BACKGROUND: Schistosoma mansoni was introduced from Africa to the Americas during the transatlantic slave trade and remains a major public health problem in parts of South America and the Caribbean. This study presents a comprehensive comparative analysis of three S. mansoni strains with different geographical origins-from Liberia, Belo Horizonte and Puerto Rico. We demonstrated significant variation in virulence and host-parasite interactions. METHODS: We investigated the phenotypic characteristics of the parasite and its eggs, as well as the immunopathologic effects on laboratory mouse organ systems. RESULTS: Our results show significant differences in worm morphology, worm burden, egg size, and pathologic organ changes between these strains. The Puerto Rican strain showed the highest virulence, as evidenced by marked liver and spleen changes and advanced liver fibrosis indicated by increased collagen content. In contrast, the strains from Liberia and Belo Horizonte had a less pathogenic profile with less liver fibrosis. We found further variations in granuloma formation, cytokine expression and T-cell dynamics, indicating different immune responses. CONCLUSION: Our study emphasizes the importance of considering intra-specific variations of S. mansoni for the development of targeted therapies and public health strategies. The different virulence patterns, host immune responses and organ pathologies observed in these strains provide important insights for future research and could inform region-specific interventions for schistosomiasis control.

Biomedizinisches Forschungszentrum Seltersberg Justus Liebig University Giessen Giessen Germany

Department of Ecology Center of Infectious Animal Diseases Faculty of Environmental Sciences Czech University of Life Sciences Czechia Institute of Parasitology Prague Czechia

Division of Tropical Medicine and Infectious Diseases Center of Internal Medicine 2 Rostock University Medical Center Germany

Institute of Organic Chemistry and Biochemistry Czech Academy of Sciences Prague Czechia

Zobrazit více v PubMed

Lo NC, Bezerra FSM, Colley DG, Fleming FM, Homeida M, Kabatereine N, et al.. Review of 2022 WHO guidelines on the control and elimination of schistosomiasis. Lancet Infect Dis. 2022;22(11):e327–e35. Epub 2022/05/21. doi: 10.1016/S1473-3099(22)00221-3 . PubMed DOI

McManus DP, Dunne DW, Sacko M, Utzinger J, Vennervald BJ, Zhou XN. Schistosomiasis. Nat Rev Dis Primers. 2018;4(1):13. Epub 2018/08/11. doi: 10.1038/s41572-018-0013-8 . PubMed DOI

Nation CS, Da’dara AA, Marchant JK, Skelly PJ. Schistosome migration in the definitive host. PLoS Negl Trop Dis. 2020;14(4):e0007951. Epub 2020/04/03. doi: 10.1371/journal.pntd.0007951 ; PubMed Central PMCID: PMC7117656. PubMed DOI PMC

Lu DB, Yu QF, Zhang JY, Sun MT, Gu MM, Webster JP, et al.. Extended survival and reproductive potential of single-sex male and female Schistosoma japonicum within definitive hosts. Int J Parasitol. 2021;51(11):887–91. Epub 2021/04/28. doi: 10.1016/j.ijpara.2021.03.005 . PubMed DOI

Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383(9936):2253–64. Epub 2014/04/05. doi: 10.1016/S0140-6736(13)61949-2 ; PubMed Central PMCID: PMC4672382. PubMed DOI PMC

Schwartz C, Fallon PG. Schistosoma "Eggs-Iting" the Host: Granuloma Formation and Egg Excretion. Front Immunol. 2018;9:2492. Epub 2018/11/22. doi: 10.3389/fimmu.2018.02492 ; PubMed Central PMCID: PMC6232930. PubMed DOI PMC

Yeh YT, Skinner DE, Criado-Hidalgo E, Chen NS, Garcia-De Herreros A, El-Sakkary N, et al.. Biomechanical interactions of Schistosoma mansoni eggs with vascular endothelial cells facilitate egg extravasation. PLoS Pathog. 2022;18(3):e1010309. Epub 2022/03/23. doi: 10.1371/journal.ppat.1010309 ; PubMed Central PMCID: PMC8939816. PubMed DOI PMC

Cheever AW, Macedonia JG, Mosimann JE, Cheever EA. Kinetics of egg production and egg excretion by Schistosoma mansoni and S. japonicum in mice infected with a single pair of worms. Am J Trop Med Hyg. 1994;50(3):281–95. Epub 1994/03/01. doi: 10.4269/ajtmh.1994.50.281 . PubMed DOI

Stavitsky AB. Regulation of granulomatous inflammation in experimental models of schistosomiasis. Infect Immun. 2004;72(1):1–12. Epub 2003/12/23. doi: 10.1128/IAI.72.1.1-12.2004 ; PubMed Central PMCID: PMC343951. PubMed DOI PMC

Lundy SK, Lukacs NW. Chronic schistosome infection leads to modulation of granuloma formation and systemic immune suppression. Front Immunol. 2013;4:39. Epub 2013/02/23. doi: 10.3389/fimmu.2013.00039 ; PubMed Central PMCID: PMC3576626. PubMed DOI PMC

Stensgaard AS, Vounatsou P, Sengupta ME, Utzinger J. Schistosomes, snails and climate change: Current trends and future expectations. Acta Trop. 2019;190:257–68. Epub 2018/09/28. doi: 10.1016/j.actatropica.2018.09.013 . PubMed DOI

Boissier J, Grech-Angelini S, Webster BL, Allienne JF, Huyse T, Mas-Coma S, et al.. Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. Lancet Infect Dis. 2016;16(8):971–9. Epub 2016/05/21. doi: 10.1016/S1473-3099(16)00175-4 . PubMed DOI

Cioli D, Pica-Mattoccia L, Basso A, Guidi A. Schistosomiasis control: praziquantel forever? Mol Biochem Parasitol. 2014;195(1):23–9. Epub 2014/06/24. doi: 10.1016/j.molbiopara.2014.06.002 . PubMed DOI

Grimes JE, Croll D, Harrison WE, Utzinger J, Freeman MC, Templeton MR. The relationship between water, sanitation and schistosomiasis: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2014;8(12):e3296. Epub 2014/12/05. doi: 10.1371/journal.pntd.0003296 ; PubMed Central PMCID: PMC4256273. PubMed DOI PMC

Deol AK, Fleming FM, Calvo-Urbano B, Walker M, Bucumi V, Gnandou I, et al.. Schistosomiasis—Assessing Progress toward the 2020 and 2025 Global Goals. N Engl J Med. 2019;381(26):2519–28. Epub 2019/12/28. doi: 10.1056/NEJMoa1812165 ; PubMed Central PMCID: PMC6785807. PubMed DOI PMC

Caldwell N, Afshar R, Baragana B, Bustinduy AL, Caffrey CR, Collins JJ, et al.. Perspective on Schistosomiasis Drug Discovery: Highlights from a Schistosomiasis Drug Discovery Workshop at Wellcome Collection, London, September 2022. ACS Infect Dis. 2023;9(5):1046–55. Epub 2023/04/21. doi: 10.1021/acsinfecdis.3c00081 ; PubMed Central PMCID: PMC10186373. PubMed DOI PMC

Fallon PG, Tao LF, Ismail MM, Bennett JL. Schistosome resistance to praziquantel: Fact or artifact? Parasitol Today. 1996;12(8):316–20. Epub 1996/08/01. doi: 10.1016/0169-4758(96)10029-6 . PubMed DOI

Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368(9541):1106–18. Epub 2006/09/26. doi: 10.1016/S0140-6736(06)69440-3 . PubMed DOI

Doenhoff MJ, Cioli D, Utzinger J. Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis. 2008;21(6):659–67. Epub 2008/11/04. doi: 10.1097/QCO.0b013e328318978f . PubMed DOI

Files VS. A study of the vector-parasite relationships in Schistosoma mansoni. Parasitology. 1951;41(3–4):264–9. Epub 1951/12/01. doi: 10.1017/s0031182000084092 . PubMed DOI

Morgan JA, Dejong RJ, Snyder SD, Mkoji GM, Loker ES. Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology. 2001;123 Suppl:S211–28. Epub 2002/01/05. doi: 10.1017/s0031182001007703 . PubMed DOI

Platt RN 2nd, Le Clec’h W, Chevalier FD, McDew-White M, LoVerde PT, Ramiro de Assis R, et al.. Genomic analysis of a parasite invasion: Colonization of the Americas by the blood fluke Schistosoma mansoni. Mol Ecol. 2022;31(8):2242–63. Epub 2022/02/14. doi: 10.1111/mec.16395 ; PubMed Central PMCID: PMC9305930. PubMed DOI PMC

Campbell G, Jones CS, Lockyer AE, Hughes S, Brown D, Noble LR, et al.. Molecular evidence supports an african affinity of the neotropical freshwater gastropod, Biomphalaria glabrata, say 1818, an intermediate host for Schistosoma mansoni. Proc Biol Sci. 2000;267(1460):2351–8. Epub 2001/01/02. doi: 10.1098/rspb.2000.1291 ; PubMed Central PMCID: PMC1690836. PubMed DOI PMC

https://iris.who.int/bitstream/handle/10665/351856/9789240041608-eng.pdf?sequence=1

World Health Organization. Schistosomiasis: number of people treated worldwide in 2013. Wkly Epidemiol Rec. 2015;90(5):25–32. PubMed

Le TH, Blair D, McManus DP. Mitochondrial DNA sequences of human schistosomes: the current status. Int J Parasitol. 2000;30(3):283–90. Epub 2000/03/17. doi: 10.1016/s0020-7519(99)00204-0 . PubMed DOI

Saoud MF. The infectivity and pathogenicity of geographical strains of Schistosoma mansoni. Trans R Soc Trop Med Hyg. 1966;60(5):585–600. Epub 1966/01/01. doi: 10.1016/0035-9203(66)90004-6 . PubMed DOI

Warren KS. A comparison of Puerto Rican, Brazilian, Egyptian and Tanzanian strains of Schistosoma mansoni in mice: penetration of cercariae, maturation of schistosomes and production of liver disease. Trans R Soc Trop Med Hyg. 1967;61(6):795–802. Epub 1967/01/01. doi: 10.1016/0035-9203(67)90037-5 . PubMed DOI

Nino Incani R, Morales G, Cesari IM. Parasite and vertebrate host genetic heterogeneity determine the outcome of infection by Schistosoma mansoni. Parasitol Res. 2001;87(2):131–7. Epub 2001/02/24. doi: 10.1007/pl00008565 . PubMed DOI

Kassim OO, Cheever AW, Richards CS. Schistosoma mansoni: mice infected with different worm strains. Exp Parasitol. 1979;48(2):220–4. Epub 1979/10/01. doi: 10.1016/0014-4894(79)90102-4 PubMed DOI

Anderson LA, Cheever AW. Comparison of geographical strains of Schistosoma mansoni in the mouse. Bull World Health Organ. 1972;46(2):233–42. Epub 1972/01/01. ; PubMed Central PMCID: PMC2480698. PubMed PMC

Higgins-Opitz SB, Dettman CD. The infection characteristics of a South African isolate of Schistosoma mansoni: a comparison with a Puerto Rican isolate in BALB/c mice and Mastomys coucha. Parasitol Res. 1991;77(2):142–51. Epub 1991/01/01. doi: 10.1007/BF00935428 . PubMed DOI

Thiongo FW, Madsen H, Ouma JH, Andreassen J, Christensen NO. Host-parasite relationships in infections with two Kenyan isolates of Schistosoma mansoni in NMRI mice. J Parasitol. 1997;83(2):330–2. Epub 1997/04/01. . PubMed

Morgan JA, Dejong RJ, Adeoye GO, Ansa ED, Barbosa CS, Bremond P, et al.. Origin and diversification of the human parasite Schistosoma mansoni. Mol Ecol. 2005;14(12):3889–902. Epub 2005/10/06. doi: 10.1111/j.1365-294X.2005.02709.x . PubMed DOI

Rollinson D, Kaukas A, Johnston DA, Simpson AJ, Tanaka M. Some molecular insights into schistosome evolution. Int J Parasitol. 1997;27(1):11–28. Epub 1997/01/01. doi: 10.1016/s0020-7519(96)00169-5 . PubMed DOI

Blanton RE. Population Structure and Dynamics of Helminthic Infection: Schistosomiasis. Microbiol Spectr. 2019;7(4). Epub 2019/07/22. doi: 10.1128/microbiolspec.AME-0009-2019 ; PubMed Central PMCID: PMC6650164. PubMed DOI PMC

Pinto-Almeida A, Mendes T, de Oliveira RN, Correa Sde A, Allegretti SM, Belo S, et al.. Morphological Characteristics of Schistosoma mansoni PZQ-Resistant and -Susceptible Strains Are Different in Presence of Praziquantel. Front Microbiol. 2016;7:594. Epub 2016/05/21. doi: 10.3389/fmicb.2016.00594 ; PubMed Central PMCID: PMC4844704. PubMed DOI PMC

Sombetzki M, Fuchs CD, Fickert P, Osterreicher CH, Mueller M, Claudel T, et al.. 24-nor-ursodeoxycholic acid ameliorates inflammatory response and liver fibrosis in a murine model of hepatic schistosomiasis. J Hepatol. 2015;62(4):871–8. Epub 2014/12/03. doi: 10.1016/j.jhep.2014.11.020 ; PubMed Central PMCID: PMC4368108. PubMed DOI PMC

Tucker MS, Karunaratne LB, Lewis FA, Freitas TC, Liang YS. Schistosomiasis. Curr Protoc Immunol. 2013;103:19 1 1–1 58. Epub 2014/02/11. doi: 10.1002/0471142735.im1901s103 . PubMed DOI

Winkelmann F, Frank M, Rabes A, Koslowski N, Schulz C, Bischofsberger M, et al.. Human serum activates the tegument of female schistosomes and supports recovery from Praziquantel. Parasitol Res. 2021;120(1):209–21. Epub 2020/12/03. doi: 10.1007/s00436-020-06968-x ; PubMed Central PMCID: PMC7846515. PubMed DOI PMC

Leontovyc A, Ulrychova L, Horn M, Dvorak J. Collection of Excretory/Secretory Products from Individual Developmental Stages of the Blood Fluke Schistosoma mansoni. Methods Mol Biol. 2020;2151:55–63. Epub 2020/05/27. doi: 10.1007/978-1-0716-0635-3_5 . PubMed DOI

Nelson GS, Saoud MF. A comparison of the pathogenicity of two geographical strains of Schistosoma mansoni in rhesus monkeys. J Helminthol. 1968;42(3):339–62. Epub 1968/01/01. doi: 10.1017/s0022149x00017946 . PubMed DOI

von Lichtenberg F. Schistosomiasis as a worldwide problem: pathology. J Toxicol Environ Health. 1975;1(2):175–84. Epub 1975/11/01. doi: 10.1080/15287397509529319 . PubMed DOI

Pearce EJ, MacDonald AS. The immunobiology of schistosomiasis. Nat Rev Immunol. 2002;2(7):499–511. Epub 2002/07/03. doi: 10.1038/nri843 . PubMed DOI

Jutzeler KS, Clec’h WL, Chevalier FD, Anderson TJC. Contribution of parasite and host genotype to immunopathology of schistosome infections. bioRxiv. 2024. Epub 2024/01/23. doi: 10.1101/2024.01.12.574230 ; PubMed Central PMCID: PMC10802613. PubMed DOI PMC

Koslowski N, Sombetzki M, Loebermann M, Engelmann R, Grabow N, Osterreicher CH, et al.. Single-sex infection with female Schistosoma mansoni cercariae mitigates hepatic fibrosis after secondary infection. PLoS Negl Trop Dis. 2017;11(5):e0005595. Epub 2017/05/26. doi: 10.1371/journal.pntd.0005595 ; PubMed Central PMCID: PMC5453606. PubMed DOI PMC

Sombetzki M, Koslowski N, Rabes A, Seneberg S, Winkelmann F, Fritzsche C, et al.. Host Defense Versus Immunosuppression: Unisexual Infection With Male or Female Schistosoma mansoni Differentially Impacts the Immune Response Against Invading Cercariae. Front Immunol. 2018;9:861. Epub 2018/05/11. doi: 10.3389/fimmu.2018.00861 ; PubMed Central PMCID: PMC5930291. PubMed DOI PMC

Bischofsberger M, Reinholdt C, Dannenhaus TA, Aleith J, Bergmann-Ewert W, Muller-Hilke B, et al.. Individually or as a Team-The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of Schistosoma mansoni. Pathogens. 2023;12(12). Epub 2023/12/22. doi: 10.3390/pathogens12121432 ; PubMed Central PMCID: PMC10746046. PubMed DOI PMC

Reinholdt C, Winkelmann F, Koslowski N, Reisinger EC, Sombetzki M. Unisexual infection with Schistosoma mansoni in mice has the potential to boost the immune response against eggs after challenge infection. Front Immunol. 2023;14:1125912. Epub 2023/03/17. doi: 10.3389/fimmu.2023.1125912 ; PubMed Central PMCID: PMC10009330. PubMed DOI PMC

Freudenstein-Dan A, Gold D, Fishelson Z. Killing of schistosomes by elastase and hydrogen peroxide: implications for leukocyte-mediated schistosome killing. J Parasitol. 2003;89(6):1129–35. Epub 2004/01/27. doi: 10.1645/GE-96R . PubMed DOI

Larkin BM, Smith PM, Ponichtera HE, Shainheit MG, Rutitzky LI, Stadecker MJ. Induction and regulation of pathogenic Th17 cell responses in schistosomiasis. Semin Immunopathol. 2012;34(6):873–88. Epub 2012/10/26. doi: 10.1007/s00281-012-0341-9 ; PubMed Central PMCID: PMC3690599. PubMed DOI PMC

Elkhawaga AA, Hosni A, Zaky DZ, Kamel AA, Mohamed NA, Abozaid MA, et al.. Association of Treg and TH17 Cytokines with HCV Pathogenesis and Liver Pathology. Egypt J Immunol. 2019;26(2):55–63. Epub 2020/01/13. . PubMed

Abd Allah MH, Zaalouk TK, Abo-Sheishaa GA, Shalash IR, Bayoumy AS. Role of IL-17A in enhancing liver fibrosis induced by TGF-beta1 and IL-13 in Schistosoma mansoni infected mice. Egypt J Immunol. 2022;29(4):174–83. Epub 2022/10/09. . PubMed

Wilson MS, Mentink-Kane MM, Pesce JT, Ramalingam TR, Thompson R, Wynn TA. Immunopathology of schistosomiasis. Immunol Cell Biol. 2007;85(2):148–54. Epub 2006/12/13. doi: 10.1038/sj.icb.7100014 ; PubMed Central PMCID: PMC3437548. PubMed DOI PMC

MacDonald AS, Straw AD, Bauman B, Pearce EJ. CD8- dendritic cell activation status plays an integral role in influencing Th2 response development. J Immunol. 2001;167(4):1982–8. Epub 2001/08/08. doi: 10.4049/jimmunol.167.4.1982 . PubMed DOI

Faveeuw C, Angeli V, Fontaine J, Maliszewski C, Capron A, Van Kaer L, et al.. Antigen presentation by CD1d contributes to the amplification of Th2 responses to Schistosoma mansoni glycoconjugates in mice. J Immunol. 2002;169(2):906–12. Epub 2002/07/05. doi: 10.4049/jimmunol.169.2.906 . PubMed DOI

Aliprantis AO, Wang J, Fathman JW, Lemaire R, Dorfman DM, Lafyatis R, et al.. Transcription factor T-bet regulates skin sclerosis through its function in innate immunity and via IL-13. Proc Natl Acad Sci U S A. 2007;104(8):2827–30. Epub 2007/02/20. doi: 10.1073/pnas.0700021104 ; PubMed Central PMCID: PMC1815266 board of Bristol-Myers Squibb Company. PubMed DOI PMC

Fallon PG, Richardson EJ, McKenzie GJ, McKenzie AN. Schistosome infection of transgenic mice defines distinct and contrasting pathogenic roles for IL-4 and IL-13: IL-13 is a profibrotic agent. J Immunol. 2000;164(5):2585–91. Epub 2000/02/29. doi: 10.4049/jimmunol.164.5.2585 . PubMed DOI

Chiaramonte MG, Donaldson DD, Cheever AW, Wynn TA. An IL-13 inhibitor blocks the development of hepatic fibrosis during a T-helper type 2-dominated inflammatory response. J Clin Invest. 1999;104(6):777–85. Epub 1999/09/24. doi: 10.1172/JCI7325 ; PubMed Central PMCID: PMC408441. PubMed DOI PMC

Steinfelder S, Andersen JF, Cannons JL, Feng CG, Joshi M, Dwyer D, et al.. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J Exp Med. 2009;206(8):1681–90. Epub 2009/07/29. doi: 10.1084/jem.20082462 ; PubMed Central PMCID: PMC2722182. PubMed DOI PMC

Hang LM, Boros DL, Warren KS. Induction of immunological hyporesponsiveness to granulomatous hypersensitivity in Schistosoma mansoni infection. J Infect Dis. 1974;130(5):515–22. Epub 1974/11/01. doi: 10.1093/infdis/130.5.515 . PubMed DOI

Cheever AW. Differential regulation of granuloma size and hepatic fibrosis in schistosome infections. Mem Inst Oswaldo Cruz. 1997;92(5):689–92. Epub 1998/05/05. doi: 10.1590/s0074-02761997000500024 . PubMed DOI

Schwartz C, Oeser K, Prazeres da Costa C, Layland LE, Voehringer D. T cell-derived IL-4/IL-13 protects mice against fatal Schistosoma mansoni infection independently of basophils. J Immunol. 2014;193(7):3590–9. Epub 2014/08/31. doi: 10.4049/jimmunol.1401155 . PubMed DOI

Phillips SM, Linette GP, Doughty BL, Byram JE, Von Lichtenberg F. In vivo T cell depletion regulates resistance and morbidity in murine schistosomiasis. J Immunol. 1987;139(3):919–26. Epub 1987/08/01. . PubMed

Boros DL, Whitfield JR. Endogenous IL-10 regulates IFN-gamma and IL-5 cytokine production and the granulomatous response in Schistosomiasis mansoni-infected mice. Immunology. 1998;94(4):481–7. Epub 1998/10/10. doi: 10.1046/j.1365-2567.1998.00544.x ; PubMed Central PMCID: PMC1364225. PubMed DOI PMC

Kaplan MH, Whitfield JR, Boros DL, Grusby MJ. Th2 cells are required for the Schistosoma mansoni egg-induced granulomatous response. J Immunol. 1998;160(4):1850–6. Epub 1998/02/20. . PubMed

Wilder JA, Yuan D. Regulation of IFN-gamma mRNA production in murine natural killer cells. Int Immunol. 1995;7(4):575–82. Epub 1995/04/01. doi: 10.1093/intimm/7.4.575 . PubMed DOI

Rani R, Jordan MB, Divanovic S, Herbert DR. IFN-gamma-driven IDO production from macrophages protects IL-4Ralpha-deficient mice against lethality during Schistosoma mansoni infection. Am J Pathol. 2012;180(5):2001–8. Epub 2012/03/20. doi: 10.1016/j.ajpath.2012.01.013 ; PubMed Central PMCID: PMC3349826. PubMed DOI PMC

Chensue SW, Warmington KS, Ruth J, Lincoln PM, Kunkel SL. Cross-regulatory role of interferon-gamma (IFN-gamma), IL-4 and IL-10 in schistosome egg granuloma formation: in vivo regulation of Th activity and inflammation. Clin Exp Immunol. 1994;98(3):395–400. Epub 1994/12/01. doi: 10.1111/j.1365-2249.1994.tb05503.x ; PubMed Central PMCID: PMC1534488. PubMed DOI PMC

Henri S, Chevillard C, Mergani A, Paris P, Gaudart J, Camilla C, et al.. Cytokine regulation of periportal fibrosis in humans infected with Schistosoma mansoni: IFN-gamma is associated with protection against fibrosis and TNF-alpha with aggravation of disease. J Immunol. 2002;169(2):929–36. Epub 2002/07/05. doi: 10.4049/jimmunol.169.2.929 . PubMed DOI

Boissier J, Morand S, Mone H. A review of performance and pathogenicity of male and female Schistosoma mansoni during the life-cycle. Parasitology. 1999;119 (Pt 5):447–54. Epub 1999/12/22. doi: 10.1017/s0031182099005004 . PubMed DOI

Sombetzki M, Reinholdt C, Winkelmann F, Rabes A, Koslowski N, Reisinger EC. A one-year unisexual Schistosoma mansoni infection causes pathologic organ alterations and persistent non-polarized T cell-mediated inflammation in mice. Front Immunol. 2022;13:1010932. Epub 2022/12/13. doi: 10.3389/fimmu.2022.1010932 ; PubMed Central PMCID: PMC9730239. PubMed DOI PMC

Basch Paul F. 1991. Schistosomes: Development, Reproduction, and Host Relations. New York: Oxford University Press.