Invasive snails and an emerging infectious disease: results from the first national survey on Angiostrongylus cantonensis in China

Abstract

Background: Eosinophilic meningitis (angiostrongyliasis) caused by Angiostrongylus cantonensis is emerging in mainland China. However, the distribution of A. cantonensis and its intermediate host snails, and the role of two invasive snail species in the emergence of angiostrongyliasis, are not well understood.

Methodology/principal findings: A national survey pertaining to A. cantonensis was carried out using a grid sampling approach (spatial resolution: 40x40 km). One village per grid cell was randomly selected from a 5% random sample of grid cells located in areas where the presence of the intermediate host snail Pomacea canaliculata had been predicted based on a degree-day model. Potential intermediate hosts of A. cantonensis were collected in the field, restaurants, markets and snail farms, and examined for infection. The infection prevalence among intermediate host snails was estimated, and the prevalence of A. cantonensis within P. canaliculata was displayed on a map, and predicted for non-sampled locations. It was confirmed that P. canaliculata and Achatina fulica were the predominant intermediate hosts of A. cantonensis in China, and these snails were found to be well established in 11 and six provinces, respectively. Infected snails of either species were found in seven provinces, closely matching the endemic area of A. cantonensis. Infected snails were also found in markets and restaurants. Two clusters of A. cantonensis-infected P. canaliculata were predicted in Fujian and Guangxi provinces.

Conclusions/significance: The first national survey in China revealed a wide distribution of A. cantonensis and two invasive snail species, indicating that a considerable number of people are at risk of angiostrongyliasis. Health education, rigorous food inspection and surveillance are all needed to prevent recurrent angiostrongyliasis outbreaks.

Figure 1. Number and infection status of potential intermediate hosts of Angiostrongylus cantonensis examined during the first national survey in mainland China, 2006/2007.

Figure 2. Predicted Angiostrongylus cantonensis prevalence within Pomacea canaliculata in mainland China, 2006/2007.

The map is based on the currently available data regarding the prevalence of A. cantonensis within P. canaliculata, smoothed by ordinary kriging. The predicted prevalences were then stratified into 10 categories by the smart quantiles technique.

Figure 3. Occurrence of Angiostrongylus cantonensis according to hosts in mainland China, 2006/2007.

Each point represents a county where the national survey was implemented. All field sites are located within a region delimited by northern latitude 18°13′–34°50′ and eastern longitude 97°50′–122°07′. The results pertaining to two invasive snail species, i.e., Pomacea canaliculata and Achatina fulica, are highlighted, and the infection status of other animals was omitted whenever infected snails were found in the same places.

Figure 4. Distribution of Pomacea canaliculata in mainland China, 2006/2007.

All field sites are located in a region delimited by the northern latitude 18°13′–34°50′ and eastern longitude 97°50′–122°07′. Also shown are the terrain and the waterways along with the point of introduction of P. canaliculata (Zhongshan city; red star). The elevation is depicted with green indicating the lowest elevation and red indicating the highest elevations.

Figure 5. Distribution of Achatina fulica in mainland China, 2006/2007.

All field sites are located in a region delimited by the northern latitude 18°13′–34°50′ and eastern longitude 97°50′–122°07′. The terrain and the waterways along with the point of introduction of the terrestrial A. fulica (Xiamen; red star) are also presented in this map. The elevation is depicted with green indicating the lowest elevation and red indicating the highest elevations.