Ecological epidemiology: the role of landscape structure in the transmission risk of the fox tapeworm Echinococcus multilocularis (Leukart 1863) (Cestoda: Cyclophyllidea: Taeniidae)
Restricted accessResearch articleFirst published online March, 2005
Ecological epidemiology: the role of landscape structure in the transmission risk of the fox tapeworm Echinococcus multilocularis (Leukart 1863) (Cestoda: Cyclophyllidea: Taeniidae)
The larval form of the fox tapeworm Echinococcus multilocularis causes a fatal liver infection in humans and has high prevalence in western China. The tapeworm lifecycle involves small mammal populations and canids, such as foxes and dogs. Human contact with infected canids may lead to the transmission of the worm to humans, causing the disease human alveolar echinococcosis. This paper introduces the tapeworm and reviews the current understanding of its transmission ecology in relation to each component of its lifecycle. Recent research indicates that landscape plays an important role in creating the necessary habitat conditions for natural transmission. Defining the landscape involves the use of satellite imagery, land cover classification and spatial analysis. The link between disease, remote sensing and landscape ecology is an expanding research area and potentially an important one in relation to Echinococcus multilocularis and alveolar echinococcosis.
Aspinall, R. and Veitch, N.1993: Habitat mapping from satellite imagery and wildlife data using a Bayesian modelling procedure in a GIS. Photogram-metric Engineering and Remote Sensing4, 537-543.
2.
Atkinson, P. J. and Unwin, D. J.2002: Density and local attribute estimation of an infectious disease using MapInfo. Computers & Geosciences28, 1095-1105.
3.
Bastin, G. N., Ludwig, J. A., Eager, R. W., Chewings, V. H. and Leidloff, A. C.2002: Indicators of landscape function: comparing patchiness metrics using remotely sensed data from rangelands. Ecological Indicators1, 247-260.
4.
Beck, L. R., Lobitz, B. M. and Wood, B. L.2000: Remote sensing and human health: new sensors and new opportunities. Emerging Infectious Diseases6, 217-226.
5.
Beeby, A.1993: Applying ecology. London: Chapman and Hall.
6.
Bergquist, N. R.2001: Vector-borne parasitic diseases: new trends in data collection and risk assessment. Acta Tropica79, 13-20.
7.
Berke, O.2001: Chloropleth mapping of regional count data of Echinococcus multilocularis among red foxes in Lower Saxony, Germany. Preventative Veterinary Medicine52, 119-131.
8.
Blackwell, G. L., Potter, M. A. and Minot, E. O.2001: Rodent and predator population dynamics in an eruptive system. Ecological Modelling25, 227-245.
9.
Bresson-Hadni, S., Vuitton, D. A., Bartholomot, B., Heyd, B., Godart, D., Meyer, J. P., Hrusovsky, S., Becker, M. C., Mantion, G., Lenys, D. and Miguet, J. P.2000: A twenty-year history of alveolar echinococcosis: analysis of a series of 117 patients from eastern France. European Journal of Gastroenterology and Hepatology12, 327-336.
10.
Brooker, S.2002: Schistosomes, snails and satellites. Acta Tropica82, 207-214.
11.
Carbajo, A. E., Scheigmann, N., Curto, S. I., de Garin, A. and Bejaran, R.2001: Dengue transmission risk maps of Argentina. Tropical Medicine and International Health6, 170-183.
12.
Cardillo, M., MacDonald, D. W. and Rushton, S. P.1999: Predicting mammal species richness and distributions: testing the effectiveness of satellite derived land cover data. Landscape Ecology14, 423-435.
13.
Chaput, E. K., Meek, J. I. and Heimer, R.2002: Spatial analysis of human granulocytic ehrlichiosis near Lyme, Connecticut. Emerging Infectious Diseases8, 943-948.
14.
Coops, N. C. and Catling, P. C.2002: Prediction of the spatial distribution and relative abundance of ground-dwelling mammals using remote sensing imagery and simulation models. Landscape Ecology17, 173-188.
15.
Craig, P. S., Deshan, L., Macpherson, C. N. L., Dazhong, S., Reynolds, D., Barnish, G., Gottstein, B. and Zhirong, W.1992: A large focus of alveolar echinococcosis in central China. The Lancet340, 826-831.
16.
Craig, P. S., Rogan, M. T. and Allan, J. C.1996: Detection, screening and community epidemiology of Taeniid cestode zoonoses: cystic echinococcosis, alveolar echinococcosis and neurocysticercosis. Advances in Parasitology38, 169-250.
17.
Craig, P. S., Giraudoux, P., Shi, D., Bartholomot, B., Barnish, G., Delattre, P., Quere, J. P., Harraga, S., Bao, G., Wang, Y., Lu, F. and Vuitton, D. A.2000: An epidemiological and ecological study of human alveolar echinococcosis transmission in South Gansu, China. Acta Tropica77, 167-177.
18.
Crellin, J. R., Marchiondo, A. A. and Andersen, F. L.1981: Comparison of suitability of dogs and cats as hosts of Echinococcus multilocularis. American Journal of Veterinary Research42, 1980-1981.
19.
Danson, F. M., Craig, P. S., Man, W., Shi, D., Pleydell, D. R. J. and Giraudoux, P.2002: Satellite remote sensing and geographical information systems for risk modelling of alveolar echinococcosis. In Craig, P. S. and Pawlowski, Z., editors, Cestode zoonoses: echinococcosis and cysticercosis. Amsterdam: IOS Press.
20.
Danson, F. M., Craig, P. S., Man, W., Shi, D. and Giraudoux, P.2004: Landscape dynamics and risk modelling of human alveolar echinococcosis. Photogrammetric Engineering and Remote Sensing70, 359-366.
21.
Delattre, P., De Sousa, B., Fichet-Calvet, E., Quere, J. P. and Giraudoux, P.1999: Vole outbreaks in a landscape context: evidence from a six year study of Microtus arvalis. Landscape Ecology14, 401-412.
22.
Deplazes, P. and Eckert, J.2001: Veterinary aspects of alveolar echinococcosis - a zoonosis of public health significance. Veterinary Parasitology98, 65-87.
23.
Deplazes, P., Alther, P., Tanner, I., Thompson, R. C. A. and Eckert, J.1999: Echinococcus multilocularis coproantigen detection by enzyme-linked immunosorbent assay in fox, dogs and cat populations. Journal of Parasitology85, 115-121.
24.
Deplazes, P., Gloor, S., Steiger, C. and Hegglin, D.2002: Urban transmission of Echinococcus multi-locularis. In Craig, P. S. and Pawlowski, Z., editors, Cestode zoonoses: echinococcosis and cysticercosis. Amsterdam: IOS Press.
25.
Eckert, J. and Deplazes, P.1999: Alveolar echinococcosis in humans: the current situation in central Europe and the need for countermeasures. Parasitology Today15, 315-319.
26.
Eckert, J., Conraths, F. J. and Tackmann, K.2000: Echinococcosis: an emerging or re-emerging zoonosis?International Journal for Parasitology30, 1283-1294.
27.
Eckert, J., Raush, R. L., Gemmell, M. A., Giraudoux, P., Kamiya, M., Liu, F. J., Schantz, P. M. and Romig, T.2001: Epidemiology of Echinococcus multilocularis, Echinococcus vogeli and Echinococcus oligarthrus. In Eckert, J., Gemmell, M. A., Meslin, F. X. and Pawlowski, Z. S., editors, WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. Paris: World Organisation for Animal Health.
28.
Elliott, P., Wakefield, J., Best, N. and Briggs, D., editors, 2000: Spatial epidemiology - methods and applications. Oxford: Oxford University Press.
29.
Fichet-Calvet, E., Pradier, B., Quere, J. P., Giraudoux, P. and Delattre, P.2000: Landscape composition and vole outbreaks: evidence from an eight year study of Arvicola terrestris. Ecography23, 659-668.
30.
Fuentes, M. V., Malone, J. B. and Mas-Coma, S.2001: Validation of a mapping and prediction model for human fasciolosis transmission in Andean very high altitude endemic areas using remote sensing data. Acta Tropica79, 87-95.
31.
Furuya, K., Nishizuka, M., Honma, H., Kumagai, M., Sato, N., Takahashi, M. and Uchino, J.1990: Prevalence of human alveolar echinococcosis in Hokkaido as evaluated by western blotting. Japanese Journal of Medical Sciences and Biology43, 43-49.
32.
Ghosha, M., Natarajan, K., Waller, L. A. and Kim. D.1999: Hierarchical Bayes GLMs for the analysis of spatial data: an application to disease mapping. Journal of Statistical Planning and Inference75, 305-318.
33.
Giraudoux, P., Delattre, P., Habert, M., Quéré, J. P., Deblay, S., Defaut, R., Duhamel, R., Moissenet, M. F., Salvi, D. and Truchetet, D.1997: Population dynamics of fossorial water vole (Arvicola terrestris scherman): a land use and landscape perspective. Agriculture, Ecosystems & Environment66, 47-60.
34.
Giraudoux, P., Delattre, P. and Raoul, F.2000: Ecological basis of molecular surveillance for microbes and parasites spread by rodents. Bulletin de la Societe de Pathologie Exotique93, 176-176.
35.
Giraudoux, P., Delattre, P., Takahashi, K., Raoul, F., Quere, J. P., Craig, P. S. and Vuitton, D. A.2002: Transmission ecology of Echinococcus multiloccularis in wildlife: what can be learned from comparative studies and multi-scale approaches? In Craig, P. S. and Pawlowski, Z., editors, Cestode zoonoses: echinococcosis and cysticercosis. Amsterdam: IOS Press.
36.
Gortâzar, C., Villafuerte, R., Lucientes, J. and Fernândez-de-Luco, D.1998: Habitat related differences in helminth parasites of red foxes in the Ebro valley. Veterinary Parasitology80, 75-81.
37.
Gottstein, B., Saucy, F., Deplazes, P., Reichen, J., Demierre, G., Zurcher, Ch., Busato, A. and Pugin, P.2001: Is a high prevalence of Echinococcus multilocularis in wild and domestic animals associated with increased disease incidence in humans?Emerging Infectious Diseases7, 408-412.
38.
Griffith, J. A., Martinko, E. A. and Price, K. P.2000: Landscape structure analysis of Kansas at three scales. Landscape and Urban Planning52, 45-61.
39.
Hay, S. I., Randolph, S. E. and Rogers, D. J., editors 2000: Remote sensing and geographical information systems in epidemiology. Advances in Parasitology 47. London: Academic Press.
40.
Hubacek, K. and Sun, L.2001: A scenario analysis of China’s land use and land cover change: incorporating biophysical information into input-output modelling. Structural Change and Economic Dynamics12, 367-397.
41.
Ihama, Y., Sato, H., Makino, Y. and Kamiya, H.2000: Two Taenia species found in Japan, with new distribution record of Taenia polyacantha Leuckart, 1856 (Cestoda: Taeniidae). Parasitology International48, 303-306.
42.
Kitron, U., Otieno, L. H., Hungerford, L. L., Oduloja, A., Brifham, W. U., Okello, O. O., Joselyn, M., Mohamed Ahmed, M. M. and Cook, E.1996: Spatial analysis of the distribution of tsetse flies in the Lambwe Valley, Kenya, using Land-sat TM satellite imagery and GIS. Journal of Animal Ecology65, 371-380.
43.
Koch, T. and Denike, K.2001: GIS approaches to the problem of disease clusters: a brief commentary. Social Science and Medicine52, 1751-1754.
44.
Lidicker, W. Z.1991: In defence of a multifactor perspective in population ecology. Journal of Mammalogy72, 631-635.
45.
Lidicker, W. Z.2000: A food web/landscape interaction model for microtine rodent density cycles. Oikos91, 435-445.
46.
Losson, B., Mignon, B., Brochier, B., Baudien, B. and Pastoret, P. P.1997: Echinococcus multilocularis infection in the red fox (Vulpes vulpes) in the province of Luxembourg (Belgium): results of a survey conducted between 1993 and 1995. Annales de Médecine Vétérinaire141, 149-155.
47.
Lounibos, L. P.2002: Invasions by insect vectors of disease. Annual Review of Entomology47, 233-266.
48.
Lucius, R. and Bilger, B.1995: Echinococcus multilocularis in Germany: increased awareness or spreading of a parasite?Parasitology Today11, 430-433.
49.
MacCracken, J. G., Uresk, D. W. and Hansen, R. M.1985: Rodent-vegetation relationships in southeastern Montana. Northwest Science57, 272-278.
50.
Marshall, S. and Cooke, S.1997: Tibet outside the Tibetan Autonomous Region. CD-ROM. Washington DC: The Alliance for Research in Tibet.
51.
McCarthy, J. and Moore, T. A.2000: Emerging helminth zoonoses. International Journal for Parasitology30, 1351-1359.
52.
Muller, R.2002: Worms and human disease, second edition. Wallingford: CABI International.
53.
National Research Council1992: Grasslands and grassland sciences in Northern China. Washington DC: National Academy Press.
54.
Palang, H., Mander, Ü. and Naveh, Z.2000: Holistic landscape ecology in action. Landscape and Urban Planning50, 1-6.
55.
Parmenter, C. A., Yates, T. L., Parmenter, R. R. and Dunnum, J. L.1999: Statistical sensitivity for detection of spatial and temporal patterns in rodent population densities. Emerging Infectious Diseases5, 118-125.
56.
Pawlowski, Z. S., Eckert, J., Vuitton, D. A., Ammann, R. W., Kern, P., Craig, P. S., Dar, K. F., De Rosa, F., Filice, C., Gottstein, B., Grimm, F., Macpherson, C. N. L., Sata, N., Todorov, T., Uchino, J., von Sinner, W. and Wen, H.2001: Echinococcosis in humans; clinical aspects, diagnosis and treatment. In Eckert, J., Gemmell, M. A., Meslin, F. X. and Pawlowski, Z., editors, WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. Paris: World Organisation for Animal Health.
57.
Petavy, A. F., Tenora, F., Deblock, S. and Sergent, V.2000: Echinococcus multilocularis in domestic cats in France: a potential risk factor for alveolar hydatid disease contamination in humans. Veterinary Parasitology87, 151-156.
58.
Randolph, S. E.2000: Ticks and tick-borne disease systems in space and from space. Advances in Parasitology47, 217-243.
59.
Raoul, F., Deplazes, P., Nonaka, N., Piarroux, R., Vuitton, D. A. and Giraudoux, P.2001: Assessment of the epidemiological status of Echinococcus multilocularis in foxes in France using ELISA coprotests on fox faeces collected in the field. International Journal for Parasitology31, 1579-1588.
60.
Rausch, R. L., Wilson, J. F., Schantz, P. M. and McMahon, B. J.1987: Spontaneous death of Echinococcus multilocularis: cases diagnosed serologically (by Em2 ELISA) and clinical significance. American Journal of Tropical Medicine and Hygiene36, 576-585.
61.
Ricotta, C.2000: From theoretical ecology to statistical physics and back: self-similar landscape metrics as a synthesis of ecological diversity and geometrical complexity. Ecological Modelling125, 245-253.
62.
Rogers, D. J.2000: Satellites, space, time and the African trypanosomiases. Advances in Parasitology47, 129-171.
63.
Romig, T., Kratzer, W., Kimmig, P., Frosch, M., Gaus, W., Flegel, W. A., Gottstein, B., Lucius, R., Beckh, K. and Kern, P.1999: An epidemiologic survey of human alveolar echinococcosis in southwestern Germany. Römerstein Study Group. American Journal of Tropical Medicine and Hygiene61, 566-573.
64.
Staubach, C., Thulke, H-H., Tackmann, K., Hugh-Jones, M. and Conraths, F. J.2001: Geographic information system aided analysis of factors associated with the spatial distribution of Echinococcus multilocularis infections of foxes. American Journal of Tropical Medicine and Hygiene65, 943-948.
65.
Stieger, C., Hegglin, D., Schwarzenbach, G., Mathis, A. and Deplazes, P.2002: Spatial and temporal aspects of urban transmission of Echinococcus multilocularis. Parasitology124, 631-640.
66.
Storandt, S. T., Virchow, D. R., Dryden, M. W., Hygnstrom, S. E. and Kazacos, K. R.2002: Distribution and prevalence of Echinococcus multilocularis in wild predators in Nebraska, Kansas, and Wyoming. Journal of Parasitology88, 420-422.
67.
Thompson, R. C. A.2001: The future impact of societal and cultural factors on parasitic disease -some emerging issues. International Journal for Parasitology31, 949-959.
68.
Thompson, R. C. A. and McManus, D. P.2001: Aetiology: parasites and life-cycles. In Eckert, J., Gemmell, M. A., Meslin, F-X. and Pawlowski, Z., editors, WHO/OIE manual on echinococcosis in humans and animals: a public health problem of global concern. Paris: World Organisation for Animal Health.
69.
Thomson, M. C. and Connor, S. J.2000: Environmental information systems for the control of arthropod vectors of disease. Medical and Veterinary Entomology14, 227-244.
70.
Thomson, M. C., Obsomer, V., Dunne, M., Connor, S. J. and Molyneux, D. H.2000: Satellite mapping of Loa loa prevalence in relation to invermectin use in west and central Africa. The Lancet356, 1077-1078.
71.
Thulke, H-H., Grimm, V., Muller, M. S., Staubach, C., Tischendorf, L., Wissel, C. and Jeltsch, F.1999: From pattern to practice: a scaling-down strategy for spatially explicit modelling illustrated by the spread and control of rabies. Ecological Modelling117, 179-202.
72.
Torgerson, P. R. and Budke, C. M.2003: Echinococcosis - an international public health challenge. Research in Veterinary Science74, 191-202.
73.
Torgerson, P. R., Williams, D. H. and Abo-Shehada, M. N.1998: Modelling the prevalence of Echinococcus and Taenia species in small ruminants of different ages in northern Jordan. Veterinary Parasitology79, 35-51.
74.
Tunaci, M., Tunaci, A., Engin, G., Ozkorkmaz, B., Ahishali, B. and Rozanes, I.1999: MRI of cerebral alveolar echinococcosis. Neuroradiology41, 844-846.
75.
Van der Giessen, J. B. W., Rombout, Y. B., Franchimont, J. H., Limper, L. P. and Homan, W. L.1999: Detection of Echinococcus multilocularis in foxes in The Netherlands. Veterinary Parasitology82, 49-57.
76.
Verburg, P. H. and van Keulen, H.1999: Exploring changes in the spatial distribution of livestock in China. Agricultural Systems62, 51-67.
77.
Verburg, P. H., Veldkamp, A. and Fresco, L. O.1999: Simulation of changes in the spatial pattern of land use in China. Applied Geography19, 211-233.
78.
Viel, J-F., Giraudoux, P., Abrial, V. and Bresson-Hadni, S.1999: Water vole (Arvicola terrestris scherman) density as risk factor for human alveolar echinococcosis. American Journal of Tropical Medicine and Hygiene61, 559-565.
79.
Wang, Q., Qiu, J., Schantz, P., He, J., Ito, A. and Liu, F.2001: Investigation of risk factors for development of human hydatidosis among households raising livestock in Tibetan areas of western Sichuan province. Chinese Journal of Parasitology and Parasito-logical Diseases19, 93-96.
80.
Wen, H. and Yang, W.1997: Public health importance of cystic echinococcosis in China. Acta Tropica67, 133-145.
81.
Wilson, D., Curran, P. J. and Steele, C. M. 2001: Remote sensing, land cover and Lyme disease in the New Forest, UK. In Geomatics, Earth observation and the information society - proceedings of the first annual conference of the Remote Sensing and Photogrammetry Society. 12-14 September, London, UK.
82.
Wood, B. L., Beck, L. R., Washino, R. K., Hibbard, K. A. and Salute, J. S.1992: Estimating high mosquito producing rice fields using spectral and spatial data. International Journal of Remote Sensing13, 2813-2826.
83.
Young, S. S. and Wang, C. Y.2001: Land-cover change analysis of China using global scale Pathfinder AVHRR Landcover (PAL) data. 1982-92, International Journal of Remote Sensing22, 1457-1479.
84.
Zhou, H. 2001: Epidemiology and transmission ecology of Echinococcus multilocularis in Xinjiang, the Peoples Republic of China: a preliminary study. PhD Thesis, Universite de Franche-Compte, Besancon, France.
