Epidemiology of intestinal polyparasitism among Orang Asli school children in rural Malaysia
Open accessAbstract
BACKGROUND: This cross-sectional study aimed to investigate the current prevalence and risk factors associated with intestinal polyparasitism (the concurrent infection with multiple intestinal parasite species) among Orang Asli school children in the Lipis district of Pahang state, Malaysia. METHODS/PRINCIPAL FINDINGS: Fecal samples were collected from 498 school children (50.6% boys and 49.4% girls), and examined by using direct smear, formalin-ether sedimentation, trichrome stain, modified Ziehl Neelsen stain, Kato-Katz, and Harada Mori techniques. Demographic, socioeconomic, environmental, and personal hygiene information were collected by using a pre-tested questionnaire. Overall, 98.4% of the children were found to be infected by at least one parasite species. Of these, 71.4% had polyparasitism. The overall prevalence of Trichuris trichiura, Ascaris lumbricoides, hookworm, Giardia duodenalis, Entamoeba spp., and Cryptosporidium spp. infections were 95.6%, 47.8%, 28.3%, 28.3%, 14.1% and 5.2%, respectively. Univariate and multivariate analyses showed that using an unsafe water supply as a source for drinking water, presence of other family members infected with intestinal parasitic infections (IPI), not washing vegetables before consumption, absence of a toilet in the house, not wearing shoes when outside, not cutting nails periodically, and not washing hands before eating were significant risk factors associated with intestinal polyparasitism among these children. CONCLUSIONS/SIGNIFICANCE: Intestinal polyparasitism is highly prevalent among children in the peninsular Malaysian Aboriginal communities. Hence, effective and sustainable control measures, including school-based periodic chemotherapy, providing adequate health education focused on good personal hygiene practices and proper sanitation, as well as safe drinking water supply should be implemented to reduce the prevalence and consequences of these infections in this population.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Studies that compared access to sanitation between men and women found largely unremarkable gender differences.
“Generally, studies that compared access to sanitation between men and women found largely unremarkable gender differences (Ugbomoiko et al., 2009;Al-Delaimy et al., 2014;Alemu et al., 2017;Baker et al., 2018).”
From A Systematic Review of Water and Gender Interlinkages: Assessing the Intersection With Health (2020) · cites this paper as Al-Delaimy et al., 2014
A single study directly analyzed the effect of gender on the frequency of waterborne diseases in adults and found no gender differences.
“A single study directly analyzed the effect of gender on the frequency of waterborne diseases in adults, and found no gender differences (Al-Delaimy et al., 2014).”
From A Systematic Review of Water and Gender Interlinkages: Assessing the Intersection With Health (2020) · cites this paper as Al-Delaimy et al., 2014
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A Simple Sequentially Rejective Multiple Test Procedure
(1979) · Scandinavian Journal of Statistics · doi:10.2307/4615733 · Cited by 21,526 · see citing works
District Laboratory Practice in Tropical Countries
Cheesbrough, M. (2005) · Cambridge University Press eBooks · doi:10.1017/cbo9780511581304 · Cited by 2,689 · see citing works
Sample Size Determination in Health Studies: A Practical Manual.
Lachenbruch, P. A., Lwanga, S. K., & Lemeshow, S. (1991) · Journal of the American Statistical Association · doi:10.2307/2290547 · Cited by 2,097 · see citing works
Use and misuse of population attributable fractions
Rockhill, B., Newman, B., & Weinberg, C. (1998) · American Journal of Public Health · doi:10.2105/ajph.88.1.15 · Cited by 1,683 · see citing works
Prevention and control of schistosomiasis and soil-transmitted helminthiasis.
(2002) · PubMed · Cited by 1,315 · see citing works
Stanley, S. L. (2003) · The Lancet · doi:10.1016/s0140-6736(03)12830-9 · Cited by 1,155 · see citing works
Rescuing the bottom billion through control of neglected tropical diseases
Hotez, P. J., Fenwick, A., Savioli, L., & Molyneux, D. H. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60233-6 · Cited by 945 · see citing works
Staining of Cryptosporidia by a Modified Ziehl-Neelsen Technique
Henriksen, S. A., & Pohlenz, J. (1981) · Acta veterinaria Scandinavica · doi:10.1186/bf03548684 · Cited by 902 · see citing works
Comparison of Stopping Rules in Forward “Stepwise” Regression
Bendel, R. B., & Afifi, A. A. (1977) · Journal of the American Statistical Association · doi:10.1080/01621459.1977.10479905 · Cited by 885 · see citing works
N UTRITIONAL I MPACT OF I NTESTINAL H ELMINTHIASIS D URING THE H UMAN L IFE C YCLE
Crompton, D. W. T., & Nesheim, M. C. (2002) · Annual Review of Nutrition · doi:10.1146/annurev.nutr.22.120501.134539 · Cited by 512 · see citing works
Knopp, S., Mgeni, A. F., Khamis, I. S., Steinmann, P., Stothard, J. R., Rollinson, D., Marti, H., & Utzinger, J. (2008) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000331 · Cited by 362 · see citing works
Comparison of Stopping Rules in Forward "Stepwise" Regression
Bendel, R. B., & Afifi, A. A. (1977) · Journal of the American Statistical Association · doi:10.2307/2286904 · Cited by 356 · see citing works
Strongyloides stercoralis: there but not seen
Montes, M., Sawhney, C., & Barros, N. (2010) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0b013e32833df718 · Cited by 252 · see citing works
Raso, G. (2004) · International Journal of Epidemiology · doi:10.1093/ije/dyh241 · Cited by 206 · see citing works
Current Views on the Clinical Relevance of Blastocystis spp.
Tan, K. S. W., Mirza, H., Teo, J. D. W., et al. (2010) · Current Infectious Disease Reports · doi:10.1007/s11908-009-0073-8 · Cited by 204 · see citing works
Haque, R., Mondal, D., Kirkpatrick, B. D., Akther, S., Farr, B. M., Sack, R. B., & Petri, W. A. (2003) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2003.69.398 · Cited by 199 · see citing works
Does helminth infection affect mental processing and educational achievement?
Nokes, C., & Bundy, D. A. P. (1994) · Parasitology Today · doi:10.1016/0169-4758(94)90348-4 · Cited by 188 · see citing works
Stoltzfus, R. J., Tielsch, J. M., Chwaya, H. M., Montresor, A., Albonico, M., & Savioli, L. (2000) · Journal of Nutrition · doi:10.1093/jn/130.7.1724 · Cited by 181 · see citing works
Prevalence and Risk Factors of Intestinal Parasitism in Rural and Remote West Malaysia
Ngui, R., Ishak, S., Chow, S.-C., Mahmud, R., & Lim, Y. A. L. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000974 · Cited by 175 · see citing works
Self-citationSokhna, C., Hesran, J. L., Mbaye, P. A., et al. (2004) · Malaria Journal · doi:10.1186/1475-2875-3-43 · Cited by 166 · see citing works
Estimating the Impact of Amebiasis on Health
Petri, W. A., Haque, R., Lyerly, D. M., et al. (2000) · Parasitology Today · doi:10.1016/s0169-4758(00)01730-0 · Cited by 165 · see citing works
Ngui, R., Lim, Y. A. L., Chong Kin, L., Sek Chuen, C., & Jaffar, S. (2012) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0001550 · Cited by 159 · see citing works
Self-citationBlastocystis: getting to grips with our guileful guest
Scanlan, P. D., & Stensvold, C. R. (2013) · Trends in Parasitology · doi:10.1016/j.pt.2013.08.006 · Cited by 156 · see citing works
Gibson, A. K., Raverty, S., Lambourn, D. M., et al. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001142 · Cited by 140 · see citing works
Matthys, B., Bobieva, M., Karimova, G., et al. (2011) · Parasites & Vectors · doi:10.1186/1756-3305-4-195 · Cited by 128 · see citing works
(1965) · Annals of Internal Medicine · doi:10.7326/0003-4819-62-2-421_3 · Cited by 126 · see citing works
Inês, E. D. J., de Souza, J. N., Santos, R. C., et al. (2011) · Acta Tropica · doi:10.1016/j.actatropica.2011.08.010 · Cited by 126 · see citing works
Polyparasitism and its impact on the immune system
Supali, T., Verweij, J. J., Wiria, A. E., et al. (2010) · International Journal for Parasitology · doi:10.1016/j.ijpara.2010.05.003 · Cited by 124 · see citing works
Brooker, S., Miguel, E. A., Moulin, S., Louba, A., Bundy, D. A. P., & Kremer, M. R. (2009) · East African Medical Journal · doi:10.4314/eamj.v77i3.46613 · Cited by 115 · see citing works
Luoba, A. I., Geissler, P., Estambale, B., Ouma, J., Alusala, D., Ayah, R., Mwaniki, D., Magnussen, P., & Friis, H. (2005) · Tropical medicine & international health · doi:10.1111/j.1365-3156.2004.01380.x · Cited by 114 · see citing works
Malabsorption of water miscible vitamin A in children with giardiasis and ascariasis
Mahalanabis, D., Simpson, T., Ml, C., Ganguli, C., Bhattacharjee, A., & Mukherjee, K. L. (1979) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/32.2.313 · Cited by 112 · see citing works
Prevention of diarrhoea and dysentery by hand washing
Han, A. M., & Hlaing, T. (1989) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(89)90737-2 · Cited by 105 · see citing works
Schmidlin, T., Hürlimann, E., Silué, K. D., Yapi, R. B., Houngbedji, C. A., Kouadio, B. A., Acka-Douabélé, C. A., Dongo, K., Ouattara, M., Zouzou, F., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065722 · Cited by 105 · see citing works
Mayer, K. H., Karp, C. L., Auwaerter, P. G., et al. (2007) · Clinical Infectious Diseases · doi:10.1086/522180 · Cited by 102 · see citing works
Prevalence of intestinal protozoa in an aborigine community in Pahang, Malaysia.
Azian, M. Y. N., San, Y. M., Gan, C.-X., et al. (2007) · PubMed · Cited by 101 · see citing works
Clustering of Ascaris lumbricoides and Trichuris trichiura infections within households
Forrester, J. E., Scott, M. E., Bundy, D. A. P., & Golden, M. H. N. (1988) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(88)90448-8 · Cited by 101 · see citing works
Giardia intestinalis genotypes: Risk factors and correlation with clinical symptoms
Mahdy, M. A. K., Surin, J., Wan, K., et al. (2009) · Acta Tropica · doi:10.1016/j.actatropica.2009.06.012 · Cited by 100 · see citing works
Al‐Mekhlafi, H. M., Surin, J., Atiya, A. S., Ariffin, W. A., Mahdy, M. A. K., & Abdullah, H. (2008) · Acta Tropica · doi:10.1016/j.actatropica.2008.05.022 · Cited by 97 · see citing works
Self-citationBelyhun, Y., Medhin, G., Amberbir, A., Erko, B., Hanlon, C., Alem, A., Venn, A. J., Britton, J. R., & Davey, G. (2010) · BMC Public Health · doi:10.1186/1471-2458-10-21 · Cited by 96 · see citing works
Naish, S., McCarthy, J. S., & Williams, G. M. (2004) · Acta Tropica · doi:10.1016/j.actatropica.2004.04.004 · Cited by 87 · see citing works
Glickman, L. T. (1999) · International Journal of Epidemiology · doi:10.1093/ije/28.1.169 · Cited by 87 · see citing works
Nasr, N. A., Al‐Mekhlafi, H. M., Ahmed, A., et al. (2013) · Parasites & Vectors · doi:10.1186/1756-3305-6-27 · Cited by 83 · see citing works
Self-citationSanchez, A., Gabrie, J., Usuanlele, M., Rueda, M. M., Canales, M., & Gyorkos, T. (2013) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0002378 · Cited by 81 · see citing works
Nasr, N. A., Al-Mekhlafi, H. M., Ahmed, A., Roslan, M. A., & Bulgiba, A. (2013) · Parasites & Vectors · doi:10.1186/1756-3305-6-28 · Cited by 79 · see citing works
Self-citationMuniz‐Junqueira, M. I., & Queiróz, E. F. O. (2002) · Revista da Sociedade Brasileira de Medicina Tropical · doi:10.1590/s0037-86822002000200002 · Cited by 78 · see citing works
Helminthiasis and Hygiene Conditions of Schools in Ikenne, Ogun State, Nigeria
Ekpo, U. F., Odoemene, S. N., Mafiana, C. F., et al. (2008) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000146 · Cited by 71 · see citing works
Al‐Mekhlafi, H. M., Al-Maktari, M. T., Jani, R., Ahmed, A., Anuar, T. S., Moktar, N., Mahdy, M. A. K., Lim, Y. A. L., Mahmud, R., & Surin, J. (2013) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002516 · Cited by 70 · see citing works
Self-citationLim, Y. A. L., Romano, N., Colin, N., Chow, S. C., & Smith, H. V. (2009) · PubMed · Cited by 70 · see citing works
Self-citationMahdy, M. A. K., Lim, Y. A. L., Surin, J., et al. (2008) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2008.02.004 · Cited by 69 · see citing works
Self-citationAhmad, A. F., Hadip, F., Ngui, R., et al. (2013) · Parasitology Research · doi:10.1007/s00436-013-3450-z · Cited by 64 · see citing works
Associations among multiple geohelminth species infections in schoolchildren from Pemba Island
Booth, M., Bundy, D. A. P., Albonico, M., Chwaya, H. M., Alawi, K. S., & Savioli, L. (1998) · Parasitology · doi:10.1017/s003118209700190x · Cited by 63 · see citing works
Gunawardena, K., Kumarendran, B., Ebenezer, R., Gunasingha, M. S., Pathmeswaran, A., & de Silva, N. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001341 · Cited by 63 · see citing works
Al‐Mekhlafi, H. M., Azlin, M., Aini, U. N., et al. (2005) · PubMed · Cited by 59 · see citing works
Self-citationAhmed, A., Al‐Mekhlafi, H. M., Choy, S. H., et al. (2011) · Parasites & Vectors · doi:10.1186/1756-3305-4-242 · Cited by 59 · see citing works
Self-citationContamination of soil with helminth parasite eggs in Nepal.
Rai, S. K., Uga, S., Ono, K., et al. (2000) · PubMed · Cited by 55 · see citing works
Fung, I. C.-H., & Cairncross, S. (2009) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2008.08.003 · Cited by 52 · see citing works
Anuar, T. S., Al‐Mekhlafi, H. M., Ghani, M. K. A., et al. (2012) · International Journal for Parasitology · doi:10.1016/j.ijpara.2012.07.003 · Cited by 50 · see citing works
Self-citationAn unceasing problem: soil-transmitted helminthiases in rural Malaysian communities.
Al‐Mekhlafi, H. M., Atiya, A. S., Lim, Y. A. L., et al. (2007) · PubMed · Cited by 49 · see citing works
Self-citationAnuar, T. S., Al‐Mekhlafi, H. M., Ghani, M. K. A., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0048165 · Cited by 49 · see citing works
Self-citationMalaria: the value of the automated depolarization analysis.
Jamaiah, I., & Rohela, M. (2005) · PubMed · Cited by 49 · see citing works
Norhayati, M., Oothuman, P., Azizi, O., et al. (1997) · PubMed · Cited by 49 · see citing works
Detection of helminth infections in dogs and soil contamination in rural and urban areas.
Azian, M. Y. N., Sakhone, L., Hakim, S. L., Yusri, M. Y., Nurulsyamzawaty, Y., Zuhaizam, A. H., Rodi, I. M., & Maslawaty, M. N. (2008) · PubMed · Cited by 45 · see citing works
Ahmed, A., Al‐Mekhlafi, H. M., Azam, M. N., Ithoi, I., Al‐Adhroey, A. H., Abdulsalam, A. M., & Surin, J. (2012) · Parasitology · doi:10.1017/s003118201100237x · Cited by 41 · see citing works
Self-citationA simple and quantitative method for the determination of tissue factor.
Norhayati, M., Zainudin, B., Mohammod, C. G., et al. (1997) · PubMed · Cited by 39 · see citing works
Sinniah, B., Sabaridah, I., Soe, M. M., et al. (2012) · PubMed · Cited by 36 · see citing works
Egger, R. J., Eh, H., Bloem, M. W., et al. (1990) · PubMed · Cited by 35 · see citing works
Giardiasis and Poor Vitamin A Status among Aboriginal School Children in Rural Malaysia
Al‐Mekhlafi, H. M., Surin, J., Sallam, A. A., et al. (2010) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2010.09-0371 · Cited by 33 · see citing works
Self-citationDetection of Hookworm and Hookworm-Like Larvae in Human Fecocultures in Suriname
Lm, J., & Oostburg, B. F. J. (1994) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1994.51.501 · Cited by 30 · see citing works
Training Manual on Diagnosis of Intestinal Parasites
Pasvol, G. (1999) · Parasitology Today · doi:10.1016/s0169-4758(98)01366-0 · Cited by 27 · see citing works
ChildhoodCryptosporidiuminfection among aboriginal communities in Peninsular Malaysia
Al‐Mekhlafi, H. M., Mahdy, M. A. K., Azlin, M., Fatmah, M. S., & Norhayati, M. (2011) · Annals of Tropical Medicine and Parasitology · doi:10.1179/136485911x12899838683368 · Cited by 21 · see citing works
Self-citationFaustini, A., Marinacci, C., Fabrizi, E., et al. (2005) · Epidemiology and Infection · doi:10.1017/s0950268805005327 · Cited by 20 · see citing works
Sex, Sex Differences, and Social Behavior
Rabinowitz, V. C., & Valian, V. V. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06625.x · Cited by 11 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [25]Norhayati M, Zainudin B, Mohammod C, Oothuman P, Azizi O, Fatmah MS (1997) The prevalence of Trichuris, Ascaris and hookworm infection in Orang Asli children. Southeast Asian J Trop Med Public Health 28: 161– 168. 9322301
- [45]Jamaiah I, Rohela M (2005) Prevalence of intestinal parasites among members of the public in Kuala Lumpur, Malaysia. Southeast Asian J Trop Med Public Health 36: 68– 71. 15906644
Cited by
Sorted by citations
A Systematic Review of Water and Gender Interlinkages: Assessing the Intersection With Health
Pouramin, P., Nagabhatla, N., & Miletto, M. (2020) · Frontiers in Water · doi:10.3389/frwa.2020.00006 · Cited by 96 · see citing works
“Studies which considered gender likewise revealed a lack of access to improved water for both men and women alike (Ugbomoiko et al., 2009; Al-Delaimy et al., 2014; Atalabi et al., 2016; Holvoet et al., 2016; Akombi et al., 2017; Baker et al., 2018).”
Background
- Authors
- Al-Delaimy, A. K., Al-Mekhlafi, H. M., Nasr, N. A., Sady, H., Atroosh, W. M., Nashiry, M., Anuar, T. S., Moktar, N., Lim, Y. A. L., & Mahmud, R.
- Affiliations
- University of Anbar (IQ)
- University of Malaya (MY)
- Universiti Teknologi MARA System (MY)
- National University of Malaysia (MY)
- Venue
- PLoS neglected tropical diseases
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-08-21
- Volume
- 8
- Issue
- 8
- Pages
- e3074
- ISSN
- 1935-2727 (ISSN-L)
- 1935-2735
- PMC
- PMC4140674
- OpenAlex
- W2171843782
- Cited by
- 110
- References
- 72
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 5 · 2023: 7 · 2022: 19 · 2021: 10 · 2020: 13 · 2019: 11 · 2018: 5 · 2017: 11 · 2016: 13 · 2015: 3 · 2014: 1
- FWCI
- 6.81
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS neglected tropical diseases (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Greater South Information System
- Funders
- Ministry of Higher Education, Malaysia
- Universiti Malaya (UM.C/625/1/HIR/MOHE/MED/18, UM-MOHE UM.C/625/1/HIR/MOHE/MED/18, UM.C/625/1/HIR)
- Majlis Amanah Rakyat
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Life Sciences › Immunology and Microbiology › Parasitology › Parasitic Infections and Diagnostics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Parasitic infections in humans and animals
- Keywords
- intestinal parasitic infections, Orang Asli, elementary school students, risk factors, Trichuris trichiura, Ascaris lumbricoides, hookworm, Giardia lamblia, Entamoeba, Cryptosporidium, unsafe drinking water, personal hygiene, sanitation
- MeSH terms
- Age Factors, Animals, Child, Cross-Sectional Studies, Feces, Female, Humans, Hygiene, Intestinal Diseases, Parasitic, Malaysia, Male, Risk Factors, Prevalence
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
