{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,3]],"date-time":"2026-02-03T20:50:20Z","timestamp":1770151820261,"version":"3.49.0"},"reference-count":60,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2019,1,29]],"date-time":"2019-01-29T00:00:00Z","timestamp":1548720000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["TropicalMed"],"abstract":"<jats:p>Ever since the first known written report of schistosomiasis in the mid-19th century, researchers have aimed to increase knowledge of the parasites, their hosts, and the mechanisms contributing to infection and disease. This knowledge generation has been paramount for the development of improved intervention strategies. Yet, despite a broad knowledge base of direct risk factors for schistosomiasis, there remains a paucity of information related to more complex, interconnected, and often hidden drivers of transmission that hamper intervention successes and sustainability. Such complex, multidirectional, non-linear, and synergistic interdependencies are best understood by looking at the integrated system as a whole. A research approach able to address this complexity and find previously neglected causal mechanisms for transmission, which include a wide variety of influencing factors, is needed. Systems epidemiology, as a holistic research approach, can integrate knowledge from classical epidemiology, with that of biology, ecology, social sciences, and other disciplines, and link this with informal, tacit knowledge from experts and affected populations. It can help to uncover wider-reaching but difficult-to-identify processes that directly or indirectly influence exposure, infection, transmission, and disease development, as well as how these interrelate and impact one another. Drawing on systems epidemiology to address persisting disease hotspots, failed intervention programmes, and systematically neglected population groups in mass drug administration programmes and research studies, can help overcome barriers in the progress towards schistosomiasis elimination. Generating a comprehensive view of the schistosomiasis system as a whole should thus be a priority research agenda towards the strategic goal of morbidity control and transmission elimination.<\/jats:p>","DOI":"10.3390\/tropicalmed4010021","type":"journal-article","created":{"date-parts":[[2019,1,29]],"date-time":"2019-01-29T11:27:52Z","timestamp":1548761272000},"page":"21","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["A Call for Systems Epidemiology to Tackle the Complexity of Schistosomiasis, Its Control, and Its Elimination"],"prefix":"10.3390","volume":"4","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5895-5585","authenticated-orcid":false,"given":"Stefanie J.","family":"Krauth","sequence":"first","affiliation":[{"name":"Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow G12 8QQ, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4736-8465","authenticated-orcid":false,"given":"Julie","family":"Balen","sequence":"additional","affiliation":[{"name":"School of Health and Related Research, University of Sheffield, Sheffield S1 4DA, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Geoffrey N.","family":"Gobert","sequence":"additional","affiliation":[{"name":"School of Biological Sciences, Queen\u2019s University Belfast, Belfast BT9 7BL, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1048-6318","authenticated-orcid":false,"given":"Poppy H. L.","family":"Lamberton","sequence":"additional","affiliation":[{"name":"Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow G12 8QQ, UK"},{"name":"Wellcome Centre for Molecular Parasitology, University of Glasgow, Glasgow G12 8QQ, UK"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,1,29]]},"reference":[{"key":"ref_1","first-page":"53","article-title":"Ein beitrag zur helminthographia humana","volume":"4","author":"Bilharz","year":"1852","journal-title":"Z. Wiss. Zool. Abt. A"},{"key":"ref_2","first-page":"454","article-title":"Fernere mittheilungen \u00fcber Distomum haematobium","volume":"4","author":"Bilharz","year":"1852","journal-title":"Z. Wiss. Zool. Abt. A"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1136\/bmj.2.1133.503","article-title":"Remarks on injurious parasites of Egypt in relation to water-drinking","volume":"2","author":"Cobbold","year":"1882","journal-title":"Br. Med. J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1007\/BF02955707","article-title":"Zur anatomie der Bilharzia haematobia (cobbold)","volume":"31","author":"Fritsch","year":"1887","journal-title":"Arch. Mikrosk. Anat."},{"key":"ref_5","first-page":"123","article-title":"Opinions and declarations rendered by the international commission on zoological nomenclature. Opinion 147","volume":"2","author":"Hemming","year":"1943","journal-title":"Bull. Zool. Nomencl."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1016\/j.actatropica.2012.04.013","article-title":"Time to set the agenda for schistosomiasis elimination","volume":"128","author":"Rollinson","year":"2013","journal-title":"Acta Trop."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1007\/BF01928195","article-title":"Weitere beitr\u00e4ge zur pathologischen anatomie der bilharzia (Distomum haematobium, cobbold)","volume":"152","author":"Kartulis","year":"1898","journal-title":"Arch. Pathol. Anat. Physiol. Klin. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/BF02906649","article-title":"Zur anatomie und histologie der Bilharzia haematobia (cobbold)","volume":"46","author":"Looss","year":"1895","journal-title":"Arch. Mikrosk. Anat."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1080\/00034983.1934.11684813","article-title":"The transmission of human bilharziasis in Sierra Leone, with an account of the life-cycle of the schistosomes concerned, S. mansoni and S. haematobium","volume":"28","author":"Gordon","year":"1934","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"King, C.H. (2017). The evolving schistosomiasis agenda 2007\u20132017\u2014Why we are moving beyond morbidity control toward elimination of transmission. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005517"},{"key":"ref_11","first-page":"56","article-title":"The development of Schistosoma mansoni","volume":"1510","author":"Lampe","year":"1927","journal-title":"Proc. R. Soc. Med."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1136\/bmj.1.2822.201","article-title":"Observations on the spread of Asiatic schistosomiasis","volume":"1","author":"Leiper","year":"1915","journal-title":"Br. Med. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1007\/BF00368227","article-title":"Mutagenicity studies with praziquantel, a new anthelmintic drug, in mammalian systems","volume":"39","author":"Machemer","year":"1978","journal-title":"Arch. Toxicol."},{"key":"ref_14","unstructured":"World Health Organization (2013). Schistosomiasis, W. Progress Report 2001\u20132011 and Strategic Plan 2012\u20132020, World Health Organization."},{"key":"ref_15","unstructured":"World Health Organization (2012). Elimination of Schistosomiasis. 65th World Health Assembly, Resolution WHA65, World Health Organization."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"S245","DOI":"10.1093\/cid\/ciy001","article-title":"Are we on our way to achieving the 2020 goals for schistosomiasis morbidity control using current world health organization guidelines?","volume":"66","author":"Toor","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"529","DOI":"10.1186\/s13071-015-1144-3","article-title":"Modelling control of Schistosoma haematobium infection: Predictions of the long-term impact of mass drug administration in Africa","volume":"8","author":"Gurarie","year":"2015","journal-title":"Parasites Vectors"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Mitchell, K.M., Mutapi, F., Mduluza, T., Midzi, N., Savill, N.J., and Woolhouse, M.E.J. (2014). Predicted impact of mass drug administration on the development of protective immunity against Schistosoma haematobium. PLoS Negl. Tropl. Dis., 8.","DOI":"10.1371\/journal.pntd.0003059"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Comas, I., and Gagneux, S. (2009). The past and future of tuberculosis research. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000600"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"El-Sayed, A.M., and Galea, S. (2017). Systems Science and Population Health, Oxford University Press.","DOI":"10.1093\/acprof:oso\/9780190492397.001.0001"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1810","DOI":"10.4269\/ajtmh.17-0368","article-title":"Defining persistent hotspots: Areas that fail to decrease meaningfully in prevalence after multiple years of mass drug administration with praziquantel for control of schistosomiasis","volume":"97","author":"Kittur","year":"2017","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.vetpar.2004.09.018","article-title":"Waterborne zoonotic helminthiases","volume":"126","author":"Nithiuthai","year":"2004","journal-title":"Vet. Parasitol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Sturmberg, J.P. (2016). The Value of Systems and Complexity Sciences for Healthcare, Springer Publishing.","DOI":"10.1007\/978-3-319-26221-5"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1071\/NB07028","article-title":"Seeing obesity as a systems problem","volume":"18","author":"Newell","year":"2008","journal-title":"N. S. W. Public Health Bull."},{"key":"ref_25","unstructured":"Epstein, P.R., and Ferber, D. (2011). Changing Planet, Changing Health: How the Climate Crisis Threatens Our Health and What We Can Do about It, University of California Press."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1742-7622-9-1","article-title":"Causal diagrams in systems epidemiology","volume":"9","author":"Joffe","year":"2012","journal-title":"Emerg. Themes Epidemiol."},{"key":"ref_27","unstructured":"Bar-Yam, Y. (2002). General Features of Complex Systems, Encyclopedia of Life Support Systems (EOLSS), UNESCO, EOLSS Publishers."},{"key":"ref_28","unstructured":"Shift cvba (2018, December 06). Shift Obesity System Influence Diagram. Available online: http:\/\/www.shiftn.com\/obesity\/Full-Map.html."},{"key":"ref_29","first-page":"A82","article-title":"A systems-oriented multilevel framework for addressing obesity in the 21st century","volume":"6","author":"Huang","year":"2009","journal-title":"Prev. Chronic Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/1478-4505-12-50","article-title":"Advancing the application of systems thinking in health","volume":"12","author":"Adam","year":"2014","journal-title":"Health Res. Policy Syst."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1186\/1478-4505-12-47","article-title":"Advancing the application of systems thinking in health: Understanding the growing complexity governing immunization services in Kerala, India","volume":"12","author":"Varghese","year":"2014","journal-title":"Health Res. Policy Syst."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1007\/s13668-013-0052-4","article-title":"Systems epidemiology: A new direction in nutrition and metabolic disease research","volume":"2","author":"Cornelis","year":"2013","journal-title":"Curr. Nutr. Rep."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1089\/omi.2011.0108","article-title":"Diving through the \u201c-omics\u201d: The case for deep phenotyping and systems epidemiology","volume":"16","author":"Haring","year":"2012","journal-title":"OMICS"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2954","DOI":"10.1158\/1055-9965.EPI-08-0519","article-title":"Systems epidemiology in cancer","volume":"17","author":"Lund","year":"2008","journal-title":"Cancer Epidemiol. Biomarkers Prev."},{"key":"ref_35","unstructured":"Israelian, N. (2018, December 06). A brief history of neglected tropical diseases. Available online: http:\/\/www.immpressmagazine.com\/a-brief-history-of-neglected-tropical-diseases\/."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Gurarie, D., Lo, N.C., Ndeffo-Mbah, M.L., Durham, D.P., and King, C.H. (2018). The human-snail transmission environment shapes long term schistosomiasis control outcomes: Implications for improving the accuracy of predictive modeling. PLoS Negl. Trop. Dis., 12.","DOI":"10.1371\/journal.pntd.0006514"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"20130434","DOI":"10.1098\/rstb.2013.0434","article-title":"The contribution of mass drug administration to global health: Past, present and future","volume":"369","author":"Webster","year":"2014","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"ref_38","first-page":"1151","article-title":"Reduced efficacy of praziquantel against Schistosoma mansoni is associated with multiple rounds of mass drug administration","volume":"63","author":"Crellen","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"E64","DOI":"10.1016\/S1473-3099(16)30535-7","article-title":"A call to strengthen the global strategy against schistosomiasis and soil-transmitted helminthiasis: The time is now","volume":"17","author":"Lo","year":"2017","journal-title":"Lancet Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"S116","DOI":"10.1017\/S0021932016000171","article-title":"Deworming delusions? Mass drug administration in east African schools","volume":"48","author":"Allen","year":"2016","journal-title":"J. Biosoc. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Sokolow, S.H., Wood, C.L., Jones, I.J., Swartz, S.J., Lopez, M., Hsieh, M.H., Lafferty, K.D., Kuris, A.M., Rickards, C., and De Leo, G.A. (2016). Global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best. PLoS Negl. Trop. Dis., 10.","DOI":"10.1371\/journal.pntd.0004794"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1093\/cid\/civ829","article-title":"Profiling nonrecipients of mass drug administration for schistosomiasis and hookworm infections: A comprehensive analysis of praziquantel and albendazole coverage in community-directed treatment in Uganda","volume":"62","author":"Chami","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.epidem.2017.02.002","article-title":"Measuring and modelling the effects of systematic non-adherence to mass drug administration","volume":"18","author":"Dyson","year":"2017","journal-title":"Epidemics"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"S16","DOI":"10.1017\/S0021932016000018","article-title":"Rumours, riots and the rejection of mass drug administration for the treatment of schistosomiasis in Morogoro, Tanzania","volume":"48","author":"Hastings","year":"2016","journal-title":"J. Biosoc. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"S56","DOI":"10.1017\/S0021932016000067","article-title":"Community co-designed schistosomiasis control interventions for school-aged children in Zanzibar","volume":"48","author":"Person","year":"2016","journal-title":"J. Biosoc. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Riccardi, N., Nosenzo, F., Peraldo, F., Sarocchi, F., Taramasso, L., Traverso, P., Viscoli, C., Di Biagio, A., Derchi, L.E., and De Maria, A. (2017). Increasing prevalence of genitourinary schistosomiasis in Europe in the migrant era: Neglected no more?. PLoS Negl. Trop. Dis., 11.","DOI":"10.1371\/journal.pntd.0005237"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/s13071-016-1311-1","article-title":"Compliance with anthelmintic treatment in the neglected tropical diseases control programmes: A systematic review","volume":"9","author":"Shuford","year":"2016","journal-title":"Parasites Vectors."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Knopp, S., Mohammed, K.A., Ali, S.M., Khamis, I.S., Ame, S.M., Albonico, M., Gouvras, A., Fenwick, A., Savioli, L., and Colley, D.G. (2012). Study and implementation of urogenital schistosomiasis elimination in Zanzibar (Unguja and Pemba islands) using an integrated multidisciplinary approach. BMC Public Health, 12.","DOI":"10.1186\/1471-2458-12-930"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Lee, Y.H., Jeong, H.G., Kong, W.H., Lee, S.H., Cho, H.I., Nam, H.S., Ismail, H.A.H.A., Alla, G.N.A., Oh, C.H., and Hong, S.T. (2015). Reduction of urogenital schistosomiasis with an integrated control project in Sudan. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0003423"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e145","DOI":"10.2196\/resprot.9166","article-title":"An integrated approach to control soil-transmitted helminthiasis, schistosomiasis, intestinal protozoa infection, and diarrhea: Protocol for a cluster randomized trial","volume":"7","author":"Raso","year":"2018","journal-title":"JMIR Res. Protoc."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Tian-Bi, Y.N.T., Ouattara, M., Knopp, S., Coulibaly, J.T., Hurlimann, E., Webster, B., Allan, F., Rollinson, D., Meite, A., and Diakite, N.R. (2018). Interrupting seasonal transmission of Schistosoma haematobium and control of soil-transmitted helminthiasis in northern and central C\u00f4te d\u2019Iivoire: A score study protocol. BMC Public Health, 18.","DOI":"10.1186\/s12889-018-5044-2"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1016\/j.actatropica.2013.11.028","article-title":"Integrated control programmes for schistosomiasis and other helminth infections in P.R. China","volume":"141","author":"Xu","year":"2015","journal-title":"Acta Trop."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/bs.apar.2016.02.004","article-title":"Integrated control strategy of schistosomiasis in the People\u2019s Republic of China: Projects involving agriculture, water conservancy, forestry, sanitation and environmental modification","volume":"92","author":"Yang","year":"2016","journal-title":"Adv. Parasitol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1016\/j.ijid.2016.09.023","article-title":"A new global strategy for the elimination of schistosomiasis","volume":"54","author":"Ross","year":"2017","journal-title":"Int. J. Infect. Dis."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/S1090-5138(98)00018-X","article-title":"The evolution of conformist transmission and the emergence of between-group differences","volume":"19","author":"Henrich","year":"1998","journal-title":"Evol. Hum. Behav."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1111\/j.1467-9280.2007.01917.x","article-title":"The constructive, destructive, and reconstructive power of social norms","volume":"18","author":"Schultz","year":"2007","journal-title":"Psychol. Sci."},{"key":"ref_57","unstructured":"Sherif, M. (1936). The Psychology of Social Norms, Harper and Brothers Publishing."},{"key":"ref_58","doi-asserted-by":"crossref","unstructured":"Giles, C.L., and Gori, M. (1998). Learning dynamic Bayesian networks. Adaptive Processing of Sequences and DATA Structures, Springer.","DOI":"10.1007\/BFb0053992"},{"key":"ref_59","unstructured":"Ventana Systems Inc. (2015). Vensim, Ventana Systems Inc."},{"key":"ref_60","unstructured":"(2019, January 29). GIMP.org. Available online: https:\/\/www.gimp.org\/."}],"container-title":["Tropical Medicine and Infectious Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2414-6366\/4\/1\/21\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:29:19Z","timestamp":1760185759000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2414-6366\/4\/1\/21"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,1,29]]},"references-count":60,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,3]]}},"alternative-id":["tropicalmed4010021"],"URL":"https:\/\/doi.org\/10.3390\/tropicalmed4010021","relation":{},"ISSN":["2414-6366"],"issn-type":[{"value":"2414-6366","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,1,29]]}}}