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Intermittent Nocturnal Hypoxia and Metabolic Risk in Obese Adolescents with Obstructive Sleep Apnea

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Intermittent Nocturnal Hypoxia and Metabolic Risk in Obese Adolescents with Obstructive Sleep Apnea Sleep and Breathing https://doi.org/10.1007/s11325-018-1631-9 SLEEP BREATHING PHYSIOLOGY AND DISORDERS • ORIGINAL ARTICLE Intermittent nocturnal hypoxia and metabolic risk in obese adolescents with obstructive sleep apnea Indra Narang1,2 & Brian W. McCrindle1,2 & Cedric Manlhiot3 & Zihang Lu1,2 & Suhail Al-Saleh1,2 & Catherine S. Birken1,2 & Jill Hamilton1,2 Received: 16 August 2017 /Revised: 6 December 2017 /Accepted: 11 January 2018 # Springer International Publishing AG, part of Springer Nature 2018 Abstract Purpose There is conflicting data regarding the independent associations of obstructive sleep apnea (OSA) with metabolic risk in obese youth. Previous studies have not consistently addressed central adiposity, specifically elevated waist to height ratio (WHtR), which is associated with metabolic risk independent of body mass index. Objective The objective of this study was to determine the independent effects of the obstructive apnea-hypopnea index (OAHI) and associated indices of nocturnal hypoxia on metabolic function in obese youth after adjusting for WHtR. Methods Subjects had standardized anthropometric measurements. Fasting blood included insulin, glucose, glycated hemoglo- bin, alanine transferase, and aspartate transaminase. Insulin resistance was quantified with the homeostatic model assessment. Overnight polysomnography determined the OAHI and nocturnal oxygenation indices. Results Of the 75 recruited subjects, 23% were diagnosed with OSA. Adjusting for age, gender, and WHtR in multivariable linear regression models, a higher oxygen desaturation index was associated with a higher fasting insulin (coefficient [standard error] = 48.076 [11.255], p < 0.001), higher glycated hemoglobin (coefficient [standard error] = 0.097 [0.041], p = 0.02), higher insulin resistance (coefficient [standard error] = 1.516 [0.364], p < 0.001), elevated alanine transferase (coefficient [standard error] = 11.631 [2.770], p < 0.001), and aspartate transaminase (coefficient [standard error] = 4.880 [1.444], p =0.001). However, there were no significant associations between OAHI, glucose metabolism, and liver enzymes. Conclusion Intermittent nocturnal hypoxia rather than the OAHI was associated with metabolic risk in obese youth after adjusting for WHtR. Measures of abdominal adiposity such as WHtR should be considered in future studies that evaluate the impact of OSA on metabolic health. Keywords Nocturnal hypoxia . Obstructive sleep apnea . Obesity . Metabolic risk Introduction nocturnal oxyhemoglobin desaturations and sleep disrup- tion [1]. The prevalence of OSA is 1–4% in otherwise Obstructive sleep apnea (OSA) is characterized by snor- healthy school children but alarmingly reported to occur ing and recurrent partial and/or complete obstruction of in 25% of obese youth [2]. Obesity predisposes to met- the upper airway and is associated with intermittent abolic disease, including diabetes and non-alcoholic fat- ty liver disease (NAFLD) in children [3]. In recent years, the presence of OSA in adults has been shown to be a risk factor for insulin resistance and NAFLD * Indra Narang independent of obesity [4, 5]. Effective treatment for OSA [email protected] with continuous positive airway pressure (CPAP) in adults is associated with improvements in glycemic control [6]. Of 1 Department of Paediatrics, Hospital for Sick Children, emerging interest is the relative causal role of OSA and asso- Toronto, Ontario, Canada ciated hypoxemia in potentiating metabolic risk in obese 2 University of Toronto, Toronto, Ontario, Canada youth. However, the current available data are conflicting 3 The Cardiovascular Data Management Centre, The Hospital for Sick and some of the disparities in the reported literature are due Children, Toronto, Canada to different definitions of OSA and obesity (which is typically Sleep Breath defined by body mass index [BMI]), limiting direct compari- score was calculated according to age and sex-specific growth sons and definitive conclusions [7]. curves of the World Health Organization, and obesity was There is recent evidence to suggest that controlling for BMI defined as a BMI z score > 1.96 [11]. Waist circumference may not adequately exclude the influence of increased visceral was measured three times to the nearest 0.1 cm using a non- adiposity [8], which is also known to be a significant risk elastic fiberglass measuring tape (Tech-Med model 4414; factor associated with cardiometabolic risk in adults [9]. Moore Medical Corp., New Britain, Connecticut) placed at Specifically, an elevated waist to height ratio (WHtR), regard- the top of the iliac crest with the subject in a standing position less of BMI percentile category, is associated with an increase [12]. The WHtR was calculated by waist circumference in in cardiometabolic risk in the pediatric population [10]. As centimeters divided by height in centimeters. A WHtR > 0.6 such, WHtR may be an important discriminatory measure- was considered to indicate greater likelihood of metabolic ment associated with metabolic risk. Thus, any models eval- risk [10]. uating the independent effects of OSA on metabolic risk Fasting blood work was drawn via an intravenous catheter should be adjusted for WHtR. Since OSA has modifiable risk inserted into the antecubital fossa. Fasting metabolic variables factors, early diagnosis and targeted interventions for OSA in collected were plasma glucose, insulin, glycated hemoglobin obese youth may be associated with improved metabolic out- A1c (HbA1c), alanine transferase (ALT), and aspartate trans- comes long-term. aminase (AST). Both ALT and AST were used as surrogate The objective of this study was to determine the relation- markers of liver inflammation and possible NAFLD. Insulin ship between the indices associated with OSA, specifically the was measured by chemiluminescence (Siemens Immulite obstructive apnea-hypopnea index (OAHI), the oxygen 2500; range of assay 15–2165 pmol L21, intra- and inter- desaturation index (ODI), and nadir oxygen saturation assay coefficient of variation [CV] < 7.6%). Insulin resistance (SaO2), with insulin resistance and hepatic enzyme levels in was quantified with the homeostatic model assessment obese youth. We hypothesized that with adjustment for central (HOMA-IR) with fasting plasma glucose and insulin measure- adiposity, specifically WHtR, the OAHI, ODI, and SaO2 are ments (HOMA-IR = [glucose (nmol/L) × insulin (μU/mL)]/ associated with metabolic risk on obese youth. 22.5). A HOMA-IR value greater than 3.16 was considered abnormal [13]. HbA1c values greater than 6.5% were consid- ered abnormal [14]. Methods Polysomnogram Study population Subjects underwent a standard overnight PSG using Natus The study sample was derived from the cross-sectional High Sleepworks system (Natus Medical Incorporated, CA, Impact Strategies Towards Overweight Reduction in Youth USA), which is a data acquisition and analysis system. PSG (HISTORY) study. The HISTORY study was designed to measurements included electroencephalogram, electro- (1) evaluate baseline metabolic status and (2) screen for oculogram, and submental and bilateral anterior tibialis elec- OSA using a formal overnight polysomnogram (PSG). tromyogram. Chest wall and abdominal movements were Subjects aged 8–18 years who were obese were consecutively measured using chest wall and abdominal belts. Other respi- recruited into this study between 2009 and 2012 using adver- ratory measurements included nasal air pressure transducer by tisements posted in the hospital, at pediatricians’ offices, and Braebon, oronasal thermal sensor, oxygen saturation (SaO2) at community pediatric obesity clinics as well as at our tertiary using a Massimo pulse oximeter (Irvine, CA), transcutaneous care institution. Exclusion criteria included known genetic or carbon dioxide (tcCO2) using a Sentec carbon dioxide sensor syndromic conditions that may contribute to obesity (e.g., (Therwil, Switzerland), and end-tidal carbon dioxide (etCO2) Prader-Willi Syndrome), use of glucose-altering medications, using a BCI Capnocheck unit (Waukesha, USA). Video and known diabetes, known liver abnormalities, use of medica- audio recordings were obtained as well as body position. tions that may significantly impact sleep architecture (e.g., Sleep architecture was assessed by standard techniques [15]. anti-depressants), youth with known OSA at the time of re- All respiratory events were scored according to the American cruitment or on CPAP treatment for OSA, developmental de- Academy of Sleep Medicine scoring guidelines [16] by a reg- lay, pregnancy, and an inability to speak English. istered certified polysomnographic technician who was blinded to the clinical status of the patients. All of the sleep Study procedures and measurements studies were reviewed and interpreted by experienced pediat- ric sleep physicians. An obstructive apnea event was scored Subjects arrived at the hospital following a 12-h overnight when airflow dropped at least 90% from baseline with chest fast. Weight and height were measured by a standard, calibrat- and/or abdominal motion throughout the entire event; the du- ed scale and wall-mounted stadiometer, respectively. BMI z ration of which was at least a minimum of two baseline Sleep Breath breaths. A hypopnea event was scored when airflow dropped Separate multivariate linear regression models were used to at least 50% from baseline, the duration of which was at least a assess the associations of OAHI, ODI, SaO2, and arousal in- minimum of two baseline
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