Obstructive Sleep Apnea in Extremely Overweight Adolescents undergoing Bariatric Surgery Maninder Kalra,* Thomas Inge,† Victor Garcia,† Stephen Daniels,‡ Louise Lawson,§ Rebecca Curti,* Aliza Cohen,† and Raouf Amin* Abstract KALRA, MANINDER, THOMAS INGE, VICTOR GARCIA, STEPHEN DANIELS, LOUISE LAWSON, REBECCA CURTI, ALIZA COHEN, AND RAOUF AMIN. Obstructive sleep apnea in extremely overweight adolescents undergoing bariatric surgery. Obes Res. 2005; 13:1175–1179. Objectives: To determine the prevalence of obstructive sleep apnea (OSA) in extremely overweight adolescents and to examine the effect of significant weight loss on OSA severity. Research Methods and Procedures: We reviewed the anthropometric and polysomnographic data on all extremely overweight adolescents who underwent laparoscopic Roux en Y gastric bypass surgery at Cincinnati Children’s Hospital Medical Center from July 2001 to September 2004. Repeat polysomnograms were performed after significant weight loss. Comparisons were made between pre- and postoperative polysomnographic data. Results: Nineteen of 34 patients (55%) who underwent bariatric surgery were diagnosed with OSA. Subsequent to surgery, 10 of these patients returned for follow-up polysomnographic testing. After significant weight loss (mean, 58 kg), OSA severity markedly decreased in all patients (median apnea-hypopnea index at baseline vs. after weight loss, 9.1 vs. 0.65). Discussion: Our study indicated that OSA was highly prev- Received for review December 17, 2004. Accepted in final form April 21, 2005. The costs of publication of this article were defrayed, in part, by the payment of page charges. This article must, therefore, be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. *Division of Pulmonary Medicine, †Division of Pediatric and Thoracic Surgery, ‡Division of Cardiology, and §Center for Epidemiology and Biostatistics, Cincinnati Children’s Hospital, Cincinnati, Ohio. Address correspondence to Maninder Kalra, Division of Pulmonary Medicine, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, Cincinnati, OH 45229. E-mail: maninder.kalra@cchmc.org Copyright © 2005 NAASO alent in extremely overweight adolescents meeting eligibility criteria for bariatric surgery. The significant weight loss after gastric bypass was associated with a marked reduction in OSA severity. Key words: weight loss, obstructive sleep apnea resolution, gastric bypass surgery, obstructive sleep apnea Introduction Over the past three decades, the prevalence of obesity in pediatric age groups has tripled, reaching epidemic proportions (1,2). This trend, together with the concomitant increase in a wide range of obesity-related disorders, has become a source of growing medical concern (3). Bariatric surgery has gradually gained acceptance as a weight loss option for a select group of extremely obese adolescents who are affected by such disorders and who have failed to lose weight with less invasive traditional approaches (4,5). In adults, bariatric surgery results in significant and sustained weight loss, which, in turn, has reversed or reduced the severity of many obesity-related disorders (6), including obstructive sleep apnea (OSA)1 (7). OSA is a disorder characterized by narrowing of the pharyngeal airway, resulting in repeated episodes of airflow cessation, oxygen desaturation, and sleep disruption (8). The evidence for an association between obesity and OSA is well documented, with obesity shown to be a risk factor for OSA in both adults and children (9 –11). In obese adults, the reported prevalence of OSA is ⬃40% (10); in extremely obese adults (BMI ⱖ 40 kg/m2), the prevalence increases to 98% (12). Of particular significance, a number of studies in extremely obese adults have shown that significant weight loss after bariatric surgery decreases the severity of OSA 1 Nonstandard abbreviations: OSA, obstructive sleep apnea; PSG, polysomnogram; AHI, apnea-hypopnea index. OBESITY RESEARCH Vol. 13 No. 7 July 2005 1175 OSA in Extremely Overweight Adolescents, Kalra et al. (7,13). Comparatively few OSA studies have been conducted in the obese pediatric population. Marcus et al. (14) reported that 36% of obese children and adolescents had abnormal polysomnograms (PSGs), and they also showed a positive correlation between the degree of obesity and the severity of OSA. Silvestri et al. (15) reported a 59% prevalence of OSAs in obese children and adolescents, similarly showing an increased trend as obesity became more severe. In a pediatric population referred for sleep problems, Mallory et al. (16) found that 37% of children and adolescents suffering from severe obesity had abnormal PSGs, and of those patients, 24% were diagnosed with OSA. While these pediatric studies lay the foundation for an association between severe obesity and OSA that parallels that reported in the adult population, gaps in knowledge still remain. Neither the prevalence of OSA in extremely overweight adolescents nor the degree of weight loss required to reverse OSA has been elucidated. The purpose of our study was to determine the prevalence of OSA in a population of extremely overweight adolescents referred to an adolescent surgical weight management program. In addition, we hypothesized that, with postoperative weight loss, OSA severity would significantly improve in this patient population. Research Methods and Procedures Study Design We conducted a retrospective chart review of all patients who underwent laparoscopic Roux-en-Y gastric bypass surgery at Cincinnati Children’s Hospital Medical Center between July 2001 and September 2004. Approval for this project was granted by our Institutional Review Board. Subjects All subjects were enrolled in the Comprehensive Weight Management Center, which offers a surgical weight loss option for extremely overweight adolescents meeting the following adolescent bariatric guidelines, as previously described (5): ● ● ● ● Girls, 13 to 18 years of age; boys, 14 to 18 years of age Failure of at least 6 months of medically supervised weight loss attempts BMI ⱖ40 kg/m2, with presence of at least one severe obesity-related comorbidity (OSA, type 2 diabetes, pseudotumor cerebri) BMI ⱖ50 kg/m2, with at least one less severe obesityrelated comorbidity (hypertension, dyslipidemia, hyperinsulinemia, gastroesophageal reflux disease, non-alcoholic fatty liver disease) Anthropometric Measures Body weights were recorded using a digital scale, and heights were measured using a calibrated wall mounted stadiometer. All weights were obtained in light clothing and 1176 OBESITY RESEARCH Vol. 13 No. 7 July 2005 without shoes. All measurements were obtained in triplicate, and mean values were used. Weight and height information were used to calculate BMI as weight (kilograms) divided by height (meters squared). PSG Data Overnight PSG reports were reviewed for the following variables: ● ● ● ● Apnea-hypopnea index (AHI): number of OSA and hypopnea episodes per hour of sleep Arousal index: number of arousals from sleep per hour of sleep Mean oxygen saturation during sleep Minimum oxygen saturation during sleep Comparisons were made between pre- and postoperative PSG variables. OSA Patients were considered to have OSA if their PSG revealed AHI ⱖ5 per hour of sleep. Data Analyses Mean values of anthropometric and PSG variables were calculated. Paired Student’s t test was used to compare normally distributed variables. The Wilcoxon signed-rank test was used to compare variables not meeting normality criteria. Spearman’s correlation coefficient was calculated to measure the association among variables. Two-tailed p values of ⬍0.05 were considered to indicate statistical significance. SAS version 8.2 was used for statistical analysis. Results The study population was comprised of 35 subjects (23 girls and 12 boys), with a mean age of 17.57 ⫾ 1.82 years. Thirty-one of 35 (90%) subjects were non-Hispanic white. All patients had a BMI ⬎95th percentile of BMI for age, with a mean BMI of 57.01 ⫾ 10.05 kg/m2 (range, 48 to 87 kg/m2). The mean weight of this cohort was 170 ⫾ 31.38 kg. Of the 35 patients who underwent gastric bypass surgery, 34 underwent preoperative polysomnography. Twenty-five of these 34 (73.5%) patients had an obstructive AHI ⬎1 (normal ⱕ1 event/h). Nineteen (55%) had an AHI ⱖ5, indicating the presence of OSA. As shown in Figure 1, the percentage of subjects with OSA significantly increased across BMI strata (p ⬍ 0.05), with close to 75% of subjects with a BMI ⬎60 kg/m2 having OSA. Of the 19 subjects with OSA, 10 (53%) underwent postoperative polysomnography after clinically significant weight loss (mean, 58 kg), with a mean interval of 5.1 ⫾ 1.2 months between baseline and repeat PSGs. The failure of the remaining nine to undergo this testing was because of OSA in Extremely Overweight Adolescents, Kalra et al. Table 2. Comparison of obesity and OSA indices before and after bariatric surgery Figure 1: The percentage of patients with OSA (AHI ⱖ 5) across BMI strata. The p value for the trend is ⬍0.05. their lack of availability; there were no significant differences in baseline BMI or AHI between these two OSA subject groups (Table 1). Among the 10 OSA subjects who had follow-up testing, there was a mean decrease in BMI of 19 units over a duration of ⬃6 months (p ⬍ 0.01). As measured by AHI, all 10 subjects showed a significant reduction in the severity of their OSA (p ⬍ 0.01), with only 1 subject having residual OSA severe enough to meet the clinical criterion for treatment (Table 2). AHI values did not, however, show a significant relationship between the reduction in BMI and the resolution of OSA (R ⫽ 0.47, p ⫽ 0.2). The average O2 saturation during sleep was ⬃95% at baseline and 96% after weight loss. In contrast, there was a significant improvement in minimum O2 saturation (p ⬍ 0.05). This increased from ⬍90% at baseline to close to 92% after weight loss. Discussion In our cohort of extremely overweight adolescents meeting eligibility criteria for bariatric surgery, we found a 55% prevalence of OSA. Furthermore, as BMI increased, there Table 1. Patients diagnosed with OSA Age (years) BMI AHI With follow-up PSG (N ⴝ 10) Without follow-up PSG (N ⴝ 9) p 16.9 ⫾ 1.77 60.8 ⫾ 11.07 9.1* 17.46 ⫾ 1.42 59.11 ⫾ 8.45 7.1* NS† NS† NS‡ * Values reported as median. † p value derived by paired Student’s t test. ‡ p value derived by Wilcoxon signed-rank test. Weight (kg) BMI AHI Arousal index Mean O2 saturation Minimum O2 saturation Baseline After weight loss p 173.1 ⫾ 27.8 60.8 ⫾ 11.07 9.1* 11.36 ⫾ 4.64 118.3 ⫾ 21.7 41.6 ⫾ 9.5 0.65* 8.13 ⫾ 3.7 ⬍0.01† ⬍0.01† ⬍0.01‡ 0.22† 94.5 ⫾ 1.65 95.5 ⫾ 1.4 0.06† 82.9 ⫾ 5.7 91.7 ⫾ 3.6 ⬍0.01† * Values reported as median. † p value derived by paired Student’s t test. ‡ p value derived by Wilcoxon signed-rank test. was a trend toward an even higher OSA prevalence. This finding is similar to that reported in other adult and pediatric studies and further supports reported findings of an association between obesity (adiposity) and OSA (9 –11). To avoid possible bias from OSA being used as an inclusion criterion for bariatric surgery in patients with a BMI between 40 and 50 kg/m2, we calculated the prevalence of OSA in patients meeting bariatric surgery eligibility criteria because of weight alone (i.e., those with BMI ⬎ 50 kg/m2); a similarly high OSA prevalence of 58% (N ⫽ 15) was found among the 26 adolescents in this group. The potential impact of this finding on overall health merits major concern in that OSA is associated with cognitive deficits (17), as well as metabolic (18) and cardiovascular (19 –21) morbidity, Moreover, its severity correlates with the degree of metabolic (22) and cardiovascular impairment (19). Consistent with prior reports in adults, we also found that after weight loss, there was a significant reduction in the severity of OSA (23). As measured by minimum O2 saturation, a significant improvement in hypoxemia during sleep was also observed after weight loss. Because overnight hypoxemia is considered to be one of the pathways for cardiovascular sequelae of OSA because of increased morning catecholamine levels (24) and prothrombosis (25), the improvement in AHI is particularly significant in obese adolescents, a group that is already at high risk for cardiovascular morbidity. These combined results highlight the benefit of bariatric surgical intervention in the resolution of obesity-related OSA and underscore why it has gradually gained recognition as a useful weight loss tool for a select group of extremely obese adolescents. This is especially important in light of the high attrition rates among obese adolescents participating in traditional medical weight loss OBESITY RESEARCH Vol. 13 No. 7 July 2005 1177 OSA in Extremely Overweight Adolescents, Kalra et al. programs (26). Continuous positive airway pressure is typically the first line of therapy for moderate to severe OSA (27). However, because of its inconvenience and discomfort, it is accepted by only 50% of adult patients initially, with only 68% of those patients remaining compliant after 1 year (28), and by an even lower proportion of adolescents (in our experience). Contrary to our expectations, we did not find a significant correlation between absolute change in OSA indices (AHI, arousal index, and minimum O2 saturation) and a decrease in obesity (BMI) after bariatric surgery. We conjecture that this finding could be partially attributed to the fact that BMI, although widely used for expressing body fat, is an indirect measure of adiposity. Thus, we are currently exploring whether magnetic resonance imaging provides more precise measurements of adipose tissue. Magnetic resonance imaging is increasingly gaining recognition as a method for assessing visceral adiposity (29) and parapharyngeal fat (30). The importance of body fat distribution in the etiology of OSA is highlighted by recent reports of a higher correlation between OSA and central obesity than between OSA and parapharyngeal fat (31). It may, thus, be prudent for future studies to examine the relationship between changes in visceral adiposity after weight loss and degree of improvement in OSA. A limitation of this study is that not all PSGs were performed at the same sleep laboratory. Nevertheless, given the striking difference in OSA severity before and after weight loss, we do not feel that variability in personnel and equipment calibration had any significant impact on our PSG results. In summary, our study indicated that OSA was highly prevalent in extremely overweight adolescents meeting eligibility criteria for bariatric surgery. The significant weight loss after bariatric surgery was associated with either the resolution of OSA in a majority or a significant reduction in OSA severity. 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