International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Autism spectrum disorders in 24 children who are deaf or hard of hearing Jareen Meinzen-Derr a,b,*, Susan Wiley c, Somer Bishop d, Patricia Manning-Courtney c, Daniel I. Choo b, Donna Murray c a
Divisions of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA Pediatric Otolaryngology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA Developmental and Behavioral Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA d Department of Psychiatry, Weill-Cornell Medical College, New York, USA b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 September 2013 Received in revised form 24 October 2013 Accepted 29 October 2013 Available online 14 November 2013
Objectives: Approximately 4% of children who are deaf or hard of hearing have co-occurring autism spectrum disorder (ASD). Making an additional diagnosis of ASD in this population can be challenging, given the complexities of determining whether speech/language and social delays can be accounted for by their hearing loss, or whether these delays might be indicative of a comorbid ASD diagnosis. This exploratory study described a population of 24 children with the dual diagnosis of ASD and hearing loss. Methods: Children completed a comprehensive ASD evaluation using standardized autism diagnostic instruments (Autism Diagnostic Observation Schedule, language and psychological testing). Children with permanent hearing loss who had a developmental evaluation between 2001 and 2011 and were diagnosed with an ASD based on the results of that evaluation were included. Information on communication modality, language and cognitive abilities was collected. Results: The median age of diagnosis was 14 months (range 1–71) for hearing loss and 66.5 months (range 33–106) for ASD. Only 25% (n = 6) children were diagnosed with ASD 48 months of age and 46% by 6 years. Twelve (50%) children were diagnosed with ASD, 11 were diagnosed with pervasive developmental disorder not otherwise specified and 1 child had Asperger’s. Most (67%) had profound degree of hearing loss. Fourteen (58%) children had received a cochlear implant, while 3 children had no amplification for hearing loss. Nine (38%) of the 24 children used speech as their mode of communication (oral communicators). Conclusions: Communication delays in children who are deaf or hard of hearing are a serious matter and should not be assumed to be a direct consequence of the hearing loss. Children who received cochlear implants completed a multidisciplinary evaluation including a developmental pediatrician, which may have provided closer monitoring of speech and language progression and subsequently an earlier ASD diagnosis. Because children who are deaf or hard of hearing with ASD are challenging to evaluate, they may receive a diagnosis of ASD at older ages. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Autism ASD Deaf Hard of hearing Hearing loss
1. Introduction Autism spectrum disorders (ASD) constitute a group of developmental disorders characterized by impairments in social interaction and communication, and by restricted, repetitive, and stereotyped patterns of behavior [1]. Early identification of children with ASD is critical in their medical management and treatment [2–8], with screening endorsed as early as 18 months of
* Corresponding author at: Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue MLC 5041, Cincinnati, OH 45229-3039, USA. Tel.: +1 513 636 7789; fax: +1 513 636 7509. E-mail address: [email protected] (J. Meinzen-Derr).
age [9–11]. Although symptoms are usually apparent by 3 years of age, most children are not diagnosed with ASD until after age 4 [12]. One of the challenges in identifying children at very young ages relates to an absence of skills (such as eye contact, gestures, pointing, and pretend play) rather than the presence of noticeable features (such as spinning parts of toys, lining up toys, or repeating phrases) [13]. However, parents often do notice developmental problems as early 12 months of age, with concerns of hearing and vision most reported in that first year [14,15]. With the implementation of universal newborn hearing screening in the United States, the age of identification for hearing loss has significantly decreased [16–18]. This earlier diagnosis has made the early language acquisition trajectory for young children who are deaf or hard of hearing approach that of
J. Meinzen-Derr et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
hearing children [19]. The dual diagnosis of hearing loss and ASD is important as nearly 40% of children with an identified permanent hearing loss have an additional disability [20]. Among this group of children with different learning patterns, the prevalence estimates of ASD have been reported to be as high as 1.7% [21] to 4% [22]. Since the comorbidity of ASD and hearing loss may significantly complicate language development, early identification of both conditions is of utmost importance to mitigate the effects of the dual diagnosis. Unfortunately, because both hearing loss alone and ASD alone could contribute to communication and social delays, identification of the true dual diagnosis is challenging [23–26]. The literature on the dual diagnosis of ASD and hearing loss is severely lacking. Thus characterizing this group of children is an appropriate first step to enhance our understanding and build the foundation for improved identification and intervention for their communication needs. The objective of this descriptive or exploratory study was to describe a population of children with the dual diagnosis of permanent hearing loss and ASD in the context of the degree of hearing loss. 2. Methods 2.1. Participants This study was approved by the Institutional Review Board at Cincinnati Children’s Hospital Medical Center (CCHMC). Children with permanent hearing loss who had a developmental evaluation between 2001 and 2011 and were diagnosed with an ASD based on the results of that evaluation were included. This developmental evaluation was part of a comprehensive approach to the medical evaluation of children with hearing loss at CCHMC, Ear and Hearing Center [27]. Children with an identified permanent hearing loss (managed by a pediatric audiologist) are referred for an interdisciplinary clinical protocol by their managing pediatric otologist. Potential referrals for this process include referrals to ophthalmology, developmental pediatrics, genetics, speech pathology, and aural rehabilitation. Children with any degree (mild to profound) of permanent hearing loss were included. The severity of hearing loss was clinically classified between mild and profound using a combination of frequency specific decibel loss and the slope of the audiogram. Type of hearing loss was also collected, and included both unilateral or bilateral hearing loss, sensorineural, conductive, mixed, or auditory neuropathy. 2.2. Clinical evaluation for autism spectrum disorder As part of clinical care, children completed a comprehensive evaluation for an ASD using standardized autism assessments. The assessment battery was not consistently administered across all children due to the time-frame, during which the children were clinically seen and the variability in children’s ability to complete specific testing instruments. Evaluations included (as seen clinically appropriate) the Gilliam Autism Rating Scale (GARS) [28], Autism Diagnostic Observation Schedule (ADOS) [29], cognitive testing, test of adaptive behavior, and language testing. The GARS was administered by a psychologist and the ADOS was administered by a speech-language pathologist. Children were seen by a developmental pediatrician who has extensive experience with children who are deaf or hard of hearing. Because autism diagnostic tools (e.g., GARS and ADOS) have not been validated for use in children who are deaf or hard of hearing, both qualitative and quantitative information from the assessments were used in conjunction with DSM-IV criteria. Thus, a team of professionals representing expertise in ASD and expertise in hearing loss arrived at a consensus opinion for the diagnosis of ASD. All evaluations were used to clarify developmental patterns and were interpreted
113
with the impact of hearing loss on scoring considered. Because the scoring algorithms for the ADOS are not valid for use in children with sensory impairments such as hearing loss, the discussion regarding the scores from the ADOS or the GARS is beyond the scope of the objectives of this study and will be addressed in a future report. Severity of an autism spectrum disorder is not routinely measured; however in general, a diagnosis of autism would be viewed as more severe than a diagnosis of pervasive developmental disorder not otherwise specified. 2.3. Cognition and language assessments When possible, standardized cognitive assessments occurred at the discretion of the clinician. For the purpose of this analysis, nonverbal intelligence quotients were used. For children who did not have a standardized cognitive assessment, a developmental assessment was available using the Revised Gesell Developmental Schedules [30,31], which provides an adaptive (performance) age equivalent. A developmental quotient was calculated based on the developmental age compared to the chronological age of the child at the time of administration (developmental age/chronologic age 100). Language assessments were conducted for clinical purposes and tools were selected as deemed appropriate by the speech-language pathologist. The Preschool Language Scales-4th edition (PLS-4) [32] and the Clinical Evaluation of Language Fundamentals (CELF) [33] were most commonly used. The CELF was more often used in children who had higher language levels. Both assessments yield standard scores and age equivalents for receptive and expressive language. Because the PLS-4 has a floor of 50 as a standardized score, a language quotient was used for the analysis. The language quotient was derived by dividing the age equivalent from the PLS-4 by the chronological age of the child at the time of testing, multiplied by 100 (age equivalent/chronological age 100). Quotients of 100 represent language ages equivalent to the chronological ages. The test results reported were results from the assessment closest to the ASD diagnosis. Communication strategies used were defined as oral, sign (any sign language or sign support) and behavior (acting out for the purpose of communicating). 2.4. Statistical analysis Because this study was meant to be a descriptive study of children who had the dual diagnosis of ASD and hearing loss, the statistics reported remained descriptive in nature. Descriptive statistics included medians with ranges for continuous variables (e.g., age) and frequencies with percentages for categorical variables (e.g., etiology). We conducted simple Spearman’s rankorder correlations to understand the relationship between language scores and ages at time of either hearing loss or ASD identification. Significant differences in subject characteristics between children with severe to profound hearing loss and children with lesser degrees of hearing loss were explored using Wilcoxon Rank Sum test for continuous variables, or a Chi-square or Fisher’s Exact test for categorical variables. Point biserial correlations (rpb) were used to explore the association between severity of hearing loss and language scores. Statistical significance was set at p 0.05. Statistical analysis was conducted using SAS1 Version 9.3 software (Cary, NC). 3. Results 3.1. Study participants Thirty-four children with hearing loss were identified as having had an evaluation for suspected ASD. Of these, three children were
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J. Meinzen-Derr et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
Table 1 Summary of basic study characteristics of children who are deaf or hard of hearing with ASD.
Males Age in months hearing loss identified Age in months ASD diagnosed ASD diagnosed by 48 months Months between ASD and HL diagnosis Etiology of HL Genetic Syndrome CMV Unknown Other Severity of hearing loss Mild–moderate Moderately severe Severe–profound Unilateral ASD diagnosis Autism PDD-NOS Asperger’s No amplification use Age in months at amplificationa Received cochlear implantb Age in months at implantation Nonverbal cognitive quotientc Vineland Adaptive Behavior Scales
Total (n = 24)
SEV–PROF (n = 16)
UNI–MILD–MOD (n = 8)
18 (75%) 14 (1–71) 66.5 (33–106) 6 (25%) 41 (6–105)
11 (69%) 12 (1–39) 57.5 (33–106) 4 (25%) 39 (16–101)
7 (88%) 31.5 (1–71) 79 (39–84) 2 (25%) 41.5 (6–81)
4 6 3 6 5
(17%) (25%) (13%) (25%) (21%)
4 2 16 2
(17%) (8%) (67%) (8%)
12 11 1 3 18 14 29 76 66
(50%) (46%) (4%) (12.5%) (2–72) (58%) (14–91) (32–133) (56–88)
2 6 3 2 3
(12%) (38%) (19%) (12%) (19%)
–
9 (56%) 7 0 2 (12.5%) 17.5 (3–57) 14 (58%) 29 (14–91) 65 (32–97) 66 (56–79)
2 (25%) 0 0 4 (50%) 2 (25%)
–
3 (38%) 4 1 1 (12.5%) 34 (2–72) – – 82.5 (46–133) 81 (74–88)
Medians with ranges reported for continuous variables and frequencies with percentages for categorical variables. SEV–PROF = severe to profound hearing loss levels; UNI–MILD–MOD = unilateral, mild, moderate hearing loss levels. a For all subjects, first time fitted with a device of any type. b Three current non-users. c One child with Asperger syndrome had nonverbal cognitive quotient of 133.
evaluated and did not meet criteria for an ASD, six children did not complete evaluations, one child appeared to have concerns for an ASD but these concerns waned over time and an autism specific evaluation was not deemed appropriate. In total, twenty-four children with a dual diagnosis of hearing loss and ASD were included. Table 1 summarizes the basic characteristics of the study population. Most (75%) children were male. Nonverbal IQ was available for 16 children, a nonverbal developmental quotient was available for an additional 6 children, and one child had only a full scale IQ reported. One child was administered a cognitive test but could not complete it. Fourteen children had a completed Vineland Adaptive Behavior Scales (VABS) using a parent informant, with adaptive behavior composite scores ranging from 56 to 88 (median 66). The child with a missing IQ had a VABS adaptive score of 68. 3.2. Autism spectrum disorder Twenty-one of 24 children had received the ADOS as part of the developmental evaluation and 16 of 24 had received the GARS. All but two children who had received the GARS assessment also received an assessment using the ADOS. The Autism Diagnostic Interview-Revised [34] was administered to the parents of one additional child. Most children (n = 16) received the Module 1 on the ADOS, indicating no, or limited spontaneous speech. Of the 24 children, 12 (50%) ultimately received a clinical diagnosis of autistic disorder, 11 (46%) received a diagnosis of pervasive developmental disorder not otherwise specified (PDD-NOS), and 1 child had a diagnosis of Asperger’s syndrome. The median age of ASD diagnosis was 66.5 months (range 33–106). The child with Asperger’s syndrome was diagnosed at 80 months of age and presented due to concerns about social engagement with peers. Only 6 (25%) children received an ASD diagnosis by 48 months of age. Five of the six children diagnosed by 48 months received the diagnosis of Autism and the remaining children diagnosed by 48 months received the diagnosis of PDD-NOS.
3.3. Hearing loss characteristics The median age of identification of hearing loss was 14 months (range 1–71). Eighteen children (75%) were born prior to the implementation of UNHS, corresponding to the large age range for identification. The median duration between the identification of hearing loss and the ASD diagnosis was 41 months (range 6–101). All children were diagnosed with their hearing loss prior to the ASD diagnosis. Most of the subjects (67%, n = 16) had a degree of hearing loss that was considered severe or profound, as indicated by audiologic records (Table 1). Children diagnosed with severe to profound hearing loss had an earlier median age of identification for hearing loss compared to children with mild, moderate, or unilateral loss, though this comparison was not statistically significant (12 vs. 31.5 months, p = 0.09). The age of hearing loss diagnosis was negatively correlated with the age of ASD diagnosis (Fig. 1), though this correlation was not statistically significant (Spearman r = 0.37, p = 0.07). A quarter of children (n = 6) had a syndromic etiology for their hearing loss. Syndromes included Usher’s syndrome, CHARGE syndrome, and Waardenburg syndrome. The etiology of hearing loss was unknown in 25% (n = 6), genetic in 17% (n = 4) and due to cytomegalovirus infection in 13% (n = 3) of cases. Twenty-one percent (n = 5) children had an etiology classified as ‘‘other’’. This category included inner ear anomalies (n = 2), auditory neuropathy with no hearing loss risk factors (n = 2) and chromosomal deletion (n = 1). Children with severe to profound hearing loss had lower nonverbal cognitive (65 vs. 82.5, p = 0.14) and adaptive abilities (66 vs. 81, p = 0.015) compared to those with milder degrees of hearing loss (Table 1). 3.4. Cochlear implants Fourteen subjects had received a cochlear implant, though three children no longer used the implant. All children obtaining a
J. Meinzen-Derr et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
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American Sign Language with gestures and behavior for communication. 3.5. Language and communication
Fig. 1. Scatter plot of the age of hearing loss diagnosis in months and the age of autism spectrum disorder (ASD) diagnosis in months. Black dots represent children with severe or profound bilateral hearing loss and autism. Empty circles represent children with unilateral, mild or moderate bilateral hearing loss and autism. Black triangles represent children with severe or profound bilateral hearing loss and PDD NOS. Empty triangles represent children with unilateral, mild or moderate bilateral hearing loss and PDD NOS.
cochlear implant had experience with hearing aids prior to implantation. Among the 14 children who received a cochlear implant, two used oral communication only as their primary communication modality (Table 2). Five children had either prelinguistic communication skills or used only behavior as means for communication. The official diagnosis of ASD was made postimplant for all but 2 children (median age of ASD diagnosis 57.5 months, range 35–102). One child presented to our center for consideration of a cochlear implant after being denied this service elsewhere because of the ASD diagnosis. The other child had unilateral hearing loss and was diagnosed with PDD-NOS. This child subsequently had a sudden onset of hearing loss in the other ear and subsequently received a cochlear implant. The children who were able to achieve oral communication skills post-implant used sign language and visual strategies to support early language development and then transitioned to oral communication capabilities. One child had been successful with a total communication approach and had good oral capabilities, but problems with the implant prompted discontinuation of access to sound. Only two children with severe to profound hearing loss did not receive a cochlear implant. Both of these children used a combination of
Nine (38%) of the 24 children with a dual diagnosis of hearing loss and ASD used speech as their mode of communication (oral communicators). Five of the 9 children with oral communication had a diagnosis of PDD-NOS, 3 had a diagnosis of ASD and 1 had a diagnosis of Asperger’s. Nine children used a combination of sign language and behavior, while 6 children used only behavior for communication. Eight (33%) children, all of whom had a cochlear implant, used some form of augmentative communication (e.g., Picture Exchange Communication System). Standardized measures of language skills were available for 14 children. The CELF was administered to 6 children; 4 had the diagnosis of PDD-NOS, one child had Asperger’s and one child had ASD (Table 3). The PLS-4 was administered to 8 children, 6 had the diagnosis of ASD and two had the diagnosis of PDD-NOS. One child received the Oral and Written Language Scales [35], which provides standard scores and age equivalents. One additional child received the MacArthur-Bates Communicative Development Inventory Words and Gestures [36], which provides age equivalents for young children. Both of these children had a diagnosis of ASD. The remaining 7 children had no available standardized language testing for the following reasons: 3 children were too disengaged or difficult to complete the assessments; 3 children received language assessments from outside the institution and the qualitative reports did not indicate a score; one child was older and the language assessments could not be located; and one child used American Sign Language (ASL) only and his language levels were not assessed in ASL. This child however, did have a score on the Peabody Picture Vocabulary Test, which provides age equivalents. Four of the children with no available standardized assessments used augmentative communication. Table 3 details the receptive and expressive language scores for individuals as a function of the language assessment that was administered. For children with language assessments using the PLS-4, all but one child (7/8) had standard receptive language scores of 50 (the floor) and half (4/8) had expressive language standard scores >50. The median language quotients for these eight children were 20.5 (range 8–48) for receptive language and 26 (range 8–53) for expressive language. The median standard scores for receptive and expressive language reported on the CELF (n = 6) were 96 (range 79–103) and 94 (range 75–120) respectively. The ages of identification of hearing loss and diagnosis of ASD
Table 2 Characteristics of individual children with cochlear implants. Subject
Age CI
Age ASD diagnosis
Etiology HL
Communication
AUG COMM
ASD diagnosis
1a 2b 3 4b 5 6 7b 8 9 10 11 12 13 14a
14 18 18 19 20 23 29 30 36 37 42 60 91 ?
57 62 36 102 35 46 71 94 54 53 78 58 51 94
CMV Auditory neuropathy Auditory neuropathy CHARGE Usher’s Type I Unknown GJB2 Autosomal dominant Likely genetic syndrome EVA Waardenburg CMV Unknown Usher’s Type I
Oral/sign/behavior Sign/behavior Pre-linguistic/sign Sign/behavior Pre-linguistic Oral Sign/behavior Sign/behavior Oral/sign/behavior Behavior Sign/behavior Oral Behavior Pre-linguistic
Yes No Yes Yes Yes No No No Yes Yes Yes No No Yes
Autism PDD-NOS Autism Autism Autism Autism PDD-NOS PDD-NOS Autism Autism PDD-NOS PDD-NOS PDD-NOS PDD-NOS
CI, cochlear implant; HL, hearing loss; AUG COMM, augmentative communication; HA, hearing aid; CMV, cytomegalovirus; EVA, enlarged vestibular aqueduct; GJB2, genetic cause of deafness. a Bilateral CI; subject 14 CI surgery occurred at a different site. b No longer using CI.
J. Meinzen-Derr et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
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Table 3 Receptive and expressive language scores for children who are deaf or hard of hearing with an ASD diagnosis. Test
ASD diagnosis
Degree of HL
Receptive standard score
Receptive language quotienta
Expressive standard score
Expressive language quotienta
NVIQ
CELF CELF CELF CELF CELF CELF PLS-IV PLS-IV OWLS PLS-IV PLS-IV PLS-IV PLS-IV PLS-IV PLS-IV PPVT CDI
Asperger PDD-NOS PDD-NOS PDD-NOS PDD-NOS Autism Autism PDD-NOS Autism Autism Autism Autism Autism PDD-NOS Autism Autism Autism
MOD–SEV MILD–MOD PROF–UNI MILD–UNI MILD–MOD MILD–MOD SEV–PROF SEV–PROF SEV–PROF SEV–PROF MILD–MOD SEV–PROF SEV–PROF SEV–PROF SEV–PROF SEV–PROF SEV–PROF
103 100 99 92 83 79 55 50 40 50 50 50 50 50 50
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Autism spectrum disorders in 24 children who are deaf or hard of hearing Jareen Meinzen-Derr a,b,*, Susan Wiley c, Somer Bishop d, Patricia Manning-Courtney c, Daniel I. Choo b, Donna Murray c a
Divisions of Biostatistics and Epidemiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA Pediatric Otolaryngology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA Developmental and Behavioral Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA d Department of Psychiatry, Weill-Cornell Medical College, New York, USA b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 September 2013 Received in revised form 24 October 2013 Accepted 29 October 2013 Available online 14 November 2013
Objectives: Approximately 4% of children who are deaf or hard of hearing have co-occurring autism spectrum disorder (ASD). Making an additional diagnosis of ASD in this population can be challenging, given the complexities of determining whether speech/language and social delays can be accounted for by their hearing loss, or whether these delays might be indicative of a comorbid ASD diagnosis. This exploratory study described a population of 24 children with the dual diagnosis of ASD and hearing loss. Methods: Children completed a comprehensive ASD evaluation using standardized autism diagnostic instruments (Autism Diagnostic Observation Schedule, language and psychological testing). Children with permanent hearing loss who had a developmental evaluation between 2001 and 2011 and were diagnosed with an ASD based on the results of that evaluation were included. Information on communication modality, language and cognitive abilities was collected. Results: The median age of diagnosis was 14 months (range 1–71) for hearing loss and 66.5 months (range 33–106) for ASD. Only 25% (n = 6) children were diagnosed with ASD 48 months of age and 46% by 6 years. Twelve (50%) children were diagnosed with ASD, 11 were diagnosed with pervasive developmental disorder not otherwise specified and 1 child had Asperger’s. Most (67%) had profound degree of hearing loss. Fourteen (58%) children had received a cochlear implant, while 3 children had no amplification for hearing loss. Nine (38%) of the 24 children used speech as their mode of communication (oral communicators). Conclusions: Communication delays in children who are deaf or hard of hearing are a serious matter and should not be assumed to be a direct consequence of the hearing loss. Children who received cochlear implants completed a multidisciplinary evaluation including a developmental pediatrician, which may have provided closer monitoring of speech and language progression and subsequently an earlier ASD diagnosis. Because children who are deaf or hard of hearing with ASD are challenging to evaluate, they may receive a diagnosis of ASD at older ages. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Autism ASD Deaf Hard of hearing Hearing loss
1. Introduction Autism spectrum disorders (ASD) constitute a group of developmental disorders characterized by impairments in social interaction and communication, and by restricted, repetitive, and stereotyped patterns of behavior [1]. Early identification of children with ASD is critical in their medical management and treatment [2–8], with screening endorsed as early as 18 months of
* Corresponding author at: Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue MLC 5041, Cincinnati, OH 45229-3039, USA. Tel.: +1 513 636 7789; fax: +1 513 636 7509. E-mail address: [email protected] (J. Meinzen-Derr).
age [9–11]. Although symptoms are usually apparent by 3 years of age, most children are not diagnosed with ASD until after age 4 [12]. One of the challenges in identifying children at very young ages relates to an absence of skills (such as eye contact, gestures, pointing, and pretend play) rather than the presence of noticeable features (such as spinning parts of toys, lining up toys, or repeating phrases) [13]. However, parents often do notice developmental problems as early 12 months of age, with concerns of hearing and vision most reported in that first year [14,15]. With the implementation of universal newborn hearing screening in the United States, the age of identification for hearing loss has significantly decreased [16–18]. This earlier diagnosis has made the early language acquisition trajectory for young children who are deaf or hard of hearing approach that of
J. Meinzen-Derr et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
hearing children [19]. The dual diagnosis of hearing loss and ASD is important as nearly 40% of children with an identified permanent hearing loss have an additional disability [20]. Among this group of children with different learning patterns, the prevalence estimates of ASD have been reported to be as high as 1.7% [21] to 4% [22]. Since the comorbidity of ASD and hearing loss may significantly complicate language development, early identification of both conditions is of utmost importance to mitigate the effects of the dual diagnosis. Unfortunately, because both hearing loss alone and ASD alone could contribute to communication and social delays, identification of the true dual diagnosis is challenging [23–26]. The literature on the dual diagnosis of ASD and hearing loss is severely lacking. Thus characterizing this group of children is an appropriate first step to enhance our understanding and build the foundation for improved identification and intervention for their communication needs. The objective of this descriptive or exploratory study was to describe a population of children with the dual diagnosis of permanent hearing loss and ASD in the context of the degree of hearing loss. 2. Methods 2.1. Participants This study was approved by the Institutional Review Board at Cincinnati Children’s Hospital Medical Center (CCHMC). Children with permanent hearing loss who had a developmental evaluation between 2001 and 2011 and were diagnosed with an ASD based on the results of that evaluation were included. This developmental evaluation was part of a comprehensive approach to the medical evaluation of children with hearing loss at CCHMC, Ear and Hearing Center [27]. Children with an identified permanent hearing loss (managed by a pediatric audiologist) are referred for an interdisciplinary clinical protocol by their managing pediatric otologist. Potential referrals for this process include referrals to ophthalmology, developmental pediatrics, genetics, speech pathology, and aural rehabilitation. Children with any degree (mild to profound) of permanent hearing loss were included. The severity of hearing loss was clinically classified between mild and profound using a combination of frequency specific decibel loss and the slope of the audiogram. Type of hearing loss was also collected, and included both unilateral or bilateral hearing loss, sensorineural, conductive, mixed, or auditory neuropathy. 2.2. Clinical evaluation for autism spectrum disorder As part of clinical care, children completed a comprehensive evaluation for an ASD using standardized autism assessments. The assessment battery was not consistently administered across all children due to the time-frame, during which the children were clinically seen and the variability in children’s ability to complete specific testing instruments. Evaluations included (as seen clinically appropriate) the Gilliam Autism Rating Scale (GARS) [28], Autism Diagnostic Observation Schedule (ADOS) [29], cognitive testing, test of adaptive behavior, and language testing. The GARS was administered by a psychologist and the ADOS was administered by a speech-language pathologist. Children were seen by a developmental pediatrician who has extensive experience with children who are deaf or hard of hearing. Because autism diagnostic tools (e.g., GARS and ADOS) have not been validated for use in children who are deaf or hard of hearing, both qualitative and quantitative information from the assessments were used in conjunction with DSM-IV criteria. Thus, a team of professionals representing expertise in ASD and expertise in hearing loss arrived at a consensus opinion for the diagnosis of ASD. All evaluations were used to clarify developmental patterns and were interpreted
113
with the impact of hearing loss on scoring considered. Because the scoring algorithms for the ADOS are not valid for use in children with sensory impairments such as hearing loss, the discussion regarding the scores from the ADOS or the GARS is beyond the scope of the objectives of this study and will be addressed in a future report. Severity of an autism spectrum disorder is not routinely measured; however in general, a diagnosis of autism would be viewed as more severe than a diagnosis of pervasive developmental disorder not otherwise specified. 2.3. Cognition and language assessments When possible, standardized cognitive assessments occurred at the discretion of the clinician. For the purpose of this analysis, nonverbal intelligence quotients were used. For children who did not have a standardized cognitive assessment, a developmental assessment was available using the Revised Gesell Developmental Schedules [30,31], which provides an adaptive (performance) age equivalent. A developmental quotient was calculated based on the developmental age compared to the chronological age of the child at the time of administration (developmental age/chronologic age 100). Language assessments were conducted for clinical purposes and tools were selected as deemed appropriate by the speech-language pathologist. The Preschool Language Scales-4th edition (PLS-4) [32] and the Clinical Evaluation of Language Fundamentals (CELF) [33] were most commonly used. The CELF was more often used in children who had higher language levels. Both assessments yield standard scores and age equivalents for receptive and expressive language. Because the PLS-4 has a floor of 50 as a standardized score, a language quotient was used for the analysis. The language quotient was derived by dividing the age equivalent from the PLS-4 by the chronological age of the child at the time of testing, multiplied by 100 (age equivalent/chronological age 100). Quotients of 100 represent language ages equivalent to the chronological ages. The test results reported were results from the assessment closest to the ASD diagnosis. Communication strategies used were defined as oral, sign (any sign language or sign support) and behavior (acting out for the purpose of communicating). 2.4. Statistical analysis Because this study was meant to be a descriptive study of children who had the dual diagnosis of ASD and hearing loss, the statistics reported remained descriptive in nature. Descriptive statistics included medians with ranges for continuous variables (e.g., age) and frequencies with percentages for categorical variables (e.g., etiology). We conducted simple Spearman’s rankorder correlations to understand the relationship between language scores and ages at time of either hearing loss or ASD identification. Significant differences in subject characteristics between children with severe to profound hearing loss and children with lesser degrees of hearing loss were explored using Wilcoxon Rank Sum test for continuous variables, or a Chi-square or Fisher’s Exact test for categorical variables. Point biserial correlations (rpb) were used to explore the association between severity of hearing loss and language scores. Statistical significance was set at p 0.05. Statistical analysis was conducted using SAS1 Version 9.3 software (Cary, NC). 3. Results 3.1. Study participants Thirty-four children with hearing loss were identified as having had an evaluation for suspected ASD. Of these, three children were
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J. Meinzen-Derr et al. / International Journal of Pediatric Otorhinolaryngology 78 (2014) 112–118
Table 1 Summary of basic study characteristics of children who are deaf or hard of hearing with ASD.
Males Age in months hearing loss identified Age in months ASD diagnosed ASD diagnosed by 48 months Months between ASD and HL diagnosis Etiology of HL Genetic Syndrome CMV Unknown Other Severity of hearing loss Mild–moderate Moderately severe Severe–profound Unilateral ASD diagnosis Autism PDD-NOS Asperger’s No amplification use Age in months at amplificationa Received cochlear implantb Age in months at implantation Nonverbal cognitive quotientc Vineland Adaptive Behavior Scales
Total (n = 24)
SEV–PROF (n = 16)
UNI–MILD–MOD (n = 8)
18 (75%) 14 (1–71) 66.5 (33–106) 6 (25%) 41 (6–105)
11 (69%) 12 (1–39) 57.5 (33–106) 4 (25%) 39 (16–101)
7 (88%) 31.5 (1–71) 79 (39–84) 2 (25%) 41.5 (6–81)
4 6 3 6 5
(17%) (25%) (13%) (25%) (21%)
4 2 16 2
(17%) (8%) (67%) (8%)
12 11 1 3 18 14 29 76 66
(50%) (46%) (4%) (12.5%) (2–72) (58%) (14–91) (32–133) (56–88)
2 6 3 2 3
(12%) (38%) (19%) (12%) (19%)
–
9 (56%) 7 0 2 (12.5%) 17.5 (3–57) 14 (58%) 29 (14–91) 65 (32–97) 66 (56–79)
2 (25%) 0 0 4 (50%) 2 (25%)
–
3 (38%) 4 1 1 (12.5%) 34 (2–72) – – 82.5 (46–133) 81 (74–88)
Medians with ranges reported for continuous variables and frequencies with percentages for categorical variables. SEV–PROF = severe to profound hearing loss levels; UNI–MILD–MOD = unilateral, mild, moderate hearing loss levels. a For all subjects, first time fitted with a device of any type. b Three current non-users. c One child with Asperger syndrome had nonverbal cognitive quotient of 133.
evaluated and did not meet criteria for an ASD, six children did not complete evaluations, one child appeared to have concerns for an ASD but these concerns waned over time and an autism specific evaluation was not deemed appropriate. In total, twenty-four children with a dual diagnosis of hearing loss and ASD were included. Table 1 summarizes the basic characteristics of the study population. Most (75%) children were male. Nonverbal IQ was available for 16 children, a nonverbal developmental quotient was available for an additional 6 children, and one child had only a full scale IQ reported. One child was administered a cognitive test but could not complete it. Fourteen children had a completed Vineland Adaptive Behavior Scales (VABS) using a parent informant, with adaptive behavior composite scores ranging from 56 to 88 (median 66). The child with a missing IQ had a VABS adaptive score of 68. 3.2. Autism spectrum disorder Twenty-one of 24 children had received the ADOS as part of the developmental evaluation and 16 of 24 had received the GARS. All but two children who had received the GARS assessment also received an assessment using the ADOS. The Autism Diagnostic Interview-Revised [34] was administered to the parents of one additional child. Most children (n = 16) received the Module 1 on the ADOS, indicating no, or limited spontaneous speech. Of the 24 children, 12 (50%) ultimately received a clinical diagnosis of autistic disorder, 11 (46%) received a diagnosis of pervasive developmental disorder not otherwise specified (PDD-NOS), and 1 child had a diagnosis of Asperger’s syndrome. The median age of ASD diagnosis was 66.5 months (range 33–106). The child with Asperger’s syndrome was diagnosed at 80 months of age and presented due to concerns about social engagement with peers. Only 6 (25%) children received an ASD diagnosis by 48 months of age. Five of the six children diagnosed by 48 months received the diagnosis of Autism and the remaining children diagnosed by 48 months received the diagnosis of PDD-NOS.
3.3. Hearing loss characteristics The median age of identification of hearing loss was 14 months (range 1–71). Eighteen children (75%) were born prior to the implementation of UNHS, corresponding to the large age range for identification. The median duration between the identification of hearing loss and the ASD diagnosis was 41 months (range 6–101). All children were diagnosed with their hearing loss prior to the ASD diagnosis. Most of the subjects (67%, n = 16) had a degree of hearing loss that was considered severe or profound, as indicated by audiologic records (Table 1). Children diagnosed with severe to profound hearing loss had an earlier median age of identification for hearing loss compared to children with mild, moderate, or unilateral loss, though this comparison was not statistically significant (12 vs. 31.5 months, p = 0.09). The age of hearing loss diagnosis was negatively correlated with the age of ASD diagnosis (Fig. 1), though this correlation was not statistically significant (Spearman r = 0.37, p = 0.07). A quarter of children (n = 6) had a syndromic etiology for their hearing loss. Syndromes included Usher’s syndrome, CHARGE syndrome, and Waardenburg syndrome. The etiology of hearing loss was unknown in 25% (n = 6), genetic in 17% (n = 4) and due to cytomegalovirus infection in 13% (n = 3) of cases. Twenty-one percent (n = 5) children had an etiology classified as ‘‘other’’. This category included inner ear anomalies (n = 2), auditory neuropathy with no hearing loss risk factors (n = 2) and chromosomal deletion (n = 1). Children with severe to profound hearing loss had lower nonverbal cognitive (65 vs. 82.5, p = 0.14) and adaptive abilities (66 vs. 81, p = 0.015) compared to those with milder degrees of hearing loss (Table 1). 3.4. Cochlear implants Fourteen subjects had received a cochlear implant, though three children no longer used the implant. All children obtaining a
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American Sign Language with gestures and behavior for communication. 3.5. Language and communication
Fig. 1. Scatter plot of the age of hearing loss diagnosis in months and the age of autism spectrum disorder (ASD) diagnosis in months. Black dots represent children with severe or profound bilateral hearing loss and autism. Empty circles represent children with unilateral, mild or moderate bilateral hearing loss and autism. Black triangles represent children with severe or profound bilateral hearing loss and PDD NOS. Empty triangles represent children with unilateral, mild or moderate bilateral hearing loss and PDD NOS.
cochlear implant had experience with hearing aids prior to implantation. Among the 14 children who received a cochlear implant, two used oral communication only as their primary communication modality (Table 2). Five children had either prelinguistic communication skills or used only behavior as means for communication. The official diagnosis of ASD was made postimplant for all but 2 children (median age of ASD diagnosis 57.5 months, range 35–102). One child presented to our center for consideration of a cochlear implant after being denied this service elsewhere because of the ASD diagnosis. The other child had unilateral hearing loss and was diagnosed with PDD-NOS. This child subsequently had a sudden onset of hearing loss in the other ear and subsequently received a cochlear implant. The children who were able to achieve oral communication skills post-implant used sign language and visual strategies to support early language development and then transitioned to oral communication capabilities. One child had been successful with a total communication approach and had good oral capabilities, but problems with the implant prompted discontinuation of access to sound. Only two children with severe to profound hearing loss did not receive a cochlear implant. Both of these children used a combination of
Nine (38%) of the 24 children with a dual diagnosis of hearing loss and ASD used speech as their mode of communication (oral communicators). Five of the 9 children with oral communication had a diagnosis of PDD-NOS, 3 had a diagnosis of ASD and 1 had a diagnosis of Asperger’s. Nine children used a combination of sign language and behavior, while 6 children used only behavior for communication. Eight (33%) children, all of whom had a cochlear implant, used some form of augmentative communication (e.g., Picture Exchange Communication System). Standardized measures of language skills were available for 14 children. The CELF was administered to 6 children; 4 had the diagnosis of PDD-NOS, one child had Asperger’s and one child had ASD (Table 3). The PLS-4 was administered to 8 children, 6 had the diagnosis of ASD and two had the diagnosis of PDD-NOS. One child received the Oral and Written Language Scales [35], which provides standard scores and age equivalents. One additional child received the MacArthur-Bates Communicative Development Inventory Words and Gestures [36], which provides age equivalents for young children. Both of these children had a diagnosis of ASD. The remaining 7 children had no available standardized language testing for the following reasons: 3 children were too disengaged or difficult to complete the assessments; 3 children received language assessments from outside the institution and the qualitative reports did not indicate a score; one child was older and the language assessments could not be located; and one child used American Sign Language (ASL) only and his language levels were not assessed in ASL. This child however, did have a score on the Peabody Picture Vocabulary Test, which provides age equivalents. Four of the children with no available standardized assessments used augmentative communication. Table 3 details the receptive and expressive language scores for individuals as a function of the language assessment that was administered. For children with language assessments using the PLS-4, all but one child (7/8) had standard receptive language scores of 50 (the floor) and half (4/8) had expressive language standard scores >50. The median language quotients for these eight children were 20.5 (range 8–48) for receptive language and 26 (range 8–53) for expressive language. The median standard scores for receptive and expressive language reported on the CELF (n = 6) were 96 (range 79–103) and 94 (range 75–120) respectively. The ages of identification of hearing loss and diagnosis of ASD
Table 2 Characteristics of individual children with cochlear implants. Subject
Age CI
Age ASD diagnosis
Etiology HL
Communication
AUG COMM
ASD diagnosis
1a 2b 3 4b 5 6 7b 8 9 10 11 12 13 14a
14 18 18 19 20 23 29 30 36 37 42 60 91 ?
57 62 36 102 35 46 71 94 54 53 78 58 51 94
CMV Auditory neuropathy Auditory neuropathy CHARGE Usher’s Type I Unknown GJB2 Autosomal dominant Likely genetic syndrome EVA Waardenburg CMV Unknown Usher’s Type I
Oral/sign/behavior Sign/behavior Pre-linguistic/sign Sign/behavior Pre-linguistic Oral Sign/behavior Sign/behavior Oral/sign/behavior Behavior Sign/behavior Oral Behavior Pre-linguistic
Yes No Yes Yes Yes No No No Yes Yes Yes No No Yes
Autism PDD-NOS Autism Autism Autism Autism PDD-NOS PDD-NOS Autism Autism PDD-NOS PDD-NOS PDD-NOS PDD-NOS
CI, cochlear implant; HL, hearing loss; AUG COMM, augmentative communication; HA, hearing aid; CMV, cytomegalovirus; EVA, enlarged vestibular aqueduct; GJB2, genetic cause of deafness. a Bilateral CI; subject 14 CI surgery occurred at a different site. b No longer using CI.
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Table 3 Receptive and expressive language scores for children who are deaf or hard of hearing with an ASD diagnosis. Test
ASD diagnosis
Degree of HL
Receptive standard score
Receptive language quotienta
Expressive standard score
Expressive language quotienta
NVIQ
CELF CELF CELF CELF CELF CELF PLS-IV PLS-IV OWLS PLS-IV PLS-IV PLS-IV PLS-IV PLS-IV PLS-IV PPVT CDI
Asperger PDD-NOS PDD-NOS PDD-NOS PDD-NOS Autism Autism PDD-NOS Autism Autism Autism Autism Autism PDD-NOS Autism Autism Autism
MOD–SEV MILD–MOD PROF–UNI MILD–UNI MILD–MOD MILD–MOD SEV–PROF SEV–PROF SEV–PROF SEV–PROF MILD–MOD SEV–PROF SEV–PROF SEV–PROF SEV–PROF SEV–PROF SEV–PROF
103 100 99 92 83 79 55 50 40 50 50 50 50 50 50
