SciELO - Scientific Electronic Library Online

vol.50 issue4Alterations in lipid transfer to High-Density Lipoprotein (HDL) and activity of paraoxonase-1 in HIV+ patientsDot-Elisa for evaluation of hydatid cyst wall, protoscoleces and hydatid cyst fluid antigens in the serodiagnosis of cystic echinococcosis author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand



  • English (pdf)
  • Article in xml format
  • How to cite this article
  • SciELO Analytics
  • Curriculum ScienTI
  • Automatic translation


Related links


Revista do Instituto de Medicina Tropical de São Paulo

On-line version ISSN 1678-9946

Rev. Inst. Med. trop. S. Paulo vol.50 no.4 São Paulo July/Aug. 2008 



Biological implications of the phenotypic plasticity in the Schistosoma mansoni - Nectomys squamipes model


Implicações biológicas da plasticidade fenotípica no modelo Schistosoma mansoni - Nectomys squamipes



Elaine Machado MartinezI; Michele Costa-SilvaI; Renata Heisler NevesII; Regina Maria Figueiredo de OliveiraI; José Roberto Machado-SilvaI

ILaboratório de Helmintologia Romero Lascasas Porto, Disciplina de Parasitologia, Departamento de Microbiologia, Imunologia e Parasitologia, Faculdade de Ciências Médicas, Uerj, Rio de Janeiro, RJ, Brasil
IILaboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brasil





The water-rat Nectomys squamipes is mostly important non-human host in schistosomiasis mansoni transmission in Brazil, due to its susceptibility, high abundance and water-contact pattern. During experimental infection of N. squamipes with Schistosoma mansoni, adult worms show phenotypic plasticity. This finding led us to investigate whether biological behavior is also affected. This was assessed comparing the biological characteristics of four S. mansoni strains: BE (State of Belém do Pará), CE (State of Pernambuco), CMO (State of Rio Grande do Norte) and SJ (State of São Paulo) using laboratory-bred N. squamipes. The infection was monitored by determination of the pre-patent period, fecal egg output, egg viability, intestinal egg count and, infectivity rate. No biological modification was observed in these parameters. Overall results highlight that N. squamipes was susceptible to several S. mansoni strains, suggesting that it might contribute to the maintenance of schistosomiasis mansoni in Brazil.

Keywords: Schistosoma mansoni; Nectomys squamipes; Epidemiology; Biological study.


O rato d´água Nectomys squamipes é importante transmissor não-humano da esquistossomose. Durante a infecção experimental em N. squamipes, os vermes adultos apresentam plasticidade fenotípica. Esses achados levaram-nos a investigar se os aspectos biológicos também são afetados. Foram comparadas as características biológicas de quatro cepas de S. mansoni: BE (Estado de Belém do Pará), CM (Estado de Pernambuco), CMO (Estado do Rio Grande do Norte) e SJ (Estado de São Paulo), utilizando como modelo experimental N. squamipes criados e mantidos em laboratório. A infecção foi monitorada para a determinação do período pré-patente, eliminação de ovos nas fezes, viabilidade dos ovos, contagem de ovos retidos no intestino e infectividade. Nenhuma modificação biológica foi observada nesses parâmetros. Os resultados sugerem que o N. squamipes é susceptível a várias cepas de S. mansoni, contribuindo para a manutenção da esquistossomose no Brasil.




Parasites have profound effects on host ecology and their effects are often influenced by the magnitude of host susceptibility to parasites. Wild rodents live in different environments causing them to be especially susceptible to a broad range of parasites. Schistosoma mansoni is the most widespread of the human-infecting schistosomes. However, rodents in both the Africa and the Neotropics also develop natural infection1,9,24,35. In addition, the possibility of closing the S. mansoni cycle without human participation had been demonstrated with rodents2 or bovine22 acting as final host. In Brazil, the water rat Nectomys squamipes (Rodentia:Sigmodontinae) is an important non-human host in schistosomiasis transmission, due to its susceptibility, high abundance, water-contact pattern6, and daily activities4. Epidemiological surveys have demonstrated naturally-infected N. squamipes in several places: Maranhão, Alagoas, Sergipe, Bahia, Minas Gerais, São Paulo, Paraná and Rio de Janeiro31. The role of N. squamipes in the transmission of schistosomiasis in the municipality of Sumidouro, Rio de Janeiro, Brazil, has been reported by biological, epidemiological and ecological studies6. The results showed that levels of infections did not change when the human population was treated with anti-parasite drugs. The authors found in some occasions a positive correlation between infection rodent rates and infection human rates. Although schistosomiasis can provoke severe damages to humans, rodents are permissive hosts with life-long infections18, which do not affect their life span33 or reproductive capacity6. In addition, morphometric analysis of hepatic granulomas showed that all measurements were smaller in naturally infected N. squamipes compared to mice3. Another study made biological and histopathological comparisons between Brazilian laboratory-reared strains of S. mansoni (BH - Belo Horizonte, MG and SJ - São José dos Campos, SP) and newly strain (SR - Campinas, SP)38. The authors showed that at week eight post-infection, the new strain was less pathogenic than the other two, since a lower number of hepatic granulomas and a smaller granuloma size were found38. Earlier studies demonstrated that N. squamipes could also be used as an alternative animal model in basic biological studies on schistosomiasis20,34.

Host-induced morphological changes (phenotypic plasticity) have been described in parasitic flatworms which are maintained in different hosts rather than their natural25. Phenotypic plasticity also occurs in S. mansoni26. However, it remains to be seen whether the phenotypic plasticity has biological implications for this helminth. To this end, the course of S. mansoni infection was monitored in experimental-infected N. squamipes.



Animals husbandry - N. squamipes were bred from stock obtained from Laboratory of Biology and Control of Schistosomiasis mansoni, Department of Tropical Medicine, Oswaldo Cruz Institute5. Each rodent was housed conventionally in polypropylene cages (40 x 33 cm) with stainless steel screen covers. Rodent chow (Nuvilab CR1, Colombo, Paraná, Brazil) and water were given ad libitum. The experiments reported here comply with ethical procedures with investigated animals10.

Parasite maintenance and rat infection procedures - This study was conducted using four different S. mansoni Brazilian strains: BE - state of Pará (01°28'03"S; 48°29'18"W), CM - state of Pernambuco (08°00'08"S; 35°01'06"W), CMO - state of Rio Grande do Norte (05°45'54"S; 35°12'04"W), and SJ - state of São Paulo (08°45'48"S; 34°54'47"W). The life-cycle has been maintained through successive passages in SW mice and laboratory-reared sympatric snail: Biomphalaria glabrata (BE, CM and CMO strains) or B. tenagophila (SJ strain) for more than five years at Department of Malacology, Oswaldo Cruz Institute, Rio de Janeiro.

Groups of 10 rats (3-4 weeks), body weight (250-300 g) were infected by subcutaneous injection of ~250 cercariae from a single strain.

Parasite infection intensity - Stool samples were collected over a 24-h period, three times a week from each rat from day 42 until 61 following cercariae exposure. The feces were read in duplicate by the Kato-Katz method processed (Helminth Tec®, Belo Horizonte, Brazil) in order to determine the number of eggs per gram of stool (epg). The egg viability was determined according to the flame cell or/and miracidium motions in histological slides by light microscopy, as previously described21. On day 63 post-infection, all rats were killed by cervical dislocation. Adult worms were recovered from the portal system and mesenteric veins, counted in a stereomicroscope and infection rate was assessed as a percentage of cercariae that had matured into adult worms12.

Tissue egg counts - The intestines of infected rats were removed and divided into four equal regions of equal length (proximal, medial distal and cecum), as previously described33. After solubilization in 10% KOH solution, eggs were counted under a light microscope, and values were extrapolated to the total organ content, as described elsewhere21. A fecundity index was calculated by the total number of eggs trapped in tissues divided by the total number of female worms.

Statistical analysis - Data analysis was performed using the Statistical Package for Social Sciences (SPSS) version 9.0. Groups were compared using Mann-Whitney, Regression and linear correlation tests and analysis of variance (One Way Anova) and the post-hoc test of Tukey. To assess correlation between variables, Pearson correlation test was used. p £ 0.05 was considered as statistically significant.



Parasitological findings - All animals became infected. Egg laying began after 40 (BE and CM strains) or 42 days (CMO and SJ strains) of infection. Few eggs were present in the feces of N. squamipes during the first weeks of examination. The fecal egg-laying peaked on 47 (BE, CMO and SJ strains) or 51 dpi (CM strain) and decreasing thereafter (Fig. 1). The animals infected with the CM strain presented highest egg excretion level than other strains. Viable eggs were observed in all experimental groups.



Regarding the pre-patent period and overall fecal egg counts no significant differences (p > 0.05) were found (Table 1). The BE strain presented lower infectivity and fecal egg excretion. Eggs concentrated mainly in the distal section in the small intestine (Fig. 2) everyone strain (p = 0.406). The cecum harbored fewer eggs however, significant differences (p = 0.0001) were observed: 1% (CMO), 3% (CM), 7% (SJ) and 10% (BE). Regression and linear correlation analyses performed on the egg distribution demonstrated a correlation between tissue counts and total number of female worms (p = 0.001 and r = 0.885) and total fecal egg-laying (p = 0.005 and r = 0.805), only for CM strain.





The infectivity rate was similar between SJ and CM strains (29.4 ± 15.4), BE (20.6 ± 10.7) and CMO (16.9 ± 11.2) strains (Table 1) however, no significant difference (p = 0.213) was found. The male/female sex-ratio was 1:1.



The present findings pointed out the importance of obtaining comprehensive biological data, which should support epidemiological observations. Vertebrate hosts behave as biological filters to parasites selecting phenotypes and genotypes within natural populations8. Hence, parasites may recognize the physiological and biochemical conditions of their hosts that are of selective importance36. The ability to adjust growth and reproduction to immediate local conditions would have been of great interest adaptive value to parasites30. Moreover, a successful parasite established within the host is capable of developmental responses to host immune factors, which are closely linked to increase the probability of transmission7.

Preliminary investigations indicated that vertebrates host exerted strong influence on the morphological features of adult flatworms. The outcome of this interaction is that specimens maintained in other hosts rather than their normal ones display a phenotypic plasticity17,21,25,26. This result prompted us to next examine whether biological behavior is modified on account of the phenotypic plasticity.

The key issues in the occurrence of phenotypic plasticity are of biological and epidemiological relevancies. Regarding the experimental model employed here, biological characteristics were not affected, despite strains have been grown on mice for decades. It is worth emphasizing that all strains compared favorable with experiments using mice models. Adult worms attain "normal" dimensions16,27,29 and supernumerary testes lobes are found14,17,21,27. The biological characteristics were not affected, because the pre-patent period, tissue egg distribution and egg laying reproduced observations in mice15,21,28. Our results showed that CM strain presented highest egg excretion level than other strains. FERNANDEZ & THIENGO11 have proved that five populations of Biomphalaria straminea from Goiás State located in the central part of Brazil were susceptible to this schistosome strain. Only CMO strain showed lower egg count in the large intestine. This finding may reflect differences in the wandering capacity among the strains37. The female transportation towards egg-laying site is subordinated to male's complex and well-developed musculature19,23. We have previously described biometric variations in worms from CMO strain16.

In this study, overall results confirm that N. squamipes is a permissive host to S. mansoni17,18,20,32,33,34. It must be also emphasized that S. mansoni adult worms might detect signals from their environment and responding appropriately in a state-dependent manner could greatly enhance its fitness36. The present study highlights the importance of water rat as a reservoir host for S. mansoni strains that might contribute to dispersion of schistosomiasis mansoni in Brazil. Moreover, from a public health perspective, if schistosomiasis mansoni control program is to be instituted in areas where water rats are commom, the program should take into account their epidemiological role13. More comparative studies are needed to investigate the occurrence of phenotypic plasticity among field S. mansoni strains.



To Maria de Fátima Bastos Martins for technical assistance, Dr. Lygia dos Reis Corrêa for kindly supply of parasites and Dr. Paulo Sérgio D'Andrea for water rat facilities.



1. ALARCÓN DE NOYA, B.; POINTIER, J.P.; COLMENARES, C. et al. - Natural Schistosoma mansoni infection in wild rats from Guadeloupe: parasitological and immunological aspects. Acta trop., 68: 11-21, 1997.         [ Links ]

2. ANTUNES, C.M.; MILWARD DE ANDRADE, R.; KATZ, N.; COELHO, P.M. & PELLEGRINO, J. - Role of Nectomys squamipes squamipes in the epidemiology of Schistosoma mansoni. Ann. trop. Med. Parasit., 67: 67-73, 1973.         [ Links ]

3. COSTA-SILVA, M.; RODRIGUES-SILVA, R.; HULSTIJN, M. et al. - Natural Schistosoma mansoni infection in Nectomys squamipes: histopathological and morphometric analysis in comparison to experimentally infected N. squamipes and C3H/He mice. Mem. Inst. Oswaldo Cruz, 97(suppl. 1): 129-142, 2002.         [ Links ]

4. D'ANDREA, P.S.; FERNANDES, F.A.; CERQUEIRA, R. & REY, L. - Experimental evidence and ecological perspectives for the adaptation of Schistosoma mansoni Sambon, 1907 (Digenea: Schistosomatidae) to a wild host, the water-rat, Nectomys squamipes Brants, 1827 (Rodentia: Sigmodontinae). Mem. Inst. Oswaldo Cruz, 97(suppl. 1): 11-14, 2002.         [ Links ]

5. D'ANDREA, P.S.; HORTA, C.; CERQUEIRA, R. & REY, L. - Breeding of the water rat (Nectomys squamipes) in the laboratory. Lab. Anim., 30: 369-376, 1996.         [ Links ]

6. D'ANDREA, P.S.; MAROJA, L.S.; GENTILE, R. et al. - 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, 2000.         [ Links ]

7. DAVIES, S.J. & McKERROW, J.H. - Developmental plasticity in schistosomes and other helminths. Int. J. Parasit., 33: 1277-1284, 2003.         [ Links ]

8. DEANE, M.P.; MANGIA, R.H.; PEREIRA, N.M. et al. - Trypanosoma cruzi: strain selection by different schedules of mouse passage of an initially mixed infection. Mem. Inst. Oswaldo Cruz, 79: 495-497, 1984.         [ Links ]

9. DUPLANTIER, J.M. & SÈNE, M. - Rodents as reservoir hosts in the transmission of Schistosoma mansoni in Richard-Toll, Senegal, West Africa. J. Helminth., 74: 129-135, 2000.         [ Links ]

10. ELLERY, A.W. - Guidelines for specification of animals and husbandry methods when reporting the results of animal experiments. Working Committee for the Biological Characterization of Laboratory Animals/GV-SOLAS. Lab. Anim., 19: 106-108, 1985.         [ Links ]

11. FERNANDEZ, M.A. & THIENGO, S.C. - Susceptibility of Biomphalaria straminea (Dunker, 1848) from Serra da Mesa Dam, Goiás, Brazil to infection with three strains of Schistosoma mansoni Sambon, 1907. Mem. Inst. Oswaldo Cruz, 97(suppl. 1): 59-60, 2002.         [ Links ]

12. FREIRE, N.; RODRIGUES-SILVA, R.; MACHADO-SILVA, J.R. & REY, L. - 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. Mem. Inst. Oswaldo Cruz, 98: 783-787, 2003.         [ Links ]

13. GENTILE, R.; COSTA-NETO, S.F.; GONÇALVES, M.M. et al. - An ecological field study of the water-rat Nectomys squamipes as a wild reservoir indicator of Schistosoma mansoni transmission in an endemic area. Mem. Inst. Oswaldo Cruz, 101(suppl. 1): 111-117, 2006.         [ Links ]

14. HULSTIJN, M.; BARROS, L.A.; NEVES, R.H. et al. - Hermaphrodites and supernumerary testicular lobes in Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by brightfield and confocal microscopy. J. Parasit., 92: 496-500, 2006.         [ Links ]

15. KASSIM, O.O.; CHEEVER, A.W. & RICHARDS, C.S. - Schistosoma mansoni: mice infected with different worm strains. Exp. Parasit., 48: 220-224, 1979.         [ Links ]

16. MACHADO-SILVA, J.R.; GALVÃO, C.; OLIVEIRA, R.M.; PRESGRAVE, O.A. & GOMES, D.C. - Schistosoma mansoni Sambon, 1907: comparative morphological studies of some Brazilian strains. Rev. Inst. Med. trop. S. Paulo, 37: 441-447, 1995.         [ Links ]

17. MACHADO-SILVA, J.R.; GALVÃO, C.; PRESGRAVE, O.A.; REY, L. & GOMES, D.C. - Host-induced morphological changes of Schistosoma mansoni Sambon, 1907 male worms. Mem. Inst. Oswaldo Cruz, 89: 411-416, 1994.         [ Links ]

18. MACHADO-SILVA, J.R.; LANFREDI, R.M. & GOMES, D.C. - Morphological study of adult male worms of Schistosoma mansoni Sambon, 1907 by scanning electron microscopy. Mem. Inst. Oswaldo Cruz, 92: 647-653, 1997.         [ Links ]

19. MAIR, G.R.; MAULE, A.G.; SHAW, C. & HALTON, D.W. - Muscling in on parasitic flatworms. Parasit. today, 14: 73-76, 1998.         [ Links ]

20. MALDONADO Jr., A.; MACHADO E SILVA, J.R.; RODRIGUES E SILVA, R.; LENZI, H.L. & REY, L. - Evaluation of the resistance to Schistosoma mansoni infection in Nectomys squamipes (Rodentia: Cricetidae), a natural host of infection in Brazil. Rev. Inst. Med. trop. S. Paulo, 36: 193-198, 1994.         [ Links ]

21. MARTINEZ, E.M.; NEVES, R.H.; OLIVEIRA, R.M.; MACHADO-SILVA, J.R. & REY, L. - Características biológicas e morfológicas de cepas brasileiras de Schistosoma mansoni em Mus musculus. Rev. Soc. bras. Med. trop., 36: 557-564, 2003.         [ Links ]

22. MODENA, C.M.; COELHO, P.M.; BARBOSA, F.S. & LIMA, W.S. - Transmission of Schistosoma mansoni under experimental conditions using the bovine—Biomphalaria glabrata-bovine model. Rev. Inst. Med. trop. S. Paulo, 35: 11-16, 1993        [ Links ]

23. MORAND, S. & MULLER-GRAF, C.D. - Muscles or testes? Comparative evidence for sexual competition among dioecious blood parasites (Schistosomatidae) of vertebrates. Parasitology, 120: 45-56, 2000.         [ Links ]

24. MORAND, S.; POINTIER, J.P. & THERON, A. - Population biology of Schistosoma mansoni in the black rat: host regulation and basic transmission rate. Int. J. Parasit., 29: 673-684, 1999.         [ Links ]

25. MOUHAID, G.; CASANOVA, J.C. & MONÉ, H. - Plasticidad fenotípica y determinación sistemática de parásitos: el caso de Echinoparyphium elegans. Acta Parasit. Portuguesa, 4: 127, 1997.         [ Links ]

26. NEVES, R.H.; COSTA-SILVA, M.; MARTINEZ, E.M. et al. - Phenotypic plasticity in adult worms of Schistosoma mansoni (Trematoda:Schistosomatidae) evidenced by brightfield and confocal laser scanning microscopies. Mem. Inst. Oswaldo Cruz, 99: 131-136, 2004.         [ Links ]

27. NEVES, R.H.; PEREIRA, M.J.; OLIVEIRA, R.M.; GOMES, D.C. & MACHADO-SILVA, J.R. - Schistosoma mansoni Sambon, 1907: morphometric differences between adult worms from sympatric rodent and human isolates. Mem. Inst. Oswaldo Cruz, 93(suppl. 1): 309-312, 1998.         [ Links ]

28. NYINDO, M. & FARAH, I.O. - The baboon as a non-human primate model of human schistosome infection. Parasit. today, 15: 478-482, 1999.         [ Links ]

29. PARAENSE, W.L. & CORREA, L.R. - Observations on two biological races of Schistosoma mansoni. Mem. Inst. Oswaldo Cruz, 76: 287-291, 1981.         [ Links ]

30. POULIN, R. - The evolution of life history strategies in parasitic animals. Advanc. Parasit., 37: 107-134, 1996.         [ Links ]

31. REY, L. - Non-human vertebrate host of Schistosoma mansoni and schistosomiasis transmission in Brazil. Res. Rev. Parasit., 53: 13-25, 1993.         [ Links ]

32. RIBEIRO, A.C.; MALDONADO JUNIOR, A.; D'ANDREA, P.S.; VIEIRA, G.O. & REY, L. - Susceptibility of Nectomys rattus (Pelzen, 1883) to experimental infection with Schistosoma mansoni (Sambon, 1907): a potential reservoir in Brazil. Mem. Inst. Oswaldo Cruz, 93: 295-299, 1998.         [ Links ]

33. RODRIGUES E SILVA, R.; MACHADO E SILVA, J.R.; FAERSTEIN, N.F.; LENZI, H.L. & REY, L. - Natural infection of wild rodents by Schistosoma mansoni. Parasitological aspects. Mem. Inst. Oswaldo Cruz, 87(suppl. 1): 271-276, 1992.         [ Links ]

34. SOUZA, V.A.; RODRIGUES E SILVA, R.; MALDONADO JUNIOR, A.; MACHADO E SILVA, J.R. & REY, L. - Nectomys squamipes (Rodentia: Cricetidae) as an experimental model for Schistosomiasis mansoni. Mem. Inst. Oswaldo Cruz, 87 (suppl. 1): 277-280, 1992.         [ Links ]

35. THERON, A.; POINTIER, J.P.; MORAND, S.; IMBERT-ESTABLET, D. & BOREL, G. - Long-term dynamics of natural populations of Schistosoma mansoni among Rattus rattus in patchy environment. Parasitology, 104: 291-298, 1992.         [ Links ]

36. THOMAS, F.; BROWN, S.P.; SUKHDEO, M. & RENAUD, F. - Understanding parasite strategies: a state-dependent approach? Trends Parasit., 18: 387-390, 2002.         [ Links ]

37. VALADARES, T.E.; COELHO, P.M.; PELLEGRINO, J. & SAMPAIO, I.B. - Schistosoma mansoni: comparação da oviposição entre as cepas LE (Belo Horizonte), SP (São Paulo) e ST (Liberia) em camundongos. Rev. Inst. Med. trop. S. Paulo, 23: 1-5, 1981.         [ Links ]

38. YOSHIOKA, L.; Zanotti-Magalhães, E.M.; Magalhães, L.A. & Linhares, A.X. - Schistosoma mansoni: a study of pathogenesis of Santa Rosa strain (Campinas, SP, Brasil) in mice. Rev. Soc. bras. Med. trop., 35: 203-207, 2002.         [ Links ]



Prof. Dr. José Roberto Machado e Silva
Laboratório de Helmintologia Romero Lascasas Porto, Disciplina de Parasitologia, Departamento de Microbiologia, Imunologia e Parasitologia, Faculdade de Ciências Médicas, Uerj
Av. Prof. Manoel de Abreu 444, 5º andar
20550-031 Rio de Janeiro, RJ, Brasil. Fax: +55-21-587.6148

Received: 22 February 2008
Accepted: 30 June 2008
CNPq fellowship

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License