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Licensed Unlicensed Requires Authentication Published by De Gruyter December 28, 2016

Exploring possibilities for an alternative approach in experimental schistosomiasis mansoni: the peritoneal cavity of mice

Vitor L.T. Mati, Rosilene S. Bicalho and Alan L. Melo
From the journal Acta Parasitologica

Abstract

The schistosome oviposition and granuloma constitution in the peritoneal cavity of AKR/J mice were evaluated. Groups of mice intraperitoneally infected with cercariae of Schistosoma mansoni were weekly euthanized during the acute (56 to 84 days post–infection (DPI)) and chronic (147 to 175 DPI) phase of infection. Schistosome developmental stages obtained via peritoneal lavage and perfusion of the portal system were inspected, counted and fixed, and peritoneal granulomata were then processed for histology. The morphological characterization and quantitative analysis of peritoneal schistosome eggs and granulomata were for the first time performed, such as the demonstration of the viability of miracidia obtained there from. Eutopic and ectopic mature schistosomes and normal pattern of worm oviposition were observed in all periods studied. However, the size of schistosome eggs from peritoneal cavity was smaller than observed for eggs laid by female worms from the portal system. The numbers of S. mansoni eggs and/or granulomata recovered from the peritoneal cavity was higher in chronic than acute infection, while the mean diameter of peritoneal chronic granulomata was smaller than for peritoneal acute granulomata. The constitution and evolution of these cellular reactions at histology were similar to that of hepatic granuloma, and peritoneal granulomata were subject to the host immunomodulation. In addition to the standardization of this experimental approach, which allows the obtaining of free schistosomal granulomata from peritoneal cavity of AKR/J mice, the potential use of these granulomata in ex vivo and in vivo studies is discussed.

Acknowledgements

We thank Mr Airton Lobo for technical assistance and the Conselho Nacional de Pesquisa e Tecnologia (CNPq) for partial financial support. V.L.T.M. was supported by Master’s and Doctoral Degree Fellowships from CNPq and A.L.M. is supported by a CNPq Fellowship.

References

Andrade Z.A., Warren K.S. 1964. Mild prolonged schistosomiasis: alterations in host response with time and the development of portal fibrosis. Transactions of the Royal Society of Tropical Medicine and Hygiene, 58, 447–456. 10.1016/0035-9203(64)90068-9Search in Google Scholar

Bicalho R.S., Melo A.L., Pereira L.H. 1993. Desenvolvimento do Schistosoma mansoni na cavidade peritoneal de camundongos da linhagem AKR/J. Revista do Instituto de Medicina Tropical de São Paulo, 35, 411–416. 10.1590/s0036-46651993000500005Search in Google Scholar

Bogéa T. 2005. Phenotypic plasticity in the cercarial indices of human and rodent samples of Schistosoma mansoni (Digenea: Schistosomatidae). Annals of Tropical Medicine and Parasitology, 99, 583–592. 10.1179/136485905x51454Search in Google Scholar

Bogliolo L. 1957. Anatomical picture of the liver in hepatosplenic schistosomiasis mansoni. Annals of Tropical Medicine and Parasitology, 51, 1–14. 10.1080/00034983.1957.11685 789Search in Google Scholar

Boros D.L., Warren K.S. 1970. Delayed hypersensitivity-type granuloma formation and dermal reaction induced and elicited by a soluble factor isolated from Schistosoma mansoni eggs. Journal of Experimental Medicine, 132, 488–507. 10.1084/jem.132.3.488Search in Google Scholar

Brener Z., Pellegrino J. 1956. Method for isolating schistosome granulomas from mouse liver. Journal of Parasitology, 42, 564–564. 10.2307/3274872Search in Google Scholar

Caldas I.R., Campi-Azevedo A.C., Oliveira L.F., Silveira A.M., Oliveira R.C., Gazzinelli G. 2008. Human schistosomiasis mansoni: immune responses during acute and chronic phases of the infection. Acta Tropica, 108, 109–117. 10.1016/j.actatropica.2008.05.027Search in Google Scholar

Carvalho A.D., Alvarenga R.J., Melo A.L. 1986. Histopatologia da esquistossomose mansoni em figado de Mus musculus infectado por amostras humanas de fase aguda e crônica da periferia de Belo Horizonte, Minas Gerais. Revista da Sociedade Brasileira de Medicina Tropical, 19, 89–94. 10.1590/s0037-86821986000200007Search in Google Scholar

Chao L.P., Jones J.T., Kusel J.R. 1986. An in vivo model for the study of chemotaxis induced by schistosomula of Schistosoma mansoni. Parasitology, 92, 117–132. 10.1017/s003118 2000063496Search in Google Scholar

Coelho P.M.Z., Pellegrino J., Pereira L.H., Mello R.T. 1976. Migration of schistosomula (Schistosoma mansoni) collected from hamsters and inoculated intraperitoneally in mice. Transactions of the Royal Society of Tropical Medicine and Hygiene, 70, 161. 10.1016/0035-9203(76)90181-4Search in Google Scholar

Curry A.J., Else K.J., Jones F., Bancroft A., Grencis R.K., Dunne D.W. 1995. Evidence that cytokine-mediated immune interactions induced by Schistosoma mansoni alter disease outcome in mice concurrently infected with Trichuris muris. Journal of Experimental Medicine, 181, 769–774. 10.1084/jem.181.2.769Search in Google Scholar PubMed PubMed Central

Doenhoff M., Musallam R., Bain J., McGregor A. 1978. Studies on the host–parasite relationship in Schistosoma mansoni-infected mice: the immunological dependence of parasite egg excretion. Immunology, 35, 771–778Search in Google Scholar

Fan P.C., Lin L.L. 1994. Encapsulated egg deposition pattern of Schistosoma japonicum in the peritoneal cavity of mice. Journal of Helminthology, 68, 125–129. 10.1017/s0022 149x0001364xSearch in Google Scholar

Fan P.C., Pao K.Y. 1970. Encapsulated eggs of Schistosoma mansoni in the peritoneal cavity of experimentally infected mice following intraperitoneal and percutaneous infections. Southeast Asian Journal of Tropical Medicine and Public Health, 1, 562–563.Search in Google Scholar

Fan P.C., Pao K.Y. 2006. Study of the morphological characteristics of Schistosoma mansoni in mice, squirrels, and hamsters. Southeast Asian Journal of Tropical Medicine and Public Health, 37, 33–39Search in Google Scholar

Goes A.M., Gazzinelli G., Rocha R., Katz N., Doughty B.L. 1991. Granulomatous hypersensitivity to Schistosoma mansoni egg antigens in human schistosomiasis. III. In vitro granuloma modulation induced by immune complexes. American Journal of Tropical Medicine and Hygiene, 44, 434–44310.4269/ajtmh.1991.44.434Search in Google Scholar PubMed

Hermeto M.V., Bicalho R.S., Silva R.E., Melo A.L., Pereira L.H. 1994. Oogram studies in mice infected with Schistosoma mansoni and treated with dexamethasone. Revista do Instituto de Medicina Tropical de São Paulo 36 99–103 10.1590/s0036-46651994000200001Search in Google Scholar PubMed

Jurberg A.D., Gonçalves T., Costa T.A., Mattos A.C., Pascarelli B.M., Manso P.P., Ribeiro-Alves M., Pelajo-Machado M., Peralta J.M., Coelho P.M., Lenzi H.L. 2009. The embryonic development of Schistosoma mansoni eggs: proposal for a new staging system. Development Genes and Evolution, 219, 219–234. 10.1007/s00427-009-0285-9Search in Google Scholar PubMed

Lenzi H.L., Kimmel E., Schechtman H., Pelajo-Machado M., Vale, B.S., Panasco M.S., Lenzi J.A. 1999. Collagen arrangement in hepatic granuloma in mice infected with Schistosoma mansoni: dependence on fiber radiation centers. Brazilian Journal of Medical and Biological Research, 32, 639–643. 10.1590/s0100-879x1999000500018Search in Google Scholar PubMed

Lenzi H.L., Lenzi J.A., Kerr I.B., Antunes S.L., Mota E.M., Oliveira D.N. 1991. Extracellular matrix in parasitic and infectious diseases. Memórias do Instituto Oswaldo Cruz, 86(Suppl. 3), 77–90. 10.1590/s0074-02761991000700012Search in Google Scholar PubMed

Lenzi H.L., Lenzi J.A., Sobral A.C. 1987. Eosinophils favor the passage of eggs to the intestinal lumen in schistosomiasis. Brazilian Journal of Medical and Biological Research, 20, 433–435Search in Google Scholar

Lenzi H.L., Romanha W.S. 2003. Schistosomal granuloma is like a small multicellular organism that operates as a complex system. In: (Ed. R. Mondaini) Proceedings of the Second Brazilian Symposium on Mathematical and Computational Biology. E-papers Serviços Editoriais, Rio de Janeiro, 257–282Search in Google Scholar

Lenzi H.L., Romanha W.S., Santos R.M., Rosas A., Mota E.M., Manso P.P., Caputo L.F., Pelajo-Machado M. 2006. Four whole-istic aspects of schistosome granuloma biology: fractal arrangement, internal regulation, autopoietic component and closure. Memórias do Instituto Oswaldo Cruz, 101(Suppl. 1), 219–231. 10.1590/s0074-02762006000900034Search in Google Scholar PubMed

LoVerde P.T., Niles E.G., Osman A., Wu W. 2004. Schistosoma mansoni male-female interactions. Canadian Journal of Zoology, 82, 357–374. 10.1139/z03-217Search in Google Scholar

Lundy S.K., Lukacs N.W. 2013. Chronic schistosome infection leads to modulation of granuloma formation and systemic immune suppression. Frontiers in Immunology, 4, 39. 10.3389/ fimmu.2013.00039Search in Google Scholar

Martinez E.M., Costa-Silva M., Neves R.H., Oliveira R.M., Machado-Silva J.R. 2008. Biological implications of the phenotypic plasticity in the Schistosoma mansoni–Nectomys squamipes model. Revista do Instituto de Medicina Tropical de São Paulo, 50, 229–232. 10.1590/s0036-46652008 000400008Search in Google Scholar

Mati V.L., Freitas R.M., Bicalho R.S., Melo A.L. 2015. Phenotypic plasticity of male Schistosoma mansoni from the peritoneal cavity and hepatic portal system of laboratory mice and hamsters. Journal of Helminthology, 89, 294–301. 10.1017/ s0022149x14000066Search in Google Scholar

Mati V.L., Freitas R.M., Melo A.L. 2010. Effects of pentoxifylline during Schistosoma mansoni infection in Swiss mice: an analysis of worm burden, fecundity and liver histopathology. Journal of Helminthology, 84, 348–354. 10.1017/ s0022149x09990733Search in Google Scholar

Mati V.L., Melo A.L. 2013. Current applications of oogram methodology in experimental schistosomiasis; fecundity of female Schistosoma mansoni and egg release in the intestine of AKR/J mice following immunomodulatory treatment with pentoxifylline. Journal of Helminthology, 87, 115–124. 10.1017/s0022149x12000144Search in Google Scholar PubMed

Mati V.L, Pinto H.A., Melo A.L. 2013. Experimental infection of Swiss and AKR/J mice with Centrocestus formosanus (Trematoda: Heterophyidae). Revista do Instituto de Medicina Tropical de São Paulo, 55, 133–136. 10.1590/s0036-46652013000200013Search in Google Scholar PubMed

Melo A.L., Hermeto M.V., Bicalho R.S., Vargas A.P., Favaretto F.J., Pereira L.H. 1994. Schistosoma mansoni: the effect of dexamethasone on the cercaria–schistosomulum transformation in vivo. Revista do Instituto de Medicina Tropical de São Paulo, 36, 89–93. 10.1590/s0036-46651994000 100014Search in Google Scholar

Melo A.L., Machado C.R., Pereira L.H. 1990. Differences between in vitro and in vivo obtained schistosomules. Revista do Instituto de Medicina Tropical de São Paulo, 32, 84–85. 10.1590/s0036-46651990000200003Search in Google Scholar PubMed

Melo A.L., Machado C.R., Pereira L.H. 1993a. Host cell adhesion to Schistosoma mansoni larvae in the peritoneal cavity of naive mice: histological and scanning electron microscopic studies. Revista do Instituto de Medicina Tropical de São Paulo, 35, 17–22. 10.1590/s0036-46651993000100003Search in Google Scholar PubMed

Melo A.L., Machado C.R., Pereira L.H. 1993b. Interaction between neutrophils and Schistosoma mansoni larvae in vivo: a transmission electron-microscopic study. Revista do Instituto de Medicina Tropical de São Paulo, 35, 29–33. 10. 1590/s0036-46651993000100005Search in Google Scholar

Melo A.L., Pereira L.H. 1980. Inhibitory effect of oxamniquine on the detachment of the tail of Schistosoma mansoni. Journal of Parasitology, 66, 1067–1068. 10.2307/3280426Search in Google Scholar

Melo A.L., Pereira L.H. 1985. Kinetics of the cercaria–schistosomulum tranformation in vivo. Revista da Sociedade Brasileira de Medicina Tropical, 18, 17–21. 10.1590/s0037-86821 985000100005Search in Google Scholar

Melo A.L., Pereira L.H., Chamone M. 1980. The effect of a previous Schistosoma mansoni infection on schistosomulum recovery from the peritoneal cavity of laboratory mice. Transactions of the Royal Society of Tropical Medicine and Hygiene, 74, 827. 10.1016/0035-9203(80)90219-9Search in Google Scholar

Melo A.L., Pereira L.H., Correa M.C. 1978. In vivo cercaria–schistosomulum transformation: inhibitory effect of oxamniquine. Transactions of the Royal Society of Tropical Medicine and Hygiene, 72, 158–159. 10.1016/0035-9203(78)90051-2Search in Google Scholar

Melo A.L., Pereira L.H., Machado C.R. 1992. Schistosoma mansoni: host cell adhesion to the different stages of the parasite in vivo. Revista do Instituto de Medicina Tropical de São Paulo, 34, 205–209. 10.1590/s0036-46651992000300004Search in Google Scholar PubMed

Melro M.C., Mariano M. 1987. Extra-tissular Schistosoma mansoni egg granulomata in the peritoneal cavity of mice. Memórias do Instituto Oswaldo Cruz, 82(Suppl. 4), 245–252.10.1590/s0074-02761987000800047Search in Google Scholar PubMed

Michaels R.M., Prata A. 1968. Evolution and characteristics of Schistosoma mansoni eggs laid in vitro. Journal of Parasitology, 54, 921–930. 10.2307/3277120Search in Google Scholar

Moore D.V., Meleney H.E. 1955. Development of Schistosoma mansoni in the peritoneal cavity of mice. Journal of Parasitology, 41, 235–245. 10.2307/3274197Search in Google Scholar

Neves R.H., Costa-Silva M., Martinez E.M., Branquinho T.B., Oliveira R.M., Lenzi H.L., Gomes D.C., Machado-Silva J.R. 2004. Phenotypic plasticity in adult worms of Schistosoma mansoni (Trematoda: Schistosomatidae) evidenced by brightfield and confocal laser scanning microscopies. Memórias do Instituto Oswaldo Cruz, 99, 131–136. 10.1590/s0074-02762004000200003Search in Google Scholar PubMed

Parra J.C., Doughty B., Colley D.G., Gazzinelli G. 1992. Human schistosomiasis mansoni: studies on in vitro granuloma modulation. Memórias do Instituto Oswaldo Cruz, 87(Suppl. 5), 79–81. 10.1590/s0074-02761992000900011Search in Google Scholar PubMed

Pearce E.J., MacDonald A.S. 2002. The immunobiology of schistosomiasis. Nature Reviews Immunology, 2, 499–511. 10.1038/nri843Search in Google Scholar PubMed

Pellegrino J., Faria J. 1965. The oogram method for the screening of drugs in Schistosomiasis mansoni. American Journal of Tropical Medicine and Hygiene, 14, 363–36910.1016/B978-0-08-011427-9.50072-XSearch in Google Scholar

Pellegrino J., Siqueira A.F. 1956. Técnica de perfusão para colheita de Schistosoma mansoni em cobaias experimentalmente infestadas. Revista Brasileira de Malariología e Doenças Tropicais, 8, 589–597. (In Portuguese)Search in Google Scholar

Pellegrino J., Oliveira C.A., Cunha A.S., Siqueira A.F. 1962. New approach to the screening of drugs in experimental schistosomiasis in mice. American Journal of Tropical Medicine and Hygiene, 11, 210–21510.4269/ajtmh.1962.11.201Search in Google Scholar

Pereira L.H., Coelho P.M., Fonseca J.J., Bredt A., Pellegrino J. 1972. Migration of Schistosoma mansoni larvae in the albino mouse. Revista do Instituto de Medicina Tropical de São Paulo, 14, 306–309Search in Google Scholar

Pereira L.H., Pellegrino J., Valadares T.E., Mello R.T., Coelho P.M. 1974. A new approach for screening prophylactic agents in schistosomiasis. Revista do Instituto de Medicina Tropical de São Paulo, 16, 123–126Search in Google Scholar

Prata A. 1957. Biópsia retal na esquistossomose mansoni: Bases e aplicações no diagnóstico e tratamento. Serviço Nacional de Educação Sanitária, Ministério da Saúde, Rio de Janeiro, pp. 197. (In Portuguese)Search in Google Scholar

Raso P., Bogliolo L. 1970. Patologia. In: (Ed. A.S. Cunha) Esquistossomose mansoni. Editora da Universidade de São Paulo, São Paulo, 77–130Search in Google Scholar

Raso P., Bernardes C., Tafuri W. L., Bogliolo L., Neves J. 1978. As dimensões do granuloma causado pelos ovos de Schistosoma mansoni no figado humano. Revista da Sociedade Brasileira de Medicina Tropical, 12, 45–49. 10.1590/ s0037-86821978000100008. (In Portuguese)Search in Google Scholar

Sandor M., Weinstock J.V., Wynn T.A. 2003. Granulomas in schistosome and mycobacterial infections: a model of local immune responses. Trends in Immunology, 24, 44–52. 10.1016/s1471-4906(02)00006-6Search in Google Scholar

Standen O.D. 1952. Experimental infection of Australorbis glabratus with Schistosoma mansoni. I. Individual and mass infection of snails, and the relationship of infection to temperature and season. Annals of Tropical Medicine and Parasitology, 46, 48–53. 10.1080/00034983.1952.11685504Search in Google Scholar

Stirewalt M.A., Kuntz R.E., Evans A.S. 1951. The relative susceptibilities of the commonly used laboratory mammals to infection by Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene, 31, 57–8210.4269/ajtmh.1951.s1-31.57Search in Google Scholar PubMed

Valadares T.E., Coelho P.M.Z., Pellegrino J., Sampaio I.B.M. 1981. Schistosoma mansoni: aspectos da oviposição da cepa LE em camundongos infectados com um casal de vermes. Revista do Instituto de Medicina Tropical de São Paulo, 23, 6–11. (In Portuguese)Search in Google Scholar

Yolles T.K., Moore D.V., Meleney H.E. 1949. Post-cercarial development of Schistosoma mansoni in the rabbit and hamster after intraperitoneal and percutaneous infection. Journal of Parasitology, 35, 276–294. 10.2307/3273303Search in Google Scholar

Received: 2016-4-8
Revised: 2016-10-20
Accepted: 2016-10-21
Published Online: 2016-12-28
Published in Print: 2017-3-1

© 2017 W. Stefański Institute of Parasitology, PAS