Impacts of body weight after surgery for obstructive sleep apnea in children

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1 International Journal of Obesity (2013) 37, & 2013 Macmillan Publishers Limited All rights reserved /13 PEDIATRIC ORIGINAL ARTICLE Impacts of body weight after surgery for obstructive sleep apnea in children W-C Hsu 1,2,7, K-T Kang 1,3,4,7, W-C Weng 2,5 and P-L Lee 2,6 OBJECTIVE: To investigate the impacts of body weight status on surgical outcomes and shifts of body weight status after adenotonsillectomy(t&a) in children with obstructive sleep apnea (OSA). METHODS: From 2009 to 2011, 161 children (mean age, 7.0±3.4 years; 78% boys) were included. All the children had clinical symptoms and preoperative polysomnographic evaluations diagnosis of OSA. Children were divided into four weight status groups (underweight, normal weight, overweight and obese), based on age and gender corrected body mass index (BMI). RESULTS: Following T&A, the four different weight status groups significantly improved in apnea/hypopnea index (AHI) and minimum oxygen saturation. However, 49.1% of the children (79/161) had residual OSA (AHI X1). The incidence of residual OSA (AHI X1) in the obese group was 75%, which was significantly higher than the other three groups (Po0.01). changes after T&A were documented, and 54% (13/24) of the underweight children shifted to normal weight status within 6 months after surgery. CONCLUSION: Although sleep parameters improved in all weight statuses, obese children had a higher incidence of residual OSA postoperatively. About half of the underweight children shifted to normal weight status after T&A. International Journal of Obesity (2013) 37, ; doi: /ijo ; published online 27 November 2012 Keywords: body weight status; obese; underweight; obstructive sleep apnea; adenotonsillectomy; child INTRODUCTION Obstructive sleep apnea (OSA) in children includes a spectrum of respiratory disorders characterized by upper airway collapse during sleep. 1,2 Untreated OSA in children is associated with cardiovascular, 3 neurocognitive 4 and somatic growth consequences. 5 The cause of OSA in children is multifactorial, although it is mainly due to enlarged tonsils and adenoids, which obstruct the airway thereby leading to loss of muscle tone during sleep. 6 Removing the tonsils and adenoids (adenotonsillectomy, T&A) is thus widely considered to be the first-line therapy for childhood sleep apnea. 7 Both obesity and underweight status are associated with childhood OSA. 8,9 Child obesity increases the risk of OSA, 10 while children with OSA are reported to have delayed growth and impaired weight gain. 11 These findings imply a complex interaction between anatomic factors, environmental conditions and individual susceptibility in children with OSA. Previous studies evaluating surgical outcomes for OSA have frequently found that obesity increases the risk of residual OSA after T&A. 10,12 However, surgical outcomes in children with different weight statuses, especially underweight and overweight statuses, have seldom been studied. Moreover, although children often gain in weight and height following T&A, 13 exactly how body weight status shifts after surgery remains unclear. The main purpose of this study was to compare the surgical outcomes for the treatment of OSA in underweight, normal weight, overweight and obese children. We also investigated the shifts in body-weight status after T&A in children with OSA, and how body weight status and pediatric OSA are related. MATERIALS AND METHODS Data collection The study protocol and the informed consent form were approved by the Ethics Committee of the National Taiwan University Hospital. Children ranging from 2 to 18 years of age with sleep problems related to OSA were recruited from the respiratory, pediatric, psychiatric and otolaryngologic clinics between January 2009 and December The exclusion criteria were (1) previous tonsil, adenoid or pharyngeal surgery, (2) cranio-facial anomalies, (3) genetic disorders, neuromuscular diseases, cognitive deficits or mental retardation. Demographic data, clinical symptoms and physical examinations were recorded. Adenoid size was determined based on lateral cephalometric radiographs. 14 The adenoidal/nasopharyngeal ratio was defined as the ratio of adenoidal depths to the nasopharyngeal diameter. An adenoidal/ nasopharyngeal ratio higher than 0.67 was considered adenoid hypertrophy. 9,14 The tonsils were graded based on the scheme of Brodsky et al.: 15 grade I) small tonsils confined to the tonsillar pillars; grade II) tonsils that extend just outside the pillars; grade III) tonsils that extend outside the pillars, but do not meet in the midline; grade IV) large tonsils that meet in the midline. Tonsillar hypertrophy was defined as grade III or above. 9,15 Body weight status Height (to the nearest 0.1 cm) was measured with a stadiometer (Cambridge, MD, UK). Weight was measured to the nearest 0.1 kg using 1 Department of Otolaryngology, National Taiwan University Hospital, Taipei, Taiwan; 2 Sleep Center, National Taiwan University Hospital, Taipei, Taiwan; 3 Department of Otolaryngology, Taipei Hospital, Department of Health, New Taipei City, Taiwan; 4 Institute of Epidemiology and Preventive Medicine, College of Public Health, National Taiwan University, Taipei, Taiwan; 5 Department of Pediatrics, National Taiwan University Hospital, Taipei, Taiwan and 6 Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan. Correspondence: Dr W-C Hsu, Department of Otolaryngology, National Taiwan University Hospital, #7, Chung-Shan South Road, Taipei 10002, Taiwan. hsuwc@ntu.edu.tw Presented at the 11th International Congress of the European Society of Pediatric Otorhinolaryngology (ESPO2012), Amsterdam, May, These authors contributed equally as first authors. Received 10 September 2012; revised 18 October 2012; accepted 28 October 2012; published online 27 November 2012

2 528 a calibrated scale. The age and gender corrected body mass index (BMI) was applied for each child by using an established guidelines. 9,16 The children were then divided into the following four groups: underweight (BMI less than or equal to the 5th percentile); normal weight (BMI higher than the 5th percentile but less than the 85th percentile); overweight (BMI higher than the 85th percentile but less than the 95th percentile) and obese (BMI higher than the 95th percentile). 16 Polysomnography Overnight polysomnography (PSG) (Embla N7000, Medcare Flaga, Reykjavik, Iceland) was performed in the sleep lab following the protocol as previously described. 17 The sleep stage and respiratory event was scored according to the American Academy of Sleep Medicine standard. 18 Obstructive apnea was defined as the presence of continued inspiratory effort associated with 490% decrease in airflow for a duration of X2 breaths. Hypopnea was defined as X50% decrease in airflow for a duration of X2 breaths associated with arousal, awakening or reduced arterialoxygen saturation in X3%. All of the sleep studies were analyzed by the same investigator to maximize inter- and intra-scorer reliability. The diagnosis of pediatric OSA was defined as the presence of an apnea/ hypopnea index (AHI) X1 event per hour in the overnight polysomnographic studies. 7,19 Residual OSA is defined as AHI X1 after T&A. Adenotonsillectomy Tonsillectomy was performed using the coblation method, and adenoidectomy was performed using the microdebrider-assisted method. 20 All surgical procedures were performed in a single-stage under general anesthesia with 2 to 3 days of hospitalization. Statistical analysis Data were analyzed using SPSS software (SPSS Inc., version 17.0, Chicago, IL,USA). Continuous data were expressed as mean and s.d., and categorical data as number and percentage. Continuous data of the four weight status groups were compared using one-way analysis of variance with the Bonferroni post hoc procedure, and categorical data were compared using the chi-square test. Pre- and post-operative sleep parameters were compared using a paired t-test. The odds ratios and 95% confidence intervals of the four groups having residual OSA were calculated using logistic regression analysis. A P value of less than 0.05 was considered statistically significant. RESULTS Study population Of the 215 children, 54 were excluded, leaving a total of 161 in the final analysis. All the 161 children had clinical OSA related symptoms, a preoperative PSG diagnosis of OSA (AHI X1) and repeated PSG postoperatively. Of the 54 subjects, who were excluded, 29 had incomplete PSG data, 18 had AHI o1 before T&A, and one had previous adenoid surgery. Another six children were excluded owing to underlying conditions, including cranio-facial anomalies (n ¼ 2), genetic disorder (n ¼ 1) and neuromuscular diseases (n ¼ 3). The mean age of all study participants was 7.0±3.4 years (78.3%, 126/161 boys). Eighteen were toddlers (o3 years), 71 were preschool age (3 5 years), 60 were school age (6 12 years) and 12 were adolescents (13 18 years). Tonsillar hypertrophy was observed in 88.8% (143/161) of all children, and adenoid hypertrophy was found in 65.2% (105/161). Table 1 summarizes the demographic data of the children by different weight status. Twenty-four children were underweight, 79 were normal weight, 22 were overweight and 36 were obese. The four groups did not significantly differ in gender, history of allergy, adenotonsillar hypertrophy and time interval from PSG to T&A. The only difference was that the obese group was slightly older than the normal weight group (P ¼ 0.045). PSG before and after T&A by different body weight status Before T&A, the obese children had the highest AHI, although this was statistically insignificant. The four groups did not significantly differ preoperatively in terms of other sleep parameters including total sleep time, percent of rapid-eye movement sleep, obstructive index, hypopnea index, average oxygen saturation, minimum oxygen saturation and arousal index. Table 2 compares the pre- and post-operative sleep studies among the four groups. Post-T&A, sleep studies found that all four groups significantly improved in AHI, hypopnea index, minimum oxygen saturation and arousal index. Additionally, the obstructive index significantly improved in the underweight, normal weight and obese children, and average oxygen saturation significantly improved in the normal weight, overweight and obese children. Residual OSA after T&A After T&A, 49.1% of the children (79/161) had residual OSA (defined as AHI X1). Of all the 161 children, 23.0% (37/161) had a AHI higher than 2, and 5.0% (8/161) had a AHI higher than 5 postoperatively. Residual OSA (AHI X1) rates in the underweight, normal weight, overweight and obese groups were 33.3, 44.3, 40.9, and 75%, respectively. Odds ratios and 95% confidence intervals having residual OSA (AHI X1) after T&A, indicated that the obese children had a significantly higher incidence of residual OSA than the normal weight children (odds ratio ¼ 3.77, Po0.01). There were no significant differences in the incidence of residual OSA between the underweight, normal weight and overweight children. Similar results could also be achieved even when residual OSA was defined as AHI X2 postoperatively (Table 3). Shifts of body weight status after T&A Figure 1 and Table 4 present the shifts in body weight status after T&A. Within a 6-month follow-up period, the most remarkable Table 1. Demographic data of the children by different weight status Age, years 6.6± ±3.2 a 8.1± ±3.7 Gender (male, %) 18 (75.0) 66 (83.5) 16 (72.7) 26 (72.2) Allergy, % 18 (75.0) 60 (75.9) 18 (81.8) 28 (77.8) Tonsillar hypertrophy, % 21 (87.5) 68 (86.1) 20 (90.9) 34 (94.4) Adenoid hypertrophy, % 18 (75.0) 56 (70.9) 14 (63.6) 24 (66.7) Days between pre-op PSG and T&A 67.7± ± ± ±66.4 Days between T&A and post-op PSG 70.6± ± ± ±93.0 Abbreviations:,PSG, polysomnography; T&A, adenotonsillectomy. Note: Continuous data are expressed as mean±s.d., and categorical data as N (%) a P ¼ vs obesity group. International Journal of Obesity (2013) & 2013 Macmillan Publishers Limited

3 Table 2. Sleep parameter changes following T&A in the children by different weight status Pre OP Post OP P-value Pre OP Post OP P-value Pre OP Post OP P-value Pre OP Post OP P-value Total sleep time (min) 381.1± ±50.9 NS 395.4± ±5.0 NS 376.2± ±32.6 NS 375.3± ±71.6 NS REM (%) 20.5± ±5.2 NS 20.2± ±0.7 NS 18.0± ±5.7 NS 18.3± ±6.4 NS AHI (events/h) 13.7± ±3.0 o ± ±0.6 o ± ±1.0 o ± ±2.4 o ± ±0.4 o ± ±0.5 o ± ±0.4 NS 8.5± ±0.6 o0.01 Obstructive index (events/ h) Central index (events/h) 0.8± ±0.6 NS 0.6± ±0.1 NS 0.3± ±0.6 NS 0.5± ±0.7 NS Hypopnea index (events/h) 5.6± ±3.0 o ± ±0.2 o ± ± ± ±2.3 o ± ±0.7 NS 97.4± ±0.1 o ± ±0.6 o ± ±1.1 o0.01 Average oxygen saturation (%) 83.7± ±4.5 o ± ±0.5 o ± ±4.0 o ± ±6.3 o0.001 Minimum oxygen saturation (%) Arousal index (events/h) 5.9± ±2.5 o ± ±0.2 o ± ±2.2 o ± ±1.7 o0.001 Abbreviations: AHI, apnea/hypopnea index; NREM, non-rapid eye movement; NS, not significant; REM, rapid eye movement. Note: Continuous data are expressed as mean±s.d., and categorical data as N (%). change was that 54% (13/24) of the underweight children gained body weights and shifted to normal weight status. Moreover, the normal weight group had a 9% (7/79) shift to overweight status and 4% (3/79) shift to underweight status. The overweight group had a 27% (6/22) shift to obesity and a 14% (3/22) shift to normal weight status. Interestingly, most obese children (92%, 33/ 36) remained obese after T&A, with only 8% (3/36) shifting to overweight status. DISCUSSION This study elucidates how body weight impacts on surgical outcomes, as well as how surgery impacts on body weight status in children with OSA. Underweight, normal weight and even overweight children had satisfactory surgical outcomes, although childhood obesity was a strong factor related to a poor surgical outcome. Another finding in our study was that T&A resulted in shifts of body weight status, most notably in children with underweight status. These findings provide clinicians with a weight status based perspective when treating children with OSA. T&A is widely regarded as the standard first-line therapy for pediatric OSA. 7 Recent studies have focused on poor outcome determinants after T&A. 12 Obesity has been shown to be a predictor of poor surgical outcomes. 12,19,21 23 However, the reasons why OSA in obese children is less likely to be cured remain contentious. Some authors have suggested that a higher preoperative AHI in obese children may be a cause, since severe OSA is less likely to be cured by T&A independent of obesity. 24 Others have suggested that obesity and AHI at diagnosis are both major determinants for surgical outcomes. 12 Adipose tissue deposited in obese children around the pharynx and neck, along with hypertrophic adenoid and tonsils compresses the pharynx and reduces its cross-sectional area. 10 The preoperative AHI in our obese children was not significantly higher than those of the other three weight groups. The mechanism of OSA in our obese children was more likely to be caused by multilevel obstructions, similar to those found in obese adults, and, therefore, less amenable to be cured by T&A. Residual OSA after T&A is also of major concern in treating pediatric OSA. Recent studies have noted the pervasiveness of residual of disease in the treatment of OSA. 19,21,24,25 Bhattacharjee et al. reported 72.8% residual OSA (AHI X1) in a study group, which included 50.6% obese children. 19 Additionally, Ye et al. found a 31% residual rate of OSA (AHI X1) in an Asian study group with 21.4% obesity. 25 Obese children comprised 22.4% of our study participants and the residual OSA rate was 49.1%. Since obesity is associated with residual OSA postoperatively, it is reasonable to suggest that the rate of residual OSA may be in direct proportion to the percentage of obese patients in study groups. Additional therapeutic options after T&A should be further studied in obese children with OSA. OSA syndrome and growth failure have been shown to correlate with each other Adenotonsillar hypertrophy is the primary cause of OSA, 2 and obstructive hypertrophic adenoids and tonsils in children with OSA further contribute to growth failure. 26,29 The American Academy of Pediatrics also identified growth failure as a serious complication of untreated OSA. 30 The pathophysiological pathway from sleep disturbances to growth failure/underweight status is of major concern in pediatricsleep medicine. Of the potential pathways, growth hormone hypotheses have received the most attention. 31 Interruptions in slow-wave sleep can lead to impaired growth hormone secretion. 13 Another proposed pathway involves increased energy expenditure during sleep in children with sleep disturbances. Higher energy expenditure in children with a low body weight, and decreased energy expenditure following T&A support this theory & 2013 Macmillan Publishers Limited International Journal of Obesity (2013)

4 530 Table 3. Residual OSA after T&A by different weight status AHIX1 8 (33.3) 35 (44.3) 9 (40.9) 27 (75.0) OR (95% CI) 0.63 ( ) Reference 0.87 ( ) 3.77 ( ) a AHIX2 3 (12.5) 13 (16.5) 4 (18.2) 17 (47.2) OR (95% CI) 0.73 ( ) Reference 1.13 ( ) 4.54 ( ) a AHIX5 1 (4.2) 3 (3.8) 0 (0.0) 4 (11.1) OR (95% CI) 1.10 ( ) Reference N.A ( ) Abbreviations: AHI, apnea/hypopnea index; CI, confidence interval; N.A. not applicable; OR, odds ratio; OSA, obstructive sleep apnea. Note: Categorical data were presented as N (%). a Po0.01. Figure 1. Shift of body weight status following T&A in children with OSA. Data were presented as a percentage of change in an individual body weight status group. Table 4. Body weight status before and after surgery in children with OSA syndrome After T&A Underweight Normal Overweight Obese Before T&A Underweight 11 (46) 13 (54) 0 (0) 0 (0) (n ¼ 24) Normal (n ¼ 79) 3 (4) 69 (87) 7 (9) 0 (0) Overweight 0 (0) 3 (14) 13 (59) 6 (27) (n ¼ 22) Obese (n ¼ 36) 0 (0) 0 (0) 3 (8) 33 (92) Abbreviations: T&A, adenotonsillectomy. Note: Data were presented as number (%). The correlations between OSA and underweight status are often overlooked in the clinical setting, and clinical physicians do not routinely screen for obstructive sleep disorders in children with delayed growth. 32,33,31 By using the same approach as in the current study to define body weight status, Mitchell et al. reported the prevalence of underweight status in children who underwent T&A as follows: 9% (7/79) in children with OSA, % (3/29) in children with severe OSA, 34 and 25% (5/20) in children with OSA and aged younger than 3 years. 35 Wang et al. 36 reported a prevalence rate of children with weight less than the 10th percentile of 20% in those with OSA who underwent T&A. In our study, 14.9% (24/161) of the children had an underweight status. The prevalence of underweight status in children undergoing T&A is estimated to be 9% 25% from the limited published data. Furthermore, to the best of our knowledge, a comparative study has never been performed for surgical outcomes in children with underweight and other weight statuses. Therefore, this study is the first to clearly demonstrate that underweight status and normal weight status children have similar surgical outcomes for OSA. This study also emphasizes anthropometric changes after T&A. Most previous studies found that children significantly increased in weight and height following T&A. 13,37,38 Interestingly, increases in height and weight have not only been found in children with underweight status, but also in normal weight and obese children. 39,40 However, exactly how body weight status changes following T&A has not been well studied. In the current study, around half of the underweight children gained body weights and shifted to normal weight status, and most obese children remained obese following T&A. All of our findings are consistent with the previous studies, in which increased weight and height appeared to occur in the overwhelming majority of children, despite differences in body weight status. There are several limitations to this study. First, the sample size was not large enough to compare the effects of other variables such as age, gender and race on surgical outcomes and body weight changes. Second, the follow-up period in this study was relatively short. We recommend that future studies should thoroughly investigate whether body weight status change is maintained over a long-term period. Third, polysomnographic evaluation is only one of several outcome measurements for pediatric OSA. Behavior, quality of life, biomarkers, metabolic profiles and neurocognitive tests are all imperative outcome measures in evaluating children with OSA. Further research is, International Journal of Obesity (2013) & 2013 Macmillan Publishers Limited

5 therefore, needed to investigate differences in these outcome measures between the different weight status groups. Despite these limitations, this study significantly contributes to clinical efforts to address body weight status and pediatric OSA. Underweight status children had excellent surgical outcomes and normalized weight status postoperatively. Most obese children remained in obesity after T&A with a high incidence of residual diseases. This study provides further evidence based correlations between body weight status, surgery and pediatric OSA syndrome. CONCLUSIONS Treating OSA in children with T&A was associated with shifts in body weight status, most notably in children with underweight status. T&A is a satisfactory treatment for OSA in children with underweight, normal weight and overweight status. However, most obese children had residual OSA following T&A, thus warranting additional therapeutic strategies postoperatively. 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