Departments of 1Surgery and 5Behavioural Medicine, Sultan Qaboos University Hospital; Departments of 2Behavioural Medicine, 3Family Medicine & Public Health, 6Physiology and 7Surgery, College of Medicine & Health Sciences, Sultan Qaboos University, Muscat, Oman; 4Department of Biostatistics, Christian Medical College, Vellore, India *Corresponding Author’s e-mail: dr.sanjayjaju@gmail.com تأثري إستئصال اللوزتني وحلمية األنف على مستوى اإلدراك والسلوك لدى األطفال الذين يعانون من الشخري أثناء النوم دراسة مبنية على املالحظة خالد الزعابي، �شمري العدوي، �شاجناي جاجو، لك�شمانن جيا�شيالن، نا�رص ال�شيباين، حممد العلوي، حممد العربي، را�شد العربي abstract: Objectives: This study aimed to evaluate cognitive and behavioural changes among 9–14-year- old Omani children with obstructive sleep apnoea (OSA) after an adenotonsillectomy (AT). Methods: This naturalistic observational study was conducted at the Sultan Qaboos University Hospital, Muscat, Oman, between January 2012 and December 2014. Omani children with adenotonsillar hypertrophy (ATH) underwent overnight polysomnography and those with confirmed OSA were scheduled for an AT. Cognitive and behavioural evaluations were performed using standardised instruments at baseline prior to the procedure and three months afterwards. Results: A total of 37 children were included in the study, of which 24 (65%) were male and 13 (35%) were female. The mean age of the males was 11.4 ± 1.9 years, while that of the females was 11.1 ± 1.5 years. Following the AT, there was a significant reduction of 56% in mean apnoea-hypopnoea index (AHI) score (2.36 ± 4.88 versus 5.37 ± 7.17; P <0.01). There was also a significant positive reduction in OSA indices, including oxygen desaturation index (78%), number of desaturations (68%) and number of obstructive apnoea incidents (74%; P <0.01 each). Significant improvements were noted in neurocognitive function, including attention/concentration (42%), verbal fluency (92%), learning/recall (38%), executive function (52%) and general intellectual ability (33%; P <0.01 each). There was a significant decrease of 21% in both mean inattention and hyperactivity scores (P <0.01 each). Conclusion: These results demonstrate the effectiveness of an AT in improving cognitive function and attention deficit hyperactivity disorder-like symptoms among children with ATH-caused OSA. Such changes can be observed as early as three months after the procedure. Keywords: Adenoidectomy; Obstructive Sleep Apnea; Cognitive Function; Behavior; Attention Deficit Hyperactivity Disorders; Children; Oman. الأطفال لدى وال�شلوك الإدراك م�شتوى على الأنف وحلمية اللوزتني ا�شتئ�شال تاأثري تقييم اإىل تهدف الدرا�شة هذه الهدف: امللخ�ص: العمانيني مبتو�شط عمر 14-9 �شنة والذين يعانون من انقطاع النف�س الإن�شدادي النومي. الطريقة: اأجريت هذه الدرا�شة املبنية على املالحظة مب�شت�شفى جامعة ال�شلطان قابو�س مب�شقط، عمان يف الفرتة املمتدة من �شهر يناير 2012 اىل �شهر دي�شمرب 2014. مت اإخ�شاع جميع الأطفال العمانيني امل�شاركني يف الدرا�شة والذين يعانون من ت�شخم اللوزتني وحلمية الأنف اىل درا�شة للنوم ومت اخ�شاع الأطفال الذين ثبت لديهم انقطاع النف�س الن�شدادي النومي اىل تدخل جراحي متمثل يف ا�شتئ�شال للوزتني وحلمية الأنف. متت درا�شة م�شتوى الدراك وال�شلوك لدى هوؤلء الأطفال قبل وبعد ثالثة اأ�شهر من التدخل اجلراحي. النتائج: بلغ عدد الأطفال امل�شاركني يف الدرا�شة 37 منهم 24 )%65( ذكور و موؤ�رص انخف�س اجلراحي التدخل بعد �شنة. 11.1 ± والإناث 1.5 �شنة 11.4 ± 1.9 الذكور امل�شاركني اعمار متو�شط بلغ اإناث. )35%( 13 انقطاع التنف�س اأثناء النوم مبعدل %56 )4.88 ± 2.36 مقارنة ب 7.17 ± 5.37؛ P >0.01(. كما اأ�شارت النتائج اأي�شا اإىل انخفا�س ملحوظ مرات وعدد )68%( الت�شبع عدد وموؤ�رص )78%( الأك�شجني ت�شبع موؤ�رص مت�شمنا النوم اأثناء النف�س انقطاع ملوؤ�رص الفرعية املوؤ�رصات يف انقطاع النف�س)%74؛ P >0.01 لكل منهما(. كما لحظ الباحثون حت�شنا كبريا يف م�شتوى الإدراك لدى الأطفال مت�شمنا م�شتوى النتباه والرتكيز )%42( وطالقة الل�شان )%92( والتعلم/الذاكرة )%38( ومهارات التنفيذ )%52( ومعدل الذكاء العام )%33؛ P >0.01 لكل منهما(. اأ�شارت الدرا�شة اآي�شا اىل انخفا�س معدل عدم النتباه وفرط احلركة بن�شبة )%21؛ P >0.01 لكل منهما(. اخلال�صة: هذه النتائج تو�شح فعالية التدخل اجلراحي )ا�شتئ�شال اللوزتني واللحمية( يف حت�شن م�شتوى الإدراك وال�شلوك لدى الأطفال الذين يعانون من اأعرا�س فرط احلركة وقلة النتباه ب�شبب انقطاع النف�س الإن�شدادي النومي ب�شبب ت�شخم اللوزتني وحلمية الأنف. من املمكن مالحظة هذه التغريات خالل ثالثة اأ�شهر بعد التدخل اجلراحي. الكلمات املفتاحية: ا�شتئ�شال حلمية الأنف؛ انقطاع النف�س الإن�شدادي النومي؛ م�شتوى الإدراك؛ ال�شلوك؛ ق�شور النتباه وفرط احلركة؛ اأطفال؛ عمان. Effects of an Adenotonsillectomy on the Cognitive and Behavioural Function of Children Who Snore A naturalistic observational study Khalid Al-Zaabi,1 Samir Al-Adawi,2 *Sanjay Jaju,3 Lakshmanan Jeyaseelan,4 Nasser Al-Sibani,2 Mohammed Al-Alawi,5 Mohammed Al-Abri,6 Rashid Al-Abri7 clinical & basic research Sultan Qaboos University Med J, November 2018, Vol. 18, Iss. 4, pp. e455–460, Epub. 28 Mar 19 Submitted 29 May 18 Revisions Req. 4 & 22 Jul 18; Revisions Recd. 11 & 28 Jul 18 Accepted 2 Aug 18 doi: 10.18295/squmj.2018.18.04.005 Effects of an Adenotonsillectomy on the Cognitive and Behavioural Function of Children Who Snore A naturalistic observational study e456 | SQU Medical Journal, November 2018, Volume 18, Issue 4 Obstruc tive sleep apnoe a (osa) is estimated to affect between 1.2–5.7% of the paediatric population.1,2 The condition is char- acterised by intermittent partial or complete obstruction of breathing during sleep.3 Among children, adenoton- sillar hypertrophy (ATH) can cause narrowing of the airway, leading to symptoms such as snoring, cessation of breathing and sleep fragmentation.4 This in turn reduces oxygen delivery to the terminal alveoli, thus affecting the gas exchange process and leading to tissue hypoxia.5 The neuropsychological sequelae of childhood OSA may include compromised cognitive, emotional and social function.6,7 An adenotonsillectomy (AT) is considered the first line of treatment for paediatric OSA.8,9 Findings from the Childhood Adenotonsillectomy Trial (CHAT) suggest that the procedure has the potential to atten- uate certain behavioural problems and enhance cognitive function.10–12 However, to the best of the authors’ knowl- edge, no studies have yet been conducted among Arab children with OSA. Furthermore, previous studies on this topic have focused on younger children (3–9-year- olds) and longer follow-up periods (≥6 months).13,14 As such, the present study aimed to explore pre- versus post-AT changes in cognitive function, attention deficit hyperactivity disorder (ADHD)-like symptoms and OSA indices among Omani children aged 9–14 years. This study also aimed to determine whether a re-eval- uation of cognitive and behavioural measures at three months post-AT could provide similar evidence to that noted at 6–12 months. Methods This naturalistic observational study was conducted at the Sultan Qaboos University Hospital (SQUH), Muscat, Oman, between January 2012 and December 2014. A total of 150 Omani children consecutively referred from local health centres with a history of snoring, mouth breathing and sleep disturbance suggestive of OSA due to ATH were targeted. However, 47 children with craniofacial or neurological abnormalities, a history of persistent and pervasive allergies or asthma, a body mass index not between the 5th and 85th perc- entile and those on psychotropic medications or deemed clinically unfit for surgical intervention were excluded from the study. The remaining 103 subjects underwent overnight polysomnography; of these, 60 were excluded as their symptoms did not fulfil the criteria for OSA. A final sample of 37 subjects were included in the study. The minimum sample size required was calculated to be 35 subjects at a two-sided alpha value of 0.5, power of 80% and expected effect size of 0.5. All of the children underwent in-hospital sleep studies using a portable level 3 sleep machine with an air flow sensor, chest and abdominal effort belt and oximeter.15 During the sleep study, the following five variables were monitored: (1) apnoea-hypopnoea index (AHI) score; (2) oxygen desaturation index (ODI) score; (3) the number of desaturations (NOD); (4) the number of obstructive apnoea (OA) incidents; and (5) the number of central apnoea (CA) incidents. AHI scores were calcul- ated based on the guidelines of the American Academy of Sleep Medicine (AASM), wherein 0–1 obstructive events per hour was considered normal, 2–5 was classified as mild OSA, 6–10 was considered moderate OSA and >10 was indicative of severe OSA.15,16 All children who fulfilled the criteria for mild-to-severe OSA were sched- uled for an AT. Those who underwent an AT also took part in another sleep study three months after the procedure to document any changes in OSA indices. Data were manually scored at baseline and three months post-AT by a sleep technologist who was blinded to the stage of research and in accordance with the AASM guidelines.15 The children were also evaluated at baseline and three months post-AT for ADHD indices and cognit- ive function (i.e. intellectual capacity, verbal fluency, attention/concentration, learning/recall and executive function). A board-certified psychologist who was blinded to the findings of the sleep study conducted cognitive evaluations of the subjects. Each child’s parents or caregivers were asked to take a checklist of ADHD symptoms from the short version of Conners’ Teacher Rating Scale (CTRS) to their child’s school so that their teacher could assess the frequency of certain behaviours associated with ADHD.17 The psychometric properties of the CTRS have been previously established among Omani children, with a cut-off value of >15 denoting ADHD cases.18 Advances in Knowledge - The findings of this study indicate that an adenotonsillectomy (AT) has beneficial effects on cognition and attention deficit hyperactivity disorder-like symptoms among children with obstructive sleep apnoea (OSA). - Such changes can be determined as early as three months after the procedure. - Previous research has focused on 3–10-year-old children; however, this study observed similar results among 9–14-year-olds. Application to Patient Care - An AT may improve cognitive and behavioural function among older paediatric patients with OSA. Khalid Al-Zaabi, Samir Al-Adawi, Sanjay Jaju, Lakshmanan Jeyaseelan, Nasser Al-Sibani, Mohammed Al-Alawi, Mohammed Al-Abri and Rashid Al-Abri Clinical and Basic Research | e457 The Raven’s Coloured Progressive Matrices test was used to establish the intellectual capacity of the participants. This test has been previously validated in the Omani population and consists of 36 items grouped into three sets.19 Each item contains a pattern with one part removed and between six and eight pictured inserts, of which the participant must choose the one with the correct pattern. The Controlled Oral Word Association Test was used to determine verbal fluency by examining lexical ability, executive control and the speed of verbal responses. The score was calculated based on the total number of acceptable words produced in three 30-second periods.20 The Digit Span Test, a subscale of the Wechsler Intelligence Scale for Children, was used to measure verbal/auditory attention and short-term memory. The score was based on the participant’s ability to recall seven pairs of random number sequences read aloud by the examiner, with the numbers read both forwards and backwards.21 The respondents’ ability to learn and remember was gauged using the Buschke Selective Reminding Test; this consists of lists of 12 words which are read aloud to the participant at the rate of approx- imately one word every two seconds. The total score was based on the number of words recalled over three trials.22 The Tower of London neuropsychological test was used to determine deficits in planning and temporal organisation, which are important constituents of exec- utive function.22 The participants were asked to realign coloured beads stacked on poles to three adjacent poles in a minimum number of moves during five trials. After two consecutive failures, the test was stopped. The total score was the sum of all correctly solved trials up to a maximum of 25 moves.23 Statistical analysis was performed using the Stat- istical Package for the Social Sciences (SPSS), Version 20.0 (IBM Corp., Armonk, New York, USA). A paired t-test or Wilcoxon test (paired samples) was used to compare the differences between pre- and post-AT indices of OSA and neurocognitive and behavioural function. Percentage changes were reported separately. This study was approved by the Medical Research & Ethics Committee of the College of Medicine & Health Sciences, Sultan Qaboos University (MREC #749). Written informed consent was obtained from the parents or guardians of all of the participants. Results A total of 37 children with OSA participated in the study, of which 24 (65%) were male and 13 (35%) were female. The mean age was 11.4 ± 1.9 years and 11.1 ± 1.5 years for males and females, respectively. The mean post-AT AHI score showed a significant reduction of 56% compared to the mean pre-AT AHI score (2.36 ± 4.88 versus 5.37 ± 7.17; P <0.01). Similarly, significant reductions were observed for the other OSA indices, including ODI score (78%), NOD (68%) and the number of OA incidents (74%; P <0.01 each). Although there was a reduction in the number of CA incidents (14%), this difference was not statistically significant (P = 0.73) [Table 1]. Following the AT, significant improvements were noted in all neurocognitive function parameters, including attention/concentration (42%), verbal fluency (92%), learning/recall (38%), executive function (52%) and general intellectual ability (33%; P <0.01 each). In addition, there was a significant decrease of 21% in both ADHD inattention and hyperactivity scores (P <0.01 each); however, the mean post-AT hyperactivity score nevertheless remained above a cut-off value of >15 (15.84 ± 4.13) [Table 2]. Discussion There is a plethora of evidence to suggest that children with cognitive and intellectual deficits and those with ADHD-like symptoms tend to have OSA.6,7 Conv- ersely, OSA has also been associated with cognitive and intellectual deficits as well as ADHD-like symptoms.24 Such findings indicate that clinicians should be vigilant Table 1: Pre- and post-adenotonsillectomy changes in obstructive sleep apnoea indices among Omani children at the Sultan Qaboos University Hospital, Muscat, Oman (N = 37) Index Mean ± SD Change, unit (%) 95% CI P value* Pre-AT Post-AT AHI score 5.37 ± 7.17 2.36 ± 4.88 −3.00 (−56%) 1.16, 4.86 <0.01 ODI score 5.19 ± 8.14 1.14 ± 2.87 −4.05 (−78%) 1.72, 6.39 <0.01 Number of desaturations 31.22 ± 57.99 10.05 ± 28.81 −21.16 (−68%) 5.65, 36.67 <0.01 Number of OA incidents 16.51 ± 22.51 4.35 ± 13.69 −12.16 (−74%) 4.59, 19.74 <0.01 Number of CA incidents 3.32 ± 6.41 2.87 ± 4.93 −0.46 (−14%) 0.84, 1.76 0.73 SD = standard deviation; AT = adenotonsillectomy; CI = confidence interval; AHI = apnoea-hypopnoea index; ODI = oxygen desaturation index; OA = obstructive apnoea; CA = central apnoea. *Using a Wilcoxon signed ranks test. Effects of an Adenotonsillectomy on the Cognitive and Behavioural Function of Children Who Snore A naturalistic observational study e458 | SQU Medical Journal, November 2018, Volume 18, Issue 4 in excluding OSA among children with cognitive and intellectual deficits and ADHD or vice versa. A prev- ious study conducted in Oman suggested that the prev- alence rate of ADHD was 8.8% among 9–10-year- olds.25 However, it is not clear what percentage of this population also had OSA. In the current study, although there was a significant decrease in mean inattention and hyperactivity scores post-AT, this change does not indicate a reversal of ADHD-like symptoms, as the mean post-AT score remained above the cut-off value of >15 on the CTRS scale.25 Longer-term evaluation would perhaps shed more light on this finding. In the current study, indices of neurocognitive and behavioural function and OSA were found to improve significantly post-AT. These findings concur with those reported in the existing literature.26–30 Previous studies on this topic have focused on evaluating cognitive and behavioural changes between 6–12 months after the surgery.13,14,31 In contrast, the current study evaluated cognitive and behavioural function over a much shorter follow-up period. Kaditis et al. recommended re-eval- uation at six weeks post-AT while a 6–12-month range was used by CHAT researchers.10–13,32 Overall, it is still unclear at exactly which point in time neuroplasticity in children with OSA is likely to occur after an AT. Further research on this topic is warranted. In previous research, ATs were commonly perf- ormed for children between 3–9 years old.13,14 The current study included children aged 9–14 years old; this age group was chosen to ensure the correct diagnosis of ADHD-like symptoms, which are more accurately identified in older children.33 Additionally, more devel- opmentally appropriate and standardised cognitive measures are available for this population.34 Finally, the neurocognitive assessment of very young children can be logistically challenging, thus supporting the assessment of older children in the current study. Studies on younger children have been justified based on the assumption that OSA can trigger irreversible morbidity and that, therefore, the intervention should be implemented as quickly as possible.35 However, no neurobiological or molecular mechanisms have yet been identified to suggest that the pathological processes triggered by OSA can only be reversed in specific age groups. The CHAT researchers have recommended that ATs be performed on 3–10-year-olds.10–12 The current study was subject to certain limitations. First, the study constituted a naturalistic observation of routine medical services provided to children referred to one tertiary care hospital in Oman and therefore did not include a control group. While naturalistic observ- ational studies have the potential to lay the groundwork for further research with more robust methodologies, generalisation of the findings of such studies should be made with caution. Second, using a symptom check- list to diagnose ADHD is considered suboptimal comp- ared to semi-structured interviews in which the diagnosis is based on the International Classification of Diseases and the Diagnostic and Statistical Manual of Mental Disorders.36 Similarly, brain scans may be of some benefit to more accurately measure cognitive impairment.37 Third, this study did not take into account variations of hypoxaemia due to complex fluctuations in the assoc- iations between hypoxaemia and cognitive variables.38 Fourth, the study may have been affected by various confounders, such as maternal education, maturity, diet, parental supervision, socioeconomic status and spontaneous changes in cognition. Finally, a level three sleep study is considered suboptimal compared to level one. However, this type of sleep study machine is widely used in clinical practice and research and is considered an acceptable tool for diagnosing OSA.39 Table 2: Pre- and post-adenotonsillectomy changes in behavioural and cognitive function indices among Omani children with obstructive sleep apnoea at the Sultan Qaboos University Hospital, Muscat, Oman (N = 37) Index Mean ± SD Change, unit (%) 95% CI P value* Pre-AT Post-AT CTRS-IA score 18.76 ± 4.79 14.86 ± 3.65 −3.89 (−21%) 2.39, 5.40 <0.01 CTRS-H score 19.92 ± 6.72 15.84 ± 4.13 −4.08 (−21%) 2.19, 5.97 <0.01 DST score 6.83 ± 2.69 9.70 ± 4.51 +3.00 (+42%) −4.16, −1.84 <0.01 COWAT score 6.07 ± 5.45 11.67 ± 8.39 +5.49 (+92%) −7.28, −3.70 <0.01 BSRT score 18.65 ± 5.72 25.65 ± 5.49 +7.00 (+38%) −9.23, −4.77 <0.01 TOL score 11.46 ± 4.74 17.43 ± 5.19 +5.97 (+52%) −7.20, −4.74 <0.01 RCPM score 18.03 ± 7.47 23.97 ± 7.19 +5.95 (+33%) −7.35, −4.54 <0.01 SD = standard deviation; AT = adenotonsillectomy; CI = confidence interval; CTRS = Conners’ Teacher Rating Scale; IA = inattention; H = hyperactivity; DST = Digit Span Test; COWAT = Controlled Oral Word Association Test; BSRT = Buschke Selective Reminding Test; TOL = Tower of London; RCPM = Raven’s Coloured Progressive Matrices. *Using a paired t-test. Khalid Al-Zaabi, Samir Al-Adawi, Sanjay Jaju, Lakshmanan Jeyaseelan, Nasser Al-Sibani, Mohammed Al-Alawi, Mohammed Al-Abri and Rashid Al-Abri Clinical and Basic Research | e459 Conclusion The results of this study indicate that an AT is effective in improving cognitive function and reducing ADHD- like symptoms among children with OSA secondary to ATH. In addition, a short follow-up period of three months is sufficient to measure such changes. This study also suggests that post-AT neurobehavioural improvements extend beyond the previously studied age range of 3–9 years. conflict of interest The authors declare no conflicts of interest. funding No funding was received for this study. References 1. Dempsey JA, Veasey SC, Morgan BJ, O’Donnell CP. Patho- physiology of sleep apnea. Physiol Rev 2010; 90:47–112. https:// doi.org/10.1152/physrev.00043.2008. 2. DelRosso LM. Epidemiology and diagnosis of pediatric obstr- uctive sleep apnea. 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