The Influence of Active and Passive Smoking on Habitual Snoring Karl A. Franklin, Tho´rarinn Gı´slason, Ernst Omenaas, Rain Jo ˜ gi, Erik Juel Jensen, Eva Lindberg, ¨ rnsdo´ttir, Lennarth Nystro ¨ m, Birger N. Laerum, Eythor Bjo ¨ rnsson, Kjell Tore´n, Maria Gunnbjo and Christer Janson Department of Respiratory Medicine, University Hospital, Umea˙; Department of Respiratory Medicine and Allergology, Uppsala University, Uppsala; and Department of Occupational and Environmental Medicine and Allergology, Sahlgrenska University Hospital, Go ¨ teborg, Sweden; Department of Pulmonary Medicine, Landspitali University Hospital, Reykjavik, Iceland; Department of Thoracic Medicine and Center for Clinical Research, Haukeland University Hospital, Bergen, Norway; Lung Clinic, Foundation Tartu University Clinics, Tartu, Estonia; Department of Respiratory Diseases, University Hospital, Aarhus, Denmark
The impact of active smoking, passive smoking, and obesity on habitual snoring in the population is mainly unknown. We aimed to study the relationship of habitual snoring with active and passive tobacco smoking in a population-based sample. A total of 15,555 of 21,802 (71%) randomly selected men and women aged 25–54 years from Iceland, Estonia, Denmark, Norway, and Sweden answered a postal questionnaire. Habitual snoring, defined as loud and disturbing snoring at least 3 nights a week, was more prevalent among current smokers (24.0%, p ⬍ 0.0001) and ex-smokers (20.3%, p ⬍ 0.0001) than in never-smokers (13.7%). Snoring was also more prevalent in neversmokers exposed to passive smoking at home on a daily basis than in never-smokers without this exposure (19.8% vs. 13.3%, p ⬍ 0.0001). The frequency of habitual snoring increased with the amount of tobacco smoked. Active smoking and passive smoking were related to snoring, independent of obesity, sex, center, and age. Ever smoking accounted for 17.1% of the attributable risk of habitual snoring, obesity (body mass index ⭓ 30 kg/m2) for 4.3%, and passive smoking for 2.2%. Smoking, both current and ex-smoking, is a major contributor to habitual snoring in the general population. Passive smoking is a previously unrecognized risk factor for snoring among adults. Keywords: epidemiology; obesity; smoking; snoring; tobacco
Habitual snoring is a common disorder, with a prevalence of 16 to 33% in men and 8 to 19% in women (1–5). Those who snore suffer from daytime sleepiness (6–8) and commonly disrupt the sleep quality of their bed partner (9). There is an increased risk of cardiovascular diseases (10–13), diabetes (14), and pregnancyinduced hypertension (15) among subjects who snore. These associations are explained at least in part by obstructive sleep apnea syndrome, of which snoring is the cardinal symptom. Snoring is, however, associated with daytime sleepiness even when sleep apnea is absent (16–18). Obesity, upper airway abnormalities, and male sex are the most well-known risk factors for snoring and sleep apnea (19– 24). Smoking has also been associated with habitual snoring (21, 25–27), but this association has been studied in far less detail and is often disregarded in studies of risk factors for snoring and
(Received in original form April 8, 2004; accepted in final form July 5, 2004) Supported financially by the Swedish Heart and Lung Foundation, the Va˚rdal Foundation for Health Care Science and Allergy Research, the Swedish Association Against Asthma and Allergy, the Icelandic Research Council, the Norwegian Research Council project 135773/330, the Norwegian Asthma and Allergy Association, the Danish Lung Association, and the Estonian Science Foundation grant no. 4350. Correspondence and requests for reprints should be addressed to Karl A. Franklin, M.D., Ph.D., Department of Respiratory Medicine, University Hospital, SE-901 85 Umea˚, Sweden. E-mail:
[email protected] Am J Respir Crit Care Med Vol 170. pp 799–803, 2004 Originally Published in Press as DOI: 10.1164/rccm.200404-474OC on July 8, 2004 Internet address: www.atsjournals.org
sleep apnea. We have found no published studies of the possible association of passive smoking and snoring in adults. Our aim was to study the relationship of habitual snoring with active and passive tobacco smoking in a large sample of men and women from five Northern European countries. Some of the results of these studies have been previously reported in the form of an abstract (28).
METHODS Subjects A postal questionnaire was sent to 21,802 randomly selected subjects from Reykjavik in Iceland; Bergen in Norway; Umea˚, Uppsala, and Go¨teborg in Sweden; Aarhus in Denmark; and Tartu in Estonia in 1999– 2001 (29). Subjects who did not respond to the first mailing were sent two reminders. This sample was enrolled in the Respiratory Health in Northern Europe survey, which is a follow-up of subjects who participated in the European Community Respiratory Health Survey 1990–1994 with a response rate of 84% (30). Men and women (20–44 years of age) were randomly selected from the national population registers for 1990, except for participants from Tartu, who were included 4 years later. Local ethics committees at each center approved the study protocols.
Questionnaire and Definitions Loud and disturbing snoring during the last few months was estimated using a five-point scale according to the Basic Nordic Sleep Questionnaire: never, less than once a week, 1–2 nights per week, 3–5 nights per week, and almost every night. Habitual snoring was defined as loud and disturbing snoring at least 3 nights a week (6, 20, 31). Smoking history was categorized as never-smokers, ex-smokers, or current smokers, and the amount of tobacco smoked was assessed in grams per day. One cigarette was equivalent to 1 g of tobacco and one cigar to 5 g. Passive smoking was considered in never-smokers exposed to tobacco smoke at home every day. They were identified from this question: “Does tobacco smoking take place in your present home?” The four alternatives were every day, one to four times per week, one to three times per month, and never. Chronic bronchitis was defined as a negative answer to “Have you ever had asthma?” and as positive answers to all three of the following questions: “Do you usually bring up phlegm, or do you have phlegm on your chest, which you have difficulty bringing up?” “Do you bring up phlegm in this way almost every day for at least 3 months every year?” “Have you had episodes of this kind for at least 2 years in a row?” Obesity was defined as body mass index of 30 kg/m2 or more from self-reported height and weight.
Statistics The analysis was performed using StatView 5.0 and Stata 7.0. Adjusted odds ratios were calculated by logistic regression, whereas adjusted risk ratios were calculated by generalized linear modeling. The adjusted risk ratios and 95% confidence interval were first analyzed on pooled data from all seven centers adjusting for center and then calculated separately at each center. Potential heterogeneity between centers was examined using standard methods for random-effects meta-analysis
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(32). The proportion of snoring that could be explained by different risk factors was calculated as the population attributable risk (PAR), which is the fraction of (incidence in exposed ⫺ incidence in unexposed)/(incidence in exposed) (33). Using Pe for the proportion of exposed and RR for adjusted risk ratio, the formula reads: PAR ⫽ Pe (RR ⫺ 1)/RR.
RESULTS A total of 15,555 subjects answered the questionnaire, including questions on snoring (response rate of 71%). Habitual snoring was reported by 18.3% of the entire population. Age, snoring prevalence, smoking habits, and body mass index are presented in Table 1. Habitual snoring was more prevalent among current smokers (24.0%, p ⬍ 0.0001) and ex-smokers (20.3%, p ⬍ 0.0001) than in never-smokers (13.7%). Snoring was also more prevalent in nonsmoking subjects who were exposed to passive smoking at home on a daily basis than in subjects never exposed to passive smoking in their homes (19.8% and 13.3%, respectively, p ⬍ 0.0001). The prevalence of snoring increased (p ⬍ 0.0001) with the amount of tobacco smoked every day (Figure 1). Active and passive smoking remained independently related to habitual snoring after adjusting for male sex, body mass index, center, and age (Tables 2 and 3). The association between snoring and risk factors was also assessed by meta-analysis. The estimates were similar to those derived when analyzing the pooled data, and no significant center heterogeneity was detected for any of the risk factors related to habitual snoring. Sex Differences
Male sex was an independent predictor of snoring (Table 2). Women had higher odds ratios for the relationship between habitual snoring and smoking than men, and this difference was statistically significant in terms of smoking less than 10 g of tobacco per day (p ⫽ 0.02) and almost significant in terms of smoking 10 or more g of tobacco per day (p ⫽ 0.06).
Figure 1. Snoring prevalence and amount of tobacco smoked every day.
Approximately 20% of the subjects snored habitually in Umea˚, Reykjavik, and Go¨teborg, whereas only 12% snored in Tartu (p ⬍ 0.00001) (Table 1). The frequency of snoring was lower in Tartu than in the other centers, even after adjustments for age, body mass index, smoking, and sex (p ⬍ 0.0001). Current smoking was most common in Bergen, Tartu, and Aarhus (⭓ 35%) and was most seldom reported in Umea˚ and Uppsala (⬍ 20%). Attributable Risk Factors for Snoring
Ever smoking accounted for 17.1% of the attributable risk of habitual snoring and varied between 10.9% and 24.2% at the different centers (Figure 2). Obesity with a body mass index of 30 kg/m2 or more accounted for 4.3% of the attributable risk and varied between 3.1% and 5.0%, whereas the attributable risk of passive smoking was 2.2% (range, 0.8–4.8%). Ever smoking had a higher attributable risk of snoring than obesity at all centers.
DISCUSSION
Chronic Bronchitis
Habitual snoring was significantly more prevalent in the 4.1% of subjects with chronic bronchitis than in subjects without it (34.9% vs. 17.6%, p ⬍ 0.001). The prevalence of snoring in relationship to current smoking and bronchitis is presented in Table 4. Smoking men and women with chronic bronchitis snored habitually in 51% and 24% of cases, respectively. Current smoking and chronic bronchitis were independent and additive risk factors for habitual snoring (Table 5). Geographic Variations
The prevalence of habitual snoring, smoking habits, and the amount of overweight differed between the centers (Table 1).
In this large population survey, active and passive smoking, obesity, and male sex were independent risk factors for habitual snoring. Ever smoking accounted for a high attributable risk of habitual snoring at every center and was around four times higher compared with the attributable risk of obesity. We found, surprisingly, that the exposure to passive smoking at home, a previously unrecognized risk factor, had an attributable risk of habitual snoring at almost the same level as obesity. Most studies focus on sex, overweight, and upper airway abnormalities as risk factors for snoring and sleep apnea. Only a few have recognized smoking as a risk factor for snoring. Two authors reported that current smoking was related to snoring,
TABLE 1. CHARACTERISTICS OF THE POPULATION
Age, yr Women, % BMI, kg/m2 BMI ⭓ 25 kg/m2 BMI ⭓ 30 kg/m2 Ex-smoking Current smoking Passive smoking* Habitual snoring
Reykjavik (n ⫽ 1,827)
Bergen (n ⫽ 2,421)
Umea˚ (n ⫽ 2,579)
Uppsala (n ⫽ 2,479)
Go¨teborg (n ⫽ 2,109)
Aarhus (n ⫽ 2,493)
Tartu (n ⫽ 1,647)
All Subjects (n ⫽ 15,555)
41 ⫾ 7 54.6 25.3 ⫾ 4.0 47.0 11.5 31.5 30.9 11.1 20.6
41 ⫾ 7 51.9 24.7 ⫾ 4.0 41.1 7.9 24.5 38.5 6.3 16.9
41 ⫾ 7 51.5 25.2 ⫾ 3.9 45.2 8.8 26.2 19.2 3.0 20.7
40 ⫾ 7 52.5 24.6 ⫾ 3.9 38.8 6.8 26.1 19.6 2.3 18.6
40 ⫾ 7 54.2 25.0 ⫾ 3.9 45.2 9.6 25.6 29.5 4.4 20.4
39 ⫾ 7 52.2 24.3 ⫾ 4.2 35.2 8.1 23.7 34.6 11.2 17.7
36 ⫾ 7 56.1 24.2 ⫾ 4.2 36.2 9.0 17.1 35.3 13.9 12.0
40 ⫾ 7 52.0 24.8 ⫾ 4.1 41.0 8.7 25.1 29.3 6.7 18.3
Definition of abbreviation: BMI ⫽ body mass index. The values are presented in percentage or as the mean ⫾ SD. * Only calculated among never-smokers.
Franklin, Gı´slason, Omenaas, et al.: Smoking and Habitual Snoring TABLE 2. RISK FACTORS FOR HABITUAL SNORING AND SEX, SMOKING STATUS, AND BODY MASS INDEX Men OR (95% CI) Gender Never smoker Ex-smoker Current smoker ⬍ 10 g/d Current smoker ⭓ 10 g/d BMI ⬍ 20 kg/m2 BMI 20–25 kg/m2 BMI 25–30 kg/m2 BMI ⬎ 30 kg/m2
2.4 (2.1–2.6) 1 1.6 (1.4–1.9) 1.5 (1.3–1.8) 2.3 (2.0–2.7) 0.8 (0.5–1.2) 1 2.0 (1.8–2.3) 4.2 (3.5–5.1)
Women OR (95% CI)
1.2 2.1 3.0 0.8 2.4 4.7
1 1 (1.0–1.5) (1.7–2.6) (2.5–3.7) (0.6–1.0) 1 (2.0–2.8) (3.8–5.8)
All OR (95% CI) 1 (1.3–1.6) (1.5–2.0) (2.3–2.9) (0.6–0.9) 1 2.1 (1.9–2.4) 4.4 (3.9–5.1) 1.4 1.8 2.6 0.7
Definition of abbreviations: BMI ⫽ body mass index; CI ⫽ confidence interval; OR ⫽ odds ratio. The results are adjusted for center and age and are presented as adjusted ORs and with 95% CIs (n ⫽ 14,216).
but ex-smoking was not (21, 25). Another two studies reported that ex-smoking was also related to snoring (26, 27). We found that current smoking, ex-smoking, and passive smoking are all major risk factors for habitual snoring. The snoring frequency increased with the amount of tobacco smoked and with the exposure to passive smoking, which further supports the hypothesis that smoking induces snoring. The odds ratio for obesity was higher than for smoking, but smoking was more prevalent than obesity in this population; this explains why smoking had a higher attributable risk and was a more common cause of snoring than obesity in this sample. The attributable risk of obesity is dependent to some extent on the threshold used for obesity. If obesity is defined as having a body mass index of 28 kg/m2 or more instead of 30 kg/m2 or more, the attributable risk increases from 4.3–8%, which is still well below the 17% of ever smoking. There is strong evidence that current smoking is related to snoring, as our findings support the findings in four previous studies. It is also evident that former smoking is related to snoring, as our study supports the findings of Hu and colleagues, which is the largest study on snoring to date (27). The association of snoring and passive smoking among adults is a novel finding and has previously only been reported in children (34, 35). The interaction between tobacco exposure and snoring is not clear. It has been suggested that it emanates from irritation and inflammatory changes in the upper airways (26, 36). Wetter and colleagues suggested that nicotine withdrawal during sleep in those who smoke might lead to sleep instability, which in turn predisposes to upper airway obstruction (25). Larsson and colleagues found an increased prevalence of snoring and obstructive
TABLE 3. THE INDEPENDENT RISK OF SNORING CAUSED BY PASSIVE SMOKING AT HOME IN NEVER-SMOKERS (N ⫽ 6,501), ADJUSTED FOR CENTER, AGE, AND BODY MASS INDEX Amount of Passive Smoking at Home None One to three times per month One to four times per week Every day
Men
Women
801 TABLE 4. PREVALENCE OF HABITUAL SNORING IN RELATION TO CURRENT SMOKING AND CHRONIC BRONCHITIS IN MEN AND WOMEN Prevalence of Habitual Snoring Smoking
Bronchitis
Men
Women
All
No No Yes Yes
23.2 28.5 39.7 50.8
8.9 17.2 20.8 23.8
15.5 22.6 30.5 39.0
No Yes No Yes
sleep apnea among patients with chronic bronchitis (37). They speculated that inflammatory airway swelling affects the upper airways in subjects with chronic bronchitis and, together with increased sputum production, contributes to increased upper airway resistance (38). Lin and Lin found an increased prevalence of bronchial hyperresponsiveness in subjects with obstructive sleep apnea, which was reduced by nasal continuous positive airway pressure therapy (39). Sanders and colleagues did, however, recently report that mild obstructive airway disease in a large community sample was not associated with sleep apnea (40). We found that chronic bronchitis and current smoking were independent and additive risk factors for snoring. We also found that current smoking was more common than chronic bronchitis. Our findings support the hypothesis that smoking contributes to snoring, independent of chronic inflammation of the upper airways. Abstinence from nicotine during sleep is one possible explanation. We observed that women who smoke ran a relatively higher risk of snoring than men who smoke. This is in line with a study reporting that women are more likely than men to develop bronchial hyperresponsiveness and respiratory symptoms when exposed to tobacco smoke (41). One study reported that the upper airway size was correlated to the severity of obstructive sleep apnea in men, but not in women (42). It is possible that structural changes in the upper airways are more important in the pathogenesis of snoring in men and that functional airway changes are more important in women. Ng and colleagues reported marked ethnic differences in snoring frequency in Singapore, where 10.9% of Indian subjects snored compared with 6.2% of Chinese (43). We found a marked geographic difference in snoring frequency, ranging from 12% in Tartu to 21% in Reykjavik and Umea˚, despite the fact that almost every subject was white. The differences still remained when controlling for age, smoking habits, and obesity. This is the first study that investigates snoring frequency in large populations from different countries. We found that geographic differences in this study were of the same magnitude as the ethnic differences reported in a study by Ng and colleagues (43). The impact of obesity and smoking habits on snoring frequency also
TABLE 5. RISK OF SNORING IN CURRENT SMOKERS AND SUBJECTS WITH CHRONIC BRONCHITIS Snoring Habitually
All
1
1
1
0.7 (0.5–1.0)
1.1 (0.7–1.7)
0.8 (0.6–1.1)
0.7 (0.4–1.5) 1.7 (1.2–2.4)
1.7 (0.7–3.8) 1.6 (1.0–2.5)
1.0 (0.6–1.7) 1.6 (1.2–2.1)
The results are presented as adjusted odds ratios with 95% confidence intervals.
Smoking No Yes No Yes
Bronchitis
Men
Women
All
No No Yes Yes
1 1.4 (1.3–1.6) 2.1 (1.5–3.0) 4.0 (2.9–5.5)
1 2.4 (2.0–2.8) 2.4 (1.6–3.7) 3.6 (2.3–5.4)
1 1.8 (1.6–1.9) 2.2 (1.7–2.9) 3.9 (3.0–5.0)
The results are adjusted for age, sex, and body mass index and are presented as adjusted odds ratios with 95% confidence intervals.
802
AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 170 2004 man E, Olin A-C, Ryde´n E, Spetz-Nystro¨m U, Stenudd Cashelunge K, Svanes C, So¨derberg M, Talvik J, Tunsa¨ter A, and Wieslander G.
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Figure 2. Population-attributable risk factors for snoring. Passive smoking was only calculated in never-smokers.
varied at different centers. We hypothesize that geographic and perhaps also ethnic differences are explained not only by different living conditions, that is, food, economy, smoking habits and so on, but also by differences in sensitivity to these varied living conditions. Unfortunately, we did not ask about alcohol consumption, which is a limitation of this study. It is likely that smokers drink more than others, and snoring is probably induced or worsened under the influence of alcohol (44). Alcohol consumption estimated by questionnaires and ␥-glutamyl transpeptidase was, however, not related to a history of snoring in a survey of middleaged men (26). It is possible that alcohol has an immediate effect on snoring, but alcohol consumption does not appear to affect the snoring frequency in a population. Self-reported risk factors and outcomes from a questionnaire, as in the present survey, are inherently less reliable than those measured directly. The reporting bias of smoking and/or snoring based on cultural norms in different populations is one example. The cross-sectional design provides no temporal relationship and weakens the causality. The follow-up was good, with a response rate of 71%, but there is still a risk of bias related to incomplete follow-up. In conclusion, both current smoking and ex-smoking are major contributory factors when it comes to habitual snoring in the general population. Passive smoking is a previously unrecognized risk factor for snoring among adults. Smoking history is important, and advice on smoking cessation should be given to patients seeking medical attention for habitual snoring and sleep apnea. Conflict of Interest Statement: K.A.F. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; T.G. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; E.O. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; R.J. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; E.J.J. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript, E.L. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; M.G. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; L.N. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; B.N.L. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; E.B. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; K.T. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript; C.J. does not have a financial relationship with a commercial entity that has an interest in the subject of this manuscript. Acknowledgment : The following scientists in the Rhine study group are acknowledged for helpful contributions: Blo¨ndal T, Bjo¨rnsdottir US, Boman G, Forsberg B, Gislason D, Gulsvik A, Ledin M-C, Lillienberg L, Lundba¨ck B, Norba¨ck D, Norr-
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