upon awakening). Is this because the odors evaporate more readily from the drying
mucosal surfaces, or because of microbial accumulation in the absence of the cleansing
and/or antibacterial effects of saliva? To what extent is drying saliva a substrate for mal-
odor production in the mouth? Some studies suggest that clinical xerostomia does not
predispose to oral malodor. Is this because of the acidic pH, different microbiota, or other
reasons?
It is evident that volatile sulfides, in particular hydrogen sulfide and methyl mercaptan,
can be readily detected in breath, and their levels correlate with breath odor. Does this
mean that they are the only gases responsible for the breath odor bouquet? Some research-
ers are of the opinion that this is the case, while others are not. Both sulfide gases are
significantly correlated with odor judge scores in many studies, regardless of the measur-
ing techniques (e.g., GC, halimeter). It should be kept in mind, however, that hydrogen
sulfide and methyl mercaptan are associated with many other types of microbial odors
(e.g., feces, sewage, animal waste, putrefying foods) that are dissimilar to breath odors.
Furthermore, one would still have to account for the variation in odor types for various
kinds of oral malodor.
As stated above, breath odor is often worst upon awakening. In the absence of poor oral
hygiene or other pathological factors, morning breath might thus be considered a normal
human characteristic, and is often termed physiological halitosis. However, there are no
studies available to determine whether people with healthy dentition and gums, with little
or non-tongue coating, who practice excellent daily oral hygiene, should have any breath
odor at all upon awakening. So should morning breath be considered a normal phenome-
non in healthy people, or not?
People with bad breath, who are completely unaware that they suffer from the problem,
are commonly encountered by us all. However, the reason for this is not yet clear. Is it
because of psychological habituation, physiological adaptation, or our physical inability to
breathe in through our nose what we breathe out through our mouth? There are thus mil-
lions of people with bad breath who do not know, and millions of others without bad breath
who are sure they do. This is compounded by the reticence of others (even family mem-
bers) to alert someone that they suffer from breath odor.
Most of us tend to worry to varying degrees about whether our breath is fine or not.
However, a significant proportion of the population (some 1–2% of the adult population)
worries a lot. For them, it is a continuous preoccupation. There are some potential factors
that lead people to be overly concerned: aggressive advertising, foul smelling tonsillar
stones (i.e., tonsilloliths), having been told once in the past, having parents with bad breath,
bad taste, etc. Why do these exaggerated worries persist and ruin people’s quality of life?
Should an exaggerated concern of bad breath be considered a continuous spectrum (accord-
ing to the original definition of halitophobia), or be separated into two dichotomous groups,
the first of which is amenable to treatment (i.e., “pseudo-halitosis”)? How close is the
unnecessary worry of having body odor to other concerns of abnormal body parts and
functions? Should the psychiatric definition of “body dysmorphic disorder” be extended to
include worries about smells, for example? To what extent can excessive worries of having
bad breath be dealt with by psychological counseling and medication? These are all ques-
tions under current discussion.
1 Introduction 3
Further, we are often asked about the possibility of ‘inheriting’ bad breath. This could
take two forms: the first, inheriting genes that predispose to bad breath (e.g., related per-
haps to the immune system, tooth, tongue, and nose anatomy) and the second, ‘inheriting’
odor producing bacterial species from our parents (the same way that caries-producing
strains are inherited). Little research has been done in this area.
There is also controversy surrounding the role of the tonsils in breath odor. Most
researchers think they play only a minor role, while there are others who think that they are
important. However, there are few studies to support the latter contention. Further, subjects
with tonsilloliths often worry about bad breath because of the odor of the tonsil stones, but
there is little information on their contribution to the overall halitosis whilst in the crypts.
Finally, we know little about the potentially causal relationship between malodorous
gases in the mouth and periodontal disease. It appears that bad breath is more directly
related to current signs of gingival bleeding and inflammation indices than pocket status or
plaque index. Given the ample data showing that malodorous gases such as hydrogen sul-
fide are highly toxic to soft tissue, might one assume that these microbial gases help pro-
mote cell death and the advance of the disease. It is also unclear to what extent the
putrefaction on the tongue impacts the health of the periodontium.
Odor judge scoring is another issue that requires future scrutiny. With all the limitations
of using human judges, they are still considered the gold standard of breath testing. Yet,
few studies are available comparing the scoring of multiple judges. Training sessions con-
ducted at Prof. John Greenman’s laboratory in Bristol teach us that judges differ in their
abilities to discriminate various odor molecules, as well as the concentrations of a given
stimulant. Will training sessions (or kits) help calibrate researchers worldwide? Hopefully,
reliable instruments able to detect low concentrations of non-sulfide gases (e.g., indole,
skatole, cadaverine, and putrescine), will become available, allowing researchers to better
ascertain their role in oral malodor, and to come up with instrumental assessments that
more closely resemble odor judge scores.
The main goal of the present textbook has been to describe, summarize, and elaborate
on the growing body of knowledge accumulated over years in both research and clinical
aspects of the field of breath odors. What we have learned, and what still remains unclear.
Breath Odors of Oral Origin
(Oral Malodor) 2
Breath odor or halitosis denotes any type of disagreeable scent felt on a person’s breath during
exhalation and speech. These odors have many different causes and may originate from
various locations such as the oral cavity, nasal cavity, upper respiratory tract, and lungs.
According to research performed in multidisciplinary breath clinics (involving profes-
sionals from various fields: dentistry, E.N.T., internal medicine, and psychology) in vari-
ous centers, some 90% of breath odors originate from within the oral cavity itself
(Table 2.1). This condition in which the malodor originates from the mouth is commonly
known as oral malodor (also termed: Fetor oris or Feotor ex ora).
The potential loci for malodor production within the oral cavity include the posterior
portion of tongue’s dorsum, subgingival areas (e.g., periodontal pockets and interdental
spaces), faulty restorations (e.g., leaking crowns and bridges), dental implants, dentures,
and abscesses. Furthermore, transient oral dryness brought about by a temporal reduction
in saliva flow plays an important part in promoting this condition.
Breath odors from the mouth are most commonly measured directly by human odor
judges, or indirectly, based on the levels of volatile sulfide compounds (VSC) within the
oral cavity (for further details, see Chap. 8).
Oral Malodor and the Tongue
The data presented in Table 2.1 clearly demonstrate that the tongue is by far the most com-
mon source for malodor production within the oral cavity. The posterior portion of the
tongue’s dorsum, where most malodor originates, is often covered by a layer of debris com-
prising cellular (bacteria, desquamated epithelial cell, white blood cells) and noncellular
components (especially proteins from saliva, postnasal, and gingival secretions). This layer
termed “tongue coating” may vary in size, thickness, and color among individuals depending
on oral activity (e.g., eating, drinking, smoking), oral hygiene, and oral health-related param-
eters (e.g., presence of periodontal disease); (Yaegaki and Sanada 1992a, b) (Fig. 2.1).
Over the last four decades, various measuring techniques have been suggested for
tongue coating evaluation and quantification, taking into account various parameters such
as coating thickness, coating area, and discoloration. Some of these methods are summa-
rized in Table 2.2.

6 2 Breath Odors of Oral Origin (Oral Malodor)
Table 2.1 Distribution of breath odor origins in subjects attending multidisciplinary clinics

Reference Patients population Confirmed breath odor problem
Quirynen et al. N = 2,000 N = 1,687 (84.3%)
(2009) (1,078 F)
Age 2–90 year Oral causes Non oral causes
(39.2 ± 14.2) N = 1,515 (89.8%) N = 97 (5.7%)
Tongue coating (TC) ENT tonsillitis
N = 868 (51.4%) N = 14 (0.8%)
Gingivitis (G) Rhinitis
N = 75 (4.4%) N = 11(0.6%)
Periodontitis (P) Sinusitis
N = 148 (8.7%) N = 4(0.2%)
Combination (TC/G/P) Nose obstruction
N = 363 (21.5%) N = 8 (0.4%)
Xerostomia Extra oral:GI tract
N = 50 (2.9%) N = 26 (1.5%)
Dental TMAU
N = 7 (0.4%) N = 1 (0.05%)
Candida Systemic
N = 4 (0.2%) N = 5 (0.2%)
Medication
N = 2 (0.1%)
Hormonal
N = 2 (0.1%)
Diet
N = 9 (0.5%)
Unknown
N = 15 (0.8%)
Oral-non oral combination
N = 75 (4.3%)
ENT + Oral:
N = 42 (2.4%)
GI + Oral:
N = 33 (1.9%)
Delanghe et al. N = 260 N = 246 (94.6%)
(1996) (135 F)
(36 ± 13.5) N = 225 (91.4%) N = 21 (8.5%)
Tongue coating ENT:
N = 92 (37.3%) Chr. tonsillitis
Gingivitis N = 15 (6%)
N = 70 (28.4%) Chr. sinusitis
Periodontitis N = 4 (1.6%)
N = 63 (25.6%) Foreign bodies
N = 1 (0.4%)
Rhinitis
N = 1 (0.4%)
Oral Malodor and the Tongue 7
Table 2.1 (continued)
Reference Patients population Confirmed breath odor problem
Seemann et al. N = 407 N = 293 (72%)
(2006) (204 F)
(41.5 ± 13.8) N = 272 (92.7%) N = 22 (7.3%)
Tongue coating ENT:
(“physiologic”) Chr. tonsillitis
N = 175 (59.7%) N = 15 (5.1%)
“Pathologic” Chr. sinusitis
N = 97(33%) N = 2 (0.6%)
Periodontitis Foreign bodies
N = 80 (27.3%) N = 2 (0.6%)
Gingival hyperplasia Systemic: diabetes
N = 10 (3.4%) N = 2 (0.6%)
Faulty restorations Smokers breath
N = 6 (2%) N = 3 (1%)
Fig. 2.1 Typical photo of a

mild tongue coating
covering the posterior third
of the tongue dorsum
Table 2.2 Tongue coating measurements

Reference Score Description
Gross et al. 0 No coating
(1975) 1 Slight coating
2 Moderate coating
3 Heavy coating
Yaegaki and Wet weight (mg) Scraping off and weighing the tongue coating.
Sanada
(1992a)
Miyazaki 0 None visible
et al. (1995) 1 <1/3 tongue dorsum surface covered
2 <2/3 tongue dorsum surface covered
3 >2/3 tongue dorsum surface covered
Mantilla Discoloration
Gomez
(2001) 0 Pink
1 White
2 Yellow/light brown
3 Brown
4 Black
Thickness
0 No coating
1 Light-thin coating
2 Heavy-thick coating
Oho et al. Area Area score × thickness score = tongue coating (range 0–6).
(2001)
0 No tongue coating
1 <1/3 tongue dorsum surface covered
2 1⁄3–2⁄3 tongue dorsum surface covered
3 >2/3 tongue dorsum surface covered
Thickness
0 No tongue coating
1 Thin tongue coating (papillae visible)
2 Thick tongue coating (papillae invisible)
Winkel et al. (Six areas grid) Tongue dorsum is divided into six areas (i.e. three
(2003) posterior and three anterior)
Coating
0 No coating
1 Light coating
2 Severe coating
Discoloration
0 No discoloration
1 Light discoloration
2 Severe discoloration
Score is calculated by adding all six scores (range 0–12)
Kim et al. Tongue coating Calculated from digital images obtained by the digital
(2009) area tongue imaging system (DTIS)
Oral Malodor and the Tongue 9
Large epidemiological studies on the prevalence of oral malodor and its related param-
eters in the general population have been conducted in Japan (Miyazaki et al. 1995), China
(Liu et al. 2006), and Switzerland (Bornstein et al. 2009). Significant associations have
been reported comparing oral malodor with the level of tongue coating (Table 2.3).
Furthermore, the level of malodor-related compounds (e.g., sulfide-containing compounds)
produced on the posterior portion of the tongue dorsum were highly correlated with the
overall mouth odor as measured by a human odor judge (r = 0.77, p < 0.01), as well as vola-
tile sulfide levels (r = 0.63, p < 0.01) (Morita et al. 2001).
Various studies comparing the tongue parameters of subjects with and without oral
malodor showed that subjects with oral malodor had significantly greater tongue coating
as compared with the no malodor controls (Haraszthy et al. 2007; Oho et al. 2001; Washio
et al. 2005). Furthermore, mechanical removal of tongue coating results in a substantial
decrease in oral malodor and its components (Yaegaki and Sanada 1992a). Research done
by Tonzetich and Ng (Tonzetich and Ng 1976) showed that tongue brushing was very
effective in reducing over 70% of the volatile sulfides as compared with about 30% reduc-
tion that resulted from tooth brushing.
Table 2.3 Correlations among malodor related parameters

Reference Malodor related parameters Correlations
Miyazaki et al. Spearman correlation
(1995)
(n = 2,672) Tongue coating vs. sulfide monitor
a
r = 0.44* − 0.57*
Periodontal conditionb vs. sulfide monitor r = 0.34* − 0.58*
Plaque indexc vs. sulfide monitor r = 0.13* − 0.31*
(*p < 0.001)
Liu et al. (2006) Pearson correlation
(n = 2,000)
Tongue coatinga vs. sulfide monitor r = 0.15* − 0.24*
Periodontal conditiond vs. sulfide monitor:
Calculus r = 0.04NS − 0.21*
Pocket depth r = 0.02NS − 0.25*
Bleeding index r = 0.02NS − 0.30*
Plaque indexc vs. sulfide monitor r = 0.08NS − 0.21*
Tongue coating1 vs. odor judge r = 0.20* − 0.31*
Periodontal conditiond vs. odor judge
Calculus r = 0.20* − 0.29*
Pocket depth r = 0.17* − 0.31*
Bleeding index r = 0.12* − 0.22*
Plaque indexc vs. odor judge r = 0.15* − 0.26*
(NS-non significant,
* p < 0.01)
Bornstein et al. Linear regression
(2009)
(n = 419) Tongue coatinge vs. sulfide monitor 4.29
Tongue coatinge vs. odor judge 2.35
Periodontal conditiond vs. odor judge 2.45
a
Tongue coating area: 0 = none, 1 = less than 1/3, 2 = less than 2/3, 3 = more then 2/3
b
According to WHO guidelines (CPITN)
c
Silness and Löe (1964)
d
Periodontal screening index (PSI)
e
0 = no coating, 1 = light coating (10%), 2 = moderate (10–50%), 3 = severe (>50%)
Table 2.4 Correlations between tongue malodor scores and malodor related parameters
Reference Malodor related parameters Correlations
Kozlovsky et al. (1994) Pearson correlation
(n = 52)
Tongue malodora vs. oral malodorb r = 0.73, p < 0.001
Tongue malodor vs. sulfide monitorc r = 0.38, p = 0.003
Tongue malodor vs. pocket depthd r = 0.47, p = 0.005
Tongue malodor vs. GIe r = 0.47, p < 0.001
Tongue malodor vs. PIf r = 0.38, p = 0.003
Bosy et al. (1994) Pearson correlation
(n = 127)
Tongue malodor vs. sulfide monitorc r = 0.40, p < 0.01
Tongue malodor vs. GIe r = 0.23, p < 0.01
Greenstein et al. (1997) Pearson correlation
(n = 123)
Sterer et al. (2002) Spearman correlation
(n = 64)
Tongue malodora vs. oral malodorb
Odor judge 1 r = 0.63, p < 0.001
Odor judge 2 r = 0.69, p < 0.001
Tongue malodor vs. sulfide monitorc
Odor judge 1 r = 0.26, p = 0.036
Odor judge 2 r = 0.38, p = 0.002
a
Tongue coating malodor scored by an odor judge (0–5)
b
Whole mouth malodor scored by an odor judge (0–5)
c
Whole mouth ppb sulfide equivalents, HalimeterTM
d
Mean probing depth
e
Gingival index (Löe and Silness 1963)
f
Plaque index (Silness and Löe 1964)
Tongue coating samples can be obtained by scraping the posterior portion of the
tongue’s dorsum using wooden spatula, plastic spoons, tooth brushes, swabs, or gauze
pads (Grapp 1933). These samples very often release a putrid malodor very similar in
character to oral malodor. Sampling the tongue coating using a plastic spoon (i.e., “spoon
test”; (Rosenberg 1996) and scoring the malodor emanating from the spoon yielded highly
significant associations with the oral malodor scores (i.e., odor judge) as well as other oral
malodor-related parameters (Table 2.4).
Oral Malodor, Gingival Health, and Periodontal Disease
The relationships between oral malodor and gingival or periodontal health are not as
straightforward as in the case of the tongue and are the cause of controversy in the litera-
ture. Conflicting data from various studies best demonstrate the complexity of this issue
(Table 2.5).
Oral Malodor, Gingival Health, and Periodontal Disease 11
Table 2.5 Oral malodor parameters and periodontal disease

Reference Parameters/Criteria Findings
Kostelc et al. (1984) Measurement of malodor related Significant increase in
(n = 10) compounds by gas chromatography in malodor related
experimental gingivitis (n = 5) and controls compounds in
(n = 5) experimental gingivitis
Rosenberg et al. Pearson correlation
(1991)
(n = 41) Odor judge 1 vs. pocket depth (No. >5 mm)
a
r = 0.184, p = 0.047
Odor judgea 2 vs. pocket depth (No. >5 mm) r = 0.107, NS
VSCb vs. pocket depth (No. >5 mm) r = 0.280, p = 0.002
Odor judgea 1 vs. gingival indexc r=0.099, NS
Odor judgea 2 vs. gingival indexc r = 0.081, NS
VSCb vs. gingival indexc r = 0.087, p = 0.053
Odor judgea 1 vs. plaque indexd r = 0.353, p = 0.0001
Odor judgea 2 vs. plaque indexd r = 0.359, p = 0.0001
VSCb vs. plaque indexd r = 0.373, p = 0.0001
Odor judgea 1 vs. floss odor r = 0.381, p = 0.0001
Odor judgea 2 vs. floss odor r = 0.422, p = 0.0001
VSCb vs. floss odor r = 0.208, p = 0.026
Yaegaki and Sanada Probing depth ³4 mm is considered VSC is significantly
(1992a) periodontal disease higher in periodontal
(n = 31) Bleeding on probing (% BOP). subjects
VSCe VSC is associated with
bleeding on probing
Bosy et al. (1994) Pearson correlation
(n = 127)
Odor judgea vs. pocket depth (No. >5 mm) r = 0.11, NS
Odor judgea vs. gingival indexc r = 0.15, NS
Odor judgea vs. plaque indexd r = 0.12, NS
Odor judgea vs. floss odor r = 0.23, p < 0.01
De Boever et al. Malodor No complaint Differences between
(1994) complaint groups (ANOVA)
(n = 55)
Odor judgef p < 0.005
VSCg p < 0.05
Bleeding on probing (% BOP) p < 0.005
Kozlovsky et al. Pearson correlation
(1994)
(n = 52) Odor judgea vs. mean pocket depth r = 0.581, p < 0.001
VSCb vs. mean pocket depth r = 0.305, p = 0.050
Odor judgea vs. gingival indexc r = 0.536, p < 0.001
VSCb vs. gingival indexc r = 0.298, p = 0.017
Odor judgea vs. plaque indexd r = 0.383, p = 0.003
VSCb vs. plaque indexd r = 0.188, p = 0.093
Soder et al. (2000) Foetor ex ore (severe malodor) Subject with severe
(n = 1,681) Probing depth scores (% of teeth with malodor (n = 41) had
probing depth >5 mm) significantly higher
Gingival index scores (redness swelling and probing depth and
bleeding) gingival index scores
(p < 0.001)
(continued)
Reference Parameters/Criteria Findings
Morita and Wang Pearson correlation
(2001)
(n = 81) Odor judgea vs. pocket depth (%³6 mm) r = 0.371, p = 0.001
VSCg vs. pocket depth (%³6 mm) r = 0.411, p < 0.001
Odor judgea vs. bleeding on probing (%) r = 0.489, p < 0.001
VSCg vs. bleeding on probing (%) r = 0.472, p < 0.001
Figueiredo et al. Probing >3 mm Probing £3 mm (n = 20) Differences between
(2002) (n = 21) groups (ANOVA)
Odor judgef p = 0.001
VSCg p = 0.02
Gingival indexc p = 0.005
Plaque indexd p = 0.006
Stamou et al. (2005) Pearson correlation
(n = 71)
Odor judge vs. probing depth
a
r = −0.054, NS
Odor judgea vs. plaque indexd r = 0.185, NS
Odor judgea vs. gingival indexc r = 0.111, NS
Tsai et al. (2008) Pearson correlation
(n = 72)
Odor judge vs. pocket depth (%>5 mm)
a
r = 0.22, NS
Odor judgea vs. bleeding on probing (%) r = 0.54, p < 0.001
NS non significant
a
Odor judge scores on a scale of 0–5
b
Volatile sulfide compounds measured by sulfide monitor (model no. 1170)
c
Gingival index (GI; Löe and Silness 1963)
d
Plaque index (PI; Silness and Löe 1964)
e
Volatile sulfide compounds (VSC) measured by gas chromatography
f
g
Volatile sulfide compounds measured by Halimeter
Many earlier studies addressing this topic suggested a relationship between oral
malodor and periodontal disease. Sulser and coworkers (Sulser et al. 1939) claimed that
gingivitis and pyorrhea (i.e., periodontitis) are among the main conditions affecting breath
odor concentration. Other researchers (Kostelc et al. 1984) found a significant increase in
malodor-related compounds in experimental gingivitis.
Studies that compared malodor-related parameters in subjects with or without peri-
odontal disease showed that oral sulfide levels were significantly higher in subjects with
periodontal pocket depths of 4 mm or more (Yaegaki and Sanada 1992a, b), and that sub-
jects with periodontal disease (pocket depth >3 mm) had significantly higher malodor
ratings as scored by an odor judge (Figueiredo et al. 2002). In another study (Soder et al.
2000), subjects with severe oral malodor (Foetor ex ore) had a significantly higher per-
centage of teeth with periodontal pocket depths of at least 5 mm as well as higher gingival
index scores (redness, swelling and bleeding). Furthermore, large studies done in Japan
Oral Malodor, Gingival Health, and Periodontal Disease 13
(Miyazaki et al. 1995), China (Liu et al., 2006), and Switzerland (Bornstein et al. 2009)
also found significant correlations comparing oral malodor and periodontal status
(Table 2.2).
In contrast, a study by Bosy and coworkers (Bosy et al. 1994) found no association
between oral malodor and periodontal disease (pocket depth ³5 mm), suggesting that these
may be two independent conditions. Another more recent study by Tsai and coworkers
(Tsai et al. 2008) also failed to show an association between malodor levels and the per-
centage of teeth with periodontal involvement (pocket depth ³5 mm). However, the latter
did find an association between malodor levels and the percentage of teeth with bleeding
on probing.
To complicate matters further, some studies (Yaegaki and Sanada 1992a, b) reported
that subjects with periodontal disease (probing depth ³4 mm) had significantly more
tongue coating (four times more wet weight) than the control non-periodontal subjects.
These studies further showed that the tongue coating was responsible for production
of 60% of the malodor-related volatile sulfide compounds and that these compounds
were associated with the percentage of sites exhibiting bleeding on probing.
These data, taken together, imply that with respect to oral malodor production, peri-
odontal disease is less dominant than tongue coating. It is also apparent that the active
inflammation process is the main link between gingival and periodontal disease, and
malodor production. Typically represented by one of its chief signs (i.e., bleeding on
probing or papillary bleeding), active gingivitis or periodontitis, accompanied by bacte-
rial activity, and increased flow of crevicular fluid and blood cells is more relevant to the
malodor production process than the presence or depth of periodontal pockets. The
inflammatory process may be further exacerbated by the malodorous compounds, which
are for the most part toxic and increase tissue permeability and damage (Ng and
Tonzetich 1984) (Fig. 2.2).
Fig. 2.2 Gingivitis; swollen

bleading gums showing
signs of inflammation
(kindly provided by
Dr. M. Perez-Davidi)
Oral Malodor and Dental Restorations
As a rule, any appliance, fixed or removable, within the oral cavity, which hinders the com-
mon practice of oral hygiene and facilitates plaque accumulation, has the potential to
increase oral malodor production.
Dental crowns and bridges are the most common examples of this principle. Dental
bridges in particular form an obstacle to maintaining good interdental hygiene by prevent-
ing regular flossing. This is also true for orthodontic appliances and splints. Furthermore,
faulty restorations, particularly if ill fitted or decemented, may even intensify the problem
by allowing bacterial proliferation and accumulation in the inner gaps between the pre-
pared tooth and the restoration, thus forming a reservoir of anaerobic bacteria.
Another such reservoir has been demonstrated in the inner space of the implant-abutment
interface (IAI) of osseointegrated dental implants. Research showed that when this interface
is situated over 2 mm in depth with respect to the surrounding soft tissue, the inner compart-
ment of the implant harbors significantly more malodor producing bacteria as compared to
implants with shallower transmucosal depth (Sterer et al. 2008).
Acrylic appliances such as dentures and obturators are known for their plaque accumu-
lating properties. Their porotic nature and increased tendency to adsorb salivary proteins,
resulting in bacterial adhesion, turns the acrylic appliance into a bacterial reservoir.
Although little research has been carried out on the composition of denture biofilm, in a
study performed by Goldberg and coworkers (Goldberg et al. 1997), certain types of mal-
odor-producing bacteria, not normally considered important members of the oral micro-
biota (i.e., Enterobacteriaceae), were shown to be dramatically increased in the case of
dentures wearers. Furthermore, when cultivated in the lab, these bacteria produce malodor
similar to denture malodor.
Apart from bacterial accumulation and denture contamination, it seems that behavioral
aspects also play a part in denture-related malodor. Research done on denture-wearing
habits and malodor showed that malodor-related compounds were significantly increased
in subjects who did not remove their dentures during the night (Nalcaci and Baran 2008).
Oral Malodor and Oral Dryness
Saliva has an important role in maintaining oral health and many oral functions (e.g., eat-
ing, talking). However, comprising 98% water, it also provides suitable moist environment
leading to an abundance of microorganisms within the oral cavity.
This mouthful of bacteria produces many by-products and waste as a result of its activ-
ity, many of which (described further in Chap. 3) are foul smelling. Some of these bacterial
by-products are more volatile than others. However, when there is a decrease in saliva flow
and the oral mucosa becomes dry, many more of these compounds and other less volatile
compounds can escape the oral surfaces, and become detected on the breath. This and
other possible mechanisms (e.g., lack of salivary antibacterial and washing effect, as well
as salivary stagnation and degradation of salivary glycoproteins) may explain why
References 15
decreasing saliva flow increases the severity of malodor in individual subjects. In a study
comparing saliva flow and malodor-related compounds in 147 subjects (Koshimune et al.
2003), lower levels of resting saliva (e.g., without stimulating saliva flow by chewing)
were associated with higher levels of malodor-related compounds.
There are some physiological conditions that affect saliva flow. For example, during
sleep saliva flow is brought to a halt (Dawes 1972). That is one of the reasons that sleep,
especially when accompanied by mouth breathing, may promote oral malodor production.
Normally, saliva flow decreases between meals. Dehydration due to insufficient fluid
intake and prolonged fasting may also result in reduced saliva flow.
Another condition that might affect saliva flow is stress. Research by Queiroz and
coworkers (Queiroz et al. 2002) showed that stress can cause salivary flow reduction and
concomitant increase in malodor-related compounds. Anxiety was also shown to elevate
these compounds (Calil and Marcondes 2006).
Many widely used medications such as antihypertensive and antidepressants drugs are
known to have reducing effect on saliva flow as an undesirable side effect. The use of such
drugs, as well as increased consumption of coffee and alcohol may cause an increase in
malodor production as a result of salivary flow decrease (Tschoppe et al. 2010).
References
Bornstein, M.M., Kislig, K., Hoti, B.B., Seemann, R., Lussi, A.: Prevalence of halitosis in the
population of the city of Bern, Switzerland: a study comparing self-reported and clinical data.
Eur. J. Oral Sci. 117(3), 261–267 (2009)
Bosy, A., Kulkarni, G.V., Rosenberg, M., McCulloch, C.A.: Relationship of oral malodor to
periodontitis: evidence of independence in discrete subpopulations. J. Periodontol. 65(1),
37–46 (1994)
Calil, C.M., Marcondes, F.K.: Influence of anxiety on the production of oral volatile sulfur com-
pounds. Life Sci. 79(7), 660–664 (2006)
Dawes, C.: Circadian rhythms in human salivary flow rate and composition. J. Physiol. 220(3),
529–545 (1972)
De Boever, E.H., De Uzeda, M., Loesche, W.J.: Relationship between volatile sulfur compounds,
BANA-hydrolyzing bacteria and gingival health in patients with and without complaints of oral
malodor. J. Clin. Dent. 4(4), 114–119 (1994)
Delanghe, G., Ghyselen, J., Feenstra, L., Van Steenberghe, D.: Experiences of a Belgian multidis-
ciplinary breath odour clinic. In: Van Steenberghe, D., Rosenberg, M. (eds.) Bad breath a mul-
tidisciplinary approach, pp. 199–208. Leuven University Press, Leuven (1996)
Figueiredo, L.C., Rosetti, E.P., Marcantonio Jr., E., Marcantonio, R.A., Salvador, S.L.: The rela-
tionship of oral malodor in patients with or without periodontal disease. J. Periodontol. 73(11),
1338–1342 (2002)
Goldberg, S., Cardash, H., Browning 3rd, H., Sahly, H., Rosenberg, M.: Isolation of Entero
bacteriaceae from the mouth and potential association with malodor. J. Dent. Res. 76(11),
1770–1775 (1997)
Grapp, G.L.: Fetor oris (halitosis): a medical and dental responsibility. Northwest Med. 32,
375–380 (1933)
Greenstein, R.B., Goldberg, S., Marku-Cohen, S., Sterer, N., Rosenberg, M.: Reduction of oral
malodor by oxidizing lozenges. J. Periodontol. 68(12), 1176–1181 (1997)
Gross, A., Barnes, G.P., Lyon, T.C.: Effects of tongue brushing on tongue coating and dental
plaque scores. J. Dent. Res. 54(6), 1236 (1975)
Haraszthy, V.I., Zambon, J.J., Sreenivasan, P.K., Zambon, M.M., Gerber, D., Rego, R., Parker, C.:
Identification of oral bacterial species associated with halitosis. J. Am. Dent. Assoc. 138(8),
1113–1120 (2007)
Kim, J., Jung, Y., Park, K., Park, J.W.: A digital tongue imaging system for tongue coating evalu-
ation in patients with oral malodour. Oral Dis. 15(8), 565–569 (2009)
Koshimune, S., Awano, S., Gohara, K., Kurihara, E., Ansai, T., Takehara, T.: Low salivary flow
and volatile sulfur compounds in mouth air. Oral Surg. Oral Med. Oral Pathol. Oral Radiol.
Endod. 96(1), 38–41 (2003)
Kostelc, J.G., Preti, G., Zelson, P.R., Brauner, L., Baehni, P.: Oral odors in early experimental
gingivitis. J. Periodontal Res. 19(3), 303–312 (1984)
Kozlovsky, A., Gordon, D., Gelernter, I., Loesche, W.J., Rosenberg, M.: Correlation between the
BANA test and oral malodor parameters. J. Dent. Res. 73(5), 1036–1042 (1994)
Liu, X.N., Shinada, K., Chen, X.C., Zhang, B.X., Yaegaki, K., Kawaguchi, Y.: Oral malodor-
related parameters in the Chinese general population. J. Clin. Periodontol. 33(1), 31–36 (2006)
Löe, H., Silness, J.: Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol
Scand 21, 533–551 (1963)
Mantilla Gomez, S., Danser, M.M., Sipos, P.M., Rowshani, B., van der Velden, U., van der
Weijden, G.A.: Tongue coating and salivary bacterial counts in healthy/gingivitis subjects and
periodontitis patients. J. Clin. Periodontol. 28(10), 970–978 (2001)
Miyazaki, H., Sakao, S., Katoh, Y., Takehara, T.: Correlation between volatile sulphur compounds
and certain oral health measurements in the general population. J. Periodontol. 66(8), 679–684
(1995)
Morita, M., Wang, H.L.: Relationship between sulcular sulfide level and oral malodor in subjects
with periodontal disease. J. Periodontol. 72(1), 79–84 (2001)
Morita, M., Musinski, D.L., Wang, H.L.: Assessment of newly developed tongue sulfide probe for
detecting oral malodor. J. Clin. Periodontol. 28(5), 494–496 (2001)
Nalcaci, R., Baran, I.: Oral malodor and removable complete dentures in the elderly. Oral Surg.
Oral Med. Oral Pathol. Oral Radiol. Endod. 105(6), e5–e9 (2008)
Ng, W., Tonzetich, J.: Effect of hydrogen sulfide and methyl mercaptan on the permeability of oral
mucosa. J. Dent. Res. 63(7), 994–997 (1984)
Oho, T., Yoshida, Y., Shimazaki, Y., Yamashita, Y., Koga, T.: Characteristics of patients complain-
ing of halitosis and the usefulness of gas chromatography for diagnosing halitosis. Oral Surg.
Oral Med. Oral Pathol. Oral Radiol. Endod. 91(5), 531–534 (2001)
Queiroz, C.S., Hayacibara, M.F., Tabchoury, C.P., Marcondes, F.K., Cury, J.A.: Relationship
between stressful situations, salivary flow rate and oral volatile sulfur-containing compounds.
Eur. J. Oral Sci. 110(5), 337–340 (2002)
Quirynen, M., Dadamio, J., Van den Velde, S., De Smit, M., Dekeyser, C., Van Tornout, M.,
Vandekerckhove, B.: Characteristics of 2000 patients who visited a halitosis clinic. J. Clin.
Periodontol. 36(11), 970–975 (2009)
Rosenberg, M.: Clinical assessment of bad breath: current concepts. J. Am. Dent. Assoc. 127(4),
475–482 (1996)
Rosenberg, M., Kulkarni, G.V., Bosy, A., McCulloch, C.A.: Reproducibility and sensitivity of oral
malodor measurements with a portable sulphide monitor. J. Dent. Res. 70(11), 1436–1440 (1991)
Seemann, R., Bizhang, M., Djamchidi, C., Kage, A., Nachnani, S.: The proportion of pseudo-halito-
sis patients in a multidisciplinary breath malodour consultation. Int. Dent. J. 56(2), 77–81 (2006)
Silness, J., Löe, H.: Periodontal disease in pregnancy. II. Correlation between oral hygiene and
periodontal condition. Acta Odontol Scand 22, 121–135 (1964)
Soder, B., Johansson, B., Soder, P.O.: The relation between foetor ex ore, oral hygiene and peri-
odontal disease. Swed. Dent. J. 24(3), 73–82 (2000)
References 17
Stamou, E., Kozlovsky, A., Rosenberg, M.: Association between oral malodour and periodontal
disease-related parameters in a population of 71 Israelis. Oral Dis. 11(Suppl 1), 72–74 (2005)
Sterer, N., Greenstein, R.B., Rosenberg, M.: Beta-galactosidase activity in saliva is associated with
oral malodor. J. Dent. Res. 81(3), 182–185 (2002)
Sterer, N., Tamary, I., Katz, M., Weiss, E.: Association between transmucosal depth of osseointe-
grated implants and malodor production. Int. J. Oral Maxillofac. Implants 23(2), 277–280
(2008)
Sulser, G.F., Brening, R.H., Fosdick, L.S.: Some conditions that effect the odor concentration of
breath. J. Dent. Res. 18(4), 355–359 (1939)
Tonzetich, J., Ng, S.K.: Reduction of malodor by oral cleansing procedures. Oral Surg. Oral Med.
Oral Pathol. 42(2), 172–181 (1976)
Tsai, C.C., Chou, H.H., Wu, T.L., Yang, Y.H., Ho, K.Y., Wu, Y.M., Ho, Y.P.: The levels of volatile
sulfur compounds in mouth air from patients with chronic periodontitis. J. Periodontal Res.
43(2), 186–193 (2008)
Tschoppe, P., Wolgin, M., Pischon, N., Kielbassa, A.M.: Etiologic factors of hyposalivation and
consequences for oral health. Quintessence Int. 41(4), 321–333 (2010)
Washio, J., Sato, T., Koseki, T., Takahashi, N.: Hydrogen sulfide-producing bacteria in tongue
biofilm and their relationship with oral malodour. J. Med. Microbiol. 54(Pt 9), 889–895 (2005)
Winkel, E.G., Roldan, S., Van Winkelhoff, A.J., Herrera, D., Sanz, M.: Clinical effects of a new
mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc-lactate on oral halitosis.
A dual-center, double-blind placebo-controlled study. J. Clin. Periodontol. 30(4), 300–306 (2003)
Yaegaki, K., Sanada, K.: Volatile sulfur compounds in mouth air from clinically healthy subjects
and patients with periodontal disease. J. Periodontal Res. 27(4 Pt 1), 233–238 (1992a)
Yaegaki, K., Sanada, K.: Biochemical and clinical factors influencing oral malodor in periodontal
patients. J. Periodontol. 63(9), 783–789 (1992b)
Biochemical and Microbial Aspects
of Oral Malodor Production 3
The General Role of Bacteria in Breath Odors
There is ample evidence that in the large majority of cases, oral malodor derives from
bacterial activity within the oral cavity. It is also likely that most cases of odor deriving
from the nasal passages and tonsils are also bacterial in origin. One indication for this is
the transient reduction of oral malodor observed following local antiseptic treatment
(e.g., mouthwash), and the elimination of many non-oral cases of halitosis following
systemic antibiotic treatment.
In a larger context, bacteria are responsible for many of the foul odors that we encounter
in everyday lives (e.g., sewage, animal waste, garbage and spoiled food, contaminated
water, body odor, etc.)
Bacteria may produce a wide variety of foul odors depending on the substrates being
degraded, and the metabolic pathways involved. It is possible that through our evolution,
we have learned to detest these types of odor components as a health hazard warning.
In the oral cavity itself, hundreds of species cohabit the many available niches, living in
different microenvironments and feeding on a variety of organic substrates. It is here that
most cases of bad breath begin.
The Bacterial Origin of Oral Odors
The diverse microbial population of the oral cavity can be divided according to various
metabolic characteristics such as nutritional requirements and oxygen tolerance. The
Gram-positive oral bacteria are generally saccharolytic and facultative in nature, which
means that they degrade and utilize monosaccharides, disaccharides, and carbohydrates as
their main energy source (e.g., fermentation) and can consume oxygen in the process.
Members of this group such as Streptococci and Actinomyces spp. are often considered to
be early colonizers of the oral biofilm, and some Gram positive (e.g., mutans streptococci)
are blamed for fermenting sugars into acids and causing dental caries.
The Gram-negative oral bacteria, on the other hand, are generally considered to be pro-
teolytic and anaerobic. These types of bacteria often prefer anaerobic conditions (i.e., lack

20 3 Biochemical and Microbial Aspects of Oral Malodor Production
of oxygen) for growth and utilize proteins, peptides, and amino acids as a major source of
carbon, nitrogen, and energy (i.e., putrefaction). Some members of the Gram-negative
community (e.g., Fusobacterium, Treponema, Porphyromonas, and Prevotella) are consid-
ered to be particularly implicated in periodontal diseases and malodor production.
To avoid being swallowed or washed away, oral bacteria are able to adhere to surfaces
as well as to each other and form plaques known as oral biofilms. The bacteria dominating
the outer exposed layers of the oral biofilms throughout the mouth are either aerobic or
aerotolerant, surviving under relatively high oxidation (Eh) levels. Following maturation
and succession of these microniches, oxygen depletion by microbes in the outer levels
allows for the proliferation of increasingly anaerobic species. In the laboratory, Gram-
positive microorganisms are generally found to inhabit the outer layers of oral biofilms,
and Gram-negative anaerobes thrive in the reduced inner layers.
Metabolic Factors Affecting Malodor Production
pH and Glucose: Fosdick and colleagues (Berg et al. 1946) reported that the putrefaction
rate of incubated saliva samples is strongly inhibited in the presence of even a small
amount of sugar, but gave no possible explanation for this observation.
In 1972, McNamara and coworkers (McNamara et al. 1972) reported that whole saliva,
adjusted to slightly acidic conditions (pH 6.5), did not produce malodor following incuba-
tion, whereas at pH 7.5, malodor was produced. This study also showed that the addition
of glucose to incubated saliva prevents malodor production and causes an increase in the
proportion of Gram-positive bacteria. McNamara concluded that glucose fermentation and
resulting acidity inactivated amino acid metabolism and favored the growth of saccharo-
lytic Gram-positive bacteria.
Kleinberg and Codipilly (1997) also demonstrated, using a salivary incubation assay, that
the addition of glucose results in pH reduction and concomitant inhibition of malodor pro-
duction, concluding that acidic pH is inhibitory to bacterial metabolism leading to malodor
formation. Whereas the saccharolytic Gram-positive oral bacteria reduce the pH by fermen-
tation and acid production (e.g., lactic acid), the proteolytic Gram-negative oral bacteria tend
to increase the pH by putrefaction (e.g., urea production). Furthermore, the activity of the
various enzymes involved (e.g., saccharolytic, proteolytic) is optimal in different pH ranges.
Another possible explanation for the effect of acidity on malodor inhibition was pro-
posed by Tonzetich and coworkers (Tonzetich et al. 1967). They suggested that various pH
conditions may affect the volatility traits of the malodor components.
Oxygen depletion and redox potential: Oxygen depletion and reduced Eh are imperative
for the development of malodor-producing anaerobic Gram-negative oral bacteria.
Berg and Fosdick (1946) showed that anaerobic conditions increased salivary putrefac-
tion and malodor production. Kleinberg (Codipilly et al. 2004) showed that low Eh read-
ings highly correlated with oral malodor ratings. Greenstein and colleagues (Greenstein
et al. 1997) demonstrated that the rate of oxygen depletion by saliva samples from human
subjects correlated with oral malodor-related parameters. Furthermore, we have recently
Biochemical Aspects 21
Fig. 3.1 Confocal laser scanning microscopy image showing VSC production (red) in the deep
layers of the biofilm
shown that volatile sulfide compounds are produced in the deep layers of mature oral bio-
film where anaerobic conditions predominate (Sterer et al. 2009) (Fig. 3.1).
Biochemical Aspects
Metabolism
Oral malodor is considered to derive primarily from the anaerobic degradation of proteina-
ceous materials by oral microorganisms. Proteins are readily available from saliva, exfoli-
ated epithelial cells, food debris, blood and crevicular fluids, and possibly postnasal drip.
The constituent proteins are hydrolyzed by proteolytic enzymes of bacterial origin, yielding
free amino acids, which can then be further broken down. Some of the molecular by-
products of this process are particularly foul-smelling.
Protein → Amino acids → Putrefactive end products

[source: Fosdick and Piez, 1953]
Deglycosylation: Salivary mucins are large glycoproteins comprised of a long protein

core surrounded by carbohydrate side chains in a bottle brush-like structure. Unlike ordi-
nary polypeptides, their proteolytic degradation requires the prior removal of their carbo-
hydrate side chains, or deglycosylation
Mucin → Protein → Amino acids → Putrefactive end products

One of the key enzymes in the deglycosylation process is b-galactosidase. Our research
has shown that b-galactosidase activity in saliva highly correlated with malodor ratings of
64 subjects (Sterer et al. 2002). Furthermore, addition of b-galactosidase or b-galactosi-
dase producing bacteria (i.e., Streptococcus salivarius) to a mucin incubation mixture pro-
moted mucin putrefaction by Porphyromonas gingivalis (Sterer and Rosenberg 2006).
The proteolytic process described above results in the breakdown of available oral
proteins (or glycoproteins) into free amino acids. These free amino acids serve as nutrients
for oral microorganisms that do not grow on carbohydrates (asaccharolytic), and their
metabolites are important pH modulators and precursors for various molecules such as
iron-scavenging siderophores. Amino acids are degraded via different metabolic pathways
such as deamination, decarboxylation, and various oxidation–reduction processes, yield-
ing different by-products, as described below.
Volatile fatty acids: The enzymatic cleavage of the amino group from various amino
acids occurs at a pH range of 6–7 and results in the production of volatile fatty acids, and
ammonia (NH3) (Table 3.1).
NH2
P – XH – XOOH + H2O → R − COOH + NH3 + 4H + CO2
Amines: Decarboxylation of nitrogen-containing amino acids occurs in the mouth

mainly at pH 6.5 (Gochman et al. 1959) and serves also as a means for the microorganisms
to regulate pH conditions. The decarboxylation of these amino acids results in the produc-
tion of various amine compounds (Table 3.2).
NH2
R − CH − COOH → R − CH2 − NH2 + CO2 + H
Indoles and Phenols: Production of indoles and phenols occurs as a result of the metab-
olism of various aromatic amino acids (Table 3.3).
Volatile sulfide compounds: Production of sulfur containing compounds results from
sulfate reduction or the metabolism of sulfur containing amino acids:
Cysteine → Hydrogen sulfide
Methionine → Methyl mercaptan
Table 3.1 Deamination products of anaerobic bacteria

Amino acid VFA produced
Alanine, glycine, serine Acetate
Threonine Propionate
Glutamate, aspartate Acetate, propionate, butyrate
Valine Isobutyrate
Leucine Isovalerate
Isoleucine 2-Methylbutyrate
Phenylalanine Phenylacetate
Tyrosine p-Hydroxyphenylacetate
Tryptophan Indoleacetate → 3-methylindole
Tyrosine Phenylacetate, phenylpropionate
Source: Mackie et al. (1998)
Table 3.2 Decarboxylation reactions by anaerobic bacteria

Amino acid Amine produced
Glycine Methylamine
Alanine Ethylamine
a-Aminobutyrate Propylamine
Ornithine Putrescine → pyrrolidineb
Argininea Putrescine → pyrrolidineb
Norvaline Butylamine
Lysine Cadaverine → piperidineb
Arginine Agmatine
Histidine Histamine
Cysteic acid Taurine
Tyrosine Tyramine
Tryptophan Tryptamine
Phenylalanine Phenylethylamine
Source: Mackie et al. (1998)
a
Decarboxylation and hydrolysis
b
Ring closure reaction
Table 3.3 Indoles and phenols

Amino acid Products
Tyrosine Phenol, p-Cresol
Tryptophan Indole, 3-Methyl Indole (Skatole)
Phenylalanine Phenyl acetate, Phenyl propionate
Malodorous Volatile Organic Compounds (VOCs) in the Oral Cavity
Many of the above compounds, as well as various other VOCs, have been detected in saliva
samples, saliva headspace, tongue-coating samples, and breath samples. These samples were
analyzed using different techniques varying from classic colorimetric techniques to modern
liquid and gas chromatography. These reported compounds are listed in Table 3.4, highlighting
those that have been implicated in oral malodor production and stating their odor characteris-
tics and thresholds:
Table 3.4 Oral VOCs detected in saliva, tongue coating samples, saliva headspace, and mouth air
Compound Odor description Odor threshold (ppm v/v) References
Acids
Acetic acid (2, 6)
Butyric acid (2, 6)
Methylpropionic acid (2)
Alcohols
Ethanol (1)
Propanol (1, 4, 5, 6)
Decanol (1)
Dodecanol (1)
Tetradecanol (1)
Hexadecanol (1)
Phenylethanol (1)
2-Ethylhexanol (1)
Benzylalcohol (1)
Aldehydes
2-heptanal (2)
2-octanal (2)
Nonanal (5)
Acetaldehyde (6)
Benzaldehyde (1, 5)
Aromatics
C2-C4 Alkyl benzenes (1)
Ethylbenzene (2)
Styrene (1, 5)
Dimethylbenzene (2)
Benzene (1)
Naphtalene (2)
Toluene (1)
Ethers
Dimethylfuran (1)
Fixed gases
Carbon disulfide (4)
Dimethyl selenide (4)
Thiopropanal-s-oxide (6)
Hydrocarbons
2-methyl-propane (2)
dimethoxy-methane (2)
trichloro-ethane (2)
1(1 ethoxyethoxy)-propane (2)
2-methyl 1-nitropropane (2)
2,4 –pentadienenitryl (2)
Isoprene (5)
Caryophyllene (5)
b-Pinene (5)
Isobutene (5)
Tridecane (5)
Dodecane (5)
Undecane (5)
Pentadecane (5)
Decane (5)
Limonene (2, 5)
C8-C12 Alkanes (1)
C17 Alkane (1)
Ketones
2-Butanone (4, 5)
2-Heptanone (2)
2-Hexanone (2)
2-Pentanone (4)
6-Methyl-2-heptanone (2)
Acetone (1, 4, 5, 6)
Nitrogen containing
compounds
Diphenylamine (1)
Pyrrolidine (2)
Putrescine (3, 7)
Cadaverine Putrid – (3, 7)
Methenamine – – (5)
Ammonia Pungent 1.5 (6, 8)
Indole Fecal 0.00030 (1, 2, 3, 4, 9)
(continued)
2-Methyl pyridine Sweat 0.031 (1, 2)
(Picoline)
3-Methyl pyridine (1)
4-Methyl pyridine (1)
Ethyl-pyridine (2)
3-Methyl-indole (Skatole) Fecal 0.0000056 (1, 2, 3 ,4)
Pyridine Rancid 0.063 (1)
Phenols
p-Cresol (1, 2)
Dimethylphenol (2)
Phenol (1, 2, 5)
Sulfur-containing
compounds
2-Methyl-thio-propane (2)
Mercapto-acetic acid (2) (2)
Methylsulphide (2) (2)
Propane-thiol (2) (2)
Methylthiopropane (2) (2)
Thiocyanic acid (2) (2)
Ethanethioic acid-S-ME (2) (2)
Methylbenzotiophene (2) (2)
Benzenecarbothiotic acid (2) (2)
Methanesulfonylazide (2) (2)
Dimethyl sulfide Cabbage 0.0030 (4, 5)
Allyl methyl sulfide (4)
Diallyl disulphide (6)
Hydrogen sulfide Rotten egg 0.00041 (4)
Methyl mercaptan Sewer 0.000070 (2, 4)
Sulfur 0.0022
Dimethyldisulfide – – (1, 2, 4, 5)
Dimethyltrisulfide (1, 2, 4, 5)
(1) Kostelc et al. (1980); (2) Claus et al. (1996); (3) Cooke et al. (2003); (4) van den Velde et al.
(2007); (5) Van den Velde et al. (2009); (6) Ross et al. (2009); (7) Goldberg et al. (1994); (8)
Amano et al. (2002); (9) Berg et al. (1946). (N = 65 compounds). Compounds that have been asso-
ciated with breath odors are written in bold. Methenamine is produced by the reaction of formal-
dehyde and ammonia (Van den Velde et al. 2009)
Research on malodorous VOCs from the oral cavity was initially carried out using sali-
vary putrefaction assays. Whole saliva was stimulated by chewing on paraffin wax and
incubated under various conditions (e.g., aerobic, anaerobic) with or without adding
additional nutrients or inhibitors (e.g., amino acids, glucose). Early work done by Fosdick
and colleagues in the 1940s and 1950s on salivary putrefaction and periodontal disease
showed that amines, indoles, and sulfides are produced in putrefied saliva concomitant
Microbial Aspects 27
with malodor production, especially if the saliva is incubated anaerobically in the pres-
ence of additional protein (Berg et al. 1946; Fosdick and Piez 1953).
Studies done by Tonzetich and colleagues (Tonzetich and Richter 1964) during the
1960s using saliva from healthy subjects, demonstrated the importance of volatile sulfide
compounds (VSCs, especially hydrogen sulfide and methyl mercaptan) as major detect-
able components of oral malodor. According to Tonzetich, volatile sulfides are the only
compounds that play a meaningful part in odor production. He showed that adding sulfur-
containing amino acid such as cysteine to the incubation mixture (precursor of hydrogen
sulfide) caused increased malodor production whereas the addition of nitrogen-containing
amino acid such as arginine (precursor of putrescine) or aromatic amino acid such as tryp-
tophan (precursor of indole) did not. Tonzetich claimed that the reason for the inability of
amines and indoles, despite their foul smell and low odor threshold, to increase salivary
malodor, was their low volatility (Tonzetich et al. 1967). In vitro, however, solutions con-
taining putrescine, cadaverine, and indole do yield odor across the pH range of 3–11 (Sterer
and Rosenberg, unpublished).
During the early 1970s, Tonzetich and colleagues reported the use of gas chromatography
coupled to a flame-photometric detector for the chemical analysis of breath malodor (Tonzetich
1971). Their findings linking volatile sulfides and malodor seemed to confirm the hegemony
of volatile sulfide compounds as the major malodorous components of breath malodor.
This viewpoint, however, has been challenged by other researchers, especially Kleinberg
and colleagues. They demonstrated that oral dryness can increase the concentration of
volatiles (Kleinberg et al. 2002). Furthermore, they showed that when the aqueous solu-
tions of odoriferous volatiles are allowed to dry on the skin, the smells of some amines,
indoles, and volatile fatty acids (VFA) are more pronounced and linger much longer than
the smell of the volatile sulfides (Kleinberg and Codipilly 1997). Kleinberg also showed
that incubating pure cultures of Gram-negative oral bacteria in the presence of various
amino acids, including nitrogen containing and aromatic ones, did result in malodor pro-
duction. Other researchers have also demonstrated significant correlations comparing odor
levels with cadaverine (Goldberg et al. 1994) and ammonia (Amano et al. 2002).
These results, taken together with clinical experience, may suggest that breath odors are
more complex, and in fact are composed of a “bouquet” of many different volatiles. This
may explain the different types and characteristics of breath odors, and the observation that
in certain individuals, odor does not correlate with one or more measured components. The
technical difficulties in measuring some of the malodor components such as low instru-
mental sensitivity or the inability of a method to detect certain compounds may also play
a part in underestimating the role of various breath malodor components.
Microbial Aspects
Malodor Producing Microorganisms
Much like other bacterial-associated ailments in the oral cavity (e.g., caries and periodontal
disease), there is an ongoing dispute among researchers as to whether oral malodor is
caused by specific bacteria (specific theory), various types of bacteria sharing the same
metabolic processes (nonspecific theory), or simply an overgrowth of the entire bacterial

population (bacterial load).
Early observations suggested that malodor production is a complex process. In 1946,
Berg and Fosdick (1946) tested the ability of 17 oral microorganisms to putrefy saliva and
increase malodor production following aerobic and anaerobic incubation. They found that
although all of the microorganisms caused some increase in salivary putrefaction, it was
evident that no single type of organism was capable of putrefying saliva as rapidly as the
mixtures normally present in the mouth.
Research also demonstrated that the putrefaction process was accompanied by a shift in
the bacterial composition of the incubation mixture. Shiota and Kunkel (1958) showed that
in incubated whole saliva, there was a decrease over time in the streptococci and lactobacilli
populations, whereas fusiforms, pH, indole, and ammonia levels increased. These processes
were inhibited when the saliva was incubated in the presence of glucose. In this instance,
streptococci and lactobacilli populations increased concomitant with a decrease in pH.
Subsequent research provided further evidence that the Gram-negative bacterial
population was primarily responsible for malodor production in vitro. McNamara and
colleagues (McNamara et al. 1972) showed that inoculation of liquid incubation medium
with Gram-negative oral bacteria, but not Gram-positive resulted in malodor produc-
tion. Furthermore, they showed that incubating whole saliva resulted in a bacterial shift
from a predominantly Gram-positive population to a predominantly Gram-negative
one. This shift was accompanied with malodor production and rise in pH. They also
showed that the addition of glucose inhibited malodor production while maintaining
Gram-positive predominance. Kleinberg and Codipilly (1997) also showed that incu-
bating pure bacterial cultures of Gram-negative oral bacteria species such as
Fusobacterium, Porphyromonas, and Prevotella in the presence of various free amino
acids resulted in malodor production whereas Gram-positive (Streptococci, Actinomyces,
and Lactobacilli) did not.
In order to evaluate whether specific types of bacteria are involved in oral malodor
production, bacterial samples were taken from the tongue dorsum of individuals with
and without oral malodor and identified using molecular techniques (e.g., PCR; polym-
erized chain reaction), thus allowing the identification of both cultivable and non-cul-
tivable bacteria (Haraszthy et al. 2007; Kazor et al. 2003; Riggio et al. 2008). Despite
the great variation between subjects reported by all the researchers, few bacteria
seemed to be unique to the oral malodor positive patients. These are specified in
Table 3.5.
All three studies reported greater bacterial diversity in oral malodor positive subjects,
and a difference in the proportions of bacterial population in each group was also noted.
Interestingly, all these studies reported Solobacterium moorei, a Gram-positive bacterium,
to be prevalent on the tongue dorsum of malodor positive subjects.
Despite the fact that two of these studies found Streptococcus salivarius prevalent in
all the subjects (Haraszthy et al. 2007; Riggio et al. 2008), one study reported it to be
found mostly in oral malodor negative subjects (Kazor et al. 2003). However, careful
examination of the data reveals that the subjects from the malodor positive group, who did
habor this bacterium, showed distinctively higher levels of volatile sulfides and malodor.
Interestingly, in one of the studies (Haraszthy et al. 2007), Fusobacterium nucleatum,
a putative malodor producing Gram-negative oral bacterium, was also present in all the
malodor negative subjects.
Microbial Aspects 29
Table 3.5 Bacteria associated with malodor from tongue dorsum

Solobacterium (Bulleidia) moorei (1, 2, 3)
Granulicatella elegans (2, 3)
Granulicatella adiacens (3)
Eubacterium species (1, 2, 3)
Firmicutes species (2)
Porphyromonas species (2)
Staphylococcus warneri (2)
Dialister species (1, 2)
Prevotella intermedia (2)
Prevotella pallens (3)
Prevotella shahii (3)
Prevotella tannerae (3)
Uncultured Prevotella sp. (3)
Atopobium parvulum (1)
Fusobacterium periodonticum (1)
Fusobacterium sulci (3)
Streptococcus phylotype (clone BW009) (1)
phylum TM7 phylotype (clone DR034) (1)
Cryptobacterium curtum (1)
Bacteroides forsythus (Tannerella forsythensis) (3)
Capnocytophaga gingivalis (3)
Capnocytophaga sputigena (3)
Escherichia coli (3)
Gemella haemolysans (3)
Gemella sanguinis (3)
Lachnospiraceae bacterium (3)
Megasphaera sp. oral clone (3)
Mogibacterium neglectum (3)
Neisseria perflava (3)
Neisseria subflava (3)
Rothia dentocariosa (3)
Streptococcus australis (3)
Streptococcus cristatus (3)
Uncultured Streptococcus sp. (3)
(1) Kazor et al. (2003); (2) Haraszthy et al. (2007); (3) Riggio et al. (2008)
Table 3.6 Bacteria associated with malodor from periodontal pockets

Prevotella intermedia (1, 2)
Prevotella nigrescens (2)
Bacteroides forsythus (1, 2)
Fusobacterium periodonticum (2)
Fusobacterium nucleatum ss nucleatum (1, 2)
Fusobacterium nucleatum ss vincentii (2)
Fusobacterium nucleatum ss polymorphum (2)
Treponema denticola (1, 2)
Treponema socranskii (2)
Porphyromonas gingivalis (1, 2)
Campylobacter rectus (2)
Campylobacter gracilis (2)
Capnocytophaga ochracea (2)
Capnocytophaga gingivalis (2)
Eubacterium nodatum (1, 2)
Selenomonas noxia (2)
Propionibacterium acnes (2)
Leptotrichia buccalis (2)
(1) Persson et al. (1990); (2) Torresyap et al. (2003)
Studies conducted on the bacteria of periodontal pockets aimed to identify the malodor
associated bacteria are summarized in Table 3.6.
Although some overlapping between malodor producing bacteria from periodontal
pockets and tongue dorsum can be seen (e.g., Eubacterium, Fusobacterium and Prevotella
species), some species (e.g., Treponema, Bacteroides and Porphyromonas) appear to be
more highly associated with malodor exuding from periodontal pockets.
Persson and coworkers (Persson et al. 1990) demonstrated the ability of certain perio-
pathogenic bacteria (e.g., Fusobacterium, Bacteroides, and Porphyromonas) sampled
from deep periodontal pockets to produce VSCs.
Some studies detected periopathogenic bacteria (Porphyromonas gingivalis, Tannerella
forsythia, Prevotella intermedia, Prevotella nigrescens, and Treponema denticola) in tongue
coating samples of subjects with oral malodor (Kato et al. 2005; Kurata et al. 2008; Tanaka
et al. 2004). However, the prevalence of these bacteria was significantly higher in subjects
who showed signs of periodontal disease (i.e., pocket depth of 4 mm and above), and higher
in subgingival plaque as compared to tongue coating and saliva (Kato et al. 2005).
Furthermore, the prevalence of these periopathogenic species in tongue coating samples
correlated with the tongue coating thickness (rather than area) and volatile sulfide levels,
References 31
but showed only poor correlations with malodor scores (Tanaka et al. 2004). Interestingly,
the improvement in periodontal health and oral VSCs resulting from periodontal therapy
did not seem to affect the prevalence of periodontal pathogens in the tongue coating (Kurata
et al. 2008). This raised the possibility that periodontal pathogens residing on the tongue
may serve as a reservoir for infection and reinfection of the periodontium.
Other studies have taken a different approach to studying the tongue dorsum microbial
differences between subjects with or without oral malodor. Rather than identifying spe-
cific bacteria, they relied on their biochemical properties, by quantifying the levels of
bacteria that are able to produce hydrogen sulfide (Hartley et al. 1996; Washio et al.
2005), as well as evaluating the total bacterial load. Both studies reported an increase in
bacterial load associated with oral malodor as well as an increase in the amount of hydro-
gen sulfide-producing bacteria. However, while one study reported that the proportions of
hydrogen sulfide producing bacteria were higher in the oral malodor positive group
(Hartley et al. 1996), the other found no difference in their proportion between groups
(Washio et al. 2005).
Most studies carried out on the microbial aspect of oral malodor report great variation
in bacterial populations among individual subjects. Given the relatively large prevalence of
this condition, it is thus unlikely that only several types of bacteria are involved.
Nevertheless, specific microbial factors appear to contribute strongly to malodor produc-
tion. It seems that microbial overgrowth (e.g., microbial load) as reflected mainly by tongue
biofilm thickness and subgingival plaque accumulation is a key factor in this condition.
The accumulation and thickening of the oral biofilms allows for the depletion of oxygen in
the deep layers of the biofilm and the creation of anaerobic niches. Whether or not this
process is accompanied by a change in the proportion of the various types of bacteria (floral
shift), or an increase in bacterial diversity, the overall bacterial activity leads to putrefactive
action in the oral cavity, which is the underlying cause of malodor production.
References
Amano, A., Yoshida, Y., Oho, T., Koga, T.: Monitoring ammonia to assess halitosis. Oral Surg.
Berg, M., Fosdick, L.S.: Studies in periodontal disease: II. Putrefactive organisms in the mouth.
J. Dent. Res. 25, 73–81 (1946)
Berg, M., Burrill, D.Y., Fosdick, L.S.: Chemical studies in periodontal disease III: putrefaction of
salivary proteins. J. Dent. Res. 25, 231–246 (1946)
Claus, D., Geypens, B., Rutgeerts, P., Ghyselen, J., Hoshi, K., Van Steenberghe, D., Ghoos, Y.:
Where gastroenterology and periodontology meets: determination of oral volatile organic
compounds using closed loop trapping and high resolution gas chromatography ion trap detec-
tion. In: Van Steenberghe, D., Rosenberg, M. (eds.) Bad breath a multidisciplinary approach,
pp. 15–27. Leuven University Press, Leuven (1996)
Codipilly, D.P., Kaufman, H.W., Kleinberg, I.: Use of a novel group of oral malodor measurements
to evaluate an anti-oral malodor mouthrinse (TriOralTM) in humans. J. Clin. Dent. 15(4),
98–104 (2004)
Cooke, M., Leeves, N., White, C.: Time profile of putrescine, cadaverine, indole and skatole in
human saliva. Arch. Oral Biol. 48(4), 323–327 (2003)
Fosdick, L.S., Piez, K.A.: Chemical studies in periodontal disease. X. Pap. chromatographic inves-
tigation putrefaction associated periodontitis. J. Dent. Res. 32(1), 87–100 (1953)
Gochman, N., Meyer, R.K., Blackwell, R.Q., Fosdick, L.S.: The amino acid decarboxylase of sali-
vary sediment. J. Dent. Res. 38, 998–1003 (1959)
Goldberg, S., Kozlovsky, A., Gordon, D., Gelernter, I., Sintov, A., Rosenberg, M.: Cadaverine as
a putative component of oral malodor. J. Dent. Res. 73(6), 1168–1172 (1994)
1113–1120 (2007)
Hartley, M.G., El Maaytah, M.A., McKenzie, C., Greenman, J.: The tongue microbiota of low
odour and malodourous individuals. Microb. Ecol. Health Dis. 9, 215–223 (1996)
Kato, H., Yoshida, A., Awano, S., Ansai, T., Takehara, T.: Quantitative detection of volatile sulfur
compound- producing microorganisms in oral specimens using real-time PCR. Oral Dis.
11(Suppl 1), 67–71 (2005)
Kazor, C.E., Mitchell, P.M., Lee, A.M., Stokes, L.N., Loesche, W.J., Dewhirst, F.E., Paster, B.J.:
Diversity of bacterial populations on the tongue dorsa of patients with halitosis and healthy
patients. J. Clin. Microbiol. 41(2), 558–563 (2003)
Kleinberg, I., Codipilly, D.M.: The biological basis of oral malodor formation. In: Rosenberg, M.
(ed.) Bad breath: research perspectives, pp. 13–39. Ramot publishing Tel Aviv University, Tel
Aviv (1997)
Kleinberg, I., Wolff, M.S., Codipilly, D.M.: Role of saliva in oral dryness, oral feel and oral mal-
odour. Int. Dent. J. 52(Suppl 3), 236–240 (2002)
Kostelc, J.G., Preti, G., Zelson, P.R., Stoller, N.H., Tonzetich, J.: Salivary volatiles as indicators of
periodontitis. J. Periodontal Res. 15(2), 185–192 (1980)
Kurata, H., Awano, S., Yoshida, A., Ansai, T., Takehara, T.: The prevalence of periodontopatho-
genic bacteria in saliva is linked to periodontal health status and oral malodour. J. Med.
Microbiol. 57(Pt 5), 636–642 (2008)
Mackie, R.I., Stroot, P.G., Varel, V.H.: Biochemical identification and biological origin of key odor
components in livestock waste. J. Anim. Sci. 76(5), 1331–1342 (1998)
McNamara, T.F., Alexander, J.F., Lee, M.: The role of microorganisms in the production of oral
malodor. Oral Surg. Oral Med. Oral Pathol. 34(1), 41–48 (1972)
Persson, S., Edlund, M.B., Claesson, R., Carlsson, J.: The formation of hydrogen sulfide and
methyl mercaptan by oral bacteria. Oral Microbiol. Immunol. 5(4), 195–201 (1990)
Riggio, M.P., Lennon, A., Rolph, H.J., Hodge, P.J., Donaldson, A., Maxwell, A.J., Bagg,
J.: Molecular identification of bacteria on the tongue dorsum of subjects with and without hali-
tosis. Oral Dis. 14(3), 251–258 (2008)
Ross, B.M., Dadgostar, N., Bloom, M., McKeown, L.: The analysis of oral air using selected ion
flow tube mass spectrometry in persons with and without a history of oral malodour. Int.
J. Dent. Hyg. 7(2), 136–143 (2009)
Shiota, T., Kunkel Jr., M.F.: In vitro chemical and bacterial changes in saliva. J. Dent. Res. 37(5),
780–787 (1958)
Sterer, N., Rosenberg, M.: Streptococcus salivarius promotes mucin putrefaction and malodor
production by Porphyromonas gingivalis. J. Dent. Res. 85(10), 910–914 (2006)
Sterer N, Shaharabany M, Rosenberg M: b-Galactosidase activity and H2S production in an exper-
imental oral biofilm. J. Breath Res. 3, 4pp (2009). doi:10.1088/1752-7155/3/1/016006
References 33
Tanaka, M., Yamamoto, Y., Kuboniwa, M., Nonaka, A., Nishida, N., Maeda, K., Kataoka, K.,
Nagata, H., Shizukuishi, S.: Contribution of periodontal pathogens on tongue dorsa analyzed
with real-time PCR to oral malodor. Microbes Infect. 6(12), 1078–1083 (2004)
Tonzetich, J.: Direct gas chromatographic analysis of sulphur compounds in mouth air in man.
Arch. Oral Biol. 16(6), 587–597 (1971)
Tonzetich, J., Richter, V.J.: Evaluation of volatile odoriferous components of saliva. Arch. Oral
Biol. 16, 39–46 (1964)
Tonzetich, J., Eigen, E., King, W.J., Weiss, S.: Volatility as a factor in the inability of certain
amines and indole to increase the odour of saliva. Arch. Oral Biol. 12(10), 1167–1175 (1967)
Torresyap, G., Haffajee, A.D., Uzel, N.G., Socransky, S.S.: Relationship between periodontal
pocket sulfide levels and subgingival species. J. Clin. Periodontol. 30(11), 1003–1010 (2003)
van den Velde, S., Quirynen, M., van Hee, P., van Steenberghe, D.: Halitosis associated volatiles
in breath of healthy subjects. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 853(1–2),
54–61 (2007)
Van den Velde, S., van Steenberghe, D., Van Hee, P., Quirynen, M.: Detection of odorous com-
pounds in breath. J. Dent. Res. 88(3), 285–289 (2009)
Washio, J., Sato, T., Koseki, T., Takahashi, N.: Hydrogen sulfide-producing bacteria in tongue
biofilm and their relationship with oral malodour. J. Med. Microbiol. 54(9), 889–895 (2005)
Odor Perception
4
Olfactory Psychophysics
The sense of smell is the least understood of all human senses. The olfaction process is a
complex one involving both physiological peripheral sensing and cognitive and emotional
central processing. The olfactory receptor neurons are situated in the olfactory epithelium
located in the upper portion of the nasal cavity. These cells project cilia into the mucus
lining of the nasal cavity, and those are responsible for the first stages of the olfaction
process. The binding of an odor molecule to the receptor results in an electrical signal that
is transducted through the neuron’s axon to the olfactory bulb, and causes the release of a
neurotransmitter (Berkowicz et al. 1994), which activates mitral and tufted cells within the
olfactory bulb to carry the information further into the brain. Within the brain, the olfac-
tory system is closely linked to areas of the brain that are involved with emotion (i.e.,
Amygdala) (Cain and Bindra 1972; Zald and Pardo 1997), memory, and learning (i.e., the
hippocampus).
We do not yet completely understand which odorants activate a certain receptor.
However, it seems that different combinations of olfactory neuron activation may have the
potential to explain the large variety of detectible odors. Research has shown that different
receptors families are expressed zonally across the olfactory epithelium (Strotmann et al.
1994), which coincides with zones of odorant sensitivity. This may suggest that odor quali-
ties are coded at the level of the olfactory bulb on the basis of distributed patterns of activ-
ity (Shepherd 1994).
Genetic variations in human odorant receptors may account for the vast differences in
odor perception between different individuals (Keller et al. 2007). Furthermore, genetic
differences in receptor expression may help to explain why some individuals with a normal
sense of smell may be “blinded” to a single odorant or a small group of closely related
odorant (i.e., specific anosmia) (Amoore 1977). However, repeated exposure to an odorant
did seem to induce the ability to detect it by subjects who were initially anosmic to it
(Dorries et al. 1989).
Research has shown that a certain amount of electrical activity is always present in the
olfactory neurons. This activity is referred to as baseline “noise” (Cain 1977), and is con-
sidered to increase olfaction sensitivity on the expense of specificity. This implies that the
receptors are easily activated by minute concentration of odorants even with marginal
odorant–receptor fit.

36 4 Odor Perception
The response to a certain odorant is terminated, presumably to allow the system to be

ready for the next stimulus. This process (i.e., adaptation) occurs both peripherally at the
receptor cell, and centrally in the brain. At the receptor cell level, olfactory adaptation is
calcium dependent (Kurahashi and Menini 1997), therefore this process may be affected
by medications or conditions that affect cellular calcium homeostasis. Central adaptation
mechanism is not yet understood. However, unlike receptor cell adaptation that is consid-
ered short term (minutes), central adaptation may last for as long as 4 weeks (Dalton and
Wysocki 1996).
Various diseases and conditions may affect olfactory function. For example, research
has shown that the neurotransmitter dopamine decreases the baseline activity (i.e., “noise”)
of mitral cells in the olfactory bulb (Duchamp-Viret et al. 1997). Therefore, in patients
with Parkinson’s disease in which dopamine synthesis is impaired, the ability to identify
odors may be reduced (Doty et al. 1991). These patients’ olfactory disorder was shown to
be independent of the cognitive, perceptual-motor, and memory manifestations of the dis-
ease (Doty et al. 1989).
Most studies conducted on the relationship between gender and olfaction have con-
cluded that at least for some odorants, females perform better than males in odor detection,
identification, and discrimination (Doty and Cameron 2009). Estrogen modulates the
activity of retinoic acid, an important factor in olfactory cells differentiation (Balboni et al.
1991). This might explain the observation that premenopause females tend to perform bet-
ter than males in olfactory function tests (Wysocki and Gilbert 1989). However, a recent
systematic review that examined the data about sex hormone alterations (e.g., menstrual
cycle, pregnancy, gonadectomy, and hormone replacement therapy) and human olfactory
function concluded that the relationship between the two is complex and any simple expla-
nation for any association between them is tenuous (Doty and Cameron 2009). One recent
study showed that females of three different age groups (19–39, 40–59, >60) performed
significantly better than males for both odor threshold and odor discrimination, thus dem-
onstrating higher olfactory sensitivity (Thuerauf et al. 2009). The researchers attributed
this to the link between odors and emotional reactivity, since females demonstrated better
emotion-linked memory (Canli et al. 2002).
Cognitive factors have been shown to impact human odor perception. Research showed
that subjects who were given a negative description of an odor gave higher intensity scores,
perceived it as irritating, and were less adaptive to it than those who were given a neutral
or positive description (Dalton et al. 1997).
Taken together, these physiological and environmental factors may help to explain the
high intra- and inter-individual variability seen in psychophysical research on olfactory
threshold (Stevens et al. 1988).
Odor Mixtures
Naturally occurring smells such as breath odors are usually a complex mixture of various
odorants. Unlike some other sensory systems in which the intensity of a complex signal is
the sum of its components (i.e., additivity), in olfaction this rule does not seem to apply.
Odor Perception and Odor Evaluation Panels 37
Studies done on two component mixtures show that in most cases, mixing the odorants
results in the suppression of the perceived intensity of one or both odors (Laing et al.
1984). Although the strength of an odor may be increased by the presence of another
(i.e., synergism), this is rarely seen in two component mixtures. However, some
researchers have reported a substantial synergistic effect in a complex mixture of many
odorants (Laska and Hudson 1991) at concentration too low to be sensed individually
(i.e., subthreshold).
Some studies have been conducted on the interactions of unpleasant odor components
(Berglund 1974). These studies showed that the odor intensity of two-, three- and four-
component mixtures of volatile sulfides (hydrogen sulfide, dimethylsulfide, dimethyldisul-
fide, and methylmercaptan) slightly exceeded the intensity of the single odorants. Another
more recent study (Laing et al. 1994), conducted on odor interactions of malodorous com-
ponents (hydrogen sulfide, butanethiol, skatol, and isovaleric acid), concluded that suppres-
sion was the dominant perceptual effect. It also concluded that there was a substantial loss
of identity of the individual odorants in the mixture, a finding that is in agreement with other
studies, which demonstrated that humans have considerable difficulty in identifying three or
four odorants in a given mixture (Laing and Francis 1989). Interestingly, it seems that the
malodor of the mixture was usually perceived as more unpleasant than any of the individual
components (Laing et al. 1994). This suggested that the loss of odorant identity was not
mostly due to the reduced odor intensity of the component but rather due to the blending of
one or more of the components to produce an even fouler smell (Laing et al. 1994).
Odor Perception and Odor Evaluation Panels
Organoleptic scores given by odor judges are the most common means of evaluating a
malodor nuisance and are considered as the golden standard in breath odor investigations.
However, given the large interpersonal variation in odor perception, using a panel of sev-
eral evaluators is recommended.
Studies conducted on the implementation of odor perception principals on the accuracy
and repeatability of organoleptic (odor judge) measurements stress the importance of
proper panel selection and training techniques. For example, it was suggested that using
varying concentration of odorant samples (i.e., n-butanol) in a double blind manner, was
less repetitive and more effective than the standard one-concentration method (Capelli
et al. 2010). Although olfactory memory seems to be linked to the experience of the panel-
ists in recognizing the measured malodor (i.e., stimulus familiarity), trained panelists were
shown to be more accurate than non-trained (naïve) ones, regardless of their level of famil-
iarity. However, panel experience did allow the trained panelists to verbalize their percep-
tion more accurately when the stimuli were familiar (Lesschaeve and Issanchou 1996).
Rosenberg and coworkers (Rosenberg et al. 1991) found that inter-examiner correla-
tions among judges with no prior experience in scoring breath odors were mostly signifi-
cant with r-values ranging from 0.14 to 0.49.
Other researchers have also reported that training improves the accuracy of odor inten-
sity scoring by both experienced and inexperienced panelists (Nachnani et al. 2005).
38 4 Odor Perception
Interestingly, training did not seem to improve the ability to discriminate and identify
different odorants in a mixture (Livermore and Laing 1996).
Researchers who studied the relationship between oral malodor intensity scale and the
concentration of some of its components (e.g., hydrogen sulfide, skatole, cadaverine) sug-
gested that the intensity score reflects the odorant–receptor binding ratio (e.g., increasing
saturation), which is logarithmic in nature and depends on the odor threshold and odor
power (i.e., the ratio between odor score and concentration) of each odorant (Greenman
et al. 2005). Understanding that the organoleptic oral malodor intensity scale is indeed an
exponential scale may enable the design of better ways to train and calibrate the odor judge
panel.
References
Amoore, J.E.: Specific anosmia and the concept of primary odors. Chem. Senses Flavour 2,
267–281 (1977)
Balboni, G.C., Zonefrati, R., Repice, F., Barni, T., Vannelli, G.B.: Immunohistochemical detection
of EGF and NGF receptors in human olfactory epithelium. Boll. Soc. Ital. Biol. Sper. 67(10–
11), 901–906 (1991)
Berglund, B.: Quantitative and qualitative analysis of industrial odors with human observers. Ann.
NY Acad. Sci. 237, 35–51 (1974)
Berkowicz, D.A., Trombley, P.Q., Shepherd, G.M.: Evidence for glutamate as the olfactory recep-
tor cell neurotransmitter. J. Neurophysiol. 71(6), 2557–2561 (1994)
Cain, W.S.: Differential sensitivity for smell: “noise” at the nose. Science 195(4280), 796–798
(1977)
Cain, D.P., Bindra, D.: Responses of amygdala single units to odors in the rat. Exp. Neurol. 35(1),
98–110 (1972)
Canli, T., Desmond, J.E., Zhao, Z., Gabrieli, J.D.: Sex differences in the neural basis of emotional
memories. Proc. Natl Acad. Sci. USA 99(16), 10789–10794 (2002)
Capelli, L., Sironi, S., Del Rosso, R., Centola, P., Bonati, S.: Improvement of olfactometric mea-
surement accuracy and repeatability by optimization of panel selection procedures. Water Sci.
Technol. 61(5), 1267–1278 (2010)
Dalton, P., Wysocki, C.J.: The nature and duration of adaptation following long-term odor expo-
sure. Percept. Psychophys. 58(5), 781–792 (1996)
Dalton, P., Wysocki, C.J., Brody, M.J., Lawley, H.J.: The influence of cognitive bias on the per-
ceived odor, irritation and health symptoms from chemical exposure. Int. Arch. Occup. Environ.
Health 69(6), 407–417 (1997)
Dorries, K.M., Schmidt, H.J., Beauchamp, G.K., Wysocki, C.J.: Changes in sensitivity to the odor
of androstenone during adolescence. Dev. Psychobiol. 22(5), 423–435 (1989)
Doty, R.L., Cameron, E.L.: Sex differences and reproductive hormone influences on human odor
perception. Physiol. Behav. 97(2), 213–228 (2009)
Doty, R.L., Riklan, M., Deems, D.A., Reynolds, C., Stellar, S.: The olfactory and cognitive deficits
of Parkinson’s disease: evidence for independence. Ann. Neurol. 25(2), 166–171 (1989)
Doty, R.L., Perl, D.P., Steele, J.C., Chen, K.M., Pierce Jr., J.D., Reyes, P., Kurland, L.T.: Olfactory
dysfunction in three neurodegenerative diseases. Geriatrics 46(Suppl 1), 47–51 (1991)
Duchamp-Viret, P., Coronas, V., Delaleu, J.C., Moyse, E., Duchamp, A.: Dopaminergic modula-
tion of mitral cell activity in the frog olfactory bulb: a combined radioligand binding-electro-
physiological study. Neuroscience 79(1), 203–216 (1997)
References 39
Greenman, J., El-Maaytah, M., Duffield, J., Spencer, P., Rosenberg, M., Corry, D., Saad, S., Lenton,
P., Majerus, G., Nachnani, S.: Assessing the relationship between concentrations of malodor
compounds and odor scores from judges. J. Am. Dent. Assoc. 136(6), 749–757 (2005)
Keller, A., Zhuang, H., Chi, Q., Vosshall, L.B., Matsunami, H.: Genetic variation in a human odor-
ant receptor alters odour perception. Nature 449(7161), 468–472 (2007)
Kurahashi, T., Menini, A.: Mechanism of odorant adaptation in the olfactory receptor cell. Nature
385(6618), 725–729 (1997)
Laing, D.G., Francis, G.W.: The capacity of humans to identify odors in mixtures. Physiol. Behav.
46(5), 809–814 (1989)
Laing, D.G., Panhuber, H., Willcox, M.E., Pittman, E.A.: Quality and intensity of binary odor
mixtures. Physiol. Behav. 33(2), 309–319 (1984)
Laing, D.G., Eddy, A., Best, D.J.: Perceptual characteristics of binary, trinary, and quaternary odor
mixtures consisting of unpleasant constituents. Physiol. Behav. 56(1), 81–93 (1994)
Laska, M., Hudson, R.: A comparison of the detection thresholds of odour mixtures and their
components. Chem. Senses 16(6), 651–662 (1991)
Lesschaeve, I., Issanchou, S.: Effects of panel experience on olfactory memory performance: influ-
ence of stimuli familiarity and labeling ability of subjects. Chem. Senses 21(6), 699–709 (1996)
Livermore, A., Laing, D.G.: Influence of training and experience on the perception of multicom-
ponent odor mixtures. J. Exp. Psychol. Hum. Percept. Perform. 22(2), 267–277 (1996)
Nachnani, S., Majerus, G., Lenton, P., Hodges, J., Magallanes, E.: Effects of training on odor
judges scoring intensity. Oral Dis. 11(Suppl 1), 40–44 (2005)
Rosenberg, M., Septon, I., Eli, I., Bar-Ness, R., Gelernter, I., Brenner, S., Gabbay, J.: Halitosis
measurement by an industrial sulphide monitor. J. Periodontol. 62(8), 487–489 (1991)
Shepherd, G.M.: Discrimination of molecular signals by the olfactory receptor neuron. Neuron
13(4), 771–790 (1994)
Stevens, J.C., Cain, W.S., Burke, R.J.: Variability of olfactory thresholds. Chem. Senses 13,
643–653 (1988)
Strotmann, J., Wanner, I., Helfrich, T., Beck, A., Meinken, C., Kubick, S., Breer, H.: Olfactory
neurones expressing distinct odorant receptor subtypes are spatially segregated in the nasal
neuroepithelium. Cell Tissue Res. 276(3), 429–438 (1994)
Thuerauf, N., Reulbach, U., Lunkenheimer, J., Lunkenheimer, B., Spannenberger, R., Gossler, A.,
Maihofner, C., Bleich, S., Kornhuber, J., Markovic, K.: Emotional reactivity to odors: olfactory
sensitivity and the span of emotional evaluation separate the genders. Neurosci. Lett. 456(2),
74–79 (2009)
Wysocki, C.J., Gilbert, A.N.: National Geographic Smell Survey. Effects of age are heterogenous.
Ann. NY Acad. Sci. 561, 12–28 (1989)
Zald, D.H., Pardo, J.V.: Emotion, olfaction, and the human amygdala: amygdala activation during
aversive olfactory stimulation. Proc. Natl Acad. Sci. USA 94(8), 4119–4124 (1997)
Breath Odors of Nasal
and Pharyngeal Origin 5
According to reports from various multidisciplinary breath odor clinics around the world,
some 4–8% of breath odor cases are ENT-related conditions (Quirynen et al. 2009;
Seemann et al. 2006). These include nasal and pharyngeal infections and conditions such
as: chronic sinusitis, chronic (caseous) tonsillitis, foreign bodies, and craniofacial anoma-
lies (e.g., cleft palate). These are specified in Table 5.1.
Chronic Sinusitis
The sinuses are drained and ventilated into the nasal cavity through small orifices
(i.e., ostium). Any obstruction in the sinuses’ drainage resulting from malformation or
disease may cause sinus secretion stagnation and bacterial infection (Stammberger 1986).
This condition differs from acute sinusitis in its symptoms, which are mostly related to
an increase in nasal secretions (i.e., postnasal drip). These include chronic cough, pro-
ductive throat cleaning, sniffling, and halitosis (Bunzen et al. 2006; Tatli et al. 2001).
Furthermore, Gram-negative anaerobic bacteria (e.g., Bacteroides sp. and Fusobacteria
sp.) that are known producers of VSC have been shown to inhabit the maxillary sinuses
(Brook 1981).
In those cases in which the breath odor results from a nasal infection, the malodor is
typically felt much stronger from the air exhaled through the nose (Rosenberg 1996).
However, it is important to stress that postnasal drip may be an important factor in tongue
malodor (Rosenberg and Leib 1997), therefore an additional oral malodor component is
expected to be present in cases of chronic sinusitis.
The diagnosis of chronic sinusitis is best confirmed by an otolaryngologic examination
using a flexible endoscope (Finkelstein 1997a). The flexible endoscope allows the clini-
cian to examine the areas of inflammation or pathologic drainage in the intranasal struc-
tures, which cannot otherwise be detected using anterior rhinoscopy or plain sinus
radiographs.
Functional endoscopic sinus surgery (FESS) is currently the preferred treatment for
chronic rhinosinusitis. In a retrospective clinical study carried out in Brazil on patients
suffering from chronic rhinosinusitis (Bunzen et al. 2006), it was shown that in 10 out of
24 patients (41.6%) who initially complained of halitosis, eight of them reported improve-
ment following this procedure.

42 5 Breath Odors of Nasal and Pharyngeal Origin
Table 5.1 ENT-related breath odor inducing conditions

Pathology Signs and Diagnosis Recommended
symptoms treatment
Chronic Nasal malodor, post Flexible endoscopy Functional
rhinosinusitis nasal drip (PND) of the nasal cavity endoscopic sinus
surgery (FESS)
Chronic caseous Occasional oral Tonsils smelling test CO2 laser cryptolysis
tonsillitis malodor, tonsilloliths
Foreign bodies Nasal malodor Anterior rhinoscopy Foreign body
(unilateral), purulent and flexible extraction
unilateral nasal endoscopy of the
discharge nasal cavity
Craniofacial Nasal and oral Clinical examination Corrective surgery
anomalies malodor, cleft palate
Chronic Caseous Tonsillitis
The tonsils contain tubular invaginations known as crypts, which extend from the tonsils’
surface to deep within its parenchyma (Finkelstein et al. 2004). In some cases, caseous
secretions may be retained within these crypts resulting in caseous tonsillitis that is consid-
ered a variant of chronic tonsillitis. This condition is characterized by the formation of
calcareous concretions known as tonsilloliths, or tonsillar calculi (Finkelstein et al. 2004).
Early clinical observations (Castellani 1930) suggested that this type of chronic tonsilli-
tis (which they termed granulomycosis of the crypts) may be a cause for halitosis (i.e., foe-
tor oris). These researchers noticed that “in certain cases of granulomycosis a most offensive
odour is emitted when the granules are extracted and squashed.” They further noticed that
these granules contained a large variety of bacteria, and were even able to isolate and grow
certain Gram-negative bacilli “which produce in agar culture exactly the same offensive
odour as was noticeable in the patient’s breath, and on squashing the white granules.”
A more recent study on the microbial composition of tonsilloliths from six individuals,
conducted using culture-independent molecular methods (i.e., PCR), demonstrated the
presence of many anaerobic bacterial species (Tsuneishi et al. 2006). These included
Eubacterium, Fusobacterium, Megasphaera, Porphyromonas, Prevotella, Selenomonas,
and Tannerella, all of which are associated with VSC production.
Chronic tonsillitis-associated malodor seems to occur intermittently (Fletcher and Blair
1988) and may be concomitant with the appearance and exfoliation of the tonsilloliths.
Research showed that patients suffering from chronic caseous tonsillitis had a significantly
higher VSC levels when tonsilloliths were present (Rio et al. 2008). Furthermore, one case
reported in Japan showed that VSC readings sharply decreased following tonsilloliths
removal (Kato et al. 2005).
Tonsil-associated malodor does not respond to standard oral care treatments (Talebian
et al. 2008). Therefore, once intraoral origins have been ruled out and the malodor persists,
especially if the malodor coincides with the appearance of tonsilloliths, then the tonsils are
a likely source of the malodor.
Foreign Bodies 43
In the past, halitosis of tonsillar origin was considered a valid indication for adenoton-
sillectomy (Arnold 1953). However, since then a more conservative method of treatment
has been applied. This method, termed laser cryptolysis (Finkelstein et al. 2004) or laser
cryptolysis by coagulation (Rio et al. 2008) is aimed at opening the crypts ostium, thus
preventing caseum retention. This procedure is carried out using CO2 laser under local
anesthesia. Research demonstrated that patient suffering from chronic caseous tonsillitis
showed significant reduction in VSC levels following this treatment (Rio et al. 2008).
Foreign Bodies
Young children typically 2–4 years of age tend to insert small objects such as plastic beads,
buttons, and small toy parts into their nostrils (Kiger et al. 2008). This type of behavior
usually ceases after the age of 5, although it may continue in older children (e.g. 10 or
11 years of age) in cases of attention deficit hyperactivity disorder (ADHD)(Perera et al.
2009), or at any age in cases of severe mental retardation (Rosenberg and Leib 1997).
In most cases, these foreign objects consist of plastic, cotton, organic matter, or paper,
materials that would not normally appear in x-rays and can only be detected using endos-
copy (Fig 5.1).
Fig. 5.1 Variety of foreign objects extracted from the nose of children (Kindly provided by
Dr. M. Marcus)
Typically, the chief complaint made by the child’s parents at the doctor’s office would
refer to the child’s severe body odor (Katz et al. 1979; Rosenberg and Leib 1997). However,
a thorough clinical examination will usually reveal that the malodor is emanating from the
nasal cavity (Rosenberg and Leib 1997) or the mouth (Syfert 1979). Upon examination, a
purulent inflammation of one nostril is noted, accompanied by a unilateral malodorous
discharged from the same nostril. This smelly discharge is smeared by the child on clothes
and hair, therefore creating the wrong impression of body odor (Syfert 1979). This can be
verified by smelling areas on the child’s body that are normally out of reach (e.g., back and
ankles) and would not present the same malodor (Rosenberg and Leib 1997).
Nasal foreign bodies in children can usually be removed using simple techniques (Kiger
et al. 2008). However, when left in place for years, these objects may calcify over time creat-
ing a growing rhinolith (i.e., nasal stone), which may result in a unilateral nasal obstruction
(Brehmer and Riemann 2010) in addition to the associated malodor. Furthermore, although
the nasal cavity is the most common site of breath odor causing foreign bodies, one case of a
malodor causing pharyngeal foreign body was reported in the literature (Kurul and Kandogan
2002), suggesting that putrefying foreign objects may also be lodged in the pharynx.
In most cases of foreign bodies’ related breath odor, the malodor did not respond to
antibiotic treatment. However, foreign body extraction results in immediate resolution of
the foul odor.
Craniofacial Anomalies
Because of the various malformations in nasal structures observed in patients with craniofacial
anomalies such as deviated nasal septum, deformed medial turbinate, underdeveloped maxil-
lary sinuses, maxillary growth deficits, choanal stenosis or atresia, atresia of the nostrils, mal-
formed external nasal valve, incompetent velopharyngeal valve, presence of pharyngeal flap,
and impairment of mucociliary transport, chronic paranasal sinusitis with accompanying breath
odor formation is more frequently seen in patients with cleft palate (Finkelstein et al. 1990).
These structural malformations in the external and internal nasal passages may also
cause nasal obstructions or high nasal airway resistance that may result in mouth breathing
(Finkelstein 1997b), in itself a risk factor for oral malodor. Furthermore, poorer oral hygiene
and dental condition have been observed in cases of cleft palate (Wong and King 1998).
Both of these are also contributing factors to oral malodor formation. Finally, oronasal fis-
tulas are often present in these patients and can serve as a continuous source of nasal con-
tamination by oral bacteria. These fistulas may also facilitate the insertions of foreign bodies
into the nasal cavity such as food or dental impression materials (Finkelstein 1997b).
Reports on breath odors in patients with craniofacial anomalies are mostly anecdotal
case reports. However, few clinical studies were published. One of these studies demon-
strated no difference between the oral VSC levels of patients with repaired clefts and the
control group (Monteiro-Amado et al. 2005), whereas a second study showed that both
oral and nasal VSC levels were elevated in cleft patients, especially in the affected nostril
(Doruk et al. 2008). These results suggest that if malodor still persists following cleft
repair, then nasal malformations or infection should be examined next.
References 45
References
Arnold, J.W.: Controversial problems in adenotonsillectomy. Calif. Med. 78(5), 444–449 (1953)
Brehmer D, Riemann R.: The rhinolith-a possible differential diagnosis of a unilateral nasal
obstruction. Case Report Med. 2010(845671) (2010)
Brook, I.: Aerobic and anaerobic bacterial flora of normal maxillary sinuses. Laryngoscope 91(3),
372–376 (1981)
Bunzen, D.L., Campos, A., Leao, F.S., Morais, A., Sperandio, F., Caldas Neto, S.: Efficacy of
functional endoscopic sinus surgery for symptoms in chronic rhinosinusitis with or without
polyposis. Braz. J. Otorhinolaryngol. 72(2), 242–246 (2006)
Castellani, A.: Foetor oris of tonsillar origin and certain bacilli causing it. Lancet 1, 623–624 (1930)
Doruk, C., Ozturk, F., Ozdemir, H., Nalcaci, R.: Oral and nasal malodor in patients with and with-
out cleft lip and palate who had undergone orthodontic therapy. Cleft Palate Craniofac. J. 45(5),
481–484 (2008)
Finkelstein, Y.: The otolaryngologist and the patient with halitosis. In: Rosenberg, M. (ed.) Bad
Breath Research Perspectives, pp. 175–187. Ramot Publishing – Tel Aviv University, Tel Aviv
(1997a)
Finkelstein, Y.: Halitosis in patients with craniofacial anomalies. In: Rosenberg, M. (ed.) Bad
Breath Research Perspectives, pp. 189–200. Ramot Publishing – Tel Aviv University, Tel Aviv
(1997b)
Finkelstein, Y., Talmi, Y.P., Zohar, Y.: On the cause of sinusitis in patients with cleft palate. Arch.
Otolaryngol. Head Neck Surg. 116(4), 490–491 (1990)
Finkelstein, Y., Talmi, Y.P., Ophir, D., Berger, G.: Laser cryptolysis for the treatment of halitosis.
Otolaryngol. Head Neck Surg. 131(4), 372–377 (2004)
Fletcher, S.M., Blair, P.A.: Chronic halitosis from tonsilloliths: a common etiology. J. La. State
Med. Soc. 140(6), 7–9 (1988)
Kato, H., Yoshida, A., Awano, S., Ansai, T., Takehara, T.: Quantitative detection of volatile sulfur
compound- producing microorganisms in oral specimens using real-time PCR. Oral Dis.
11(Suppl 1), 67–71 (2005)
Katz, H.P., Katz, J.R., Bernstein, M., Marcin, J.: Unusual presentation of nasal foreign bodies in
children. JAMA 241(14), 1496 (1979)
Kiger JR, Brenkert TE, Losek JD.: Nasal foreign body removal in children. Pediatr. Emerg. Care
24(11), 785–92; quiz 790–2 (2008)
Kurul, S., Kandogan, T.: Pharyngeal foreign body in a child persisting for three years. Emerg.
Med. J. 19(4), 361–362 (2002)
Monteiro-Amado, F., Chinellato, L.E., de Rezende, M.L.: Evaluation of oral and nasal halitosis
parameters in patients with repaired cleft lip and/or palate. Oral Surg. Oral Med. Oral Pathol.
Oral Radiol. Endod. 100(6), 682–687 (2005)
Perera H, Fernando SM, Yasawardena AD, Karunaratne I.: Prevalence of attention deficit hyper-
activity disorder (ADHD) in children presenting with self-inserted nasal and aural foreign bod-
ies. Int. J. Pediatr. Otorhinolaryngol. [Epub ahead of print] (2009
Periodontol. 36(11), 970–975 (2009)
Rio, A.C., Franchi-Teixeira, A.R., Nicola, E.M.: Relationship between the presence of tonsilloliths
and halitosis in patients with chronic caseous tonsillitis. Br. Dent. J. 204(2), E4 (2008)
475–482 (1996)
Rosenberg, M., Leib, E.: Experiences of an Israeli malodor clinic. In: Rosenberg, M. (ed.) Bad Breath
Research Perspectives, pp. 137–148. Ramot Publishing – Tel Aviv University, Tel Aviv (1997)
Seemann, R., Bizhang, M., Djamchidi, C., Kage, A., Nachnani, S.: The proportion of pseudo-halitosis
patients in a multidisciplinary breath malodour consultation. Int. Dent. J. 56(2), 77–81 (2006)
Stammberger, H.: Endoscopic endonasal surgery–concepts in treatment of recurring rhinosinusitis.
Part I. Anatomic and pathophysiologic considerations. Otolaryngol. Head Neck Surg. 94(2),
143–147 (1986)
Syfert, D.F.: Nasal foreign bodies and bromidrosis. JAMA 242(10), 1031 (1979)
Talebian A, Tazhibi M, Iranpoor R, Semyari H, Taherzadeh M.: Relationship between tonsil odor
and oral malodor: a clinical study on 48 Iranian patients. J. Breath Res. 2(017016) (2008)
Tatli, M.M., San, I., Karaoglanoglu, M.: Paranasal sinus computed tomographic findings of chil-
dren with chronic cough. Int. J. Pediatr. Otorhinolaryngol. 60(3), 213–217 (2001)
Tsuneishi, M., Yamamoto, T., Kokeguchi, S., Tamaki, N., Fukui, K., Watanabe, T.: Composition of
the bacterial flora in tonsilloliths. Microbes Infect. 8(9–10), 2384–2389 (2006)
Wong, F.W., King, N.M.: The oral health of children with clefts–a review. Cleft Palate Craniofac.
J. 35(3), 248–254 (1998)
Breath Odors and the
Gastrointestinal Tract 6
In the absence of well-informed science, people intuitively associate breath odors with the
digestive system. Perhaps, the stomach odors that arise transiently during eructation (burp-
ing) lead many to assume that breath odor may originate in the stomach. Looking into old
medical texts on this topic (Howe 1898; Shifman et al. 2002), in which indigestion, consti-
pation, and dyspepsia are considered prime causes of breath odors, further illustrates this
point. Even nowadays, patients complaining of breath odors to their physicians or dentists
are often referred to the gastroenterologist (Delanghe et al. 1996).
Most researchers agree that the gastrointestinal tract is rarely involved in breath odor
production. The esophagus is a closed flat tube, and odors are unlikely to be steadily
released into the oral cavity. Yet, some researchers have reported evidence that give sup-
port to a possible link between breath odor and various gastrointestinal diseases and symp-
toms. At first, these were mostly anecdotal observations such as case reports linking
between pyloric stenosis and halitosis (Tydd and Dyer 1974). However, large controlled
studies were also conducted showing higher prevalence of halitosis in patients suffering
from inflammatory bowel diseases (Katz et al. 2003). Most of these studies focused on two
gastrointestinal conditions; reflux and Helicobater pylori infection.
Gastroesophageal Reflux Disease (GERD)
Reflux (regurgitation), commonly referred to as heartburn, is the emersion of the acidic

content of the stomach through the esophagus. Although, no rational was offered as to why
this specific condition was considered as a cause for breath odors, several studies (Di Fede
et al. 2008; Moshkowitz et al. 2007; Struch et al. 2008) claimed to show a possible associa-
tion between GERD and halitosis. However, rather than relying on objective parameters
(e.g., odor judge, sulfide levels), these studies based their breath odor diagnosis on self-
reported questionnaires. Unfortunately, when it comes to halitosis, self-perception is nota-
bly unreliable (for further details see Chap. 10). Furthermore, the largest of these studies
(Struch et al. 2008) conducted in a general population (over 3,000 participants) considered
both “bad breath” and “bad taste in your mouth” as positive for halitosis. Another criticism
is that oral conditions, more commonly associated with breath odors, were not taken into
account. For example, in the same study mentioned above, subjects self-reporting of hali-
tosis had higher prevalence of gingival bleeding, which is directly related to oral malodor.

48 6 Breath Odors and the Gastrointestinal Tract
Another study (Carr et al. 2000) conducted in small children with or without GERD by
reviewing their medical charts did not show any difference between the prevalence of hali-
tosis in GERD positive and controls (Table 6.1).
Helicobacter pylori (Hp) Infection
Helicobacter pylori is a spiral Gram-negative bacterium that is related to gastritis, gastric

ulcer, and cancer. Associating Hp with breath malodor also started with an anecdotal
observation. In the mid 1980s, Marshall ingested the cultivated bacteria to develop gastri-
tis and fulfill Koch’s postulate (Marshall et al. 1985). While being infected, his colleagues
noticed “putrid” odor in his breath.
Several studies were conducted in order to test the possible association between Hp infec-
tion and breath odors. Some of these studies (Gasbarrini et al. 1998; Moshkowitz et al. 2007;
Schubert et al. 1992; Werdmuller et al. 2000) failed to find a link between the two. Again,
these studies relied on self-reported halitosis rather than an objective means as the criterion
for determining the presence of breath odors. Furthermore, few, if any, attempts were made
to examine possible oral causes for the presence of malodor. Conversely, other studies
(Candelli et al. 2003; Claus et al. 1996; Li et al. 2005) did show an association between Hp
infection and halitosis. One of these studies (Claus et al. 1996) did rely on objective param-
eters (i.e., odor judge scores and GC measurements) in order to establish the presence of
halitosis. Moreover, oral malodor-related parameters (PI-plaque index, GI-gingival index,
PPD-periodontal pockets depth, TC-tongue coating) were also determined. Results of this
study showed significantly higher mouth air malodor and H2S levels in Hp-positive subjects,
whereas no difference was seen in oral health parameters (however they did differ in age
groups). Interestingly, this study links between the presence of an Hp infection and breath
odors of oral origin (mouth air) rather than extra oral origin (lung air) (Table 6.2).
Another factor that may cause physicians to link Hp infection and breath odors is the
clinical observation that the malodor tends to disappear following Hp eradication treat-
ment. The first report to this effect was published in the early 1990s (Tiomny et al. 1992),
showing the disappearance of breath malodor (as reported by respective family members)
in four out of five patients following Hp eradication treatment (4 weeks) with metronida-
zole (although an earlier case report by Tydd in 1974, showed the same effect with tetra-
cycline in pyloric stenosis patients). Several other larger studies (Ierardi et al. 1998;
Katsinelos et al. 2007; Serin et al. 2003; Shashidhar et al. 2000) have also reported similar
results. However, malodor production is for the most part bacterial in origin and any use of
antibiotics, especially those targeted against Gram-negatives and anaerobes such as met-
ronidazole, would be expected to affect the oral population of malodor producing bacteria
and decrease or eliminate the malodor for a certain period of time.
To shed more light on this problem, one study (Ierardi et al. 1998) employed an antisep-
tic mouthwash containing chlorhexidine as a control showing no effect on oral volatile
sulfide compounds levels in HP-positive subjects, whereas eradication therapy did reduce
them. Another study (Katsinelos et al. 2007) offered long-term follow-up that showed the
resolving of the malodor over a period of more than 6 months.
Nevertheless, other reports (Delanghe et al. 1996) and clinical experience show that
3–6 weeks following the end of the antibiotic course, the malodor gradually returns even
though Hp is completely eradicated from the stomach (Table 6.3).
Table 6.1 Reflux and halitosis
Reference Aims Malodor criteria Findings Criticism and comments
Carr et al. (2000) ENT symptoms and Charts review 15% halitosis in GERD+
gastroesophageal reflux 24% halitosis in GERD–
disease (GERD) in small
children (n = 295)
Moshkowitz et al. (2007) Possible association between Questionnaire Halitosis was associated Self reported
GERD and halitosis with GERD, heartburn,
(n = 132) belching and sour taste
Struch et al. (2008) Self reported halitosis and Interview: “do you often GERD related symptoms Self reported (+Associating
GERD in general population suffer from bad taste in your (heartburn, acid regurgita- bad taste with bad breath)
(n = 3,005) mouth or from bad breath?” tion) were associated with
halitosis subjects complain-
ing of halitosis had more
gingival bleeding and
PPD > 4 mm
Di Fede et al. (2008) Oral manifestations in “Subjective halitosis” 49% halitosis in GERD+ Self reported
GERD (n = 400) 31% halitosis
in GERD– (p = 0.0004)
49
50
Table 6.2 Hp and halitosis

Reference Aims Malodor/oral parameters Findings and conclusions Criticism and comments
Schubert et al. (1992) Symptoms, gastritis and Hp InterviewHp: biopsy No correlation between Hp Self reported
and halitosis
Gasbarrini et al. (1998) Hp infection and GI Hp: [13C] urea breath test Prevalence of halitosis did Self reported
symptoms in IDDM not differ between Hp + and
– groups
Werdmuller et al. (2000) Clinical presentation of Halitosis by question- Hp + 29% halitosis Hp– 34% Self reported
functional dyspepsia in naireHp: biopsy halitosis Conc: combination
Hp + (n = 222) and Hp– of retrosternal pain, weight
(n = 182) pat. loss, food intolerance, and
absence of halitosis was
predictive of Hp infection
Moshkowitz et al. (2007) GERD and halitosis QuestionnaireHp: rapid No correlation was found Self reported
urease test (CLO test) between Hp infection status
and halitosis occurrence and
severity
Claus et al. (1996) Halitosis and Hp (n = 80; Odor judge, GC Significantly higher mouth 44.7 mean age for Hp+ 33.8
31Hp+, 49Hp–) Hp: [13C] urea breath test air malodor and H2S levels mean age for Hp–
in Hp+ No difference in oral
health parameters (PI, GI,
PPD, TC)
Candelli et al. (2003) Hp and GI symptoms in Questionnaire Hp: [13C] urea Higher prevalence of However, after correction for
IDDM breath test halitosis in Hp + then Hp – age, the difference was not
and in diabetics then significant. Self reported
controls
Li et al. (2005) Dyspeptic symptoms Questionnaire Halitosis was more often Self reported
(n = 782) found in dyspeptic patients
6 Breath Odors and the Gastrointestinal Tract
with Hp infection (p < 0.01)

Table 6.3 Hp eradication therapy and halitosis
Reference Aims Malodor/Hp criteria Findings and conclusions Criticism and comments
(intervention)
Tiomny et al. (1992) Halitosis and Hp Halitosis: reported by a Halitosis disappeared
In three couples in which family memberHp: biopsy following treatment
one or both had halitosis [14C] urea breath test (4 weeks)
(Metronidazole)
Ierardi et al. (1998) Halitosis and Hp in Halitosis: Halimeter In Hp persistent (11/30) “sulfide levels decreased
dyspeptic pat. complaining >190ppbHp: [13C] urea CHX mw showed no effect without declining to below
of halitosis. 52/58(90%) had breath test (amoxicillin/ on VSC but following the cut off value even in the
objective halitosis: 30(57%) CHX mw/metronidazole) Metronidazole use in 9/11, patients whose eradication
Hp + 22(43%) Hp– Hp and halitosis disappeared treatment was unsuccessful”
Shashidhar et al. (2000) Hp eradication in children Halitosis: questionnaire Eradication achieved in 56% No significant correlation
(n = 28; 11y) (patient + parent)Hp: biopsy Halitosis before treatment was observed between level
(clarithromycin, amoxicillin) reported in 45%, after in 22% of infection and pretreatment
symptoms
Serin et al. (2003) Halitosis as an indication for Halitosis: questionnaire Halitosis was resolved After the follow up period,
Hp eradication therapy (patient + relatives)Hp: regardless of eradication halitosis was not
(n = 148) biopsy (clarithromycin, status, but more significantly reevaluated.
amoxicillin) 4–6 weeks in the eradicated group.
followup
Katsinelos et al. (2007) Eradication therapy Hp Halitosis: questionnaire Halitosis was resolved in
halitosis: long term outcome (patient + relatives)Hp: [13C] 16/18 (over 6–108 months
(n = 18) urea breath test (clarithro- followup)
mycin, amoxicillin/
metronidazole, tetracycline)
51
52
Table 6.4 Oral Hp and halitosis

Reference Aims/criteria Malodor/oral parameters Findings and conclusions Criticism and comments
(intervention)
Adler et al. (2005) Oral Hp (PCR) associated Halimeter >100ppb Hp was found in 87% of
with glossitis and halitosis tongue biopsies of patients
with glossitis and halitosis
(but not in plaque and saliva)
as compared to 2.6% in the
control.
Suzuki et al. (2008) Salivary Hp (PCR) and OJ (0–5), GC, PPD ≥ 5mm, No difference between
halitosis TC (0–4), Saliva flow, PCR Hp + and Hp– in malodor,
periopathogens: Pg, Td, Pi. total VSC and TC, but
significantly higher PPD,
methyl mercaptan, and
periopathogens
6 Breath Odors and the Gastrointestinal Tract
References 53
Although some studies imply an association between Hp infection and halitosis, no satis-
factory explanation has been offered as to how the two might be linked together (Hoshi et al.
2002). Several studies were carried out to investigate the presence of Hp in the oral cavity and
its relation to oral malodor (Adler et al. 2005; Suzuki et al. 2008). One of these studies (Suzuki
et al. 2008) found that subjects who were positive for Hp in their saliva had significantly more
periodontal pockets and were also positive to periopathogenic bacteria (Porphyromonas gin-
givalis, Treponema denticola, prevotella intermedia), all of which are known malodor pro-
ducers. Although Hp has been shown to be able to produce volatile sulfide compounds on its
own (Lee et al. 2006), a possible association with other VSC producing bacteria, which are
much more abundant in the oral cavity, might seem more reasonable (Table 6.4).
In summary, most researchers agree that breath odor from the stomach is rare. Systemic
antibiotics used to treat stomach ailments also suppress the oral microbiota, resulting in a
transient reduction in malodor that is sometimes erroneously interpreted as odor from the
stomach. Several isolated studies show positive correlations comparing HP and breath
odor; these warrant further study.
References
Adler, I., Denninghoff, V.C., Alvarez, M.I., Avagnina, A., Yoshida, R., Elsner, B.: Helicobacter
pylori associated with glossitis and halitosis. Helicobacter 10(4), 312–317 (2005)
Candelli, M., Rigante, D., Marietti, G., Nista, E.C., Crea, F., Bartolozzi, F., Schiavino, A.,
Pignataro, G., Silveri, N.G., Gasbarrini, G., Gasbarrini, A.: Helicobacter pylori, gastrointesti-
nal symptoms, and metabolic control in young type 1 diabetes mellitus patients. Pediatrics
111(4 Pt 1), 800–803 (2003)
Carr, M.M., Nguyen, A., Nagy, M., Poje, C., Pizzuto, M., Brodsky, L.: Clinical presentation as a
guide to the identification of GERD in children. Int. J. Pediatr. Otorhinolaryngol. 54(1), 27–32
(2000)
Claus, D., Geypens, B., Rutgeerts, P., Ghyselen, J., Hoshi, K., Van Steenberghe, D., Ghoos, Y.:
Where gastroenterology and periodontology meets: determination of oral volatile organic com-
pounds using closed loop trapping and high resolution gas chromatography ion trap detection.
In: Van Steenberghe, D., Rosenberg, M. (eds.) Bad Breath a Multidisciplinary Approach, pp.
15–27. Leuven University Press, Leuven (1996)
Delanghe, G., Ghyselen, J., Feenstra, L., Van Steenberghe, D.: Experiences of a Belgian multidis-
ciplinary breath odour clinic. In: Van Steenberghe, D., Rosenberg, M. (eds.) Bad Breath a
Multidisciplinary approach, pp. 199–208. Leuven University Press, Leuven (1996)
Di Fede, O., Di Liberto, C., Occhipinti, G., Vigneri, S., Lo Russo, L., Fedele, S., Lo Muzio, L.,
Campisi, G.: Oral manifestations in patients with gastro-oesophageal reflux disease: a single-
center case-control study. J. Oral Pathol. Med. 37(6), 336–340 (2008)
Gasbarrini, A., Ojetti, V., Pitocco, D., De Luca, A., Franceschi, F., Candelli, M., Sanz Torre, E.,
Pola, P., Ghirlanda, G., Gasbarrini, G.: Helicobacter pylori infection in patients affected by
insulin-dependent diabetes mellitus. Eur. J. Gastroenterol. Hepatol. 10(6), 469–472 (1998)
Hoshi, K., Yamano, Y., Mitsunaga, A., Shimizu, S., Kagawa, J., Ogiuchi, H.: Gastrointestinal
diseases and halitosis: association of gastric Helicobacter pylori infection. Int. Dent. J. 52,
207–211 (2002)
Howe, J.W.: The Breath, and the Diseases Which Give It a Fetid Odor, 4th edn. D. Appleton and
Company, New York (1898)
54 6 Breath Odors and the Gastrointestinal Tract
Ierardi, E., Amoruso, A., La Notte, T., Francavilla, R., Castellaneta, S., Marrazza, E., Monno,
R.A., Francavilla, A.: Halitosis and Helicobacter pylori: a possible relationship. Dig. Dis. Sci.
43(12), 2733–2737 (1998)
Katsinelos, P., Tziomalos, K., Chatzimavroudis, G., Vasiliadis, T., Katsinelos, T., Pilpilidis, I.,
Triantafillidis, I., Paroutoglou, G., Papaziogas, B.: Eradication therapy in Helicobacter pylori-
positive patients with halitosis: long-term outcome. Med. Princ. Pract. 16(2), 119–123 (2007)
Katz, J., Shenkman, A., Stavropoulos, F., Melzer, E.: Oral signs and symptoms in relation to dis-
ease activity and site of involvement in patients with inflammatory bowel disease. Oral Dis.
9(1), 34–40 (2003)
Lee, H., Kho, H.S., Chung, J.W., Chung, S.C., Kim, Y.K.: Volatile sulfur compounds produced by
Helicobacter pylori. J. Clin. Gastroenterol. 40(5), 421–426 (2006)
Li, X.B., Liu, W.Z., Ge, Z.Z., Zhang, D.R., Zhao, Y.J., Dai, J., Xue, H.B., Xiao, S.D.: Analysis of
clinical characteristics of dyspeptic symptoms in Shanghai patients. Chin. J. Dig. Dis. 6(2),
62–67 (2005)
Marshall, B.J., Armstrong, J.A., McGechie, D.B., Glancy, R.J.: Attempt to fulfil Koch’s postulates
for pyloric Campylobacter. Med. J. Aust. 142(8), 436–439 (1985)
Moshkowitz, M., Horowitz, N., Leshno, M., Halpern, Z.: Halitosis and gastroesophageal reflux
disease: a possible association. Oral Dis. 13(6), 581–585 (2007)
Schubert, T.T., Schubert, A.B., Ma, C.K.: Symptoms, gastritis, and Helicobacter pylori in patients
referred for endoscopy. Gastrointest. Endosc. 38(3), 357–360 (1992)
Serin, E., Gumurdulu, Y., Kayaselcuk, F., Ozer, B., Yilmaz, U., Boyacioglu, S.: Halitosis in patients
with Helicobacter pylori-positive non-ulcer dyspepsia: an indication for eradication therapy?
Eur. J. Intern. Med. 14(1), 45–48 (2003)
Shashidhar, H., Peters, J., Lin, C.H., Rabah, R., Thomas, R., Tolia, V.: A prospective trial of lanso-
prazole triple therapy for pediatric Helicobacter pylori infection. J. Pediatr. Gastroenterol.
Nutr. 30(3), 276–282 (2000)
Shifman, A., Orenbuch, S., Rosenberg, M.: Bad breath – a major disability according to the
Talmud. Isr. Med. Assoc. J. 4(10), 843–845 (2002)
Struch, F., Schwahn, C., Wallaschofski, H., Grabe, H.J., Volzke, H., Lerch, M.M., Meisel, P.,
Kocher, T.: Self-reported halitosis and gastro-esophageal reflux disease in the general popula-
tion. J. Gen. Intern. Med. 23(3), 260–266 (2008)
Suzuki, N., Yoneda, M., Naito, T., Iwamoto, T., Masuo, Y., Yamada, K., Hisama, K., Okada, I.,
Hirofuji, T.: Detection of Helicobacter pylori DNA in the saliva of patients complaining of
halitosis. J. Med. Microbiol. 57(Pt 12), 1553–1559 (2008)
Tiomny, E., Arber, N., Moshkowitz, M., Peled, Y., Gilat, T.: Halitosis and Helicobacter pylori. A
possible link? J. Clin. Gastroenterol. 15(3), 236–237 (1992)
Tydd, T.F., Dyer, N.H.: Pyloric stenosis presenting with halitosis. Br. Med. J. 3(5926), 321
(1974)
Werdmuller, B.F., van der Putten, T.B., Balk, T.G., Lamers, C.B., Loffeld, R.J.: Clinical presenta-
tion of Helicobacter pylori-positive and -negative functional dyspepsia. J. Gastroenterol.
Hepatol. 15(5), 498–502 (2000)
Other Sources of Breath Odors
7
Although relatively rare, especially among the ambulatory population, breath odors may
be a sign of a systemic condition or a metabolic disorder (Table 7.1). Usually, this symp-
tom will appear in a later stage of the disease when the patient is already diagnosed.
However, sometimes the breath odor may be an early sign or even the only sign for the
underlying disorder or disease.
More commonly, exogenous sources such as food substances, smoking, or medications
may also play a part in breath odor formation (Table 7.1). These various sources may con-
tribute odor components either directly from the upper respiratory tract or indirectly
through the blood via alveolar air. The latter is also referred to as “blood borne halitosis”
(Tangerman and Winkel 2010). In this case, the odor component is absorbed through the
blood stream and released through the alveoli into the lung air. As such, these breath odors
will be present in both the mouth and nasal exhalations.
Breath odors may originate from neoplasm and infections of the lower respiratory tract
such as bronchogenic carcinoma, bronchiectasis, and anaerobic pulmonary infection
(Gordon et al. 1985; Lorber 1975; Preti et al. 1988). The chemical analysis of breath sam-
ples from patients with lung cancer has shown elevated levels of acetone, methylethylke-
tone, and n-propanol (Gordon et al. 1985). Alternatively, putrid smell might appear
following a secondary bacterial infection of the tumor. Although putrid breath odor typi-
cally appears relatively late in the course of an anaerobic lung infection, following other
symptoms such as fever, cough, and chest pains, it has been reported that in some cases it
can serve as an early sign of the disease (Lorber 1975).
The “odor of decaying apples” on the breath of patients with uncontrolled diabetes mel-
litus was first recorded in the late eighteenth century (Crofford et al. 1977). In uncontrolled
patients, this disease, which is termed “hunger in the midst of plenty,” causes an increase in
lipid metabolism that results in the ketonic breath. This results from the formation of acetone,
acetoacetate, and b-hydroxybutyrate, which are transferred from the blood to the alveolar air
and exhaled through the breath (Rooth and Ostenson 1966). Furthermore, diabetes also
affects oral health and may aggravate oral diseases and conditions (e.g., gingivitis, periodon-
titis, and decrease in saliva flow) that contribute to oral malodor production (Ship 2003).
Liver cirrhosis may give rise to a characteristic breath odor known as Fetor hepaticus.
This is a sweet, musty, or slightly fecal smell on the breath which sometimes resembles the
smell of a fresh cadaver. The impaired liver function decreases the metabolism of various
malodorous compounds such as dimethyl sulfide and other ketones causing their increased
blood levels and appearance on the breath (Van den Velde et al. 2008).

56
Table 7.1 Some of the systemic and external sources of breath odors

Source Odor characteristics Odor components References
Lung disease:
Pulmonary infection, lung cancer Putrid Acetone, methylethylketone, Lorber (1975), Gordon et al. (1985)
n-propanol
Diabetes mellitus (uncontrolled) Fruity Acetone, ketones Rooth and Ostenson (1966)
Liver (hepatic) cirrhosis Musty, fresh cadaver (“fetor Dimethyl sulfide, ketones Van den Velde et al. (2008)
hepaticus”)
Kidney (renal) failure, uremia Ammoniac, urine like Ammonia, dimethylamine, Simenhoff et al. (1977)
trimethylamine
Metabolic disorder:
Trimethylaminuria (TMAU) Fish like (“fish odor syndrome”) Trimethylamine Preti et al. (1992)
Medication:
Disulfiram Sulfurous Carbon disulfide O’Reilly and Motley (1977)
Cysteamine Dimethyl sulfide Besouw et al. (2007)
Food:
Garlic Garlic Allyl methyl sulfide Suarez et al. (1999)
Onion Onion Methyl propyl sulfide
Tobacco smoking:
Cigars, cigarettes “Smoker’s breath” Trimethyl pyridine dimethyl Bazemore et al. (2006)
pyrazine
7 Other Sources of Breath Odors
References 57
“Uremic breath” is a typical breath odor of patients with end-stage chronic renal failure.
This type of breath odor has been described as “ammoniacal”, “urine-like”, and “fetid”
odor and was attributed mainly to amine compounds such as dimethylamine and trimeth-
ylamine (Simenhoff et al. 1977). As with liver cirrhosis and diabetes, this is also a blood-
borne breath odor resulting from an organ failure and consequently elevated blood levels
of the odorous compounds.
Apart from organ failure (e.g., liver, kidneys, pancreas), an impaired metabolic pathway,
typically resulting from an inherited mutation of an enzyme coding gene, may also result in
the accumulation of an odorous metabolite in the blood. An example of such a metabolic
disorder that forms another type of blood-borne breath odor known as “fish odor syndrome”
or TMAU (i.e., trimethylamineuria)(Leopold et al. 1990). This condition results from the
impaired N-oxidation and secretion of trimethylamine, a choline metabolite, and is esti-
mated to be present in various degrees in about 1% of the population (Ayesh et al. 1993).
Various medications may also cause a type of blood-borne breath odors. For example,
medications such as disulfiram and cysteamine have been previously shown to cause
breath odors possibly through the formation of sulfurous compounds, mainly dimethyl
sulfide (Besouw et al. 2007; Murata et al. 2003). Some researchers suggested that dimethyl
sulfide is the only VSC molecule that is transportable by blood since – SH containing
VSCs like hydrogen sulfide and methyl mercaptan quickly reacts with the blood by bind-
ing or oxidation (Tangerman and Winkel 2010).
Some food substances such as onion and garlic contain sulfurous compounds such as
allyl methyl sulfide and methyl propyl sulfide that can cause distinctive breath odors last-
ing up to 72 h following ingestion (Suarez et al. 1999). Although most of the malodor
emanates directly from remnants in the oral cavity, mid 1930s research showed a distinct
blood-borne element to garlic breath by feeding the garlic straight into the stomach and
detecting it on the breath after several hours (Blankenhorn and Richards 1936).
Another common external source for breath odor is tobacco smoke. Smoking habits
often cause a characteristic ashtray like smell known as “smoker’s breath.” The chemical
analysis of tobacco and tobacco smoke showed it to contain many volatile sulfide com-
pounds (Stedman 1968). However, in a study conducted in the general population in Japan,
no association was found between smoking habits and the oral levels of volatile sulfide
compounds (Miyazaki et al. 1995). Another study on the chemical composition of cigar
smokers’ breath detected other odor components such as trimethyl pyridine and dimethyl
pyrazine from various samples including tongue samples (Bazemore et al. 2006).
References
Ayesh, R., Mitchell, S.C., Zhang, A., Smith, R.L.: The fish odour syndrome: biochemical, familial,
and clinical aspects. BMJ 307(6905), 655–657 (1993)
Bazemore, R., Harrison, C., Greenberg, M.: Identification of components responsible for the odor
of cigar smoker’s breath. J. Agric. Food Chem. 54(2), 497–501 (2006)
Besouw, M., Blom, H., Tangerman, A., de Graaf-Hess, A., Levtchenko, E.: The origin of halitosis
in cystinotic patients due to cysteamine treatment. Mol. Genet. Metab. 91(3), 228–233 (2007)
58 7 Other Sources of Breath Odors
Blankenhorn, M.A., Richards, C.E.: Garlic breath odor. J. Am. Med. Assoc. 107(6), 409–410
(1936)
Crofford, O.B., Mallard, R.E., Winton, R.E., Rogers, N.L., Jackson, J.C., Keller, U.: Acetone in
breath and blood. Trans. Am. Clin. Climatol. Assoc. 88, 128–139 (1977)
Gordon, S.M., Szidon, J.P., Krotoszynski, B.K., Gibbons, R.D., O’Neill, H.J.: Volatile organic com-
pounds in exhaled air from patients with lung cancer. Clin. Chem. 31(8), 1278–1282 (1985)
Leopold, D.A., Preti, G., Mozell, M.M., Youngentob, S.L., Wright, H.N.: Fish-odor syndrome
presenting as dysosmia. Arch. Otolaryngol. Head Neck Surg. 116(3), 354–355 (1990)
Lorber, B.: “Bad breath”: presenting manifestation of anaerobic pulmonary infection. Am. Rev.
Respir. Dis. 112(6), 875–877 (1975)
(1995)
Murata, T., Fujiyama, Y., Yamaga, T., Miyazaki, H.: Breath malodor in an asthmatic patient caused
by side-effects of medication: a case report and review of the literature. Oral Dis. 9(5), 273–276
(2003)
O’Reilly, R.A., Motley, C.H.: Breath odor after disulfiram. JAMA 238(24), 2600 (1977)
Preti, G., Labows, J.N., Kostelc, J.G., Aldinger, S., Daniele, R.: Analysis of lung air from patients
with bronchogenic carcinoma and controls using gas chromatography-mass spectrometry.
J. Chromatogr. 432, 1–11 (1988)
Preti, G., Clark, L., Cowart, B.J., Feldman, R.S., Lowry, L.D., Weber, E., Young, I.M.: Non-oral
etiologies of oral malodor and altered chemosensation. J. Periodontol. 63(9), 790–796 (1992)
Rooth, G., Ostenson, S.: Acetone in alveolar air, and the control of diabetes. Lancet 2(7473)
1102–1105 (1966)
Ship, J.A.: Diabetes and oral health: an overview. J. Am. Dent. Assoc. 134(Spec No), 4S–10S
(2003)
Simenhoff, M.L., Burke, J.F., Saukkonen, J.J., Ordinario, A.T., Doty, R.: Biochemical profile or
uremic breath. N. Engl. J. Med. 297(3), 132–135 (1977)
Stedman, R.L.: The chemical composition of tobacco and tobacco smoke. Chem. Rev. 68(2),
153–207 (1968)
Suarez, F., Springfield, J., Furne, J., Levitt, M.: Differentiation of mouth versus gut as site of origin of
odoriferous breath gases after garlic ingestion. Am. J. Physiol. 276(2 Pt 1), G425–G430 (1999)
Tangerman, A., Winkel, E.G.: Extra-oral halitosis: an overview. J. Breath Res. 4(017003),
6 (2010)
Van den Velde, S., Nevens, F., Van Hee, P., van Steenberghe, D., Quirynen, M.: GC-MS analysis
of breath odor compounds in liver patients. J. Chromatogr. B Analyt. Technol. Biomed. Life
Sci. 875(2), 344–348 (2008)
Measurements of Breath Odors
and Related Parameters 8
Breath odors, much like other odor nuisances (e.g., sewage, garbage, livestock waste),
are perceived in everyday life by our sense of smell. The human nose can pick up the
scent of a large variety of different odorants at very low concentrations that are some-
times below instrumental detection thresholds. That is why organoleptic measurements
employing human odor judges are still considered the “golden standard” in various odor
testing scenarios, including breath odors evaluation both for research and the clinical
setting.
However, organoleptic measurement by a human odor judge has a few drawbacks,
including potential lack of objectivity and interpersonal variation. To overcome this, a
panel of judges is often employed and training methods carried out. Adjunct instrumental
methods for measuring malodor-related parameters have been devised, including the
instrumental measurement of volatile sulfides and other malodor-associated components,
as well as microbial and biochemical assays.
Odor Judge Scoring
Environmental odor nuisances are generally judged by various criteria collectively known
as the FIDO factors (Mackie et al. 1998). These include: frequency (number of odor
occurrences in a given time), intensity (strength of odor), duration (period of time for
odor occurrence), and offensiveness (unpleasantness or character of odor). However, in
the case of breath odors, odor intensity scales are considered the main tool for odor quan-
tification both for research and clinical proposes. On some occasions (e.g., breath fresh-
eners testing), offensiveness/pleasantness scales or characteristics may also be
employed.
Due to the importance attributed to odor intensity in the determination of an odor prob-
lem, various odor intensity rating methods were developed. These can be divided into two
categories: scaling and dilution. Scaling involves grading the odor intensity using an arbi-
trary scale ranging from “no odor” to “extremely strong odor” either dichotomously (pres-
ent or absent) or with intermittent level criteria (e.g., “faint”, “moderate” ext.) on a typical
four-, five-, or six-point scale. Dilution methods are based on mixing the sample with odor
free air in various concentrations in order to determine detectability or odor threshold
concentration.

60 8 Measurements of Breath Odors and Related Parameters
Table 8.1 Breath odor intensity scale (organoleptic scale)

Odor intensity level Level description
0 No odor
1 Barley noticeable odor
2 Slight but clearly noticeable odor
3 Moderate odor
4 Strong odor
5 Extremely strong odor
The most widely used odor intensity organoleptic scale in breath odor research is a six-
point scale (Table 8.1) also known as the “0–5 scale”, and sometimes erroneously referred
to as the “Rosenberg scale” (Rosenberg and McCulloch 1992), since it was first introduced
in 1919 (Allison and Katz 1919).
Generally, the odor judge or panelist evaluates the odor by sniffing the exhaled air at a fixed
distance (10 cm) from the subject’s mouth, and scoring the odor according to the scale (Fig. 8.1).
This can be done directly from the subject’s mouth (e.g., during exhalation, speech – “count to
20”, blowing through a straw), or indirectly using a sampling bag. A partition screen is some-
times employed to blind the odor judge to the subject’s appearance (Murata et al. 2002).
In our initial studies, we adopted the ‘forced choice’ approach, i.e., the judge is forced to
choose one of the 0–5 categories (Rosenberg et al. 1991a). But during the research, we
sometimes faced dilemmas. How does one score the level of an odor that is somewhere
between slight and moderate? One possibility was to use a visual analogue scale that is often
used in perception studies, for example, to register the level of pain. In such instances, the
judge has the option of drawing the line anywhere along the scale. We used this approach in
one study, allowing the odor judge to score anywhere on a scale of 0 (no odor) to 10 (unbear-
ably strong odor) (Goldberg et al. 1994). Since the scoring on such a scale is ostensibly
linear and continuous, statistic analysis based on linear data can be more readily justified.
Fig. 8.1 Organoleptic (odor

judge) assessment of breath
odor
Instrumental Measuring of Malodor-Related Compounds 61
In subsequent studies, we used a similar approach. We went back to the six-point

descriptive scale, but allowed judges to score at will in between the finite descriptors
(e.g., give a score of 2.5, between slight and moderate) (Greenstein et al. 1997). When the
sample size is large (e.g., n = 100), the results approximate data obtained using a continu-
ous scale. Analysis using statistical tools developed for studying continuous data (e.g.,
linear regression analysis, Pearson correlation coefficients) can then be employed with
greater confidence.
Interpersonal variation in odor perception between odor judges still remains a major
problem (Rosenberg et al. 1991b). In order to try and standardize odor judge scoring, cali-
bration and training methods have been proposed. Odor judge training protocol based on
the American Society of Testing and Materials Standards (introduction to sensory scales,
use of n-butanol reference and sniffing techniques) was shown to reduce odor judge errors
(Nachnani et al. 2005).
Dilution methods are usually device dependent. They are based on an apparatus or
instrument designed to mix and dilute the odor sample to a set of concentrations enabling
the judge to determine the minimal odor detectability or odor threshold. Some of these
devices are handheld and used in field studies (e.g., olfactometer). In early studies on oral
malodor done by Fosdick and colleagues, they reported the use of a device called the
osmoscope as a sample dilution method designed to determine odor intensity (Brening
et al. 1939).
Recently, a non-apparatus-dependent dilution method was reported (Bornstein et al.
2009). This method relies on the distance between the odor judge’s nose and the patient’s
mouth as the diluting factor (i.e., 1 m, 30 and 10 cm) assuming that a higher intensity mal-
odor would be sensed from a greater distance. Although organoleptic scales (continuous as
possible) are more robust for research, this simple method was deemed suitable for a clini-
cal setting.
Instrumental Measuring of Malodor-Related Compounds
Gas Chromatography (GC)
The need for objective, quantitative techniques to serve as auxiliary tests for the organo-
leptic measurement for both research and the clinic led to the development of various
instrumental measuring techniques.
The use of gas chromatography for the quantification of volatile sulfide compounds
(VSC) in mouth air was first reported by Tonzetich in the early 1970s (Tonzetich 1971).
Since then, many studies have employed this method and reported significant correlations
between GC measurements of VSC and malodor levels as evaluated organoleptically by
odor judges (Table 8.2).
Traditional GC has a few distinctive disadvantages such as being time consuming,
costly, and requiring a professional technician for operation; conversely, it allows for the
detection and quantitation of specific compounds. This feature has helped in the identifica-
tion of various compounds present in mouth air and breath samples (see Chap. 3) and may
Table 8.2 Association between gas chromatography measurement of mouth air VSC levels and oral
malodor scores
Reference Parameters Correlations
Schmidt et al. (1978) Odor judge scores (0–3; 3 judges) Kendall correlation
(n = 102) Study I (n = 36) r = 0.28, p < 0.05
Study II (n = 66) r = 0.35, p < 0.001
Shimura et al. (1996) Odor judge scores (0–4; 3 judges) Pearson correlation
(n = 21) r = 0.71, p < 0.01
Oho et al. (2001) Odor judge scores (0–3; 3 judges) Spearman correlation
(n = 155) r = 0.69, p < 0.0001
Amano et al. (2002) Odor judge scores (0–3; 3 judges) Spearman correlation
(n = 61) r = 0.47, p < 0.01
Tanaka et al. (2004b) Odor judge scores (0–5; 1 judge) Spearman correlation
(n = 78) r = 0.63, p < 0.05
Awano et al. (2004) Odor judge scores (0–5; 3 judges) Spearman correlation
(n = 127) CH3SH r = 0.75, p < 0.001
H2S r = 0.59, p < 0.001
Total VSC r = 0.74, p < 0.001
Nonaka et al. (2005) Odor judge scores (not specified) Correlation (not
(n = 66) specified)
r = 0.73, p- not specified
Hunter et al. (2005) Odor judge scores (0–5; 2 judges) Pearson correlation
(n = 25) CH3SH r = 0.61, p < 0.001
H2S r = 0.63, p < 0.001
Total VSC r = 0.65, p < 0.001
help identify the role of specific volatiles in malodor of various origins. For example,
whereas hydrogen sulfide is produced largely from the tongue dorsum, methyl mercaptan
is elevated in cases with periodontitis (Yaegaki and Sanada 1992). Furthermore, other non-
sulfide compounds detected by GC (e.g., pyridine, picoline) were also associated with the
presence of periodontal disease (Kostelc et al. 1981).
The technical complexity of GC along with the other drawbacks had limited its applica-
tion mainly to research and rendered it unsuitable for the clinic. However, recent attempts
to simplify this system have resulted in a simpler instrument suitable for the clinical setting
(Murata et al. 2006).
Sulfide Monitor
In the early 1990s, Rosenberg and coworkers suggested the use of a portable sulfide moni-
tor, originally designed for ambient air quality measurement in working and living envi-
ronments (Fig. 8.2), for the measurement of sulfide levels in mouth air (Rosenberg et al.
1991a, b). Although this device measures the total concentration of volatile sulfide
Biochemical Assays 63
Fig. 8.2 Sulfide monitor

(Interscan corp. CA) 1170
series
c ompounds and does not distinguish between the individual sulfide compounds, its read-
ings correlate significantly with odor judge scores in numerous studies (Table 8.3).
Its simple operation, small size, rapid sample analysis, and relatively low cost made the
sulfide monitor the most popular means for VSC measurements in both research and clini-
cal settings. Furthermore, in studies carried out using both GC and sulfide monitor for mea-
suring oral VSCs levels (Furne et al. 2002; Oho et al. 2001), the two correlated significantly
with one another, yielding correlation coefficients of 0.73 (p < 0.01) and 0.84 (p < 0.0001).
Measuring Techniques of Malodor-Related Compounds
Other measuring techniques for the detection of VSC as well as other malodor-related com-
pounds (e.g., ammonia, amines) have been reported in the literature (Table 8.4). These
include various techniques ranging from simple colorimetric assays and small portable semi-
conductor-based sulfide monitors to more complex methods involving elaborate laboratory
equipment such as chemical sensors array and high-performance liquid chromatography.
Biochemical Assays
BANA Test
In 1990, Loesche and coworkers (Loesche et al. 1990) suggested the use of the synthetic
peptide benzoyl-DL-arginine-naphthylamide (BANA) as a diagnostic test for the presence
of several anaerobic periopathogenic bacteria (i.e., Treponema denticola, Porphyromonas
Table 8.3 Association between sulfide monitor (Halimeter) measurement of mouth air VSC levels
and oral malodor scores
Reference Parameters Correlations
Rosenberg et al. (1991b) Spearman correlation
(n = 75)
Odor judge scores (0–5; 7 judges) r = 0.60, p < 0.001
Rosenberg et al. (1991a) Odor judge scores (0–5; 2 judges) Pearson correlation
(n = 41) Odor judge 1 r = 0.55, p < 0.0001
Odor judge 2 r = 0.43, p < 0.0001
De Boever et al. (1994) Pearson correlation
(n = 55)
Odor judge scores (0–4; 1 judge) r = 0.63, p < 0.001
Kozlovsky et al. (1994) Pearson correlation
(n = 52) Odor judge scores (10 cm
continuous scale; 1 judge) r = 0.47, p < 0.001
Greenstein et al. (1997) Odor judge scores (0–5; 2 judges) Pearson correlation
(n = 123) Odor judge 1 r = 0.27, p = 0.003
Odor judge 2 r = 0.39, p < 0.001
Willis et al. (1999) (n = 30) Pearson correlation
Odor judge scores (0–10; 3 judges) r = 0.41, p = 0.027
Oho et al. (2001) (n = 155) Spearman correlation
Sterer et al. (2002) (n = 64) Odor judge scores (0–5; 2 judges) Spearman correlation
Odor judge 1 r = 0.37, p = 0.002
Odor judge 2 r = 0.46, p < 0.001
Iwanicka-Grzegorek et al. Spearman correlation
(2005) (n = 124)
Stamou et al. (2005) (n = 71) Pearson correlation
Sterer et al. (2008) (n = 42) Spearman correlation
Vandekerckhove et al. (2009) Spearman correlation
(n = 280)
gingivalis, and Bacteroides forsythus). These bacteria posses a trypsin-like activity that
enables them to break down a synthetic peptide attached to a color producing indicator,
yielding a color reaction indicative of their presence.
Since these bacteria are Gram-negative anaerobic bacteria that can produce malodorous
compounds as a by-product of their proteolytic activity, it was suggested that the BANA
test may serve as a diagnostic test for oral malodor and malodor-related microorganisms.
Several studies have compared BANA test results from various oral samples (e.g., plaque,
tongue coating, saliva) with odor judge scores and VSC levels (Table 8.5).
Biochemical Assays 65
Table 8.4 Association between malodor-related compounds measurement (chemical sensors, gas

detectors, colorimetric assays, and chromatography) and oral malodor scores
Reference Compounds Method Correlations with
malodor
Goldberg et al. (1994) Cadaverine High performance liquid Pearson correlation
(n = 52) chromatography (HPLC) r = 0.37, p = 0.027
Shimura et al. (1997) VSC Portable monitor with a Pearson correlation
(n = 94) zinc-oxide thin-film r = 0.82, p < 0.01
semiconductor sensor
Morita et al. (2001) Sulfide ions Sulfide electrode tongue Spearman correlation
(n = 20) probe r = 0.77, p < 0.01
Amano et al. (2002) Ammonia Portable ammonia-moni- Pearson correlation
(n = 61) toring device r = 0.16, NS
Tanaka et al. (2004a) Volatiles (low Chemical sensor array Spearman correlation
(n = 78) boiling point) (“electronic nose”) r = 0.71, p < 0.05
Iwanicka-Grzegorek Salivary amines Ninhydrin method Spearman correlation
et al. (2005) (n = 124) (low molecular r = 0.60, p < 0.001
weight)
Sopapornamorn et al. VSC Portable monitor with a Pearson correlation
(2006) (n = 260) zinc-oxide thick-film r = 0.64, p < 0.01
semiconductor sensor
Table 8.5 Oral malodor parameters and the BANA test

Reference Parameters/criteria Findings
De Boever et al. Malodor No complaint Differences between
(1994) (n = 55) complaint groups (ANOVA)
BANA tongue NS
BANA plaque p < 0.05
Kozlovsky et al. Spearman correlation
(1994) (n = 52)
Odor judgea and BANA shallow pockets (<4 mm) r = 0.33, p = 0.016
Odor judgea and BANA deep pockets (³4 mm) r = 0.26, p = 0.034
Odor judgea and BANA tongue r = 0.36, p = 0.008
Odor judgea and BANA saliva r = 0.36, p = 0.009
Morita and Pearson correlation
Wang (2001)
(n = 81) Odor judgea and BANA healthy sites (<4 mm) r = 0.02, NS
Odor judgea and BANA low-moderate (4–6 mm) r = 0.27, p = 0.015
Odor judgea and BANA severe sites (>6 mm) r = 0.23, p = 0.042
Odor judgea and BANA tongue r = 0.27, p = 0.014
Figueiredo et al. Pearson correlation
(2002) (n = 41)
VSC and BANA subgingival plaque (£3 mm)
b
r = 0.4, NS
VSCb and BANA subgingival plaque (>3 mm) r = 0.55, p = 0.01
VSCb and BANA tongue r = 0.07–0.14, NS
VSCb and BANA saliva r = 0.06–0.10, NS
NS non significant
a
b
Sulfide monitor (Halimeter) readings
The data from these and other studies show that BANA testing of subgingival plaque
samples, especially from periodontal patients, is more often associated with oral malodor
as compared to saliva or tongue samples. However, the correlations, while significant, are
lower than those obtained comparing odor judge scores and VSC levels.
b-Galactosidase Activity Assay
Some of the salivary proteins available for bacterial degradation are glycoproteins (e.g.,
salivary mucins) that are comprised of carbohydrate side chains surrounding a protein
core. These side chains must first be removed in order to expose the protein core and make
it available for proteolytic degradation. b-Galactosidase is a key enzyme in this deglyco-
sylation process, which is usually carried out by Gram-positive oral bacteria, mainly strep-
tococci (Sterer and Rosenberg 2006).
In 2002, we reported that the activity of b-Galactosidase in saliva is associated with oral
malodor scores (Sterer et al. 2002), suggesting that the quantification of the enzyme’s
activity in saliva may serve as a diagnostic tool for oral malodor (Fig. 8.3). Since then,
further studies have been conducted to test this premise (Table 8.6).
Fig. 8.3 b-galactosidase assay; color indicator (blue) correlates with malodor levels
Salivary Incubation Assays 67
Table 8.6 Oral malodor parameters and b-Galactosidase activity

Reference Parameters Findings
Sterer et al. (2002) Spearman correlation
(n = 64)
Odor judge 1 and b-Galactosidase assay
a
r = 0.38, p = 0.002
Odor judge 2a and b-Galactosidase assay r = 0.47, p < 0.001
VSCb and b-Galactosidase assay r = 0.18, NS
Stamou et al. (2005) Pearson correlation
(n = 71)
Odor judge and b-Galactosidase assay
a
r = 0.52, p = 0.001
VSCb and b-Galactosidase assay r = 0.38, p = 0.001
Rosenberg et al. Spearman correlation
(2007) (n = 88)
Odor judge and b-Galactosidase assay
a
r = 0.59, p < 0.001
VSCb and b-Galactosidase assay r = 0.31, p < 0.001
Yoneda et al. (2010) b-Galactosidase b-Galactosidase Differences between groups
(n = 49) positive (n = 10) negative (n = 39) (t-test)
Odor judgea p = 0.012
VSCb p < 0.001
NS non significant
a
b
Cysteine Challenge
The addition of cysteine, a sulfur-containing amino acid, to incubated dental plaque

(Tonzetich and Carpenter 1971) or a suspension of Gram-negative oral bacteria (Solis
Gaffar et al. 1979) resulted in increased production of VSCs and malodor. Furthermore,
when healthy subjects rinsed their mouths with a cysteine solution (Wåler 1997), VSC
production rose sharply, especially from the tongue dorsum.
In 2002, Kleinberg (Kleinberg and Codipilly 2002) reported the use of a cysteine chal-
lenge testing based on successive rinsing with 5 mL of 6 mM cysteine solution for 30 s in
20 min intervals for a period of 7 h. Using these tests, they demonstrated the effect of vari-
ous oral cleansing procedures and products on VSC production in the mouth.
Salivary Incubation Assays
Salivary incubation assays have been used over the past 60 years in oral malodor research.
This system represents the complexity of the oral environment both in terms of bacterial
diversity and substrate availability. Furthermore, this system tends to produce malodor
components following brief anaerobic incubation of only a few hours.
Quirynen and coworkers (Quirynen et al. 2003) reported the use of a salivary incubation
assay in a pilot study of eight healthy subjects. Their results showed strong correlations
between VSC measured from the saliva samples following 3 h anaerobic incubation and
Table 8.7 Association between microbial assays and oral malodor parameters

Reference Assay Parameters Association
Hartley et al. Differential agar Regression analysis
(1996) (n = 50) for H2S producing
bacteria Odor judgea and % Black r = 0.37, p < 0.001
CFUb
Quirynen et al. Salivary incubation Pearson correlation
(2003) (n = 8) assay
Odor judge and VSC saliva
c d e
r = 0.54, p < 0.001
Haraszthy et al. Polymerase chain c2 analysis
(2007) (n = 13) reaction (PCR)
Halitosisa, d and % S. mooreif c2 = 0.22, p < 0.05
Sterer et al. Microscopic sulfide Spearman correlation
(2008) (n = 42) assay (MSA) Odor judgea and MSA scoresg r = 0.48, p = 0.001
a
Odor judge scores (mouth air) on a scale of 0–5
b
Black colonies on growth agar supplemented with ferrous sulfate
c
Odor judge scores (mouth air) on a scale of 0–4
d
e
Following 3 h anaerobic incubation
f
Identified by direct amplification of 16S ribosomal DNA
g
Digital images analysis for black pixels (Image Pro Plus)
oral malodor scores as rated by an odor judge (Table 8.7). They concluded that salivary
incubation assay may serve as an indirect method for oral malodor measurements.
An attempt was made to find a salivary incubation assay that yields odor that more
closely resembles breath odor (Goldberg et al. 1997). Among various additions, it was
found that decarboxylase medium, when inoculated with saliva, produces an odor closely
resembling the character of breath odor.
Microbial Assays
The identification of oral malodor-producing bacteria is based mainly on their ability to

produce hydrogen sulfide. This is commonly done using a differential agar containing lead
or iron. These metal ions precipitate with the sulfide ions creating a black salt that stains
the bacterial colony formed on the differential agar and allows for the enumeration of the
putative malodor producing bacteria in a given sample (Fig. 8.4). This method was used in
order to show an association between oral malodor ratings and malodor producing bacteria
from tongue coating samples (Hartley et al. 1996) (Table 8.7).
However, this technique requires prolonged anaerobic incubation of up to 7 days.
Further, it is limited to the detection of cultivable bacteria, which comprise about 30% of
the total bacterial population in the oral cavity. In 2008, we suggested a new technique
based on the same principle, but that does not require bacterial cultivation (Sterer et al.
2008). We added the iron salt to samples of whole saliva that were kept overnight in
37°C, and the cell-associated black precipitate was observed microscopically (Fig. 8.5).
Microbial Assays 69
Fig. 8.4 Differentiating agar

for VSC producing bacteria
(shown as black colonies)
Fig. 8.5 Microscopic sulfide

assay; VSC producing
bacteria are stained black
(With permission from JBR)
The black precipitate that was quantified by a computerized analysis of the digital images
captured from the microscopic slides was significantly associated with oral malodor lev-
els of 42 subjects. ROC curve analysis showed the technique to have a diagnostic accu-
racy of 0.70 as compared to 0.78 of the Halimeter.
The study of cultivable and non-cultivable bacteria using molecular techniques such as
DNA hybridization and PCR were mostly used for dichotomous comparisons of oral bac-
terial populations of halitosis-positive and negative patients (see Chap. 3), although asso-
ciations between the PCR quantification of malodor-associated bacteria and halitosis have
also been demonstrated (Haraszthy et al. 2007).
References
Allison, V.C., Katz, S.H.: An investigation of stenches and odors for industrial purposes. J. Ind.
Eng. Chem. 11(4), 336–338 (1919)
Amano, A., Yoshida, Y., Oho, T., Koga, T.: Monitoring ammonia to assess halitosis. Oral Surg.
Awano, S., Koshimune, S., Kurihara, E., Gohara, K., Sakai, A., Soh, I., Hamasaki, T., Ansai, T.,
Takehara, T.: The assessment of methyl mercaptan, an important clinical marker for the diag-
nosis of oral malodor. J. Dent. 32(7), 555–559 (2004)
Eur. J. Oral Sci. 117(3), 261–267 (2009)
Brening, R.H., Sulser, G.F., Fosdick, L.S.: The determination of halitosis by the use of the osmo-
scope and the cryoscopic method. J. Dent. Res. 18(2), 127–132 (1939)
De Boever, E.H., De Uzeda, M., Loesche, W.J.: Relationship between volatile sulfur compounds,
BANA-hydrolyzing bacteria and gingival health in patients with and without complaints of oral
malodor. J. Clin. Dent. 4(4), 114–119 (1994)
Figueiredo, L.C., Rosetti, E.P., Marcantonio Jr., E., Marcantonio, R.A., Salvador, S.L.: The rela-
tionship of oral malodor in patients with or without periodontal disease. J. Periodontol. 73(11),
1338–1342 (2002)
Furne, J., Majerus, G., Lenton, P., Springfield, J., Levitt, D.G., Levitt, M.D.: Comparison of vola-
tile sulfur compound concentrations measured with a sulfide detector vs. gas chromatography.
J. Dent. Res. 81(2), 140–143 (2002)
Goldberg, S., Kozlovsky, A., Gordon, D., Gelernter, I., Sintov, A., Rosenberg, M.: Cadaverine as
a putative component of oral malodor. J. Dent. Res. 73(6), 1168–1172 (1994)
Goldberg, S., Kozlovsky, A., Rosenberg, M.: Association of diamines with oral malodor. In:
Rosenberg, M. (ed.) Bad Breath Research Perspectives, pp. 71–85. Ramot Publishing Tel Aviv
University, Tel Aviv (1997)
1113–1120 (2007)
Hartley, M.G., El-Maaytah, M.A., McKenzie, C., Greenman, J.: The tongue microbiota of low
odour and malodorous individuals. Microb. Ecol. Health Dis. 9, 215–223 (1996)
Hunter, C.M., Niles, H.P., Vazquez, J., Kloos, C., Subramanyam, R., Williams, M.I., Cummins, D.,
Lenton, P.A., Majerus, G.J.: Breath odor evaluation by detection of volatile sulfur compounds –
correlation with organoleptic odor ratings. Oral Dis. 11(Suppl 1), 48–50 (2005)
Iwanicka-Grzegorek, K., Lipkowska, E., Kepa, J., Michalik, J., Wierzbicka, M.: Comparison of
ninhydrin method of detecting amine compounds with other methods of halitosis detection.
Oral Dis. 11(Suppl 1), 37–39 (2005)
Kleinberg, I., Codipilly, D.M.: Cysteine challenge testing: a powerful tool for examining oral
malodour processes and treatments in vivo. Int. Dent. J. 52(Suppl 3), 221–228 (2002)
Kostelc, J.G., Zelson, P.R., Preti, G., Tonzetich, J.: Quantitative differences in volatiles from
healthy mouths and mouths with periodontitis. Clin. Chem. 27(6), 842–845 (1981)
Kozlovsky, A., Gordon, D., Gelernter, I., Loesche, W.J., Rosenberg, M.: Correlation between the
BANA test and oral malodor parameters. J. Dent. Res. 73(5), 1036–1042 (1994)
Loesche, W.J., Bretz, W.A., Kerschensteiner, D., Stoll, J., Socransky, S.S., Hujoel, P., Lopatin, D.E.:
Development of a diagnostic test for anaerobic periodontal infections based on plaque hydroly-
sis of benzoyl-DL-arginine-naphthylamide. J. Clin. Microbiol. 28(7), 1551–1559 (1990)
References 71
Mackie, R.I., Stroot, P.G., Varel, V.H.: Biochemical identification and biological origin of key odor
components in livestock waste. J. Anim. Sci. 76(5), 1331–1342 (1998)
Morita, M., Musinski, D.L., Wang, H.L.: Assessment of newly developed tongue sulfide probe for
detecting oral malodor. J. Clin. Periodontol. 28(5), 494–496 (2001)
Morita, M., Wang, H.L.: Relationship of sulcular sulfide level to severity of periodontal disease
and BANA test. J. Periodontol. 72(1), 74–78 (2001)
Murata, T., Yamaga, T., Iida, T., Miyazaki, H., Yaegaki, K.: Classification and examination of hali-
tosis. Int. Dent. J. 52(Suppl 3), 181–186 (2002)
Murata, T., Rahardjo, A., Fujiyama, Y., Yamaga, T., Hanada, M., Yaegaki, K., Miyazaki, H.:
Development of a compact and simple gas chromatography for oral malodor measurement.
J. Periodontol. 77(7), 1142–1147 (2006)
Nachnani, S., Majerus, G., Lenton, P., Hodges, J., Magallanes, E.: Effects of training on odor
judges scoring intensity. Oral Dis. 11(Suppl 1), 40–44 (2005)
Nonaka, A., Tanaka, M., Anguri, H., Nagata, H., Kita, J., Shizukuishi, S.: Clinical assessment of oral
malodor intensity expressed as absolute value using an electronic nose. Oral Dis. 11(Suppl 1),
35–36 (2005)
Oho, T., Yoshida, Y., Shimazaki, Y., Yamashita, Y., Koga, T.: Characteristics of patients complain-
ing of halitosis and the usefulness of gas chromatography for diagnosing halitosis. Oral Surg.
Quirynen, M., Zhao, H., Avontroodt, P., Soers, C., Pauwels, M., Coucke, W., van Steenberghe, D.:
A salivary incubation test for evaluation of oral malodor: a pilot study. J. Periodontol. 74(7),
937–944 (2003)
malodor measurements with a portable sulphide monitor. J. Dent. Res. 70(11), 1436–1440 (1991a)
Rosenberg, M., Septon, I., Eli, I., Bar-Ness, R., Gelernter, I., Brenner, S., Gabbay, J.: Halitosis
measurement by an industrial sulphide monitor. J. Periodontol. 62(8), 487–489 (1991b)
Rosenberg, M., McCulloch, C.A.: Measurement of oral malodor: current methods and future pros-
pects. J. Periodontol. 63(9), 776–782 (1992)
Rosenberg, M., Knaan, T., Cohen, D.: Association among bad breath, body mass index, and alco-
hol intake. J. Dent. Res. 86(10), 997–1000 (2007)
Schmidt, N.F., Missan, S.R., Tarbet, W.J.: The correlation between organoleptic mouth-odor ratings
and levels of volatile sulfur compounds. Oral Surg. Oral Med. Oral Pathol. 45(4), 560–567 (1978)
Shimura, M., Yasuno, Y., Iwakura, M., Shimada, Y., Sakai, S., Suzuki, K., Sakamoto, S.: A new
monitor with a zinc-oxide thin film semiconductor sensor for the measurement of volatile sul-
fur compounds in mouth air. J. Periodontol. 67(4), 396–402 (1996)
Shimura, M., Watanabe, S., Iwakura, M., Oshikiri, Y., Kusumoto, M., Ikawa, K., Sakamoto, S.:
Correlation between measurements using a new halitosis monitor and organoleptic assessment.
J. Periodontol. 68(12), 1182–1185 (1997)
Solis Gaffar, M.C., Fischer, T.J., Gaffar, A.: Instrumental evaluation of odor produced by specific
oral microorganisms. J. Soc. Cosmet. Chem. 30, 241–247 (1979)
Sopapornamorn, P., Ueno, M., Vachirarojpisan, T., Shinada, K., Kawaguchi, Y.: Association
between oral malodor and measurements obtained using a new sulfide monitor. J. Dent. 34(10),
770–774 (2006)
Stamou, E., Kozlovsky, A., Rosenberg, M.: Association between oral malodour and periodontal
disease-related parameters in a population of 71 Israelis. Oral Dis. 11(Suppl 1), 72–74 (2005)
Sterer, N., Rosenberg, M.: Streptococcus salivarius promotes mucin putrefaction and malodor
production by Porphyromonas gingivalis. J. Dent. Res. 85(10), 910–914 (2006)
Sterer, N., Hendler, A., Perez Davidi, M., Rosenberg, M.: A novel microscopic assay for oral mal-
odor related microorganisms. J. Breath Res. 2, 026003 (2008) (5 pp)
Tanaka, M., Anguri, H., Nonaka, A., Kataoka, K., Nagata, H., Kita, J., Shizukuishi, S.: Clinical
assessment of oral malodor by the electronic nose system. J. Dent. Res. 83(4), 317–321
(2004a)
Tanaka, M., Yamamoto, Y., Kuboniwa, M., Nonaka, A., Nishida, N., Maeda, K., Kataoka, K.,
Nagata, H., Shizukuishi, S.: Contribution of periodontal pathogens on tongue dorsa analyzed
with real-time PCR to oral malodor. Microbes Infect. 6(12), 1078–1083 (2004b)
Arch. Oral Biol. 16(6), 587–597 (1971)
Tonzetich, J., Carpenter, P.A.: Production of volatile sulphur compounds from cysteine, cystine
and methionine by human dental plague. Arch. Oral Biol. 16(6), 599–607 (1971)
Vandekerckhove, B., Van den Velde, S., De Smit, M., Dadamio, J., Teughels, W., Van Tornout, M.,
Quirynen, M.: Clinical reliability of non-organoleptic oral malodour measurements. J. Clin.
Periodontol. 36(11), 964–969 (2009)
Wåler, S.M.: On the transformation of sulfur containing amino acids and peptides to volatile sulfur
compounds (vsc) in the human mouth. Eur. J. Oral Sci. 105, 534–537 (1997)
Willis, C.L., Gibson, G.R., Holt, J., Allison, C.: Negative correlation between oral malodour and
numbers and activities of sulphate-reducing bacteria in the human mouth. Arch. Oral Biol.
44(8), 665–670 (1999)
Yaegaki, K., Sanada, K.: Volatile sulfur compounds in mouth air from clinically healthy subjects
and patients with periodontal disease. J. Periodontal Res. 27(4 Pt 1), 233–238 (1992)
Yoneda, M., Masuo, Y., Suzuki, N., Iwamoto, T., Hirofuji, T.: Relationship between b-galactosi-
dase activity in saliva and parameters associated with oral malodor. J. Breath Res. 4(1), 017108
(2010) (6 pp)
Breath Odor Diagnosis
9
Unlike other complaints such as pain, discomfort, or impaired esthetics, breath odors are
not sensed by the patients themselves but rather by people around them (e.g., friends, fam-
ily members, coworkers). As a result, patients are unable to give a reliable report on their
condition (e.g., onset, frequency, duration, intensity). Therefore, it is important to make
sure that the patient brings a family member or a close friend (i.e., “confidant”) to the
appointment (Rosenberg 1996).
Additionally, modern society is constantly exposed to commercial advertisements
stressing the importance of fresh breath, fuelling excessive anxiety surrounding this issue,
also known as halitophobia (for more details, see Chap. 12). One result of this phenome-
non is that about 20% of the patients complaining of breath odors present in the clinic
without any appreciable odor that can be objectively detected (Quirynen et al. 2009;
Seemann et al. 2006).
The first diagnostic challenge in the clinic is to confirm whether or not the patient is
suffering from an objective malodor problem, referred to by some researchers as genuine
halitosis (Yaegaki and Coil 2000).
Pre-appointment Instructions
In order to enable the clinician to properly diagnose breath odor problems, patients should
avoid any malodor mitigating activities such as eating, drinking, or gum chewing for 2–3 h
prior to their appointment (Rosenberg 1996). Avoiding eating or drinking for longer peri-
ods of time (e.g., 6–12 h) has been suggested in the literature (Murata et al. 2002; Richter
1996). However, such a restriction may be problematic in the case of small children or
diabetic patients, does not imitate normal everyday life, and may lead to over diagnosis
and over treatment.
In light of the fact that in most cases malodor production results from bacterial activity,
malodor diagnosis should not be performed during or immediately following antibiotic
treatment. If a patient is receiving antibiotics, malodor diagnosis should be postponed till
3–4 weeks following treatment. Performing malodor diagnosis during or immediately fol-
lowing antibiotic treatment may result in misdiagnosing a genuine halitosis patient.

74 9 Breath Odor Diagnosis
On the day of examination, patients should maintain their regular everyday oral hygiene
activity. However, these activities should not include mouthrinse use and should not be
performed within 2–3 h prior to the appointment to avoid malodor reduction.
To avoid external effects on malodor measurements, consumption of onion, garlic,
alcoholic beverages, coffee, as well as smoking should be avoided for 12 h prior to the
appointment. Scented lipstick, cologne, or perfumes should not be worn on the day of
examination, as they can confuse odor judge assessment.
Patient Interview
Due to the sensitive nature of the subject, patient interviewing should be done discreetly in
a private setting (Lenton et al. 2001). A fruitful discussion on the subject can only be car-
ried out in a calm, relaxed atmosphere where trust can be established.
In some cases, the patient’s chief complaint is self-perceived malodor, which often
relies on two forms of sensation: oral discomfort (e.g., bad taste, dryness) and the interpre-
tation of various human gestures (e.g., head averting, nose covering, and back stepping) of
people encountered by the patient (see Chaps. 10 and 12). It is important to stress that these
sensations are mostly unassociated with malodor and that reliable information regarding
breath odor problems (e.g., onset, frequency, duration, intensity) can only be provided by
a ‘confidant,’ i.e., family member or a close friend of the patient (Rosenberg 1996).
A complete medical history should be taken to rule out any possible systemic or ENT
conditions or medications that may contribute or cause malodor. Dental history should also
be taken with an emphasis on oral hygiene practice including frequency of tooth brushing,
flossing, tongue cleaning, and mouthrinsing. Special attention should be given to habits of
smoking, alcohol and coffee consumption, and eating habits (e.g., avoiding breakfast).
Factors such as mouth breathing (e.g., snoring) and insufficient fluid intake should also be
addressed, as they can promote oral dryness. Allergic reactions, specifically in the form of
allergic rhinitis (sneezing and “running nose”) may cause increased postnasal drip.
Examination
Organoleptic Measurements
In order to assess the severity of the problem, the clinician should instruct the patient to
refrain from talking for 5 min. Then, the patient is asked to exhale through the mouth or talk
(e.g., “count to twenty”) and the clinician rates the malodor intensity on his breath using a
0–5 grading scale (Rosenberg et al. 1991) from a set distance of 10 cm. Next, the patient is
instructed to exhale through the nose and malodor is again evaluated in the same manner.
In cases that the malodor is felt from the mouth, an oral etiology is suspected and a
thorough examination of the oral cavity is warranted. If, however, the malodor is felt pri-
marily from the nose, a nasopharyngeal etiology is more likely and the patient should be
Examination 75
referred to an ENT specialist. In rare cases in which the malodor is similar in quality and
intensity from both the mouth and the nose, a systemic or external etiology is suspected.
In some cases, no malodor is felt and the problem cannot be confirmed. In these cases,
when a close friend or family member maintains that there is an odor problem, the exami-
nation should be repeated on a different occasion, preferably in the late afternoon or late
morning hours (Miyazaki et al. 1995). Otherwise, if malodor cannot be detected, then hali-
tophobia is the most likely cause for the patient’s complaint.
Oral VSC Quantification
The instrumental quantification of volatile sulfide compounds within the oral cavity is an
important adjunct tool in oral malodor diagnosis. It enables the clinician to record and
present to the patient a measurable objective parameter associated with the malodor. This
helps either to confirm or rule out the existence of a malodor problem as defined organo-
leptically, as well as following improvement.
The most commonly used instrument for this purpose is the portable sulfide monitor
(i.e., Halimeter™). Its simple use, low maintenance, quick response, and portability make
it an applicable instrument for both research and the clinic. Its major disadvantages are its
sensitivity to other compounds (e.g., alcohol) and its inability to distinguish between vari-
ous sulfide compounds.
Gas chromatography (GC) has been used since the early 1970s as the method of choice
for mouth air samples VSC identification and quantification. However, this technique
requires high technical skills and maintenance. Recently, a more simple-to-use instrument
was devised based on GC technology (i.e., OralChroma™; (Murata et al. 2006)).
Examination of the Oral Cavity
In cases where an oral etiology is suspected, a thorough examination of the oral cavity is
warranted. This should include the tongue, gingival, and periodontal tissues, as well as
clinical and radiographical examination of the teeth.
When examining the tongue, special attention should be given to the presence and
extent of tongue coating. The extent of the tongue coating can be either scored and recorded
using a simple tongue coating index based on coating area and/or thickness (for more
details see Chap. 2), or by digital images analysis (Kim et al. 2009). Following scoring,
tongue coating can be sampled using swab, gauze pad, brush, or plastic spoon (“spoon
test”; (Rosenberg 1996)). It is important to make sure that the sample is obtained from the
posterior third of the tongues dorsum. This can be done by holding the tip of the extended
tongue using a gauze pad with one hand and sampling with the other. Then, the malodor
emanating from this sample can be scored organoleptically (e.g., 0–5 scale) and compared
to the oral odor present (both by the clinician and the confidant).
Patients should be checked for the presence of periodontal pocket of 5 mm or more and
gingival index as well as plaque index should be recorded. Special attention should be
given to sites with signs of active inflammation (i.e., bleeding on probing). An interdental
76 9 Breath Odor Diagnosis
plaque sample from these sites can be obtained using regular unscented dental floss, spe-
cial floss (e.g., Superfloss™) or an interdental brush. These samples can also be scored
organoleptically (e.g., 0–5 scale) and compared to the overall quality of the oral odor.
Clinical and radiographical examination of the teeth should be conducted in order to
identify any possible contributing factors including faulty dental restorations (e.g., over-
hanging margins, food impaction sites, caries lesions), and leaky crowns (e.g., decemented
crowns). Removable dentures should be evaluated separately outside of the oral cavity.
This could be done by placing them for a few minutes in a closed plastic bag and evaluat-
ing the malodor produced (Rosenberg 1996).
Biochemical and Microbial Assays
The growing body of knowledge accumulated over the last decades regarding the microbial
and biochemical processes involved in malodor production has led to the development of
several auxiliary diagnostic assays that can be implemented in the clinic (i.e., “chair side”).
These assays play a role in providing additional quantitatively measurable malodor-
related parameters for the clinician as well as providing an important tool for patient
education.
Biochemical assays (e.g., BANA test, b-galactosidase assay) are enzymatic-based
assays typically producing a color response as a result of an enzymatic activity related to
the malodor production process (e.g., proteolysis, deglycosylation). These color producing
reactions are relatively rapid and enable the visualization and quantification of an other-
wise abstract notion such as malodor production. Furthermore, these assays offer addi-
tional corroboration for the diagnosis of the suspected malodor origin and etiology.
Microbial assays are less commonly used because they usually require additional equip-
ment and prolonged incubation. However, some clinicians do utilize live microscopy (e.g.,
wet mount, phase microscopy) to demonstrate to the patient the bacterial nature and abun-
dance of plaque samples taken from various locations in the mouth (e.g., teeth, tongue).
References
Kim, J., Jung, Y., Park, K., Park, J.W.: A digital tongue imaging system for tongue coating evalu-
ation in patients with oral malodour. Oral Dis. 15(8), 565–569 (2009)
Lenton, P., Majerus, G., Bakdash, B.: Counseling and treating bad breath patients: a step-by-step
approach. J. Contemp. Dent. Pract. 2(2), 46–61 (2001)
(1995)
Murata, T., Yamaga, T., Iida, T., Miyazaki, H., Yaegaki, K.: Classification and examination of hali-
tosis. Int. Dent. J. 52(Suppl 3), 181–186 (2002)
Murata, T., Rahardjo, A., Fujiyama, Y., Yamaga, T., Hanada, M., Yaegaki, K., Miyazaki, H.:
Development of a compact and simple gas chromatography for oral malodor measurement.
J. Periodontol. 77(7), 1142–1147 (2006)
References 77
Periodontol. 36(11), 970–975 (2009)
Richter, J.L.: Diagnosis and treatment of halitosis. Compend. Contin. Educ. Dent. 17(4), 370–372,
374–376 (1996) (passim; quiz 388)
malodor measurements with a portable sulphide monitor. J. Dent. Res. 70(11), 1436–1440
(1991)
475–482 (1996)
Seemann, R., Bizhang, M., Djamchidi, C., Kage, A., Nachnani, S.: The proportion of pseudo-
halitosis patients in a multidisciplinary breath malodour consultation. Int. Dent. J. 56(2), 77–81
(2006)
Yaegaki, K., Coil, J.M.: Examination, classification, and treatment of halitosis; clinical perspec-
tives. J. Can. Dent. Assoc. 66(5), 257–261 (2000)
Self-Assessment of Breath Odors
10
The inability of a person to sense his own breath results in a situation called the “bad breath
paradox” (Scott Harper, personal communication). According to this paradox, most of the
people suffering from breath odors are unaware of their condition, whereas many others
that do not have any breath odor worry excessively that they do. For example, in a study
of 88 subjects attending a routine health check up, 19 thought that they had bad breath, but
this was not confirmed by the odor judge. Conversely, nine had breath odor (as determined
by the odor judge) but were not aware of it (Rosenberg et al. 2007). In another study con-
ducted in Japan (Iwakura et al. 1994), 80% of the patients who visited the clinic claimed
to be self-aware of their condition, while only 24% had actual malodor.
Some researchers attributed the inability to sense one’s own breath to olfactory accom-
modation or adaptation (Spouge 1964), i.e., continuous exposure to an odor stimuli result-
ing in specific desensitization of the olfactory system to that odorant. However, research
indicates that this may not be the case, since subjects were able to sense the malodor of
their saliva (Greenstein et al. 1997; Rosenberg et al. 1995) even though this malodor osten-
sibly comprises many of the same odorants. Therefore, it seems that the explanation for
this phenomenon is much simpler. Since the malodor components are extremely volatile
from the time the person exhales them, until he inhales again, their concentration drops
below their detection threshold. That may be why people cannot detect their own odor
while the people facing them can.
Most researchers found no correlations between self-reported breath odor ratings and
breath odor objective clinical measurements as carried out by the trained odor judge
(Bornstein et al. 2009; Rosenberg et al. 1995) and therefore concluded that self-reported
breath odor is an unreliable parameter. One study, on the other hand, did conclude that
“self-estimation of bad breath correlated well with the presence of oral malodor” (Romano
et al. 2010). However, a critical review of the results of this study shows no correlation
between the self-assessment and the odor judge ratings or other clinical parameters.
Despite these facts, many studies still erroneously rely on self-reported breath odors, usu-
ally by means of a questionnaire as an objective parameter in breath odor investigations
(for examples, see Chap. 6).
It seems that the physical inability to detect one’s breath odor is not the only limitation
in self-assessment of breath odors. Research showed that even when given a sample of
their odor (e.g., tongue coating sample), subjects lacked the ability to objectively rate and
score the odor. It seems that there are psychological factors that color our objectivity about
our own body traits, including smells. For example, in 1995, a study was reported on

80 10 Self-Assessment of Breath Odors
s elf-assessment of bad breath involving 52 subjects, 43 of whom were concerned that they
did have bad breath (Rosenberg et al. 1995). They were asked to fill out a questionnaire,
asking them to score their own oral malodor as follows:
(a) Preconception score – prior to measurement, subjects were asked to score the level of
bad breath, which they thought they had at that time.
(b) M outh odor – subjects were asked to cup their hands over their mouth and nose, exhale
through the mouth and breath in through the nose, and subsequently score the odor.
(c) Tongue odor – subjects were asked to lick their wrist and smell and score that odor.
(d) S aliva odor – subjects were asked to smell and score their own saliva, placed in a
plastic dish
(e) Post-measurement score – subjects were asked to again rate their own odor, following
all three self-tests.
All these subjects and samples were also scored by an experienced odor judge.
The results of this study showed that with the exception of saliva, subjects’ self-assess-
ments were completely unrelated to odor judge scores, volatile sulfides, cadaverine, or oral
status. Instead, they remained closely associated with their preconception scores. Even
after the three attempts at smelling their own malodor, the post-measurement scores
remained unassociated with any of the objective parameters, yet highly associated with the
subjective preconception score (r = 0.72, p < 0.001).
One year following the initial experiment, 32 of the concerned subjects were invited
back to the laboratory for a follow-up assessment (Rosenberg et al. 1999). Although the
mouth odor and saliva odor of the subjects had significantly improved according to the
odor judge, p = 0.006 and p = 0.009, respectively, (they had been given instructions during
the initial study 1 year prior and 85% had sought dental care), the subjects’ self-assess-
ments of mouth odor and saliva odor showed no significant improvement (p = 0.22 and
p = 0.50, respectively). Instead, they seemed to sense a slight but significant improvement
in tongue odor (p = 0.017), which was not supported by the objective odor judge (p = 0.98).
Their self-assessment of tongue odor was closely associated again with their preconcep-
tion of how bad they thought the odor would be (r = 0.65, p < 0.001), and how they scored
it at the initial consultation (r = 0.71, p < 0.001). None of the self scores were significantly
related to any of the odor judge scores.
It appears that subjects who are concerned about having breath odors tend to give their
breath samples higher scores as compared to the objective scores given by the odor judge
(Eli et al. 2001). Subjects recruited for reasons other than breath concerns may exhibit
higher levels of overall agreement with objective parameters. For example, among the 88
subjects attending a routine medical checkup, self-reporting of halitosis as compared with
odor judge scoring (at a cutoff of greater than or equal to 2) yielded an accuracy of 67%.
In another recent study (Nalcaci and Baran 2008), 254 “healthy elderly” Turkish sub-
jects (mean age 62) were asked regarding their oral health status. Among them, 28%
reported that they suffered from bad breath. Most of these subjects also reported oral dry-
ness (74%). Although each subject underwent a comprehensive dental examination, includ-
ing tongue coating level, the researchers did not actually smell the odor of the subjects, nor
did they perform any adjunct testing for VSC levels. Nevertheless, a significant and
References 81
relatively high correlation between self-reported bad breath and tongue coating levels
(p = 0.59, p = 0.0001) was recorded, followed by self-reported oral dryness (p = 0.41,
p = 0.0001).
Self-assessment of breath odors appears to be associated with various factors such as
lack of good oral hygiene, smoking, presence of tongue coating, subjective oral dryness,
wearing dentures, gum disease, alcohol consumption age (over 30), and gender (females)
(Al-Ansari et al. 2006; Nalcaci and Baran 2008; Settineri et al. 2010). Females seem to
give themselves higher malodor scores than men. For instance, one study reported that
women scored significantly higher than men in rating their own malodor although men
were assigned higher scores by the odor judge. In that study, 25 out of 88 women gave
themselves the highest score of “5” (on a 0–5 scale) as compaired to “3.5” given by the
odor judge. Nevertheless, self estimates of both genders were still significantly higher than
odor judge scores (Rosenberg and Leib 1997).
References
Al-Ansari, J.M., Boodai, H., Al-Sumait, N., Al-Khabbaz, A.K., Al-Shammari, K.F., Salako, N.:
Factors associated with self-reported halitosis in Kuwaiti patients. J. Dent. 34(7), 444–449
(2006)
Bornstein, M.M., Stocker, B.L., Seemann, R., Burgin, W.B., Lussi, A.: Prevalence of halitosis in
young male adults: a study in swiss army recruits comparing self-reported and clinical data.
J. Periodontol. 80(1), 24–31 (2009)
Eli, I., Baht, R., Koriat, H., Rosenberg, M.: Self-perception of breath odor. J. Am. Dent. Assoc.
132(5), 621–626 (2001)
Iwakura, M., Yasuno, Y., Shimura, M., Sakamoto, S.: Clinical characteristics of halitosis: differ-
ences in two patient groups with primary and secondary complaints of halitosis. J. Dent. Res.
73(9), 1568–1574 (1994)
Nalcaci, R., Baran, I.: Factors associated with self-reported halitosis (SRH) and perceived taste
disturbance (PTD) in elderly. Arch. Gerontol. Geriatr. 46(3), 307–316 (2008)
Romano, F., Pigella, E., Guzzi, N., Aimetti, M.: Patients’ self-assessment of oral malodour and its
relationship with organoleptic scores and oral conditions. Int. J. Dent. Hyg. 8(1), 41–46 (2010)
Rosenberg, M., Kozlovsky, A., Gelernter, I., Cherniak, O., Gabbay, J., Baht, R., Eli, I.: Self-
estimation of oral malodor. J. Dent. Res. 74(9), 1577–1582 (1995)
Rosenberg, M., Leib, E.: Experiences of an Israeli malodor clinic. In: Rosenberg, M. (ed.) Bad Breath
Research Perspectives, pp. 137–148. Ramot Publishing – Tel Aviv University, Tel Aviv (1997)
Rosenberg, M., Kozlovsky, A., Wind, Y., Mindel, E.: Self-assessment of oral malodor 1 year
following initial consultation. Quintessence Int. 30(5), 324–327 (1999)
Rosenberg, M., Knaan, T., Cohen, D.: Association among bad breath, body mass index, and
alcohol intake. J. Dent. Res. 86(10), 997–1000 (2007)
Settineri, S., Mento, C., Gugliotta, S.C., Saitta, A., Terranova, A., Trimarchi, G., Mallamace, D.:
Self-reported halitosis and emotional state: impact on oral conditions and treatments. Health
Qual. Life Outcomes 8, 34 (2010)
Spouge, J.D.: Halitosis: a review of its causes and treatment. Dent. Pract. 14, 307–317 (1964)
Breath Odors, Prevalence,
Gender, and Age 11
Prevalence
Breath odors are a common condition. Various studies conducted around the world in
different populations, using different measuring techniques and varying threshold criteria
have reported different prevalence of this condition, ranging from as low as 2% of the
population to over 60% (Table 11.1).
It is clear that the lack of standardization in threshold criteria and measuring techniques
is the cause for this large variation. For example, a study that was conducted in Sweden
(Soder et al. 2000), which used “strong, noticeably unpleasant odor” (i.e., “Foetor ex ore”)
as the criterion for breath odors, reported 2.4% prevalence in a population of 1681 sub-
jects. Using such a high threshold that is equivalent to an odor judge score “4” (i.e., “strong
malodor”) on a 0–5 scale yielded a similarly low prevalence (2.14%) in a study done in
Swaziland (Bornstein et al. 2009). However, in the same study, when an odor judge score
of “2” and above was applied as a threshold for malodor (i.e., “mild, clearly noticeable
malodor”), prevalence reached 31.5%.
Some of these studies regarded odor judge scores of “2” and above as the threshold
value for breath odors (Bornstein et al. 2009; Iwanicka-Grzegorek et al. 2005; Liu et al.
2006; Rosenberg et al. 2007). Using this criterion, they reported that 27.5–31.5% of the
subjects were positive for breath odors, concluding that the prevalence of breath odors in
the general population is a little over 25%.
A few studies based their breath odor assessment solely on oral VSC levels (Miyazaki
et al. 1995; Miyazaki et al. 1997), as measured using a sulfide monitor (i.e., Halimeter),
whereas others used VSC measurements adjacent to organoleptic scorings (Bornstein et al.
2009; Iwanicka-Grzegorek et al. 2005; Liu et al. 2006). These studies regarded different
VSC concentration values as cutoff points for breath odor conformation (e.g., 75, 110,
125 ppb, respectively). It is important to stress that although VSC readings using Halimeter
are in high correlation with organoleptic scores and their value is an important parameter
for clinical follow up, the absolute value of a given reading would vary between different
instruments depending on the sensor’s freshness. Therefore, setting a universal cutoff
value would be impractical.

84
Table 11.1 Prevalence of breath odors

Reference Subjects Malodor parameter Criteria/cutoff Prevalence
population (%)
Sulser et al. (1939) n = 200 Age n.d. Osmoscope (indirect method) Malodor score of PO2 and above (“objectionable”) 56
Morris and Read (1949) No. n.d. Osmoscope (direct method; 2 Malodor score of PO3 and above (1–6) (“halitosis”) 65
Age 18–60 years operators)
Miyazaki et al. (1995) n = 2,672 VSC measured by Halimeter VSC level ³ 75 ppb
Age 18–64 years Less than 2 h following meals 6–14
More than 2 h following meals 16–23
Miyazaki et al. (1997) n = 2,601 VSC measured by Halimeter VSC level ³ 75 ppb
Age 18–64 years Less then 2.5 h following meals 8–15
More then 2.5 h following meals 18–25
Loesche et al. (1996) n = 270 Questionnaire “Been told you have” 24
Age ³ 60 years “Think you have” 31
Soder et al. (2000) n = 1681 Organoleptic Strong, noticeably unpleasant odor (“Foetor ex ore”) 2.4
Mean age 36 years
Iwanicka-Grzegorek et al. n = 295 Organoleptic Malodor score ³ 2 (0–5) 29.7
(2005) Age 18–74 years Halimeter VSC levels ³ 125 ppb 24.5
Liu et al. (2006) n = 2000 Organoleptic Malodor score ³ 2 (0–5) 27.5
Age 15–64 years Halimeter VSC levels ³ 75 ppb 35.4
³110 ppb 20.3
Nadanovsky et al. (2007) n = 344 Informants questionnaire “Yes” to: “family member with bad breath?” 15
Age 1–87 years
Rosenberg et al. (2007) n = 88 (46M) Organoleptic Malodor score ³ 2 (0–5) 29.8
Age 20–55 years
Bornstein et al. (2009) n = 419 Organoleptic Malodor score ³ 2 (0–5) 31.5
Age 18–94 years Halimeter ³3 (0–5) 11.4
³4 (0–5) 2.14
11 Breath Odors, Prevalence, Gender, and Age
VSC levels ³ 75 ppb 27.9

³110 ppb
Gender 85
Gender
Gender is usually not taken into account in breath odor investigations since most studies
report no difference between male and female subjects in the prevalence or levels of mal-
odor (Miyazaki et al. 1995; Sulser et al. 1939). However, as shown in Table 11.2, some
studies did report a variation between males and females. One study conducted in the gen-
eral population of China (Liu et al. 2006) showed elevated VSC levels in females in the
age group of 35–44 years as compared to males. Although this study did not find similar
results in the other age groups, it has been reported in the literature that women showed a
two- to fourfold increase in VSC levels in mouth air during and shortly prior to menstrua-
tion (Calil et al. 2008; Tonzetich et al. 1978), especially in women with signs of periodon-
tal disease (Kawamoto et al. 2010). This increase in VSC levels coincided with hormonal
levels and salivary flow reduction.
On the other hand, another study conducted in Brazil reported a much higher prevalence
of breath odors in males as compared to females (Nadanovsky et al. 2007), although this
study relied on questionnaire reports by a family member rather than actual measurements.
Table 11.2 Gender, age and breath odors

Reference Subjects Gender Age
Sulser et al. n = 200 Equal prevalence in Malodor increased
(1939) (64% males) males and females with age
Age groups: (on average)
£20 (n = 20)
21–50 (n = 144)
³51 (n = 36)
Miyazaki et al. n = 2,672 No difference in VSC No difference in VSC
(1995) (64% males) levels between males levels between age
Age groups: and females groups
15–24 (n = 317)
25–34 (n = 595)
35–44 (n = 916)
45–54 (n = 615)
55–64 (n = 229)
Liu et al. (2006) n = 2000 Significantly higher No difference in VSC
(50% males) VSC level in females levels between age
Age groups: in age group groups
15–24 (n = 400) 35–44 years.
25–34 (n = 400) Correlations between
gender and VSC
35–44 (n = 400)
levels (logistic
45–54 (n = 400) regression analysis)
55–64 (n = 400)
Nadanovsky n = 344 Higher prevalence in Higher prevalence in
et al. (2007) (49% males) males (21%) then people over 20 years
Age 1–87 years females (9%) old (17%) than under
(mean 39 ± 18) 20 years old (7%) for
both sexes
86 11 Breath Odors, Prevalence, Gender, and Age
Age
Although some researchers reported an increase in breath odors with age (Sulser et al.
1939), most studies that were conducted on adult populations do not consider age to be a
risk factor (Table 11.2). However, under the age of 20, breath odors seem to be much less
prevalent (Nadanovsky et al. 2007).
Whether or not age plays a part in the prevalence and severity of this problem is yet to
be determined. However, it is clear that the origins of oral malodor and its character may
vary with age. In children and adolescents, oral malodor was associated with tongue coat-
ing and plaque index (Amir et al. 1999; Nalcaci and Sonmez 2008). Whereas the tongue
seems to play a major role in oral malodor throughout life, other factors may add on and
vary. For example, after the age of 45, periodontal disease becomes associated with mal-
odor production (Bosy et al. 1994). The taking of various medications may affect saliva
flow in subjects over the age of 50 (e.g., antihypertensive drugs), and in the elderly popula-
tion, denture-related problems may contribute to malodor production.
References
Amir, E., Shimonov, R., Rosenberg, M.: Halitosis in children. J. Pediatr. 134(3), 338–343 (1999)
Eur. J. Oral Sci. 117(3), 261–267 (2009)
Bosy, A., Kulkarni, G.V., Rosenberg, M., McCulloch, C.A.: Relationship of oral malodor to periodon-
titis: evidence of independence in discrete subpopulations. J. Periodontol. 65(1), 37–46 (1994)
Calil, C.M., Lima, P.O., Bernardes, C.F., Groppo, F.C., Bado, F., Marcondes, F.K.: Influence of
gender and menstrual cycle on volatile sulphur compounds production. Arch. Oral Biol. 53(12),
1107–1112 (2008)
Iwanicka-Grzegorek, E., Michalik, J., Kepa, J., Wierzbicka, M., Aleksinski, M., Pierzynowska, E.:
Subjective patients’ opinion and evaluation of halitosis using halimeter and organoleptic scores.
Oral Dis. 11(Suppl 1), 86–88 (2005)
Kawamoto, A., Sugano, N., Motohashi, M., Matsumoto, S., Ito, K.: Relationship between oral
malodor and the menstrual cycle. J. Periodontal Res. 45(5), 681–687 (2010)
Liu, X.N., Shinada, K., Chen, X.C., Zhang, B.X., Yaegaki, K., Kawaguchi, Y.: Oral malodor-
related parameters in the Chinese general population. J. Clin. Periodontol. 33(1), 31–36 (2006)
Loesche, W.J., Grossman, N., Dominguez, L., Schork, A.: Oral malodour in the elderly. In: Van
Steenberghe, D., Rosenberg, M. (eds.) Bad Breath a Multidisciplinary Approach, pp. 181–194.
Leuven University Press, Leuven (1996)
(1995)
Miyazaki, H., Sakao, S., Katoh, Y., Takehara, T.: Oral malodor in the general population of Japan.
In: Rosenberg, M. (ed.) Bad Breath Research Perspectives, pp. 118–136. Ramot Publishing –
Tel Aviv University, Tel Aviv (1997)
Morris, P.P., Read, R.R.: Halitosis; variations in mouth and total breath odor intensity resulting
from prophylaxis and antisepsis. J. Dent. Res. 28(3), 324–333 (1949)
References 87
Nadanovsky, P., Carvalho, L.B., Ponce de Leon, A.: Oral malodour and its association with age
and sex in a general population in Brazil. Oral Dis. 13(1), 105–109 (2007)
Nalcaci, R., Sonmez, I.S.: Evaluation of oral malodor in children. Oral Surg. Oral Med. Oral
Pathol. Oral Radiol. Endod. 106(3), 384–388 (2008)
Rosenberg, M., Knaan, T., Cohen, D.: Association among bad breath, body mass index, and alco-
hol intake. J. Dent. Res. 86(10), 997–1000 (2007)
Soder, B., Johansson, B., Soder, P.O.: The relation between foetor ex ore, oral hygiene and peri-
odontal disease. Swed. Dent. J. 24(3), 73–82 (2000)
Sulser, G.F., Brening, R.H., Fosdick, L.S.: Some conditions that effect the odor concentration of
breath. J. Dent. Res. 18(4), 355–359 (1939)
Tonzetich, J., Preti, G., Huggins, G.R.: Changes in concentration of volatile sulphur compounds of
mouth air during the menstrual cycle. J. Int. Med. Res. 6(3), 245–254 (1978)
Psychological Aspects of Breath Odors
12
Halitophobia
In some 15–30% of patients complaining of a serious breath odor problem, little or no malodor
can be detected by the examiner either organoleptically by smelling the patient’s breath or
using laboratory techniques (Quirynen et al. 2009; Seemann et al. 2006). These patients vary
in their level of conviction regarding their perceived odor problem. Some are uncertain and
just wish to confirm or rule out a breath odor problem, whereas others firmly believe that the
problem exists. In extreme cases, patients may appear psychotic and/or contemplate suicide
(Yaegaki and Coil 1999). Some researchers have dichotomously subclassified these patients
into “Pseudohalitosis” and “Halitophobia” based on their treatment response and need of
psychiatric consultation (Yaegaki and Coil 2000). Alternatively, other researchers regard
“Halitophobia” as a “mild to severe” spectrum of conditions that includes any level of exag-
gerated concern of having a breath odor problem (Rosenberg and Leib 1997).
Convinced of the somatic basis of their complaint, many halitophobic patients visit vari-
ous medical specialists (e.g., dentists, ENT, gastroenterologists, etc.) in the hope of finding a
cure for their perceived ailment. For example, one study (Seemann et al. 2006) reported that
76% of the halitophobic patients that visited the clinic had received prior treatments for bad
breath, 36% received gastroscopies and 14% underwent an ENT operation – all that without
having any detectable signs of bad breath. Only 9% of those patients went through an actual
organoleptic evaluation of their breath before they underwent these medical procedures.
Olfactory Reference Syndrome (ORS)
Halitophobia is considered one manifestation of Olfactory Reference Syndrome (Pryse-

Phillips 1971), described as “preoccupation about body odour accompanied by shame,
embarrassment, significant distress, avoidance behaviour and social isolation” (Lochner
and Stein 2003). Halitophobia has also been considered as a type of monosymptomatic
delusion (“delusional halitosis”), alongside parasitosis.
Psychological disorders, in which a person is convinced of giving off bodily odors
perceived by others, have been reported in the literature since the late 1800s. These

90 12 Psychological Aspects of Breath Odors
d isorders were termed “Bromidrosiphobia” (Sutton 1919), “Chronic olfactory paranoid

syndrome” (Videbech 1966), and “Taijin-kyofusho” (Suzuki et al. 2004).
Pryse-Phillips (1971) noted that in patients suffering from ORS, the belief of giving off
bodily odors was accompanied by certain behaviors such as excessive washing and use of
deodorants and perfumes, social avoidance, and multiple medical consultations. Furthermore,
ideas of reference were another common feature. Patients believed that people made comments
or gestures regarding their bodily odors especially in confined spaces (e.g., trains, buses).
A recent systematic review (Begum and McKenna 2011) was conducted on ORS case
reports based on the following diagnostic criteria:
1. A persistent false belief that one emits a malodorous smell; this belief may encompass
a range of insight (i.e., does not have to be delusional).
2. The belief causes clinically significant distress, is time consuming (i.e., preoccupies the
individual for at least 1 h per day), or results in significant impairment in social, occu-
pational, or other important areas of functioning.
3. The belief is not better accounted for by another mental disorder or general medical
condition.
This study reported that the mean age of onset for ORS was 21 with 58% of the cases being less
than 20 years old. Low mood was present in 39% and anxiety in 42% of the cases. In 49% of
the subjects, precipitant events were present, and were mainly (85%) smell-related experiences
(remarks or gestures from family members or classmates) accompanied by shame and embar-
rassment. The smells included smells of feet, underarm, groin, sweat, urine, feces, bad breath,
and sexual odors. In 59% of the cases, the patient could not smell the smell himself. In 57%, the
belief in the perceived odor was fixed or firmly held, whereas in other cases that belief was held
in less than full conviction (e.g., admitted that the preoccupation was excessive and unreason-
able). Referential ideas in the form of misinterpretation of comments and gestures were com-
mon (74%) and were all related to social references. Furthermore, it is possible that some of the
precipitating events were not real but rather an early symptom of the disorder.
Unlike common views, which regard ORS as typically chronic, persistent, and tending to
worsen over time, the current review (Begum and McKenna 2011) concluded that around
two thirds of the treated cases showed improvement or recovery. Of all forms of treatment,
the best response was seen with psychotherapy (78%), especially behavioral therapy.
ORS shows some common features with other psychiatric disorders (Table 12.1). As a
result, there is an ongoing debate in the literature regarding the classification of ORS either
as a separate disorder or an expansion of another disorder (e.g., malodor aspect of body
dysmorphic disorder).
Back to Halitophobia
Despite the many resembling features stated above, there is one key difference between
body odors and breath odors. Unlike other bodily odors, a person cannot normally smell
his own breath. This physiological fact, on the one hand, and the relatively large prevalence
Back to Halitophobia
Table 12.1 Similar and dissimilar features of organoleptic reference syndrome (ORS) as compared with other disorders (Begum and McKenna 2011)
Disorder Organoleptic reference syndrome (ORS)
Similar Dissimilar
Delusional disorder In most cases, ORS is a delusional belief (complete In some cases, ORS has a non-delusional form (good
conviction of emitting malodor). insight, overvalued ideation).
Social phobia In most cases, ORS patients are concerned about the Social phobia is typically associated with an act
social implication of emitting malodor (experiencing (speaking, eating, writing, etc.) rather than body odors.
shame, embarrassment, and anxiety or avoiding social
situations).
Obsessive compulsive disorder Most cases of ORS show excessive, repetitive compul- Only few cases of OCD are delusional, and ideas of
(OCD) sive behaviors that are aimed at checking or eliminating reference (how the condition is perceived by others) are
the perceived odor. much less common.
Body dysmorphic disorder (BDD) Core belief of a bodily defect that leads to social The core beliefs, repetitive behaviors, and treatment
avoidance. Preoccupation and frequent seeking of responses may differ. Currently, limited to physical
medical (nonmental) treatment to alleviate the perceived defects.
problem.
Hypochondriasis Preoccupation with the body, obsessional thinking, and Hypochondriasis is characterized by a core fear of
repetitive behavior (seeking medical diagnosis and having a serious disease.
treatments).
91
92 12 Psychological Aspects of Breath Odors
of breath odors might explain the high proportion of patients who express an exaggerated
concern of having a breath odor problem (i.e., Halitophobia). In a study on social phobia
conducted in 1997 in Canada on a population of 1,206 subjects [Stein M, unpublished data
from a community survey (Stein et al. 2000)], 15.8% worried “a lot” about how their
breath smelled, 2.8% had seen a professional about their breath, and 2.7% claimed that
their breath concern interfered with their lives (e.g., socially, professionally).
Based on clinical experience and research, halitophobic patients often:
1. Present with a high degree of certainty and conviction that they suffer from bad breath.
The descriptions of which are often exaggerated (e.g., very foul smell that can be sensed
across the room).
2. Possess a lot of information on the subject of bad breath, often nonscientific in nature.
3. Have had frequent consultations with various medical specialists (e.g., dentists, ENT,
gastroenterologists, etc.).
4. Practice a high degree of oral hygiene, often obsessively (although they often claim that
it does not alleviate the odor).
5. Exhibits a high level of grooming and attention to external appearance.
6. Are sometimes secretive concerning their perceived problem, often confiding in no one
over the course of years of distress. They may encounter difficulty in discussing the
situation with anyone, including the professional at the consultation. They sometimes
break down in tears at the initial consultation. They often bridle and express anger,
disbelief, and disappointment when told that their complaint of bad breath has not been
verified by the clinical examination.
7. Are able to somehow carry on with their lives, despite the self-perceived “predic
ament.”
8. Tend to use various evasive methods and avoidance techniques to prevent others from
smelling them (e.g., avoiding close encounters of professional or social origin, chewing
gum incessantly, and standing downwind during a conversation).
9. Appear to be more concerned by the social implications of their perceived affliction,
rather than expressing anxiety that it is a life-threatening medical condition.
Much like ORS patients complaining of other bodily odors, halitophobic patients often
report on a precipitating event that is mostly odor related. These may include:
1. Referral comments and remarks by family or friends (e.g., having been told once in the
past), a sporadic event that made a lifelong impact (associated with shame and
embarrassment).
2. Presence of foul-smelling particles coughed up and expelled from the throat (i.e.,
Tonsilloliths).
3. Having a family member (parent or sibling) with bad breath.
Apart from referral comments and gestures (e.g., rubbing nose, stepping back) that are auto-
matically attributed to breath odors, halitophobic patients also often rely on self-perceived
cues such as bad taste and oral dryness as signs for their perceived breath odor. These subjec-
tive signs are mostly psychosomatic and are the result of the exaggerated concerns and pre-
occupation regarding the perceived breath odor problem, rather than real conditions.
References 93
Some researchers dealing with the subject of the management of Halitophobic patients
have noted that in most cases these patients refuse to accept the fact that their condition is
psychological (Yaegaki and Coil 1999). Furthermore, this lack of acceptance and total
conviction often leads to confrontation between the doctor and the patient. To avoid these
conflicts, it was proposed not to engage in an argument on the objectivity of the complaint,
but rather put the emphasis on educating the patient (e.g., oral hygiene instructions).
However, research has shown that this type of approach is not successful (Iwu and Akpata
1990) since most of these patients practice good oral hygiene and are looking for some-
thing new.
In patients who show less conviction in their belief, a simple explanation or demonstra-
tion (e.g., using Halimeter) may be effective in persuading the patient in the absence of an
objective malodor problem. In severe, more delusional cases, the resistance would be
much higher. Nevertheless, it is the clinician’s responsibility not to “skirt the issue” and to
inform the patient about his suspected condition. This should be done in an empathetic
manner, giving the patient detailed explanation of his condition and recommending psy-
chological consultation when warranted.
References
Begum, M., McKenna, P.J.: Olfactory reference syndrome: a systematic review of the world litera-
ture. Psychol. Med. 41(3), 453–461 (2011). Epub 2010 Jun 9
Iwu, C.O., Akpata, O.: Delusional halitosis. Review of the literature and analysis of 32 cases.
Br. Dent. J. 168(7), 294–296 (1990)
Lochner, C., Stein, D.J.: Olfactory reference syndrome: diagnostic criteria and differential diagno-
sis. J. Postgrad. Med. 49(4), 328–331 (2003)
Pryse-Phillips, W.: An olfactory reference syndrome. Acta Psychiatr. Scand. 47(4), 484–509 (1971)
Periodontol. 36(11), 970–975 (2009)
Rosenberg, M., Leib, E.: Experiences of an Israeli malodor clinic. In: Rosenberg, M. (ed.)
Bad breath research perspectives, pp. 137–148. Ramot Publishing – Tel Aviv University,
Tel Aviv (1997)
Seemann, R., Bizhang, M., Djamchidi, C., Kage, A., Nachnani, S.: The proportion of pseudo-
halitosis patients in a multidisciplinary breath malodour consultation. Int. Dent. J. 56(2),
77–81 (2006)
Stein, M.B., Torgrud, L.J., Walker, J.R.: Social phobia symptoms, subtypes, and severity: findings
from a community survey. Arch. Gen. Psychiatry 57(11), 1046–1052 (2000)
Sutton, R.L.: Bromidrosiphobia. J. Am. Med. Assoc. 72, 1267–1268 (1919)
Suzuki, K., Takei, N., Iwata, Y., Sekine, Y., Toyoda, T., Nakamura, K., Minabe, Y., Kawai, M., Iyo,
M., Mori, N.: Do olfactory reference syndrome and jiko-shu-kyofu (a subtype of taijin-kyofu)
share a common entity? Acta Psychiatr. Scand. 109(2), 150–155 (2004). Discussion 155
Videbech, T.: Chronic olfactory paranoid syndromes. A contribution psychopathology sense smell.
Acta Psychiatr. Scand. 42(2), 183–213 (1966)
Yaegaki, K., Coil, J.M.: Clinical dilemmas posed by patients with psychosomatic halitosis.
Quintessence Int. 30(5), 328–333 (1999)
Yaegaki, K., Coil, J.M.: Examination, classification, and treatment of halitosis; clinical perspectives.
J. Can. Dent. Assoc. 66(5), 257–261 (2000)
Oral Malodor Management
13
The key to a successful resolution of a breath odor complaint is a correct diagnosis of its
source (for more details see Chap. 9). Once the objectivity of the complaint has been substan-
tiated and the source of the malodor located, an appropriate treatment may be implemented.
Breath odors may arise from a variety of sources such as systemic and ENT-related
conditions (described in Chaps. 5–7), which warrant the referral of the patient to the appro-
priate physician/specialist. However, in most cases (over 90%), the source of the problem
is anaerobic bacterial activity within the oral cavity itself (e.g., tongue, gums, teeth, resto-
rations). Therefore, oral caretakers (e.g., dentists, hygienists) should be knowledgeable in
this field and responsible for its treatment.
Successful resolution of an oral malodor problem depends on patient cooperation on two
levels: (1) Since self-assessment of oral malodor is mostly unreliable, the patient must enlist
the assistance of a close friend or family member to monitor his/her condition. This objec-
tive evaluation is important not only for the clinician’s follow up but also imperative for the
patient’s ability to regain his/her confidence in social situations. (2) Similar to other bacte-
rial-related problems of the oral cavity such as caries and periodontal disease, the long-term
successful outcome of oral malodor treatment relies mainly on the patient’s ability to main-
tain good oral hygiene with an emphasis on proper tongue and interdental cleaning.
Mechanical Therapy
Most of the many different species of bacteria residing in the oral cavity are unable to
inhabit any other sites in the human body. Therefore, they are under constant threat of
being washed out or swallowed and their ability to adhere to oral surfaces and form bio-
films is imperative to their survival. These oral biofilms are tissue-like structures consisting
of cellular and extracellular matrix and are highly resistance to rinsing, washing, deter-
gents, and even antibiotics. This is one reason why mechanical cleaning procedures such
as brushing and cleaning of dental and oral surfaces are the cornerstone of oral hygiene.
Because of the fact that the malodor-producing bacteria reside mainly on the tongue
dorsum and interdental spaces, areas which are normally inaccessible to regular tooth-
brushing, it is not surprising that toothbrushing alone has a very weak short-term effect on
oral malodor reduction. The data presented in Table 13.1 shows the effect of various oral
hygiene procedures on malodor-related parameters.

96 13 Oral Malodor Management
Table 13.1 Effect of oral hygiene activities on oral malodor and related parameters
Reference Oral hygiene activities Criteria and Follow up duration and
(No. of malodor outcome
subjects) parameters
Tonzetich and Single activity VSC (H2S, GC) 1 h follow up
Ng (1976) Brushing:
(n = 8) Teeth 29% reduction
Tongue 74% reduction
Tongue and teeth 76% reduction
Eating 83% reduction
Suarez et al. Single activity VSC (H2S, GC) 8 h follow up
(2000) Brushing:
(n = 8) Teeth 25% reduction
Tongue 65% reduction
Rinsing:
3% H2O2 90% reduction
Eating 40% reduction
No treatment 10% reduction
Seemann et al. Single activity tongue VSC (Halimeter) Up to 30 min follow up
(2001a) Cleaning using: >130 ppb
(n = 28) Tongue cleaner included 42% reduction
Tongue scraper 40% reduction
Toothbrush 33% reduction
Pedrazzi et al. Tongue cleaning (three times VSC (hand held Follow up time not stated
(2004) a day for 1 week): sulfide monitor)
(n = 10) Tongue scraper 75% reduction
Toothbrush 40% reduction
Faveri et al. Three times a day for 1 week Odor judge 8 h follow up
(2006) (following professional scores (single
(n = 19) cleaning): judge) 0–3 scale
Tooth brushing (TB) 90% increase (1.1–2.0)
TB + Flossing (Fl) 85% increase (1.1–1.9)
TB + Tongue scraping (TS) 20% increase (1.1–1.3)
TB + Fl + TS 24% increase (0.9–1.1)
Farrell et al. Four times in 24h VSC (Halimeter) 3 h follow up
(2006) Tooth brushing (NaF) 159 ppb
(n = 26) Tooth brushing (triclosan) 143 ppb
Tooth + tongue brushing 126 ppb (significantly
(triclosan) better than tooth brushing
alone, p = 0.035)
The data presented in this table suggest that tongue cleaning is the most effective oral
hygiene activity in reducing oral malodor and related parameters. Furthermore, it is evi-
dent that not all tongue cleaning methods are equally effective. For instance, cleaning the
tongue using a toothbrush appeared to be less effective than using a tongue cleaner designed
specifically for this purpose (Pedrazzi et al. 2004; Seemann et al. 2001a). The effect of
eating, especially abrasive foods, on malodor reduction was also attributed in part to its
tongue cleaning properties (Suarez et al. 2000) (Fig. 13.1).
Chemical Therapy 97
Fig. 13.1 Tongue cleaning
Chemical Therapy
Although tongue cleaning seems to be very effective in reducing malodor and malodor-
related parameters (e.g., VSC), its effectiveness is relatively short term (under 2 h). Research
done by Quirynen and colleges (Quirynen et al. 2004) showed that although tongue clean-
ing did reduce tongue coating, it did not reduce the bacterial load on the tongue. In other
words, the mechanical cleaning of the tongue appears to affect their food supply (substrate)
rather than the bacteria themselves. Therefore, antimicrobial agents must be incorporated
into the treatment protocol in order to achieve long-term efficacy of the treatment.
Various chemical agents such as chlorhexidine, cetylpyridinium chloride, essential oils, tri-
closan, chlorine dioxide, hydrogen peroxide and zinc, have been shown to be, individually or
combined, effective in reducing oral malodor (Tables 13.2 and 13.3). The proposed mechanism
of action for these agents is mostly antibacterial or antiseptic; however, some of them are able
to chemically bind or alter malodor components (e.g., binding of sulfide ions by zinc), thus
rendering them non-malodorous. Therefore, combining different agents with different mecha-
nisms of action (e.g., antibacterial and sulfide binding) may result in a superior outcome.
These antibacterial agents have been incorporated into various delivery systems
(e.g., mouthrinse, dentifrices, lozenges) produced to treat oral malodor. However, since
oral malodor is generally considered a cosmetic issue for regulatory purposes, there are
many products available in the market that claim to alleviate oral malodor, yet have rela-
tively little data to substantiating these claims. In 2003, the American Dental Association
(ADA) Council on Scientific Affairs published guidelines for products used in the man-
agement of oral malodor regarding the safety and effectiveness of these products (Wozniak
2005). According to the ADA, safety issues include long-term follow up (6 months) for
Table 13.2 Effect of mouthrinses containing various active ingredients on oral malodor and related
parameters
Reference Delivery system, Criteria and malodor Follow up duration
(No. of application and parameters and outcome
subjects) active ingredients
Rosenberg Mouthrinse (twice Odor judge scores (single 8–10 h follow-up
et al. (1992) for 1 day) judge)
(n = 60) TPM/CPC 0–5 scale 33% reduction (1.5–1)
0.2% CHX 76% reduction (1.7–0.4)
Kozlovsky Mouthrinse (twice a Odor judge scores (two ³8 h follow-up
et al. (1996) day for 6 weeks) judges)
(n = 50) TPM/CPC 0–5 scale 80% reduction (2.1–0.4)
EO 70% reduction (2.4–0.7)
Yaegaki and Mouthrinse (single VSC (Halimeter) 3.5 h follow-up
Sanada (1992) use) Subjects with ³75 ppb
(n = 9) included
TPM/CPC 80% reduction
Control mouthrinse 30% reduction
Bosy et al. Mouthrinse (twice a Odor judge scores (two Follow up time not
(1994) day for 1 week) judges) reported
(n = 101) 0.2% CHX 0–5 scale 64% reduction (2.8–1)
Subjects with ³2 included
Frascella et al. Mouthrinse (single Odor judge scores (three 8 h follow-up
(2000) use) judges)
(n = 31) 0.1% CD 0–4 intensity scale (−3 to 50% reduction (1.2–0.6)
+3 pleasantness scale)
Control (water) Subjects with £−1 9% reduction (1.4–1.3)
included
Borden et al. Mouthrinse (twice a Odor judge scores (two 4 h follow-up
(2002) day for 4 weeks) judges)
(n = 95) EO 0–5 scale 11% reduction (4.1–3.7)
CPC Subjects with >2 included 23% reduction (4.2–3.2)
Placebo No reduction (3.9–3.9)
CD/Zn 11% reduction (4–3.6)
Schmidt and Mouthrinse (single Odor judge scores (three 3 h follow-up
Tarbet (1978) use) judges)
(n = 62) ZnCl 0–3 scale 37% reduction (1.6–1)
Control (saline) Subjects with ³1 included 14% increase (1.5–1.7)
No treatment 15% increase (1.6–1.9)
De Boever and Mouthrinse (twice a Odor judge scores (single Follow up time not
Loesche (1995) day for 1 week) judge) reported
(n = 16) 0.12% CHX 0–4 scale 69% reduction (2.9–0.9)
Winkel et al. Mouthrinse (twice a Odor judge scores (single Follow up time not
(2003) day for 2 weeks) judge) reported (morning)
(n = 40) CHX/CPC/ZnLc 0–5 scale 46% reduction (2.8–1.5)
(0.05, 0.05, 0.14%) Subjects with >1 included
Placebo 7% reduction (2.7–2.5)
Chemical Therapy 99
Wigger-Alberti Mouthrinse (twice a Odor judge scores (seven Follow up time not
et al. (2010) day for 3 weeks) judges) reported (morning)
(n = 174) AmF-SnF/ZnLc 0–5 scale 22% reduction (3.2–2.5)
(0.025, 0.2, 0.12%)
CHX/CPC/ZnLc Subjects with >2 included 26% reduction (3.1–2.3)
(0.05, 0.05, 0.14%)
0.12% CHX 27% reduction (3.3–2.4)
Control (water) 6% reduction (3.2–3)
van Mouthrinse (twice a Odor judge scores (single 20–30 min Follow up
Steenberghe day for 12 days) judge)
et al. (2001) 0.2% CHX 0–4 scale 78% reduction (1.8–0.4)
(n = 12) CHX/NaF 89% reduction (1.8–0.2)
(0.12, 0.05%)
CHX/CPC/ZnLc 100% reduction (1.8–0)
(0.05, 0.05, 0.14%)
Shinada et al. Mouthrinse (twice a Odor judge scores (two Over night (average 8 h)
(2010) day for 7 days) judges) follow up
(n = 15) 0.1% CD 0–5 scale 32% reduction (2.1–1.4)
Rassamee- Mouthrinse VSC (Halimeter) 3 h follow up
masmaung (single use) Subjects with ³80 ppb
et al. (2007) included
(n = 60) Herbal 38% reduction
Placebo 23% reduction
(twice a day for Follow up time not
2 weeks) reported (morning)
Herbal 60% reduction
Quirynen et al. Mouthrinse (twice a Odor judge scores (single 20–30 min Follow up
(2002) day for 7 days) judge)
(n = 16) 0.2% CHX 0–4 scale 88% reduction (1.6–0.2)
CHX/CPC/ZnLc
(0.05, 0.05, 0.14%) 81% reduction (1.6–0.3)
AmF-SnF 72% reduction (1.8–0.5)
Pitts et al. 1981 Mouthrinse (single Odor judge scores (five 2 h follow up
(n = 17) use) judges)
EO 1–9 pleasantness scale 9% reduction (6.7–6.1)
Control (water) 3% increase (6.1–6.3)
Pitts et al. Mouthrinse (single Odor judge scores (five 3 h follow up
(1983) use) judges)
(n = 30) EO 1–9 pleasantness scale 6% reduction (6.7–6.3)
Placebo 2% increase (6.6–6.7)
Control (water) No reduction (6.7–6.7)
(continued)
Peruzzo et al. Mouthrinse (3 times VSC (Halimeter) 12 h follow up (morning
(2007) a day for 4 days) breath)
(n = 14) 0.1% CD 12% reduction
Placebo 112% increase
Carvalho et al. Mouthrinse (twice a VSC (Halimeter) 12 h follow up (morning
(2004) day for 4 days) breath)
(n = 12) 0.2% CHX 70% reduction
0.12% CHX 63% reduction
0.03% Triclosan 29% reduction
EO 24% reduction
0.05% CPC 14% reduction
Control (hydro-alc) 21% increase
TPM two phase (oil:water) mouthrinse, CPC cetylpyridinum chloride, CHX chlorhexidine,
EO essential oils, CD chlorine dioxide, Zn zinc, ZnCl zinc chloride, ZnLc zinc lactate, NaF sodium
fluoride, AmF amine fluoride, SnF stannous fluoride
Table 13.3 Effect of dentifrices and other delivery systems containing various active ingredients on
oral malodor and related parameters
Reference Delivery system, Criteria and Follow up duration
(No. of application and malodor and outcome
subjects) active ingredients parameters
Newby et al. (2008) Dentifrice (single VSC (GC) 1 h follow up
(n = 16) application)
0.3% ZnCl (A) H2S > 300 ppb 44% reduction
0.3% ZnCl (B) included 48% reduction
0.3% Triclosan 26% reduction
Olshan et al. (2000) Dentifrice (single Odor judge scores 1.2 h follow up
application) (five judges)
23.5% red (7.3–5.6–7.0)
EO 1–9 pleasantness
scale. Subjects with
³6 included
Study 1 Control (NaFl) 7.1% red (7.3–6.8–7.2)
(n = 80)
EO/1% ZnCt 21.3% red (6.5–5.1–6.3)
Study 2 Control (NaFl) 7.1% red (6.6–6.1–6.5)
(n = 90)
Sharma et al. (1999) Dentifrice (single Odor judge scores 12 h follow up
(n = 63) application) (four judges)
0.3% Triclosan 1–9 pleasantness 28% reduction (6.6–4.8)
unpleasant breath
included
Control (NaFl) 9% reduction (6.6–6.0)
Chemical Therapy 101
Reference Delivery system, Criteria and Follow up duration
(No. of application and malodor and outcome
subjects) active ingredients parameters
Waler (1997) Chewing gum (single VSC (Halimeter) Immediately following
(n = 11) application) treatment
2 mg ZnAc 45% reduction
0.5 mg ZnAc 16% reduction
Aqueous solution
(single application)
0.02% ZnCl 45% reduction
Control (water) 7% reduction
Young et al. (2002) Lozenges (single VSC (GC) Cystein 3 h follow up
(n = 10) application) challenge
ZnGl 75% reduction
ZnAc 70% reduction
ZnCt No reduction
ZnAm 70% reduction
Greenstein et al. Lozenges (three Odor judge scores 2–3 h follow up
(1997) applications in 24h) (two judges)
(n = 123) Oxidizing agent 0–5 scale 50% reduction (1.6–0.8)
Breath mint 20% reduction (1.6–1.3)
Chewing gum 17% reduction (1.6–1.3)
Control 35% reduction (1.6–1.0)
Sterer et al. (2008) MAT (single Odor judge scores 2 h follow up
(n = 26) application) (two judges)
Herbal 0–5 scale 57% reduction (3.4–1.5)
Placebo No reduction (3.1–3.4)
Hu et al. (2005) Dentifrice (twice a Odor judge scores 12 h Follow up (morning
(n = 81) day for 3 weeks) (four judges) breath)
0.3% Triclosan 1–9 pleasantness 56% reduction (7.8–3.4)
unpleasant breath
included
Control (NaFl) 9% reduction (7.8–7.1)
Niles et al. (2005) Dentifrice (twice a VSC (GC) Over night follow up
(n = 17) day for 1 week) (morning breath)
0.3% Triclosan >300 ppb included 57% reduction
Control (NaFl) 10% reduction
CHX chlorhexidine, EO essential oils, MAT mucoadhesive tablet, ZnAc zinc acetate, ZnGl zinc
gluconate, ZnAm zinc amino chelated, ZnCl zinc chloride, ZnCT zinc citrate, NaF sodium
fluoride
adverse effects on soft and hard oral tissues, allergic and toxic effects, and the development
of opportunistic and pathogenic organisms. Effectiveness should be established through
well-designed blinded and controlled clinical studies on subjects with oral malodor (odor
judge score ³2, on a 0–5 scale), and the outcome measured by trained and calibrated odor
judges (at least two judges).
The most common delivery system for active chemical agents in the treatment of oral
malodor is mouthrinse. Table 13.2 shows the results of various clinical trials testing differ-
ent active ingredient in a mouthrinse formulation on oral malodor and related parameters.
These results show the efficacy of the different active ingredients over varying periods of
time ranging from few hours to day-long effects of 10–12 h. It is clear that not all the active
ingredients demonstrate the same efficacy in reducing malodor levels. Chlorhexidine (0.2%),
which seems to be highly effective is reported to cause many unpleasant side effects (Bosy
et al. 1994). Following use of a 0.2% chlorhexidine mouthrinse twice a day for a week, 90
out of 101 subjects who participated in the study reported some side effect, which included
change in the taste of food (60%), burning sensation on the tip of the tongue (26%), staining
of the tongue (17%) and teeth (12%), and pain or sloughing of gingival tissue (4%).
The use of an effective mouthrinse (i.e., gargling) has an important part in oral malodor
management. Gargling at least once a day should be done on a regular basis in order to
control bacterial growth on the tongue dorsum. However, whether or not regular use of an
effective mouthrinse has a cumulative effect is an open question. While some studies show
that a repeated use yields better results than a single application (Kozlovsky et al. 1996;
Rassamee-masmaung et al. 2007), others indicate that the effectiveness of the mouthrinse
does not improve with a prolonged use (Borden et al. 2002). In other words, this mode of
treatment should be applied regularly and constantly.
Some evidence may suggest that the regular use of an alcohol-containing mouthrinse is
related to the occurrence of oral and pharyngeal cancer (Winn et al. 1991). This is mainly
attributed to the conversion of alcohol to acetaldehyde by some of the microorganisms in
the oral cavity (Shuster et al. 2004). However, since alcohol is not considered an active
ingredient and there are many effective mouthrinses available that do not contain alcohol,
it would be safer to recommend the use of an alcohol-free mouthrinse.
Other delivery systems for antimicrobial agents such as dentifrices (tooth paste), loz-
enges, chewing gums, and mucoadhesive tablets have also been reported as an effective
means to reduce oral malodor (Table 13.3).
Of course, most oral hygiene protocols include the use of toothpaste. At this point, it is
important to stress that the detergent in the toothpaste (e.g., sodium lauryl sulfate) is a
strong anionic agent that may bind cationic chemical agents (e.g., chlorhexidine, cetylpyridi-
num chloride) and hinder or inhibit their antibacterial activities. Therefore, it is advisable
to keep toothbrushing with toothpaste and gargling with mouthrinse as separate activities.
Professional Treatment
Some attempts have been made to suggest a treatment-need-based classification

for oral malodor (Yaegaki and Coil 2000). According to this classification, tongue-
related malodor is considered as “physiologic halitosis,” thus requiring primarily home
Professional Treatment 103
care treatments (e.g., improved oral hygiene including regular tongue cleaning com-
bined with mouthrinsing). Conversely, other causes such as periodontal disease and
faulty restorations, which require professional treatment, are termed “pathologic hali-
tosis.” However, other clinicians (Richter 1996) have suggested that tongue-related
malodor is in itself a pathologic condition (i.e., anaerobic bacterial glossitis) that war-
rants, in some cases, professional tongue debridment.
The relationship between periodontal disease and oral malodor is not straightforward
(Chap. 2). It is likely that both are exacerbated by gingival inflammation brought about by
interdental plaque accumulation. Thus, it is not surprising that periodontal treatment,
supragingival prophylaxis, and professional teeth cleaning can reduce malodor. Table 13.4
shows a number of studies that looked into the effect of these treatments on oral malodor.
The results of these studies clearly demonstrate the importance of professional treat-
ment in oral malodor management. This is especially true for patients who are unable to
Table 13.4 Effect of professional oral care activities on oral malodor and related parameters
Reference Professional oral care Criteria and malodor Follow up
(No. of activities parameters duration and
subjects) outcome
Adachi Weekly treatments (scaling VSC (CH3SH, hand 18 months follow up
et al.(2002) and cleaning of teeth, held sulfide monitor)
(n = 67) interdental spaces, dentures Significant
and tongue): difference between
POHC groups (p < 0.05)
Control (regular OH) 20 ppb
55 ppb
Seemann et al. Scaling and polishing VSC (Halimeter) 1 week follow up
(2001b) compared with tooth Significant
(n = 65) brushing and flossing (no difference between
tongue cleaning) groups (p < 0.05)
PTC 80 ppb
TB + Fl 110 ppb
Seemann et al. PTC (Scaling and polish- VSC (Halimeter) 1 month follow up:
(2004) ing), OH (TB and Fl only) 28% reduction
(n = 40) No treatment (control) No reduction
Quirynen et al. Test group: Odor judge scores 2 months follow up:
(1998) OSFMD (scaling – root (single judge
(n = 24) planing, subgingival 0–3 scale
irrigation and tongue Periodontal patients
brushing with 1% CHX gel). included
Twice a day:
OH (TB + IDB + TC)
Mouthrinse
82% reduction
(0.2% CHX)
(2.2–0.4)
Control:
SPT (scaling–root planing)
68% reduction
OH (TB + IDB + TC)
(1.9–0.6)
(continued)
Reference Professional oral care Criteria and malodor Follow up
(No. of activities parameters duration and
subjects) outcome
Quirynen et al. Combined therapy: VSC (Halimeter) 6 months follow up
(2005) OSFMD Periodontal patients
(n = 45) Twice a day: included
OH (TB + IDB + TC)
Mouthrinse:
0.05% CHX, CPC 67% reduction
Tsai et al. Sequential treatments Odor judge scores Immediately
(2008) Following baseline: (single judge, 0–5 following treatment:
(n = 25) Tongue scraping (TS) scale) 21% reduction
Periodontal patients, (3.8–3.0)
2 weeks after TS: malodor scores of ³2
NSPT (scaling–root included 1 month follow up:
planning, faulty restorations 36% reduction
removal) (3.8–2.44)
OH (twice a day)
1 month after NSPT
Twice a day:
OH (TB + IDB + TC) 1 month follow up:
Mouthrinse 67% reduction
(0.12% CHX, CPC) (3.8–1.24)
Roldan et al. Supragingival prophylaxis Odor judge scores 3 months follow up:
(2005) Twice a day: (single judge, 0–5 50% reduction
(n = 17) OH (TB + Fl + TC) scale) (2.7–1.4)
Mouthrinse Malodor scores of ³1
(0.05% CHX, CPC, ZnLc) included
Kara et al. Scaling Odor judge scores » 3 weeks follow up:
(2006) OH (tooth and tongue (single judge, 0–5 85% reduction
(n = 150) brushing twice a day) scale) (3.7–0.5)
Children (7–12 years
old)
Malodor scores of ³2
included
POHC professional oral health care, OH oral hygiene, PTC professional tooth cleaning, TB tooth
brushing, Fl flossing, TC tongue cleaning, OSFMD one stage full mouth disinfection, SPT stan-
dard periodontal therapy, NSPT non surgical periodontal therapy, CPC cetylpyridinum chloride,
CHX chlorhexidine, ZnLc zinc lactate
maintain good oral hygiene like the handicapped, elderly, and small children (Adachi et al.
2002; Kara et al. 2006). Professional treatment seems to be particularly beneficial in peri-
odontal patients (Quirynen et al. 2005; Tsai et al. 2008). Interestingly, one-stage full-mouth
disinfection yields better results in reducing oral malodor than the standard periodontal
therapy (Quirynen et al. 1998). In addition to the standard scaling and root planing (within
24 h), this procedure also includes the use of a disinfecting agent (1% CHX gel) for
References 105
application within the periodontal pockets and for brushing the tongue. Although it is
unclear which of these actions has the most effect on reducing malodor, in periodontal
patients and/or those with excessive tongue coating, tongue debridement should be
included when performing professional treatment.
References
Adachi, M., Ishihara, K., Abe, S., Okuda, K., Ishikawa, T.: Effect of professional oral health care
on the elderly living in nursing homes. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod.
94(2), 191–195 (2002)
Borden, L.C., Chaves, E.S., Bowman, J.P., Fath, B.M., Hollar, G.L.: The effect of four mouthrinses on
oral malodor. Compend. Contin. Educ. Dent. 23(6), 531–536 (2002). 538, 540 passim; quiz 548
Bosy, A., Kulkarni, G.V., Rosenberg, M., McCulloch, C.A.: Relationship of oral malodor to periodon-
titis: evidence of independence in discrete subpopulations. J. Periodontol. 65(1), 37–46 (1994)
Carvalho, M.D., Tabchoury, C.M., Cury, J.A., Toledo, S., Nogueira-Filho, G.R.: Impact of mouthrinses
on morning bad breath in healthy subjects. J. Clin. Periodontol. 31(2), 85–90 (2004)
De Boever, E.H., Loesche, W.J.: Assessing the contribution of anaerobic microflora of the tongue
to oral malodor. J. Am. Dent. Assoc. 126(10), 1384–1393 (1995)
Farrell, S., Baker, R.A., Somogyi-Mann, M., Witt, J.J., Gerlach, R.W.: Oral malodor reduction by
a combination of chemotherapeutical and mechanical treatments. Clin. Oral Investig. 10(2),
157–163 (2006)
Faveri, M., Hayacibara, M.F., Pupio, G.C., Cury, J.A., Tsuzuki, C.O., Hayacibara, R.M.: A cross-
over study on the effect of various therapeutic approaches to morning breath odour. J. Clin.
Periodontol. 33(8), 555–560 (2006)
Frascella, J., Gilbert, R.D., Fernandez, P., Hendler, J.: Efficacy of a chlorine dioxide-containing
mouthrinse in oral malodor. Compend. Contin. Educ. Dent. 21(3), 241–244 (2000)
Hu, D., Zhang, Y.P., Petrone, M., Volpe, A.R., Devizio, W., Giniger, M.: Clinical effectiveness of
a triclosan/copolymer/sodium fluoride dentifrice in controlling oral malodor: a 3-week clinical
trial. Oral Dis. 11(Suppl 1), 51–53 (2005)
Kara, C., Tezel, A., Orbak, R.: Effect of oral hygiene instruction and scaling on oral malodour in
a population of Turkish children with gingival inflammation. Int. J. Paediatr. Dent. 16(6),
399–404 (2006)
Kozlovsky, A., Goldberg, S., Natour, I., Rogatky-Gat, A., Gelernter, I., Rosenberg, M.: Efficacy of
a 2-phase oil: water mouthrinse in controlling oral malodor, gingivitis, and plaque. J. Periodontol.
67(6), 577–582 (1996)
Newby, E.E., Hickling, J.M., Hughes, F.J., Proskin, H.M., Bosma, M.: Control of oral malodour by
dentifrices measured by gas chromatography. Arch. Oral Biol. 53(Suppl 1), S19–S25 (2008)
Niles, H.P., Hunter, C., Vazquez, J., Williams, M.I., Cummins, D.: The clinical comparison of a
triclosan/copolymer/fluoride dentifrice vs a breath-freshening dentifrice in reducing breath
odor overnight: a crossover study. Oral Dis. 11(Suppl 1), 54–56 (2005)
Olshan, A.M., Kohut, B.E., Vincent, J.W., Borden, L.C., Delgado, N., Qaqish, J., Sharma, N.C.,
McGuire, J.A.: Clinical effectiveness of essential oil-containing dentifrices in controlling oral
malodor. Am. J. Dent. 13, 18C–22C (2000). Spec No
Pedrazzi, V., Sato, S., de Mattos, M.G., Lara, E.H., Panzeri, H.: Tongue-cleaning methods: a
comparative clinical trial employing a toothbrush and a tongue scraper. J. Periodontol. 75(7),
1009–1012 (2004)
Peruzzo, D.C., Jandiroba, P.F., Nogueira Filho Gda, R.: Use of 0.1% chlorine dioxide to inhibit the
formation of morning volatile sulphur compounds (VSC). Braz. Oral Res. 21(1), 70–74 (2007)
Pitts, G., Pianotti, R., Feary, T.W., McGuiness, J., Masurat, T.: The in vivo effects of an antiseptic
mouthwash on odor-producing microorganisms. J. Dent. Res. 60(11), 1891–1896 (1981)
Pitts, G., Brogdon, C., Hu, L., Masurat, T., Pianotti, R., Schumann, P.: Mechanism of action of an
antiseptic, anti-odor mouthwash. J. Dent. Res. 62(6), 738–742 (1983)
Quirynen, M., Mongardini, C., van Steenberghe, D.: The effect of a 1-stage full-mouth disinfection
on oral malodor and microbial colonization of the tongue in periodontitis. A pilot study.
J. Periodontol. 69(3), 374–382 (1998)
Quirynen, M., Avontroodt, P., Soers, C., Zhao, H., Pauwels, M., Coucke, W., van Steenberghe, D.:
The efficacy of amine fluoride/stannous fluoride in the suppression of morning breath odour.
J. Clin. Periodontol. 29(10), 944–954 (2002)
Quirynen, M., Avontroodt, P., Soers, C., Zhao, H., Pauwels, M., van Steenberghe, D.: Impact of
tongue cleansers on microbial load and taste. J. Clin. Periodontol. 31(7), 506–510 (2004)
Quirynen, M., Zhao, H., Soers, C., Dekeyser, C., Pauwels, M., Coucke, W., Steenberghe, D.: The
impact of periodontal therapy and the adjunctive effect of antiseptics on breath odor-related
outcome variables: a double-blind randomized study. J. Periodontol. 76(5), 705–712 (2005)
Rassamee-masmaung, S., Sirikulsathean, A., Amornchat, C., Hirunrat, K., Rojanapanthu, P.,
Gritsanapan, W.: Effects of herbal mouthwash containing the pericarp extract of Garcinia man-
gostana L on halitosis, plaque and papillary bleeding index. J. Int. Acad. Periodontol. 9(1),
19–25 (2007)
Richter, J.L.: Diagnosis and treatment of halitosis. Compend. Contin. Educ. Dent. 17(4), 370–372
(1996). 374–6 passim; quiz 388
Roldan, S., Herrera, D., O’Connor, A., Gonzalez, I., Sanz, M.: A combined therapeutic approach
to manage oral halitosis: a 3-month prospective case series. J. Periodontol. 76(6), 1025–1033
(2005)
Rosenberg, M., Gelernter, I., Barki, M., Bar-Ness, R.: Day-long reduction of oral malodor by a
two-phase oil:water mouthrinse as compared to chlorhexidine and placebo rinses. J. Periodontol.
63(1), 39–43 (1992)
Schmidt, N.F., Tarbet, W.J.: The effect of oral rinses on organoleptic mouth odor ratings and levels
of volatile sulfur compounds. Oral Surg. Oral Med. Oral Pathol. 45(6), 876–883 (1978)
Seemann, R., Kison, A., Bizhang, M., Zimmer, S.: Effectiveness of mechanical tongue cleaning on oral
levels of volatile sulfur compounds. J. Am. Dent. Assoc. 132(9), 1263–1267 (2001a). quiz 1318
Seemann, R., Passek, G., Zimmer, S., Roulet, J.F.: The effect of an oral hygiene program on oral
levels of volatile sulfur compounds (VSC). J. Clin. Dent. 12(4), 104–107 (2001b)
Seemann, R., Passek, G., Bizhang, M., Zimmer, S.: Reduction of oral levels of volatile sulfur
compounds (VSC) by professional toothcleaning and oral hygiene instruction in non-halitosis
patients. Oral Health Prev. Dent. 2(4), 397–401 (2004)
Sharma, N.C., Galustians, H.J., Qaquish, J., Galustians, A., Rustogi, K.N., Petrone, M.E., Chaknis, P.,
Garcia, L., Volpe, A.R., Proskin, H.M.: The clinical effectiveness of a dentifrice containing triclo-
san and a copolymer for controlling breath odor measured organoleptically twelve hours after
toothbrushing. J. Clin. Dent. 10(4), 131–134 (1999)
Shinada, K., Ueno, M., Konishi, C., Takehara, S., Yokoyama, S., Zaitsu, T., Ohnuki, M., Wright,
F.A., Kawaguchi, Y.: Effects of a mouthwash with chlorine dioxide on oral malodor and sali-
vary bacteria: a randomized placebo-controlled 7-day trial. Trials 11, 14 (2010)
Shuster, A., Osherov, N., Rosenberg, M.: Alcohol-mediated haemolysis in yeast. Yeast 21(16),
1335–1342 (2004)
Sterer, N., Nuas, S., Mizrahi, B., Goldenberg, C., Weiss, E.I., Domb, A., Davidi, M.P.: Oral mal-
odor reduction by a palatal mucoadhesive tablet containing herbal formulation. J. Dent. 36(7),
535–539 (2008)
References 107
Suarez, F.L., Furne, J.K., Springfield, J., Levitt, M.D.: Morning breath odor: influence of treat-
ments on sulfur gases. J. Dent. Res. 79(10), 1773–1777 (2000)
Tonzetich, J., Ng, S.K.: Reduction of malodor by oral cleansing procedures. Oral Surg. Oral Med.
Oral Pathol. 42(2), 172–181 (1976)
Tsai, C.C., Chou, H.H., Wu, T.L., Yang, Y.H., Ho, K.Y., Wu, Y.M., Ho, Y.P.: The levels of volatile
sulfur compounds in mouth air from patients with chronic periodontitis. J. Periodontal Res.
43(2), 186–193 (2008)
van Steenberghe, D., Avontroodt, P., Peeters, W., Pauwels, M., Coucke, W., Lijnen, A., Quirynen,
M.: Effect of different mouthrinses on morning breath. J. Periodontol. 72(9), 1183–1191
(2001)
Waler, S.M.: The effect of zinc-containing chewing gum on volatile sulfur-containing compounds
in the oral cavity. Acta Odontol. Scand. 55(3), 198–200 (1997)
Wigger-Alberti W, Gysen K, Axmann EM, Wilhelm KP: Efficacy of a new mouthrinse formula-
tion on the reduction of oral malodour in vivo A randomized, double-blind, placebo-controlled,
3 week clinical study. J. Breath Res. 4 (2010). doi:10.1088/1752-7155/4/1/017102
Winkel, E.G., Roldan, S., Van Winkelhoff, A.J., Herrera, D., Sanz, M.: Clinical effects of a new
mouthrinse containing chlorhexidine, cetylpyridinium chloride and zinc-lactate on oral halito-
sis. A dual-center, double-blind placebo-controlled study. J. Clin. Periodontol. 30(4), 300–306
(2003)
Winn, D.M., Blot, W.J., McLaughlin, J.K., Austin, D.F., Greenberg, R.S., Preston-Martin, S.,
Schoenberg, J.B., Fraumeni Jr., J.F.: Mouthwash use and oral conditions in the risk of oral and
pharyngeal cancer. Cancer Res. 51(11), 3044–3047 (1991)
Wozniak, W.T.: The ADA guidelines on oral malodor products. Oral Dis. 11(Suppl 1), 7–9
(2005)
Yaegaki, K., Coil, J.M.: Examination, classification, and treatment of halitosis; clinical perspec-
tives. J. Can. Dent. Assoc. 66(5), 257–261 (2000)
Yaegaki, K., Sanada, K.: Effects of a two-phase oil-water mouthwash on halitosis. Clin. Prev.
Dent. 14(1), 5–9 (1992)
Young, A., Jonski, G., Rolla, G.: The oral anti-volatile sulphur compound effects of zinc salts and
their stability constants. Eur. J. Oral Sci. 110(1), 31–34 (2002)
History of Breath Odors
14
Culture and Folklore
Breath odors are an age-old, worldwide problem, and over the centuries different cultures
have developed different folk remedies. In Thailand, sufferers chew the peels of oversize
guavas. Iraqis keep cloves between their teeth. Italians chew parsley. Indians chew fennel
seeds. Brazilians cite cinnamon as a folk remedy. Indeed, many plant extracts contain
antibacterial molecules. These molecules are often oily and aromatic, and can be extracted
as part of the “essential oil” fraction. Essential oils are used in mouthrinses, toothpastes,
and chewing gums, sometimes for their antibacterial effect, and sometimes for their aroma.
Essential oil compounds that inhibit oral microorganisms include eugenol from clove, thy-
mol from thyme, and eucalyptol from eucalyptus. Chinese imbibe crushed eggshells in rice
wine, but will also eat a grapefruit for alcohol breath, and for garlic odor, persimmon or red
dates. In Singapore, traditional Chinese pharmacy offers a concoction of bark, leaves, and
other dried items for relief from too much “heatiness” (yang), which they believe is a
major cause of bad breath. Finally, almost all of us believe in the mouth-freshening poten-
tial of mint (although actually, most types of mint are not very effective).
Bad breath is discussed at length in the Jewish Talmud, as well as by Egyptian, Greek,
and Roman writers. The most ancient recorded remedy for bad breath may date back to
Chap. 37, the book of Genesis. Joseph, having been thrown into a pit by his spiteful broth-
ers, is taken to Egypt by a caravan of Ishmaelites. The Bible tells us that the camels bore
spices, balm, and ladanum. Because of later writings in the Talmud, we can deduce that
ladanum might refer to gum mastic, the resin of the Pistacia lentiscus, a small tree that
flourishes in the Mediterranean basin. It was produced since Biblical times by making inci-
sions in the bark of the tree during summer months and collecting the resin drops. Gum
mastic has been chewed around the Mediterranean for thousands of years, and is still
farmed on the Greek island of Chios, off the shore of Turkey. Quite remarkably, this gum
has antibacterial properties, and has been used for various medicinal and dental purposes
over the centuries (Fig. 14.1).
Bad breath remedies have been prevalent since the earliest recorded times. The Ebers
papyrus, over 3,500 years old (University of Leipzig library), describes aromatic concoc-
tions proposed to counter dental ailments, including swollen gums. Some 2,000 years ago,
the Roman perfume entrepreneur Cosmo supposedly sold breath-freshening pastilles to his
fellow friends and countrymen. His competitors questioned their efficacy.

110 History of Breath Odors
Fig. 14.1 Mastic gum; resin

pieces from the Pestacia
lentiscus tree
Ancient Judaism regarded bad breath as a severe infliction, akin to having lost a limb,
or suffering from leprosy. According to the Talmud (dating back over 1,500 years), priests
were not allowed to carry out holy duties in the Temple if they had bad breath (Shifman
et al. 2002). According to Jewish law, a man who marries a woman and subsequently dis-
covers that she has bad breath can summarily divorce her without even fulfilling the terms
of the marriage contract (ketuba). This differs from medieval Welsh law, in which a wife
was able to divorce her husband on the grounds of oral malodor (Paul Meara, University
of Wales Swansea, personal communication).
According to the Jewish Talmud, working with flax predisposes to bad breath. In ancient
times, flax fibers were wet by saliva in order to spin them into a finer yarn. According to
the Talmud, this activity damages the woman’s lips and causes bad breath, and therefore a
husband may not compel his wife to spin flax (Nahum Ben Yehuda, Bar Ilan University,
personal communication).
Specific vegetables are mentioned in the Talmud as bad breath risks, particularly raw
peas and extensive consumption of lentils. The Talmud suggests a variety of aromatic
spices, including ginger and cinnamon, as oral fresheners. Another recommended remedy
is the mastic chewing gum described above. The Talmud states that while frivolous chew-
ing of mastic is forbidden on the Sabbath, it is allowed as a cure for bad breath.
Islam also deals at length with bad breath and oral hygiene. There is the famous story
that the prophet Muhammad once asked someone to leave the mosque because of his bad
breath. Islam stresses the importance of hygiene, and good smells. A case in point is the
siwak (sometimes spelled sewak, or miswak), a short stick that is regarded by Moslems as
a holy instrument. By wetting and chewing or pounding on one of the ends, a kind of
toothbrush is formed, which can be used to clean both teeth and soft tissue. Siwaks are
made from the aerial roots of certain trees and may contain antibacterial agents. Modern
mint-flavored siwaks are also available (Fig. 14.2).
Early Scientific and Medical Literature 111
Fig. 14.2 Siwak; a stick used

by Muslims to clean the
mouth
Bad breath is usually considered taboo in Islam, as it is in Judaism. One exception is

bad breath due to fasting during the Ramadan, which according to Islamic teaching is
considered by Allah to be more esteemed than the smell of roses.
Early Scientific and Medical Literature
In the late eighteenth century, Dr. Joseph W. Howe wrote a medical text on bad breath,
which was published in four editions from 1874 to 1898 (“The Breath and the Diseases
which give it a fetid odor with directions for treatment”; D. Appleton and company,
1898). Dr. Howe was, inter alia, Professor of Clinical Surgery at Bellevue Hospital
Medical College.
According to Dr. Howe, bad breath is liable to occur at all periods of life, and is more
common among menfolk. “Yet how few of the afflicted persons detect the cause of their
isolation, or recognize the barrier which effectually prevents the approach of those near
and dear to them!” He wrote of the difficulty in telling someone that they suffer from bad
breath. “With the best intentions in the world, we rarely whisper a word of their disorder
or suggest a source of relief. This false kindness – this demoralizing weakness – is
universal.”
Dr. Howe clearly linked bad breath to the oral cavity. “When the teeth and mucous
membrane of the mouth are kept clean…the offensive odor of the breath will disappear.”
He also alerted parents to malodor due to nasal foreign bodies in children. “Children of
tender years frequently insert peas, beans, and foreign substances into the nasal cavities,
which enlarge by the absorption of moisture, and, by increase of pressure, cause great
irritation. Peas and beans have been known to sprout in the nasal cavities after having
remained there several days, giving rise to serious inflammation of the mucous membrane
and spongy bones. The discharge takes place generally from the nostril in which the for-
eign body is located.”
Some of the oral remedies recommended by Dr. Howe, such as carbolic acid (phenol),
are toxic and would likely not be condoned in this day and age. Other active ingredients,
which he recommended, include powdered cinnamon, cardamom, oil of nutmeg, rhubarb,
myrrh and oil of peppermint, charcoal cake, powdered coriander, sweet-flag (hallucino-
genic at high concentrations), and leaves of partridge-berry (Gaultheria procumbens). For
cigarette smokers, he recommended small pieces of cascarilla or cinnamon bark. For
tongue coating (which he considered related to digestive disorders), he recommended
scraping the tongue, and washing the mouth with a solution of myrrh tincture and laven-
der water.
Another worthy reference from the nineteenth century is the review by D.C. Hawxhurst
(1873). He was keenly aware of the importance of postnasal drip (“catarrh”) as a major
cause of bad breath and wrote about the importance of tonsilloliths:
In the fauces there sometimes occur little nodular bodies, made up of cheese-like matter,
which constitutes the source of a peculiar fetor.
He also alerted his colleagues to odors resulting from diet:

The diet too should receive attention. …Known polluters of the breath, such as beer, wine,
sour-krout, and hard cider, may easily be entirely avoided.
Hawxhurst was keenly aware and also cautioned his dentist colleagues to avail them-
selves of the kindly offices of “some trustworthy friend,” to let them know if they suffered
from bad breath.
Modern History
During the first half of the twentieth century, particularly in the 1930s and 1940s, dental
researchers like Glenn F. Sulser and Leonard S. Fosdick from the Northwestern University
Dental School in Chicago began studying the microbial and biochemical aspects of oral
malodor production using salivary incubation assays. They were the first researchers to
demonstrate that oral malodor production comes from the anaerobic microbial degradation
of proteins into foul-smelling by-products (Berg et al. 1946; Fosdick and Piez 1953). They
discovered the relationship between salivary putrefaction and periodontal disease (Berg
et al. 1947), and were the first to try and quantify oral malodor instrumentally using the
Osmoscope (Brening et al. 1939) (Fig. 14.3).
In 1933, an American dentist named G.L. Grapp published a paper summarizing a study
of 500 patients (Grapp 1933). He concluded that most bad breath comes from the back of
the tongue. He found that the tongues of 90% of those he checked had a visible coating.
Modern History 113
Fig. 14.3 The Fair-Wells osmoscopes 1935 (with permission

from IOPscience)
Type B metal osmo-

scope. For use with
air or liquid dilution
method of threshold
odour determinations
Grapp showed that the posterior (back) two-thirds of the tongue were responsible for the
odor by wiping that area with gauze, and then smelling it. Grapp suggested that bad breath
arose from insufficient chewing of foods by modern man. He also designed a tongue cleaner
and showed that breath improves when the very back of the tongue is cleaned. Actually,
tongue cleaning has been practiced in India for hundreds, if not thousands, of years (it is
taught in their ancient Ayurveda medicine). Furthermore, tongue cleaners were also used in
Europe since the mid-nineteenth century. A collection of these antique tongue cleaners is
on display at the British Dental Association museum (64 Wimpole St., London).
In the 1960s, Joseph Tonzetich from the University of British Columbia in Canada
demonstrated the role of volatile sulfide compounds, especially hydrogen sulfide and
methyl mercaptan as important components of oral malodor (Tonzetich et al. 1967).
Dr. Tonzetich pioneered the use of gas chromatography combined with a flame photomet-
ric detector in breath analysis (Tonzetich 1971) and is widely considered the modern day
pioneer of the entire field.
In the early 1970s, Thomas F McNamara showed the role of Gram-negative rather than
Gram-positive oral bacteria in malodor production (McNamara et al. 1972). McNamara
also demonstrated the inhibitory effect of glucose and acidic pH on the process of malodor
production.
References
Berg, M., Burrill, D.Y., Fosdick, L.S.: Chemical studies in periodontal disease III: putrefaction of
salivary proteins. J. Dent. Res. 25, 231–46 (1946)
Berg, M., Burrill, D.Y., Fosdick, L.S.: Chemical studies in periodontal disease; putrefaction rate as
index of periodontal disease. J. Dent. Res. 26(1), 67–71 (1947)
Brening, R.H., Sulser, G.F., Fosdick, L.S.: The determination of halitosis by the use of the osmo-
scope and the cryoscopic method. J. Dent. Res. 18(2), 127–32 (1939)
Fosdick, L.S., Piez, K.A.: Chemical studies in periodontal disease. X. Paper chromatographic
investigation of the putrefaction associated with periodontitis. J. Dent. Res. 32(1), 87–100
(1953)
Grapp, G.L.: Fetor oris (halitosis): a medical and dental responsibility. Northwest Med. 32, 375–80
(1933)
Hawxhurst, D.: Offensive breath. Dent. Regist. 27, 105–10 (1873)
McNamara, T.F., Alexander, J.F., Lee, M.: The role of microorganisms in the production of oral
malodor. Oral Surg. Oral Med. Oral Pathol. 34(1), 41–8 (1972)
Shifman, A., Orenbuch, S., Rosenberg, M.: Bad breath – a major disability according to the
Talmud. Isr. Med. Assoc. J. 4(10), 843–5 (2002)
Arch. Oral Biol. 16(6), 587–97 (1971)
Tonzetich, J., Eigen, E., King, W.J., Weiss, S.: Volatility as a factor in the inability of certain
amines and indole to increase the odour of saliva. Arch. Oral Biol. 12(10), 1167–75 (1967)
Future Prospects
15
A growing body of knowledge has accumulated over the last 60 years in the field of breath
odor research. This knowledge enabled researchers and clinicians to devise means for bet-
ter understanding, diagnosing, and managing this condition. However, some questions
regarding this issue are still left open and require further investigation.
It is clear that breath odors are primarily the result of bacterial activity within the oral
cavity. However, many of these bacteria are prevalent in the population without causing
any problems. Therefore, it is safe to assume that other factors (oral conditions, salivary
composition, the immune system, etc.) may play a role in promoting malodor production.
Identifying these promoting factors (e.g., genetic and environmental factors), will give us
a better understanding of this condition and will help us recognize possible risk factors.
To this day, there is no reliable instrumental method to measure breath odor. In fact,
the gold standard in this field remains the human nose. Using odor judges to evaluate and
rate the malodor presents many problems, especially in the clinical settings. The reason
that most currently available instrumental methods show only a moderate concurrence
with the human nose (i.e., Pearson r-values of around 0.6) derives most probably from the
fact that most of these instruments rely on the measurement of VSCs, which may repre-
sent only some of the gases contributing to breath odors. There have been a few attempts
to develop a sensor array (also known as “electronic nose”) capable of measuring several
different chemical compounds to measure breath, so far without success. The inability of
a person to sense his own breath odor presents a major setback in both diagnosing and
treating breath odor problems as well as creating a lot of psychological problems.
Therefore, devising a handheld breath analyzer or a self-applied breath test (e.g., color
enzymatic assays), has been and still is one of the major goals of research and develop-
ment in this field. We envision that in the future, highly sensitive odor chips will be avail-
able, which can be incorporated in mobile phones, enabling practically everyone to check
their breath “on the go.”
Given the bacterial nature of this condition, it is not surprising that most treatment
approaches rely on antiseptic compounds as an important tool. However, most of these
antiseptics commonly found in oral rinses are nonspecific and kill all types of oral bacteria
indiscriminately. Some attempts have been made to utilize a more selective approach. For
example, the in vitro exposure of bacterial samples to various wavelengths of light, either
with or without using photosensitizing agents (Soukos et al. 2005), showed this technique
to be potentially selective against anaerobic oral bacteria, most likely due to the phototoxic
effect that is mediated by the formation of reactive oxygen species (ROS). Furthermore,

116 15 Future Prospects
exposure to blue light has dramatically reduced malodor production by oral bacteria
mixtures concomitant with reduction in the proportion of anaerobic Gram-negative bacteria
(Sterer and Feuerstein 2005).
Other approaches using nonchemical selective active ingredients such as various herbal
medicinals or probiotics were also reported to be effective against anaerobic oral bacteria
both in vivo and in vitro (Burton et al. 2006; Sterer and Rubinstein 2006). Furthermore,
applying these active ingredients using a sustained release delivery system showed them
to be effective in reducing oral malodor in human subjects (Sterer et al. 2008).
These and other questions are under study by many researchers around the world cur-
rently involved in this ever growing field of research.
References
Burton, J.P., Chilcott, C.N., Moore, C.J., Speiser, G., Tagg, J.R.: A preliminary study of the effect
of probiotic Streptococcus salivarius K12 on oral malodour parameters. J. Appl. Microbiol.
100(4), 754–764 (2006)
Soukos, N.S., Som, S., Abernethy, A.D., Ruggiero, K., Dunham, J., Lee, C., Doukas, A.G.,
Goodson, J.M.: Phototargeting oral black-pigmented bacteria. Antimicrob. Agents Chemother.
49(4), 1391–1396 (2005)
Sterer, N., Feuerstein, O.: Effect of visible light on malodour production by mixed oral microflora.
J. Med. Microbiol. 54(Pt 12), 1225–1229 (2005)
Sterer, N., Rubinstein, Y.: Effect of various natural medicinals on salivary protein putrefaction and
malodor production. Quintessence Int. 37(8), 653–658 (2006)
Sterer, N., Nuas, S., Mizrahi, B., Goldenberg, C., Weiss, E.I., Domb, A., Davidi, M.P.: Oral mal-
odor reduction by a palatal mucoadhesive tablet containing herbal formulation. J. Dent. 36(7),
535–539 (2008)
Index
A Delusional halitosis, 89
Amino acids Dental restorations
arginine, 23 crowns and bridges, 14
cysteine, 22 dental implants, 14
deamination, 22 dentures, 14
decarboxylation, 22 orthodontic appliances, 14
lysine, 23 splints, 14
methionine, 22 Diabetes mellitus, 55
tryptophan, 23
Antimicrobial agents E
cetylpyridinium chloride, 97 Evaluation panels
chlorhexidine, 97 experience, 37
chlorine dioxide, 97 training, 37
essential oils, 97
hydrogen peroxide, 97 G
triclosan, 97 b-Galactosidase, 22
zinc, 97 b-Galactosidase activity assay, 66
Genuine halitosis, 73
B Gingivitis, 12
Bacteria bleeding, 13
Fusobacterium nucleatum, 28 inflammation, 13
hydrogen sulfide producing bacteria, 31 Glucose, 20
Porphyromonas gingivalis, 30 Gram-negative oral bacteria, 19
Prevotella intermedia, 29 Gram-positive oral bacteria, 19
Solobacterium moorei, 28
Streptococcus salivarius, 28 H
Bad breath paradox, 79 Halitophobia
BANA test, 64 perceived odor problem, 89
pseudohalitosis, 89
C social phobia, 92
Chronic renal failure, 57 Helicobacter pylori
Cleft palate antibiotics, 48
oronasal fistulas, 44
Confidant, 73 L
Cysteine challenge testing, 67 Live microscopy, 76
Liver cirrhosis, 55
D
Delivery systems M
chewing gums, 102 Measurements of VSC, 61
lozenges, 102 GC, 62
mucoadhesive tablets, 102 sulfide monitor, 62

DOI: 10.1007/978-3-642-19312-5, Springer-Verlag Berlin Heidelberg 2011
118 Index
Microscopic sulfide assay, 69 Pistacia lentiscus, 109

Mouth rinse, 102 Proteins, 21
salivary mucins, 22
N
Nasal foreign bodies R
rhinolith, 44 Reflux, 47
O S
Oganoleptic measurement Salivary incubation assay, 67
count to twenty, 74 Self-reported breath odors, 79
Olfaction Sinuses
accommodation, 79 chronic sinusitis, 41
adaptation, 36 functional endoscopic sinus surgery
sensitivity, 36 (FESS), 41
specific anosmia, 35 postnasal drip, 41
threshold, 79 Siwak, 110
Olfactory reference syndrome (ORS), 89 Smoking, 57
body dysmorphic disorder, 90
One-stage full-mouth disinfection, 104 T
Onion, 57 Tongue
Oral dryness coating, 5
alcohol, 15 cleaning, 96
medications, 15 debridement, 105
mouth breathing, 15 dorsum, 5
saliva flow, 14 spoon test, 10
stress, 15 Tonsils
Oral malodor crypts, 42
Fetor oris, 5 laser cryptolysis, 43
Organoleptic measurement tonsillitis, 42
dilution methods, 61 tonsilloliths, 42
odor intensity scale, 60 Trimethylamineuria, 57
odor judge, 59
Osmoscope, 112 V
Oxygen Volatile organic compounds (VOCs), 24
anaerobic conditions, 20 cadaverine, 23
indole, 23
P putrescine, 23
Periodontal disease Volatile sulfide compounds
pocket depths, 12 hydrogen sulfide, 22
pH, 20 methyl mercaptan, 22

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Breath Odors

ISBN 978-3-642-19311-8 e-ISBN 978-3-642-19312-5

Springer Heidelberg Dordrecht London New York

Library of Congress Control Number: 2011929777

© Springer-Verlag Berlin Heidelberg 2011

Cover design: eStudioCalamar, Figueres/Berlin

Printed on acid-free paper

Springer is part of Springer Science+Business Media (www.springer.com)

Tel Aviv, Israel N. Sterer and M. Rosenberg

2 Breath Odors of Oral Origin (Oral Malodor)..................................................... 5

3 Biochemical and Microbial Aspects of Oral Malodor Production.................... 19

5 Breath Odors of Nasal and Pharyngeal Origin................................................... 41

6 Breath Odors and the Gastrointestinal Tract...................................................... 47

7 Other Sources of Breath Odors............................................................................ 55

8 Measurements of Breath Odors and Related Parameters................................. 59

9 Breath Odor Diagnosis.......................................................................................... 73

10 Self-Assessment of Breath Odors......................................................................... 79

11 Breath Odors, Prevalence, Gender, and Age....................................................... 83

12 Psychological Aspects of Breath Odors................................................................ 89

13 Oral Malodor Management.................................................................................. 95

14 History of Breath Odors........................................................................................ 109

15 Future Prospects.................................................................................................... 115

Index ............................................................................................................................ 117

N. Sterer, M. Rosenberg, Breath Odors, 1

Oral Malodor and the Tongue

N. Sterer, M. Rosenberg, Breath Odors, 5

Table 2.1 Distribution of breath odor origins in subjects attending multidisciplinary clinics

Fig. 2.1 Typical photo of a

Table 2.2 Tongue coating measurements

Table 2.3 Correlations among malodor related parameters

Oral Malodor, Gingival Health, and Periodontal Disease

Table 2.5 Oral malodor parameters and periodontal disease

Fig. 2.2 Gingivitis; swollen

Oral Malodor and Dental Restorations

Oral Malodor and Oral Dryness

The General Role of Bacteria in Breath Odors

The Bacterial Origin of Oral Odors

N. Sterer, M. Rosenberg, Breath Odors, 19

Metabolic Factors Affecting Malodor Production

Protein → Amino acids → Putrefactive end products

Deglycosylation: Salivary mucins are large glycoproteins comprised of a long protein

Mucin → Protein → Amino acids → Putrefactive end products

P – XH – XOOH + H2O → R − COOH + NH3 + 4H + CO2

Amines: Decarboxylation of nitrogen-containing amino acids occurs in the mouth

R − CH − COOH → R − CH2 − NH2 + CO2 + H

Table 3.1 Deamination products of anaerobic bacteria

Table 3.2 Decarboxylation reactions by anaerobic bacteria

Table 3.3 Indoles and phenols

Malodorous Volatile Organic Compounds (VOCs) in the Oral Cavity

Malodor Producing Microorganisms

metabolic processes (nonspecific theory), or simply an overgrowth of the entire bacterial

Table 3.5 Bacteria associated with malodor from tongue dorsum

Table 3.6 Bacteria associated with malodor from periodontal pockets

N. Sterer, M. Rosenberg, Breath Odors, 35

The response to a certain odorant is terminated, presumably to allow the system to be

Odor Perception and Odor Evaluation Panels

Tel Aviv, Israel N. Sterer and M. Rosenberg

d isorders were termed “Bromidrosiphobia” (Sutton 1919), “Chronic olfactory paranoid