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Experimental infection with Schistosoma mansoni isolated from the wild rodent Holochilus sciureus shows a low parasite burden but induces high schistosomiasis severity in BALB/c mice

Published online by Cambridge University Press:  01 June 2022

Guilherme Silva Miranda Open the ORCID record for Guilherme Silva Miranda [Opens in a new window] ,
João Gustavo Mendes Rodrigues ,
Michelle Carvalho de Rezende ,
Samira Diniz Resende ,
Genil Mororó Araújo Camelo ,
Jeferson Kelvin Alves de Oliveira Silva ,
Laura Maggi ,
Vanessa Fernandes Rodrigues ,
Vinícius Gustavo de Oliveira  and
Deborah Aparecida Negrão-Corrêa Open the ORCID record for Deborah Aparecida Negrão-Corrêa [Opens in a new window]
Guilherme Silva Miranda
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil Department of Biology, Federal Institute of Education, Science and Technology of Maranhão, São Raimundo das Mangabeiras, Brazil
João Gustavo Mendes Rodrigues
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Michelle Carvalho de Rezende
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Samira Diniz Resende
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Genil Mororó Araújo Camelo
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Jeferson Kelvin Alves de Oliveira Silva
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Laura Maggi
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Vanessa Fernandes Rodrigues
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Vinícius Gustavo de Oliveira
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
Deborah Aparecida Negrão-Corrêa*
Affiliation:
Department of Parasitology, Federal University of Minas Gerais, Institute of Biological Sciences, Belo Horizonte, Brazil
*
Author for correspondence: Deborah Negrão-Corrêa, E-mail: [email protected]
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Abstract

Wild mammals, especially rodents, can participate in the life cycle of Schistosoma mansoni; however, the impact of these parasite strains on the severity of schistosomiasis remains unclear. The aim of this study was to comparatively evaluate the parasitological and immunopathological alterations induced by an S. mansoni strain isolated from the wild rodent Holochilus sciureus (HS strain) and a parasite strain isolated from a human (LE strain) in experimentally infected mice. Male BALB/c mice were subcutaneously infected with 50 cercariae/mouse of either the HS or the LE strain and were evaluated for 12 weeks. In the experimental groups, the parasite burden was estimated by worm and egg (feces and tissues) count, and immunopathological alterations were evaluated in the liver and intestines. Compared to experimental infection with the LE parasite strain, HS-infected mice showed reduced number of parasite worms but higher fecundity rate, significant reduction in IL-5, IL-10 and IL-13 concentrations, lower EPO-activity in liver homogenate and higher concentrations of TNF-α, IFN-γ, IL-12 and IL-17 in the small intestine homogenate. Moreover, HS infection resulted in higher concentrations of NO end-products in both the liver and intestine, suggesting a predominance of the Th1/Th17 immune response. HS-infected mice also showed higher plasma transaminase levels, formed larger granulomas, and had a higher mortality rate in comparison with LE-infected mice. Data indicate that BALB/c mice infected with the HS strain of S. mansoni showed reduced susceptibility to the parasite but stronger tissue inflammation and high disease severity.

Keywords

Holochilus sciureusimmune responseparasite burdenwild strain of Schistosoma mansonischistosomiasis severitySchistosoma-induced granulomatous inflammation
Type
Research Article
Information
Parasitology , Volume 149 , Issue 11 , September 2022 , pp. 1381 - 1396
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Abath, FG, Morais, CN, Montenegro, CE, Wynn, TA and Montenegro, SM (2006) Immunopathogenic mechanisms in schistosomiasis: what can be learnt from human studies? Trends in Parasitology 22, 85–91.CrossRefGoogle ScholarPubMed
Alarcón de Noya, B, Pointier, JP, Colmenares, C, Théron, A, Balzan, C, Cesari, IM, González, S and Noya, O (1997) Natural Schistosoma mansoni infection in wild rats from Guadeloupe: parasitological and immunological aspects. Acta Tropica 68, 11–21.CrossRefGoogle ScholarPubMed
Alves-Filho, JC, Sônego, F, Souto, FO, Freitas, A, Verri, WA Jr, Auxiliadora-Martins, M, Basile-Filho, A, McKenzie, AN, Xu, D, Cunha, FQ and Liew, FY (2010) Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nature Medicine 16, 708–712.CrossRefGoogle Scholar
Anderson, LA and Cheever, AW (1972) Comparison of geographical strains of Schistosoma mansoni in the mouse. Bulletin of the World Health Organization 46, 233–242.Google ScholarPubMed
Angeles, JMM, Mercado, VJP and Rivera, PT (2020) Behind enemy lines: immunomodulatory armamentarium of the schistosome parasite. Frontiers in Immunology 11, 1018.CrossRefGoogle ScholarPubMed
Araújo, N, Souza, CPD, Dias, EP and Katz, N (1986) Comportamento da cepa LE de Schistosoma mansoni, após passagem em hospedeiro humano infectado acidentalmente. Revista da Sociedade Brasileira de Medicina Tropical 19, 213–218.CrossRefGoogle Scholar
Barbosa, FS, Barbosa, I and Arruda, F (1962) Schistosoma mansoni: natural infection of cattle in Brazil. Science 138, 831.CrossRefGoogle ScholarPubMed
Barcelos, LS, Talvani, A, Teixeira, AS, Vieira, LQ, Cassali, GD, Andrade, SP and Teixeira, MM (2005) Impaired inflammatory angiogenesis, but not leukocyte influx, in mice lacking TNFR1. Journal of Leukocyte Biology 78, 352–358.CrossRefGoogle Scholar
Barral, V, Morand, S, Pointier, JP and Théron, A (1996) Distribution of schistosome genetic diversity within naturally infected Rattus rattus detected by RAPD markers. Parasitology 113, 511–517.CrossRefGoogle ScholarPubMed
Barron, L and Wynn, TA (2011) Macrophage activation governs schistosomiasis-induced inflammation and fibrosis. European Journal of Immunology 41, 2509–2514.CrossRefGoogle ScholarPubMed
Bastos, OC, Magalhães, LA and Pareja, GB (1979) Estudo da infecção esquistossomótica produzida pelas linhagens humana e silvestre do Vale do Rio Paraíba do Sul, SP (Brasil), em camundongos isogênicos. Revista de Saúde Pública 13, 335–340.CrossRefGoogle Scholar
Bastos, OC, Silva, AM, de Souza, EP, Lemos Neto, RC and Piedrabuena, AE (1982) Occurrence of human and wild strains of Schistosoma mansoni in pre-Amazonia. I. Study of mollusks. Revista de Saúde Pública 16, 292–298.CrossRefGoogle ScholarPubMed
Betson, M, Sousa-Figueiredo, JC, Kabatereine, NB and Stothard, JR (2012) Use of fecal occult blood tests as epidemiologic indicators of morbidity associated with intestinal schistosomiasis during preventive chemotherapy in young children. The American Journal of Tropical Medicine and Hygiene 87, 694–700.CrossRefGoogle ScholarPubMed
Bina, JC and Prata, A (2003) Esquistossomose na área hiperendêmica de Taquarendi: I Infecção pelo Schistosoma mansoni e formas graves. Revista da Sociedade Brasileira de Medicina Tropical 36, 211–216.CrossRefGoogle Scholar
Booth, M, Mwatha, JK, Joseph, S, Jones, FM, Kadzo, H, Ireri, E, Kazibwe, F, Kemijumbi, J, Kariuki, C, Kimani, G, Ouma, JH, Kabatereine, NB, Vennervald, BJ and Dunne, DW (2004) Periportal fibrosis in human Schistosoma mansoni infection is associated with low IL-10, low IFN-gamma, high TNF-alpha, or low RANTES, depending on age and gender. The Journal of Immunology 172, 1295–1303.CrossRefGoogle ScholarPubMed
Boulanger, D, Reid, GD, Sturrock, RF, Wolowczuk, I, Balloul, JM, Grezel, D, Pierce, RJ, Otieno, MF, Guerret, S, Grimaud, A, Butterworth, AE and Capron, A (1991) Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunology 13, 473–490.CrossRefGoogle ScholarPubMed
Brunet, LR, Finkelman, FD, Cheever, AW, Kopf, MA and Pearce, EJ (1997) IL-4 protects against TNF-alpha-mediated cachexia and death during acute schistosomiasis. The Journal of Immunology 159, 777–785.CrossRefGoogle ScholarPubMed
Burke, ML, Jones, MK, Gobert, GN, Li, YS, Ellis, MK and McManus, DP (2009) Immunopathogenesis of human schistosomiasis. Parasite Immunology 31, 163–176.CrossRefGoogle ScholarPubMed
Bustinduy, AL, Sousa-Figueiredo, JC, Adriko, M, Betson, M, Fenwick, A, Kabatereine, N and Stothard, JR (2013) Fecal occult blood and fecal calprotectin as point-of-care markers of intestinal morbidity in Ugandan children with Schistosoma mansoni infection. PLoS Neglected Tropical Diseases 7, e2542.CrossRefGoogle ScholarPubMed
Carneiro, CS, Bastos, OC, Neto, RCL, Liance, M, Picot, H and Houin, R (1991) Identity of two strains of Schistosoma mansoni studied by Western blot. Revista da Sociedade Brasileira de Medicina Tropical 24, 65–66.Google Scholar
Catalano, S, Sène, M, Diouf, ND, Fall, CB, Borlase, A, Léger, E, Bâ, K and Webster, JP (2018) Rodents as natural hosts of zoonotic Schistosoma species and hybrids: an epidemiological and evolutionary perspective from West Africa. The Journal of Infectious Diseases 218, 429–433.CrossRefGoogle ScholarPubMed
Catalano, S, Léger, E, Fall, CB, Borlase, A, Diop, SD, Berger, D, Webster, BL, Faye, B, Diouf, ND, Rollinson, D, Sène, M, Bâ, K and Webster, JP (2020) Multihost transmission of Schistosoma mansoni in Senegal, 2015–2018. Emerging Infectious Diseases 26, 1234–1242.CrossRefGoogle ScholarPubMed
Cheever, AW (1968) Conditions affecting the accuracy of potassium hydroxide digestion techniques for counting Schistosoma mansoni eggs in tissues. Bulletin of the World Health Organization 39, 328–331.Google ScholarPubMed
Cheever, AW, Hoffmann, KF and Wynn, TA (2000) Immunopathology of schistosomiasis mansoni in mice and men. Immunology Today 21, 465–466.CrossRefGoogle ScholarPubMed
Cheever, AW, Lenzi, JÁ, Lenzi, HL and Andrade, ZA (2002) Experimental models of Schistosoma mansoni infection. Memórias do Instituto Oswaldo Cruz 97, 917–940.CrossRefGoogle ScholarPubMed
Colley, DG and Loker, ES (2018) New tools for old questions: how strictly human are “Human schistosomes”-and does it matter? The Journal of Infectious Diseases 218, 344–346.CrossRefGoogle ScholarPubMed
Colley, DG and Secor, WE (2014) Immunology of human schistosomiasis. Parasite Immunology 36, 347–357.CrossRefGoogle ScholarPubMed
Corraliza, IM, Campo, ML, Soler, G and Modolell, M (1994) Determination of arginase activity in macrophages: a micromethod. Journal of Immunological Methods 174, 231–235.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
Coulson, PS, Smythies, LE, Betts, C, Mabbott, NA, Sternberg, JM, Wei, XG, Liew, FY and Wilson, RA (1998) Nitric oxide produced in the lungs of mice immunized with the radiation-attenuated schistosome vaccine is not the major agent causing challenge parasite elimination. Immunology 93, 55–63.CrossRefGoogle Scholar
D'Andrea, PS, Maroja, LS, Gentile, R, Cerqueira, R, Maldonado Júnior, A and Rey, L (2000) The parasitism of Schistosoma mansoni (Digenea-Trematoda) in a naturally infected population of water rats, Nectomys squamipes (Rodentia-Sigmodontinae) in Brazil. Parasitology 120, 573–582.CrossRefGoogle Scholar
Da Silva, FL, Del-Rei, RP, Fraga, DBM, Leony, LM, Souza, AMGCD and Santos, FLN (2018) Alterations in the lipid profiles and circulating liver enzymes in individuals infected by Schistosoma mansoni. Revista da Sociedade Brasileira de Medicina Tropical 51, 795–801.CrossRefGoogle Scholar
De Jesus, AR, Silva, A, Santana, LB, Magalhães, A, de Jesus, AA, de Almeida, RP, Rêgo, MA, Burattini, MN, Pearce, EJ and Carvalho, EM (2002) Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. The Journal of Infectious Disease 185, 98–105.CrossRefGoogle ScholarPubMed
Dessie, N, Lema, W and Aemero, M (2020) Hematological and biochemical profile of patients infected with Schistosoma mansoni in comparison with apparently healthy individuals at Sanja Town, Northwest Ethiopia: a cross-sectional study. Journal of Tropical Medicine 2020, 4083252.CrossRefGoogle ScholarPubMed
do Carmo-Silva, CF, Teles-Reis, A, Silva-Soares, RF, Rodrigues, JGM, Lira, MGS, Nogueira, RA, Viegas-Melo, D, Cardoso, DT, Miranda, GS and Silva-Souza, N (2019) Spatial and seasonal distribution of Holochilus sciureus with Schistosoma mansoni infection in an endemic area for schistosomiasis in Brazil. Acta Parasitologica 64, 932–937.CrossRefGoogle Scholar
Dunne, DW and Cooke, A (2005) A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nature Reviews Immunology 5, 420–426.CrossRefGoogle ScholarPubMed
Dunne, DW, Butterworth, AE, Fulford, AJ, Kariuki, HC, Langley, JG, Ouma, JH, Capron, A, Pierce, RJ and Sturrock, RF (1992) Immunity after treatment of human schistosomiasis: association between IgE antibodies to adult worm antigens and resistance to reinfection. European Journal of Immunology 22, 1483–1494.CrossRefGoogle ScholarPubMed
Duplantier, JM and Sène, M (2000) Rodents as reservoir hosts in the transmission of Schistosoma mansoni in Richard-Toll, Senegal, West Africa. Journal of Helminthology 74, 129–135.CrossRefGoogle ScholarPubMed
Euzébio, AA Jr, Zuim, NR, Linhares, AX, Magalhães, LA and Zanotti-Magalhães, EM (2012) Experimental evaluation of the pathogenicity of different strains of Schistosoma mansoni. Interdisciplinary Perspectives on Infectious Diseases 2012, 894940.CrossRefGoogle ScholarPubMed
Fallon, PG (2000) Immunopathology of schistosomiasis: a cautionary tale of mice and men. Immunology Today 21, 29–35.CrossRefGoogle ScholarPubMed
Fallon, PG, Richardson, EJ, Smith, P and Dunne, DW (2000) Elevated type 1, diminished type 2 cytokines and impaired antibody response are associated with hepatotoxicity and mortalities during Schistosoma mansoni infection of CD4-depleted mice. European Journal of Immunology 30, 470–480.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Fernandes, A, Pereira, AT, Eschenazi, PD, Schilter, HC, Sousa, AL, Teixeira, MM and Negrão-Corrêa, D (2008) Evaluation of the immune response against Strongyloides venezuelensis in antigen-immunized or previously infected mice. Parasite Immunology 30, 139–149.CrossRefGoogle ScholarPubMed
Finlay, JB, Liu, X, Ermel, RW and Adamson, TW (2015) Maternal weight gain as a predictor of litter size in Swiss Webster, C57BL/6J, and BALB/cJ mice. Journal of the American Association for Laboratory Animal Science 54, 694–699.Google ScholarPubMed
Freire, N, Rodrigues-Silva, R, Machado-Silva, JR and Rey, L (2003) A comparative parasitologic study on Biomphalaria glabrata snail and C3H/He mice infected with human and murine isolates of Schistosoma mansoni derived from Sumidouro, Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 98, 783–787.CrossRefGoogle Scholar
Gentile, R, Costa-Neto, SF, Gonçalves, MM, Bonecker, ST, Fernandes, FA, Garcia, JS, Barreto, MG, Soares, MS, D'Andrea, PS, Peralta, JM and Rey, L (2006) An ecological field study of the water-rat Nectomys squamipes as a wild reservoir indicator of Schistosoma mansoni transmission in an endemic area. Memórias do Instituto Oswaldo Cruz 101, 111–117.CrossRefGoogle Scholar
Gentile, R, Barreto, MG, Gonçalves, MM, Soares, DP and D'Andrea, PS (2012) The role of wild rodents in the transmission of Schistosoma mansoni in Brazil. In Rokni, MB (ed.), Schistosomiasis. London: Intech Open Access Publisher, pp. 231–254.Google Scholar
Giannini, EG, Testa, R and Savarino, V (2005) Liver enzyme alteration: a guide for clinicians. Canadian Medical Association Journal 172, 367–379.CrossRefGoogle ScholarPubMed
Gordon, S (2003) Alternative activation of macrophages. Nature Reviews Immunology 3, 23–35.CrossRefGoogle ScholarPubMed
Gryseels, B, Polman, K, Clerinx, J and Kestens, L (2006) Human schistosomiasis. The Lancet 368, 1106–1118.CrossRefGoogle ScholarPubMed
Hambrook, JR and Hanington, PC (2021) Immune evasion strategies of schistosomes. Frontiers in Immunology 11, 624178.CrossRefGoogle ScholarPubMed
Hams, E, Aviello, G and Fallon, PG (2013) The Schistosoma granuloma: friend or foe? Frontiers in Immunology 4, 89.CrossRefGoogle ScholarPubMed
Hanelt, B, Mwangi, IN, Kinuthia, JM, Maina, GM, Agola, LE, Mutuku, MW, Steinauer, ML, Agwanda, BR, Kigo, L, Mungai, BN, Loker, ES and Mkoji, GM (2010) Schistosomes of small mammals from the Lake Victoria Basin, Kenya: new species, familiar species, and implications for schistosomiasis control. Parasitology 137, 1109–1118.CrossRefGoogle Scholar
Herbert, DR, Hölscher, C, Mohrs, M, Arendse, B, Schwegmann, A, Radwanska, M, Leeto, M, Kirsch, R, Hall, P, Mossmann, H, Claussen, B, Förster, I and Brombacher, F (2004) Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20, 623–635.CrossRefGoogle ScholarPubMed
Hesse, M, Piccirillo, CA, Belkaid, Y, Prufer, J, Mentink-Kane, M, Leusink, M, Cheever, AW, Shevach, EM and Wynn, TA (2004) The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. The Journal of Immunology 172, 3157–3166.CrossRefGoogle ScholarPubMed
Hoffmann, KF, Cheever, AW and Wynn, TA (2000) IL-10 and the dangers of immune polarization: excessive type 1 and type 2 cytokine responses induce distinct forms of lethal immunopathology in murine schistosomiasis. The Journal of Immunology 164, 6406–6416.CrossRefGoogle ScholarPubMed
Ivey, CL, Williams, FM, Collins, PD, Jose, PJ and Williams, TJ (1995) Neutrophil chemoattractants generated in two phases during reperfusion of ischemic myocardium in the rabbit. Evidence for a role for C5a and interleukin-8. Journal of Clinical Investigation 95, 2720–2728.CrossRefGoogle ScholarPubMed
Katz, N, Dias, EP, Araújo, N and Souza, CD (1973) Estudo de uma cepa humana de Shistosoma mansoni resistente a agentes esquistossomicidas. Revista da Sociedade Brasileira de Medicina Tropical 7, 381–387.CrossRefGoogle Scholar
Kovach, MA and Standiford, TJ (2012) The function of neutrophils in sepsis. Current Opinion in Infectious Diseases 25, 321–327.CrossRefGoogle ScholarPubMed
La Flamme, AC, Patton, EA, Bauman, B and Pearce, EJ (2001) IL-4 plays a crucial role in regulating oxidative damage in the liver during schistosomiasis. The Journal of Immunology 166, 1903–1911.CrossRefGoogle Scholar
Lenzi, HL, Kimmel, E, Schechtman, H, Pelajo-Machado, M, Romanha, WS, Pacheco, RG, Mariano, M and Lenzi, JÁ (1998) Histoarchitecture of schistosomal granuloma development and involution: morphogenetic and biomechanical approaches. Memórias do Instituto Oswaldo Cruz 93, 141–151.CrossRefGoogle ScholarPubMed
Luna, LG (1968) Manual of the Histologic Staining Methods of the Armed Forces Institute of Pathology, 3rd Edn. New York, USA: McGrawHill.Google Scholar
Lundy, SK and Lukacs, NW (2013) Chronic schistosome infection leads to modulation of granuloma formation and systemic immune suppression. Frontiers in Immunology 4, 39.CrossRefGoogle ScholarPubMed
Maggi, L, Rocha, IC, Camelo, GMA, Fernandes, VR and Negrão-Corrêa, D (2021) The IL-33/ST2 pathway is not essential to Th2 stimulation but is key for modulation and survival during chronic infection with Schistosoma mansoni in mice. Cytokine 138, 155390.CrossRefGoogle Scholar
Martinez, EM, Neves, RH, Oliveira, RMFD, Machado-Silva, JR and Rey, L (2003) Características biológicas e morfológicas de cepas brasileiras de Schistosoma mansoni em Mus musculus. Revista da Sociedade Brasileira de Medicina Tropical 36, 557–564.CrossRefGoogle ScholarPubMed
Martins-Leite, P, Gazzinelli, G, Alves-Oliveira, LF, Gazzinelli, A, Malaquias, LC, Correa-Oliveira, R, Teixeira-Carvalho, A and Silveira, AM (2008) Effect of chemotherapy with praziquantel on the production of cytokines and morbidity associated with schistosomiasis mansoni. Antimicrobial Agents and Chemotherapy 52, 2780–2786.CrossRefGoogle ScholarPubMed
Masamba, P and Kappo, AP (2021) Immunological and biochemical interplay between cytokines, oxidative stress and schistosomiasis. International Journal of Molecular Sciences 22, 7216.CrossRefGoogle ScholarPubMed
McManus, DP, Dunne, DW, Sacko, M, Utzinger, J, Vennervald, BJ and Zhou, XN (2018) Schistosomiasis. Nature Reviews Disease Primers 4, 13.CrossRefGoogle ScholarPubMed
Miranda, GS, Miranda, BS, Rodrigues, JGM, Lira, MGS, Nogueira, RA, Viegas-Melo, D and Silva-Souza, N (2017) Research note. The wild water-rats and their relevance in the context of schistosomiasis mansoni in Brazil: what we know and recommendations for further research. Helminthologia 54, 165–169.CrossRefGoogle Scholar
Modena, CM, dos Santos Lima, W and Coelho, PM (2008) Wild and domesticated animals as reservoirs of schistosomiasis mansoni in Brazil. Acta Tropica 108, 242–244.CrossRefGoogle ScholarPubMed
Mwatha, JK, Kimani, G, Kamau, T, Mbugua, GG, Ouma, JH, Mumo, J, Fulford, AJ, Jones, FM, Butterworth, AE, Roberts, MB and Dunne, DW (1998) High levels of TNF, soluble TNF receptors, soluble ICAM-1, and IFN-gamma, but low levels of IL-5, are associated with hepatosplenic disease in human schistosomiasis mansoni. The Journal of Immunology 160, 1992–1999.CrossRefGoogle ScholarPubMed
Negrão-Corrêa, D, Souza, DG, Pinho, V, Barsante, MM, Souza, AL and Teixeira, MM (2004) Platelet-activating factor receptor deficiency delays elimination of adult worms but reduces fecundity in Strongyloides venezuelensis-infected mice. Infection and Immunity 72, 1135–1142.CrossRefGoogle ScholarPubMed
Nelson, GS (1960) Schistosome infections as zoonoses in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene 54, 301–324.CrossRefGoogle ScholarPubMed
Neves, RH, Pereira, MJS, De Oliveira, RMF, Gomes, DC and Machado-Silva, JR (1998) Schistosoma mansoni Sambom, 1907: morphometric differences between adult worms from sympatric rodent and human isolates. Memórias do Instituto Oswaldo Cruz 93, 309–312.CrossRefGoogle ScholarPubMed
Oliveira, VG, Rodrigues, VF, Moreira, JMP, Rodrigues, JL, Maggi, L, Resende, SD and Negrão-Corrêa, D (2022) Eosinophils participate in modulation of liver immune response and tissue damage induced by Schistosoma mansoni infection in mice. Cytokine 149, 155701.CrossRefGoogle ScholarPubMed
Pastorelli, L, Garg, RR, Hoang, SB, Spina, L, Mattioli, B, Scarpa, M, Fiocchi, C, Vecchi, M and Pizarro, TT (2010) Epithelial-derived IL-33 and its receptor ST2 are dysregulated in ulcerative colitis and in experimental Th1/Th2 driven enteritis. Proceedings of the National Academy of Sciences of the United States of America 107, 8017–8022.CrossRefGoogle ScholarPubMed
Pastorelli, L, De Salvo, C, Cominelli, MA, Vecchi, M and Pizarro, TT (2011) Novel cytokine signaling pathways in inflammatory bowel disease: insight into the dichotomous functions of IL-33 during chronic intestinal inflammation. Therapeutic Advances in Gastroenterology 4, 311–323.CrossRefGoogle ScholarPubMed
Pearce, EJ and MacDonald, AS (2002) The immunobiology of schistosomiasis. Nature Reviews Immunology 2, 499–511.CrossRefGoogle ScholarPubMed
Pearce, EJ, Kane, CM, Sun, J, Taylor, JJ, McKee, AS and Cervi, L (2004) Th2 response polarization during infection with the helminth parasite Schistosoma mansoni. Immunological Reviews 201, 117–126.CrossRefGoogle ScholarPubMed
Pellegrino, J and Katz, N (1968) Experimental chemotherapy of schistosomiasis mansoni. In Dawes, B (ed.), Advances in Parasitology. London, New York: Academic Press, pp. 233–291.Google Scholar
Pellegrino, J and Siqueira, AF (1956) Técnica de perfusão para colheita de Schistosoma mansoni em cobaias experimentalmente infestadas. Revista Brasileira de Malária 8, 589–597.Google Scholar
Reddy, GK and Enwemeka, CS (1996) A simplified method for the analysis of hydroxyproline in biological tissues. Clinical Biochemistry 29, 225–229.CrossRefGoogle ScholarPubMed
Rey, L (1993) Non-human vertebrate hosts of Schistosoma mansoni and schistosomiasis transmission in Brazil. Research and Reviews in Parasitology 53, 13–25.Google Scholar
Rezende, MC, Moreira, JMP, Fernandes, LLM, Rodrigues, VF and Negrão-Corrêa, D (2020) Strongyloides venezuelensis-infection alters the profile of cytokines and liver inflammation in mice co-infected with Schistosoma mansoni. Cytokine 127, 154931.CrossRefGoogle ScholarPubMed
Rutitzky, LI and Stadecker, MJ (2006) CD4 T Cells producing pro-inflammatory interleukin-17 mediate high pathology in schistosomiasis. Memórias do Instituto Oswaldo Cruz 101, 327–330.CrossRefGoogle ScholarPubMed
Schwartz, C and Fallon, PG (2018) Schistosoma “Eggs-Iting” the host: granuloma formation and egg excretion. Frontiers in Immunology 9, 2492.CrossRefGoogle ScholarPubMed
Sire, C, Durand, P, Pointier, JP and Théron, A (1999) Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplified polymorphic DNA markers. The Journal of Parasitology 85, 436–441.CrossRefGoogle Scholar
Smythies, LE, Betts, C, Coulson, PS, Dowling, MA and Wilson, RA (1996) Kinetics and mechanism of effector focus formation in the lungs of mice vaccinated with irradiated cercariae of Schistosoma mansoni. Parasite Immunology 18, 359–369.CrossRefGoogle ScholarPubMed
Standley, CJ, Mugisha, L, Verweij, JJ, Adriko, M, Arinaitwe, M, Rowell, C, Atuhaire, A, Betson, M, Hobbs, E, van Tulleken, CR, Kane, RA, van Lieshout, L, Ajarova, L, Kabatereine, NB and Stothard, JR (2011) Confirmed infection with intestinal schistosomiasis in semi-captive wild-born chimpanzees on Ngamba Island, Uganda. Vector Borne and Zoonotic Diseases 11, 169–176.CrossRefGoogle ScholarPubMed
Strath, M, Warren, DJ and Sanderson, CJ (1985) Detection of eosinophils using an eosinophil peroxidase assay. Its use as an assay for eosinophil differentiation factors. Journal of Immunological Methods 83, 209–215.CrossRefGoogle ScholarPubMed
Théron, A (1984) Early and late shedding patterns of Schistosoma mansoni cercariae: ecological significance in transmission to human and murine hosts. The Journal of Parasitology 70, 652–655.CrossRefGoogle ScholarPubMed
Théron, A, Pointier, JP, Morand, S, Imbert-Establet, D and Borel, G (1992) Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment. Parasitology 104, 291–298.CrossRefGoogle ScholarPubMed
Tsikas, D (2007) Analysis of nitrite and nitrate in biological fluids by assays based on the Griess reaction: appraisal of the Griess reaction in the L-arginine/nitric oxide area of research. Journal of Chromatography B 851, 51–70.CrossRefGoogle ScholarPubMed
Vannella, KM, Ramalingam, TR, Borthwick, LA, Barron, L, Hart, KM, Thompson, RW, Kindrachuk, KN, Cheever, AW, White, S, Budelsky, AL, Comeau, MR, Smith, DE and Wynn, TA (2016) Combinatorial targeting of TSLP, IL-25, and IL-33 in type 2 cytokine-driven inflammation and fibrosis. Science Translational Medicine 8, 337ra65.CrossRefGoogle ScholarPubMed
Wang, B, Liang, S, Wang, Y, Zhu, XQ, Gong, W, Zhang, HQ, Li, Y and Xia, CM (2015) Th17 down-regulation is involved in reduced progression of schistosomiasis fibrosis in ICOSL KO mice. PLoS Neglected Tropical Diseases 9, e0003434.CrossRefGoogle ScholarPubMed
Warren, KS (1967) 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. Transactions of the Royal Society of Tropical Medicine and Hygiene 61, 795–802.CrossRefGoogle ScholarPubMed
Webster, JP, Neves, MI, Webster, BL, Pennance, T, Rabone, M, Gouvras, AN, Allan, F, Walker, M and Rollinson, D (2020) Parasite population genetic contributions to the schistosomiasis consortium for operational research and evaluation within sub-Saharan Africa. The American Journal of Tropical Medicine and Hygiene 103, 80–91.CrossRefGoogle Scholar
Weerakoon, KG, Gobert, GN, Cai, P and McManus, DP (2015) Advances in the diagnosis of human schistosomiasis. Clinical Microbiology Reviews 28, 939–967.CrossRefGoogle ScholarPubMed
World Health Organization (2020) Status of Schistosomiasis Endemic Countries: 2018, 2018. Available at https://apps.who.int/neglected_diseases/ntddata/sch/sch.html.Google Scholar
Zhang, Y, Chen, L, Gao, W, Hou, X, Gu, Y, Gui, L, Huang, D, Liu, M, Ren, C, Wang, S and Shen, J (2012) IL-17 neutralization significantly ameliorates hepatic granulomatous inflammation and liver damage in Schistosoma japonicum infected mice. European Journal of Immunology 42, 1523–1535.CrossRefGoogle ScholarPubMed