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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.28 no.4 Jaboticabal Oct./Dec. 2019  Epub Oct 10, 2019 

Short Communication

Parasitological and histological aspects of Holochilus sciureus naturally infected by Schistosoma mansoni

Aspectos parasitológicos e histológicos de Holochilus sciureus naturalmente infectados por Schistosoma mansoni

Nêuton da Silva-Souza1 

Ana Patrícia de Carvalho da Silva2 

Renata Mondego de Oliveira3 

Maria Gabriela Sampaio Lira4 

Ranielly Araújo Nogueira4 

Tatiane Aranha da Penha-Silva5 

Solange de Araújo Melo5 

Fábio Henrique Evangelista de Andrade5 

Larissa Sarmento dos Santos-Ribeiro5 

Alcina Vieira de Carvalho Neta1 

Ana Lucia Abreu-Silva5  *

1Departamento de Química e Biologia, Universidade Estadual do Maranhão – UEMA, São Luís, MA, Brasil

2Universidade Federal do Tocantins – UFT, Araguaína, TO, Brasil

3Rede Nordeste de Biotecnologia – RENORBIO, Universidade Federal do Maranhão – UFMA, São Luís, MA, Brasil

4Programa de Pós Graduação em Ciências da Saúde, Universidade Federal do Maranhão – UFMA, São Luís, MA, Brasil

5Departamento de Patologia, Universidade Estadual do Maranhão – UEMA, São Luís, MA, Brasil


Schistosomiasis is a neglected disease that affects millions of people around the world, being common in the state of Maranhão. A total of 225 rodents of the Holochilus sciureus species from the Western Lowland Maranhão were studied, of which 144 animals (64%) exhibited Schistosoma eggs in their feces samples. Macroscopic lesions characterized as well-defined whitish areas on the liver and spleen surfaces were observed. Histopathological examination revealed multifocal granulomas in the esophagus, liver, spleen, pancreas and duodenum, with structures compatible with Schistosoma mansoni eggs, as well as severe hepatic micro-vacuolar degeneration, multifocal and coalescent, with proliferation of random bile ducts and associated epithelial hyperplasia to areas of fibrosis. Adult forms of the parasite were observed in the blood vessels of the portal space. The lungs exhibited moderate and diffuse interstitial pneumonia with intralesional S. mansoni eggs. In the kidneys, hyaline cylinders were observed in the pelvis and diffuse hemorrhage. In conclusion, H. sciureus displays a pathological picture similar to human being. This rodent plays a role as sentinel in Baixada Maranhense.

Keywords:  Rodent; schistosomiasis; histopathology; host


A esquistossomose é uma doença negligenciada que afeta milhões de pessoas em todo o mundo, sendo comum no estado do Maranhão. Um total de 225 roedores da espécie Holochilus sciureus da Planície Ocidental do Maranhão foram estudados, dos quais 144 animais (64%) apresentaram ovos de Schistosoma em suas fezes. Lesões macroscópicas caracterizadas como áreas esbranquiçadas bem definidas nas superfícies do fígado e baço foram observadas. O exame histopatológico revelou granulomas multifocais no esôfago, fígado, baço, pâncreas e duodeno, com estruturas compatíveis com ovos de Schistosoma mansoni, degeneração micro-vacuolar hepática grave, multifocal e coalescente, com proliferação de ductos biliares aleatórios e hiperplasia epitelial associada a áreas de fibrose. Formas adultas do parasito foram observadas nos vasos sanguíneos do espaço portal. Os pulmões exibiram pneumonia intersticial moderada e difusa com ovos de S. mansoni intralesionais. Nos rins, foram observados cilindros hialinos na pelve e hemorragia difusa. Em conclusão, H. sciureus apresenta um quadro patológico semelhante ao ser humano. Este roedor desempenha um papel de sentinela na Baixada Maranhense.

Palavras-chave:  Roedor; esquistossomose; histopatologia; hospedeiro

Schistosomiasis is the second most important parasitic disease worldwide, in terms of impact on public health. It is estimated that it affects approximately 200 million people around the world and is responsible for 200,000 deaths per year (COLLEY et al., 2014). Schistosoma mansoni is the causative agent of schistosomiasis in Brazil and the intermediate host is a fresh water snail of the genus Biomphalaria (KATZ et al., 1972; MIRANDA et al., 2015).

In the Brazilian state of Maranhão, schistosomiasis remains a public health problem (MENDES et al., 2017), predominantly in the western lowlands, which are one of the poorest regions in the state. This micro-region contains vegetations formed by immense flooded fields, which facilitates the incorporation of routine activities. Thus, schistosomiasis is characterized as an occupational disease in this region, once people who live there have several reasons for maintaining contact with contaminated water (FERREIRA et al., 1998). Additionally, other authors (BASTOS et al., 1982, 1985; MIRANDA et al., 2015; LIRA et al., 2016) have reported the participation of a wild rodent named Holochilus sciureus in the epidemiology of schistosomiasis.

All these aspects, combined with the existence of a climate that favors the spread of S. mansoni and the presence of natural vectors (CANTANHEDE et al., 2014) seem to favor the expansion and establishment of schistosomiasis in the western lowlands. The aim of the present study was to describe natural infection in H. sciureus, an alternative host, addressing its parasitological and histological aspects.

The present study was performed in the municipality of São Bento (02°41’45”S and 44°49’17”W, 2 m above sea level), in the micro-region of West Lowland (Brazil), an endemic area for schistosomiasis. During one year, from August 2013 to July 2014, twenty Tomahawk live traps were placed near a swamp area at 10-m spacing for one night per month. Fecal samples were collected from each of the 225 rodents caught and analyzed using the Kato-Katz methods (KATZ & ALMEIDA, 2003).

Among 144 positive rodents, 126 animals were released back to the nature, and 18 were euthanized in a CO2 chamber. This experiment was approved by the Ethics Committee on Animal Experimentation of the Universidade Estadual do Maranhão, under protocol number 05/2014. All experiments strictly followed the institutional guidelines for the care and use of animals (IBAMA license number 14345-3 and registration number 543545).

Fragments of liver, spleen, esophagus, small intestine and lung of euthanized animals were collected and fixed in formalin (10%) for 2 hours. Afterwards, organs samples were processed into a paraffin block. Paraffin-embedded tissues were sectioned at 5 µm and stained with Hematoxylin and Eosin (H&E).

The result showed that among 144 animals out 225 rodents (64%) exhibited Schistosoma eggs in their feces samples. Despite the fact that the capture process was performed over 11 months, animals parasitized by S. mansoni were only found in the dry season (from August to November). Schistosomiasis is a neglected disease and its prevalence in Maranhão State ranges 9 to 12% (CANTANHEDE et al., 2011). However, in Baixada Maranhense (western lowlands) that is composed by 21 municipalities the true prevalence of this disease is unknown.

Studies performed in one of these municipalities, São Bento, showed that H. sciureus, previously classified as Holochilus brasiliensis can play a role as a reservoir for S. mansoni in this region, given that it has been found naturally infected and expels eggs worms in the feces and it reproduces a chronic disease when experimentally infected (BASTOS et al., 1982; BASTOS et al., 1985; SILVA-SOUZA & VASCONCELOS, 2005; LIRA et al., 2016). Since, the genus Holochilus can be considered as an important alternative definite host in the maintenance of the life cycle of Schistosoma (KAWAZOE & PINTO, 1983; MIRANDA et al., 2015; MARTINS et al., 2015). The high frequency of schistosomiasis in Maranhão is also related to occupational activities such as fishing and hunting.

The occurrence of natural infection in wild animal such as African monkey and -several species of rodents as Oxymycterus sp., Necromys lasiurus, Akodon spp., Sooretamys spp., Calomys spp., Proechimys sp., Cavia aperea, Rattus rattus and Rattus norvegicus was reported by Gentile et al. (2012). These authors also describe that genera Nectomys and Holochilus are involved in wild cycle of S. mansoni.

Besides that, in this area has been reported the occurrence of a wild strain of S. mansoni named S strain (MIRANDA et al., 2017) isolated from Biomphalaria glabrata, which in experimental condition showed three times more virulence to the snails than H strain isolated from miracidium obtained from human stools (BASTOS et al., 1984).

Natural infected rodent presented in the macroscopic exam, well-defined whitish areas were observed on the liver, spleen surfaces and free in the abdominal cavity (Figure 1), measuring about 1 mm. Histopathology showed in the liver multifocal periportal granulomas around ovoid structures, measuring approximately 35µm (diameter), with a thick, hyaline, yellow wall, containing laterally projected spicules and miracidium, compatible with S. mansoni eggs (Figure 2A). The following alterations were also observed: severe, multifocal to coalescent, micro-vacuolar degeneration; random bile duct proliferation; and epithelial hyperplasia associated with fibrosis areas. Adult forms of the parasite were frequently observed in the blood vessels of the portal space.

Figure 1 (A) Photomacrography of free adult worm of Schistosoma mansoni in abdominal region of Holochilus brasiliensis. (B) In the upper right corner adult worm in histological section stained with H&E, Bars = 400 µm. 

Figure 2 (A) Granuloma around Schistosoma mansoni eggs (thin arrows), containing miracidium (m) and bile duct proliferation (thick arrows) in the liver. (B) Inter alveolar septal thickening with histiocyte and lymphocyte infiltrate containing S. mansoni egg (thin arrow). (C) Granuloma with S. mansoni eggs (thin arrows) and epithelioid macrophages (thick arrow) in large intestine submucosa and (D) granuloma in exocrine portion of pancreas (thin arrow) containing S. mansoni egg. Hematoxylin and Eosin. Bars = 400 µm. 

Macro and microscopic analysis revealed changes on the liver surface (whitish areas, fibrosis, and granulomas) similar to the results of experimental studies with Mus musculus (CARVALHO et al., 1986; AMARAL et al., 2017) and Mus spretus (PÉREZ DEL VILLAR et al., 2013). The liver is the most affected organ by the infection and presence of of S. mansoni eggs (SILVA-SOUZA & VASCONCELOS, 2005; LOPES et al., 2006; SILVA et al., 2012; PÉREZ DEL VILLAR et al., 2013).

The histological analysis of the lungs exhibited moderate and diffuse interstitial pneumonia with intralesional S. mansoni eggs (Figure 2B). In the lamina propria of the duodenum and outer longitudinal muscle tunica was observed granulomas with rounded eggs, miracidium and epithelioid macrophages (Figure 2C). In the spleen, S. mansoni eggs were also observed both in white and red pulp.

The exocrine region of the pancreas exhibited multiple granulomas, containing neutrophils and eosinophils, as well as rounded eggs with miracidium (Figure 2D). There was an intense and diffuse infiltration of lymphocytes, histiocytes, plasma cells and eosinophils in the lamina propria of the esophagus, involving eggs. In the stomach, S. mansoni eggs were found in the crypts and, in the kidneys, hyaline cylinders in the pelvis and diffuse hemorrhage were observed. As demonstrated by our results Holochilus causes lesions in several organs, leading a severe picture of schistosomiasis. What could explain this severity? The S strain is also more pathogenic to the rodents as described by Bastos et al. (1984) to the snail? Or S. mansoni was recently introduced in this environment and the rodents did not adapt to the parasite infection?

In the present study, there was a high frequency of rodents with positive results in the stool examination and all euthanatized rodents developed a severe disease, characterized by the presence of granulomas in the liver, lungs, intestine and the exocrine part of the pancreas. In humans, the occurrence of hepatic granuloma, which are responsible for portal hypertension, is very common (GRYSEELS et al., 2006).

A high frequency of positive animals in stool examinations during the dry season has been reported (BASTOS et al., 1985). Flooding occurs in this area in the rainy season. In the beginning of this season, rodents that survived the drought probably deposit S. mansoni eggs in small water collections, promoting the infection of snails that subsequently infect humans or other rodents (LEAL et al., 2013; OLIVEIRA et al., 2013).

The control of schistosomiasis is very difficult in the studied area, due to the absence of adequate sanitary conditions, the use of water from the fields in activities like fishing, recreation and laundry, as well as the abundance of snails. In addition, the existence of wild rodents plays an important role in the maintenance of the life cycle of parasites. According to model-based-maps, socioeconomic, environmental and climatic factors contribute to the distribution of schistosomiasis in Brazil. Thus, a governmental intervention is necessary in order to control the disease and the presence of H. sciureus, an alternative host for S. mansoni in the epidemiological chain of schistosomiasis, in this area. In conclusion, H. sciureus reproduce a schistosomiasis picture that resembles human disease.


This work was supported by FAPEMA (Process REBAX-00921/11), and PROCAD NF 0681/10. Dr. Ana Lucia Abreu-Silva (CNPq n° 309542/2013-8) is a CNPq senior researcher.


Amaral KB, Silva TP, Dias FF, Malta KK, Rosa FM, Costa-Neto SF, et al. Histological assessment of granulomas in natural and experimental Schistosoma mansoni infections using Whole slide imaging. PLoS One 2017; 12(9): e0184696. PMid:28902908. [ Links ]

Bastos OC, Sadigursky M, Nascimento MDSB, Brazil R, Holanda JC. Holochilus sciureus nanus Thomas, 1897. Sugestão de modelo experimental para a filariose, leishmaniose e esquistossomose. Rev Inst Med Trop São Paulo 1984; 26(6): 307-315. PMid:6535233. [ Links ]

Bastos OC, Silva AMA, Souza EP, Lemos RC No, Piedrabuena AE. Ocorrência de linhagens humana e silvestre de Schistosoma mansoni, na pré-amazônia. I - Estudo em molusco. Rev Saude Publica 1982; 16(5): 292-298. PMid:7167724. [ Links ]

Bastos OC, Silva SMF, Leal GMJP, Bacelar JM No. Variações nos níveis das células sanguíneas periféricas encontradas em Holochilus brasiliensis nanus Thomas, 1897, infectados com Schistosoma mansoni Sambon, 1907, próprio da Pré-Amazônia. Rev Saude Publica 1985; 19(5): 431-437. PMid:3939165. [ Links ]

Cantanhede SPD, Fernandez MA, Mattos AC, Montresor LC, Silva-Souza N, Thiengo SC. Freshwater gastropods of the Baixada Maranhense Microregion, an endemic area for schistosomiasis in the State of Maranhão, Brazil: I - qualitative study. Rev Soc Bras Med Trop 2014; 47(1): 79-85. PMid:24603742. [ Links ]

Cantanhede SPD, Ferreira AP, Mattos IE. Esquistossomose mansônica no Estado do Maranhão, Brasil, 1997-2003. Cad Saude Publica 2011; 27(4): 811-816. PMid:21603764. [ Links ]

Carvalho ADV, Alvarenga RJ, Melo AL. Histopatologia da esquistossomose mansoni em fígado de Mus musculus infectado por amostras humanas de fase aguda e crônica da periferia de Belo Horizonte, Minas Gerais. Rev Soc Bras Med Trop 1986; 19(2): 89-94. PMid:3124224. [ Links ]

Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet 2014; 383(9936): 2253-2264. PMid:24698483. [ Links ]

Ferreira LA, Lima FL, Anjos MR, Costa JML. Forma tumoral encefálica esquistossomótica: apresentação de um caso tratado cirurgicamente. Rev Soc Bras Med Trop 1998; 31(1): 89-93. PMid:9477702. [ Links ]

Gentile R, Soares MS, Barreto MGM, Gonçalves MML, D’Andrea PS. The role of wild rodents in the transmission of schistosoma mansoni in Brazil. In: Rokni MB, editor. Schistosomiasis [online]. London: IntechOpen; 2012 [cited 2019 April 11]. p. 231-254. Available from: [ Links ]

Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006; 368(9541): 1106-1118. PMid:16997665. [ Links ]

Katz N, Almeida K. Esquistossomose, xistosa, barriga d’água. Cienc Cult 2003; 55(1): 38-41. [ Links ]

Katz N, Chaves A, Pellegrino J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 1972; 14(6): 397-400. PMid:4675644. [ Links ]

Kawazoe U, Pinto ACM. Importância epidemiológica de alguns animais silvestres na esquistossomose mansônica. Rev Saude Publica 1983; 17(5): 345-366. PMid:6658353. [ Links ]

Leal OB No, Gomes EC, Oliveira FJ Jr, Andrade R, Reis DL, Souza-Santos R, et al. Biological and environmental factors associated with risk of schistosomiasis mansoni transmission in Porto de Galinhas, Pernambuco State, Brazil. Cad Saude Publica 2013; 29(2): 357-367. PMid:23459821. [ Links ]

Lira MGS, Miranda GS, Rodrigues JGM, Nogueira RA, Gomes GCC, Cantanhêde LG, et al. Aspectos biológicos de Holochilus sp., hospedeiro natural da esquistossomose. Cienc Anim Bras 2016; 17(1): 143-153. [ Links ]

Lopes IC, Santos VR, Souza VLB, Rodrigues IRC. Histopathological study of Schistosoma mansoni infection in the murine model using the PC (Pará) and LILA (Maranhão) strains. Mem Inst Oswaldo Cruz 2006; 101(Suppl 1): 273-277. PMid:17308781. [ Links ]

Martins DS, Xavier MF, Masiero FS, Cordeiro J, Thyssen PJ. Schistosomiasis in Southern Brazil 17 years after the confirmation of the first autochthonous case. Rev Soc Bras Med Trop 2015; 48(3): 354-357. PMid:26108019. [ Links ]

Mendes MFC, Ribeiro DML, Melo BO, Bomfim MRQ. Epidemiological investigation of schistosomiasis mansoni in municipalities in the Maranhão State, Brazil. J Geospat Model 2017; 2(3): 12-18. [ Links ]

Miranda GS, Miranda BS, Rodrigues JGM, Lira MGS, Nogueira RS, Viegas-Melo D, et al. The wild water-rats and their relevance in the context of schistosomiasis mansoni in Brazil: what we know and recommendations for further research. Helminthologia 2017; 54(2): 165-169. [ Links ]

Miranda GS, Rodrigues JGM, Lira MGS, Nogueira RA, Gomes GCC, Silva-Souza N. Monitoramento de positividade para Schistosoma mansoni em roedores Holochilus sp. naturalmente infectados. Cienc Anim Bras 2015; 16(3): 456-463. [ Links ]

Oliveira DS, Santos VB, Melo AGS, Lima AS, Carvalho CD, Allegretti SM, et al. Schistosomiasis mansoni in urban Northeast Brazil: influence of rainfall regime on the population dynamics of Biomphalaria sp. Rev Soc Bras Med Trop 2013; 46(5): 654-657. PMid:24270258. [ Links ]

Pérez del Villar L, Vicente B, Galindo-Villardón P, Castellanos A, Pérez-Losada J, Muro A. Schistosoma mansoni experimental infection in Mus spretus (SPRET/EiJ strain) mice. Parasite 2013; 20: 27. PMid:23985166. [ Links ]

Silva AM, Côrrea CL, Neves RH, Machado-Silva JR. A high-fat diet associated with acute schistosomiasis mansoni causes disorganization in splenic architecture in mice. Exp Parasitol 2012; 132(2): 193-199. PMid:22781278. [ Links ]

Silva-Souza N, Vasconcelos SD. Histopathology of Holochilus brasiliensis (Rodentia: Cricetidae) infected with Schistosoma mansoni (Schistosomatida: Schistosomatidae). Rev Patol Trop 2005; 34(2): 145-150. [ Links ]

Received: April 11, 2019; Accepted: August 29, 2019

*Corresponding author: Ana Lucia Abreu-Silva, Departamento de Patologia, Universidade Estadual do Maranhão, Avenida Lourenço Vieira da Silva, CEP 65055-970, São Luís, MA, Brasil. e-mail:

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