07singhi (906) 24/4/02 12:15 pm Page 162 Clinical Spectrum of Cerebral Palsy in North India—An Analysis of 1000 Cases by Pratibha D. Singhi,a Munni Ray,a and Gunmala Surib Department of Pediatrics, Postgraduate Institute of Medical Education and Research, Chandigarh, India b University Business School, Punjab University, Chandigarh, India a Summary One thousand children with cerebral palsy (CP) were reviewed to study their clinical profile, etiological factors and associated problems. Spastic quadriplegia constituted the predominant group (61 per cent), followed by spastic diplegia (22 per cent). Dyskinetic CP was present in 7.8 per cent of the cases. Acquired CP, particularly secondary to nervous system infections, constituted a significant proportion of cases. The clinical spectrum of CP is different in developing countries compared with developed countries. Associated problems were present in a majority (75 per cent) of cases, of which mental retardation was the commonest (72.5 per cent). Comprehensive assessment and early management of these problems are emphasized, which can minimize the extent of disabilities. Introduction Changes in the epidemiology of cerebral palsy (CP) have been reported from developed countries.1–3 Advances in perinatology have led to increasing survival of preterms and a change in the distribution of clinical types of CP.4,5 For the developing countries no accurate data regarding incidence, prevalence or clinical spectrum of CP is available. The purpose of this study was to evaluate the clinical profile of CP and to determine the associated risk factors among North Indian children. Materials and Methods The study included 1000 consecutive children with CP who were seen at The Rehabilitation Centre for Disabled Children, Chandigarh from 1985 to 1993. The Centre provides assessment and intervention services to children with various types of disabilities brought from all over North India after referral from hospitals and doctors, or directly from the community by the parents. Cerebral palsy was defined as a non-progressive disorder that manifests as abnormality of motion and posture and results from a central nervous system injury sustained in the early period of brain development, usually defined as the first 3 or 5 years of life.6 A detailed history was taken from the mother using a prestructured proforma followed by a complete physical, developmental and neurological examin- Correspondence: Dr Pratibha D. Singhi, Department of Pediatrics, Postgraduate Institute of Medical, Education and Research, Chandigarh, India. Fax 91–0172–744401. E-mail <[email protected]. nic.in>. 162 Journal of Tropical Pediatrics ation. For labeling a child as having birth asphyxia, Apgar scores when available were considered. In the absence of these, the following criteria were used: (i) history of delayed cry > 5 min after birth; (ii) baby turning blue and requiring oxygen therapy with baby having difficulty in respiration, lethargy and/or seizures within 72 h of birth. Protein energy malnutrition (PEM) was graded according to the criteria proposed by the Nutrition Sub-Committee of Indian Academy of Pediatrics (1972),7 by expressing the weight of the child as a percentage of the expected and classifying as follows: normal, > 80 per cent; grade I, 71–80 per cent; grade II, 61–70 per cent; grade III, 50–60 per cent; grade IV, < 50 per cent of expected weight for age. Sociodemographic and family structure details were recorded. Assessment of intelligence/development quotient (IQ/DQ) and an ENT and ophthalmologic evaluation was performed in all children. The cases of CP were classified, using the Swedish classification, into spastic (tetraplegia, diplegia, hemiplegia), ataxic and dyskinetic (including athetosis; dystonia) and mixed.8 The etiological classification was also used as: (i) congenital (prenatal, perinatal and mixed pre- and perinatal causes); and (ii) acquired CP occurring in a child born normally and due to identifiable factors acquired after birth. Clinical psychologists conducted psychometric evaluations and children were categorized into mild (IQ = 50–70), moderate (IQ = 30–50) and severe (IQ < 30) mental retardation. All children were screened for a hearing defect, and in those suspected of having a hearing loss formal audiometry was done. Children with active seizures or with a definite history of recurrent seizures were considered to have epilepsy. Behavioural problems were considered significant if Vol. 48 June 2002 Oxford University Press 2002 07singhi (906) 24/4/02 12:15 pm Page 163 P. D. SINGHI ET AL. they were severe enough to be perceived as problems by parents or interfered with therapy or education. All children were also evaluated by a team of therapists, provided appropriate rehabilitation, and were periodically followed-up. Data were entered in Foxpro and descriptive statistics were calculated using SPSS software package. Results The age at the time of presentation ranged from 2 months to 16 years (mean age: 36.4 ± 31.9 months). A male preponderance was noted (67.5 per cent). About half (50.2 per cent) of the patients were below 2 years of age at the time of their first visit, 34.2 per cent were between 2 and 5 years, and 15.6 per cent were above 5 years of age. The presenting problems were delay in motor milestones (88.8 per cent), delayed speech (47.6 per cent), seizures (28.1 per cent), and behavior problems. The majority of the cases were congenital (77 per cent). Antenatal problems (Fig. 1) were reported in 25 per cent of the mothers. In 33.6 per cent of cases the deliveries were conducted at home; 85 per cent were normal vaginal deliveries, 9.9 per cent were caesarian section. 1.5 per cent were breech, 3.7 per cent required instrumentation; 86.8 per cent were term, and 13.2 per cent were preterm. Delayed cry was reported in 49.2 per cent cases. About half (49.6 per cent) of the children were first borns; 27.6 per cent were second, and 22.8 per cent were third in birth order. The predisposing neonatal factors are shown in Table 1. Of the 23 per cent cases of acquired CP, 63.5 per cent were due to TABLE 1 Neonatal factors predisposing to cerebral palsy Prematurity Birth asphyxia Neonatal convulsions Neonatal septicemia Neonatal jaundice Low birthweight Twins CP cases (n = 1000) % 132 453 252 146 215 204 12 13.2 45.3 25.2 14.6 21.6 20.4 1.2 CNS infections such as meningitis and encephalitis, and 30.1 per cent were due to bilirubin encephalopathy (secondary to Rh incompatibility or G6PD deficiency) and 2.7 per cent due to head injury. The distribution of cases of CP is shown in Table 2; 70 per cent were spastic and 61 per cent had quadriplegia. The associated problems as seen in the whole group are shown in Table 3 and those in relation to types of CP are shown in Table 4. About half (50.6 per cent) of cases were malnourished; 28.1 per cent had grades III and IV malnutrition. Children with mixed CP were most malnourished (68.35 per cent) followed by those with athetoid (59.50 per cent), hypotonic/ataxic (51.95 per cent), and spastic (42.86 per cent) CP. Children with spastic hemiplegia were least malnourished (36.18 per cent). Most children (88.6 per cent) had a head circumference less than a 2 SD of normal. Mental retardation was seen in 72.5 per cent cases; 42.7 per cent had severe, 26.0 per cent moderate, and 31.3 per cent had mild mental retardation. All cases of mixed CP and athetoid CP had mental retardation compared with 62.5 per cent of cases of spastic and 75.3 per cent of cases of hypotonic CP. Convulsions were seen in 327 children, most commonly in those with spastic hemiplegia (42.0 per cent), diplegia (32.5 per cent), quadriplegia (31.6 per cent), mixed (35.3 per cent), hypotonic (25.9 per cent), and athetoid (27.4 per cent) CP. The various types of seizures seen as depicted in Fig. 2. TABLE 2 Distribution of types of cerebral palsy cases Type of cerebral palsy FIG. 1. Antenatal complications in mothers of children with cerebral palsy. , Antepartum hemorrhage; , fever; , pre-eclamptic toxemia; , drugs; , other. Journal of Tropical Pediatrics Vol. 48 June 2002 Spastic Quadriplegia Diplegia Hemiplegia Right Left Dyskinetic/athetoid Hypotonic/ataxic Mixed n 700 427 154 119 58 61 84 77 139 % 70 61 22 17 8.4 7.7 13.9 163 07singhi (906) 24/4/02 12:15 pm Page 164 P. D. SINGHI ET AL. TABLE 3 Associated problems in children with cerebral palsy Associated problems Mental retardation Speech disorder Visual disorder Hearing disorder Convulsions Behavior problems Malnutrition n % 725 78 410 140 327 72 506 72.5 7.8 41.0 14.0 32.0 7.2 50.6 FIG. 2. Types of seizures in children with cerebral palsy. , Generalized tonic clonic; , focal; , atonic; , unclassified; , myoclonic. Ocular defects were found in 41 per cent of children. These were found more commonly in children with dyskinetic CP (45.24 per cent) followed by mixed (43.9 per cent), spastic (38.0 per cent), and hypotonic (20.9 per cent) CP. Refractory errors were detected in 48 per cent of cases. Hypermetropia was more common than myopia. Strabismus was found in 24.5 per cent cases; 84 per cent had convergent and 16 per cent had divergent squint. Optic atrophy (10.87 per cent), nystagmus (4 per cent), and cataracts (3.9 per cent) were also seen. Ptosis, corneal opacity, chorioretinitis and cortical blindness were seen in 2–4 per cent cases. Speech delay was reported in 82 per cent of cases of cerebral palsy. Hearing loss and speech motor problems were most commonly seen in dyskinetic CP. Discussion The preponderance of spastic cerebral palsy cases in our study is similar to that reported by others.10 However, distribution of the clinical types of spastic cases was very different. Whereas spastic diplegia is generally the commonest form reported from developed countries,1 in our series spastic quadriplegia was most commonly seen, as is also seen in other developing countries. In developed countries, a progressive decrease in spastic quadriplegia and a relative increase in spastic diplegia has been attributed to the decrease in perinatal mortality rate, with increasing survival rates of extremely premature infants.4,5 This situation has not yet been achieved in our country except in a few tertiary care centres. Other studies from more developed countries have found hemiplegia to be the commonest form of spastic CP.10 In our study this was seen in only17 per cent cases. While athetoid CP, particularly secondary to neonatal hyperbilirubinemia, has virtually disappeared from many parts of the world, it still constitutes a significant proportion of CP cases in India, and 41.6 per cent of our cases had a history of significant neonatal jaundice. The role of perinatal complications, in particular TABLE 4 Associated problems in relation to types of cerebral palsy Types of CP Spastic quadriplegia Spastic hemiplegia Spastic diplegia Mixed Hypotonic/ ataxic Athetoid dyskinetic 164 Total Seizures Mental retardation Speech defects Visual defects Hearing defects Microcephaly Malnutrition Behavior problems 427 135 (31.6%) 50 (32.5%) 50 (42.0%) 49 (35.3%) 20 (25.9%) 23 (27.4%) 276 (64.6%) 73 (61.3%) 95 (61.7%) 139 (100%) 58 (75.3%) 84 (100%) 31 (7.3%) 8 (6.7%) 10 (6.5%) 14 (10.1%) 6 (7.8%) 9 (10.7%) 181 (42.4%) 32 (26.9%) 69 (44.8%) 61 (43.9%) 29 (20.9%) 38 (45.2%) 58 (13.6%) 12 (10.1%) 16 (10.4%) 14 (10.1%) 12 (15.6%) 28 (33.3%) 399 (93.3%) 106 (89.1%) 119 (77.3%) 124 (89.2%) 72 (95.3%) 66 (78.6%) 212 (49.7%) 43 (36.1%) 66 (42.9%) 95 (68.4%) 40 (52.0%) 50 (59.5%) 28 (6.55%) 11 (9.2%) 10 (6.5%) 8 (5.8%) 7 (9.1%) 8 (9.5%) 119 154 139 77 84 Journal of Tropical Pediatrics Vol. 48 June 2002 07singhi (906) 24/4/02 12:15 pm Page 165 P. D. SINGHI ET AL. birth asphyxia, in the causation of CP has been challenged.11,12 However, we found history indicative of birth asphyxia in a large number of cases. This is similar to other studies from Nigeria, Malta, and other developing countries.13–15 Occurrence of severe birth asphyxia, which is rarely seen in developed countries, continues to be a major problem in many developing countries where obstetric facilities are virtually non-existent for a vast majority of women in rural areas. Several studies have reported a significant association between low birthweight and cerebral palsy.11,12,16,17 Higher survival rate of preterm, low birthweight infants, usually attributed to more advanced obstetric care, is associated with a higher rate of CP in these infants.18 However, unlike western figures, most children in our study were term babies. Acquired cases of CP, particularly secondary to CNS infections and bilirubin encephalopathy, constitute a significant proportion of CP in our country as well as other developing countries.19,20 Although a direct causative role of antenatal problems cannot be commented on with certainty, they were reported in a third of cases. A significant association between antepartum hemorrhage and cerebral palsy has been reported11,16 and refuted.12,18 Toxemia in the mother as a risk factor for cerebral palsy in the baby has been found by several authors.11,12 A large proportion of mothers gave history of fever in the early antenatal period; however, tests for intrauterine infections in their babies were negative. Most of the babies in our study were born by normal vaginal delivery. Instrument-assisted delivery18 and caesarian section10,21 have been associated with cerebral palsy,18 but others have differed on this.10,22 Multiple pregnancy has been considered an important prenatal risk factor for CP.10 However, in our study only four pairs of twins were identified. Almost all children with cerebral palsy have at least one additional disability associated with damage to CNS.23 Approximately two-thirds of children with cerebral palsy have mental retardation.6 Our findings are in accordance with this. Children with spastic quadriplegia and mixed type of cerebral palsy have the worst intellectual outcome. Epilepsy in children with cerebral palsy occurs frequently.24 Seizures are reported to be least common in children with choreoathetoid and ataxic types of CP,25 as was also found in our study. Most epileptic patients with cerebral palsy have locationrelated epilepsies; focal and generalized seizures dominate the clinical picture.24 Although generalized seizures were commonest, 32 per cent of our children had myoclonic seizures – this figure is higher than that described in literature.26 Epilepsy was Journal of Tropical Pediatrics Vol. 48 June 2002 significantly more common in those children with cerebral palsy who had mental retardation (85.4 per cent) compared with those without mental retardation (14.6 per cent). The poor nutritional status of children in the study is explained by feeding problems, gastroesophageal reflux, inability to independently access food or communicate hunger and constipation.27,28 Hearing loss and dysarthria, seen in our children with dyskinetic or mixed CP, were similar to that reported in the literature.29 Ocular problems and difficult behavior were other problems requiring intervention. In conclusion the spectrum of CP in North India differs from that seen in the West. The shift to predominant involvement of preterm survivors is still not apparent. Severe birth asphyxia is an important predisposing factor for CP. Acquired CP, particularly secondary to CNS infections and kernicterus, constitutes a significant proportion of CP cases. Targeting the preventable causes of CP may help reduce, to some extent, the enormous problem of childhood disability in the country. References 1 Riikonen R, Raumavrita S, Sinivuori E, Seppala T. Changing pattern of cerebral palsy in the southwest region of Finland. Acta Paediatr Scand 1989; 78: 581–87. 2 Pharoah POD, Platt MJ, Cooke T. The changing epidemiology of cerebral palsy. Arch Dis Child 1996; 75: F169–73. 3 Stanley F, Blair E, Alberman E. How common are the cerebral palsies? In Bax MCO, Hart HM (eds), Cerebral Palsies: Epidemiology and Causal Pathways. MacKeith Press, Suffolk, 2000: pp. 22–39. 4 Hagberg B, Hagberg G, Zetterstrom R. Decreasing perinatal mortality—increasing in cerebral palsy morbidity. Acta Paediatr Scand 1989; 78: 664–70. 5 Hagberg B, Hagberg G. The changing panorama of infantile hydrocephalus and cerebral palsy over forty years. A Swedish survey. Brain Dev (Tokyo) 1989; 11: 368–73. 6 Eicher PS, Batshaw M. Cerebral palsy. Pediatr Clin North Am 1993; 40: 537–51. 7 Nutrition subcommittee of Indian Academy of Pediatrics. Classification of Protein Calorie Malnutrition. Indian Paediatr 1972; 9: 360. 8 Hagberg B, Hagberg G, Olow I. The changing panorama of cerebral palsy in Sweden. I. Prevalence and origin during the birth year period 1983–1986. Acta Paediatr 1993; 82: 387–93. 9 Makwabe CM, Mgone CS. The pattern and etiology of cerebral palsy as seen in Dares-Salam, Tanzania. East Afr Med J 1984; 12: 896–99. 10 O’Reilly DE, Walentynawicz JE. Etiological factors in cerebral palsy. A historical review. 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Epilepsy and cerebral palsy. In: Aicardi J (ed.), Epilepsy in Children, 2nd edn. Raven Press, New York, 1994; 350–51. 25 Crothers B, Paine RS. The Natural History of Cerebral Palsy. Harvard University Press, Cambridge, MA, 1959. 26 Zafeiriou DI, Kontopoulos EE, Tsikoulas I, Anastasiou A. Epilepsy and EEG findings in congenital hemiplegia: long term outcome (Abstract). Epilepsy 1996; 37 (Suppl 4): 110. 27 Rempel GR, Colwell SO, Nelson RP. Growth in children with cerebral palsy fed via gastrostomy. Paediatrics 1988; 82: 857–62. 28 Jones PM. Feeding disorders in children with multiple handicaps. Dev Med Child Neurol 1989; 31: 404–6. 29 Cohen BA, Schenk VA, Sweeny DB. Meningitis related hearing loss evaluated with hearing loss evaluated with evoked potentials. Paediatr Neurol 1988; 4: 18–22. Journal of Tropical Pediatrics Vol. 48 June 2002
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