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The past, present and future of childhood malaria mortality in Africa Robert W. Snow, Jean-Francois Trape and Kevin Marsh During the past few years, there has been a historic series of declarations of renewed commitment to malaria control in Africa. Whether the burden of malaria is increasing in Africa is a moot point. This article attempts to re-construct the evidence for the trends in childhood mortality as a result of Plasmodium falciparum infection over the last century in Africa.

The 20th century witnessed major gains in the fight against infectious diseases worldwide. In addition to the much publicized smallpox eradication campaign, progress was made towards reducing or eliminating the threats posed by polio, diphtheria, measles, tetanus, hepatitis B and leprosy. Prospects are now good for new vaccine-based attacks on pneumoccocal and haemophilus disease. However, other infectious diseases (most notably HIV, TB and malaria) continue to provide barriers to the progress of global health community. It is estimated that >80% of global mortality are a result of HIV and malaria in Africa1. Although it has been possible to track and model the public health impact of the emerging HIV and AIDS pandemic in Africa2, we remain much less certain about the historical patterns of mortality caused by P. falciparum. The risks of malaria mortality in childhood have been examined throughout the 20th century and to a point when the Roll Back Malaria (RBM) initiative proposes to halve malaria mortality in Africa by the year 2010 (Ref. 3). Burden of Malaria in Africa project

Bob Snow* The Wellcome Trust/Kenya Medical Research Institute Collaborative Programme, PO Box 43640, Nairobi, Kenya *e-mail: rsnow@ wtnairobi.minicom.net Jean-Francois Trape Institut de Recherche pour le Developpement, BP 1386, Dakar, Senegal. Kevin Marsh Centre for Geographic Medicine, Kenya Medical Research Institute, PO Box 230, Kilifi, Kenya.

The Burden of Malaria in Africa (BOMA) project was established in 1998 to develop a database of all available evidence on morbidity, disability and mortality associated with P. falciparum infection in Africa. The data obtained by the BOMA project have been located using traditional methods of electronic database searches (Medline, Embase and Popline) and manual searches of pre-electronic English and French tropical and regional biomedical journals. In addition, unpublished Ministry of Health and regional conference material have been accessed from libraries in Kenya, Uganda, Sudan and South Africa. All of this material has been cross-referenced to locate additional sources of information. The data have been abstracted, geo-referenced and matched to markers of malaria endemicity onto a pre-coded proforma and entered into a relational database (Access 97, Microsoft®, 1996). Correspondence with authors has also enabled improved resolution of data by age and time and has revealed information on malaria endemicity that was not provided in the original reports. http://parasites.trends.com

Malaria mortality in Africa since 1912

For the purposes of the present analysis, only selected mortality reports from areas of Africa that had documented stable, endemic transmission with minimum parasite prevalence among children of 30% have been included. Thirty-eight studies reported annualized rates of all-cause and malaria-specific mortality in childhood and for which it has been possible to define endemicity4–30. One additional site was included (Chingale, Malawi14) for which no direct evidence of endemicity was available; however, we have assumed that this site falls within our criteria of stable endemicity from modeled assumptions governing P. falciparum transmission in this area31. These combined data span 83 years from 1912 to 1995 and cover 13 countries in sub-Saharan Africa (Senegal, The Gambia, Guinea Bissau, Sierra Leone, Ghana, Nigeria, Benin, Democratic Republic of Congo, Burundi, Uganda, Kenya, Tanzania, Malawi). These data have been classified according to one of three time-periods: pre-1960, 1960–1989 and the 1990s. These periods have been selected to correspond approximately with important changes in access to effective malaria treatment following the rapid expansion of primary care services and the wider promotion of chloroquine (CQ) after 1960, and the emergence of significant antimalarial drug resistance in sub-Saharan Africa after 1990 (Ref. 3). Eight reports cover the period before 1960* (Refs 4–9), 20 reports cover the period 1960–1989 (Refs 10–23) and 11 reports cover the 1990s16,24–30. Figure 1 shows the median and inter-quartile range estimates of malaria-specific and all-cause childhood (in 0–4 year olds) mortality for the three surveillance periods. The period from 1960 to 1989 was characterized by a median malaria-specific mortality for African children of 7.8 per 1000 children aged 0–4 years per annum (p.a.), a decline of 18% compared with the estimates recorded pre-1960 (9.5 per 1000 children aged 0–4 years p.a.). However, the 11 studies on childhood malaria-specific mortality during the 1990s provided a median estimate of 10.2 per 1000 *Within the pre-1960 data set, courtesy copies of the annual medical reports prepared by Director’s of Medical Services of various Anglophone African countries between 1913 and 1935 were used. These reports were located in the Kenyan Ministry of Health’s archives. These reports were circulated by the British Colonial Medical Office to all Directors of Medical Services and as such should be available in other countries in addition to the Public Record Office, Kew, London, UK, under Colonial Office number CO544.

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Malaria mortality per 1000 children per year

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20 18 x

15 13 10 8 5 3 0

pre-1960

1960–1989

1990–1995

All-cause mortality per 1000 children per year

Year 80 70 60 50 40 30

childhood survival over the last century32. Economic development, provision of basic health care services and vaccination programs have been argued as the principal driving forces behind this transition32–33. The data reviewed here suggest this transition has continued through the early 1990s, despite reported deterioration in health care financing in Africa34. It remains to be seen how the pervasive effects of the HIV pandemic impacts on pediatric survival during the late 1990s and throughout the early part of this century. Against a background of overall improvements in child survival in areas of stable, endemic malaria transmission in Africa, malaria mortality in childhood appears to have declined during the ~30-year period following independence from colonial rule. The starting point of this decline was, almost certainly, much higher in most of rural Africa because many of the mortality reports pre-1960 are derived from urban and peri-urban communities. The gains encountered during 1960–1989 appear to have been lost during the 1990s when approximately a third of all mortality in childhood was attributable to malaria. This general pattern is supported by more detailed comparisons of malaria-specific mortality at sites in Africa for which temporal data were available during an 80-year period in Tanzania, Senegal and Kenya (Table 1).

20

Malaria mortality in specific areas of Africa over time 10 0 pre-1960

1960–1989

1990–1995

Year TRENDS in Parasitology

Fig. 1. (a) Box plot showing median (central thick lines), 25% and 75% quartile ranges around the median (box width) and upper and lower limits (T) of malaria-specific mortality estimates per 1000 children aged 0– 4 years per annum pre-1960 (Refs 4–9); 1960–1989 (Refs 10–23) and 1990–1995 (Refs 16, 24–30 and R.W. Snow and V.O. Mung’ala, unpublished). There is a single outlier (x) which is more than three times the box width7. (b) Box plot showing median (central thick lines), 25% and 75% quartile ranges around the median (box width) and upper and lower limits (T) all-cause mortality estimates per 1000 children aged 0–4 years per annum pre-1960 (Refs 4–9); 1960–1989 (Refs 10–23) and 1990–1995 (Refs 16, 24–30 and R.W. Snow and V.O. Mung’ala, unpublished).

children aged 0–4 years p.a., similar to that described during the pre-independence surveillance data. By contrast, the annualized risks of all-cause mortality recorded at the same sites demonstrate a continued decline over the three time periods (Fig. 1b), and that overall childhood mortality during the early 1990s was 34% lower than the median estimates of all-cause mortality recorded during the pre-independence surveys. The net result is a rise in the proportion of all deaths attributed to malaria: 18% pre-1960, 12% between 1960 and 1989, rising to 30% during the 1990s. The selected data captured in Fig. 1b are consistent with the wide series of demographic observations collected in sub-Saharan Africa concerning an overall epidemiological transition in http://parasites.trends.com

Wilson prospectively followed a cohort of children over several years, during the early 1930s, in the Tanga region of Tanzania and documented malariaattributable deaths among children in one village7. During the early 1990s, Salum and colleagues30 repeated prospective mortality surveillance in the same region and described a malaria mortality rate similar to that defined by Wilson 60 years earlier (Table 1). Further down the Tanzanian coast, at Bagamoyo, Mtango and Neuvians prospectively recorded childhood malaria-specific mortality between 1983 and 1985 (Ref. 15). Seven to ten years later at Bagamoyo, malaria-specific mortality had almost doubled to a rate of 15.4 deaths per 1000 p.a. (Ref. 29) (Table 1). Similarly, three separate areas of Senegal have witnessed at least a doubling of malaria-specific mortality from the mid-to-late 1980s compared with the early 1990s16 (Table 1). One further, less geographically specific comparison, is worth highlighting. On the Kenyan coast, two districts populated by similar ethnic groups living under similar ecological conditions, separated by 100 km have been studied using similar demographic surveillance systems (DSSs). The initial study was probably the first ever DSS study undertaken in Africa with support from the Colonial Development Fund in Kwale district where ~5000 children aged 0–4 years were studied during 1932 and 1933 (Ref. 5). A subsequent study was undertaken as part of epidemiological investigations among

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Table 1. Selected community-based demographic studies of malaria-specific mortality in childhood Area

Date of mortality surveys

Malaria-specific mortality per 1000 children aged 0–4 years per year

Malaria as a percentage of all-cause mortality in children 0–4 years old

Refs

Tanga,Tanzania

1933–1934 1992–1993

15.8 15.4

29 36

7 30

Bagamoyo,Tanzania

1983–1985 1992–1994

7.8 15.4

23 46

15 29

Niakar, Senegal

1984–1989 1990–1995

6.4 10.2

10 23

16 16

Bandafasi, Senegal

1984–1989 1990–1995

3.8 6.7

5 10

16 16

Mlomp, Senegal

1985–1989 1990–1995

0.6 4.7

3 17

16 16

Coast, Kenya

1932–1935 1991–1995

6.6 6.7

14 35

5 26,a

aR.W.

Snow and V.O. Mung’ala, unpublished.

10 000 children aged 0–4 years in the Kilifi district 60 years later, between 1991 and 1995 (Ref. 26, R.W. Snow and V.O. Mung’ala, unpublished). Comparing the two studies suggests similar risks of malaria-specific mortality despite being separated by 60 years; however, by the 1990s malaria had doubled as a proportion of all deaths in childhood (Table 1). Data limitations

The data presented in Fig. 1 represent a mixture of demographic approaches to mortality assessment. The pre-1960 data derive primarily from intensive civil registration systems organized among defined communities of pre-independence anglophone Africa where malaria was classified as a notifiable disease requiring medical certification. These data were obtained from annual medical reports from the Directors of Medical Services or Colonial Administration reports in Kenya5, Tanzania7, Southern Nigeria6, Gold Coast (Ghana)8 and Sierra Leone4. There is no indication on the completeness of registration achieved by these surveillance systems and they could well be incomplete in their coverage of deaths in the community. From several reports on these systems8,9 it would appear that great efforts were made by medical officers of health to ascertain causes of death, including reviews of clinical case notes accompanied by autopsies. By contrast, all the post-independence data have been abstracted from specialized, prospective DSS and the completeness of death registration is likely to have been much higher than those from pre-independence civil registration. These DSS studies have employed the verbal autopsy method to determine whether childhood deaths were likely to have been a direct result of malaria. Ascertaining cause of death through interviews with bereaved relatives not only has inherent difficulties of within-study precision35, but is also prone to http://parasites.trends.com

between-study variability where standardized diagnostic algorithms are not employed. Data recorded pre-1960 are likely to have provided a reasonably precise definition of cause of death but would have been incomplete in their coverage of all fatal events in the community. Conversely, demographic data collected post-1960 would have achieved greater coverage of deaths in the community but would have been less precise in the causal structure of mortality. Hence, it would be inappropriate to apply detailed statistical analyses to the data in Fig. 1. but advisable to apply a great deal of circumspection when concentrating on absolute values for any given estimate. Do these data, therefore, provide any insights into the trends in malaria’s contribution to child survival in Africa over the 20th century? We believe there are some basic observations meriting comment. First, it is striking that against a consistent downward trend in overall childhood mortality, whatever is collectively called malaria mortality in each data set has risen proportionately as an attributable cause of death in childhood since 1990, compared with the periods pre-1960 and 1960–1989. Second, several independent studies within similar geographical areas employing comparable demographic methods support the broad assertion that malaria-associated mortality has risen since the mid-1980s and is consistent with rates of malaria mortality in childhood described up to 60 years earlier in the same region after 1990. Understanding malaria mortality changes since 1912

During the first half of the 1900s, passionate pleas were made to combat malaria in Africa, viewed then as an impediment to economic and social development in the region36,37. There is now a renewed emphasis on malaria as a development

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Acknowledgements This work forms part of the Burden of Malaria in Africa (BOMA) project funded by the Wellcome Trust, UK and the Kenya Medical Research Institute (KEMRI). R.W.S and K.M. are supported by the Wellcome Trust as part of their Senior Fellowships program (#033340; #631342) and are affiliated to the Centre for Tropical Medicine, University of Oxford, UK. We are grateful to Brian Greenwood for comments on the manuscript. This paper is published with the permission of the director KEMRI.

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TRENDS in Parasitology Vol.17 No.12 December 2001

issue38. It has been proposed that US$ one billion of development money is required each year to tackle the burden facing malaria endemic regions of the world such as Africa39. Through such investment the RBM campaign aims to reduce malaria mortality by a half before the year 2010 (Ref. 3). When planning how best to invest in malaria control in Africa, it might be worth asking what led to the apparent decline in malaria-attributable mortality during the 30-year period after independence? Despite the successes of the WHO eradication campaign in many parts of the world following the Second World War, most of Africa was regarded as a lost cause, and in practice the eradication of malaria in Africa was never attempted40. Insecticide-treated bednets, a more recent tool for the control of malaria, were not used outside of specialized projects in Africa before 1990. One potentially important factor in Africa between 1960 and the late 1970s might have resulted from the rapid expansion in the provision of basic health services to increasingly large sectors of the population41. Co-incidental with this expansion in health services would have been access to CQ, a cheap and extremely effective antimalarial drug. It is not entirely clear when informal, self-treatment with CQ (now the majority behavior in many countries) became so popular, but a review of the evidence suggested this practice was already widespread across Africa during the 1980s42. Why has the downward trend in malaria-specific mortality apparently reversed over the past ten years despite a continued decline in all-cause mortality? There are several obvious explanations, such as declining household wealth linked to a changing

References 1 World Health Organisation (1999) The World Health Report 1999: Making a difference. pp 49–63, World Health Organisation 2 Anderson, R.M. et al. (1991) The spread of HIV-1 in Africa: sexual contact patterns and the predicted demographic impact of AIDS. Nature 352, 581–589 3 Nabarro, D.N. and Taylor, E. (1998) The ‘Roll Back Malaria’ campaign. Science 280, 2067–2068 4 Government of Colony and Protectorate of Sierra Leone (1913–1917) Annual reports of the Medical Department for the years ending 31st December 1912–1916. Government Printers, Freetown, Sierra Leone 5 Government of the Colony and Protectorate of Kenya (1935) Medical Department annual report, including the Medical Research Laboratory annual report for 1933. Government Printers, Nairobi, Kenya 6 Government of Colony and Protectorate of Nigeria (1934–35) Annual reports of the Medical & Health Department for the years 1932 and 1933. Government Printers, Lagos, Nigeria 7 Wilson, D.B. (1936) Report of the malaria unit, Tanga 1933–1934 (together with a report on a study of malaria in India). Colonial Development Fund (malaria research scheme), Government Printer, Dar es Salaam, Tanzania http://parasites.trends.com

health-sector based on cost-retrieval43, or generalized deterioration in the quality of clinical care34. Although access to and quality of health care is undoubtedly sub-optimal in many areas, one would have to explain why this has not impacted to the same degree on nonmalaria childhood mortality. Global warming has also been mooted as a general cause of changing malariaspecific mortality in several parts of Africa44. However, the communities included in this analysis lie well within the fringes of stable transmission in Africa, where transmission is not likely to be affected by changes in ambient temperature. In Africa, control of malarial morbidity and mortality rests in practice almost entirely on the treatment of clinical episodes. Over the past ten years or so there has been a precipitous decline in the efficacy of CQ across Africa and, in our view, this is the most plausible single factor contributing to the change in malaria-specific childhood mortality16,45–46. Perspective

In summary, there are strong reasons to believe that, despite the absence of a targeted campaign, from the 1960s onwards malaria mortality in Africa was declining in parallel with overall changes in childhood mortality. Over the past ten years, this trend seems to have reversed, with malaria-specific mortality apparently rising and accounting for an increasing proportion of overall childhood mortality. The reasons for this are not clear. Whatever the case, it is important to realize that the starting point for new efforts to roll back malaria is not a level playing field and that the mortality burden is moving upwards to what it was before most of Africa gained independence.

8 Colbourne, M.J. and Edington, G.M. (1954) Mortality from malaria in Accra. J. Trop. Med. Hyg. 57, 203–210 9 Bruce-Chwatt, L.J. (1952) Malaria in African infants and children in southern Nigeria. Ann. Trop. Med. Parasitol. 46, 173–200 10 Bradley, A.K. and Gilles, H.M. (1984) Malumfashi endemic diseases research project, XXI: pointers to causes of deaths in the Malumfashi area, northern Nigeria. Ann. Trop. Med. Parasitol. 78, 265–271 11 Goldberg, H.I. and M’Bodji, F.E. (1988) Infant and early childhood mortality in the Sine-Saloum region of Senegal. J. Biosocial Sci. 20, 471–484 12 Spencer, H.C. et al. (1987) Impact on mortality and fertility of a community-based malaria control programme in Saradidi, Kenya. Ann. Trop. Med. Parasitol. 81, 36–45 13 Greenwood, B.M. et al. (1988) Comparison of two strategies for control of malaria within a primary health care programme in The Gambia. Lancet I, 1121–1127 14 Lindskog, U. et al. (1988) Childhood mortality in relation to nutritional status and water supply – A prospective study from rural Malawi. Acta Paediatrics Scand. 77, 260–268 15 Mtango, F.D.E. and Neuvians, D. (1986) Acute respiratory infections in children under five years. Control project in Bagamoyo district, Tanzania. Trans. R. Soc. Trop. Med. Hyg. 80, 851–858

16 Trape, J.F. et al. (1998) Impact of chloroquine resistance on malaria mortality. Comptes Rendus de l’Académie des Sciences, Paris, Série III 321, 689–697 17 Delacollette, C. et al. (1989) Etude de la mortalite globale et de la mortalite au paludisme dans le Kivu montagneus, Zaire. Revue Epidémiologique et Santé-Publique 37, 161–166 18 Molbak, K. et al. (1992) Persistent and acute diarrhoea as the leading causes of child mortality in urban Guinea-Bissau. Trans. R. Soc. Trop. Med. Hyg. 86, 216–220 19 Alonso, P.L. et al. (1991) The effect of insecticidetreated bed nets on mortality of Gambian children. Lancet 337, 1499–1502 20 Vella, V. et al. (1992) Determinants of child mortality in South-West Uganda. J. Biosocial Sci. 24, 103–112 21 Velema, J.P. et al. (1991) Malaria morbidity and mortality in children under three years of age on the coast of Benin, West Africa. Trans. R. Soc. Trop. Med. Hyg. 85, 430–435 22 Van den Broeck, J. et al. (1993) Influence of nutritional status on child mortality in rural Zaire. Lancet 341, 1491–1495 23 Jaffar, S. et al. (1997) Changes in the pattern of infant and childhood mortality in Upper River Division, The Gambia, from 1989 to 1993. Trop. Med. Int. Health. 2, 28–37

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24 Delacollette, C. and Barutwanayo, M. (1993) Mortalite et morbidite aux jeunes ages dans une region a paludisme hyperendemique stable, commune de Nyanza Lac, Imbo Sud, Burundi. Bulletin de la Société de Pathologie Exotique 86, 1–7 25 Barnish, G. et al. (1993) The epidemiology of malaria in southern Sierra Leone. Parasitologia 35, 1–4 26 Snow, R.W. et al. (1994) The role of the district hospital in child survival at the Kenyan coast. African J. Health Sci. 1, 71–75 27 Binka, F.N. et al. (1996) Impact of permethrinimpregnated bed nets on child mortality in Kassena-Nakana district, Ghana: a randomised controlled trial. Trop. Med. Int. Health. 1, 147–154 28 Government of Tanzania (1997) Policy implications of adult morbidity and mortality: end of Phase 1 report. Ministry of Health, Dar es Salaam, Republic of Tanzania. 29 Premji, Z. et al. (1997) Community based studies on childhood mortality in a malaria holoendemic area on the Tanzanian coast. Acta Tropica 63, 101–109 30 Salum, F.M. et al. (1994) Mortality of under fives in a rural area of holoendemic malaria transmission. Acta Tropica 58, 29–34

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31 Craig, M.H. et al. (1999) African climatic model of malaria transmission based on monthly rainfall and temperature. Parasitol Today 15, 105–111. 32 Ewbank, D.C. and Gribble, J.N. (1993) Effect of Health Programs on child mortality in sub-Saharan Africa. National Academy Press, Washington DC, USA. p. 191. 33 Hill, A. (1992) Trends in childhood mortality in sub-Saharan mainland Africa. In Mortality and Society in sub-Saharan Africa (Van de Walle, E. et al., eds) pp. 10–31, Clarendon Press 34 Castro-Leal, F. et al. (2000) Public spending on health care in Africa: do the poor benefit? Bull. WHO 78, 66–74 35 Snow, R.W. et al. (1992) Childhood deaths in Africa: Uses and limitations of verbal autopsies. Lancet 340, 351–356 36 League of Nations (1936) Malaria under African conditions. Q. Bull. Health Organ. League of Nations 5, 134–137 37 Colbourne, M.J. (1966). Malaria in Africa. Oxford University Press, pp. 29–49 38 Sachs, J. (1999) Helping the World’s poorest. The Economist, 14 August, pp. 17–20 39 World Health Organisation (2000) The Abuja declaration on Roll Back Malaria in Africa by the African heads of State and Government, 25th April

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2000, Abuja, Nigeria. Statement prepared by RBM, World Health Organisation, Geneva Litsios, S. (1998) Arnoldo Gabaldon’s independent path for malaria control and public health in the Tropics: a lost ‘paradigm’ for WHO. Parassitologia 40, 231–238 Packard, R.M. (1998) ‘No other logical choice’: Global malaria eradication and the politics of international health in the post-war era. Parassitologia 40, 217–229 Foster, S. (1995) Treatment of malaria outside formal health services. J. Trop. Med. Hyg. 98, 29–34 Creese, A. (1991) User charges for health care: a review of recent experience. Health Policy and Planning 6, 309–319 Mouchet, J. et al. (1998) Evolution of malaria in Africa for the past 40 years: impact of climatic and human factors. J. Am. Mosquito Control Assoc. 14, 121–130 Greenberg, A.E. et al. (1989) Hospital-based surveillance of malaria-related paediatric morbidity and mortality in Kinshasa, Zaire. Bull. WHO 67, 189–196 Shanks, G.D. et al. (2000) Changing patterns of clinical malaria since 1965 among a tea estate population located in the Kenyan highlands. Trans. R. Soc. Trop. Med. Hyg. 94, 253–255

Parasites that cause problems in Malaysia: soil-transmitted helminths and malaria parasites Balbir Singh and Janet Cox-Singh Malaysia is a developing country with a range of parasitic infections. Indeed, soil-transmitted helminths and malaria parasites continue to have a significant impact on public health in Malaysia. In this article, the prevalence and distribution of these parasites, the problems associated with parasitic infections, the control measures taken to deal with these parasites and implications for the future will be discussed.

Balbir Singh* Janet Cox-Singh Faculty of Medicine and Health Sciences, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia. *e-mail: [email protected]

Malaya, occupying a strategic position in South East Asia, has played a historically important role in the study of parasitic diseases in the tropics. The Institute for Medical Research (Kuala Lampur, Malaysia), which celebrated its centenary last year, carried out most of the pioneering work on tropical diseases, particularly on malaria and filariasis (http://www.imr.gov.my). The modern Malaysian Federation, comprising Peninsular Malaysia (formerly Malaya), and the Malaysian Borneo States of Sabah and Sarawak, was formed in 1963 and has maintained the tradition in research and the control of parasitic diseases (Table 1). The Malaysian population of ~22 million (http://www.statistics. gov.my) occupies http://parasites.trends.com

diverse environmental niche areas and, although migration to cities is common, a significant proportion of the population remains in remote rural areas where parasitic infections are prevalent. Soil-transmitted helminths

Ascaris lumbricoides, Trichuris trichiura and hookworms are the most common intestinal parasitic infections of medical importance in Malaysia. However, it is difficult to estimate with certainty the current overall incidence of infection with soiltransmitted helminths (STHs) among the Malaysian population. The last large-scale survey of STHs was undertaken in 1991 and involved 9863 samples from 43 squatter communities around the capital, Kuala Lumpur1. The results of this survey, comprising individuals from all age groups, indicated an overall prevalence of STH infection in 58% of the population (T. trichiura, 49%; A. lumbricoides, 33%; and hookworm, 6%) and did not differ significantly from results obtained in a large-scale survey

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