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Role of dog behaviour and environmental fecal contamination in transmission of Echinococcus multilocularis in Tibetan communities

Published online by Cambridge University Press:  22 August 2011

A. VANISCOTTE*
Affiliation:
Department of Chrono-environment, UMR UFC/CNRS 6249 aff. INRA, University of Franche-Comté, 25030 Besançon cedex, France Department of Arctic and Marine Biology, University of Tromsø, Norway-9037
F. RAOUL
Affiliation:
Department of Chrono-environment, UMR UFC/CNRS 6249 aff. INRA, University of Franche-Comté, 25030 Besançon cedex, France
M. L. POULLE
Affiliation:
Laboratoire de Parasitologie-Mycologie, EA 3800, University of Reims Champagne-Ardennes (URCA), IFR 53, 51 rue Cognacq, 51096 Reims, France URCA-CERFE, 5 rue de la Héronniere, 08240 Boult-aux-Bois, France
T. ROMIG
Affiliation:
Department of Parasitology, University of Hohenheim, 70599 Stuttgart, Germany
A. DINKEL
Affiliation:
Department of Parasitology, University of Hohenheim, 70599 Stuttgart, Germany
K. TAKAHASHI
Affiliation:
Hokkaido Institute of Public Health, Kita 19, Nishi 12, 060-0819 Sapporo, Japan
M. H. GUISLAIN
Affiliation:
URCA-CERFE, 5 rue de la Héronniere, 08240 Boult-aux-Bois, France
J. MOSS
Affiliation:
Cestode Zoonoses Research Group, Division of Biological Sciences, School of Environment and Life Sciences, University of Salford, The Crescent, Salford M5 4WT, UK
L. TIAOYING
Affiliation:
Institute of Parasitic Diseases, Sichuan Center for Disease Control and Prevention, Chengdu 610041, Sichuan, China
Q. WANG
Affiliation:
Institute of Parasitic Diseases, Sichuan Center for Disease Control and Prevention, Chengdu 610041, Sichuan, China
J. QIU
Affiliation:
Institute of Parasitic Diseases, Sichuan Center for Disease Control and Prevention, Chengdu 610041, Sichuan, China
P. S. CRAIG
Affiliation:
Cestode Zoonoses Research Group, Division of Biological Sciences, School of Environment and Life Sciences, University of Salford, The Crescent, Salford M5 4WT, UK
P. GIRAUDOUX
Affiliation:
Department of Chrono-environment, UMR UFC/CNRS 6249 aff. INRA, University of Franche-Comté, 25030 Besançon cedex, France
*
*Corresponding author: Department of Arctic and Marine Biology, University of Tromsø, Norway-9037. Tel: 0047 77 64 44 21. E-mail: amelie.vaniscotte@uit.no

Summary

On the Eastern Tibetan Plateau region (Sichuan province, China) dogs are regarded as important definitive hosts of Echinococcus multilocularis. We studied dog spatial behaviour in 4 Tibetan villages in order to determine the role of dogs in environmental contamination and their potential interactions with small mammal intermediate hosts. We identified definitive host species and Echinococcus spp. infection status of feces collected in the field by PCR methods and analysed the spatial distribution of canid feces. Nocturnal space utilization of GPS collared dogs in and around villages was also undertaken. E. multilocularis DNA was amplified in 23% of dog feces (n=142) and in 15% of fox feces (n=13) but this difference was not significant. However, dog feces were more frequently observed (78% of collected feces) than fox feces and are therefore assumed to largely contribute to human environment contamination. Feces were mainly distributed around houses of dog owners (0–200 m) where collared dogs spent the majority of their time. Inside villages, the contamination was aggregated in some micro-foci where groups of dogs defecated preferentially. Finally, small mammal densities increased from the dog core areas to grasslands at the periphery of villages occasionally used by dogs; male dogs moving significantly farther than females. This study constitutes a first attempt to quantify in a spatially explicit way the role of dogs in E. multilocularis peri-domestic cycles and to identify behavioural parameters required to model E. multilocularis transmission in this region.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Afonso, E., Lemoine, M., Poulle, M.-L., Ravat, M.-C., Romand, S., Thulliez, P., Villena, I., Aubert, D., Riche, B., Rabilloud, M. and Gilot-Fromont, E. (2008). Spatial distribution of soil contamination by Toxoplasma gondii in relation to cat defecation behaviour in an urban area. International Journal for Parasitology 38, 10171023.CrossRefGoogle Scholar
Anvik, J., Hague, A. and Rahaman, A. (1974). A method of estimating urban dog populations and its application to the assessment of canine fecal polution and endoparasitism in Saskatchewan. Canine Veterinary Journal 15, 219223.Google Scholar
Bailey, D. and Alimadhi, F. (2008). logit. mixed: Mixed effects logistic. In: Zelig: Everyones Statistical Software (ed. Kosuke, I., King, G. and Lau, O.). URL http://gking.harvard.edu/zeligGoogle Scholar
Boitani, L. and Ciucci, P. (1995). Comparative social ecology of feral dogs and wolves. Ethology Ecology and Evolution 7, 4972.CrossRefGoogle Scholar
Boitani, L., Francisci, F., Ciucci, P. and Andreoli, G. (1995). Population biology and ecology of feral dogs in Central Italy. In The Domestic Dog: its Ecology, Behaviour and Evolution (ed. Serpell, J. E.), pp. 217244. Cambridge University Press, Cambridge, UK.Google Scholar
Budke, C. M., Campos-Ponce, M., Qian, W. and Torgerson, P. R. (2005 a). A canine purgation study and risk factor analysis for echinococcosis in a high endemic region of the Tibetan Plateau. Veterinary Parasitology 127, 4349.CrossRefGoogle Scholar
Budke, C. M., Jiamin, Q., Craig, P. and Torgerson, P. (2005 b). Modeling the transmission of Echinococcus granulosus and Echinococcus multilocularis in dogs for a high endemic region of the Tibetan Plateau. International Journal for Parasitology 35, 163170.CrossRefGoogle ScholarPubMed
Burnham, K. and Anderson, D. (1998). Model Selection and Multimodel Inference, 2nd Edn.Springer-Verlag, New York, USA.CrossRefGoogle Scholar
Calenge, C. (2006). The package ‘adehabitat’ for the r software: A tool for the analysis of space and habitat use by animals. Ecological Modelling 197, 516519.CrossRefGoogle Scholar
Ciucci, P., Boitani, L., Francisci, F. and Andreoli, G. (1997). Home range, activity and movements of a wolf pack in central Italy. The Zoological Society of London 243, 803819.CrossRefGoogle Scholar
Clark, P. and Evans, F. (1954). Distance to nearest neighbour as a measure of spatial relationships in populations ecology. Ecology 35, 445453.CrossRefGoogle Scholar
Craig, P., Giraudoux, P., Shi, D., Bartholomot, B., Barnish, G., Delattre, P., Quéré, J., Harraga, S., Bao, G., Wang, Y., Lu, F., Ito, A. and Vuitton, D. (2000). An epidemiological and ecological study of human alveolar echinococcosis transmission in South Gansu, China. Acta Tropica 77, 167177.CrossRefGoogle ScholarPubMed
Craig, P. S., MacPherson, C. N. L., Watson-Jones, D. L. and Nelson, G. S. (1988). Immunodetection of Echinococcus eggs from naturally infected dogs and from environmental contamination sites in settlements in Turkana, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 268274.CrossRefGoogle ScholarPubMed
Craig, P. and The Echinococcosis Working Group in China (2006). Epidemiology of human alveolar echinococcosis in China. Parasitology International 55, 221225.CrossRefGoogle ScholarPubMed
Deplazes, P., Hegglin, D., Gloor, S. and Romig, T. (2004). Wilderness in the city: the urbanization of Echinococcus multilocularis. Trends in Parasitology 20, 7784.CrossRefGoogle ScholarPubMed
Dinkel, A., Kern, S., Brinker, A., Vaniscotte, A., Giraudoux, P., Mackenstedt, U. and Romig, T. (2011). A real-time multiplex nested PCR system for coporological diagnosis of Echinococcus multilocularis and host species. Parasitological Research. doi: 10.1007/s00436-011-2272-0. Online First.CrossRefGoogle ScholarPubMed
Dinkel, A., Romig, T. and Mackenstedt, U. (2006). PCR system for the combined detection of Echinococcus multilocularis and host species from faecal samples. Deutsche Gesellschaft für Parasitologie 22 Jahrestagung, Wien, 22.–25.02.2006, ISBN 3-200-00559-9:138.Google Scholar
Dinkel, A., Von Nickisch-Rosenegk, M., Bilger, B., Merli, M., Lucius, R. and Romig, T. (1998). Detection of Echinococcus multilocularis in the definitive host: coprodiagnosis by PCR as an alternative to necropsy. Journal of Clinical Microbiology 36, 18711876.CrossRefGoogle ScholarPubMed
Eckert, J. and Deplazes, P. (2004). Biological, Epidemiological, and Clinical Aspects of Echinococcosis, a Zoonosis of Increasing Concern. Clinical Microbiology Review 17, 107135.CrossRefGoogle ScholarPubMed
Giraudoux, P., Delattre, P., Takahashi, K., Raoul, F., Quéré, J., Craig, P. and Vuitton, D. (2002). Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multiscale approaches? In Cestode Zoonoses: Echinococcosis and Cysticercosis (ed. Craig, P. S. and Pawlowski, Z.), pp. 251266. IOS Press Amsterdam, The Netherlands.Google Scholar
Giraudoux, P., Pleydell, D., Raoul, F., Quéré, J., Wang, Q., Yang, Y., Vuitton, D., Qiu, J., Yang, W. and Craig, P. (2006). Transmission ecology of Echinococcus multilocularis: what are the ranges of parasite stability among various host communities in China? Parasitology International 55, 237246.CrossRefGoogle ScholarPubMed
Gong, M. H. and Hu, J. (2003). The summer microhabitat selection of Tibetan fox in the northwest plateau of Sichuan. Acta Theriologica Sinica 23, 267269.Google Scholar
Habluetzel, A., Traldi, G., Ruggieri, S., Attili, A., Scuppa, P., Marchetti, R., Menghini, G. and Esposito, F. (2003). An estimation of Toxocara canis prevalence in dogs, environmental egg contamination and risk of human infection in the Marche region of Italy. Veterinary Parasitology 113, 243252.CrossRefGoogle ScholarPubMed
Hegglin, D., Bontadina, F., Contesse, P., Gloor, S. and Deplazes, P. (2007). Plasticity of predation behaviour as a putative driving force for parasite life-cycle dynamics: the case of urban foxes and Echinococcus multilocularis tapeworm. Functional Ecology 21, 552560.CrossRefGoogle Scholar
Hodder, K., Kenward, R., Walls, S. and Clarke, R. (1998). Estimating core ranges: a comparison of techniques using the Common buzzard (Buteo buteo). Journal of Raptor Research 32, 8289.Google Scholar
Macpherson, C. (2005). Human behaviour and the epidemiology of parasitic zoonoses. International Journal for Parasitology 35, 13191331.CrossRefGoogle ScholarPubMed
Macpherson, C. and Craig, P. S. (2000). Dogs and cestode zoonoses. In Dogs, Zoonoses and Public Health (ed. Macpherson, C., Meslin, F. and Wandeler, A.), pp. 177211. CABI International, Wallingford, UK.CrossRefGoogle Scholar
Macpherson, C., Meslin, F. and Wandeler, A. (2000). Dogs, Zoonoses and Public Health. CABI International, Wallingford, UK.CrossRefGoogle Scholar
Marston, C. (2008). Spatial modelling of small mammal distributions in relation to parasite transmission in western china. Ph.D. thesis, School of Environment and Life Sciences University of Salford, Salford, UK.Google Scholar
Meek, P. (1999). The movement, roaming behaviour and home range of free-roaming domestic dogs, Canis lupus familiaris, in coastal New South Wales. Wildlife Research 26, 847855.CrossRefGoogle Scholar
Okubo, A. and Levin, S. (2001). Diffusion and ecological problems: modern perspectives. In Interdisciplinary Applied Mathematics 2nd Edn. (ed. Antman, S. S., Marsden, J. E., Sirovich, L. and Wiggins, S.), Springer Verlag, New York, USA.Google Scholar
O'Lorcain, P. (1994). Prevalence of Toxocara canis ova in public playgrounds in the Dublin area of Ireland. Journal of Helminthology 68, 237241.CrossRefGoogle ScholarPubMed
Qiu, J., Chen, X., Ren, M., Luo, C., Liu, D. and Liu, X. (1995). Epidemiological study on alveolar hydatid disease in qinghai-xizang (Tibetan) plateau. Journal of Practical Parasitic Diseases 3, 106109.Google Scholar
Qiu, J., Liu, F., Schantz, P., Ito, A., Carol, D. and He, J. (1999). Epidemiological survey of hydatidosis in Tibetan areas of Western Sichuan Province. Archivos Internacionales de la Hidatidosis, 23–84.Google Scholar
R Development Core Team (2008). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.orgGoogle Scholar
Raoul, F., Deplazes, P., Nonakac, N., Piarroux, R., Vuitton, D. and Giraudoux, P. (2001). Assessment of the epidemiological status of Echinococcus multilocularis in foxes in France using elisa coprotests on fox feces collected in the field. International Journal for Parasitology 31, 15791588.CrossRefGoogle ScholarPubMed
Raoul, F., Deplazes, P., Rieffel, D., Lambert, J. C. and Giraudoux, P. (2010). Predator's dietary response to prey density variation and consequences for a cestode transmission. Oecologia 164, 129139.CrossRefGoogle ScholarPubMed
Raoul, F., Quéré, J., Rieffel, D., Bernard, N., Takahashi, K., Scheifler, R., Ito, A., Wang, Q., Qiu, J., Yang, W., Craig, P. and Giraudoux, P. (2006). Distribution of small mammals in a pastoral landscape of the Tibetan Plateau (Western Sichuan, China) and relationship with grazing practices. Mammalia 70, 214225.CrossRefGoogle Scholar
Robardet, E., Giraudoux, P., Caillot, C., Boue, F., Cliquet, F., Augot, D. and Barrat, J. (2008). Infection of foxes by Echinococcus multilocularis in urban and suburban areas of Nancy, France: infuence of feeding habits and environment. Parasite 15, 7785.CrossRefGoogle Scholar
Schantz, P. M., Wang, H., Qiu, J., Liu, F. J., Saito, E., Emshoff, A., Ito, A., Roberts, J. M. and Delker, C. (2003). Echinococcosis on the Tibetan Plateau: prevalence and risk factors for cystic and alveolar echinococcosis in Tibetan populations in Qinghai Province, China. Parasitology 127, 109120.CrossRefGoogle ScholarPubMed
Seaman, D. E. and Powell, R. A. (1990). Identifying patterns and intensity of home range use. Bears: Their Biology and Management. A Selection of Papers from the Eighth International Conference on Bear Research and Management, Victoria, British Columbia, Canada 8, 243249.Google Scholar
Seaman, D. E. and Powell, R. A. (1996). An evaluation of the accuracy of kernel density estimators for home range analysis. Ecology 77, 20752085.CrossRefGoogle Scholar
Shaikenov, B. S., Rysmukhambetova, A. T., Massenov, B., Deplazes, P., Mathis, A. and Togerson, P. R. (2004). Short report: the use of a polymerase chain reaction to detect Echinococcus Granulosus (G1 Strain) eggs in soil samples. American Journal of Tropical Medicine and Hygiene 71, 441443.CrossRefGoogle ScholarPubMed
Thompson, R. A., Kutz, S. J. and Smith, A. (2009). Parasite zoonoses and wildlife: emerging issues. International Journal of Environmental Health Research 6, 678693.Google ScholarPubMed
Tiaoying, L., Qiu, J., Wen, Y., Craig, P. S., Xingwang, C., Xiao, N., Ito, A., Giraudoux, P., Wulamu, M., Wen, Y. and Schantz, P. (2005). Echinococcosis in Tibetan populations, Western Sichuan province, China. Emerging Infectious Diseases 11, 18661873.CrossRefGoogle ScholarPubMed
Veit, P., Bilger, B., Schad, V., Schäfer, J., Frank, W. and Lucius, R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 7986.CrossRefGoogle ScholarPubMed
Vuitton, D., Zhou, H., Bresson-hadni, S., Wang, Q., Piarroux, M., Raoul, F. and Giraudoux, P. (2003). Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127, 87107.CrossRefGoogle ScholarPubMed
Wang, Q., Raoul, F., Budke, C., Craig, P. S., Xiao, Y., Vuitton, D. A., Campos-Ponce, M., Qiu, D. C., Pleydell, D. and Giraudoux, P. (2010). Grass height and transmission ecology of Echinococcus multilocularis in tibetan communities, China. Chinese Medical Journal 123, 6167.Google ScholarPubMed
Wang, Q., Vuitton, D., Qiu, J., Giraudoux, P., Xiao, Y., Schantz, P., Raoul, F., Li, T., Wen, Y. and Craig, P. (2004). Fenced pasture: a possible risk factor for human alveolar echinococcosis in Tibetan pastoralist communities of Sichuan, China. Acta Tropica 90, 285293.CrossRefGoogle ScholarPubMed
Wang, Z., Wang, X. and Liu, X. (2007). Selection of land cover by the Tibetan fox Vulpes ferrilata on the eastern Tibetan Plateau, western Sichuan Province, China. Acta Theriologica 52, 215223.CrossRefGoogle Scholar
Watson Jones, D. L. and Macpherson, C. N. L. (1988). Hydatid disease in the Turkana district of Kenya V1. Man:dog contact and its role in the transmission and control of hydatidosis amongst the Turkana. Annals of Tropical Medicine and Parasitology 82, 343356.CrossRefGoogle Scholar
WHO and WSPA (1990). Guidelines for Dog Population Management. World Health Organisation, Geneva, Switzerland.Google Scholar
Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70, 164168.CrossRefGoogle Scholar
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. (2005). Echinococcus shiquicus n. sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693701.CrossRefGoogle Scholar