First Report of Gray Foxes (Urocyon cinereoargenteus) Infected with Bat-Associated rabies Virus (Desmodus rotundus rabies virus) in Costa Rica

Abstract

Objective: Rabies is a lethal zoonotic viral disease that affects mammals. Although Costa Rica has not reported any cases of canine rabies since 1987, cases of bat-transmitted rabies virus in domestic animals are recorded annually. Cases in wild carnivores remain sporadic, and surveillance of these species has intensified during the past 7 years. Herein, we present three cases of gray foxes (Urocyon cinereoargenteus) infected with bat-associated rabies virus (Desmodus rotundus rabies virus) in residential neighborhoods of Costa Rica.

Methods: Brain tissue samples from the foxes were analyzed with histological and molecular methods, including RT-PCR and Sanger sequencing.

Results: Test findings confirmed the presence of vampire bat rabies virus in wild mammals (gray fox) inhabiting peri-urban areas near humans and domestic animals.

Conclusions: This study underscores the urgent need to review current rabies protocols to ensure timely provision of prophylactic medical care for people and pets with suspected exposure. Furthermore, educating the public regarding the risks associated with rabies transmission in wildlife is essential to prevent incidents with potential to endanger public health.

Keywords

Rabies / gray fox / Desmodus rotundus / zoonotic / wildlife surveillance / necropsy / One Health / Costa Rica

References

[1] Horton DL, McElhinney LM, Marston DA, Wood JLN, Russell CA, Lewis N, et al. Quantifying antigenic relationships among the lyssaviruses. J Virol. 2010; 84(22): 11841-11848.

[2] Belotto A, Leanes LF, Schneider MC, Tamayo H, Correa E. Overview of rabies in the Americas. Virus Res. 2005; 111(1): 5-12.

[3] León B, González SF, Solís LM, Ramírez-Cardoce M, Moreira-Soto A, Cordero-Solórzano JM, et al. Rabies in Costa Rica - next steps towards controlling bat-borne rabies after its elimination in dogs. Yale J Biol Med. 2021; 94(2): 311-329.

[4] Hutter SE, Brugger K, Sancho Vargas VH, González R, Aguilar O, León B, et al. Rabies in Costa Rica: documentation of the surveillance program and the endemic situation from 1985 to 2014. Vector Borne Zoonotic Dis. 2016; 16(5): 334-341.

[5] King JM, Roth-Johnson L, Dodd DC, Newsom ME . The necropsy book: a guide for veterinary students, residents, clinicians, pathologists, and biological researchers . Ithaca, New York, USA: Cornell University; 2013.

[6] Alvarado-Fernández JC, Salas-Rojas C, Estrella-Morales J, González R, Cordero-Solorzano JM, Aguilar-Arguedas O, et al. Evaluation of a rapid immunochromatographic assay for the diagnosis of rabies in regional laboratories of Costa Rica. Veterinaria México OA [Internet]. Available from: https://veterinariamexico.fmvz.unam.mx/index.php/vet/article/view/1106. Cited 2024 Sep 19.

[7] Streicker DG, Fallas González SL, Luconi G, Barrientos RG, Leon B. Phylodynamics reveals extinction-recolonization dynamics underpin apparently endemic vampire bat rabies in Costa Rica. Proc Biol Sci. 2019; 286(1912): 20191527.

[8] Reidarson TH, McBain J, House C, King DP, Stott JL, Krafft A, et al. Morbillivirus infection in stranded common dolphins from the Pacific Ocean. J Wildl Dis. 1998; 34(4): 771-776.

[9] de Novaes Oliveira R, de Souza SP, Lobo RSV, Castilho JG, Macedo CI, Carnieli P, et al. Rabies virus in insectivorous bats: implications of the diversity of the nucleoprotein and glycoprotein genes for molecular epidemiology. Virology. 2010; 405(2): 352-360.

[10] Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol. 2018; 35(6): 1547-1549.

[11] Ding N-Z, Xu D-S, Sun Y-Y, He H-B, He C-Q. A permanent host shift of rabies virus from Chiroptera to Carnivora associated with recombination. Sci Rep. 2017; 7(1): 289.

[12] del Pilar Sánchez M, Díaz Sanchez OA, Sanmiguel RA, Ramirez AA, Escobar L . Rabia en las Américas, varios desafíos y “Una Sola Salud”: artículo de revisión. Rev Investig Vet Perú. 2020; 30: 1361-1381.

[13] Blanton JD, Palmer D, Rupprecht CE. Rabies surveillance in the United States during 2009. J Am Vet Med Assoc. 2010; 237(6): 646-657.

[14] De Mattos CC, De Mattos CA, Loza-Rubio E, Aguilar-Setién A, Orciari LA, Smith JS. Molecular characterization of rabies virus isolates from Mexico: implications for transmission dynamics and human risk. Am J Trop Med Hyg. 1999; 61(4): 587-597.

[15] Páez A, Saad C, Núñez C, Bóshell J. Molecular epidemiology of rabies in northern Colombia 1994-2003. Evidence for human and fox rabies associated with dogs. Epidemiol Infect. 2005; 133(3): 529-536.

[16] Condori RE, Aragon A, Breckenridge M, Pesko K, Mower K, Ettestad P, et al. Divergent rabies virus variant of probable bat origin in 2 gray foxes, New Mexico, USA. Emerg Infect Dis. 2022; 28(6): 1137-1145.

[17] Theimer TC, Dyer AC, Keeley BW, Gilbert AT, Bergman DL. Ecological potential for rabies virus transmission via scavenging of dead bats by mesocarnivores. J Wildl Dis. 2017; 53(2): 382-385.

[18] Rabia. Protocolo de vigilancia y control de la rabia en humanos. Costa Rica: Ministerio de Salud; 2015: 1-16.

[19] Troupin C, Dacheux L, Tanguy M, Sabeta C, Blanc H, Bouchier C, et al. Large-scale phylogenomic analysis reveals the complex evolutionary history of rabies virus in multiple carnivore hosts. PLoS Pathog. 2016; 12(12): e1006041.

[20] Kuzmin IV, Shi M, Orciari LA, Yager PA, Velasco-Villa A, Kuzmina NA, et al. Molecular inferences suggest multiple host shifts of rabies viruses from bats to mesocarnivores in Arizona during 2001-2009. PLoS Pathog. 2012; 8(6): e1002786.

[21] Shafaati M, Akbarpour S, Priyanka, Saied AA, Choudhary OP. Tackling rabies by one health approach: pitfalls on the road to global eradication. New Microbes New Infect. 2023; 52: 101098.