Xia et al. Parasites & Vectors (2017) 10:136 DOI 10.1186/s13071-017-2059-y RESEARCH Open Access Village-based spatio-temporal cluster analysis of the schistosomiasis risk in the Poyang Lake Region, China Congcong Xia1,2,3,4, Robert Bergquist5, Henry Lynn1,2,3,4, Fei Hu6, Dandan Lin6, Yuwan Hao7, Shizhu Li7*, Yi Hu1,2,3,4* and Zhijie Zhang1,2,3,4* Abstract Background: The Poyang Lake Region, one of the major epidemic sites of schistosomiasis in China, remains a severe challenge. To improve our understanding of the current endemic status of schistosomiasis and to better control the transmission of the disease in the Poyang Lake Region, it is important to analyse the clustering pattern of schistosomiasis and detect the hotspots of transmission risk. Results: Based on annual surveillance data, at the village level in this region from 2009 to 2014, spatial and temporal cluster analyses were conducted to assess the pattern of schistosomiasis infection risk among humans through purely spatial(LocalMoran’s I, Kulldorff and Flexible scan statistic) and space-time scan statistics (Kulldorff). A dramatic decline was found in the infection rate during the study period, which was shown to be maintained at a low level. The number of spatial clusters declined over time and were concentrated in counties around Poyang Lake, including Yugan, Yongxiu, Nanchang, Xingzi, Xinjian, De’an as well as Pengze, situated along the Yangtze River and the most serious area found in this study. Space-time analysis revealed that the clustering time frame appeared between 2009 and 2011 and the most likely cluster with the widest range was particularly concentrated in Pengze County. Conclusions: This study detected areas at high risk for schistosomiasis both in space and time at the village level from 2009 to 2014 in Poyang Lake Region. The high-risk areas are now more concentrated and mainly distributed at the river inflows Poyang Lake and along Yangtze River in Pengze County. It was assumed that the water projects including reservoirs and a recently breached dyke in this area were partly to blame. This study points out that attempts to reduce the negative effects of water projects in China should focus on the Poyang Lake Region. Keywords: Schistosomiasis, Spatio-temporal, Poyang Lake Region, China Background the founding of the People’s Republic of China in 1994 Intestinal schistosomiasis caused by infection with S. [4]. Over the past 60 years, China has been taking effect- japonicum, a water-borne parasitic disease, has brought ive steps towards eliminating Schistosoma japonicum [5]. about significant economic and public health concerns During 1992–2001, the World Bank committed a loan in south-east Asia [1, 2] with a history of more than of 71 million US dollars that was expanded by matching 2100 years in China [3]. Epidemiological surveys showed funds at the same level from the Government of China that approximately 100 million people were at risk, with for schistosomiasis control mainly based on chemother- up to 12 million being infected with schistosomiasis, at apy and snail control. These measures reduced the prevalence by over 50% [6], while the further emphasis of control activities through a revised strategy was initi- * Correspondence: [email protected]; [email protected]; [email protected] 7National Institute of Parasitic Diseases, Chinese Center for Disease Control ated from 2005 based on new diagnostic techniques, and Prevention, Key Laboratory of Parasite and Vector Biology, Ministry of replacement of cows with machines and a boost of Health, Shanghai 200032, China health education made further significant progress in 1Department of Epidemiology and Biostatistics, School of Public Health, Fudan University, Shanghai 200032, China controlling this disease [6]. According to the latest Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Xia et al. Parasites & Vectors (2017) 10:136 Page 2 of 10 report in 2014, the number of people infected was esti- we also applied a new spatial scan statistic method mated to be 115,614, which was a decrease of 83.4% since (Flexible scan statistic). 2000 [7]. Meanwhile, of the 12 endemic provinces located In this study, S. japonicum prevalence data at the along the Yangtze River, five (Shanghai, Zhejiang, Fujian, village level from 2009 to 2014 in Jiangxi Province, Guangdong, Guangxi) reached transmission interruption China, was evaluated to analyse the spatial and criterion, and four (Sichuan, Yunnan, Jiangsu, Hubei) temporal clustering of schistosomiasis, using the three reached transmission control criterion [8]. methods mentioned above to help improve our Despite the remarkable success achieved in schisto- understanding of the current endemic status in the somiasis control in China through the measures men- Poyang Lake Region. tioned, schistosomiasis remains a serious problem in the lake and marshland regions, especially along the middle of the Yangtze River basin (including both Dongting and Methods Poyang Lakes). Contributing factors are the parasite’s Study area complicated transmission process based on a snail inter- Poyang Lake, the largest freshwater lake in China, is situ- mediate host, anthropogenic environment transform- ated in the northern part of Jiangxi Province and near the ation and regional climate change [5, 9, 10]. It has been southern bank of the middle and lower reaches of River estimated that people infected with S. japonicum in Yangtze (Fig. 1). Five main tributaries, rivers Gan, Fu, Xiu, swamp and lake areas account for approximately 86% of Rao and Xin, flow into Poyang Lake. Poyang Lake is a typ- the total number in the whole country [11]. Poyang Lake ical seasonal water-land transition lake with dramatic Region, which includes the largest freshwater lake in intra-annual fluctuation of the water level (historically China, constitutes the largest continuous area endemic ranging from 7.1 m in the winter dry season to 19.0 m in for schistosomiasis in the country and was historically the summer rainy season) [20], leading to a variation of reported with 2.5 million people at risk for infection and lake coverage from around 500 km2 in the winter to a 340,000 infected [12]. peak of approximately 4125 km2 in the summer [21]. The year 2016 represents the aftermath of the preced- During flooding, water recharges from River Yangtze, ing year’s ultra-strong El Nino [13] and, the climate has while it is deficient at the other extreme of the season, been extraordinarily complex with 27 rainstorms since which generates flood plains from April to September the flooding season according to the National Climate and a landscape of marshlands from November to early Center in China [14]. The water level at the Hukou March [12]. These dramatic variations of the water hydrometric station in Poyang Lake was 1.18 m higher level along with the humid, subtropical monsoon in than last year at the corresponding period, and flooding Jiangxi Province govern the distribution of the parasite’s disasters occurred in Jiangxi Province including Poyang, intermediate snail host O. hupensis [22]. Duchang, Yongxiu Counties. Flooding impacts the schis- This study covered the core region surrounding the tosomiasis situation negatively and, indeed, the number lake with about 18 endemic counties, including 1374 ad- of acute cases of the disease have been markedly higher ministrative villages. The latitude and longitude coordi- in years characterised by flooding [15]. Investigation of nates of each village were obtained by a handheld Global cluster patterns is therefore distinctly important for Position System (GPS) instrument (MobileMapper10, implementing control measures during and after floods. Thales Navigation, Paris, France). It is widely acknowledged that the epidemiology of S. japonicum infections has a particular spatial char- acteristic in China because it depends on the pres- Calculation of infection rates ence of a sole intermediate host snail, Oncomelania Village-level data on schistosomiasis endemicity in hu- hupensis, whose specific climatic and environmental man from 2009 to 2014 were collected and processed. conditions for reproduction governs the distribution The database was setup under annually conventional of schistosomiasis [16–18]. Recent advancement of surveillance in each endemic village of Jiangxi Province. specific spatial analysis tools, such as SaTScan and A two-step diagnostic approach confirmed human FlexScan facilitate the investigation of schistosomiasis’ infection with schistosomiasis. Residents in endemic epidemiological patterns in space and time at scales villages were first screened by the indirect haemagglu- varying from local to regional [17]. In previous stud- tination (IHA) serology test and those found to be ies [6, 19], spatial clusters of schistosomiasis have positive were further tested by the faecal Kato-Katz ever been detected in endemic areas, but they only parasitological test, currently the gold standard for made use of traditional spatial scan statistics as SaTS- diagnosis of S. japonicum [23]. can spatial scan and Local Moran’sI.Consideringthat In this study, one indicator was calculated to reflect the extent of these clusters are commonly irregular, the endemic risk with the following formula: Xia et al. Parasites & Vectors (2017) 10:136 Page 3 of 10 Fig. 1 Location of the study area and the spatial distribution of survey data. Poyang Lake is situated in the northern part of Jiangxi Province and near the southern bank of the middle and lower reaches of River Yangtze.