Systematic review of the helminth community in opossums of the genus Didelphis (Family: Didelphidae)
DOI:
https://doi.org/10.5380/avs.v30i3.98575Resumo
Gambás são animais de grande importância para a saúde pública devido à sua versatilidade e adaptabilidade aos ambientes. Sua diversidade alimentar acaba expondo esses animais a muitos parasitas gastrointestinais, incluindo aqueles de interesse zoonótico. No entanto, a literatura técnico-científica é limitada e com poucos estudos abordando a diversidade de helmintos parasitários encontrados em gambás, principalmente quando se considera o poliparasitismo. Dado o número limitado de relatos, é crucial atualizar os achados existentes, principalmente quanto à localização e espécie de Didelphis, para incentivar novas pesquisas. Este artigo é uma revisão sistemática da literatura qualitativa e quantitativa com foco na descrição de helmintos relatados em gambás do gênero Didelphis no período de 1948 a setembro de 2024. A busca ativa foi realizada por meio da busca de artigos em todos os idiomas nas plataformas SciELO, PubMed e BVS, adotando a combinação dos descritores em inglês registrados na BVS: Helminths e Didelphis com o operador booleano AND. Após a aplicação dos critérios de inclusão e exclusão ao longo de quase 77 anos, foram encontrados 111 artigos somando as três bases de dados dentro do período estipulado. Com a aplicação dos critérios de inclusão e exclusão, 68 trabalhos formaram o presente estudo. Com base na revisão, 4 espécies de gambás do gênero Didelphis são as espécies com mais dados publicados. Neste grupo, a diversidade de parasitas é grande tanto entre as classes quanto entre as espécies devidamente identificadas. No entanto, poucos estudos foram realizados no Brasil, e estes foram principalmente em espécimes da região Norte. Por se tratar de uma região que possui grande presença de espécies e um ambiente particular, estudos mais aprofundados são de interesse, dada a riqueza de famílias e espécies relatadas.
Referências
Acosta-Virgen K, López-Caballero J, García-Prieto L, et al. Helminths of three species of opossums (Mammalia, Didelphidae) from Mexico. Zookeys. 511; 131-152. 2015. (https://doi.org/10.3897/zookeys.511.9571)
Adnet FAO, Anjos DHS, Menezes-Oliveira A, et al. Further description of Cruzia tentaculata (Rudolphi, 1819) Travassos, 1917 (Nematoda: Cruzidae) by light and scanning electron microscopy. Parasitology Research. 104; 1207-1211. 2009. (https://10.1007/s00436-008-1316-6)
Aragón-Pech RA, Ruiz-Piña HA, Rodrígues-Vivas RI, et al. Prevalence, Abundance, and Intensity of Eggs and Oocysts of Gastrointestinal Parasites in the Opossum Didelphis virginiana Kerr, 1792 in Yucatan, Mexico. Helminthologia. 55(2); 119-126. 2018. (https://doi.org/10.2478/helm-2018-0008)
Babero BB. Further studies on helminths of the opossum, Didelphis virginiana, with a description of a new species from this host. Journal of Parasitology. 46; 445-463. 1960.
Bezerra-Santos MA, Furtado LFV, Rabelo EML, et al. High prevalence of Ancylostoma caninum infection in black-eared opossums (Didelphis aurita) in an urban environment. Parasitology Research. 119; 2343-2346. 2020. (https://doi.org/10.1007/s00436-020-06708-1)
Bezerra-Santos, MA, Fontes CS, Nogueira BCF, et al. Gastrointestinal parasites in the opossum Didelphis aurita: Are they a potential threat to human health? Journal of Parasitology. 44(2); 355-363. 2020. (https://doi.org/10.1007/s12639-020-01205-9)
Boullosa RG, Costa-Neto S, Morgado L, et al. A longitudinal survey of gastrointestinal parasites of the black-eared opossum Didelphis aurita at an urban-sylvatic interface area in Southeast Brazil: a morphological and ecological characterization based on helminth eggs. Parasitology Research. 120(11); 3815-3825. 2021. (https://doi.org/10.1007/s00436-021-07314-5)
Bowman DD, Smith JL, Little MD. Lagochilascaris sprenti sp. n. (Nematoda: ascarididae) from the opossum, Didelphis virginiana (Marsupialia: didelphidae). Journal of Parasitology. 69(4); 754-760. 1983.
Campbell ML, Gardner SL, Navone GT. A New Species of Mathevotaenia (Cestoda: Anoplocephalidae) and other Tapeworms from Marsupials in Argentina. Journal of Parasitology. 89(6); 1181-1185. 2003. (https://doi.org/10.1645/GE-1778)
Cañeda-Guzmán IC, Chambrier A, Scholz T. Thaumasioscolex didelphidis N. Gen., N. Sp. (Eucestoda: Proteocephalidae) from the Black-Eared Opossum Didelphis marsupialis from Mexico, the First Proteocephalidean Tapeworm from a Mammal. Journal of Parasitology. 87(3); 639-646. 2001. (https://doi.org/10.1645/0022-3395(2001)087[0639:TDNGNS]2.0.CO;2)
Cardoso TS, Andreazzi CS, Maldonado-Junior A, et al. Functional traits shape small mammal-helminth network: patterns and processes in species interactions. Parasitology. 148(8); 947-955. 2021. (https://doi:10.1017/S0031182021000640)
Chagas CRF, Monticelli C, Lima CFM, et al. Parasites Diversity, Abundance, Prevalence, and Richness Infecting Didelphis aurita (Didelphimorphia: Didelphidae) in the Atlantic Rainforest, Brazil. Pathogens. 13(806); 1-13,2024. (https://doi.org/10.3390/pathogens13090806)
Chagas-Moutinho VA, Oliveira-Menezes A, Cárdenas MQ, et al. Further description of Aspidodera raillieti (Nematoda: Aspidoderidae) from Didelphis marsupialis (Mammalia: Didelphidae) by light and scanning electron microscopy. The Journal of Parasitology. 101; 1331-1336. 2007. (https://10.1007/s00436-007-0641-5)
Chagas-Moutinho VA, Sant’Anna V, Oliveira-Menezes A, et al. New Aspidoderidae species parasite of Didelphis aurita (Mammalia: Didelphidae): A light and scanning electron microscopy approach. Acta Tropica. 130; 162-166. 2014. (https://doi.org/10.1016/j.actatropica.2013.10.005)
Cirino BS, Costa-Neto SF, Cardoso TS, et al. Gleasonian structure in the helminth metacommunity of the opossum Didelphis albiventris in two extremes of the Atlantic Forest. Journal of Helminthology. 96(7); 2022. (https://doi:10.1017/S0022149X21000791)
Cleveland CA, Eberhard ML, Garrett KB, et al. Dracunculus Species in Meso-mammals from Georgia, United States, and Implications for the Guinea Worm Eradication Program in Chad, Africa. Journal of Parasitology. 106(5); 616-622. 2020. (https://doi.org/10.1645/18-178)
Coelho PM, Dias M, Mayrink W, et al. Wild reservoirs of Schistosoma mansoni from Caratinga, an endemic schistosomiasis area of Minas Gerais State, Brazil. The American Journal of Tropical Medicine and Hygiene. 28(1); 163-164. 1979.
Costa-Neto SF, Cardoso TS, Boullosa RG, Metacommunity structure of the helminths of the black-eared opossum Didelphis aurita in peri-urban, sylvatic and rural environments in south-eastern Brazil. Journal of Helminthology. 93(6); 720-731. 2019. (https://doi:10.1017/S0022149X18000780)
Costa-Neto SF, Simões RO, Mota EM, et al. Lungworm Heterostrongylus heterostrongylus Travassos, 1925 from the black-eared opossum in South America: Morphologic, histopathological and phylogenetic aspects. Veterinary Parasitology, 228; 144-152. 2016. (https://doi.org/10.1016/j.vetpar.2016.08.018)
Crites JL. A redescription of Cruzia americana, a nematode parasitic in the opossum, Didelphis marsupialis virginiana. Journal of Parasitology. 42(1); 68-72. 1956.
Cruz ACMS, Prieto OH, Borda JT, et al. [Description of the external morphology of Duboisiella proloba Baer, 1983 (Trematoda: Strigeida) from Didelphis albiventris in Argentina, by scanning electron microscope]. Boletin chileno de Parasitologia. 55(3-4); 103-105. 2000.
Días-Camacho SP, Delgado-Vargas F, Willms K. et al. Intrahepatic growth and maturation of Gnathostoma turgidum in the natural definitive opossum host, Didelphis virginiana. Parasitology International. 59(3); 338-343. 2010. (https://doi.org/10.1016/j.parint.2010.04.004)
Diaw OT. Coexistence de nématodes trichostrongyloides chez des marsupiaux de Guyane [Coexistence of nematodes Trichostrongyloidea in marsupials from French Guyana (author's transl)]. Ann Parasitol Hum Comp. 51(3); 355-363. 1976.
Díaz-Camacho SP, Willms K, Rendón-Maldonado JG, et al. Discovery of an Endemic Area of Gnathostoma turgidum Infection among Opossums, Didelphis virginiana, in Mexico. Journal of Parasitology. 95(3); 617-622. 2009. (https://doi.org/10.1645/GE-1871.1)
Dubois G. Description de l'adulte présumé de Bursotrema tetracotyloides Szidat, 1960, et d'une nouvelle espèce du genre Didelphodiplostomum Dubois, 1944, parasites de Didelphis azarae Temminck, 1825 (Trematoda: Alariinae). Ann Parasitol Hum Comp. 51(3); 341-347. 1976.
Ducan Jr, RB, Reinemeyer CR, Funk RS. Fatal Lungworm Infection in an Opossum. Journal of Wildlife Diseases. 25(2); 266-269. 1989. (https://doi.org/10.7589/0090-3558-25.2.266)
Dunagan TT, Miler DM. Anatomy of the cerebral ganglion in Oligacanthorhynchus tortuosa (Acanthocephala) from the opossum (Didelphis virginiana). Journal of Parasitology. 67(6); 881-885. 1981.
Ellis RD, Pung OJ, Richardson DJ. Site selection by intestinal helminths of the Virginia opossum (Didelphis virginiana). Journal of Parasitology. 85(1); 1-5. 1999.
Esslinger JH, Smith JL. Dipetalonema (Acanthocheilonema) didelphis sp. n. (Nematoda: Filarioidea) from opossums, with a redescription of D. (A.) pricei (Vaz and Pereira 1934). Journal of Parasitology. 65(6); 928-933. 1979.
Faria MB, Melo FR. Didelphis imperfecta, Didelphimorphia, Didelphidae (Mondolfi & Pérez-Hernández, 1984): a new record in the Brazilian Amazon. Boletim da Sociedade Brasileira de Mastozoologia. 79; 44-46, 2017.
Freitas LC, Júnior-Maldonado A, Mendonça RFB, et al. Helminth community structure of Didelphis marsupialis (Didelphimorphia, Didelphidae) in a transition area between the Brazilian Amazon and the Cerrado. Revista Brasileira de Parasitologia Veterinária. 31(2); 1-12. 2022. (https://doi.org/10.1590/S1984-29612022031)
Freitas LC, Silva BEA, Vilela RV, et al. Morphological and Genetic Characterization of Didelphonema longispiculata (Nematoda: Spiruroidea) in the Black-Eared Opossum Didelphis marsupialis. Journal of Parasitology. 108(6); 627-636. 2022. (https://doi.org/10.1645/21-59)
García-Varela M, Andrade-Gómez L, López-Caballero J, et al. Morphological and molecular data reveal a new species of Lueheia (Acanthocephala: Plagiorhynchidae) from Turdus migratorius (Turdidae) in central Mexico and its phylogenetic implications within the family. Parasitology Research. 119; 3221-3231. 2020. (https://doi.org/10.1007/s00436-020-06748-7)
Gardner AL. Mammals of South America, Volume 1. University of Chicago Press. 690p. 2008. (http://dx.doi.org/10.7208/chicago/9780226282428.001.0001)
Gerhold RW, Kurth K, Claiborne A, et al. Survey of Baylisascaris spp. in Eastern Tennessee Wildlife and Detection of Baylisascaris spp. Eggs in Virginia Opossum (Didelphis virginiana) Feces. Journal of Wildlife Diseases. 54(4); 874-876. 2018. (https://doi.org/10.7589/2017-12-303)
Gray JB, Anderson RC. Observations on Turgida turgida (Rudolphi, 1819) (Nematoda: Physalopteroidea) in the American Opossum (Didelphis Virginiana). Journal of Wildlife Diseases. 18(3); 279-285. 1982. (https://doi.org/10.7589/0090-3558-18.3.279)
Jimémez FA, Campbell ML, Byler C, et al. Gastrointestinal helminths of opossums (Mammalia: Didelphidae) from Bolivia. Parasitology. 151; 637-649. 2024. (https://doi.org/10.1017/S0031182024000490)
Jiménez FA, Catzeflis F, Gardner SL. Structure of Parasite Component Communities of Didelphid Marsupials: Insights From a Comparative Study. Journal of Parasitology. 97(5); 779-787. 2011. (https://doi.org/10.1645/GE-2711.1)
Jurkevicz RMB, Silva DA, Neto JMF, et al. Absence of Trichinella spp. Larvae in carcasses of road-killed wild animals in Paraná state, Brazil. Revista Brasileira de Parasitologia Veterinária. 31(4); 1-5. 2022. (https://doi.org/10.1590/S1984-29612022054)
Kim DT, Stewart TB, Bauer RW, et al. Parastrongylus (=Angiostrongylus) cantonensis is Now Endemic in Louisiana Wildlife. Journal of Parasitology. 88(5); 1024-1026. 2002. (https://doi.org/10.1645/0022-3395(2002)088[1024:PACNEI]2.0.CO;2)
Kinsella JM, Winegarner CE. A field study of Anatrichosoma infections in the opossum, Didelphis virginiana. Journal of Parasitology. 61(4); 779-781. 1975.
Kunt RE, Myers BJ, Moore JA, et al. Parasitological aspects of Schistosoma haematobium (Iran) infection in the American opossum (Didelphis marsupialis L.). International Journal for Parasitology. 5(1); 21-26. 1975. (https://doi.org/10.1016/0020-7519(75)90092-2)
Lamberski N, Reader JR, Cook LF, et al. A RETROSPECTIVE STUDY OF 11 CASES OF LUNGWORM (DIDELPHOSTRONGYLUS HAYESI) INFECTION IN OPOSSUMS (DIDELPHIS VIRGINIANA). Journal of Zoo and Wildlife Medicine. 33(2); 151-156. 2002. (https://doi.org/10.1638/1042-7260(2002)033[0151:ARSOCO]2.0.CO;2)
Li, L. Redescription of Cruzia americana Maplestone, 1930 (Nematoda: Kathlaniidae), a parasite of Didelphis virginiana (Kerr) (Mammalia: Didelphidae) in the USA. Systematic Parasitology. 96; 433-440. 2019. (ttps://doi.org/10.1007/s11230-019-09853-z)
López-Crespo RA, Lópes-Mayagoitia AL, Ramírez-Romero R, et al. PULMONARY LESIONS CAUSED BY THE LUNGWORM (DIDELPHOSTRONGYLUS HAYESI) IN THE OPOSSUM (DIDELPHIS VIRGINIANA) IN COLIMA, MEXICO. Journal of Zoo and Wildlife Medicine. 48(2): 404-412. 2017. (https://doi.org/10.1638/2016-0156R1.1)
Matey VE, Kuperman BI, Kinsella JM. Scanning Electron Microscopy of Turgida turgida (Nematoda: Spiruroidea), Parasite of the Virginia Opossum, Didelphis virginiana, From Southern California. Journal of Parasitology. 87(5); 1199-1202. 2001. (https://doi.org/10.1645/0022-3395(2001)087[1199:SEMOTT]2.0.CO;2)
Miller CL, Kinsella JM, Garner MM, et al. Endemic Infections of Parastrongylus (=Angiostrongylus) costaricensis in Two Species of Nonhuman Primates, Raccoons, and an Opossum From Miami, Florida. Journal of Parasitology. 92(2); 406-408. 2006. (https://doi.org/10.1645/GE-653R.1)
Monet-Mendoza A, Osorio-Sarabia D, García-Prieto L. Helminths of the Virginia Opossum Didelphis virginiana (Mammalia: Didelphidae) in Mexico. Journal of Parasitology. 91(1); 2013-2019. 2005. (https://doi.org/10.1645/GE-273R)
Nawa Y, Cruz-Otero MC, Zazueta-Ramos ML, et al. Is Gnathostoma turgidum an Annual Parasite of Opossums? Drastic Seasonal Changes of Infection in Didelphis virginiana in Mexico. Journal of Parasitology. 95(4); 908-912. 2009. (https://doi.org/10.1645/GE-1988.1)
Nettles VF, Prestwood AK, Davidson WR. SEVERE PARASITISM IN AN OPOSSUM. Journal of Wildlife Diseases. 11(3); 419-420. 1975. (https://doi.org/10.7589/0090-3558-11.3.419)
Nichelason AE, Rejmanek D, Dabritz HA, et al. Evaluation of Cruzia americana, Turgida turgida, and Didelphostrongylus hayesi Infection in the Virginia Opossum (Didelphis virginiana) and Risk Factors Along the California Coast. Journal of Parasitology. 94(5); 1166-1168. 2008. (https://doi.org/10.1645/GE-1363.1)
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Research Methods and Reporting. 2021. (https://doi.org/10.1136/bmj.n71)
Pence DB, Little MD. Anatrichosoma buccalis sp. n. (Nematoda: Trichosomoididae) from the Buccal Mucosa of the Common Opossum, Didelphis marsupialis L. The Journal of Parasitology. 58(4); 767-773. 1972. (https://doi.org/10.2307/3278311)
Pinto HA, Mati VLT, Melo AL. Toxocara cati (Nematoda: Ascarididae) in Didelphis albiventris (Marsupialia: Didelphidae) from Brazil: a case of pseudoparasitism. Revista Brasileira de Parasitologia Veterinária. 23(4); 522-525. 2014. (https://doi.org/10.1590/S1984-29612014074)
Prestwood AK, Nettles VF, Farrell RL. Pathologic manifestations of experimentally and naturally acquired lungworm infections in opossums. American Journal of Veterinary Research. 38(4); 529-532. 1977.
Prestwood AK. Didelphostrongylus hayesi gen. et sp. n. (Metastrogyloidea: Filaroididae) from the opossum, Didelphis marsupialis. Journal of Parasitology. 62(2); 272-275. 1976.
Ramírez-Cañas SA, Lopez-Caballero JD, Mata-López R. Morphological and Molecular Data Reveal Two New Species of Viannaia (Nematoda: Viannaiidae), Parasitizing Opossums (Mammalia: Didelphidae) in Mexico. Journal of Parasitology. 107(3); 388-403. 2021. (https://doi.org/10.1645/18-199)
Ribicich M, Gamble HR, Bope J, et al. Trichinella infection in wild animals from endemic regions of Argentina. Parasitology Research. 107; 377-380. 2010. (https://10.1007/s00436-010-1873-3)
Salgado-Maldonado G, Cruz-Reyes A. Porrorchis nickoli n. sp. (Acanthocephala: Plagiorhynchidae) from mammals in southeastern Mexico, first known occurrence of Porrorchis in the western hemisphere. Journal of Parasitology. 88(1); 146-152. 2002. (https://doi.org/10.1645/0022-3395(2002)088[0146:PNNSAP]2.0.CO;2)
Sandars DF. On some trematodes from the manicou, Didelphis marsupialis insularis (Allen) from the West Indies. Journal of Helminthology. 32(3); 145-158. 1958. (https://doi.org/10.1017/s0022149x00019556)
Silva MGQ, Costa HMA. Helminths of White-bellied Opossum from Brazil. Journal of Wildlife Diseases. 35(2); 371-374. 1999. (https://doi.org/10.7589/0090-3558-35.2.371)
Smith JL, Bowman DD, Little MD. Life cycle and development of Lagochilascaris sprenti (Nematoda: ascarididae) from opossums (Marsupialia: didelphidae) in Louisiana. Jornal of Parasitology. 69(4); 736-745. 1983.
Snyder DE, Hamir AN, Hanlon CA, et al. Lung Lesions in an Opossum (Didelphis virginiana) Associated with Capillaria didelphis. Journal of Wildlife Diseases. 27(1); 175-177. 1991. (https://doi.org/10.7589/0090-3558-27.1.175)
Souza R, Velela RV, Gentile R, et al. Population genetic structure and morphological diversity of Cruzia tentaculata (Nematoda: Ascaridida), a parasite of marsupials (Didelphinae), along the Atlantic Forest on the eastern coast of South America. Parasitology. 149(11); 1487-1504. 2022. (https://doi.org/10.1017/S0031182022000981)
Stewart TB, Dean D. Didelphonema longispiculata (Hill, 1939) Wolfgang, 1953 (Nematoda: Spiruroidea) and other helminths from the opossum (Didelphis marsupialis virginiana) in Georgia. Journal of Parasitology. 57(3); 687-688. 1971.
Teodoro AKM, Cutolo AA, Motoie G, et al. Gastrointestinal, skin, and blood parasites in Didelphis spp. from urban and sylvatic areas in São Paulo state. Veterinary Parasitology Regional Studies and Reports Brazil. 16; 1-7. 2019. (https://doi.org/10.1016/j.vprsr.2019.100286)
Torres-Montoya EH, Zazueta-Moreno JM, Osuna-Martínez LU, et al. Histopathological changes in the liver and stomach of Didelphis virginiana (Didelphimorphia: Didelphidae) during natural infection with Gnathostoma turgidum (Nematoda: Gnathostomidae). Journal of Helminthology. 92(6); 765-768. 2018. (https://doi:10.1017/S0022149X17000980)
Torres-Montoya H, Galaviz-Renteria X, Castillo-Ureta H, et al. Spontaneous Cure after Natural Infection with Gnathostoma turgidum (Nematoda) in Virginia Opossums (Didelphis virginiana). Journal of Wildlife Diseases. 50(2): 344-348. 2014. (https://doi.org/10.7589/2013-04-092)
Varella K, Vilela RV, Gentile R, et al. Population genetic structure and phenotypic diversity of Aspidodera raillieti (Nematoda: Heterakoidea), a parasite of Didelphini marsupials in Brazil's South and Southeast Atlantic Forest. Parasite & Vectors. 15(1); 1-19. 2022. (https://doi:10.1186/s13071-022-05288-6)
Vielmo A, Schwertz CI, Piva MM, et al. Eosinophilic meningoencephalitis caused by rat lungworm (Angiostrongylus cantonensis) migration in a white-eared opossum (Didelphis albiventris) with concurrent distemper virus in southern Brazil. Parasitology Research. 121(5); 1545-1549. 2022. (https://doi:10.1007/s00436-022-07471-1)
Zabott MV, Pinto SB, Viott AM, et al. Helmintofauna de Didelphis albiventris (Lund, 1841) no município de Palotina, Paraná, Brasil. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR. 20(1); 19-22. 2017.
Publicado
Como Citar
Edição
Seção
Licença
Este trabalho está licenciado sob uma licença Creative Commons Attribution-ShareAlike 4.0 International License.
Autores que publicam nesta revista concordam com os seguintes termos:
- Autores mantém os direitos autorais e concedem à revista o direito de primeira publicação, com o trabalho simultaneamente licenciado sob a Creative Commons - Atribuição 4.0 Internacional que permite o compartilhamento do trabalho com reconhecimento da autoria e publicação inicial nesta revista.
- Autores têm autorização para assumir contratos adicionais separadamente, para distribuição não-exclusiva da versão do trabalho publicada nesta revista (ex.: publicar em repositório institucional ou como capítulo de livro), com reconhecimento de autoria e publicação inicial nesta revista.
- Autores têm permissão e são estimulados a publicar e distribuir seu trabalho online (ex.: em repositórios institucionais ou na sua página pessoal) a qualquer ponto antes ou durante o processo editorial, já que isso pode gerar alterações produtivas, bem como aumentar o impacto e a citação do trabalho publicado.
