|Year : 2012 | Volume
| Issue : 2 | Page : 117-126
Communication skills, sensory integration functions, and auditory brainstem response ( findings in a group of Egyptian children with autistic features)
Kamal L. Samy1, Dalia M. Osman2, Mona H. Selim3, Reham A. Mohamed4
1 Department of ENT, Kasr El-Aini Hospital, Cairo University, Cairo, Egypt
2 Phoniatric Unit, Kasr El-Aini Hospital, Cairo University, Cairo, Egypt
3 Audiology Unit, Kasr El-Aini Hospital, Cairo University, Cairo, Egypt
4 Phoniatric Unit, Hearing and Speech Institute, Cairo, Egypt
|Date of Submission||30-Nov-2011|
|Date of Acceptance||22-Dec-2011|
|Date of Web Publication||17-Jun-2014|
Dalia M. Osman
Phoniatric Unit, Kasr El-Aini Hospital, Cairo University, 39 el Meqyas Street, El Roda, 11451 Cairo
Source of Support: None, Conflict of Interest: None
The aim of this work was to study the correlation between communication skills, sensory integration dysfunction, and auditory brainstem response (ABR) findings in a group of children with autistic features in order to gain a better understanding of some of the communication deficits commonly encountered in these children.
The study was conducted on 25 Egyptian children with autistic features and 25 age-matched and sex-matched typically developing children. All the children’s age ranged from 4 to 9 years. Each child was subjected to the following: history taking, communication assessment, sensory integration dysfunction questionnaire, psychometric evaluation, the Childhood Autism Rating Scale, basic audiological evaluation, and assessment of ABR (20 and 70 c/s). The results obtained from the two groups were then compared. In addition, correlation studies of all the results obtained were carried out.
There were significant differences between the two groups under study in terms of communication skills, sensory integration dysfunction, and ABR waves III, III–V, V (20 c/s), I–V, and Vº (70 c/s). There was a significant negative correlation between ABR waves I and III and behavior, intentionality, capacity of symbols, reasoning, and total communication scores. There was a significant negative correlation between ABR waves III and V and forms, behaviors, intentionality, capacity of symbols, imitation, and total communication scores. There was a significant positive correlation between auditory sensory dysfunction scores and ABR wave V and waves III–V. There was a significant negative correlation between sensory integration dysfunction and intelligent quotient and communication skills. There was a significant positive correlation between sensory integration dysfunction scores and the severity of autism.
Conclusion and recommendations
Some of the communication difficulties shown by children with autism might be related to sensory integration dysfunction. Auditory defects in autism may involve lower levels of neural transmission. Reducing sensory integration deficits can aid in minimizing some of the features commonly encountered in children with autism. This would also aid in further development of their sociocommunication skills. ABR, as an objective tool, may be used as a prognostic indicator.
Keywords: auditory brainstem response, autism, communication skills, sensory integration dysfunction
|How to cite this article:|
Samy KL, Osman DM, Selim MH, Mohamed RA. Communication skills, sensory integration functions, and auditory brainstem response ( findings in a group of Egyptian children with autistic features). Egypt J Otolaryngol 2012;28:117-26
|How to cite this URL:|
Samy KL, Osman DM, Selim MH, Mohamed RA. Communication skills, sensory integration functions, and auditory brainstem response ( findings in a group of Egyptian children with autistic features). Egypt J Otolaryngol [serial online] 2012 [cited 2020 Aug 10];28:117-26. Available from: http://www.ejo.eg.net/text.asp?2012/28/2/117/134546
| Introduction|| |
According to the Diagnostic and Statistical Manual of Mental Disorders, 4th ed. (DSM-IV) 1, autism is characterized by qualitative impairments in social interaction (at least two features); marked impairment in the use of multiple nonverbal behaviors, failure to develop peer relationships, lack of spontaneous seeking to share enjoyment with other people, and lack of social or emotional reciprocity, in addition to qualitative impairments in communication as manifested by at least one of the following: delay in the development of spoken language, marked impairment in the ability to initiate or sustain a conversation with others, stereotyped and repetitive use of language, lack of varied, spontaneous make-believe play, and restricted repetitive stereotyped patterns of behavior, interests, and activities with an onset before 3 years of age.
There is enormous heterogeneity in terms of communication skills among autistic children 2. Nevertheless, children with autism usually show common abnormalities for example, immediate and delayed/deferred echolalia 3. They usually have difficulties with pronouns and may produce a lot of jargon and/or neologism 4,5. Assessment of communication skills in children having difficulties should include evaluating the child's ability to request his needs as well as his vocal and motor imitation skills 6.
Among the features commonly encountered in autism is sensory integration dysfunction 7,8 to the extent that some authors believe that sensory perceptual assessment is vital in any autism communication profile 9. Sensory integration is the ability to take information through the senses, to place it together with prior information, memories, and knowledge stored in the brain, and to make a meaningful response 10. In children with sensory integration dysfunction, some parts of the brain do not receive the sensory information they need to serve their function 11.
Sensory integration disorders can be classified into modulation and discrimination disorders. Modulation disorders can take the form of under-reaction, over-reaction, or fluctuation between the two extremes. In contrast, discrimination disorders can be defined as the ability to differentiate touch, force, and information about body position in space 12.
There is increased evidence that in some individuals with autism, lack of adequate language and communication skills may be related to issues other than social-cognitive abilities 13. Among these factors is abnormal auditory pathway functioning. This can act as a major contributing factor to inhibition of typical language development in children with autism. Abnormalities in the auditory pathway can occur at different levels of the auditory pathway, from the cochlea 14 to the cortex 15, leading to negative effects on communicative competence in autism.
Some autistic persons have been reported to have brainstem dysfunction 16. Auditory-evoked potentials refer to the brain responses induced by the presentation of auditory stimuli. They are time-linked to certain specified events 17. They consist of a sequence of positive and negative deflections or peaks that are named according to their polarity (positive/negative) and latency (timing in relation to stimulus onset), their serial order, or cognitive meaning 18. The most commonly used auditory-evoked potential methodology is the auditory brainstem response (ABR); it can provide an objective estimate of the auditory brainstem pathway particularly in very young and/or uncooperative participants 19.
An ABR recording consists of five to seven waves. The most commonly studied ABR responses are waves I, III, and V. Wave I is generated in the first afferent auditory neuron, in the distal part of the cochlear nerve. Wave III is generated in the ipsilateral cochlear nuclei and wave V in the lateral lemniscus, but with contributions from multiple anatomical structures 20.
Autism encompasses many features including language difficulties, social difficulties, and repetitive movements 21. There is growing evidence that sensory integration and the auditory brainstem operate differently in autism. These abnormalities, along with reduced mental skills and the severity of the autism itself, can negatively influence communication skills.
The aim of this work was to study the correlation between communication skills, sensory integration dysfunction, and ABR findings in a group of children with autistic features in order to gain a better understanding of some of the communication deficits commonly encountered in these children.
| Patients and methods|| |
The tested participants included 50 Egyptian children in the age group of 4–9 years. There were 25 were healthy typically developing children free from any history of language difficulties; these were included in the Control group and the other 25 were children previously diagnosed with autistic features according to the DSM-IV-TR criteria 1.
These were included in the Autism group. Children in the Autism group were selected from the Phoniatric outpatient clinic of Kasr El-Aini Hospital and the Hearing and Speech Institute. This research was conducted between October 2007 and December 2008 and the study protocol was approved by the Otolaryngology Department Council of Cairo University. A written consent to participate in this research was obtained from the children’s parents before commencement of the study. Information on age, developmental history, and medical reports were obtained through an interview that had been carried out with the parents before the start of the study. Thereafter, each child under study was subjected to the following:
- Psychometric evaluation: The intelligent quotient (IQ) of each child was calculated using the Stanford Binet Intelligence Scale 22. The distribution of children with autism according to IQ was as follows: 50% mild mental retardation, 40% borderline IQ, 5% below average IQ, and 5% average IQ.
- The Childhood Autism Rating Scale (CARS) 23: CARS was used to diagnose and rate the severity of autism. The distribution of autistic patients according to CARS was as follows: 50% had mild autistic features and 50% had moderate autistic features.
- Assessment of communication skills (designed in the current study): Communication assessment included evaluation of the child’s signals, forms, requesting abilities, behavior, intentionality, readability of communication behaviors, capacity of symbols and reasoning, vocal and motor imitation, and reasoning [Appendix 1].
- Sensory Integration Dysfunction Questionnaire (designed in the current study): The sensory integration dysfunction questionnaire included questions addressing dysfunctions in auditory, visual, olfactory, vestibular, and tactile sensations [Appendix 2].
- Basic audiological assessment: Play audiometry using warble tones was performed at frequencies of 0.5, 1, 2, and 4 kHz using a dual-channel clinical audiometer (AC 40; Interacoustics, Denmark) with TDH 39 earphones. Immittancemetry including tympanometry and acoustic reflex threshold measurement (ipsilateral and contralateral at frequencies 0.5, 1, 2 and 4 kHz) was also performed using an Interacoustic AZ-26 middle ear analyzer (Interacoustics) calibrated according to the ISO standards, Assens, Denmark. Immittancemetry was performed to exclude children with middle ear pathologies.
- ABR: Auditory-evoked potentials in the form of an ABR using a filter setting of 100–1500 Hz, a time window of 10 ms, a stimulus in the form of a rarefaction click with a duration of 100 ms, a sweep count of 2000, and an intensity of 100 dB nHL were used. Electrodes were mounted with the recording electrode on the forehead, the reference electrode on the ipsilateral mastoid, and the ground electrode on the contralateral mastoid. The total test duration was around 15 min. The following measures were obtained: the absolute latencies of waves I, III, and V at 20 c/s, relative interpeak latencies of I–III, III–V, and I–V at 20 c/s, absolute latency of wave V at 70 c/s, amplitude of wave V at 20 and 70 c/s, and latency shift and wave V at 70 versus 20 c/s. The ‘Vivosonic digital processing technique’ was used. It is a wireless system for electrophysiological assessment and hearing screening whose main platform is scalable and hence did not require sedation of patients. ABR was carried out using the Vivosonic brain-evoked response audiometer model V-500 (BDT version 4; Vivosonic Inc., Toronto, Canada) with ER-3A insert earphones.
An IBM-compatible personal computer was used to store and analyze the data. Calculations were carried out using statistical software package for the social sciences (SPSS, version 10; Armonk, New York, USA). Data were tabulated and statistically analyzed to evaluate differences between the groups under study in terms of various parameters. Correlations were performed between the studied parameters. Statistical analysis included the arithmetic mean, SD, Hypothesis Student’s (t) test, and Pearson’s correlation coefficient. The correlation between variables was determined using the Pearson correlation test. This test determines whether the changes in one variable are accompanied by a corresponding change in the other variable. A significant correlation may be positive, indicating that the change in the two variables is in the same direction, or negative, indicating that the change in the two variables is in the opposite direction. Results were considered nonsignificant if P value was greater than 0.05 and significant if P value was less than 0.05.
| Results|| |
Play audiometry showed within-normal warble tone thresholds at all tested frequencies in autistic children and controls, with no significant differences (P>0.05).
Significant differences were found between the two groups under study in terms of communication skills [Table 1] and sensory integration dysfunction [Table 2], and ABR wave III, waves III–V, wave V, waves I–V, and wave Vº. However, nonsignificant differences were found in terms of wave I, waves I–III, V amplitude, Vº amplitude, and V–Vº latency differences [Table 3].
|Table 1: Comparison of the Autism group and the Control group in the scores obtained for communication skills|
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|Table 2: Comparison of the sensory integration dysfunction score obtained by the Autism group and the Control group|
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|Table 3: Comparison between the auditory brainstem response latency (ms) and amplitude (µV) obtained by the Autism group and the Control group|
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A significant negative correlation was found between waves I and III and each of behavior, intentionality, reasoning, capacity of symbols, and total communication scores and between waves III and V and each of communication forms, behaviors, intentionality, capacity of symbols, imitation, and total communication scores [Table 4] and [Table 5]. However, a significant positive correlation was found between auditory dysfunction scores and each of wave V and waves III–V [Table 6] and [Table 7].
|Table 4: Correlation coefficient between auditory brainstem response and age, intelligent quotient, and Childhood Autism Rating Scale|
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|Table 5: Correlation coefficient between auditory brainstem response findings (20 c/s) and communication scores|
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|Table 6: Correlation coefficient between auditory brainstem response findings (70 c/s) and communication scores|
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|Table 7: Correlation coefficient between auditory brainstem response latencies and amplitudes (20 c/s) and sensory integration dysfunction scores|
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A significant negative correlation was found between the total sensory integration dysfunction scores and IQ and communication skills. However, a significant positive correlation was found between the total sensory integration dysfunction scores and CARS scores [Table 8] and [Table 9].
|Table 8: Correlation coefficient between auditory brainstem response latencies and amplitudes (70 c/s) and sensory integration dysfunction scores|
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|Table 9: Correlation coefficient between sensory integration dysfunction scores, intelligent quotient, Childhood Autism Rating Scale, and communication skills scores|
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| Discussion|| |
Impairment in communication is one of the core symptoms in autism 24. Communication is highly dependent on the input that is received from the surrounding environment and the way a person responds is highly dependent on what is perceived. Children with autism usually do not respond in a way that is expected from them. They have different sense, perception, abilities, and thinking systems (SPATS), which, in turn, negatively influence their learning, behavior, and language development 9.
Receptors of different senses are located in the peripheral nervous system. However, it is believed that the sensory integration problems stem from neurological dysfunction in the central nervous system. This explains how sensory integration techniques can facilitate attention, awareness, and reduce overall arousal 12. The current study found significant differences between the Control group and the Autism group in terms of auditory, visual, olfactory as well as vestibular dysfunction [Table 2]. Some of the children with autism showed features suggestive of hypersensitivity, whereas others showed features suggestive of hyposensitivity. The former was manifested in the form of unjustified defensiveness or hyper-responsiveness (over-reaction) to sensory information that most individuals would consider harmless, for example, covering the ears on hearing a loud noise or extreme intolerance to certain phone rings. Previous researches have also reported similar findings; autistic children were found to frequently cover their ears in the absence of any disturbing sound, which, in turn, reflected their hypersensitivity 10. This might be secondary to either auditory overload , that is, there are too many stimuli entering one or more of the child’s auditory system, or it might be due to a highly aroused nervous system that cannot differentiate between threatening and non-threatening inputs 25.
For other children, the dysfunction seemed to be more toward the hyposensitive side; children seemed to frequently seek sounds, for example, enjoy listening to the cracking of a candy wrap close to their ears. Other parents reported that their autistic children frequently failed to respond to their names despite their ability to immediately respond when their favorite song is played two rooms away, what is commonly referred to as selective hearing.
Some autistic children were reported to be very irritable, difficult to soothe, emotionally labile, and hypersensitive to touch, whereas others were reported to frequently seek tactile sensations, biting others, inappropriately hugging them, or touching their cheeks. Others showed features suggestive of a hyposensitive olfactory system; they tended to use excessive smell to explore odors of various objects.
However, others seemed hypersensitive, reacting negatively to smell, vestibular, or tactile stimulation. Such sensory problems may be the underlying reason for behaviors such as rocking, spinning, and hand flapping. Some children were reported to flicker objects in front of their eyes or enjoyed being in dark places, reflecting hypersensitive or hyposensitive vision, respectively.
From the previously mentioned observations, it could be deduced that children with autism usually show features suggestive of sensory integration dysfunction. However, they can differ considerably in their sensory dysfunction patterns. Treatment of sensory disorders can help in reducing self-stimulatory behavior in such children. Yet, the intervention program has to be tailored according to the sensory needs of each child as what is appropriate for one child may be useless or even harmful to another.
The significant negative correlation obtained between sensory integration dysfunction and communication skills [Table 9] implies a relationship between sensory dysfunction and communication difficulties; the more the sensory dysfunction, the worse the communication difficulties are expected to be. This might be due to the attention problems and regulatory disorders that usually occur secondary to sensory integration dysfunction, hindering typical communication development in children with autism; communication development requires considerable attention from the child’s side and the ability to attend to a task depends on the ability to screen out or inhibit unnecessary information, background noise, or visual distracters. Children with sensory integration dysfunction face huge difficulties with responding to or registering sensory information without this screening ability and are considered to be easily distractible, hyperactive, or uninhibited. These children constantly seek orienting sensory input that others ignore. Furthermore, children with sensory integration disorders often have regulatory disorders. This can be manifested in the form of difficulty establishing appropriate sleep and eating patterns or over-reaction to ordinary environmental stimuli. Insufficient sleep along with easy distractibility can, in turn, aid in reducing the benefit a child with autism can receive from the surrounding environment.
Sensory integration occurs in the nervous system and is generally believed to take place in the midbrain and brainstem levels. It requires complex interactions between coordination, attention, arousal system, autonomic functions, emotions, memory, as well as cognition 26. This might partially explain the significant positive correlation that was found between the auditory sensory dysfunction score and each of ABR wave V and ABR waves III−V [Table 7].
A significant negative correlation was found between IQ and sensory integration dysfunction [Table 9]. This implies that the lower the IQ, the more the features of sensory integration dysfunction, a fact that should be taken into consideration while establishing a differential diagnosis between mental deficiency and autism as some of the children with a low IQ may exhibit some of the sensory features commonly encountered in children with autism.
However, a positive correlation was found between sensory integration dysfunction scores and CARS scores [Table 9], that is, the greater the severity of autism, the more frequent the sensory integration dysfunction features. Similar findings were obtained in previous studies that revealed a significant correlation between sensory integration disorders and autistic features 24,27.
These findings suggest that the more severe the autistic features, the more the sensory integration dysfunctions. Children with sensory integration dysfunctions are often blamed for their misbehavior. Improving sensory processing in these children can help in improving their social interactions, which would, in turn, help in further developing their sociocommunication skills.
Some auditory processing difficulties have been reported in children with autism. Processing of auditory information at the cortical level was found to be affected in children with autism. However, abnormalities found at the subcortical level were reported to be inconsistent 28.
Some authors believe that an abnormal auditory pathway can act as a major contributing factor to autistic features to the extent that some researchers recommend including auditory abnormalities among the diagnostic criteria of the disorder 29. Previous studies on auditory perception of linguistic and social auditory stimuli among individuals with autism have revealed impaired perception. Such findings may correlate with impaired language skills and social isolation observed among individuals with autism. However, studies of auditory perception of pitch and music among individuals with autism have shown enhanced perception versus normal controls. These findings may correlate with the restricted, highly focused behaviors observed in autism 30. These findings suggest impaired global processing and enhanced local processing, which, in turn, could prove useful in understanding the apparent auditory integration dysfunction features that have been reported in autistic children.
On comparing the absolute and interpeak latencies and amplitudes of ABR waves obtained by children with autism with those obtained by controls using a rate of 20 c/s, a statistically significant shift in wave III and interpeak latency (IPL) III–V in addition to a statistically significant shift in wave V and IPL I–V were found [Table 3]. On using the system with a high rate (70 c/s), a delay in the Autism group compared with the control group was evident in the latency of wave Vº. Hence, it can be concluded that autism mainly affects the latency of the ABR waves and not the amplitude. A slowing in nerve conduction in the auditory system, as expressed by the prolongation of ABR absolute and interpeak latencies, can be deduced. This finding supports the brainstem hypothesis: that there is a dysfunction or immaturity of the lower part of the central auditory nervous system in autism 20.
These findings are consistent with the view that there is electrophysiological evidence of auditory defects in autism that may involve lower levels of neural transmission at a very early stage, within several milliseconds after stimulus presentation, as manifested by the abnormalities in the brainstem. The results obtained showed a delay in brainstem propagation, mainly involving the later waves. This delay becomes especially apparent on stressing the system using a high repetition rate. However, it seems that the effect of autism was, generally, on ABR wave latencies and not on amplitudes. There are different explanatory models for the observed combination of ABR abnormalities. One possible explanation is an abnormality in brainstem anatomy. A genetic defect affecting the HOXA 1 gene on chromosome 7 can explain this abnormality. Moreover, hyperserotonemia is the best replicated biochemical abnormality in autistic patients. Serotonine has been found to stop axon elongation for synapse formation of particular neurons 31.
The brainstem and midbrain are early centers in the processing pathway for sensory integration. These brain regions are involved in processes including coordination, attention, arousal, and automatic function, which are part of the sensory integration function 31. In the present study, a significant positive correlation was found between wave V latency and IPL III–V and auditory dysfunction only on using a low rate of 20 c/s [Table 7]. According to these findings, it can be suggested that brainstem dysfunction can be a contributing factor to the auditory sensory integration dysfunction present in autism.
This study showed a nonsignificant correlation between ABR latencies and amplitudes and CARS scores in the Autism group [Table 4]. On the basis of these results, it could be assumed that no deficit specific to the auditory function in autistic children is located at the level of the middle ear or the cochlea. This is in accordance with the emerging evidence that suggests that atypical behaviors in response to sound represent a perceptual disorder mediated at higher not lower levels of the auditory system 32.
The nonsignificant correlation between ABR results, age, and IQ [Table 4] suggests that autistic features, rather than age, or lower mentality, correlated with brainstem transmission time. The autistic characteristics may be related to dysfunction of the brainstem that affects the processing of sensory input through the auditory pathway. The brainstem lesion may be part of a generalized process of neurological damage that accounts for the deviant language, cognitive, and social development in the spectrum of autistic disorder 20.
As ABR does not change with age in autistic children, whereas it changes in normal children, there might be a maturational defect in myelination within the brainstem in autism. This defect may have a wide distribution throughout the central nervous system in autism 20.
There was a significant correlation between the ABR IPL of waves I–III and III–V (nerve conduction time in the brainstem) and verbal and nonverbal communication [Table 5]. These results imply that brainstem lesions, especially an IPL shift of I–III and III–V, have an impact on communication skills. This is in agreement with other investigators who reported that brainstem lesions may account for the deviant language present in autism 33.
No significant correlation was found between ABR results, IQ, and CARS [Table 4]. However, a significant negative correlation was found between ABR IPLs and most of the studies on communication skills [Table 5] and a significant positive correlation was found between ABR wave latencies and auditory sensory integration dysfunction [Table 7]. This implies that IPL prolongation, as a marker of the neuropathologic process, would not be necessary to develop autism and would not consequently be the sole liability factor for autism. This agrees with the findings previously obtained by other researchers who found that only IPL prolongation is insufficient in the development of autism unless it interacts with other genetic, environmental, and neurological factors 34.
These findings suggest the existence of brainstem abnormalities in children with autism. This is in agreement with the findings previously obtained by other researchers 35, who found significant dysmorphology in the superior olivary complex, a collection of auditory brainstem nuclei, in the autistic brain 35,36.
| Conclusion|| |
Some of the communication difficulties exhibited by children with autism might be related to sensory integration dysfunction. Autistic children presented with a normal hearing sensitivity, as evidenced by play audiometry. ABR results showed a delay in brainstem propagation, mainly involving the later waves. This delay was also apparent on stressing the system, using a high repetition rate, indicating a possible impaired synaptic function. Effect of autism is mainly on ABR wave latencies and not on amplitudes. The brainstem dysfunction present in autistic children affects communication and sensory integration functions, and hence affects the process of coordination, attention, and arousal, which are part of the sensory integration function.
| Recommendations|| |
Reducing sensory integration deficits can aid in minimizing some of the features commonly encountered in children with autism. This would also help in further development of their sociocommunication skills. ABR, as an objective tool, may be used as a prognostic indicator to monitor the progress achieved by therapy in children with autistic features.
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]