Impact evaluation of schistosomiasis control into elimination interventions models in P. R. China and Africa

Objective: Evidence-based and innovative approaches aiming to reduce or eliminate the local and global burden of schistosomiasis are urgently needed. Local elimination has proved difficult and requires vigorous political and financial commitment for prolonged long-term benefits. Yet, available literature provides limited evidence on the impact and effectiveness of different local and national schistosomiasis programs and community interventions models. Integrated schistosomiasis control interventions models in P.R. China have provided hopes that elimination can be achievable goal both endemic areas in China and African countries, where most vulnerable children population lives. Methods: The paper overviewed to what extent and impact of various implemented models and programs, and provides an understanding of the robustness of schistosomiasis control towards elimination interventions in endemic communities in P.R. China and African countries. Results: It provides vital evidence to galvanize governments and global stakeholders in upholding cost-effective interventions models and research innovations in guiding sustainable decision-making policies and priorities towards achieving global schistosomiasis elimination in China and Africa. Conclusion: Successful Chinese lessons learnt and experiences from varied schistosomiasis models integration and policies practice holds immense promise when transfer and apply within an integrated trans-disciplinary and intersectorial sectors schistosomiasis approaches in ending schistosomiasis endemicity and epidemics episodes in both P.R. China and African countries. Furthermore ensuring community engagement and participation, health education and resilience towards community projects ownership are essential in sustained national schistosomiasis elimination programmes and eventual eradication benefits. J Microbiol Infect Dis 2017; 7(2): 104-118

___

  • 1. World Health Organization. First WHO report on neglected tropical diseases: working to overcome the global impact of neglected tropical diseases. Geneva: WHO Press; 2010.
  • 2. World Health Organization (WHO), 2015 Schistosomiasis: Key facts. http://www.who.int/mediacentre/factsheets/fs115/e n/ accessed, 15th December 2015
  • 3. Xu J, Bergquist R, Qian YJ, et al. China-Africa and China-Asia Collaboration on Schistosomiasis Control: A SWOT Analysis. Adv Parasitol 2016; 92:435-66.
  • 4. Tambo E, Khater EI, Chen JH, Bergquist R, Zhou XN. Nobel prize for the artemisinin and ivermectin discoveries: a great boost towards elimination of the global infectious diseases of poverty. Infect Dis Poverty 2015; 28;4:58.
  • 5. Collins C, Xu J, Tang S: Schistosomiasis control and the health system in China. Inf Dis Poverty 2012, 1 (1):7.
  • 6. Bergquist R, Tanner M: Controlling schistosomiasis in South-East Asia: a tale of two countries. Adv Parasitol 2010, 72:109–144.
  • 7. WHO: Accelerating work to overcome the global impact of neglected tropical diseases-a roadmap for implementation. Geneva: WHO Press; 2012.
  • 8. Savioli L, Fenwick A, Rollinson D, Albonico M, Ame SM. An achievable goal: control and elimination of schistosomiasis. Lancet 2015 22; 386 (9995):739.
  • 9. Krauth SJ, Greter H, Stete K, et al. All that is blood is not schistosomiasis: experiences with reagent strip testing for urogenital schistosomiasis with special consideration to very-low prevalence settings. Parasit Vectors 2015; 8:584.
  • 10. Anderson R, Hollingsworth TD, Truscott J, Brooker S: Optimisation of mass chemotherapy to control soil-transmitted helminth infection. Lancet 2012, 379 (9813):289–290.
  • 11. Sacko M, Magnussen P, Keita AD, Traore MS, Landoure A, et al. Impact of Schistosoma haematobium infection on urinary tract pathology, nutritional status and anaemia in school-aged children in two different endemic areas of the Niger River Basin, Mali. Acta Trop 2011; 120 Suppl 1:S142-50
  • 12. Bergquist R, Whittaker M: Strengthening control of neglected tropical diseases in the Asia Pacific region: implications for health information priorities. Inf Dis Poverty 2012, 1(1):4.
  • 13. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Tropica 2000; 77:41-51.
  • 14. Utzinger J, Bergquist R, Olveda R, Zhou XN: Important helminth infections in South-East Asia diversity, potential for control and prospects for elimination. Adv Parasitol 2010, 72:1-30.
  • 15. Brooker S, Hotez PJ, Bundy DAP: The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PloS Negl Trop Dis 2010, 4:e779.
  • 16. Donald P. McManus and Alex Loukas: Current Status of Vaccines for Schistosomiasis. Clin Microbiol Rev 2008, 21 (1):225.
  • 17. Doumenge JP et al. Atlas of the global distribution of schistosomiasis. Geneva: World Health Organization; 1987.
  • 18. Hotez PJ, Ehrenberg JP: Escalating the global fight against neglected tropical diseases through interventions in the Asia Pacific region. Adv Parasitol 2010, 72:31–53.
  • 19. Bergquist R, Utzinger J, McManus DP Trick or treat: the role of vaccine in integrated schistosomiasis control. PLoS Negl Trop Dis 2008; 2: e244. doi:10.1371/journal.pntd.0000244
  • 20. Mo AX, Colley DG. Workshop report: Schistosomiasis vaccine clinical development and product characteristics. Vaccine 2015 Dec 22. pii: S0264-410X(15)01823-X.
  • 21. Driguez P, McManus DP, Gobert GN. Clinical implications of recent findings in schistosome proteomics. Expert Rev Proteomics 2016; 13(1):19-33.
  • 22. Gurarie D, Yoon N, Li E, et al. Modelling control of Schistosoma haematobium infection: predictions of the long-term impact of mass drug administration in Africa. Parasit Vectors 2015 22;8:529.
  • 23. Da’Dara AA, Li YS, Xiong T, et al. DNA-based vaccine protects against zoonotic schistosomiasis in water buffalo. Vaccine 2008; 26: 3617–3625
  • 24. Williams GM, Sleigh AC, Li YS, et al. Mathematical modelling of schistosomiasis japonica: comparison of control strategies in the Peoples’ Republic of China. Acta Trop 2002; 82: 253-262.
  • 25. Wang LD, Chen HG, Guo, JG, et al. A strategy to control transmission of Schistosoma japonicum in China. N Eng J Med 2009; 360: 121-128
  • 26. Liu ZC, He HB, Wang ZX, et al. Effect of marshland isolation and grazing prohibition on schistosomiasis control in Dongting Lake region [in Chinese]. Chin J Schisto Control 2010; 22: 459-463.
  • 27. Zeng QR, Hou JW, He YK, et al. Analyses on morbidity and chemotherapy effects of Schistosoma japonicum infection in fishermen on Dongting Lake. Chin J Parasitol Parasit Dis 2004; 22:199-203.
  • 28. Zhou J, Huang CY, He YK, et al. Epidemiological evaluation of schistosomiasis in migrant fishermen in Dongting Lake region. Chin J Schisto Control 2010; 22: 464-467.
  • 29. McCreesh N, Nikulin G, Booth M. Predicting the effects of climate change on Schistosoma mansoni transmission in eastern Africa. Parasit Vectors. 2015; 8:4.
  • 30. Xu J, Yu Q, Tchuenté LA, et al. Enhancing collaboration between China and African countries for schistosomiasis control. Lancet Infect Dis 2016; 16 (3):376-83.
  • 31. Stothard JR, Campbell SJ, Osei-Atweneboana MY, et al. Towards interruption of schistosomiasis transmission in sub-Saharan Africa: developing an appropriate environmental surveillance framework to guide and to support 'end game' interventions. Infect Dis Poverty 2017; 6 (1):10.
  • 32. Hürlimann E, Schur N, Boutsika K, et al. Toward an open-access global database for mapping, control, and surveillance of neglected tropical diseases. PLoS Negl Trop Dis 2011, 5(12):e1404.
  • 33. Clements ACA, Firth S, Dembelé R, et al. Use of Bayesian geostatistical prediction to estimate local variations in Schistosoma haematobium infection in western Africa. Bull World Health Organ 2009, 87:921-929.
  • 34. Sun LP, Liang YS, Wu HH, et al. A Google Earthbased surveillance system for schistosomiasis japonica implemented in the lower reaches of the Yangtze River, China. Parasit Vectors 2011, 4:223.
  • 35. Fenwick A, Webster JP, Bosque-Oliva E, et al. The Schistosomiasis Control Initiative (SCI): rationale, development and implementation from 2002-2008. Parasitology 2009, 136:1719-1730.
  • 36. McManus DP, Gray DJ, Li YS, et al. Schistosomiasis in the Peoples’ Republic of China: the era of the Three Gorges Dam. Clin Microbiol Rev 2010; 23: 442-466.
  • 37. Gray DJ, Williams GM, Li YS, et al. A clusterrandomised intervention trial against S. japonicum in the Peoples’ Republic of China: bovine and human transmission. PLoS One 2009; 4: e5900.
  • 38. Da’Dara AA, Li YS, Xiong T, Zhou J, et al. DNAbased vaccine protects against zoonotic schistosomiasis in water buffalo. Vaccine 2008; 26: 3617–3625.
  • 39. Tambo E, Ugwu CE, Guan Y, Wei D, Xiao-Ning, Xiao-Nong Z. China-Africa Health Development Initiatives: Benefits and Implications for Shaping Innovative and Evidence-informed National Health Policies and Programs in Sub-saharan African Countries. Int J MCH AIDS 2016; 5 (2):119-133.
  • 40. Katz N, Chavez A, Pellegrino J. A simple device for quantitative stool thicksmear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 1972; 14: 397-400.
  • 41. Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L. Guidelines for the evaluation of soiltransmitted helminthiasis and schistosomiasis at community level. A guide for managers of control programmes. Geneva: World Health Organization. 1998 pp 1-45.
  • 42. Hou XY, McManus DP, Gray DJ, et al. A randomised, double-blind, placebo-controlled trial on the safety and efficacy of combined praziquantel and artemether treatment for acute Schistosomiasis japonica in China. Bull World Hlth Org 200886: 788-795.
  • 43. Yuan LP, Manderson L, Tempongko MS, Wei W, Aiguo P. The impact of educational videotapes on water contact behaviour of primary school students in the Dongting Lakes region, China. Trop Med Int Health 2000; 5: 538–544.
  • 44. Dessein A, Chevillard C, Arnaud V, et al. Variants of CTGF are associated with hepatic fibrosis in Chinese, Sudanese and Brazilians infected with schistosomes. J Exp Med 2009; 206: 2321-2328.
  • 45. Massenet D, Toukour A, Kamwa Ngassam RI, Djao R, Portal JL, Tchuem Tchuente LA. Changes in the distribution of human schistosomiasis in far North Province, Cameroon, since 1986. Annals of Trop Medicin Parasit 2011; 105: 325-328
  • 46. Saotoing P, Vroumsia T, Njan AM, Tchuenguem FN, Messi J. Epidemiological survey of schistosomiasis due to Schistosoma haematobium in some primary schools in the town of Maroua, far north region Cameroon. International Journal of Tropical Medicine 2011; 6: 19-24
  • 47. Njiokou F, Yimta Tsemo LC, Kuete T, Same Ekobo A. Dynamics of intestinal schistosomiasis in Cameroon: evolution of transmission in the mixed zone of Nkolmebanga, Lekie. Medecine Tropicale 2004; 64: 351-354
  • 48. Mao CP. A review of the epidemiology of schistosomiasis japonica in China. Am J Trop Med 1948; 28: 659-672.
  • 49. Chen XY, Wang LY, Cai JM, et al. Schistosomiasis control in China: the impact of a 10-year World Bank Loan Project (1992– 2001). Bull World Health Organ 2005; 83: 43-48.
  • 50. Yuan HC, Jiagang G, Bergquist R, et al. The 1992- 1999 World Bank schistosomiasis research initiative in China: outcome and prospectives. Parasitol Int 2000; 49: 195-207.
  • 51. Li YS, Sleigh AC, Tanner M, et al. Five-year impact of repeated praziquantel chemotherapy on sub-clinical morbidity due to Schistosoma japonicum in China. Trans Roy Soc Trop Med Hyg 2002; 96: 438-443.
  • 52. Ross AG, Sleight AC, Li YS, McManus DP. Schistosomiasis in the People’s Republic of China: prospects and challenges for the 21st century. Clin Microbiol Rev 2001; 14: 270-295.
  • 53. Zhou XN, Wang LY, Chen MG, et al. The publichealth significance and control of schistosomiasis in China-then and now. Acta Trop 2005; 96: 97-105.
  • 54. Zhou XN, Gou JG, Wu XH, et al. Epidemiology of schistosomiasis in the People’s Republic of China, 2004. Emerg Infect Dis 2007; 13: 1470–1476.
  • 55. Wang LD, Zhou XN. Schistosomiasis control: experience and lessons from China. Lancet 2008; 372: 1793–1795.
  • 56. McManus DP, Li YS, Gary D, Ross AG. Conquering ‘snail fever’: schistosomiasis and its control in China. Expert Rev Anti Infect Ther 2009; 7: 473–485.
  • 57. McManus DP, Gray D, Li YS, et al. Schistosomiasis in the People’s Republic of China: the era of the Three Gorges Dam. Clin Microbiol Rev 2010; 23: 442-466.
  • 58. Li YS, Sleigh AC, Ross AGP, et al. Epidemiology of Schistosoma japonicum in China: morbidity and strategies for control in the Dongting Lake region. Int J Parasitol 2000; 30: 273–281.
  • 59. Li YS, Raso G, Zhao ZY, et al. The impact of large water management projects on schistosomiasis transmission and control in the Dongting Lake region, China. Emerg Infect Dis 2007; 13: 973– 979.
  • 60. Li YS, Sleigh AC, Ross AGP, et al. Two year impact of praziquantel for Schistosoma japonicum infection in China: re-infection, subclinical disease and fibrosis marker measurements. Trans Roy Soc Trop Med Hyg 2000; 94: 191–197.
  • 61. Sandbach FR. Farewell to the god of plague - the control of schistosomiasis in China. Soc Sci Med 1977; 11: 27–33.
  • 62. Zheng J. Achievements and challenges in schistosomiasis control in China. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2009;27: 398-401.
  • 63. Raso G, Li YS, Zhao Z, et al. Spatial distribution of human Schistosoma japonicum infections in the Dongting Lake Region, China. PLoS ONE 2009; 4: e6947. doi:10.1371/journal.pone.0006947.
  • 64. Johansen MV, Bøgh HO, Nansen P, Christensen NO. Schistosoma japonicum infection in the pig as a model for human schistosomiasis japonica. Acta Trop 2000; 76: 85–99.
  • 65. Gray DJ, Williams GM, Li YS, et al. A cluster randomised intervention trial against Schistosoma japonicum in the Peoples’ Republic of China: bovine and human transmission. PLoS One 2009; 4: e5900. doi:10.1371/journal.pone.0005900.
  • 66. Joanne P. Webster, Charlotte M. Gower, Alice J. Norton: Evolutionary concepts in predicting and evaluating the impact of mass chemotherapy schistosomiasis control programmes on parasites and their hosts. Evolutionary Applications J 2008 1(1).
  • 67. Yi-biao Zhou, Hui-min Zheng and Qing-wu Jiang: A diagnostic challenge for schistosomiasis japonica in China: consequences on praziquantelbased morbidity control. Parasites & Vectors 2011, 4:194.
  • 68. Enk MJ, Oliveira e Silva G, Rodrigues NB Diagnostic Accuracy and Applicability of a PCR System for the Detection of Schistosoma mansoni DNA in Human Urine Samples from an Endemic Area. PLoS One 2012; 7(6): e38947.
  • 69. Guo JG, Li YS, Gray DJ, et al. A drug-based intervention study on the importance of buffaloes for human Schistosoma japonicum infection around Poyang Lake, Peoples’ Republic of China. Am J Trop Med Hyg 2006; 74: 335–341.
  • 70. Galappaththi-Arachchige HN, Amlie Hegertun IE, Holmen S, et al. Association of Urogenital Symptoms with History of Water Contact in Young Women in Areas Endemic for S. haematobium. A Cross-Sectional Study in Rural South Africa. Int J Environ Res Public Health. 2016;13 (11). pii: E1135.
  • 71. Cai KP, Zuo JZ, He HB, Zhuo SJ. Impact of changes in mud siltation of Dongting Lake on the endemic factors of schistosomiasis after building the Three Gorges Dam. Pract Prevent Med 2000; 7: 1–3.
  • 72. Zhou XN, Bergquist R, Leonardo L, et al. Schistosomiasis japonica control and research needs. Adv Parasitol 2010; 72: 145-178.
  • 73. Zhu HM, Xiang S, Yang K, Wu XH, Zhou XN. Three Gorges Dam and its impact on the potential transmission of schistosomiasis in regions along the Yangtze River. Ecohealth 2008; 5: 137–148.
  • 74. Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006; 368: 1106– 1118.
  • 75. Li YS, Chen D, Ross AG, Zhou J, Burke ML, et al. Severe hepatosplenic schistosomiasis: clinicopathological study of 102 cases undergoing splenectomy. Hum Pathol 2011; 42: 111–119.
  • 76. Dai JR, Wang W, Liang YS, et al. A novel molluscicidal formulation of niclosamide. Parasitol Res 2008; 103: 405–412.
  • 77. Yuan LP, Manderson L, Tempongko MS, Wei W, Aiguo P. The impact of educational videotapes on water contact behaviour of primary school students I the Dongting Lakes region, China. Trop Med Int Hlth 2000; 5: 538–544.
  • 78. Yuan LP, Manderson L, Ren MY, et al. Schoolbased interventions to enhance knowledge and improve case management on schistosomiasis: a case study from Hunan, China. Acta Trop 2005; 96: 248-254.
  • 79. Kosinski KC, Kulinkina AV, Tybor D, Osabutey D, Bosompem KM, Naumova EN. Agreement among Four Prevalence Metrics for Urogenital Schistosomiasis in the Eastern Region of Ghana. Biomed Res Int 2016; 2016:7627358.
  • 80. Kariuki HC, Ivy JA, Muchiri EM, Sutherland LJ, King CH. Divergent Effects of Schistosoma haematobium Exposure on Intermediate-Host Snail Species Bulinus nasutus and Bulinus globosus from Coastal Kenya. Am J Trop Med Hyg 2017; 96 (4):850-855.
  • 81. Arnaud V, Fu X, Wang Y, et al. Cytokines in severe hepatic central and peripheral fibrosis in humans infected with Schistosoma japonicum: IL- 10 and IFN-c likely play crucial regulatory roles. J Infect Dis 2008; 198: 418-426.
  • 82. Ross AG, Li YS, Sleigh AC, et al. Epidemiological features of Schistosoma japonicum among fishermen and other occupational groups in the Dongting Lake Region (Hunan Province) of China. Am J Trop Med Hyg 1997; 57: 302–308.
  • 83. Bergquist R, Johansen MV, Utzinger J. Diagnostic dilemmas in helminthology: what tools to use and when? Trends Parasitol 2009; 25: 151–156.
  • 84. Ellis MK, Li YS, Hou XY, Chen HG, McManus DP. sTNFR-II and sICAM-1 are associated with acute disease and hepatic inflammation in schistosomiasis japonica. Int J Parasitol 2008; 38: 717-723.
  • 85. Hou XY, Ellis M, McManus, DP, et al. Diagnostic value of non-invasive biomarkers for stagespecific diagnosis of hepatic fibrosis in patients with advanced schistosomiasis japonica. Int J Parasitol 2011; 41: 325-332.
  • 86. Bustinduy AL, Friedman JF, Kjetland EF, et al. Expanding Praziquantel (PZQ) Access beyond Mass Drug Administration Programs: Paving a Way Forward for a Pediatric PZQ Formulation for Schistosomiasis. PLoS Negl Trop Dis 2016 22; 10(9):e0004946.
  • 87. Hsiang MS, Carlton EJ, Zhang Y, et al. Use of ultrasonography to evaluate Schistosoma japonicum-related morbidity in children, Sichuan Province, China, 2000-2007. Am J Trop Med Hyg 2010; 82: 103-111.
  • 88. Li YS, Kardorff R, Richter J, et al. Ultrasound organometry: the importance of body-height adjusted normal ranges in assessing liver and spleen parameters among Chinese subjects with Schistosoma japonicum infection. Acta Trop 2004; 92: 133-138.
  • 89. Chiavaroli R, Grima P, Grima P. Detection of early liver fibrosis in patients with intestinal schistosomiasis: sonographic and histologic findings in Schistosoma mansoni infection. Infection 36: 585-589.
  • 90. Okosun KO, Smith R. Optimal control analysis of malaria-schistosomiasis co-infection dynamics. Math Biosci Eng 2017; 14(2):377-405
  • 91. Xiao SH. Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Trop 2005; 96:153-167.
  • 92. Utzinger J, Xiao SH, Tanner M, Keiser J. Artemisinins for schistosomiasis and beyond. Curr Opin Investig Drugs 2007; 8: 105-116.
  • 93. Li YS, Chen HG, He HB, et al. A double-blind field trial on the effects of artemether on Schistosoma japonicum infection in a highly endemic focus in southern China. Acta Trop 2005; 96:184-190.
  • 94. Hou XY, McManus DP, Gray DJ, et al. A randomized, double blind, placebo-controlled trial of safety and efficacy of combined praziquantel and artemether treatment for acute schistosomiasis japonica in China. Bull World Hlth Org 2008; 86: 788-795.
  • 95. Gray DJ, McManus DP, Li Y, Williams GM, Bergquist R, Ross AG. Schistosomiasis elimination: lessons from the past guide the future. Lancet Infect Dis 2010; 10: 733-736.
  • 96. Balen J, McManus DP, Li Y, et al. Comparison of two approaches for measuring household wealth via an asset-based index in rural and peri-urban settings of Hunan province, People’s Republic of China. Emerg Themes Epi 2010; 7: 7
  • 97. Mutapi F, Maizels R, Fenwick A, Woolhouse M. Human schistosomiasis in the post mass drug administration era. Lancet Infect Dis 2017; 17 (2):e42-e48.
  • 98. Lo NC, Addiss DG, Hotez PJ, et al. A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: the time is now. Lancet Infect Dis. 2017; 17 (2):e64-e69.
  • 99.Tambo E, Ugwu CE, Guan Y, Wei D, Ning X, XiaoNong X. China-Africa Health Development Initiatives: Benefits and Implications for Shaping Innovative and Evidence-informed National Health Policies and Programs in Sub-saharan African Countries. Int J MCH AIDS 2016; 5(2): 119-133.
  • 100. Adeline P. Mewabo, Roger S. et al. Assessing the prevalence of urogenital schistosomaisis and transmission risk factors amongst school-aged children around Mapé dam ecological suburbs in Malantouen district, Cameroon. Infect Dis Povert 2017 6:40.
  • 101. Tchuenté LT, Rollinson D, Stothard JR, Molyneux D. Moving from control to elimination of schistosomiasis in sub-Saharan Africa: time to change and adapt strategies. Infect Diseases of Povert 2017 6:42.
  • 102. Stothard JR, Campbell SJ, Osei-Atweneboana MY, et al. Towards interruption of schistosomiasis transmission in sub-Saharan Africa: developing an appropriate environmental surveillance framework to guide and to support ‘end game’ interventions. Infect Dis Povert 2017 6:10.
  • 103.Hotez PJ, Pecoul B, Rijal S, et al. Eliminating the Neglected Tropical Diseases: Translat Scienc New Technol. PLoS Negl Trop Dis 2016; 10(3): e0003895.