Bat Reservoirs for Rabies Virus and Epidemiology of Rabies in Colombia: a review

Jimmy Fernando Cifuentes Jiménez, Rubén Darío Pérez Lopéz, Noel Verjan Garcia

Resumen


La rabia es una enfermedad zoonóticas mortal causada por un virus ARNneurotrópico de la familia Rhabdoviridae. La enfermedad se caracterizapor encefalitis y es responsable de múltiples muertes anuales de personasy animales. Quirópteros insectívoros, frugívoros y hematófagos son losprincipales transmisores, reservorios y vectores del virus. En Colombia, untotal de 35 casos de rabia humana fueron reportados entre 2000- 2014,veintidós de ellos fueron transmitidos por murciélagos. La variante genéticaV3 (murciélagos hematófagos) fue responsable de 24 muertes humanas,mientras que la variante genética V4 (murciélagos insectívoros) causó tresmuertes humanas. La enfermedad es transmitida al humano principalmente por gatos infectados que pudieron haber cazado murciélagos infectados. El diagnósticose realiza mediante la detección del virus en animales rabiosos y técnicas comoRT-PCR podrían utilizarse para promover la vigilancia activa de las poblaciones demurciélagos. La rabia es una enfermedad prevenible y la vacunación en animalesdomésticos confiere inmunidad protectora, sin embargo, la cobertura de vacunaciónen animales domésticos en Colombia es aún limitada. Esta revisión recoge datosepidemiológicos de las variantes genéticas del virus en especies de quirópteros reportadascomo transmisores del virus en el mundo y enfatiza en los casos de rabiareportados en Colombia durante las últimas décadas.

 

Bat Reservoirs for Rabies Virus and Epidemiology ofRabies in Colombia: a review

Rabies is a fatal zoonotic disease caused by a neurotropic RNA virus partof the family Rhabdoviridae. The disease is characterized by encephaliticinflammation and is responsible for a number of annual fatal deaths ofpeople and animals in the world. Chiropters such as insectivorous, frugivorousand hematophagous bats are the major transmitters, reservoirs,and vectors of the rabies virus. In Colombia, a total of thirty-five cases ofhuman rabies occurred between 2000 2014. Of the thirty-five cases twenty-two were transmitted by bats. The genetic variant V3 (hematophagousbats) were responsible for 24 human deaths, while the genetic variant V4,carried by insectivorous bats, caused three human deaths. The disease ismainly linked to infected cats that may have hunted infected bats and thentransmitted the virus to humans. Diagnosis is usually made by detectionof the virus from infected animals and techniques such as RT-PCR, whichmight be used to promote active surveillance in bat populations. Rabies isa preventable disease and vaccination of pets confers protective immunity,however, vaccination coverage of pets in Colombia is still limited. This reviewarticle collects epidemiological data of rabies virus genetic variantsassociated with chiropters species that have been reported to transmit thevirus in the world and emphasizes on rabies cases reported in Colombiaduring the last decades.

Keywords: Chiroptera, genetic variants, Rhabdoviridae, zoonotic diseases.

 

Reservatórios de morcegos do vírus da raiva e epidemiologiada raiva na Colômbia: uma revisão

A raiva é uma enfermidade zoonótica fatal causada pelo vírus neurotrópico do ARNda família Rhabdoviridae. A enfermidade é conhecida por encefalite e é responsáveldas numerosas mortes anuais de animais e pessoas. Quirópteros e insetívoros, frugívorose sanguessugas são os principais transmissores, reservatórios e vetores dovírus. Na Colômbia o Instituto Nacional de Saúde relatou um total de 35 casos de raivahumana entre 2000- 2014. Vinte dois deles foram transmitidos pelos morcegos.A variante genética V3 (morcegos hematófagos) foi responsável de 24 mortes humanas.Enquanto a variante genética V4 (morcegos insetívoros) provoco três morteshumanas. A enfermidade está ligada principalmente á os gatos infectados que poderiamter caçado morcegos infectados e, em seguida, transmitida a os seres humanos.Diagnóstico e normalmente feito a través da detecção do vírus em animais raivosose técnicas tais como RT- PCR poderiam se utilizar para promover a vigilânciaativa das populações de morcegos. A raiva é uma enfermidade evitável em animaisdomésticos cuja vacinação confere imunidade protetora, no entanto, a cobertura devacinação em animais de estimação na Colômbia ainda é limitada, precisando demais cobertura. Este artigo de revisão recolha dados epidemiológicos e variantesgenéticas do vírus, e a diversidade de espécies de morcego reportado como transmissoresdo vírus no mundo. O manuscrito também resume os principais casosde raiva reportados na Colômbia nas últimas décadas e enfatiza a necessidade dereforçar a vigilância ativa para o diagnóstico de raiva em morcegos em todo o país.

Palavras-chave: Chiroptera, doença zoonótica, Rhabdoviridae, variantes genéticas.

DOI: http://dx.doi.org/10.21615/cesmvz.12.2.5


Palabras clave


Chiroptera, enfermedad zoonótica, Rhabdoviridae, variantes genéticas.

Citas


Calisher CH, Ellison J. The other rabies viruses: The emergence and importance

of lyssaviruses from bats and other vertebrates. Travel Med Infect Dis. 2012;10

(2): 69–79. doi:10.1016/j.tmaid.2012.01.003.

Jackson AC. Rabies. 3rd Editio. (Elsevier Inc, red). Canada: Academic Press; 2013.

doi:10.1016/B978-0-12-396547-9.00001-8.

Williamson JG. Rabies: Symptoms, Treatment And Prevention. (Williamson J g., red).

New york: Nova Science Publishers, Inc.; 2010. http://www.novapublishers.com.

Kuzmin I V, Mayer AE, Niezgoda M, et al. Shimoni bat virus, a new representative

of the Lyssavirus genus. Virus Res. 2010; 149 (2): 197–210. doi:10.1016/j.virusres.

01.018.

Kuzmin I V, Turmelle AS, Agwanda B, et al. Commerson’s leaf-nosed bat (Hipposideros

commersoni) is the likely reservoir of Shimoni bat virus. Vector Borne

Zoonotic Dis. 2011; 11 (11): 1465–1470. doi:10.1089/vbz.2011.0663.

Sato G, Tanabe H, Shoji Y, et al. Rapid discrimination of rabies viruses isolated

from various host species in Brazil by multiplex reverse transcription-polymerase

chain reaction. J Clin Virol. 2005; 33 (4): 267–273. doi:10.1016/j.jcv.2004.11.015.

Craig Greene. Infectious Diseases of the Dog and Cat. 4th Edition. (elsevier, red).;

https://www.elsevier.com/books/infectious-diseases-of-the-dog-and-cat/

greene/978-1-4160-6130-4

Scheffer KC, Iamamoto K, Asano KM, et al. Murciélagos hematófagos como reservorios

de la rabia. Rev Peru Med Exp Salud Publica. 2014;31(2):302–309. http://www.

scielosp.org/scielo.php?script=sci_arttext&pid=S1726-46342014000200018&lng=

en&nrm=iso&tlng=ennhttp://www.scielosp.org/pdf/rpmesp/v31n2/

a18v31n2.pdf.

Condori Condori RE, Streicker DG, Sanchez CC, Velasco Villa A. Enzootic and epizootic

rabies associated with vampire bats, peru. Emerg Infect Dis. 2013; 19 (9):

–1469. doi:10.3201/eid1809.130083.

OIE. Rabies; 2008. http://www.oie.int/fileadmin/Home/eng/Animal_Health_in_

the_World/docs/pdf/Disease_cards/RABIES_FINAL.pdf.

Black EM, Lowings JP, Smith J, Heaton PR, McElhinney LM. A rapid RT-PCR method

to differentiate six established genotypes of rabies and rabies-related viruses

using TaqMan TM technology. J Virol Methods. 2002;105 (1): 25–35. doi:10.1016/

S0166-0934(02)00062-9.

Mendes W da S, Moura da Silva AA, Fonseca Neiva R, et al. An outbreak of

bat-transmitted human rabies in a village in the Brazilian Amazon. Rev Saúde

Pública. 2009; 43 (6): 1075–1077. http://www.scielo.br/scielo.php?script=sci_

arttext&pid=S0034-89102009000600021

Hemachudha T, Ugolini G, Wacharapluesadee S, Sungkarat W, Shuangshoti S,

Laothamatas J. Human rabies: neuropathogenesis, diagnosis, and management.

Lancet Neurol. 2013; 12 (5): 498–513. doi:10.1016/S1474-4422(13)70038-3.

Leung AKC, Davies HD, Ellis Hon KL. Rabies: Epidemiology, pathogenesis, and

prophylaxis. Adv Ther. 2007; 24 (6): 1340–1347. doi:10.1007/BF02877781.

Stepien AE, Tripodi M, Arber S. Monosynaptic Rabies Virus Reveals Premotor

Network Organization and Synaptic Specificity of Cholinergic Partition Cells.

Neuron. 2010; 68 (3): 456–472. doi:10.1016/j.neuron.2010.10.019.

Jackson AC. Rabies virus infection: an update. J Neurovirol. 2003; 9 (2): 253–258.

doi:10.1080/13550280390193975.

Dietzschold B, Faber M, Schnell MJ. New approaches to the prevention and eradication

of rabies. Expert Rev Vaccines. 2003; 2 (3): 399–406. doi:10.1586/14760584.2.3.399.

McKay N, Wallis L. Rabies: a review of UK management. EMJ. 2005; 22 (5): 316–

doi:10.1136/emj.2003.013805.

Allendorf SD, Cortez A, Heinemann MB, et al. Rabies virus distribution in tissues

and molecular characterization of strains from naturally infected non-hematophagous

bats. Virus Res. 2012; 165 (2):119–125. doi:10.1016/j.virusres.2012.01.011.

WHO. Frequently Asked Questions on rabies. © World Health Organization. http://

www.who.int/rabies/resources/SEA_CD_278_FAQs_Rabies.pdf?ua=1. Published

Mantilla JC, Sierra JC, Garcia E, Pradilla G. Forma paralitica de un caso de rabia

humana trasmitida por murciélago, simulando Síndrome de Guillain Barre: Presentación

de un caso de autopsia. Salud UIS. 2010; 42: 139–151. http://www.scielo.

org.co/scielo.php?pid=S0121-08072010000200008&script=sci_abstract&tlng=

es

Turmelle AS, Jackson FR, Green D, McCracken GF, Rupprecht CE. Host immunity

to repeated rabies virus infection in big brown bats. J Gen Virol. 2010; 91: 2360–

doi:10.1099/vir.0.020073-0.

Sodré MM, Gama AR da, Almeid MF de. Update list of bat species postive for

rabies in brazil. Rev Inst Med Trop Sao Paulo. 2010; 52 (2): 75–81. doi:10.1590/

S0036-46652010000200004.

Fahl WO, Carnieli Jr P, Galera Castilho J, et al. Desmodus rotundus and Artibeus

spp. bats might present distinct rabies virus lineages. Braz J Infect Dis. 2012; 16

(6): 545–551. doi:10.1016/j.bjid.2012.07.002.

Fahl WO, Garcia AIE, Achkar SM, et al. Rabia transmitida por murciélagos en

brasil. Acta Biol Colomb. 2015; 20 (3): 21–35. http://dx.doi.org/10.15446/abc.

v20n3.45481.

Johnson N, Aréchiga Ceballos N, Aguilar Setien A. Vampire bat rabies: Ecology, epidemiology

and control. Viruses. 2014; 6 (5): 1911–1928. doi:10.3390/v6051911.

Paez A, Polo L, Heredia D, et al. Brote de rabia humana transmitida por gato

en el municipio de Santander de Quilichao, Colombia, 2008. Rev salud pública.

;11(6):931–943. http://www.scielo.org.co/scielo.php?script=sci_arttext&

pid=S0124-00642009000600009.

Favi C M, Bassaletti C Á, López D J, Rodríguez A L, Yung P V. Descripción epidemiológica

del reservorio de rabia en murciélagos de la Región Metropolitana:

Chile. 2000-2009. Rev Chil Infect. 2011; 28 (3): 223–228. doi:10.4067/S0716-

Badrane H, Tordo N. Host Switching in Lyssavirus History from the Chiroptera

to the Carnivora Orders. J Virol. 2001; 75 (17): 8096–8104. doi:10.1128/

JVI.75.17.8096.

Klug BJ, Turmelle AS, Ellison JA, Baerwald EF, Barclay RMR. Rabies prevalence

in migratory tree-bats in Alberta and the influence of roosting ecology and sampling

method on reported prevalence of rabies in bats. J Wildl Dis. 2011; 47 (1):

–77. doi:10.7589/0090-3558-47.1.64.

Oliveira R de N, Souza SP, Vaz Lobo R spinelli, 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. doi:10.1016/j.virol.2010.05.030.

Silva LHQ da, Cunha EMS, Wagner AP, Cardoso TC, Souza M do C, Ferrai CIL. Isolamento

do virus rabico em molossus ater (Chiroptera: Molossidae) no Estado de

Sao paulp. 1999; 33 (5). https://www.ncbi.nlm.nih.gov/labs/articles/10689381/

Galera Castilho J, Carnieli Jr P, Durymanova EA, et al. Human rabies transmitted

by vampire bats: Antigenic and genetic characterization of rabies virus isolates

from the Amazon region (Brazil and Ecuador). Virus Res. 2010; 153 (1): 100–105.

doi:10.1016/j.virusres.2010.07.012.

Baer GM, Adams DB. Rabies in Insectivorous Bats in the United States , 1953-

Public Health Rep. 1965; 85 (7): 637–645. https://www.ncbi.nlm.nih.gov/pmc/

articles/PMC2031685/

Humphrey GL, Kemp GE, Wood EG. A fatal case of rabies in a woman bitten by

an insectivorous bat. Public Health Rep. 1960; 75 (4): 317–326. https://www.ncbi.

nlm.nih.gov/pmc/articles/PMC1929432/

Bell JF. Transmission of rabies to laboratory animals by bite of naturally infected

insectivorous bat. Science (80-). 1959; 129:1490–1491. doi:10.1126/science.

3361.1490-a.

Nadin Davis SA, Huang W, Armstrong J, et al. Antigenic and genetic divergence of

rabies viruses from bat species indigenous to Canada. Virus Res. 2001; 74 (1–2):

–156. doi:10.1016/S0168-1702(00)00259-8.

Schatz J, Teifke JP, Mettenleiter TC, et al. Lyssavirus distribution in naturally infected

bats from Germany. Vet Microbiol. 2014; 169 (1–2): 33–41. doi:10.1016/j.

vetmic.2013.12.004.

P. Sánchez Serrano L, Abellán García C, Díaz García O. Rabia en España. ¿Qué

ocurre con la rabia en quirópteros? Semer - Med Fam. 2003; 29 (5): 268–270.

doi:10.1016/S1138-3593(03)74190-2.

Botvinkin A, Poleschuk E, Kuzmin I, et al. Novel lyssaviruses isolated from

bats in Russia. Emerg Infect Dis. 2003; 9 (12): 1623–1625. doi:10.3201/

eid0912.030374.

Kuzmin I V, Niezgoda M, Franka R, et al. Lagos bat virus in Kenya. J Clin Microbiol.

; 46 (4): 1451–1461. doi:10.1128/JCM.00016-08.

Markotter W. Molecular epidemiology and pathogenesis of Lagos bat virus, a rabies-

related virus specific to Africa. postgraduate thesis, Faculty of Natural and

Agricultural Science, University of Pretoria, Pretoria, 2007. 185 p. https://repository.

up.ac.za/handle/2263/26844

Sugay W, Nilsson MR. Isolamento Do Vírus Da Raiva De Morcegos Hematófagos

Do Estado De Sao Paulo, Brasil. Boletín la Of Sanit Panam. 1966:310–315. http://

hist.library.paho.org/Spanish/BOL/v60n4p310.pdf

Núñez Mejía C, Bonelo Perdomo A, Hernández Rojas C, Zapata Osorio J, Torres

Valencia G. Dispersión del virus rabia en areas urbanas de Colombia asociada a

especies de murciélagos que comparten refugios. Rev Asoc Col Cienc Biol. 2010;

: 68–72. http://www.ojs.asociacioncolombianadecienciasbiologicas.org/index.

php/accb/article/viewFile/89/89

Oria M F V, Machado S MC. Determinación de la dieta de algunas especies de

murciélagos (Mammalia: Chiroptera) de la cordillera central de venezuela. FARAUTE

Ciens y Tec. 2007; 2 (2): 5–15. http://faraute.facyt.uc.edu.ve/sites/default/

files/articulos/Determinación de la dieta de algunas especias de murciélagos

(Mammalia: Chiroptera).pdf.

Páez A, Nuñe C, García C, Boshell J. Epidemiología molecular de epizootias de

rabia en Colombia, 1994-2002 : evidencia de rabia humana y canina asociada

con quirópteros. Biomedica. 2003; 23: 19–30. doi:http://dx.doi.org/10.7705/biomedica.

v23i1.1194.

Alarcon Morales A, Osorio mesa E, Bernal Cubides C, Lleras Pizarro A. Aislamiento

De Virus Rabico De Murcielagos En Colombia. Caldasia. 1968; 10: 167–

http://www.bdigital.unal.edu.co/33812/1/33727-126546-1-PB.pdf

Núñez C, Páez A, Hernández C, Escobar H, Bonelo A. Transmisión del virus de la

rabia entre murciélagos urbanos del departamento del Valle del Cauca, Colombia,

-2008. Infectio. 2012; 16 (1): 23–29. doi:10.1016/S0123-9392(12)70054-1.

Páez A, Nũñez C, García C, Bóshell J. Molecular epidemiology of rabies epizootics

in Colombia: Evidence for human and dog rabies associated with bats. J Gen Virol.

; 84 (4): 795–802. doi:10.1099/vir.0.18899-0.

Páez A, Rey G, Agudelo C, et al. Brote de rabia urbana transmitida por perros en

el distrito de Santa Marta, Colombia, 2006-2008. Biomedica. 2009; 29: 424–436.

http://www.revistabiomedica.org/index.php/biomedica/article/view/14

Valderrama J, García I, Figueroa G, et al. Brotes de rabia humana transmitida por

vampiros en los municipios de Bajo y Alto Baudó, departamento del Chocó, Colombia

-2005. Biomédica. 2006; 26: 387–396. doi:10.7705/biomedica.v26i3.357.

Torro G, Martinez M, Saad C, Díaz A, Vega RL. Guía práctica para la atención integral

de personas agredidas por un animal potencialmente transmisor de rabia. 1st ed.

Bogota D.C; 2009. http://www.ins.gov.co/temas-de-interes/Rabia/Guia Rabia.pdf.

Páez A, Velasco Villa A, Rey G, Rupprecht CE. Molecular epidemiology of rabies in

Colombia 1994-2005 based on partial nucleoprotein gene sequences. Virus Res.

; 130 (1–2): 172–181. doi:10.1016/j.virusres.2007.06.008.

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: 529–536. doi:10.1017/S0950268805003699.

Alberico M, Saavedra R CA, García Paredes H. Murciélagos caseros de Cali (Valle del

Cauca - Colombia) House bats of Cali, Colombia. Caldasia. 2005; 27 (1): 117–126. http://

www.scielo.org.co/scielo.php?script=sci_arttext&pid=S0366-52322005000100006

INS. Informe final del evento agresiones por animales potencialmente transmisores

de rabia, Colombia 2014.; 2014. http://www.ins.gov.co/lineas-de-accion/Subdireccion-

Vigilancia/Informe%20de%20Evento%20Epidemiolgico/Agresiones%20por%20

animales%20potencialmente%20transmisores%20de%20rabia%202014.pdf

Parra E a, Neira M, Roa D. Rabia humana por virus tipo 3 , Bajo Baudó , Chocó. Biomedica.

; 24: 237–238. http://www.scielo.org.co/pdf/bio/v24n3/v24n3a02.pdf

McElhinney LM, Marston DA, Brookes SM, Fooks AR. Effects of carcase decomposition

on rabies virus infectivity and detection. J Virol Methods. 2014; 207: 110–

doi:10.1016/j.jviromet.2014.06.024.

OIE. CHAPTER 2.1.13. RABIES. In: Manual of Diagnostic Tests and Vaccines for Terrestrial

Animals - OIE. ; 2013: 1–26. http://www.oie.int/es/normas-internacionales/

manual-terrestre/acceso-en-linea/

Wacharapluesadee S, Tepsumethanon V, Supavonwong P, Kaewpom T, Intarut N,

Hemachudha T. Detection of rabies viral RNA by TaqMan real-time RT-PCR using

non-neural specimens from dogs infected with rabies virus. J Virol Methods.

; 184: 109–112. doi:10.1016/j.jviromet.2012.05.013.

Whitfield SG, Fekadu M, Shaddock JH, Niezgoda M, Warner CK, Messenger SL. A

comparative study of the fluorescent antibody test for rabies diagnosis in fresh

and formalin-fixed brain tissue specimens. J Virol Methods. 2001; 95: 145–151.

doi:10.1016/S0166-0934(01)00304-4.

Aravindh Babu RP, Monoharan S, Ramadass P, Chandran NDJ. Evaluation of RTPCR

Assay for Routine Laboratory Diagnosis of Rabies in Post Mortem Brain

Samples from Different Species of Animals. Indian J Virol. 2012; 23 (3): 392–396.

doi:10.1007/s13337-012-0109-9.

Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual, Volume 2.

rd editio. Cold Spring Harbor Laboratory Press; 2001. doi: http://dx.doi.

org/10.1016/0092-8674(90)90210-6.

Biswal M, Ratho R, Mishra B. Usefulness of reverse transcriptase-polymerase

chain reaction for detection of rabies RNA in archival samples. Jpn J Infect Dis,.

; 60 (5): 298–299. https://www.ncbi.nlm.nih.gov/pubmed/17881871

Cardoso Lopes M, Rossignolo Venditti LL, Queiroz LH. Comparison between RTPCR

and the mouse inoculation test for detection of rabies virus in samples kept

for long periods under different conditions. J Virol Methods. 2010; (1–2): 19–23.

doi:10.1016/j.jviromet.2009.11.017.

Smreczak M, Orlowska A, Trębas P, Żmudziński JF. Application of Heminested

RT-PCR to the Detection of Eblv1 and Classical Rabies Virus Infections in Bats

and Terrestrial Animals. Bull Vet Inst Pulawy. 2008; 52: 15–18. http://www.piwet.

pulawy.pl/jvetres/images/stories/pdf/20081/20081015018.pdf

Fooks AR, Johnson N, Freuling CM, et al. Emerging Technologies for the Detection

of Rabies Virus: Challenges and Hopes in the 21st Century. PLoS Negl Trop Dis.

; 3 (9): 1–12. doi:10.1371/journal.pntd.0000530.

Hoffmann B, Beer M, Reid SM, et al. A review of RT-PCR technologies used in

veterinary virology and disease control: Sensitive and specific diagnosis of five

livestock diseases notifiable to the World Organisation for Animal Health. Vet

Microbiol. 2009; 139: 1–23. doi:10.1016/j.vetmic.2009.04.034.

Nazarenko I a, Bhatnagar SK, Hohman RJ. A closed tube format for amplification

and detection of DNA based on energy transfer. Nucleic Acids Res. 1997; 25 (12):

–2521. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC146748/

Espy MJ, Uhl JR, Sloan LM, et al. Real-Time PCR in Clinical Microbiology : Applications

for Routine Laboratory Testing. Clin Microbiol Rev. 2006; 19 (1): 165–256.

doi:10.1128/CMR.19.1.165.

Nagaraj T, Vasanth JP, Desai A, Kamat A, Madhusudana SN, Ravi V. Ante mortem diagnosis

of human rabies using saliva samples: Comparison of real time and conventional

RT-PCR techniques. J Clin Virol. 2006; 36: 17–23. doi:10.1016/j.jcv.2006.01.009.

Jackson AC. Advances in Virus Research Volume 79. Vol 53. First edit. (Margaret

Kielian, Maramorosch K, C. T, reds). Elsevier Inc.; 2011. doi:10.1017/

CBO9781107415324.004.

Wasniewski M, Labbe a, Tribout L, et al. Evaluation of a rabies ELISA as an alternative

method to seroneutralisation tests in the context of international trade

of domestic carnivores. J Virol Methods. 2014; 195: 211–220. doi:10.1016/j.jviromet.

10.021.

Wasniewski M, Guiot AL, Schereffer JL, Tribout L, Mahar K, Cliquet F. Evaluation

of an ELISA to detect rabies antibodies in orally vaccinated foxes and raccoon

dogs sampled in the field. J Virol Methods. 2013; 187: 264–270. doi:10.1016/j.

jviromet.2012.11.022.

Ministerio de salud y proteccion social. ¿Que es la rabia?; 2014.

WHO. WHO | About rabies. © World Health Organization. http://www.who.int/rabies/

about/en/. Published 2016. Toegang verkry Januarie 25, 2016.

Blackwood JC, Streicker DG, Altizer S, Rohani P. Resolving the roles of immunity,

pathogenesis, and immigration for rabies persistence in vampire bats. Proc Natl

Acad Sci U S A. 2013; 110 (51): 20837-20842. doi:10.1073/pnas.1308817110.

MINSALUD. Cobertura Municipal de Vacunación Antirrábica de Perros Y Gatos

; 2014. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/

RIDE/VS/PP/SA/cobertura-municipal-vacunacion-antirrabica-2014.pdf


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