Sleep, 20(12):1157-1161
© 1997 American Sleep Disorders Association and Sleep Research Society
Arousals and Nocturnal Respiration in
Symptomatic Snorers and NonSnorers
*Soren Berg, tSusan Nash, tPhilip Cole and tVictor Hoffstein
Summary: The purpose of the present investigation was to examine the relationship among upper airway resistance, snoring, and arousals, all measured simultaneously, in non apneic snorers complaining of excessive daytime
sleepiness (EDS). To accomplish this task, we selected a group of nine nonapneic snorers who presented because
of snoring, EDS, tiredness, or fatigue. Ten healthy, alert, nonapneic, nonsnoring subjects recruited from among the
hospital personnel acted as a comparison group. All subjects had nocturnal polysomnography, which included
measurements of snoring, nasal and pharyngeal airway pressure, esophageal pressure, and total respiratory flow.
Each polysomnogram was analyzed to identify all arousals and all respiratory events, i.e. apneas, hypopneas, and
periods of increased upper airway resistance. Each arousal was examined to determine whether it was associated
with a respiratory event, and each respiratory event was examined to determine whether it was associated with an
arousal. The results were compared between snorers and nonsnorers. There was no significant difference between
the two groups in the total sleep time (182 :!: 61 minutes in controls vs. 188 :!: 50 minutes in patients) or the total
number of arousals per hour of sleep (24 :!: 12 in controls vs. 28 :!: 10 in snorers). However, the distribution of
arousals, i.e. electroencephalogram (EEG) vs. respiratory, was different in snorers and nonsnorers. In snorers 55%
of arousals were respiratory, whereas in nonsnorers only 17% of arousals were associated with respiratory events.
Not unexpectedly, the snorers had significantly more respiratory events during the night (512) than controls (112).
However, the relative proportion of these events that was accompanied by arousals was similar in both groups. We
conclude that the difference in daytime function between symptomatic snorers and asymptomatic non snorers is
unlikely to be due strictly to the number of arousals during the night; however, it is possible that respiratory and
EEG arousals have different impacts on daytime performance, which may explain the difference in daytime function
between our two groups. Key Words: Upper airway resistance syndrome-Snoring-Sleepiness-Arousals.
Many habitual snorers referred to sleep disorders
centers complain of excessive daytime tiredness, fatigue, or sleepiness, thus raising a possibility of obstructive sleep apnea. However, in many of them nocturnal
polysomnography does not demonstrate sleep apnea but
confirms loud and continuous snoring. Guillerninault et
al. (1,2) postulated that these patients may have cyclical
increases of upper airway resistance throughout the
night, causing arousals from sleep, thus leading to sleep
fragmentation and daytime dysfunction. However, no
simultaneous measurements of upper airway resistance,
snoring, and arousals have been performed in well-defined groups of nonapneic snorers with daytime sleepiness and nonsnoring healthy controls, Such measurements would help to determine how frequently episodes
of increased upper airway resistance are associated with
arousals, and whether there are any differences in the
Accepted for publication August 1997.
Address correspondence and reprint requests to Dr. V. Hoffstein,
St. Michael's Hospital, 30 Bond Street, Toronto, ON M5B 1W8,
Canada
number and pattern of arousals in sleepy snorers vs.
asymptomatic nonsnorers.
Consequently, the present investigation was designed to test the hypothesis that nonapneic snorers
who complain of excessive daytime sleepiness have
more arousals than healthy nonsnorers, and that most
of the arousals in the former group are associated with
respiratory events, i.e. apneas, hypopneas, and episodes of elevated upper airway resistance.
METHODS
Patients
We searched our database to select patients who satisfied the following criteria: 1) chief presenting complaint was excessive daytime sleepiness, tiredness, or fatigue; 2) all admitted to being habitual snorers, thus raising a possibility of sleep apnea; 3) all had undergone
diagnostic nocturnal polysomnography that confirmed
the snoring and demonstrated the absence of sleep apnea,
1157
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*University Hospital, Lund, Sweden; and
tSt, Michael's Hospital, University of Toronto, Toronto, Ontario, Canada
1158
S. BERG ET AL.
Polysomnography
All patients and controls had nocturnal polysomnography which included monitoring of electroencephalogram (EEG), electromyogram (chin and legs), electrooculogram, electrocardiogram, oxygen saturation,
chest wall and abdominal movements, and snoring
sounds, as described previously (3). Upper airway
pressures at 8, 12, and 16 cm from the nares, corresponding to the posterior nasal cavity, rhinopharynx,
and hypopharynx, respectively, were also monitored
using open catheters (infant feeding tubes, 8F). Esophageal pressure was measured using a specially designed microchip sensor catheter (Reditech Corp., Copenhagen, Denmark), with the sensor head placed in
the middle third of the esophagus (4). Flow was measured using a tight-fitting, full-face continuous positive
airway pressure (CPAP) mask modified to serve as a
pneumotachograph. Pressure and flow signals, displayed on a chart recorder together with other polysomnographic variables, were digitized at 50 Hz and
processed using appropriate software to calculate airway resistance.
All measurements were performed during stable periods of well-defined non-rapid eye movement (nonREM) sleep and a minimum of 3 minutes after the
latest sleep stage shift.
Polysomnograms were scored three times: 1) to identify the arousals, 2) to identify respiratory events, and 3)
to identify the linkages between the two. The person
Sleep. Vol. 20. No. 12. 1997
scoring polysomnograms (S.N.) was not aware of whether it belonged to a snorer or to a control subject.
Definition of respiratory events
Respiratory events were classified as apneas, hypopneas, or episodes of increased upper airway resistance. Apneas were defined as a complete cessation of
oronasal flow lasting 10 seconds or more. Hypopneas
were defined as a reduction of at least 50% in oronasal
flow lasting 10 seconds or longer and reduction in oxygen saturation by at least 4% from baseline. Increased
upper airway resistance events were differentiated
from hypopneas as follows: they were defined as episodes during which there was an increase of 20% or
more in peak-to-peak pressure amplitude, compared
with baseline, lasting at least 15 seconds, with reduction in flow not exceeding 50% of baseline; these
events were usually not accompanied by significant
oxygen desaturation. Baseline peak-to-peak esophageal pressure fluctuations were obtained during awake,
unobstructed breathing. Initially, we also identified
snoring events as episodes of snoring lasting at least
15 seconds; however, it soon became apparent that this
identification was redundant, because all snoring
events were associated with increased upper airway
resistance, although the opposite was not always true.
We then examined each respiratory event to see whether it was associated with an arousal.
Definition of arousals
Arousals were defined according to American Sleep
Disorders Association criteria as 3-15 seconds of alpha and fast theta EEG frequency (5). Each arousal
was examined to decide whether it was associated with
a respiratory event. This was determined by checking
for the presence of apnea, hypopnea, or increased
esophageal pressure, i.e. upper airway resistance, in
the 30-second period preceding each arousal. If a respiratory event was not accompanied by an arousal as
defined above, we examined the EEG to determine if
there was a shorter burst of alpha activity lasting between 1 and 3 seconds. These EEG events were termed
"microarousals". No effort was made to count all such
events but only those that were associated with episodes of increased upper airway resistance. Arousals
that were not associated with respiratory events were
termed "EEG arousals".
Data analysis
Anthropometric and sleep data, including apnea index, hypopnea index, upper airway resistance index,
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as defined by the apnea/hypopnea index as < 10; and 4)
none had any concurrent disease or were taking any
medication. The patients were contacted and asked to
undergo another polysomnography with measurements
of upper airway resistance. Twenty-five patients were
contacted, 12 of whom agreed to participate. Subsequently, three patients were excluded because of failure to
complete the required investigations. The remaining nine
patients were used for data analysis.
We also selected a comparison group consisting of 13
hospital personnel who were healthy and had no complaints whatsoever. Polysomnography revealed that three
individuals snored lightly, whereas the remaining 10 had
no snoring or sleep apnea. These 10 individuals formed
the comparison group. Although comparing a group of
healthy subjects to a group of snorers with complaints
of daytime sleepiness may at first seem inappropriate,
we wanted to compare the groups from the "opposite
ends of the arousal spectrum", i.e. the group that is expected to have the lowest number of arousals (healthy,
asymptomatic subjects) with the group that is expected
to have the highest number of arousals (snoring, symptomatic patients).
1159
SNORING, AROUSALS, AND DAYTIME DYSFUNCTION
TABLE 1.
Variable
Age (years)
Body mass index (kg/m')
Weight (kg)
TABLE 3.
Anthropometric data
Controls
(mean:!: SO)
Patients
(mean:!: SO)
30 :!: 5
25 :!: 2
77 :!: 8
47 :!: 12*
27 :!: 4
84 :!: 15
Sleep architecture and Epworth sleepiness
score
Controls
Patients
(mean:!: SD) (mean:!: SO)
Variable
* Significantly (p < 0.05) different from controls.
182
66
14
38
9
10
6
:!:
:!:
:!:
:!:
:!:
:!:
:!:
188 :!:
63 :!:
19 :!:
36 :!:
2:!:
10 :!:
13 :!:
61
21
7
13
7
5
3
50
20
6
20
1*
6
3*
* Significantly (p < 0.05) different from controls.
trast, such events (a total of 10) were identified in only
two of 10 controls.
NC).
DISCUSSION
RESULTS
All snorers and nonsnorers were males. On the average, snorers were 17 years older than nonsnorers.
Body mass index was not significantly different between both groups (Table 1).
Respiratory data (Table 2) confirm that both groups
were nonapneics, although snorers had significantly
more respiratory events (apneas, hypopneas, and episodes of elevated upper airway resistance) than nonsnorers. Baseline esophageal pressure and maximum
pressure during an episode with elevated upper airway
resistance were not different between the groups.
Sleep architecture (Table 3) shows that the amount
of slow-wave sleep (expressed as a percent of total
sleep time) was significantly lower in snorers than
nonsnorers. Epworth sleepiness score was significantly
higher in snorers. Relatively low total sleep time and
sleep efficiency in snorers and controls were probably
due to invasive instrumentation.
Total arousal index was similar in both groups, but
the types of arousals were different (Table 4). Snorers
had significantly more arousals associated with respiratory events than nonsnorers. Although the latter
group had fewer respiratory events, a similar percentage of them were associated with arousals (Table 5).
In seven of nine patients, a total of 35 respiratory
events were associated with microarousals; by conTABLE 2.
Variable
Apnea index
Hypopnea index
Upper airway resistance index
Baseline esophageal pressure (cm H 20)
Maximum esophageal pressure (% of baseline)
This study indicates that snorers with daytime dysfunction have similar arousal index values but different
types of arousals than nonsnoring, asymptomatic controls; most arousals in symptomatic snorers occur in
association with respiratory events, whereas controls
have mostly "pure EEG" arousals.
The similarity in the numbers of arousals in both
groups is surprising and unexpected, particularly because our snorers were older than the controls, which
should further accentuate the difference in arousals.
On the basis of the existing data (1,2,6-8), we expected the opposite, i.e. symptomatic snoring patients
would have more arousals than controls, consistent
with the currently accepted view that arousals lead to
sleep fragmentation causing daytime dysfunction.
Consequently, we must consider the possibility that
our study design and patient selection simply failed to
detect the difference in arousals, where in fact such a
difference exists.
One possibility is that, despite patients' complaints,
our groups were in fact not different with respect to
their daytime function, which would explain why we
found similar numbers of arousals in both of them.
This is a difficult issue to resolve, because we defined
sleepiness strictly on the basis of subjective complaint
rather than objective measurements such as the multiple sleep latency test (MSLT). However, there is no
Respiratory data
Controls
(mean:!: SO)
0.2
1.1
2.2
7
195
:!:
:!:
:!:
:!:
:!:
0.4
3
2
2
53
Patients
(mean:!: SO)
2
3
12
9
195
:!:
:!:
:!:
:!:
:!:
2*
2*
8*
4
44
* Significantly (p < 0.05) different from controls.
Sleep, Vol. 20, No. 12, 1997
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and arousal index, were compared between patients
and controls using unpaired t tests. Frequency of different arousals (i.e. the percentage of EEG and respiratory arousals) in both groups was compared using
chi-square tests. All statistical analysis was performed
using SAS software, release 6.10 (SAS Institute, Cary,
Total sleep time (minutes)
% Sleep efficiency
% Stage I time
% Stage II time
% Slow-wave sleep time
% REM sleep time
Epworth sleepiness score
S. BERG ET AL.
1160
TABLE 4.
Variable
Total arousal index
EEG arousal index
Apnea arousal index
Hypopnea arousal index
DAR arousal index
TABLE 5.
Arousals
Controls
(mean:':: SD)
24
20
0.1
1
1.8
:':: 12
:':: 9
:':: 0.3
:!: 3
:':: 1.6
Patients
(mean:':: SD)
28:'::
13 :'::
2 :'::
3 :!:
10 :'::
10
7*
2*
2*
7*
EEG, electroencephalogram; DAR, upper airway resistance.
* Significantly (p < 0.05) different from controls.
Sleep, Vol. 20, No. 12, 1997
Variable
Controls
Patients
Total number of arousals
% associated with respiratory events
678
17
748
55*
Total number of respiratory events
% associated with arousals
129
89
512
81
* Significantly (p < 0.05) different from controls.
(12), which may explain why our group of sleepy
snorers did not have more arousals than nonsnorers.
Furthermore, the effect of sleepiness on the arousal
response is not well understood and may alter the
arousal threshold (13). Another possibility is that the
"arousal strength", i.e. duration of arousals, is longer
in snoring patients compared with controls. We did not
systematically record the duration of each arousal (other than to confirm that it was within the range of 315 seconds), but the possibility that arousals are longer
in snorers than in controls, and that this may account
for their daytime symptoms, clearly needs to be explored further.
Is it possible that daytime sleepiness among nonapneic snorers is unrelated to either snoring or arousals? For example, Downey et al. (14), in their retrospective analysis of children with upper airway resistance syndrome, were unable to demonstrate a statistically significant difference in the arousal index
between children with UARS and either normal controls or children with sleep apnea. Jennum and Sj~l
(15) examined daytime sleepiness and cognitive function in snorers and patients with sleep apnea and found
that many snorers (almost 10%) complained of unintended sleepiness; however, because only respiratory
measurements were performed during sleep, the authors were unable to comment on the arousals and
their possible relationship to cognitive function. Philip
et al. (16) examined sleep latency and performance
tests in normal volunteers subjected to one night of
sleep disturbance induced by repetitive short auditory
stimuli sufficient to cause an arousal. The authors
found that one night of sleep fragmentation was sufficient to reduce significantly sleep latency the following day but did not affect performance tests. Martikainen et al. (17) examined evolution of symptoms
among habitual snorers over a period of 5 years. These
authors found that approximately 14% of habitual
snorers complain of daytime sleepiness, with 2.44.5% reporting traffic accidents due to sleepiness.
However, when a small sample, consisting of 22 men,
had nocturnal polysomnography, almost 30% were
found to have sleep apnea. This raises the question of
whether it was only patients with unsuspected obstructive sleep apnea who had problems with excessive
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evidence that the MSLT can resolve between "mild"
sleepiness and "no" sleepiness (1,2). Furthermore,
measurement of sleep latencies in this situation is not
helpful. Finding a significantly shorter sleep latency
among symptomatic snorers would strengthen our conclusion, but finding similar sleep latencies in both
groups would still leave us with the problem of having
to explain the definite complaint of sleepiness, tiredness, or fatigue consistently voiced by this group.
Another possibility is that airway resistance in our
group of snorers was not as high as that in the group
of patients with upper airway resistance syndrome
(UARS) studied by Guilleminault et al. (2). In our patients, the mean esophageal pressure nadir was only
-15 cm H 20, compared with -33 cm H 20 in the
group studied by Guilleminault et al. (2). Only during
frank apneas did we observe more negative esophageal
pressures, comparable to those measured in patients
studied by other investigators. It is quite possible that
stronger respiratory efforts coupled with higher upper
airway resistance would produce more arousals.
Can our results explain the fundamental difference
between our groups, i.e. daytime dysfunction? The answer to this question is a speculative one and depends
on the interpretation of arousals. If we assume that all
arousals, independent of whether or not they are associated with respiratory events, are equivalent, then
our results do not indicate a relationship between
arousals and daytime dysfunction. However, if we assume that all arousals are not equivalent, and in particular that those associated with increased work in
breathing and reduction in oxygen saturation may lead
to daytime dysfunction, whereas pure EEG arousals do
not, then our results could explain why the patients are
more sleepy than the controls. The possibility that respiratory arousals may lead to daytime dysfunction is
implicit in the results of previous investigations (911); e.g. Telakivi et al. (9) found that in nonapneic
snorers it was not the total number of arousals but
rather the number of desaturations exceeding 4% that
correlated best with certain indices of daytime dysfunction. Arousal responses appear to be mediated by
brain stem mechanisms and are not necessarily accompanied by cortical effects, such as typical EEG pattern
Distribution of arousals and their association
with respiratory events
SNORING, AROUSALS, AND DAYTIME DYSFUNCTION
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daytime sleepiness. Recently, Lofaso et al. (18) was
unable to find any difference in complaints of daytime
sleepiness, fatigue, and Epworth sleepiness scale
scores between two groups of snorers with and without
fragmented sleep. On the other hand, Martin et al. (19)
found that in normal individuals one night of sleep
fragmentation induced by repetitive sound stimuli
leads to reduction in sleep latency and impairment of
daytime function. The results presented above illustrate that the relationship among snoring, arousals, and
daytime sleepiness continues to be a matter of debate,
not necessarily because such an association does not
exist, but perhaps because it is masked by the lack of
uniform definition of snoring, arousals, and daytime
sleepiness.
Recently, Fietze et al. (20) studied respiratory and
movement arousals in patients with sleep apnea at
baseline and while on nasal CPAP. The latter abolished
abnormal respiratory events and reduced the number
of respiratory arousals but had no effect on movement
arousals. Because daytime function of these patients
improves when they are treated with CPAp, the implication is that respiratory arousals, rather than movement arousals, may be responsible for daytime dysfunction.
In summary, we found that nonapneic snoring patients complaining of excessive daytime sleepiness
have similar total numbers of arousals as asymptomatic controls. However, these patients have significantly more respiratory events. We speculate that it is
not the number of arousals per se but the type of arousal (pure EEG vs. respiratory) that may lead to daytime
symptoms.
1161