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Soil-Transmitted Helminthiasis in Laos: A Community-Wide Cross-Sectional Study of Humans and Dogs in a Mass Drug Administration Environment
James V. Conlan
James V. Conlan
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Boualam Khamlome
Boualam Khamlome
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Khamphouth Vongxay
Khamphouth Vongxay
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Aileen Elliot
Aileen Elliot
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Louise Pallant
Louise Pallant
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Banchob Sripa
Banchob Sripa
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Stuart D. Blacksell
Stuart D. Blacksell
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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Stanley Fenwick
Stanley Fenwick
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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R. C. Andrew Thompson
R. C. Andrew Thompson
School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia; Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos; National Animal Health Centre, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos; Tropical Disease Research Laboratory, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand; Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand; Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, Oxford, United Kingdom
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We conducted a community cross-sectional survey of soil-transmitted helminthiasis in humans and dogs in four provinces in northern Laos. We collected and tested human and dog fecal samples and analyzed results against sociodemographic data. The prevalence of Ascaris lumbricoides, Trichuris trichiura, hookworm, and Strongyloides stercoralis was 26.1% (95% confidence interval [CI] = 23.7–28.4%), 41.5% (95% CI = 38.8–44.1%), 46.3% (95% CI = 43.3–49.0%), and 8.9% (95% CI = 7.4–10.4%), respectively. We observed strong heterogeneity for helminthiasis by ethnicity, province, and wealth status, which coincided with a risk profile demonstrating that Mon-Khmer persons and the poorest households are highly vulnerable. Necator americanus was the dominant hookworm species infecting humans and Ancylostoma ceylanicum was the only Ancylostoma species detected. Hookworm prevalence in village dogs was 94%, and the dominant species was A. ceylanicum. Necator americanus was also detected in dogs. It appears that dogs have a role in human hookworm transmission and warrant further investigation.
Author Notes
Financial support: This study was supported by the Australian Centre for International Agricultural Research (project no. AH2006/161). James V. Conlan was supported by a Murdoch University Research Studentship award.
Authors’ addresses: James V. Conlan, Aileen Elliot, Louise Pallant, Stanley Fenwick, and R. C. Andrew Thompson, School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia, Australia, E-mails: james.conlan@foodstandards.gov.au, a.elliot@murdoch.edu.au, l.pallant@murdoch.edu.au, stanley_fenwick@dai.com, and a.thompson@murdoch.edu.au. Boualam Khamlome, Department of Hygiene and Prevention, Ministry of Health, Vientiane, Laos, E-mail: drboualam2004@yahoo.com.au. Khamphouth Vongxay, Department of Livestock and Fisheries, Ministry of Agriculture and Forestry, Vientiane, Laos, E-mail: kamputvongxay@yahoo.com. Banchob Sripa, Tropical Disease Research Laboratory, Division of Experimental Pathology, Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand, E-mail: banchob@kku.ac.th. Stuart D. Blacksell, Mahidol–Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Bangkok, Thailand, E-mail: stuart@tropmedres.ac.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19 : 547– 551.
-
2.
Hotez PJ, Ehrenberg JP, 2010. Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region. Adv Parasitol 72 : 31– 53.
-
3.
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 367 : 1521– 1532.
-
4.
Pullan R, Brooker S, 2008. The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology 135 : 783– 794.
-
5.
Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, Kurtis JD, Mor V, Olveda RM, Friedman JF, 2008. The synergistic effect of concomitant schistosomiasis, hookworm, and Trichuris infections on children's anemia burden. PLoS Negl Trop Dis 2 : e245.
-
6.
Steinmann P, Utzinger J, Du ZW, Zhou XN, 2010. Multiparasitism: a neglected reality on global, regional and local scale. Adv Parasitol 73 : 21– 50.
-
7.
Rim HJ, Chai JY, Min DY, Cho SY, Eom KS, Hong SJ, Sohn WM, Yong TS, Deodato G, Standgaard H, Phommasack B, Yun CH, Hoang EH, 2003. Prevalence of intestinal parasite infections on a national scale among primary schoolchildren in Laos. Parasitol Res 91 : 267– 272.
-
8.
World Health Organization, 2009. First Mekong-Plus Programme Managers Workshop on Lymphatic Filariasis and Other Helminthiasis. Available at: http://www.wpro.who.int/internet/files/mvp/ CambodiaLFNTD_report2.pdf.
-
9.
Phommasack B, Saklokham K, Chanthavisouk C, Nakhonesid-Fish V, Strandgaard H, Montresor A, Shuey DA, Ehrenberg J, 2008. Coverage and costs of a school deworming programme in 2007 targeting all primary schools in Lao PDR. Trans R Soc Trop Med Hyg 102 : 1201– 1206.
-
10.
Keiser J, Utzinger J, 2008. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 299 : 1937– 1948.
-
11.
Knopp S, Mohammed KA, Speich B, Hattendorf J, Khamis IS, Khamis AN, Stothard JR, Rollinson D, Marti H, Utzinger J, 2010. Albendazole and mebendazole administered alone or in combination with ivermectin against Trichuris trichiura: a randomized controlled trial. Clin Infect Dis 51 : 1420– 1428.
-
12.
Keiser J, Utzinger J, 2010. The drugs we have and the drugs we need against major helminth infections. Adv Parasitol 73 : 197– 230.
-
13.
Flohr C, Tuyen LN, Lewis S, Minh TT, Campbell J, Britton J, Williams H, Hien TT, Farrar J, Quinnell RJ, 2007. Low efficacy of mebendazole against hookworm in Vietnam: two randomized controlled trials. Am J Trop Med Hyg 76 : 732– 736.
-
14.
Bethony J, Chen J, Lin S, Xiao S, Zhan B, Li S, Xue H, Xing F, Humphries D, Yan W, Chen G, Foster V, Hawdon JM, Hotez PJ, 2002. Emerging patterns of hookworm infection: influence of aging on the intensity of Necator infection in Hainan Province, People's Republic of China. Clin Infect Dis 35 : 1336– 1344.
-
15.
Humphries DL, Stephenson LS, Pearce EJ, The PH, Dan HT, Khanh LT, 1997. The use of human faeces for fertilizer is associated with increased intensity of hookworm infection in Vietnamese women. Trans R Soc Trop Med Hyg 91 : 518– 520.
-
16.
Gandhi NS, Jizhang C, Khoshnood K, Fuying X, Shanwen L, Yaoruo L, Bin Z, Haechou X, Chongjin T, Yan W, Wensen W, Dungxing H, Chong C, Shuhua X, Hawdon JM, Hotez PJ, 2001. Epidemiology of Necator americanus hookworm infections in Xiulongkan Village, Hainan Province, China: high prevalence and intensity among middle-aged and elderly residents. J Parasitol 87 : 739– 743.
-
17.
Sato M, Sanguankiat S, Yoonuan T, Pongvongsa T, Keomoungkhoun M, Phimmayoi I, Boupa B, Moji K, Waikagul J, 2010. Copro-molecular identification of infections with hookworm eggs in rural Lao PDR. Trans R Soc Trop Med Hyg 104 : 617– 622.
-
18.
Jiraanankul V, Aphijirawat W, Mungthin M, Khositnithikul R, Rangsin R, Traub RJ, Piyaraj P, Naaglor T, Taamasri P, Leelayoova S, 2011. Incidence and risk factors of hookworm infection in a rural community of central Thailand. Am J Trop Med Hyg 84 : 594– 598.
-
19.
Anten JF, Zuidema PJ, 1964. Hookworm infection in Dutch servicemen returning from West New Guinea. Trop Geogr Med 64 : 216– 224.
-
20.
Traub RJ, Inpankaew T, Sutthikornchai C, Sukthana Y, Thompson RC, 2008. PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Vet Parasitol 155 : 67– 73.
-
21.
Anonymous, 2006. Population and Housing Census 2005. Vientiane, Laos: Steering Committee for Census of Population and Housing, Department of Statistics, Ministry of Planning and Investment.
-
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World Health Organization, 2008. Review on the Epidemiological Profile of Helminthiases and their Control in the Western Pacific Region, 1997–2008. Available at: http://www.wpro.who.int/NR/rdonlyres/0077CD18-11FE-4F89-B1EE-864F5D7F48CF/0/Helminths10YearReview_reformattedv2_.pdf.
-
23.
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG, 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23 : 2947– 2948.
-
24.
Steinmann P, Zhou XN, Li YL, Li HJ, Chen SR, Yang Z, Fan W, Jia TW, Li LH, Vounatsou P, Utzinger J, 2007. Helminth infections and risk factor analysis among residents in Eryuan county, Yunnan province, China. Acta Trop 104 : 38– 51.
-
25.
Raso G, Utzinger J, Silué KD, Ouattara M, Yapi A, Toty A, Matthys B, Vounatsou P, Tanner M, N’Goran EK, 2005. Disparities in parasitic infections, perceived ill health and access to health care among poorer and less poor schoolchildren of rural Côte d’Ivoire. Trop Med Int Health 10 : 42– 57.
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