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SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH
AN UNCEASING PROBLEM: SOIL-TRANSMITTED HELMINTHIASES IN RURAL MALAYSIAN COMMUNITIES
MS Hesham Al-Mekhlafi1, AS Atiya2, YAL Lim1, AK Mohammed Mahdy1, WA Wan Ariffin3, H Che Abdullah4 and Johari Surin1
1Department of Parasitology, 2Department of Social and Preventive Medicine 3Department of Pediatric, Faculty of Medicine, University of Malaya, Kuala Lumpur; 4Vector Borne and Disease Control Division (VBDC), Ministry of Health, Kuala Lumpur, Malaysia
Abstract. Despite great development in socioeconomic status throughout 50 years of inde- pendence, Malaysia is still plagued with soil-transmitted helminthiases (STH). STH continue to have a significant impact on public health particularly in rural communities. In order to deter- mine the prevalence of STH among rural Orang Asli children and to investigate the possible risk factors affecting the pattern of this prevalence, fecal samples were collected from 292 Orang Asli primary schoolchildren (145 males and 147 females) age 7-12 years, from Pos Betau, Kuala Lipis, Pahang. The samples were examined by Kato-Katz and Harada Mori tech- niques. Socioeconomic data were collected using pre-tested questionnaires. The overall preva- lence of ascariasis, trichuriasis, and hookworm infections were 67.8, 95.5 and 13.4%, respec- tively. Twenty-nine point eight percent of the children had heavy trichuriasis, while 22.3% had heavy ascariasis. Sixty-seven point seven percent of the children had mixed infections. Age >10 years (p=0.016), no toilet in the house (p=0.012), working mother (p=0.040), low house- hold income (p=0.033), and large family size (p=0.028) were identified as risk factors for as- cariasis. Logistic regression confirmed low income, no toilet in the house and working mother as significant risk factors for ascariasis. The prevalence of STH is still very high in rural Malay- sian communities. STH may also contribute to other health problems such as micronutrient deficiencies, protein-energy malnutrition and poor educational achievement. Public health per- sonnel need to reassess current control measures and identify innovative and integrated ways in order to reduce STH significantly in rural communities.
INTRODUCTION tosomiasis represent more than 40% of the disease burden caused by all tropical dis- Soil-transmitted helminthiases (STH) are eases, excluding malaria. considered as the most prevalent infections Unlike blood parasites and Schistosoma, of humankind despite great development in STH can live in silence as chronic infections socioeconomic status worldwide. The WHO and the greatest morbidity is among children (1996) estimated that more than one billion of and mothers of childbearing age (Savioli et al, the world’s population are infected either by 1992; Nurdia et al, 2001). The main impact of one or more of STH, particularly Ascaris STH infections is their associations with mal- lumbricoides, Trichuris trichiura and hook- nutrition, vitamin A deficiency (VAD) and iron worm. These infections together with schis- deficiency anemia (IDA), which may have ef- Correspondence: Professor Johari Surin, Depart- fects at the community level in regard to work ment of Parasitology, Faculty of Medicine, Univer- and productivity in adults (Gilgen et al, 2001) sity of Malaya, 50603 Kuala Lumpur, Malaysia. and growth, learning and school performance Tel: 006-03-79674747; Fax: 006-03-79764754 in children (Nokes and Bundy, 1994; Ramdath E-mail: [email protected] et al, 1995; Al-Mekhlafi et al, 2005).
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According to environmental, socioeco- Each village is comprised of a small popula- nomic and cultural-behavioral factors, the tion and most of the residents work as labor- prevalence and distribution of STH may differ ers, farmers or rubber tappers. Most of the from one region to another and sometimes houses had electricity and piped water as the within the country itself (de Silva et al, 2003). main source of drinking water while water for Data from recent studies revealed that STH domestic needs (bathing, washing clothes and are prevalent in Southeast Asia and are still feeding animals) is collected from the rivers considered as public health problems in Thai- located adjacent to the villages. There is no land (Tomono et al, 2003), Vietnam (Uga et al, adequate or proper sanitation. There is a clinic 2005) and Indonesia (Nurdia et al, 2001). Stud- in the area for health services equipped with ies indicate there is a web of risk factors as- an ambulance to send critical cases to the sociated with the high prevalence and inten- nearest hospital (50 km). sity of STH including age, low family income, Subjects inadequate sanitation, presence of animals in The school had an enrolment of 405 pu- the house, drinking water from rivers and wells, pils in the age range of 7-12 years. A total of low levels of education among parents, geoph- 292 (72.1%) schoolchildren who were present agy and poor personal hygiene (Geissler et al, during the visits participated voluntarily in this 1998; Anantaphruti et al, 2004; Naish et al, study and delivered stool samples for exami- 2004). nation (universal sampling). Of these children, Malaysia is a developing country with a only 277 children came for interview, filled in range of parasitic infections. STH continue to the questionnaire to analyze the association have a significant impact on public health in between STH and the variables in these chil- Malaysia, particularly in rural communities dren. (Dissanaike et al, 1977; Bundy et al, 1988; Throughout many visits to the villages to Norhayati et al, 1997; Zulkifli et al, 2000; Al- observe their activities during daytime, most Mekhlafi et al, 2006). Through a better under- of the children were noted to play in the soil standing of the relationship of risk factors to without wearing shoes or slippers. Some of the dynamics of transmission of STH it should the children play and swim in the rivers after be possible to implement effective control school and in their leisure time. Besides that, measures. Within this context, the present their personal hygienic practices were also study was undertaken to determine the cur- poor. The headmaster of the school and the rent prevalence and distribution of STH among parents of the children consented to take part aboriginal children living in rural areas in Pen- in this study after a clear explanation was insular Malaysia and to study the possible risk given. factors that may affect the pattern of this prevalence in Malaysia. Data collection Subjects’ socioeconomic data and fecal MATERIALS AND METHODS samples were collected during many visits to the school in order to cover those who were Study area absent and hence missed at any visit. A list of A cross-sectional study was carried out all the students’ names and classes was col- between February and July 2006 among pri- lected from the headmaster’s office. Each child mary schoolchildren of Pos Betau School, was coded accordingly and particulars were Kuala Lipis, Pahang, Malaysia. The schoolchil- entered in the data sheet. Information on bio- dren were from 18 villages around the school. data and socioeconomic status were collected
Vol 38 No. 6 November 2007 999 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH through a pre-designed questionnaire. trichiura and hookworm in individual children Fresh fecal samples were collected into was analyzed using Spearman’s correlation wide mouth screw-cap 100 ml clean contain- coefficient. ers. The samples were examined by Kato-Katz Variables that were significantly associ- technique as described by Martin and Beaver ated with prevalence of infection were included (1968) for the presence of A. lumbricoides, T. in a logistic multivariate model (stepwise pro- trichiura and hookworm eggs. Egg counts, as cedure). Univariate analysis relating ascariasis a measure of worm burden, were also carried to each of the variables was done by means out using this technique and the results were of odds ratios (OR) and 95% confidence in- recorded as eggs per gram of stool (epg). The terval (95% CI) calculated by logistic regres- intensity of infection was graded as heavy, sion models. moderate or light according to criteria pro- Ethical consideration posed by the WHO (1987). In order to detect This study was approved by the Medical hookworm larva in light infections, Harada Mori Ethics Committee of the University of Malaya fecal cultivation technique using a test-tube Medical Center, Malaysia. During the visits to was also carried out (Jozefzoon and Oostburg, the school and the villages community meet- 1994). ings were held with the headmaster of the Data analysis school, the heads of the villages, the parents Statistical analysis of the data was per- and their school-age children before the com- formed using SPSS 11.5 (SPSS, Chicago, IL, mencement of the study in order to give a clear USA). For descriptive data, rate (percentage) explanation of the objectives of the study. In- was used to assess the prevalence of infec- formed verbal consent was obtained from the tions. The egg counts of A. lumbricoides, T. participants. trichiura and hookworm, examined for normal- ity by the Kolmogorov-Smirnov test, were not RESULTS normally distributed so the assessment of the variation of egg counts by age and gender Demographic characteristics were done after log transformation. Two hundred ninety-two primary school- A chi-square test on proportions and a children (145 males and 147 females) age 7- Mann-Whitney U test were used where appro- 12 years with a median age of 9.6 years priate to test for associations between vari- (Interquartile range 3.0) participated in this ables. Univariate and multivariate analyses study. Thirty-four point three percent of fathers were used to determine risk factors. As a re- had a formal education of at least 6 years. Only sult of the high prevalence of trichuriasis and 22.4% of mothers had a similar level of formal low prevalence of hookworm infections, which education. Characteristics of study subjects distorted the association with other variables, including their socioeconomic status are pre- the dependent variable was ascariasis only as sented in Table 1. a statistical model, while the independent vari- Prevalence and distribution of STH ables were age, gender, educational levels of The prevalence of STH infections in these the parents, employment status of the mother, children according to intensity of infection and household income, family size, presence of gender is shown in Table 2. The overall preva- toilet in the house, presence of animals in the lence of ascariasis, trichuriasis, and hookworm house and source of drinking water. The cor- infections were 67.8, 95.5 and 13.4%, respec- relation of mean epg for A. lumbricoides, T. tively. Almost one third (29.8%) of children had
1000 Vol 38 No. 6 November 2007 STH IN RURAL MALAYSIAN COMMUNITIES heavy trichuriasis, while 22.3% had heavy as- between males and females. Almost two third cariasis. All hookworm infections in this popu- (67.7%) of the infected children had mixed in- lation were light infections. There were no sig- fections, while 32.3% had single infections. nificant differences in the prevalence of STH The most prevalent mixed infections were as- and mean eggs/gram feces (worm burden) cariasis and trichuriasis (54.2%).
A positive correlation (rs=0.221, p<0.001) between the egg counts of A. lumbricoides Table 1 and T. trichiura, and T. trichiura and hookworm General characteristics of Orang Asli (r =0.325, p<0.01) passed by the same indi- children participating in this study. s vidual was observed. The same correlation Characteristics Frequency was also seen when the data were stratified (%) by age (≤ 10 years and > 10 years). A posi- Age groups (years) (n=292) tive correlation between mean epg for A. ≤10 years 30.8 lumbricoides and T. trichiura was seen in males >10 years 69.2 (p<0.01) but not in females when the data Gender were stratified by gender. A weak correlation Males 49.7 (p<0.05) between T. trichiura and hookworm Socioeconomic status was also detected among males only. Paternal education level (at least 6 years) 34.3 Maternal education level (at least 6 years) 22.4 Univariate and multivariate analysis for risk fac- Low household income (
Table 2 Prevalence of ascariasis, trichuriasis and hookworm infections according to intensity of infection and gender.
Type of infections
Ascariasis Trichuriasis Hookworm infection No. (%) No. (%) No. (%)
Intensity of infection Negative 94 (32.2) 13 (4.5) 253 (86.6) Light infection 74 (25.3) 110 (37.6) 39 (13.4) Moderate infection 59 (20.2) 82 (28.1) 0 Severe infection 65 (22.3) 87 (29.8) 0 Gender Male 93 (64.1) 138 (95.2) 19 (13.1) Female 105 (71.4) 141 (95.9) 20 (13.6) Total 198 (67.8) 279 (95.5) 39 (13.4)
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Table 3 Odds ratios for potential risk factors with ascariasis among Orang Asli children.
Prevalence of ascariasis Variables N OR (95% CI) p
Paternal education 0.96 (0.842-1.22) 0.898 ≥6 years formal education 67 No formal education 127 Maternal education 0.77 (0.93-1.21) 0.417 ≥6 years formal education 46 No formal education 148 Maternal employment status 1.8 (1.03-3.01) 0.040a,b Working 105 Not working 89 Low household income 2.0 (1.1-3.7) 0.033a,b
1002 Vol 38 No. 6 November 2007 STH IN RURAL MALAYSIAN COMMUNITIES where poverty prevails, where sanitation is in- fection had a higher prevalence (93.9%) in Ni- adequate or non-existent and where more geria (Adenusi et al, 2003) and also in aborigi- health awareness and care are needed and nal communities in northern Australia with a recommended to deliver anthelmintics to- prevalence reaching 93% in children 5-14 gether with vitamin A supplements. years of age (Thompson et al, 2001). Resis- Since the 1970s, several studies in Ma- tance of moderate and severe trichuriasis to laysia have demonstrated a high prevalence antihelminthic drugs which has been reported of ascariasis, trichuriasis and hookworm in- to be prevalent in Malaysia (Rajeswary et al, fections in Orang Asli children, where the 1994; Norhayati et al, 1998a) may be one of prevalences range between 30.2-69.0%, the possible reasons. 15.8-98.2% and 6-51.0%, respectively Trichuriasis, with or without concomitant (Dissanaike et al, 1977; Bundy et al, 1988; ascariasis has also been associated with mal- Norhayati et al, 1997; Zulkifli et al, 2000; Sagin nutrition, iron deficiency anemia and growth et al, 2002; Al-Mekhlafi et al, 2006). The find- stunting (Robertson et al, 1992; Saldiva et al, ings of the present study confirmed that as- 1999; Al-Mekhlafi et al, 2005). Severe ascari- cariasis, trichuriasis and hookworm infections asis has been associated with malnutrition are still endemic in the Orang Asli community (Stephenson et al, 1993; Saldiva et al, 1999) in Malaysia with almost all of the children stud- and has been considered as one of the causes ied (98.6%) infected by either one or more of acute abdominal pain in tropical countries STH. The prevalence was similar with the re- (Kamiya et al, 1993). In Malaysia, clinical fea- sults reported recently among Orang Asli chil- tures of severe trichuriasis have been de- dren in Selangor, Malaysia (Al-Mekhlafi et al, scribed in few previous studies (McKay et al, 2006) and higher than the prevalences re- 1971; Kamath, 1973). It has also been re- ported by previous studies (Norhayati et al, ported that ascariasis was responsible for 1997; Zulkifli et al, 2000), this may indicate 42.0% and 41.0% of all acute abdominal the continuance of this problem. The present emergencies and intestinal obstruction, re- study also confirms previous findings that the spectively, in children aged 7 years and under prevalence and mean epg for STH were not admitted to Kuala Lumpur Hospital (Mahmud, significantly different between genders (Chan 1973). et al, 1992; Norhayati et al, 1997). This may It is not surprising to observe a positive suggest that there is no difference in socio- significant correlation between A. lumbricoides behavioral activity or immune status between and T. trichiura due to the similar mode of in- males and females. fection and high prevalence and mean epg for Trichuriasis proved to be the most com- both species in the community. There was no mon STH infection in Malaysia and this ob- correlation between A. lumbricoides and hook- servation is in agreement with previous local worm and this may reflect the low prevalence studies (Norhayati et al, 1997; Rahman, 1998; and mean epg for hookworm in the commu- Sagin et al, 2002; Al-Mekhlafi et al, 2006). nity. A similar trend in correlation has been re- Ascariasis is the predominant infection in ported previously in Malaysia (Norhayati et al, China where about 600 million people are in- 1998a) as well as in studies conducted in fected (Xu et al, 1995). It has also been found other countries (Ferreira et al, 1994). to be the most common in Indonesia (Widjana The findings of this study show the preva- and Sutisna, 2000), Yemen (Azazy et al, 2002), lence of heavy infection is high and that al- Brazil (Scolari et al, 2000) and Africa most one third of children had heavy worm (Crompton and Tulley, 1987). Hookworm in- burdens. In the case of hookworm infection,
Vol 38 No. 6 November 2007 1003 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH all the infected children had light infections, Although there were a large number of domes- and this may be due to the different mode of tic animals (dogs, cats and hens) this factor transmission. WHO (2006) indicated that STH was not significantly associated with the high may have a negative impact on the economic prevalence of ascariasis in our study. development of communities and nations, re- Interestingly, the presence of domestic sulting from failure to treat school-age children animals was significantly associated with the who are infected. These children are often worm burden where the mean egg/g of those physically and intellectually compromised by having animals was significantly higher than anemia, leading to attention deficits, learning others. This observation was in contrast to disabilities, school absenteeism and higher other studies which documented an associa- dropout rates and this may yield a generation tion between the presence of domestic ani- of adults disadvantaged by the irreversible mals and STH (Traub et al, 2002; Neisum et- sequelae of infections. Proper attention should al, 2005). A working mother was one of the be given to these infections, especially in en- major risk factors for ascariasis in this com- demic areas. Both the intensity and continu- munity, this in agreement with studies in Thai- ance of infection are the key factors for the land (Tomono et al, 2003) and India (Naish et pathological changes and long-term compli- al, 2004). We observed a significantly higher cations. prevalence of ascariasis in children under 10 In our study we identified low household years of age. This may be attributed to the income and large family size as significant risk greater exposure to STH as a result of exces- factors in the prevalence of ascariasis and this sive mobility of children of this age. In our was in accordance with previous studies model, there was no significant association (Rajeswari et al, 1994). This may be attributed between source of drinking water and paren- to the horizontal spread of infection among tal education and prevalence of STH. Signifi- family members where poverly prevails. Work- cant associations for these factors were ob- ing mothers and low household income have served by Norhayati et al (1998b). been also reported as predictors of malnutri- In conclusion, this study showed that tion among Orang Asli children (Al-Mekhlafi et ascariasis, trichuriasis and hookworm infec- al, 2005). Sanitation is a key factor in para- tions are still prevalent and therefore of a public sitic infections. Information from the question- health concern in Orang Asli communities in naire showed that most of the participants Malaysia. The high prevalence of severe as- prefered the rivers as a defecation site. Def- cariasis and trichuriasis may contribute to ecation around the house and playing places other health and medical problems which are was also observed among young children. This also prevalent in these communities such as practice is likely to enhance the transmission micronutrient deficiency (IDA and VAD), pro- of infection. In this study, the absence of a tein-energy malnutrition, poor school perfor- toilet in the house was identified as a contrib- mance and other acute illnesses among chil- uting factor for ascariasis in accordance with dren. Public health personnel need to reas- previous studies (Muller et al, 1989; Rai et al, sess current control measures and identify in- 2000). Personal hygiene can play a crucial role novative and integrated ways in order to re- in protection from STH. During the visits to duce STH significantly in rural communities. the villages, we observed that toddlers and Improvement of socioeconomic status, sani- young children were playing in groups outside tation, health education together with periodic the houses barefoot and eating unwashed mass deworming should prove to be a better vegetables and fruits contaminated with soil. strategy to control STH.
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ACKNOWLEDGEMENTS gastrointestinal helminthes infection in urban slum children from Kuala Lumpur, Malaysia. We gratefully acknowledge funding by the Trans R Soci Trop Med Hyg 1998: 82: 289-94. University of Malaya (Research grant No. Chan L, Kan SP, Bundy DA. The effect of repeated P0101/2006B). We also express our gratitude chemotherapy on the prevalence and intensity to the headmaster and teachers of Sekolah of Ascaris lumbricoides and Trichuris trichiura Kebangsaan Betau, Dr Sa’iah Abdullah and infection. Parasitology 1992; 104: 371-7. Mr Kim Tai from the Department of Orang Asli Crompton DWT, Tulley JJ. How much ascariasis is Affairs, Ministry of Rural Development, Staff there in Africa? Parasitol Today 1987; 3: 123- of Clinic Pos Betau, Mr Wan Hafiz from De- 7. partment of Parasitology, Faculty of Medicine, de Silva1 N, Brooker S, Hotez P, Montresor A, UM, Mr Adel Amran and Mr Abdulsalam Al- Engels D, Savioli L. Soil-transmitted helminth Mekhlafi from UKM for their fruitful help. We infections: updating the global picture. Trends also wish to thank the children for their volun- Parasitol 2003; 19: 547-51. tary participation in this study. Dissanaike AS, Vijayamma T, Kan SP, Ong HT. Stud- ies on parasitic infections in Orang Asli (Ab- REFERENCES origines) in Peninsular Malaysia. Med J Malay- sia 1977; 32: 48-55. Adenusi AA, Ogunyomi EO. Relative prevalence of Egger RJ, Hofhuis EH, Bloem MW, et al. Associa- the human hookworm species, Necator tion between intestinal parasitoses and nutri- americanus and Ancylostoma duodenale in an tional status in 3-8-year-old children in North- urban community in Ogun state, Nigeria. Afri- east Thailand. Trop Geogr Med 1990; 42: 312- can J Biotech 2003; 2: 470-3. 23. Al-Mekhlafi HM, Azlin M, Nor Aini U, et al. Malnutri- Ferreira CS, Ferreira MU, Noguera MR. The preva- tion and soil-transmitted helminthiasis among lence of infection by intestinal parasites in an Orang Asli children in Selangor, Malaysia. Asia urban slum in Sao Paulo, Brazil. J Trop Med Pacific J Clin Nutr 2005;14: 188-94. Hyg 1994: 97: 121-7. Al-Mekhlafi HM, Azlin M, Nor Aini U, et al. Preva- Geissler PW, Mwaniki D, Thiong F, Friis H. Geoph- lence and distribution of soil-transmitted hel- agy as a risk factor for geohelminth infections: minthiases among Orang Asli children in pe- a longitudinal study of Kenyan primary school- ripheral areas in Selangor, Malaysia. South- children. Trans R Soc Trop Med Hyg 1998; 92: east Asian J Trop Med Public Health 2006; 37: 7-11. 40-7. Gilgen D, Mascie-Taylor CG, Rosetta L. Intestinal Anantaphruti MT, Waikagul J, Maipanich W, helminth infections, anaemia and labour pro- Nuamtanong S, Pubampen S. Soil-transmit- ductivity of female tea pluckers in Bangladesh. ted helminthiases and health behaviors among Trop Med Int Health 2001; 6: 449-57. schoolchildren and community members in a Jozefzoon LME, Oostburg BFJ. Detection of hook- west-central border area of Thailand. South- worm and hookworm-like larvae in human east Asian J Trop Med Public Health 2004; 35: fecocultures in Suriname. Am J Trop Med Hyg 260-6. 1994; 51: 501-5. Azazy AA, Al-Mahbashi TY, Al-Mekhlafi HM. Preva- Kamath KR. Severe infection with Trichuris trichiura lence of intestinal and blood parasites among in Malaysian children. Am J Trop Med Hyg school children in Sana’a and Al-Mahweet 1973; 22: 600-5. provinces, Yemen. Yemen Med J 2002: 4: 50- Kamiya T, Morishita T, Mondaril T. Duodenoscopic 5. management in biliary ascariasis: ultrasonog- Bundy DAP, Kan SP, Rose R. Age related preva- raphy, endoscopic retrograde cholangio- lence, intensity and frequency distribution of pancreatography and biliary drainage.
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