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(Chest. 2004;125:127-134.)
© 2004 American College of Chest Physicians

A Community Study of Sleep-Disordered Breathing in Middle-Aged Chinese Women in Hong Kong*

Prevalence and Gender Differences

Mary S. M. Ip, MD, FCCP; Bing Lam, MRCP, FCCP; Lawrence C. H. Tang, MD; Ian J. Lauder, PhD; Toi Yan Ip, MPhil and Wah Kit Lam, MD, FCCP

* From the Departments of Medicine (Drs. M.S.M. Ip, B. Lam, W.K. Lam and Ms. T.Y. Ip) and Statistics and Actuarial Science (Dr. Lauder), The University of Hong Kong; and Department of Obstetrics and Gynecology (Dr. Tang), Kwong Wah Hospital, Hong Kong, SAR, China.

Correspondence to: Mary S. M. Ip, MD, FCCP, Department of Medicine, The University of Hong Kong, 4/F, Professorial Block, Queen Mary Hospital, Pokfulam Rd, Hong Kong, SAR, China; e-mail: msmip{at}hkucc.hku.hk


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: To investigate the prevalence of sleep-disordered breathing (SDB) and obstructive sleep apnea syndrome (OSAS) in community-based, middle-aged Chinese women, and to compare the differences between gender with a similar study in men.

Design: A cross-sectional study conducted in Hong Kong from 1998 to 2000.

Setting: Sleep questionnaires were distributed to women (30 to 60 years old) in three offices and two community centers. All were invited to undergo full polysomnography in a sleep laboratory.

Participants: Questionnaires were distributed to 1,532 women, and 854 questionnaires were returned. Polysomnography was conducted in 106 respondents.

Measurements and results: Conservative estimated prevalence of SDB (apnea-hypopnea index [AHI] >= 5) and OSAS (AHI >= 5 plus excessive daytime sleepiness [EDS]) were 3.7% and 2.1%, respectively. Age-specific prevalence of OSAS was 0.5%, 2.2%, and 6.1% in the 30- to 39-year-old, 40- to 49-year-old, and 50- to 60-year-old age groups, respectively. Stepwise multiple logistic regression analysis identified body mass index (BMI) and age as predictors of SDB. Compared to Chinese men, the prevalence of SDB and OSAS in women was lower, but the gender difference decreased with age. The AHI of affected women was also significantly lower despite comparable BMI. Compared to men, women with SDB had same degree of self-reported snoring and a similar degree of EDS despite the lower AHI.

Conclusions: This study demonstrated an estimated prevalence of OSAS at 2.1% among middle-aged Chinese women in Hong Kong, with a 12-fold rise from the fourth to the sixth decade of life. BMI and age were significant independent predictors of SDB. Compared to men, women with SDB had lower AHIs, despite similar BMIs.

Key Words: middle-aged Chinese women • polysomnography • sleep apnea


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Obstructive sleep apnea has long been observed in clinical practice to be more common in men,1 2 3 although it has been documented in population studies4 5 6 that the male dominance of sleep-disordered breathing (SDB) may not be as high, suggesting an underpresentation and/or underrecognition of this problem in women in the clinic population. SDB may also have different prevalence and risk factors in different communities and ethnic groups. We have previously reported that 4.1% of middle-aged Chinese men in a community cohort of office workers in Hong Kong had symptomatic obstructive sleep apnea.7 In this article, we report the prevalence of SDB in a community-based population of women aged 30 to 60 years, and compare their demographic, anthropometric, and clinical features with those of male counterparts.7


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
This study was performed in Hong Kong. Data were collected from July 1998 to November 2000. The study protocol has been previously described in the report on SDB prevalence in middle-aged men.7 Briefly, community-based subjects were approached with a questionnaire, and were also invited to undergo polysomnography. Anthropometric measurements and BP were measured, and blood for fasting lipids and glucose testing was obtained (results on analysis of these data will be separately presented). Interpretation of sleep studies and assessment of daytime sleepiness were all made similarly. The study was approved by the Ethics Committee of The University of Hong Kong.

Sample
The target population was women 30 to 60 years old in the community. Questionnaires (modified from National Auxillary Publications Services document No. 050174 ), similar to that used in a study of men, with addition of questions on menopause and hormone replacement therapy, were distributed to the office staff of three public institutions, and to visitors of two community centers in Hong Kong. The public institutions were government departments for non-health-related functions, while the community centers were operated by nongovernment organizations that provided a variety of welfare activities for the community.

Collection of Polysomnographic Data
Studies were conducted at the sleep laboratory at Queen Mary Hospital. Polysomnography (Alice 3 System; Respironics, Pittsburgh, PA), consisting of continuous polygraphic recording from surface leads for EEG, electrooculography, electromyography (chin and legs), ECG, thermistors for nasal and oral airflow, thoracic and abdominal impedance belts for respiratory effort, pulse oximetry for oxyhemoglobin level, tracheal microphone for snoring, and sensors for sleep position.

Interpretation of Polysomnographic Data
Polysomnographic records were scored manually. Sleep data were scored according to standard criteria.8 An abnormal breathing event during objectively measured sleep was defined in the same way as the study in men7 for the benefit of comparability, according to the criteria of either a complete cessation of airflow lasting >= 10 s (apnea) or a discernible reduction in airflow accompanied by a decrease of >= 4% in oxyhemoglobin saturation (hypopnea). The average number of episodes of apnea and hypopnea per hour of sleep (apnea-hypopnea index [AHI]) was calculated as the summary measurement of SDB. Arousals were identified according to established criteria.9

Assessment of Daytime Sleepiness
Daytime sleepiness was assessed with four subjective questions. Using a 5-point scale (0 to 4), the subjects rated the following: how often they felt excessively sleepy during the daytime; how often they felt unrefreshed or tired during the day, regardless of how long they had slept; how often they fell asleep or dozed off momentarily while watching television, reading, or at meeting/church; and how often they felt sleepy while driving. The answer was considered positive if the score was >= 2. Subjects were identified as having excessive daytime sleepiness (EDS) if they gave a positive response to three of the four questions.

Definition of SDB and Obstructive Sleep Apnea Syndrome
The minimum criterion for SDB was AHI >= 5, and data for three AHI cutoff threshold values at 5, 10, and 15, respectively, are presented. Similarly, the minimum criterion for diagnosis of obstructive sleep apnea syndrome (OSAS) was AHI >= 5 in the presence of EDS (as defined by the questions above), and data for three cutoff AHI values are presented.

Calculation of Prevalence
This was calculated as previously described.7 Briefly, questionnaire respondents were classified as habitual snorers and nonhabitual snorers based on self-reported symptoms. Within each group, the age and body mass index (BMI) of those who underwent polysomnography and those who did not were compared. If significant differences were found, a conservative estimate was adopted, treating the subjects with SDB documented by polysomnography as the only subjects with SDB in the entire corresponding questionnaire group. The overall prevalence of SDB in the entire cohort would be calculated as follows: (estimated No. of subjects with SDB among snorers and nonsnorers)/(total No. of questionnaire respondents) x 100%.

Age-adjusted and BMI-adjusted prevalence rates were calculated by categorizing subjects into three age groups (30 to 39 years, 40 to 49 years, 50 to 60 years) and whether their BMIs were < 23 and >= 23, where 23 is the recently proposed threshold BMI value for overweight Asians.10

Statistical Analysis
Descriptive statistics were used to summarize subject characteristics and questionnaire data. Comparison between groups was done with the Student t test (two sided) for continuous variables and {chi}2 test for discrete variables; p < 0.05 was considered statistically significant. To adjust the effect of various factors on the likelihood of snoring and SDB developing, multiple logistic regression analysis was employed. This analysis included all variables that were found to be significant in the respective between-group comparisons (Tables 1 , 2 ). Stepwise logistic regression was used to determine the principal covariates affecting SDB. Comparison of anthropometric parameters, polysomnography data, and symptoms were compared between subjects in this study and their male counterparts in the previous reported study.7


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  		Table 1.. Different Features Between Snorers and Nonsnorers*

 

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  		Table 2.. Correlates of SDB*

 
Data from both men and women were pooled for analysis of the association of SDB with obesity, reflected by body habitus parameters. Using multiple logistic regression, a separate model was fitted for each measure of body habitus because of multicollinearity. Age and sex were included in all the models. Furthermore, the risks of SDB associated with an increment of 1 SD in body habitus parameters were calculated,4 and the odds ratios (ORs) and their 95% confidence intervals (CIs) were compared between this Chinese population and that reported in white subjects.4 All analyses were done with the SPSS package (release 10.0 for Windows; SPSS; Chicago; IL).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Questionnaire Data
Questionnaires were distributed to 1,532 women, and 854 were returned (56%); 839 completed questionnaires were analyzed. The questionnaire respondents had age distribution and corresponding BMIs that were similar to that of the general community.11 12 Their demographics, sleep-related symptoms, and medical history are shown in Table 1 . Eighty-one percent were in the working population, of whom a vast majority were office workers with a secondary education level.

The percentage of self-reported habitual snorers was 15%, and the mean age, BMI, and features suggestive of sleep apnea were significantly higher among habitual snorers (Table 1) . Both habitual snorers and nonhabitual snorers showed significant difference in BMI between subjects who came for polysomnography and those who did not (snorers, p = 0.046; nonsnorers, p < 0.001). Stepwise logistic regression identified history of hypertension, witnessed breathing irregularity, nasal congestion at night, BMI, and leg movements during sleep as significant correlates of habitual snoring.

Polysomnographic Data
One hundred six questionnaire respondents came for polysomnography. Ten subjects were receiving antihypertensive medications and/or antidiabetic medications, 3 subjects took sedatives/hypnotics more than five times a month, and 6 subjects were receiving miscellaneous medications, including nasal steroids, antihistamines, antiulcer drugs, and thyroxine replacement.

Of the 106 polysomnographic evaluations, 1 was rejected due to a technical fault in the recording. The distribution of sleep stages of the polysomnography-positive (AHI >= 5) and polysomnography-negative groups were similar, but those with AHI >= 5 had more snoring (p = 0.001).

Prevalence of SDB and OSAS
Among the 105 patients who underwent polysomnography, 31 subjects (30%), 16 subjects (15%), and 10 subjects (10%) had AHIs >= 5, >= 10, and >= 15, respectively. Due to the significant difference in BMI of the subjects who came for polysomnography and those who did not, the projection of the prevalence of SDB was based on the conservative estimate (ie, assuming no subject in the no-polysomnography group would have SDB). Since the age distribution and BMI of the questionnaire respondents were similar to those of the general middle-aged female population (30 to 60 years old) in Hong Kong, it would be acceptable to use the questionnaire respondents as the denominator of evaluation. Hence, the estimated prevalence of OSAS in the entire female cohort 30 to 60 years old would be 2.1% (Fig 1 ), with the age-specific prevalence of OSAS rising from 0.5 to 6.1% (Fig 2 ). At various cutoff points of AHI, estimated prevalence of SDB and OSAS were, respectively, 3.7% and 2.1% (AHI >= 5), 1.9% and 1.4% (AHI >= 10), and 1.2% and 0.8% (AHI >= 15) [Fig 1 ].



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  		Figure 1.. Prevalence rates using various cutoff points for AHI. SDB is defined as AHI >= 5, >= 10, or >= 15. OSAS is defined as EDS plus AHI >= 5, >= 10, or >= 15.

 


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  		Figure 2.. Age-specific prevalence rates of SDB (AHI >= 5) and OSAS (AHI >= 5 and EDS) in women.

 
Factors Associated With SDB
The significant correlates of SDB in the polysomnography subjects are shown in Table 2 . Age, BMI, neck circumference, waist circumference, hip girth, BP measurements, and menopause status correlated with AHI, but not EDS. Stepwise logistic regression selected and retained BMI and age as the principal covariates.

Figure 2 shows the age-specific prevalence of SDB and OSAS in the target population. An increasing trend for SDB and OSAS with age was present, and this was seen in subjects with BMI < 23 and BMI >= 23 (Table 3 ). The prevalence of both SDB and OSAS in subjects 50 to 60 years old was markedly higher than in subjects 30 to 39 years old, in both the normal weight and overweight subjects (Table 3) .


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  		Table 3.. Prevalence of SDB and OSAS in Different Age and BMI Groups

 
Table 4 shows the ORs estimating the increased risk of SDB associated with an increment of 1 SD in the value of the specific measure of body habitus for obesity, using pooled data of men and women, compared to that of a previous study in white subjects.4 The intervals overlapped for all covariates apart from waist-hip ratio. Thus the OR for this covariate was regarded as significantly different (p < 0.05).


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  		Table 4.. Relative Risks for SDB and Measures of Body Habitus*

 
Comparison of Men and Women
Figure 3 shows the total and age-specific prevalence of OSAS of men and women. Women had a lower prevalence than men across all age groups, although the difference between the two sexes was much larger in the 30- to 39-year-old age group compared to the 50- to 60-year-old age group.



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  		Figure 3.. Age-specific prevalence rates of OSAS (AHI >= 5 and EDS) in middle-aged Chinese men and women.

 
The mean AHIs of women with SDB (Fig 4 ) were lower than those of the men as a total and in corresponding age groups, despite similar BMIs (Fig 5 ). Compared to men, women had relatively higher rapid eye movement (REM)-AHI in proportion to their total AHI: total AHI in women, 12.8 ± 8.1 (mean ± SD); REM-AHI, 22.4 ± 15.1; total AHI in men, 21.7 ± 14.9; REM-AHI, 26.3 ± 18.6. In terms of symptoms, women and men with SDB had the same degree of self-reported snoring (women, 45%; men, 61%; not significant) and similar degree of daytime sleepiness as represented by Epworth sleepiness scale (women,10.1 ± 5.1; men, 9.8 ± 4.4).



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  		Figure 4.. AHI in men and women with SDB in different age groups.

 


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  		Figure 5.. BMI in men and women with SDB in different age groups.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
In this community-based study of the prevalence of SDB among middle-aged women assessed by complete polysomnography, we conservatively estimate that approximately 3.7% of this cohort had SDB at AHI >= 5, and 2.1% were symptomatic with daytime sleepiness. SDB among women has received growing recognition in recent years. Population studies4 5 have demonstrated a prevalence of symptomatic obstructive sleep apnea of 1 to 2% among middle-aged white women. Our study presents the first data of SDB and OSAS in a Chinese community based on polysomnographic documentation.

This study, very similar in design to that of the study7 in men, has a similar limitation of potential bias introduced by the partial questionnaire response rate and restricted polysomnography participation rate. However, the questionnaire respondents had an age distribution within the target age strata and age-specific BMIs similar to those of the local population, allowing the results to be projected to the general population. The proportion of office workers in this study sample was higher than that of the general population in the same age strata. The effect of occupation or educational level on the prevalence of sleep apnea has not been well reported. These factors might affect the occurrence of SDB indirectly, through lifestyle and behavioral patterns that in turn influence body weight control. Since the average BMI of study subjects was similar to that of the general population, these differences in demographics probably would not affect the validity of generalization of the prevalence data to the community at large.

Medications such as sedatives, tricyclic antidepressants, and stimulant drugs may alter sleep architecture and occurrence of SDB. A number of drugs, including sedatives, antidepressants, antihistamines, and lipophilic ß-blockers, may result in daytime sleepiness that confounds the symptoms of sleep apnea. Drug effect was unlikely to have affected the findings in this study, as there was no significant difference in the frequency of the use of these drugs between subjects with and without SDB/OSAS.

Since the polysomnography participants had many more associated features of SDB than those who did not undergo polysomnography, we have adopted the conservative estimate of prevalence, assuming that all those who did not undergo polysomnography did not have SDB. This is likely to result in some underestimation of the prevalence.

The estimated prevalence of OSAS at 2.1% in Chinese women 30 to 60 years old is similar to that of studies4 6 of white subjects utilizing similar diagnostic criteria. It is also comparable to that of a study13 in Asian women in Singapore utilizing a diagnostic triad of self-reported snoring, sleep symptoms of apnea/hypopnea, and/or hypertension/wide neck circumference that arrived at an estimated SDB prevalence of 2.3% in female subjects 40 to 59 years old.

As in men, higher BMI and advancing age were predictive of the presence of SDB in women. The prevalence of OSAS increased nearly 12-fold in the 50- to 60-year-old group, compared to the 30- to 39-year-old group. Although men also showed increasing prevalence with age, the escalation in the sixth decade was much less marked. It also appeared that within this middle-aged population, younger men and women with SDB were more obese than those who were in their fifties. This may reflect an increasing influence of advancing age on the development of SDB as found in other studies14 that focus on elderly population. Since women have a distinct change in hormonal status relating to menopause, which corresponds temporally to age, it is tempting to speculate that this increase in prevalence of SDB, despite a lower BMI, may be related to menopause. However, there were not enough women above or below the age threshold of 50 years with different menopause status in our study population, and analysis of the prevalence of OSAS in relation to menopausal status independent of age was not possible. It has also been reported that prevalence of SDB in postmenopausal women receiving hormonal replacement therapy was similar to that of premenopausal women,15 but again there were too few women receiving hormonal replacement therapy in this study population to make any meaningful analysis. Although the prevalence of SDB increased with age, the group mean AHI across the 3 decades was similar, which differed from the finding of higher AHI in postmenopausal women in a previous study.16

Obesity is a significant risk factor for SDB in white populations.4 6 17 18 In this study in women and the previous study7 in men, higher BMI is a major risk factor for SDB in Chinese subjects as well. Using the definition of BMI >= 23 in Asians as the overweight threshold,10 our subjects with SDB, whose mean BMI was 27, were definitely obese by peer comparison. In comparison with white subjects in the Wisconsin study,4 Chinese subjects had a lower risk attributable to central obesity, as indicated by the significant difference in the waist:hip ratios, and a pattern of lower risks relating to other obesity indexes such as BMI, neck circumference, and subcutaneous fat. This finding supports the notion that risk factors apart from obesity, such as craniofacial structure,19 may be of greater pathogenic importance in Chinese compared to white populations.

Apart from a lower prevalence of SDB in women, gender differences in features of OSA have been reported in studies20 21 22 of white subjects. Consistent with other data, our study showed that the severity of SDB as indicated by AHI in Chinese women was mostly in the mild range. The overall male:female ratio for OSAS was 2:1, but increased from 1.3:1 in the group with mild OSA (AHI >= 5 to 15) to 9:1 in the group with severe OSA (AHI >= 30) [data not shown]. It is also observed that women with SDB had lower AHIs compared to male counterparts despite a highly comparable BMIs between men and women. Similar to a previous Canadian study,20 AHI during REM sleep relative to the total AHI was higher in women, although this may just reflect that women had less severe obstructive sleep apnea.

The Wisconsin Sleep Cohort Study23 reported that white women with SDB had similar symptoms as those of men. In our study, Chinese women with SDB had a similar degree of snoring and daytime sleepiness as men. The gender disparity of SDB in the clinical setting24 and this community study suggests that SDB is underrecognized in women, despite similar symptoms as those in men.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
To the best of our knowledge, this is the first report of prevalence of OSAS in middle-aged Chinese women using full overnight polysomnography. The study demonstrated that symptomatic OSAS affects at least 2.1% of this community-based population between 30 years and 60 years old, and prevalence increases markedly in the sixth decade of life. BMI and age were significant predictors of SDB. Compared to their male counterparts, the overall severity of SDB, as indicated by AHI in women, was significantly lower, despite comparable BMI. Women also had a similar degree of daytime sleepiness as male counterparts, despite lower AHI. Compared to white subjects, the relative risks of acquiring SDB in Chinese middle-aged subjects conferred by obesity is probably less.


   Acknowledgements
 
The authors thank Ms. Wendy Mok for assistance in statistical analysis. We also gratefully acknowledge the institutions and the community centers for allowing us to invite their staff/attendees to participate in the study.


   Footnotes
 
Abbreviations: AHI = apnea-hypopnea index; BMI = body mass index; CI = confidence interval; EDS = excessive daytime sleepiness; OR = odds ratio; OSAS = obstructive sleep apnea syndrome; REM = rapid eye movement; SDB = sleep-disordered breathing

This study was supported by the Competitive Earmarked Research Grant No. HKU457/96M from the Hong Kong Research Grants Council, Hong Kong.

Received for publication March 19, 2003. Accepted for publication August 20, 2003.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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