Background Alveolar echinococcosis (AE) presents a serious public health challenge within China. Mass screening ultrasound surveys can detect pre-symptomatic AE, but targeting areas identified from hospital records is inefficient regarding AE. Prediction of undetected or emerging hotspots would increase detection rates. Voles and lemmings of the subfamily Arvicolinae are important intermediate hosts in sylvatic transmission systems. Their populations reach high densities in productive grasslands where food and cover are abundant. Habitat availability is thought to affect arvicoline population dynamic patterns and definitive host–intermediate host interactions. Arvicoline habitat correlates with AE prevalence in Western Europe and southern Gansu Province, China. Methods and Findings Xiji County, Ningxia Hui Autonomous Region, borders southern Gansu. The aims of this study were to map AE prevalence across Xiji and test arvicoline habitat as a predictor. Land cover was mapped using remotely sensed (Landsat) imagery. Infection status of 3,205 individuals screened in 2002–2003 was related, using generalised additive mixed models, to covariates: gender; farming; ethnicity; dog ownership; water source; and areal cover of mountain pasture and lowland pasture. A Markov random field modelled additional spatial variation and uncertainty. Mountain pasture and lowland pasture were associated with below and above average AE prevalence, respectively. Conclusions Low values of the normalised difference vegetation index indicated sub-optimality of lowland pasture for grassland arvicolines. Unlike other known endemic areas, grassland arvicolines probably did not provide the principal reservoir for Echinococcus multilocularis in Xiji. This result is consistent with recent small mammal surveys reporting low arvicoline densities and high densities of hamsters, pikas and jerboas, all suitable intermediate hosts for E. multilocularis, in reforested lowland pasture. The risk of re-emergence is discussed. We recommend extending monitoring to: southern Haiyuan County, where predicted prevalence was high; southern Xiji County, where prediction uncertainty was high; and monitoring small mammal community dynamics and the infection status of dogs.
References
[1]
Patz JA, Confalonieri UEC, Amerasinghe FP, Chua KB, Daszak P, et al. (2005) Ecosystem regulation of infectious diseases. In: Hassan R, Scholes R, Ash N, editors. Ecosystems and Human Well-Being: Curent State and Trends, Volume 1. Findings of the Condition and Trends Working Group of the Ecosystem Assessment. Washington, DC: Island Press, Millennium Ecosystem Assessment Series. pp. 391–415. http://www.millenniumassessment.org/docu？ments/document.283.aspx.pdf.
[2]
Corvalan C, Hales S, McMichael A, et al. (2005) Ecosystems and human well-being: Health synthesis. Technical report, World Health Organization, http://www.who.int/globalchange/ecosyste？ms/ecosystems05/en/index.html. ISBN 92 4 156309 5.
[3]
Pawlowski ZS, Eckert J, Vuitton DA, Ammann RW, Kern P, et al. (2001) Echinococcosis in humans: clinical aspects, diagnosis and treatment. In: Eckert J, Gemmell M, Meslin F, Pawlowski Z, editors. WHO/OIE Manual on echinococcosis in humans and animals. pp. 20–66.
[4]
Kern P, Bardonnet K, Renner E, Auer H, Pawlowski Z, et al. (2003) European echinococcosis registry: Human alveolar echinococcosis, Europe, 1982–2000. Emerg Infect Dis 9: 343–349. doi: 10.3201/eid0903.020341
[5]
Vuitton DA (2003) The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Trop 85: 119–132. doi: 10.1016/S0001-706X(02)00230-9
[6]
Duscher G, Pleydell D, Prosl H, Joachim A (2006) Echinococcus multilocularis in Austrian foxes from 1991 until 2004. J Vet Med B 53: 138–144. doi: 10.1111/j.1439-0450.2006.00930.x
[7]
Schantz P, Liu FJ, Qiu JM, Wang F, Ito A, et al. (1998) A survey of hydatid disease (echinococcosis) in Tibetan populations in China: preliminary results. In: International Symposium on Environmental Adaptation of Echinococcus. Hokkaido University, Sapporo, Japan. http://133.87.224.209/lecture/1998/sympo？1998.html.
[8]
Qiu JM, Zhang ZZ, Schantz PM (1999) Epidemiology of Echinococcus in a Tibetan community in western Sichuan. Proceedings of the workshop of Echinococcosis, Control Stratefy in China. Institute for Endemic disease research and control, Urumqi. (In Chinese).
[9]
Li T, Qiu J, Wen Y, Craig PS, Chen X, et al. (2005) Echinococcosis in Tibetan populations western Sichuan Province, China. Emerg Infect Dis 11: 1866–1873. doi: 10.3201/eid1112.050079
[10]
Craig PS, Giraudoux P, Shi D, Bartholomot B, Barnish G, et al. (2000) An epidemiological and ecological study of human alveolar echinococcosis transmission in south Gansu, China. Acta Trop 77: 167–177. doi: 10.1016/S0001-706X(00)00134-0
[11]
Yang YR, Sun T, Li Z, Zhang J, Teng J, et al. (2006) Community surveys and risk factor analysis of human alveolar and cystic echinococcosis in Ningxia Hui Autonomous Region, China. B World Health Organ 84: 714–21. Erratum in: B World Health Organ. 84:840. doi: 10.2471/blt.05.025718
[12]
Danson FM, Graham AJ, Pleydell D, Campos-Ponce M, Giraudoux P, et al. (2003) Multi-scale spatial analysis of human ae risk in China. Parasitology 127: S133–S141.
[13]
Giraudoux P, Pleydell D, Raoul F, Quéré JP, Wang Q, et al. (2006) Transmission ecology of Echinococcus multilocularis: what are the ranges of parasite stability among various host communities in China? Parasitol Int 55: S237–S246. doi: 10.1016/j.parint.2005.11.036
[14]
Budke CM, Qiu JM, Zinsstag J, Wang Q, Torgerson PR (2004) Use of disability adjusted life years in the estimation of the disease burden of echinococcosis for a high endemic region of the Tibetan Plateau. Am J Trop Med Hyg 71: 56–64.
[15]
Bartholomot B, Vuitton DA, Harraga S, Shi DZ, Giraudoux P, et al. (2002) Combined ultrasonographic and serological screening of hepatic alveolar echinococcosis in central China. Am J Trop Med Hyg 66: 23–29.
[16]
Ito A, Urbani C, Jiamin Q, Vuitton DA, Dongchuan Q, et al. (2003) Control of echinococcosis and cysticercosis: a public health challenge to international cooperation in China. Acta Trop 86: 3–17. doi: 10.1016/S0001-706X(02)00269-3
[17]
Rausch RL (1995) Life cycle patterns and geographic distribution of Echinococcus species. In: Thomson RC, Lymbery AJ, editors. Echinococcus and hydatid disease. Wallingford: Cab International. pp. 89–119.
[18]
Giraudoux P, Delattre P, Takahashi K, Raoul F, Quéré JP, et al. (2002) Transmission ecology of Echinococcus multilocularis in wildlife: what can be learned from comparative studies and multi-scale approaches? Cestode zoonoses: an emergent and global problem. Amsterdam: IOS press, NATO Sciences Series. pp. 251–262.
[19]
Giraudoux P, Craig PS, Delattre P, Bartholomot B, Bao G, et al. (2003) Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitology 127: S121–S131. doi: 10.1017/s0031182003003512
[20]
Viel JF, Giraudoux P, Arbial V, Bresson-Hadni S (1999) Water vole (Arvicola terrestris) density as risk factor for human alveolar echinococcosis. Am J Trop Med Hyg 61: 559–565. doi: 10.1097/00001648-199807001-00120
[21]
Giraudoux P, Raoul F, Bardonnet K, Vuillaume P, Tourneux F, et al. (2001) Alveolar echinococcosis: characteristics of a possible emergence and new perspectives in epidemiosurveillance. Med Maladies Infect 31: 247–256. doi: 10.1016/s0399-077x(01)80065-2
[22]
Pleydell DRJ, Raoul F, Tourneux FP, Danson FM, Graham A, et al. (2004) Modelling the spatial distribution of Echinococcus multilocularis infection in foxes. Acta Trop 91: 253–265. doi: 10.1016/j.actatropica.2004.05.004
[23]
Giraudoux P, Quéré JP, Delattre P, Bao GS, Wang XM, et al. (1998) Distribution of small mammals along a deforestation gradient in southern Gansu, central China. Acta Theriol 43: 349–362.
[24]
Chen JC, Yao ZY, Liao CH (1982) Report on the damage caused by rodent pests in the grassland of southern Gansu, China. Chinese Journal of Zoology 3:
[25]
Eckert J, Rausch RL, Gemmel MA, Giraudoux P, Kamiya M, et al. (2001) Epidemiology of Echinococcus multilocularis, Echinococcus vogeli and Echinococcus oligarthrus. In: Eckert J, Gemmell M, Meslin F, Pawlowski Z, editors. WHO/OIE Manual on Echinococcosis in humans and animals: a public health problem of global concern. Paris: OIE/WHO. pp. 164–182.
[26]
Osman I, Jiao W, Liao L, Chai J (1998) Comparative observation on experimental infection with Echinococcus multilocularis in Cricetulus Migratorius and Meriones meridianus. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 16: 130–2. (In Chinese).
[27]
Danson FM, Craig PS, Man W, Shi DZ, Giraudoux P (2004) Landscape dynamics and risk modelling of human alveolar echinococcosis. Photogramm Eng Rem S 70: 359–366.
[28]
Raoul F, Quéré JP, Rieffel D, Bernard N, Takahashi K, et al. (2006) Distribution of small mammals in a pastoral landscape of the Tibetan plateaus (western Sichuan, China) and relationship with grazing practices. Mammalia 70: 214–225. doi: 10.1515/mamm.2006.042
[29]
Wang Q, Vuitton DA, Xiao YF, Budke CM, Campos-Ponce M, et al. (2006) Pasture types and Echinococcus multilocularis, Tibetan communities. Emerg Infect Dis 12: 1008–10. doi: 10.3201/eid1206.041229
[30]
Lidicker WZ (1988) Solving the enigma of microtine “cycles”. J Mammal 69: 225–235. doi: 10.2307/1381374
[31]
Lidicker WZ (1995) The landscape concept: something old, something new. In: Lidicker WZ, editor. Landscape approaches to Mammalian Ecology and Conservation. University of Minnesota Press. pp. 3–19.
[32]
Hansson F (2002) Rodent dynamics, population regulation and predation in changeable landscapes: important factors for Echinococcus transmission. In: Craig PS, Pawlowski Z, editors. Cestode Zoonoses: Echinococcosis and Cysticercosis. London, NATO Science Series.
[33]
Ostfeld RS (1992) Small mammal herbivores in a patchy environment: Individual strategies and population responses. In: Hunter MD, Ohgushi T, Price PW, editors. Effects of Resource distribution on Animal-plant interactions. London: Academic Press. pp. 43–74.
[34]
Delattre P, Giraudoux P, Baudry J, Musard P, Toussaint M, et al. (1992) Land use patterns and types of common vole (Microtus arvalis) population kinetics. Agric Ecosyst Environ 39: 153–169. doi: 10.1016/0167-8809(92)90051-c
[35]
Giraudoux P, Delattre P, Habert M, Quéré JP, Deblay S, et al. (1997) Population dynamics of fossorial water vole (Arvicola terrestris scheman) at regional-scale: a land usage and landscape perspective. Agric Ecosyst Environ 66: 47–60. doi: 10.1016/s0167-8809(97)80706-2
[36]
Liu JY, Tian HQ, Liu ML, Zhuang DF, Melillo JM, et al. (2005) China's changing landscape during the 1990s: Large-scale land transformations estimated with satellite data. Geophys Res Lett 32: doi: 10.1029/2004gl021649
[37]
Wang T, Wu W, Xue X, Sun Q, Zhang W, et al. (2004) Spatial-temporal changes of sandy desertified land during last 5 decades in north China. Acta Geogr Sin 59: 203–212.
[38]
Huang MB, Zhang L, Gallichand J (2003) Runoff responses to afforestation in a watershed of the Loess Plateau, China. Hydrol Process 17: 2599–2609. doi: 10.1002/hyp.1281
[39]
Li WH (2004) Degradation and restoration of forest ecosystems in China. Forest Ecol Manage 201: 33–41. doi: 10.1016/j.foreco.2004.06.010
[40]
Lin YG, Hong LX (1991) The biology and the geographical distribution of Echinococcus multilocularis infection in China. Endemic Disease Bulletin 6: 117–127. (In Chinese).
[41]
Wang HL, Yi YC, Ma Z, Zhang XP, Cheng RP, et al. (1991) A report of mass screening on alveolar and cystic echinococcus in Xiji County, Ningxia, China. Chinese Chi Sheng Chung Hsueh Yu Chi Sheng Chung Ping Tsa Chih 9: 143–145. (In Chinese).
[42]
Craig P (2006) Epidemiology of human alveolar echinococcosis in China. Parasitol Int 55: S221–S225. doi: 10.1016/j.parint.2005.11.034
[43]
Ningxia Meteorological Institute, Yinchuan, China.
[44]
Gemmell MA, Roberts MG, Beard TC, Lawson JR (2001) Epidemiology. In: Eckert J, Gemmell M, Meslin F, Pawlowski Z, editors. Manual on Echinococcosis in humans and animals: a public health problem of global concern. Paris: OIE/WHO. pp. 100–142.
[45]
Epi info. http://www.cdc.gov/epiinfo/about.htm.
[46]
GRASS Development Team (2008) Geographic Resources Analysis Support System (GRASS GIS) Software. Open Source Geospatial Foundation, USA. URL http://grass.osgeo.org.
[47]
R Development Core Team (2007) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org. ISBN 3-900051-07-0.
[48]
Atkinson PM, Lewis P (2000) Geostatistical classification for remote sensing: an introduction. Comput Geosci 26: 361–371. doi: 10.1016/s0098-3004(99)00117-x
[49]
Erdas 8.4. http://gi.leica-geosystems.com.
[50]
Wood SN (2006) Generalized Additive Models: An Introduction with R. Texts in Statistical Science. Boca Raton: Chapman and Hall/CRC.
[51]
Brezger A, Kneib T, Lang SBayesx - software for bayesian inference in structured additive regression models. http://www.stat.uni-muenchen.de/bayesx/b？ayesx.html.
[52]
Besag J, York J, Mollie A (1991) Bayesian image restoration with two applications in spatial statistics (with discussion). Ann I Stat Math 43: 1–59. doi: 10.1007/bf00116466
[53]
Rue H (2001) Fast sampling of gaussian markov random fields with applications. J R Stat Soc Series B (Methodological) 63: 325–338. doi: 10.1111/1467-9868.00288
[54]
Lang S, Brezger A (2004) Bayesian p-splines. J Comput Graph Stat 13: 183–212. doi: 10.1198/1061860043010
[55]
Spiegelhalter DJ, Best NG, Carlin BP, van der Linde A (2002) Bayesian measures of model complexity and fit. J R Stat Soc Series B (Methodological) 65: 583–639. doi: 10.1111/1467-9868.00353
[56]
Venables WN, Ripley BD (2002) Modern applied statistics with S. 4th Ed. New York: Springer.
[57]
Diggle PJ, Ribeiro PJ, Christensen O (2001) Model-based geostatistics: Lecture notes from TMR and MaPhySto summer school on spatial statistics and computational methods. http://www.math.auc.dk/merete/SS-and-CM2？001/pdproc.pdf.
[58]
Cressie N (1991) Statistics for Spatial data. New York: Wiley.
[59]
Vuitton DA, Zhou H, Bresson-Hadni S, Wang Q, Piarroux M, et al. (2003) Epidemiology of alveolar echinococcosis with particular reference to China and Europe. Parasitology 127: S87–S107. doi: 10.1017/s0031182003004153
[60]
Yang YR, Vuitton DA, Jones MK, Craig PS, McManus DP (2005) Brain metastasis of alveolar echinococcosis in a hyperendemic focus of Echinococcus multilocularis infection. T Roy Soc Trop Med H 99: 937–941. doi: 10.1016/j.trstmh.2005.04.020
[61]
Vuitton DA, Zhang SL, Yang YR, Godot V, Beurtona I, et al. (2006) Survival strategy of Echinococcus multilocularis in the human host. Parasitol Int 55: S51–S55. doi: 10.1016/j.parint.2005.11.007
[62]
Yang YR, Ellis M, Sun T, Li ZZ, Liu XZ, et al. (2006) Unique family clustering of human echinococcosis cases in a chinese community. Am J Trop Med Hyg 74: 487–494.
[63]
Raoul F, Pleydell D, Quéré JP, Vaniscotte A, Rieffel D, et al. Small mammal assemblage response to deforestation and afforestation in central China. Mammalia 72: In press. doi: 10.1515/mamm.2008.045
[64]
Ooi HK, Inaba C, Kamiya M (1992) Experimental evaluation of mink and Apodemus speciosus in the Echinococcus multilocularis life-cycle in Hokkaido, Japan. J Wildlife Dis 28: 472–473.
[65]
Zhou HX, Wen H, Wang YH, Delattre P, Quéré P, et al. (1998) Experimental susceptibility of Spermophilus erythrogenys to Echinococcus multilocularis. Ann Trop Med Parasit 92: 335–337. doi: 10.1080/00034989859915
[66]
Sakamoto T, Ishii A, Kobayashi C (1996) Long term observation on the change of growth and pathology of Echinococcus multilocularis by serial passages in mongolian gerbils. In: Ito , Sato , editors. Alveolar Echinococcosis: strategy for eradication of alveolar echinococcosis of the liver. Sapporo, Japan: Fuji Shoin Sapporo. pp. 89–93.
[67]
Kepron C, Schoen J, Novak M, Blackburn BJ (1999) Nmr study of lipid changes in organs of jirds infected with Echinococcus multilocularis. Comp Biochem Phys B 124: 347–353. doi: 10.1016/s0305-0491(99)00126-1
[68]
Yongzu Z (1997) Distribution of mammalian species in China. Beijing: China Forestry Publ. House. ISBN 7-5038-1599-X.
[69]
He L, García-Perea R, Wei FW, Gisbert J, Li M (2004) Distribution and conservation of the Chinese Mountain Cat (Felis bieti). Oryx 38: 55–61. doi: 10.1017/s0030605304000092
[70]
Yang YR, Craig PS, Vuitton DA, Williams GM, Sun T, et al. Serological prevalence of echinococcosis and risk factors for infection amongst children in rural communities of southern Ningxia, China. Tropical Medicine and International Health. In press. doi: 10.1111/j.1365-3156.2008.02101.x
