1921
Volume 87, Issue 2
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

In May of 2010, two communities (Truenococha and Santa Marta) reported to be at risk of vampire bat depredation were surveyed in the Province Datem del Marañón in the Loreto Department of Perú. Risk factors for bat exposure included age less than or equal to 25 years and owning animals that had been bitten by bats. Rabies virus neutralizing antibodies (rVNAs) were detected in 11% (7 of 63) of human sera tested. Rabies virus ribonucleoprotein (RNP) immunoglobulin G (IgG) antibodies were detected in the sera of three individuals, two of whom were also seropositive for rVNA. Rabies virus RNP IgM antibodies were detected in one respondent with no evidence of rVNA or RNP IgG antibodies. Because one respondent with positive rVNA results reported prior vaccination and 86% (six of seven) of rVNA-positive respondents reported being bitten by bats, these data suggest nonfatal exposure of persons to rabies virus, which is likely associated with vampire bat depredation.

[open-access] This is an Open Access article distributed under the terms of the American Society of Tropical Medicine and Hygiene's Re-use License which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Loading

Article metrics loading...

The graphs shown below represent data from March 2017
/content/journals/10.4269/ajtmh.2012.11-0689
2012-08-01
2019-11-13
Loading full text...

Full text loading...

/deliver/fulltext/14761645/87/2/206.html?itemId=/content/journals/10.4269/ajtmh.2012.11-0689&mimeType=html&fmt=ahah

References

  1. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, Miranda ME, Shaw A, Zinsstag J, Meslin FX, , 2005. Re-evaluating the burden of rabies in Africa and Asia. Bull World Health Organ 83: 360368. [Google Scholar]
  2. Rupprecht CE, Hanlon CA, Hemachudha T, , 2002. Rabies re-examined. Lancet Infect Dis 2: 327343.[Crossref] [Google Scholar]
  3. Messenger SL, Smith JS, Rupprecht CE, , 2002. Emerging epidemiology of bat-associated cryptic cases of rabies in humans in the United States. Clin Infect Dis 35: 738747.[Crossref] [Google Scholar]
  4. Salmon-Mulanovich G, Vasquez A, Albujar C, Guevara C, Laguna-Torres VA, Salazar M, Zamalloa H, Caceres M, Gomez-Benavides J, Pacheco V, Contreras C, Kochel T, Niezgoda M, Jackson FR, Velasco-Villa A, Rupprecht C, Montgomery JM, , 2009. Human rabies and rabies in vampire and nonvampire bat species, southeastern Peru, 2007. Emerg Infect Dis 15: 13081310.[Crossref] [Google Scholar]
  5. Oliveira RD, de Souza SP, Lobo RSV, Castilho JG, Macedo CI, Carnieli P, Fahl WO, Achkar SM, Scheffer KC, Kotait I, Carrieri ML, Brandao PE, , 2010. Rabies virus in insectivorous bats: implications of the diversity of the nucleoprotein and glycoprotein genes for molecular epidemiology. Virology 405: 352360.[Crossref] [Google Scholar]
  6. Diaz AM, Papo S, Rodriguez A, Smith JS, , 1994. Antigenic analysis of rabies-virus isolates from Latin America and the Caribbean. Zoonoses Public Health 41: 153160. [Google Scholar]
  7. de Mattos CA, Favi M, Yung V, Pavletic C, de Mattos CC, , 2000. Bat rabies in urban centers in Chile. J Wildl Dis 36: 231240.[Crossref] [Google Scholar]
  8. Favoretto SR, Carrieri ML, Cunha EM, Aguiar EA, Silva LH, Sodre MM, Souza MC, Kotait I, , 2002. Antigenic typing of Brazilian rabies virus samples isolated from animals and humans, 1989–2000. Rev Inst Med Trop Sao Paulo 44: 9195.[Crossref] [Google Scholar]
  9. Arellano-Sota C, , 1988. Vampire bat-transmitted rabies in cattle. Rev Infect Dis 10 (Suppl 4): S707S709.[Crossref] [Google Scholar]
  10. Carneiro AJ, Franke CR, Stocker A, Dos Santos F, Ungar de Sa JE, Moraes-Silva E, Alves JN, Brunink S, Corman VM, Drosten C, Drexler JF, , 2010. Rabies virus RNA in naturally infected vampire bats, northeastern Brazil. Emerg Infect Dis 16: 20042006.[Crossref] [Google Scholar]
  11. Velasco-Villa A, Orciari LA, Juarez-Islas V, Gomez-Sierra M, Padilla-Medina I, Flisser A, Souza V, Castillo A, Franka R, Escalante-Mane M, Sauri-Gonzalez I, Rupprecht CE, , 2006. Molecular diversity of rabies viruses associated with bats in Mexico and other countries of the Americas. J Clin Microbiol 44: 16971710.[Crossref] [Google Scholar]
  12. Schneider MC, Romijn PC, Uieda W, Tamayo H, da Silva DF, Belotto A, da Silva JB, Leanes LF, , 2009. Rabies transmitted by vampire bats to humans: an emerging zoonotic disease in Latin America? Rev Panam Salud Publica 25: 260269.[Crossref] [Google Scholar]
  13. Warner CK, Zaki SR, Shieh WJ, Whitfield SG, Smith JS, Orciari LA, Shaddock JH, Niezgoda M, Wright CW, Goldsmith CS, Sanderlin DW, Yager PA, Rupprecht CE, , 1999. Laboratory investigation of human deaths from vampire bat rabies in Peru. Am J Trop Med Hyg 60: 502507. [Google Scholar]
  14. Lopez A, Miranda P, Tejada E, Fishbein DB, , 1992. Outbreak of human rabies in the Peruvian jungle. Lancet 339: 408411.[Crossref] [Google Scholar]
  15. Gómez-Benavides J, , 2011. Veintiocho de Setiembre, día Mundial de Prevención de la Rabia. Bol Epidemiol Lima: Dirección General de Epidemiología. Lima, Peru: Ministerio de Salud, 825826. [Google Scholar]
  16. Canahuiri J, Vargas E, , 2009. Caso Confirmado de Rabia Humana en la Comunidad Indígena Amazónica de Quebrada Kandungos, Distrito de Río Santiago, Provincia de Condorcanqui. DIRESA Amazonas. Bol. Epidemiol. Lima, Peru: Ministerio de Salud, 276. [Google Scholar]
  17. Canahuiri J, , 2009. Rabia Silvestre Humana en la Comunidad Indígena Amazónica del Centro Poblado Los Angeles, Quiteni, Distrito Río Tambo, Provincia Satipo, Junín, 2009. Bol Epidemiol. Lima, Peru: Ministerio de Salud, 805. [Google Scholar]
  18. Canahuiri J, , 2009. Probable Brote de Rabia Transmitida por Vampiro en la Comunidad Nativa (CC.NN) Cachiaco, Distrito Nieva, Provincia Condorcanqui, DIRESA Amazonas. Bol Epidemiol. Lima, Peru: Ministerio de Salud, 839. [Google Scholar]
  19. Dirección General de Epidemiología, 2010. Brote de Rabia Humana Silvestre en Comunidades Nativas Kigkis y Sumpa del Distrito Nieva, Provincia Condorcanqui, DIRESA Amazonas. Bol Epidemiol. Lima, Peru: Ministerio de Salud, 137138.
  20. Dirección General de Epidemiología, 2011. Brote de Rabia Silvestre en la Comunidad Nativa San Ramón- Yupicusa, Distrito Imaza, Provincia Bagua, Amazonas – 2011: Situación Actual. Bol Epidemiol. Lima, Peru: Ministerio de Salud, 123124. [Google Scholar]
  21. CDC, 2008. Human rabies prevention—United States, 2008: recommendations of the Advisory Committee on Immunization Practices. MMWR Recomm Rep 57: 128. [Google Scholar]
  22. Blancou J, , 1988. Ecology and epidemiology of fox rabies. Rev Infect Dis 10 (Suppl 4): S606S609.[Crossref] [Google Scholar]
  23. Hanlon CA, Niezgoda M, Rupprecht C, Jackson A, Wunner W, , 2007. Rabies in terrestrial animals. , eds. Rabies, 2nd Ed. London: Academic Press, 201258.[Crossref] [Google Scholar]
  24. Trimarchi C, Debbie JG, , 1977. Naturally occurring rabies virus and neutralizing antibody in two species of insectivorous bats of New York state. J Wildl Dis 13: 366369.[Crossref] [Google Scholar]
  25. Lord RD, Fuenzalida E, Delpietro H, Larghi OP, de Diaz AM, Lazaro L, , 1975. Observations on the epizootiology of vampire bat rabies. Bull Pan Am Health Organ 9: 189195. [Google Scholar]
  26. Turmelle AS, Allen LC, Jackson FR, Kunz TH, Rupprecht C, McCracken GF, , 2010. Ecology of rabies virus exposure in colonies of Brazilian free-tailed bats (Tadarida brasiliensis) at natural and man-made roosts in Texas. Vector Borne Zoonotic Dis 10: 165175.[Crossref] [Google Scholar]
  27. Burns KF, Shelton DF, Grogan EW, , 1958. Bat rabies: experimental host transmission studies. Ann N Y Acad Sci 70: 452466.[Crossref] [Google Scholar]
  28. Allworth A, Murray K, Morgan J, , 1996. A human case of encephalitis due to a lyssavirus recently identified in fruit bats. Commun Dis Intell 20: 504. [Google Scholar]
  29. Paweska JT, Blumberg LH, Liebenberg C, Hewlett RH, Grobbelaar AA, Leman PA, Croft JE, Nel LH, Nutt L, Swanepoel R, , 2006. Fatal human infection with rabies-related Duvenhage virus, South Africa. Emerg Infect Dis 12: 19651967.[Crossref] [Google Scholar]
  30. Lumio J, Hillbom M, Roine R, Ketonen L, Haltia M, Valle M, Neuvonen E, Lahdevirta J, , 1986. Human rabies of bat origin in Europe. Lancet 1: 378.[Crossref] [Google Scholar]
  31. Bell JF, , 1964. Abortive rabies infection. I. Experimental production in white mice and general discussion. J Infect Dis 114: 249257.[Crossref] [Google Scholar]
  32. Hattwick MA, Weis TT, Stechschulte CJ, Baer GM, Gregg MB, , 1972. Recovery from rabies. A case report. Ann Intern Med 76: 931942.[Crossref] [Google Scholar]
  33. Willoughby RE, Jr Tieves KS, Hoffman GM, Ghanayem NS, Amlie-Lefond CM, Schwabe MJ, Chusid MJ, Rupprecht CE, , 2005. Survival after treatment of rabies with induction of coma. N Engl J Med 352: 25082514.[Crossref] [Google Scholar]
  34. Porras C, Barboza JJ, Fuenzalida E, Adaros HL, Oviedo AM, Furst J, , 1976. Recovery from rabies in man. Ann Intern Med 85: 4448.[Crossref] [Google Scholar]
  35. Alvarez L, Fajardo R, Lopez E, Pedroza R, Hemachudha T, Kamolvarin N, Cortes G, Baer GM, , 1994. Partial recovery from rabies in a nine-year-old boy. Pediatr Infect Dis J 13: 11541155.[Crossref] [Google Scholar]
  36. CDC, 1977. Rabies in a laboratory worker—New York. MMWR Morb Mortal Wkly Rep 26: 183184. [Google Scholar]
  37. Madhusudana SN, Nagaraj D, Uday M, Ratnavalli E, Kumar MV, , 2002. Partial recovery from rabies in a six-year-old girl. Int J Infect Dis 6: 8586.[Crossref] [Google Scholar]
  38. CDC, 2010. Presumptive abortive human rabies—Texas, 2009. MMWR Morb Mortal Wkly Rep 59: 185190. [Google Scholar]
  39. Smith JS, Yager P, Baer G, Meslin FX, Kaplan MM, Koprowski H, , 1996. A rapid fluorescent focus inhibition test (RFFIT) for determining rabies virus-neutralizing antibody. , eds. Laboratory Techniques in Rabies. Geneva: World Health Organization, 181192. [Google Scholar]
  40. Reed LJ, Muench H, , 1938. A simple method of estimating fifty percent endpoints. Am J Hyg 27: 493497. [Google Scholar]
  41. Noah DL, Drenzek CL, Smith JS, Krebs JW, Orciari L, Shaddock J, Sanderlin D, Whitfield S, Fekadu M, Olson JG, Rupprecht CE, Childs JE, , 1998. Epidemiology of human rabies in the United States, 1980 to 1996. Ann Intern Med 128: 922930.[Crossref] [Google Scholar]
  42. Black D, Wiktor TJ, , 1986. Survey of raccoon hunters for rabies antibody titers: pilot study. J Fla Med Assoc 73: 517520. [Google Scholar]
  43. Orr PH, Rubin MR, Aoki FY, , 1988. Naturally acquired serum rabies neutralizing antibody in a Canadian Inuit population. Arctic Med Res 47 (Suppl 1): 699700. [Google Scholar]
  44. Follmann EH, Ritter DG, Beller M, , 1994. Survey of fox trappers in northern Alaska for rabies antibody. Epidemiol Infect 113: 137141.[Crossref] [Google Scholar]
  45. Moore SM, Gordon CR, Briggs D, Jackson A, Wunner W, , 2007. Rabies serology. , eds. Rabies, 2nd Ed. London: Academic Press, 471488.[Crossref] [Google Scholar]
  46. Lodmell DL, , 1983. Genetic control of resistance to street rabies virus in mice. J Exp Med 157: 451460.[Crossref] [Google Scholar]
  47. Lodmell DL, Chesebro B, , 1984. Murine resistance to street rabies virus: genetic analysis by testing second-backcross progeny and verification of allelic resistance genes in SJL/J and CBA/J mice. J Virol 50: 359362. [Google Scholar]
  48. Templeton JW, Holmberg C, Garber T, Sharp RM, , 1986. Genetic control of serum neutralizing-antibody response to rabies vaccination and survival after a rabies challenge infection in mice. J Virol 59: 98102. [Google Scholar]
  49. Rodriguez-Delfin LA, Rubin-de-Celis VE, Zago MA, , 2001. Genetic diversity in an Andean population from Peru and regional migration patterns of Amerindians in South America: data from Y chromosome and mitochondrial DNA. Hum Hered 51: 97106.[Crossref] [Google Scholar]
  50. Callegari-Jacques SM, Salzano FM, Weimer WA, Hutz MH, Black EL, Santos SEB, Guerreiro JF, Mestrineri MM, Pandey JP, , 1994. Further blood genetic studies on Amazonian diversity—data from four Indian groups. Ann Hum Biol 21: 465481.[Crossref] [Google Scholar]
  51. Batista Dos Santos SE, Rodrigues JD, Ribeiro Dos Santos AKC, Zago MA, , 1999. Differential contribution of indigenous men and women to the formation of an urban population in the Amazon region as revealed by mtDNA and Y-DNA. Am J Phys Anthropol 109: 175180.[Crossref] [Google Scholar]
  52. Moore SM, Wilkerson MJ, Davis RD, Wyatt CR, Briggs DJ, , 2006. Detection of cellular immunity to rabies antigens in human vaccinees. J Clin Immunol 26: 533545.[Crossref] [Google Scholar]
  53. Hooper DC, Morimoto K, Bette M, Weihe E, Koprowski H, Dietzschold B, , 1998. Collaboration of antibody and inflammation in clearance of rabies virus from the central nervous system. J Virol 72: 37113719. [Google Scholar]
  54. Dietzschold B, Wang HH, Rupprecht CE, Celis E, Tollis M, Ertl H, Heber-Katz E, Koprowski H, , 1987. Induction of protective immunity against rabies by immunization with rabies virus ribonucleoprotein. Proc Natl Acad Sci USA 84: 91659169.[Crossref] [Google Scholar]
  55. Turner GS, Nicholson KG, Tyrrell DA, Aoki FY, , 1982. Evaluation of a human diploid cell strain rabies vaccine: final report of a three year study of pre-exposure immunization. J Hyg (Lond) 89: 101110.[Crossref] [Google Scholar]
  56. Turmelle AS, Jackson FR, Green D, McCracken GF, Rupprecht CE, , 2010. Host immunity to repeated rabies virus infection in big brown bats. J Gen Virol 91: 23602366.[Crossref] [Google Scholar]
  57. Crepin P, Audry L, Rotivel Y, Gacoin A, Caroff C, Bourhy H, , 1998. Intravitam diagnosis of human rabies by PCR using saliva and cerebrospinal fluid. J Clin Microbiol 36: 11171121. [Google Scholar]
  58. Anderson LJ, Nicholson KG, Tauxe RV, Winkler WG, , 1984. Human rabies in the United States, 1960 to 1979: epidemiology, diagnosis, and prevention. Ann Intern Med 100: 728735.[Crossref] [Google Scholar]
  59. Kasempimolporn S, Hemachudha T, Khawplod P, Manatsathit S, , 1991. Human immune response to rabies nucleocapsid and glycoprotein antigens. Clin Exp Immunol 84: 195199.[Crossref] [Google Scholar]
  60. Wang ZW, Sarmento L, Wang Y, Li XQ, Dhingra V, Tseggai T, Jiang B, Fu ZF, , 2005. Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol 79: 1255412565.[Crossref] [Google Scholar]
  61. Morimoto K, Hooper DC, Spitsin S, Koprowski H, Dietzschold B, , 1999. Pathogenicity of different rabies virus variants inversely correlates with apoptosis and rabies virus glycoprotein expression in infected primary neuron cultures. J Virol 73: 510518. [Google Scholar]
  62. Faber M, Pulmanausahakul R, Hodawadekar SS, Spitsin S, McGettigan JP, Schnell MJ, Dietzschold B, , 2002. Overexpression of the rabies virus glycoprotein results in enhancement of apoptosis and antiviral immune response. J Virol 76: 33743381.[Crossref] [Google Scholar]
  63. Morimoto K, Patel M, Corisdeo S, Hooper DC, Fu ZF, Rupprecht CE, Koprowski H, Dietzschold B, , 1996. Characterization of a unique variant of bat rabies virus responsible for newly emerging human cases in North America. Proc Natl Acad Sci USA 93: 56535658.[Crossref] [Google Scholar]
  64. Wiktor TJ, Dietzschold B, Leamnson RN, Koprowski H, , 1977. Induction and biological properties of defective interfering particles of rabies virus. J Virol 21: 626635. [Google Scholar]
  65. Briggs DJ, Jackson A, Wunner W, , 2007. Human rabies vaccines. , eds. Rabies, 2nd Ed. London: Academic Press, 505515.[Crossref] [Google Scholar]
  66. Briggs DJ, Schwenke JR, , 1992. Longevity of rabies antibody titre in recipients of human diploid cell rabies vaccine. Vaccine 10: 125129.[Crossref] [Google Scholar]
  67. Fuenzalida E, , 1972. Human pre-exposure rabies immunization with suckling mouse brain vaccine. Bull World Health Organ 46: 561563. [Google Scholar]
  68. Perrin P, Versmisse P, Delagneau JF, Lucas G, Rollin PE, Sureau P, , 1986. The influence of the type of immunosorbent on rabies antibody EIA; advantages of purified glycoprotein over whole virus. J Biol Stand 14: 95102.[Crossref] [Google Scholar]
  69. Lee TK, Hutchinson HD, Ziegler DW, , 1977. Comparison of rabies humoral antibody titers in rabbits and humans by indirect radioimmunoassay, rapid-fluorescent-focus-inhibition technique, and indirect fluorescent-antibody assay. J Clin Microbiol 5: 320325. [Google Scholar]
  70. Gómez-Benavides J, Laguna-Torres VA, Recuenco S, , 2010. The real significance of being bitten by a hematophagous bat in indigenous communities in the remote Peruvian Amazon. Rev Peru Med Exp Salud Publica 27: 649658.[Crossref] [Google Scholar]
  71. Greenhall AM, Joermann G, Schmidt U, Seidel MR, , 1983. Desmodus rotundus. Mammalian Species 202: 16.[Crossref] [Google Scholar]
  72. Greenhall AM, Greenhall AM, Schmidt U, , 1988. Feeding behavior. , eds. Natural History of Vampire Bats. Boca Raton, FL: CRC Press, 111131. [Google Scholar]
  73. Constantine DG, Greenhall AM, Schmidt U, , 1988. Transmission of pathogenic microorganisms by vampire bats. , eds. Natural History of Vampire Bats. Boca Raton: CRC Press, Inc., 167189. [Google Scholar]
  74. de Verteuil E, Urich FW, , 1936. The study and control of paralytic rabies transmitted by vampire bats in Trinidad, B.W.I. Trans R Soc Trop Med Hyg 29: 317347.[Crossref] [Google Scholar]
  75. Goncalves MA, Sa-Neto RJ, Brazil TK, , 2002. Outbreak of aggressions and transmission of rabies in human beings by vampire bats in northeastern Brazil. Rev Soc Bras Med Trop 35: 461464.[Crossref] [Google Scholar]
  76. Prieto JF, Baer GM, , 1972. An outbreak of bovine paralytic rabies in Tuxtepec, Oaxaca, Mexico. Am J Trop Med Hyg 21: 219225. [Google Scholar]
  77. McCarthy TJ, , 1989. Human depredation by vampire bats (Desmodus rotundus) following a hog cholera campaign. Am J Trop Med Hyg 40: 320322. [Google Scholar]
  78. Rupprecht CE, Turmelle A, Kuzmin IV, , 2011. A perspective on lyssavirus emergence and perpetuation. Curr Opin Virol 1: 662670.[Crossref] [Google Scholar]
  79. Badrane H, Bahloul C, Perrin P, Tordo N, , 2001. Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 75: 32683276.[Crossref] [Google Scholar]
  80. Markotter W, Kuzmin IV, Rupprecht CE, Nel LH, , 2009. Lagos bat virus virulence in mice inoculated by the peripheral route. Epidemiol Infect 137: 11551162.[Crossref] [Google Scholar]
  81. Hughes GJ, Kuzmin IV, Schmitz A, Blanton J, Manangan J, Murphy S, Rupprecht CE, , 2006. Experimental infection of big brown bats (Eptesicus fuscus) with Eurasian bat lyssaviruses Aravan, Khujand, and Irkut virus. Arch Virol 151: 20212035.[Crossref] [Google Scholar]
  82. Franka R, Johnson N, Muller T, Vos A, Neubert L, Freuling C, Rupprecht CE, Fooks AR, , 2008. Susceptibility of North American big brown bats (Eptesicus fuscus) to infection with European bat lyssavirus type 1. J Gen Virol 89: 19982010.[Crossref] [Google Scholar]
  83. Johnson N, Vos A, Neubert L, Freuling C, Mansfield KL, Kaipf I, Denzinger A, Hicks D, Nunez A, Franka R, Rupprecht CE, Muller T, Fooks AR, , 2008. Experimental study of European bat lyssavirus type-2 infection in Daubenton's bats (Myotis daubentonii). J Gen Virol 89: 26622672.[Crossref] [Google Scholar]
  84. Banyard AC, Hayman D, Johnson N, McElhinney L, Fooks AR, , 2011. Bats and lyssaviruses. Adv Virus Res 79: 239289.[Crossref] [Google Scholar]
  85. Dodet B, Africa Rabies Bureau (AfroREB), 2009. The fight against rabies in Africa: from recognition to action. Vaccine 27: 50275032.[Crossref] [Google Scholar]
  86. Favoretto SR, de Mattos CC, de Morais NB, Carrieri ML, Rolim BN, Silva LM, Rupprecht CE, Durigon EL, de Mattos CA, , 2006. Rabies virus maintained by dogs in humans and terrestrial wildlife, Ceara State, Brazil. Emerg Infect Dis 12: 19781981.[Crossref] [Google Scholar]
  87. Favi M, de Mattos CA, Yung V, Chala E, Lopez LR, de Mattos CC, , 2002. First case of human rabies in chile caused by an insectivorous bat virus variant. Emerg Infect Dis 8: 7981.[Crossref] [Google Scholar]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2012.11-0689
Loading
/content/journals/10.4269/ajtmh.2012.11-0689
Loading

Data & Media loading...

Supplementary PDF

  • Received : 03 Nov 2011
  • Accepted : 13 Apr 2012
  • Published online : 01 Aug 2012

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error