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

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          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.

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          Most cited references 95

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          Statistics for Spatial Data

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            Is Open Access

            European Echinococcosis Registry: Human Alveolar Echinococcosis, Europe, 1982–2000

            Surveillance for alveolar echinococcosis in central Europe was initiated in 1998. On a voluntary basis, 559 patients were reported to the registry. Most cases originated from rural communities in regions from eastern France to western Austria; single cases were reported far away from the disease-“endemic” zone throughout central Europe. Of 210 patients, 61.4% were involved in vocational or part-time farming, gardening, forestry, or hunting. Patients were diagnosed at a mean age of 52.5 years; 78% had symptoms. Alveolar echinococcosis primarily manifested as a liver disease. Of the 559 patients, 190 (34%) were already affected by spread of the parasitic larval tissue. Of 408 (73%) patients alive in 2000, 4.9% were cured. The increasing prevalence of Echinococcus multilocularis in foxes in rural and urban areas of central Europe and the occurrence of cases outside the alveolar echinococcosis–endemic regions suggest that this disease deserves increased attention.
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              Fast sampling of Gaussian Markov random fields

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                September 2008
                3 September 2008
                : 2
                : 9
                Affiliations
                [1 ]Department of Chrono-environment, UMR UFC/CNRS 6249 aff. INRA, Université de Franche-Comté, Besançon, France
                [2 ]Ningxia Medical College, Ningxia Hui Autonomous Region, People's Republic of China
                [3 ]Queensland Institute of Medical Research, Brisbane, Queensland, Australia
                [4 ]University of Salford, Salford, United Kingdom
                [5 ]Université de Franche-Comté, Besançon, France
                [6 ]Sichuan Provincial Center for Diseases Control and Prevention, Chengdu, Sichuan, People's Republic of China
                London School of Hygiene & Tropical Medicine, United Kingdom
                Author notes

                Conceived and designed the experiments: YRY PSC DPM DAV PG. Performed the experiments: YRY. Analyzed the data: DRJP QW. Contributed reagents/materials/analysis tools: DRJP YRY FMD DPM. Wrote the paper: DRJP YRY FMD FR PSC DPM DAV PG. Performed geo-referencing of patients: DRJP.

                Article
                07-PNTD-RA-0264R3
                10.1371/journal.pntd.0000287
                2565701
                18846237
                99889ebd-9183-4251-ba3d-c62737d3c4ce
                Pleydell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                Page count
                Pages: 10
                Categories
                Research Article
                Ecology/Spatial and Landscape Ecology
                Infectious Diseases/Neglected Tropical Diseases

                Infectious disease & Microbiology

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