- Email: [email protected]
Who Are the “Occasional” Snorers?
Who Are the “Occasional” Snorers?* Dan Teculescu, MD; Bernard Hannhart, MD; Catherine Aubry, MD; Bettina Montaut-Verient, MD; Jean-Marc Virion, PhD; Jean-Pierre Michaely, PhD; and Rene´ Gueguen, PhD
Study objectives: To assess the prevalence of occasional snoring in a group of middle-aged men, and to compare anthropometric variables and prevalence of sleep-related symptoms of subjects who occasionally snore with those of other snoring categories. Design: A field survey of a sample of middle-aged men in France. Participants: Male employees of a local university and subjects from the community attending a preventive medicine center. Participation rate was 93.5%. Measurements: Anthropometric variables were recorded in 499 subjects aged 23 to 66 years (mean, 44.3 years). The subjects completed a standard sleep questionnaire and were classified according to the snoring frequency as never, rarely, sometimes, occasional, several nights per week, and every night. The subjects who snore occasionally represented 8.6% of the total. Results: The anthropometric data of subjects who snore occasionally were similar to those of subjects who habitually snore. When compared with subjects who do not snore, older age and a larger neck girth were significant. Subjects who snore occasionally were also significantly more often subjects who snore loudly, and tended more frequently to have breathing stops during sleep. Conclusions: Our epidemiologic study shows that approximately 9% of a sample of middle-aged men snore occasionally. Subjects who snore occasionally have anthropometric characteristics close to those of subjects who snore habitually. The prevalence of the main sleep-related symptoms is between that of subjects who do not snore and of subjects who snore habitually. In an epidemiologic setting, inclusion of subjects who snore occasionally as subjects who do not snore or subjects who snore habitually will lead to bias. The present results suggest they should be identified and considered as a separate category. (CHEST 2002; 122:562–568) Key words: breathing sleep disorder; male subjects; obstructive sleep apnea syndrome; occasional snoring; snoring frequency Abbreviations: BMI ⫽ body mass index; OR ⫽ odds ratio; OSAS ⫽ obstructive sleep apnea syndrome
definitions have been proposed for snoring. M any In their review of the clinical significance of
snoring, Lugaresi and Partinen1 favor the definition of Robin2: “sounds made by vibrations in the soft palate and posterior faucial pillars during sleep.” Long considered a simple familial or social nuisance,3 snoring came to medical attention when its significant association with obstructive sleep apnea *From INSERM Unit 420 (Drs. Teculescu and Hannhart, and Mr. Michaely), Vandœuvre; the Center of Preventive Medicine (Dr. Aubry and Mr. Gueguen), Vandœuvre; the Department of ENT Diseases (Dr. Montaut-Verient), Nancy University Hospital, Nancy; and the Center of Clinical Investigations (Mr. Virion), Vandœuvre, France. This work was performed at the French National Institutes of Health and Medical Research (INSERM) Unit 420, Vandœuvre, France. Manuscript received August 15, 2001; revision accepted January 23, 2002. Correspondence to: Dan Teculescu, MD, INSERM Unite´ 420, BP 184, 54505 Vandœuvre, France; e-mail: Dan.Teculescu@nancy. inserm.fr 562
syndrome (OSAS) was recognized.4 Epidemiologic surveys3,5 have found OSAS to be present in 2% of women and 4% of men in an active population, but such studies are rare for technical reasons (subject needs to agree to sleep for 1 night in the sleep laboratory) and financial reasons (participants are paid $100 and the cost of the polysomnographic procedure is high). A series of studies were devoted to the prevalence of snoring, with the dual objective of detecting subjects at risk for OSAS, and for better understanding the risk factors for snoring and its possible consequences. Stradling and Crosby6 reported that subjects who snore but do not have apnea could have excessive daytime sleepiness, and suggested that snoring significantly reduced sleep quality even in the absence of obstructive apneas. In laboratory studies, snoring sound has been recorded using microphones placed either on the subject’s sternum or over the subject’s head,7 and Clinical Investigations
then is digitally processed and analyzed.8 This approach is inapplicable in field surveys, where information on snoring is usually collected using questionnaires. A series of shortcomings and limitations of such questionnaires has been described: a large proportion of “do not know” responses9 –11; underreporting by subjects12 or overreporting by wives of husbands’ snoring13; or lack of standardization of the questionnaires, etc. Some authors recorded snoring frequency dichotomously,14,15 others used a 3-point scale,11,16,17 some used a 4-point scale,18 –22 and others used a 5-point scale.5,23–25 Some authors report “habitual” snoring without any operational definition,26 whereas in other studies snoring remains ill-defined.27,28 As stressed by Young,13 while self-report of symptoms may be (relatively) valid in patient settings, it is less so in population samples, where “no direct health benefit of accurate reporting is present.” This probably partly explains the multiplication of questionnaires, making the comparison of results between different studies very difficult. A significant standardization effort was made in 1988 by the working group of the Scandinavian Society for Sleep Research and recently by the National Institutes of Health Specialized Centers of Research in Cardiopulmonary Disorders of Sleep (Universities of Pennsylvania and Wisconsin). The frequency of the main symptoms was defined on a quantitative and subjective (so-called Likert) scale.13 The Basic Nordic Sleep Questionnaire contained 27 items in 21 questions.29 The question about snoring frequency was labeled, “Do you snore while sleeping?” with a choice of five answers: 1, never or less than once per month; 2, less than once per week; 3, on 1 to 2 nights per week; 4, on 3 to 5 nights per week; and 5, every night or almost every night. To reduce misclassification, the American version introduced a “do not know” category. Research teams using the Basic Nordic Sleep Questionnaire30 –32 or the North American version5,33 to evaluate snoring prevalence labeled subjects who answered 4 or 5 as “habitual snorers” and subjects answering “never” or “less than once per week” as “nonsnorers.” The latter category served as a reference group for the evaluation of the risk factors for snoring. The classification of the intermediate category, ie, the subjects who snore occasionally, remained problematic, however. The subjects who snored “at least once a week, but pattern may be irregular” were included among the subjects who habitually snore by some authors,34 whereas most authors included them among the subjects who do not snore.5,35–39 Strictly speaking, these subjects are neither subjects who do not snore, nor subjects who habitually www.chestjournal.org
snore. We therefore decided to analyze the subgroup of subjects who snore occasionally in a sample of middle-aged male subjects, with two objectives: first, to see whether their anthropometric data and life habits are closer to those of groups of habitual snorers or to the subjects who do not snore; and second, to see whether the prevalence of the other OSAS symptoms are different from those of the extreme groups mentioned above.
Materials and Methods Subjects Two groups of male subjects aged ⱖ 20 year and sleeping with a bedmate were studied. The first group consisted of employees from a local university who attended a yearly preventive medical examination. An explanatory letter was sent to each subject, explaining the purpose of the study, stressing the noninvasive character of the protocol, and noting the right to deny participation. Three hundred thirty-four of the 357 male subjects present on the campus volunteered (93.6%). The second group was made up of male subjects from the community (northeastern France) who attended a free preventive medical check-up in a regional center of preventive medicine, serving approximately 2 million people. Of the 216 subjects who were approached (in consecutive order on the computer file) 202 subjects agreed to participate (93.5%). After a full explanation, written consent was obtained. The study protocol was approved by the Regional Committee on Ethics in Medical Research. Anthropometry Height and weight were measured using standard methods, and body mass index (BMI) was calculated. The circumferences of the neck (at the cricothyroid membrane level),38 waist, and hip were measured with a cloth tape, and the waist-to-hip ratio was obtained. All of the measurements were performed by the same observer. Questionnaire A French version of the 32-item Wisconsin University Sleep Cohort Study Questionnaire5 was completed by the subjects, with assistance from their spouses. Detailed explanations were given to the subjects; for example, subjects were urged to answer “do not know” rather than leave the question unanswered. The 3-month test-retest repeatability of the French version of the questionnaire was assessed in a subsample of the second group of subjects and was found to be satisfactory.40 For example, the question, “Have you ever been told that you snore?” had a Cohen’s (concordance test) of 0.86; “How often do you seem to have momentary periods during sleep when you stop breathing or you breathe abnormally?” had a Cohen’s of 0.50; and “How often do you, gasp, choke, or make snorting sounds during sleep?” had a Cohen’s of 0.74. Nose and Throat Examination The policy of the Regional Ethics in Medical Research Committee was to exclude any invasive diagnostic procedure in epidemiologic research. Accordingly, we limited the instrument CHEST / 122 / 2 / AUGUST, 2002
563
Table 1—Anthropometric Data According to Snoring Category* Variables
Never
Rarely
Sometimes
Occasional (ⱖ 1/wk)
Several Nights/wk
Every Night
Do Not Know
Subjects, No. Age, yr Height, cm Weight, kg BMI Neck circumference, cm Waist circumference, cm Hip circumference, cm Waist/hip ratio
107 40.4 ⫾ 9.1 175.2 ⫾ 6.5 74.0 ⫾ 10.3 24.1 ⫾ 3.1 38.4 ⫾ 2.7 86.2 ⫾ 8.8 97.6 ⫾ 5.7 0.88 ⫾ 0.05
56 41.7 ⫾ 8.6 174.7 ⫾ 7.6 76.8 ⫾ 11.4 25.2 ⫾ 3.2 39.4 ⫾ 2.6 88.2 ⫾ 8.9 98.7 ⫾ 6.5 0.89 ⫾ 0.05
103 43.8 ⫾ 10.6 174.1 ⫾ 7.0 78.3 ⫾ 9.7 25.9 ⫾ 2.9 39.2 ⫾ 2.3 90.2 ⫾ 7.8 99.6 ⫾ 6.2 0.90 ⫾ 0.05
43 47.4 ⫾ 9.7 174.3 ⫾ 5.4 80.1 ⫾ 15.0 26.3 ⫾ 4.5 40.2 ⫾ 2.5 91.4 ⫾ 11.5 100.8 ⫾ 8.5 0.91 ⫾ 0.06
75 45.6 ⫾ 9.5 173.5 ⫾ 7.7 79.9 ⫾ 11.9 26.5 ⫾ 3.6 39.9 ⫾ 2.4 91.6 ⫾ 8.9 99.7 ⫾ 5.7 0.92 ⫾ 0.06
101 48.3 ⫾ 9.2 173.0 ⫾ 7.3 84.4 ⫾ 13.5 28.2 ⫾ 3.9 40.8 ⫾ 2.7 96.9 ⫾ 10.4 102.5 ⫾ 7.2 0.94 ⫾ 0.06
14 43.8 ⫾ 12.1 169.1 ⫾ 8.4 73.4 ⫾ 12.4 26.7 ⫾ 3.9 38.9 ⫾ 2.9 87.2 ⫾ 10.4 96.5 ⫾ 6.1 0.90 ⫾ 0.08
*Data are presented as mean ⫾ SD.
to a tongue blade and simplified the score proposed for clinical purposes by Wilms et al,41 assessing semiquantitatively the nasal septum, nasal mucosa, soft palate, uvula, tonsils, tongue, and chin abnormalities. All subjects were examined by the same observer; details of the ear, nose, and throat examination have been given elsewhere.42 Statistical Analysis Data processing (analysis of variance, univariate analysis using Cochrane-Armitage trend test, and logistic regression)43 was performed using the Statistical Analysis System (version 8.1; SAS Institute; Cary, NC).
Results Complete data were obtained in 499 subjects aged 23 to 66 years (mean, 44.3; SD, 9.9 years). To the question, “Please estimate how often you snore,” 21.4% of the subjects answered “never,” 11.2% answered “rarely,” 20.6% answered “sometimes,” 8.6% answered “at least once a week,” 15.0% answered “several nights per week,” 20.2% answered “every night,” and 3.8% answered “do not know.”
The latter group was excluded from further analysis. Age, weight, BMI, neck circumference, waist circumference, and hip circumferences, and the waist/ hip ratio showed a nearly linear increase through the six snoring frequency categories; height was somewhat lower in the last two groups, contributing to the increase in BMI (Table 1). In a second stage of the analysis, subjects who never snore, rarely snore, and sometimes snore were grouped together as subjects who do not snore; subjects snoring at least 3 nights per week or every night were grouped as habitual snorers; this yielded two extreme categories to be compared with the subjects who snore occasionally. As expected, habitual snorers differed significantly from subjects who do not snore in all of the anthropometric variables, except height (Table 2). Compared with subjects who do not snore, subjects who snore occasionally were significantly older and had a larger neck circumference; none of the differences with the habitual snorers were significant. Among the nose and
Table 2—Anthropometric Data in Occasional Snorers, as Compared to Habitual Snorers and Nonsnorers* p Value From t Test Raw/With Bonferroni Adjustment Variables
Nonsnorers
Occasional Snorers
Habitual Snorers
Occasional vs Nonsnorers
Occasional vs Habitual Snorers
Habitual vs Nonsnorers
Subjects, No. Age, yr Height, cm Weight, kg BMI Neck circumference, cm Waist circumference, cm Hip circumference, cm Waist/hip ratio Current smokers, %
266 42.0 ⫾ 9.7 174.7 ⫾ 6.9 73.3 ⫾ 10.4 25.0 ⫾ 3.2 38.9 ⫾ 2.5 88.1 ⫾ 8.6 98.6 ⫾ 6.1 0.89 ⫾ 0.05 21.0
43 47.4 ⫾ 9.7 174.3 ⫾ 5.4 80.1 ⫾ 15.0 26.3 ⫾ 4.5 40.2 ⫾ 2.5 91.4 ⫾ 11.5 100.8 ⫾ 8.5 0.91 ⫾ 0.06 32.6
176 47.2 ⫾ 9.4 173.2 ⫾ 7.4 82.5 ⫾ 13.0 27.5 ⫾ 3.8 40.4 ⫾ 2.6 94.6 ⫾ 10.1 101.3 ⫾ 6.8 0.93 ⫾ 0.06 26.1
⬍ 0.01/0.01 0.03/0.55 0.05/1.00 0.71/1.00 ⬍ 0.01/0.05 0.72/1.00 0.04/0.99 0.19/1.00 0.10†
0.87/1.00 0.38/1.00 0.24/1.00 0.06/1.00 0.68/1.00 0.05/1.00 0.64/1.00 ⬍ 0.01/0.12 0.17†
⬍ 0.001/0.001 0.03/0.77 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/⬍ 0.001 0.215†
*Data are presented as mean ⫾ SD unless otherwise indicated. †From Cochram-Armitage trend test. 564
Clinical Investigations
Table 3—Nose and Throat Abnormalities in Nonsnorers, Occasional Snorers, and Habitual Snorers* Variables
Nonsnorers
Nasal septum Nasal mucosa Nasal permeability Soft palate Uvula Palatine tonsils
50.8 6.4 13.5 22.0 31.9 17.4
Occasional Habitual Snorers Snorers p Value† 53.5 4.8 16.3 27.9 53.5 11.9
55.4 4.0 16.1 38.2 45.4 24.3
0.333 0.268 0.448 0.001 0.003 0.092
*Data are presented as %. †Based on the two-sided Cochran-Armitage Z trend test.
throat data, soft palate and uvula abnormalities were significantly different across the three groups (Table 3). The prevalence of the main sleep-related symptoms among the three groups of subjects is presented in Table 4. With the exception of, “Need for coffee to stay awake. . . ,” a significant increasing trend is present for the prevalence of all symptoms. Finally, we did a logistic regression analysis of the main sleep-related symptoms, using the subjects who snore occasionally as referent group (Table 5). Differences between subjects who snore occasionally and habitual snorers were found for loud snoring (odds ratio [OR], 2.70), snoring for ⬎ 20 years (OR, 4.80), and very difficult to wake up in the morning (OR, 8.80). With respect to personal medical history, only two subjects gave a history of narcolepsy; 3.6% admitted to doctor-diagnosed sleep apnea. The prevalence of the latter was 1.2% in subjects who do not snore, 2.4% (nonsignificant) in subjects who snore occasionally, and 7.4% in habitual snorers (OR 6.7; confidence interval, 1.9 to 24.0). The prevalence of asthma, chronic bronchitis, coronary heart disease, allergy, and stroke was not significant between the groups. The prevalence of hypertension was low in
subjects who snore occasionally (2.4%) and significantly higher among subjects who habitually snore (16.9%) as compared with subjects who do not snore (8.2%) [OR, 2.3; confidence interval, 1.2 to 4.1]. Discussion Perusing the literature, we found that the classification of subjects who snore occasionally was rather arbitrary, as a consequence of the vague definition of this group. We analyzed the demographic data, life habits, and risk factors for snoring in a sample of 499 male subjects, aged 23 to 66 years, to evaluate the possible differences between subjects who snore occasionally and the extreme groups of subjects who snore habitually and subjects who do not snore. We found that subjects who snore occasionally represented approximately 9% of this sample of middleaged men from the community, and that their anthropometric data were close to those of habitual snorers. The prevalence of loud snoring was significantly increased with respect to subjects who do not snore; the trend to a higher prevalence of breathing stops and difficult waking in the morning did not reach significance. A number of weak points of this study should be acknowledged. Snoring was based on self-reporting, as is usual in epidemiologic studies. We only took into account frequency of snoring and did not analyze its duration, effect of position, or disruptiveness44; no count of number of snores per hour (snoring index) was obtained. Subjects with complaints of insomnia or excessive daytime sleepiness were not excluded to obtain a group of primary subjects who snore,45 nor did we exclude subjects with sleep apnea, to limit the sample to subjects who snore but do not have apnea. Finally, the number of subjects included was relatively limited, and this influenced the study power, especially when the prevalence of a symptom was low. With higher
Table 4 —Prevalence of Main Sleep-Related Symptoms in Nonsnorers, Occasional Snorers, and Habitual Snorers Question/Symptoms 4/Loud snoring? 6/How many years you think you have been snoring? ⬍ 10 yr ⬎ 20 yr 8/Often gasp, choke, or make snorting sounds? 10/Frequent periods when you stop breathing or breathe abnormally? 13f/Very difficult to wake up in the morning? 13j/Feeling of excessive daytime sleepiness? 13l/Nasal congestion, obstruction, or discharge at night? 13o/Need for coffee to stay awake during the day?
Nonsnorers
Occasional Snorers
Habitual Snorers
p Value*
14.9
38.1
62.7
⬍ 0.0001
53.3 10.7 0.8 2.1 15.0 8.7 5.7 6.4
43.3 6.7 2.8 7.7 2.3 4.7 11.6 9.3
35.5 26.1 16.8 16.5 17.2 16.0 14.3 10.9
0.009 ⬍ 0.0001 ⬍ 0.0001 0.046 0.021 0.009 0.24
*p value from 2 for trend. www.chestjournal.org
CHEST / 122 / 2 / AUGUST, 2002
565
Table 5—Prevalence of Main Sleep-Related Breathing Disorders in Occasional vs Habitual Snorers and Nonsnorers Symptoms Loud snoring Occasional snorers* Habitual snorers Nonsnorers How many years do you think you have been snoring? ⬍ 10 yr Occasional snorers Habitual snorers Nonsnorers ⬎ 20 yr Occasional snorers Habitual snorers Nonsnorers Often gasp, choke, make snorting sounds Occasional snorers Habitual snorers Nonsnorers Frequent period you stop breathing or breathe abnormally Occasional snorers Habitual snorers Nonsnorers Very difficult to wake up in the morning Occasional snorers Habitual snorers Nonsnorers Feeling of excessive daytime sleepiness Occasional snorers Habitual snorers Nonsnorers Nasal congestion, obstruction or discharge at night Occasional snorers Habitual snorers Nonsnorers Need for coffee to stay awake during the day Occasional snorers Habitual snorers Nonsnorers
Regression Coefficient
SE
Odds Ratio
95% Confidence Interval
1.01 ⫺ 1.26
0.36 0.39
1.00 2.70† 0.28
1.40–5.50† 0.13–0.61
1.56 ⫺ 0.54
0.79 0.45
1.00 0.94 0.58
0.40–2.20 0.24–1.40
1.56 0.26
0.79 0.85
1.00 4.80† 1.30
1.00–23.00† 0.24–6.90
1.95 ⫺ 1.23
1.04 1.24
1.00 7.10 0.29
0.92–54.00 0.03–3.30
0.86 ⫺ 1.38
0.64 0.75
1.00 2.40 0.25
0.67–8.30 0.06–1.10
2.17 2.01
1.03 1.03
1.00 8.80† 7.40
1.20–66.00† 0.99–56.00
1.36 0.66
0.75 0.76
1.00 3.90 1.90
0.89–17.00 0.44–8.60
0.24 ⫺ 0.78
0.52 0.55
1.00 1.30 0.46
0.45–3.50 0.16–1.30
1.18 ⫺ 0.41
0.58 0.58
1.00 1.20 0.67
0.38–3.70 0.21–2.10
*Referent group. †Indicates significance.
prevalence, the power was satisfactory: for example, at a 95% confidence level and a relative risk of 3.5, we had 94.9% power to detect a significant difference for loud snoring in the subjects who snore occasionally. The strengths of this study were the inclusion of a sample of subjects homogeneous with respect to age, gender, and race, and the use of a validated standard questionnaire. The prevalence of occasional snoring in various populations is difficult to compare because of the use of different definitions, as mentioned before. In French youth, “sometimes snoring” was not different between girls (15%) and boys (15.9%),46 data that are comparable to those reported by Lugaresi et al1 in their San Marino study, which indicated a rate of 16.8% for men. Higher figures were reported from Wisconsin (31.0%),5 from the United Kingdom 566
(47.1%),6 from Finland47for men (60.0%), and from the United States for female nurses (65.%).17 Older age, excess weight, central obesity, and larger neck circumference are known risk factors for habitual snoring48; our data in habitual snorers confirm this. The quasicontinuum alteration of demographic data along the various categories of snoring (Table 1) adds a welcome reassuring validity to the self-report as an epidemiologic tool. It would be tempting, in this respect, to consider subjects who snore occasionally as a step in the natural history of snorers disease; prospective studies are necessary to test this hypothesis. Our attention was caught by the fact that the higher BMI in subjects who snore habitually was in part the result of their smaller height. Thirty-five years ago, as Fletcher et al49 described two types of COPD patients, the “pink Clinical Investigations
puffer” and the “blue and bloated,” they depicted the latter as stout. We wonder whether a link could exist between habitual snoring and the bronchitic type of airway obstruction in the frame of the overlap syndrome. Subjects who snore occasionally in the present study had mean anthropometric values similar to habitual snorers; the difference for subjects who do not snore was significant only for age and for neck circumference. Older age in subjects who snore occasionally was reported by Lindberg et al.50 Koskenvuo et al34 reported a higher proportion of BMI ⬎ 27, less leisure jogging, and a higher prevalence of systemic hypertension in subjects who snore occasionally compared with subjects who do not snore. The subjects who snore occasionally among the French adolescents studied by Delasnerie-Laupretre et al46 had a significantly higher BMI when compared with subjects who do not snore; the effect was present in both sexes. Scandinavian authors34,50 insisted on the role of smoking as a risk factor for snoring; in the present study, current smoking was only present as a (nonsignificant) trend. The nose and throat examination (Table 3) showed that soft palate and uvula abnormalities are present not only in habitual snorers, but in those who snore occasionally as well. These two ear, nose, and throat findings were previously found to be risk factors for breathing pauses as well.42 We are not aware of any analysis of the prevalence of the main sleep-related symptoms in subjects who snore occasionally compared with subjects who snore habitually or subjects who do not snore. An association with loud snoring was somewhat expected in both habitual and occasional snorers. Because no direct measurement of snoring intensity was obtained in the present study, this effect could in part be caused by a better perception of snoring by this category of subjects or their bedmates. The prevalence of grasping/choking, breathing pauses, excessive daytime sleepiness, and nasal congestion/discharge at night was increased in habitual subjects who snore. When subjects who snore occasionally were taken as reference group, using a logistic regression procedure, we found habitual snorers to snore significantly more often for a long time (⬎ 20 years; OR, 4.80), to snore loudly (OR, 2.70), and to experience difficulty in waking in the morning (OR, 8.80). Systemic hypertension was significantly more prevalent in habitual snorers (16.9% vs 8.2%) compared with subjects who do not snore, but the proportion was not increased in subjects who snore occasionally, a result at variance with the findings of Koskenvuo et al.34 Doctor-diagnosed sleep apnea was twice as frequent among subjects who snore occasionally compared with those who do not snore (2.4% vs 1.2%); however, the numbers were too small for statistical significance. www.chestjournal.org
Conclusion In a sample of 499 middle-aged French men, we found 9% to be subjects who snore occasionally according to the definition proposed by Young et al.5 The anthropometric characteristics of the subjects who snore occasionally were close to those of the habitual snorers; age and neck circumferences were significantly larger than those of subjects who do not snore. When responding to the questionnaire, subjects who snore occasionally admitted more often to loud snoring and to breathing pauses during sleep. They also had more frequent soft palate and uvula abnormalities. Our results suggest that occasional snoring is at present not satisfactorily defined; inclusion of subjects who snore occasionally among subjects who do not snore or who snore habitually is not justified and represents a source of bias. Until a more precise definition is adopted, it seems advisable to consider subjects who snore occasionally a special, separate group. Subjects who snore occasionally possibly represent a step in the natural history of “heavy snorers’ disease”51, but only prospective studies could test this hypothesis. ACKNOWLEDGMENT: The authors thank Mr. Bruno Phe´ lut for help with computer files, Ms. Aline Berthelin for manuscript processing, and the study subjects for their willing participation.
References 1 Lugaresi E, Cirignotta F, Coccagna G, et al. Clinical significance of snoring. In: Saunders NA, Sullivan CE, eds. Sleep and breathing. New York, NY: Marcel Dekker, 1984; 283–298 2 Robin IG. Snoring. Proc R Soc Med 1968; 61:575–582 3 Lugaresi E, Partinen M. Prevalence of snoring. In: Saunders NA, Sullivan CE, eds. Sleep and breathing. New York, NY: Marcel Dekker, 1994; 337–362 4 Guilleminault C, Tilkian A, Dement WC. The sleep apnea syndromes. Annu Rev Med 1976; 27:465– 484 5 Young T, Palta M, Dempsey J, et al. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 1993; 328:1230 –1235 6 Stradling JR, Crosby JH. Predictors and prevalence of obstructive sleep apnoea and snoring in 1001 middle-aged men. Thorax 1991; 46:85–90 7 Wilson K, Mulrooney T, Gawtry RR. Snoring: an acoustic monitoring technique. Laryngoscope 1985; 95:1174 –1177 8 Hoffstein V. Snoring. Chest 1996; 109:201–222 9 Hoffstein V. Snoring: is it the ear of the beholder? Sleep 1994; 17:522–526 10 Enright PL, Newman AB, Wahl PW, et al. Prevalence and correlates of snoring and observed apneas in 5,201 older adults. Sleep 1996; 19:531–538 11 Gottlieb D, Yao Q, Redline S, et al. Does snoring predict sleepiness independently of apnea and hypopnea frequency? Am J Respir Crit Care Med 2000; 162:1512–1517 12 Wiggins CL, Schmidt-Nowara WW, Coultas DB, et al. Comparison of self- and spouse reports of snoring and other symptoms associated with sleep apnea syndrome. Sleep 1990; 13:245–252 CHEST / 122 / 2 / AUGUST, 2002
567
13 Young T. Epidemiology as a research tool in breathing disorders in sleep. In: Saunders NA, Sullivan CE, ed. Sleep and breathing. New York, NY: Marcel Dekker, 1994; 311–336 14 Hoffstein V, Szalai JP. Predictive value of clinical features in diagnosing obstructive sleep apnea. Sleep 1993; 16:118 –122 15 Jennum P, Schulz-Larsen K, Davidsen M, et al. Snoring and risk of stroke and ischemic heart disease in a 70-year old population: a 6-year follow up study. Int J Epidemiol 1994; 23:1159 –1164 16 Ficker JH, Wiest GH, Lehnert G, et al. Are snoring medical students at risk of failing their exams? Sleep 1999; 22:205–209 17 Hu FB, Willet WC, Colditz GA, et al. Prospective study of snoring and risk of hypertension in women. Am J Epidemiol 1999; 150:806 – 816 18 Bloom JW, Kaltenborn WT, Quan SF. Risk factors in a general population for snoring: importance of cigarette smoking and obesity. Chest 1988; 93:678 – 683 19 Stradling JR, Crosby JH. Relation between systemic hypertension and sleep hypoxaemia or snoring: analysis in 748 men drawn from the general practice. BMJ 1990; 300:75–78 20 Jennum P, Hein HO, Suadicani P, et al. Cardio-vascular risk factors in snorers: a cross-sectional study of 3,323 men aged 54 to 74 years. Chest 1992; 102:1371–1376 21 Honsberg AE, Dodge RR, Cline MG, et al. Incidence and remission of habitual snoring over a 5- to 6-year period. Chest 1995; 108:604 – 609 22 Ferini-Strambi L, Zucconi M, Castronuovo V, et al. Snoring and sleep apnea: a population study in Italian women. Sleep 1999; 22:859 – 864 23 Klink ME, Quan SF, Kaltenborn WT, et al. Risk factors associated with complaints of insomnia in a general adult population. Arch Intern Med 1992; 152:1634 –1637 24 Fitzpatrick MF, Martin K, Fossey E, et al. Snoring, asthma and sleep disturbance in Britain: a community-based survey. Eur Respir J 1993; 6:531–535 25 Hui DS, Chan JK, Ho AS, et al. Prevalence of snoring and sleep-disordered breathing in a student population. Chest 1999; 116:1530 –1536 26 Jennum P, Sjol A. Epidemiology of snoring and obstructive sleep apnea in a Danish population, age 30 – 60. J Sleep Res 1992; 1:240 –244 27 Olson LG, King MT, Hensley MJ, et al. A community study of snoring and sleep-disordered breathing: prevalence. Am Rev Respir Dis 1995; 152:711–716 28 Ohayon MM, Guilleminault C, Priest RG, et al. Snoring and breathing pauses during sleep: telephone interview survey of a United Kingdom population sample. BMJ 1997; 314:860– 863 29 Partinen M, Gislason T. Basic Nordic Sleep Questionnaire (BNSQ): a quantitated measure of subjective sleep complaints. J Sleep Res 1995; 4:150 –155 30 Janson C, Gislason T, De Backer W, et al. Daytime sleepiness, snoring and gastro-oesophageal reflux among young adults in three European countries. J Intern Med 1955; 237:277–285 31 Palomaki H, Partinen M, Juvela S, et al. Snoring as a risk factor for sleep-related brain infarction. Stroke 1989; 20: 1311–1315
568
32 Smirne S, Palazzi S, Zucconi M, et al. Habitual snoring as a risk factor for acute vascular disease. Eur Respir J 1993; 6:1357–1361 33 Zielinski J, Zgierska A, Polakowska M, et al. Snoring and excessive daytime somnolence among Polish middle-aged adults. Eur Respir J 1999; 14:946 –950 34 Koskenvuo M, Partinen M, Kaprio J, et al. Snoring and cardiovascular risk factors. Ann Med 1994; 26:371–376 35 Jennum P, Schultz-Larsen K, Christensen N. Snoring, sympathetic activity and cardiovascular risk factors in a 70-year old population. Eur J Epidemiol 1993; 9:477– 482 36 Jennum P, Schultz-Larsen K, Christensen NJ. Snoring and athero-sclerotic manifestations in a 70-year old population. Eur J Epidemiol 1996; 12:285–290 37 Marin JM, Gascon JM, Carrizo S, et al. Prevalence of sleep apnea syndrome in the Spanish adult population. Int J Epidemiol 1997; 25:381–386 38 Stradling JR, Crosby JH. Predictors and prevalence of obstructive sleep apnea and snoring in 1001 middle-aged men. Thorax 1991; 46:85–90 39 Crocker BD, Olson LG, Saunders NA, et al. Estimation of the probability of disturbed breathing during sleep before a sleep study. Am Rev Respir Dis 1990; 142:14 –18 40 Teculescu D, Guillemin F, Hannhart B, et al. Validation of the French version of the Madison University Sleep Questionnaire: the three months test/retest repeatability. Presented at the American Thoracic Society Annual Meeting, May 18 –23, 2001, San Francisco, CA 41 Wilms D, Popovich J, Conway W, et al. Anatomic abnormalities in obstructive sleep apnea. Ann Otol Rhinol Laryngol 1982; 91:595–596 42 Teculescu D, Montaut-Verient B, Hannhart B, et al. Breathing pauses during sleep: can a non-invasive ENT examination help identify subjects at risk in epidemiological settings? Med Hypotheses 2001; 56:653– 656 43 Altman DG. Practical statistics for medical research. New York, NY: Chapman and Hall, 1991 44 Young TB. Some methodologic and practical issues of reported snoring validity. Chest 1991; 99:531–532 45 Thorpy MJ. International classification of sleep disorders: diagnostic and coding manual. Diagnostic Classification Steering Committee. Rochester, MN: American Sleep Disorders Association, 1990 46 Delasnerie-Laupretre N, Patois E, Valatx J-L, et al. Sleep, snoring and smoking in high school students. J Sleep Res 1993; 2:138 –142 47 Koskenvuo M, Kaprio J, Telakivi T, et al. Snoring as a risk factor for ischaemic heart disease and stroke in men. BMJ 1987; 294:16 –19 48 Bresnitz EA, Goldberg R, Kosinski RM. Epidemiology of obstructive sleep apnea. Epidemiol Rev 1994; 16:210 –227 49 Fletcher CM, Jones NL, Burrows B, et al. American emphysema and British bronchitis. Am Rev Respir Dis 1964; 90:1–13 50 Lindberg E, Janson C, Gislason T, et al. Snoring and hypertension: a 10-year follow-up. Eur Respir J 1998; 11:884 – 889 51 Lugaresi E, Mondini S, Zucconi M, et al. Staging of heavy snorers’ disease: a proposal. Bull Eur Physiopathol Respir 1983; 19:590 –594
Clinical Investigations
Study objectives: To assess the prevalence of occasional snoring in a group of middle-aged men, and to compare anthropometric variables and prevalence of sleep-related symptoms of subjects who occasionally snore with those of other snoring categories. Design: A field survey of a sample of middle-aged men in France. Participants: Male employees of a local university and subjects from the community attending a preventive medicine center. Participation rate was 93.5%. Measurements: Anthropometric variables were recorded in 499 subjects aged 23 to 66 years (mean, 44.3 years). The subjects completed a standard sleep questionnaire and were classified according to the snoring frequency as never, rarely, sometimes, occasional, several nights per week, and every night. The subjects who snore occasionally represented 8.6% of the total. Results: The anthropometric data of subjects who snore occasionally were similar to those of subjects who habitually snore. When compared with subjects who do not snore, older age and a larger neck girth were significant. Subjects who snore occasionally were also significantly more often subjects who snore loudly, and tended more frequently to have breathing stops during sleep. Conclusions: Our epidemiologic study shows that approximately 9% of a sample of middle-aged men snore occasionally. Subjects who snore occasionally have anthropometric characteristics close to those of subjects who snore habitually. The prevalence of the main sleep-related symptoms is between that of subjects who do not snore and of subjects who snore habitually. In an epidemiologic setting, inclusion of subjects who snore occasionally as subjects who do not snore or subjects who snore habitually will lead to bias. The present results suggest they should be identified and considered as a separate category. (CHEST 2002; 122:562–568) Key words: breathing sleep disorder; male subjects; obstructive sleep apnea syndrome; occasional snoring; snoring frequency Abbreviations: BMI ⫽ body mass index; OR ⫽ odds ratio; OSAS ⫽ obstructive sleep apnea syndrome
definitions have been proposed for snoring. M any In their review of the clinical significance of
snoring, Lugaresi and Partinen1 favor the definition of Robin2: “sounds made by vibrations in the soft palate and posterior faucial pillars during sleep.” Long considered a simple familial or social nuisance,3 snoring came to medical attention when its significant association with obstructive sleep apnea *From INSERM Unit 420 (Drs. Teculescu and Hannhart, and Mr. Michaely), Vandœuvre; the Center of Preventive Medicine (Dr. Aubry and Mr. Gueguen), Vandœuvre; the Department of ENT Diseases (Dr. Montaut-Verient), Nancy University Hospital, Nancy; and the Center of Clinical Investigations (Mr. Virion), Vandœuvre, France. This work was performed at the French National Institutes of Health and Medical Research (INSERM) Unit 420, Vandœuvre, France. Manuscript received August 15, 2001; revision accepted January 23, 2002. Correspondence to: Dan Teculescu, MD, INSERM Unite´ 420, BP 184, 54505 Vandœuvre, France; e-mail: Dan.Teculescu@nancy. inserm.fr 562
syndrome (OSAS) was recognized.4 Epidemiologic surveys3,5 have found OSAS to be present in 2% of women and 4% of men in an active population, but such studies are rare for technical reasons (subject needs to agree to sleep for 1 night in the sleep laboratory) and financial reasons (participants are paid $100 and the cost of the polysomnographic procedure is high). A series of studies were devoted to the prevalence of snoring, with the dual objective of detecting subjects at risk for OSAS, and for better understanding the risk factors for snoring and its possible consequences. Stradling and Crosby6 reported that subjects who snore but do not have apnea could have excessive daytime sleepiness, and suggested that snoring significantly reduced sleep quality even in the absence of obstructive apneas. In laboratory studies, snoring sound has been recorded using microphones placed either on the subject’s sternum or over the subject’s head,7 and Clinical Investigations
then is digitally processed and analyzed.8 This approach is inapplicable in field surveys, where information on snoring is usually collected using questionnaires. A series of shortcomings and limitations of such questionnaires has been described: a large proportion of “do not know” responses9 –11; underreporting by subjects12 or overreporting by wives of husbands’ snoring13; or lack of standardization of the questionnaires, etc. Some authors recorded snoring frequency dichotomously,14,15 others used a 3-point scale,11,16,17 some used a 4-point scale,18 –22 and others used a 5-point scale.5,23–25 Some authors report “habitual” snoring without any operational definition,26 whereas in other studies snoring remains ill-defined.27,28 As stressed by Young,13 while self-report of symptoms may be (relatively) valid in patient settings, it is less so in population samples, where “no direct health benefit of accurate reporting is present.” This probably partly explains the multiplication of questionnaires, making the comparison of results between different studies very difficult. A significant standardization effort was made in 1988 by the working group of the Scandinavian Society for Sleep Research and recently by the National Institutes of Health Specialized Centers of Research in Cardiopulmonary Disorders of Sleep (Universities of Pennsylvania and Wisconsin). The frequency of the main symptoms was defined on a quantitative and subjective (so-called Likert) scale.13 The Basic Nordic Sleep Questionnaire contained 27 items in 21 questions.29 The question about snoring frequency was labeled, “Do you snore while sleeping?” with a choice of five answers: 1, never or less than once per month; 2, less than once per week; 3, on 1 to 2 nights per week; 4, on 3 to 5 nights per week; and 5, every night or almost every night. To reduce misclassification, the American version introduced a “do not know” category. Research teams using the Basic Nordic Sleep Questionnaire30 –32 or the North American version5,33 to evaluate snoring prevalence labeled subjects who answered 4 or 5 as “habitual snorers” and subjects answering “never” or “less than once per week” as “nonsnorers.” The latter category served as a reference group for the evaluation of the risk factors for snoring. The classification of the intermediate category, ie, the subjects who snore occasionally, remained problematic, however. The subjects who snored “at least once a week, but pattern may be irregular” were included among the subjects who habitually snore by some authors,34 whereas most authors included them among the subjects who do not snore.5,35–39 Strictly speaking, these subjects are neither subjects who do not snore, nor subjects who habitually www.chestjournal.org
snore. We therefore decided to analyze the subgroup of subjects who snore occasionally in a sample of middle-aged male subjects, with two objectives: first, to see whether their anthropometric data and life habits are closer to those of groups of habitual snorers or to the subjects who do not snore; and second, to see whether the prevalence of the other OSAS symptoms are different from those of the extreme groups mentioned above.
Materials and Methods Subjects Two groups of male subjects aged ⱖ 20 year and sleeping with a bedmate were studied. The first group consisted of employees from a local university who attended a yearly preventive medical examination. An explanatory letter was sent to each subject, explaining the purpose of the study, stressing the noninvasive character of the protocol, and noting the right to deny participation. Three hundred thirty-four of the 357 male subjects present on the campus volunteered (93.6%). The second group was made up of male subjects from the community (northeastern France) who attended a free preventive medical check-up in a regional center of preventive medicine, serving approximately 2 million people. Of the 216 subjects who were approached (in consecutive order on the computer file) 202 subjects agreed to participate (93.5%). After a full explanation, written consent was obtained. The study protocol was approved by the Regional Committee on Ethics in Medical Research. Anthropometry Height and weight were measured using standard methods, and body mass index (BMI) was calculated. The circumferences of the neck (at the cricothyroid membrane level),38 waist, and hip were measured with a cloth tape, and the waist-to-hip ratio was obtained. All of the measurements were performed by the same observer. Questionnaire A French version of the 32-item Wisconsin University Sleep Cohort Study Questionnaire5 was completed by the subjects, with assistance from their spouses. Detailed explanations were given to the subjects; for example, subjects were urged to answer “do not know” rather than leave the question unanswered. The 3-month test-retest repeatability of the French version of the questionnaire was assessed in a subsample of the second group of subjects and was found to be satisfactory.40 For example, the question, “Have you ever been told that you snore?” had a Cohen’s (concordance test) of 0.86; “How often do you seem to have momentary periods during sleep when you stop breathing or you breathe abnormally?” had a Cohen’s of 0.50; and “How often do you, gasp, choke, or make snorting sounds during sleep?” had a Cohen’s of 0.74. Nose and Throat Examination The policy of the Regional Ethics in Medical Research Committee was to exclude any invasive diagnostic procedure in epidemiologic research. Accordingly, we limited the instrument CHEST / 122 / 2 / AUGUST, 2002
563
Table 1—Anthropometric Data According to Snoring Category* Variables
Never
Rarely
Sometimes
Occasional (ⱖ 1/wk)
Several Nights/wk
Every Night
Do Not Know
Subjects, No. Age, yr Height, cm Weight, kg BMI Neck circumference, cm Waist circumference, cm Hip circumference, cm Waist/hip ratio
107 40.4 ⫾ 9.1 175.2 ⫾ 6.5 74.0 ⫾ 10.3 24.1 ⫾ 3.1 38.4 ⫾ 2.7 86.2 ⫾ 8.8 97.6 ⫾ 5.7 0.88 ⫾ 0.05
56 41.7 ⫾ 8.6 174.7 ⫾ 7.6 76.8 ⫾ 11.4 25.2 ⫾ 3.2 39.4 ⫾ 2.6 88.2 ⫾ 8.9 98.7 ⫾ 6.5 0.89 ⫾ 0.05
103 43.8 ⫾ 10.6 174.1 ⫾ 7.0 78.3 ⫾ 9.7 25.9 ⫾ 2.9 39.2 ⫾ 2.3 90.2 ⫾ 7.8 99.6 ⫾ 6.2 0.90 ⫾ 0.05
43 47.4 ⫾ 9.7 174.3 ⫾ 5.4 80.1 ⫾ 15.0 26.3 ⫾ 4.5 40.2 ⫾ 2.5 91.4 ⫾ 11.5 100.8 ⫾ 8.5 0.91 ⫾ 0.06
75 45.6 ⫾ 9.5 173.5 ⫾ 7.7 79.9 ⫾ 11.9 26.5 ⫾ 3.6 39.9 ⫾ 2.4 91.6 ⫾ 8.9 99.7 ⫾ 5.7 0.92 ⫾ 0.06
101 48.3 ⫾ 9.2 173.0 ⫾ 7.3 84.4 ⫾ 13.5 28.2 ⫾ 3.9 40.8 ⫾ 2.7 96.9 ⫾ 10.4 102.5 ⫾ 7.2 0.94 ⫾ 0.06
14 43.8 ⫾ 12.1 169.1 ⫾ 8.4 73.4 ⫾ 12.4 26.7 ⫾ 3.9 38.9 ⫾ 2.9 87.2 ⫾ 10.4 96.5 ⫾ 6.1 0.90 ⫾ 0.08
*Data are presented as mean ⫾ SD.
to a tongue blade and simplified the score proposed for clinical purposes by Wilms et al,41 assessing semiquantitatively the nasal septum, nasal mucosa, soft palate, uvula, tonsils, tongue, and chin abnormalities. All subjects were examined by the same observer; details of the ear, nose, and throat examination have been given elsewhere.42 Statistical Analysis Data processing (analysis of variance, univariate analysis using Cochrane-Armitage trend test, and logistic regression)43 was performed using the Statistical Analysis System (version 8.1; SAS Institute; Cary, NC).
Results Complete data were obtained in 499 subjects aged 23 to 66 years (mean, 44.3; SD, 9.9 years). To the question, “Please estimate how often you snore,” 21.4% of the subjects answered “never,” 11.2% answered “rarely,” 20.6% answered “sometimes,” 8.6% answered “at least once a week,” 15.0% answered “several nights per week,” 20.2% answered “every night,” and 3.8% answered “do not know.”
The latter group was excluded from further analysis. Age, weight, BMI, neck circumference, waist circumference, and hip circumferences, and the waist/ hip ratio showed a nearly linear increase through the six snoring frequency categories; height was somewhat lower in the last two groups, contributing to the increase in BMI (Table 1). In a second stage of the analysis, subjects who never snore, rarely snore, and sometimes snore were grouped together as subjects who do not snore; subjects snoring at least 3 nights per week or every night were grouped as habitual snorers; this yielded two extreme categories to be compared with the subjects who snore occasionally. As expected, habitual snorers differed significantly from subjects who do not snore in all of the anthropometric variables, except height (Table 2). Compared with subjects who do not snore, subjects who snore occasionally were significantly older and had a larger neck circumference; none of the differences with the habitual snorers were significant. Among the nose and
Table 2—Anthropometric Data in Occasional Snorers, as Compared to Habitual Snorers and Nonsnorers* p Value From t Test Raw/With Bonferroni Adjustment Variables
Nonsnorers
Occasional Snorers
Habitual Snorers
Occasional vs Nonsnorers
Occasional vs Habitual Snorers
Habitual vs Nonsnorers
Subjects, No. Age, yr Height, cm Weight, kg BMI Neck circumference, cm Waist circumference, cm Hip circumference, cm Waist/hip ratio Current smokers, %
266 42.0 ⫾ 9.7 174.7 ⫾ 6.9 73.3 ⫾ 10.4 25.0 ⫾ 3.2 38.9 ⫾ 2.5 88.1 ⫾ 8.6 98.6 ⫾ 6.1 0.89 ⫾ 0.05 21.0
43 47.4 ⫾ 9.7 174.3 ⫾ 5.4 80.1 ⫾ 15.0 26.3 ⫾ 4.5 40.2 ⫾ 2.5 91.4 ⫾ 11.5 100.8 ⫾ 8.5 0.91 ⫾ 0.06 32.6
176 47.2 ⫾ 9.4 173.2 ⫾ 7.4 82.5 ⫾ 13.0 27.5 ⫾ 3.8 40.4 ⫾ 2.6 94.6 ⫾ 10.1 101.3 ⫾ 6.8 0.93 ⫾ 0.06 26.1
⬍ 0.01/0.01 0.03/0.55 0.05/1.00 0.71/1.00 ⬍ 0.01/0.05 0.72/1.00 0.04/0.99 0.19/1.00 0.10†
0.87/1.00 0.38/1.00 0.24/1.00 0.06/1.00 0.68/1.00 0.05/1.00 0.64/1.00 ⬍ 0.01/0.12 0.17†
⬍ 0.001/0.001 0.03/0.77 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/0.001 ⬍ 0.001/⬍ 0.001 0.215†
*Data are presented as mean ⫾ SD unless otherwise indicated. †From Cochram-Armitage trend test. 564
Clinical Investigations
Table 3—Nose and Throat Abnormalities in Nonsnorers, Occasional Snorers, and Habitual Snorers* Variables
Nonsnorers
Nasal septum Nasal mucosa Nasal permeability Soft palate Uvula Palatine tonsils
50.8 6.4 13.5 22.0 31.9 17.4
Occasional Habitual Snorers Snorers p Value† 53.5 4.8 16.3 27.9 53.5 11.9
55.4 4.0 16.1 38.2 45.4 24.3
0.333 0.268 0.448 0.001 0.003 0.092
*Data are presented as %. †Based on the two-sided Cochran-Armitage Z trend test.
throat data, soft palate and uvula abnormalities were significantly different across the three groups (Table 3). The prevalence of the main sleep-related symptoms among the three groups of subjects is presented in Table 4. With the exception of, “Need for coffee to stay awake. . . ,” a significant increasing trend is present for the prevalence of all symptoms. Finally, we did a logistic regression analysis of the main sleep-related symptoms, using the subjects who snore occasionally as referent group (Table 5). Differences between subjects who snore occasionally and habitual snorers were found for loud snoring (odds ratio [OR], 2.70), snoring for ⬎ 20 years (OR, 4.80), and very difficult to wake up in the morning (OR, 8.80). With respect to personal medical history, only two subjects gave a history of narcolepsy; 3.6% admitted to doctor-diagnosed sleep apnea. The prevalence of the latter was 1.2% in subjects who do not snore, 2.4% (nonsignificant) in subjects who snore occasionally, and 7.4% in habitual snorers (OR 6.7; confidence interval, 1.9 to 24.0). The prevalence of asthma, chronic bronchitis, coronary heart disease, allergy, and stroke was not significant between the groups. The prevalence of hypertension was low in
subjects who snore occasionally (2.4%) and significantly higher among subjects who habitually snore (16.9%) as compared with subjects who do not snore (8.2%) [OR, 2.3; confidence interval, 1.2 to 4.1]. Discussion Perusing the literature, we found that the classification of subjects who snore occasionally was rather arbitrary, as a consequence of the vague definition of this group. We analyzed the demographic data, life habits, and risk factors for snoring in a sample of 499 male subjects, aged 23 to 66 years, to evaluate the possible differences between subjects who snore occasionally and the extreme groups of subjects who snore habitually and subjects who do not snore. We found that subjects who snore occasionally represented approximately 9% of this sample of middleaged men from the community, and that their anthropometric data were close to those of habitual snorers. The prevalence of loud snoring was significantly increased with respect to subjects who do not snore; the trend to a higher prevalence of breathing stops and difficult waking in the morning did not reach significance. A number of weak points of this study should be acknowledged. Snoring was based on self-reporting, as is usual in epidemiologic studies. We only took into account frequency of snoring and did not analyze its duration, effect of position, or disruptiveness44; no count of number of snores per hour (snoring index) was obtained. Subjects with complaints of insomnia or excessive daytime sleepiness were not excluded to obtain a group of primary subjects who snore,45 nor did we exclude subjects with sleep apnea, to limit the sample to subjects who snore but do not have apnea. Finally, the number of subjects included was relatively limited, and this influenced the study power, especially when the prevalence of a symptom was low. With higher
Table 4 —Prevalence of Main Sleep-Related Symptoms in Nonsnorers, Occasional Snorers, and Habitual Snorers Question/Symptoms 4/Loud snoring? 6/How many years you think you have been snoring? ⬍ 10 yr ⬎ 20 yr 8/Often gasp, choke, or make snorting sounds? 10/Frequent periods when you stop breathing or breathe abnormally? 13f/Very difficult to wake up in the morning? 13j/Feeling of excessive daytime sleepiness? 13l/Nasal congestion, obstruction, or discharge at night? 13o/Need for coffee to stay awake during the day?
Nonsnorers
Occasional Snorers
Habitual Snorers
p Value*
14.9
38.1
62.7
⬍ 0.0001
53.3 10.7 0.8 2.1 15.0 8.7 5.7 6.4
43.3 6.7 2.8 7.7 2.3 4.7 11.6 9.3
35.5 26.1 16.8 16.5 17.2 16.0 14.3 10.9
0.009 ⬍ 0.0001 ⬍ 0.0001 0.046 0.021 0.009 0.24
*p value from 2 for trend. www.chestjournal.org
CHEST / 122 / 2 / AUGUST, 2002
565
Table 5—Prevalence of Main Sleep-Related Breathing Disorders in Occasional vs Habitual Snorers and Nonsnorers Symptoms Loud snoring Occasional snorers* Habitual snorers Nonsnorers How many years do you think you have been snoring? ⬍ 10 yr Occasional snorers Habitual snorers Nonsnorers ⬎ 20 yr Occasional snorers Habitual snorers Nonsnorers Often gasp, choke, make snorting sounds Occasional snorers Habitual snorers Nonsnorers Frequent period you stop breathing or breathe abnormally Occasional snorers Habitual snorers Nonsnorers Very difficult to wake up in the morning Occasional snorers Habitual snorers Nonsnorers Feeling of excessive daytime sleepiness Occasional snorers Habitual snorers Nonsnorers Nasal congestion, obstruction or discharge at night Occasional snorers Habitual snorers Nonsnorers Need for coffee to stay awake during the day Occasional snorers Habitual snorers Nonsnorers
Regression Coefficient
SE
Odds Ratio
95% Confidence Interval
1.01 ⫺ 1.26
0.36 0.39
1.00 2.70† 0.28
1.40–5.50† 0.13–0.61
1.56 ⫺ 0.54
0.79 0.45
1.00 0.94 0.58
0.40–2.20 0.24–1.40
1.56 0.26
0.79 0.85
1.00 4.80† 1.30
1.00–23.00† 0.24–6.90
1.95 ⫺ 1.23
1.04 1.24
1.00 7.10 0.29
0.92–54.00 0.03–3.30
0.86 ⫺ 1.38
0.64 0.75
1.00 2.40 0.25
0.67–8.30 0.06–1.10
2.17 2.01
1.03 1.03
1.00 8.80† 7.40
1.20–66.00† 0.99–56.00
1.36 0.66
0.75 0.76
1.00 3.90 1.90
0.89–17.00 0.44–8.60
0.24 ⫺ 0.78
0.52 0.55
1.00 1.30 0.46
0.45–3.50 0.16–1.30
1.18 ⫺ 0.41
0.58 0.58
1.00 1.20 0.67
0.38–3.70 0.21–2.10
*Referent group. †Indicates significance.
prevalence, the power was satisfactory: for example, at a 95% confidence level and a relative risk of 3.5, we had 94.9% power to detect a significant difference for loud snoring in the subjects who snore occasionally. The strengths of this study were the inclusion of a sample of subjects homogeneous with respect to age, gender, and race, and the use of a validated standard questionnaire. The prevalence of occasional snoring in various populations is difficult to compare because of the use of different definitions, as mentioned before. In French youth, “sometimes snoring” was not different between girls (15%) and boys (15.9%),46 data that are comparable to those reported by Lugaresi et al1 in their San Marino study, which indicated a rate of 16.8% for men. Higher figures were reported from Wisconsin (31.0%),5 from the United Kingdom 566
(47.1%),6 from Finland47for men (60.0%), and from the United States for female nurses (65.%).17 Older age, excess weight, central obesity, and larger neck circumference are known risk factors for habitual snoring48; our data in habitual snorers confirm this. The quasicontinuum alteration of demographic data along the various categories of snoring (Table 1) adds a welcome reassuring validity to the self-report as an epidemiologic tool. It would be tempting, in this respect, to consider subjects who snore occasionally as a step in the natural history of snorers disease; prospective studies are necessary to test this hypothesis. Our attention was caught by the fact that the higher BMI in subjects who snore habitually was in part the result of their smaller height. Thirty-five years ago, as Fletcher et al49 described two types of COPD patients, the “pink Clinical Investigations
puffer” and the “blue and bloated,” they depicted the latter as stout. We wonder whether a link could exist between habitual snoring and the bronchitic type of airway obstruction in the frame of the overlap syndrome. Subjects who snore occasionally in the present study had mean anthropometric values similar to habitual snorers; the difference for subjects who do not snore was significant only for age and for neck circumference. Older age in subjects who snore occasionally was reported by Lindberg et al.50 Koskenvuo et al34 reported a higher proportion of BMI ⬎ 27, less leisure jogging, and a higher prevalence of systemic hypertension in subjects who snore occasionally compared with subjects who do not snore. The subjects who snore occasionally among the French adolescents studied by Delasnerie-Laupretre et al46 had a significantly higher BMI when compared with subjects who do not snore; the effect was present in both sexes. Scandinavian authors34,50 insisted on the role of smoking as a risk factor for snoring; in the present study, current smoking was only present as a (nonsignificant) trend. The nose and throat examination (Table 3) showed that soft palate and uvula abnormalities are present not only in habitual snorers, but in those who snore occasionally as well. These two ear, nose, and throat findings were previously found to be risk factors for breathing pauses as well.42 We are not aware of any analysis of the prevalence of the main sleep-related symptoms in subjects who snore occasionally compared with subjects who snore habitually or subjects who do not snore. An association with loud snoring was somewhat expected in both habitual and occasional snorers. Because no direct measurement of snoring intensity was obtained in the present study, this effect could in part be caused by a better perception of snoring by this category of subjects or their bedmates. The prevalence of grasping/choking, breathing pauses, excessive daytime sleepiness, and nasal congestion/discharge at night was increased in habitual subjects who snore. When subjects who snore occasionally were taken as reference group, using a logistic regression procedure, we found habitual snorers to snore significantly more often for a long time (⬎ 20 years; OR, 4.80), to snore loudly (OR, 2.70), and to experience difficulty in waking in the morning (OR, 8.80). Systemic hypertension was significantly more prevalent in habitual snorers (16.9% vs 8.2%) compared with subjects who do not snore, but the proportion was not increased in subjects who snore occasionally, a result at variance with the findings of Koskenvuo et al.34 Doctor-diagnosed sleep apnea was twice as frequent among subjects who snore occasionally compared with those who do not snore (2.4% vs 1.2%); however, the numbers were too small for statistical significance. www.chestjournal.org
Conclusion In a sample of 499 middle-aged French men, we found 9% to be subjects who snore occasionally according to the definition proposed by Young et al.5 The anthropometric characteristics of the subjects who snore occasionally were close to those of the habitual snorers; age and neck circumferences were significantly larger than those of subjects who do not snore. When responding to the questionnaire, subjects who snore occasionally admitted more often to loud snoring and to breathing pauses during sleep. They also had more frequent soft palate and uvula abnormalities. Our results suggest that occasional snoring is at present not satisfactorily defined; inclusion of subjects who snore occasionally among subjects who do not snore or who snore habitually is not justified and represents a source of bias. Until a more precise definition is adopted, it seems advisable to consider subjects who snore occasionally a special, separate group. Subjects who snore occasionally possibly represent a step in the natural history of “heavy snorers’ disease”51, but only prospective studies could test this hypothesis. ACKNOWLEDGMENT: The authors thank Mr. Bruno Phe´ lut for help with computer files, Ms. Aline Berthelin for manuscript processing, and the study subjects for their willing participation.
References 1 Lugaresi E, Cirignotta F, Coccagna G, et al. Clinical significance of snoring. In: Saunders NA, Sullivan CE, eds. Sleep and breathing. New York, NY: Marcel Dekker, 1984; 283–298 2 Robin IG. Snoring. Proc R Soc Med 1968; 61:575–582 3 Lugaresi E, Partinen M. Prevalence of snoring. In: Saunders NA, Sullivan CE, eds. Sleep and breathing. New York, NY: Marcel Dekker, 1994; 337–362 4 Guilleminault C, Tilkian A, Dement WC. The sleep apnea syndromes. Annu Rev Med 1976; 27:465– 484 5 Young T, Palta M, Dempsey J, et al. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 1993; 328:1230 –1235 6 Stradling JR, Crosby JH. Predictors and prevalence of obstructive sleep apnoea and snoring in 1001 middle-aged men. Thorax 1991; 46:85–90 7 Wilson K, Mulrooney T, Gawtry RR. Snoring: an acoustic monitoring technique. Laryngoscope 1985; 95:1174 –1177 8 Hoffstein V. Snoring. Chest 1996; 109:201–222 9 Hoffstein V. Snoring: is it the ear of the beholder? Sleep 1994; 17:522–526 10 Enright PL, Newman AB, Wahl PW, et al. Prevalence and correlates of snoring and observed apneas in 5,201 older adults. Sleep 1996; 19:531–538 11 Gottlieb D, Yao Q, Redline S, et al. Does snoring predict sleepiness independently of apnea and hypopnea frequency? Am J Respir Crit Care Med 2000; 162:1512–1517 12 Wiggins CL, Schmidt-Nowara WW, Coultas DB, et al. Comparison of self- and spouse reports of snoring and other symptoms associated with sleep apnea syndrome. Sleep 1990; 13:245–252 CHEST / 122 / 2 / AUGUST, 2002
567
13 Young T. Epidemiology as a research tool in breathing disorders in sleep. In: Saunders NA, Sullivan CE, ed. Sleep and breathing. New York, NY: Marcel Dekker, 1994; 311–336 14 Hoffstein V, Szalai JP. Predictive value of clinical features in diagnosing obstructive sleep apnea. Sleep 1993; 16:118 –122 15 Jennum P, Schulz-Larsen K, Davidsen M, et al. Snoring and risk of stroke and ischemic heart disease in a 70-year old population: a 6-year follow up study. Int J Epidemiol 1994; 23:1159 –1164 16 Ficker JH, Wiest GH, Lehnert G, et al. Are snoring medical students at risk of failing their exams? Sleep 1999; 22:205–209 17 Hu FB, Willet WC, Colditz GA, et al. Prospective study of snoring and risk of hypertension in women. Am J Epidemiol 1999; 150:806 – 816 18 Bloom JW, Kaltenborn WT, Quan SF. Risk factors in a general population for snoring: importance of cigarette smoking and obesity. Chest 1988; 93:678 – 683 19 Stradling JR, Crosby JH. Relation between systemic hypertension and sleep hypoxaemia or snoring: analysis in 748 men drawn from the general practice. BMJ 1990; 300:75–78 20 Jennum P, Hein HO, Suadicani P, et al. Cardio-vascular risk factors in snorers: a cross-sectional study of 3,323 men aged 54 to 74 years. Chest 1992; 102:1371–1376 21 Honsberg AE, Dodge RR, Cline MG, et al. Incidence and remission of habitual snoring over a 5- to 6-year period. Chest 1995; 108:604 – 609 22 Ferini-Strambi L, Zucconi M, Castronuovo V, et al. Snoring and sleep apnea: a population study in Italian women. Sleep 1999; 22:859 – 864 23 Klink ME, Quan SF, Kaltenborn WT, et al. Risk factors associated with complaints of insomnia in a general adult population. Arch Intern Med 1992; 152:1634 –1637 24 Fitzpatrick MF, Martin K, Fossey E, et al. Snoring, asthma and sleep disturbance in Britain: a community-based survey. Eur Respir J 1993; 6:531–535 25 Hui DS, Chan JK, Ho AS, et al. Prevalence of snoring and sleep-disordered breathing in a student population. Chest 1999; 116:1530 –1536 26 Jennum P, Sjol A. Epidemiology of snoring and obstructive sleep apnea in a Danish population, age 30 – 60. J Sleep Res 1992; 1:240 –244 27 Olson LG, King MT, Hensley MJ, et al. A community study of snoring and sleep-disordered breathing: prevalence. Am Rev Respir Dis 1995; 152:711–716 28 Ohayon MM, Guilleminault C, Priest RG, et al. Snoring and breathing pauses during sleep: telephone interview survey of a United Kingdom population sample. BMJ 1997; 314:860– 863 29 Partinen M, Gislason T. Basic Nordic Sleep Questionnaire (BNSQ): a quantitated measure of subjective sleep complaints. J Sleep Res 1995; 4:150 –155 30 Janson C, Gislason T, De Backer W, et al. Daytime sleepiness, snoring and gastro-oesophageal reflux among young adults in three European countries. J Intern Med 1955; 237:277–285 31 Palomaki H, Partinen M, Juvela S, et al. Snoring as a risk factor for sleep-related brain infarction. Stroke 1989; 20: 1311–1315
568
32 Smirne S, Palazzi S, Zucconi M, et al. Habitual snoring as a risk factor for acute vascular disease. Eur Respir J 1993; 6:1357–1361 33 Zielinski J, Zgierska A, Polakowska M, et al. Snoring and excessive daytime somnolence among Polish middle-aged adults. Eur Respir J 1999; 14:946 –950 34 Koskenvuo M, Partinen M, Kaprio J, et al. Snoring and cardiovascular risk factors. Ann Med 1994; 26:371–376 35 Jennum P, Schultz-Larsen K, Christensen N. Snoring, sympathetic activity and cardiovascular risk factors in a 70-year old population. Eur J Epidemiol 1993; 9:477– 482 36 Jennum P, Schultz-Larsen K, Christensen NJ. Snoring and athero-sclerotic manifestations in a 70-year old population. Eur J Epidemiol 1996; 12:285–290 37 Marin JM, Gascon JM, Carrizo S, et al. Prevalence of sleep apnea syndrome in the Spanish adult population. Int J Epidemiol 1997; 25:381–386 38 Stradling JR, Crosby JH. Predictors and prevalence of obstructive sleep apnea and snoring in 1001 middle-aged men. Thorax 1991; 46:85–90 39 Crocker BD, Olson LG, Saunders NA, et al. Estimation of the probability of disturbed breathing during sleep before a sleep study. Am Rev Respir Dis 1990; 142:14 –18 40 Teculescu D, Guillemin F, Hannhart B, et al. Validation of the French version of the Madison University Sleep Questionnaire: the three months test/retest repeatability. Presented at the American Thoracic Society Annual Meeting, May 18 –23, 2001, San Francisco, CA 41 Wilms D, Popovich J, Conway W, et al. Anatomic abnormalities in obstructive sleep apnea. Ann Otol Rhinol Laryngol 1982; 91:595–596 42 Teculescu D, Montaut-Verient B, Hannhart B, et al. Breathing pauses during sleep: can a non-invasive ENT examination help identify subjects at risk in epidemiological settings? Med Hypotheses 2001; 56:653– 656 43 Altman DG. Practical statistics for medical research. New York, NY: Chapman and Hall, 1991 44 Young TB. Some methodologic and practical issues of reported snoring validity. Chest 1991; 99:531–532 45 Thorpy MJ. International classification of sleep disorders: diagnostic and coding manual. Diagnostic Classification Steering Committee. Rochester, MN: American Sleep Disorders Association, 1990 46 Delasnerie-Laupretre N, Patois E, Valatx J-L, et al. Sleep, snoring and smoking in high school students. J Sleep Res 1993; 2:138 –142 47 Koskenvuo M, Kaprio J, Telakivi T, et al. Snoring as a risk factor for ischaemic heart disease and stroke in men. BMJ 1987; 294:16 –19 48 Bresnitz EA, Goldberg R, Kosinski RM. Epidemiology of obstructive sleep apnea. Epidemiol Rev 1994; 16:210 –227 49 Fletcher CM, Jones NL, Burrows B, et al. American emphysema and British bronchitis. Am Rev Respir Dis 1964; 90:1–13 50 Lindberg E, Janson C, Gislason T, et al. Snoring and hypertension: a 10-year follow-up. Eur Respir J 1998; 11:884 – 889 51 Lugaresi E, Mondini S, Zucconi M, et al. Staging of heavy snorers’ disease: a proposal. Bull Eur Physiopathol Respir 1983; 19:590 –594
Clinical Investigations