TRANSACTIONS OF THE ROYAL SOCIETY OF TROPICAL MEDICINE AND HYGIENE (2003) 97, 161-165

Cognitive performance at school entry of children living in malaria-endemic areas of Sri Lanka

Deepika Fernando 1, Renu W i c k r e m a s i n g h e 2, K. N. Mendis 4 and A. R. W i c k r e m a s i n g h e 3 1Department of Parasitology, Faculty of Medicine, University of Colombo, Colombo, Sri Lanka; Departments of 2Parasitology, and 3Department of Community Medicine and Family Medicine, Faculty of Medical Sciences, University of Sri Jayewardenepura, Nugegoda, Sri Lanka; 4Roll Back Malaria Project, World Health Organization, Geneva, Switzerland

Abstract In a cross-sectional study, carried out in January 1997 at the beginning of the school year, the impact of repeated attacks of malarial infection on the cognitive performance of children at school entry in moderate malaria-endemic areas of Sri Lanka was investigated. The cognitive performance of 325 schoolchildren in grade 1 (mostly aged 5 -6 years) in 2 districts of Sri Lanka which are endemic for malaria (Anuradhapura and Moneragala) was assessed by an entry performance test developed by the National Institute of Education, Sri Lanka. The indices assessed included writing, language and mathematical skills. There was no difference in any of the cognitive performance indices between children from Anuradhapura and Moneragala districts. The scores of most of the indices decreased as the number of malaria infections experienced by a child increased and the ability to identify letters was significantly impaired by the number of malaria infections a child had experienced after controlling for socio-economic and nutritional status. These findings suggest that repeated attacks of malaria in children can have an adverse impact on their development.

Keywords: malaria, schoolchildren, cognitive performance, Sri Lanka

Introduct ion Malaria is a public health problem in more than 90

countries inhabited by 40% of the world's population, and is responsible for up to 500 million clinical epi- sodes and 2.7 million deaths a year, predominantly in young children in sub-Saharan Africa (WHO, 1996). Malaria has returned in epidemic proportions to many countries causing high morbidity and mortality in peo- ple of all ages and is most serious in populations living under the most difficult and impoverished conditions.

In Sri Lanka, malaria is one of the most important public health problems; in the past it has consumed as much as 60% of the public health budget (AMC, 1986) and a population of 10.33 million is at risk of develop- ing malaria (WHO, 1997). In areas of unstable malaria such as Sri Lanka the incidence rates are highest in children aged 6-15 years (Mendis et al., 1992). Young children aged < 5 years and older age groups (> 25 years) suffer less frequent infections due, probably, to a lower exposure to mosquito bites in the former and an acquired immunity in the latter group (Mendis et al., 1990). From the age of about 5 years, the risk of exposure to malaria increases steadily due to the in- creased movement of individuals outdoors and occupa- tion-related movements (Mendis et al., 1990). Thus, the schoolchild is most vulnerable to repeated attacks of malaria. In terms of susceptibility to malarial infec- tions, it is estimated that children (aged < 15 years), who constitute about 35% of the population, contri- bute to as much as 44% of the total infectious reservoir in endemic areas of Sri Lanka (Gamage-Mendis et al., 1991). Therefore, even in moderately endemic areas of the world such as Sri Lanka, children carry the most significant burden of malarial disease in the community and constitute the major reservoir of infection.

In recent years there has been growing recognition that society's investment in the education of school- children might lead to greater returns with small addi- tional investments in the health of the children (Pollitt, 1990). Intestinal helminth infections have been identified as potentially important in this context, not only because they are among the most common

Address for correspondence: Dr Deepika Fernando, Depart- ment of Parasitology, Faculty of Medicine, University of Colombo, P. O. Box 271, Kynsey Road, Colombo 8, Sri Lanka; phone +94 1 765841, fax +94 1 598014, e-mail deepfern@slt.lk

infections of school-aged children and tend to occur at highest intensity in this age group, but also, and more importantly, because some of the more common con- sequences of infection (nutritional deficiency and impaired physical development) are likely to have negative consequences on cognitive function and learning ability (Nokes & Bundy, 1994).

Malnutrition early in life is linked to deficits in children's intellectual development that persist in spite of schooling, and impair their learning ability. Two hundred and twenty-six million children aged < 5 years in developing countries (40% of all children in the world) are estimated to suffer from moderate or severe stunting. High levels of stunting among children sug- gest that there will also be long-term deficits in mental and physical development that can leave children ill prepared to take maximum advantage of learning op- portunities in school (UNICEF, 1998).

Few studies have attempted to assess the impact of repeated malarial infections on childhood growth and development and almost none have addressed the im- pact on their cognitive performance. A study of weight curves of children who suffered from acute clinical malaria in Africa shows that an acute attack of malaria tended to retard growth. This retardation did not appear to be in any way permanent for when the malarious children had developed sufficient resistance to the noxious effects of the disease they rapidly re- gained their weight (McGregor et al., 1956).

In this study, we investigated the association between the number of past malarial infections and cognitive performance of children at school entry in moderate malaria-endemic areas of Sri Lanka.

Materials and Methods Study area and population

The study was conducted among students who were admitted to grade 1 (mostly aged 5 -6 years) in schools in 2 districts of Sri Lanka. The schools were located in Anuradhapura and Moneragala districts which are situ- ated in the dry zone of the country and are endemic for malaria. Students were selected from 7 schools of which 4 were in Anuradhapura and 3 in Moneragala; all 7 schools were in the same category in terms of facilities and resources as defined by the Department of Education, Sri Lanka, having classes up to grade 11 (type 2 schools). All students who gained entry to grade 1 in the selected schools were eligible for inclusion (n = 344). Only the children who were present on that

162 D. FERNANDO ETAL,

day and whose parents were present were recruited in to the study (n = 327). Two children were excluded from the study due to the presence of a chronic illness. There were no refusals among those recruited which comprised a sample of 325 children. None of the children were suffering from an acute illness on the day of the test.

The cross-sectional study was carried out in January 1997 at the beginning of the school year. The annual school year in Sri Lanka comprises 3 terms or trime- sters, the first of which commences in January of each year. Grade 1 is the first year of formal schooling which begins at approximately 6 years of age. Many children had attended nurseries and pre-schools previously although this is not compulsory for school admission.

Survey Cognitive performances were assessed by the entry

performance of children admitted to grade 1 within 1 month of the commencement of the school year to minimize other factors that could influence the out- come such as different facilities being available in different schools, including human and physical resources. The entry performance was measured using a test developed by the National Institute of Education (NIL), Sri Lanka (Siriwardhana, 1986). The NIL is an educational research centre in Sri Lanka where the school curriculum is reviewed and evaluated. The chil- dren were assessed with regard to writing, language and mathematical skills. The test developed by the NIL is culture-specific and standardized for the entire country. Each component of the test included a series of sub- components. For example, the language skills compo- nent consisted of subcomponents for reading, sentence structure and letter reading. There are no published national norms for this test. The test instrument was administered by research assistants who were given training for 3 d prior to the study.

All parents were informed in advance that at least one parent should be present in school at a notified time during the day the survey was being carried out. Socio-economic data regarding the family and informa- tion on past history of malarial attacks experienced by the child were collected from the parent or the guardian by direct interview using a structured questionnaire. The heights and weights of the children were recorded by trained technicians using standard methods.

Permission to conduct the study was obtained from the Ethical Review Committee, Faculty of Medicine, University of Colombo, respective school principals and zonal education officers. Informed consent was obtained from respective parents/guardians and class teachers. The results were made available to both the teachers and parents.

Data analysis Data were analysed using two-sample ~ tests and

analysis of variance to test for differences in means between groups. Prevalences of underweight, stunting and wasting were calculated as a proportion of all children whose Z score for the respective index was < - 2 SDs of the median WHO/NCHS (National Cen- ter for Health Statistics) reference values, respectively (WHO Working Group, 1986; Dibley et al., 1987). EpiInfo (CDC, Atlanta, GA, USA) was used to gener- ate Z scores. Analysis of covariance was used to control for potential confounding factors.

Results A total of 158 children from Anuradhapura District

and 167 children from Moneragala District were stud- ied. The characteristics of the children and their past malarial experiences are given in Table 1. The parents of children from Anuradhapura were better educated and the families had a higher income than those from Moneragala. The history of malaria during the past

year and the lifetime of the children in the 2 areas were significantly different, both were significantly higher in children from Moneragala than in Anuradhapura ( P = 0.001 for both). The family history of malaria indicated that more infections were experienced by families residing in Moneragala compared with those in Anuradhapura.

Anthropometric indices Of the 317 children who were included in the analy-

sis, 28% were underweight, 20% were stunted and 14% were wasted based on the NCHS standards. Twenty-six percent of the children from Anuradhapura and 30% of the children from Moneragala were under- weight, 26% and 15%, respectively, were stunted, and 11% and 16%, respectively, were wasted. The degree of underweight and wasting was significantly different among males in the 2 districts ( P = 0 . 0 3 0 and P < 0.001, respectively), while among females, the de- gree of stunting and wasting was significantly different in the 2 districts ( P = 0.040 and P < 0.001, respec- tively). When the 2 districts were considered together, though not significant, underweight and wasting were higher among girls than boys; the respective percen- tages for girls and boys were 30% and 25% for under- weight, 20% for both genders for stunting, and 17% and 11% for wasting (data not shown).

Cognitive performance The cognitive performances that were assessed in-

cluded (i) writing skills; (ii) language performance such as reading skills, letter reading and sentence structure; and (iii) mathematical performance such as ability to count, identify numbers and measure quantity. The means and SDs of the scores of each of the above are given in Table 2 by the area of residence. There was no difference in any of the parameters between children from Moneragala and Anuradhapura, except for letter reading where the children from Anuradhapura per- formed better.

In a further analysis, the malaria attacks during a child's lifetime were categorized into 3 groups (Table 3); the first comprised children who had never had an attack of malaria, the second children who had had 1-4 attacks of malaria and the third children who had had i> 5 attacks of malaria during their lifetime. All indices of cognitive performance were poorer in chil- dren who had experienced /> 5 attacks of malaria dur- ing their lifetime compared to the children in the other 2 groups. Letter reading and total language scores were the only indices where the differences approached a level of statistical significance (Table 3).

In a multiple regression model, the total number of malaria attacks experienced by the children was signifi- cantly associated with letter reading ( P < 0.001) and was of borderline significance for total language scores ( P = 0.093) after controlling for parents' educational status, monthly family income and anthropometry (Table 4). Parents' educational status was also signifi- cantly associated with letter reading and total language scores. Children who had experienced no attacks of malaria scored approximately 5 marks more out of a total of 26 marks (or 19%) in letter reading and 4 marks more out of 94 marks (4.3%) in the total language scores, compared to children who experi- enced > 5 attacks of malaria during their lifetime.

D i s c u s s i o n This study was undertaken to determine whether

repeated attacks of malaria in childhood have an ad- verse impact on the cognitive performance of children at school entry. Malaria, which appears periodically in epidemic proportions in most of Asia, has in the past had devastating effects on the economies of countries as well as general human development. It is generally a disease of the rural poor and is considered an important

COGNITIVE PERFORMANCE AT SCHOOL ENTRY IN SRI LANKA 163

Table 1. Character i s t ics o f s tudy chi ldren at schoo l entry in two districts o f Sri Lanka, J a n u a r y 1997

No. of children (%)

Anuradhapura Moneragala Total

Gender Male 66 (41.8) 78 (46.7) 144 (44.3) Female 92 (58.2) 89 (53.3) 181 (55.7)

Age (years) 4-4.9 11 (7.0) 15 (9.0) 26 (8.0) 5-5.9 137 (86.7) 143 (85.6) 280 (86.2) /> 6 10 (6.3) 9 (5.4) 18 (5.8)

Mothers' education (Grade a) None 4 (2.5) 16 (9.6) 20 (6.2) 1-5 35 (22.2) 51 (30.5) 86 (26.5) 6-10 106 (67.1) 88 (52.7) 194 (59.7) > 10 13 (8.2) 12 (7.2) 25 (7.7)

Fathers' education (Grade a) None 2 (1.3) 12 (7.2) 14 (4.3) 1-5 38 (24.1) 73 (43.7) 111 (34.2) 6 -10 103 (65.2) 79 (47.3) 182 (56.0) > 10 15 (9.5) 3 (1.8) 18 (5.5)

Monthly family income (SL Rs b) < 1000 33 (20.9) 92 (55.1) 125 (38.5) 1000 to < 3000 70 (44.3) 46 (27.5) 116 (35.7) 3000 to < 5000 37 (23.4) 20 (12.0) 57 (17.5)

5000 18 (11.4) 9 (5.4) 27 (8.3) No. of malaria attacks during lifetime

None 112 (70.9) 42 (25.1) 154 (47.4) 1-4 22 (13.9) 22 (13.2) 44 (13.5) ~> 5 24 (15.2) 103 (61.7) 127 (39.1)

No. of malaria attacks during past year None 136 (86.1) 116 (69.5) 252 (77.5) 1-4 16 (10.1) 36 (21.6) 52 (16.0) ~> 5 6 (3.8) 15 (9.0) 21 (6.5)

aGrade of formal school education. bMonthly family income in Sri Lankan Rupees (SL Rs) (US$1 = 70 SL Rs).

Table 2. Cognit ive p e r f o r m a n c e o f s tudy chi ldren at schoo l entry in two districts o f Sri Lanka, J a n u a r y 1997

Mean score -4- SD

Indicator of cognitive performance ~ Anuradhapura Moneragala (n = 150-158) b (n = 160-166) b

1. Task keeping 6.88 ± 2.76 7.06 ± 2.29 2. Concentration 5.94 ± 2.40 6.01 -4- 2.00 3. Ethic sense 4.11 4- 2.45 4.08 ± 2.23 4. Writing skills 54.46 -4- 16.94 54.19 -4- 16.24 5. Language skills

5.1 Reading skills 11.71 ± 4.35 11.42 ± 3.86 5.2 Sentence structure 17.00 -4- 9.88 17.63 ± 7.63 5.3 Letter reading 9.26 ± 7.18 7.38 ± 6.82

6. Mathematical skills 6.1 Ability to count 0.15 -4- 0.67 0.12 4- 0.60 6.2 Measuring quantity 6.79 -4- 4.52 6.67 ± 4.07 6.3 Identifying numbers 1.72 -4- 1.21 1.59 -4- 1.05

~Differences between indicators of cognitive performance were statistically significant only for letter reading (P < 0.05). bSome children could not complete all parts of the test and the sample sizes varied slightly between tests.

factor leading to poverty. The massive malaria epi- demic of 1934-35 in Sri Lanka claimed more than 80 000 lives and led to widespread social and economic devastation (Bruce Chwatt, 1985). However, in recent times with the global burden of malaria in most parts of

the world being reduced to a mere fraction of what it was at the turn of the last century, it is being measured by other methods, such as its impact on the economy, cognitive performance and growth and development. Available evidence (World Bank, 1993) indicates that

164 D. FERNANDO E T A L .

Table 3. Cognit ive per formance o f study chi ldren in re lat ion to attacks o f malar ia during their l i fe t ime at school entry in two districts o f S r i Lanka, January 1997

Ind ica to r of cognitive pe r fo rmance

M e a n score ± SD

N o attacks 1 - 4 attacks ~> 5 attacks (n = 154) (n = 44) (n = 126) F a pb

1. Task keeping 7.11 ± 2.65 2. C o n c e n t r a t i o n 6.10 ± 2.24 3. Eth ic sense 4.10 ± 2.52 4. Wr i t ing scores 54.50 ± 16.63 5. Language scores

5.1 Reading skills 11.96 ± 4.53 5.2 Sen tence s t ruc ture 17.27 ± 9.46 5.3 Le t te r reading 11.25 ± 8.52

6. Ma thema t i ca l scores 6.1 Abili ty to coun t 0.16 ± 0.67 6.2 Measu r ing quant i ty 6.94 ± 4.48 6.3 Ident i fying n u m b e r s 1.75 ± 1.14

7. To ta l language scores c 40.49 ± 15.31 8. Tota l ma thema t i ca l scores d 8.84 ± 5.52

6.91 ± 2.47 6.83 ± 2.39 0.427 0.653 6.00 -4- 2.19 5.82 ± 2.18 0.521 0 .594 4.04 -4- 2.21 4.11 4- 2 .16 0.013 0.987

55.70 ± 16.85 53.63 ± 16.48 0.269 0 .764

11.95 ± 2.91 10.95 ± 3.86 2 .332 0.098 18.47 ± 9.15 16.99 ± 7.79 0.468 0.626

7.63 ± 3.46 4.91 ± 3.56 34.155 <0 .001

0.15 4- 0.60 0.12 -t- 0.615 0.133 0 .876 6.74 ± 3.93 6.46 ± 4.18 0 .420 0.657 1.68 ± 1.21 1.54 ± 1.10 1.164 0 .314

38.06 ± 10.37 32.85 ± 10.57 12.014 <0 .001 8.58 ± 4.72 8.12 ± 5.14 0 .642 0 .526

aF test, analysis of variance comparing the scores of the 3 categories of malaria attacks. up value indicates significance level. P < 0.001, statistically significant. CTotal scores for reading, sentence structure and letter reading. dTotal scores for ability to count, quantity and identifying numbers.

Table 4. Analys i s o f v a r l a n c e us ing letter reading and total language scores as the dependent variable for s tudy chi ldren at school entry in two districts o f Sri Lanka, January 1997

Let te r reading Tota l language score

P [3 P

No. of malar ia at tacks dur ing lifetime a < 0 . 0 0 1 0.093 N o n e 5.105 <0 .001 3.881 0.036 1 - 4 1.600 0.162 3 .139 0 .170

No. of malar ia at tacks dur ing past year a 0.211 0 .626 N o n e 2 .862 0.079 2 .806 0.387 1 - 4 2 .249 0.191 1.423 0.679

Fa the r s ' educa t ion (grade) u 0.007 0.001 6 - 1 0 - 4 . 5 5 0 0.008 - 7 . 9 1 8 0 .020 1 - 5 - 6 . 0 9 9 0.001 - 1 2 . 3 0 5 0.001 N o n e - 4 . 9 3 0 0 .044 - 1 4 . 0 0 0 0 .004

M o t h e r s ' educa t ion (grade) b 0.010 0.005 6 - 1 0 - 0 . 7 3 8 0 .616 0.403 0.891 1 - 5 - 3 . 2 5 3 0.039 - 5 . 3 5 0 0.089 N o n e 0.165 0 .936 1.101 0.789

M o n t h l y family income (SL Rs) c 0.280 0.535 3000 to < 5000 - 0 . 6 0 9 0.686 - 3 . 3 5 4 0 .266 1000 to < 3000 - 1 . 1 0 4 0.433 - 4 . 0 8 0 0 .148 < 1000 0.487 0.739 - 3 . 9 8 6 0.173

Weight- for-age a N o r m a l 0 .814 0.415 0 .678 0 .734

Height- for-age e N o r m a l - 0 . 3 4 9 0 .724 - 3 . 4 5 1 0 .082

Weight - for -he igh t f N o r m a l - 1.386 0.246 - 1.594 0 .504

[3, regression coefficient. aReference group, ~ 5 malaria attacks. bReference group, education > grade 10. CMonthly family income in Sri Lankan Rupees (SL Rs); (US$1 = 70 SL Rs); reference group,/> SL Rs 5000. dReference group, underweight children. eReference group, stunted children. eReference group, wasted children.

malar ia is a costly disease, and an es t imated U S $ 1 8 0 0 mil l ion is be ing spen t annual ly on direct costs of b o t h p reven t ion and care and on indirect costs such as lost product iv i ty and t ime costs. Th i s is approximate ly

equivalent to the ent ire gross na t iona l p roduc t of some countr ies .

Malar ia can have substant ia l and lifelong effects on a chi ld 's cognitive pe r fo rmance and school ing t h rough

COGNITIVE PERFORMANCE AT SCHOOL ENTRY IN SRI LANKA 165

the impact of malaria- induced chronic anaemia and t ime lost or wasted in the classroom. T h e parasite may have an effect on the child's behaviour or mental process due to altered function of the central nervous system (e.g. cerebral malaria). A child suffering from malaria may be unable to at tend school or participate in school activities due to ill health (Connolly & Kvals- vig, 1993). T h e impact of parasitic diseases on the cognitive performance of schoolchildren has been in- vestigated. Several studies have shown an association between intensity of intestinal helminthiasis and poor cognitive performance and absenteeism from school; an improvement in the educational achievement of infected children has been observed following anthel- mintic and supportive treatment, indicating that the infection per se, rather than associated sociological factors, was responsible for impaired learning (Nokes et al., 1994). In planning the present study we postulated the hypothesis that repeated malarial attacks impair cognitive performance based on the debilitating nature of malaria that has been experienced in this part of the world and its well-known chronic effects such as anae- mia (Bradley-Moore et al., 1985; Hedberg et al., 1993).

It is unlikely that school absenteeism would have played any role in the cognitive performance of the study children as the test was administered within 3 weeks of the beginning of the school year. Children with chronic illness such as nephrotic syndrome and heart disease were excluded from the study. N o n e of the children had any acute illness on the day of the test which would exclude the possibility of such conditions having an adverse impact on cognitive performance. Cognit ive performance at school entry may also be affected by pre-school attendance; 87% of children had at tended pre-school for an average durat ion of 19 months. It is unlikely that the 13% children who had no pre-school educat ion would have had a significant impact on the differences in cognitive performance ob- served in this study.

Even in countries such as Sri Lanka in which a relatively good health system exists and t rea tment is sought early by patients, observing a dose-response relationship between indices of cognitive performance and the number of malarial attacks is a significant finding. In Sri Lanka, health care services are well developed, accessible to a large proport ion of the popu- lation, affordable as they are free of charge, and well utilized by the public. Coupled with a relatively high literacy rate (approximately 90%) this has resulted in the presentat ion of malaria patients, on average, within 3 d of the onset of symptoms, probably contributing to the low incidence of severe and complicated malaria and low malaria mortali ty in Sri Lanka (Gunawardena, 1998). This has made early diagnosis and prompt t reatment the mainstay of the National Malaria Control Programme. In situations where diagnosis and treat- ment is delayed, and severe and complicated malaria is more prevalent, the effects of repeated attacks of malar- ia on cognitive performance may be more marked and more discernible. N o n e of the children we studied had had an attack of severe and complicated malaria which may have contr ibuted to a more significant relationship between past history of malaria and cognitive perform- ance. These findings demonstrate the need for further research to examine the effects of malaria on cognitive development and school performance of children.

Acknowledgements We acknowledge technical assistance provided by Ms An-

usha Gallewate, Mr Jagath Rajakaruna and Mr Sudath Weer- asinghe. Our thanks are due to the Head and staff of the

Malaria Research Unit and Head and staff of the Department of Parasitology, University of Colombo, Sri Lanka for their support. This investigation received financial support from the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (Grant No. 970315).

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Received 17 July 2002; revised 18 September 2002; accepted for publication 1 October 2002