24 Delacollette, C. and Barutwanayo, M. (1993)

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region a paludisme hyperendemique stable,

commune de Nyanza Lac, Imbo Sud, Burundi.

Bulletin de la Société de Pathologie Exotique 86,

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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.

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27 Binka, F.N. et al. (1996) Impact of permethrin-

impregnated 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

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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

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30 Salum, F.M. et al. (1994) Mortality of under fives

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31 Craig, M.H. et al. (1999) African climatic model of

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597Review

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

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 soil-

transmitted 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

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.

Parasites that cause problems in

Malaysia: soil-transmitted helminths

and malaria parasites

Balbir Singh and Janet Cox-Singh

Balbir Singh*

Janet Cox-Singh

Faculty of Medicine andHealth Sciences,Universiti MalaysiaSarawak, 94300 KotaSamarahan, Sarawak,Malaysia.*e-mail:bsingh@fhs.unimas.my

conducted in similar communities in 1982 (Ref. 2).

Data from several more recent small-scale studies

clearly indicate that STHs and other intestinal

parasites are highly prevalent in rural communities

where sanitation remains poor (Table 1). These

studies include aboriginal groups3,4 and communities

in fishing villages*, plantations5, islands6,7 and forest

fringe areas8.

The problems associated with STH infections are

largely proportional to the worm burden. T. trichiura,

with or without concomitant A. lumbricodes infection,

has been associated with malnutrition, anaemia and

growth stunting in severe infections9. Although it is

well established that hookworm infections can lead to

iron-deficiency anaemia, the evidence linking STH

infections to impaired cognitive function and

educational performances in children remains

inconclusive10. Severe Ascaris infection can lead to

death, but STH infections are generally associated

with relatively low mortality rates; hence, helminth

control programmes are also accorded low priority.

Nevertheless, the Malaysian Ministry of Health

recognized that intestinal helminths were a major

public health problem and launched a worm control

programme in 1974. During the initial phase of this

programme (1974–1976), >220 000 pupils from year

one (aged 7 years), six (aged 12 years) and nine (aged

15 years) across 1486 schools in Peninsular Malaysia

were given a single dose of the anthelmintic, pyrantel

pamoate (P. Oothuman, unpublished). Between 1993

and 1995, ~1.3 million 7-year-old schoolchildren and

1.15 million 12-year-old schoolchildren were treated.

It is not possible to determine the effect of these

single-dose treatment regimens because assessments

were not undertaken. It seems unlikely that such a

programme, aimed only at a small proportion of

schoolchildren while neglecting pre-school and older

children, would have had a significant long-term

impact on reducing the prevalence of STHs because

re-infection following treatment is rapid5. An

integrated approach aimed at improving the

socioeconomic, nutritional and environmental status

of the communities with periodic mass anthelmintic

treatment and health education should prove to be a

better strategy because STH infections are closely

associated with environmental and socioeconomic

factors. A rural environmental sanitation programme

aimed at providing pour-flush latrines and safe

drinking water for every household in rural areas is

currently being implemented nationwide11. In

combination with health education and community

participation activities, the programme aims to reduce

the incidence of communicable diseases associated

with poor environmental sanitation. Many obstacles

are encountered during implementation of such

programmes, not least the financial constraints. For

example, in Sarawak, ~US$5.3 million was spent by

the State Department of Health on supplying water

and latrines, and on related rural environmental

sanitation projects between 1995 and 1997

(Refs 11,12). Although the programme does not

include mass anthelmintic treatment, it promotes

simple techniques on animal husbandry and vegetable

gardening in an effort to improve the nutritional

status of the rural communities. Continued financial

support for the rural environmental sanitation

programme is expected to have a positive impact on

rural health in general and, particularly, on the

prevalence and severity of STH infections.

Malaria

Malaria remains the most common vector-borne

parasitic disease in Malaysia despite a decline in the

annual number of cases. The number of microscopy-

confirmed cases decreased from 243 870 in 1961 to

44 226 by 1980 and fluctuated over the next 16 years

between 36 853 in 1992 and 59 208 cases in 1995

(Ref. 13). Since 1995, there was a dramatic reduction

in the number of cases, with only 11 106 cases reported

in 1999 (Ref. 14). Plasmodium falciparum is the most

predominant species in Malaysia with Plasmodium

vivax and Plasmodium malariae being the next

prevalent species. However, Malaysia can be divided

broadly into three geographically distinct regions with

respect to malaria transmission: Peninsular Malaysia,

TRENDS in Parasitology Vol.17 No.12 December 2001

http://parasites.trends.com

598 Review

*B. Singh et al. (1994) Abstract number 016.5(396), Eighth

International Congress of Parasitology (ICOPA), Izmir, Turkey.

Table 1. Percentage prevalence of soil-transmitted helminths at different

locations in Malaysia.

Ascaris Trichuris Hookworm Total prevalence Refs

of soil-transmitted

helminthsa

Peninsular Malaysia

Dengkil 62.9 91.7 28.8 NR 3

Sabak Bernam 27.7 37.9 0.5 60.3 5

Penang 33.4 92.0 19.7 NR 6

Penang 40.3 33.3 34.1 NR 7

Cherang Laut 65.2 80.9 27.0 85.4 b

Post Brooke 59.5 41.7 6.0 79.8 4

Sarawak

Serian 18.0 34.3 11.0 47.5 8aAbbreviation: NR, not reportedbData from B. Singh et al. unpublished

TRENDS in Parasitology

Thailand

Peninsular Malaysia

Singapore

Brunei Sabah

Sarawak

IndonesiaIndonesia

SabakBernam

Dengkil

Penang

Cherang Laut Post Brooke Serian

Sabah and Sarawak. There are clear distinctions

between these regions in the number of malaria cases

and the distribution of Plasmodium species (Table 2).

Malaria is one of 27 notifiable infectious diseases, and

it is required by law to report every microscopy-

confirmed case to the relevant District Department of

Health14. The malaria prevalence data for Malaysia is

based on such reports, and the majority of malaria

cases was detected when individuals who were ill

sought treatment at hospitals or rural health clinics.

However, the prevalence of Plasmodium species in

Malaysia is probably underestimated because

self-medicated individuals and sub-clinical or

microscopy-negative infections were not included in

these reports. More accurate epidemiological data can

be obtained by using highly sensitive molecular-based

detection methods that indicated higher proportions

of single and mixed infections than did microscopy in

two surveys in Malaysia15,16.

The health problems caused by malaria parasites

are largely dependent on the parasite species. Of the

four Plasmodium species that infect humans, only

P. falciparum is responsible for mortality, with

between 21 and 43 falciparum-related deaths per

year in Malaysia during the past ten years13,14. Severe

morbidity and mortality as a result of P. falciparum

infection is moderated by rapid access to appropriate

treatment; however, the emergence of antimalarial

drug resistance is a major cause for concern.

Chloroquine-resistant P. falciparum was first

reported in Peninsular Malaysia in 1966 (Ref. 17) and

by 1979 chloroquine resistance was widespread. The

combination of pyrimethamine and sulfadoxine (PSD)

was then introduced as the recommended treatment

for uncomplicated falciparum malaria in the

Peninsula and Sabah. In the early 1990s, clinicians in

Peninsular Malaysia were concerned by parasite

breakthrough following PSD treatment

(Choo Keng Ee, pers. commun.) and PSD resistance

was confirmed by an in vivo drug resistance study in

1996 (Ref. 18). By contrast, PSD remained effective

for uncomplicated falciparum malaria in Sabah during

the same period. The difference in the drug response

phenotype between the two P. falciparum populations

was supported by the genotypes present in each

population. The predominant genotypes of parasite

isolates collected in 1994 from the Peninsula were

those associated with PSD resistance19. By contrast,

the Sabah isolates collected in 1996 predominantly

possessed genotypes that were predictive of a

favorable clinical outcome, although the presence of

key point mutations suggested a limited future for

PSD in treating falciparum malaria. Indeed,

preliminary results from a current study in Sabah

provide evidence for the emergence of PSD-resistant

P. falciparum isolates (http://www.imr.gov.my).

Although P. falciparum isolates are exhibiting

increased resistance to antimalarials, to date there

have been no reports of P. vivax and P. malariae

isolates showing resistance to chloroquine.

The need for malaria control in Malaysia has been

recognized for a long time; the Malaria Advisory

Board was set up in 1911. The concept of eradication

was adopted with the launching of the Malaria

Eradication Programme in 1961, but was revised to

the concept of control ten years later following

recognition that malaria eradication was not an

achievable goal14. Currently, the Vector-Borne

Diseases Control Programme is mainly responsible

for malaria control nationwide. The objectives of this

programme are to reduce the morbidity and mortality

of malaria and to prevent the recurrence of malaria in

non-malarious areas. The programme has been

successful in significantly reducing the annual

number of cases of malaria in Malaysia (Table 2); all

the major cities and towns are now designated as

non-malarious (http://dph.gov.my).

Malaria control in Sabah took longer to achieve

than in the Peninsula owing to a large and remote

rural population coupled with an efficient mosquito

vector, Anopheles balabacensis20. However, in the

early 1990s, a concerted effort was made to achieve

malaria control in Sabah. Regular indoor residual

spraying with DDT was one of the major vector

control strategies. In 1993, a nationwide bednet

programme was introduced to malarious areas,

where the coverage of DDT spraying was poor as a

result of inaccessibility or refusal by the community.

By 1997, ~250 000 permethrin-impregnated bednets

were distributed in Sabah, protecting approximately

TRENDS in Parasitology Vol.17 No.12 December 2001

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599Review

Table 2. Distribution of the different human malaria species in Malaysia for 1995 and 1999a

Species Peninsular Malaysiab Sabahc Sarawakd Malaysia

1995 1999 1995 1999 1995 1999 1995 1999

Plasmodium falciparum 3740 1712 30 999 3052 411 786 35 150 5550Plasmodium vivax 3751 1712 15 858 1207 959 2031 20 568 4950Plasmodium malariae 16 23 615 75 207 269 838 367Plasmodium ovale 0 0 0 0 0 0 0 0Mixed species 245 46 2393 124 14 69 2652 239Total 7752 3493 49 865 4458 1591 3155 59 208 11 106

aAnnual number of microscopy-confirmed cases of malaria for Peninsular Malaysia, Sabah, Sarawak and the total number for Malaysia.bData taken from Vector-Borne Diseases Section, 1999 Annual Report, Division of Disease Control, Dept of Public Health, Ministry of HealthMalaysia.cData taken from Sabah State Vector-Borne Diseases Control Programme 1999 Annual Report.dData taken from Sarawak State Vector-Borne Diseases Control Programme 1999 Annual Report.

half a million people (Sabah State Vector-Borne

Diseases Control Programme, 1997 Annual Report).

Greater community involvement and commitment to

malaria control resulted from the bednet programme

in addition to associated health and child-to-child

education projects. Another strategy that contributed

significantly to the success of malaria control was the

training and stationing of microscopists in malarious

areas for early detection and treatment of malaria

cases. Perhaps the strategy is not so unusual, but the

fact that such a labor-intensive programme was

operating successfully in remote communities reflects

extraordinary coordination and commitment by the

staff of the Sabah State Vector-Borne Diseases

Control Programme. On many occasions, having

embarked on malaria and filariasis surveys in Sabah,

with target communities taking up to eight hours to

reach, we have been surprised to be met on arrival by

the public health worker or community nurse at the

rural health clinic. The network of these health clinics

approaches a concept of healthcare for all, and by

1997 all clinics in malaria-endemic areas in Sabah

had a trained microscopist (Sabah State Vector-Borne

Diseases Control Programme 1997 Annual Report).

Malaria control is complex and the current

situation in Sabah is potentially volatile. It is likely

that the success of the control programme was aided

by extreme climatic conditions. During the period

from January to March 1998, Northern Borneo

experienced a very severe drought linked to the

El Niño Southern Oscillation (ENSO) event of

1997–1998. The drought had a huge impact on the

fig wasp populations21 and is thought to have severely

reduced mosquito populations. There is no premise

for predicting what will happen to malaria

transmission in Sabah during the next few years.

Issues such as determining the relative weight of

influence of each of the many variables that led to a

reduction in the annual incidence of malaria in Sabah

need to be considered. Was the malaria control

programme mainly responsible? If so, the programme

needs to be maintained. Was it the drought associated

with the ENSO? If so, what will happen when the

rains return? Was it a combination of the drought, the

programme and an improvement in living standards

associated with development? Whatever the cause,

the malaria situation needs time to stabilize and

requires careful monitoring.

Perspective

The process of rapid development in Malaysia

combined with efforts to improve the socioeconomic

conditions of rural populations might well lead to a

significant reduction in the incidence of STHs and

possibly malaria. However, the Malaysian

environment has all the necessary conditions to

support malaria transmission, and concern for the

resurgence of local malaria parasite populations, or

establishment of imported parasite populations, is

justifiable given that Malaysia borders Indonesia and

Thailand. We believe that even if the human malaria

parasite populations decline to relatively low levels,

malaria control programmes, currently given high

priority in Malaysia, need to be maintained.

TRENDS in Parasitology Vol.17 No.12 December 2001

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600 Review

Acknowledgements

We thank Hasan AbdulRahman and PakeerOothuman for providinguseful information andhelpful discussion duringthe preparation of thisarticle. We would like tothank AnandRadhakrishnan for criticalreading of the manuscriptand Jaynsen Patrick Sibatfor assistance withgraphics.

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