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Table 1. 
Demographics of 36 Children Whose Parents Completed the Child Behavior Checklist Before Tonsillectomy and Adenoidectomy
Demographics of 36 Children Whose Parents Completed the Child Behavior Checklist Before Tonsillectomy and Adenoidectomy
Table 2. 
Preoperative Obstructive Symptom Scores for 35 Children Scheduled for Tonsillectomy and Adenoidectomy
Preoperative Obstructive Symptom Scores for 35 Children Scheduled for Tonsillectomy and Adenoidectomy
Table 3. 
Impact of Tonsillectomy and Adenoidectomy on Obstructive Symptoms for the 15 Children With Both Preoperative and Postoperative Scores
Impact of Tonsillectomy and Adenoidectomy on Obstructive Symptoms for the 15 Children With Both Preoperative and Postoperative Scores
Table 4. 
Entry Child Behavior Checklist (CBCL) Scores and Classification
Entry Child Behavior Checklist (CBCL) Scores and Classification
Table 5. 
Impact of Tonsillectomy and Adenoidectomy on Child Behavior Checklist (CBCL) Scores and Classification
Impact of Tonsillectomy and Adenoidectomy on Child Behavior Checklist (CBCL) Scores and Classification
1.
Brouilette  RHanson  DDavid  R  et al.  A diagnostic approach to suspected obstructive sleep apnea in children. J Pediatr. 1984;10510- 14Article
2.
Goldstein  NASculerati  NWalsleben  JABhatia  NFriedman  DMRapoport  DM Clinical diagnosis of pediatric obstructive sleep apnea validated by polysomnography. Otolaryngol Head Neck Surg. 1994;111611- 617Article
3.
Guilleminault  CKorobkin  RWinkle  R A review of 50 children with obstructive sleep apnea syndrome. Lung. 1981;159275- 287Article
4.
Leach  JOlson  JHermann  JManning  S Polysomnographic and clinical findings in children with obstructive sleep apnea. Arch Otolaryngol Head Neck Surg. 1992;118741- 744Article
5.
Carroll  JL Sleep-related upper-airway obstruction in children and adolescents. Child Adolesc Psychiatr Clin North Am. 1996;5617- 647
6.
Brouillette  RTFernbach  SKHunt  CE Obstructive sleep apnea in infants and children. J Pediatr. 1982;10031- 40Article
7.
Hunt  CEBrouillette  RT Abnormalities of breathing control and airway maintenance in infants and children as a cause of cor pulmonale. Pediatr Cardiol. 1982;3249- 256Article
8.
Talbot  ARRobertson  LW Cardiac failure with tonsil and adenoid hypertrophy. Arch Otolaryngol. 1973;98277- 281Article
9.
Richardson  MASeid  ABCotton  RTBenton  CKramer  M Evaluation of tonsils and adenoids in sleep apnea syndrome. Laryngoscope. 1980;901106- 1110Article
10.
Frank  YKravath  REPollak  CPWeitzman  ED Obstructive sleep apnea and its therapy: clinical and polysomnographic manifestations. Pediatrics. 1983;71737- 742
11.
Messner  AH Evaluation of obstructive sleep apnea by polysomnography prior to pediatric adenotonsillectomy. Arch Otolaryngol Head Neck Surg. 1999;125353- 356Article
12.
Ali  NJPitson  DJStradling  JR Snoring, sleep disturbance, and behaviour in 4-5 year olds. Arch Dis Child. 1993;68360- 366Article
13.
Ali  NJPitson  DJStradling  JR Sleep disordered breathing: effects of adenotonsillectomy on behaviour and psychological functioning. Eur J Pediatr. 1996;15556- 62Article
14.
Guilleminault  CHWinkle  RKorobkin  RSimmons  B Children and nocturnal snoring: evaluation of the effects of sleep related respiratory resistive load and daytime functioning. Eur J Pediatr. 1982;139165- 171Article
15.
Rhodes  SKShimoda  KCWaid  LR  et al.  Neurocognitive deficits in morbidly obese children with obstructive sleep apnea. J Pediatr. 1995;127741- 744Article
16.
Weissbluth  MDavis  ATPoncher  JReiff  J Signs of airway obstruction during sleep and behavioral, developmental, and academic problems. J Dev Behav Pediatr. 1983;4119- 121Article
17.
Greene  MGCarroll  JL Consequences of sleep-disordered breathing in childhood. Curr Opin Pulm Med. 1997;3456- 463Article
18.
Achenbach  TM Manual for the Child Behavior Checklist/2-3 and 1992 Profile.  Burlington Dept of Psychiatry, University of Vermont1992;
19.
Achenbach  TM Manual for the Child Behavior Checklist/4-18 and 1991 Profile.  Burlington Dept of Psychiatry, University of Vermont1991;
20.
Gustafson  TL True Epistat Reference Manual. 5th ed. Richardson, Tex Epistat Services1994;
21.
Employment Policy Foundation, Fact and Fallacy. Vol 2 (No. 1) Available at: http://www.epf.org/ff/ff2-1.htm. Accessed April 8, 1999.
22.
Gozal  D Sleep-disordered breathing and school performance in children. Pediatrics. 1998;102616- 620Article
23.
Bédard  M-AMontplaisir  JMalo  JRicher  FRouleau  I Persistent neuropsychological deficits and vigilance impairment in sleep apnea syndrome after treatment with continuous positive airways pressure (CPAP). J Clin Exp Neuropsychol. 1993;15330- 341Article
24.
Findley  LJBarth  JTPowers  DCWilhoit  SCBoyd  DGSuratt  PM Cognitive impairment in patients with obstructive sleep apnea and associated hypoxemia. Chest. 1986;90686- 690Article
25.
Findley  LJUnverzagt  MESuratt  PM Automobile accidents involving patients with obstructive sleep apnea. Am Rev Respir Dis. 1988;138337- 340Article
Original Article
April 2000

Impact of Tonsillectomy and Adenoidectomy on Child Behavior

Author Affiliations

From the Division of Pediatric Otolaryngology, State University of New York Health Science Center at Brooklyn (Drs Goldstein and Rosenfeld); Department of Pediatric Otolaryngology, Allegheny General Hospital, Pittsburgh, Pa (Dr Post); and Department of Communication Science and Disorders, University of Pittsburgh, and Department of Audiology and Communication Disorders, Children's Hospital of Pittsburgh (Dr Campbell).

Arch Otolaryngol Head Neck Surg. 2000;126(4):494-498. doi:10.1001/archotol.126.4.494
Abstract

Objective  To measure the impact of tonsillectomy and adenoidectomy (T&A) on children's behavioral and emotional problems using a standardized assessment.

Design  Prospective study.

Setting  Tertiary care children's hospital.

Patients  Thirty-six children, aged 2 through 18 years, with symptoms of nighttime snoring, observed apneas, and daytime mouth breathing and physical examination results demonstrating 3+ or 4+ tonsils scheduled for T&A.

Intervention  Parents completed a standard survey of their children's symptoms of sleep apnea and a standardized measure of children's competencies and problems, the Child Behavior Checklist for ages 2 through 3 years or 4 through 18 years, before T&A and 3 months postoperatively.

Main Outcome Measure  The Child Behavior Checklist total problem score.

Results  The preoperative Child Behavior Checklist total problem score was consistent with abnormal behavior for 10 children (28%). After T&A (n=15), only 2 scores were abnormal, but the change was not statistically significant. In contrast, the mean total problem score was 7.5 points lower after surgery (95% confidence interval, 5.1-9.7), indicating a significant decrease (P<.001, matched t test).

Conclusions  This pilot study demonstrates a high prevalence (28%) of abnormal behavior in children undergoing T&A for chronic upper airway obstruction. Scores on a standardized measure of behavior improve following T&A, but larger studies with increased statistical power are needed to clarify the degree of improvement and its clinical importance.

CHILDREN WITH obstructive sleep apnea syndrome (OSAS) usually are brought to medical attention because of nighttime breathing difficulties. Parents report symptoms of snoring, apneic pauses, choking, gasping, struggling to breath, restless sleep, unusual sleeping positions, and frequent awakenings.14 Although daytime sleepiness may be present, it is not a universal symptom in children compared with adults.5 Pediatric OSAS has also been associated with cor pulmonale and right-sided heart failure,3,4,68 systemic hypertension,3,9 failure to thrive,3,4,6 enuresis,3,10 and neurocognitive and behavioral abnormalities.

The diagnosis of pediatric OSAS may be confirmed by polysomnography. However, there are few normative data available for polysomnography in children, sleep laboratories able to adequately study children are not widely available, and the studies are time-consuming and expensive. Thus, since tonsillectomy and adenoidectomy (T&A) is curative in most children, many children with suspected OSAS undergo T&A without preoperative polysomnography.11

Although behavioral disturbances, including learning difficulties, attention disorders, hyperactivity, aggression, and antisocial behavior, have been reported in children with sleep apnea, there have been few studies using standardized behavioral assessments.3,6,1216 Most studies have relied on parental reports of children's behavior before and after treatment.6,14,17 The objective of this study was to determine the impact of T&A on the behavioral and emotional problems of children with OSAS or upper airway obstruction using a standardized assessment, the Child Behavior Checklist (CBCL).18,19

PATIENTS AND METHODS

Parents of children aged 2 through 18 years who were scheduled for T&A were recruited from the Otolaryngology Clinic at the Children's Hospital of Pittsburgh, Pittsburgh, Pa, between August 1996 and April 1998. To be included, the children were required to have symptoms of nighttime snoring, observed apneas, and daytime mouth breathing, and results of their physical examination had to demonstrate 3+ or 4+ tonsils. Children with craniofacial syndromes, neuromuscular disorders, behavioral disorders, learning disabilities, and psychiatric disease and children whose parents did not read or understand English were excluded. Polysomnography was not performed in any child before T&A. The protocol was approved by the Children's Hospital of Pittsburgh Human Rights Committee, and a convenience sample was recruited.

Before T&A and 3 months postoperatively, parents completed 2 forms: (1) a standard questionnaire that recorded demographic information, family socioeconomic status, level of parent's education, and frequency (always, almost always, sometimes, never) of 11 symptoms of pediatric OSAS or upper airway obstruction and (2) the CBCL for ages 2 through 3 years (CBCL/2-3) or ages 4 through 18 years (CBCL/4-18). The CBCLs are valid and reliable and have been used widely since 1991 to study behavior in a variety of clinical situations.

The responses to the symptom questionnaire were scored as follows: always, 3; almost always, 2; sometimes, 1; and never, 0. The CBCL/2-3 is a 100-item survey, and the CBCL/4-18 is a 118-item survey of specific childhood behaviors. Each item is scored as follows: not true, 0; somewhat or sometimes true, 1; and very true or often true, 2. The CBCL/4-18 also has 35 questions regarding children's competencies in school, activities, and social contexts, which are scored based on the amount and quality of participation. Raw scores are converted to normalized T scores, which are compared with the scores of children in normative samples. Scores are then divided into normal (<95th percentile), borderline(≥95th percentile but <98th percentile), or abnormal (≥98th percentile) ranges.

The CBCL/2-3 is scored to obtain a total problem score, which provides a global index of the child's behavioral and emotional problems. The responses can be further divided into scores for internalizing (anxious/depressed and withdrawn) and externalizing (aggressive behavior and destructive behavior), and scores for the individual syndrome scales (anxious/depressed, withdrawn, sleep problems, somatic problems, aggressive behavior, and destructive behavior) can be calculated. The CBCL/4-18 is scored to obtain a total problem score, scores for internalizing (withdrawn, somatic complaints, anxious/depressed) and externalizing (delinquent behavior and aggressive behavior) groupings, scores for the individual syndrome scales (withdrawn, somatic complaints, anxious/depressed, social problems, thought problems, attention problems, delinquent behavior, and aggressive behavior), and a total competence score.

Comparison of preoperative and postoperative T scores were performed using a matched, 2-tailed t test, and preoperative and postoperative T score classifications (normal, borderline, and abnormal) were compared by the log-likelihood ratio test. P<.05 was considered statistically significant.20

RESULTS

Parents of 36 children completed the CBCL preoperatively. Patient demographics are presented in Table 1. The male-female ratio was 2:1, and the mean patient age was 4.6 years (range, 2-10 years). Most families were middle class or upper middle class (annual family income between $21 000 and $100 000),21 and the mean education level of the parent who completed the form was 2 years of postsecondary education. Fifteen parents returned the postoperative surveys. There were no clinical or demographic differences between those who returned the second survey and those who did not.

Mean preoperative and postoperative symptom scores are presented in Table 2 and Table 3. One parent did not complete the standard questionnaire, and some responses were left incomplete by the parents. The postoperative scores were much lower than the preoperative scores, as would be expected after T&A. Entry T scores and score classifications for the total problem score, internalizing and externalizing groupings, and the individual syndrome scales are presented in Table 4. Sample size varied because some of the syndrome scales are applicable to only the CBCL/2-3 or the CBCL/4-18, and there were many incomplete responses for the total competence items. The total problem score was abnormal for 10 patients (28%), the internalizing group was abnormal for 3 patients (8%), the externalizing group was abnormal for 9 patients (25%), and the individual syndrome scales were abnormal for between 0% and 20% of patients. Problem scales most affected were total competence (20%), sleep problems (17%), somatic complaints (11%), social problems (8%) and destructive behavior (8%).

The change in T score and change in classification after T&A for the 15 patients with complete data are presented in Table 5. The mean total problem score was 7.5 points lower after surgery, resulting in a statistically significant decrease (P<.001). Scores were also significantly lower after T&A for the internalizing subgroup and the individual syndrome scales of withdrawn, somatic complaints, anxious/depressed, attention problems, and thought problems. Sleep problems, destructive behavior, and total competence were not subjected to analysis because of the small numbers of patients in these groups. Although there were trends toward improvement, changes in classification were not significant for the total problem score or the individual syndrome scales. There were no significant relationships between family income and level of parent education and entry T scores or changes in classification postoperatively.

COMMENT

This pilot study demonstrates a high prevalence (28%) of abnormal behavior in children undergoing T&A for OSAS or chronic upper airway obstruction. The CBCL scores significantly improved following T&A, although changes in classification (normal, borderline, or abnormal) were not statistically significant. Subclasses that showed significant improvement after T&A were withdrawn behavior, somatic complaints, anxious/depressed, attention problems, and thought problems.

Although widely cited as a common complication of pediatric OSAS, neurocognitive and behavioral disturbances have mostly been inferred from case series where parents' reports were the sole criteria for evaluation. Reports of improved behavior after treatment of OSAS have also largely consisted of anecdotal observations by parents and teachers. There have been only 4 prior reports using standardized measures to assess the developmental and behavioral disturbances of children with OSAS.

Ali et al12 performed overnight pulse oximetry and overnight video recordings on 66 children with suspected sleep apnea and 66 controls. They administered 3 subscales of the Conners' Behavior Rating Scale to their parents and teachers. Only 7 children (all in the high-risk group) had a detectable breathing disorder, but the high-risk children had significantly higher scores on the hyperactive and inattentive Conners' subscales completed by both the parents and teachers and a significantly higher score on the aggressive subscale completed by the parents. In a follow-up study, Ali et al13 repeated their evaluation along with the administration of the continuous performance test, a measure of sustained attention in children, to 33 children with suspected sleep apnea who were scheduled for T&A. Of these 33 children, 12 displayed a sleep and breathing disorder (SBD group) by video recording and pulse oximetry, and 21 had normal sleep. Eleven of these children were matched by age and sex to those in the SBD group (snorer group). Ten other children without a history of snoring served as controls. After T&A, the SBD group showed a small but statistically significant improvement in all 3 behavior subscales of the Conners' Parent Rating Scale, whereas the snorer group improved only on the hyperactivity subscale. There were no significant changes for any of the groups on the Conners' Teacher Rating Scale. Following T&A, there were significant improvements on the continuous performance test by both the SBD and snorer groups.

Rhodes et al15 administered the Wide Range Assessment of Memory and Learning to 14 morbidly obese children, 5 with OSAS. The 5 children with OSAS had significantly lower scores on general memory, verbal memory, learning, and vocabulary. Gozal22 evaluated 297 first-grade children whose school performance was in the lowest 10th percentile by a detailed OSAS questionnaire and a single night recording of pulse oximetry and transcutaneous partial pressure of carbon dioxide. Sleep-associated gas exchange abnormalities were identified in 54 children. Of these children, 24 underwent T&A, and their mean grades during the second grade increased significantly compared with the 30 children whose parents declined treatment.

Limitations of these studies include small sample sizes,12,13,15 lack of a control group or lack of a control group consisting of otherwise healthy children,15,22 selecting the study group from a special patient population,15,22 or evaluating only a limited range of neurocognitive and behavioral functions.12,13,15 Limitations of our pilot study include small sample size and the lack of a control group. However, the CBCL is a validated, comprehensive survey of children's behavioral and emotional problems used extensively in pediatric psychiatry, pediatric psychology, pediatrics, special education, forensic situations, and evaluation of problems related to child abuse.18,19 Our results agree with prior studies in emphasizing improvement in attention and thought problems after T&A but do not support improvement in aggressive or antisocial tendencies.

Adults with OSAS have been shown to experience deficits in attention, memory, intellectual abilities, problem-solving functions, and psychomotor skills using a wide range of validated tests.17,23,24 Many of these behavioral and neurocognitive functions improve following successful treatment.17,23 Recent studies have reported the higher incidence of traffic accidents in adult patients with OSAS.25 Although the physiologic mechanism by which OSAS produces its neurocognitive and behavioral effects is unknown, disrupted sleep patterns and hypoxemia are integral to their development.23,24 Although these defects are present in adults with sleep apnea, we cannot generalize these findings to children.

Our pilot data suggest that behavioral, emotional, and neurocognitive difficulties are present in children with OSAS and improve after treatment. Further larger-scale work is needed to define the precise spectrum of these abnormalities, clarify the degree of improvement after treatment of OSAS, elucidate their clinical importance, and provide data to allow their early recognition.

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Article Information

Accepted for publication November 16, 1999.

Presented at the annual meeting of the American Society of Pediatric Otolaryngology, Palm Desert, Calif, April 29, 1999.

Reprints: Nira A. Goldstein, MD, Department of Otolaryngology, State University of New York Health Science Center at Brooklyn, 450 Clarkson Ave, Campus Box 126, Brooklyn, NY 11203-2098 (e-mail: ngoldstein@netmail.hscbklyn.edu).

References
1.
Brouilette  RHanson  DDavid  R  et al.  A diagnostic approach to suspected obstructive sleep apnea in children. J Pediatr. 1984;10510- 14Article
2.
Goldstein  NASculerati  NWalsleben  JABhatia  NFriedman  DMRapoport  DM Clinical diagnosis of pediatric obstructive sleep apnea validated by polysomnography. Otolaryngol Head Neck Surg. 1994;111611- 617Article
3.
Guilleminault  CKorobkin  RWinkle  R A review of 50 children with obstructive sleep apnea syndrome. Lung. 1981;159275- 287Article
4.
Leach  JOlson  JHermann  JManning  S Polysomnographic and clinical findings in children with obstructive sleep apnea. Arch Otolaryngol Head Neck Surg. 1992;118741- 744Article
5.
Carroll  JL Sleep-related upper-airway obstruction in children and adolescents. Child Adolesc Psychiatr Clin North Am. 1996;5617- 647
6.
Brouillette  RTFernbach  SKHunt  CE Obstructive sleep apnea in infants and children. J Pediatr. 1982;10031- 40Article
7.
Hunt  CEBrouillette  RT Abnormalities of breathing control and airway maintenance in infants and children as a cause of cor pulmonale. Pediatr Cardiol. 1982;3249- 256Article
8.
Talbot  ARRobertson  LW Cardiac failure with tonsil and adenoid hypertrophy. Arch Otolaryngol. 1973;98277- 281Article
9.
Richardson  MASeid  ABCotton  RTBenton  CKramer  M Evaluation of tonsils and adenoids in sleep apnea syndrome. Laryngoscope. 1980;901106- 1110Article
10.
Frank  YKravath  REPollak  CPWeitzman  ED Obstructive sleep apnea and its therapy: clinical and polysomnographic manifestations. Pediatrics. 1983;71737- 742
11.
Messner  AH Evaluation of obstructive sleep apnea by polysomnography prior to pediatric adenotonsillectomy. Arch Otolaryngol Head Neck Surg. 1999;125353- 356Article
12.
Ali  NJPitson  DJStradling  JR Snoring, sleep disturbance, and behaviour in 4-5 year olds. Arch Dis Child. 1993;68360- 366Article
13.
Ali  NJPitson  DJStradling  JR Sleep disordered breathing: effects of adenotonsillectomy on behaviour and psychological functioning. Eur J Pediatr. 1996;15556- 62Article
14.
Guilleminault  CHWinkle  RKorobkin  RSimmons  B Children and nocturnal snoring: evaluation of the effects of sleep related respiratory resistive load and daytime functioning. Eur J Pediatr. 1982;139165- 171Article
15.
Rhodes  SKShimoda  KCWaid  LR  et al.  Neurocognitive deficits in morbidly obese children with obstructive sleep apnea. J Pediatr. 1995;127741- 744Article
16.
Weissbluth  MDavis  ATPoncher  JReiff  J Signs of airway obstruction during sleep and behavioral, developmental, and academic problems. J Dev Behav Pediatr. 1983;4119- 121Article
17.
Greene  MGCarroll  JL Consequences of sleep-disordered breathing in childhood. Curr Opin Pulm Med. 1997;3456- 463Article
18.
Achenbach  TM Manual for the Child Behavior Checklist/2-3 and 1992 Profile.  Burlington Dept of Psychiatry, University of Vermont1992;
19.
Achenbach  TM Manual for the Child Behavior Checklist/4-18 and 1991 Profile.  Burlington Dept of Psychiatry, University of Vermont1991;
20.
Gustafson  TL True Epistat Reference Manual. 5th ed. Richardson, Tex Epistat Services1994;
21.
Employment Policy Foundation, Fact and Fallacy. Vol 2 (No. 1) Available at: http://www.epf.org/ff/ff2-1.htm. Accessed April 8, 1999.
22.
Gozal  D Sleep-disordered breathing and school performance in children. Pediatrics. 1998;102616- 620Article
23.
Bédard  M-AMontplaisir  JMalo  JRicher  FRouleau  I Persistent neuropsychological deficits and vigilance impairment in sleep apnea syndrome after treatment with continuous positive airways pressure (CPAP). J Clin Exp Neuropsychol. 1993;15330- 341Article
24.
Findley  LJBarth  JTPowers  DCWilhoit  SCBoyd  DGSuratt  PM Cognitive impairment in patients with obstructive sleep apnea and associated hypoxemia. Chest. 1986;90686- 690Article
25.
Findley  LJUnverzagt  MESuratt  PM Automobile accidents involving patients with obstructive sleep apnea. Am Rev Respir Dis. 1988;138337- 340Article
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