Molecular evidence on the presence of Schistosoma japonicum infection in snails along the Yangtze River, 2015-2019.

BACKGROUND: Due to sustained control activities, the prevalence of Schistosoma japonicum infection in humans, livestock and snails has decreased significantly in P. R. China, and the target has shifted from control to elimination according to the Outline of Healthy China 2030 Plan. Applying highly sensitive methods to explore the presence of S. japonicum infection in its intermediate host will benefit to assess the endemicity or verify the transmission interruption of schistosomiasis accurately. The aim of this study was to access the presence of S. japonicum infection by a loop-mediated isothermal amplification (LAMP) method through a 5-year longitudinal study in five lake provinces along the Yangtze River. METHODS: Based on previous epidemiological data, about 260 villages with potential transmission risk of schistosomiasis were selected from endemic counties in five lake provinces along the Yangtze River annually from 2015 to 2019. Snail surveys were conducted in selected villages by systematic sampling method and/or environmental sampling method each year. All live snails collected from field were detected by microscopic dissection method, and then about one third of them were detected by LAMP method to assess the presence of S. japonicum infection with a single blind manner. The infection rate and nucleic acid positive rate of schistosomes in snails, as well as the indicators reflecting the snails' distribution were calculated and analyzed. Fisher's exact test was used to examine any change of positive rate of schistosomes in snails over time. RESULTS: The 5-year survey covered 94,241 ha of environment with 33,897 ha of snail habitats detected accumulatively. Totally 145.3 ha new snail habitats and 524.4 ha re-emergent snail habitats were found during 2015-2019. The percentage of frames with snails decreased from 5.93% [45,152/761,492, 95% confidence intervals (CI): 5.88-5.98%] in 2015 to 5.25% (30,947/589,583, 95% CI: 5.19-5.31%) in 2019, while the mean density of living snails fluctuated but presented a downward trend generally from 0.20 snails/frame (155,622/761,492, 95% CI: 0.17-0.37) in 2015 to 0.13 snails/frame (76,144/589,583, 95% CI: 0.11-0.39) in 2019. A total of 555,393 live snails were collected, none of them was positive by dissection method. Totally 17 pooling snail samples were determined as positives by LAMP method among 8716 pooling samples with 174,822 of living snails, distributed in 12 villages of Hubei, Hunan, Jiangxi and Anhui provinces. The annual average positive rate was 0.41% (95% CI: 0.13-0.69%) in 2015, 0% in 2016, 0.36% (95% CI: 0.09-0.63%) in 2017, 0.05% (95% CI: 0-0.16%) in 2018, 0.05% (95% CI: 0-0.15%) in 2019, respectively, presenting a downward trend from 2015 to 2019 with statistical significance (χ2 = 11.64, P < 0.05). CONCLUSIONS: The results suggest that S. japonicum infection still persisted in nature along the Yangtze River and traditional techniques might underestimate the prevalence of schistosomiasis in its intermediate hosts. Exploring and integrating molecular techniques into national surveillance programme could improve the sensitivity of surveillance system and provide guidance on taking actions against schistosomiasis.

Efforts to eliminate schistosomiasis in Hubei province, China: 2005-2018.

BACKGROUND: The Hubei province is one of the most schistosomiasis-epidemic-prone provinces in China. A series of strategies were adopted by the government to curb the rebound schistosomiasis endemic status that has prevailed since the early 2000s. This study aimed to elucidate the trends of schistosomiasis transmission and to appraise the effectiveness of the integrated control strategy in lake and marshland areas. METHODS: Surveillance data of schistosomiasis in the Hubei province between 2005 and 2018 were analyzed, including conventional health control measures, integrated strategies, and measures that focused on the infection source. According to the local annual plan for schistosomiasis control in endemic counties, previous measures were human and snail control and surveillance. Residents aged 6-65 years were screened by an immunological detection method called indirect hemagglutination assay (IHA) after the transmission season each year. All residents who tested positive were then asked to provide a fecal sample for examination by the miracidium hatching technique (MHT) to detect the presence of schistosomes. Moreover, systematic snail surveys were conducted as a part of the combined environmental sampling method. The latter included integrated strategies and measures that focused on the infection source. Bovine stool samples were also collected and concurrently assessed using the MHT by the agriculture department, river-hardening slope protection was constructed by the water conservancy department, and forestation promotion was conducted by the forest department. The effectiveness of the integrated control strategy was assessed using two indicators of resident and livestock infection rates and three indicators of snail epidemics across all endemic areas. RESULTS: From 2005 to 2018, a total of 28. 46 million and 2. 05 million residents were assessed by immunological (IHA) and etiological (MHT) detection techniques, respectively. Snail surveys and molluscicide application were performed in 2. 26 hectares and 0. 37 hectares, respectively. Moreover, 2. 60 million bovines were assessed by etiological detection techniques (MHT). The river-hardening slope protection project was implemented in 503 places, and 46 thousand hectares in endemic areas underwent environmental modification. Forestation was implemented at an area of 0. 15 million hectares. Between 2005 and 2018, the epidemic indicators, including resident and livestock infection rates and the infested areas and infection rate of snails, all presented downward trends. The resident infection rate decreased from 3. 78% in 2005 to 0% in 2016, which persisted through 2018. The livestock infection rate decreased from 5. 63% in 2005 to 0% in 2013, which also persisted through 2018. From 2005 to 2018, the snail-inhabited area was slightly reduced, but the area of infected snails decreased to 0 in 2012; this persisted through 2018. All counties met the goal for schistosomiasis infection control, transmission control, and disruption of schistosomiasis activity in 2008, 2013, and 2018 separately. That means the goal has been achieved in each stage. CONCLUSIONS: The decline of the schistosomiasis epidemic rate demonstrates that the Chinese government was successful in meeting its public health goal in Hubei province. In the next decade, precision interventions must be implemented in endemic counties with a relatively low epidemic status to achieve the goals of the Outline of the Healthy China 2030 Plan. A similar strategy can be applied in other countries to eliminate schistosomiasis globally.

Dynamics of spatiotemporal distribution of schistosomiasis in Hubei Province, China.

Schistosomiasis caused by parasitic flatworms of blood flukes, remains a major public health concern in China. The significant progress in controlling schistosomiasis in China over the past decades has resulted in the remarkable reduction in the prevalence and intensity of Schistosoma japonicum infection to an extremely low level. Therefore, the elimination of schistosomiasis has been promoted by the Chinese national government. Hubei Province is the major endemic area, that is, along the middle and low reaches of the Yangtze River in the lake and marshland regions of southern China. Eliminating the transmission of schistosomiasis in Hubei Province is challenging. The current issue is to determine the distributions and clusters of schistosomiasis transmission. In this study, we assessed the spatial distribution of schistosomiasis and the risk at the county level in Hubei Province from 2011 to 2015 to provide guidance on the elimination of schistosomiasis transmission in lake and marshland regions. Spatial database of human S.japonicum infection from 2011 to 2015 at the county level in the study area was built based on the annual schistosomias is surveillance data. Moran's I, the global spatial autocorrelation statistics, was utilized to describe the spatial autocorrelation of human S. japonicum infection. In addition, purely spatial scan statistics combined with space-time scan statistics were used to determine the epidemic clusters. Infection rates of S. japonicum decreased in each endemic county in Hubei from 2011 to 2015. Human S. japonicum infection rate showed statistical significance by global autocorrelation analysis during the study period (Moran's I > 0, P < 0.01). This result suggested that there were spatial clusters present in the distribution of S. japonicum infection for the five years. Purely spatial analysis of human S. japonicum infection showed one most likely cluster and one secondary cluster from 2011 to 2015, which covered four and one counties, respectively. Spatiotemporal clustering analysis determined one most likely cluster and one secondary cluster both in 2011-2012, which appeared in 4 and 5 counties, respectively. However, the number of clustering foci decreased with time, and no cluster was detected after 2013.The clustering foci were both located at the Jianghan Plain, along the middle reaches of the Yangtze River and its connecting branch Hanbei River. Spatial distribution of human S. japonicum infections did not change temporally at the county level in Hubei Province. A declining trend in spatiotemporal clustering was observed between 2011 and 2015. However, effective control strategies and integrated prevention should be continuously performed, especially at the Jianghan Plain area along the Yangtze and Hanbei River Basin. Multivariate statistical analysis was carried out to investigate the risk of missing examinations, missing treatment, and unstandardized treatment events. The results showed that age, education level and Sanitary latrines are risk factors for missing examinations (b > 0, OR >1), and treatment times in past and feeding cattle in village group are protective factors (b < 0, OR <1). We also found that age and education level are risk factors for missing treatment (b > 0, OR >1). Study of the risk for un-standardized treatment revealed that occupation is risk factors (b > 0, OR >1), though, education level is protective factors (b < 0, OR <1). Therefore, precise prevention and control should be mainly targeted at these special populations.

A spatial analysis of human Schistosoma japonicum infections in Hubei, China, during 2009-2014.

BACKGROUND: The province of Hubei is located in the middle of China, near the middle and lower reaches of the River Yangtze, and is an area where schistosomiasis is endemic. It is challenging to control this disease in this environment, and it would be useful to identify clusters of infection and transmission, as well as their distributions during recent years. Therefore, this study aimed to analyze the spatial distribution of schistosomiasis in Hubei, in order to facilitate the effective control and elimination of this disease. METHODS: We collected schistosomiasis surveillance data from all endemic counties in Hubei during 2009-2014. A geographical information system (ArcGIS, version 10.1) was used to link the counties' geographical data with the epidemiological data, and the spatial scanning method (FleXScan v3.1.2) was used to identify spatial clusters of human infections with Schistosoma japonicum. RESULTS: In Hubei, patients who exhibited stool test results that were positive for S. japonicum accounted for > 50 % of all cases in China during 2009-2014. However, each endemic county in Hubei exhibited a declining trend in the number of human S. japonicum infections during the study period. The ArcGIS analyses revealed that the middle reaches of the River Yangtze were highly endemic for S. japonicum infections. Spatial scan analyses revealed the following infection clusters: two clusters in ten counties during 2009, two clusters in nine counties during 2010, three clusters in 12 counties during 2011, two clusters in 12 counties during both 2012 and 2013 and two clusters in ten counties during 2014. Most of the cluster regions were located in the lake and marshland regions along the basins of the River Yangtze. CONCLUSION: We successfully identified schistosomiasis clusters at the county level in Hubei during 2009-2014, and our results revealed that the clusters were typically located in lake and marshland regions. These data may be useful for controlling and eliminating schistosomiasis in other high-risk areas.

[Efficacy of the Sentinel Mouse Method in Monitoring Schistosoma japonicum Infection in Key #br# Water Areas of Hanchuan City].

Objective: To understand the water infectivity of schistosomes in key water areas of Hanchuan City, and explore the use of sentinel mice in surveillance and forecast of schistosomiasis. Methods: Surveillance and forecast sites were set up in North Han River, Diaocha Lake, and Miaowu Ditch in 2014. Sentinel mice （male Kunming mice, n=20 in each site） were placed there within the first ten-day period of June and September, respectively. Field detections lasted 4 h each, for a total of 2 days. The loss and death rates of mice were recorded. Humans and livestocks with activities in these sites were also examined for schistosome infection. The sentinel mice recovered were raised in laboratory for 35 days, dissected, and examined for liver granulomas and adult worm counting. The distribution of sites with positive detections and their infection status were analyzed. Emergency measures were taken in the positive sites. Results: A total of 13（5 sites in North Han River, 5 in Diaocha Lake, and 3 in Miaowu Ditch） surveillance and forecast sites were set up. No infected snail was detected in any of these sites in spring 2014. The detection rate of living snails in North Han River （18.7%, 224/1 201) was significantly higher than that in Diaocha Lake（12.8%, 852/6 644） and in Miaowu Ditch （6.4%, 202/3 147）（P<0.01）. Of the 520 mice placed, 6 were lost, and 514 were recovered, among which 4 mice died during laboratory raising. The remaining 510 sentinel mice were then dissected, revealing infection in 4 mice, with a positive rate of 0.8%. Twenty-seven Schistosoma japonicum worms were collected, and the mean worm burden of positive mice was 6.8 worms per mouse. Three sites (Sansi village, Kangjia village and Doubu village) were found to be positive sites of infection in September, with the detailed number of 2, 1 and 0 in North Han River, Diaocha Lake, and Miaowu Ditch respectively, with a positive rate of 1.5% （3/197）, 0.5% （1/195） and 0 （0/118） in sentinel mice （P>0.05）. In addition, among the 22 cattle found in the 13 sites, 2 were infected with schistosomes; and among the 62 fishermen and boatmen, 2 were infected. Emergency measures were taken in the three positive sites, and no high endemicity occurred. Conclusion: The monitoring of sentinel mice infections can improve the sensitivity of the surveillance and forecast system of schistosomiasis. The infected fishermen and cattle remain the major source of schistosomiasis transmission in Hanchuan City.

Spatial analysis of Schistosomiasis in Hubei Province, China: a GIS-based analysis of Schistosomiasis from 2009 to 2013.

BACKGROUND: Schistosomiasis remains a major public health problem in China. The major endemic areas are located in the lake and marshland regions of southern China, particularly in areas along the middle and low reach of the Yangtze River. Spatial analytical techniques are often used in epidemiology to identify spatial clusters in disease regions. This study assesses the spatial distribution of schistosomiasis and explores high-risk regions in Hubei Province, China to provide guidance on schistosomiasis control in marshland regions. METHODS: In this study, spatial autocorrelation methodologies, including global Moran's I and local Getis-Ord statistics, were utilized to describe and map spatial clusters and areas where human Schistosoma japonicum infection is prevalent at the county level in Hubei province. In addition, linear logistic regression model was used to determine the characteristics of spatial autocorrelation with time. RESULTS: The infection rates of S. japonicum decreased from 2009 to 2013. The global autocorrelation analysis results on the infection rate of S. japonicum for five years showed statistical significance (Moran's I > 0, P < 0.01), which suggested that spatial clusters were present in the distribution of S. japonicum infection from 2009 to 2013. Local autocorrelation analysis results showed that the number of highly aggregated areas ranged from eight to eleven within the five-year analysis period. The highly aggregated areas were mainly distributed in eight counties. CONCLUSIONS: The spatial distribution of human S. japonicum infections did not exhibit a temporal change at the county level in Hubei Province. The risk factors that influence human S. japonicum transmission may not have changed after achieving the national criterion of infection control. The findings indicated that spatial-temporal surveillance of S. japonicum transmission plays a significant role on schistosomiasis control. Timely and integrated prevention should be continued, especially in the Yangtze River Basin of Jianghan Plain area.

[Impact of implementation of Three Gorges Project on schistosomiasis endemic situation in Hubei Province].

OBJECTIVE: To understand the change of hydrological regime in the Yangtze River and schistosomiasis endemic situation after the implementation of Three Gorges Project in Hubei Province. METHODS: The data of hydrological regime of the Yangtze River, schistosomiasis epidemic situation, and Oncomelania hupensis snail status were collected and analyzed in Hubei Province from 2002 to 2012. RESULTS: After the implementation of the Three Gorges Project in 2003, the water level of the Yangtze River slightly rose from January to March, the average water level in May and August both reduced compared with that in 2002, and the time of water withdrawal was moved up. The endemic situation of schistosomiasis showed a decline tendency in areas along the Yangtze River in Hubei Province. The positive rate of serological tests in the residents and the Schistosoma ja- ponicum infection rate in bovine decreased by 2.97% and 92.64% respectively. The numbers of human and bovine infected with S. japonicum decreased by 48.35% and 94.48%, respectively. CONCLUSION: After the implementation of the Three Gorges Project, the schistosomiasis endemic situation shows a decline tendency in the areas along the Yangtze River in Hubei Province, but the long-term monitoring still need to be carried out.

[Surveillance of schistosomiasis in Hubei Province in 2013].

OBJECTIVE: To understand the dynamic schistosomiasis situation in Hubei Province so as to provide the evidence for formulating the effective control strategy. METHODS: According to the Scheme of Schistosomiasis Surveillance in Hubei Province (the 2009 edition) , 207 endemic villages were selected and investigated for the schistosome infections of residents and livestock, and the distribution of Oncomelania hupensis snails. RESULTS: The average infection rates of residents and cattle were 0.35% and 0.15% respectively, and the endemic situation of fishermen and farmers were relatively serious (0.44% and 0.42%, respectively). The density of living snails was 0.30 snail/0.1m2, but no infected snails were found. CONCLUSION: The endemic situation of schistosomiasis in Hubei Province was stable in 2013, but the efforts for the infectious source control still should be strengthened.

[Prediction of epidemic tendency of schistosomiasis with time-series model in Hubei Province].

OBJECTIVE: To study the endemic trend of schistosomiasis japonica in Hubei Province, so as to provide the theoretical basis for surveillance and forecasting of schistosomiasis. METHODS: The time-series auto regression integrated moving average (ARIMA) model was applied to fit the infection rate of residents of Hubei Province from 1987 to 2013, and to predict the short-term trend of infection rate. RESULTS: The actual values of infection rate of residents were all in the 95% confidence internals of value predicted by the ARIMA model. The prediction showed that the infection rate of residents of Hubei Province would continue to decrease slowly. CONCLUSION: The time-series ARIMA model has good prediction accuracy, and could be used for the short-term forecasting of schistosomiasis.

[Effect of comprehensive schistosomiasis control strategy based on infection source control in Hanchuan City].

OBJECTIVE: To evaluate the effect of comprehensive schistosomiasis control measures based on infection source control in Hanchuan City (marshland and lake endemic regions). METHODS: The data of comprehensive schistosomiasis control in Hanchuan City from 2004 to 2013 were collected, and the change trends of the Oncomelania hupensis snail status and the infection situation of human and livestock were analyzed to evaluate the control effect. RESULTS: After the implementation of the comprehensive measures, the infection rates of residents and cattle decreased from 6.38% and 8.11% in 2004 to 0.16% and 0 in 2013 respectively. There were no acute schistosomiasis patients since 2007, no new infection cases since 2011, and no infected snails since 2012. Compared with 2004, the occurrence rate of frames with living snails and the average density of living snails decreased by 56.78% and 68.35%, respectively, but the snail area and susceptible area increased by 0.62% and 7.10%, respectively. In 2013, all the 367 endemic villages in 26 townships reached the criteria of transmission controlled. CONCLUSIONS: The comprehensive schistosomiasis control measures based on infection source control can control the schistosomiasis transmission effectively in marshland and lake endemic regions. When consolidating the achievement, the snail area in inner embankment should be compressed to prevent the schistosome re-infection in human and livestock.