- Email: [email protected]
Impact of adenotonsillectomy on ADHD and nocturnal enuresis in children with chronic adenotonsillar hypertrophy
AMERI CA N JOURNAL OF OT OLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
Available online at www.sciencedirect.com
ScienceDirect www.elsevier.com/locate/amjoto
Impact of adenotonsillectomy on ADHD and nocturnal enuresis in children with chronic adenotonsillar hypertrophy Battal Tahsin Somuk, MD a , Hasan Bozkurt, MD b,⁎, Göksel Göktaş, MD a , Osman Demir, PHD c , Levent Gürbüzler, MD a , Ahmet Eyibilen, MD a a b c
Department of Otolaryngology, Head and Neck Surgery, Gaziosmanpasa University Hospital, Tokat, Turkey Department of Child and Adolescent Psychiatry, Gaziosmanpasa University Hospital, Tokat, Turkey Department of Biostatistics, Gaziosmanpasa University Hospital, Tokat, Turkey
ARTI CLE I NFO
A BS TRACT
Article history:
Objective: Children with chronic adenotonsillar hypertrophy (CAH) are more likely to have
Received 26 May 2015
symptoms of attention deficit hyperactivity disorder (ADHD) and enuresis nocturna (EN) and benefit from surgery. The aim of this study was to evaluate the effect of adenotonsillectomy on ADHD and EN symptoms in children with CAH. Study design: Cross-sectional study was conducted. Setting: Parent-based questionnaires. Methods: Parents of children with CAH were given Turgay DSM-IV Based Child and Adolescent Behavior Disorders Screening and Rating Scale (T-DSM-IV) and Nocturnal Enuresis Questionnaire (NEQ) before and six months after adenotonsillectomy. Inattention (IA) and hyperactivity–impulsivity (HI) subscores of T-DSM-IV were used in the present study. The rates of ADHD and EN were compared before and after surgery. Results: A total of 75 children between 5 and 16 years of age and their families participated in the study. All 75 families completed T-DSM-IV and NEQ. Mean IA (5.69 ± 4.88 versus 4.46 ± 4.40) and HI (6.53 ± 5.60 versus 5.93 ± 5.45) scores as well as total ADHD scores (12.22 ± 8.99 versus 10.42 ± 8.70) improved significantly after surgery. This significance was found to be statistically important (p < 0.05). Furthermore 26 of the subjects were diagnosed with primer EN before adenotonsillectomy and 14 of these enuretic children had total remission six months after surgery. The frequency of EN dropped from 34.7% to 16.0% and this remission rate was found to be statistically significant (p < 0.05). Conclusion: Children with CAH had high frequency of ADHD and EN symptoms in the present study. Adenotonsillectomy was found to be effective in improvement of these symptoms. © 2015 Elsevier Inc. All rights reserved.
1.
Introduction
The impact of chronic adenotonsillar hypertrophy (CAH) and related symptoms on childhood development and behavior has
been well published. Symptomatic CAH manifesting various degrees of airway obstruction can lead to sleep problems like sleep disordered breathing (SDB), neurocognitive dysfunction [1,2], externalizing symptoms, such as hyperactivity, impulsivity,
⁎ Corresponding author at: Department of Child and Adolescent Psychiatry, Gaziosmanpasa University Medical Faculty Hospital, Tokat, Turkey. Tel.: +90 356 2129500. E-mail address: [email protected] (H. Bozkurt). http://dx.doi.org/10.1016/j.amjoto.2015.08.003 0196-0709/© 2015 Elsevier Inc. All rights reserved.
28
AMERI CAN JOURNAL OF OTOLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
aggression, oppositional behavior, conduct problems [3–6], and somatization and internalizing symptoms, such as anxiety, depression, social withdrawal, and emotional instability [7–9]. Several studies have found that CAH has been associated with attention deficit hyperactivity disorder (ADHD), and treatment of CAH may diminish symptoms of ADHD in a subset of children. ADHD and other disruptive behavior disorders have been found to be the most common psychiatric diagnoses in children undergoing adenotonsillectomy [6]. Because ADHD is one of the most common psychiatric disorder of childhood, relation with ADHD and CAH has become more important in this context. Children with ADHD symptoms should be assessed from view of CAH and surgery is often associated with improvement in these symptoms and decreased need for stimulants. On the other hand, CAH in childhood is occasionally associated with enuresis nocturna (EN) [10]. Higher incidence of enuresis with a percentage of 35 was reported in children with obstructive sleep apnea syndrome (OSAS) compared with their healthy peers and adenotonsillectomy significantly improved enuresis in these children [11]. In addition, enuresis is also common in children with ADHD although the mechanism of enuresis in ADHD remains elusive. Previous studies have demonstrated a significantly increased prevalence of ADHD in children with enuresis [12,13]. So children with ADHD and drug resistant enuresis should be assessed in consideration of the possibility of CAH and related disorders. The purpose of this study is to investigate the rates of ADHD and EN symptoms in children with CAH and also the impact of adenotonsillectomy on these symptoms in this population. Possible mechanisms will be discussed.
2.
Materials and methods
2.1.
Participants
Subjects for this study were recruited from a sample of pediatric cases referred to Otorhinolaryngology Department of Gaziosmanpasa University Medical Faculty Hospital between January 2013 and June 2014. The study enrolled 75 children with CAH ranging in age from 5 to 16 years. Children with autism spectrum disorders or mental retardation (IQ < 70), and having diagnosis of any neurologic or metabolic disorder were excluded from the study.
2.2.
Measures
2.2.1. Turgay DSM-IV Based Child and Adolescent Behavior Disorders Screening and Rating Scale (T-DSM-IV) The scale was developed by Turgay et al. [14] and translated and adapted to Turkish by Ercan et al. [15]. It is based on the DSM-IV diagnostic criteria and evaluates inattention (IA) (9 items), hyperactivity–impulsivity (HI) (9 items), opposition defiance (OD) (8 items), and conduct disorder (CD) (15 items). Greater scores reflect increase in severity. Symptoms are scored by assigning a severity estimate for each symptom on a 4-point Likert-type scale (0 = not at all, 1 = just a little, 2 = quite a bit, and 3 = very much). IA and HI subforms of the scale were used to assess ADHD rating in this study.
2.2.2.
Nocturnal Enuresis Questionnaire (NEQ)
This questionnaire was developed by the authors to assess nocturnal enuresis. It includes specific questions about enuresis nocturna based on DSM-IV criteria. NEQ was filled by the help of a clinician to diagnose EN in the present study.
2.3.
Procedure
Children who referred to Otorhinolaryngology Department with such complaints like nasal congestion, snoring, sleeplessness, mouth sleeping and night sweating underwent clinical examination. A routine ear–nose–throat examination, fiberoptic nasopharyngoscopy and tympanometry were performed during the preoperative period. Following the evaluation, the parents of children with an indication of adenotonsillectomy were informed about the study. In order to determine the frequency of ADHD and EN, parents were asked to fill out T-DSM-IV scale by themselves and NEQ by the help of a clinician at the preoperative visits. There were no intraoperative or postoperative complications. After discharge, the patients were followed up periodically until the sixth postoperative month. At postoperative month six, the parents filled out the forms by the same way as in the preoperative period and the patients underwent a general examination. All families completed T-DSM-IV and NEQ both in the preoperative and postoperative periods. Written informed consent from parents was taken and the faculty ethical committee approved the study.
2.4.
Statistical analysis
Statistical analysis was performed by using commercial software (IBM SPSS Statistics 19). Values are expressed as N (%) or mean ± SD. Independent samples T test was used for continuous variables in comparisons between two groups. Yates corrected chi-square test or Fisher’s test was used for comparisons of qualitative variables. Paired samples test was used for comparison of two dependent measurements. p < 0.05 was considered as statistically significant.
3.
Results
The study consisted of 75 subjects (46 males and 29 females) with a mean ± SD of 9.28 ± 3.13 (between 5 and 16) years of age. Mean IA (5.69 ± 4.88 versus 4.46 ± 4.40) (before versus after surgery) and HI (6.53 ± 5.60 versus 5.93 ± 5.45) scores as well as total ADHD scores (12.22 ± 8.99 versus 10.42 ± 8.70) improved significantly after surgery. This significance was found to be statistically important (p < 0.05). Furthermore 26 of the subjects were diagnosed with primer EN before adenotonsillectomy and 14 of these enuretic children had total remission six months after surgery. The frequency of EN dropped from 34.7% to 16.0% and this remission rate was found to be statistically significant (p < 0.05). Table 1 shows the comparison of ADHD scores and EN rates of the sample before and after adenotonsillectomy. Decrease in IA and HI scores and remission in EN were also statistically significant in both males and females.
AMERI CA N JOURNAL OF OT OLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
Table 1 – ADHD scores and EN rates before and after surgery.
ADHD scores (mean ± SD) IA HI EN rates (N %) Yes No
4.
Before AT
After AT
p Value
5.69 ± 4.88 6.53 ± 5.60
4.46 ± 4.40 5.93 ± 5.45
0.002 <0.001
26 (34.7%) 49 (65.3%)
12 (16.0%) 63 (84%)
<0.001 0.031
Discussion
In this study, we evaluated the ADHD and EN symptoms and also the effect of adenotonsillectomy six months after surgery on the rate of these symptoms in children with CAH. The results are remarkable and also consistent with other studies carried out in individuals with symptomatic CAH. We used the term symptomatic CAH not only for sleep problems like SDB or OSAS but also all obstructive upper airway problems in the present study. A relation between symptomatic CAH and ADHD has been shown in many studies [6,16–19]. It was reported that symptom severity of ADHD and ADHD-related problems determined with such scales were found in a higher rate in children with CAH compared with healthy control group [16]. Prepubertal elementary school children whom had been scheduled for adenotonsillectomy were found to have higher prevalence of ADHD than their healthy peers [6]. Similarly, in our study, children with CAH showed an increased severity of symptoms of ADHD on T-DSM-IV. Adenotonsillectomy was found to be effective in improvement of combined ADHD symptoms in the present study which is in agreement with other studies. Weber et al. [17] demonstrated an improvement in attention deficit, hyperactivity and impulsivity six months after surgery in 8–11 years old children. Furthermore in a study of 66 school-aged children with ADHD and mild obstructive sleep apnea (OSA) by Huang et al. [18], 27 cases received methylphenidate, 25 underwent adenotonsillectomy, and 14 were assigned to a wait-and-see protocol. They found that the total ADHD scores of the group that underwent adenotonsillectomy improved compared to both the methylphenidate group and the untreated cases. Another study evaluating 35 children aged 5–12 years with CAH and ADHD found that the symptoms of both attention deficit and hyperactivity improved after the adenotonsillectomy [19]. Additionally, when compared subdivisions of ADHD, both IA and HA scores were found to be higher in our study. Related results in the literature are contradictory. Only attention deficit rather than hyperactivity and impulsivity was demonstrated to be associated with symptomatic CAH and improvements after adenotonsillectomy were generally observed in this area based on the findings of some studies [16,20–23]. Regarding the underlying mechanisms, intermittent hypoxia due to CAH related SDB is thought to play an important role in the relationship between SDB and neurocognitive deficits such as attention, memory and intelligence [24]. Moreover hypoxia may also result in selective impairments in executive function, while
29
sleep disorder may preferentially influence attention [25]. On the other hand there were also studies emphasizing higher inattention and hyperactivity rates related to CAH and improvements in both areas after surgery consistent with the present study. A study evaluating the effect of adenotonsillectomy on ADHD symptoms of children with CAH found that frequency of combined ADHD decreased significantly six months after surgery similar to our findings [19]. In the present study, we also found that EN was associated with symptomatic CAH and adenotonsillectomy had a favorable therapeutic effect on enuresis in children with CAH presenting this symptom. This finding is consistent with the literature demonstrating the relationship with EN and CAH. Obstructive upper airway problems were found to be very common in patients with EN and EN was also considered as a common symptom of obstructive upper airway problems [26]. The high prevalence of enuresis in children with symptomatic CAH is thought to be due to the effects of obstructive upper airway problems on arousal response, bladder pressure and urinary hormone secretion [27]. Moreover change in the rates of only disruptive behavior disorders and enuresis among all DSM-IV psychiatric diagnoses before and after adenotonsillectomy was found to be statistically significant but the other diagnoses indicated no difference in another study [6]. In our patients, the adenotonsillectomy indication was based on the anamnesis taken from the parents, the physical examination and the evaluation that was performed with flexible fiberoptic nasopharyngoscopy. Although the American Academy of Pediatrics [28] has recommended that the indications of adenotonsillectomy due to SDB should be based on the objective sleep test, less than 10% of adenotonsillectomies in North America are confirmed with polysomnography (PSG) [29]. Some studies also demonstrated that PSG may overlook mild SDBs and patients with normal PSG should also be operated [30]. PSG is also an expensive, time-consuming and difficult measurement especially for young children. So adenotonsillectomy in the present study was performed for symptomatic CAH, not only sleep problems but also other obstructive upper airway problems.
5.
Conclusion
Although the present study showed that higher rates of ADHD and EN in children with CAH and adenotonsillectomy have a beneficial effect on ADHD and EN symptoms of these children, there are limitations to this study such as small sample size, lack of control group and short follow-up period. Therefore, it is suggested that further randomized controlled studies should be conducted with larger sample sizes and longer follow-up periods to provide definitive evidence. Also we cannot dismiss the possibility that parental bias and expectancy effects may produce illusory improvements. So face to face interview for diagnosing psychiatric symptoms rather than scales is necessary. Based on the findings of our study, symptoms of ADHD and nocturnal enuresis should be born in mind in children with CAH or vice versa. Because adenotonsillectomy is shown to be curative for such symptoms, children with CAH whose parents report behavioral or emotional problems should be
30
AMERI CAN JOURNAL OF OTOLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
evaluated carefully to ensure necessary treatment at an early stage. Our study contributes to the literature by shedding light on the frequency of ADHD and EN in children with symptomatic CAH and therapeutic effect of adenotonsillectomy on these comorbidities.
REFERENCES
[1] Kurnatowski P, Putyński L, Lapienis M, et al. Neurocognitive abilities in children with adenotonsillar hypertrophy. Int J Pediatr Otorhinolaryngol 2006;70:419–24. [2] Blunden S, Lushington K, Kennedy D, et al. Behavior and neurocognitive performance in children aged 5–10 years who snore compared to controls. J Clin Exp Neuropsychol 2000;22: 554–68. [3] Ali NJ, Pitson D, Stradling JR. Sleep disordered breathing: effects of adenotonsillectomy on behaviour and psychological functioning. Eur J Pediatr 1996;155:56–62. [4] Ali NJ, Pitson D, Stradling JR. Snoring, sleep disturbance, and behaviour in 4–5 year olds. Arch Dis Child 1993;68:360–6. [5] Gottlieb DJ, Vezina RM, Chase C, et al. Symptoms of sleep-disordered breathing in 5-year-old children are associated with sleepiness and problem behaviors. Pediatrics 2003;112:870–7. [6] Dillon JE, Blunden S, Ruzicka DL, et al. DSM-IV diagnoses and obstructive sleep apnea in children before and 1 year after adenotonsillectomy. J Am Acad Child Adolesc Psychiatry 2007;46:1425–36. [7] Mitchell RB, Kelly J. Child behavior after adenotonsillectomy for obstructive sleep apnea syndrome. Laryngoscope 2005; 115:2051–5. [8] Aronen ET, Liukkonen K, Simola P, et al. Mood is associated with snoring in preschool-aged children. J Dev Behav Pediatr 2009;30:107–14. [9] Soylu E, Soylu N, Yıldırım YS, et al. The prevalence of psychiatric symptoms in preschool children with adenotonsillar hypertrophy. Int J Pediatr Otorhinolaryngol 2013;77:1094–8. [10] Brooks LJ, Topol HI. Enuresis in children with sleep apnea. J Pediatr 2003;142:515–8. [11] Brouilette R, Hanson D, David R, et al. A diagnostic approach to suspected obstructive sleep apnea in children. J Pediatr 1984;105:10–4. [12] Baeyens D, Roeyers H, D’Haese L, et al. The prevalence of ADHD in children with enuresis: comparison between a tertiary and non-tertiary care sample. Acta Paediatr 2006;95:347–52. [13] Baeyens D, Roeyers H, Hoebeke P, et al. Attention deficit/hyperactivity disorder in children with nocturnal enuresis. J Urol 2004;171:2576–9. [14] Turgay A. Disruptive Behavior Disorders Child and Adolescent Screening and Rating Scales for Children, Adolescents, Parents and Teachers. Michigan: Integrative Therapy Institute Publication; 1994.
[15] Ercan ES, Amado S, Somer O, et al. Development of a test battery for the assessment of attention deficit hyperactivity disorder. Turk J Child Adolesc Ment Health 2001;8:132–44. [16] Soylu E, Soylu N, Yildirim YS, et al. Psychiatric disorders and symptoms severity in patients with adenotonsillar hypertrophy before and after adenotonsillectomy. Int J Pediatr Otorhinolaryngol 2013;77:1775–81. [17] Weber SA, Lima Neto AC, Ternes FJ, et al. Hyperactivity and attention deficit syndrome in obstructive sleep apnea syndrome: is there improvement with surgical management? Braz J Otorhinolaryngol 2006;72:124–9. [18] Huang YS, Guilleminault C, Li HY, et al. Attention deficit/ hyperactivity disorder with obstructive sleep apnea: a treatment outcome study. Sleep Med 2007;8:18–30. [19] Dadgarnia MH, Baradaranfar MH, Fallah R, et al. Effect of adenotonsillectomy on ADHD symptoms of children with adenotonsillar hypertrophy. Acta Med Iran 2012;50:547–51. [20] Aydogan M, Toprak D, Hatun S, et al. The effect of recurrent tonsillitis and adenotonsillectomy on growth in childhood. Int J Pediatr Otorhinolaryngol 2007;71:1737–42. [21] Kurnatowski P, Putyński L, Lapienis M, et al. Physical and emotional disturbances in children with adenotonsillar hypertrophy. J Laryngol Otol 2008;122:931–5. [22] Ezzat WF, Fawaz S, Abdelrazek Y. To what degree does adenotonsillectomy affect neurocognitive performance in children with obstructive sleep apnea hypopnea syndrome due to adenotonsillar enlargement? ORL J Otorhinolaryngol Relat Spec 2010;72:215–9. [23] Suratt PM, Barth JT, Diamond R, et al. Reduced time in bed and obstructive sleep-disordered breathing in children are associated with cognitive impairment. Pediatrics 2007;119:320–9. [24] O’Brien LM, Gozal D. Behavioral and neurocognitive implications of snoring and obstructive sleep apnea in children: facts and theory. Paediatr Respir Rev 2002;3:3–9. [25] Blunden S, Lushington K, Lorenzen B, et al. Neuropsychological and psychosocial function in children with a history of snoring or behavioral sleep problems. J Pediatr 2005;146:780–6. [26] Aydil U, Iseri E, Kizil Y, et al. Obstructive upper airway problems and primary enuresis nocturna relationship in pediatric patients: reciprocal study. J Otolaryngol Head Neck Surg 2008;37:235–9. [27] Cinar U, Vural C, Cakir B, et al. Nocturnal enuresis and upper airway obstruction. Int J Pediatr Otorhinolaryngol 2001;59: 115–8. [28] 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;109:704–12. [29] Weatherly RA, Mai EF, Ruzicka DL, et al. Identification and evaluation of obstructive sleep apnea prior to adenotonsillectomy in children: a survey of practice patterns. Sleep Med 2003;4:297–307. [30] O’Brien LM, Mervis CB, Holbrook CR, et al. Neurobehavioral implications of habitual snoring in children. Pediatrics 2004; 114:44–9.
Available online at www.sciencedirect.com
ScienceDirect www.elsevier.com/locate/amjoto
Impact of adenotonsillectomy on ADHD and nocturnal enuresis in children with chronic adenotonsillar hypertrophy Battal Tahsin Somuk, MD a , Hasan Bozkurt, MD b,⁎, Göksel Göktaş, MD a , Osman Demir, PHD c , Levent Gürbüzler, MD a , Ahmet Eyibilen, MD a a b c
Department of Otolaryngology, Head and Neck Surgery, Gaziosmanpasa University Hospital, Tokat, Turkey Department of Child and Adolescent Psychiatry, Gaziosmanpasa University Hospital, Tokat, Turkey Department of Biostatistics, Gaziosmanpasa University Hospital, Tokat, Turkey
ARTI CLE I NFO
A BS TRACT
Article history:
Objective: Children with chronic adenotonsillar hypertrophy (CAH) are more likely to have
Received 26 May 2015
symptoms of attention deficit hyperactivity disorder (ADHD) and enuresis nocturna (EN) and benefit from surgery. The aim of this study was to evaluate the effect of adenotonsillectomy on ADHD and EN symptoms in children with CAH. Study design: Cross-sectional study was conducted. Setting: Parent-based questionnaires. Methods: Parents of children with CAH were given Turgay DSM-IV Based Child and Adolescent Behavior Disorders Screening and Rating Scale (T-DSM-IV) and Nocturnal Enuresis Questionnaire (NEQ) before and six months after adenotonsillectomy. Inattention (IA) and hyperactivity–impulsivity (HI) subscores of T-DSM-IV were used in the present study. The rates of ADHD and EN were compared before and after surgery. Results: A total of 75 children between 5 and 16 years of age and their families participated in the study. All 75 families completed T-DSM-IV and NEQ. Mean IA (5.69 ± 4.88 versus 4.46 ± 4.40) and HI (6.53 ± 5.60 versus 5.93 ± 5.45) scores as well as total ADHD scores (12.22 ± 8.99 versus 10.42 ± 8.70) improved significantly after surgery. This significance was found to be statistically important (p < 0.05). Furthermore 26 of the subjects were diagnosed with primer EN before adenotonsillectomy and 14 of these enuretic children had total remission six months after surgery. The frequency of EN dropped from 34.7% to 16.0% and this remission rate was found to be statistically significant (p < 0.05). Conclusion: Children with CAH had high frequency of ADHD and EN symptoms in the present study. Adenotonsillectomy was found to be effective in improvement of these symptoms. © 2015 Elsevier Inc. All rights reserved.
1.
Introduction
The impact of chronic adenotonsillar hypertrophy (CAH) and related symptoms on childhood development and behavior has
been well published. Symptomatic CAH manifesting various degrees of airway obstruction can lead to sleep problems like sleep disordered breathing (SDB), neurocognitive dysfunction [1,2], externalizing symptoms, such as hyperactivity, impulsivity,
⁎ Corresponding author at: Department of Child and Adolescent Psychiatry, Gaziosmanpasa University Medical Faculty Hospital, Tokat, Turkey. Tel.: +90 356 2129500. E-mail address: [email protected] (H. Bozkurt). http://dx.doi.org/10.1016/j.amjoto.2015.08.003 0196-0709/© 2015 Elsevier Inc. All rights reserved.
28
AMERI CAN JOURNAL OF OTOLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
aggression, oppositional behavior, conduct problems [3–6], and somatization and internalizing symptoms, such as anxiety, depression, social withdrawal, and emotional instability [7–9]. Several studies have found that CAH has been associated with attention deficit hyperactivity disorder (ADHD), and treatment of CAH may diminish symptoms of ADHD in a subset of children. ADHD and other disruptive behavior disorders have been found to be the most common psychiatric diagnoses in children undergoing adenotonsillectomy [6]. Because ADHD is one of the most common psychiatric disorder of childhood, relation with ADHD and CAH has become more important in this context. Children with ADHD symptoms should be assessed from view of CAH and surgery is often associated with improvement in these symptoms and decreased need for stimulants. On the other hand, CAH in childhood is occasionally associated with enuresis nocturna (EN) [10]. Higher incidence of enuresis with a percentage of 35 was reported in children with obstructive sleep apnea syndrome (OSAS) compared with their healthy peers and adenotonsillectomy significantly improved enuresis in these children [11]. In addition, enuresis is also common in children with ADHD although the mechanism of enuresis in ADHD remains elusive. Previous studies have demonstrated a significantly increased prevalence of ADHD in children with enuresis [12,13]. So children with ADHD and drug resistant enuresis should be assessed in consideration of the possibility of CAH and related disorders. The purpose of this study is to investigate the rates of ADHD and EN symptoms in children with CAH and also the impact of adenotonsillectomy on these symptoms in this population. Possible mechanisms will be discussed.
2.
Materials and methods
2.1.
Participants
Subjects for this study were recruited from a sample of pediatric cases referred to Otorhinolaryngology Department of Gaziosmanpasa University Medical Faculty Hospital between January 2013 and June 2014. The study enrolled 75 children with CAH ranging in age from 5 to 16 years. Children with autism spectrum disorders or mental retardation (IQ < 70), and having diagnosis of any neurologic or metabolic disorder were excluded from the study.
2.2.
Measures
2.2.1. Turgay DSM-IV Based Child and Adolescent Behavior Disorders Screening and Rating Scale (T-DSM-IV) The scale was developed by Turgay et al. [14] and translated and adapted to Turkish by Ercan et al. [15]. It is based on the DSM-IV diagnostic criteria and evaluates inattention (IA) (9 items), hyperactivity–impulsivity (HI) (9 items), opposition defiance (OD) (8 items), and conduct disorder (CD) (15 items). Greater scores reflect increase in severity. Symptoms are scored by assigning a severity estimate for each symptom on a 4-point Likert-type scale (0 = not at all, 1 = just a little, 2 = quite a bit, and 3 = very much). IA and HI subforms of the scale were used to assess ADHD rating in this study.
2.2.2.
Nocturnal Enuresis Questionnaire (NEQ)
This questionnaire was developed by the authors to assess nocturnal enuresis. It includes specific questions about enuresis nocturna based on DSM-IV criteria. NEQ was filled by the help of a clinician to diagnose EN in the present study.
2.3.
Procedure
Children who referred to Otorhinolaryngology Department with such complaints like nasal congestion, snoring, sleeplessness, mouth sleeping and night sweating underwent clinical examination. A routine ear–nose–throat examination, fiberoptic nasopharyngoscopy and tympanometry were performed during the preoperative period. Following the evaluation, the parents of children with an indication of adenotonsillectomy were informed about the study. In order to determine the frequency of ADHD and EN, parents were asked to fill out T-DSM-IV scale by themselves and NEQ by the help of a clinician at the preoperative visits. There were no intraoperative or postoperative complications. After discharge, the patients were followed up periodically until the sixth postoperative month. At postoperative month six, the parents filled out the forms by the same way as in the preoperative period and the patients underwent a general examination. All families completed T-DSM-IV and NEQ both in the preoperative and postoperative periods. Written informed consent from parents was taken and the faculty ethical committee approved the study.
2.4.
Statistical analysis
Statistical analysis was performed by using commercial software (IBM SPSS Statistics 19). Values are expressed as N (%) or mean ± SD. Independent samples T test was used for continuous variables in comparisons between two groups. Yates corrected chi-square test or Fisher’s test was used for comparisons of qualitative variables. Paired samples test was used for comparison of two dependent measurements. p < 0.05 was considered as statistically significant.
3.
Results
The study consisted of 75 subjects (46 males and 29 females) with a mean ± SD of 9.28 ± 3.13 (between 5 and 16) years of age. Mean IA (5.69 ± 4.88 versus 4.46 ± 4.40) (before versus after surgery) and HI (6.53 ± 5.60 versus 5.93 ± 5.45) scores as well as total ADHD scores (12.22 ± 8.99 versus 10.42 ± 8.70) improved significantly after surgery. This significance was found to be statistically important (p < 0.05). Furthermore 26 of the subjects were diagnosed with primer EN before adenotonsillectomy and 14 of these enuretic children had total remission six months after surgery. The frequency of EN dropped from 34.7% to 16.0% and this remission rate was found to be statistically significant (p < 0.05). Table 1 shows the comparison of ADHD scores and EN rates of the sample before and after adenotonsillectomy. Decrease in IA and HI scores and remission in EN were also statistically significant in both males and females.
AMERI CA N JOURNAL OF OT OLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
Table 1 – ADHD scores and EN rates before and after surgery.
ADHD scores (mean ± SD) IA HI EN rates (N %) Yes No
4.
Before AT
After AT
p Value
5.69 ± 4.88 6.53 ± 5.60
4.46 ± 4.40 5.93 ± 5.45
0.002 <0.001
26 (34.7%) 49 (65.3%)
12 (16.0%) 63 (84%)
<0.001 0.031
Discussion
In this study, we evaluated the ADHD and EN symptoms and also the effect of adenotonsillectomy six months after surgery on the rate of these symptoms in children with CAH. The results are remarkable and also consistent with other studies carried out in individuals with symptomatic CAH. We used the term symptomatic CAH not only for sleep problems like SDB or OSAS but also all obstructive upper airway problems in the present study. A relation between symptomatic CAH and ADHD has been shown in many studies [6,16–19]. It was reported that symptom severity of ADHD and ADHD-related problems determined with such scales were found in a higher rate in children with CAH compared with healthy control group [16]. Prepubertal elementary school children whom had been scheduled for adenotonsillectomy were found to have higher prevalence of ADHD than their healthy peers [6]. Similarly, in our study, children with CAH showed an increased severity of symptoms of ADHD on T-DSM-IV. Adenotonsillectomy was found to be effective in improvement of combined ADHD symptoms in the present study which is in agreement with other studies. Weber et al. [17] demonstrated an improvement in attention deficit, hyperactivity and impulsivity six months after surgery in 8–11 years old children. Furthermore in a study of 66 school-aged children with ADHD and mild obstructive sleep apnea (OSA) by Huang et al. [18], 27 cases received methylphenidate, 25 underwent adenotonsillectomy, and 14 were assigned to a wait-and-see protocol. They found that the total ADHD scores of the group that underwent adenotonsillectomy improved compared to both the methylphenidate group and the untreated cases. Another study evaluating 35 children aged 5–12 years with CAH and ADHD found that the symptoms of both attention deficit and hyperactivity improved after the adenotonsillectomy [19]. Additionally, when compared subdivisions of ADHD, both IA and HA scores were found to be higher in our study. Related results in the literature are contradictory. Only attention deficit rather than hyperactivity and impulsivity was demonstrated to be associated with symptomatic CAH and improvements after adenotonsillectomy were generally observed in this area based on the findings of some studies [16,20–23]. Regarding the underlying mechanisms, intermittent hypoxia due to CAH related SDB is thought to play an important role in the relationship between SDB and neurocognitive deficits such as attention, memory and intelligence [24]. Moreover hypoxia may also result in selective impairments in executive function, while
29
sleep disorder may preferentially influence attention [25]. On the other hand there were also studies emphasizing higher inattention and hyperactivity rates related to CAH and improvements in both areas after surgery consistent with the present study. A study evaluating the effect of adenotonsillectomy on ADHD symptoms of children with CAH found that frequency of combined ADHD decreased significantly six months after surgery similar to our findings [19]. In the present study, we also found that EN was associated with symptomatic CAH and adenotonsillectomy had a favorable therapeutic effect on enuresis in children with CAH presenting this symptom. This finding is consistent with the literature demonstrating the relationship with EN and CAH. Obstructive upper airway problems were found to be very common in patients with EN and EN was also considered as a common symptom of obstructive upper airway problems [26]. The high prevalence of enuresis in children with symptomatic CAH is thought to be due to the effects of obstructive upper airway problems on arousal response, bladder pressure and urinary hormone secretion [27]. Moreover change in the rates of only disruptive behavior disorders and enuresis among all DSM-IV psychiatric diagnoses before and after adenotonsillectomy was found to be statistically significant but the other diagnoses indicated no difference in another study [6]. In our patients, the adenotonsillectomy indication was based on the anamnesis taken from the parents, the physical examination and the evaluation that was performed with flexible fiberoptic nasopharyngoscopy. Although the American Academy of Pediatrics [28] has recommended that the indications of adenotonsillectomy due to SDB should be based on the objective sleep test, less than 10% of adenotonsillectomies in North America are confirmed with polysomnography (PSG) [29]. Some studies also demonstrated that PSG may overlook mild SDBs and patients with normal PSG should also be operated [30]. PSG is also an expensive, time-consuming and difficult measurement especially for young children. So adenotonsillectomy in the present study was performed for symptomatic CAH, not only sleep problems but also other obstructive upper airway problems.
5.
Conclusion
Although the present study showed that higher rates of ADHD and EN in children with CAH and adenotonsillectomy have a beneficial effect on ADHD and EN symptoms of these children, there are limitations to this study such as small sample size, lack of control group and short follow-up period. Therefore, it is suggested that further randomized controlled studies should be conducted with larger sample sizes and longer follow-up periods to provide definitive evidence. Also we cannot dismiss the possibility that parental bias and expectancy effects may produce illusory improvements. So face to face interview for diagnosing psychiatric symptoms rather than scales is necessary. Based on the findings of our study, symptoms of ADHD and nocturnal enuresis should be born in mind in children with CAH or vice versa. Because adenotonsillectomy is shown to be curative for such symptoms, children with CAH whose parents report behavioral or emotional problems should be
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AMERI CAN JOURNAL OF OTOLAR YNGOLOGY– H E AD AN D N E CK M EDI CI N E AN D S U RGE RY 3 7 ( 2 0 16 ) 27 – 3 0
evaluated carefully to ensure necessary treatment at an early stage. Our study contributes to the literature by shedding light on the frequency of ADHD and EN in children with symptomatic CAH and therapeutic effect of adenotonsillectomy on these comorbidities.
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