The potential risk of Schistosoma mansoni transmission by the invasive freshwater snail Biomphalaria straminea in South China.

Dan-Dan Lin ,Dongjuan Yuan,Yanhua Zhang,Ya Yang,Benjamin Sanogo,Shuo Wan,Lifu Wang,Zhongdao Wu,Suoyu Xiang,Xi Sun,Shuling Du,Ping He,Tao Ding,Xufen Zeng ,Jerome H L Hui ,You-Sheng Liang ,Xiaofeng Zeng ,Zongyi Deng ,Ziquan Lv

doi:10.1371/journal.pntd.0008310

Abstract

Schistosomes infect more than 200 million people worldwide, and globally, over 700 million people are at risk of infection. The snail Biomphalaria straminea, as one of the intermediate hosts of Schistosoma mansoni, consecutively invaded Hong Kong in 1973, raising great concern in China. In this study, a malacological survey was conducted over a period of four years, and investigations were performed on the mechanism of susceptibility of B. straminea to S. mansoni. B. straminea was investigated in China from 2014 to 2018. Out of 185 investigated sites, 61 were positive for stages of black B. straminea (BBS), which shows pigmented spots. Twenty of the 61 sites were positive for red B. straminea (RBS), which is partially albino and red colored. Phylogenetic analyses based on cox1 and 18S rRNA sequences demonstrated that both phenotypes were clustered with Brazilian strains. No S. mansoni infections were detected in field-collected snail. However, in laboratory experiments, 4.17% of RBS were susceptible to a Puerto Rican strain of S. mansoni, while BBS was not susceptible. The highest susceptibility rate (70.83%) was observed in the F2 generation of RBS in lab. The density of RBS has increased from south to north and from west to east in Guangdong since 2014. Five tyrosinase tyrosine metabolism genes were upregulated in BBS. Transcriptome comparisons of RBS and BBS showed that ficolin, C1q, MASP-like, and membrane attack complex (MAC)/perforin models of the complement system were significantly upregulated in BBS. Our study demonstrated that B. straminea is widely distributed in Hong Kong and Guangdong Province, which is expanding northwards very rapidly as a consequence of its adaptation to local environments. Our results suggest that B. straminea from South China is susceptible to S. mansoni, implying the high potential for S. mansoni transmission and increased S. mansoni infection risk in China.

Highlights

Schistosomiasis, a major neglected tropical disease, occurs as a result of an infection by parasitic trematodes of the genus Schistosoma
Our study suggested that B. straminea is susceptible to S. mansoni, implying a high potential risk of S. mansoni transmission in South China
Our study demonstrated that B. straminea, which has spread in Guangdong Province, may be compatible with S. mansoni, implying high risk of S. mansoni transmission and infection in China

Summary

Introduction

Schistosomiasis, a major neglected tropical disease, occurs as a result of an infection by parasitic trematodes of the genus Schistosoma. The majority of infected persons were children[1] This disease occurred in 78 countries of South America, Asia and Africa and was referred to as a “disease of poverty”, limiting children’s development, food production and the working ability of adults[1]. Schistosoma mansoni is one of the most widespread species causing human Schistosoma infections and is mainly distributed on the Arabian Peninsula and in Egypt, Libya, Sudan, sub-Saharan Africa, Brazil, some Caribbean islands, Suriname and Venezuela[2]. Biomphalaria snails are mainly distributed in Africa, Suriname, Venezuela, the Dominican Republic, Guadeloupe, St. Lucia, and in large areas of Brazil. Research on the biology and distributions of the Biomphalaria species has indicated that 4

Methods

Results

Discussion

Conclusion