ObjectiveTo measure the impact of tonsillectomy and adenoidectomy (T&A) on children's behavioral and emotional problems using a standardized assessment.DesignProspective study.SettingTertiary care children's hospital.PatientsThirty-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.InterventionParents 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 MeasureThe Child Behavior Checklist total problem score.ResultsThe 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 ttest).ConclusionsThis 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.Although daytime sleepiness may be present, it is not a universal symptom in children compared with adults.Pediatric OSAS has also been associated with cor pulmonale and right-sided heart failure,systemic hypertension,failure to thrive,enuresis,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.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.Most studies have relied on parental reports of children's behavior before and after treatment.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).PATIENTS AND METHODSParents 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 ttest, 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.RESULTSParents 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),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.Table 1. Demographics of 36 Children Whose Parents Completed the Child Behavior Checklist Before Tonsillectomy and AdenoidectomyCharacteristicNo. (%)SexMale24 (67)Female12 (33)Age, y24 (11)38 (22)46 (17)57 (19)67 (19)72 (6)8091 (3)101 (3)RaceWhite30 (83)Black5 (14)East Asian1 (3)Family income, $ (in thousands)<206 (17)20-3510 (28)36-506 (17)51-754 (11)76-1005 (14)Unknown5 (14)Parent's education level*11th grade1 (3)12th grade11 (31)1st year college5 (14)2nd year college3 (8)3rd year college1 (3)4th year college2 (6)1st year postgraduate4 (11)2nd year postgraduate3 (8)Unknown6 (17)*Asked of the parent who completed the Child Behavior Checklist.Mean preoperative and postoperative symptom scores are presented in Table 2and 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%).Table 2. Preoperative Obstructive Symptom Scores for 35 Children Scheduled for Tonsillectomy and AdenoidectomySymptomSample SizeMean Preoperative Score (95% Confidence Interval)Snoring352.5 (2.3 to 2.7)Apneic pauses341.8 (1.5 to 2.1)Nighttime gasping341.4 (1.1 to 1.7)Nighttime choking350.9 (0.6 to 1.2)Restless sleep351.9 (1.5 to 2.2)Frequent awakenings351.5 (1.2 to 1.8)Enuresis*230.5 (0.2 to 0.8)Neck extension during sleep331.4 (1.1 to 1.7)Daytime sleepiness351.1 (0.8 to 1.5)Mouth breathing352.1 (1.8 to 2.4)Chronic rhinorrhea340.8 (0.6 to 1.6)*For children 4 years or older.Table 3. Impact of Tonsillectomy and Adenoidectomy on Obstructive Symptoms for the 15 Children With Both Preoperative and Postoperative ScoresSymptomSample SizeMean Preoperative Score (95% Confidence Interval)Sample SizeMean Postoperative Score (95% Confidence Interval)Snoring152.5 (2.1 to 2.9)140.4 (0.1 to 0.6)Apneic pauses151.9 (1.3 to 2.4)150.2 (−0.01 to 0.4)Nighttime gasping141.5 (1.1 to 2.0)150.07 (−0.06 to 0.2)Nighttime choking151.1 (0.5 to 1.7)150.07 (−0.06 to 0.2)Restless sleep152.0 (1.6 to 2.4)150.5 (0.3 to 0.8)Frequent awakenings151.7 (1.2 to 2.1)140.4 (0.2 to 0.7)Enuresis*110.6 (0.2 to 1.0)110.2 (−0.06 to 0.4)Neck extension during sleep151.8 (1.4 to 2.2)150.3 (0.1 to 0.6)Daytime sleepiness151.4 (0.9 to 1.9)150.6 (0.3 to 0.9)Mouth breathing152.2 (1.8 to 2.6)150.5 (0.3 to 0.8)Chronic rhinorrhea151.0 (0.6 to 1.4)150.1 (−0.05 to 0.3)*For children 4 years or older.Table 4. Entry Child Behavior Checklist (CBCL) Scores and ClassificationCBCL Problem ScaleSample SizeMean T Score (95% Confidence Interval)Classification, No. (%)NormalBorderlineAbnormalInternalizing3651.8 (48.4 to 55.1)27 (75)6 (17)3 (8)Externalizing3653.9 (50.2 to 57.6)24 (67)3 (8)9 (25)Withdrawn3654.6 (52.5 to 56.6)32 (89)3 (8)1 (3)Somatic complaints3658.4 (56.0 to 60.9)28 (78)4 (11)4 (11)Anxious/depressed3654.0 (52.1 to 55.9)34 (94)2 (6)0Aggressive behavior3657.2 (54.3 to 60.1)27 (75)7 (19)2 (6)Delinquent behavior2455.1 (52.4 to 57.9)21 (88)2 (8)1 (4)Attention problems2457.0 (54.0 to 60.0)19 (79)5 (21)0Thought problems2454.7 (52.1 to 57.3)23 (96)01 (4)Social problems2455.5 (52.7 to 58.2)22 (92)02 (8)Sleep problems1261.9 (56.4 to 67.5)7 (58)3 (25)2 (17)Destructive behavior1259.0 (52.3 to 65.3)10 (83)1 (8)1 (8)Total competence (social, activities, school)1045.1 (38.7 to 51.5)7 (70)1 (10)2 (20)Total problems3655.4 (52.1 to 58.7)25 (69)1 (3)10 (28)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.Table 5. Impact of Tonsillectomy and Adenoidectomy on Child Behavior Checklist (CBCL) Scores and ClassificationCBCL Problem ScaleSample SizeChange in T Score*Change in Classification†Final Classification, No. (%)Mean (95% CI)P‡NormalBorderlineAbnormalP§NormalBorderlineAbnormalInternalizing15+8.1 (5.5 to 10.6)<.001+20−2.5413 (87)1 (7)1 (7)Externalizing15+1.7 (−2.3 to 5.6).38+20−2.7112 (80)03 (20)Withdrawn15+2.9 (1.5 to 4.3)<.001+10−1.4914 (93)1 (7)0Somatic complaints15+6.2 (1.8 to 10.6).009+3−1−2.1814 (93)1 (7)0Anxious/depressed15+2.7 (1.1 to 4.4).003+2−20.2315 (100)00Aggressive behavior15+3.0 (−0.4 to 6.4).08+3−2−1.4113 (87)1 (7)1 (7)Delinquent behavior11−0.3 (−6.4 to 5.8).920+1−1.2510 (91)1 (9)0Attention problems11+5.0 (2.4 to 7.6).002+3−30.1011 (100)00Thought problems11+4.2 (1.4 to 6.9).007000>.9911 (100)00Social problems11+3.5 (−0.9 to 7.8).11+1+1−2.1210 (91)1 (9)0Total problems15+7.5 (5.1 to 9.7)<.001+2+1−3.4812 (80)1 (7)2 (13)*Difference in postoperative vs preoperative values; plus signs indicate improvement value.†Plus signs indicate additional patients in classification range postoperatively; minus signs, fewer patients in classification range postoperatively.‡t Test matched samples, 2-tailed P.§Log-likelihood ratio test.COMMENTThis 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 alperformed 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 alrepeated 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 aladministered 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. Gozalevaluated 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,lack of a control group or lack of a control group consisting of otherwise healthy children,selecting the study group from a special patient population,or evaluating only a limited range of neurocognitive and behavioral functions.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.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.Many of these behavioral and neurocognitive functions improve following successful treatment.Recent studies have reported the higher incidence of traffic accidents in adult patients with OSAS.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.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. 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JAMA Otolaryngology - Head & Neck Surgery – American Medical Association
Published: Apr 1, 2000