Landscape Composition and Spatial Prediction of Alveolar Echinococcosis in Southern Ningxia, China

Abstract

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.

Author Summary

In humans, larvae of the fox tapeworm Echinococcus multilocularis typically infect the liver where metastasis, calcification and necrosis cause the zoonotic disease alveolar echinococcosis (AE). Treatment is difficult. Early detection greatly increases patient life expectancy but under-detection is a problem. Understanding the ecological conditions that elevate AE risk would help identify at-risk communities. Voles and lemmings of the subfamily Arvicolinae are important intermediate hosts in most AE endemic areas, and arvicoline habitat has been proposed as a predictor of AE risk. Using a model of spatial autocorrelation with land cover identified from satellite remote sensing imagery, we identified AE hotspots in southern Ningxia Hui Autonomous Region (NHAR), China. Hotspots were not located near optimal arvicoline habitats. Thus, non-arvicolines provide principal reservoirs in NHAR and the range of ecological conditions sustaining E. multilocularis transmission in China is greater than previously thought. We also show: social factors explain higher prevalence in females than males; dogs increase infection risk; and we argue that water source quality is important via interaction with other environmental variables. Our map of AE prevalence represents the current state-of-the-art regarding the spatial distribution of AE in southern NHAR and provides an important baseline for future monitoring programs there.