Evaluation of neurocognitive abilities in children affected by obstructive sleep apnea syndrome before and after adenotonsillectomy
Obstructive sleep apnoea syndrome (OSAS) is the most severe form of sleep-related disordered breathing (SRDB) and is characterised by snoring, apnoeas, and/or hypopnoeas associated to hypoxia, hypercarbia, or repeated arousals from sleep. OSAS has three major categories of morbidities: neurobehavioural, cardiovascular and somatic growth failure. The gold standard for objective diagnosis of obstructive-SRDB severity is polysomnography (PSG). The indication for surgical treatment in children is moderate-severe OSAS (AHI, apnoea hypopnoea index > 5/h) and in mild OSAS (AHI 2-5/h) with complications or morbidity. The entire spectrum of PSG-defined SRDB (ranging from Primary Snoring to severe OSAS) may correlate with behavioural, attentional and executive function deficits relating to hypoxia and sleep disruption: in some cases, these alterations may mimic attention deficit hyperactivity disorder (ADHD). The aim of this research was to evaluate visuoperceptual and constructional abilities, paediatric sleep questionnaire and polysomnographic scores before and 6 months after adenotonsillectomy with objective and subjective information. We included 59 children who underwent neuropsychiatric and otolaryngologist clinical evaluation and the Beery-Buktenica Developmental Test of Visual-Motor Integration (VMI); children parents were asked to fill in the Paediatric Sleep Questionnaire (PSQ); each child underwent PSG. At 6 months after adenotonsillectomy, all patients were evaluated again. There is a significant difference in PSQ parameters, VMI standard, visual tests scores and PSG parameters before and after adenotonsillectomy in children affected by OSAS. These results showed the achievement of therapeutic benefits with improvement of the quality of life for both children and their parents.
Sleep-related disordered breathing (SRDB), pathologic nocturnal respiratory functioning, includes clinical conditions that range from primary snoring (PS) to obstructive sleep apnoea syndrome (OSAS) and represents one of the most common sleep disorders in childhood affecting up to one-third of children (prevalence up to 34.5%) 1,2.
OSAS is believed to be present in about 1% to 3% in children aged 2 to 18 with no gender predominance; furthermore, chronic snoring may be present in more than 10% of children 3-5. PS and OSAS are the two extreme conditions of a wide spectrum of increased resistance in the upper airways 3-5.
PS is the mildest form of SRDB and is defined as habitual snoring without discrete respiratory events, gas exchange abnormalities, or evidence of sleep fragmentation; OSAS is the most severe form of SRDB and is characterised by snoring, apneoas, and/or hypopnoeas associated with hypoxia, hypercarbia, or repeated arousals from sleep 6.
OSAS has three major categories of morbidities: neurobehavioural, cardiovascular and somatic growth failure 7,8. Symptoms in children with OSAS include snoring, breathing difficulty and/or breathing pauses during sleep, excessive sweating and enuresis; daytime symptoms may include oral breathing, headaches and excessive sleepiness, behavioural and neurocognitive changes such as attention deficit, hyperactivity, irritability, learning difficulties, memory loss and intelligence alterations 9-12. In adults but less so in children, OSAS is associated with arterial systemic hypertension due to alterations in the renin-angiotensin axis secondary to hypoxia during sleep; left ventricular wall thickness; pulmonary vascular hypertension 13,14. The gold standard for diagnosing OSAS is overnight polysomnography (PSG) which gives information about the frequency and severity of respiratory events and associated blood gas changes 15.
The European Respiratory Society (ERS) Task Force on diagnosis and management of obstructive SRDB in childhood (2 to 18 years old) analysed selected evidence from 362 articles since prospective cohort studies describing its clinical topics and randomised, double-blind, placebo-controlled trials, regarding its treatments, are scarce 16. Kaditis et al. summarised the conclusions of the ERS Task Force indicating seven steps for diagnosis and management of SRDB in children (Tab. I) 16,17.
Some clinical conditions can be considered as factors predicting long-term persistence of obstructive SRDB: obesity and increasing BMI percentile, male sex, severity of OSAS (AHI > 5 episodes/h), African-American Ethnicity and persistent tonsillar hypertrophy with a narrow mandible 18,19.
The gold standard for objective diagnosis of obstructive-SRDB severity is PSG and is indicated in children candidate to adenotonsillectomy especially in the presence of obesity, craniofacial deformities, neuromuscular disorders, complex abnormalities such as Chiari malformation, Down syndrome and Prader-Willi syndrome or when the need for treatment is unclear 20,21. Furthermore, PSG is indicated before and after rapid maxillary expansion or application of oral appliances, continuous positive airway pressure (CPAP) or noninvasive positive pressure ventilation (NPPV) treatments and when symptoms of OSAS persist after therapy 20.
The AHI, or the number of mixed, obstructive or central apnoeas and hypopnoeas per hour of total sleep time, is the most commonly used parameter to describe the severity of SRDB 22.
In children without SRDB symptoms or associated morbidities, the 90th percentile for the AHI according to the American Academy of Sleep Medicine (AASM 2007 scoring rules) is 3.2 episodes/h for the second year of life, up to 2.5 episodes/h for the ages > 2 and ≤ 6 years, and up to 2.1 episodes/h for the ages > 6 and < 18 years 23. OSAS is defined when AHI ≥ 2 episodes/h or in presence of SRDB symptoms when AHI ≥ 1 episode/h: mild OSAS if AHI 2-5 episodes/h; moderate-severe OSAS if AHI > 5 episodes/h (Tab. II) 18,23.
Indications for treatment in children is moderate-severe OSAS (AHI > 5/h) or mild OSAS (AHI 2-3/h) only when morbidities are present 18. The need for combined treatments (adenotonsillectomy when needed, weight loss, CPAP, NPPV) is a priority in these clinical conditions: major craniofacial abnormalities, neuromuscular disorders (i.e. Duchenne muscular dystrophy), achondroplasia, Chiari malformation, Down syndrome, mucopolysaccharidoses, Prader-Willi syndrome 24-26.
The entire spectrum of PSG-defined SRDB (ranging from PS to severe OSAS) may correlate with behavioural, attentional and executive function deficits relating to hypoxia and sleep disruption 27.
It is important to emphasise the risk of greater impairment of both behavioural and cognitive functions in children with milder forms of SRDB so that PS is not a universally benign condition 28. Preschool children with obstructive SRDB are more vulnerable in their adaptative and behavioural function vs. cognitive function: this age has a sort of ‘window of opportunity’ for early treatment by preventing cognitive deficits arising later in childhood 28.
Some authors analysed neurocognitive function in children with OSAS after CPAP-treatment (5-6 months): significant improvements in their abilities to analyse and synthesise abstract information, multitasking, simultaneous processing, divided attention and in recognition and recall for visual information were all shown 29.
Sleep disruption, even without respiratory compromise, may induce neurocognitive alterations, and for this reason the severity of SRDB, from PS to OSAS, does not correlate with neurocognitive deficits 30.
Cognitive functions are correlated with sleep fragmentation and thus to SRDB: arousals seem to be an important defensive mechanism against sleep fragmentations induced by SRDB 31. Children with high levels of arousal seem to present a high degree of protection against cognitive consequences of SRDB 32.
The aim of the present study is to analyse changes in neurocognitive and behavioural functions in children 4 to 11 years old affected by moderate-severe OSAS, after surgical treatment with adenotonsillectomy to investigate the role of obstruction in SRDB symptoms.
We evaluated visuoperceptual and constructional abilities, PSQ and full overnight polysomnographic values, before and 6 months after adenotonsillectomy, giving objective and subjective information about sleep disturbances in OSAS.
Materials and methods
We enrolled 86 children with obstructive SRBD, aged between 4 to 11 years old, referred by primary care paediatricians for snoring and suspected apnoeas to the Clinic of Child and Adolescent Neuropsichiatry and then to the Ear Nose and Throat Unit of the University of Campania “Luigi Vanvitelli” between October 2015 and April 2018.
Each child underwent neuropsychiatric and otolaryngologic clinical evaluation and VMI test, and parents were asked to fill in the PSQ.
Three overnight full sleep PSG were performed, and obstructive AHI were identified as normal, mild, moderate, or severe OSAS.
Inclusion criteria were: history of habitual snoring and/or apnea; frequent and continuous breathing pauses referred by parents; nocturnal difficult breathing; daytime hyperactivity; attentive deficit, poor school performance. Moreover, children with moderate (respiratory disturbance index of 5-10 episodes/h with average SaO2 > 95%) or severe (respiratory disturbance index >10 episodes/h with an average < 95% SaO2) OSAS were included; tonsillar and adenoidal grading 3-4, clinical febrile episodes (FE) and frequent acute pharyngotonsillitis2; age between 4 and 11 years.
Children were excluded if they had any of the following: sensorineural hearing loss; tube-tympanic alterations (OME otitis media with effusion, acute otitis media recurrent AOM); nasal obstruction due to nasal septal deviation or hypertrophy of inferior and middle turbinates, obesity (BMI ≥ 90th percentile); cardiac and pulmonary metabolic disorders; craniofacial anomalies; neuromuscular disorders and genetic syndromes.
During the first step of enrollment, we excluded 27 children: 15 did not meet inclusion criteria (4 obese children, BMI ≥ 90th percentile; 2 affected by otitis media with effusions associated to conductive hearing loss; 1 affected by craniofacial anirmalities, Pierre Robin Sequence and 8 children affected by mild OSA (AHI < 2); 10 children declined to participate; 2 children for other reasons.
At the end of this evaluation, we included 59 children affected by moderate-severe OSA (AHI > 5) with adenotonsillar hypertrophy.
The second step of treatment included adenotonsillectomy performed in the Ear Nose and Throat Unit of University of Campania “Luigi Vanvitelli”.
The third step included follow-up at 6 months after surgery: children underwent sleep PSG, VMI test and their parents filled in the PSQ. During this step, 22 patients refused to continue.
The last step of the analysis of data included 37 children mean age 8.44 ± 2.26 (Fig. 1).
Paediatric Sleep Questionnaire
PSQ is a SRBD scale questionnaire for children parents containing 22 items, indicating the presence of apnoeas. These items regard frequency, loud snoring, observed apnoeas, alterations in breathing during sleep, daytime symptoms and signs such as sleepiness, inattentive and hyperactive behaviour. Responses are “yes” (= 1 score), “no” (= 0 score), and “do not know” (= missing). A cut-off value of 0.33, which would be most effective in identifying pediatric OSA, was used.
Beery-Buktenica Developmental Test of Visual-Motor Integration (VMI)
The Beery-Buktenica Developmental Test of Visual-Motor Integration Performances in Children (VMI task) is a paper-and-pencil test in which children have to imitate or copy up to 27 geometric forms with increasing complexity using paper and pencil 32. The test was stopped when a child made more than two errors in a row 32. Copying errors were marked if they reflected problems in fine motor coordination and a pure visuospatial problem. The Beery VMI task is specifically designed for children and takes about 10 minutes to complete 32. The Beery VMI scores were standardised for age and gender using normative data for the Italian general population 32.
The percentile scores were used for diagnosing the visuomotor abnormalities in our sample. A value less than or equal to the 5th percentile was considered to indicate VMI impairment.
Overnight full polysomnography recordings (PSGs)
The polysomnographic recording was performed using a videorecorder connected to probes, electrodes and bands suitable to the patients’ age and weight. The exam is computerised and uses the Embletta System, a system recognised and appointed by the American Academy of Sleep Medicine for the study of sleep apnoea. The recording time is 6-8 hours, and supervised by medical and technical staff, who interpreted the data collected. We analysed sleep and respiratory parameters: Sleep Latency, SL (min); REM Latency, RL (min); Total Sleep Time, TST (min); Sleep Period Time, SPT or TIB-SL (min); Wake After Sleep Onset, WASO (min); 1-2-3 NREM, N1-N2-N3 (%TST); REM (%TST); Sleep Efficiency, SE or TST/TIB% (%); Arousal Index, AI (n Arousal/h sleep); Periodic Limb Movement Index, PLMI (n PLM/ h Sleep); AHI (number of AH/h sleep) Nadir SaO2 during sleep; Nadir SaO2 mean during sleep; Oxygen Desaturation Index, ODI (n desaturation/h sleep); TST % with SaO2 < 90%; TST % with SaO2 < 80%.
Each child underwent ear, nose and throat evaluation characterised by otoscopy, anterior rhinoscopy and oropharyngoscopy with particular attention to febrile episodes per year in the last 3 years. We evaluated haemochrome, antistreptolysin test, erythrocyte sedimentation rate, and creatine phosphokinase for all children. These clinical parameters are important to understand the indication for surgical treatment in children with adeno-tonsillar hypertrophy.
The tonsils were subjectively measured using a grading system. In grade I, the tonsils were hidden in the tonsillar fossa and were barely visible behind the anterior pillars. In grade II, the tonsils were visible behind the anterior pillars and occupied up to 50% of the pharyngeal space (the distance between the medial borders of the anterior pillars). In grade III, the tonsils occupied between 50 and 75% of the pharyngeal space. In grade IV, the tonsils occupied more than 75% of the pharyngeal space.
Adenoids were analysed during rhinofiberoptic evaluation: a grading system for adenoid hypertrophy was created based on the anatomical relationships between the adenoid tissue and the vomer, soft palate, and torus tubaris. The grading is based on the relationship of the adenoids to adjacent structures when the patient is at rest (i.e., when the soft palate is not elevated).
Patients underwent general anaesthesia in oral intubation maintaining supine in the Rose position. Adenoidectomy was performed followed by extracapsular tonsillectomy using cold/hot technique for dissection and cold/hot for homeostasis 33,34.
This study was conducted according to the World Medical Association Declaration of Helsinki and was retrospectively registered with number 28/2018.
Nonparametric analyses using the Wilcoxon Test were used to evaluate the effects of treatment (pre- and post-adenotonsillectomy) in the variables examined: PSQ test scores, VMI test standard scores (VMI, test motor and visual test), PSGs parameters (TIB, SPT, TST, SOL, FRL, SS-h, AWN-h, SE%, WASO-min, N1-min, N2-min, N3-min, REM-min, WASO spt, N1-spt, N2-spt, N3-spt, REM spt, N1-tst, N2-tst, N3-tst, REM-tst, PSQ, AHI, ODI, OD%, PLMI).
Pearson’s correlation was used to assess the mean preoperative and postoperative VMI scores with preoperative and postoperative polysomnographic parameters. The threshold for statistical significance was p < 0.05. All statistical analyses were performed with a statistical software package (STATISTICA 8.0, StatSoft Inc.)
The data collected before and 6 months after adenotonsillectomy are indicated in Tables III and IV. Table III shows the results of PSQ and VMI tests. There was a significant difference for PSQ parameters, VMI standard and VMI visual test (p < 0.05), but not for the VMI motor test.
In Table IV PSG parameters before and after adenotonsillectomy are shown. There was a significant difference for macrostructural sleep and respiratory parameters TIB, SPT, TST, SOL, SS-h, AWN-h, SE%, WASO-min, N1-min, N2-min, N3-min, REM-min, WASO spt, N1-spt, N2-spt, N3-spt, N1-tst, N2-tst, N3-tst, PSQ, AHI, ODI, OD%, PLMI (p < 0.05).
Clinical evaluation at PSQ six months after adenotonsillectomy showed a reduction in values compared with those before surgery (Fig. 2).
VMI standard scores, VMI motor test and VMI visual test scores showed improvements in performance at 6 months after surgery, which was significant for standard and visual scores (Figs. 3, 4) and not significant for motor scores (Fig. 5).
Spearman rank order correlation between preoperative and postoperative VMI scores and preoperative and postoperative PSG parameters was statistically significant p < 0.05 (Tab. V): there was no linear correlation. There was a significant difference for PSQ parameters, VMI standard, visual tests scores and PSG parameters, but not for motor test scores before and after adenotonsillectomy in children affected by OSAS. When comparting VMI standard, motor and visual tests score with PSG parameters, the difference before and after surgery was statistically significant.
Diagnosis and treatment of suspected mechanical OSAS in children represent a highly controversial issue for the differences in terms of diagnostic resources and therapeutic approach. Only careful evaluation of medical history and clinical presentation together with polysomnography, can provide the right diagnostic classification and, consequently, the correct choice of treatment 35-38. The resolution of mechanical obstruction must be as fast as possible in order to reduce the risk of cardiac, metabolic and neurological complications 7,8. Our attention is focused on the close relationship between OSAS and neurocognitive and neurobehavioral disorders in very young children with a mean age of 8.44 ± 2.26. The set of symptoms referred by patients or by children’s parents together with respiratory distress is often characterised by attention deficit and hyperactivity, irritability and learning disorders 9-12. Recent studies have shown a clear relationship of cause and effect between nocturnal hypoxia leading to respiratory events (obstructive apnoeas and hypopnoeas), alteration of the structure of sleep with fragmentation and arousals and neurocognitive deficit 9-12. In particular, it has been established that in OSAS patients the brain area mostly involved in the hypo-anoxic stress is the prefrontal cortex 9,38. It presents a considerable reduction in activity in all stages of sleep and seems to be disconnected from other cortex areas 9,37. Many authors have shown considerable improvement after adenotonsillectomy in children’s cognitive performance (memory, learning, IQ) and in quality of life (reduced daytime sleepiness, irritability and mood alteration) 15,38. These authors have used: Differential Ability Scales (similar to I.Q.), Non Verbal Cluster 36; Behavioral Assessment System for Children 39 (BASC), to evaluate the behaviour (mood, hyperactivity and somatisation); Epworth sleepiness Stairs and Osler Test (to evaluate semantic, episodic and work memory) 15; the Standfort Binet Intelligence Scale 5th edition and the Developmental Neuropsychological Assessment (NEPSY) for neuropsychological skills 40.
VMI test has never been performed to evaluate visual-motor performances in children with OSAS.
The Beery-Buktenuica Developmental Test of Visual-Motor Integration (VMI; Beery & Beery, 2004) was developed to assess visuoperceptual and constructional abilities in children and adolescents and is among the most widely administered neuropsychological tests 32,41,42. This test has been used to evaluate children with traumatic brain injury and attention-deficit/hyperactivity disorder (ADHD) 42.
We evaluated children with OSAS using VMI standard scores, motor and visual test scores, PSQ and PSG parameters before and at 6 months after adenotonsillectomy. Visuoperceptual and constructional performances were improved in all children after surgical treatment; analysis of sleep quality (respiratory parameters and neurological ones) showed better sleep macrostructural architecture and better respiratory scores after adenotonsillectomy than before.
The results showed the achievement of therapeutic benefits. Six months after the mechanical removal of the obstruction there was an improvement of cognitive performance and quality of life.
Dealing with a subject so controversial for the lack of homogeneity in terms of diagnostic and therapeutic resources, such as OSAS in children, we chose a multidisciplinary approach. Nowadays there are no studies in the literature specifically correlating mechanical OSAS and visual-spatial skills. We first assessed the deficiencies and then the improvements in visual-spatial skills in children affected by OSAS before and after adenotonsillectomy. Our idea has been confirmed by the results obtained from the 6 month postoperative VMI tests. At any starting level, all children showed improvement in performance. Thus, at 6 months after adenotonsillectomy important therapeutic benefits have been demonstrated both in visual-motor performance and in the child’s quality of life according to the objective data of PSG.
Figures and tables
|Step 1||Child at risk of SDB if (one or more)1.1. Symptoms of upper airway obstruction (snoring, apnoea, restless sleep, oral breathing)1.2. Finding on exam (tonsillar hypertrophy, obesity, midface deficiency, mandibular hypoplasia, neuromuscular disorders, Down syndrome, Prader-Willi Syndrome)1.3. Objective findings related to SDB (lateral neck radiography, flexible nasopharyngoscopy, cephalometry, upper airway MRI or CT)1.4. Prematurity or family history of SDB|
|Step 2||Recognition of morbidity and conditions coexisting with SRDB2.1. Morbidity Cardiovascular system: elevated blood pressure pulmonary hypertension and cor pulmonale Central nervous system: excessive daytime sleepiness inattention/hyperactivity cognitive deficits/academic difficulties behavioural problems enuresis and somatic growth delay or growth failure decreased quality of life Conditions coexisting with SRDB (probably common pathogenesis): history of recurrent otitis media or tympanostomy tube placement recurrent wheezing or asthma metabolic syndrome oral-motor dysfunction|
|Step 3||Recognition factors predicting long-term persistence of SDB3.1. Obesity and increasing BMI percentile Male sex Obstructive AHI > 5 episodes/h African-American ethnicity Untreated tonsillar hypertrophy, narrow mandible|
|Step 4||Objective diagnosis and assessment of SDB severity4.1. PSG or polygraphy if child at risk for SDB (step 1 and 2)4.2. OSAS-definition 1: SDB symptoms in combination with obstructive AHI ≥ 2 episodes/h or obstructive apnea index ≥ 1 episodes/h OSAS-definition 2: SDB symptoms and AHI ≥ 1 episodes/h (including central events) 4.3. If AHI ≥ 5 episodes/h SDB unlikely to resolve spontaneously and child at risk for morbidity4.4. if PSG or polygraphy not available: ambulatory PSG or polygraphy, nocturnal oximetry, Paediatric Sleep Questionaire or Sleep Clinical Record|
|Step 5||Indication for treatment of SDB5.1. AHI > 5 episodes/h irrespective of the presence of morbidity Treatment may be beneficial if AHI 1-5 episodes/h especially in the presence of morbidity from the cardiovascular system (see 2.1.); from the central nervous system (see 2.1.); enuresis; somatic growth delay or growth failure; decreased quality of life; risk factors for SDB persistence (see step 3) If at risk for SDB and PSG or polygraphy not available, treatment is considered when positive oximetry or SDB questionnaire (see 4.4.) or morbidity present 5.2. Unclear whether should treat primary snoring (evaluation annually)5.3. OSAS treatment is a priority in the presence of: major craniofacial abnormalities; neuromuscular disorders; achondroplasia; Chiari malformation; Down syndrome; mucopolysaccharidoses; Prader-Willi syndrome|
|Step 6||Stepwise treatment approach to SDB6.1. A stepwise treatment approach (from 6.2. to 6.9.) is usually implemented until complete resolution of SDB6.2. Weight loss if the child is overweight or obese6.3. Nasal corticosteroids and/or montelukast6.4. Adenotonsillectomy6.5. Unclear whether adenoidectomy or tonsillectomy alone are adequate6.6. Rapid maxillary expansion and orthodontic appliances6.7. CPAP or NPPV (for nocturnal hypoventilation)6.8. Craniofacial surgery6.9. Tracheostomy|
|Step 7||Recognition and management of persistent SDB7.1. Outcomes monitored after intervention (6 weeks - 12 months): symptom, PSG, quality of life, cardiovascular or central nervous system morbidity, enuresis, growth rate If PSG not available: polygraphy, oxymetry/captography PSG after 6 weeks after adenotonsillectomy (persistent SDB symptom or at risk of persistent OSAS preoperatively); after 12 weeks of montelukast/nasal steroids PSG after 12 months of rapid maxillary expansion (earlier if symptoms persist) and after 6 months with an oral appliance PSG for titration of CPAP, NPPV and then annually; PSG as predictor of successful decannulation with tracheostomy Airway re-evaluation by nasopharyngoscopy, drug-induced sleep endoscopy, MRI|
|Normal values or OSAS definition||AHI (episodes/h)|
|No SRDB symptoms or morbidity||3.2 AHI (2 years old) (90th percentile)2.5 AHI (2-6 years old) (90th percentile)2.1 AHI (6-18 years old) (90th percentile)|
|SRDB symptoms and/or morbidity|
|Mild OSAS||2-5 AHI|
|Moderate-severe OSAS||> 5 AHI|
|Mean (DS)||Mean (DS)||U||Z||p|
|PSQ||0.37 (0.15)||0.15 (0.07)||0.00||5.011926||0.000001|
|VMI st||106.42 (17.84)||111.24 (13.32)||61.50000||4.375023||0.000012|
|VMI motor test st||103.87 (25.39)||114.35 (17.67)||60.00000||1.679970||0.092964|
|VMI visual test st||97.78 (15.82)||107.43 (14.61)||24.00000||4.854568||0.000001|
|Spearman Rank Order CorrelationsMD pairwise deletedMarked correlations are significant at p < 0.05000|
|VMI st||VMI motor test st||VMI visual test st|
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© Società Italiana di Otorinolaringoiatria e chirurgia cervico facciale , 2020
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