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Developmental Profiles and Temperament Patterns in Children With Spastic Cerebral Palsy: Relationships With Subtypes and Severity
J Formos Med Assoc 2011;110(8):527–536
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Volume 110 Number 8 August 2011
Journal of the Formosan Medical Association
ISSN 0929 6646
Journal of the
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Formosan Medical Association Taipei, Taiwan
Original Article
Developmental Profiles and Temperament Patterns in Children With Spastic Cerebral Palsy: Relationships With Subtypes and Severity Chia-Ling Chen,1,6 Keh Chung Lin,2 Ching-Yi Wu,3 Chia-Hui Chen,1 Wen-Yu Liu,1 Chung-Yao Chen4,5* Background/Purpose: Elucidating developmental profiles and temperament patterns in children with cerebral palsy (CP) could help clinicians elaborate more flexible strategies for treating these children. This study investigated the developmental profiles and temperament patterns in children with spastic CP (sCP) of different subtypes and severities. Methods: One hundred and five children, aged 3–6 years, with sCP and 66 children with typical development (TD) were analyzed. Children with sCP were classified into spastic diplegia (SD; n = 60), and spastic quadriplegia (SQ; n = 45) groups. Motor severity was classified via the Gross Motor Function Classification System (GMFCS). Development quotients (DQs) of eight domains and temperament scores of nine dimensions were evaluated. Results: The SQ group had lower DQs in all developmental functions than the SD group (p < 0.01). The DQ distributions of developmental profiles showed the same trend in SD and SQ groups, and both groups displayed lowest DQs in the gross motor domain. The SQ group was less adaptable and approachable than the TD group (p < 0.05), and both sCP groups had lower attention span and persistence and a higher threshold of responsiveness than the TD group (p < 0.05). Correlation analysis showed that GMFCS levels were highly related to all developmental functions (r < −0.54, p < 0.01) and weakly related to some temperament dimensions in children with sCP. Conclusion: The subtype and severity of sCP were associated with developmental profiles in children with sCP. Temperament patterns were different between SD and SQ groups, but only weakly related to motor deficit. These data could allow clinicians to anticipate the developmental profiles and temperament patterns and plan appropriate therapeutic strategies for children with sCP. Key Words: assessment, cerebral palsy, developmental function, outcome, temperament
©2011 Elsevier & Formosan Medical Association .
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Graduate Institute of Early Intervention, Department of Physical Therapy, 3Graduate Institute of Clinical Behavioral Science, Department of Occupational Therapy and 5Department of Physical Therapy, College of Medicine, Chang Gung University, Taoyuan, 2Graduate Institute of Occupational Therapy, College of Medicine, National Taiwan University, Taipei, 4Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Keelung, and 6Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Linkou, Taiwan. Received: April 7, 2010 Revised: May 7, 2010 Accepted: July 5, 2010
*Correspondence to: Dr Chung-Yao Chen, Department of Rehabilitation Medicine, Chang Gung Memorial Hospital, 222, Maijin Road, Anle District, Keelung City 204, Taiwan. E-mail: [email protected]
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Even newborn babies display observable emotional and behavioral styles. Each child has peculiar and innate traits. Individual differences in traits during childhood and adolescence are described as temperament or personality traits.1 Temperament is inherited and emerges early in life and stabilizes during development.2 Personality is a developmental outcome and can change throughout a lifetime.3 Temperament and personality are influenced by genetic and complex environmental factors,4,5 such as parenting skills,6 or parental marital status.7 Therefore, temperament is influenced over time by genetic inheritance, maturation and experience.1,3 Interactions occur between temperament traits and child development. Temperament, although stable, is not static.8 Previous studies have revealed significant relationships between temperament and developmental stage from infancy to middle childhood,9 and from childhood to early adulthood.10,11 Individual temperamental differences are largely determined by biological factors. However, child behavior is modified as the nervous system matures and self-regulatory and cognitive skills develop. Studies have found that temperamental differences can affect the emotions, behavior and development of children, including their exploration, discovery and learning processes.1,12 Cerebral palsy (CP) describes a group of disorders of the development of movement and posture causing activity limitation, that are attributed to non-progressive disturbances that occur in the developing fetus or infant brain.13 Spastic CP (sCP), the most common type, is further classified on the topographic distribution of the body affected, such as spastic hemiplegia, spastic diplegia (SD) and spastic quadriplegia (SQ).14,15 Children with sCP are likely to have more difficulties in development of cognition, learning, speech, social skills and motor functions, possibly influencing their behavior and ability to express emotion appropriately. Ross16 has reported that preterm infants diagnosed with CP are often less adaptable, less persistent and more withdrawn from new stimulation. 528
Therapy for children with CP is focused on underlying functional impairments. Elucidating developmental profiles and temperament patterns in children with CP might help clinicians improve the relationship between clinicians and children, understand developmental problems, and elaborate more flexible strategies for treating children with different developmental profiles and temperament patterns.12 Temperament is associated with motor development,17 and neurodevelopmental functions.18 Bayley scores are correlated with temperament scores in premature infants16,18 and normal infants.19 The temperament continues to influence the development of children during their school-age years.20 The neurodevelopmental variations in children with CP with different subtypes and motor severities, associated with various types of brain damage, might cause potential differences in development and temperament. However, few researchers have studied developmental profiles and temperament patterns in children with sCP, who have various CP subtypes or motor severity. In this study, we hypothesized that developmental profiles and temperament patterns vary in children with sCP with different CP subtypes and severity. This study investigated the developmental profiles and temperament patterns in children with SD or SQ.
Materials and Methods Participants The study population included children with sCP treated in the Department of Physical Medicine and Rehabilitation at Chang Gung Memorial Hospital from September 2001 to November 2005. Inclusion criteria were CP with SD or SQ, and age 3–6 years. SD is defined as motor disability involving primarily lower extremities, with upper motor neuron signs in the lower limbs.15 SQ is defined as massive total motor disability involving all four limbs and trunk, with upper motor neuron signs in all limbs.15 Exclusion criteria were any of the following during the previous 3 months: (1) significant J Formos Med Assoc | 2011 • Vol 110 • No 8
Development and temperament in cerebral palsy
medical problems such as active pneumonia or urinary tract infection; (2) progressive neurological disorder; (3) any major surgical treatment such as orthopedic surgery or neurosurgery; (4) any treatment with nerve or motor point block such as a botulinum toxin injection; and (5) any dental procedure such as tooth extraction. Finally, 105 children with sCP were enrolled. These children were classified into two groups based on the topographic distribution of limb involvement: SD (n = 60), and SQ (n = 45). Another 66 age- and sex-matched children with typical development (TD) were selected as a control group. The study was approved by the Human Ethics Committee at this hospital. All participants’ parents/caregivers gave informed consent. All children underwent assessment of developmental profiles, temperament patterns, and motor severity. Developmental profiles were assessed using Chinese Child Development Inventory (CCDI),21 a Chinese revision of the Minnesota Child Development Inventory.22 The CCDI has been widely used to assess developmental profiles in children with developmental delay in Taiwan.23 The CCDI, a 320-item questionnaire, consists of statements describing child behavior, to which parents/caregivers were asked to answer “yes” or “no” if the child had or had not ever exhibited the specified behavior. The scoring process yielded age equivalents in eight domains of developmental function. These eight domains included gross motor (GM, 34 items), fine motor (FM, 44 items), expressive language (EL, 54 items), concept comprehension (CC, 67 items), situation comprehension (SC, 44 items), self help (SH, 36 items), personal social (PS, 34 items), and general development (GD, 131 items). The GD domains integrated seven items and 124 items from the other seven domains. The validity and reliability of the CCDI were > 0.83 and > 0.88, respectively.21 The development quotient (DQ) was determined as a percentage of developmental age divided by chronological age. The Chinese version of Childhood Temperament Inventory (CCTI),24 originally developed by Thomas and Chess,25 was used to assess J Formos Med Assoc | 2011 • Vol 110 • No 8
temperament patterns. The CCTI consisted of 72 items that described particular behavior in a variety of situations. The parents/caregivers were asked to rate the frequency of their children’s behavior on a seven-point scale from 1 (never) to 7 (always). The 72 items, eight in each dimension, were classified into nine dimensions of temperament: (1) activity level, with high scores indicating high activity level; (2) rhythmicity, with high scores indicating high regularity; (3) approach–withdrawal, with high scores meaning high willingness to approach new stimuli; (4) adaptability, with high scores indicating high adaptability; (5) attention span and persistence, with high scores indicating more persistence; (6) distractibility, with high scores indicating high degree of distraction; (7) threshold of responsiveness, with high scores indicating high threshold; (8) intensity of reaction, with high scores indicating high intensity of reaction; (9) mood pattern, with high scores indicating more positive mood. The average score in each dimension was calculated as the average score of corresponding items. The Gross Motor Function Classification System (GMFCS)26 was used to measure motor severity of sCP. The same physiatrist, one of the authors, assessed the GMFCS levels of children with sCP. The GMFCS graded the self-initiated movement of sCP patients with particular emphasis on their functional abilities (sitting, crawling, standing and walking) and their need for assistive devices (e.g. walkers, crutches and canes) and wheeled mobility. The GMFCS used a fivepoint scale (I–V) from “independent” (level I) to “dependent” (level V). The clinical data, including associated comorbidity, current usage of medication, and family environments of children with CP were analyzed. The associated comorbidity included epilepsy, mental retardation, attention deficit/hyperactivity disorder, autism, and visual and hearing problems. Current usage of medication consisted of anticonvulsants, antispasticity medication, and central nervous system medication, such as ritalinlike stimulants, piracetam, and clonidine, were recorded. The family environments included 529
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family’s economic status and parents’ educational levels. The family’s economic status was categorized into three grades: low, < NT$370,000 per year; middle, NT$370,000–NT$990,000 per year; and high, > NT$990,000 per year. The parents’ educational levels were categorized into three grades: low, less than high school; middle, high school; and high, university or higher. The higher educational status of parents was selected for data analysis. In addition, the demographic data, including age and sex, of all children were also recorded.
Statistical analysis Group differences in continuous data (age and temperament scores) among two sCP groups and TD group were compared by analysis of variance test with post hoc Tukey multiple comparisons. Group differences in developmental profile (all DQs) between two sCP groups were compared with an independent t test. Group differences in sex and clinical data were determined by the χ2 test. The Mann–Whitney test was used to determine group differences in the family data and severity of GMFCS levels. Pearson correlation was used to determine the relations among severity, developmental profiles and temperament patterns. A p value < 0.05 was considered statistically significant.
Results The three groups did not significantly differ in age and sex (Table 1). The parents’ educational levels and family’s economic status did not differ between both CP groups (Table 1). The SQ group was associated with higher incidences of epilepsy and mental retardation, and currently used more medication than did the SD group (p < 0.001) (Table 1). However, the associated comorbidity of attention deficit/hyperactivity disorder, autism, and hearing and visual problems did not differ between both CP groups. The SD group had better GMFCS levels than the SQ group had (p < 0.001) (Table 1). Approximately 95% of children in the 530
SD group were GMFCS levels I and II. However, 60% of children in the SQ group had a GMFCS level above II (Table 1). The SQ group had lower DQs in all developmental functions than the SD group had (p < 0.01) (Table 1). The DQ distribution pattern of developmental profiles showed the same trend in the SD and SQ groups, and both groups displayed lowest DQs in the GM domain (Figure 1). The largest difference between the two groups was found in the FM domain (38%). By contrast, the smallest difference occurred in the GM domain (25%). The DQs of other developmental functions were 63–82% in the SD group, whereas those were 37–56% in the SQ group (Figure 1). Temperament patterns were different between the sCP and TD groups (Figure 2). Both SQ and SD groups had lower attention span and persistence, and a higher threshold of responsiveness than the TD group had (p < 0.05) (Figure 2). The SQ group was less approachable than the TD group was (p < 0.05) (Figure 2). Furthermore, the SQ group had lower adaptability than the TD and SD groups had (p < 0.01) (Figure 2). Pearson correlation analysis indicated that GMFCS levels were highly and negatively correlated with all DQs (r = −0.54 to −0.76, p < 0.01, Table 2). GMFCS levels were weakly, although still significantly, correlated with some temperament patterns (Table 2). The significant correlation between DQs and temperament patterns were mostly weak, except for the relationship between the threshold of responsiveness and DQs (r = −0.20 to −0.44, p < 0.05, Table 2).
Discussion Our results suggest that the severity of motor deficits was associated with the developmental profiles, but not the temperament patterns. Different subtypes of sCP demonstrated some unique temperament patterns and developmental profiles. The differences between the two groups of children with CP could have been due to the motor J Formos Med Assoc | 2011 • Vol 110 • No 8
Development and temperament in cerebral palsy
Table 1. Demographic, family and clinical data and motor severity in children with spastic bilateral cerebral palsy, and demographic data from children with typical developmenta Children with CP (n = 105)
Demographic Age (yr)c Sex, maleb Family Parents’ educational level Low: below high school Middle: high school High: university or higher Family’s economic status (NT$ /yr) Low: < 370,000 Middle: 370,000–990,000 High: > 990,000 Clinical Associated comorbidity Epilepsy Attention deficit/hyperactivity disorder Autism Mental retardation Hearing impairment Vision impairment Current medication usage GMFCS levelsb Level I Level II Level III Level IV Level V
Diplegia (n = 60)
Quadriplegia (n = 45)
4.9 ± 1.5 42 (70.0)
4.7 ± 2.1 25 (55.6)
7 (11.7) 26 (43.3) 27 (45.0)
6 (13.3) 23 (51.1) 16 (35.6)
13 (21.7) 38 (63.3) 9 (15.0)
11 (24.4) 31 (68.9) 3 (6.7)
3 (5.0) 10 (16.7) 4 (6.7) 11 (18.3) 0 (0) 16 (26.7) 8 (13.3)
14 (31.1) 5 (11.1) 1 (2.2) 31 (68.9) 3 (6.7) 15 (33.3) 15 (33.3)
Children with TD (n = 66)
4.7 ± 1.1 39 (59.1)
p
0.730 0.418
0.622
0.438
< 0.001 0.575 0.389 < 0.001 0.076 0.459 0.014 < 0.001
43 (71.7) 14 (23.3) 3 (5.0) 0 (0) 0 (0)
0 (0) 17 (37.8) 13 (28.9) 7 (15.6) 8 (17.8)
Data are presented as mean ± standard deviation or n (%); bc2 or Mann–Whitney tests for categorical data; cone-way analysis of variance test with post hoc Tukey multiple comparisons for continuous data. CP = cerebral palsy; TD = typical development; GMFCS = Gross Motor Function Classification System.
a
functions, cognitive functions, language skills, or their interactions. However, CP subtypes and motor severity, not developmental functions, were selected in this study for predicting the temperament patterns and developmental profiles, for several reasons. First, the CP subtypes can reflect underlying brain damage,14 in addition to the involved body parts and functional level. For example, children with SQ CP often have associated severe intraventricular hemorrhage and periventricular leukomalacia.14 Accordingly, children J Formos Med Assoc | 2011 • Vol 110 • No 8
with SQ were more severely involved than those with SD in gross motor function as well as in other domains of development. Second, the CP subtype and motor severity are classified quickly and easily (within 5 minutes) by clinicians. However, various developmental functions are evaluated by multidisciplinary assessments. The professionals need a lot of time (1 hour on average for each disciplinary assessment) to assess developmental functions, such as cognition and speech functions. Third, the developmental functions are 531
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100 Developmental quotient (%)
* *
80
*
* *
*
* 60 * 40
Diplegia
20
Quadriplegia 0 GM
FM
EL CC SC SH Chinese child development inventory
PS
GD
Figure 1. Developmental quotient measured by Chinese Child Development Inventory in children with cerebral palsy. *p < 0.01 (independent t test). GM = gross motor; FM = fine motor; EL = expressive language; CC = concept comprehension; SC = situation comprehension; SH = self help; PS = personal social development; GD = general development. 5.5
BN* AB*
Diplegia Quadriplegia Normal
Average score
5.0 BN† AN† BN*
4.5
AN† BN*
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Chinese childhood temperament inventory Figure 2. Average score of Chinese Childhood Temperament Inventory in children with cerebral palsy and children with typical development (TD). AN: significant differences between SD and TD groups; BN: significant differences between SQ and TD groups; AB: significant differences between SD and SQ groups (One-way analysis of variance test with post hoc Tukey multiple comparisons). *p < 0.01, †p < 0.05.
selected as the dependent variables. Fourth, all developmental functions are correlated with each other. Temperament pattern can be influenced by biological and environmental factors, as well as by their interactions. The motor and non-motor functions affect temperament patterns and developmental profiles in children with CP. For example, children’s cognitive, speech, and personal–social 532
development could influence their temperament. Comorbidity and current use of medication, such as anticonvulsants, central nervous system medications, and anti-spasticity medications, might modify temperament patterns and developmental profiles. In this study, children with SQ CP currently used more medication and were associated with higher incidences of comorbidity, such as epilepsy and mental retardation, than those J Formos Med Assoc | 2011 • Vol 110 • No 8
Development and temperament in cerebral palsy
Table 2. Pearson correlations of motor severity, developmental profiles and temperament patterns in children with spastic bilateral cerebral palsy Motor severity GMFCS levels Motor severity GMFCS levels Temperament patterns Activity level Rhythmicity (Regularity) Approach/withdrawal Adaptability Intensity of reaction Quality of mood Attention span & persistence Distractibility Threshold of responsiveness
Developmental profiles
GM
FM
EL
CC
SC
SH
PS
GD
–0.758** –0.715** –0.565** –0.541** –0.661** –0.754** –0.641** –0.681**
–0.102 0.022 –0.241* –0.329** –0.050 –0.106 –0.023
0.158 –0.125 0.111 0.252** 0.143 0.062 0.141
–0.076 –0.089 ** –0.205* 0.292
–0.082 –0.014
–0.114 0.026
0.123 0.293** 0.206* 0.041 0.276**
0.129 0.285** 0.152 0.096 0.226*
–0.160 0.071 0.189 0.290** 0.132 0.119 0.280**
–0.073 0.034 0.203* 0.347** 0.136 0.104 0.244*
0.007 –0.032 0.119 0.306** 0.122 0.041 0.203*
–0.089 0.049 0.111 0.281** 0.132 0.069 0.244*
–0.075 0.031 0.158 0.305** 0.166 0.094 0.260**
0.027 0.121 0.120 0.052 0.001 0.088 0.076 ** ** ** ** ** ** –0.387 –0.396 –0.421 –0.444 –0.317 –0.351 –0.412**
*p < 0.05; **p < 0.01. GMFCS = Gross Motor Function Classification System; GM = gross motor; FM = fine motor; EL = expressive language; CC = concept comprehension; SC = situation comprehension; SH = self help; PS = personal social development; GD = general development.
with SD CP. The SD group had better cognition, speech, personal–social functions and GMFCS levels than the SQ group had. However, the family factors did not differ between both CP groups. These findings suggest that the differences in the developmental profile and temperament pattern between SD and SQ groups actually resulted from brain damage, which causes various motor functions and CP subtypes. The motor impairment of sCP was related to developmental profiles in children with sCP. In other words, children with sCP and worse GMFCS levels had more motor, cognition, speech, personal–social, and self-care impairments than those with sCP and better GMFCS levels. Children with CP, especially those with poor GMFCS levels, often demonstrate developmental disabilities in multiple domains, such as cognition, speech, and behavior. Children’s functional impairments in cognition, speech, personal–social, and self-care might also be influenced by nonmotor comorbidity. Our results showed that the J Formos Med Assoc | 2011 • Vol 110 • No 8
SD group had better GMFCS levels than the SQ group had. The differences in the developmental profile between the SD and SQ groups might actually reflect the deviations between different motor functions, rather than CP subtypes. Furthermore, children with sCP with greater motor impairment also have greater disability to explore their environment, learn new strategies, interact socially and perform self-care functions. These could be the reasons why GMFCS was highly correlated with developmental profiles. Previous studies also have suggested that GMFCS predicts motor change in children with CP,27 and motor impairments predict gross motor function and everyday activities.28 Therefore, using GMFCS level rather than CP subtype might provide more useful information for understanding variations in developmental profiles in children with CP. Different sCP subtypes with particular pathophysiology29,30 demonstrate different developmental profiles. In the present study, children with SQ had lower DQs in all developmental 533
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functions than those with SD, and both groups displayed lowest DQs in the GM domain. In premature infants, SD, often associated with white matter disorder, is the dominant form of CP.29 In the SD group, the major delay in CCDI was GM domain, and DQs in the other domains were all > 60%, as compared to those in normal children. The DQ in the GD domain was nearly 80% in the SD group. Besides, the largest difference in developmental profiles between the SD and SQ groups was found in the FM domain. The selectively legs dysfunction and relatively preserved hand and cognitive function in the SD group might be the reasons for these findings. Children with SQ often had a difficult delivery with evidence of perinatal asphyxia or brain anomalies, and have a high percentage of mental retardation.15,31,32 Significant cognitive involvement in children with SQ might be the important cofactor, along with motor impairment, of why differences in language and comprehension domains were larger between the SD and SQ groups than differences in the GM domain. Temperament patterns vary among children with different CP subtypes. In the present study, children with SQ were less adaptable and approachable than were normal children, which was not found in the SD group. Besides, children with SQ were less adaptable than were children with SD. Koeda also has suggested that children with CP have lower adaptability than normal children have.33 Was the motor impairment of sCP the major reason for the difference? Although the GMFCS levels were significantly correlated with the approach and the adaptability, the different GMFCS levels could explain < 10% of the variability (coefficient of determination < 0.1) in approach and adaptability. The relatively large sample size (n = 105) might be the reason for this weak but significant correlation. Previous studies also have found poorer performance on the Bayley Mental Scales in preterm infants, who were diagnosed with CP later, and 1-year outcome was significantly associated with temperament characteristics of lower adaptability, and more withdrawal from new stimulation.16 Therefore, we 534
can speculate that cognitive impairments play a more important role than motor impairment for less adaptable and approachable children in the SQ group. Children learn different self-regulatory strategies for responding to external stimuli as cognition develops. Flexible and adaptable innate traits in regulatory processes can enhance responsiveness in individual and external contexts.34 Therefore, strategies to improve adaptability and approachability, such as selecting the same treatment room to allow these children to be more adaptable to the environment, and more personal social interaction programs, should be considered in planning therapeutic programs for children with SQ CP. Programs that use a high intensity of stimulation are proposed when treating children with sCP. The higher the threshold of responsiveness, the more difficulty children have in shifting and focusing their attention. The threshold of responsiveness is related to the level of stimulation, such as sensory stimuli, environmental objects, and social contacts. In the present study, children with sCP had a higher threshold of responsiveness that adversely affected the regulatory processes to the external environment, which further impeded development. Given that the GMFCS levels were weakly correlated with the threshold of responsiveness, and could explain < 10% of the variability in it, the frequently associated deficits such as cognitive, visual and hearing impairment might have accounted for the higher threshold of responsiveness in children with sCP. Among the different temperament patterns, the threshold of responsiveness was the only one that reached medium correlation (r < −0.4) with the developmental profiles of the CCDI. Therefore, not only the motor deficit, but also the high threshold of responsiveness should be seriously managed when planning therapeutic strategies for children with sCP. Comorbidity such as visual and hearing impairment and visual perception dysfunction should be routinely screened and treated. Sensory integration programs with a high level of stimulation might be offered as part of rehabilitative strategies. J Formos Med Assoc | 2011 • Vol 110 • No 8
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Rehabilitative programs with multiple shortduration sessions are suggested when treating children with sCP. In the present study, sCP groups had lower attention span and persistence than the TD group had, but the distractibility did not differ between the two groups. Attention function is a filter of perceptual–cognitive activity. Suslow et al have found that attention is highly related to cognition and social interaction.35 In the present study, the findings that motor impairment was not correlated with persistence and distractibility support their results that attention is highly related to cognition. The reason why distractibility did not differ between the sCP and TD groups might be related to the high threshold of responsiveness found in children with sCP. Therefore, the learning and cognitive processes in children with sCP cannot be sustained for a long period, even though they are not easily distracted by external stimuli. Treatment programs with higher stimulation intensity and shorter duration are suggested for children with sCP. There were several limitations in our study. We only recruited children with SD and SQ. Therefore, our results cannot be generalized to CP with other subtypes, such as spastic hemiplegic or dyskinetic types. The associated deficits commonly found in children with CP, such as mental retardation, visual and hearing perception deficits, were not thoroughly evaluated by subspecialists or formal evaluation tools. In fact, it is difficult to evaluate precisely these associated deficits with confidence in children at these young ages. Therefore, these possible covariates could not be further analyzed. Social and parental factors were also important for children’s development. Children under early intervention therapy at medical centers often have parents with higher socioeconomic and well-educated status. Therefore, our results might have been different if participants had been recruited from children with sCP who were not receiving treatment. In conclusion, the severity of motor deficit was highly related to all developmental functions and weakly related to some temperament dimensions in children with sCP. Among temperament J Formos Med Assoc | 2011 • Vol 110 • No 8
dimensions, only threshold of responsiveness reached medium correlation with developmental profiles in children with sCP. Developmental profiles and temperament patterns varied among children with different subtypes of sCP. The data provided in the present study might allow clinicians to anticipate the developmental profiles and temperament patterns and plan appropriate therapeutic strategies for children with sCP.
Acknowledgment The authors would like to thank the Health Administration of Executive Yuan, Taiwan, for financially supporting this research under Contract No. GMRPG360101.
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10. Chess S, Thomas A. Temperamental individuality from childhood to adolescence. J Am Acad Child Psychiatry 1977;16:218–26. 11. Chess S, Thomas A. The New York Longitudinal Study (NYLS): the young adult periods. Can J Psychiatry 1990; 35:557–61. 12. Rothbart MK, Jones LB. Temperament, self-regulation, and education. School Psych Rev 1998;27:479–91. 13. Rosenbaum P, Paneth N, Leviton A, et al. A report: the definition and classification of cerebral palsy April 2006. Dev Med Child Neurol Suppl 2007;109:8–14. 14. Jones MW, Morgan E, Shelton JE, et al. Cerebral palsy: introduction and diagnosis (part I). J Pediatr Health Care 2007;21:146–52. 15. Matthews DJ, Wilson P. Cerebral palsy. In: Molnar GE, Alexander MA, eds. Pediatric Rehabilitation. 3rd edition. Philadelphia: Hanley & Belfus, 1999:193–218. 16. Ross G. Temperament of preterm infants: its relationship to perinatal factors and one-year outcome. J Dev Behav Pediatr 1987;8:106–10. 17. Menzies A. Effect of infant temperament and prone position on motor development. Aust J Adv Nurs 1984;2:24–31. 18. Sajaniemi N, Salokorpi T, von Wendt L. Temperament profiles and their role in neurodevelopmental assessed preterm children at two years of age. Eur Child Adolesc Psychiatry 1998;7:145–52. 19. Sostek AM, Anders TF. Relationships among the Brazelton Neonatal Scale, Bayley Infant Scales, and early temperament. Child Dev 1977;48:320–3. 20. McClowry SG. The influence of temperament on development during middle childhood. J Pediatr Nurs 1995;10: 160–5. 21. Hsu C, Su S, Shao S, et al. Chinese child development inventory: a tentative normative data. Acta Paediatri Sin 1978;19:142–52. 22. Ireton H, Thwing E. The Minnesota Child Development Inventory. Minneapolis, MN: University of Minnesota, 1974.
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23. Chen IC, Chen CL, Wong MK, et al. Clinical analysis of 1048 children with developmental delay. Chang Gung Med J 2002;25:743–50. 24. Hsu CC. Teaching Your Child Based on Temperament. 4th edition. Taipei: Health-World, 2001. 25. Thomas A, Chess S. Temperament and Development. New York: Brunner/Mazel, 1977:18–26. 26. Palisano R, Rosenbaum P, Walter S, et al. Gross motor function classification system for cerebral palsy. Dev Med Child Neurol 1997;39:214–23. 27. Bartlett DJ, Palisano RJ. A multivariate model of determinants of motor change for children with cerebral palsy. Phys Ther 2000;80:598–614. 28. Ostensjo S, Carlberg EB, Vollestad NK. Motor impairments in young children with cerebral palsy: relationship to gross motor function and everyday activities. Dev Med Child Neurol 2004;46:580–9. 29. Nelson KB, Chang T. Is cerebral palsy preventable? Curr Opin Neurol 2008;21:129–35. 30. McQuillen PS, Ferriero DM. Selective vulnerability in the developing central nervous system. Pediatr Neurol 2004; 30:227–35. 31. Okumura A, Hayakawa F, Kato T, et al. MRI findings in patients with spastic cerebral palsy. I: correlation with gestational age at birth. Dev Med Child Neurol 1997;39: 363–8. 32. Okumura A, Kato T, Kuno K, et al. MRI findings in patients with spastic cerebral palsy. II: correlation with type of cerebral palsy. Dev Med Child Neurol 1997;39:369–72. 33. Koeda T. Hypoxic brain damage and higher cortical dysfunction in children. No To Hattatsu 1994;26:137–41. [In Japanese] 34. Derryberry D, Rothbart MK. Reactive and effortful processes in the organization of temperament. Dev Psychopathol 1997;9:633–52. 35. Suslow T, Schonauer K, Arolt V. Attention training in the cognitive rehabilitation of schirozphrenic patients: a review of efficacy studies. Acta Psychiatr Scand 2001;103:15–23.
J Formos Med Assoc | 2011 • Vol 110 • No 8
Contents lists available at ScienceDirect
Volume 110 Number 8 August 2011
Journal of the Formosan Medical Association
ISSN 0929 6646
Journal of the
Formosan Medical Association Resveratrol for prophylaxis of ischemic stroke Microglia and chronic pain ART in HIV-1-discordant couples in Taiwan Prognostic evaluation of patients with multicentric papillary thyroid microcarcinoma
Journal homepage: http://www.jfma-online.com
Formosan Medical Association Taipei, Taiwan
Original Article
Developmental Profiles and Temperament Patterns in Children With Spastic Cerebral Palsy: Relationships With Subtypes and Severity Chia-Ling Chen,1,6 Keh Chung Lin,2 Ching-Yi Wu,3 Chia-Hui Chen,1 Wen-Yu Liu,1 Chung-Yao Chen4,5* Background/Purpose: Elucidating developmental profiles and temperament patterns in children with cerebral palsy (CP) could help clinicians elaborate more flexible strategies for treating these children. This study investigated the developmental profiles and temperament patterns in children with spastic CP (sCP) of different subtypes and severities. Methods: One hundred and five children, aged 3–6 years, with sCP and 66 children with typical development (TD) were analyzed. Children with sCP were classified into spastic diplegia (SD; n = 60), and spastic quadriplegia (SQ; n = 45) groups. Motor severity was classified via the Gross Motor Function Classification System (GMFCS). Development quotients (DQs) of eight domains and temperament scores of nine dimensions were evaluated. Results: The SQ group had lower DQs in all developmental functions than the SD group (p < 0.01). The DQ distributions of developmental profiles showed the same trend in SD and SQ groups, and both groups displayed lowest DQs in the gross motor domain. The SQ group was less adaptable and approachable than the TD group (p < 0.05), and both sCP groups had lower attention span and persistence and a higher threshold of responsiveness than the TD group (p < 0.05). Correlation analysis showed that GMFCS levels were highly related to all developmental functions (r < −0.54, p < 0.01) and weakly related to some temperament dimensions in children with sCP. Conclusion: The subtype and severity of sCP were associated with developmental profiles in children with sCP. Temperament patterns were different between SD and SQ groups, but only weakly related to motor deficit. These data could allow clinicians to anticipate the developmental profiles and temperament patterns and plan appropriate therapeutic strategies for children with sCP. Key Words: assessment, cerebral palsy, developmental function, outcome, temperament
©2011 Elsevier & Formosan Medical Association .
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Graduate Institute of Early Intervention, Department of Physical Therapy, 3Graduate Institute of Clinical Behavioral Science, Department of Occupational Therapy and 5Department of Physical Therapy, College of Medicine, Chang Gung University, Taoyuan, 2Graduate Institute of Occupational Therapy, College of Medicine, National Taiwan University, Taipei, 4Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Keelung, and 6Department of Physical Medicine and Rehabilitation, Chang Gung Memorial Hospital, Linkou, Taiwan. Received: April 7, 2010 Revised: May 7, 2010 Accepted: July 5, 2010
*Correspondence to: Dr Chung-Yao Chen, Department of Rehabilitation Medicine, Chang Gung Memorial Hospital, 222, Maijin Road, Anle District, Keelung City 204, Taiwan. E-mail: [email protected]
J Formos Med Assoc | 2011 • Vol 110 • No 8
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Even newborn babies display observable emotional and behavioral styles. Each child has peculiar and innate traits. Individual differences in traits during childhood and adolescence are described as temperament or personality traits.1 Temperament is inherited and emerges early in life and stabilizes during development.2 Personality is a developmental outcome and can change throughout a lifetime.3 Temperament and personality are influenced by genetic and complex environmental factors,4,5 such as parenting skills,6 or parental marital status.7 Therefore, temperament is influenced over time by genetic inheritance, maturation and experience.1,3 Interactions occur between temperament traits and child development. Temperament, although stable, is not static.8 Previous studies have revealed significant relationships between temperament and developmental stage from infancy to middle childhood,9 and from childhood to early adulthood.10,11 Individual temperamental differences are largely determined by biological factors. However, child behavior is modified as the nervous system matures and self-regulatory and cognitive skills develop. Studies have found that temperamental differences can affect the emotions, behavior and development of children, including their exploration, discovery and learning processes.1,12 Cerebral palsy (CP) describes a group of disorders of the development of movement and posture causing activity limitation, that are attributed to non-progressive disturbances that occur in the developing fetus or infant brain.13 Spastic CP (sCP), the most common type, is further classified on the topographic distribution of the body affected, such as spastic hemiplegia, spastic diplegia (SD) and spastic quadriplegia (SQ).14,15 Children with sCP are likely to have more difficulties in development of cognition, learning, speech, social skills and motor functions, possibly influencing their behavior and ability to express emotion appropriately. Ross16 has reported that preterm infants diagnosed with CP are often less adaptable, less persistent and more withdrawn from new stimulation. 528
Therapy for children with CP is focused on underlying functional impairments. Elucidating developmental profiles and temperament patterns in children with CP might help clinicians improve the relationship between clinicians and children, understand developmental problems, and elaborate more flexible strategies for treating children with different developmental profiles and temperament patterns.12 Temperament is associated with motor development,17 and neurodevelopmental functions.18 Bayley scores are correlated with temperament scores in premature infants16,18 and normal infants.19 The temperament continues to influence the development of children during their school-age years.20 The neurodevelopmental variations in children with CP with different subtypes and motor severities, associated with various types of brain damage, might cause potential differences in development and temperament. However, few researchers have studied developmental profiles and temperament patterns in children with sCP, who have various CP subtypes or motor severity. In this study, we hypothesized that developmental profiles and temperament patterns vary in children with sCP with different CP subtypes and severity. This study investigated the developmental profiles and temperament patterns in children with SD or SQ.
Materials and Methods Participants The study population included children with sCP treated in the Department of Physical Medicine and Rehabilitation at Chang Gung Memorial Hospital from September 2001 to November 2005. Inclusion criteria were CP with SD or SQ, and age 3–6 years. SD is defined as motor disability involving primarily lower extremities, with upper motor neuron signs in the lower limbs.15 SQ is defined as massive total motor disability involving all four limbs and trunk, with upper motor neuron signs in all limbs.15 Exclusion criteria were any of the following during the previous 3 months: (1) significant J Formos Med Assoc | 2011 • Vol 110 • No 8
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medical problems such as active pneumonia or urinary tract infection; (2) progressive neurological disorder; (3) any major surgical treatment such as orthopedic surgery or neurosurgery; (4) any treatment with nerve or motor point block such as a botulinum toxin injection; and (5) any dental procedure such as tooth extraction. Finally, 105 children with sCP were enrolled. These children were classified into two groups based on the topographic distribution of limb involvement: SD (n = 60), and SQ (n = 45). Another 66 age- and sex-matched children with typical development (TD) were selected as a control group. The study was approved by the Human Ethics Committee at this hospital. All participants’ parents/caregivers gave informed consent. All children underwent assessment of developmental profiles, temperament patterns, and motor severity. Developmental profiles were assessed using Chinese Child Development Inventory (CCDI),21 a Chinese revision of the Minnesota Child Development Inventory.22 The CCDI has been widely used to assess developmental profiles in children with developmental delay in Taiwan.23 The CCDI, a 320-item questionnaire, consists of statements describing child behavior, to which parents/caregivers were asked to answer “yes” or “no” if the child had or had not ever exhibited the specified behavior. The scoring process yielded age equivalents in eight domains of developmental function. These eight domains included gross motor (GM, 34 items), fine motor (FM, 44 items), expressive language (EL, 54 items), concept comprehension (CC, 67 items), situation comprehension (SC, 44 items), self help (SH, 36 items), personal social (PS, 34 items), and general development (GD, 131 items). The GD domains integrated seven items and 124 items from the other seven domains. The validity and reliability of the CCDI were > 0.83 and > 0.88, respectively.21 The development quotient (DQ) was determined as a percentage of developmental age divided by chronological age. The Chinese version of Childhood Temperament Inventory (CCTI),24 originally developed by Thomas and Chess,25 was used to assess J Formos Med Assoc | 2011 • Vol 110 • No 8
temperament patterns. The CCTI consisted of 72 items that described particular behavior in a variety of situations. The parents/caregivers were asked to rate the frequency of their children’s behavior on a seven-point scale from 1 (never) to 7 (always). The 72 items, eight in each dimension, were classified into nine dimensions of temperament: (1) activity level, with high scores indicating high activity level; (2) rhythmicity, with high scores indicating high regularity; (3) approach–withdrawal, with high scores meaning high willingness to approach new stimuli; (4) adaptability, with high scores indicating high adaptability; (5) attention span and persistence, with high scores indicating more persistence; (6) distractibility, with high scores indicating high degree of distraction; (7) threshold of responsiveness, with high scores indicating high threshold; (8) intensity of reaction, with high scores indicating high intensity of reaction; (9) mood pattern, with high scores indicating more positive mood. The average score in each dimension was calculated as the average score of corresponding items. The Gross Motor Function Classification System (GMFCS)26 was used to measure motor severity of sCP. The same physiatrist, one of the authors, assessed the GMFCS levels of children with sCP. The GMFCS graded the self-initiated movement of sCP patients with particular emphasis on their functional abilities (sitting, crawling, standing and walking) and their need for assistive devices (e.g. walkers, crutches and canes) and wheeled mobility. The GMFCS used a fivepoint scale (I–V) from “independent” (level I) to “dependent” (level V). The clinical data, including associated comorbidity, current usage of medication, and family environments of children with CP were analyzed. The associated comorbidity included epilepsy, mental retardation, attention deficit/hyperactivity disorder, autism, and visual and hearing problems. Current usage of medication consisted of anticonvulsants, antispasticity medication, and central nervous system medication, such as ritalinlike stimulants, piracetam, and clonidine, were recorded. The family environments included 529
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family’s economic status and parents’ educational levels. The family’s economic status was categorized into three grades: low, < NT$370,000 per year; middle, NT$370,000–NT$990,000 per year; and high, > NT$990,000 per year. The parents’ educational levels were categorized into three grades: low, less than high school; middle, high school; and high, university or higher. The higher educational status of parents was selected for data analysis. In addition, the demographic data, including age and sex, of all children were also recorded.
Statistical analysis Group differences in continuous data (age and temperament scores) among two sCP groups and TD group were compared by analysis of variance test with post hoc Tukey multiple comparisons. Group differences in developmental profile (all DQs) between two sCP groups were compared with an independent t test. Group differences in sex and clinical data were determined by the χ2 test. The Mann–Whitney test was used to determine group differences in the family data and severity of GMFCS levels. Pearson correlation was used to determine the relations among severity, developmental profiles and temperament patterns. A p value < 0.05 was considered statistically significant.
Results The three groups did not significantly differ in age and sex (Table 1). The parents’ educational levels and family’s economic status did not differ between both CP groups (Table 1). The SQ group was associated with higher incidences of epilepsy and mental retardation, and currently used more medication than did the SD group (p < 0.001) (Table 1). However, the associated comorbidity of attention deficit/hyperactivity disorder, autism, and hearing and visual problems did not differ between both CP groups. The SD group had better GMFCS levels than the SQ group had (p < 0.001) (Table 1). Approximately 95% of children in the 530
SD group were GMFCS levels I and II. However, 60% of children in the SQ group had a GMFCS level above II (Table 1). The SQ group had lower DQs in all developmental functions than the SD group had (p < 0.01) (Table 1). The DQ distribution pattern of developmental profiles showed the same trend in the SD and SQ groups, and both groups displayed lowest DQs in the GM domain (Figure 1). The largest difference between the two groups was found in the FM domain (38%). By contrast, the smallest difference occurred in the GM domain (25%). The DQs of other developmental functions were 63–82% in the SD group, whereas those were 37–56% in the SQ group (Figure 1). Temperament patterns were different between the sCP and TD groups (Figure 2). Both SQ and SD groups had lower attention span and persistence, and a higher threshold of responsiveness than the TD group had (p < 0.05) (Figure 2). The SQ group was less approachable than the TD group was (p < 0.05) (Figure 2). Furthermore, the SQ group had lower adaptability than the TD and SD groups had (p < 0.01) (Figure 2). Pearson correlation analysis indicated that GMFCS levels were highly and negatively correlated with all DQs (r = −0.54 to −0.76, p < 0.01, Table 2). GMFCS levels were weakly, although still significantly, correlated with some temperament patterns (Table 2). The significant correlation between DQs and temperament patterns were mostly weak, except for the relationship between the threshold of responsiveness and DQs (r = −0.20 to −0.44, p < 0.05, Table 2).
Discussion Our results suggest that the severity of motor deficits was associated with the developmental profiles, but not the temperament patterns. Different subtypes of sCP demonstrated some unique temperament patterns and developmental profiles. The differences between the two groups of children with CP could have been due to the motor J Formos Med Assoc | 2011 • Vol 110 • No 8
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Table 1. Demographic, family and clinical data and motor severity in children with spastic bilateral cerebral palsy, and demographic data from children with typical developmenta Children with CP (n = 105)
Demographic Age (yr)c Sex, maleb Family Parents’ educational level Low: below high school Middle: high school High: university or higher Family’s economic status (NT$ /yr) Low: < 370,000 Middle: 370,000–990,000 High: > 990,000 Clinical Associated comorbidity Epilepsy Attention deficit/hyperactivity disorder Autism Mental retardation Hearing impairment Vision impairment Current medication usage GMFCS levelsb Level I Level II Level III Level IV Level V
Diplegia (n = 60)
Quadriplegia (n = 45)
4.9 ± 1.5 42 (70.0)
4.7 ± 2.1 25 (55.6)
7 (11.7) 26 (43.3) 27 (45.0)
6 (13.3) 23 (51.1) 16 (35.6)
13 (21.7) 38 (63.3) 9 (15.0)
11 (24.4) 31 (68.9) 3 (6.7)
3 (5.0) 10 (16.7) 4 (6.7) 11 (18.3) 0 (0) 16 (26.7) 8 (13.3)
14 (31.1) 5 (11.1) 1 (2.2) 31 (68.9) 3 (6.7) 15 (33.3) 15 (33.3)
Children with TD (n = 66)
4.7 ± 1.1 39 (59.1)
p
0.730 0.418
0.622
0.438
< 0.001 0.575 0.389 < 0.001 0.076 0.459 0.014 < 0.001
43 (71.7) 14 (23.3) 3 (5.0) 0 (0) 0 (0)
0 (0) 17 (37.8) 13 (28.9) 7 (15.6) 8 (17.8)
Data are presented as mean ± standard deviation or n (%); bc2 or Mann–Whitney tests for categorical data; cone-way analysis of variance test with post hoc Tukey multiple comparisons for continuous data. CP = cerebral palsy; TD = typical development; GMFCS = Gross Motor Function Classification System.
a
functions, cognitive functions, language skills, or their interactions. However, CP subtypes and motor severity, not developmental functions, were selected in this study for predicting the temperament patterns and developmental profiles, for several reasons. First, the CP subtypes can reflect underlying brain damage,14 in addition to the involved body parts and functional level. For example, children with SQ CP often have associated severe intraventricular hemorrhage and periventricular leukomalacia.14 Accordingly, children J Formos Med Assoc | 2011 • Vol 110 • No 8
with SQ were more severely involved than those with SD in gross motor function as well as in other domains of development. Second, the CP subtype and motor severity are classified quickly and easily (within 5 minutes) by clinicians. However, various developmental functions are evaluated by multidisciplinary assessments. The professionals need a lot of time (1 hour on average for each disciplinary assessment) to assess developmental functions, such as cognition and speech functions. Third, the developmental functions are 531
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100 Developmental quotient (%)
* *
80
*
* *
*
* 60 * 40
Diplegia
20
Quadriplegia 0 GM
FM
EL CC SC SH Chinese child development inventory
PS
GD
Figure 1. Developmental quotient measured by Chinese Child Development Inventory in children with cerebral palsy. *p < 0.01 (independent t test). GM = gross motor; FM = fine motor; EL = expressive language; CC = concept comprehension; SC = situation comprehension; SH = self help; PS = personal social development; GD = general development. 5.5
BN* AB*
Diplegia Quadriplegia Normal
Average score
5.0 BN† AN† BN*
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AN† BN*
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Chinese childhood temperament inventory Figure 2. Average score of Chinese Childhood Temperament Inventory in children with cerebral palsy and children with typical development (TD). AN: significant differences between SD and TD groups; BN: significant differences between SQ and TD groups; AB: significant differences between SD and SQ groups (One-way analysis of variance test with post hoc Tukey multiple comparisons). *p < 0.01, †p < 0.05.
selected as the dependent variables. Fourth, all developmental functions are correlated with each other. Temperament pattern can be influenced by biological and environmental factors, as well as by their interactions. The motor and non-motor functions affect temperament patterns and developmental profiles in children with CP. For example, children’s cognitive, speech, and personal–social 532
development could influence their temperament. Comorbidity and current use of medication, such as anticonvulsants, central nervous system medications, and anti-spasticity medications, might modify temperament patterns and developmental profiles. In this study, children with SQ CP currently used more medication and were associated with higher incidences of comorbidity, such as epilepsy and mental retardation, than those J Formos Med Assoc | 2011 • Vol 110 • No 8
Development and temperament in cerebral palsy
Table 2. Pearson correlations of motor severity, developmental profiles and temperament patterns in children with spastic bilateral cerebral palsy Motor severity GMFCS levels Motor severity GMFCS levels Temperament patterns Activity level Rhythmicity (Regularity) Approach/withdrawal Adaptability Intensity of reaction Quality of mood Attention span & persistence Distractibility Threshold of responsiveness
Developmental profiles
GM
FM
EL
CC
SC
SH
PS
GD
–0.758** –0.715** –0.565** –0.541** –0.661** –0.754** –0.641** –0.681**
–0.102 0.022 –0.241* –0.329** –0.050 –0.106 –0.023
0.158 –0.125 0.111 0.252** 0.143 0.062 0.141
–0.076 –0.089 ** –0.205* 0.292
–0.082 –0.014
–0.114 0.026
0.123 0.293** 0.206* 0.041 0.276**
0.129 0.285** 0.152 0.096 0.226*
–0.160 0.071 0.189 0.290** 0.132 0.119 0.280**
–0.073 0.034 0.203* 0.347** 0.136 0.104 0.244*
0.007 –0.032 0.119 0.306** 0.122 0.041 0.203*
–0.089 0.049 0.111 0.281** 0.132 0.069 0.244*
–0.075 0.031 0.158 0.305** 0.166 0.094 0.260**
0.027 0.121 0.120 0.052 0.001 0.088 0.076 ** ** ** ** ** ** –0.387 –0.396 –0.421 –0.444 –0.317 –0.351 –0.412**
*p < 0.05; **p < 0.01. GMFCS = Gross Motor Function Classification System; GM = gross motor; FM = fine motor; EL = expressive language; CC = concept comprehension; SC = situation comprehension; SH = self help; PS = personal social development; GD = general development.
with SD CP. The SD group had better cognition, speech, personal–social functions and GMFCS levels than the SQ group had. However, the family factors did not differ between both CP groups. These findings suggest that the differences in the developmental profile and temperament pattern between SD and SQ groups actually resulted from brain damage, which causes various motor functions and CP subtypes. The motor impairment of sCP was related to developmental profiles in children with sCP. In other words, children with sCP and worse GMFCS levels had more motor, cognition, speech, personal–social, and self-care impairments than those with sCP and better GMFCS levels. Children with CP, especially those with poor GMFCS levels, often demonstrate developmental disabilities in multiple domains, such as cognition, speech, and behavior. Children’s functional impairments in cognition, speech, personal–social, and self-care might also be influenced by nonmotor comorbidity. Our results showed that the J Formos Med Assoc | 2011 • Vol 110 • No 8
SD group had better GMFCS levels than the SQ group had. The differences in the developmental profile between the SD and SQ groups might actually reflect the deviations between different motor functions, rather than CP subtypes. Furthermore, children with sCP with greater motor impairment also have greater disability to explore their environment, learn new strategies, interact socially and perform self-care functions. These could be the reasons why GMFCS was highly correlated with developmental profiles. Previous studies also have suggested that GMFCS predicts motor change in children with CP,27 and motor impairments predict gross motor function and everyday activities.28 Therefore, using GMFCS level rather than CP subtype might provide more useful information for understanding variations in developmental profiles in children with CP. Different sCP subtypes with particular pathophysiology29,30 demonstrate different developmental profiles. In the present study, children with SQ had lower DQs in all developmental 533
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functions than those with SD, and both groups displayed lowest DQs in the GM domain. In premature infants, SD, often associated with white matter disorder, is the dominant form of CP.29 In the SD group, the major delay in CCDI was GM domain, and DQs in the other domains were all > 60%, as compared to those in normal children. The DQ in the GD domain was nearly 80% in the SD group. Besides, the largest difference in developmental profiles between the SD and SQ groups was found in the FM domain. The selectively legs dysfunction and relatively preserved hand and cognitive function in the SD group might be the reasons for these findings. Children with SQ often had a difficult delivery with evidence of perinatal asphyxia or brain anomalies, and have a high percentage of mental retardation.15,31,32 Significant cognitive involvement in children with SQ might be the important cofactor, along with motor impairment, of why differences in language and comprehension domains were larger between the SD and SQ groups than differences in the GM domain. Temperament patterns vary among children with different CP subtypes. In the present study, children with SQ were less adaptable and approachable than were normal children, which was not found in the SD group. Besides, children with SQ were less adaptable than were children with SD. Koeda also has suggested that children with CP have lower adaptability than normal children have.33 Was the motor impairment of sCP the major reason for the difference? Although the GMFCS levels were significantly correlated with the approach and the adaptability, the different GMFCS levels could explain < 10% of the variability (coefficient of determination < 0.1) in approach and adaptability. The relatively large sample size (n = 105) might be the reason for this weak but significant correlation. Previous studies also have found poorer performance on the Bayley Mental Scales in preterm infants, who were diagnosed with CP later, and 1-year outcome was significantly associated with temperament characteristics of lower adaptability, and more withdrawal from new stimulation.16 Therefore, we 534
can speculate that cognitive impairments play a more important role than motor impairment for less adaptable and approachable children in the SQ group. Children learn different self-regulatory strategies for responding to external stimuli as cognition develops. Flexible and adaptable innate traits in regulatory processes can enhance responsiveness in individual and external contexts.34 Therefore, strategies to improve adaptability and approachability, such as selecting the same treatment room to allow these children to be more adaptable to the environment, and more personal social interaction programs, should be considered in planning therapeutic programs for children with SQ CP. Programs that use a high intensity of stimulation are proposed when treating children with sCP. The higher the threshold of responsiveness, the more difficulty children have in shifting and focusing their attention. The threshold of responsiveness is related to the level of stimulation, such as sensory stimuli, environmental objects, and social contacts. In the present study, children with sCP had a higher threshold of responsiveness that adversely affected the regulatory processes to the external environment, which further impeded development. Given that the GMFCS levels were weakly correlated with the threshold of responsiveness, and could explain < 10% of the variability in it, the frequently associated deficits such as cognitive, visual and hearing impairment might have accounted for the higher threshold of responsiveness in children with sCP. Among the different temperament patterns, the threshold of responsiveness was the only one that reached medium correlation (r < −0.4) with the developmental profiles of the CCDI. Therefore, not only the motor deficit, but also the high threshold of responsiveness should be seriously managed when planning therapeutic strategies for children with sCP. Comorbidity such as visual and hearing impairment and visual perception dysfunction should be routinely screened and treated. Sensory integration programs with a high level of stimulation might be offered as part of rehabilitative strategies. J Formos Med Assoc | 2011 • Vol 110 • No 8
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Rehabilitative programs with multiple shortduration sessions are suggested when treating children with sCP. In the present study, sCP groups had lower attention span and persistence than the TD group had, but the distractibility did not differ between the two groups. Attention function is a filter of perceptual–cognitive activity. Suslow et al have found that attention is highly related to cognition and social interaction.35 In the present study, the findings that motor impairment was not correlated with persistence and distractibility support their results that attention is highly related to cognition. The reason why distractibility did not differ between the sCP and TD groups might be related to the high threshold of responsiveness found in children with sCP. Therefore, the learning and cognitive processes in children with sCP cannot be sustained for a long period, even though they are not easily distracted by external stimuli. Treatment programs with higher stimulation intensity and shorter duration are suggested for children with sCP. There were several limitations in our study. We only recruited children with SD and SQ. Therefore, our results cannot be generalized to CP with other subtypes, such as spastic hemiplegic or dyskinetic types. The associated deficits commonly found in children with CP, such as mental retardation, visual and hearing perception deficits, were not thoroughly evaluated by subspecialists or formal evaluation tools. In fact, it is difficult to evaluate precisely these associated deficits with confidence in children at these young ages. Therefore, these possible covariates could not be further analyzed. Social and parental factors were also important for children’s development. Children under early intervention therapy at medical centers often have parents with higher socioeconomic and well-educated status. Therefore, our results might have been different if participants had been recruited from children with sCP who were not receiving treatment. In conclusion, the severity of motor deficit was highly related to all developmental functions and weakly related to some temperament dimensions in children with sCP. Among temperament J Formos Med Assoc | 2011 • Vol 110 • No 8
dimensions, only threshold of responsiveness reached medium correlation with developmental profiles in children with sCP. Developmental profiles and temperament patterns varied among children with different subtypes of sCP. The data provided in the present study might allow clinicians to anticipate the developmental profiles and temperament patterns and plan appropriate therapeutic strategies for children with sCP.
Acknowledgment The authors would like to thank the Health Administration of Executive Yuan, Taiwan, for financially supporting this research under Contract No. GMRPG360101.
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J Formos Med Assoc | 2011 • Vol 110 • No 8