Wang L , Utzinger J , Zhou X , 2008. Schistosomiasis control: experiences and lessons from China. Lancet 372: 1793–1795.
GBD 2017 DALYs and HALE Collaborators , 2018. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392: 1859–1922.
Zhang J , Yue M , Hu Y , Bergquist R , Su C , Gao F , Cao Z , Zhang Z , 2020. Risk prediction of two types of potential snail habitats in Anhui Province of China: model-based approaches. PLoS Negl Trop Dis 14: e0008178.
Keiser J , Chollet J , Xiao S , Mei J , Jiao P , Utzinger J , Tanner M , 2009. Mefloquine: an aminoalcohol with promising antischistosomal properties in mice. PLoS Negl Trop Dis 3: e350.
Yang G , Zhou X , Sun L , Wu F , Zhong B , Qiu D , Utzinger J , Bradshaw CJA , 2011. Compensatory density feedback of Oncomelania hupensis populations in two different environmental settings in China. Parasit Vectors 4: 133–139.
Yang K , Li W , Sun L , Huang Y , Zhang J , Wu F , Hang D , Steinmann P , Liang Y , 2013. Spatio-temporal analysis to identify determinants of Oncomelania hupensis infection with Schistosoma japonicum in Jiangsu Province, China. Parasit Vectors 6: 138–145.
Yang G , Liu L , Zhu H , Griffiths SM , Tanner M , Bergquist R , Utzinger J , Zhou X , 2014. China’s sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis 14: 881–892.
Zhang L , Xu Z , Dang H , Li Y , Lu S , Xu J , Li S , Zhou X , 2020. Endemic status of schistosomiasis in People’s Republic of China in 2019. Chin J Schistosomiasis Control 32: 551–558.
Wang X , Zhou X , Wu X , Yang K , Lu S , 2008. Study on the spatio-temporal distribution of seroprevalence of Schistosoma japonicum. Chin J Schistosomiasis Control 26: 290–294, 298.
Zhang S , Sun C , Wang M , Lin D , Zhou X , Wang T , 2016. Epidemiological features and effectiveness of schistosomiasis control programme in lake and marshland region in the People’s Republic of China. Adv Parasitol 92: 39–71.
Li S et al., 2021. Spatio-temporal variations of emerging sites infested with schistosome-transmitting Oncomelania hupensis in Hunan Province, China, 1949–2016. Parasit Vectors 14: 7–18.
Wang Y , Zhuang D , 2015. A rapid monitoring and evaluation method of schistosomiasis based on spatial information technology. Int J Environ Res Public Health 12: 15843–15859.
Cheng G , Li D , Zhuang D , Wang Y , 2016. The influence of natural factors on the spatio-temporal distribution of Oncomelania hupensis. Acta Trop 164: 194–207.
Zhou Y et al., 2014. HIV-, HCV-, and co-infections and associated risk factors among drug users in southwestern China: a township-level ecological study incorporating spatial regression. PLoS One 9: e93157.
Liu K , Xu X , Chen Y , Li R , Tang Y , Wei F , 2015. Analysis on influence of meteorological factors on Oncomelania density. Chin J Epidemiol 36: 1274–1278.
Wang CZ , Lu DB , Guo CX , Li Y , Gao YM , Bian CR , Su J , 2014. Compatibility of Schistosoma japonicum from the hilly region and Oncomelania hupensis hupensis from the marshland region within Anhui, China. Parasitol Res 113: 4477–4484.
Hu Y , Zhang Z , Chen Y , Wang Z , Gao J , Tao B , Jiang Q , Jiang Q , 2013. Spatial pattern of schistosomiasis in Xingzi, Jiangxi Province, China: the effects of environmental factors. Parasit Vectors 6: 214–221.
Wang S , Chen Y , Huang J , Liu Z , Li J , Ma J , 2020. Spatial relationships between alcohol outlet densities and drunk driving crashes: an empirical study of Tianjin in China. J Safety Res 74: 17–25.
Chen Y , Cai S , Liu J , Xiao Y , Jiang Y , Dai L , 2015. Spatial regression analysis on climatic factors and snail distribution in marshland schistosomiasis transmission areas. Chin J Dis Control Prev 19: 277–280.
Li Y , He Z , He M , Jiang J , Li J , Zhou Y , Zhang Z , Jiang Q , 2010. Impact of the changing water level on the variance of Oncomelania hupensis populations in lake area with general additive model. Chin J Schistosomiasis Control 31: 1148–1154.
Yang Y , Zhou Y , Song X , Li S , Zhong B , Wang T , Bergquist R , Zhou X , Jiang Q , 2016. Integrated control strategy of schistosomiasis in the People’s Republic of China: projects involving agriculture, water conservancy, forestry, sanitation and environmental modification. Adv Parasitol 92: 237–268.
Attwood SW , Ibaraki M , Saitoh Y , Nihei N , Janies DA , 2015. Comparative phylogenetic studies on Schistosoma japonicum and its snail intermediate host Oncomelania hupensis: origins, dispersal and coevolution. PLoS Negl Trop Dis 9: e0003935.
Dong Y , Li Z , Feng X , Dong X , 2011. Relationship between environmental remote sensing alternate indexes and Oncomelania snail distribution in hilly and mountainous areas. Chin J Schistosomiasis Control 23: 258–261.
Leonardo L et al., 2020. Oncomelania hupensis quadrasi: snail intermediate host of Schistosoma japonicum in the Philippines. Acta Trop 210: 105547–105595.
Zhou Y , Liang S , Chen G , Rea C , He Z , Zhang Z , Wei J , Zhao G , Jiang Q , 2011. An integrated strategy for transmission control of Schistosoma japonicum in a marshland area of China: findings from a five-year longitudinal survey and mathematical modeling. Am J Trop Med Hyg 85: 83–88.
Luc A , 1995. Local indicators of spatial association: LISA. Geogr Anal 27: 93–115.
Liu M , Feng Y , Yang K , 2021. Impact of micro-environmental factors on survival, reproduction and distribution of Oncomelania hupensis snails. Infect Dis Poverty 10: 47–56.
Hong Q , Zhou X , Hang D , Sun L , Yang G , Huang Y , Yang K , 2003. Observation on the amount of oxygen consumption by Oncomelania hupensis under low temperature. Chin J Parasitol Parasit Dis 1: 33–35.
Jiang T et al., 2020. Spatio-temporal distribution of Oncomelania hupensis snails along the Danyang section of the Beijing-Hangzhou Grand Canal and the Danyang-Jintan-Liyang Canal. Chin J Schistosomiasis Control 32: 10–14.
Zhang Z , Ong S , Peng W , Zhou Y , Zhuang J , Zhao G , Jiang Q , 2008. A model for the prediction of Oncomelania hupensis in the lake and marshland regions, China. Parasitol Int 57: 121–131.
Yang Y , Huang S , Pei F , Chen Y , Jiang Q , Deng Z , Zhou Y , 2018. Spatial distribution and habitat suitability of Biomphalaria straminea, intermediate host of Schistosoma mansoni, in Guangdong, China. Infect Dis Poverty 7: 109–118.
Sun Z , Zhang Z , Xu D , Zhou X , Zhou Y , Gong Z , Liu S , 2002. Climate factors on distribution of snail in Jiangning county in Jiangsu Province. J Fourth Mil Med Univ 23: 1026–1028.
Li S , Li S , Ren G , Zhou J , Hu B , Tang L , Wang H , Liu H , He Z , 2017. Strategy and effect of Oncomelania hupensis snail control in inside embankment areas in Junshan District, Hunan Province from 1998 to 2017. Chin J Schistosomiasis Control 29: 550–553.
Wang J , Liao H , Zhong G , Yu B , Huang S , 2002. Effect of environmental modification combined with mollusciciding for snail control. Chin J Schistosomiasis Control 14: 200–202.
Wang H , Yihuo W , Zhou Y , Liu G , Zhang Z , Peng W , Jiang Q , 2010. Impact of micro-environment on Oncomelania hupensis distribution in mountains areas. Chin J Schistosomiasis Control 22: 233–237.
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This study explored the environmental determinants of different months on snail density measured in April at different types of snail habitats (marshlands, inner embankments, and hills) by considering spatial effects. Data were gathered from surveys on snails that were conducted in Hunan Province in April 2016, and information was collected on environmental variables. To investigate the environmental factors influencing snail density in various types of snail habitats, the ordinary least square model, spatial lag model, and spatial error model were all used. The environmental determinants for snail density showed different effects in the three types of snail habitats. In marshlands, snail density measured in April was associated positively with the normalized difference vegetation index (NDVI) and was associated negatively with flooding duration and annual hours of sunshine. Extreme temperatures correlated strongly to snail density measured in April (P < 0.05). In areas inside embankments, snail density measured in April increased with a decreased distance between snail habitat and the nearest river (P < 0.05). In hills, extreme heat, annual hours of sunshine, NDVI in September, and annual average land surface temperature (LST) were associated negatively with snail density measured in April, whereas index of moisture (IM) was associated positively with snail density measured in April (P < 0.05). The effects of LST and hours of sunshine on snail density measured in April varied with months of the year in the three different types of snail habitats (P < 0.05). Our study might provide a theoretical foundation for preventing snail transmission and subsequent spread of schistosomiasis.
These authors contributed equally to this work.
Financial support: This study received financial support from the National Natural Science Foundation of China (Grant No. 81673236).
Authors’ addresses: Yingyan Zheng, Fudan University School of Public Health, Shanghai, China, Department of Scientific Research, Children’s Hospital of Fudan University, National Children’s Medical Center, Shanghai, China, Key Laboratory of Public Health Safety, Fudan University, Ministry of Education, Shanghai, China, and Fudan University Center for Tropical Disease Research, Shanghai, China, E-mail: 19211020083@fudan.edu.cn. Ying Shi, Fudan University School of Public Health, Shanghai, China, Key Laboratory of Public Health Safety, Fudan University, Ministry of Education, Shanghai, China, Fudan University Center for Tropical Disease Research, Shanghai, China, and Tongren Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China, E-mail: 18211020083@fudan.edu.cn. Shengming Li, Weicheng Deng, Jie Zhou, and Benjiao Hu, Hunan Institute for Schistosomiasis Control, Yueyang, China, E-mails: lsmpa001@163.com, dwc9051@163.com, zhoujiekb@163.com, and 84133166@qq.com. Honglin Jiang, Na Zhang, Zhengzhong Wang, Ying Xiong, Qingwu Jiang, and Yibiao Zhou, Fudan University School of Public Health, Shanghai, China, Key Laboratory of Public Health Safety, Fudan University, Ministry of Education, Shanghai, China, and Fudan University Center for Tropical Disease Research, Shanghai, China, E-mails: hljiang20@fudan.edu.cn, 19211020005@fudan.edu.cn, 20211020023@fudan.edu.cn, 20211020140@fudan.edu.cn, jiangqw@fudan.edu.cn, and ybzhou@fudan.edu.cn. Yue Chen, School of Epidemiology and Public Health, Faculty of Medicine, University of Ottawa, Ottawa, ON, Canada, E-mail: yue.chen@uottawa.ca.
Wang L , Utzinger J , Zhou X , 2008. Schistosomiasis control: experiences and lessons from China. Lancet 372: 1793–1795.
GBD 2017 DALYs and HALE Collaborators , 2018. Global, regional, and national disability-adjusted life-years (DALYs) for 359 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet 392: 1859–1922.
Zhang J , Yue M , Hu Y , Bergquist R , Su C , Gao F , Cao Z , Zhang Z , 2020. Risk prediction of two types of potential snail habitats in Anhui Province of China: model-based approaches. PLoS Negl Trop Dis 14: e0008178.
Keiser J , Chollet J , Xiao S , Mei J , Jiao P , Utzinger J , Tanner M , 2009. Mefloquine: an aminoalcohol with promising antischistosomal properties in mice. PLoS Negl Trop Dis 3: e350.
Yang G , Zhou X , Sun L , Wu F , Zhong B , Qiu D , Utzinger J , Bradshaw CJA , 2011. Compensatory density feedback of Oncomelania hupensis populations in two different environmental settings in China. Parasit Vectors 4: 133–139.
Yang K , Li W , Sun L , Huang Y , Zhang J , Wu F , Hang D , Steinmann P , Liang Y , 2013. Spatio-temporal analysis to identify determinants of Oncomelania hupensis infection with Schistosoma japonicum in Jiangsu Province, China. Parasit Vectors 6: 138–145.
Yang G , Liu L , Zhu H , Griffiths SM , Tanner M , Bergquist R , Utzinger J , Zhou X , 2014. China’s sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis 14: 881–892.
Zhang L , Xu Z , Dang H , Li Y , Lu S , Xu J , Li S , Zhou X , 2020. Endemic status of schistosomiasis in People’s Republic of China in 2019. Chin J Schistosomiasis Control 32: 551–558.
Wang X , Zhou X , Wu X , Yang K , Lu S , 2008. Study on the spatio-temporal distribution of seroprevalence of Schistosoma japonicum. Chin J Schistosomiasis Control 26: 290–294, 298.
Zhang S , Sun C , Wang M , Lin D , Zhou X , Wang T , 2016. Epidemiological features and effectiveness of schistosomiasis control programme in lake and marshland region in the People’s Republic of China. Adv Parasitol 92: 39–71.
Li S et al., 2021. Spatio-temporal variations of emerging sites infested with schistosome-transmitting Oncomelania hupensis in Hunan Province, China, 1949–2016. Parasit Vectors 14: 7–18.
Wang Y , Zhuang D , 2015. A rapid monitoring and evaluation method of schistosomiasis based on spatial information technology. Int J Environ Res Public Health 12: 15843–15859.
Cheng G , Li D , Zhuang D , Wang Y , 2016. The influence of natural factors on the spatio-temporal distribution of Oncomelania hupensis. Acta Trop 164: 194–207.
Zhou Y et al., 2014. HIV-, HCV-, and co-infections and associated risk factors among drug users in southwestern China: a township-level ecological study incorporating spatial regression. PLoS One 9: e93157.
Liu K , Xu X , Chen Y , Li R , Tang Y , Wei F , 2015. Analysis on influence of meteorological factors on Oncomelania density. Chin J Epidemiol 36: 1274–1278.
Wang CZ , Lu DB , Guo CX , Li Y , Gao YM , Bian CR , Su J , 2014. Compatibility of Schistosoma japonicum from the hilly region and Oncomelania hupensis hupensis from the marshland region within Anhui, China. Parasitol Res 113: 4477–4484.
Hu Y , Zhang Z , Chen Y , Wang Z , Gao J , Tao B , Jiang Q , Jiang Q , 2013. Spatial pattern of schistosomiasis in Xingzi, Jiangxi Province, China: the effects of environmental factors. Parasit Vectors 6: 214–221.
Wang S , Chen Y , Huang J , Liu Z , Li J , Ma J , 2020. Spatial relationships between alcohol outlet densities and drunk driving crashes: an empirical study of Tianjin in China. J Safety Res 74: 17–25.
Chen Y , Cai S , Liu J , Xiao Y , Jiang Y , Dai L , 2015. Spatial regression analysis on climatic factors and snail distribution in marshland schistosomiasis transmission areas. Chin J Dis Control Prev 19: 277–280.
Li Y , He Z , He M , Jiang J , Li J , Zhou Y , Zhang Z , Jiang Q , 2010. Impact of the changing water level on the variance of Oncomelania hupensis populations in lake area with general additive model. Chin J Schistosomiasis Control 31: 1148–1154.
Yang Y , Zhou Y , Song X , Li S , Zhong B , Wang T , Bergquist R , Zhou X , Jiang Q , 2016. Integrated control strategy of schistosomiasis in the People’s Republic of China: projects involving agriculture, water conservancy, forestry, sanitation and environmental modification. Adv Parasitol 92: 237–268.
Attwood SW , Ibaraki M , Saitoh Y , Nihei N , Janies DA , 2015. Comparative phylogenetic studies on Schistosoma japonicum and its snail intermediate host Oncomelania hupensis: origins, dispersal and coevolution. PLoS Negl Trop Dis 9: e0003935.
Dong Y , Li Z , Feng X , Dong X , 2011. Relationship between environmental remote sensing alternate indexes and Oncomelania snail distribution in hilly and mountainous areas. Chin J Schistosomiasis Control 23: 258–261.
Leonardo L et al., 2020. Oncomelania hupensis quadrasi: snail intermediate host of Schistosoma japonicum in the Philippines. Acta Trop 210: 105547–105595.
Zhou Y , Liang S , Chen G , Rea C , He Z , Zhang Z , Wei J , Zhao G , Jiang Q , 2011. An integrated strategy for transmission control of Schistosoma japonicum in a marshland area of China: findings from a five-year longitudinal survey and mathematical modeling. Am J Trop Med Hyg 85: 83–88.
Luc A , 1995. Local indicators of spatial association: LISA. Geogr Anal 27: 93–115.
Liu M , Feng Y , Yang K , 2021. Impact of micro-environmental factors on survival, reproduction and distribution of Oncomelania hupensis snails. Infect Dis Poverty 10: 47–56.
Hong Q , Zhou X , Hang D , Sun L , Yang G , Huang Y , Yang K , 2003. Observation on the amount of oxygen consumption by Oncomelania hupensis under low temperature. Chin J Parasitol Parasit Dis 1: 33–35.
Jiang T et al., 2020. Spatio-temporal distribution of Oncomelania hupensis snails along the Danyang section of the Beijing-Hangzhou Grand Canal and the Danyang-Jintan-Liyang Canal. Chin J Schistosomiasis Control 32: 10–14.
Zhang Z , Ong S , Peng W , Zhou Y , Zhuang J , Zhao G , Jiang Q , 2008. A model for the prediction of Oncomelania hupensis in the lake and marshland regions, China. Parasitol Int 57: 121–131.
Yang Y , Huang S , Pei F , Chen Y , Jiang Q , Deng Z , Zhou Y , 2018. Spatial distribution and habitat suitability of Biomphalaria straminea, intermediate host of Schistosoma mansoni, in Guangdong, China. Infect Dis Poverty 7: 109–118.
Sun Z , Zhang Z , Xu D , Zhou X , Zhou Y , Gong Z , Liu S , 2002. Climate factors on distribution of snail in Jiangning county in Jiangsu Province. J Fourth Mil Med Univ 23: 1026–1028.
Li S , Li S , Ren G , Zhou J , Hu B , Tang L , Wang H , Liu H , He Z , 2017. Strategy and effect of Oncomelania hupensis snail control in inside embankment areas in Junshan District, Hunan Province from 1998 to 2017. Chin J Schistosomiasis Control 29: 550–553.
Wang J , Liao H , Zhong G , Yu B , Huang S , 2002. Effect of environmental modification combined with mollusciciding for snail control. Chin J Schistosomiasis Control 14: 200–202.
Wang H , Yihuo W , Zhou Y , Liu G , Zhang Z , Peng W , Jiang Q , 2010. Impact of micro-environment on Oncomelania hupensis distribution in mountains areas. Chin J Schistosomiasis Control 22: 233–237.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 3513 | 1601 | 305 |
Full Text Views | 267 | 18 | 0 |
PDF Downloads | 123 | 14 | 0 |