Annals of Medicine, 2015; Early Online: 1–5 © 2015 Informa UK, Ltd. ISSN 0785-3890 print/ISSN 1365-2060 online DOI: 10.3109/07853890.2015.1015601

ORIGINAL ARTICLE

Associations between sleep disturbances and diabetes mellitus among blacks with metabolic syndrome: Results from the Metabolic Syndrome Outcome Study (MetSO) Alberto R. Ramos1, Douglas M. Wallace1, Seithikurippu Ratnas Pandi-Perumal2, Natasha J. Williams2, Chimene Castor3, Mary Ann Sevick2, Samy I. Mcfarlane4 & Girardin Jean-Louis2 Ann Med Downloaded from informahealthcare.com by Kainan University on 04/25/15 For personal use only.

1Department of Neurology, Miller School of Medicine, University of Miami, Miami, FL, USA, 2Center for Healthful Behavior Change (CHBC),

Division of Health and Behavior, Department of Population Health, NYU Langone Medical Center, New York, USA, 3Department of Nutritional Sciences, Howard University, Washington, DC, USA, and 4Department of Medicine, State University of New York, Downstate Medical Center, New York, USA

Abstract Introduction. The association between sleep disturbances and cardiometabolic diseases has been understudied in blacks with metabolic syndrome. Methods. This study is a cross-sectional analysis of the Metabolic Syndrome Outcome Study (MetSO) trial. We assessed insomnia symptoms, sleep duration, and risk for sleep apnea. Multivariate logistic regression models evaluated the association between sleep disturbances with diabetes mellitus (DM) and the combined outcomes of DM and hypertension as well as DM and dyslipidemia. Results. The sample consisted of 1,013 participants, mean age of 62 ⴞ 14 years and 61% female. DM was diagnosed in 60% of the sample. Sleep apnea risk was observed in 48% of the sample, while 10% had insomnia symptoms and 65% reported short sleep duration (⬍ 6 hours). Sleep apnea risk, but not insomnia or sleep duration, was associated with DM (OR 1.66; 95% CI 1.21–2.28), adjusting for age, sex, income, obesity (BMI ⱖ 30 kg/m2), tobacco use, alcohol use, hypertension, dyslipidemia, and depression. In fully adjusted models, sleep apnea risk was associated with the combined outcome of DM–hypertension (OR 1.95; 95% CI 1.42–2.69), but not with diabetes–dyslipidemia. Conclusion. We observed a strong association between sleep apnea risk and diabetes mellitus among blacks with metabolic syndrome. Key words: Black race/ethnicity, diabetes mellitus, metabolic syndrome, sleep apnea

Introduction Sleep apnea is a chronic condition and major public health problem that affects over 18 million adults in the United States (1,2). It is characterized by episodes of partial (hypopnea) or complete upper airway collapse (apnea) during sleep, leading to hypoxemia and sleep fragmentation (2). The high prevalence of insulin resistance, type 2 diabetes (T2DM), and cardiovascular diseases

Key messages • Sleep apnea risk, but not insomnia or sleep duration, was associated with diabetes mellitus in blacks with metabolic syndrome. • Unrecognized sleep apnea, rather than short sleep duration or insomnia, may contribute to the increased cardiometabolic risk in this vulnerable population.

(CVDs) among those with obstructive sleep apnea suggests a strong association among these medical conditions. Sleep apnea has received increasing attention during the last decade due to its independent associations with CVDs (2), the leading cause of death in most ethnicities in the United States. In addition, excessive daytime sleepiness (EDS), resulting from sleep apnea, is detrimental to mood, job performance, and increases occupational injuries and transportation-related accidents (3). Non-Hispanic blacks have a high prevalence of cardiometabolic diseases such as T2DM, hypertension, and obesity (4), but there is a paucity of data on the associations between sleep disruption and cardiometabolic disease risk factors in this population. There are race/ethnic differences in the prevalence of sleep apnea (5,6). Several population-based and clinical studies have shown increased risk of sleep apnea among non-Hispanic blacks (herein referred to as blacks), when compared to nonHispanic whites (herein referred to as whites), after controlling for age, gender, and obesity (5–7). For example, in a sample of community-dwelling blacks from the Jackson Heart Study, symptoms of snoring were reported by 66.3% of men and 58% of women, while daytime sleepiness was reported by 68.6% of men and 61.4% of women (8,9). The Cleveland Family Study demonstrated a higher frequency of sleep apnea in black (31%) compared to white (10%) participants (6).

Correspondence: Alberto Ramos, MD, MSPH, FAASM, Co-Director, UHealth Sleep Medicine Program, Assistant Professor of Neurology, University of Miami Miller School of Medicine, University of Miami, Miami, FL, USA. Fax: ⫹ 1-305-243-5403. E-mail: [email protected] (Received 28 November 2014; accepted 25 January 2015)

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In addition, short (ⱕ 5–6 hours) and long sleep (ⱖ 8–9 hours) durations are associated with increased mortality (9) and cardiometabolic diseases such as obesity, T2DM, and hypertension (10–12). Similar to sleep apnea, there are race/ethnic differences in sleep duration, with blacks consistently reporting shorter and longer sleep durations, relative to whites (13–16). However, available studies have not accounted for the confounding effects of sleep apnea. Type 2 diabetes mellitus affected more than 25 million people, caused over 71,000 deaths in 2007 in the United States, and disproportionately affected minority populations (17,18). Similar to sleep apnea and short or long sleep durations, population-based and clinical studies have consistently shown that blacks are twice as likely to be diagnosed with diabetes as their white counterparts, but the determinants of these disparities are not fully understood (4). Therefore, characterizing and understanding the risk of sleep apnea, short or long sleep durations, and insomnia symptoms in this high-risk population is important as sleep disruption is modifiable. Accumulating evidence from epidemiological and clinical studies, involving diverse populations, suggests that markers of sleep disruption are also independent risk factors for cardiometabolic diseases among adults. Thus, it is important to assess the associations between sleep disruption and cardiometabolic diseases, in a population at high risk for cardiovascular disease. In a prior analysis of this cohort, increased risk for sleep apnea had a strong association with resistant hypertension (8). The current analysis aims to expand further the associations with cardiometabolic diseases by evaluating sleep disturbances (sleep apnea risk, sleep duration, and insomnia symptoms) with T2DM to diabetes mellitus in an outpatient-based sample of blacks with metabolic syndrome. Our hypothesis was that sleep apnea risk, short and long sleep durations, and insomnia symptoms were primarily associated with T2DM. Furthermore, we explored associations between sleep disturbances and extreme cardiometabolic phenotypes, by combining the diagnosis of T2DM and hypertension, as well as diabetes and dyslipidemia as secondary outcomes.

Methods Population The Metabolic Syndrome Outcome (MetSO) Study (19) is a wellcharacterized registry of over 1,013 black participants, 60% of whom being of Caribbean origin, with cardiometabolic diseases (20). Briefly, MetSO was conducted to increase access for at-risk minority participants into clinical research and intervention programs. Eligible participants were adults (ⱖ 18 years old) with self-reported race/ethnicity as black/African American, with the diagnosis of metabolic syndrome (MetS), and who completed the Apnea Risk Evaluation System (ARES™) Questionnaire (19,20).

Outcomes: diabetes mellitus, hypertension, and dyslipidemia The main outcome was the physician’s rendered diagnosis of T2DM according to the criteria of the American Diabetes Association (21). Clinical data include measures of body mass index (BMI), blood pressure (BP), cholesterol high density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides, and fasting plasma glucose (FPG) or hemoglobin (HbA1c) for those who have a diagnosis of T2DM. History of depression and tobacco and alcohol use was based on the participant’s self-report and the clinical information obtained from the electronic medical records from four outpatient clinics associated with SUNY Downstate Medical Center. All data and measurements were collected by trained clinical research staff (19).

Weight was measured without shoes and using a validated digital scale. Waist circumference was measured at the end of normal expiration by locating the upper hip bone and the top of the right iliac crest and placing the measuring tape horizontally around the abdomen at the level of the iliac crest. Blood pressure (BP) measurements were taken following American Heart Association guidelines using a BPTru automated BP monitors. The HDL- and total cholesterol levels were obtained according to the National Cholesterol Education Program standard guidelines for total cholesterol measurement (19).

Primary exposure: risk for sleep apnea, sleep duration, and insomnia symptoms The Apnea Risk Evaluation System (ARES™) Questionnaire was used to identify those at high risk for sleep apnea (22). In summary, ARES™ asks for demographic and anthropometric data, diseases associated with increased risk for sleep apnea (i.e. hypertension, diabetes mellitus), or prior diagnosis of sleep apnea and includes the Epworth Sleepiness Scale. The Epworth Sleepiness Scale (ESS) asks individuals to characterize the likelihood of dozing during eight everyday activities and has become the most widely used measure for assessing sleepiness in clinical practice and research. Daytime sleepiness was categorized as the sum score of ⱖ 10 based on the established definition (23). The ARES™ has a sensitivity of 0.94, specificity of 0.79, positive predictive value of 0.91, and negative predictive value of 0.86. Sleep duration was based on the participants’ estimated habitual sleep time (sleep duration) with the question: ‘In the last 24 hours, how much sleep did you get?’ Sleep duration was recorded in 1-hour increments and categorized into short sleep (⬍ 6 hours), average sleep (6–8 hours), and long sleep (⬎ 8 hours) duration based on prior definitions (15). Insomnia symptoms were assessed with the following three questions: ‘Do you have difficulty falling asleep?’ (Difficulty falling asleep); ‘Do you have difficulty staying asleep?’ (Difficulty maintaining sleep); ‘Do you wake up earlier in the morning than you mean to?’ Information on sleep medicine use and naps during the day was also obtained (19). The Institution Review Board at New York University and SUNY Downstate Medical Center approved this study. All participants provided informed consent prior to enrollment into the study.

Statistical analysis Chi-square and Student’s t tests were used to compare proportions and means, respectively. We then generated bivariate descriptive statistics for the overall analytic sample and the outcomes of interest. We fit logistic regression models to examine the relationship between the risk for sleep apnea, short and long sleep durations (as a combined exposure), and insomnia symptoms with diabetes mellitus. The models were adjusted for age, sex, income (continuous measure), obesity (defined as BMI ⱖ 30 kg/m2), tobacco use, alcohol use, hypertension, dyslipidemia, and depression. We also utilized multivariate logistic regression analyses to evaluate associations of the primary exposures with dual diagnosis of diabetes and hypertension as well as diabetes and dyslipidemia, adjusting for the main covariates. All analyses were performed using SPSS (version 18.0; SPSS Inc., Chicago, IL, USA). A statistical level of P ⬍ 0.05 was considered significant.

Results The sample consisted of 1,013 participants, mean age of 62 years and 61% female. Table I shows the demographics and medical factors for the overall sample.

Diabetes mellitus and sleep apnea in blacks Table I. Demographics, medical factors, and sleep symptoms in the Metabolic Syndrome Outcome Study (MetSO) trial. Total n ⫽ 1,013 Mean ⫾ SD, or n (%) 62 ⫾ 14 135 ⫾ 17 75 ⫾ 11 106 ⫾ 37 48 ⫾ 16 135 ⫾ 77 612 (60) 477 (47) 578 (57) 661 (65) 266 (26) 71 (7) 493 (48) 528 (52) 102 (10)

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Age, years Systolic BP, mmHg Diastolic BP, mmHg LDL, mg/dL HDL, mg/dL Triglycerides, mg/dL Diabetes mellitus Dyslipidemia Hypertension ⱕ 6 hours of sleep 7–8 hours of sleep ⱖ 9 hours of sleep High risk for apnea Daytime sleepiness Insomnia symptoms

Diabetes mellitus was diagnosed in 60% of the sample. Forty-eight percent of the participants were at high risk for sleep apnea, 65% reported short sleep duration, and 10% had insomnia symptoms. There was an increased frequency of sleep apnea risk in participants with diabetes compared to those without diabetes; but no differences were observed in the frequency of the short and long sleep durations, insomnia symptoms, medical co-morbidities, and daytime sleepiness (Table II). Multivariate logistic regression analysis, adjusting for age, sex, income, obesity (defined as BMI ⱖ 30 kg/m2), tobacco use, alcohol use, hypertension, dyslipidemia, depression, short and long sleep durations, and insomnia symptoms, demonstrated that high risk for sleep apnea had a 66% increased likelihood of diabetes mellitus. Age, sex, and dyslipidemia were the main covariates that were associated with diabetes mellitus in multivariable model (Table III). Evaluation of our secondary outcomes in multivariate logistic regression showed that high risk for sleep apnea was associated with the combined outcome of diabetes–hypertension (OR 1.95; 95% CI 1.42–2.69), but not with diabetes–dyslipidemia (data not shown).

Discussion This study provides clinically relevant information on the association between sleep apnea risk and T2DM among blacks with MetS. In accordance with our study, an independent association

Table II. Medical and sleep factors by diabetes status in MetSO. Diabetes n ⫽ 612 (60%) No diabetes n ⫽ 401 (40%) Mean ⫾ SD, or n (%) Mean ⫾ SD, or n (%) Age, years Systolic BP, mmHg Diastolic BP, mmHg LDL, mg/dL HDL, mg/dL Triglycerides, mg/dL ⱕ 6 hours of sleep 7–8 hours of sleep ⱖ 9 hours of sleep High risk for apnea a Daytime sleepiness Insomnia symptoms

62 ⫾ 14 136 ⫾ 17 75 ⫾ 11 102 ⫾ 36 47 ⫾ 14 134 ⫾ 74 400 (65) 161 (26) 41 (6) 320 (52) 322 (53) 60 (10)

60 ⫾ 14 133 ⫾ 19 76 ⫾ 12 111 ⫾ 38 49 ⫾ 19 138 ⫾ 83 261 (65) 105 (26) 30 (7) 173 (43) 206 (51) 42 (10)

BP ⫽ blood pressure; HDL ⫽ high-density lipoprotein cholesterol; LDL ⫽ lowdensity lipoprotein. aP ⬍ 0.05.

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Table III. Associations between sleep apnea risk, demographics, and medical factors with diabetes mellitus in blacks with metabolic syndrome. High risk for sleep apnea Short or long sleep Insomnia, yes versus no Age, years Women versus men Income Tobacco use Alcohol use Obesity Dyslipidemia Hypertension Depression

OR

95% CI

1.66 1.03 1.15 1.02 0.61 1.06 1.20 1.00 0.66 1.52 1.19 0.75

1.21–2.28 0.73–1.45 0.69–1.89 1.01–1.03 0.43–0.85 0.78–1.45 0.89–1.61 0.99–1.00 0.38–1.16 1.09–2.14 0.68–2.07 0.44–1.28

between sleep apnea (risk), insulin resistance, and T2DM has been demonstrated in several large population-based studies (24,25). The novelty of our findings relies on the unique large population of blacks with MetS and the opportunity to account specifically for short sleep duration and insomnia symptoms, which are known contributors to cardiometabolic disease in this at-risk population (26). In contrast to our findings, in a multi-ethnic clinic-based sample of 1,008 participants composed of 66.9% blacks, 16.9% whites, and 14.9% Hispanic/Latinos, the association between sleep apnea diagnosed by polysomnography (PSG) and T2DM was fully attenuated by age and obesity (27). While the aforementioned study quantified sleep apnea by PSG, the diagnosis of T2DM was based on retrospective chart review. It is plausible that misclassification of diabetes status could have pulled the results toward the null in this cohort. Alternatively, our analysis was based on selfreports, which could lead to systematic bias by the over-reporting of sleep symptoms (28). In our study, the association between sleep apnea risk and diabetes was resilient to adjustments for obesity, a risk factor for both sleep apnea and T2DM (26,29). The associations between sleep apnea (risk) and glucose metabolic dysregulation may be explained by coexisting diseases that have obesity as a common denominator. However, our findings suggest that sleep apnea risk may exacerbate the cardiometabolic disease attributed to obesity and the MetS in this population (4,6,20). Despite the strong association between sleep apnea risk and T2DM, the mechanisms by which disruption of glucose metabolism occur in sleep apnea are not fully explained. Sleep apnea may contribute to diabetes mellitus through pronounced physiological perturbations associated with intermittent hypoxemia and increased sympathetic tone (26,30). Obesity is a known risk factor for sleep apnea and has been associated with a host of inflammatory and metabolic abnormalities that promote insulin resistance (3,5). In addition, sleep apnea results in sleep deficiency, which contributes to increased obesity. Sleep deficiency, obesity, and hypoxia (in sleep apnea) have been independently associated with increased inflammation, oxidative stress, impaired glucose tolerance, and insulin resistance. Thus, the increased risk of diabetes associated to sleep apnea risk may occur through various pathways (3,5). There was an increased frequency of short sleep duration and insomnia symptoms in our study population, but these did not differ by diabetes status and were not associated with our outcomes. Short sleep duration and long sleep duration have been shown to compromise insulin sensitivity (31), increase total and LDL cholesterol levels, and are associated with obesity, diabetes, and hypertension, all potent risk factors for cardiovascular disease (10,11,32). It is plausible that most of the variance from sleep-related cardiovascular risk observed in our sample of blacks is explained

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by unrecognized sleep apnea, rather than sleep duration and/or curtailed sleep (e.g. insomnia). There are several strengths to our study which lend confidence to the findings. The study evaluated a large outpatient population at increased risk of cardiometabolic disease with systematic measurements of demographics, medical factors, sleep symptoms, and risk for sleep apnea. One of the strengths of the present study is the large sample of blacks with metabolic syndrome, a group that has been under-represented in clinical studies that permitted the evaluation of the associations of interest in this population. Despite these strengths, there are several weaknesses. First, the cross-sectional nature of our study impedes inferences about causality. Second, we did not obtain polysomnography (PSG) or quantified sleep duration with actigraphy. Self-reported sleep measures have weak to moderate correlations with objective data (28). In addition, we were not able to account for the variability of self-reported sleep duration across days of the week (i.e. work days versus off-days) and did not account for sleep-inducing (sedative) medications. Finally, the ARES™ sleep questionnaire is not able to convey information regarding the severity of sleep apnea. However, the ARES™ sleep questionnaire is validated and shown to have a high positive predictive value for the diagnosis of sleep apnea by polysomnography. In addition, self-reports of sleep duration have been used across many population-based studies with strong associations with morbidity and mortality risk (9). Future studies with objective measures (i.e. PSG and actigraphy) are needed to confirm the associations observed in our sample. In conclusion, we observed a strong association between the risk for sleep apnea and diabetes mellitus among black participants with metabolic syndrome. Our findings suggest that sleep apnea is a major public health problem in this population at greater risk of cardiovascular disease. Sleep disruption is a modifiable risk factor that should be examined in longitudinal and treatment studies.

Acknowledgements We are extremely grateful to the study participants who took the time to participate in this study. Without their participation, this study would not have been possible. Funding: The authors sincerely acknowledge the financial support received from National Institutes of Health R01MD004113, 1KL2TR000461 (A.R.R.), NCT01946659. Declaration of interest: This study was not an industry-supported study. No author has a financial relationship with a commercial entity that has interest in the subject of the manuscript. The authors declared no potential conflicts of interest with respect to the financial interest, research, authorship, and/or publication of this article. The sponsors had no role in the design and conduct of the study: collection, management, analysis, and interpretation of the data, preparation, review, or approval of the manuscript, and decision to submit the manuscript for publication. Statement of human and animal rights: All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2008 (5).

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Associations between sleep disturbances and diabetes mellitus among blacks with metabolic syndrome: Results from the Metabolic Syndrome Outcome Study (MetSO).

The association between sleep disturbances and cardiometabolic diseases has been understudied in blacks with metabolic syndrome...
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