Effect of
adenotonsillectomy
on sleep problems,
attention deficit
hyperactivity disorder
symptoms, and quality
of life of children with
adenotonsillar
hypertrophy and
sleep-disordered
breathing
Serhat Tu¨rko
glu
1,
Battal Tahsin Somuk
2,
Emrah Sapmaz
2, and Ayhan Bilgic¸
3Abstract
Objective: Chronic adenotonsillar hypertrophy is the most common etiologic reason for upper airway obstruction in childhood and has been found to be associ-ated with a variety of psychiatric disorders and poor quality of life. In the present study, we investigated the impact of adenotonsillectomy on attention deficit
1
Department of Child and Adolescent Psychiatry, Selc¸uk University Faculty of Medicine, Konya, Turkey
2
Department of Otolaryngology Head and Neck Surgery, Gaziosmanpasa University Faculty of Medicine, Tokat, Turkey
3
Department of Child and Adolescent Psychiatry, Meram Faculty of Medicine, Necmettin Erbakan University, Konya, Turkey
Corresponding Author:
Serhat Tu¨rkoglu, Department of Child and Adolescent Psychiatry, Selc¸uk University Faculty of Medicine, 42075 Selc¸uklu/Konya, Turkey.
Email: [email protected]
The International Journal of Psychiatry in Medicine 2019, Vol. 54(3) 231–241 ! The Author(s) 2019 Article reuse guidelines: sagepub.com/journals-permissions DOI: 10.1177/0091217419829988 journals.sagepub.com/home/ijp
hyperactivity disorder symptoms, sleep problems, and quality of life in children with chronic adenotonsillar hypertrophy.
Methods: The parents of children with chronic adenotonsillar hypertrophy filled out the Conners’s Parent Rating Scale-Revised Short form (CPRS-RS), Children’s Sleep Habits Questionnaire (CSHQ), and Pediatric Quality of Life Inventory, Parent ver-sion (PedsQL-P) before and six months after adenotonsillectomy.
Results: A total of 64 children were included in the study (mean age¼ 6.8 2.4 years; boy:girl ratio¼ 1). The mean attention deficit hyperactivity disorder index and oppositionality subdomain scores of the CPRS-RS and all of the CSHQ subdomain scores (bedtime resistance, sleep-onset delay, sleep anxiety, night waking, parasom-nias, sleep-disordered breathing, and daytime sleepiness) except for sleep duration significantly decreased after adenotonsillectomy (p< 0.05). The PedsQL-P total score and both PedsQL-P physical health and psychosocial health subdomain scores were significantly higher at six months after adenotonsillectomy (p< 0.001). Conclusions: Child and adolescent psychiatrists should check the symptoms of chronic adenotonsillar hypertrophy to identify children with chronic adenotonsillar hypertrophy who suffer from sleep disturbance, attention deficit hyperactivity disorder symptoms, and oppositionality. Adenotonsillectomy seems to be beneficial for coexisting attention deficit hyperactivity disorder and sleep disorder symptoms and quality of life in these children.
Keywords
sleep problems, adenotonsillectomy, attention deficit hyperactivity disorder, quality of life, chronic adenotonsillar hypertrophy
Introduction
Enlargement of tonsils and adenoids with significant upper airway obstruction, also known as adenotonsillar hypertrophy, is the most common cause of chronic airway obstruction in children. It can be easily treated by simple adenotonsil-lectomy (AT) in most cases.1Different types of sleeping disorders ranging from loud snoring to severe obstructive sleep apnea may be observed in patients with upper airway obstruction due to chronic adenotonsillar hypertrophy (CAH). CAH influences sleep architecture by causing increased arousal during sleep, shorter total sleep time, increased REM sleep latency, decreased sleep efficiency, and decreased REM sleep in children.2It is known that sleep disorders caused by respiratory problems may lead to many serious clinical conditions (e.g., hearing/visual problems, obesity, cor pulmonale, cardiac insufficiency, hyper-tension, growth retardation, and maxillomandibular anomalies) by affecting many systems.3,4 Children with CAH experience not only sleep disturbances
and these conditions but also inattention, hyperactivity, dysfunction in memory and executive functioning, and behavioral problems such as social withdrawal or aggression.5Furthermore, numerous studies of children with CAH have reported more emotional instability and anxiety symptoms.6In addition, 20% to 40% of children with CAH, respiratory problems, and sleep disturbance have clinically significant symptoms of inattention, hyperactivity, and impulsivity.7,8 Positive changes in their attention (sustained and divided attention), hyperactivity, and behavioral problems were observed in the postoperative period.9–12 Although neurochemical alterations caused by decreased arterial blood oxygen saturation as well as subsequent intermittent or chronic hypoxemia episodes of brain have been accused of the impairment in behavior and neurocognitive performance, the definite pathophysiologic mechanism has not been yet cleared.13
Attention deficit hyperactivity disorder (ADHD) is a complex multifactorial disorder and one of the most common neurodevelopmental disorders in child-hood, with core symptoms of inattention, hyperactivity, and impulsivity. It begins in early childhood and commonly continues through adolescence and early adulthood and often leads to academic, social, and occupational dysfunc-tion.14 Patients with ADHD commonly develop comorbid disruptive behavior disorders such as oppositional defiant disorder and conduct disorder, if not treated adequately.15 These comorbid disruptive behavior disorders lead to severe functional impairment and psychosocial problems and make treatment more difficult.16 According to a meta-analysis, the rates of sleep problems including pediatric obstructive sleep apnea syndrome, periodic limb movement, enuresis, and delayed sleep phase syndrome were significantly higher among children with ADHD when compared to a control group.17Naseem et al. pro-posed that sleep disturbance might be one of the underlying reasons of ADHD.18 Therefore, these may indicate the causal relationship between ADHD and sleep disorder.
Quality of life (QoL) describes an individual’s nominative perception of his or her status in life, as evidenced by their social, physical, and psychological func-tioning. We need to use self- or caregiver-administered instruments to quantify the impact of a disease on physical symptoms, emotional state, and family interaction for investigating QoL in children. CAH, sleep problems, and ADHD symptoms have a negative impact on QoL in the early course of these diseases, and the impact is already present at diagnosis.19 Thus, the burden associated with these disorders is high for affected individuals, their families, and society.20 Studies associated with pediatric CAH found that QoL was sig-nificantly decreased. Furthermore, many studies and case reports showed that children with CAH had remarkable short-/long-term amelioration of QoL after AT as qualified by shifts in PedsQoL-P scores.19,21
The purpose of this study was to evaluate sleep problems, ADHD symptoms, and QoL in children with CAH and to examine the impact of AT on these symptoms and QoL using parent-reported scales in this population.
Methods
Setting and participants
Sixty-four children aged 4–15 years who were admitted to the Department of Otorhinolaryngology at the University Medical Faculty Hospital with an indi-cation for AT were included in the study. The tonsil size was classified according to the Friedman staging system as stage 1, 2, 3, and 4.22In addition to having a tonsil size of stage 3/4, patients who had adenoid hypertrophy obstructing the choana by 75% or more on flexible fiberoptic nasopharyngoscopy and whose parents had witnessed sleep apnea were accepted as CAH and sleep-disordered breathing (SDB). Children who had autism spectrum disorders or intellectual disabilities and neurologic or metabolic disorders, who underwent AT for any sign of infection but no airway obstruction, and who had craniofacial anomalies were excluded from the study. The intellectual level of the patients was deter-mined by the Wechsler Intelligence Scale for Children-Revised (WISC-R), Stanford-Binet Intelligence Test, and clinical examination. The clinical exami-nation that included the assessment of daily adaptive functions was conducted by a child and adolescent psychiatrist.
This study was confirmed by the University’s Institutional Review Board. The patients’ parents who participated in the study gave written informed con-sent. The patient information sheet summarizing the study protocol was given to the parents who agreed to participate in the study. They provided written informed consent. All children gave oral consent. At first, routine ear/nose/ throat examination, tympanometry, and fiberoptic nasopharyngoscopy were done before the operative period. ATs were performed using curettage and cold dissection methods by the same surgeon. After all evaluations and exami-nations, the parents of children with an indication for AT were informed about the surgery and study. All patients were followed up periodically until the sixth postoperative month. They were assessed before surgery and 6 months after surgery in terms of ADHD symptoms, sleep problems, and QoL using the below-mentioned scales by the child–adolescent psychiatrist.
Measures
Pediatric Quality of Life Inventory, Parent version (PedsQL-P): Varni et al. developed the PedsQL-P to evaluate health-related QoL (HRQOL) in children between the ages of 2 and 18 years old.23 Each item is scored on a five-point Likert-type scale. They yield a total score and two subscale scores as “psychosocial” and “physical health.” Cakin Memik et al. conducted the reli-ability and validity study of the PedsQL-P for Turkish children and adoles-cents.24,25 The PedsQL-P is a quick, simple measurement tool that is scored on a five-point Likert-type scale. The scale includes both parent and child
versions. Higher PedsQL-P total scores are associated with higher comfort levels. In the current study, the Cronbach’s alpha coefficient of this scale was determined as 0.89 for the child self-report and 0.92 for the parent proxy report in 8- to 12-year-old children and as 0.91 for the child self-report and 0.93 for the parent proxy report in 13- to 18-year-old adolescents. Higher PedsQL total scores indicate better HRQOL.
Conners Parent Rating Scale-Revised Short (CPRS-RS): The CPRS-RS is the most useful and popular rating scale for ADHD domains. Conners et al. conducted the revision of this scale.26The CPRS-RS that contains 27 items was translated and transcribed for Turkish children by Kaner et al. The Turkish version of the CPRS-RS was found to be reliable, valid, and appropriate for clinical purpose and research.27 Parents answer to each item on a four-point Likert-type scale (0¼ never, 1 ¼ rarely, 2 ¼ often, and 3 ¼ always). A four sub-scale scores was identified for ADHD symtomps, including hyperactivity (6 items), oppositional (6 items), cognitive problems/inattention (6 items), and ADHD Index (12 items). The Cronbach’s alpha coefficient of this scale was determined to be between 0.73 and 0.86. The CPRS-RS has a high test–retest reliability (between 0.56 and 0.72).
Children’s Sleep Habits Questionnaire (CSHQ): The CSHQ is a sleep assess-ment instruassess-ment in children and rated by parents. It consist of 33 items (eight subscale scores) and 48 items (total score) that contain key sleep domains and include medical and sleep behavior disorders in children.28Higher scores in all subscales show more serious sleep problems. The CSHQ contains eight domains: daytime sleepiness, sleep anxiety, sleep duration, night waking, sleep-onset delay, parasomnias, SDB, and bedtime resistance. Perdahlı Fis et al. conducted the validity and reliability study of the Turkish version of this scale.29 The Cronbach’s alpha coefficient and test–retest reliability coefficient of the sub-scales were respectively 0.78 and 0.81.
Stanford-Binet Intelligence Test: It was developed by Terman and Merill.30 It is an oral and performance test. Fifteen different subtests of this test were organized in a manner that would measure four types of intelligence regarded as the signs of intelligence. These are short-term memory, verbal judgment, quantitative judgment, and abstract/visual judgment. It was adapted to Turkish language by Ugurel-Semin.31 These tests can be used in children between the ages of 2 and 16 years old.
Wechsler Intelligence Scale for Children-Revised: It was developed for determining the general intelligence levels by Wechsler in 1949. The scale was revised in 1974 and named as WISC-R.32 The Turkish adaptation study of the scale was made by Savasır and Sahin.33 It contains two sections (verbal and performance) that consist of 12 subtests measuring various intelligence func-tions. The WISC-R can be used in children between between the ages of 6 and 16 years old.
Statistical methods
The SPSS package program, version 21.0 (SPSS Inc., Chicago, IL, USA) was used to perform all data analyses. The Kolmogorov-Smirnov test was used for the analysis of compliance with the normal distribution. The Chi-square test or Fisher’s exact test was performed for the comparison of categorical variables. The Paired t-test (a parametric test) was applied for comparing normally dis-tributed data. The Mann-Whitney U and Wilcoxon two-sample paired signed-rank tests were applied for comparing non-normally distributed data. The Chi-square and McNemar tests were performed for the comparison of qualitative data. A value of p< 0.05 was considered statistically significant.
Results
A total of 64 subjects (32 boys and 32 girls) were included in the study. The mean age was 6.8 2.4 years (range 4–15 years). When the preoperative and postoper-ative ADHD parent scores of the patients with AT were evaluated, the mean ADHD index (11.98 6.94 vs. 10.35 6.44) (p < 0.05, t ¼ 2.46) and oppositional scores (6.73 3.72 vs. 5.87 3.52) (p < 0.05, t ¼ 2.46) showed statistically signif-icant improvement after AT. Cognitive problems/inattention and hyperactivity scores were decreased but not statistically significant (p> 0.05). The seven domain scores (daytime sleepiness, sleep-onset delay, night waking, bedtime resistance, sleep anxiety, parasomnias, and SDB, except for sleep duration) of the CSHQ were statistically significantly decreased after AT. The PedsQL-P total score (66.57 12.94 vs. 73.58 12.46) and both PedsQL-P physical health (64.20 19.81 vs. 69.84 18.63) (p < 0.05, t ¼ –2.67) and psychosocial health subdomain scores (67.83 12.89 vs. 75.57 13.16) (p < 0.05, t ¼ –4.92) were sig-nificantly higher at six months after AT (p< 0.05, t ¼ –4.73). All scale scores are shown in Table 1.
Discussion
CAH and ADHD symptoms are common health problems in childhood. In many studies, sleep disturbance, ADHD, behavioral disorders, and other psychiatric disorders have been suggested to be frequently met in children with upper airway obstruction including CAH.8,34,35 The present study showed that AT for pediatric adenotonsillar hypertrophy led to significant improvements in sleep problems, ADHD-like symptoms including behavioral problems, and QoL.
The results of our study were similar to the results of a previous study show-ing that daytime sleepiness, sleep-onset delay, night wakshow-ing, bedtime resistance, sleep anxiety, parasomnias, and SDB improved at six months after AT. Similarly, Walker et al. showed that sleep disturbance improved significantly
after AT in children with CAH/SDB.36In a study conducted by Biyani et al. in 2017, sleep disturbances including narcolepsy and sleep apnea showed signifi-cant improvement following AT in children with CAH.37 In another study, Constantin et al. demonstrated that AT improved sleep disturbance and QoL.38 Our results are consistent with these results. Improvement of sleep dis-orders is important for improvement in both ADHD-like symptoms and QoL. The majority of brain hormones affecting neurodevelopmental processes are secreted during a night’s sleep. In this respect, the increase in the quality of sleep is quite important in terms of neurocognitive development.39
In our study, the mean ADHD index and oppositional scores of the CPRS-RS decreased significantly after AT, to the extent that the parents were relieved about their children’s behaviors. We think that ADHD index scores are very important for a global view on the severity of ADHD symptoms. In a study performed by Huang et al., 66 school-age children with SDB including CAH and ADHD were divided into three groups: 27 were treated with methylpheni-date (MPH), 25 underwent AT, and 14 had no treatment. After a period of six months, the severity of symptoms and signs was more reduced in both AT and MPH groups than in the nontreatment group. In addition, the AT group
Table 1. Distribution of PedsQL-P, CPRS-RS, and CSHQ scale scores, according to before and after AT.
Before AT After AT z/t/v2 p
PedsQL-P
Physical Health Total Score 64.20 19.81 69.84 18.63 –2.67 <0.001
Psychosocial Health Total Score 67.83 12.89 75.57 13.16 –4.92 <0.001
Total Scale Score 66.57 12.94 73.58 12.46 –4.73 <0.001
CPRS-RS Cognitive problem-inattention 5.32 3.66 4.95 3.82 0.96 >0.05 Hyperactivity 5.06 3.49 4.96 3.42 0.28 >0.05 Oppositional 6.73 3.72 5.87 3.52 2.46 <0.05 ADHD Index 11.98 6.94 10.35 6.44 2.41 <0.05 CSHQ Bedtime resistance 10.73 2.82 9.75 2.61 3.06 <0.05 Sleep-onset delay 1.48 0.64 1.34 0.56 –1.96 <0.05 Sleep duration 4.48 2.13 4.21 1.46 –0.48 >0.05 Sleep anxiety 7.39 2.28 6.70 2.20 2.66 <0.05 Night waking 4.75 1.57 4.26 1.32 –2.92 <0.05 Parasomnias 10.37 2.72 9.18 1.96 4.71 <0.001 Sleep-disordered breathing 6.26 2.17 4.03 1.62 –5.61 <0.001 Daytime sleepiness 12.28 3.03 11.21 3.28 2.81 <0.05 CSHQ totale 57.76 9.19 50.71 7.98 –5.61 <0.001
PedsQL-P: Pediatric Quality of Life Inventory, Parent; CPRS-RS: Conners Parent Rating Scale-Revised Short; CSHQ: Children’s Sleep Habits Questionnaire; AT: Adenotonsillectomy.
showed more significant improvements in sleep quality, obstructive apnea, impulsivity, attention, and ADHD index scores compared with the MPH group.40 Goldstein et al. evaluated 64 children between the ages of 2 and 18 years old with the Child Behavior Checklist before AT and three months post-operatively. Behavioral and emotional difficulties in children with CAH/SDB before treatment improved after the intervention.6 In another study, Weber et al. showed a significant improvement in ADHD index scores at six months after AT in children with CAH/SDB.41The improvement in ADHD-like symp-toms may be associated with the improvement in both sleep disturbance and intermittent/chronic hypoxemia episodes of brain. ADHD is a neurodevelop-mental disorder arising from hypovigilance rather than hypervigilance. Actually, if hypovigilance is the etiology of such a disorder, it is expected that a child suffering from ineffective or insufficient sleep secondary to upper airway obstruction such as obstructive apnea syndrome will have a more severe form of ADHD. Therefore, if sleep apnea resolves and sleep quality improves, ADHD symptoms will heal more rapidly.39
This study showed that children with CAH achieved a significant improve-ment in QoL after AT. Similar to our study, some studies have found that children with CAH achieved a significant improvement in QoL in the short and long term after AT.19,21 Nowadays, QoL is accepted as an important health measurement in clinical medicine. The measurement of QoL is quite important because CAH, sleep problems, and ADHD-like symptoms are prev-alent as comorbid conditions. Therefore, the effect of treatment on QoL should be assessed. Schilder showed similar results with our study in children with CAH/SDB symptoms and also found that early AT compared with watchful waiting provided improvement in behavior, polysomnographic findings, and QoL but no improvement in executive function or attention.42 Similarly, Marcus et al. suggested that AT compared with watchful waiting in children with CAH/SDB reduced symptoms and improved the secondary outcomes of polysomnographic findings associated with CAH and QoL but did not signifi-cantly improve executive function or attention.43
Our study has several limitations. The first limitation of our study is that there was no one-year follow-up of a reduction in the severity of ADHD symp-toms. The second limitation of our study is the absence of teacher ratings. Because an interval of six months made a separation between baseline and follow-up measures, the teacher’s observation ratings could reduce potential factors that confound the evaluation. The third limitation of our study is the absence of polysomnography; however, polysomnography is also a costly and difficult measurement especially for children. The fourth limitation of our study is that we had a small sample size.
In conclusion, the results of this study showed that AT significantly improved oppositional/ADHD symptoms and sleep disturbance. In this way, AT signifi-cantly improves QoL in children with CAH. Sleep is not always assessed in
children with ADHD; however, children with ADHD should be assessed for sleep quality, checked for enlarged tonsils, and questioned for presence of snor-ing. In children with CAH, sleep disturbance should be taken into consideration as an underlying cause of ADHD-like symptoms. Therefore, child–adolescent psychiatrists should work with otolaryngology/head and neck specialists and other specialists performing AT in order to identify children with ADHD symp-toms and sleep disturbance who suffer from CAH. Thus, long-term medical therapy and its potential complications can be avoided.
Author contributions
All authors made a substantial contribution to the conception and design or analysis and interpretation of data, drafting the article or revising it critically for important intellectual content, and final approval of the version to be published.
Declaration of conflicting interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author(s) received no financial support for the research, authorship, and/or publi-cation of this article.
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