Adenotonsillectomy for Obstructive Sleep Apnea in Children With Prader-Willi Syndrome
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1 Pediatric Pulmonology 41:74 79 (2006) Adenotonsillectomy for Obstructive Sleep Apnea in Children With Prader-Willi Syndrome M. Pavone, MD, 1 * M.G. Paglietti, MD, 1 A. Petrone, MD, 1 A. Crinò, MD, 2 G.C. De Vincentiis, MD, 3 and Renato Cutrera, MD, PhD 1 Summary. The aim of our study was to evaluate the efficacy of adenotonsillectomy for the treatment of obstructive sleep apnea syndrome (OSA) in pediatric patients with Prader-Willi syndrome (PWS), and to describe the postoperative complications. Five patients (4 males; median age, 4.4 years; range, years) were studied. All patients underwent an overnight cardiorespiratory sleep study. All patients had adenotonsillar hypertrophy (ATH), and two were also obese. The preoperative obstructive apnea/hypopnea index (AHI; median and range) was 12.2 ( ) events/hr; the mean oxygen saturation was 95 (79 96)%; the nadir oxygen saturation was 71 (58 78)%; and the oxygen desaturation index (ODI) was 15.8 ( ) events/hr. Preoperatively, patients were classified as having moderate to severe OSA. A second sleep study, performed 16 (3 43) months after adenotonsillectomy, showed a significant decrease in AHI (P ¼ 0.009) and ODI (P ¼ 0.009). Mean and nadir oxygen saturation did not differ significantly postsurgery (P ¼ 0.188, P ¼ 0.073, respectively). Four out of five children showed at least one postoperative complication. Difficult awakening from anesthesia, hemorrhages, and respiratory complications requiring reintubation and/or supplemental oxygen administration were observed. In conclusion, patients with PWS and OSA who underwent adenotonsillectomy showed a significant decrease in AHI and number of oxygen desaturations. Pediatr Pulmonol. 2006; 41: ß 2005 Wiley-Liss, Inc. Key words: obstructive sleep apnea; adenotonsillar hypertrophy; adenotonsillectomy; obesity; Prader-Willi syndrome. INTRODUCTION Prader-Willi syndrome (PWS) is a congenital condition caused by a genetic defect involving the paternal chromosome 15. A microdeletion of the long arm of chromosome 15 (15q 11 q13), or a maternal uniparental disomy, was demonstrated in approximately 70% and in 28% of cases, respectively. Mutation in the imprinting center was reported only in a minority of cases (1 2%). 1,2 PWS is clinically characterized by neonatal hypotonia, failure to thrive, early childhood obesity, characteristic facial appearance, small hands and feet, hypogonadism, several central nervous system abnormalities, mild mental retardation, short stature, and behavioral disorders (e.g., hyperphagia). 3 Hypothalamic dysfunction was considered for the clinical manifestation. 4 Hypotonia and obesity are considered important risk factors for developing sleep-disordered breathing (SDB) in PWS. 5 Adenotonsillar hypertrophy (ATH) is the leading cause of obstructive sleep apnea syndrome (OSA) in childhood, and the peak age for adenoid and tonsillar hypertrophy with related OSA is 3 6 years. Adenotonsillar hypertrophy frequently narrows the nasopharynx and oropharynx, leading to partial or complete obstruction of the upper airways. 6 In childhood, if ATH is the predominant factor ß 2005 Wiley-Liss, Inc. contributing to OSA, adenotonsillectomy (A&T) represents the first line of treatment. 6 8 The complication rate after adenotonsillectomy ranges from 0 32%. 9,10 More than 20% of children with OSA have respiratory compromise. Several studies identified the population at high risk for postoperative complications. 11,12 Preoperative sleep studies and postoperative overnight observation were 1 Respiratory Unit, Bambino Gesù Children s Research Hospital, Rome, Italy. 2 Endocrinology Unit, Bambino Gesù Children s Research Hospital, Rome, Italy. 3 Otorhinolaryngology Unit, Bambino Gesù Children s Research Hospital, Rome, Italy. *Correspondence to: Martino Pavone, M.D., Bambino Gesù Children s Research Hospital, Piazza S. Onofrio 4, Rome, Italy. pavone@opbg.net Received 8 July 2005; Accepted 27 August DOI /ppul Published online 10 November 2005 in Wiley InterScience (
2 Adenotonsillectomy in Prader-Willi Syndrome 75 recommended for patients at high risk for postoperative complications. 12 Many studies were previously published about sleepdisordered breathing (SDB) in PWS. Nevertheless, few data are available about adenotonsillectomy for the treatment of OSA in these patients. The aim of our study was to evaluate the efficacy of A&T for the treatment of OSA in children with PWS, and to describe the postoperative complications. METHODS Subjects From January 2000 May 2005, all patients diagnosed with PWS (54 subjects) and followed in the Endocrinology Unit of our hospital had undergone an overnight cardiorespiratory sleep study as part of an ongoing study on the characteristics of their SDB. From these patients, we selected five children according to the following inclusion criteria: 1) age range, 1 18 years; 2) no prior history of tonsillectomy and/or adenoidectomy; 3) presence of pathological adenotonsillar hypertrophy (see below for definitions); 4) presence of moderate to severe OSA confirmed by sleep study (see Results). The diagnosis of PWS was established according to consensus clinical criterion, 3 and was confirmed by genetic analysis, including a methylation test and/or fluorescent in situ hybridization (FISH) test for chromosome 15. For each subject, the body mass index (BMI) was calculated, and obesity was defined according to criteria for children. 13 All patients underwent a complete ear, nose, and throat (ENT) examination, including anterior rhinoscopy, oroscopy, and nasal endoscopy with a flexible fiberoscope. Tonsils were classified as grade I, occupying less than 25% of the oropharynx; grade II, occupying more than 25% and less than 50% of the oropharynx; grade III, occupying more than 50% and less than 75% of the oropharynx; and grade IV, occupying more than 75% of the oropharynx. Tonsil hypertrophy grades III and IV were considered pathological. Adenoid size was measured by estimating the percentage of the posterior choanal area that was ABBREVIATIONS AHI A&T ATH BMI CAI GH ODI OSA PWS SDB TST Obstructive apnea/hypopnea index Adenotonsillectomy Adenotonsillar hypertrophy Body mass index Central apnea index Growth hormone Oxygen desaturation index Obstructive sleep apnea syndrome Prader-Willi syndrome Sleep-disordered breathing Total sleep time occluded by adenoid tissue. Adenoid hypertrophy was graded as follows: grade I, the adenoid obstructing less than 25% of the choana; grade II, the adenoid obstructing less than 50% of the choana; grade III, the adenoid obstructing more than 50% and less than 75% of the choana; and grade IV, the adenoid obstructing more than 75% of the choana. Adenoid hypertrophy grades III and IV were considered pathological. Before monitoring, information about clinical history and medications was obtained from the parents of each patient. Snoring, breathing difficulty during sleep, and apneas were reported for all subjects. Three patients were receiving growth hormone treatment at the time of the baseline sleep study. The decision to perform adenotonsillectomy was based on clinical symptoms, with OSA proven by sleep study and evidence of adenotonsillar hypertrophy. The Ethics Committee of our hospital approved this clinical study, and one parent of every child gave written informed consent. Sleep Study Sleep studies were performed on the respiratory ward, and were supervised by experienced nurses. All studies were commenced at the child s usual bedtime, and were performed in a dark, quiet room. No sedation or sleep deprivation was used. All patients were accompanied by one of their parents throughout the night. A SomnoStar PT2 (Sensor Medics Corp.) seven-channel recorder was used to measure heart rate, pulse rate, pulse waveforms, arterial oxygen saturation (SaO 2 ), and calibrated respiratory inductive plethysmography (RIP; thoracic, abdominal, and summation channels). This technique was previously used in children, and technical details were published elsewhere. 14,15 Oronasal airflow was additionally measured via a thermistor, using an auxiliary channel of the equipment. Sleep respiratory events and behavior were recorded by an infrared video camera. End-tidal carbon dioxide (PETCO 2 ) was measured by capnography (CO2SMO, Novametrix Medical Systems, Wallingford, CT). The capnograph was calibrated before each study. For this study, we measured the mean and peak PETCO 2 (in mmhg) and the percent of total sleep time (see below for definition) spent with a PETCO 2 above 45 mmhg. Respiratory Parameters Obstructive apneas were detected when the absence of airflow was associated with the presence of chest/ abdominal wall motion, and were quantitated when they were longer than two respiratory cycle times. Obstructive hypopneas were detected when the reduction of airflow 50% was associated with the presence of chest/abdominal wall motion and with desaturation 4%. Central
3 76 Pavone et al. apneas were detected when the absence of airflow was not associated with chest or abdominal motion, and were quantitated when they were 10 sec long or of any length associated with 4% desaturation. Central apneas were also quantitated when they were equal to or longer than 20 sec. Mixed apneas had both a central component (3-sec duration, or twice the respiratory cycle length) and an obstructive component (of any length). Apneas occurring immediately following body movements or sighs were excluded. The obstructive apnea/hypopnea index (AHI) was defined as the number of mixed/obstructive apnea/ hypopneas per hour of sleep. Obstructive sleep apnea for this study was defined as an AHI 1 event/hr. 7,8,16,17 The central apnea index (CAI) was defined as the number of central apneas per hour of sleep. Oximetry artifacts in the pulse waveform tracing were discarded manually following visual inspection of traces, and oxygen desaturation index (ODI) was defined as the number of desaturations (drop in SaO 2 4% of baseline value) per hour of sleep. Periodic breathing (PB) was defined as three or more respiratory pauses of 3-sec duration, with <20 sec of normal respiration between pauses. The total amount of PB was calculated in minutes and expressed as a percentage of total sleep time (see below for definition). Because of the absence of electroencephalographic recordings, sleep and wakefulness were distinguished using regularity of cardiorespiratory signals, behavioral observations, and the subject s appearance on video. This method was previously validated and found to have overall agreement with conventional polysomnography for a sleep/wakefulness discrimination of 94%. 16 Total sleep time (TST) was quantitated, and respiratory parameters were expressed as a percentage of TST. Statistical Analysis Statistical analysis was performed using the SPSS for Windows program, version 9.0 (SPSS, Inc., Chicago, IL). Data are expressed as median and range, except where otherwise specified. Statistics for nonparametric data were used because of the low number of subjects studied. Sleep study results before and after adenotonsillectomy were compared using the Mann-Whitney U-test for nonparametric data. The level of significance was set at RESULTS Subject Characteristics Detail about population characteristics are provided in Table 1. All subjects had a positive methylation test; a deletion of chromosome 15 q11 q13 was detected by FISH in 3 subjects. All subjects had ATH, and 2 were obese. Sleep Study Findings A summary of sleep study findings is provided in Table 1. All patients had moderate to severe OSA. One patient had central apneas 20 sec. Sleep Study Findings After Adenotonsillectomy A second cardiorespiratory sleep study was performed 16 (3 43) months after A&T. The median delay between surgery and postoperative sleep study was due to one child being temporarily lost at follow-up and revaluated several months after surgery. Details about improvement after surgery are shown in Table 1. We found a significant decrease in AHI, number of oxygen desaturations, TABLE 1 Pre- and Postoperative Characteristics of PWS Patients Studied 1 Pre-A&T (n ¼ 5) Post-A&T (n ¼ 5) P value Age (years) 4.4 ( ) 6.1 ( ) BMI (kg/m 2 ) 18.7 ( ) 19.6 ( ) TST (hr) 8.6 ( ) 7.7 ( ) CAI (events/hr) 0.1 ( ) 1.9 ( ) AHI (events/hr) 12.2 ( ) 1.6 ( ) SaO 2 mean (%) 95 (79 96) 97 (94 97) SaO 2 nadir (%) 71 (58 78) 86 (71 91) SaO 2 < 90% (%TST) 7.2 ( ) 0.9 ( ) ODI (events/hr) 15.8 ( ) 2.2 ( ) Periodic breathing (%TST) 0.1 ( ) 1.8 ( ) Mean PETCO 2 (mmhg) 41.7 (40 48) 43.9 (41 50) Peak PETCO 2 (mmhg) 49 (47 68) 52 (45 58) PETCO 2 > 45 mmhg (%TST) 7 (1 27) 12 (0 42) Unless otherwise specified, results are given as median and range. PWS, Prader-Willi syndrome; A&T, adenotonsillectomy; BMI, body mass index; TST, total sleep time; CAI, central apnea index; AHI, mixedobstructive apnea/hypopnea index; SaO 2 mean, mean oxygen saturation value; SaO 2 nadir, lowest oxygen saturation value; ODI, Oxygen desaturation index; SaO 2 < 90%, percentage of TST spent with saturation value below 90%; PETCO 2, end tidal CO 2 ; PETCO 2 > 45 mmhg (%TST), percent of total sleep time spent with PETCO 2 above 45 mmhg.
4 Adenotonsillectomy in Prader-Willi Syndrome 77 and percent of time spent with oxygen saturation below 90%. Mean and nadir oxygen saturation did not differ significantly after A&T. AHI fell below 1 event/hr in one patient, and was nearly normal in the others (Fig. 1). Oxygen desaturations below 90% were found in 4 out of 5 patients after A&T. Table 2 also reports detailed data about BMI and durations of GH treatment. Children treated with GH (0.25 mg/kg/week) improved for OSA as well as those untreated. In the postoperative sleep study, the child treated for the longest time (38 months) showed improvement of OSA, but a higher level of PETCO 2 (mean PETCO 2 increased from 40 mmhg to 50 mmhg; peak PETCO 2 increased from 47 to 58 mmhg; %TSTwith PETCO 2 >45 mmhg increased from 3% to 18% of TST) and an increased number of central apneas (from 1.2 to 3.7 events/hr of sleep). At the time of the postoperative sleep study, parents of all children reported an overall improvement in snoring, breathing difficulty during sleep, and perception of apneas during sleep. Postoperative Complications Postoperative complications were observed in our PWS patients. Difficult awakening from anesthesia, hemorrhages, laryngospasm, supplemental oxygen administration, and/or reintubation were reported. Four out of 5 patients showed at least one postoperative complication. Details of postoperative complications are given in Table 2. DISCUSSION In this study, we evaluated the breathing pattern during sleep before and after adenotonsillectomy in 5 children with PWS and OSA. All patients improved after surgery. Postoperative complications were observed in the majority of them. Childhood OSA management is based on a combination of clinical evaluation, confirmation of OSA through a sleep study, and evaluation of treatment options. 7,8 Childhood OSA is frequently associated with adenotonsillar hypertrophy. Several facts suggest that OSA is due to a combination of structural and neuromuscular factors. AHI (events/hr) PREOPERATIVE AHI POSTOPERATIVE AHI Fig. 1. Pre- and postoperative mixed-obstructive apnea/hypopnea index (AHI) in 5 children with PWS. Postoperative AHI was obtained 16 (3 43) months after adenotonsillectomy. TABLE 2 Preoperative Characteristics and Postoperative Complications 1 Age at surgery (years) Postoperative complications Preoperative SaO2 nadir (%) Preoperative AHI (events/hr) GH treatment duration (months) Presence of comorbidities BMI (kg/m 2 ) Patients (sex) P.P. (male) None Mild hemorrhage S.G. (male) Obesity No complications S.S. (male) None Difficult awakening from anesthesia M.S. (male) None Hemorrhage laryngospasm, reintubation, O 2 therapy 2 in PICU B.M. (female) Obesity O 2 therapy 2 for 48 hr, first postoperative 24 hr in PICU 1 PICU, pediatric intensive care unit; AHI, mixed-obstructive apnea/hypopnea index; SaO2 nadir, lowest oxygen saturation value; BMI, body mass index; GH, growth hormone. 2 O2 therapy, supplemental oxygen administration.
5 78 Pavone et al. However, the relative contribution of each component cannot be predicted. 6 Adenotonsillectomy represents the treatment of choice in children, and it is curative in % of children with OSA, even if the children are obese. 7,8,18 Additional treatment options are available for children who do not respond to A&T, or the small minority in whom A&T is contraindicated or delayed. 7,8 Continuous positive pressure ventilation (CPAP) was reported to be effective in both infants and children 19 Sleep studies should be performed postoperatively to evaluate the resolution of OSA and/or hypoventilation, 5 especially for obese 18 or hypotonic patients, and for those with other contributing factors to OSA which are less likely to have complete resolution of OSA after surgery. Management of OSA in children with PWS is similar to that recommended for healthy children; few data are available about A&T in children with PWS. Nixon and Brouillette 5 reported on a 7-year-old girl with a preoperative AHI greater than 100 obstructive apneas and hypopneas per hour, with multiple respiratory arousals and desaturations (lowest oxygen saturation, 50%). Adenotonsillectomy led to a reduction in AHI to 2.8 events/hr. Despite the progressive increase in body weight, the following sleep studies were negative for OSA. Her parents reported resolution of snoring and an improvement in her daytime sleepiness and behavior. Conversely, Schluter et al. 20 described persistent irregular findings in 3 PWS children studied after adenotonsillectomy. All our patients showed preoperatively moderate to severe OSA and marked adenotonsillar hypertrophy; 2 patients were also obese. After adenotonsillectomy, we found a significant improvement in OSA (AHI decreased from 12.2 to 1.6 events/hr), along with number of oxygen desaturations and percent of time spent with oxygen saturation below 90%. A limitation of this study was that the postoperative sleep study was performed 16 (3 43) months after A&T. This delay was due to one child being temporarily lost at follow-up and reevaluated several months after surgery. Considering this delay, we cannot completely attribute the improvement of OSA to surgery. Nevertheless, it is reasonable to consider A&T as effective in the treatment of OSA, because BMI did not increase significantly between the pre- and postoperative sleep study. Recently, there has been much interest in growth hormone (GH) treatments of PWS children Several reports stressed the improved body composition and other physical and mental benefits. 21,22 Deaths of children with PWS are reported among GH-treated as well as untreated children. 21 A possible contribution of GH to these events has not yet been definitively excluded. 23 Before institution of GH therapy, it is recommended for all these patients to have a sleep study and otorhinolaryngologic examination performed, and tonsillectomy in the case of enlarged tonsils. 21 In our study, 3 out of 5 patients were treated with GH. Children treated with GH improved for OSA as well as those untreated. In the postoperative sleep study, the child who experienced the longest treatment (38 months) showed improvement of OSA, but a higher level of PETCO 2 and increased number of central apneas. Due to our limited data, we cannot relate these changes in respiratory pattern to the GH treatment. Furthermore, we cannot rule out that once A&T was performed, these changes could be related to the natural history of his SDB. OSA is a dynamic process resulting from a combination of structural and neuromotor abnormalities. 6 PWS patients are at increased risk for obstructive sleep apneas for several reasons, including not only adenotonsillar hypertrophy, but also obesity, facial dysmorphisms, 24 sticky secretions, hypotonia, and restrictive lung disease due to muscle weakness or scoliosis. In addition, in these patients, ventilatory and arousal responses to hypercapnia and hypoxia are both reduced and may contribute to worsening of OSA. 5 These considerations suggest the systematic postoperative reevaluation of OSA in all children with PWS, in order to evaluate the effective improvement and/or need for other treatment options. Potential complications of adenotonsillectomy include anesthetic complications, postoperative problems (e.g., pain, poor oral intake), hemorrhages, and respiratory complications such as worsening of OSA Death in the immediate postoperative period was also reported. 25 Several studies identified a high-risk profile for the development of postoperative complications. This profile includes age below 3 years, failure to thrive, obesity, cardiac complications such as right ventricular hypertrophy, craniofacial anomalies, neuromuscular disease, severe OSA, and sleep O 2 saturations <80%. 11,12,22 Although a low number of patients was studied, we found that the majority of them developed at least one postoperative complication. Preoperatively, 2 patients were younger than 3 years of age, 3 patients had an AHI greater than 10 events/hr, and all patients had nadir oxygen saturation levels below 80%. Difficult awakening from anesthesia, hemorrhages, respiratory complications requiring reintubation, and/or supplemental oxygen administration were observed. These findings suggest the need for monitoring of all pediatric patients with PWS after A&T because of the risk of postoperative complications. In conclusion, patients with PWS with OSA and pathological adenotonsillar hypertrophy who underwent adenotonsillectomy showed a significant improvement in AHI and oxygen saturation parameters. Caution should be taken regarding potential postoperative complications. REFERENCES 1. Holm VA. The diagnosis of Prader-Willi syndrome. In: Holm VA, Sulzbacher SJ, Pipes PL, editors. The Prader-Willi syndrome. Baltimore: University Park Press; p
6 Adenotonsillectomy in Prader-Willi Syndrome Butler MG. Prader-Willi syndrome: current understanding of cause and diagnosis. Am J Med Genet 1990;35: Holm VA, Cassidy SB, Butler MG, et al. Prader-Willi syndrome: consensus diagnostic criteria. Pediatrics 1993;91: Hanson J. A view of aetiology and pathogenesis of Prader-Willi syndrome. In: Holm VA, Sulzbacher SJ, Pipes PL, editors. The Prader-Willi syndrome. Baltimore: University Park Press; p Nixon GM, Brouillette RT. Sleep and breathing in Prader-Willi syndrome. Pediatr Pulmonol 2002;34: Marcus CL. Sleep-disordered breathing in children. Am J Respir Crit Care Med 2001;164: American Thoracic Society. Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med 1996;153: American Academy of Pediatrics, Section on Pediatric Pulmonology, Subcommittee on Obstructive Sleep Apnea Syndrome. Clinical practice guideline: diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2002;109: Slovik Y, Tal A, Tarasiuk A, et al. Complications of adenotonsillectomy in children with OSAS younger than two years of age. Int J Pediatr Otorhinolaryngol 2003;67: Berkowitz RG, Zalzal GH. Tonsillectomy in children under 3 years of age. Arch Otolaryngol Head Neck Surg 1990;116: Rosen GM, Muckle RP, Mahowald MW, et al. Postoperative respiratory compromise in children with obstructive sleep apnea syndrome: can it be anticipated? Pediatrics 1994;93: Biavati MJ, Manning SC, Phillips DL. Predictive factors for respiratory complications after tonsillectomy and adenoidectomy in children. Arch Otolaryngol Head Neck Surg 1997;123: Cole TJ, Bellizzi MC, Flegal KM, Dietz WH. Establishing a standard definition for child overweight and obesity worldwide: international survey. Br Med J [Clin Res] 2000;320: Cantineau JP, Escourrou P, Sartene R, Gaultier C, Goldman M. Accuracy of respiratory inductive plethysmography during wakefulness and sleep in patients with obstructive sleep apnea. Chest 1992;102: Morielli A, Ladan S, Ducharme FM, Brouillette RT. Can sleep and wakefulness be distinguished in children by cardiorespiratory and videotape recordings? Chest 1996;109: Marcus CL, Omlin KJ, Basinki DJ, et al. Normal polysomnographic values for children and adolescents. Am Rev Respir Dis 1992;146: Uliel S, Tauman R, Greenfeld M, Sivan Y. Normal polysomnographic respiratory values in children and adolescents. Chest 2004;125: Mitchell RB, Kelly J. Adenotonsillectomy for obstructive sleep apnea in obese children. Otolaryngol Head Neck Surg 2004;131: Massa F, Gonsalez S, Laverty A, Wallis C, Lane R. The use of nasal continuous positive airway pressure to treat obstructive sleep apnoea. Arch Dis Child 2002;87: Schluter B, Buschatz D, Trowitzsch E, Aksu F, Vestische AW. Respiratory control in children with Prader-Willi syndrome. Eur J Pediatr 1997;156: Eiholzer U. Deaths in children with Prader-Willi syndrome. A contribution to the debate about the safety of growth hormone treatment in children with PWS. Horm Res 2005;63: Carrel AL, Moerchen V, Myers SE, Bekx MT, Whitman BY, Allen DB. Growth hormone improves mobility and body composition in infants and toddlers with Prader-Willi syndrome. J Pediatr 2004;145: Allen DB, Carrel AL. Growth hormone therapy for Prader-Willi syndrome: a critical appraisal. J Pediatr Endocrinol Metab [Suppl] 2004;17: Richards A, Quaghebeur G, Clift S, Holland A, Dahlitz M, Parkes D. The upper airway and sleep apnoea in the Prader-Willi syndrome. Clin Otolaryngol 1994;19: Reider AA, Flanary V. The effect of polysomnography on pediatric adenotonsillectomy postoperative management. Otolaryngol Head Neck Surg 2005;32:
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