- Letter to the Editor
- Open Access
Apropos: factors impacting on progress towards elimination of transmission of schistosomiasis japonica in China
Parasites & Vectors volume 7, Article number: 408 (2014)
Currently, China is moving towards the elimination of schistosomiasis japonica. In a previous review, the factors affecting the progress towards the elimination of transmission of schistosomiasis in China have been summarized. Nevertheless, some factors were neglected. Hereby, we describe four other factors which may threaten the achievement of the goal of schistosomiasis elimination in China.
To the Editor
After nearly 60 years of effort, China has achieved great success in the control of schistosomiasis japonica, and currently, the prevalence and intensity of Schistosoma japonicum infection have been reduced to an extremely low level [1, 2]. The elimination of this neglected tropical parasitic disease has been, therefore, put on the governmental agenda . In a previous review, Zhou and colleagues summarized the factors affecting the progress towards the elimination of the transmission of schistosomiasis japonica in China . These factors, in our opinion, may indeed have potential impact on schistosomiasis elimination, and should be taken into account during the development of the strategy targeting the elimination of the disease in China. However, some other factors were neglected. Hereby, we describe four other factors that may threaten schistosomiasis elimination in China, including political and financial support, climate change, praziquantel resistance, and potential transmission of African schistosomiasis.
The experiences and lessons from the past 5 decades of schistosomiasis control in China have shown that political will and financial support are critically important to the effective control of the disease . At the first stage (from mid-1950s to early 1980s) of the progress of schistosomiasis control in China, there was strong political will among the leaders of the New China to control schistosomiasis, which was called “god of plague” by Chairman Mao, the founder of the People's Republic of China. To wipe out “god of plague”, transmission control strategy with emphasis on control of the snail intermediate host was implemented, and mass campaigns were launched with aims to snail control by environmental modification and mollusciciding. At this stage, snail habitats were greatly shrunk, and the number of schistosomiasis cases reduced remarkably . The introduction of praziquantel, a highly effective, low-cost anti-schistosomiasis drug, led to the national schistosomiasis control strategy shifting from transmission control to morbidity control (from mid-1980s to 2003). The governmental commitment to eliminate schistosomiasis and the 10-year implementation of the World Bank Loan Project for Schistosomiasis Control (1992–2001) that provided sufficient funds resulted in great achievements [7, 8]. During this stage, Shanghai municipality, Guangxi Autonomous Region and Fujian, Guangdong and Zhejiang provinces achieved the national criteria for elimination of schistosomiasis . However, the termination of the World Bank Loan Project for Schistosomiasis Control led to a sharp decline in the funds allocated to schistosomiasis control. In addition, many anti-schistosomiasis institutions were incorporated into general centre for disease control and prevention (CDC) systems around the year 2000, and the professional teams in schistosomiasis were greatly weakened. Such a situation resulted in a resurgence of schistosomiasis japonica in China [10, 11]. In 2004, Chinese government made schistosomiasis one of the highest priorities in communicable disease control, and a new integrated strategy with emphasis on the control of infectious sources was developed to control the transmission of S. japonicum. The control interventions have been made possible due to the strong governmental will to eliminate the disease by 2020 and adequate investment in public health owing to China’s rapid economic development, and the strategy has been shown high effective [13–15]. By 2012, the prevalence of S. japonicum infection in both human and livestock has been decreased to less than 1% in most endemic counties . From the history of schistosomiasis control in China, it is considered that reduced political will and financial support may pose a great threat to the progress of schistosomiasis elimination .
Climate change has been proved a driver of the transmission of vector-borne diseases [18, 19], and it has been demonstrated that schistosomiasis, a snail-borne parasitic disease, appears to be affected by the climate change [20, 21]. In China, the geographical distribution of the snail host O. hupensis is restricted to areas where the mean January temperature is above 0°C . The rise of temperature may cause snail survival and reproduction in currently non-breeding sites, resulting in the potential transmission of schistosomiasis. It was predicted that the temperature increases by 0.9°C in 2030 and 1.6°C in 2050 in China, which may expand schistosomiasis transmission into currently non-endemic areas in the north, with an additional 783883 km2 area , and 20.7 million people at risk of infection by 2050 . It is therefore considered that climate change may affect, in a long-term manner, the progress of schistosomiasis elimination in China.
Praziquantel is currently the only drug of choice for the treatment of human schistosomiases. Evidence from Africa and South America has shown that resistance to praziquantel may emerge following long-term, extensive and repeated use [25–27]. In China, praziquantel-based chemotherapy has been implemented to control the morbidity and reduce the prevalence and intensity of S. japonicum infection for nearly 4 decades, and the strategy has been proved highly effective . There is therefore a great concern about the development of drug resistance . We evaluated the sensitivity of S. japonicum to praziquantel in highly, moderately and lowly endemic regions of China, and no evidence of resistance to praziquantel was detected [30, 31]. However, there are still some cases infected with S. japonicum in whom standard treatment regimen fails to clear the infection . In addition, it has been proved that S. japonicum subjected to drug pressure may develop resistance to praziquantel . The potential emergence of praziquantel resistance would seriously threaten the elimination of schistosomiasis in China, since praziquantel-based chemotherapy is still critical to the national schistosomiasis control program and no alternatives have been developed. Identification of populations at a high risk of praziquantel resistance is of urgent need.
China is only endemic for S. japonicum. Biomphalaria straminea, an intermediate host of S. mansoni in South America, was first discovered in southern China in 1981 as an invasive snail species, and the snail habitants appear extensive expansion . With the continuous rise in the detection of schistosomiasis cases caused by S. manosni in mainland China, the likelihood of transmission of schistosomiasis mansoni in China receives worldwide attention . The lack of highly effective diagnostics, high mobility of the imported cases infected with S. mansoni, and their non-specific syndromes which may easily lead to missed diagnosis and misdiagnosis, and the lack of a sensitive surveillance-response system make it extremely difficult to tackle the risk of the transmission of S. mansoni in China, which poses a threat to the progress of schistosomiasis elimination in China . Determination of the compatibility of B. straminea present in southern China to S. mansoni, and the susceptibility of the cercariae released from B. straminea to definitive hosts, should be given high priority.
Although these factors may have a potential impact on the progress towards the elimination of transmission of schistosomiasis in China, we do believe the goal of schistosomiasis elimination can be achieved in China by 2020 with the strong political and financial support from the Chinese Government and enhanced multi-sector collaborations.
Yang GJ, Liu L, Zhu HR, Griffiths SM, Tanner M, Bergquist R, Utzinger J, Zhou XN: China's sustained drive to eliminate neglected tropical diseases. Lancet Infect Dis. 2014, in press
Zhou XN, Bergquist R, Leonardo L, Yang GJ, Yang K, Sudomo M, Olveda R: Schistosomiasis japonica control and research needs. Adv Parasitol. 2010, 72: 145-178.
Collins C, Xu J, Tang S: Schistosomiasis control and the health system in P.R. China. Infect Dis Poverty. 2012, 1: 8-10.1186/2049-9957-1-8.
Zhou YB, Liang S, Jiang QW: Factors impacting on progress towards elimination of transmission of schistosomiasis japonica in China. Parasit Vectors. 2012, 5: 275-10.1186/1756-3305-5-275.
Wang L, Utzinger J, Zhou XN: Schistosomiasis control: experiences and lessons from China. Lancet. 2008, 372: 1793-1795. 10.1016/S0140-6736(08)61358-6.
Hipgrave D: Communicable disease control in China: From Mao to now. J Glob Health. 2011, 1: 224-238.
Xianyi C, Liying W, Jiming C, Xiaonong Z, Jiang Z, Jiagang G, Xiaohua W, Engels D, Minggang C: Schistosomiasis control in China: the impact of a 10-year World Bank Loan Project (1992–2001). Bull World Health Organ. 2005, 83: 43-48.
Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, Chen XY, Zheng J, Utzinger J: The public health significance and control of schistosomiasis in China–then and now. Acta Trop. 2005, 96: 97-105. 10.1016/j.actatropica.2005.07.005.
Wu XH, Chen MG, Zheng J: Surveillance of schistosomiasis in five provinces of China which have reached the national criteria for elimination of the disease. Acta Trop. 2005, 96: 276-281. 10.1016/j.actatropica.2005.07.021.
Liang S, Yang C, Zhong B, Qiu D: Re-emerging schistosomiasis in hilly and mountainous areas of Sichuan, China. Bull World Health Organ. 2006, 84: 139-144. 10.2471/BLT.05.025031.
Berry-Cabán CS: Return of the God of Plague: Schistosomiasis in China. J Rural Trop Public Health. 2007, 6: 45-53.
Wang LD, Chen HG, Guo JG, Zeng XJ, Hong XL, Xiong JJ, Wu XH, Wang XH, Wang LY, Xia G, Hao Y, Chin DP, Zhou XN: A strategy to control transmission of Schistosoma japonicum in China. N Engl J Med. 2009, 360: 121-128. 10.1056/NEJMoa0800135.
Chen YY, Liu JB, Huang XB, Cai SX, Su ZM, Zhong R, Zou L, Miao XP: New integrated strategy emphasizing infection source control to curb Schistosomiasis japonica in a marshland area of Hubei Province China: findings from an eight-year longitudinal survey. PLoS One. 2014, 9: e89779-10.1371/journal.pone.0089779.
Liu R, Dong HF, Jiang MS: The new national integrated strategy emphasizing infection sources control for schistosomiasis control in China has made remarkable achievements. Parasitol Res. 2013, 112: 1483-1491. 10.1007/s00436-013-3295-5.
Hong XC, Xu XJ, Chen X, Li YS, Yu CH, Yuan Y, Chen YY, Li RD, Qiu J, Liu ZC, Yi P, Ren GH, He HB: Assessing the effect of an integrated control strategy for schistosomiasis japonica emphasizing bovines in a marshland area of Hubei Province China: a cluster randomized trial. PLoS Negl Trop Dis. 2013, 7: e2122-10.1371/journal.pntd.0002122.
Li SZ, Zheng H, Gao J, Zhang LJ, Zhu R, Xu J, Guo JG, Xiao N, Zhou XN: Endemic status of schistosomiasis in People's Republic of China in 2012. Chin J Schisto Control. 2013, 25: 557-563. In Chinese
Fan KW: Central-provincial relations for anti-schistosomiasis policy in China. Iran J Public Health. 2012, 41: 1-11.
Githeko AK, Lindsay SW, Confalonieri UE, Patz JA: Climate change and vector-borne diseases: a regional analysis. Bull World Health Organ. 2000, 78: 1136-1147.
Kilpatrick AM, Randolph SE: Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. Lancet. 2012, 380: 1946-1955. 10.1016/S0140-6736(12)61151-9.
Mas-Coma S, Valero MA, Bargues MD: Climate change effects on trematodiases, with emphasis on zoonotic fascioliasis and schistosomiasis. Vet Parasitol. 2009, 163: 264-280. 10.1016/j.vetpar.2009.03.024.
McCreesh N, Booth M: Challenges in predicting the effects of climate change on Schistosoma mansoni and Schistosoma haematobium transmission potential. Trends Parasitol. 2013, 29: 548-555. 10.1016/j.pt.2013.08.007.
Liang YS, Wang W, Li HJ, Shen XH, Xu YL, Dai JR: The South-to-North Water Diversion Project: effect of the water diversion pattern on transmission of Oncomelania hupensis, the intermediate host of Schistosoma japonicum in China. Parasit Vectors. 2012, 5: 52-10.1186/1756-3305-5-52.
Zhou XN, Yang GJ, Yang K, Wang XH, Hong QB, Sun LP, Malone JB, Kristensen TK, Bergquist NR, Utzinger J: Potential impact of climate change on schistosomiasis transmission in China. Am J Trop Med Hyg. 2008, 78: 188-194.
Yang GJ, Vounatsou P, Zhou XN, Tanner M, Utzinger J: A potential impact of climate change and water resource development on the transmission of Schistosoma japonicum in China. Parassitologia. 2005, 47: 127-134.
Doenhoff MJ, Kusel JR, Coles GC, Cioli D: Resistance of Schistosoma mansoni to praziquantel: is there a problem?. Trans R Soc Trop Med Hyg. 2002, 96: 465-469. 10.1016/S0035-9203(02)90405-0.
Couto FF, Coelho PM, Araújo N, Kusel JR, Katz N, Jannotti-Passos LK, Mattos AC: Schistosoma mansoni: a method for inducing resistance to praziquantel using infected Biomphalaria glabrata snails. Mem Inst Oswaldo Cruz. 2011, 106: 153-157. 10.1590/S0074-02762011000200006.
Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, Wynn NB, Mutuku MW, Karanja DM, Colley DG, Black CL, Secor WE, Mkoji GM, Loker ES: Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl Trop Dis. 2009, 3: e504-10.1371/journal.pntd.0000504.
Zhou YB, Zhao GM, Jiang QW: Effects of the praziquantel-based control of schistosomiasis japonica in China. Ann Trop Med Parasitol. 2007, 101: 695-703. 10.1179/136485907X241488.
Seto EY, Wong BK, Lu D, Zhong B: Human schistosomiasis resistance to praziquantel in China: should we be worried?. Am J Trop Med Hyg. 2011, 85: 74-82. 10.4269/ajtmh.2011.10-0542.
Wang W, Dai JR, Li HJ, Shen XH, Liang YS: Is there reduced susceptibility to praziquantel in Schistosoma japonicum? Evidence from China. Parasitology. 2010, 137: 1905-1912. 10.1017/S0031182010001204.
Wang W, Dai JR, Li HJ, Shen XH, Liang YS: The sensitivity of Schistosoma japonicum to praziquantel: a field evaluation in areas with low endemicity of China. Am J Trop Med Hyg. 2012, 86: 834-836. 10.4269/ajtmh.2012.11-0701.
Wang W, Wang L, Liang YS: Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitol Res. 2012, 111: 1871-1877. 10.1007/s00436-012-3151-z.
Wang W, Li HJ, Qu GL, Xing YT, Yang ZK, Dai JR, Liang YS: Is there a reduced sensitivity of dihydroartemisinin against praziquantel-resistant Schistosoma japonicum?. Parasitol Res. 2014, 113: 223-228. 10.1007/s00436-013-3647-1.
Attwood SW, Huo GN, Qiu JW: Update on the distribution and phylogenetics of Biomphalaria (Gastropoda: Planorbidae) populations in Guangdong Province, China. Acta Trop. 2014, in press
Lu P, Wang W, Dai J, Liang Y: Imported African schistosomiasis: is it an emerging public health concern in China?. J Travel Med. 2014, 21: 72-73. 10.1111/jtm.12073_1.
Wang W, Liang YS, Hong QB, Dai JR: African schistosomiasis in mainland China: risk of transmission and countermeasures to tackle the risk. Parasit Vectors. 2013, 6: 249-10.1186/1756-3305-6-249.
This work was supported by the Special Fund for Scientific Research in the Public Interest of National Health and Family Planning Commission (2015QS00077), Natural Science Foundation of Jiangsu Province (BK20141105), Jiangsu Provincial Special Fund for the Scientific Research of Clinical Medicine (BL2014021), Jiangsu Department of Health (Q201404), the Open Fund of Key Laboratory of Public Health Safety, Ministry of Education (grant no. GW2014-3), and Jiangsu Government Scholarship for Overseas Studies (grant no. JS-2012-130). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.
The authors declare that they have no competing interest.
WW prepared the first draft of the manuscript; JRD and YSL provided strategic advice and assisted the editing of the manuscript. All authors read and approved the final version of the manuscript.
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Wang, W., Dai, JR. & Liang, YS. Apropos: factors impacting on progress towards elimination of transmission of schistosomiasis japonica in China. Parasites Vectors 7, 408 (2014). https://doi.org/10.1186/1756-3305-7-408