Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-26T18:51:04.889Z Has data issue: false hasContentIssue false

Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission

Published online by Cambridge University Press:  04 March 2004

P. GIRAUDOUX
Affiliation:
ISTE (EA 3184 MRT – UC INRA; EA 2276), Université de Franche-Comté 25030 Besançon Cedex, France
P. S. CRAIG
Affiliation:
Biosciences Research Institute & School of Environment & Life Sciences, University of Salford, M5 4WT, Salford, U.K.
P. DELATTRE
Affiliation:
UMR 1062, Centre de Biologie et Gestion Populations, CS0016 34988, Montferrier Cedex, France
G. BAO
Affiliation:
Department of Parasitology, Lanzhou Medical College, 85 Dun Gang Xi Road, 730000 Lanzhou, P.R. of China
B. BARTHOLOMOT
Affiliation:
ISTE (EA 3184 MRT – UC INRA; EA 2276), Université de Franche-Comté 25030 Besançon Cedex, France
S. HARRAGA
Affiliation:
ISTE (EA 3184 MRT – UC INRA; EA 2276), Université de Franche-Comté 25030 Besançon Cedex, France
J.-P. QUÉRÉ
Affiliation:
UMR 1062, Centre de Biologie et Gestion Populations, CS0016 34988, Montferrier Cedex, France
F. RAOUL
Affiliation:
ISTE (EA 3184 MRT – UC INRA; EA 2276), Université de Franche-Comté 25030 Besançon Cedex, France
Y. WANG
Affiliation:
Xinjiang Medical College, 1 Li Yu Shan Road, 830000 Urumqi, P.R. of China
D. SHI
Affiliation:
Department of Parasitology, Lanzhou Medical College, 85 Dun Gang Xi Road, 730000 Lanzhou, P.R. of China
D.-A. VUITTON
Affiliation:
ISTE (EA 3184 MRT – UC INRA; EA 2276), Université de Franche-Comté 25030 Besançon Cedex, France

Abstract

An area close to the Qinghai-Tibet plateau region and subject to intensive deforestation contains a large focus of human alveolar echinococcosis while sporadic human cases occur in the Doubs region of eastern France. The current review analyses and compares epidemiological and ecological results obtained in both regions. Analysis of rodent species assemblages within quantified rural landscapes in central China and eastern France shows a significant association between host species for the pathogenic helminth Echinococcus multilocularis, with prevalences of human alveolar echinococcosis and with land area under shrubland or grassland. This suggests that at the regional scale landscape can affect human disease distribution through interaction with small mammal communities and their population dynamics. Lidicker's ROMPA hypothesis helps to explain this association and provides a novel explanation of how landscape changes may result in increased risk of a rodent-borne zoonotic disease.

Type
Research Article
Copyright
© 2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AMMAN, R. & ECKERT, J. (1995). Clinical diagnosis and treatment of Echinococcosis in Humans. In Echinococcus and Hydatid Disease ( ed. R. C. A. Thomson & A. J. Lymbery), pp. 411463. Wallingford, Oxford, CAB International.
ANGELSTAM, M., LINDSTRÖM, E. & WIDEN, P. (1984). Role of predation in short term population fluctuations of some birds and mammals in Fennoscandia. Ecologia (Berlin) 62, 199208.CrossRefGoogle Scholar
ASHFORD, R. W. (1991). The human parasite fauna: towards an analysis and interpretation. Annals of Tropical Medicine and Parasitology 85, 189198.CrossRefGoogle Scholar
BARCLAY, C. M. & RUBINSTEIN, G. (1997). Hantavirus in Argentina. Nature 386, 320320.CrossRefGoogle Scholar
BRESSON-HADNI, S., LAPLANTE, J. J., LENYS, D., ROHMER, P., GOTTSTEIN, B., JACQUIER, P., MERCET, P., MEYER, J. P., MIGUET, J. P. & VUITTON, D. A. (1994). Seroepidemiological screening of Echinococcus multilocularis infection in a European area endemic for Alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 51, 837846.CrossRefGoogle Scholar
CHEN, J. C., YAO, Z. Y. & LIAO, C. H. (1982). Report on the damage caused by rodent pest in the grassland of South Gansu, China. Chinese Journal of Zoology 3, 25.Google Scholar
COMBES, C. (2001). Parasitism. The Ecology and Evolution of Intimate Interactions. Chicago and London, The University of Chicago Press.
COMBES, C., LEGER, N. & GOLVAN, Y. J. (1975). Le rôle du rat dans la dynamique de l'endéme schistosomienne en Guadeloupe. Compte-Rendus de l'Académie des Sciences, Paris, III 281, 10591061.Google Scholar
COURANT, F., BRUNET-LECOMTE, P., VOLOBOUEF, V., CHALINE, J., QUÉRÉ, J. P., NADACHOWSKI, A., MONTUIRE, S., BAO, G., VIRIOT, L., RAUSCH, R., ERBAJEVA, M., SHI, D. & GIRAUDOUX, P. (1999). Identification of Microtus limnophilus in a large focus of Alveolar Echinococcosis (south Gansu, China). Compte-Rendu de l'Académie des Sciences, Paris, III 322, 473480.Google Scholar
CRAIG, P. S., ALLAN, J. C. & ROGAN, M. T. (1996). Detection, screening and community epidemiology of taeniid cestode zoonosis: cystic echinococcosis, alveolar echinococcosis and cysticercosis. Advances in Parasitology 38, 169250.CrossRefGoogle Scholar
CRAIG, P. S., DESHAN, L., MACPHERSON, C. N. L., DAZHONG, S., REYNOLDS, D., BARNISH, G., GOTTSTEIN, B. & ZHIRONG, W. (1992). A large focus of alveolar echinococcosis in central China. The Lancet 340, 826831.CrossRefGoogle Scholar
CRAIG, P. S., GIRAUDOUX, P., SHI, D., BARTHOLOMOT, B., BARNISH, G., DELATTRE, P., QUÉRÉ, J. P., HARRAGA, S., BAO, G., WANG, Y. H., LU, F., ITO, A. & VUITTON, D. A. (2000). An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Tropica 77, 167177.CrossRefGoogle Scholar
DANSON, F. M., CRAIG, P. S., MAN, W., SHI, D. Z., PLEYDELL, D. & GIRAUDOUX, P. (2002). Satellite remote sensing and geographical information systems for risk modelling of alveolar echinococcosis. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem ( ed. P. S. Craig & Z. Pawlowski), pp. 267285. Amsterdam, IOS Press.
DELATTRE, P., DUPLANTIER, J. M., FICHET-CALVET, E. & GIRAUDOUX, P. (1998). Modifications de milieux et pullulations de rongeurs. Conséquences en agriculture et en santé publique. Cahiers Agricultures 7, 285298.Google Scholar
DELATTRE, P., GIRAUDOUX, P., BAUDRY, J., QUERE, J. P. & FICHET, E. (1996). Effect of landscape structure on Common Vole (Microtus arvalis) distribution and abundance at several space scales. Landscape Ecology 11, 279288.CrossRefGoogle Scholar
DELATTRE, P., GIRAUDOUX, P., BAUDRY, J., TRUCHETET, D., MUSARD, P., TOUSSAINT, M., STAHL, P., POULE, M. L., ARTOIS, M., DAMANGE, J. P. & QUERE, J. P. (1992). Land use patterns and types of common vole (Microtus arvalis) population kinetics. Agriculture, Ecosystems and Environment 39, 153169.CrossRefGoogle Scholar
DELATTRE, P., GIRAUDOUX, P. & QUERE, J. P. (1990). Conséquences épidémiologiques de la réceptivité d'un nouvel hôte intermédiaire du Ténia multiloculaire (Echinococcus multilocularis) et de la localisation spatio-temporelle des rongeurs infestés. Compte-Rendus de l'Académie des Sciences, Paris, III 310, 339344.Google Scholar
DELATTRE, P., PASCAL, M. & DAMANGE, J. P. (1985). Vers une stratégie d'étude épidémiologique de l'Echinococcose alvéolaire. A propos de cas d'infestation observés chez Microtus arvalis P. dans le Doubs (France). Annales de Parasitologie Humaine et Comparée 60, 389403.CrossRefGoogle Scholar
DELATTRE, P., PASCAL, M., LE PESTEUR, M. H., GIRAUDOUX, P. & DAMANGE, J. P. (1988). Caractéristiques écologiques et épidémiologiques de l'Echinococcus multilocularis au cours d'un cycle complet des populations d'un hôte intermédiaire (Microtus arvalis). Canadian Journal of Zoology 66, 27402750.CrossRefGoogle Scholar
EUZET, L. & COMBES, C. (1980). Les problèmes de l'espèce chez les animaux parasites. Mémoires de la Société Zoologique de France 40, 239285.Google Scholar
GIRAUDOUX, P. (1991). Utilisation de l'espace par les hôtes du ténia multiloculaire (Echinococcus multilocularis): conséquences épidémiologiques. Thèse de doctorat, Université de Bourgogne.
GIRAUDOUX, P., DELATTRE, P., HABERT, M., QUERE, J. P., DEBLAY, S., DEFAUT, R., DUHAMEL, R., MOISSENET, M. F., SALVI, D. & TRUCHETET, D. (1997). Population dynamics of fossorial water vole (Arvicola terrestris scherman): a land usage and landscape perpective. Agriculture Ecosystems and Environment 66, 4760.CrossRefGoogle Scholar
GIRAUDOUX, P., DELATTRE, P., QUERE, J. P. & DAMANGE, J. P. (1994). Distribution and kinetics of rodent populations in a region under agricultural land abandonment. Acta Oecologica 15, 385400.Google Scholar
GIRAUDOUX, P., DELATTRE, P., TAKAHASHI, K., RAOUL, F., QUÉRÉ, J. P., CRAIG, P. & VUITTON, D. (2002). Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multi-scale approaches? In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem ( ed. P. Craig & Z. Pawlowski), pp. 267285. Amsterdam, IOS Press.
GIRAUDOUX, P., QUERE, J. P., DELATTRE, P., BAO, G., WANG, X., SHI, D., VUITTON, D. & CRAIG, P. S. (1998). Distribution of small mammals along a deforestation gradient in south Gansu, China. Acta Theriologica 43, 349362.CrossRefGoogle Scholar
GIRAUDOUX, P., VUITTON, D., BRESSON-HADNI, S., CRAIG, P., BARTHOLOMOT, B., BARNISH, G., LAPLANTE, J. J., ZHONG, S. D., WANG, Y. H. & LENYS, D. (1996). Mass screening and epidemiology of Alveolar echinococcosis in France, Western Europe, and in Gansu, Central China: from epidemiology towards transmission ecology. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver ( ed. J. Ito & N. Sato), pp. 197211. Sapporo 060, Japan, Fuji Shoin.
GOLVAN, Y. J. & RIOUX, J. A. (1961). Ecologie des mérions du kurdistan iranien. Relation avec l'épidémiologie de la peste rurale. Annales de Parasitologie Humaine et Comparée 36, 449558.CrossRefGoogle Scholar
HANSSON, L. (1995). Development and application of landscape approaches in mammalian ecology. In Landscape approaches in Mammalian Ecology and Conservation ( ed. W. Z. J. Lidicker), pp. 2039. Minneapolis, University of Minnesota Press.
HANSSON, L. (2002). Rodent dynamics, population regulation and predation in changeable landscapes: importance for Echinococcus transmission. In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem ( ed. P. S. Craig & Z. Pawlowski), pp. 267285. Amsterdam, IOS Press.
HOLMES, J. C. (1986). The structure of helminth communities. International Journal for Parasitology 17, 203208.Google Scholar
HOUIN, R., DENIAU, M. & LIANCE, M. (1980). Arvicola terrestris (L.), premier rongeur trouvé naturellement infesté par Echinococcus multilocularis, Leuckart, 1863, en France. Compte-Rendus de l'Académie des Sciences, Paris, série D 290, 12691271.Google Scholar
HSIA, W. P. (1958). On the changing tendencies of the rodent population in the recent cut-over land at Dailing, Northeast China. Acta Zoologica Sinica 10, 431437.Google Scholar
HSIA, W. P. & CHU, S. K. (1963). A supplementary study on the changing tendencies of the rodent population in the recent cut-over land at Dailing, Northeastern China. Acta Zoologica Sinica 15, 538543.Google Scholar
KITTREDGE, D. B. J. (1996). Changes in global forest distribution. In Conservation of Faunal Diversity in Forested Landscape ( ed. R. M. Degraaf & R. I. Miller), pp. 3760. London, Chapman & Hall.CrossRef
LIDICKER, W. Z. (1985). Population structuring as a factor in understanding microtine cycles. Acta Zoologica Fennica 173, 2327.Google Scholar
LIDICKER, W. Z. (2000). A food web/landscape interaction model for Microtine density cycles. Oikos 91, 432445.CrossRefGoogle Scholar
LIDICKER, W. Z. Jr. (1988). Solving the enigma of microtine ‘cycles’. Journal of Mammalogy 69, 225235.CrossRefGoogle Scholar
LIDICKER, W. Z. Jr. ( ed. ) (1995). Landscape Approaches in Mammalian Ecology and Conservation. Minneapolis, University of Minnesota Press.
LUCIUS, R. & BILGER, B. (1995). Echinococcus multilocularis: increased awareness or spreading of a parasite? Parasitology Today 11, 430434.Google Scholar
LUNDKVIST, A., APEKINA, N., MYASNIKOV, Y., VAPALANTI, O., VAHERI, A. & PLYUSNIN, A. (1997). Dobrava hantavirus outbreak in Russia. The Lancet 350, 781782.CrossRefGoogle Scholar
MALYGIN, V. M., ORLOV, V. N. & YATSENKO, V. N. (1990). Species independence of Microtus limnophilus, its relations with M. oeconomus and distribution of these species Mongolia Zoologica Zhurnal 69, 115127.Google Scholar
MOLYNEUX, D. H. (1997). Patterns of change in vector borne diseases. Annals of Tropical Medicine and Parasitology 91, 827839.Google Scholar
OKSANEN, T. (1990). Exploitation ecosystems in heterogeneous habitat complexes. Evolutionary Ecology 4, 220234.CrossRefGoogle Scholar
OSTFELD, R. S. (1992). Small-mammal herbivores in a patchy environment: individual strategies and population responses. In Effects of Resource Distribution on Animal-Plant Interactions ( ed. M. D. Hunter, T. Ohgushi & P. W. Price), pp. 4374. London, Academic Press.CrossRef
PAWLOVSKI, E. N. (1964). Natural Foci of Transmissible Diseases in Connexion with the Landscape Epidemiology of Zooanthroponosis. Moskwa-Leningrad, Nowka.
PESSON, B. & CARBIENER, R. (1989). Ecologie de l'échinococcose alvéolaire en Alsace: le parasitisme du Renard roux (Vulpes vulpes L.). Bulletin d'Écologie 20, 295301.Google Scholar
PETAVY, A. F., DEBLOCK, S. & GILOT, B. (1984). Mise en évidence de la larve du Taenia multiloculaire chez 2 campagnols (Microtus arvalis et Clethrionomys glareolus) dans le foyer d'échinococcose alvéolaire du Massif Central (France). Compte-Rendus de l'Académie des Sciences, Paris, série III 299, 735737.Google Scholar
RAOUL, F. (2001). Ecologie de la transmission de l'échinococcose alvéolaire. Dépendance au paysage et à la relation proies-prédateurs. Thèse de doctorat, Université de Franche-Comté.
RAOUL, F., DEFAUT, R., MICHELAT, D., MONTADERT, M., PÉPIN, D., QUÉRÉ, J., TISSOT, B., DELATTRE, P. & GIRAUDOUX, P. (2001 a). Landscape effects on the population dynamics of small mammal communities and prey-resource variations: a preliminary analysis. Revue d'Écologie, Terre et Vie 56, 339352.Google Scholar
RAOUL, F., DEPIERRE, V., SCHEIFLER, R., MAAS, R., PETAVY, A. F., VUITTON, D. & GIRAUDOUX, F. (1999). Landscape effect on Echinococcus multilocularis winter prevalence in foxes in the Jura massif, France. Helminthologia 36, 48.Google Scholar
RAOUL, F., DEPLAZES, P., NONAKA, N., PIARROUX, R., VUITTON, D. A. & GIRAUDOUX, P. (2001 b). Assessment of the epidemiological status of Echinococcus multilocularis using fox faeces collected in the field and ELISA coprotests. International Journal for Parasitology 31, 15791588.Google Scholar
RAUSCH, R. L. (1995). Life-cycle patterns and geographic distribution of Echinococcus species. In Echinococcus and Hydatid Disease ( ed. R. C. A. Thomson & A. J. Lymbery), pp. 89134. Wallingford, Oxford, CAB International.
RIOUX, J. A., DEREURE, J. & PERIÈRES, J. (1990). Approche écologique du “risque épidémiologique”. L'exemple des leishmanioses. Bulletin d'Écologie 21, 19.Google Scholar
ROBERTS, M. G. & AUBERT, M. F. A. (1995). A model for the control of Echinococcus multilocularis in France. Veterinary Parasitology 56, 6774.CrossRefGoogle Scholar
ROMIG, T. (2002). Spread of Echinococcus multilocularis in Europe? In Cestode Zoonoses: Echinococcosis and Cysticercosis. An Emergent and Global Problem ( ed. P. Craig & Z. Pawlowski), pp. 6580. Amsterdam, IOS Press.
SAKAMOTO, T., ISHII, A. & KOBAYASHI, C. (1996). Long term observation on the change of growth and pathogenicity of Echinococcus multilocularis by serial passages in Mongolian gerbils. In Alveolar Echinococcosis: Strategy for Eradication of Alveolar Echinococcosis of the Liver ( ed. J. Ito & N. Sato), pp. 8993. Sapporo 060, Japan, Fuji Shoin.
SCHANTZ, P., CHAI, J., CRAIG, P. S., ECKERT, J., JENKINS, D. J., MACPHERSON, C. N. L. & THAKUR, A. (1995). Epidemiology and control of hydatid disease. In Echinocococcus and Hydatid Disease ( ed. R. C. A. Thompson & A. J. Lymbery), pp. 477. Wallingford, Oxford, CAB International.
TACKMANN, K., LÖSCHNER, U., MIX, H., STAUBACH, C., THULKE, H.-H. & CONRATH, F. J. (1998). Spatial distribution patterns of Echinococcus multilocularis (Leuckart 1863) (Cestoda: Cyclophyllidea: Taeniidae) among red foxes in an endemic focus in Brandenburg, Germany. Epidemiology and Infection 120, 101109.CrossRefGoogle Scholar
Thompson, R. C. A. & Lymbery, A. J. (eds) (1995). Echinococcus and Hydatid Disease. Wallingford, Oxford, CAB International.
TRAPE, J. F., GODELUCK, B., DIATTA, G., ROGIER, C., LEGROS, F., ALBERGEL, J. & AL, E. (1996). The spread of tick-borne borreliosis in West Africa and its relation to sub-saharian drought. American Journal of Tropical Medicine and Hygiene 54, 289293.CrossRefGoogle Scholar
VEIT, P., BILGER, B., SCHAD, V., SCHÄFER, F. W. & LUCIUS, R. (1995). Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110, 7986.CrossRefGoogle Scholar
VIEL, J. F., GIRAUDOUX, P., ABRIAL, V. & BRESSON-HADNI, S. (1999). Water vole (Arvicola terrestris scherman) density as risk factor for human alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene 61, 559565.CrossRefGoogle Scholar
WEBER, J. M. & AUBRY, S. (1993). Predation by foxes, Vulpes vulpes, on the fossorial form of the water vole, Arvicola terrestris scherman, in western Switzerland. Journal of Zoology, London 229, 553559.CrossRefGoogle Scholar
WEIGLER, B. J. (1995). Zoonotic hantaviruses: New concerns for the United States. Journal of the American Veterinary Medecine Association 206, 979986.Google Scholar
ZHOU, H. X. (2001). Eco-epidemiology of Echinococcus multilocularis in Xinjiang (Chine): a pilot study. Thèse de doctorat, Université de Franche-Comté.