An update on the prevalence of cerebral palsy: a systematic review and meta-analysis

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1 DEVELOPMENTAL MEDICINE & CHILD NEUROLOGY REVIEW An update on the prevalence of cerebral palsy: a systematic review and meta-analysis MARYAM OSKOUI 1 FRANZINA COUTINHO 2 JONATHAN DYKEMAN 3 NATHALIE JETT E 3 TAMARA PRINGSHEIM 4 1 Departments of Pediatrics and Neurology, McGill University, Montreal, Quebec; 2 School of Physical and Occupational Therapy, McGill University, Montreal, Quebec; 3 Department of Clinical Neurosciences and Hotchkiss Brain Institute, Department of Community Health Sciences and Institute of Public Health, University of Calgary, Calgary, Alberta; 4 Departments of Clinical Neurosciences and Pediatrics, University of Calgary, Calgary, Alberta, Canada. Correspondence to Dr Maryam Oskoui, Departments of Pediatrics and Neurology, McGill University, Montreal Children s Hospital, 2300 Tupper Street, A-512, Montreal, Quebec, Canada H3H 1P3. PUBLICATION DATA Accepted for publication 22nd October Published online 24th January AIMS The aim of this study was to provide a comprehensive update on (1) the overall prevalence of cerebral palsy (CP); (2) the prevalence of CP in relation to birthweight; and (3) the prevalence of CP in relation to gestational age. METHOD A systematic review and meta-analysis was conducted and reported, based on the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) statement. Population-based studies on the prevalence of CP in children born in 1985 or after were selected. Statistical analysis was carried out using computer package R, version RESULTS A total of 49 studies were selected for this review. The pooled overall prevalence of CP was 2.11 per 1000 live births (95% confidence interval [CI] ). The prevalence of CP stratified by gestational age group showed the highest pooled prevalence to be in children weighing 1000 to 1499g at birth (59.18 per 1000 live births; 95% CI ), although there was no significant difference on pairwise meta-regression with children weighing less than 1000g. The prevalence of CP expressed by gestational age was highest in children born before 28 weeks gestation ( per 1000 live births; 95% CI ; p<0.0327). INTERPRETATION The overall prevalence of CP has remained constant in recent years despite increased survival of at-risk preterm infants. Cerebral palsy (CP) encompasses a heterogeneous group of early-onset, non-progressive, neuromotor disorders that affect the developing fetal or infant brain. 1 CP is one of the most common causes of childhood physical disability, with an estimated lifetime cost, for persons born in the United States in 2000, of 11.5 billion dollars. 2 Accurate prevalence estimates are needed to guide operational health policies and to aid with appropriate resource allocation. In the past decade, two limited reviews on the prevalence of CP have been published. 3,4 The first, published in 2007, looked at both the overall prevalence of CP and the prevalence reported by birthweight in preterm infants. The overall median prevalence estimate reported was 2.4 per 1000 live births. 3 For preterm infants, a median prevalence of 11.2 per 1000 live births was reported among children weighing between 1500g and 2499g at birth, and 63.5 per 1000 live births among children weighing less than 1500g. This review did not follow the PRIS- MA (Preferred Reporting Items for Systematic Reviews and Meta-analyses) statement and had several methodological limitations. Only English-language articles were included, published between 1 January 1990 and 31 January 2005, searching a single bibliographic database (Pub- Med). A meta-analysis was not performed; rather, the overall prevalence estimates of selected studies were combined equally to provide a median estimate. Studies reporting prevalence estimates with different denominators (live births, neonatal survivors, children at a certain age) were combined, and studies including participants born before 1985 were included. A second systematic review, published in 2008, examined the prevalence of CP only in relation to gestational age and demonstrated a significant decrease in the prevalence of CP with increasing gestational age. 4 The prevalence ranged from 146 (95% confidence interval [CI] ) per 1000 children born at 22 to 27 weeks of gestation, steadily declining thereafter to an estimated 62 (95% CI 49 78) per 1000 children born at 28 to 31 weeks, 7 (95% CI 6 9) per 1000 at 32 to 36 weeks gestation, and 1.13 (95% CI ) per 1000 in term-born infants. This systematic review used rigorous methodology, searching four bibliographic databases (MEDLINE, CINAHL, Cochrane library, and Science The Authors. Developmental Medicine & Child Neurology 2013 Mac Keith Press DOI: /dmcn

2 Direct) with a clearly stated search strategy, including studies published from 1985 to 2006 and excluding those with participants born prior to A meta-analysis was performed, when possible, to provide pooled estimates of prevalence; however, the studies used various denominators, such as live births and neonatal survivors assessed at various ages, limiting the possibility of such pooling. A rigorous systematic review of the overall prevalence of CP is lacking in the literature. Furthermore, more published data have become available in recent years on CP prevalence, both overall and in at-risk populations. The goal of this study was to provide a comprehensive update on the prevalence of CP and to systematically review (1) the overall prevalence of CP; (2) the prevalence of CP in relation to birthweight; and (3) the prevalence of CP in relation to gestational age. METHOD Search strategy Two bibliographic databases (MEDLINE and EMBASE) were searched on 8 February 2011 to identify all potential citations related to the prevalence of CP published between 1985 and February Only studies presenting data on children born during 1985 or later were included, owing to considerable changes in perinatal care, and also because a more uniform definition of CP and routine use of imaging began in The search strategy was developed with the help of a health sciences librarian and adapted for MEDLINE and EMBASE (Appendix SI, supporting information published online). References from MEDLINE and EMBASE were combined and downloaded into a reference manager (Endnote X2). Abstracts of all references were screened independently by two reviewers (MO and FC) to select population-based studies on the prevalence of CP reporting cohorts of all live-born children, all preterm survivors, or expressed by gestational age or birthweight. Studies published in both French or English were included. When cohorts ranging before and after 1985 were reported, we included studies that allowed for a subgroup analysis of cohorts born after Studies reporting on a single subtype of CP (such as spastic diplegia only), conference proceedings, interventional studies, review articles, and case control studies not including full cohorts as cases were excluded. When multiple articles reporting data from the same study population were encountered, the most comprehensive study was selected. References of the two available systematic reviews were manually searched to identify further potential references. Two reviewers assessed study quality using a qualitative tool adapted from previously published scales (Appendix SII, supporting information published online). Studies with a quality score below 5 (range 1 4) were excluded (Table SI, supporting information published online); for articles included in the study, the mean score was 6. Disagreement pertaining to inclusion of articles was resolved by consensus between the two reviewers. What this paper adds This is the first worldwide CP prevalence estimate provided by meta-analysis. The overall prevalence of CP worldwide is 2.11 per 1000 live births. The prevalence of CP has remained constant in recent years, despite improved survival of at-risk preterm infants. Data extraction Two reviewers independently abstracted the following information on the methods and results from each article meeting all eligibility criteria: reference, year of publication, geographical location of the study, birth cohorts included, data sources, assessment of diagnosis and diagnostic criteria used, age at diagnosis, as well as the overall number of cases, population surveyed and denominator used (live births, neonatal survivors, children at a specified age). Data sources were also classified as population-based data (e.g. data from patient registries) or administrative data (e.g. data from physician billing diagnostic codes or hospital discharge summaries). Subgroup information for number of cases and numbers surveyed based on gestational age and birthweight was also collected. Data analyses It was decided a priori that a random effects model would be used to calculate the pooled prevalence of CP and 95% CIs for all predetermined groups. To assess for significant between-study heterogeneity, the Cochran s Q statistic was calculated and I 2 was used to quantify between-study heterogeneity; however, both measures of heterogeneity were used only descriptively and not in decision-making regarding model selection. 6 The following prevalence estimates were calculated: (1) the overall prevalence of CP in children at certain ages and in all live births; (2) the prevalence of CP in relation to four birthweight categories for live births (<1000g, g, g, and >2500g) and using three birthweight categories for neonatal survivors (<1500g, g, and >2500g); and (3) the prevalence of CP in extremely preterm newborn infants in relation to five gestational weeks (23wks, 24wks, 25wks, 26wks, and 27wks) and the prevalence of CP in relation to four gestational age categories (<28wks, 28 31wks, 32 36wks, and >36wks). Pairwise meta-regression analysis was performed to assess whether CP prevalence was significantly different between groups. Furthermore, to investigate whether the prevalence of CP had changed over time, meta-regressions were performed including terms for the start and end years of data collection for each study. These were chosen as surrogates for year-by-year prevalence estimates, which were often not provided by the studies. To address the decision to combine studies that included postneonatal cases with those that did not, a stratified analysis was completed to see whether these groups of studies were different from each other. A cumulative meta-analysis was conducted on the overall prevalence of CP per 1000 live births to assess the impact of studies published since the 510 Developmental Medicine & Child Neurology 2013, 55:

3 last review on the overall estimate. Publication bias was assessed using the Egger regression test, Begg and Mazumdar correlation test, and a visual inspection of funnel plots. A sensitivity analysis was also carried out to assess the effect of the methodological quality on the results. For all tests, p<0.05 was deemed to be significant. Statistical analyses were carried out in R version The meta package (version 2.1 0, 2012 was used to produce the pooled estimates and forest plots. In accordance with the random effects model, the studies were weighted according to the inverse of their variance along with the between-study heterogeneity (tau-squared) arrived at with a DerSimonian Laird estimator. The metafor package (installed in R) was used to conduct the meta-regression using restricted maximum likelihood estimation. 8 RESULTS Selected studies A total of 1521 references from MEDLINE and EMBASE were initially identified. A manual search of the references cited in two available systematic reviews of CP prevalence yielded an additional 16 abstracts. Duplicates were removed (323) and the remaining 1214 abstracts were screened, with 91 being selected for full-text review. Of these, 35 were excluded: two did not provide data on CP prevalence, one was a letter to the editor, seven did not provide data for sub-analysis of infants born in or after 1985, 13 had a quality score of 4 or less, and 12 were in languages other than English or French. The 13 studies excluded based on quality assessment are described in Table SI. Of the remaining 56 studies, seven were excluded because they presented data from the same study population, leaving a total of 49 studies included for the metaanalysis. The meta-analysis included 29 studies on overall CP prevalence and 20 on CP prevalence in preterm survivors (Table I). The selection process details are outlined in Figure 1. Overall prevalence of cerebral palsy The study by Sinha et al. 29 was excluded from analysis because it focused on a small ethnic community with a high rate of consanguinity that did not represent a true population-based estimate in the study region. Pooling 19 studies that reported estimates using live births as the denominator, the overall prevalence of CP was 2.11 per 1000 live births (95% CI ; Fig. 2a). The cumulative meta-analysis demonstrates that the overall prevalence of CP has remained stable with the addition of new studies over the past 10 years (Fig. 2b). There was no significant difference in overall prevalence per 1000 live births between studies using population-based data (1.93; 95% CI ) and studies using administrative data (2.19; 95% CI ). A meta-regression sorting the studies by start year of each cohort and end year of cohort was also conducted, and showed no significant difference by either start (p=0.34) or end year (p = 0.54). When assessing the importance of including postneonatal cases, the overall estimates of the two groups of studies were almost identical. Studies including these cases had a prevalence of 2.10 ( ) and those excluding the cases had a prevalence of 2.11 ( ). The overall prevalence appeared higher using studies reporting children at a specific age (range 18mo 8y) as the denominator (Fig. S1, supporting information published online), with a pooled prevalence of 2.91 per 1000 children (95% CI ). Prevalence of cerebral palsy by birthweight The pooled prevalence of CP in children per 1000 live births was calculated by birthweight category (Fig. 3). The prevalence was highest in children weighing 1000 to 1499g (59.18 per 1000 live births; 95% CI ), and lowest in children weighing over 2500g (1.33 per 1000 live births; 95% CI ). The prevalence among children weighing under 1000g was not significantly different from the prevalence among those weighing 1000 to 1499g (p=0.8159), but in both cases was significantly higher than among children weighing 1500 to 2499g (p<0.001). The prevalence among children weighing over 2500g was significantly lower than in all other birthweight groups (p<0.001). Three studies reported the prevalence of CP in relation to birthweight per 1000 neonatal survivors: (95% CI ) in children under 1500g, 8.33 (95% CI ) in children weighing between 1500g and 2499g, and 1.16 (95% CI ) in children weighing over 2500g. The prevalence of CP is significantly lower among children weighing between 1500g and 2499g than in those weighing under 1500g (p<0.001). Among children with a birthweight over 2500g the prevalence of CP was significantly lower than in all other groups (p<0.001). Prevalence of cerebral palsy in relation to gestational age The pooled prevalence per 1000 live births was calculated for each gestational age group (Fig. 4). The prevalence was highest, at (95% CI ), among children born before 28 weeks of gestation and lowest, at 1.35 (95% CI ), for children born after 36 weeks. Pairwise meta-regression showed that the prevalence of CP was significantly lower among children born between 28 and 31 weeks gestation than in children born before 28 weeks gestation (p=0.0327). Prevalence was significantly lower among children born between 32 and 36 weeks gestation than among those born more preterm (p<0.001), and was significantly lower among children born after 36 weeks gestation than in all other groups (p<0.001). There were fewer studies reporting the prevalence of CP in neonatal survivors in relation to gestational age group. The prevalence was (95% CI ) per 1000 neonatal survivors born before 28 weeks and (95% CI ) per 1000 neonatal survivors born between 28 weeks and 31 weeks; the number of studies Review 511

4 Table I: Selected studies. (a) Selected studies on overall cerebral palsy (CP) prevalence. (b) Selected studies on cerebral palsy prevalence in infants born preterm Reference Location Birth cohort Data/source Number methodology Age a with CP Number surveyed Prevalence per 1000 Denominator Quality scores (a) Rice et al. 9 Australia Administrative database Live births 6 Robertson et al. 10 Canada Administrative database Children at 8y 7 Smith et al. 11 Canada Administrative database Live births 7 Liu et al. 12 China Health care records Children <7y 7 Ravn et al. 13 Denmark Administrative database Live births 6 Sigurdardottir et al. 14 Iceland Administrative database and Live births 6 other sources Mongan et al. 15 Ireland Administrative database and other sources Neonatal survivors 7 Dolk et al. 16 Northern Ireland, UK Multiple sources: agencies, parents, MD Wichers et al. 17 Netherlands Administrative database and other sources > Live births 7 Any Children at 10y 7 Andersen et al. 18 Norway Administrative database Live births 6 Lie et al. 19 Norway Administrative database Live births 6 Hagberg et al. 20 Sweden Administrative database > Live births 6 Hagberg et al. 21 Sweden Administrative database > Live births 6 Himmelmann et al. 22 Sweden Hospital clinical chart review and other Himmelmann et al. 23 Sweden Hospital clinical chart review and rehabilitation reports Live births Live births 6 Hjern and Thorngren-Jerneck 24 Sweden Administrative database > Live births 5 Nordmark et al. 25 Sweden Hospital/chart review NA Live births 6 Westbom et al. 26 Sweden Administrative database Live births 7 and other sources Ozturk et al. 27 Turkey Multiple sources, confirmed > Live births 5 by two MDs Colver et al. 28 UK Administrative database Neonatal survivors 6 and other Sinha et al. 29 UK Administrative database Live births 5 > Live births 7 Surman et al. 30 UK Administrative database and other sources Pharoah et al. 31 Scotland, UK Hospital clinical chart review and other Arneson et al. 32 USA 1999 Administrative database and other sources Bhasin et al. 33 USA 1996, 2000 Hospital clinical chart review and other Live births Children at 5y Children at 8y 6 Petrini et al. 34 USA Administrative database Live births 6 Winter et al. 35 USA Administrative database and > Live births 5 other sources Yeargin-Allsopp et al. 36 USA 1994 Multiple sources Children at 8y 8 Reference Location Birth cohort Age a Number with CP Number surveyed Prevalence per 1000 Denominator per 1000 Quality score (b) Doyle et al. 38 Australia <28wks GA survivors at 2y 6 Doyle et al. 39 Australia wks GA survivors at 5y 6 Roberts et al. 40 Australia wks GA survivors at 8y Developmental Medicine & Child Neurology 2013, 55:

5 Table I: Continued Reference Location Birth cohort Age a Number with CP Number surveyed Prevalence per 1000 Denominator per 1000 Quality score Gray et al. 41 Australia wks GA survivors at 2y 6 Sutton et al. 42 Australia wks GA survivors at 12mo 6 Weber et al. 43 Austria <26wks GA survivors at 12mo 7 Robertson et al. 44 Canada wks GA live births 5 Vincer et al. 45 Canada wks GA live births 5 Lefebvre et al. 46 Canada wks GA survivors at 18mo 5 Jacobs et al. 47 Canada wks GA survivors at 18 24mo 5 Salokorpi et al. 48 Finland ELBW survivors at 4y 6 Tommiska et al. 49 Finland ELBW survivors at 2y 6 Beaino et al. 50 France wks GA survivors at 5y 7 Marret et al. 51 France wks GA survivors at 5y 5 Burguet et al. 52 France wks GA survivors at 2y 6 Valleur et al. 53 France <28wks GA survivors at 6y 5 Were and Bwibo 54 Kenya Not provided BW g survivors at 2y 5 Leversen et al. 55 Norway wks GA, BW g survivors at 2y 6 Marlow et al. 56 UK and Ireland <26wks GA survivors at 6y 6 Vohr et al. 57 USA wks GA survivors at 18mo 6 a Age: age at ascertainment (years). The study by Serdaroglu et al. 37 was excluded from analysis. This study was based in Turkey on a parental questionnaire for children born in Out of children surveyed, 186 were identified with CP, yielding a prevalence of 4.4 per 1000 children aged 2 16y. MD, physicians; NA, not available. GA, gestational age; ELBW, extremely low birthweight; BW, birthweight. was too small to calculate a pooled prevalence in older gestational age groups. Prevalence of cerebral palsy per gestational week in extremely preterm infants The pooled prevalence per 1000 neonatal survivors at a predetermined age was calculated per gestational week from 23 to 27 weeks (see Fig. S2, supporting material published online). The pooled prevalence was highest in children born at 23 weeks gestation (261.42; 95% CI ) and lowest in children born at 27 weeks gestation (102.70; 95% CI ). Pairwise metaregression showed that the prevalence among children born at 27 weeks gestation was significantly lower than that among children born at 23 weeks gestation (p=0.0063). Evaluation of potential bias For the overall prevalence estimate of CP per 1000 live births, no significant publication bias was detected on visual inspection of funnel plots of the standard error by the logit of the prevalence rate and supported by statistical testing. For the Begg and Mazumdar rank correlation test, Kendall s tau-b is (p-value ). Egger s regression test showed an intercept of (95% CI to ), with t= , df=20 (p-value ). For the prevalence estimate of CP in preterm survivors, no significant publication bias was detected on visual inspection of funnel plots of the standard error by the logit of the prevalence rate and supported by statistical testing. For the Begg and Mazumdar rank correlation test, Kendall s tau-b is (p-value ). Egger s test showed an intercept of (95% CI to ), with t= , df=17 (p-value ). In our selection process, 12 studies were excluded based on language: three were written in Spanish, five in Chinese, one in Polish, two in Japanese, and one in German. Of these, two presented data on live births, five presented data on children at a particular age, of which three reported on the same population, and four presented data on preterm survivors. DISCUSSION Main findings This study, through a systematic review and meta-analysis of the available literature, provides an updated estimate of the overall prevalence of CP, as well as its relationship with gestational age and birthweight. The most commonly reported denominators were live births, neonatal survivors, and survivors at a predetermined age. Overall prevalence estimates were similar using live births or neonatal survivors; however, in the preterm subgroup the estimates are expected to differ as perinatal mortality is higher among preterm infants have in term-born newborn infants. There were fewer studies reporting the prevalence of CP per neonatal survivors in relation to gestational age group. The Review 513

6 Included Eligibility Screening Identification Records identified through database searching (n=1521) Additional records identified through other sources (n=16) Records after duplicates removed (n=1214) Records excluded (n=1137) Full-text articles excluded, Full-text articles assessed with reasons (n=35) for eligibility 2: No data on cerebral palsy (n=91) prevalence 1: Letter 7: Articles Eligible studies meeting 7: Sub analysis for children excluded as data inclusion criteria born after 1985 not on same study (n=56) possible populations 13: Quality score 4 or less 12: Studies in other languages Studies included in quantitative synthesis (meta-analysis) (n=49) Figure 1: Flow chart of study selection. pooled estimate for children born at gestational age 28 to 31 weeks is unexpectedly higher than children born at a gestational age of less than 28 weeks; however, there were fewer studies reporting the former group and the pooled estimate shows a larger confidence interval, and this difference was not significant in a pairwise meta-regression analysis. Most studies reporting estimates on preterm survivors were based on population-based registries following groups of infants born preterm. For overall prevalence, sources of case ascertainment varied considerably between studies. Most European studies used population-based patient registries with multiple sources of case ascertainment and uniformly applied diagnostic inclusion criteria. In North America, several states reported data from population-based registries; however, both Canadian studies used administrative databases with ICD-9 codes as diagnostic criteria. Prospective population-based patient registries are favoured as more validated data sources, but they are associated with higher operational costs than large pre-existing administrative databases. It is encouraging, however, that estimates from population-based studies and administrative data did not differ significantly in our analysis. Although prevalence estimates were comparable across geographic sites and cultural groups, one study that was excluded from analysis reported prevalence estimates that were much higher. 29 This study focused on a British ethnic community (Bradford District Health Authority) with a high rate of consanguinity, highlighting the potential genetic aetiology in this population. The overall prevalence of CP estimate in our review is 2.11 per 1000 live births, consistent with the prevalence reported by an earlier review without meta-analysis. 3 This prevalence was also shown to have remained constant in recent years with the addition of new published studies. A number of factors may contribute to an increased prevalence of CP, such as a improved survival in preterm infants and higher numbers of multiple births, which often result in preterm births. There are also a number of factors that may contribute to a decreased prevalence of CP, such as the use of antenatal corticosteroids, cooling for term-born 514 Developmental Medicine & Child Neurology 2013, 55:

7 (a) Study Prevalence 95% CI Study Prevalence 95% CI (b) Hagberg, [2.06; 2.70] Adding Hagberg, 1996 (k = 1) 2.36 [2.07; 2.70] Pharoah, 1998 Hagberg, 2001 Nordmark, 2001 Winter, 2002 Surman, 2003 Himmelmann, 2005 Dolk, 2006 Westbom, 2007 Ozturk, 2007 Smith, 2008 Andersen, 2008 Hjern, 2008 Rice, 2009 Sigurdardottir, 2009 Petrini, 2009 Ravn, 2010 Lie, 2010 Himmelmann, [1.99; 2.21] Adding Pharoah, 1998 (k = 2) 2.19 [1.96; 2.44] 2.12 [1.86; 2.40] Adding Hagberg, 2001 (k = 3) 2.15 [2.02; 2.28] 2.21 [1.87; 2.60] Adding Nordmark, 2001 (k = 4) 2.14 [2.05; 2.23] 2.00 [1.82; 2.19] Adding Winter, 2002 (k = 5) 2.11 [2.03; 2.21] 2.04 [1.89; 2.21] Adding Surman, 2003 (k = 6) 2.10 [2.02; 2.17] 1.92 [1.65; 2.24] Adding Himmelmann, 2005 (k = 7) 2.09 [2.02; 2.16] 2.17 [1.99; 2.36] Adding Dolk, 2006 (k = 8) 2.10 [2.03; 2.17] 2.73 [2.45; 3.04] Adding Westbom, 2007 (k = 9) 2.17 [2.04; 2.31] 1.12 [0.91; 1.36] Adding Ozturk, 2007 (k = 10) 2.06 [1.89; 2.26] 2.68 [2.45; 2.92] Adding Smith, 2008 (k = 11) 2.11 [1.93; 2.32] 2.10 [1.89; 2.32] Adding Andersen, 2008 (k = 12) 2.11 [1.94; 2.30] 1.79 [1.70; 1.88] Adding Hjern, 2008 (k = 13) 2.08 [1.91; 2.27] 2.20 [1.97; 2.45] Adding Rice, 2009 (k = 14) 2.09 [1.93; 2.27] 2.29 [1.92; 2.70] Adding Sigurdardottir, 2009 (k = 15) 2.10 [1.94; 2.27] 2.53 [2.27; 2.80] Adding Petrini, 2009 (k = 16) 2.13 [1.97; 2.29] 2.16 [2.02; 2.30] Adding Ravn, 2010 (k = 17) 2.13 [1.99; 2.28] 1.82 [1.71; 1.94] Adding Lie, 2010 (k = 18) 2.11 [1.97; 2.26] 2.17 [1.87; 2.50] Adding Himmelmann, 2010 (k = 19) 2.11 [1.98; 2.25] Pooled totals 2.11 [1.98; 2.25] Pooled totals 2.11 [1.98; 2.25] I squared = 89.5%, Q = 171.8, df = 18, p < Figure 2: Overall prevalence of cerebral palsy per 1000 live births. asphyxiated infants, and the use of magnesium sulphate. Contributing genetic aetiologies may either be increasing or decreasing. The analysis of CP based on birthweight showed, as expected, that the prevalence decreases significantly among children born with a birthweight above 1500g. This prevalence estimate was similar irrespective of the denominator used in the calculation, that is per 1000 live births or per 1000 neonatal survivors. One of the reasons for this similarity in prevalence estimates could be the small number of high-quality studies included that report prevalence of CP using neonatal survivors as the denominator and inclusion of term-born low-birthweight infants, among whom mortality may be lower. As reported in an earlier meta-analysis, the prevalence of CP shows an inverse relationship to gestational age. 4 The prevalence estimate for preterm births varied significantly based on the denominator, though a decline in CP prevalence was observed with increased gestational age. 3,4 When reported as a proportion of neonatal survivors, the prevalence estimates were, as expected, larger than the corresponding estimates reported as a proportion of live births, although these proportions revealed a similar declining trend with increasing gestational age. Strengths and limitations This review is based on rigorous methods and quality assessment of the selected studies. Efforts were made to report the meta-analysis based on the PRISMA statement. 58 Additionally, analysis using the random effects model aimed to account for heterogeneity between studies. In comparison with previous reviews, our meta-analysis analysed a greater number of studies, used only data from study cohorts born in or after 1985 to account for changes in clinical practice, and computed pooled prevalence estimates based on comparable common denominators. All efforts were made to adjust for potential bias. Though many studies used administrative data, the diagnosis of CP based on ICD-9 coding has not, to our knowledge, been validated in these databases. Administrative databases are susceptible to limitations such as inaccuracy in diagnostic code entry, resulting in possible misclassification bias, multiple entries from varying sources, a lack of universal case definitions, and financial incentives in coding in some countries. 59 North American studies are also restricted to a few provinces or states, with questionable generalizability of the available data to the rest of the country, where demographic and social variables may differ. There was significant heterogeneity across studies, and an attempt was made to adjust for this by using a random effects model and by pooling only studies with similar denominators. There were several factors contributing to potential selection bias in our review. First, there is a potential ascertainment bias by individual studies using different definitions and age at diagnosis of CP without reference to functional severity. Mortality in the first years of life would lead to exclusion of more severe cases, while a late age of diagnosis or ascertainment only through rehabilitation facilities may exclude milder cases. This may have had an impact Review 515

8 (a) (b) Study Prevalence 95% CI Study Prevalence 95% CI Hagberg, [26.08; 81.52] Hagberg, [29.59; 96.79] Himmelmann, [47.63; ] Himmelmann, [31.40; 97.62] Lie, [69.03; ] Nordmark, [23.12; 92.79] Pharoah, [33.35; 51.71] Surman, [31.33; 57.15] Hagberg, [58.48; ] Hagberg, [46.17; 96.53] Himmelmann, [34.44; 81.29] Himmelmann, [25.33; 70.40] Lie, [57.15; 79.95] Nordmark, [23.39; 65.11] Pharoah, [50.16; 64.90] Smith, [38.83; 70.60] Surman, [45.16; 66.01] Pooled totals [43.38; 73.95] Pooled totals [53.06; 66.01] I squared = 75%, Q = 28, df = 7, p = I squared = 38.7%, Q = 13.1, df = 8, p = Birthweight <1000g (c) (d) Study Prevalence 95% CI Study Prevalence 95% CI Birthweight g Dolk, [9.82; 12.89] Hagberg, [8.33; 15.23] Hagberg, [10.16; 18.56] Himmelmann, [4.22; 10.17] Himmelmann, [6.62; 13.95] Lie, [10.74; 14.32] Nordmark, [4.46; 11.53] Pharoah, [9.30; 11.40] Sigurdardottir, [10.84; 23.11] Smith, [7.93; 12.49] Surman, [8.19; 11.15] Winter, [4.89; 7.52] Dolk, 2006 Hagberg, 2001 Hagberg, [1.12; 1.35] 1.25 [1.05; 1.48] 1.37 [1.14; 1.64] Himmelmann, [0.98; 1.47] Himmelmann, [1.19; 1.72] Lie, 2010 Nordmark, 2001 Petrini, 2009 Pharoah, 1998 Smith, 2008 Surman, 2003 Winter, [1.06; 1.25] 1.40 [1.12; 1.73] 2.10 [1.86; 2.36] 1.14 [1.06; 1.23] Sigurdardottir, [1.01; 1.61] 1.79 [1.59; 1.99] 1.16 [1.04; 1.29] 1.10 [0.96; 1.26] Pooled totals [8.94; 11.58] Pooled totals 1.33 [1.19; 1.49] I squared = 78.1%, Q = 50.2, df = 11, p < I squared = 90.9%, Q = 132, df = 12, p < Birthweight g Birthweight >2500g Figure 3: Prevalence of cerebral palsy (CP) in relation to birthweight. (a) Birthweight less than 1000g; (b) birthweight between 1000g and 1499g; (c) birthweight between 1500g and 2500g; (d) birthweight over 2500g. on the numerator, though the extent of impact cannot be established. Furthermore, estimating the impact on health care costs and planning of services would need to take into consideration the severity of dysfunction in affected children, which is not provided in most studies. A second potential source of selection bias is referral filter bias, as some studies reported cases from academic institutions, which may impose a bias in access to care. In this meta-analysis, data from 8 of the 48 studies were hospital based. These hospital-based studies were included as the institutes were considered to be centres of excellence and representative of the population they served. A third potential source of selection bias is publication bias. Although efforts were made to make the search strategy as comprehensive as possible, the search did not include unpublished material or data from the grey literature. However, based on inspection of funnel plots and supported by statistical testing, we did not find significant evidence of publication bias for either the overall prevalence estimate or the estimate in premature survivors. The fourth potential source of selection bias in this review is language bias, as only studies published in English and French were selected. The impact of excluding studies published in languages other than English has been 516 Developmental Medicine & Child Neurology 2013, 55:

9 (a) Study Prevalence 95% CI Study Prevalence 95% CI (b) Hagberg, 2001 Hagberg, 1996 Himmelmann, 2005 Himmelmann, 2010 Hjern, 2008 Nordmark, 2001 Sigurdardottir, [54.97; ] [49.75; ] [44.39; ] [29.03; 95.03] [49.02; 71.46] [37.91; ] [41.99; ] Weber, [157.52; ] Hagberg, [43.90; 80.81] Hagberg, [36.89; 74.71] Himmelmann, [25.79; 60.04] Himmelmann, [27.61; 65.47] Hjern, [24.57; 32.85] Marret, [39.39; 68.55] Nordmark, [18.13; 52.54] Pooled totals [54.49; ] Pooled totals [32.70; 56.94] I squared = 91.1%, Q = 78.3, df = 7, p < I squared = 83.3%, Q = 35.9, df = 6, p < Gestational age <28 weeks Gestational age weeks (c) Study Prevalence 95% CI Study Prevalence 95% CI (d) Hagberg, 2001 Hagberg, 1996 Himmelmann, 2005 Himmelmann, 2010 Hjern, [4.28; 8.63] 7.79 [5.52; 10.68] 6.66 [4.53; 9.44] 6.09 [4.05; 8.79] 3.34 [2.80; 3.95] Marret, [13.40; 30.32] Nordmark, [2.63; 7.46] Petrini, [5.60; 9.38] Hagberg, [1.06; 1.49] Hagberg, [1.12; 1.62] Himmelmann, [0.89; 1.36] Himmelmann, [1.18; 1.72] Hjern, [1.01; 1.16] Nordmark, [1.12; 1.73] Petrini, [1.76; 2.26] Sigurdardottir, [0.96; 1.55] Topp, [1.28; 1.74] Pooled totals 6.75 [4.59; 9.94] I squared = 92.2%, Q = 90.1, df = 7, p < Gestational age weeks Pooled totals 1.35 [1.15; 1.59] I squared = 90.5%, Q = 84.2, df = 8, p < Gestational age >36 weeks Figure 4: Prevalence of cerebral palsy (CP) in relation to gestational age per 1000 live births. (a) Gestational age less than 28 weeks; (b) gestational age between 28 weeks and 31 weeks; (c) gestational age between 32 weeks and 36 weeks; (d) gestational age over 36 weeks. shown to have generally little effect on summary treatment effect estimates. 60 In our selection process, 12 studies were excluded based on language. A language bias cannot be excluded. CONCLUSIONS This meta-analysis provides updated prevalence estimates of CP across different populations, showing a constant overall estimate per live births in recent years despite the addition of new data and increased survival of at-risk preterm infants. Although the prevalence of disease is unchanged, future studies are needed to evaluate a change over time in the phenotypic spectrum of CP. Studies on the prevalence of CP in adolescence and adulthood would also be important future goals as the majority of children with CP are expected to survive into adulthood. Further studies are also needed in North America and Canada, as the available data are restricted to a few regions, principally regions in Canada. Direct comparison of case ascertainment from patient registries and administrative databases is needed to establish the validity of the diagnosis of CP in the latter, as administrative databases are increasingly used for surveillance because of their larger sampling frame, lower operational cost, and availability of longitudinal data. Accurate and updated prevalence estimates are imperative in estimating the burden of illness and planning appropriate health resource allocation for this vulnerable patient population. ACKNOWLEDGEMENTS This study was funded by an operational grant from the Public Health Agency of Canada (PHAC) in conjunction with the Neu- Review 517

10 rological Health charities of Canada (NHCC).The PHAC and the NHCC did not participate in the design and conduct of the study; in the collection, analysis, and interpretation of the data; or in the preparation, review, or approval of the manuscript. DISCLOSURES N Jette is an Alberta Innovates Health Solutions Population Health Investigator and holds a Canada Research Chair Tier 2 in Neurological Health Services Research. T Pringsheim receives salary/research support from Alberta Health and Wellness, the Canadian Institute of Health Research, and the Public Health Agency of Canada. SUPPORTING INFORMATION Additional supporting information may be found in the online version of this article: Appendix SI: Description of the search strategy. Appendix SII: Quality assessment tool. Table SI: Description of excluded studies based on quality assessment. Figure S1: Overall prevalence of CP per children at a specified age. 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