Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T05:04:19.285Z Has data issue: false hasContentIssue false
  • English
  • Français

Schistosomiasis then and now: what has changed in the last 100 years?

Published online by Cambridge University Press:  22 January 2020

R. Alan Wilson Open the ORCID record for R. Alan Wilson [Opens in a new window]
R. Alan Wilson*
Affiliation:
Centre for Immunology and Infection, Department of Biology, University of York, YorkYO10 5DD, UK
*
Author for correspondence: R. Alan Wilson, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Only with the completion of the life cycles of Fasciola hepatica in 1883 and 30 years later those of Schistosoma japonicum (1913), Schistosoma haematobium and Schistosoma mansoni (1915) did research on schistosomiasis really get underway. One of the first papers by Cawston in 1918, describing attempts to establish the means of transmission of S. haematobium in Natal, South Africa, forms the historical perspective against which to judge where we are now. Molecular biology techniques have produced a much better definition of the complexity of the schistosome species and their snail hosts, but also revealed the extent of hybridization between human and animal schistosomes that may impact on parasite adaptability. While diagnostics have greatly improved, the ability to detect single worm pair infections routinely, still falls short of its goal. The introduction of praziquantel ~1982 has revolutionized the treatment of infected individuals and led directly to the mass drug administration programmes. In turn, the severe pathological consequences of high worm burdens have been minimized, and for S. haematobium infections the incidence of associated squamous cell carcinoma has been reduced. In comparison, the development of effective vaccines has yet to come to fruition. The elimination of schistosomiasis japonica from Japan shows what is possible, using multiple lines of approach, but the clear and present danger is that the whole edifice of schistosome control is balanced on the monotherapy of praziquantel, and the development of drug resistance could topple that.

Keywords

Bladder cancerchemotherapydiagnosiseliminationmass drug administrationmolluscan hostpathogenesispathologySchistosome speciesvaccine
Type
Review Article
Information
Parasitology , Volume 147 , Issue 5 , April 2020 , pp. 507 - 515
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adema, CM, Hillier, LW, Jones, CS, Loker, ES, Knight, M, Minx, P, Oliveira, G, Raghavan, N, Shedlock, A, do Amaral, LR, Arican-Goktas, HD, Assis, JG, Baba, EH, Baron, OL, Bayne, CJ, Bickham-Wright, U, Biggar, KK, Blouin, M, Bonning, BC, Botka, C, Bridger, JM, Buckley, KM, Buddenborg, SK, Lima Caldeira, R, Carleton, J, Carvalho, OS, Castillo, MG, Chalmers, IW, Christensens, M, Clifton, S, Cosseau, C, Coustau, C, Cripps, RM, Cuesta-Astroz, Y, Cummins, SF, di Stephano, L, Dinguirard, N, Duval, D, Emrich, S, Feschotte, C, Feyereisen, R, FitzGerald, P, Fronick, C, Fulton, L, Galinier, R, Gava, SG, Geusz, M, Geyer, KK, Giraldo-Calderon, GI, de Souza Gomes, M, Gordy, MA, Gourbal, B, Grunau, C, Hanington, PC, Hoffmann, KF, Hughes, D, Humphries, J, Jackson, DJ, Jannotti-Passos, LK, de Jesus Jeremias, W, Jobling, S, Kamel, B, Kapusta, A, Kaur, S, Koene, JM, Kohn, AB, Lawson, D, Lawton, SP, Liang, D, Limpanont, Y, Liu, S, Lockyer, AE, Lovato, TL, Ludolf, F, Magrini, V, McManus, DP, Medina, M, Misra, M, Mitta, G, Mkoji, GM, Montague, MJ, Montelongo, C, Moroz, LL, Munoz-Torres, MC, Niazi, U, Noble, LR, Oliveira, FS, Pais, FS, Papenfuss, AT, Peace, R, Pena, JJ, Pila, EA, Quelais, T, Raney, BJ, Rast, JP, Rollinson, D, Rosse, IC, Rotgans, B, Routledge, EJ, Ryan, KM, Scholte, LLS, Storey, KB, Swain, M, Tennessen, JA, Tomlinson, C, Trujillo, DL, Volpi, EV, Walker, AJ, Wang, T, Wannaporn, I, Warren, WC, Wu, XJ, Yoshino, TP, Yusuf, M, Zhang, SM, Zhao, M and Wilson, RK (2017) Whole genome analysis of a schistosomiasis-transmitting freshwater snail. Nature Communications 8, 15451.CrossRefGoogle ScholarPubMed
Andrade, ZA (2009) Schistosomiasis and liver fibrosis. Parasite Immunology 31, 656–663.CrossRefGoogle ScholarPubMed
Ashton, PD, Harrop, R, Shah, B and Wilson, RA (2001) The schistosome egg: development and secretions. Parasitology 122, 329–338.CrossRefGoogle ScholarPubMed
Boissier, J, Grech-Angelini, S, Webster, BL, Allienne, JF, Huyse, T, Mas-Coma, S, Toulza, E, Barre-Cardi, H, Rollinson, D, Kincaid-Smith, J, Oleaga, A, Galinier, R, Foata, J, Rognon, A, Berry, A, Mouahid, G, Henneron, R, Mone, H, Noel, H and Mitta, G (2016) Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. Lancet Infectious Diseases 16, 971–979.CrossRefGoogle ScholarPubMed
Brand, KG (1979) Schistosomiasis − cancer: etiological considerations. A review. Acta Tropica 36, 203–214.Google ScholarPubMed
Caldeira, RL, Teodoro, TM, Jannotti-Passos, LK, Lira-Moreira, PM, Goveia, CO and Carvalho, OD (2016) Characterization of South American snails of the genus Biomphalaria (Basommatophora: Planorbidae) and Schistosoma mansoni (Platyhelminthes: Trematoda) in molluscs by PCR-RFLP. Biomedical Research International 2016, 1045391.CrossRefGoogle ScholarPubMed
Cawston, FG (1915) Bilharziosis in Natal. British Medical Journal 2, 746.CrossRefGoogle ScholarPubMed
Cawston, FG (1918) Bilharziasis in Natal. Parasitology 11, 83–93.CrossRefGoogle Scholar
Cheever, AW, Torky, AH and Shirbiney, M (1975) The relation of worm burden to passage of Schistosoma haematobium eggs in the urine of infected patients. American Journal of Tropical Medicine and Hygiene 24, 284–288.CrossRefGoogle ScholarPubMed
Cheever, AW, Kamel, IA, Elwi, AM, Mosimann, JE and Danner, R (1977) Schistosoma mansoni and S. haematobium infections in Egypt. II. Quantitative parasitological findings at necropsy. American Journal of Tropical Medicine and Hygiene 26, 702–716.CrossRefGoogle ScholarPubMed
Cheever, AW, Kamel, IA, Elwi, AM, Mosimann, JE, Danner, R and Sippel, JE (1978) Schistosoma mansoni and S. haematobium infections in Egypt. III. Extrahepatic pathology. American Journal of Tropical Medicine and Hygiene 27, 55–75.CrossRefGoogle ScholarPubMed
Christinet, V, Lazdins-Helds, JK, Stothard, JR and Reinhard-Rupp, J (2016) Female genital schistosomiasis (FGS): from case reports to a call for concerted action against this neglected gynaecological disease. International Journal for Parasitology 46, 395–404.CrossRefGoogle ScholarPubMed
Cioli, D, Pica-Mattoccia, L and Archer, S (1995) Antischistosomal drugs: past, present … and future? Pharmacology and Therapeutics 68, 35–85.CrossRefGoogle Scholar
Colley, DG (2014) Morbidity control of schistosomiasis by mass drug administration: How can we do it best and what will it take to move on to elimination? Tropical Medicine and Health 42, 25–32.CrossRefGoogle Scholar
Colley, DG, Andros, TS and Campbell, CH Jr (2017) Schistosomiasis is more prevalent than previously thought: what does it mean for public health goals, policies, strategies, guidelines and intervention programs? Infectious Diseases of Poverty 6, 63.CrossRefGoogle ScholarPubMed
Corstjens, PL, De Dood, CJ, Kornelis, D, Fat, EM, Wilson, RA, Kariuki, TM, Nyakundi, RK, Loverde, PT, Abrams, WR, Tanke, HJ, Van Lieshout, L, Deelder, AM and Van Dam, GJ (2014) Tools for diagnosis, monitoring and screening of Schistosoma infections utilizing lateral-flow based assays and upconverting phosphor labels. Parasitology 141, 1841–1855.CrossRefGoogle ScholarPubMed
Costain, AH, MacDonald, AS and Smits, HH (2018) Schistosome egg migration: mechanisms, pathogenesis and host immune responses. Frontiers in Immunology 9, 3042.CrossRefGoogle ScholarPubMed
Coutinho, A and Barreto, FT (1969) Treatment of hepatosplenic schistosomiasis mansoni with niridazole: relationships among liver function, effective dose, and side effects. Annals of the New York Academy of Sciences 160, 612–628.CrossRefGoogle ScholarPubMed
Crosnier, C, Brandt, C, Rinaldi, G, McCarthy, C, Barker, C, Clare, S, Berriman, M and Wright, GJ (2019) Systematic screening of 96 Schistosoma mansoni cell-surface and secreted antigens does not identify any strongly protective vaccine candidates in a mouse model of infection. Wellcome Open Research 4, 159.CrossRefGoogle ScholarPubMed
Doenhoff, MJ, Pearson, S, Dunne, DW, Bickle, Q, Lucas, S, Bain, J, Musallam, R and Hassounah, O (1981) Immunological control of hepatotoxicity and parasite egg excretion in Schistosoma mansoni infections: stage specificity of the reactivity of immune serum in T-cell deprived mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 41–53.CrossRefGoogle ScholarPubMed
Douglas, AD, Baldeviano, GC, Lucas, CM, Lugo-Roman, LA, Crosnier, C, Bartholdson, SJ, Diouf, A, Miura, K, Lambert, LE, Ventocilla, JA, Leiva, KP, Milne, KH, Illingworth, JJ, Spencer, AJ, Hjerrild, KA, Alanine, DG, Turner, AV, Moorhead, JT, Edgel, KA, Wu, Y, Long, CA, Wright, GJ, Lescano, AG and Draper, SJ (2015) A PfRH5-based vaccine is efficacious against heterologous strain blood-stage Plasmodium falciparum infection in aotus monkeys. Cell Host & Microbe 17, 130–139.CrossRefGoogle ScholarPubMed
Fallon, PG and Doenhoff, MJ (1994) Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. American Journal of Tropical Medicine and Hygiene 51, 83–88.CrossRefGoogle ScholarPubMed
Farah, IO, Mola, PW, Kariuki, TM, Nyindo, M, Blanton, RE and King, CL (2000) Repeated exposure induces periportal fibrosis in Schistosoma mansoni-infected baboons: role of TGF-beta and IL-4. Journal of Immunology 164, 5337–5343.CrossRefGoogle ScholarPubMed
Fenwick, A and Jourdan, P (2016) Schistosomiasis elimination by 2020 or 2030? International Journal for Parasitology 46, 385–388.CrossRefGoogle ScholarPubMed
Fenwick, A, Rollinson, D and Southgate, V (2006) Implementation of human schistosomiasis control: challenges and prospects. Advances in Parasitology 61, 567–622.CrossRefGoogle ScholarPubMed
Groah, SL, Weitzenkamp, DA, Lammertse, DP, Whiteneck, GG, Lezotte, DC and Hamman, RF (2002) Excess risk of bladder cancer in spinal cord injury: evidence for an association between indwelling catheter use and bladder cancer. Archives of Physical Medicine and Rehabilitation 83, 346–351.CrossRefGoogle ScholarPubMed
Guan, W, Li, SZ, Abe, EM, Webster, BL, Rollinson, D and Zhou, XN (2016) The genetic diversity and geographical separation study of Oncomelania hupensis populations in mainland China using microsatellite loci. Parasites and Vectors 9, 28.CrossRefGoogle ScholarPubMed
Hewitson, JP and Maizels, RM (2014) Vaccination against helminth parasite infections. Expert Review of Vaccines 13, 473–487.CrossRefGoogle ScholarPubMed
Hotez, PJ, Bottazzi, ME, Bethony, J and Diemert, DD (2019) Advancing the development of a human schistosomiasis vaccine. Trends in Parasitology 35, 104–108.CrossRefGoogle ScholarPubMed
Ishida, K and Hsieh, MH (2018) Understanding urogenital schistosomiasis-related bladder cancer: an update. Frontiers in Medicine 5, 223.CrossRefGoogle ScholarPubMed
Kane, RA, Stothard, JR, Emery, AM and Rollinson, D (2008) Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes? Parasites and Vectors 1, 15.CrossRefGoogle ScholarPubMed
Karanja, DM, Colley, DG, Nahlen, BL, Ouma, JH and Secor, WE (1997) Studies on schistosomiasis in western Kenya: i. Evidence for immune-facilitated excretion of schistosome eggs from patients with Schistosoma mansoni and human immunodeficiency virus coinfections. American Journal of Tropical Medicine and Hygiene 56, 515–521.CrossRefGoogle ScholarPubMed
Kariuki, TM, Farah, IO, Wilson, RA and Coulson, PS (2008) Antibodies elicited by the secretions from Schistosome cercariae and eggs are predominantly against glycan epitopes. Parasite Immunology 30, 554–562.CrossRefGoogle ScholarPubMed
Katsurada, F (1904) Determination of the cause of a new parasite disease seen in Yamanashi and other prefectures [in Japanese]. [Tokyo Iji Shinshi] Tokyo Medical Journal 1371, 13–32.Google Scholar
Katz, N, Chaves, A and Pellegrino, J (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de São Paulo 14, 397–400.Google ScholarPubMed
Kaur, I, Schramm, G, Everts, B, Scholzen, T, Kindle, KB, Beetz, C, Montiel-Duarte, C, Blindow, S, Jones, AT, Haas, H, Stolnik, S, Heery, DM and Falcone, FH (2011) Interleukin-4-inducing principle from Schistosoma mansoni eggs contains a functional C-terminal nuclear localization signal necessary for nuclear translocation in mammalian cells but not for its uptake. Infection and Immunity 79, 1779–1788.CrossRefGoogle Scholar
Kayuni, SA, Corstjens, P, LaCourse, EJ, Bartlett, KE, Fawcett, J, Shaw, A, Makaula, P, Lampiao, F, Juziwelo, L, de Dood, CJ, Hoekstra, PT, Verweij, JJ, Leutscher, PDC, van Dam, GJ, van Lieshout, L and Stothard, JR (2019) How can schistosome circulating antigen assays be best applied for diagnosing male genital schistosomiasis (MGS): an appraisal using exemplar MGS cases from a longitudinal cohort study among fishermen on the south shoreline of Lake Malawi. Parasitology 146, 1785–1795.CrossRefGoogle ScholarPubMed
Kelley, JM, Elliott, TP, Beddoe, T, Anderson, G, Skuce, P and Spithill, TW (2016) Current threat of triclabendazole resistance in Fasciola hepatica. Trends in Parasitology 32, 458–469.CrossRefGoogle ScholarPubMed
King, CH, Dickman, K and Tisch, DJ (2005) Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365, 1561–1569.CrossRefGoogle ScholarPubMed
Kittur, N, Castleman, JD, Campbell, CH, King, CH and Colley, DG (2016) Comparison of Schistosoma mansoni prevalence and intensity of infection, as determined by the circulating cathodic antigen urine assay or by the Kato-Katz fecal assay: a systematic review. American Journal of Tropical Medicine and Hygiene 94, 605–610.CrossRefGoogle ScholarPubMed
Kjetland, EF, Leutscher, PD and Ndhlovu, PD (2012) A review of female genital schistosomiasis. Trends in Parasitology 28, 58–65.CrossRefGoogle ScholarPubMed
Knopp, S, Corstjens, PL, Koukounari, A, Cercamondi, CI, Ame, SM, Ali, SM, de Dood, CJ, Mohammed, KA, Utzinger, J, Rollinson, D and van Dam, GJ (2015) Sensitivity and specificity of a urine circulating anodic antigen test for the diagnosis of Schistosoma haematobium in low endemic settings. PLOS Neglected Tropical Diseases 9, e0003752.CrossRefGoogle Scholar
Le, L and Hsieh, MH (2017) Diagnosing urogenital schistosomiasis: dealing with diminishing returns. Trends in Parasitology 33, 378–387.CrossRefGoogle ScholarPubMed
Leger, E and Webster, JP (2017) Hybridizations within the genus Schistosoma: implications for evolution, epidemiology and control. Parasitology 144, 65–80.CrossRefGoogle ScholarPubMed
Leiper, RT (1915) Report on the results of the Bilharzia mission in Egypt, 1915. Journal of the Royal Army Medical Corps 25, 1–48.Google Scholar
Leiper, RT (1916) On the relation between the terminal-spined and lateral-spined eggs of bilharzia. British Medical Journal 1, 411.CrossRefGoogle ScholarPubMed
Leiper, RT and Atkinson, EL (1915) Observations on the spread of Asiatic schistosomiasis. British Medical Journal 1, 201–192 204.CrossRefGoogle ScholarPubMed
Lewis, SA (2000) Everything you wanted to know about the bladder epithelium but were afraid to ask. American Journal of Physiology-Renal Physiology 278, F867–F874.CrossRefGoogle Scholar
Li, XH, Xu, YX, Vance, G, Wang, Y, Lv, LB, van Dam, GJ, Cao, JP and Wilson, RA (2015) Evidence that rhesus macaques self-cure from a Schistosoma japonicum infection by disrupting worm esophageal function: a new route to an effective vaccine? PLOS Neglected Tropical Diseases 9, e0003925.CrossRefGoogle Scholar
Li, XH, Kondrashin, A, Greenwood, B, Lindblade, K, Loku Galappaththy, G and Alonso, P (2019) A historical review of WHO certification of malaria elimination. Trends in Parasitology 35, 163–171.CrossRefGoogle ScholarPubMed
Looss, A (1909) Bilharziosis of women and girls in Egypt in the light of the “Skin-Infection Theory”. British Medical Journal 1, 773–777.CrossRefGoogle Scholar
Mandahl-Barth, G (1965) The species of the genus Bulinus, intermediate hosts of Schistosoma. Bulletin of the World Health Organisation 33, 33–44.Google Scholar
Mathieson, W and Wilson, RA (2010) A comparative proteomic study of the undeveloped and developed Schistosoma mansoni egg and its contents: the miracidium, hatch fluid and secretions. International Journal for Parasitology 40, 617–628.CrossRefGoogle ScholarPubMed
Mitta, G, Gourbal, B, Grunau, C, Knight, M, Bridger, JM and Theron, A (2017) The compatibility between Biomphalaria glabrata snails and Schistosoma mansoni: an increasingly complex puzzle. Advances in Parasitology 97, 111–145.CrossRefGoogle ScholarPubMed
Miyagawa, Y (1912) Route of migration of Schistosoma japonicum from the skin to the portal vein, and morphology of the young worm at the time of penetrating the skin [in Japanese]. Tokyo Medical Journal 26, 3–4.Google Scholar
Miyairi, K and Suzuki, M (1913) On the development of Schistosoma japonicum. [Tokyo Iji Shinshi] the Tokyo Medical Journal] 1836, 1961–1965.Google Scholar
Nacif-Pimenta, R, da Silva Orfano, A, Mosley, IA, Karinshak, SE, Ishida, K, Mann, VH, Coelho, PMZ, da Costa, JMC, Hsieh, MH, Brindley, PJ and Rinaldi, G (2019) Differential responses of epithelial cells from urinary and biliary tract to eggs of Schistosoma haematobium and S. mansoni. Science Reports 9, 10731.CrossRefGoogle ScholarPubMed
Ogongo, P, Kariuki, TM and Wilson, RA (2018) Diagnosis of Schistosomiasis mansoni: an evaluation of existing methods and research towards single worm pair detection. Parasitology 145, 1355–1366.CrossRefGoogle ScholarPubMed
Panic, G and Keiser, J (2018) Acting beyond 2020: better characterization of praziquantel and promising antischistosomal leads. Current Opinion in Pharmacology 42, 27–33.CrossRefGoogle ScholarPubMed
Pennington, LF, Alouffi, A, Mbanefo, EC, Ray, D, Heery, DM, Jardetzky, TS, Hsieh, MH and Falcone, FH (2017) H-IPSE is a pathogen-secreted host nucleus-infiltrating protein (Infiltrin) expressed exclusively by the Schistosoma haematobium egg stage. Infection and Immunity 85, e00301-17.CrossRefGoogle ScholarPubMed
Picquet, M, Ernould, JC, Vercruysse, J, Southgate, VR, Mbaye, A, Sambou, B, Niang, M and Rollinson, D (1996) The epidemiology of human schistosomiasis in the Senegal river basin. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 340–346.CrossRefGoogle ScholarPubMed
Pila, EA, Li, H, Hambrook, JR, Wu, X and Hanington, PC (2017) Schistosomiasis from a snail's perspective: advances in snail immunity. Trends in Parasitology 33, 845–857.CrossRefGoogle ScholarPubMed
Riveau, G, Schacht, AM, Dompnier, JP, Deplanque, D, Seck, M, Waucquier, N, Senghor, S, Delcroix-Genete, D, Hermann, E, Idris-Khodja, N, Levy-Marchal, C, Capron, M and Capron, A (2018) Safety and efficacy of the rSh28GST urinary schistosomiasis vaccine: a phase 3 randomized, controlled trial in Senegalese children. PLOS Neglected Tropical Diseases 12, e0006968.CrossRefGoogle ScholarPubMed
Rollinson, D, Knopp, S, Levitz, S, Stothard, JR, Tchuem Tchuente, LA, Garba, A, Mohammed, KA, Schur, N, Person, B, Colley, DG and Utzinger, J (2013) Time to set the agenda for schistosomiasis elimination. Acta Tropica 128, 423–440.CrossRefGoogle ScholarPubMed
Salem, S, Mitchell, RE, El-Alim El-Dorey, A, Smith, JA and Barocas, DA (2011) Successful control of schistosomiasis and the changing epidemiology of bladder cancer in Egypt. BJU International 107, 206–211.CrossRefGoogle ScholarPubMed
Scott, JA (1937) The incidence and distribution of the human schistosomes in Egypt. American Journal of Hygiene 25, 566–614.Google Scholar
Secor, WE and Colley, DG (2018) When should the emphasis on schistosomiasis control move to elimination? Tropical Medicine and Infectious Disease 3. Article number 85.CrossRefGoogle Scholar
Shen, J, Lai, DH, Wilson, RA, Chen, YF, Wang, LF, Yu, ZL, Li, MY, He, P, Hide, G, Sun, X, Yang, TB, Wu, ZD, Ayala, FJ and Lun, ZR (2017) Nitric oxide blocks the development of the human parasite Schistosoma japonicum. Proceedings of the National Academy of Sciences USA 114, 10214–10219.CrossRefGoogle ScholarPubMed
Skelly, PJ and Wilson, RA (2006) Making sense of the schistosome surface. Advances in Parasitology 63, 185–284.CrossRefGoogle ScholarPubMed
Stelma, FF, Talla, I, Sow, S, Kongs, A, Niang, M, Polman, K, Deelder, AM and Gryseels, B (1995) Efficacy and side effects of praziquantel in an epidemic focus of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 53, 167–170.CrossRefGoogle Scholar
Symmers, WSC (1904) Note on a new form of liver cirrhosis due to the presence of the ova of Bilharzia haematobia. Journal of Pathology and Bacteriology 9, 237–239.CrossRefGoogle Scholar
Tanaka, H and Tsuji, M (1997) From discovery to eradication of schistosomiasis in Japan: 1847−1996. International Journal for Parasitology 27, 1465–1480.CrossRefGoogle ScholarPubMed
Taylor, AB, Roberts, KM, Cao, X, Clark, NE, Holloway, SP, Donati, E, Polcaro, CM, Pica-Mattoccia, L, Tarpley, RS, McHardy, SF, Cioli, D, LoVerde, PT, Fitzpatrick, PF and Hart, PJ (2017) Structural and enzymatic insights into species-specific resistance to schistosome parasite drug therapy. Journal of Biological Chemistry 292, 11154–11164.CrossRefGoogle ScholarPubMed
Thomas, AP (1883) The life history of the liver-fluke (Fasciola hepatica). Quarterly Journal of Microscopical Science 23, 90–133.Google Scholar
Tricker, AR, Mostafa, MH, Spiegelhalder, B and Preussmann, R (1989) Urinary excretion of nitrate, nitrite and N-nitroso compounds in Schistosomiasis and bilharzia bladder cancer patients. Carcinogenesis 10, 547–552.CrossRefGoogle ScholarPubMed
Turner, GA (1909) Bilharziosis in South Africa. Parasitology 1, 195–217.CrossRefGoogle Scholar
von Lichtenberg, F (1987) Consequences of infections with schistosomes. In Rollinson, D and Simpson, AJG (eds), The Biology of Schistosomes: From Genes to Latrines. London: Academic Press, pp. 185–232.Google Scholar
Wang, T, Wyeth, RC, Liang, D, Bose, U, Ni, G, McManus, DP and Cummins, SF (2019) A Biomphalaria glabrata peptide that stimulates significant behaviour modifications in aquatic free-living Schistosoma mansoni miracidia. PLOS Neglected Tropical Diseases 13, e0006948.CrossRefGoogle ScholarPubMed
Webster, BL, Diaw, OT, Seye, MM, Webster, JP and Rollinson, D (2013) Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLOS Neglected Tropical Diseases 7, e2110.CrossRefGoogle ScholarPubMed
Webster, BL, Alharbi, MH, Kayuni, S, Makaula, P, Halstead, F, Christiansen, R, Juziwelo, L, Stanton, MC, LaCourse, EJ, Rollinson, D, Kalua, K and Stothard, JR (2019) Schistosome interactions within the Schistosoma haematobium group, Malawi. Emerging Infectious Diseases 25, 1245–1247.CrossRefGoogle ScholarPubMed
Weerakoon, KG, Gobert, GN, Cai, P and McManus, DP (2015) Advances in the diagnosis of human schistosomiasis. Clinical Microbiology Reviews 28, 939–967.CrossRefGoogle Scholar
Wilson, RA (2012) Proteomics at the schistosome-mammalian host interface: any prospects for diagnostics or vaccines? Parasitology 139, 1178–1194.CrossRefGoogle ScholarPubMed
Wilson, RA and Coulson, PS (2009) Immune effector mechanisms against schistosomiasis: looking for a chink in the parasite's armour. Trends in Parasitology 25, 423–431.CrossRefGoogle ScholarPubMed
Wilson, RA, van Dam, GJ, Kariuki, TM, Farah, IO, Deelder, AM and Coulson, PS (2006) The detection limits for estimates of infection intensity in schistosomiasis mansoni established by a study in non-human primates. International Journal for Parasitology 36, 1241–1244.CrossRefGoogle Scholar
Wilson, RA, Langermans, JA, van Dam, GJ, Vervenne, RA, Hall, SL, Borges, WC, Dillon, GP, Thomas, AW and Coulson, PS (2008) Elimination of Schistosoma mansoni adult worms by rhesus macaques: basis for a therapeutic vaccine? PLOS Neglected Tropical Diseases 2, e290.CrossRefGoogle ScholarPubMed
World_Health_Organisation (2018) Schistosomiasis and soil transmitted helminthiases: numbers of people treated in 2017. Weekly Epidemiological Record 93, 681–692.Google Scholar
Yang, YYM, Wilson, RA, Thomas, SRL, Kariuki, TM, van Diepen, A and Hokke, CH (2019) Micro array-assisted analysis of anti-schistosome glycan antibodies elicited by protective vaccination with irradiated cercariae. Journal of Infectious Diseases 219, 1671–1680.CrossRefGoogle ScholarPubMed
Zhang, SM, Bu, L, Laidemitt, MR, Lu, L, Mutuku, MW, Mkoji, GM and Loker, ES (2018) Complete mitochondrial and rDNA complex sequences of important vector species of Biomphalaria, obligatory hosts of the human-infecting blood fluke. Schistosoma mansoni. Science Reports 8, 7341.Google ScholarPubMed