- Email: [email protected]
Children with cochlear implants: Cognitive skills, adaptive behaviors, social and emotional skills
International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Children with cochlear implants: Cognitive skills, adaptive behaviors, social and emotional skills Andrea De Giacomo a, Francesco Craig a, Alessandra D’Elia b, Francesca Giagnotti b, Emilia Matera a, Nicola Quaranta b,* a
Child Neuropsychiatry Unit, Department of Basic Medical Science, Neuroscience and Sense Organs, Hospital Polyclinic of Bari, University of ‘‘Aldo Moro’’ Bari, Piazza Giulio Cesare 1, Italy Otolaryngology Unit, Department of Basic Medical Science, Neuroscience and Sensory Organs, University of Bari ‘‘A. Moro’’, Italy
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 July 2013 Received in revised form 12 September 2013 Accepted 15 September 2013 Available online 9 October 2013
Objective: The aim of this study is to examine cognitive skills, adaptive behavior, social and emotional skills in deaf children with cochlear implant (CI) compared to normal hearing children. Methods: The study included twenty children affected by profound hearing loss implanted with a CI compared to 20 healthy children matched to chronological age and gender. Results: Results of this study indicated that 55% of children with CI showed a score in the normal range of nonverbal intelligence (IQ > 84), 40% in the borderline range (71 < IQ < 84) and 5% were in mild range (50 < IQ < 70). No significant differences were found after comparison with normal hearing children. Children with CI reported more abnormalities in emotional symptoms (p = .018) and peer problems (p = .037) than children with normal hearing. Age of CI was negatively correlated with IQ (p = .002), positively correlated with emotional symptoms (p = .04) and with peer problems (p = .02). Conclusions: CI has a positive effect on the lives of deaf children, especially if it is implanted in much earlier ages. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Cochlear implant Deaf children Nonverbal intelligence Adaptive behavior Social and emotional skills
1. Introduction The auditory function has a crucial role in the main stages of child development. The importance of early intervention for children with hearing loss has been demonstrated persuasively in areas including speech perception, production and spoken language, cognitive skills, adaptive behavior, social and emotional outcomes that may drastically limit the quality of life of deaf people [1]. The Joint Committee on Infant Hearing [2] has advocated hearing screening for all newborns, with the goal of confirming hearing loss before 3 months of age and beginning hearing rehabilitation before 6 months of age. Several issues have a bearing on decisions about the beneficial effect of very early CI for the development of age-appropriate spoken language in infants and children. Previous studies reported that neural organization and/or structure related to speech perception/production were affected by the length of auditory deprivation, but the extent and the potential reversibility of changes in the neural architecture are
* Corresponding author at: Otolaryngology Unit, Department of Neuroscience and Sensory Organs, Hospital Polyclinic of Bari, University of ‘‘Aldo Moro’’ Bari, Piazza Giulio Cesare 1, Italy. Tel.: +39 080 5478850; fax: +39 080 5478752. E-mail address: [email protected] (N. Quaranta). 0165-5876/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.09.015
presently not completely known [3]. Children with CI showed distinctive developmental patterns in basic academic skills such as language and reading compared both to children with normal hearing and to children with severe deafness, who have not been implanted [4,5]. These studies provided evidence that by decreasing the age at implantation better outcomes could be obtained in terms of spoken language and speech perception. Thus implantation should ideally occur not only early enough for normal language progress to be achieved, but also before delays could be established. The implicit corollary from all these observations is that cochlear implants (CIs) should be fitted in infants/children as soon as a correct diagnosis of severe to profound hearing loss has been obtained. Indeed the significant advantage of early intervention in children with significant hearing loss was demonstrated in literature. Whereas a great deal of research has been devoted to understanding hearing and spoken language development in deaf children with CIs, very little is currently known about general cognitive development after CI. Studies of some aspects of cognitive capabilities comparing children with normal hearing and children with hearing impairment revealed that the latter experience difficulties at the cognitive level [6–8]. Non-verbal intelligence is meant as fluid intelligence, considered the truest measure of a person’s innate ability. It has been
1976
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
previously suggested that a lack of experience with sound during early development may have an impact on cognitive functions [6], but data in literature is not unique in defining a profile of nonverbal intelligence in children with CI probably due to the study population and survey method. Some authors have, in fact, suggested that children with CI performed at a lower level than hearing children on tasks such as serial memory, phonological processing, short-term/working memory and inhibition-concentration [9–12]. Other researchers have instead reported that deaf individuals may show good performances in nonverbal tasks as spatial working memory and visual attention [13,14]. Less is known about the effects of early intervention for children with hearing loss on adaptive behaviors, social and emotional outcomes. In deaf children previous studies have shown a relation between cognitive abilities and behavioral adaptability [15] and between behavioral adaptability and better communication and family support [16]. Recently, Oghalai et al. [17] reported that children with CI had a normal developmental rate of adaptive behavior after CI. In addition, earliest CI was associated with lowest levels of loneliness during middle and late childhood [18]. Punch conducted parent/teacher surveys containing subscale surveys of social skills and participation, which revealed negative qualitative parent data and negative qualitative and quantitative teacher data, indicating suboptimal social outcomes in children with CI [19]. Social participation and emotional wellbeing became more problematic for some children as they reached adolescence and appeared to struggle with issues around being deaf, feeling selfconscious about the CI external equipment they needed to wear and fitting in with hearing peers. Loy et al. [20] examined if deaf children with CI showed similar psychosocial issues as typical hearing peers. They detected that for profoundly deaf children who regularly use a CI, feelings about life were no better or worse than their hearing peers; while individual areas of difficulty may be different the aggregate scores remained the same. In order to clarify the role of CI in deaf individuals, the main objective of this study was to evaluate the cognitive skills, adaptive behavior, social and emotional skills after cochlear implantation in deaf children and to explore the complex association between all these aspects with the impact of CI implantation age. 2. Methods 2.1. Subjects The study included twenty children affected by profound hearing loss implanted with a unilateral CI at the Otolaryngology Unit of the University of Bari, Italy. Inclusion criteria for the study were: bilateral pre-verbal profound sensorineural hearing loss, appropriate amplification before unilateral CI, oral habilitation before and after cochlear implantation, open set speech perception after CI. Exclusion criteria included history of seizure disorder, learning disability, progressive neurological problems, traumatic brain injury, additional significant disabilities (e.g., blindness, autism), not used spoken Italian as their primary mode of communication or any other serious medical condition. For the evaluation of cognitive and behavioral functions the children were assessed at the Child and Adolescent Neuropsychiatric Unit of the Neurologic and Psychiatric Department of University of Bari, ‘‘Aldo Moro’’, while speech perception was evaluated with age appropriate tests translated and validated in Italian language [21] at the Otolaryngology Department of the same University. The control group consisted of 20 healthy children matched to chronological age and gender with normal hearing. These children were recruited from regular primary and secondary schools and
were fully informed about the experiment. The same exclusion criteria used in the CI group were used to select the control group Parental informed consent was obtained for all participants and the study was approved by the local ethical committee of the ‘‘Azienda Ospedaliero-Universitaria Consorziale Policlinico di Bari’’ (St. 3845; Prot.264/CE). 2.2. Assessment The first step of the evaluation included a collection of clinical and socio-demographic data. Data included parents’ marital status, occupation and years of education, as well as age at identification and status of hearing loss, age of enrollment in the intervention program, developmental milestones, medical and psychological history on paternal and maternal sides, and the child’s medical and psychological history. The second study step involved the administration of standardized instruments to assess cognitive skills, adaptive behavior, social and emotional skills, speech perception, production and spoken language. The Leiter International Performance Scale-Revised [22] is a standardized, individually administered, nonverbal test designed to assess cognitive functions in children and adolescents ages 2–0 to 20–11 years. The Leiter-R includes the Visualization and Reasoning Battery with 10 subtests of nonverbal intellectual ability related to visualization, reasoning and spatial ability; and the Attention and Memory Battery with 10 subtests of nonverbal attention and memory function. The Fluid Reasoning composite is comprised of subtests that show evidence of providing a unique fluid measure of seriation, reasoning and pattern generation. The Full IQ score represents a measure of general nonverbal intelligence. The IQ is them sum of the subtests that compose the IQ estimate, and the subtests represented vary depending on the age of the student. The IQ score includes several aspects of cognition and it is comprised of highly correlated subtests to obtain a single measure of intellectual ability. The Vineland Adaptive Behavior Scale (VABS) [23] assesses personal and social skills, with norms up to 18 years old. Two interview editions, one with 577 items, the other with 297, gather information through semi-structured interviews; both include a Motor Skills Domain for children less than 6 years old and an optional Maladaptive Behavior Domain for children age 5 through 18 is optional. The VABS is a measure of personal and social skills needed for everyday life. Assessed domains include Communication, Daily Living, Motor Skills, and Socialization. Raw scores are converted to age-equivalent standard scores for each domain and for the composite adaptive behavior score. The Strengths and Difficulties Questionnaire (SDQ) [24] form P (Parents), is a parent-reported instrument designed to provide information on children’s behaviors and relationships. The SDQ contains 25 items divided equally among five scales such that subscale scores are generated for Emotional Symptoms (especially aspects related to anxiety and depression), Conduct Problems, Hyperactivity-Inattention (which also contains items on attention problems), Peer Problems (e.g. peer rejection), and Prosocial Behavior. The scores are added together to produce a total overall stress score. The ranges indicating abnormalities are 7–10 for hyperactivity, 4–10 for conduct problems, 5–10 for emotional difficulties, 0–4 for prosocial behaviors and 4–10 for peers relationship. SDQ translated into over sixty languages, including Italian by A. De Giacomo et al., available online at www.sdqinfo.com. 2.3. Data analysis All demographic and clinical variables were subjected to statistical analysis. Descriptive analysis was conducted for
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
1977
Table 1 Results: Leiter-R, VABS and SDQ in IC and control group.
LEITER-R VABS
SDQ
IQ Communication a.e Daily Living skills a.e Socialization a.e Total Maladaptive Overall stress Emotional symptoms Behavior Problems Hyperactivity Peer problems Prosocial
IC group N = 20
IC control N = 20
89.05 13.682 103.01 49.18 99.55 51.6 105.99 56.56 644.9 190.47 35% 35% 20% 0% 30 20
90.10 21.856 107.35 32.03 97.95 41.35 106.65 43.8 681.1 124.36 5% 5% 10% 5% 5 15
Z
p .799 .81 .298 .135 .203 0.127 5.625 2.055 3.02 4.329 .173
.425 .935 .766 .892 .839 .892 .018* .151 .220 .037* .677
Leiter International performance scale-Revised (Leiter-R); Vineland Adaptive Behavior Scale (VABS); Strengths and Difficulties Questionnaire (SDQ); a.e. age equivalent score * P < .05.
socio-demographics featuring. In order to assess clinical variables the nonparametric test ‘‘Mann–Whitney’’ was used for assessing whether one of two samples of independent observations tended to have larger values than the other. The chi-squared test was used to compare the relative proportions of social and emotional problems between children with CI and children of control group. The Spearman correlation coefficient was used to examine whether or not there is a significant correlation between IQ and age of CI with the outcome variables. The significance level was set at p < 0.05. For statistical processing we used the data processing program SPSS version 20.0. 3. Results The group of children with CI consisted of 20 participants, 8 girls and 12 boys, with mean age 9.17 3.1 (range 5–15 years). All children were implanted with unilateral Nucleus CI (Cochlear Corporation, Sidney, Australia) at a mean age of 37.5 months (range 12–67 months) with an average use of CI of 79.5 months (range 18– 129 months). The control group consisted of 20 healthy children, 5 girls and 15 boys, with mean age 10.08 + 2.5 (range 4–16 years). No statistically significant difference between participants and control group on age (p = 0.33) and gender (p = 0.248) was found. In the group of children with CI, 55% of children showed a score in the normal range of Leiter-R (IQ > 84), 40% in the borderline range (71 < IQ < 84) and 5% in mild range (50 < IQ < 70). In the control group, 60% of children showed a score in the normal range of Leiter-R (IQ > 84), 30% were in the borderline range (84 < IQ < 71) and 10% were in mild range (50 < IQ < 70). Mann–Whitney Test was conducted to determine whether the
CI and normal hearing groups differed in their IQ, but no statistical difference was found (Table 1). On the VABS, children with CI did not significantly differ from the children with normal hearing in any domains. The SDQ scores of CI group and control group were compared in order to investigate behaviors and relationships problems of children. In the survey subscale Overall stress, Behavior problems, Hyperactivity and Prosocial skills, parents indicated relatively positive outcomes for their children. We found a statistical significant difference in emotional symptoms (p = .018) and peer problems (p = .037). No others statistically significant differences between the CI and normal hearing groups were found. The results of Leiter-R, VABS and SDQ are reported in Table 1. Correlations between the measures of IQ and Age of CI with adaptive behavior, social and emotional skills were computed by means of Spearman rank-order correlation (Table 2). For the CI children the following correlations turned out to be significant: age of CI was significantly negative correlated with IQ (p = .002), significantly positive correlated with emotional symptoms (p = .04) and significantly positive correlated with peer problems (p = .02). No significant correlations were found between IQ with the others scores of VABS and SDQ. 4. Discussion The purpose of this study was to assess the non-verbal cognitive skills, adaptive behavior, social and emotional skills in deaf children that reached an open set perception after CI. This association has not been previously described. Although the majority of published studies investigating CI children have focused on children’s audition, speech production and perception,
Table 2 Spearman rank-order correlations for children with CI. IQ Value Age IQ Communication a.e. Daily Living Skills a.e. Socialization e.q. Total Maladaptive Peer problems Hyperactivity-inattention Emotional symptoms Conduct problems Overall stress Pro-social *
p < 0.05.
0.15 – 0.07 0.16 0.05 0.15 0.13 0.14 0.27 0.35 0.4 0.36
Age CI p 0.51 – 0.75 0.47 0.8 0.5 0.59 0.53 0.23 0.12 0.08 0.1
Value 0.243 0.643 0.094 0.159 0.067 0.11 0.558 0.223 0.452 0.372 0.151 0.02
p 0.3 0.002* 0.69 0.5 0.78 0.64 0.02* 0.34 0.04* 0.1 0.537 0.93
1978
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
and spoken language development, very little is currently known about general cognitive development in this population following implantation and whether particular cognitive abilities can help to explain the enormous variation in language outcomes. The results of this study indicated that CI children had a typical development of nonverbal intelligence. In fact, no significant differences of IQ were found between CI children and normalhearing children. After implantation, nonverbal intelligence did not differ significantly between CI children and normal hearing children. It seemed that hearing rehabilitation allowed deaf children with CI the access to sound environment and to verbal language helping implanted children to perform better in some aspects of cognitive abilities. These findings were in agreement with literature data suggesting that deaf individuals performed properly non-verbal tasks [13,14], reinforcing the use of visualization, reasoning and working memory skills in daily life to compensate for the loss of speech information. Very little was found in the literature on the question of adaptive behavior in CI children. In our study, no significant differences were found between CI children and normal hearing children in behavioral adaptability. These data suggested that CI was associated with improvements in behavioral adaptability confirming literature data evidencing that deaf children had a normal developmental rate of adaptive behavior after CI [17]. So far, there has been little discussion on the effects of early intervention for children with hearing loss on social and emotional aspects such as the development of self-regulation, self-control, social competence and peer relationships. Our results indicated that CI children did not differ from control subjects in overall stress, behavior problems, hyperactivity and prosocial skills. On the contrary, we detected that CI children reported more abnormalities in emotional symptoms and peer problems than children with normal hearing. This was consistent with a previous study using the SDQ among children with CI [25] suggesting in clinical practice the need to identify psychosocial problems in CI children using screening instruments. In the current study we have also analyzed the correlation between cognitive skills, adaptive behavior, social and emotional skills after CI in deaf children. The most interesting finding was that the age of CI had a negative correlation with IQ, underling that an earlier CI favored the increase of non-verbal cognitive development. This result supported the fact that IQ was directly associated with age of CI suggesting that, although a period of auditory deprivation may result in linguistic disorders, the CI could produce a restore of non-verbal cognition. Nevertheless, age at implantation corresponded to an increase of emotional and pro-social problems. This suggests that early language experiences with CI may have broader implications. In fact, the early access to CI may enhance children’s speech and language development and later decrease emotional problems (e.g. feelings of loneliness due to peer nonacceptance as normal children) allowing the formation of positive relationships with peers. The findings of this study were consistent with those of Fortunato-Tavares et al. [26] who found that CI had a positive effect on the lives of child users, especially if it is implanted in earlier ages. Unexpectedly no significant correlations between IQ and adaptive behavior were found. These data suggested that intelligence and adaptive behaviors are separate constructs even if highly related. However, with a small sample size, caution must be applied, as the findings might not be transferable to other studies. Another limitation of this study was that it was not a population-based study, therefore issues of clinical ascertainment bias may arise; however, this concern was mitigated in between group comparisons due to highly similar referral sources. Future studies should examine the cognitive skills,
adaptive behavior and emotional skills in the context of total population samples. In conclusion, understanding the social and emotional aspects of child development such as the development of self-regulation and self-control, social competence and peer relationships is essential to supporting the development of this growing group of children. The present study emphasizes the importance of early detection and intervention for children with hearing loss as essential to cognitive skills, adaptive behavior, social and emotional skills. These results favored early CI and suggested the importance to support the use of CI in order to improving nonverbal cognitive skills and personal autonomy in the development of children with hearing loss. Conflict of interest None. References [1] E.A. Schorr, F.P. Roth, N.A. Fox, Quality of life for children with cochlear implants: perceived benefits and problems and the perception of single words and emotional sounds, J. Speech Lang. Hear. Res. 52 (2009) 141–152. [2] Joint Committee on Infant Hearing, Year 2000 position statement: principles and guidelines for early hearing detection and intervention programs, Pediatrics 106 (2000) 798–817. [3] R.J. Ruben, I. Rapin, Plasticity of the developing auditory system, Ann. Otolaryngol. 89 (1980) 303–311. [4] G. Le Maner-Idrissi, G. Rouxel, C. Pajon, V. Dardier, Z. Gavornikova-Baligand, G. Tan-Bescond, et al., Cochlear implant and lexical diversity development in deaf children: intra and interindividual differences, Curr. Psychol. Lett. 25 (2009), Special section p2. [5] M.T. Le Normand, Evaluation du lexique de production chez des enfants sourds profonds munis d’un implant cochle´aire sur un suivi de trois ans, Re´e´ducation Orthophonique 217 (2004) 125–140. [6] J.P. Rauschecker, Auditory cortical plasticity: a comparison with other sensory systems, Trends Neurosci. 22 (1999) 74–80. [7] S. Fukuda, K. Fukushima, Y. Maeda, K. Tsukamura, R. Nagayasu, N. Toida, et al., Language development in multiply handicapped child after cochlear implantation, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 627–633. [8] P. Kushalnagar, T.D. Toplski, B. Schick, T.C. Edwards, A.M. Skalicky, D.L. Patrick, Mode of communication, perceived level of understanding, and perceived quality of life in youth who are deaf or hard of hearing, J. Deaf Stud. Deaf Educ. 16 (2011) 512–523. [9] W.G. Kronenberger, D.B. Pisoni, S.C. Henning, B.G. Colson, Executive functioning skills in long-term users of cochlear implants: a case control study, J. Pediatr. Psychol. (May) (2013) (Epub ahead of print). [10] B. Lyxell, B. Sahle´n, M. Wass, T. Ibertsson, B. Larsby, M. Ha¨llgren, et al., Cognitive development in children with cochlear implants: relations to reading and communication, Int. J. Audiol. 47 (2008) 47–52. [11] B. Lyxell, M. Wass, B. Sahle´n, C. Samuelsson, L. Asker-Arnason, T. Ibertsson, et al., Cognitive development, reading and prosodic skills in children with cochlear implants, Scand. J. Psychol. 50 (5) (2009) 463–474. [12] M. Wass, T. Ibertsson, B. Lyxell, B. Sahle´n, M. Ha¨llgren, B. Larsby, et al., Cognitive and linguistic skills in children with cochlear implants – measures of accuracy and latency as indicators of development, Scand. J. Psychol. 49 (2008) 559–576. [13] A.A. Zekveld, J.B. Deijen, S.T. Goverts, S.E. Kramer, The relationship between nonverbal cognitive functions and hearing loss, J. Speech Lang. Hear. Res. 50 (2007) 74–82. [14] D. Bavelier, M.W. Dye, P.C. Hauser, Do deaf individuals see better? Trends Cogn. Sci. 10 (2006) 512–518. [15] P. Kushalnagar, K. Krull, J. Hannay, P. Mehta, S. Caudle, J. Oghalai, Intelligence, parental depression, and behavior adaptability in deaf children being considered for cochlear implantation, J. Deaf Stud. Deaf Educ. 12 (2007) 335–349. [16] R.H. MacTurk, K.P. Meadow-Orlans, L.S. Koester, P.E. Spencer, Social support, motivation, language, and interaction. A longitudinal study of mothers and deaf infants, Am. Ann. Deaf 138 (1993) 19–25. [17] J.S. Oghalai, S.E. Caudle, B. Bentley, H. Abaya, J. Lin, D. Baker, et al., Cognitive outcomes and familial stress after cochlear implantation in deaf children with and without developmental delays, Otol. Neurotol. 33 (2012) 947–956. [18] E.A. Schorr, Early Cochlear Implant Experience and Emotional Functioning During Childhood: Loneliness in Middle and Late Childhood, Alexander Graham Bell Association for the Deaf and Hard of Hearing, 3417 Volta Place, NW, Washington, 2006. [19] R. Punch, M.B. Hyde, Communication, psychosocial, and educational outcomes of children with cochlear implants and challenges remaining for professionals and parents, Int. J. Otolaryngol. (2011) 573280. [20] B. Loy, A.D. Warner-Czyz, L. Tong, E.A. Tobey, P.S. Roland, The children speak: an examination of the quality of life of pediatric cochlear implant users, Otolaryngol. Head Neck Surg. 142 (2) (2010) 247–253.
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979 [21] E. Genovese, E. Orzan, M. Turrini, G. Babighian, E. Arslan, Speech perception test in Italian language for profoundly deaf children, Acta Otorhinolaryngol. Ital. 15 (1995) 383–390. [22] G.H. Roid, L.J. Miller, Leiter international performance scale – revised: examiner’s manual, in: G.H. Roid, L.J. Miller (Eds.), Leiter International Performance Scale – Revised, Stoelting Co., Wood Dale, IL, 1997. [23] S.E. Sparrow, D.A. Balla, D.V. Cicchetti, Vineland Adaptive Behavior (Survey Form), American Guidances Service, Circle Pines, MN, 1984.
1979
[24] R. Goodman, The strengths and difficulties questionnaire: a research note, J. Child Psychol. Psychiatry 38 (1997) 581–586. [25] L. Anmyr, K. Larsson, M. Olsson, A. Freijd, Strengths and difficulties in children with cochlear implants-comparing self-reports with reports from parents and teachers, Int. J. Pediatr. Otorhinolaryngol. 76 (2012) 1107–1112. [26] T. Fortunato-Tavares, D. Befi-Lopes, R.F. Bento, C.R. Andrade, Children with cochlear implants: communication skills and quality of life, Braz. J. Otorhinolaryngol. 78 (2012) 15–25.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Children with cochlear implants: Cognitive skills, adaptive behaviors, social and emotional skills Andrea De Giacomo a, Francesco Craig a, Alessandra D’Elia b, Francesca Giagnotti b, Emilia Matera a, Nicola Quaranta b,* a
Child Neuropsychiatry Unit, Department of Basic Medical Science, Neuroscience and Sense Organs, Hospital Polyclinic of Bari, University of ‘‘Aldo Moro’’ Bari, Piazza Giulio Cesare 1, Italy Otolaryngology Unit, Department of Basic Medical Science, Neuroscience and Sensory Organs, University of Bari ‘‘A. Moro’’, Italy
b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 July 2013 Received in revised form 12 September 2013 Accepted 15 September 2013 Available online 9 October 2013
Objective: The aim of this study is to examine cognitive skills, adaptive behavior, social and emotional skills in deaf children with cochlear implant (CI) compared to normal hearing children. Methods: The study included twenty children affected by profound hearing loss implanted with a CI compared to 20 healthy children matched to chronological age and gender. Results: Results of this study indicated that 55% of children with CI showed a score in the normal range of nonverbal intelligence (IQ > 84), 40% in the borderline range (71 < IQ < 84) and 5% were in mild range (50 < IQ < 70). No significant differences were found after comparison with normal hearing children. Children with CI reported more abnormalities in emotional symptoms (p = .018) and peer problems (p = .037) than children with normal hearing. Age of CI was negatively correlated with IQ (p = .002), positively correlated with emotional symptoms (p = .04) and with peer problems (p = .02). Conclusions: CI has a positive effect on the lives of deaf children, especially if it is implanted in much earlier ages. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Cochlear implant Deaf children Nonverbal intelligence Adaptive behavior Social and emotional skills
1. Introduction The auditory function has a crucial role in the main stages of child development. The importance of early intervention for children with hearing loss has been demonstrated persuasively in areas including speech perception, production and spoken language, cognitive skills, adaptive behavior, social and emotional outcomes that may drastically limit the quality of life of deaf people [1]. The Joint Committee on Infant Hearing [2] has advocated hearing screening for all newborns, with the goal of confirming hearing loss before 3 months of age and beginning hearing rehabilitation before 6 months of age. Several issues have a bearing on decisions about the beneficial effect of very early CI for the development of age-appropriate spoken language in infants and children. Previous studies reported that neural organization and/or structure related to speech perception/production were affected by the length of auditory deprivation, but the extent and the potential reversibility of changes in the neural architecture are
* Corresponding author at: Otolaryngology Unit, Department of Neuroscience and Sensory Organs, Hospital Polyclinic of Bari, University of ‘‘Aldo Moro’’ Bari, Piazza Giulio Cesare 1, Italy. Tel.: +39 080 5478850; fax: +39 080 5478752. E-mail address: [email protected] (N. Quaranta). 0165-5876/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.09.015
presently not completely known [3]. Children with CI showed distinctive developmental patterns in basic academic skills such as language and reading compared both to children with normal hearing and to children with severe deafness, who have not been implanted [4,5]. These studies provided evidence that by decreasing the age at implantation better outcomes could be obtained in terms of spoken language and speech perception. Thus implantation should ideally occur not only early enough for normal language progress to be achieved, but also before delays could be established. The implicit corollary from all these observations is that cochlear implants (CIs) should be fitted in infants/children as soon as a correct diagnosis of severe to profound hearing loss has been obtained. Indeed the significant advantage of early intervention in children with significant hearing loss was demonstrated in literature. Whereas a great deal of research has been devoted to understanding hearing and spoken language development in deaf children with CIs, very little is currently known about general cognitive development after CI. Studies of some aspects of cognitive capabilities comparing children with normal hearing and children with hearing impairment revealed that the latter experience difficulties at the cognitive level [6–8]. Non-verbal intelligence is meant as fluid intelligence, considered the truest measure of a person’s innate ability. It has been
1976
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
previously suggested that a lack of experience with sound during early development may have an impact on cognitive functions [6], but data in literature is not unique in defining a profile of nonverbal intelligence in children with CI probably due to the study population and survey method. Some authors have, in fact, suggested that children with CI performed at a lower level than hearing children on tasks such as serial memory, phonological processing, short-term/working memory and inhibition-concentration [9–12]. Other researchers have instead reported that deaf individuals may show good performances in nonverbal tasks as spatial working memory and visual attention [13,14]. Less is known about the effects of early intervention for children with hearing loss on adaptive behaviors, social and emotional outcomes. In deaf children previous studies have shown a relation between cognitive abilities and behavioral adaptability [15] and between behavioral adaptability and better communication and family support [16]. Recently, Oghalai et al. [17] reported that children with CI had a normal developmental rate of adaptive behavior after CI. In addition, earliest CI was associated with lowest levels of loneliness during middle and late childhood [18]. Punch conducted parent/teacher surveys containing subscale surveys of social skills and participation, which revealed negative qualitative parent data and negative qualitative and quantitative teacher data, indicating suboptimal social outcomes in children with CI [19]. Social participation and emotional wellbeing became more problematic for some children as they reached adolescence and appeared to struggle with issues around being deaf, feeling selfconscious about the CI external equipment they needed to wear and fitting in with hearing peers. Loy et al. [20] examined if deaf children with CI showed similar psychosocial issues as typical hearing peers. They detected that for profoundly deaf children who regularly use a CI, feelings about life were no better or worse than their hearing peers; while individual areas of difficulty may be different the aggregate scores remained the same. In order to clarify the role of CI in deaf individuals, the main objective of this study was to evaluate the cognitive skills, adaptive behavior, social and emotional skills after cochlear implantation in deaf children and to explore the complex association between all these aspects with the impact of CI implantation age. 2. Methods 2.1. Subjects The study included twenty children affected by profound hearing loss implanted with a unilateral CI at the Otolaryngology Unit of the University of Bari, Italy. Inclusion criteria for the study were: bilateral pre-verbal profound sensorineural hearing loss, appropriate amplification before unilateral CI, oral habilitation before and after cochlear implantation, open set speech perception after CI. Exclusion criteria included history of seizure disorder, learning disability, progressive neurological problems, traumatic brain injury, additional significant disabilities (e.g., blindness, autism), not used spoken Italian as their primary mode of communication or any other serious medical condition. For the evaluation of cognitive and behavioral functions the children were assessed at the Child and Adolescent Neuropsychiatric Unit of the Neurologic and Psychiatric Department of University of Bari, ‘‘Aldo Moro’’, while speech perception was evaluated with age appropriate tests translated and validated in Italian language [21] at the Otolaryngology Department of the same University. The control group consisted of 20 healthy children matched to chronological age and gender with normal hearing. These children were recruited from regular primary and secondary schools and
were fully informed about the experiment. The same exclusion criteria used in the CI group were used to select the control group Parental informed consent was obtained for all participants and the study was approved by the local ethical committee of the ‘‘Azienda Ospedaliero-Universitaria Consorziale Policlinico di Bari’’ (St. 3845; Prot.264/CE). 2.2. Assessment The first step of the evaluation included a collection of clinical and socio-demographic data. Data included parents’ marital status, occupation and years of education, as well as age at identification and status of hearing loss, age of enrollment in the intervention program, developmental milestones, medical and psychological history on paternal and maternal sides, and the child’s medical and psychological history. The second study step involved the administration of standardized instruments to assess cognitive skills, adaptive behavior, social and emotional skills, speech perception, production and spoken language. The Leiter International Performance Scale-Revised [22] is a standardized, individually administered, nonverbal test designed to assess cognitive functions in children and adolescents ages 2–0 to 20–11 years. The Leiter-R includes the Visualization and Reasoning Battery with 10 subtests of nonverbal intellectual ability related to visualization, reasoning and spatial ability; and the Attention and Memory Battery with 10 subtests of nonverbal attention and memory function. The Fluid Reasoning composite is comprised of subtests that show evidence of providing a unique fluid measure of seriation, reasoning and pattern generation. The Full IQ score represents a measure of general nonverbal intelligence. The IQ is them sum of the subtests that compose the IQ estimate, and the subtests represented vary depending on the age of the student. The IQ score includes several aspects of cognition and it is comprised of highly correlated subtests to obtain a single measure of intellectual ability. The Vineland Adaptive Behavior Scale (VABS) [23] assesses personal and social skills, with norms up to 18 years old. Two interview editions, one with 577 items, the other with 297, gather information through semi-structured interviews; both include a Motor Skills Domain for children less than 6 years old and an optional Maladaptive Behavior Domain for children age 5 through 18 is optional. The VABS is a measure of personal and social skills needed for everyday life. Assessed domains include Communication, Daily Living, Motor Skills, and Socialization. Raw scores are converted to age-equivalent standard scores for each domain and for the composite adaptive behavior score. The Strengths and Difficulties Questionnaire (SDQ) [24] form P (Parents), is a parent-reported instrument designed to provide information on children’s behaviors and relationships. The SDQ contains 25 items divided equally among five scales such that subscale scores are generated for Emotional Symptoms (especially aspects related to anxiety and depression), Conduct Problems, Hyperactivity-Inattention (which also contains items on attention problems), Peer Problems (e.g. peer rejection), and Prosocial Behavior. The scores are added together to produce a total overall stress score. The ranges indicating abnormalities are 7–10 for hyperactivity, 4–10 for conduct problems, 5–10 for emotional difficulties, 0–4 for prosocial behaviors and 4–10 for peers relationship. SDQ translated into over sixty languages, including Italian by A. De Giacomo et al., available online at www.sdqinfo.com. 2.3. Data analysis All demographic and clinical variables were subjected to statistical analysis. Descriptive analysis was conducted for
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
1977
Table 1 Results: Leiter-R, VABS and SDQ in IC and control group.
LEITER-R VABS
SDQ
IQ Communication a.e Daily Living skills a.e Socialization a.e Total Maladaptive Overall stress Emotional symptoms Behavior Problems Hyperactivity Peer problems Prosocial
IC group N = 20
IC control N = 20
89.05 13.682 103.01 49.18 99.55 51.6 105.99 56.56 644.9 190.47 35% 35% 20% 0% 30 20
90.10 21.856 107.35 32.03 97.95 41.35 106.65 43.8 681.1 124.36 5% 5% 10% 5% 5 15
Z
p .799 .81 .298 .135 .203 0.127 5.625 2.055 3.02 4.329 .173
.425 .935 .766 .892 .839 .892 .018* .151 .220 .037* .677
Leiter International performance scale-Revised (Leiter-R); Vineland Adaptive Behavior Scale (VABS); Strengths and Difficulties Questionnaire (SDQ); a.e. age equivalent score * P < .05.
socio-demographics featuring. In order to assess clinical variables the nonparametric test ‘‘Mann–Whitney’’ was used for assessing whether one of two samples of independent observations tended to have larger values than the other. The chi-squared test was used to compare the relative proportions of social and emotional problems between children with CI and children of control group. The Spearman correlation coefficient was used to examine whether or not there is a significant correlation between IQ and age of CI with the outcome variables. The significance level was set at p < 0.05. For statistical processing we used the data processing program SPSS version 20.0. 3. Results The group of children with CI consisted of 20 participants, 8 girls and 12 boys, with mean age 9.17 3.1 (range 5–15 years). All children were implanted with unilateral Nucleus CI (Cochlear Corporation, Sidney, Australia) at a mean age of 37.5 months (range 12–67 months) with an average use of CI of 79.5 months (range 18– 129 months). The control group consisted of 20 healthy children, 5 girls and 15 boys, with mean age 10.08 + 2.5 (range 4–16 years). No statistically significant difference between participants and control group on age (p = 0.33) and gender (p = 0.248) was found. In the group of children with CI, 55% of children showed a score in the normal range of Leiter-R (IQ > 84), 40% in the borderline range (71 < IQ < 84) and 5% in mild range (50 < IQ < 70). In the control group, 60% of children showed a score in the normal range of Leiter-R (IQ > 84), 30% were in the borderline range (84 < IQ < 71) and 10% were in mild range (50 < IQ < 70). Mann–Whitney Test was conducted to determine whether the
CI and normal hearing groups differed in their IQ, but no statistical difference was found (Table 1). On the VABS, children with CI did not significantly differ from the children with normal hearing in any domains. The SDQ scores of CI group and control group were compared in order to investigate behaviors and relationships problems of children. In the survey subscale Overall stress, Behavior problems, Hyperactivity and Prosocial skills, parents indicated relatively positive outcomes for their children. We found a statistical significant difference in emotional symptoms (p = .018) and peer problems (p = .037). No others statistically significant differences between the CI and normal hearing groups were found. The results of Leiter-R, VABS and SDQ are reported in Table 1. Correlations between the measures of IQ and Age of CI with adaptive behavior, social and emotional skills were computed by means of Spearman rank-order correlation (Table 2). For the CI children the following correlations turned out to be significant: age of CI was significantly negative correlated with IQ (p = .002), significantly positive correlated with emotional symptoms (p = .04) and significantly positive correlated with peer problems (p = .02). No significant correlations were found between IQ with the others scores of VABS and SDQ. 4. Discussion The purpose of this study was to assess the non-verbal cognitive skills, adaptive behavior, social and emotional skills in deaf children that reached an open set perception after CI. This association has not been previously described. Although the majority of published studies investigating CI children have focused on children’s audition, speech production and perception,
Table 2 Spearman rank-order correlations for children with CI. IQ Value Age IQ Communication a.e. Daily Living Skills a.e. Socialization e.q. Total Maladaptive Peer problems Hyperactivity-inattention Emotional symptoms Conduct problems Overall stress Pro-social *
p < 0.05.
0.15 – 0.07 0.16 0.05 0.15 0.13 0.14 0.27 0.35 0.4 0.36
Age CI p 0.51 – 0.75 0.47 0.8 0.5 0.59 0.53 0.23 0.12 0.08 0.1
Value 0.243 0.643 0.094 0.159 0.067 0.11 0.558 0.223 0.452 0.372 0.151 0.02
p 0.3 0.002* 0.69 0.5 0.78 0.64 0.02* 0.34 0.04* 0.1 0.537 0.93
1978
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979
and spoken language development, very little is currently known about general cognitive development in this population following implantation and whether particular cognitive abilities can help to explain the enormous variation in language outcomes. The results of this study indicated that CI children had a typical development of nonverbal intelligence. In fact, no significant differences of IQ were found between CI children and normalhearing children. After implantation, nonverbal intelligence did not differ significantly between CI children and normal hearing children. It seemed that hearing rehabilitation allowed deaf children with CI the access to sound environment and to verbal language helping implanted children to perform better in some aspects of cognitive abilities. These findings were in agreement with literature data suggesting that deaf individuals performed properly non-verbal tasks [13,14], reinforcing the use of visualization, reasoning and working memory skills in daily life to compensate for the loss of speech information. Very little was found in the literature on the question of adaptive behavior in CI children. In our study, no significant differences were found between CI children and normal hearing children in behavioral adaptability. These data suggested that CI was associated with improvements in behavioral adaptability confirming literature data evidencing that deaf children had a normal developmental rate of adaptive behavior after CI [17]. So far, there has been little discussion on the effects of early intervention for children with hearing loss on social and emotional aspects such as the development of self-regulation, self-control, social competence and peer relationships. Our results indicated that CI children did not differ from control subjects in overall stress, behavior problems, hyperactivity and prosocial skills. On the contrary, we detected that CI children reported more abnormalities in emotional symptoms and peer problems than children with normal hearing. This was consistent with a previous study using the SDQ among children with CI [25] suggesting in clinical practice the need to identify psychosocial problems in CI children using screening instruments. In the current study we have also analyzed the correlation between cognitive skills, adaptive behavior, social and emotional skills after CI in deaf children. The most interesting finding was that the age of CI had a negative correlation with IQ, underling that an earlier CI favored the increase of non-verbal cognitive development. This result supported the fact that IQ was directly associated with age of CI suggesting that, although a period of auditory deprivation may result in linguistic disorders, the CI could produce a restore of non-verbal cognition. Nevertheless, age at implantation corresponded to an increase of emotional and pro-social problems. This suggests that early language experiences with CI may have broader implications. In fact, the early access to CI may enhance children’s speech and language development and later decrease emotional problems (e.g. feelings of loneliness due to peer nonacceptance as normal children) allowing the formation of positive relationships with peers. The findings of this study were consistent with those of Fortunato-Tavares et al. [26] who found that CI had a positive effect on the lives of child users, especially if it is implanted in earlier ages. Unexpectedly no significant correlations between IQ and adaptive behavior were found. These data suggested that intelligence and adaptive behaviors are separate constructs even if highly related. However, with a small sample size, caution must be applied, as the findings might not be transferable to other studies. Another limitation of this study was that it was not a population-based study, therefore issues of clinical ascertainment bias may arise; however, this concern was mitigated in between group comparisons due to highly similar referral sources. Future studies should examine the cognitive skills,
adaptive behavior and emotional skills in the context of total population samples. In conclusion, understanding the social and emotional aspects of child development such as the development of self-regulation and self-control, social competence and peer relationships is essential to supporting the development of this growing group of children. The present study emphasizes the importance of early detection and intervention for children with hearing loss as essential to cognitive skills, adaptive behavior, social and emotional skills. These results favored early CI and suggested the importance to support the use of CI in order to improving nonverbal cognitive skills and personal autonomy in the development of children with hearing loss. Conflict of interest None. References [1] E.A. Schorr, F.P. Roth, N.A. Fox, Quality of life for children with cochlear implants: perceived benefits and problems and the perception of single words and emotional sounds, J. Speech Lang. Hear. Res. 52 (2009) 141–152. [2] Joint Committee on Infant Hearing, Year 2000 position statement: principles and guidelines for early hearing detection and intervention programs, Pediatrics 106 (2000) 798–817. [3] R.J. Ruben, I. Rapin, Plasticity of the developing auditory system, Ann. Otolaryngol. 89 (1980) 303–311. [4] G. Le Maner-Idrissi, G. Rouxel, C. Pajon, V. Dardier, Z. Gavornikova-Baligand, G. Tan-Bescond, et al., Cochlear implant and lexical diversity development in deaf children: intra and interindividual differences, Curr. Psychol. Lett. 25 (2009), Special section p2. [5] M.T. Le Normand, Evaluation du lexique de production chez des enfants sourds profonds munis d’un implant cochle´aire sur un suivi de trois ans, Re´e´ducation Orthophonique 217 (2004) 125–140. [6] J.P. Rauschecker, Auditory cortical plasticity: a comparison with other sensory systems, Trends Neurosci. 22 (1999) 74–80. [7] S. Fukuda, K. Fukushima, Y. Maeda, K. Tsukamura, R. Nagayasu, N. Toida, et al., Language development in multiply handicapped child after cochlear implantation, Int. J. Pediatr. Otorhinolaryngol. 67 (2003) 627–633. [8] P. Kushalnagar, T.D. Toplski, B. Schick, T.C. Edwards, A.M. Skalicky, D.L. Patrick, Mode of communication, perceived level of understanding, and perceived quality of life in youth who are deaf or hard of hearing, J. Deaf Stud. Deaf Educ. 16 (2011) 512–523. [9] W.G. Kronenberger, D.B. Pisoni, S.C. Henning, B.G. Colson, Executive functioning skills in long-term users of cochlear implants: a case control study, J. Pediatr. Psychol. (May) (2013) (Epub ahead of print). [10] B. Lyxell, B. Sahle´n, M. Wass, T. Ibertsson, B. Larsby, M. Ha¨llgren, et al., Cognitive development in children with cochlear implants: relations to reading and communication, Int. J. Audiol. 47 (2008) 47–52. [11] B. Lyxell, M. Wass, B. Sahle´n, C. Samuelsson, L. Asker-Arnason, T. Ibertsson, et al., Cognitive development, reading and prosodic skills in children with cochlear implants, Scand. J. Psychol. 50 (5) (2009) 463–474. [12] M. Wass, T. Ibertsson, B. Lyxell, B. Sahle´n, M. Ha¨llgren, B. Larsby, et al., Cognitive and linguistic skills in children with cochlear implants – measures of accuracy and latency as indicators of development, Scand. J. Psychol. 49 (2008) 559–576. [13] A.A. Zekveld, J.B. Deijen, S.T. Goverts, S.E. Kramer, The relationship between nonverbal cognitive functions and hearing loss, J. Speech Lang. Hear. Res. 50 (2007) 74–82. [14] D. Bavelier, M.W. Dye, P.C. Hauser, Do deaf individuals see better? Trends Cogn. Sci. 10 (2006) 512–518. [15] P. Kushalnagar, K. Krull, J. Hannay, P. Mehta, S. Caudle, J. Oghalai, Intelligence, parental depression, and behavior adaptability in deaf children being considered for cochlear implantation, J. Deaf Stud. Deaf Educ. 12 (2007) 335–349. [16] R.H. MacTurk, K.P. Meadow-Orlans, L.S. Koester, P.E. Spencer, Social support, motivation, language, and interaction. A longitudinal study of mothers and deaf infants, Am. Ann. Deaf 138 (1993) 19–25. [17] J.S. Oghalai, S.E. Caudle, B. Bentley, H. Abaya, J. Lin, D. Baker, et al., Cognitive outcomes and familial stress after cochlear implantation in deaf children with and without developmental delays, Otol. Neurotol. 33 (2012) 947–956. [18] E.A. Schorr, Early Cochlear Implant Experience and Emotional Functioning During Childhood: Loneliness in Middle and Late Childhood, Alexander Graham Bell Association for the Deaf and Hard of Hearing, 3417 Volta Place, NW, Washington, 2006. [19] R. Punch, M.B. Hyde, Communication, psychosocial, and educational outcomes of children with cochlear implants and challenges remaining for professionals and parents, Int. J. Otolaryngol. (2011) 573280. [20] B. Loy, A.D. Warner-Czyz, L. Tong, E.A. Tobey, P.S. Roland, The children speak: an examination of the quality of life of pediatric cochlear implant users, Otolaryngol. Head Neck Surg. 142 (2) (2010) 247–253.
A. De Giacomo et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 1975–1979 [21] E. Genovese, E. Orzan, M. Turrini, G. Babighian, E. Arslan, Speech perception test in Italian language for profoundly deaf children, Acta Otorhinolaryngol. Ital. 15 (1995) 383–390. [22] G.H. Roid, L.J. Miller, Leiter international performance scale – revised: examiner’s manual, in: G.H. Roid, L.J. Miller (Eds.), Leiter International Performance Scale – Revised, Stoelting Co., Wood Dale, IL, 1997. [23] S.E. Sparrow, D.A. Balla, D.V. Cicchetti, Vineland Adaptive Behavior (Survey Form), American Guidances Service, Circle Pines, MN, 1984.
1979
[24] R. Goodman, The strengths and difficulties questionnaire: a research note, J. Child Psychol. Psychiatry 38 (1997) 581–586. [25] L. Anmyr, K. Larsson, M. Olsson, A. Freijd, Strengths and difficulties in children with cochlear implants-comparing self-reports with reports from parents and teachers, Int. J. Pediatr. Otorhinolaryngol. 76 (2012) 1107–1112. [26] T. Fortunato-Tavares, D. Befi-Lopes, R.F. Bento, C.R. Andrade, Children with cochlear implants: communication skills and quality of life, Braz. J. Otorhinolaryngol. 78 (2012) 15–25.