Necrotising Ulcerative Gingivitis: A Literature Review

James Duftya / Nikolaos Gkraniasb / Nikos Donosc

s that there is a lack of good quality research available. This paper aims to scrutinise the literature and provide an up-to-date summary of the available inform
ubMed Clinical Queries and Google Scholar. Keyword searches were carried out, utilising MeSH terms and free text. English language articles primarily were inc
It is an opportunistic bacterial infection which is predominantly associated with spirochetes. Treatment of NUG must be provided on a case-by-case basis, tailore
responses to the oral biofilm. Risk factors must be investigated and addressed. Treatment should consist of gentle superficial debridement, oral hygiene instructi

Oral Health Prev Dent 2017; 15: 321–327. doi: 10.3290/j.ohpd.a38766 Submitted for publication: 27.01.16; accepted for publication: 24.04.16.

N ecrotising ulcerative gingivitis (NUG) was defined by the

1999 International Workshop for the Classification of
Periodontal Diseases as ‘an infection characterized by gin-
Thus, a review of the literature was performed to
provide an up-to-date summary of the history, prevalence,
clinical manifestations, aetiology and treatment of NUG.
gival necrosis presenting as ‘punched-out’ papillae, with
gingival bleeding and pain’.33 Secondary features include
‘fetid breath and pseudomembrane formation’. 33 Its acute, MATERIALS AND METHODS
painful and destructive nature makes it unique when com-
pared with other periodontal diseases. 50 Yet despite the A literature search was performed electronically using the
historical reports of the disease available since ancient Cochrane Library, Ovid Medline, Embase, PubMed Clinical
times (401 BC), there is still much we do not know about Queries and Google Scholar. Keyword searches were
this disease.38 carried out, utilising MeSH terms and free text. The search
terms utilised included: gingivitis, necrotizing ulcerative,
ulcerative stomatitides OR Vincent’s gingivitis OR
fusospirillary gingi- vitides OR Vincent gingivitis OR
a Senior Dental Officer, Defence Medical Services, Ministry of Defence, UK. Research necrotizing ulcerative gingivi- tis OR fusospirillary gingivitis
question, completed the searches, analysed the literature, wrote the manuscript. OR infection Vincent’s OR phagedenic gingivitis OR
b Senior Clinical Lecturer and Honorary Consultant, Centre for Oral Clinical Re- search, infection Vincent OR gingivitides fu- sospirillary OR
Barts and The London School of Medicine and Dentistry, Queen Mary University of
London, UK. Co-wrote, proofread and revised manuscript. membranous gingivitides acute OR Vincent’s stomatitis OR
c Professor, Centre for Oral Clinical Research, Barts and The London School of Medicine
gingivitis acute membranous OR anginas Vin- cent OR
and Dentistry, Queen Mary University of London, UK. Contributed substantially to gingivitis phagedenic OR phagedenic gingivitides OR acute
research idea, guided the research, proofread and revised the manuscript. membranous gingivitis OR gingivitis necrotizing ulcer- ative
Correspondence: Professor Nikos Donos, Centre for Oral Clinical Research, In- stitute
OR Vincent angina OR gingivitides acute membranous OR
of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary Vincent stomatitis OR gingivitis Vincent’s OR gingivitides
University of London, London, UK. Tel: +44-20-7882-3063; Email: n.donos@qmul.ac.uk phagedenic OR mouth trench OR ulcerative gingivitis necrotiz-
ing OR stomatitides ulcerative OR acute necrotizing ulcer-
ative gingivitis OR gingivitis fusospirillary OR angina Vincent
OR Vincent’s infection OR ulcerative stomatitis.

Vol 15, No 4, 2017 1

Dufty et al

Primarily English-language articles were included, with field, as it became recognised as a separate entity from the tonsillar
key foreign-language (French and German) articles condition.48
included where possible from the 1900s to the present day.
Rele- vant journals identified from the (electronic and
hand) search were then downloaded / acquired or
requests for those unavailable put in to the Defence
Medical Services Library, the British Library, the Eastman
Dental Library and the University of Bern. Papers not
directly relevant to the review were excluded after review
by the first author.

RESULTS

Following comprehensive searches of the above databases,

57 articles were included in the review.

Historical References of NUG

The war records of Xenophon’s troops, dating from the 4th
century BC, are credited as the first reference to an oral
disease with signs and symptoms similar to NUG. 26 Xeno-
phon noted, during his Army’s retreat from Persia (401 BC),
that many of his soldiers suffered from ulcerated, sore,
foul- smelling oral problems. 30 Prior to this, most of these
NUG- like symptoms had been attributed to scurvy. 48 It
wasn’t until a British Physician, James Lind, wrote about
scurvy in 1772 and noted that oral ulceration was not
always associ- ated with it, that a separate diagnosis was
sought for these oral symptoms.48 In 1778, John Hunter
was credited with making this first distinction between the
oral symptoms of scurvy and NUG. He described the ‘gum
between the teeth’ as being ‘swollen and spongy with
ulceration, tenderness and bleeding’.48 However, much of
the literature in the 19th century that came from French
authors does not appear to acknowledge Hunter’s
conclusions.26
In 1859, Bergeron described a NUG-like clinical picture
while serving with French soldiers. Furthermore, he drew
evidence from the available literature to show that the
same infection affected the general population of adults as
well as children.26 In 1886, Hirsch expanded the diagnostic
features of NUG to include involvement of the submaxillary
lymph glands, ropy saliva, malaise and fever. 26
Plaut and Vincent recognised the involvement of
fusiform spirochetes in NUG in the 1890s. 55 It is Vincent,
however, who is widely credited with the identification and
under- standing of what would eventually become known
as NUG.30 Vincent was a physician serving with the Military
Medical Service of France. Part of his remit was to look at
the differences between oral fusiform-spirochete
infections, namely tuberculosis and syphilis. In 1892,
Vincent recog- nised the ulcero-membranous condition
that affected the oral cavity and tonsils that would later
bear his name ‘Vin- cent’s angina’. 30 Plaut further
described the condition in relation to the tonsils in 1894,
with Birnheim in 1898 point- ing out the similarity between
the bacteriology associated with Vincent’s angina and the
ulcerative gingivitis. 48 Follow- ing these publications,
Vincent’s infection drew greater in- terest from the dental
 Much was written about NUG during and population (including dependents) at military dental centres
following the First World War, with significant in Fort Knox, Kentucky, USA. The number of cases seen over
evidence being presented by Colyer. 13 His a 12-
research showed a prevalence of 0.3% for troops month period represented a prevalence rate of 0.19%.4
in the rear and up to 0.7% for troops returning Falkler et al17 studied NUG in a US periodontal clinic.
from the trenches.13 Bowman discussed the wide From their results, we can calculate the prevalence rate to
prevalence of ulceromembranous stomatitis be 0.93%. Horning et al29 studied a military population
amongst troops returning from the front line.7 based at the Naval Training Center in San Diego, California.
Although he distinguished the condition from
Vincent’s angina, he did not describe specific
preva- lence data, merely stating that the disease
seemed to have been rife. Bouty, 5 despite writing
primarily about Vincent’s angina among soldiers
in France, noted that pyorrhoea al- veolaris
(periodontal disease) often presented as well as
stomatitis and gingivitis. 5 The reports on Vincent’s
infection may therefore have been misleading, as
not all studies have distinguished between the
tonsillar and gingival infections.

Vincent’s Infection as a Solely Gingival Problem

Part of the difficulty in determining the
prevalence of NUG before, during and after the
First World War, despite its ap- parently high
frequency (leading to the introduction of the term
‘trench mouth’), is distinguishing exactly which
dis- ease was being described in each report. 44
‘Vincent’s an- gina’ is described as confined to the
throat/ tonsillar area, and ‘Vincent’s infection’ as
confined to the mouth. 31 Other authors have
noted how Vincent’s disease has been desig-
nated in various ways, depending on its
anatomical location or the pathological process
involved.39 Pindborg’s list of 33 possible terms for
NUG magnifies the extent of the prob- lem. 44 As
he puts it, ‘No doubt the list of synonyms has not
been exhausted… but it appears on the basis
thereof how difficult it can be to form an estimate
of the existing litera- ture when so different terms
are used’.44
Therefore, despite many texts referring to
trench mouth and what we now call NUG, there
are many others that uti- lise different
nomenclature and some in which it is unclear
which form of the disease was studied.

Studies After World War 2

Many of the studies on NUG have been based on
military populations. Dean and Singleton 14
investigated the preva- lence of NUG in US Coast
Guard and Marine trainees, where they found an
overall prevalence of 8.4%.
Pindborg studied Danish Naval Sailors and Army
soldiers during the period 1945–1948. 6960 men
were examined with an incidence of NUG of
6.9%.44 Yet only five years later in a US military
population in 1956, a lower rate of approxi- mately
2% of subjects was reported by Grupe and
Wilder.21 Manson and Rand37 reported on 61
recurrent cases of Vincent’s infection who
attended the Royal Dental Hospital, London.
Barnes et al4 went on to study 218 patients who
were receiving treatment for NUG in the military
 Dufty et al

They found a prevalence of NUG of 0.45% (calculated from do not distinguish between the necrotising periodontal dis- eases.
data; 0.5% was actually recorded in the paper). Staging pathways for NUG have not been widely ad-
The most recent prevalence data we have for NUG in
the military is from Collet-Schaub,12 who studied the
prevalence of NUG in Swiss Army recruits. No cases of NUG
were de- tected and the study provides a prevalence rate
calculated to be < 0.03% (actually 0.0%, as no NUG was
seen).12

Prevalence of NUG
The studies discussed above support the statement that
NUG is rare.1 There is a wide range in variance in the preva-
lence from the literature, ranging from < 0.03% to
9.4%.12,14 The highest rates were reported during the First
and Second World Wars.7,14,22 However, since then, there
has been an overall decline in the prevalence of NUG. 1
Albandar and Ti- noco1 point out that as a rare disease,
there are few stud- ies designed to assess its prevalence.
Melnick et al38 state that the ‘true prevalence of … NUG…
is unknown’, with most of the evidence coming from
studies based on military recruits, which are unlikely to be
truly representative of the general population. In fact, it is
difficult to determine what prevalence should be expected
in a general military popula- tion, but from analysis of more
recent studies it can be ex- pected to be < 1%.
Table 1 and Fig 1 illustrate the prevalence of NUG in dif-
ferent specific populations studied during the period 1943–
2000.

Clinical Characteristics and Diagnosis

Necrotising ulcerative gingivitis is a painful oral condition. 50
It is unique amongst the periodontal diseases in that it
demonstrates an acute presentation, characterised by the
rapid onset of pain from the gingivae that is accompanied
by bleeding and necrosis of the interdental gingiva. 50
The three key clinical signs of NUG are intense pain,
punched-out appearance of the gingival papilla, and
gingivae that bleed with little or no provocation. 33,50 Fever,
regional lymphadenopathy, malaise, malodor / fetor oris
and metallic taste may also be signs. 1 Patients suffering
from NUG tend to seek treatment due to the intensity of
the pain.50
Chronic forms of NUG have been presented in the litera-
ture.44 However, it is most likely that these are recurrences
of the disease.50 Other differential diagnoses should be ruled
out as part of the diagnostic process. 28 These include
apthous stomatitis, traumatic ulcers, desquamative gingivitis,
erythema multiforme, agranulocytosis, infectious mononucle-
osis, acute leukaemia, allergic stomatitis and secondary
syphilis. It is believed that primary herpetic
gingivostomatitis most resembles NUG, yet it could be
argued that, despite the similarities of some of the clinical
manifestations of both dis- eases, they are patently
dissimilar.28
Pindborg et al46 set out a staging system for the diagno-
sis of NUG. They described four stages: tip of interdental
papilla only involved, involvement of marginal gingiva with
presence of punched-out papilla, attached gingiva also in-
volved, and exposure of bone. Unfortunately, these stages
opted, and diagnosis now relies on the key Rosebury failed to show any good evidence of its
clinical signs associated with the different transmission.49 This state- ment is supported by the
disease processes, even though there may be literature that regards NUG as an endogenous infection.
some overlap. Maintaining sanitary conditions in the military environment
is still essential for the prevention of transmission of other
Aetiology communicable diseases, for example, diarrhoea and vomit-
NUG is an opportunistic bacterial infection ing.2 From the perspective of NUG, it would be more useful
which is predom- inantly associated with to look at which factors predispose an individual to the
spirochetes, with the main cultivat- able disease.
bacteria being Treponema sp. and
Fusobacterium sp.27,36 Rowland50 states that
amongst the periodontal diseases, NUG is one
of the strongest examples that shows a
primary bacterial aetiology.
Plaut and Vincent’s work in 1894 and 1896
were the first studies that suggested the
bacterial aetiology of NUG.10 Cahn9 discovered
bacterial invasion of the periodon- tal tissues in
a patient with NUG. Many years later, Listgar-
ten35 used electron microscopy to investigate
gingival bi- opsy specimens from eight patients
who had lesions typical of NUG. He described
four zones of bacterial invasion. Starting from
the most superficial layer, these were the bac-
terial zone, neutrophil-rich zone, necrotic zone,
and zone of spirochetal infiltration. These layers,
however, were not al- ways clearly demarcated
and could be missing altogether. This study also
showed that spirochetes invade non-ne- crotic
tissue as well as necrotic tissue. Spirochetes
were present in all four zones, although more so
in the deep than the superficial tissues.
Unfortunately, this study was unable to shed
any light on the pathogenesis of NUG.35
Spirochetes, fusiforms and bacteroides have
all been frequently cultivated from NUG
lesions,17,36 but a definitive periodontal
pathogen is yet to be implicated in the onset or
progression of this disease. 24 It has been
suggested that the bacteria involved in NUG
may not be different from those involved in
gingivitis, and recent research gives plau- sibility
to the statement that it is a mixed bacterial
infection which is modified by particular risk
factors.20,47 Yet its bac- terial aetiology does
appear to indicate that it should be considered
as different from other periodontal diseases.50

Transmissibility
Concerns about the transmissibility of NUG
persisted in the military during World War 1,
World War 2 and beyond, 48 leading to the
incidence of NUG in soldiers within barracks and
in the field being investigated. A higher
incidence of NUG was found in soldiers in field
conditions. However, it was also noted that
there may be less opportunity for trans- mission
whilst outdoors, as soldiers had their own
cooking and eating equipment and slept in the
open air, rather than in the group rooms within
the barracks.52.
The American Dental Association stated that
NUG was not communicable, after research by
Dufty et a l

Table 1 Prevalence of NUG

Author, year Population Population size NUG prevalence rate

Hall, 194322 UK military 22,675 0.17% Royal Navy
1200 0.6% Army
1000 0.15% RAF

Dean and Singleton Jr, 1945 14 US military 75,000 7.3%–9.5%

(overall 8.4%)

Pindborg, 195144 Danish military 6960 6.9%

Grupe and Wilder, 195621 US military 2622 2.2%

Giddon et al, 196319 US college students 326 2.5%

Smitt, 196555 Dutch military 5992 2.0%

Barnes et al, 19734 US military 113,000 0.19%

Wirthlin and Devine, 197858 US military 21,000 0.2%

Stevens et al, 198457 US patients 9978 0.51%

Falkler et al, 198717 US patients 3725 0.9%

Horning et al, 199029 US military 10,000 0.5% (actually 0.45%)

Collet-Schaub, 200012 Swiss military 4395 < 0.03%

Predisposing Factors the

Factors that have been suggested to contribute to the
de- velopment of NUG include smoking, psychological
stress, malnutrition, oral hygiene, socioeconomic status
and im- munosuppression.11,18,19,32,41,45,50,53,57

Smoking
Smoking was initially associated with NUG in the 1940s. 26
Following on from this, Pindborg studied the tobacco con-
sumption and gingival status of Danish Royal Marines. 45 It
was found that smokers, particularly heavy smokers, were
more likely to suffer with NUG when compared to non-
smokers.
Kowolik and Nisbet32 found 98 out of 100 (98%) pa-
tients presenting with NUG for the first time were smokers.
Stevens et al57 demonstrated comparable findings, with the
observation of 94% of NUG patients being smokers.

Psychological factors
Reports have shown a positive correlation between
psycho- logical stress and NUG.19,28,41,42,52 Effects of
stress, which may affect the periodontium, include
lowered resistance to infection, endocrine dysfunction,
changes in diet and oral hygiene, and parafunctional
habits.42 Furthermore, person- ality types that may have
had difficulty in adapting to the military environment
have also shown an association with NUG.18 In the US
Army, Shields53 found that NUG patients were under a
greater amount of emotional stress than in a control
group. Nevertheless, it has been argued that the
evidence for stress in NUG is not convincing, although
potential physiological alterations associated with
stress are feasible. 17 Potentially, there are many
confounding fac- tors, and consideration should
be given to what else may be implicated and why
other individuals in the same envi- ronment are
not similarly affected.

Malnutrition
Malnutrition has been associated with NUG. 28,42
Vitamin deficiency, particularly of vitamin C, has
been linked with an increased risk of NUG. 38
However, the effect of malnutrition and its link
with NUG currently remains unclear.42

Oral hygiene
Poor oral hygiene has been associated with NUG,
with NUG patients having poorer oral hygiene and
greater deposits of calculus when compared to a
control group.4,28 Pre-existing gingivitis has
frequently been associated with NUG. 44,45

Socioeconomic status
There appears to be an increased risk of NUG
associated with lower socioeconomic status,
where status is measured by occupation, income
and education.38,57 This is of par- ticular interest
when considering recent findings from British
Army recruits (when compared with Royal Navy
and Royal Air Force recruits), showing that they
are from the most de- prived quintiles on the
Index of Multiple Deprivation.15

Immunosuppression
NUG has been described in patients with systemic
disease and immunosuppression, including patients
with von Wille-
 Dufty et al

Prevalence of NUG vae can be very painful, often precluding the possibility of
instrumentation. Where manual plaque control is not pos-
9 sible, chemical plaque control should be utilised, until the
8 patient is able to tolerate the use of a toothbrush and
7
inter- proximal cleaning devices.34
Prevalence (%)

6
5 Again, the literature is divided as to optimal treatment
4
3 regimens. Hartnett and Shiloah24 state that reports on the
2 treatment of NUG are few, with highly varied treatment mo-
1
dalities. They recommend non-surgical therapy, with the use
0
1943 1945 1951 1956 1964 1965 1973 1978 1984 1987 1990 2000 of antimicrobials where there is evidence of systemic in-
volvement (lymphadenopathy, fever, malaise) and concomi-
tant use of 0.12% chlorhexidine mouthwash. They point out
that there have been no controlled studies on the use of
chlorhexidine mouthwash in NUG patients.24
Fig 1 Prevalence of NUG from the published literature 1943–2000. Three percent (3%) hydrogen peroxide has been used as
a mouth rinse for the debridement of necrotic areas. Its ef-
fect is thought to be due to the liberation of oxygen and the
effect on the anaerobic bacteria. Chlorhexidine mouth rinse
brand’s disease, malignancy, drug-induced agranulocytosis, (0.2%) twice a day may be useful when mechanical brush-
systemic lupus erythematosus and acquired immunodefi- ing is not possible, but should only really be considered as
ciency syndrome (AIDS).42 an adjunct to mechanical debridement and good personal
plaque control.24
Seasonal Variation Metronidazole would appear to be the antibiotic of
The seasonality of NUG has been investigated in several choice, as it is more effective than oxidising antiseptics
studies, yet there is unfortunately no consistent evidence (e.g. hydrogen peroxide) and has no local side effects. 40 It
showing increased occurrence of infection during any one is as efficacious as penicillin, has a shorter course, pro-
season.38 duces no known hypersensitivity or allergic reactions, has
had fewer problems with the development of resistant spe-
Age at Presentation cies and has a narrower spectrum, therefore having less
NUG is regarded as a disease of young adults in developed effect on commensal bacteria when compared to penicil-
countries, with a mean age of onset of 23 years. 38 The lin.40 Its use in NUG was first noted by Shinn, 54 when met-
mean age of the patients in the Manson and Rand study 37 ronidazole, which was prescribed for vaginal
was 24.6 years, with the majority of patients being in the trichomoniasis, also resulted in the resolution of the NUG.
20-24 year-old age group. The number of recurrences It is recom- mended as the drug of choice for NUG, at a
ranged from one to more than three. More than one area dose of 400 mg three times a day for three days by both
was usually affected, with the mandibular anterior region the British National Formulary8 and by the Faculty of
being affected most commonly. 37 In the Barnes et al General Dental Practice guidelines.43
study,4 the vast majority of patients were young (mean age In Horning and Cohen’s study, 28 6% of cases were
22 years), male, Caucasian soldiers. treated with scaling and polishing, 5% also were prescribed
a concomitant antiseptic mouthrinse, and 85% of cases
Treatment were prescribed an antibiotic. All cases progressed favour-
Many different forms of treatment have been suggested ably by the 24- to 48-h evaluation, although they did note
over the centuries, from the use of topical iodine, boric acid that significant attachment loss had occurred in cases that
rinses, chromic acid, mercury, silver compounds, aniline initially presented with the more severe forms of NUG.
dyes, sodium perborate rinses, glycerine, hydrogen peroxide Haroian and Vissichelli23 developed instructions for the
and arsenicals to antibiotics and root surface debride- treatment of NUG, recommending debridement, frequent
ment.6,16,37,50 It was only in the 1960s that debridement mouthrinses of either warm salt water or 3% hydrogen per-
became recognised as a viable technique for the treatment oxide solution, administration of antibiotics in cases where
of NUG.24 It had previously been rejected due to the per- fever and lymphadenopathy were present, oral health care
ceived risks that it could lead to bacteraemia and the po- instructions and patient motivation, and follow-up and re-
tentially life-threatening Vincent’s angina. 24 Nevertheless, it evaluation. Looking at Haroian and Vissichelli’s guidelines,
is clear that the response to therapy is different from other it is apparent that they are broadly the same as those used
forms of periodontal disease, since removal of the bacterial to manage periodontal diseases in general, with the excep-
challenge results in a quick resolution of the disease. 50,56 tion being the use of mouthwashes when oral hygiene might
Treatment can be split into two separate phases: the acute be difficult, or antibiotics where regional spread of infection is
phase and the maintenance phase. The acute phase of noted.23,42
treatment aims to arrest disease and relieve pain. 34 Specific advice should also be given in relation to any
Treatment during the acute phase is difficult, as the gingi- risk factors identified in the patient’s history. Whilst we
Dufty et al

have discussed the fact that the evidence may not be con- 12. Collet-Schaub D. The prevalence of acute necrotizing ulcerative gingivitis
clusive, advice on diet and stress reduction should occur in Swiss military collectives [in German]. Schweiz Monatsschr Zahnmed
2000;110:538–541.
and smoking cessation advice must be given. 23 These fac-
13. Colyer CG. Acute ulcerative gingivitis. Br Med J 1918;2(3015):396–398.
tors also have much wider health implications.
14. Dean HT, Singleton Jr DE. Vincent’s infection—a wartime disease: prelim-
inary considerations on the epidemiology of ulcerative gingivostomatitis.
Treatment summary Am J Public Health 1945;35:433–440.
15. Elmer TB, Langford J, McCormick R, Morris AJ. Is there a differential in
Treatment of NUG must be provided on a case-by-case the dental health of new recruits to the British Armed Forces? A pilot
basis, tailored to what the individual can tolerate and the study. BDJ 2011;211:E18–E18.
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