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Acta Parasitologica

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Volume 62, Issue 2 (Jun 2017)

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The role of domestic dogs in the transmission of zoonotic helminthes in a rural area of Mekong river basin

Marcello Otake Sato
  • Corresponding author
  • Department of Tropical Medicine and Parasitology, Dokkyo Medical University, Mibu, Tochigi 321-0293, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Megumi Sato / Tippayarat Yoonuan
  • Department of Helminthology Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
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/ Tiengkham Pongvongsa / Surapol Sanguankiat
  • Department of Helminthology Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Sengchanh Kounnavong / Wanna Maipanich
  • Department of Helminthology Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
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  • De Gruyter OnlineGoogle Scholar
/ Yuichi Chigusa
  • Department of Tropical Medicine and Parasitology, Dokkyo Medical University, Mibu, Tochigi 321-0293, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Kazuhiko Moji / Jitra Waikagul
  • Department of Helminthology Faculty of Tropical Medicine, Mahidol University, Bangkok 10400, Thailand
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-04-18 | DOI: https://doi.org/10.1515/ap-2017-0047

Abstract

Dogs have been bred since ancient times for companionship, hunting, protection, shepherding and other human activities. Some canine helminth parasites can cause significant clinical diseases in humans as Opisthorchis viverrini causing cholangiocarcinoma in Southeast Asian Countries. In this study, socio-cultural questionnaire, canine parasitological analysis, necropsy, parasite molecular confirmation and dog roaming data were evaluated in Savannakhet, Lao-PDR, a typical Mekong Basin area. Dog owners comprised 48.8% of the studied population, with 61.2% owning one dog, 25.1% 2 dogs, 8.5% 3 dogs and 1.8% owning more than 4 dogs. Data from GPS logger attached to dogs showed they walked from 1.4 to 13.3 km per day, covering an area of 3356.38m2 average, with a routine of accessing water sources. Thirteen zoonotic helminth species were observed. Causative agents of visceral and cutaneous larva migrans occurred in 44.1% and 70% of the samples respectively. Spirometra erinaceieuropaei was detected in 44.1% of samples. Importantly, O. viverrini was found in 8.8% of samples. Besides the known importance of dogs in the transmission of Ancylostoma spp., Toxocara spp. and S. erinaceieuropaei, the observed roaming pattern of dogs confirmed it as an important host perpetuating O. viverrini in endemic areas; their routine access to waterbodies may spread O. viverrini eggs in a favorable environment for the fluke development, facilitating the infection of fishes, and consequently infecting humans living in the same ecosystem. Therefore, parasitic NTDs control programs in humans should be done in parallel with parasite control in animals, especially dogs, in the Mekong River basin area.

Keywords: Eco-health; helminth zoonosis; GIS; NTDs; Laos; Monsoon; Mekong Basin; canines

References

  • Acosta-Jamett G., Cleaveland S., Cunningham A.A., Bronsvoort B.M. 2010. Demography of domestic dogs in rural and urban areas of the Coquimbo region of Chile and implications for disease transmission. Preventive Veterinary Medicine, 94, 272–281. CrossrefGoogle Scholar

  • Aunpromma S., Tangkawattana P., Papirom P., Kanjampa P., Tesana S., Sripa B., Tangkawattana S. 2012. High prevalence of Opisthorchis viverrini infection in reservoir hosts in four districts of Khon Kaen Province, an opisthorchiasis endemic area of Thailand. Parasitology International, 61, 60–64. CrossrefGoogle Scholar

  • Brindley P.J., da Costa J.M., Sripa B. 2015. Why does infection with some helminths cause cancer? Trends in Cancer, 1, 174–182. CrossrefGoogle Scholar

  • Chai J.Y., Han E.T., Shin E.H., Sohn W.M., Yong T.S., Eom K.S., et al. 2009. High prevalence of Haplorchis taichui, Phaneropsolus molenkampi, and other helminth infections among people in Khammouane province, Lao PDR. The Korean Journal of Parasitology, 47, 243–247. CrossrefGoogle Scholar

  • Chai J.Y., Park J.H., Han E.T., Guk S.M., Shin E.H., Lin A., et al. 2005. Mixed infections with Opisthorchis viverrini and intestinal flukes in residents of Vientiane Municipality and Saravane Province in Laos. Journal of Helminthology, 79, 283–289. https://doi.org/10.1079/JOH2005302Crossref

  • Chen J., Xu M.J., Zhou D.H., Song H.Q., Wang C.R., Zhu X.Q. 2012. Canine and feline parasitic zoonoses in China. Parasites and Vectors. 5, 152. CrossrefGoogle Scholar

  • Conlan J.V., Khamlome B., Vongxay K., Elliot A., Pallant L., Sripa B., et al. 2012. Soil-transmitted helminthiasis in Laos: a community-wide cross-sectional study of humans and dogs in a mass drug administration environment. American Journal of Tropical Medicine and Hygiene, 86, 624–634. CrossrefGoogle Scholar

  • Dai R.S., Li Z.Y., Li F., Liu D.X., Liu W., Liu G.H., et al. 2009. Severe infection of adult dogs with helminths in Hunan Province, China poses significant public health concerns. Veterinary Parasitology. 160, 348–350. CrossrefGoogle Scholar

  • Despommier D. 2003. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clinical Microbiology Reviews, 16, 265–72. CrossrefGoogle Scholar

  • Eckert J., Conraths F.J., Tackmann K. 2000. Echinococcosis: an emerging or re-emerging zoonosis? International Journal for Parasitology, 30, 1283–1294. CrossrefGoogle Scholar

  • Eguía-Aguilar P., Cruz-Reyes A., Martinez-Maya J.J. 2005. Ecological analysis and description of the intestinal helminths present in dogs in Mexico City. Veterinary Parasitology, 127, 139–146. CrossrefGoogle Scholar

  • El-Shehabi F.S., Abdef-Afez S.K., Kamhawi S.A. 1999. Prevalence of intestinal helminths of dogs and fox from Jordan. Parasitology Research, 85, 928–934. CrossrefGoogle Scholar

  • Enes J.E., Wages A.J., Malone J.B., Tesana S. 2010. Prevalence of Opisthorchis viverrini infection in the canine and feline hosts in three villages, Khon Kaen Province, Northeastern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 41, 36–42Google Scholar

  • FAO. 2014. Dog population management. Report of the FAO/WSPA/IZSAM expert meeting – Banna, Italy, 14–19 March 2011. Animal Production and Health Report. No. 6. Rome.Google Scholar

  • Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar

  • Hashizume H., Sato M., Sato M.O., Ikeda S., Yoonuan T., Sanguankiat S., Pongvongsa T., Moji K., Minamoto T. 2017. Application of environmental DNA analysis for the detection of Opisthorchis viverrini DNA in water samples. Acta Tropica, 169, 1–7. CrossrefGoogle Scholar

  • Ing M.B., Schantz P.M., Turner J.A. 1998. Human coenurosis in North America: case reports and review. Clinical Infectious Diseases, 27, 519–523.Google Scholar

  • Jacobs D.E., Zhu X., Gasser R.B., Chilton N.B. 1997. PCR-based methods for identification of potentially zoonotic ascaridoid parasites of the dog, fox and cat. Acta Tropica, 68, 191–200. CrossrefGoogle Scholar

  • Kalkofen U.P. 1987. Hookworms of dogs and cats. The Veterinary Clinics of North America. Small Animal Practice, 17, 1341–1354.Google Scholar

  • Kamsa-Ard S., Luvira V., Pugkhem A., Luvira V., Thinkhamrop B., Suwanrungruang K., Bhudhisawasdi V. 2015. Association between praziquantel treatment and cholangiocarcinoma: a hospital-based matched case-control study. BMC Cancer. 15, 776. CrossrefGoogle Scholar

  • Koonmee S., Intapan P.M., Yamasaki H., Sugiyama H., Muto M., Kuramochi T., et al. 2011. Molecular identification of a causative parasite species using formalin-fixed paraffin embedded (FFPE) tissues of a complicated human pulmonary sparganosis case without decisive clinical diagnosis. Parasitology International, 60, 460–464. CrossrefGoogle Scholar

  • Liu Q., Li M.W., Wang Z.D., Zhao G.H., Zhu X.Q. 2015. Human sparganosis, a neglected food borne zoonosis. Lancet Infectious Diseases, 15, 1226–1235. CrossrefGoogle Scholar

  • Loukas A., Opdebeeck J., Croese J., Prociv P. 1994. Immunologic incrimination of Ancylostoma caninum as a human enteric pathogen. American Journal of Tropical Medicine and Hygiene, 50, 69–77Google Scholar

  • Maipanich W., Chaisiri K., Yoonuan T., Sato M., Sato M.O., Pongvongsa T., et al. 2011. Zoonotic Helminth Contamination of the Environment in Rural Villages of Southern Lao PDR. The Journal of Tropical Medicine and Parasitology, 34, 54–61Google Scholar

  • Maizels R.M., Meghji M., 1984. Repeated patent infection of adult dogs with Toxocara canis. Journal of Helminthology, 58, 327–333. CrossrefGoogle Scholar

  • Miyamoto K., Kirinoki M., Matsuda, H., Hayashi N., Chigusa Y., Sinuon M., et al. 2014. Field survey focused on Opisthorchis viverrini infection in five provinces of Cambodia. Parasitology International, 63, 366–373. CrossrefGoogle Scholar

  • Ngarmamonpirat C., Waikagul J., Petmitr S., Dekumyoy P., Rojekittikhun W., Anantapruti M.T. 2005. Analysis of sequence variation in Gnathostoma spinigerum mitochondrial DNA by single-strand conformation polymorphism analysis and DNA sequence. Parasitology International, 54, 65–68. CrossrefGoogle Scholar

  • Ngui R., Lee S.C., Yap N.J., Tan T.K., Aidil R.M., Chua K.H., et al. 2014. Gastrointestinal parasites in rural dogs and cats in Selangor and Pahang states in Peninsular Malaysia. Acta Parasitologica, 59, 737–44. CrossrefGoogle Scholar

  • Norman S.H., Kreutner Jr. A. 1980. Sparganosis: clinical and pathologic observations in ten cases. Southern Medical Journal, 73, 297–300Google Scholar

  • Oliveira-Sequeira T.G.C., Amarante A.F., Ferrari T.B., Nunes L.C. 2002. Prevalence of intestinal parasites in dogs from São Paulo State, Brazil. Veterinary Parasitology, 103, 19–27. CrossrefGoogle Scholar

  • Overgaauw P.A.M. 1997. Aspects of Toxocara epidemiology: toxocarosis in dogs and cats. Critical Reviews in Microbiology, 23, 233–251. CrossrefGoogle Scholar

  • Perry B.D. 1993. Dog ecology in eastern and southern Africa: implications for rabies control. Onderstepoort Journal of Veterinary Research, 60, 429–436.Google Scholar

  • Petney T.N., Andrews R.H., Saijuntha W., Wenz-Mücke A., Sithithaworn P. 2013. The zoonotic, fish-borne liver flukes Clonorchis sinensis, Opisthorchis felineus and Opisthorchis viverriniInternational Journal for Parasitology, 43, 1031–1046. CrossrefGoogle Scholar

  • Phommasack B., Saklokham K., Chanthavisouk C., Nakhonesid-Fish V., Strandgaard H., Montresor A., et al. 2008. Coverage and costs of a school deworming programme in 2007 targeting all primary schools in Lao PDR. Transactions of the Royal Society of Tropical Medicine and Hygiene, 102, 1201–1206. CrossrefGoogle Scholar

  • Prociv P., Croese J. 1990. Human eosinophilic enteritis caused by dog hookworm Ancylostoma caninum. The Lancet, 335, 1299–1302. CrossrefGoogle Scholar

  • Ramirez-Barrios R.A., Barboza-Mena G., Munoz J., Angulo-Cubillan F., Hernandez E., Gonzalez F., Escalona F. 2004. Prevalence of intestinal parasites in dogs under veterinary care in Maracaibo, Venezuela. Veterinary Parasitology, 121, 11–20. CrossrefGoogle Scholar

  • Rojekittikhun W., Mahittikorn A., Prummongkol S., Puangsa-art S., Chaisiri K., Kusolsuk T. 2013. Prevalence of gastrointestinal parasitic infections in refuge dogs and cats and evaluation of two conventional examination techniques. The Journal of Tropical Medicine and Parasitology, 36, 58–67.Google Scholar

  • Rojekittikhun W., Chaisiri K., Mahittikorn A., Pubampen S., SaNguankiat S., Kusolsuk T., et al. 2014. Gastrointestinal parasites of dogs and cats in a refuge in Nakhon Nayok, Thailand. Southeast Asian Journal of Tropical Medicine and Public Health, 45, 31–9Google Scholar

  • Sager H., Moret C.S., Grimm F., Deplazes P., Doherr M.G., Gottstein B. 2006. Coprological study on intestinal helminths in Swiss dogs: temporal aspects of anthelminthic treatment. Parasitology Research, 98, 333–338. CrossrefGoogle Scholar

  • Saowakontha S., Pipitgool V., Pariyanonda S., Tesana S., Rojsathaporn K., Intarakhao C. 1993. Field trials in the control of Opisthorchis viverrini with an integrated programme in endemic areas of northeast Thailand. Parasitology, 106, 283–288. CrossrefGoogle Scholar

  • Sato M., Pongvongsa T., Sanguankiat S., Yoonuan T., Dekumyoy P., Kalambaheti T., et al. 2010b. Copro-DNA diagnosis of Opisthorchis viverrini and Haplorchis taichui infection in an endemic area of Lao PDR. Southeast Asian Journal of Tropical Medicine and Public Health. 41, 28–35Google Scholar

  • Sato M., Pongvongsa T., Sanguankiat S., Yoonuan T., Kobayashi J., Boupha B., et al. 2015. Patterns of trematode infections of Opisthorchis viverrini (Opisthorchiidae) and Haplorchis taichui (Heterophyidae) in human populations from two villages in Savannakhet Province, Lao PDR. Journal of Helminthology, 89, 439–445. CrossrefGoogle Scholar

  • Sato M., Sanguankiat S., Yoonuan T., Pongvongsa T., Keomoungkhoun M., Phimmayoi I., et al. 2010a. Copro-molecular identification of infections with hookworm eggs in rural Lao PDR. Transactions of the Royal Society of Tropical Medicine and Hygiene, 104, 617–622. CrossrefGoogle Scholar

  • Sato M., Yoonuan T., Sanguankiat S., Nuamtanong S., Pongvongsa T., Phimmayoi I., et al. 2011. Human Trichostrongylus colubriformis infection in a rural Laotian village. American Journal of Tropical Medicine and Hygiene, 84, 52–54. CrossrefGoogle Scholar

  • Sato M.O., Sako Y., Nakao M., Wandra T., Yamasaki H., Nakaya K., Ito A. 2007. Usefulness of immunological and molecular tools: programs towards control and eradication of cysticercosis in endemic areas. Southeast Asian Journal of Tropical Medicine and Public Health, 38S1, 159–165Google Scholar

  • Sato M.O., Sato M., Chaisiri K., Maipanich W., Yoonuan T., Sanguankiat S., et al. 2014. Nematode infection among ruminants in monsoon climate (Ban-Lahanam, Lao PDR) and its role as food-borne zoonosis. Revista Brasileira de Parasitologia Veterinaria, 23, 80–4CrossrefGoogle Scholar

  • Sithithaworn P., Andrews R.H., Nguyen V.D., Wongsaroj T., Sinuon M., Odermatt P., et al. 2012. The current status of opisthorchiasis in the Mekong Basin. Parasitology International, 61, 10–16. CrossrefGoogle Scholar

  • Sripa B. 2003. Pathobiology of opisthorchiasis: an update. Acta Tropica, 88, 209–220. CrossrefGoogle Scholar

  • Thrusfield M., 2005. Surveys. In: (Ed. M. Thrusfield) Veterinary epidemiology. Blackwell, Oxford, pp. 228–242Google Scholar

  • Touch S., Yoonuan T., Nuamtanong S., Homsuwan N., Phupisut O., Thaenkham U., Waikagul J. 2013. Seasonal variation of Opisthorchis viverrini metacercarial infection in cyprinid fish from Southern Cambodia. The Journal of Tropical Medicine and Parasitology, 36, 1–7Google Scholar

  • Traub R.J., Inpankaew T., Sutthikornchai C., Sukthana Y., Thompson A.R.C. 2008. PCR-based coprodiagnostic tools reveal dogs as reservoirs of zoonotic ancylostomiasis caused by Ancylostoma ceylanicum in temple communities in Bangkok. Veterinary Parasitology, 155, 67–73. CrossrefGoogle Scholar

  • Traub R.J., Robertson I.D., Irwin P.J., Mencke N., Thompson R.C. 2005. Canine gastrointestinal parasitic zoonoses in India. Trends in Parasitology, 21, 42–48. CrossrefGoogle Scholar

  • Vonghachack Y., Dekumyoy P., Yoonuan T., Sanguankiat S., Nuamtanong S., Thaenkham U., et al. 2010. Sero-epidemiological survey of gnathostomiasis in Lao PDR. Parasitology International, 59, 599–605. CrossrefGoogle Scholar

  • Waikagul J., Anantaphruti M.T., Nuamtanong S., Sanguankait S. 1997. Evaluation of the modified formalin detergent technique for detection of intestinal parasites. In Hayashi et al. eds, Collected Papers on the Control of Soil-transmitted Helminthiases (by the APCO Research Group) 6, 5–11Google Scholar

  • Wang G.D., Zhai, W., Yang H.C., Wang L., Zhong L., Liu Y.H., et al. 2016. Out of southern East Asia: the natural history of domestic dogs across the world. Cell Research, 26, 21–33. CrossrefGoogle Scholar

  • WHO 1987. Prevention and control of intestinal parasitic infections. Report of a WHO Expert Committee. World Health Organization Technical Reports Series, 749, 1–86Google Scholar

  • Wongratanacheewin S., Pumidonming W., Sermswan R.W., Maleewong W. 2001. Development of a PCR-based method for the detection of Opisthorchis viverrini in experimentally infected hamsters. Parasitology, 122, 175–180. CrossrefGoogle Scholar

About the article

Received: 2016-11-10

Revised: 2016-12-28

Accepted: 2017-01-20

Published Online: 2017-04-18

Published in Print: 2017-06-01


Citation Information: Acta Parasitologica, ISSN (Online) 1896-1851, ISSN (Print) 1230-2821, DOI: https://doi.org/10.1515/ap-2017-0047.

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