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Association of Obstructive Sleep Apnea in Rapid Diabetes Care Volume 37, February 2014 355 Daniela Grimaldi,1,2 Guglielmo Beccuti,1,3 Association of Obstructive Sleep CLIN CARE/EDUCATION/NUTRITION/PSYCHOSOCIAL Carol Touma,1,3 Eve Van Cauter,1,3 and Apnea in Rapid Eye Movement Babak Mokhlesi1,2 Sleep With Reduced Glycemic Control in Type 2 Diabetes: Therapeutic Implications OBJECTIVE Severity of obstructive sleep apnea (OSA) has been associated with poorer gly- cemic control in type 2 diabetes. It is not known whether obstructive events during rapid eye movement (REM) sleep have a different metabolic impact com- pared with those during non-REM (NREM) sleep. Treatment of OSA is often limited to the first half of the night, when NREM rather than REM sleep predominates. We aimed to quantify the impact of OSA in REM versus NREM sleep on hemoglobin A1c (HbA1c)insubjectswithtype2diabetes. RESEARCH DESIGN AND METHODS All participants underwent polysomnography, and glycemic control was assessed by HbA1c. RESULTS 6 Our analytic cohort included 115 subjects (65 women; age 55.2 9.8 years; BMI 1 6 2 – Department of Medicine, Sleep, Metabolism, 34.5 7.5 kg/m ). In a multivariate linear regression model, REM apnea hypopnea and Health Center, University of Chicago, index (AHI) was independently associated with increasing levels of HbA1c (P = Chicago, IL 2 0.008). In contrast, NREM AHI was not associated with HbA1c (P = 0.762). The mean Department of Medicine, Section of Pulmonary and Critical Care, Sleep Disorders Center, adjusted HbA1c increased from 6.3% in subjects in the lowest quartile of REM AHI P University of Chicago, Chicago, IL to 7.3% in subjects in the highest quartile of REM AHI ( = 0.044 for linear trend). 3Department of Medicine, Section of Our model predicts that 4 h of continuous positive airway pressure (CPAP) use Endocrinology, Diabetes and Metabolism, would leave 60% of REM sleep untreated and would be associated with a decrease University of Chicago, Chicago, IL in HbA1c by approximately 0.25%. In contrast, 7 h of CPAP use would cover more Corresponding author: Babak Mokhlesi, [email protected]. than 85% of REM sleep and would be associated with a decrease in HbA1c by as much as 1%. Received 20 April 2013 and accepted 2 October 2013. CONCLUSIONS This article contains Supplementary Data online In type 2 diabetes, OSA during REM sleep may influence long-term glycemic at http://care.diabetesjournals.org/lookup/ suppl/doi:10.2337/dc13-0933/-/DC1. control. The metabolic benefits of CPAP therapy may not be achieved with the © 2014 by the American Diabetes Association. typical adherence of 4 h per night. See http://creativecommons.org/licenses/by- Diabetes Care 2014;37:355–363 | DOI: 10.2337/dc13-0933 nc-nd/3.0/ for details. 356 REM OSA and Type 2 Diabetes Diabetes Care Volume 37, February 2014 In 2011, the Centers for Disease Control randomized, placebo-controlled clinical diagnosed type 2 diabetes, we also and Prevention reported that nearly trial examining the impact of continuous recruited in the community using an 26 million American adults, 8.3% of the positive airway pressure (CPAP) advertisement inviting subjects at risk population, had type 2 diabetes (1). The treatment on HbA1c in patients with for type 2 diabetes based on age and alarming increase in overweight and type 2 diabetes were surprisingly adiposity to participate in a research obesity has played a pivotal role in the disappointing (16). One potential reason study on sleep and metabolism. All rise of type 2 diabetes prevalence. The for the failure of OSA treatment to participants without an established obesity epidemic has also been improve chronic glycemic control in diagnosis of type 2 diabetes had to associated with an increased prevalence patients with type 2 diabetes is undergo a standard 75-g oral glucose of sleep disturbances, particularly insufficient CPAP use. Notably, the mean tolerance test and meet the American obstructive sleep apnea (OSA) (2,3). nightly CPAP use in this clinical trial was Diabetes Association guidelines for the Over the past decade, both laboratory 3.6 h. As most of rapid eye movement diagnosis of type 2 diabetes (23). (REM) sleep occurs in the early morning and epidemiologic studies have All participants were in stable condition fi hours before habitual awakening, one identi ed poor sleep quality and OSA as and, when on pharmacological possibility is that with suboptimal putative novel risk factors for type 2 treatment, on a stable antidiabetic – adherence to CPAP therapy, obstructive diabetes (4 6). OSA is a treatable medication regimen for the preceding apneas and hypopneas during REM sleep chronic sleep disorder characterized by 3 months. Exclusion criteria were were disproportionately untreated recurrent episodes of complete (apnea) unstable cardiopulmonary conditions, compared with events in non-REM or partial (hypopnea) obstruction of the neurological disorders, psychiatric (NREM) sleep. This may be relevant to upper airway. OSA leads to intermittent disease, shift work, chronic insomnia, or glycemic control because it is now well hypoxemia and hypercapnia, increased any prior or current treatment for OSA established that compared with NREM oxidative stress, cortical microarousals, (upper airway surgery, CPAP therapy, sleep, REM sleep is associated with sleep fragmentation, and chronic sleep oral appliances, or supplemental greater sympathetic activity in healthy loss. Indeed, prevalence estimates of oxygen). We previously reported the subjects as well as in patients with OSA OSA, defined as apnea–hypopnea index association of OSA severity categories (17–19). Further, compared with (AHI) $5 events per hour, in nondiabetic (no, mild, moderate, and severe OSA) events in NREM sleep, obstructive obese adults have ranged from 50 to with chronic glycemic control in type 2 apneas and hypopneas during REM 68% (7,8). diabetes using 60 of the participants sleep last nearly 30 s longer and are included in this analysis (9). In recent years, evidence has associated with significantly larger accumulated to indicate that OSA is oxygen desaturation (20–22). The study was approved by the both a risk factor for type 2 diabetes and Therefore, obstructive events during University of Chicago Institutional an exceptionally frequent comorbidity REM sleep, as compared with NREM Review Board, and all participants gave with an adverse impact on glycemic sleep, may have a larger adverse effect written informed consent. control. Five independent studies, on insulin release and action. This issue totaling nearly 1,400 patients with type has major clinical implications for the Experimental Protocol 2 diabetes, have shown that the duration of CPAP use that is needed to Subjects were admitted to the Clinical prevalence of OSA (assessed by reverse the negative consequences of Resource Center or the Sleep Research polysomnography [PSG]) ranges OSAonglycemiccontrolintype2 Laboratory of the Sleep, Health, and between 58 and 86% (9,10). Several diabetes. We have therefore Metabolism Center at the University of studies have established a robust performed a detailed analysis Chicago to undergo an overnight in- associationdindependent of adiposity comparing the contributions of NREM laboratory PSG. Height and weight were and other known confoundersdbetween versus REM OSA to glycemic control as measured in all participants. Self- the presence and severity of OSA and assessed by levels of HbA1c in a large reported ethnicity-based diabetes risk insulin resistance and glucose cohort of adults with type 2 diabetes. was categorized as low-risk category intolerance in nondiabetic adults (non-Hispanic whites) and high-risk (11–14). Two studies that used the gold RESEARCH DESIGN AND METHODS category (African Americans, Hispanics, standard of in-laboratory PSG to Participants and Asians). The duration of type 2 accurately quantify the severity of OSA We prospectively recruited subjects diabetes and the number of medications reported a robust association between with established type 2 diabetes using were verified by questionnaires as well increasing OSA severity and increasing an advertisement posted in the primary as review of the patients’ medical levels of hemoglobin A1c (HbA1c)in care and endocrinology clinics at the records. Insulin use was defined as the patients with type 2 diabetes, after University of Chicago, inviting current use of insulin by subject’s controlling for multiple potential participation in a research study on report. HbA1c was used as clinical confounders (9,15). While the findings of sleep and diabetes. Eligible individuals indicator of glycemic control. HbA1c these two studies suggested that the had to meet the criteria for type 2 values (defined as the proportion of effective treatment of OSA may be a diabetes based on physician diagnosis hemoglobin that is glycosylated) were nonpharmacologic strategy to improve using standard criteria (23). In order to obtained from the patient’schartif glucose control, the results of the only include individuals with newly assessed during the previous three care.diabetesjournals.org Grimaldi and Associates 357 months (n = 17,15% of subjects) or AHI was 15–29, and severe OSA if the AHI including “tolerance” and “variance measured on a single blood sample was $30. REM AHI was calculated as the inflation factor” (SPSS Statistics v20, drawn on the morning after the PSG number of apneas and hypopneas during IBM, Armonk, NY). Values for HbA1c, (n = 98, 85% of the subjects). HbA1c was REM sleep divided by total time in REM years of type 2 diabetes, and REM and measured by Bio-Rad variant classic sleep in hours. NREM AHI was calculated NREM AHI were submitted to natural log boronate affinity-automated high- by dividing the number of apneas and (Ln) transformation. In order to deal performance liquid chromatography hypopneas during NREM sleep by total with zero values, the total AHI, REM AHI, (Bio-Rad, Hercules, CA). The intra-assay time in NREM sleep in hours. The oxygen and NREM AHI were log transformed coefficient of variation was 0.5–1.0%, desaturation index (ODI) was defined as using the formula AHI = log(AHI + 0.01).
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