OSAS in children: correlation between endoscopic and polysomnographic findings

OSAS in children: Correlation between endoscopic and polysomnographic findings FABIANA C. P. VALERA, MD, MELISSA A. G. AVELINO, MD, MÁRCIA B. PETTERMANN, MD, REGINALDO FUJITA, MD, SHIRLEY S. N. PIGNATARI, MD, GUSTAVO A. MOREIRA, MD, MÁRCIA L. PRADELLA-HALLINAN, MD, SÉRGIO TUFIK, MD, and LUC L. M. WECKX, MD, São Paulo, Brazil OBJECTIVES: To correlate polysomnographic findings with clinical history of apnea, the degree of obstruction caused by tonsillar hypertrophy, and to age group. STUDY DESIGN AND SETTING: 267 children with a clinical diagnosis of obstructive sleep apnea (OSAS) were evaluated. Patients were divided into preschool- and school-age categories, and subdivided in 3 additional groups, according to tonsillar hypertrophy. Polysomnographic findings were compared within groups. RESULTS: 34% of children had history of OSAS and normal polysomnographic findings. Tonsillar hypertrophy was correlated to more severe apnea among preschool-age children, but not among school-age children. Among children with tonsillar hypertrophy, more severe apnea was observed in preschool-age children than in school-age children. CONCLUSIONS: There is little correlation between polysomnographic and clinical findings in children with OSAS. SIGNIFICANCE: Adenotonsillar hypertrophy leads to more severe polysomnographic patterns in preschool-age children. More severe apnea is observed in younger children with adenotonsillar hypertrophy than in older ones. (Otolaryngol Head Neck Surg 2005;132:268-72.) From the Division of Pediatric Otorhinolaryngology, Federal University of São Paulo (Drs Valera, Avelino, Pettermann, Fujita, Pignatari, and Weckx); the Division of Otorhinolaryngology, School of Medicine of Ribeirão Preto, University of São Paulo (Dr Valera); and the Division of Polysonmography, Federal University of São Paulo (Drs Moreira, Pradella-Hallinan, and Tufik), São Paulo, Brazil. Presented at the Annual Meeting of the American Academy of Otolaryngology–Head and Neck Surgery, San Diego, CA, September 22-25, 2003 and received the Foundation Award. Reprint requests: Fabiana C. P. Valera, Divisão de Otorrinolaringologia Pediátrica, Universidade Federal de São Paulo, Rua dos Otonis, 674 Vila Clementino, São Paulo SP Brazil; e-mail, facpvalera@uol.com.br. 0194-5998/$30.00 Copyright © 2005 by the American Academy of Otolaryngology–Head and Neck Surgery Foundation, Inc. doi:10.1016/j.otohns.2004.09.033 268 H ypertrophy of the adenoids and/or tonsils is considered to be the most important risk factor for the development of obstructive sleep apnea (OSAS) in children, particularly between 2 and 6 years of age.1 During this time period, enlargement of the adenoid and tonsil frequently narrows the nasopharynx and oropharynx leading to a partial or total obstruction of the upper airway. Snoring is the most frequent complaint by parents seeking medical evaluation for children with OSAS.2,3 However, there are other symptoms related to apneas that are occasionally encountered, which need to be specifically elicited. These symptoms include night sweats, night gasps, nocturnal enuresis, irritability, hyperactivity, behavioral problems, diminished attentiveness at school, and morning headache.3,4 Daytime sleepiness is not a common complaint among young children with OSAS because their sleeps are not as fragmented as those of adults with OSAS.3,5 According to Lipton,6 8% to 27% of children snore but only 2% of them have OSAS; the majority of these children have normal breathing patterns during the daytime,2 which makes the diagnosis more difficult to establish. The great majority of children who have OSAS snore, even though most children who snore do not have OSAS. It is important to stress that some infants with significant OSAS may not exhibit snoring.2 OSAS in children is characterized mostly by partial and persistent obstruction of the upper airway, instead of total and intermittent obstruction observed in adults. This obstruction pattern in children is called persistent hypoventilation, and it compromises their breathing pattern during sleep. Contrary to what is observed in adults, long-lasting partial obstruction in children can be as detrimental to respiration as intermittent total obstruction. Moreover, because children have diminished functional residual capacity when compared to adults, they present more severe symptoms in response to less aggressive forms of apnea.1,5 Apnea, hypopnea, and snoring occur as a consequence of a narrowed airway, which causes an increased respiratory effort. During sleep, particularly in the rapid eye movement (REM) phase, as body musculature relaxes, OSAS becomes accentuated, eliciting the symptoms mentioned above. Moreover, in a small proportion of children, more severe clinical sequelae Otolaryngology– Head and Neck Surgery Volume 132 Number 2 may occur, such as cor pulmonale, systemic arterial hypertension, failure to thrive, and mental retardation.3,6,7 Risk factors for the development of OSAS in children include hypertrophy of tonsils and/or adenoids, neuromuscular diseases associated with hypotonia, obesity, genetic diseases associated with the hypoplasia of the middle third of the face, micrognathia and a narrow nasopharynx, laryngomalacia, metabolic diseases, and brain malformations involving the skull base.2 The gold-standard exam for the definitive diagnosis of OSAS is polysomnography, but it is important to appreciate that the diagnostic criteria are different for adults and children. Applying adult diagnostic criteria to children will exclude many severe respiratory disturbances in children, and therefore decrease the incidence and the scale of OSAS.8,9 Many medical centers, including ours, follow the polysomnographic patterns for children standardized by the American Thoracic Society.2 Polysomnography is indicated not merely to differentiate apnea from primary snoring (which has no apnea, hypoventilation, or cardiovascular consequences), but also as a prognostic indicator.2 Children with severe apnea should be monitored during the immediate postoperative period after adenotonsillectomy or other pharyngeal surgical procedures (preferentially in an intensive care unit), and should be submitted to a subsequent polysomnographic examination, if possible. Unfortunately, the cost of this exam can be a limiting factor. Nevertheless, polysomnography is particularly useful when there is a clinical suspicion of OSAS but no clear evidence of adenotonsillar hypertrophy, as well as in children who present significant risk factors for developing associated apnea, such as craniofacial malformation and neurological diseases. The purposes of this study were: (1) to verify whether there is a correlation between clinical complaints of apnea and polysomnographic findings in children with adenotonsillar hypertrophy; (2) to determine whether there are polysomnographic patterns or differences between obstruction caused by adenoid hypertrophy alone and adenoid hypertrophy associated with tonsil hypertrophy; and (3) to make a polysomnographic comparison between children of different age groups. MATERIALS AND METHODS Two hundred and sixty-seven children with a clinical history of snoring and apnea were evaluated at the Division of Pediatric Otolaryngology of the Federal University of São Paulo from 1999 to 2002. All the selected patients had history of persistent (for more VALERA et al 269 than a 3-month period) snoring, with frequent apnea, defined as cessation of breathing during sleep, although parents could not precisely determine the number and the duration of these periods. The study group was composed by 143 boys and 124 girls, with ages ranging from 1 to 13 years of age (mean, 5.5 years). Children with craniofacial malformations, morbid obesity, genetic syndromes, and neurological diseases were excluded. Patients were divided into 2 age categories: the preschool group, which included children from 1 to 6 years of age (152 patients, 87 boys and 65 girls); and school children group, comprising patients from 7 to 13 years of age (115 children, 56 boys and 59 girls). The parents were asked to answer a questionnaire related to their children’s symptoms and to sign the informed consent if they agreed to participate to the study. All children underwent otorhinolaryngological examination including anterior rhinoscopy, oroscopy, and nasal endoscopy with 3.2-mm-diameter Machida flexible fiberscope. Tonsils were classified according to Brodsky into: grade 0, limited to tonsil fossa; grade I, tonsils occupy less than 25% of oropharynx; grade II, tonsils occupy more than 25% and less than 50% of oropharynx; grade III, tonsils occupy more than 50% and less than 75% of oropharynx; or grade IV, tonsils occupy more than 75% of oropharynx. Tonsils were subsequently classified as nonobstructive (grades 0, I, or II) or obstructive (grades III or IV). Adenoid size was measured by estimating the percentage of posterior choanal area that was occluded by adenoid tissue, and was classified as obstructive if it occupied more than 70% of posterior choana, or nonobstructive. The children in each age category were subdivided into 3 distinct groups: group 1, both tonsils and adenoids are nonobstructive; group 2, tonsils were nonobstructive but adenoids were obstructive; group 3, both tonsils and adenoids were obstructive (the 7 cases with obstructive tonsils and nonobstructive adenoids were included in this category for statistical reasons). All patients underwent polysomnographic examination during nocturnal sleep of at least 7 hours’ duration. Respiratory disturbance index/hour (RDI), i.e. the number of obstructive apneas and hypopneas per hour, minimal O2 saturation level (nadir), mean O2 saturation level, bradycardia, and arrhythmia/paradoxical inspiration were used to classify the results as normal, primary snoring, or mild, moderate, or severe apnea, based on the American Thoracic Society standardized criteria.2 To facilitate the polysomnographic analysis, only the 3 most important factors (RDI, nadir, and mean O2 270 VALERA et al saturation level) were evaluated. The arousal index was not analyzed. Sleeping pattern was classified according to RDI, nadir, and mean O2 saturation level: normal, RDI lower than 1.0 and nadir and mean O2 saturation greater than 90%; mild, RDI between 1.0 and 5.0 or nadir and mean O2 saturation lower than 90%; or moderate, RDI greater than 5.0 or nadir and mean O2 saturation lower than 85%. Statistical analysis were performed by means of Mann-Whitney test, stating significance at a P value of ⬍0.05. This study has followed the principles outlined in the Declaration of Helsinki. RESULTS The mean values (⫾SD) for age, RDI, nadir, and mean O2 saturation in all 3 groups of children of each age category are shown in Table 1. In preschool-age children, the mean values for RDI and nadir were categorized as a normal sleeping pattern (0.4 ⫾ 0.5 and 93.0 ⫾ 2.8, respectively) in group 1. Nevertheless, moderate apnea pattern was observed in groups 2 (5.1 ⫾ 10.4 and 85.4 ⫾ 16.2, respectively) and 3 (5.2 ⫾ 6.4 and 85.3 ⫾ 10.5, respectively). The mean O2 saturation levels were comparable to normal values in all 3 studied groups. In school-age children, the mean values for RDI were similar to those of mild apnea in group 1(1.0 ⫾ 1.6), group 2 (2.2 ⫾ 4.4), and group 3 (3.6 ⫾ 7.3). Nadir values corresponded to normal sleeping pattern in group 1 (92.2 ⫾ 4.4) and group 2 (91.2 ⫾ 5.9), but only to mild apnea in group 3 (87.4 ⫾ 13.3); the mean O2 saturation levels showed normal values in all 3 groups. In group 1 (without adenoid and/or tonsil obstruction), 30.5% had apnea detected by polysomnographic exams. Ninety-one children (39 in the preschool-age group and 52 in school-age group) presented with clinical complaints of snoring and apnea but did not exhibit polysomnographic evidence of OSAS. Statistical analysis of the polysomnographic results among the 3 groups in both age categories is shown in Table 2. In preschool-age children, the analysis of RDI and nadir values between groups 1 and 2 and between groups 1 and 3 reached statistically significant differences (P values are shown in Table 2). Differences for these 2 measures were not significant between groups 2 and 3 in preschool-age children, and there were no statistically significant differences in the mean oxygen saturation levels for any of the 3 preschool-age groups analyzed. None of the comparisons among any of the groups of school-age children yielded statistically significant results. Otolaryngology– Head and Neck Surgery February 2005 The data were then analyzed according to age category (preschool- versus school-age children), and the results are illustrated in Table 3. There was statistical distinction between preschoolage and school-age children for RDI values in groups 2 (P ⬍ 0.01) and 3 (P ⬍ 0.001), but not for group 1. When comparing nadir levels, a statistical difference was observed between the age groups in group 3 (P ⬍ 0.01), but there was not a statistical difference for groups 1 and 2. Comparison of mean O2 saturation values did not reach statistical significance for any of the group comparisons. DISCUSSION In children with adenotonsillar hypertrophy, there is a tendency among otorhinolaryngologists to diagnose OSAS clinically based exclusively upon the medical history and clinical complaints. Unfortunately, the medical history has been shown to poorly correlate with polysomnographic findings.1,2,7,10,12 In 1995, Carroll et al10 compared questionnaire data concerning clinical components of OSAS and polysomnographic findings in children with adenotonsillar hypertrophy. Their results established a poor correlation between the clinical symptoms of OSAS and polysomnography. In our study, the lack of correlation between clinical complaints and OSAS in children was also observed, regardless the severity of the symptoms related by the parents. We have observed that more than 25% of preschool-age children and more than 45% of schoolage children had clinical history compatible with OSAS, although the polysomnographic findings were normal. Because all the children evaluated in this study had OSAS complaints, it excludes a group of children with no complaints of OSAS by history, but who might have polysomnographic findings compatible with OSAS. We found association between clinical/endoscopic findings and polysomnographic patterns in preschoolage children, when comparing the group without any hypertrophy to the groups with adenoid hypertrophy and with adenoid and tonsil hypertrophy, the latter having worst polysomnographic findings than the former. There was no difference between the group with isolated adenoid hypertrophy and that with adenoid hypertrophy associated with tonsil hypertrophy in preschool-age children, and there were no differences among any of the groups of school-age children. Therefore, the presence of adenoid and/or tonsil hypertrophy was correlated to higher RDI scores and worse nadir values in preschool-age children (leading to moderate apnea), but not in the school-age children. In both age groups, there were no differences between isolated adenoid hypertrophy (group 2) and ad- Otolaryngology– Head and Neck Surgery Volume 132 Number 2 VALERA et al 271 Table 1. Means of age, RDI, nadir, and mean O2 saturation level for each group Group 1 Preschool School Preschool School Preschool School Group 2 Group 3 Age (y) RDI Nadir (%) Mean sat. (%) 3.6 ⫾ 1.3 8.6 ⫾ 1.9 3.6 ⫾ 1.3 8.1 ⫾ 2.3 3.6 ⫾ 1.2 7.8 ⫾ 1.8 0.4 ⫾ 0.5 1.0 ⫾ 1.6 5.1 ⫾ 10.4 2.2 ⫾ 4.4 5.2 ⫾ 6.4 3.6 ⫾ 7.3 93.0 ⫾ 2.8 92.2 ⫾ 4.4 85.4 ⫾ 16.2 91.2 ⫾ 5.9 85.3 ⫾ 10.5 87.4 ⫾ 13.3 96.0 ⫾ 1.2 94.8 ⫾ 2.2 93.9 ⫾ 6.1 96.2 ⫾ 1.9 94.9 ⫾ 2.8 95.4 ⫾ 2.6 Sat., saturation. Table 2. Significance value (P) for Mann-Whitney’s test, comparing the groups within each age category Preschool Group Group Group Group Group Group School 1 1 2 1 1 2 ⫻ ⫻ ⫻ ⫻ ⫻ ⫻ Group Group Group Group Group Group 2 3 3 2 3 3 RDI (P) Nadir (P) Mean sat. (P) 0.000 0.000 0.330 0.634 0.182 0.397 0.003 0.000 0.304 0.735 0.265 0.364 0.188 0.315 0.482 0.698 0.345 0.412 Sat., saturation. Table 3. Significance value (P) for Mann-Whitney’s test, comparing each polysomnographic factor between age categories (preschool versus school children) Group 1 Group 2 Group 3 RDI (P) Nadir (P) Mean sat. (P) 0.521 0.006 0.000 0.502 0.113 0.008 0.594 0.216 0.114 Sat., saturation. enoid hypertrophy associated with tonsils hypertrophy (group 3): both patterns of airway obstruction exhibited the same degree of OSAS. Guilleminault et al,8 Laurikainen et al,14 and Brooks et al13did not find a strong correlation between endoscopic and polysomnographic findings in children, as was reported by the American Academy of Pediatrics.7 Although we found the same results in older children, we documented in younger children that the presence of adenoid hypertrophy, either isolated or associated with tonsil hypertrophy, was related to more severe patterns of OSAS. We have also analyzed the results according to age category, and we have observed that the age was inversely correlated to the degree of apnea in children with adenoid and/or tonsil hypertrophy, but not in children with any evidence of hypertrophy. Thus, younger children are predisposed to have more severe apnea than older ones (with lower values of both RDI and nadir). This observation cannot be due to the degree of adenoid and/or tonsil hypertrophy, because the groups of children under comparison had the same degree of obstruction. Thus, other factors besides adenotonsillar obstruction might exert a definitive influence over the development of apnea, particularly in younger children. Although the identification of these factors is merely speculative at this point, pharyngeal muscular tonus, genetic influences, and developmental conditions that alter the structural relationships in the involved area could be considered. Marcus5 stated that the pathogenesis of OSAS is due to the combination of structural factors, such as tonsils hypertrophy and craniofacial anomalies, and neurological factors, such as airway muscle tonus. In some children, structural factors will predominate, whereas in other children the neurological factors are more important in the development of OSAS. Regardless, during sleep, muscle tone decreases and children with normal breathing patterns while awake can develop OSAS.11 We observed that there was a higher tendency of apnea in preschool-age children with adenoid and/or tonsil hypertrophy than in school-age children. This observation may reflect the influence of the development and growth phases, as well as neurologic and muscular maturation, as suggested by Ward and Marcus1 and Marcus.5 Our results indicate that the clinical history and physical examination findings in children are insufficient to make an accurate diagnosis of OSAS. Clinical information is important to raise a suspicion of the 272 VALERA et al diagnosis, but the ultimate diagnosis is solely confirmed by polysomnographic examination. Children with a clinical history of OSAS, but who have no evidence of adenotonsillar hypertrophy may benefit from this examination to clarify whether or not OSAS is present, especially if consideration is being given to a surgical approach. CONCLUSIONS Based on the results of our study, we concluded that in children: (1) There is little correlation between clinical history of snoring and apnea and the polysomnographic findings. Thus, the diagnosis of OSAS cannot be made based exclusively upon clinical features. (2) Adenotonsillar hypertrophy leads to more severe apnea patterns in preschool-age children. There is no correlation between the degree of obstruction and polysomnographic findings in older children. (3) The apnea pattern does not differ between isolated adenoid hypertrophy and adenoid hypertrophy associated with tonsil hypertrophy. (4) OSAS is more severe in younger children with adenotonsillar hypertrophy than in older children. Neurological factors could play an auxiliary role in OSAS development in these young children. REFERENCES 1. Ward SL, Marcus CL. Obstructive sleep apnea in infants and young children. J Clin Neurophysiol 1996;13:198-207. Otolaryngology– Head and Neck Surgery February 2005 2. American Thoracic Society. Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med 1996;153:866-78. 3. American Thoracic Society. Cardio-respiratory sleep studies in children. Am J Respir Crit Care Med 1999;160:1381-7. 4. Brunetti L, Rana S, Lospalluti ML, et al. Prevalence of obstructive sleep apnea syndrome in a cohort of 1207 children of southern Italy. Chest 2001;120:1930-5. 5. Marcus CL. Pathophysiology of childhood obstructive sleep apnea: current concepts. Resp Physiol 2000;119:143-54. 6. Lipton AJ, Gozal D. Treatment of obstructive sleep apnea in children: do we really know how? Sleep Med Rev 2003;7:61-80. 7. American Academy of Pediatrics. Clinical Practice Guideline: Diagnosis and Management of Childhood Obstructive Sleep Apnea Syndrome. Pediatrics 2002;109:704-12. 8. Guilleminault C, Pelayo R, Leger D, et al. Recogniton of sleepdisordered breathing in children. Pediatrics 1996;98:871-82. 9. Lind MG, Lundell BP. Tonsillar hyperplasia in children: a cause of obstructive sleep apnea, CO2 retention and retarded growth. Arch Otolaryngol 1982;108:650-4. 10. Carroll J, McColley S, Marcus C, et al. Inability of clinical history to distinguish primary snoring from obstructive sleep apnea syndrome in children. Chest 1995;108:610-16. 11. Sanchez-Armengol A, Capote-Gil F, Cano-Gomez S, et al. Polysomnographic studies in children with adenotonsillar hypertrophy and suspected obstructive sleep apnea. Pediatr Pulmonol 1996,22:101-5. 12. Brouillette RT, Morielle A, Leimanis A, et al. Nocturnal pulse oximetry as an abbreviated testing modality for pediatric obstructive sleep apnea. Pediatrics 2000;105:405-12. 13. Brooks LJ, Stephens BM, Bacevice AM. Adenoid size is related to severity but not the number of episodes of obstructive apnea in children. J Ped 1998;12:303-10. 14. Laurikainen E, Erkinjuntti M, Alihanka J, et al. Radiological parameters of the bony nasopharynx and the adenotonsillar size compared with sleep apnea episodes in children. Int J Pediatr Otorhinolaryngol 1987;12:303-10.