Transmission ecosystems of Echinococcus multilocularis in China and Central Asia

Abstract

From continental to regional scales, the zoonosis alveolar echinococcosis (AE) (caused by Echinococcus multilocularis) forms discrete patches of endemicity within which transmission hotspots of much larger prevalence may occur. Since the late 80s, a number of hotspots have been identified in continental Asia, mostly in China, wherein the ecology of intermediate host communities has been described. This is the case in south Gansu, at the eastern border of the Tibetan plateau, in south Ningxia, in the western Tian Shan of Xinjiang, and in the Alay valley of south Kyrgyzstan. Here we present a comparative natural history and characteristics of transmission ecosystems or ecoscapes. On this basis, regional types of transmission and their ecological characteristics have been proposed in a general framework. Combining climatic, land cover and intermediate host species distribution data, we identified and mapped 4 spatially distinct types of transmission ecosystems typified by the presence of one of the following small mammal 'flagship' species: Ellobius tancrei, Ochotona curzoniae, Lasiopodomys brandtii or Eospalax fontanierii. Each transmission ecosystem had its own characteristics which can serve as a reference for further in-depth research in the transmission ecology of E. multilocularis. This approach may be used at fine spatial scales to characterize other poorly known transmission systems of the large Eurasian endemic zone, and help in consideration of surveillance systems and interventions.

Fig. 1.

Map of China and main locations cited in the text. The background is the Global Land One-kilometre Base Elevation model, provided by the US National Oceanic and Atmospheric Administration. Coordinates reference system in degrees (WGS84).KGZ, Kyrgyzstan; NX, Ningxia; Rt, Rangtang.

Fig. 2.

View of some of the hotspots studied. a, Outbreak of Arvicola terrestris and Microtus arvalis in the Jura massif grassland, France (tumuli are earth expelled by A. terrestris when digging galleries), b, outbreak of Ellobius tancrei, Sary-Mogol grassland, south Kyrgyzstan (note the typical conical tumuli with lateral opening); c, typical habitat of Microtus gregalis along streams, Sary-Mogol, south Kyrgyzstan; d, outbreak of Ellobius tancrei and Microtus obscurus, Narati, Tien Shan, Xingjiang, China; e, outbreak of Ochotona curzoniae, Tuanji, eastern Tibetan plateau, Sichuan, China; f, field terraces, Xiji, Ningxia; g, grassland and afforested areas in Xiji. Field terraces and early stages of recently afforested areas are typical habitats for Eospalax fontanierii and Cricetulus longicaudatus; h, in 1996, field terraces of Ban Ban Wan (human AE prevalence: 16%) and deforestation in progress on the other side of the valley, Zhang, Gansu, China.

Fig. 3.

Grassland land cover and distribution range of flagship species, after IUCN (2012), modified.

Fig. 4.

Relative density of Ellobius tancrei population and grass density in Sary-Mogol, Alay Valley. 56 locations were selected at an average distance of 1·2 km from each other. 20 intervals of 10 paces were walked at each point in may 2012. The score of relative density of E. tancrei was the number of intervals where fresh E. tancrei indices could be observed (see e.g. Giraudoux et al. ; Quéré et al. 2000). The NDVI (Normalized Difference Vegetation Index), an index commonly used to estimate the relative density of plant cover, was computed from a Landsat ETM image acquired the 16th of June 2004. The relationship between E. tancrei score and NDVI was modelled using a general additive model with a Poisson error, and a thin plate regression smoother (using a three dimensional basis) (Wood, 2006). The empirical variogram of residuals was included within the limits of the variogram envelop obtained from 99 random permutations of the original data, indicating that no spatial autocorrelation could be detected. The correlation between E. tancrei score and NDVI was found statistically significant at a probability lower than 0·00001.

Fig. 5.

Distribution of fox species. The distribution of the red fox covers the totality of the area.

Fig. 6.

Transmission systems and their flagship species. Except in the Eospalax fontanierii area (E.f.), more intense transmission and hotspots are more likely found in areas with larger ratio of permanent grassland. Question marks are placed on a number of areas of large ratio of permanent grassland but where no reference studies on small mammal communities and transmission are yet available.