Abstract
During bacterial and viral pathogen investigation of 30 specimens of bats captured in periurban forest areas in the city of Belém, Pará, Brazil, a case of cerebral filariasis was observed. In the course of histopathological examination, adult filariae were found in pseudocystic cavities brain of Molossus barnesi (Molossidae) and classified morphologically as Litomosoides by the shape of the spicules—left spicule with a handle longer than the blade; right spicule curved, with a sclerotized heel supporting a dorsal notch; the area rugosa constituted by a ventral band of small longitudinal crests; tail rounded in males; long esophagus with a slightly glandular distal portion; and a muscular bent vagina. All the specimens lack a stoma (buccal capsule). We compared our filarioids with the description of specimens of Molossinema wimsatti. Morphological characteristics of M. wimsatti resemble the genus Litomosoides. Thus, we believe that M. wimsatti is a synonym of L. molossi Esslinger, 1973, and filarioid specimens from material reported by Lichtenfels et al. (Trans Am Micros Soc 100:216–219, 1981) and from de Souto et al. (J. Helminthol 1195:e65, 2021) most probably correspond to Litomosoides. We suggest that the reduction of the buccal capsule may be attributable to the ectopic location. No evidence of tissue responses by the host was observed. This is the first record of Litomosoides infecting brain tissue of Molossus barnesi from Brazil, representing a record of a new host species. More specimens of bats should be examined in order to find filarioids in the brain and verify its taxonomic position using molecular techniques.
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The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Amato JF, Amato SB (2010) Técnicas gerais para coleta e preparação de helmintos endoparasitos de aves. Ornitologia e Conservação: Ciência Aplicada, Técnicas De Pesquisa e Levantamento 16:369–393
Bain O, Petit G, Diagne M (1989) Étude de quelques Litomosoides parasites de Rongeurs; consequénces taxonomiques. Ann Parasitol Hum Comp 64:268–289. https://doi.org/10.1051/parasite/1989644268
Bain O, Babayan S, Gomes J, Rojas G, Guerrero R (2002) First account of the larval biology of a Litomosoides filaria, from a bat. Parassitologia 44:89–92
Bain O, Casiraghi M, Martin C, Uni S (2008) The Nematoda Filarioidea: critical analysis linking molecular and traditional approaches. Parasite 15:342–348. https://doi.org/10.1051/parasite/2008153342
Boussinesq M, Bain O, Chabaud AG, Gardon-Wendel N, Kamgno J, Chippaux JP (1995) A new filariid zoonosis of the cerebrospinal fluid of a man probably caused by Meningonema peruzzii, a parasite of the central nervous system of Cercopithecidae. Parasite 2:173–176. https://doi.org/10.1051/parasite/1995022173
Caballero E (1939) A new filariid from Mexican bats. Trans Amer Micr Soc 58:4–7. https://doi.org/10.2307/3222787
Caballero y Caballero E (1944) Una nueva especie del género Litomosoides y consideraciones acerca de los caracteres sistemáticos de las especies de este género. Anales Inst Biol Univ Nac Autón México 15: 383-388
Calderon A, Guzman C, Salazar-Bravo J, Figueiredo LT, Mattar S, Arrieta G (2016) Viral zoonoses that fly with bats: a review. Manter: J Parasite Biodivers 7:1–15. https://doi.org/10.13014/K2BG2KWF
de Souto EP, Oliveira AM, Campos EM, Vilela VL, de Barros CS, Dantas AF, Nogueira de Galiza GJ (2021) Molossinema wimsatti infection in the brain of Pallas’s mastiff bats (Molossus molossus). J Helminthol 1195:e65. https://doi.org/10.1017/S0022149X21000602
Desportes C (1946) Des filaires dans le tube digestif. Ann Parasitol Hum Comp 21:138–141. https://doi.org/10.1051/parasite/1946213138
Dreyer G, Dreyer P, Piessens WF (1999) Extralymphatic disease due to bancroftian filariasis. Braz J Med Biol Res 32:1467–1472. https://doi.org/10.1590/s0100-879x1999001200003
Dukes DC, Gelfand M, Gadd KG, Clarke VD, Goldsmid JM (1968) Cerebral filariasis caused by Acanthocheilonema perstans. Cent Afr J Med 14:21–27
Esslinger JH (1973) The genus Litomosoides Chandler, 1931 (Filarioidea: Onchocercidae) in Colombian bats and rats. J Parasitol 59:225–246. https://doi.org/10.2307/3278809
Fernandes TF, dos Santos AN, Furtado AP, de Vasconcelos FT, dos Santos JN (2019) A new species of Metadelphis Travassos, 1944 (Digenea: Dicrocoeliidae) from the gall-bladder of Molossus molossus (Pallas) (Chiroptera: Molossidae) in the Brazilian eastern Amazon. Syst Parasitol 96:617–624. https://doi.org/10.1007/s11230-019-09869-5
Fernandes TF, dos Santos JN, de Vasconcelos Melo FT, Achatz TJ, Greiman SE, Bonilla CC, Tkach VV (2021) Interrelationships of Anenterotrema (Digenea: Dicrocoeliidae) from Neotropical bats (Mammalia: Chiroptera) with description of a new species from Molossus molossus in Brazil. Parasitol Res 120:2003–2016. https://doi.org/10.1007/s00436-021-07133-8
Freitas JF, Mendonça JM (1961) Novo capilariineo do gênero Aonchotheca López-Neyra, 1949 (Nematoda, Trichuroidea). Mem Inst Oswaldo Cruz 59:59–63. https://doi.org/10.1590/S0074-02761961000100006
Gardner SL, Jiménez-Ruiz FA (2009) Methods of endoparasite analysis. In: Kunz T, Parsons S (eds) Ecological and behavioral methods for the study of bats. Johns Hopkins University Press, pp 795–805
Georgi JR, Georgi ME, Jiang J, Frongillo M (1987) Molossinema wimsatti gen. et sp. n. (Nematoda: Onchocercinae) from the brain of Molossus ater (Chiroptera: Molossidae). Proc Helminthol Soc Wash 54:225–230. https://doi.org/10.1017/S0022149X21000602
Guerrero R, Bain O, Attout T, Martin C (2006) The infective larva of Litomosoides yutajensis Guerrero et al., 2003 (Nematoda: Onchocercidae), a Wolbachia-free filaria from bat. Parasite 13:127–130. https://doi.org/10.1051/parasite/2006132127
Hayman DT, Bowen RA, Cryan PM, McCracken GF, O’Shea TJ, Peel AJ, Gilbert A, Webb CT, Wood JL (2013) Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses Public Health 60:2–21
Jimenez FA, Notarnicola J, Gardner SL (2021) Host-switching events in Litomosoides Chandler, 1931 (Filarioidea: Onchocercidae) are not rampant but clade dependent. J Parasitol 107:320–335. https://doi.org/10.1645/20-35
Lichtenfels JR, Bhatnagar KP, Whittaker FH, Frahm HD (1981) Filarioid nematodes in olfactory mucosa, olfactory bulb, and brain ventricular system of bats. Trans Am Micros Soc 100:216–219. https://doi.org/10.2307/3225804
Linnaeus C (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Laurentius Salvius: Holmiae, p 824
Milanez de Campos JR, Barbas CS, Filomeno LT, Fernandez A, Minamoto H, Filho JV, Jatene FB (1997) Human pulmonary dirofilariasis: analysis of 24 cases from São Paulo. Brazil Chest 112(3):729–733. https://doi.org/10.1378/chest.112.3.729
Mourão ED, Avilla LS, Lent H (2002) Redescrição de Litomosoides brasiliensis Almeida, 1936 (Nematoda: Filariidae) Parasito de Anoura caudifera (Chiroptera: Phyllostomidae). Mem Inst Oswaldo Cruz 97:495–499. https://doi.org/10.1590/S0074-02762002000400007
Notarnicola J, Bain O, Navone GT (2000) Two new species of Litomosoides (Nematoda: Filarioidea) in Sigmodontines (Rodentia: Muridae) from Rio De La Plata Marshland, Argentina. J Parasitol 86:1318–1325. https://doi.org/10.1645/0022-3395(2000)086[1318:TNSOLN]2.0.CO;2
Notarnicola J, Digiani MC, López PM (2010a) Redescriptions of the nematodes Litomosoides patersoni (Mazza, 1928) (Onchocercidae) and Stilestrongylus stilesi Freitas, Lent and Almeida, 1937 (Heligmonellidae) parasites of Holochilus chacarius (Rodentia, Cricetidae) from Salta, Argentina. J Parasitol 96:993–1001. https://doi.org/10.1645/GE-2448.1
Notarnicola J, Jiménez Ruíz FA, Gardner SL (2010b) Litomosoides (Nemata: Filarioidea) of bats from Bolivia with records for three known species and the description of a new species. J Parasitol 96(4):775–782. https://doi.org/10.1645/GE-2371.1
Orihel TC (1973) Cerebral filariasis in Rhodesia—a zoonotic infection? Am J Trop Med Hyg 22:596–599. https://doi.org/10.4269/ajtmh.1973.22.596
Orihel TC, Esslinger JH (1973) Meningonema peruzzii gen. et sp. n. (Nematoda: Filarioidea) from the central nervous system of African monkeys. J Parasitol 59:437–441. https://doi.org/10.2307/3278768
Otranto D, Diniz DG, Dantas-Torres F, Casiraghi M, de Almeida IN, dos Santos JN, Furtado AP, de Almeida EF, Bain O (2011) Human intraocular filariasis caused by Dirofilaria sp. nematode. Brazil Emerg Infect Dis 17:863–866. https://doi.org/10.3201/eid1705.100916
Oviedo MC, Notarnicola J, Miotti MD, Claps LE (2016) Emended description of Litomosoides molossi (Nematoda: Onchocercidae) and first records of Litomosoides species parasitizing argentinean bats. J Parasitol 102:440–450. https://doi.org/10.1645/15-776
Pallas PS (1766) Miscellanea zoologica. Quibus novae imprimis atque obscurae animalium species describuntur et observationibus iconibusque illustrantur. Petrum van Cleef. Hagí Comitum., xii + 224 pp.;14 pls
Petit G (1980) Sur les Filaires du genre Litomosa (Nematoda: Filarioidea), parasites de Chauves-souris. Bull Mus Natl Hist Nat 2:365–374
Sandground JH (1934) Description of a species of the filariid genus Litomosoides from Glossophaga soricina (Cheiroptera). Ann Mag Nat Hist 14:595–599. https://doi.org/10.1080/00222933408654934
Santana Lima VF, Rocha PA, Dias Silva MA, Beltrão-Mendes R, Ramo RA, Giannelli A, Rinaldi L, Cringoli G, Estrela PC, Alves LC (2018) Survey on helminths and protozoa of free-living neotropical bats from Northeastern Brazil. Acta Trop 185:267–272. https://doi.org/10.1016/j.actatropica.2018.06.002
Santos CP, Gibson DI (2015) Checklist of the helminth parasites of South American bats. Zootaxa 3937:471–499. https://doi.org/10.11646/zootaxa.3937.3.3
Shrivastava A, Arora P, Khare A, Goel G, Kapoor N (2017) Central nervous system filariasis masquerading as a glioma: case report. J Neurosurg 127:691–693. https://doi.org/10.3171/2016.9.JNS161092
Suteri P, Kaushal M (2020) Space occupying lesion of brain: an unusual site for a common infection. Diagn Cytopathol 782–784. https://doi.org/10.1002/dc.24455
Thatcher VE (1993) Trematódeos Neotropicais. Instituto Nacional de Pesquisas da Amazônia, Manaus, 553 pp.
Tibayrenc M, Bain O, Ramachandran CP (1979) Deux nouvelles Litomosa (Filarioidea) de chauve-souris. Bull Nat Hist Nat Paris 4(1):183–189
Vicente JJ, de Oliveira H, Gomes DC, Pinto RM (1997) Nematóides do Brasil. Parte V: Nematóides de Mamíferos. Rev Bras Zool 14(Suppl 1):1–452. https://doi.org/10.1590/S0101-81751997000500001
Wenk P (1967) The invasion route of the metacyclical larvae of Litomosoides carinii Chandler 1931 (Filariidae). Z Parasitenkd 28:240–263. https://doi.org/10.1007/BF00260265
Yorke W, Maplestone PA (1926) The Nematode parasites of vertebrates. J. and A. Churchill Ltd., London, U.K., p 536
Acknowledgements
The authors would like to thank the researcher Dr. Wilson Uieda, retired Professor at the Universidade Estadual Paulista Júlio de Mesquita Filho, Botucatu campus, for his collaboration with the taxonomic identification of bats, as well as the Programa de Pós-graduação em Saúde e Produção Animal na Amazônia (PPGSPAA-UFRA). PIBIC-CNPq, Brazil for the granted to CA, JC, JS, EF, and PNPD-CAPES, Brazil for the granted to DFC.
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DFC-WLP-CA-NS: conceptualization, investigation, methodology, supervision and writing—original draft preparation. JC-JS-EF-MB-SA-NS: formal analysis, investigation and methodology. JN-SLG: investigation, methodology, writing—review and editing.
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Conga, D.F., Araújo, C.Y., Souza, N.F. et al. Cerebral filariasis infection with Litomosoides in Molossus barnesi (Chiroptera: Molossidae) in the Brazilian eastern Amazon, with comments on Molossinema wimsatti Georgi, Georgi, Jiang and Fronguillo, 1987. Parasitol Res 123, 125 (2024). https://doi.org/10.1007/s00436-024-08139-8
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DOI: https://doi.org/10.1007/s00436-024-08139-8