Official Journal of the European Paediatric Neurology Society
Original article Bilateral spastic cerebral palsyPrevalence through four decades, motor function and growth Kate Himmelmann
, Eva Beckung, Gudrun Hagberg, Paul Uvebrant
The Queen Silvia Childrens Hospital/Sahlgrenska University Hospital, Go teborg, Sweden a r t i c l e i n f o Article history: Received 29 September 2006 Received in revised form 21 December 2006 Accepted 24 December 2006 Keywords: Cerebral palsy Bilateral spastic Prevalence Motor function Growth a b s t r a c t The aim was to depict changes in the prevalence and severity of bilateral spastic cerebral palsy (CP) over a 40-year period. Another objective was to characterise the group born in 19911998 with respect to gross motor function, spasticity and growth. Data were obtained from the CP register of western Sweden and rehabilitation records. Results: After a rise to 1.27 per 1000 live births in 19831986, the prevalence decreased signicantly, in children born both preterm and at term, to 0.69 in 19951998. After 1975, more children were born preterm than at term. There was a signicant decrease in severe bilateral spastic CP during the same period, mainly in children born at term. In all, 46% of the children born at term and 33% of those born preterm had a severe motor impairment, i.e. no walking ability. In the 167 children born in 19911998, the gross motor function classication system (GMFCS) level was I in 14%, II in 34%, III in 10%, IV in 25% and Vin 17%. The GMFCS level correlated with the gross motor function measure (GMFM) and the Ashworth spasticity scores, as well as with the deviation in postnatal weight and height. We conclude that the prevalence of bilateral spastic CP has decreased since the mid- 1980s, parallel to a reduction in the severity of the motor impairment. Children born preterm have predominated since the mid-1970s. The severity of the motor impairment correlated with the degree of spasticity, GMFM and growth. The percentage of children who were underweight was substantial. & 2007 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. 1. Introduction The panorama of cerebral palsy (CP) in western Sweden has been closely monitored for four decades in an ongoing study, currently covering the birth years 19591998. Epidemiology, distribution of types of CP and accompanying impairments have been described 19 and gross and ne motor function in children born in 19911998 were recently reported. 10 The group of spastic diplegia constitutes more than one-third of all CP and even more if combined with the group of spastic tetraplegia into the concept of bilateral spastic CP, 11,12 as proposed by the Surveillance of CP in Europe (SCPE) 13 and the Washington workshop on denition and classication of CP. 14 This concept has been widely accepted as an alternative to the often confusing terms diplegia, tetraplegia, quadriplegia and double hemiplegia, with varying denitions between countries and authors. 10,11,13,15 It has given us the means not only to describe but also to compare between populations, evaluate change and predict needs in this particular group. Other issues that have been brought to attention in recent years are the prerequisites for activity and participation, 8,16 as ARTICLE IN PRESS 1090-3798/$ - see front matter & 2007 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ejpn.2006.12.010
E-mail address: kate.himmelmann@vgregion.se (K. Himmelmann). E UR OP E A N J OUR NA L OF PAE DI AT R I C NE UR OL O GY 11 ( 2007) 215 222 well as the nutrition and growth of children with CP. Intrauterine growth may sometimes deviate, 17 but the post- natal growth deviation, 18 which may result in shortness and often severe underweight, is even more signicant. The aims of this study were to depict changes in the live birth prevalence and severity of motor impairment in bilateral spastic CP over time in western Sweden, to describe differences between children born preterm and at full-term and to characterise the group with respect to motor function, spasticity and growth. 2. Material and methods The prevalence of bilateral spastic CP and the severity of the gross motor impairment, categorised as independent walking (mild), walking with aids (moderate) and wheel-chair depen- dence (severe), were analyzed in 763 children with bilateral spastic CP from a total of 1683 children with CP born in 19591998. They constituted 97% of all children with CP born in this period in the region. 17,9 A further classication of gross motor function into the ve levels of the Gross Motor Function Classication System (GMFCS) 19 was applied to the 167 children born in 19911998 and previously described. 10 Children in the relevant age band (612 years) can walk unaided at GMFCS levels III and walk with aids at level III, while children at levels IVV are dependent on wheeled mobility. Twenty-three children (14%) were originally diagnosed as spastic tetraplegia and 144 as spastic or atactic diplegia. The Gross Motor Function Measure (GMFM) 20 is a test of ve dimensions of gross motor function: (A) lying and rolling, (B) sitting, (C) crawling and kneeling, (D) standing and (E) walking, running and jumping. A total score is obtained by calculating the mean percentage of the points obtained for each dimension. GMFM data were obtained from 100 of the 167 children. Muscle tone was assessed using the modied Ashworth score (05) according to Peacock-Staudt, 21 where 1 is normal muscle tone. The muscle groups assessed were left and right adductors, quadriceps, hamstrings and plantar exors. The Ashworth score for the knee extensors was used for calcula- tions, as it has been shown to correlate with measurements of function, including the GMFM. 22 Muscle tone was assessed in 76 of the 167 children. Swedish growth charts for weight and height were used. 23,24 Body weight was available in 124 children and height in 106 of these. Body mass index (BMI) was calculated in these 106 children. 25 2.1. Procedure Data were derived from the CP register of western Sweden. 7,9 Exceptions were growth data (body weight and height), GMFM and muscle tone, which were collected from local and regional rehabilitation records. GMFCS levels were re-evalu- ated in all children, 26 years after the initial classication. For muscle tone, only assessments performed between the ages of four and 12 years by one of the authors (KH) were included. 2.2. Statistics The w 2 test and w 2 test for trend in proportion were used for comparisons of proportions. A paired t-test was used for comparisons of paired continuous data. Spearmans correla- tion coefcient was used for correlations. The level of signicance was set at po0:05. 2.3. Ethics The study was approved by the Ethics Committee at the Medical Faculty at the University of Go teborg. Informed consent was obtained from the parents of the children born in 19911998. 3. Results 3.1. Birth years 19591998 The changing trend in the prevalence of bilateral spastic CP over the 40-year period 19591998 for children born at term and preterm, respectively, is shown in Fig. 1. After a signicant decrease in the 1960s (po0:01), the prevalence of bilateral spastic CP in the birth year period 19671970 was 0.52 per 1000 live born and it rose to 1.27 in 19831986 (po0:01), followed by another decrease to 0.69 per 1000 live born (po0:01) in the latest 4-year cohort of children born in 19951998. The prevalence changes were signicant for both the preterm and the full-term group. A contemporary steep decrease in perinatal mortality took place (Fig. 2). The two preterm groups, children born moderately preterm, i.e. 3236 weeks of gestation, and very preterm, i.e. before 32 weeks, followed a similar pattern, but with a shift in time. The moderately preterm group had its peak in the birth-year period 19791982, while the very preterm group had its peak later, in the birth-year period 19911994. The prevalence of the term group decreased over the period (po0:01) after a temporary increase in 19831990. The percentage of children born at term decreased during the period (po0:05) and, after 1975, more children with bilateral spastic CP were born preterm than at full term. In the preterm group, the percentage of children born before 32 weeks of gestation rose from 14 in 36 (39%) in children born in 19751978 to 29 in 41 (72%) born in 19951998 (po0:001). The live birth prevalence and distribution of the severity of the gross motor impairment in the 763 children, 426 (56%) of whom were born preterm, is presented in Fig. 3. After a rise in predominantly severe bilateral spastic CP from 1959 to 1986 (po0:001), there was a signicant decrease (po0:01). The decrease in severity occurred in children born at term (po0:01), with no contemporary decrease in severity in children born preterm. The distribution of motor impairment over time is shown in Fig. 4a for children born preterm and in Fig. 4b for children born at term. As can be seen, a larger percentage of the children born at term had a severe motor impairment compared with those born preterm, 156 of 337 (46%) and 142 of 426 (33%), respectively (po0:001). This difference persisted throughout the whole 40-year period. ARTICLE IN PRESS E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 216 There was a male predominance in the preterm group, with 254 boys (59%) and 172 girls (po0:01), as well as in the term group, with 186 boys (56%) and 151 girls. There was no signicant difference between boys and girls in the distribution of the severity of the motor impairment, but in both groups there were larger percentages with severe motor impairments among those born at term (boys; po0:05, girls; po0:001). 3.2. Birth years 19911998 3.2.1. Gross motor function In the re-evaluation, the GMFCS level of the 167 children born in 19911998 was modied in four cases, three of which had changed from levels III to II and one from III to IV. Twenty-four children (14%) performed at GMFCS level I, 57 (34%) at level II, ARTICLE IN PRESS 0 0.2 0.4 0.6 0.8 1 1.2 1.4 59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98 Term 32-36 w < 32 w Total Birth year P r e v a l e n c e
p e r
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Fig. 1 Crude prevalence of bilateral spastic CP in children born in 19591998. Of children with bilateral spastic CP, 337 children were born at term and 426 preterm, whereof 248 before 32 weeks of gestation. 0.1 1 10 100 59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98 Birth year P e r
1
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( C P ) PNM CP BSCP Fig. 2 Perinatal mortality per 1000 born, crude prevalence of CP and bilateral spastic CP per 1000 live births in 19591998 in western Sweden. EUROPEAN J OURNAL OF PAEDI ATRI C NEUROLOGY 11 ( 2007) 215 222 217 17 (10%) at level III, 41 (25%) at level IVand 28 (17%) at level V. Sixty-nine of 98 (70%) ambulatory children and 40 of 69 (58%) non-ambulatory children were born preterm. The distribution of GMFCS levels in the sub-groups of children in which body weight and height, GMFM and muscle tone data were analyzed did not differ from that in the whole group. The mean GMFM score at a mean age of 6.5 years (range 412) for the ve dimensions and for the total score by GMFCS level in 100 children (60%) is shown in Fig. 5. There was a correlation between the GMFCS level and the total GMFM score, as well as between GMFCS and the ve separate GMFM dimensions, Spearmans r 1.0 (po0:01). 3.2.2. Spasticity Spasticity, expressed as Ashworth scores, in eight selected muscle groups in the lower extremities is shown in Fig. 6. The median Ashworth score in children performing at GMFCS level I was 1, in children with assisted walking 2 and in non- walkers the median score was 3. The Ashworth scores correlated with the severity of the motor impairment (po0:01) and the median Ashworth score for the knee extensors correlated with the GMFCS levels, Spearmans r 0.949, p 0:014, and thereby with walking ability. 3.2.3. Growth Information on body weight was available in 124 (74%) of the 167 children, representing 67% of the children at GMFCS level I, 72% at level II, 76% at level III, 76% at level IVand 82% of the children at level V. The weight deviation at follow-up correlated to the GMFCS level, Spearmans r 0.975, po0:001. The more severe the motor impairment, the larger the percentage of children who weighed less than 2 SD, po0:02. No such correlation was found between birth weight and GMFCS level. The mean weight deviation at follow-up at a mean age of 7.1 years (range 412 years) compared with birth weight deviation in 120 children by the different GMFCS levels is shown in Fig. 7. There was a signicant difference between mean weight deviation at birth and at the time of follow-up. This was true for children born both preterm and at full term, po0:01 and 0:01, respectively. There was a signicant correlation between the mean deviation in height at follow-up and the severity of the motor impairment (GMFCS level), Spearmans r 0.9, po0:05, and a larger percentage of children with a body height of o2SD was found among those with a severe motor impairment (GMFCS IVV), po0:05. In these 106 children, BMI was calculated. No correlation was found between the severity of the motor impairment and BMI. Fifteen children had a BMI of less than 2 SD, while six had a BMI over 2 SD. Another 16 children had a body weight and height below2 SD producing a BMI within 2 SD from the mean. 4. Discussion Changes over time within the CP population are plausible, with more preterm and more fragile children surviving. At the same time, the severity of impairment may be reduced with more advanced care. This was clearly illustrated in the ARTICLE IN PRESS 0 0.2 0.4 0.6 0.8 1 1.2 1.4 59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98 Birth year P r e v a l e n c e
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b i r t h s Mild Moderate Severe Total Fig. 3 Prevalence per 1000 live births by the severity of the motor impairment in 763 children with bilateral spastic CP born in 19591998. E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 218 present study, where the marked decrease in perinatal mortality coincided with an initial rise in the prevalence of bilateral spastic CP, predominantly in children born preterm, followed by a decrease. Children born at 3236 weeks of gestation were the rst to follow this pattern, followed by those born before 32 weeks. In this study, we found a reduction in the percentage of children born at term in the bilateral spastic group. Although the motor impairment was more severe than in children born preterm, the severity decreased over the last 15-year period. This was in accordance with the ndings reported by Blair et al. in Western Australia, 26 who also found more severe impairments in children born at term and decreasing disability scores over time. A previous collaborative survey from south-west Germany and western Sweden revealed comparable prevalence gures for bilateral spastic CP in the two countries. 11 Spasticity is a characteristic in the majority of children with CP. It is generally postulated that spasticity is related to the severity of the motor impairment 27 and various treatments, ARTICLE IN PRESS 0% 20% 40% 60% 80% 100% 59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98 Mild Moderate Severe Mild Moderate Severe Birth year 0% 20% 40% 60% 80% 100% 59-62 63-66 67-70 71-74 75-78 79-82 83-86 87-90 91-94 95-98 Birth year a b Fig. 4 (a) Distribution of the severity of the gross motor impairment in 426 children with bilateral spastic CP born preterm in 19591998. (b) Distribution of the severity of the gross motor impairment in 337 children with bilateral spastic CP born at term in 19591998. EUROPEAN J OURNAL OF PAEDI ATRI C NEUROLOGY 11 ( 2007) 215 222 219 such as selective dorsal rhizotomy, 28 intrathecal baclofen 29 and botulinum toxin 30 have been designed in order to improve function and/or quality of life. However, the methods for measuring spasticity that are available to most clinicians, such as the Ashworth scale, are less accurate than instru- mented measures, with inconsistencies especially in the mid- range values. 22 The nding in this study of a correlation between the degree of spasticity and the gross motor function, expressed as GMFCS level, supports the hypothesis that spasticity contributes to the motor impairment, but motor function may also be impaired by weakness, lack of selective motor control, balance problems, perception dif- culties and contractures. Strength, in particular, has been shown to correlate well with motor function in walkers with spastic diplegia 31 and to be possible to improve by training. 32 The classication of motor function by means of the GMFCS has improved the opportunity to describe gross motor function in a simple, comprehensive and uniform way in children with CP within and between countries, as in the European collaboration SCPE. 13,34 In this study, the GMFCS classication remained stable over time, as Palisano recently reported. 33 A change in GMFCS level afliation was made in only four children (2%), originally performing at level III, three for the better, while one had deteriorated. The GMFCS can serve as a framework for comparisons of measures of spasticity, the rate and number of accompanying impair- ments and GMFMs, one of which is the GMFM, for example. The GMFM is a valid measure with good inter- and intra-rater reliability 35 that has gained widespread use since its intro- duction in 1993. 20 One limitation is the fact that the maximum achievement is that of a healthy 5-year old, which creates a ceiling effect in the results of the most able children. ARTICLE IN PRESS 0 20 40 60 80 100 I II III IV V G M F M
% T E D C B A GMFCS Fig. 5 Gross motor function measure (GMFM) by gross motor function classication system (GMFCS) levels in 100 children with bilateral spastic CP. A lying and rolling, B sitting, C crawling and kneeling, D standing, E walking, running and jumping, T total score. 5.00 10.00 15.00 20.00 25.00 30.00 I n=8 II n=30 III n=6 IV n=22 V n=10 GMFCS S u m
o f
A s h w o r t h
s c o r e s Fig. 6 Sums of Ashworth spasticity scores from eight muscle groups (adductors, hamstrings, quadriceps and plantar exors) in both legs by gross motor function classication system (GMFCS) level in 76 children. Medians with boxes denoting the 2575th percentile, whiskers extend from the largest to the smallest value. Maximum score 85 40. -2 -1.5 -1 -0.5 0 0.5 Birth weight deviation Weight deviation at follow-up GMFCS S D
s c o r e I II III IV V Fig. 7 Weight deviation (SD) at birth and at follow-up at a mean age of 7.1 years in 120 children with bilateral spastic CP. E UR OP E AN J OUR NAL O F PAE DI AT R I C NE UR OL OG Y 11 ( 2007) 215 222 220 In this study, as in that by Abel, 36 performance in the ve dimensions and the total score on the GMFM correlated with the level of GMFCS. A correlation was also found between GMFCS levels and the deviation in body weight at the time of follow-up, but not with weight at birth, indicating that low body weight was an acquired problem. In this study, 28% of the children with bilateral spastic CP weighed less than 2 SD and 31% had a height of less than 2 SD. This percentage is comparable with the situation in developing countries such as Ethiopia and India, where more than 30% of children weigh less than 2SD. 37 A corresponding pattern was not found for BMI and this could be explained by the fact that low weight and short stature in combination, a frequent nding in malnutrition, can produce a BMI that is within normal limits for age. This was the case in 15%. Another 15% had a low BMI due to low body weight. Measuring growth in children with CP is a challenge. Skin-fold measures are recommended by some 18 but considered by others to overestimate the nutritional status, due to the muscle wasting in this group. Muscle wasting takes place especially in the legs, representing 25% of the body weight, and low weight in non-ambulant children with spastic quadriplegia has been explained by atrophy of the leg muscles because of non-use. 38 Malnutrition due to feeding problems and sometimes increased energy demands is an important factor for underweight in children with CP and, as shown in this survey, bilateral CP is no exception. The consequences for motor performance and other abilities, 39 such as cognitive function, need to be considered. 40,41 We conclude that the live birth prevalence of bilateral spastic CP has decreased since the mid-1980s, parallel to a decrease in the severity of the motor impairment. Since the mid-1970s, bilateral spastic CP has been dominated by children born preterm, while, in the 1990s, 70% of those performing at GMFCS levels IIII were born preterm. The severity of the motor impairment, which correlated with the degree of spasticity, has decreased during the last 15 years. The percentage of children with underweight and stunting is substantial, especially in those with a severe motor impairment. Acknowledgements This investigation was supported by grants from the Folke Bernadotte, the Linnea and Josef Carlsson, the Petter Silfvers- kio ld, the Gunvor and Josef Aner, the Sven Jerring and the Ha ggqvist Family Foundations and the Va stra Go taland Region. We are indebted to the Medical Birth Registry Ofce at the Swedish National Board of Health and Welfare for information on vital statistics. R E F E R E N C E S 1. Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral palsy in Sweden 19541970. I. Analysis of the general changes. Acta Paediatr Scand 1975;64:18792. 2. Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral palsy in Sweden 19541970. II. Analysis of the various syndromes. 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