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Global developmental abilities of cochlear implanted children with spastic cerebral palsy: two experimental groups

Abstracts

PURPOSE:

To analyze gross motor, fine motor-adaptive, language, social function performance, and communicative behaviors among cochlear-implanted children with spastic cerebral palsy (CP) and children with CP without hearing loss (HL) and to compare them with children with normal development.

METHODS:

Prospective cross-sectional study involving 12 children with mean age of 63 months, distributed into two experimental groups: G1 - 4 children with CP and cochlear implant (CI) users and G2 - 4 children with CP without HL. A third group (G3) was the control group with four typically developing children. In the experimental groups, six children were classified in level II and two in level IV, using the Gross Motor Function Classification System. We used the Denver Developmental Screening Test II and the Communicative Behavior Observation (CBO).

RESULTS:

G3 showed better performance than G1 and G2 in all evaluations. G2 showed better results than G1 in language, communication, personal-social, and fine motor-adaptive areas, except in the gross motor area. Aspects of language and communicative behaviors were lower in both experimental groups, especially in G1. Skills related to personal-social area showed no differences among the groups.

CONCLUSION:

Motor impairment of G1 and G2 and HL in G1 affected the development in the assessed areas, but these factors did not restrict personal-social development. Children with CP did not achieve high development in social function; however, the difference with relation to G3 was not statically significant. The CI provided a channel for oral language reception and social interaction, which has a key role in determining the quality of life.

Cerebral palsy; Cochlear implantation; Language; Hearing; Communication


OBJETIVO:

Analisar o desempenho motor grosso, motor fino-adaptativo, linguagem, pessoal-social e comportamentos comunicativos de crianças com paralisia cerebral (PC) usuárias de implante coclear (IC) e crianças com PC sem deficiência auditiva (DA), e compará-las com crianças com desenvolvimento típico de linguagem.

MÉTODOS:

Estudo prospectivo transversal de 12 crianças, idade média de 63 meses, distribuídas em dois grupos experimentais: G1 - quatro crianças com PC e IC; G2 - quatro crianças com PC sem DA; e G3 - quatro crianças do grupo controle. Seis crianças foram classificadas no nível II e duas no nível IV no Gross Motor Function Classification System (GMFCS). Foram utilizados o Teste de Screening do Desenvolvimento Denver-II (TSDD-II) e a Observação do Comportamento Comunicativo (OCC).

RESULTADOS:

G3 apresentou desempenho superior ao de G1 e de G2 em todas as avaliações. G2 foi superior a G1 em linguagem, comunicação, pessoal-social e motor fino-adaptativo, exceto na área motora grossa. Os aspectos de linguagem e comportamentos comunicativos foram inferiores nos dois grupos experimentais, especialmente no G1. As habilidades avaliadas na área pessoal-social não apresentaram diferenças entre os grupos.

CONCLUSÃO:

A limitação motora de G1 e G2 e a DA de G1 influenciaram o desenvolvimento nas áreas avaliadas, porém esses fatores não restringiram o desenvolvimento pessoal-social. A habilidade pessoal-social também esteve rebaixada para os grupos com PC, porém a diferença dessa função com G3 não foi significante. O IC proporcionou um canal de recepção da linguagem oral e interação social, o que o determina como uma ferramenta para a melhoria da qualidade de vida nessas crianças.

Paralisia cerebral; Implante coclear; Linguagem; Audição; Comunicação


INTRODUCTION

The term cerebral palsy (CP) describes a group of movement and postural disorders attributed to nonprogressive dysfunctions that occur during fetal or child brain development( 11. Bax M, Goldstein M, Rosenbaum P, Leviton A, Paneth N. Proposed definition and classification of cerebral palsy. Dev Med Child Neurol. 2005;47(8):571-6. , 22. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, et al. A report: definition and classification of cerebral palsy April 2006. Dev Med Child Neurol. 2007;109:8-14. ). Motor disorders in CP are usually followed by sensation, perception, cognition, communication, and behavioral dysfunctions, as well as epilepsies and secondary musculoskeletal problems( 11. Bax M, Goldstein M, Rosenbaum P, Leviton A, Paneth N. Proposed definition and classification of cerebral palsy. Dev Med Child Neurol. 2005;47(8):571-6.

2. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, et al. A report: definition and classification of cerebral palsy April 2006. Dev Med Child Neurol. 2007;109:8-14.
- 33. Shevell MI, Dagenais L, Hall N. REPACQ Consortium: comorbidities in cerebral palsy and their relationship to neurologic subtype and GMFCS level. Neurology. 2009;72(24):2090-6. ).

Literature shows the effect of the motor condition of CP on several areas of development( 33. Shevell MI, Dagenais L, Hall N. REPACQ Consortium: comorbidities in cerebral palsy and their relationship to neurologic subtype and GMFCS level. Neurology. 2009;72(24):2090-6.

4. Pirila S, van der Meere J, Pentikainen T, Ruusu-Niemi P, Korpela R, Kilpinen J, et al. Language and motor speech skill in children with cerebral palsy. J Commun Disord. 2007;40(2):116-28.

5. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62.

6. Aisen MLI, Kerkovickd D, Mast J, Mulroy S, Wren TA, Kay RM, et al. Cerebral palsy: clinical care and neurological rehabilitation. Lancet Neurol. 2011;10(9):844-52.

7. Vasconcelos RLM, Moura TL, Campos TF, Lindquist ARR, Guerra RO. Functional performance assessment of children with cerebral palsy according to motor impairment levels. Rev Bras Fisioter. 2009;13(5):390-7.

8. Zanudin A, Burns Y, Gray PH, Danks M, Poulsen L, Watter P. Perinatal events and motor performance of children born with ELBW and nondisabled. Pediatr Phys Ther. 2013;25(1):30-5.

9. Hadders-Algra A, Mijna MD. General movement: a window for early identification of children at high risk for developmental disorders. J Pediatrics. 2004;145(2):12-8.

10. Vargus-Adams JN, Martin LK, Maignan SH, Klein AC, Salisbury S. The GMFM, PEDI, and CP-QOL and perspectives on functioning from children with CP, parents, and medical professionals. J Pediatr Rehabil Med. 2011;4(1):3-12.
- 1111. Reid SM, Carlin JB, Reedihough DS. Using the Gross Motor Function Classification System to describe patterns of motor severity in cerebral palsy. Dev Med Child Neurol. 2011;53(11):1007-12. ). In the presence of motor delay, the child may lose opportunities to acquire knowledge, which is influenced by the relationships the child establishes with the environment and with important interferences for general learning and quality of life( 55. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62. , 77. Vasconcelos RLM, Moura TL, Campos TF, Lindquist ARR, Guerra RO. Functional performance assessment of children with cerebral palsy according to motor impairment levels. Rev Bras Fisioter. 2009;13(5):390-7. , 1111. Reid SM, Carlin JB, Reedihough DS. Using the Gross Motor Function Classification System to describe patterns of motor severity in cerebral palsy. Dev Med Child Neurol. 2011;53(11):1007-12. ).

Hearing impairment (HI) is common, especially because the etiological factor of CP may be the same for hearing loss( 1212. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8. , 1313. Özdemir S, Tuncer Ü, Tarkan O, Kirog?lu M, Çetik F, Akar F. Factors contributing to limited or non-use in the cochlear implant systems in children: 11 years experience. Int J Pediatr Otorhinolaryngol. 2013;77(3):407-9. ). Studies present a rate of 12 to 30% of hearing loss (HL) in children with CP( 1414. Reid SM, Modak MB, Berkowitz RG, Reddihough DS. A population-based study and systematic review of hearing loss in children with cerebral palsy. Dev Med Child Neurol. 2011;53(11):1038-45. ). The early identification of HL in these children is also relevant due to the impact on communication, cognitive, and psychosocial development( 99. Hadders-Algra A, Mijna MD. General movement: a window for early identification of children at high risk for developmental disorders. J Pediatrics. 2004;145(2):12-8.

10. Vargus-Adams JN, Martin LK, Maignan SH, Klein AC, Salisbury S. The GMFM, PEDI, and CP-QOL and perspectives on functioning from children with CP, parents, and medical professionals. J Pediatr Rehabil Med. 2011;4(1):3-12.

11. Reid SM, Carlin JB, Reedihough DS. Using the Gross Motor Function Classification System to describe patterns of motor severity in cerebral palsy. Dev Med Child Neurol. 2011;53(11):1007-12.

12. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8.

13. Özdemir S, Tuncer Ü, Tarkan O, Kirog?lu M, Çetik F, Akar F. Factors contributing to limited or non-use in the cochlear implant systems in children: 11 years experience. Int J Pediatr Otorhinolaryngol. 2013;77(3):407-9.

14. Reid SM, Modak MB, Berkowitz RG, Reddihough DS. A population-based study and systematic review of hearing loss in children with cerebral palsy. Dev Med Child Neurol. 2011;53(11):1038-45.

15. Bacciu A, Pasanisi E, Vincenti V, Ormitti F, Di Lella F, Guida M, et al. Cochlear implantation in children with cerebral palsy. A preliminary report. Int J Pediatr Otorhinolaryngol. 2009;73(5):717-21.

16. Edwards LC. Children with cochlear implants and complex needs: a review of outcome research and psychological practice. J Deaf Stud Deaf Educ. 2007;12(3):258-68.
- 1717. Santos MJD, Bevilacqua MC, Moret ALM, Lamônica DAC, Costa OA, Yamaguti EH. Indication process of cochlear implant for a child with cerebral palsy: a case report. Rev Soc Bras Fonoaudiol. 2011;16(4):474-8. ).

Besides hearing aids, the cochlear implant (CI) has been advised for children with CP and for those with deep and/or severe sensorineural HL. It has shown good results concerning hearing ability and language, as well as aspects of quality of life( 1212. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8. , 1313. Özdemir S, Tuncer Ü, Tarkan O, Kirog?lu M, Çetik F, Akar F. Factors contributing to limited or non-use in the cochlear implant systems in children: 11 years experience. Int J Pediatr Otorhinolaryngol. 2013;77(3):407-9. , 1515. Bacciu A, Pasanisi E, Vincenti V, Ormitti F, Di Lella F, Guida M, et al. Cochlear implantation in children with cerebral palsy. A preliminary report. Int J Pediatr Otorhinolaryngol. 2009;73(5):717-21. , 1818. Meinzen-Derr J, Wiley S, Grether S, Choo DI. Children with cochlear implants and developmental disabilities: a language skills with developmentally matched hearing peers. Res Dev Disabil. 2011;32(2):757-67.

19. Wiley S, Jahnke M, Meinzen-Derr J, Choo D. Perceived qualitative benefits of cochlear implants in children with multi-handicaps. Int J Pediatr Otorhinolayngol. 2005;69(6):791-8.

20. Santos MJD, Moret ALM, Lamônica DA, Costa AO, Bevilacqua MC. Cochlear implants in children with cerebral palsy. In: Nikolopoulos TP, editor. Proceedings of the 10th European Symposium on Paediatric Cochlear Implantation; 2011 May 12-15; Athenas, Greece. Bologna: Medimond; 2011. p. 135-40.

21. Steven RA, Green KM, Broomfield SJ, Henderson LA, Ramsden RT, Bruce IA. Cochlear implantation in children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 2011;75(11):1427-30.

22. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52.

23. Santos MJD. Cochlear implant in children with cerebral palsy [dissertação]. Bauru: Universidade de São Paulo; 2012.
- 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. ).

Besides data related to speech perception, a few studies analyzed other aspects of global development regarding the performance of children with CP after CI( 1313. Özdemir S, Tuncer Ü, Tarkan O, Kirog?lu M, Çetik F, Akar F. Factors contributing to limited or non-use in the cochlear implant systems in children: 11 years experience. Int J Pediatr Otorhinolaryngol. 2013;77(3):407-9. , 2020. Santos MJD, Moret ALM, Lamônica DA, Costa AO, Bevilacqua MC. Cochlear implants in children with cerebral palsy. In: Nikolopoulos TP, editor. Proceedings of the 10th European Symposium on Paediatric Cochlear Implantation; 2011 May 12-15; Athenas, Greece. Bologna: Medimond; 2011. p. 135-40. , 2121. Steven RA, Green KM, Broomfield SJ, Henderson LA, Ramsden RT, Bruce IA. Cochlear implantation in children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 2011;75(11):1427-30. , 2323. Santos MJD. Cochlear implant in children with cerebral palsy [dissertação]. Bauru: Universidade de São Paulo; 2012. ), and none of them presented how the development of children with CP without HI takes place, in comparison with that of children with CP undergoing the process of hearing rehabilitation by using a CI.

The objective of this study was to analyze the performance of cochlear implanted children with CP, children with CP and normal hearing, and children without CP and HL, in the areas of gross motor (GM), fine-motor personal-social (PS) and communication behaviors

METHODS

This study received the appoval by the research ethics committee of the Bauru School of Dentistry, University of São Paulo (FOB-USP) (protocol numbers 096/2010 and 019/2010), and all the legal representatives of the children participating in the study signed the informed consent form. The evaluations were conducted in the facilities of the Speech Language Pathology and Audiology clinic in FOB-USP for groups of children with CP and no HI and for children with normal hearing, language, and motor function development. Children with CP using CI were followed up by the Cochlear Implant Sector in the Center of Audiology Studies at the Hospital for Rehabilitation of Craniofacial Anomalies at USP.

The sample consisted of 12 children aged between 44 and 84 months divided into three groups and paired according to gender and chronological age (Table 1). Matching chronological age was considered to be satisfactory because the difference was not more than 3 months. Both experimental groups presented with CP, and the third group (control) had proper development for their age:

Table 1
Sample characterization
  • Group 1 (G1): four children with spastic CP andcochlear implant users with no intellectual disability;

  • Group 2 (G2): four children with spastic CP, with no hearing impairment or intellectual disability; and

  • Group 3 (G3): four children with typical development.

Children in G1 were followed up under Cochlear Implant Program in the Hospital for Rehabilitation of Craniofacial Anomalies at USP and they met all the eligibility criteria for the CI surgery( 2525. Geers AE. Techniques for assessing auditory speech perception and lipreading enhancement in young deaf children. Volta Review. 1994;96(5):85-96. ); requirements involved preserved intellectual skills. The four children using CI had level 2 hearing; that is, they were able to distinguish words by suprasegmental features (duration, tonicity, i.e., pé - menino, mão - geladeira)( 2626. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-23. ) and, in some situations, it was necessary to use gestures. Only one child (participant 1) produced isolated words more frequently, being in category 2 of expressive language( 2626. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-23. ). The other children produced only a few full words, or those considered to be intelligible, therefore, they communicated by gestures and vocalizations.

All the participants in G1 and G2 attended school and rehabilitation centers, being assisted in the fields of Physical Therapy and Speech Language and Audiology Therapy since early childhood. Children using CI attended weekly therapy to develop hearing skills.

Children in G2 and G3 underwent a psychological evaluation with Stanford-Binet Intelligence Scale, and results were found to be within normality rates. Children in G1 were assessed by a team of specialized psychologists, excluding the presence of cognitive changes. No children in G1 or G2 presented seizures or episodes of epilepsy.

All evaluations were conducted by speech language pathologists having experience in the application of the instruments used in the study and assisting children with CP. The motor function of children in G1 and G2 was classified according to the Gross Motor Function Classification System (GMFCS( 2727. Ferreira AT. Receptive and expressive vocabulary of children with Down Syndrome [dissertação]. Bauru: Universidade de São Paulo; 2012. ) (Table 1).

Communicative behavior observation (CBO)( 2828. Frankenburg WK, Doods J, Archer P, Bresnick B, Maschka P, Edelman N, et al. Denver II Training Manual. Denver: Denver Developmental Materials; 1992. ) protocol was used and analyzed the following categories: interaction, communicative intention, eye contact, vocalization, production of words, production of sentence, respect to changing shifts, maintenance of dialogical activity, comprehension of concrete and abstract situations, acceptance of simple orders, acceptance of complex orders, symbolic act of playing, use of gestures, time of attention, function of informing, function of protesting, function of requesting, and function of offering and mimicking. These categories used to analyze the communicative behavior were calculated by the following criteria: 0 - did not present it; 1 - presented it in restricted situations of interest; and 2 - presented it in any situation. For statistical treatment, scores obtained after the evaluation of recordings about the status of ludic activity were added. By considering the total number of items and analysis criteria, the maximum sum reached 40 points.

The Denver Developmental Screening Test II (DDST-II)( 2929. Albrecht GL, Devlieger PJ: The disability paradox: high quality of life against all odds. Soc Sci Med. 1999;48(8):977-88. ) was applied in the areas of GM, FMA, LG, and PS. Initially, while administering the instrument, the age of the child was calculated in months and, afterwards, a vertical line was traced in the specific protocol of the test. The procedures related to this age group were applied for all the areas, according to the rules of application of the procedure. The analyses were carried out in accordance with the instructions of the instruments. Statistical tests included analysis of variance and Tukey's test (p ≤ 0.05), chosen according to the characteristics of the variables.

RESULTS

Table 2 presents mean, minimum, and maximum scores obtained by the groups in the skills tested by the CBO( 2828. Frankenburg WK, Doods J, Archer P, Bresnick B, Maschka P, Edelman N, et al. Denver II Training Manual. Denver: Denver Developmental Materials; 1992. ) and the DDST-II( 2929. Albrecht GL, Devlieger PJ: The disability paradox: high quality of life against all odds. Soc Sci Med. 1999;48(8):977-88. ). It can be observed that mean, minimum, and maximum scores obtained in G1 are lower in all the assessed aspects than those in other groups.

Table 2
Mean, minimum, and maximum values of the skills tested by the Denver Developmental Screening Test II and in the communicative behavior observation in the three groups of the study

The analysis of variance was significant in all the assessed areas, except for the personal-social feature. Therefore, Table 3 presents the results of the statistical analysis carried out using the Tukey's test, for only those aspects that were found significant in the analysis of variance.

Table 3
Correlations between the four assessed areas in the Denver Developmental Screening Test II and score in the communicative behavior observation between the three analyzed groups

DISCUSSION

Children with CP may present with developmental changes in different domains, because motor disorders affect childhood development in general( 33. Shevell MI, Dagenais L, Hall N. REPACQ Consortium: comorbidities in cerebral palsy and their relationship to neurologic subtype and GMFCS level. Neurology. 2009;72(24):2090-6.

4. Pirila S, van der Meere J, Pentikainen T, Ruusu-Niemi P, Korpela R, Kilpinen J, et al. Language and motor speech skill in children with cerebral palsy. J Commun Disord. 2007;40(2):116-28.

5. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62.

6. Aisen MLI, Kerkovickd D, Mast J, Mulroy S, Wren TA, Kay RM, et al. Cerebral palsy: clinical care and neurological rehabilitation. Lancet Neurol. 2011;10(9):844-52.
- 77. Vasconcelos RLM, Moura TL, Campos TF, Lindquist ARR, Guerra RO. Functional performance assessment of children with cerebral palsy according to motor impairment levels. Rev Bras Fisioter. 2009;13(5):390-7. ). Motor difficulties are limited to experiences of the children not only regarding interaction with people, objects, and events, but also regarding how to manipulate objects, repeat actions, control their own bodies and body scheme. Therefore, the child with neuropsychomotor development delay may lose concrete opportunities to evolve his or her abilities, thus causing gaps in the perceptive, cognitive, linguistic, and social areas( 55. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62. , 77. Vasconcelos RLM, Moura TL, Campos TF, Lindquist ARR, Guerra RO. Functional performance assessment of children with cerebral palsy according to motor impairment levels. Rev Bras Fisioter. 2009;13(5):390-7.

8. Zanudin A, Burns Y, Gray PH, Danks M, Poulsen L, Watter P. Perinatal events and motor performance of children born with ELBW and nondisabled. Pediatr Phys Ther. 2013;25(1):30-5.

9. Hadders-Algra A, Mijna MD. General movement: a window for early identification of children at high risk for developmental disorders. J Pediatrics. 2004;145(2):12-8.
- 1010. Vargus-Adams JN, Martin LK, Maignan SH, Klein AC, Salisbury S. The GMFM, PEDI, and CP-QOL and perspectives on functioning from children with CP, parents, and medical professionals. J Pediatr Rehabil Med. 2011;4(1):3-12. ). So, limitations to explore the environment voluntarily are expected, which can lead to flaws in the sensory input, causing deficit in perceptive areas and damage in the development of language and cognition. As there will be important reflections in the interpretations of information coming from the environment, there may be difficulties to judge the received information properly( 55. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62. ).

In CP, motor impairment should be analyzed by considering functional aspects, once functionality is considered to be a health feature. By using the GMFCS( 2626. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-23. ), it was possible to characterize the motor function in terms of functionality, particularly emphasizing trunk and gait control. The motor scores obtained by participants in G1 and G2 (Table 1) indicate the level of functional autonomy to act independently in an environment.

Some authors showed that degree of motor disorders is directly related to functional capacity, that is, the higher the motor severity, the higher the functional capacity, and this can reflect on the global development of skills in the several fields( 77. Vasconcelos RLM, Moura TL, Campos TF, Lindquist ARR, Guerra RO. Functional performance assessment of children with cerebral palsy according to motor impairment levels. Rev Bras Fisioter. 2009;13(5):390-7. , 1010. Vargus-Adams JN, Martin LK, Maignan SH, Klein AC, Salisbury S. The GMFM, PEDI, and CP-QOL and perspectives on functioning from children with CP, parents, and medical professionals. J Pediatr Rehabil Med. 2011;4(1):3-12. , 1111. Reid SM, Carlin JB, Reedihough DS. Using the Gross Motor Function Classification System to describe patterns of motor severity in cerebral palsy. Dev Med Child Neurol. 2011;53(11):1007-12. ), because, for the child, the performance of movements favors the construction of sensorimotor patterns. These are necessary to develop functional activities that contribute to the learning process.

In GM skill, assessed by the DDST-II, performance differences between the control group (G3) and the other groups (G1 and G2) were expected, once the main characteristics of CP are changed in motor function classification. The scores obtained in GMFCS already indicated that this area would be more affected for these groups (Table 1).

The motor performance of individuals with CP is influenced by abnormal postural reactions, changes in tonic reflexes, persistence of primitive responses, and delay in neuropsychomotor development, depending on the severity of neurological damage and motor sequelae, which define the clinical variability several clinical outcome( 11. Bax M, Goldstein M, Rosenbaum P, Leviton A, Paneth N. Proposed definition and classification of cerebral palsy. Dev Med Child Neurol. 2005;47(8):571-6. , 22. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, et al. A report: definition and classification of cerebral palsy April 2006. Dev Med Child Neurol. 2007;109:8-14. ).

The FMA analyzes the ability of the child regarding the organization of stimuli, perception of relations, decomposition of the whole in several parts and its reintegration, and the use of these skills in daily tasks during manual activities. In this context, it is important that the children can perform activities independently, aiming to develop their motor skills in a more elaborate and coordinated way, even if adaptations are necessary to improve their performances. This can cause relevant progress on the interaction of the children with CP, favoring their global development.

Findings regarding the motor area in this study (Table 2) show a specially relevant characteristic of CP, that is, the diversity of clinical outcome regarding the acquisition and performances in the different development dimensions, as reported in literature( 77. Vasconcelos RLM, Moura TL, Campos TF, Lindquist ARR, Guerra RO. Functional performance assessment of children with cerebral palsy according to motor impairment levels. Rev Bras Fisioter. 2009;13(5):390-7.

8. Zanudin A, Burns Y, Gray PH, Danks M, Poulsen L, Watter P. Perinatal events and motor performance of children born with ELBW and nondisabled. Pediatr Phys Ther. 2013;25(1):30-5.

9. Hadders-Algra A, Mijna MD. General movement: a window for early identification of children at high risk for developmental disorders. J Pediatrics. 2004;145(2):12-8.

10. Vargus-Adams JN, Martin LK, Maignan SH, Klein AC, Salisbury S. The GMFM, PEDI, and CP-QOL and perspectives on functioning from children with CP, parents, and medical professionals. J Pediatr Rehabil Med. 2011;4(1):3-12.
- 1111. Reid SM, Carlin JB, Reedihough DS. Using the Gross Motor Function Classification System to describe patterns of motor severity in cerebral palsy. Dev Med Child Neurol. 2011;53(11):1007-12. ). Besides, these situations predict disorders related to sensation, perception, cognition, communication, behaviors, among others( 11. Bax M, Goldstein M, Rosenbaum P, Leviton A, Paneth N. Proposed definition and classification of cerebral palsy. Dev Med Child Neurol. 2005;47(8):571-6.

2. Rosenbaum P, Paneth N, Leviton A, Goldstein M, Bax M, et al. A report: definition and classification of cerebral palsy April 2006. Dev Med Child Neurol. 2007;109:8-14.
- 33. Shevell MI, Dagenais L, Hall N. REPACQ Consortium: comorbidities in cerebral palsy and their relationship to neurologic subtype and GMFCS level. Neurology. 2009;72(24):2090-6. ), which interfere in global development in a different and particular way.

It can be inferred that motor limitation may have an impact on global development; however, it may not have been sufficient to interfere substantially in acquisition of language skills in G2 (Table 2). In G1, both comorbidities, motor limitation and HI, interfered with language more strongly. Participants in G1 produced isolated words, and their linguistic ability was restricted to immediate events and objects related to their daily routine. All of them presented with hearing level 2( 2626. Palisano R, Rosenbaum P, Walter S, Russell D, Wood E, Galuppi B. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev Med Child Neurol. 1997;39(4):214-23. ) and began communication by the oral language, unlike the other groups in which participants were able to produce more elaborated sentences. These results show that hearing privation is a determinant and prevalent factor for the oral language acquisition and development( 1717. Santos MJD, Bevilacqua MC, Moret ALM, Lamônica DAC, Costa OA, Yamaguti EH. Indication process of cochlear implant for a child with cerebral palsy: a case report. Rev Soc Bras Fonoaudiol. 2011;16(4):474-8. , 2222. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52.

23. Santos MJD. Cochlear implant in children with cerebral palsy [dissertação]. Bauru: Universidade de São Paulo; 2012.

24. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304.
- 2525. Geers AE. Techniques for assessing auditory speech perception and lipreading enhancement in young deaf children. Volta Review. 1994;96(5):85-96. ). In G1, mean time of CI use was 20 months, which is considerable to observe open-set speech perception skills and oral language and communication skills among children without CP( 2525. Geers AE. Techniques for assessing auditory speech perception and lipreading enhancement in young deaf children. Volta Review. 1994;96(5):85-96. ).

Studies reported slower development of hearing and language skills among children with CP, especially regarding expressive language development( 44. Pirila S, van der Meere J, Pentikainen T, Ruusu-Niemi P, Korpela R, Kilpinen J, et al. Language and motor speech skill in children with cerebral palsy. J Commun Disord. 2007;40(2):116-28. , 1212. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8. , 2020. Santos MJD, Moret ALM, Lamônica DA, Costa AO, Bevilacqua MC. Cochlear implants in children with cerebral palsy. In: Nikolopoulos TP, editor. Proceedings of the 10th European Symposium on Paediatric Cochlear Implantation; 2011 May 12-15; Athenas, Greece. Bologna: Medimond; 2011. p. 135-40. ), due to the interference of the involved motor aspects. Other studies( 1616. Edwards LC. Children with cochlear implants and complex needs: a review of outcome research and psychological practice. J Deaf Stud Deaf Educ. 2007;12(3):258-68. , 1717. Santos MJD, Bevilacqua MC, Moret ALM, Lamônica DAC, Costa OA, Yamaguti EH. Indication process of cochlear implant for a child with cerebral palsy: a case report. Rev Soc Bras Fonoaudiol. 2011;16(4):474-8. , 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. ) that analyzed the progress of CI use among children with CP and/or multiple disabilities did not indicate a relationship between the hearing and language performance and age at which children underwent CI, unlike what can be observed in studies that focus on the progress of CI use among children with no associated disabilities. This should be further analyzed due to the several variables involved, when it comes to populations with multiple disabilities.

According to some studies( 55. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62. , 99. Hadders-Algra A, Mijna MD. General movement: a window for early identification of children at high risk for developmental disorders. J Pediatrics. 2004;145(2):12-8. ), the development trajectory is determined by complex interactions between biological, psychosocial, and environmental factors and, to know the profile of childhood development, it is necessary to verify the variables that interfere in this process.

The social environment also favors language development, that is, if family or other social environments integrate in daily and social life activities of the children, requiring elaborate linguistic contents, the children will have chances of not only acquiring verbal skills, but also expanding their linguistic structures, thus becoming, according to their capacity, effective communicators. All the participants in this study attended school, and those in G1 and G2 also attended therapeutic activities, involving the development of linguistic and communicational skills. Therefore, we cannot deny the influence of sensory loss on the acquisition of linguistic skills, even for children in G1, who participated in stimulation programs since early childhood.

A noteworthy aspect pertaining to CBO is that children with CP without HI (G2) presented more developed communicational behaviors than those with CP and HI (G1) (Table 3). We can infer that individuals in G1, even after participating in early intervention programs addressing motor and linguistic aspects, were influenced by their hearing conditions, time of sensory privation, time of implant surgery, and hearing rehabilitation, besides other variables, such as individual characteristics, maturation, motivation, and family and school environment, involved in the language acquisition process, as shown in literature( 1212. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8. , 2222. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52. , 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. , 2525. Geers AE. Techniques for assessing auditory speech perception and lipreading enhancement in young deaf children. Volta Review. 1994;96(5):85-96. ). Studies also reported restricted oral language development among children with HL and CP or other motor function changes( 1212. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8. , 1313. Özdemir S, Tuncer Ü, Tarkan O, Kirog?lu M, Çetik F, Akar F. Factors contributing to limited or non-use in the cochlear implant systems in children: 11 years experience. Int J Pediatr Otorhinolaryngol. 2013;77(3):407-9. , 1515. Bacciu A, Pasanisi E, Vincenti V, Ormitti F, Di Lella F, Guida M, et al. Cochlear implantation in children with cerebral palsy. A preliminary report. Int J Pediatr Otorhinolaryngol. 2009;73(5):717-21. , 1616. Edwards LC. Children with cochlear implants and complex needs: a review of outcome research and psychological practice. J Deaf Stud Deaf Educ. 2007;12(3):258-68. , 1818. Meinzen-Derr J, Wiley S, Grether S, Choo DI. Children with cochlear implants and developmental disabilities: a language skills with developmentally matched hearing peers. Res Dev Disabil. 2011;32(2):757-67.

19. Wiley S, Jahnke M, Meinzen-Derr J, Choo D. Perceived qualitative benefits of cochlear implants in children with multi-handicaps. Int J Pediatr Otorhinolayngol. 2005;69(6):791-8.
- 2020. Santos MJD, Moret ALM, Lamônica DA, Costa AO, Bevilacqua MC. Cochlear implants in children with cerebral palsy. In: Nikolopoulos TP, editor. Proceedings of the 10th European Symposium on Paediatric Cochlear Implantation; 2011 May 12-15; Athenas, Greece. Bologna: Medimond; 2011. p. 135-40. , 2222. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52. , 2323. Santos MJD. Cochlear implant in children with cerebral palsy [dissertação]. Bauru: Universidade de São Paulo; 2012. ).

Besides hearing and motor privation factors, it is also important that no child presented with intellectual changes; therefore, the development of language skills is observed, even if slowly, for children using CI. Other researchers have reported the same( 1919. Wiley S, Jahnke M, Meinzen-Derr J, Choo D. Perceived qualitative benefits of cochlear implants in children with multi-handicaps. Int J Pediatr Otorhinolayngol. 2005;69(6):791-8.

20. Santos MJD, Moret ALM, Lamônica DA, Costa AO, Bevilacqua MC. Cochlear implants in children with cerebral palsy. In: Nikolopoulos TP, editor. Proceedings of the 10th European Symposium on Paediatric Cochlear Implantation; 2011 May 12-15; Athenas, Greece. Bologna: Medimond; 2011. p. 135-40.

21. Steven RA, Green KM, Broomfield SJ, Henderson LA, Ramsden RT, Bruce IA. Cochlear implantation in children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 2011;75(11):1427-30.

22. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52.

23. Santos MJD. Cochlear implant in children with cerebral palsy [dissertação]. Bauru: Universidade de São Paulo; 2012.
- 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. ). A study( 1818. Meinzen-Derr J, Wiley S, Grether S, Choo DI. Children with cochlear implants and developmental disabilities: a language skills with developmentally matched hearing peers. Res Dev Disabil. 2011;32(2):757-67. ) presented that cognitive skills, especially nonverbal ones, for individuals with HI and associated disabilities, should always be evaluated once they show language levels that are disproportional to their nonverbal cognitive skills or their cognitive potential.

Cognitive function( 44. Pirila S, van der Meere J, Pentikainen T, Ruusu-Niemi P, Korpela R, Kilpinen J, et al. Language and motor speech skill in children with cerebral palsy. J Commun Disord. 2007;40(2):116-28.

5. Lamônica DAC, Ferraz PMDP. Leucomalácia periventricular e diplegia espástica: implicações nas habilidades psicolingüísticas. Pró-Fono R Atual Cient. 2007;19(4):357-62.
- 66. Aisen MLI, Kerkovickd D, Mast J, Mulroy S, Wren TA, Kay RM, et al. Cerebral palsy: clinical care and neurological rehabilitation. Lancet Neurol. 2011;10(9):844-52. , 2222. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52. ) and functionality in other fields of development should be taken into account during rehabilitation and follow-up of children with CP using CI( 1818. Meinzen-Derr J, Wiley S, Grether S, Choo DI. Children with cochlear implants and developmental disabilities: a language skills with developmentally matched hearing peers. Res Dev Disabil. 2011;32(2):757-67. , 2121. Steven RA, Green KM, Broomfield SJ, Henderson LA, Ramsden RT, Bruce IA. Cochlear implantation in children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 2011;75(11):1427-30. , 2222. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52. , 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. , 3030. Shelly A, Jahnke M, Meinzen-Derr J, Choo D. The relationship between quality of life and functioning for children with cerebral palsy. Dev Med Child Neurol. 2008;50(3):199-203. ), including in the evaluations to indicate CI( 2020. Santos MJD, Moret ALM, Lamônica DA, Costa AO, Bevilacqua MC. Cochlear implants in children with cerebral palsy. In: Nikolopoulos TP, editor. Proceedings of the 10th European Symposium on Paediatric Cochlear Implantation; 2011 May 12-15; Athenas, Greece. Bologna: Medimond; 2011. p. 135-40. ).

One interesting finding of this study was the performance of groups concerning personal-social function. In the DDST-II, the personal-social score assesses reactions of the child in response to stimuli from social environment as compared to the independent performance of daily and concrete tasks, involving organization of, and response to stimuli; social skill; and understanding of the context. HI interferes in the development of verbal communicative skills, affecting social functions. However, such damage was not relevant to limit the social activity in G1. We can infer that this can be attributed to the intellectual skills and benefits derived from CI, which has the objective of establishing contact with the world of sound, thus proportioning the development of hearing and linguistic skills for communication, even if slowly. Also, after the child with CP receives the benefit of speech perception by CI, the child starts presenting receptive language. These skills are sufficient and useful in enabling the child communicate and interact with the environment, which is essential for the development of personal-social function and implies social involvement( 2121. Steven RA, Green KM, Broomfield SJ, Henderson LA, Ramsden RT, Bruce IA. Cochlear implantation in children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 2011;75(11):1427-30. , 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. ), which also implies improved quality of life. Another explanation for this result can be related to the participation in therapeutic processes and school life.

Studies showed that the possibility of reciprocal social relations may have a positive effect on the learning process in general and on the quality of life of people who have severe motor disorders. This is because if the individual is inserted in a social community effectively, his or her interaction, integration, and learning is notably high, as well as quality of life that is observed among individuals with or without severe motor disorders( 2929. Albrecht GL, Devlieger PJ: The disability paradox: high quality of life against all odds. Soc Sci Med. 1999;48(8):977-88. , 3030. Shelly A, Jahnke M, Meinzen-Derr J, Choo D. The relationship between quality of life and functioning for children with cerebral palsy. Dev Med Child Neurol. 2008;50(3):199-203. ).

CI was found to be a proper treatment for HI among children with CP, helping in the development of hearing and language skills that provide ways to interact and communicate with the social environment( 1212. Daneshi A, Hassanzadeh S. Cochlear implantation in prelingually deaf persons with additional disability. J Laryngol Otol. 2007;121(7):635-8. , 1313. Özdemir S, Tuncer Ü, Tarkan O, Kirog?lu M, Çetik F, Akar F. Factors contributing to limited or non-use in the cochlear implant systems in children: 11 years experience. Int J Pediatr Otorhinolaryngol. 2013;77(3):407-9. , 1616. Edwards LC. Children with cochlear implants and complex needs: a review of outcome research and psychological practice. J Deaf Stud Deaf Educ. 2007;12(3):258-68. , 1717. Santos MJD, Bevilacqua MC, Moret ALM, Lamônica DAC, Costa OA, Yamaguti EH. Indication process of cochlear implant for a child with cerebral palsy: a case report. Rev Soc Bras Fonoaudiol. 2011;16(4):474-8. , 2121. Steven RA, Green KM, Broomfield SJ, Henderson LA, Ramsden RT, Bruce IA. Cochlear implantation in children with cerebral palsy. Int J Pediatr Otorhinolaryngol. 2011;75(11):1427-30.

22. Birman CS, Elliott EJ, Gibson WPR. Pediatric Cochlear Implants: additional disabilities, prevalence, risk factors, and effect on language outcomes. Otol Neurotol. 2012;33(8):1347-52.

23. Santos MJD. Cochlear implant in children with cerebral palsy [dissertação]. Bauru: Universidade de São Paulo; 2012.
- 2424. Moret AL, Bevilacqua MC, Costa AC. Cochlear implant: hearing and language in pre-lingual deaf children. Pró-Fono R Atual Cient. 2007;19(3):295-304. ). Longitudinal follow-ups involving more individuals with CP who use CI are necessary to know the trajectory of the global development of these children.

Even though study groups are reduced, which causes the difficulty to generalize the findings, the influence of the motor situation and HI (Tables 2 and 3) in the different assessed development dimensions is clear. This leads to reflections about the importance of diagnosing and intervening earlier, with the objective of improving the quality of life of people with CP with and without other comorbidities.

CONCLUSION

In the comparison between groups of individuals with CP and the control group, the influence of motor and hearing changes on the development of the assessed skills was observed. G1 presented slower development in relation to the other groups in all the areas, especially in communicative language and behaviors. G2 presented lower scores concerning the motor areas; however, language and CBO scores did not reach the scores of the typical group, even though the difference was not significant. Social skills were also low in groups with CP; however, the difference between the development of this function in relation to the control group (G3) was not significant.

ACKNOWLEDGMENTS

Special thanks (in memoriam) to Prof. Dr. Maria Cecília Bevilacqua, who contributed with this study by analyzing data and written content. This article contains data from two master's studies: one of them was undertaken by Dr. Dionísia Lamônica, and the other one by Dr. Maria Cecília Bevilacqua.

Thanks to the São Paulo Research Foundation, which supported two master's projects that resulted in this study(processes no 2010/03202-5 and 2011/03482-0).

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  • Financial support: São Paulo Research Foundation (FAPESP).
  • Study carried out at the Center of Audiology Studies, Rehabilitation Hospital of Craniofacial Anomalies, Universidade de São Paulo- USP and the Speech Language Pathology and Audiology Department at the Dental School of Bauru, Universidade de São Paulo - USP - Bauru (SP), Brazil.
  • *
    DACL contributed with data analysis and writing the manuscript; MJDS and CSTP contributed by collecting data from the study participants, with data analysis and writing the manuscript; LNTS contributed with data analysis and writing the manuscript.

Publication Dates

  • Publication in this collection
    June 2014

History

  • Received
    25 Aug 2013
  • Accepted
    21 May 2014
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