Effects of an Adenotonsillectomy on the Cognitive and Behavioural Function of Children Who Snore A naturalistic observational study

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.


O
bstructive sleep apnoea (osa) is estimated to affect between 1.2-5.7% of the paediatric population. 1,2The condition is characterised by intermittent partial or complete obstruction of breathing during sleep. 3Among children, adenotonsillar 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. 5he neuropsychological sequelae of childhood OSA may include compromised cognitive, emotional and social function. 6,7n adenotonsillectomy (AT) is considered the first line of treatment for paediatric OSA. 8,91][12] However, to the best of the authors' knowledge, no studies have yet been conducted among Arab children with OSA.Furthermore, previous studies on this topic have focused on younger children (3-9-yearolds) and longer follow-up periods (≥6 months). 13,14As 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-evaluation 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 5 th and 85 th percentile 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. 15During 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 calculated 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. 15,16All children who fulfilled the criteria for mild-to-severe OSA were scheduled 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. 15he children were also evaluated at baseline and three months post-AT for ADHD indices and cognitive 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. 17The 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.
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. 19Each 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. 20he 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. 21The 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 approximately one word every two seconds.The total score was based on the number of words recalled over three trials. 22The Tower of London neuropsychological test was used to determine deficits in planning and temporal organisation, which are important constituents of executive function. 22The 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. 23tatistical analysis was performed using the Statistical 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].

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. 6,7Conversely, OSA has also been associated with cognitive and intellectual deficits as well as ADHD-like symptoms. 24uch findings indicate that clinicians should be vigilant in excluding OSA among children with cognitive and intellectual deficits and ADHD or vice versa.A previous study conducted in Oman suggested that the prevalence rate of ADHD was 8.8% among 9-10-yearolds. 25However, 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. 25Longer-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.7][28][29][30] Previous studies on this topic have focused on evaluating cognitive and behavioural changes between 6-12 months after the surgery. 13,14,31In contrast, the current study evaluated cognitive and behavioural function over a much shorter follow-up period.12][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.