Case report: Filarial infection of a parti-coloured bat: Litomosa sp. adult worms in abdominal cavity and microfilariae in bat semen

. 2023 ; 10 () : 1284025. [epub] 20230921

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu kazuistiky, časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37808105

BACKGROUND: Filarial infections have been understudied in bats. Likewise, little is known about pathogens associated with the reproductive system in chiropterans. While semen quality is critical for reproductive success, semen-borne pathogens may contribute to reproductive failure. METHODS: For the first time we performed electroejaculation and used computer-assisted semen analysis to provide baseline data on semen quality in a parti-coloured bat (Vespertilio murinus). RESULTS: The semen quality values measured in the V. murinus male appeared high (semen concentration = 305.4 × 106/mL; progressive and motile sperm = 46.58 and 60.27%, respectively). As an incidental finding, however, microfilariae were observed in the bat semen examined. At necropsy, eight adult filarial worms, later genetically identified as Litomosa sp., were found in the peritoneal cavity, close to the stomach, of the same particoloured bat male dying as a result of dysmicrobia and haemorrhagic gastroenteritis in a wildlife rescue centre. Histopathology revealed microfilariae in the testicular connective tissue and the epidydimal connective and fat tissues. A PCR assay targeting cytochrome c oxidase subunit 1 confirmed that adult worms from the peritoneal cavity and testicular microfilariae were of the same filarial species. Mildly engorged argasid mite larvae attached to the bat skin proved negative for filarial DNA and the adult filarial worms proved negative for endosymbiont Wolbachia. CONCLUSION: While the standard filarial life cycle pattern involves a vertebrate definitive host and an invertebrate vector, represented by a blood-sucking ectoparasite, our finding suggests that microfilariae of this nematode species may also be semen-borne, with transmission intensity promoted by the polygynous mating system of vespertilionid bats in which an infected male mates with many females during the autumn swarming. Presence of microfilariae may be expected to decrease semen quality and transmission via this route may challenge the success of reproductive events in females after mating. Further investigation will be necessary to better understand the bat-parasite interaction and the life cycle of this filarial worm.

Zobrazit více v PubMed

Gardner SL, Jiménez-Ruiz FA. Methods for the study of bats endoparasites In: Kunz TH, Parsons S, editors. Ecological and Behavioral Methods for the Study of Bats. Baltimore, Maryland: The Johns Hopkins University Press; (2009). 795–805.

Gardner SL, Whitaker JO. Endoparasites In: Barnard SM, editor. Bats in Captivity - Volume 1: Biological and Medical Aspects. Washington DC: Logos Press; (2009). 445–58.

Hosek J, Horácek I. Nematodes parasitizing the palaearctic bats: host-parasite relations In: Hanák V, Horáček I, Gaisler J, editors. European Bat Research. Praha: Charles University Press; (1987). 465–73.

Guerrero R, Martin C, Gardner SL, Bain O. New and known species of Litomosoides (Nematoda: Filarioidea): important adult and larval characters and taxonomic changes. Comp Parasitol. (2002) 69:177–95. doi: 10.1654/1525-2647(2002)069[0177:NAKSOL]2.0.CO;2 DOI

Junker K, Barbuto M, Casiragh M, Martin C, Uni S, Boomker J, et al. . Litomosa chiropterorum Ortlepp, 1932 (Nematoda: Filarioidea) from a south African miniopterid: redescription, Wolbachia screening and phylogenetic relationships with Litomosoides. Parasite. (2009) 16:43–50. doi: 10.1051/parasite/2009161043, PMID: PubMed DOI

Léger C. Bat parasites (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) in France (1762-2018): a literature review and contribution to a checklist. Parasite. (2020) 27:61. doi: 10.1051/parasite/2020051, PMID: PubMed DOI PMC

Martin C, Bain O, Jouvenet N, Raharimanga V, Robert V, Rousset D. First report of Litomosa spp. (Nematoda: Filarioidea) from Malagasy bats; review of the genus and relationships between species. Parasite. (2006) 13:3–10. doi: 10.1051/parasite/2006131003, PMID: PubMed DOI

Notarnicola J, Ruíz FAJ, Gardner SL. Litomosoides (Nemata: Filarioidea) of bats from Bolivia with records for three known species and the description of a new species. J Parasitol. (2010) 96:775–82. doi: 10.1645/GE-2371.1, PMID: PubMed DOI

Ohbayashi M, Kamiya H. Nematode parasites from Vespertilio orientalis Wallin. Jpn J Vet Res. (1979) 27:11–5. PMID: PubMed

Petit G. On filariae of the genus Litomosa, parasites of bats. Bulletin du Muséum National d’Histoire Naturelle, A (Zoologie, Biologie et Écologie Animales). (1980) 2:365–74. doi: 10.5962/p.283844 DOI

Ramasindrazana B, Dellagi K, Lagadec E, Randrianarivelojosia M, Goodman SM, Tortosa P. Diversity, host specialization, and geographic structure of filarial nematodes infecting Malagasy bats. PLoS One. (2016) 11:e0145709. doi: 10.1371/journal.pone.0145709, PMID: PubMed DOI PMC

Rendón-Franco E, López-Díaz O, Martínez-Hernández F, Villalobos G, Muñoz-García CI, Aréchiga-Ceballos N, et al. . Litomosoides sp. (Filarioidea: Onchocercidae) infection in frugivorous bats (Artibeus spp.): pathological features, molecular evidence, and prevalence. Trop Med Infect Dis. (2019) 4:77. doi: 10.3390/tropicalmed4020077 PubMed DOI PMC

Vogeler AV, Tschapka M, Kalko EKV, Cottontail VM. Litomosoides microfilaria in seven neotropical bat species. J Parasitol. (2018) 104:713–7. doi: 10.1645/15-719 PubMed DOI

de Souto E, Oliveira A, Campos É, Vilela V, De Barros C, Dantas A, et al. . Molossinema wimsatti infection in the brain of Pallas’s mastiff bats (Molossus molossus). J Helminthol. (2021) 95:e65. doi: 10.1017/S0022149X21000602 PubMed DOI

Taylor MJ, Bandi C, Hoerauf A. Wolbachia. Bacterial endosymbionts of filarial nematodes. Adv Parasitol. (2005) 60:245–84. doi: 10.1016/S0065-308X(05)60004-8 PubMed DOI

Morales-Hojas R. Molecular systematics of filarial parasites, with an emphasis on groups of medical and veterinary importance, and its relevance for epidemiology. Infect Genet Evol. (2009) 9:748–59. doi: 10.1016/j.meegid.2009.06.007, PMID: PubMed DOI

Taylor MJ, Voronin D, Johnston KL, Ford L. Wolbachia filarial cellular and molecular interactions. Cell Microbiol. (2013) 15:520–6. doi: 10.1111/cmi.12084, PMID: PubMed DOI

Genchi C, Kramer H, Sassera D, Bandi C. Wolbachia and its implications for the immunopathology of filariasis. endocr metab immune disord drug. Targets. (2012) 12:53–6. doi: 10.2174/187153012799279108, PMID: PubMed DOI

Manoj RRS, Latrofa MS, Epis S, Otranto D. Wolbachia: endosymbiont of onchocercid nematodes and their vectors. Parasites Vectors. (2021) 14:245. doi: 10.1186/s13071-021-04742-1, PMID: PubMed DOI PMC

Lagrange E, Bettini S. Descrizione di una nuova filaria, Litomosa ottavianii Lagrange e Bettini 1948, parassita di pipistrelli. Riv Parassitol. (1948) 9:61–77.

Wilson DE, Mittermeier RA. Handbook of the Mammals of the World, vol. 9. Barcelona: Bats. Lynx Edicions; (2019). 1008 p.

Hajkova P, Pikula J. Veterinary treatment of evening bats (Vespertilionidae) in the Czech Republic. Vet Rec. (2007) 161:139–40. doi: 10.1136/vr.161.4.139, PMID: PubMed DOI

Fasel NJ, Helfenstein F, Buff S, Richner H. Electroejaculation and semen buffer evaluation in the microbat Carollia perspicillata. Theriogenology. (2015) 83:904–10. doi: 10.1016/j.theriogenology.2014.11.030, PMID: PubMed DOI

Feldman AT, Wolfe D. Tissue processing and hematoxylin and eosin staining In: Day CE, editor. Histopathology: Methods and Protocols. New York: Humana Press, Springer; (2014). 31–43. PubMed

Mann BC, Bezuidenhout JJ, Swanevelder ZH, Grobler AF. MinION 16S datasets of a commercially available microbial community enables the evaluation of DNA extractions and data analyses. Data Brief. (2021) 36:107036. doi: 10.1016/j.dib.2021.107036 PubMed DOI PMC

Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, et al. . Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. (2013) 42:D633–42. doi: 10.1093/nar/gkt1244 (2013) PubMed DOI PMC

Casiraghi M, Anderson T, Bandi C, Bazzocchi C, Genchi C. A phylogenetic analysis of filarial nematodes: comparison with the phylogeny of Wolbachia endosymbionts. Parasitology. (2001) 122:93–103. doi: 10.1017/S0031182000007149 PubMed DOI

Ren WB, Wei HY, Yang Y, Shao SX, Wu HX, Chen XM, et al. . Molecular detection and phylogenetic analyses of Wolbachia in natural populations of nine galling aphid species. Sci Rep. (2020) 10:12025. doi: 10.1038/s41598-020-68925-z PubMed DOI PMC

Fasel NJ, Wesseling C, Fernandez AA, Vallat A, Glauser G, Helfenstein F, et al. . Alternative reproductive tactics, sperm mobility and oxidative stress in Carollia perspicillata (Seba’s short-tailed bat). Behav Ecol Sociobiol. (2017) 71:11. doi: 10.1007/s00265-016-2251-7 DOI

Hermes R, Hildebrandt TB, Göritz F, Fasel NJ, Holtze S. First cryopreservation of phyllostomid bat sperm. Theriogenology. (2019) 131:28–31. doi: 10.1016/j.theriogenology.2019.03.014, PMID: PubMed DOI

Racey PA. The prolonged storage and survival of spermatozoa in Chiroptera. Reproduction. (1979) 56:391–402. doi: 10.1530/jrf.0.0560391, PMID: PubMed DOI

De Jong CE, Jonsson N, Field H, Smith C, Crichton EG, Phillips N, et al. . Collection, seminal characteristics and chilled storage of spermatozoa from three species of free-range flying fox (Pteropus spp.). Theriogenology. (2005) 64:1072–89. doi: 10.1016/j.theriogenology.2005.02.016, PMID: PubMed DOI

Poiani A. Complexity of seminal fluid: a review. Behav Ecol Sociobiol. (2006) 60:289–310. doi: 10.1007/s00265-006-0178-0 DOI

Talwar P, Hayatnagarkar S. Sperm function test. J Hum Reprod Sci. (2015) 8:61–9. doi: 10.4103/0974-1208.158588, PMID: PubMed DOI PMC

Hayes DJ, Carter NS. An investigation of fructose utilization in Acanthocheilonema viteae. Parasitology. (1990) 101:445–50. doi: 10.1017/s0031182000060649, PMID: PubMed DOI

Crichton EG, Krutzsch PH, Wimsatt WA. Studies on prolonged spermatozoa survival in chiroptera—I. the role of uterine free fructose in the spermatozoa storage phenomenon. Comp Biochem Physiol A Physiol. (1981) 70:387–95. doi: 10.1016/0300-9629(81)90195-X DOI

Neuweiler G. The Biology of Bats. Oxford: Oxford University Press; (2000). 310 p.

Pikula J, Bandouchova H, Kovacova V, Linhart P, Piacek V, Zukal J. Reproduction of rescued Vespertilionid bats (Nyctalus noctula) in captivity: veterinary and physiologic aspects. Vet Clin North Am Exot Anim Pract. (2017) 20:665–77. doi: 10.1016/j.cvex.2016.11.013, PMID: PubMed DOI

Zhao S, Zhu W, Xue S, Han D. Testicular defense systems: immune privilege and innate immunity. Cell Mol Immunol. (2014) 11:428–37. doi: 10.1038/cmi.2014.38, PMID: PubMed DOI PMC

Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science. (2012) 335:936–41. doi: 10.1126/science.1214935, PMID: PubMed DOI PMC

Krutzsch PH. Anatomy, physiology and cyclicity of the male reproductive tract In: Crichton EG, Krutzsch PH, editors. Reproductive Biology of Bats. New York: Academic Press; (2000). 91–155.

Bain O, Wanji S, Vuong PN, Maréchal P, Le Goff L, Petit G, et al. . Larval biology of six filariae of the sub-family Onchocercinae in a vertebrate host. Parasite. (1994) 1:241–54. doi: 10.1051/parasite/1994013241, PMID: PubMed DOI

Guiton R, Drevet JR. Viruses, bacteria and parasites: infection of the male genital tract and fertility. Basic Clin Androl. (2023) 33:19. doi: 10.1186/s12610-023-00193-z, PMID: PubMed DOI PMC

Prasoon D, Agrawal P. Wuchereria bancrofti and cytology: a retrospective analysis of 110 cases from an endemic area. J Cytol. (2020) 37:182–8. doi: 10.4103/joc.Joc_59_20, PMID: PubMed DOI PMC

Brezina PR, Yunus F, Garcia J, Zhao Y. Description of the parasite Wucheria bancrofti microfilariae identified in follicular fluid following transvaginal oocyte retrieval. J Assist Reprod Gen. (2011) 28:433–6. doi: 10.1007/s10815-011-9538-4 PubMed DOI PMC

Li J, Li L, Jiang H, Yuan L, Zhang L, Ma JE, et al. . Fecal Bacteriome and Mycobiome in bats with diverse diets in South China. Current Microbiol. (2018) 75:1352–61. doi: 10.1007/s00284-018-1530-0, PMID: PubMed DOI

Foti M, Spena MT, Fisichella V, Mascetti A, Colnaghi M, Grasso M, et al. . Cultivable Bacteria associated with the microbiota of Troglophile bats. Animals. (2022) 12:2684. doi: 10.3390/ani12192684, PMID: PubMed DOI PMC

Singh P, Mosci R, Rudrik JT, Manning SD. Draft genome sequence of a Diarrheagenic Morganella morganii isolate. Genome Announc. (2015) 3:e01165–15. doi: 10.1128/genomeA.01165-15, PMID: PubMed DOI PMC

Kriss M, Hazleton KZ, Nusbacher NM, Martin CG, Lozupone CA. Low diversity gut microbiota dysbiosis: drivers, functional implications and recovery. Curr Opin Microbiol. (2018) 44:34–40. doi: 10.1016/j.mib.2018.07.003, PMID: PubMed DOI PMC

Madden AA, Oliverio AM, Kearns PJ, Henley JB, Fierer N, Starks PTB, et al. . Chronic stress and captivity alter the cloacal microbiome of a wild songbird. J Experimental Biol. (2022) 225:jeb243176. doi: 10.1242/jeb.243176 PubMed DOI

Olsson A. Gastrointestinal disorders In: Barnard SM, editor. Bats in Captivity. Volume 1: Biological and Medical Aspects. Washington, DC: Logos Press; (2009). 165–74.

Hebert PDN, Ratnasingham S, de Waard JR. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc R Soc Lond. (2003) 270 Suppl 1:S96–9. doi: 10.1098/rsbl.2003.0025, PMID: PubMed DOI PMC

Guerrero R, Bain O, Attout T, Martin C. The infective larva of Litomosoides yutajensis Guerrero et al., 2003 (Nematoda: Onchocercidae), a Wolbachia-free filaria from bat. Parasite. (2006) 13:127–30. doi: 10.1051/parasite/2006132127, PMID: PubMed DOI

Casiraghi M, Bain O, Guerrero R, Martin C, Pocacqua V, Gardner SL, et al. . Mapping the presence of Wolbachia pipientis on the phylogeny of filarial nematodes: evidence for symbiont loss during evolution. Int J Parasitol. (2004) 34:191–203. doi: 10.1016/j.ijpara.2003.10.004 PubMed DOI

Fenn K, Blaxter M. Are filarial nematode Wolbachia obligate mutualist symbionts? Trends Ecol Evol. (2004) 19:163–6. doi: 10.1016/j.tree.2004.01.002, PMID: PubMed DOI

McNulty SN, Foster JM, Mitreva M, Dunning Hotopp JC, Martin J, Fischer K, et al. . Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One. (2010) 5:e11029. doi: 10.1371/journal.pone.0011029, PMID: PubMed DOI PMC

Cross JH. Chapter 92: Filarial nematodes In: Baron S, editor. Medical Microbiology. 4th ed. Galveston (TX): University of Texas Medical Branch at Galveston; (1996) PubMed

Bain O, Babayan S, Gomes J, Rojas G, Guerrero R. First account on the larval biology of a Litomosoides filaria, from a bat. Parassitologia. (2002) 44:89–92. PMID: PubMed

van Schaik J, Dekeukeleire D, Kerth G. Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species. Mol Ecol. (2015) 24:2324–35. doi: 10.1111/mec.13171, PMID: PubMed DOI

Mantovani A, Jackson RF. Transplacental transmission of microfilariae of Dirofilaria immitis in the dog. J Parasitol. (1996) 52:116. doi: 10.2307/3276400 DOI

Eberhard ML, Hitch WL, Mcneeley DF, Lammie PJ. Transplacental transmission of Wuchereria bancrofti in Haitian women. J Parasitol. (1993) 79:62–6. doi: 10.2307/3283278, PMID: PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...