Skip to main content
Log in

Morphological and morphometric study of cercariae and adult worms of Schistosoma mansoni (SLM strain) isolated from infected mice

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

In northeastern Brazil, the schistosomiasis is historically endemic and considered as a public health problem. The Schistosoma mansoni São Lourenço da Mata (SLM—PE, Brazil) strain was used in several paper already published; however, morphological and morphometric studies about this strain was never done. In this work, scanning electron microscopy (SEM) was used in morphological and morphometric analysis of cercariae and adult worms. Cercariae were obtained from Biomphalaria glabrata snails and adult worms from mice, both infected by the S. mansoni SLM strain, fixed and prepared for SEM. The results showed that cercariae of S. mansoni measures 254.9 μm of length. The bodies are covered by spines, with a ventral sucker, an oral sucker with sensory receivers, and a pair of penetration glands in the head. The area of tail and body and the distance between suckers were 3,011.77, 1,530.32, and 42.9 μm, respectively. Adult worms of S. mansoni were divided into three main regions: the anterior, medial, and posterior, besides the gynecophoral canal in males. The measure of adult worms of S. mansoni was 4 mm males and 5 mm females. The anterior region length of the male was 470 μm and of the female 271 μm. All the parameters were assayed in ten samples. The morphometric values found in the SLM strain were smaller than other S. mansoni strains described in the literature as well as other helminths. This is the first morphological and morphometric study with the SLM strain of S. mansoni being extremely important for improving control strategies and life quality of the local population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figs. 1–6
Figs. 7–10
Figs. 11–16
Figs. 17–22
Figs. 23–28

Similar content being viewed by others

References

  • Abdul-Ghani R, Loutfy N, El Sahn A, Hassan A (2009) Current chemotherapy arsenal for Schistosomiasis mansoni: alternatives and challenges. Parasitol Res 104:955–965

    Article  PubMed  Google Scholar 

  • Abdul-Salam JB, Sreelatha S (2004) Description and surface topography of the cercaria of Austrobilharzia sp. (Digenea: Schistosomatidae). Parasitol Intern 53:11–21

    Article  CAS  Google Scholar 

  • Anderson LA, Cheever AW (1972) Comparison of geographical strains of Schistosoma mansoni in the mouse. Bull World Health Organ 46:233–242

    PubMed  CAS  Google Scholar 

  • Attallah AM, Wahba MA, Elsheikha HM, Abbas AT, Abdel Aziz MM, El-Hemaly MA (2008) Outcomes of Schistosoma mansoni infection in outbred albino mice exposed to Larvin contaminant. Parasitol Res 103:567–576

    Article  PubMed  CAS  Google Scholar 

  • Barbosa CS, Silva CB (1992) Epidemiologia da Esquistossomose mansônica no Engenho Bela Rosa, Município de São Lourenço da Mata, Pernambuco. Brasil Cad Saúde Públ 8(1):83–87

    Article  Google Scholar 

  • Barbosa CS, Barbosa FS (1998) Padrão epidemiológico da esquistossomose em comunidade de pequenos produtores rurais de Pernambuco. Brasil Cad Saúde Públ 14(1):129–137

    Article  Google Scholar 

  • Barbosa CS, Domingues ALC, Abath A (2001) Epidemia de esquistossomose aguda na praia de Porto de Galinhas. Pernambuco Brasil Cad Saúde Públ 17(3):725–728

    Article  CAS  Google Scholar 

  • Bogéa T, Caira JN (2001a) Chaetotaxy and ultrastructure of sensory receptors in the cercaria of a species of Allassogonoporus Olivier, 1938 (Digenea: Lecithodendriidae). Syst Parasitol 50:1–11

    Article  PubMed  Google Scholar 

  • Bogéa T, Caira JN (2001b) Ultrastructure and chaetotaxy of sensory receptors in the cercaria of a species of Allopodocotyle Pritchard, 1966 (Digenea: Opecoelidae). Mem Inst Oswaldo Cruz 96(2):205–214

    Article  PubMed  Google Scholar 

  • Brasil (2005) Ministério da Saúde. Secretaria de Vigilância em Saúde. Guia de vigilância epidemiológica, 6rd edn Brasília, Brasil, pp 297–298

  • Brasil (2011) Ministério da Saúde. Secretaria de Vigilância em Saúde. Sistema Nacional de Vigilância em Saúde, Relatório de Situação, Pernambuco, 5rd edn Brasília, Brasil, p.7

  • Burden CS, Ubelaker JE (1981) Schistosoma mansoni and Schistosoma haematobium: differences in development. Exp Parasitol 51:28–34

    Article  PubMed  CAS  Google Scholar 

  • Cavalcanti MGS, Araújo HRC, Paiva MHS, Silva GM, Barbosa CCGS, Silva LF, Brayner FA, Alves LC (2009) Ultrastructural and cytochemical aspects of Schistosoma mansoni cercaria. Micron 40:394–400

    Article  PubMed  CAS  Google Scholar 

  • Coles GC, Thurston JP (1970) Testes number in East African Schistosoma mansoni. J Helminthol 44:69–73

    Article  PubMed  CAS  Google Scholar 

  • Dolgikh, AV (1965) Trematode larvae, parasites in the Black Sea mollusk Nassa reticulata var. pontica Mont. Biologiya Morya Bentos Kiev. Nauk Dumka 122–138

  • Dorsey CH, Cousin CE, Lewis FA, Stirewalt MA (2002) Ultrastructure of the Schistosoma mansoni cercaria. Micron 33(3):279–323

    Article  PubMed  Google Scholar 

  • Duvall RH, Dewitt WB (1967) An improved perfusion technique for recovering adults schistosomes from laboratory animals. AmJTrop Med Hyg 16:483

    CAS  Google Scholar 

  • Engels D, Chitsulo L, Montresor A, Savioli L (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Trop 82:139–146

    Article  PubMed  CAS  Google Scholar 

  • FUNASA (2002) Fundação Nacional de Saúde Guia de Vigilância Epidemiológica, 1

  • Gobert GN, Stenzel DJ, McManus DP, Jones MK (2003) The ultrastructural architecture of the adult Schistosoma japonicum tegument. Int J Parasitol 33:1561–1575

    Article  PubMed  Google Scholar 

  • Gryseels B, Polman K, Clerinx J, Kestens L (2006) Human schistosomiasis. Lancet 368:1106–1118

    Article  PubMed  Google Scholar 

  • Gupta BC, Basch PF (1988) Surface maturation in female Schistosoma mansoni, S. mattheei and Schistosomatium douthitti. Int J Parasitol 18(2):275–280

    Article  PubMed  CAS  Google Scholar 

  • Hicks RM, Newmann J (1977) The surface structure of the tegument of Schistosoma haematobium. Cell Biol Intern Rep 1:157–167

    Article  CAS  Google Scholar 

  • Hockley DJ (1973) Ultrastructure of tegument of Schistosoma. Adv Parasitol 11:233–305

    Article  PubMed  CAS  Google Scholar 

  • Jiraungkoorskul W, Sahaphong S, Sobhon P, Riengrojpitak S, Kangwanrangsan N (2006) Schistosoma mekongi: the in vitro effect of praziquantel and artesunate on the adult fluke. Exp Parasitol 113:16–23

    Article  PubMed  CAS  Google Scholar 

  • Jones MK, Gobert GN, Zhang L, Sunderland P, McManus DP (2004) The cytoskeleton and motor proteins of human schistosomes and their roles in surface maintenance and host–parasite interactions. BioEssays 26:752–765

    Article  PubMed  CAS  Google Scholar 

  • Katz N, Chaves A, Pellegrino JÁ (1972) Simple device for quantitative stool thick-smear technique in mansonic schistosomiasis. Rev Inst Med Trop São Paulo 14:397–400

    PubMed  CAS  Google Scholar 

  • Katz N, Peixoto SV (2000) Análise crítica da estimativa do número de portadores de esquistossomose mansônica no Brasil. Rev Soc Bras Med Trop 33:3

    Article  Google Scholar 

  • Kock S, Böckeler W (1998) Observations on cercarial chaetotaxy as a means for the identification of European species of Trichobilharzia Skrjabin & Zakharow, 1920 (Digenea: Schistosomatidae). Syst Parasitol 43:159–166

    Article  Google Scholar 

  • Kuntz RE, Tulloch GS, Davidson DL (1976) Scanning electron microscopy of the integumental surfaces of Schistosoma haematobium. J Parasitol 62:63–69

    Article  PubMed  CAS  Google Scholar 

  • Kusel JR, Al-Adham BH, Doenhoff MJ (2007) The schistosome in the mammalian host: understanding the mechanisms of adaptation. Parasitol 134:1477–1526

    CAS  Google Scholar 

  • López-Alvarez ML (1980) Contribuição ao estudo ultra-estrutural do Schistosoma mansoni Sambon,1907. Dissertation, Federal University of Rio de Janeiro

  • Machado-Silva JR, Galvão C, Presgrave AO, Rey L, Gomes DC (1994) Host-induced morphological changes of Schistosoma mansoni Sambon, 1907 male worms. Mem Inst Oswaldo Cruz 89:411–416

    Article  PubMed  CAS  Google Scholar 

  • Machado-Silva JR, Galvão C, Oliveira RMF, Presgrave OAF, Gomes DC (1995) Schistosoma mansoni Sambon, 1907: comparative morphological studies of some Brazilian strains. Rev Inst Med Trop São Paulo 37:441–443

    Article  PubMed  CAS  Google Scholar 

  • Machado-Silva JR, Lanfredi RM, Gomes DC (1997) Morphological study of adult male worms of Schistosoma mansoni Sambon: 1907 by scanning electron microscopy. Mem Inst Oswaldo Cruz 92(5):647–653

    Article  PubMed  CAS  Google Scholar 

  • Machado-Silva JR, Silva CH, Pereira MJS, Pinto RM, Oliveira RMF, Gomes DC (2000) Evaluation of differences in Brazilian strains of Schistosoma mansoni cercariae of both sexes by means of morphometrics analysis. Mem Inst Oswaldo Cruz 95:839–842

    Article  PubMed  CAS  Google Scholar 

  • Machado-Silva JR, Neves RH, Ormond L, Hulstijn M, Gomes DC (2003) Caracterização de cepas de Schistosoma mansoni por morfometria de vermes adultos provenientes de infecção unissexual. Rev Soc Bras Med Trop 36(6):755–757

    Article  PubMed  Google Scholar 

  • Magalhães LA, Carvalho JF (1973) Estudo morfológico de Schistosoma mansoni pertencentes a linhagens de Belo Horizonte (MG) e de São José dos Campos (SP). Rev de Saúde Pública de São Paulo 7:289–294

    Article  Google Scholar 

  • Martinez EM, Neves RH, Oliveira RMF, Machado-Silva JR, Rey L (2003) Características biológicas e morfológicas de cepas brasileiras de Schistosoma mansoni em Mus musculus. Rev Soc Bras Med Trop 36(5):557–564

    Article  PubMed  Google Scholar 

  • Meuleman EA, Lyaruu DM, Khan MA, Holzmann PJ, Sminia T (1978) Ultrastructural changes in the body wall of Schistosoma mansoni during the transformation of the miracidium into the mother sporocyst in the snail host Biomphalaria pfeifferi. Z Parasitenkd 56(3):227–42

    Article  PubMed  CAS  Google Scholar 

  • Miller FH, Tulloch GS, Kuntz RE (1972) Scanning electron microscopy of integumental surface of Schistosoma mansoni. J Parasitol 58:693–698

    Article  PubMed  Google Scholar 

  • Nakano T, Fujino T, Washioka H, Tonosaki A, Goto K, Fried B (2003) Tegumentary papillae of Echinostoma caproni cercariae (Trematoda: Echinostomatidae). Parasitol Res 89:446–450

    PubMed  CAS  Google Scholar 

  • Neves RH, Pereira MJS, Oliveira RMF, Gomes DC, Machado-Silva JR (1998) Schistosoma mansoni Sambon, 1907: morphometrics differences between adult worms from sympatric rodent and human isolates. Mem Inst Oswaldo Cruz 93(1):309–312

    Article  PubMed  Google Scholar 

  • Neves RH, Oliveira AS, Machado-Silva JR, Coutinho EM, Lenzi HL, Gomes DC (2002) Phenotypic characterization of Schistosoma mansoni adult worms recovered from undernourished mice: a morphometric study focusing on the reproductive system. Rev Soc Bras Med Trop 35:405–407

    Article  PubMed  Google Scholar 

  • Neves, DP, Melo, AL, de Linardi, PM, Vitor, RWA (2005) Schistosoma mansoni. In: Atheneu (ed) Parasitologia Humana, 11rd edn. São Paulo, Brasil, pp 193–212

  • Oliveira AS, Barbosa AA Jr, Gomes DC, Machado-Silva JR, Barros AF, Neves RH, Coutinho EM (2003) Morphometric study of Schistosoma mansoni adult worms recovered from undernourished infected mice. Mem Inst Oswaldo Cruz 98(5):623–627

    Article  PubMed  Google Scholar 

  • Paraense WL, Corrêa LR (1981) Observations on two biological races of Schistosoma mansoni. Mem Inst Oswaldo Cruz 76:287–291

    Article  PubMed  CAS  Google Scholar 

  • Palombi A (1940) Gli stadi larvali del Trematodi del Golfo di Napoli. 3 contributo allo studio della morfologia, biologia e sistematica delle cercarie marine. Riv Parassitol 4:1–25

    Google Scholar 

  • Pearce EJ, MacDonald AS (2002) The immunobiology of Schistosomiasis. Nat Reviews 2:499–511

    Article  CAS  Google Scholar 

  • Pereira ASA, Padilha RJR, Lima-Filho JL, Chaves MEC (2011) Scanning electron microscopy of the human low-density lipoprotein interaction with the tegument of Schistosoma mansoni. Parasitol Res 109:1395–1402

    Article  PubMed  Google Scholar 

  • Rey L (2002) Schistosoma mansoni. In: Koogan G (ed) Bases da parasitologia médica, 2nd edn. Brasil, Rio de Janeiro, p 379

    Google Scholar 

  • Robson RT, Erasmus DA (1970) The ultrastructure, based on stereoscan observations, of the oral sucker of the cercaria of Schistosoma mansoni with special reference to penetration. Z Parasitenkd 35:76–86

    Article  PubMed  CAS  Google Scholar 

  • Rouquayrol, MZ, Filho, NA (2003) Epidemiologia e Saúde. In: Medsi (ed) Epidemiologia e Saúde, 6rd edn. Rio de Janeiro, Brasil

  • Russell-Pinto F, Bartoli F (2002) Cercaria sevillana n. sp., a new cercaria (Digenea: Microphallidae) from Nassarius reticulatus (L.) (Mollusca: Prosobranchia) in Portugal. Syst Parasitol 53:175–182

    Article  PubMed  Google Scholar 

  • Schneider O, Zelck UE (2001) Differential display analysis of hemocytes from schistosome-resistant and schistosome-susceptible intermediate hosts. Parasitol Res Berlin 87(6):489–491

    Article  CAS  Google Scholar 

  • Senft AW, Gibler WB (1977) Schistosoma mansoni tegumental appendages: scanning microscopy following thiocarbohydrazide-osmium preparation. AmJTrop Med Hyg 26:1169–1177

    CAS  Google Scholar 

  • Sobhon P, Koonchornboon T, Yuan HC, Upatham ES, Saitongdee P, Krautrachue M, Bubphaniroj P, Vongpayabal P (1986) Comparison of the surface morphology of adult Schistosoma japonicum (Chinese, Philippine and Indonesian strains) by scanning electron microscopy. Intern J Parasitol 16(3):205–216

    Article  CAS  Google Scholar 

  • Soliman GN, El Assal FM, Mansour NS, Garo K (1986) Comparison of two Egyptian strains of Schistosoma mansoni in hamsters. Z Parasitenkd 72:353–363

    Article  PubMed  CAS  Google Scholar 

  • Southgate VR, Knowles RJ (1977) On Schistosoma margrebowiei Le Roux, 1933: the morphology of the Egg, Miraeidium and Cerearia, the compatibility with Speeies of Bulinus, and development in Mesocricetus auratus. Z Parasitenk 54:233–250

    Article  PubMed  CAS  Google Scholar 

  • Southgate VR, Ross GC, Knowles RJ (1981) On Schistosoma leiperi Le Roux, 1955: scanning electron microscopy of adult worms, compatibility with species of Bulinus, development in Mesocricetus auratus, and isoenzymes. Z Parasitenkd 66:63–81

    Article  CAS  Google Scholar 

  • Souza FPC, Vitorino RR, Costa AP, Faria-Junior FC, Santana LA, Gomes AP (2011) Esquistossomose mansônica: aspectos gerais, imunologia, patogênese e história natural. Rev Bras Clin Med São Paulo 9(4):300–307

    Google Scholar 

  • Storey DM, Ogbogu VC (1991) Observations on third-stage larval and adults of Litomosoides carinii (Nematoda: Filarioidea) by scanning and transmission electron microscopy. Ann Trop Med Parasitol 85:111–121

    PubMed  CAS  Google Scholar 

  • Van der Werf M, Vlas SJ, Broker S, Looman CWN, Nagelkerke NJD, Habbema JDF, Engels D (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86:125–139

    Article  PubMed  Google Scholar 

  • Van Hellemond JJ, Retra K, Brouwers FHM, Bas WM, Balkom V, Yazdanbakhsh M, Shoemaker CB, Tielens AGM (2006) A function of the tegument of schistosomes: clues from the proteome and lipidome. Intern J Parasitol 36:691–699

    Article  Google Scholar 

  • Vitorino RR, Souza FPC, Costa AP, Faria-Junior FC, Santana LA, Gomes AP (2012) Esquistossomose mansônica: diagnóstico, tratamento, epidemiologia, profilaxia e controle. Rev Bras Clin Med São Paulo 10(1):39–45

    Google Scholar 

  • WHO (2012) World Health Organization. Schistosomiasis, Media Centre Fact sheet January, 115

    Google Scholar 

Download references

Acknowledgments

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). The authors would like to thank Dr. Humberto Bertão for their technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. E. C. Chaves.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pereira, A.S.A., Cavalcanti, N.L., Nascimento, G.A.F. et al. Morphological and morphometric study of cercariae and adult worms of Schistosoma mansoni (SLM strain) isolated from infected mice. Parasitol Res 112, 1087–1096 (2013). https://doi.org/10.1007/s00436-012-3235-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-3235-9

Keywords

Navigation