Variability in seroprevalence of rabies virus neutralizing antibodies and associated factors in a colorado population of big brown bats (Eptesicus fuscus)

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  O'Shea, Thomas J ^a   Bowen, Richard A ^b   Stanley, Thomas R ^a   Shankar, Vidya ^b,c,f   Rupprecht, Charles E ^d,e  

^a FORT COLLINS SCIENCE CENTER   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d ROSS UNIVERSITY SCHOOL OF VETERINARY MEDICINE   (Saint Kitts and Nevis)

^e Erasmus Forum A434   (United States)

^f National Center for Telehealth and Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECTICIDE; NEUTRALIZING ANTIBODY; VIRUS RNA;

ADULT; AGE; ANIMAL EUTHANASIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ARTICLE; BAT; DROUGHT; ENVIRONMENTAL STRESS; EPTESICUS FUSCUS; EXPLANATORY VARIABLE; FEMALE; JUVENILE ANIMAL; MALE; NONHUMAN; POPULATION STRUCTURE; RABIES; RABIES VIRUS; SEASON; SEROLOGY; SEROPREVALENCE; SEX DIFFERENCE; UNITED STATES;

ANIMAL DISEASES; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CHIROPTERA; COLORADO; FEMALE; MALE; RABIES; RABIES VIRUS; RISK FACTORS; SEASONS; SEROEPIDEMIOLOGIC STUDIES;

EID: 84899652780     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086261     Document Type: Article

References (91)

1. Burns KF, Farinacci CG, Murnane TG (1956) Insectivorous bats naturally infected with rabies in southwestern United States. Am J Public Health 46: 1089-1097.
2. Constantine DG, Tierkel ES, Kleckner MD, Hawkine DM (1968) Rabies in New Mexico cavern bats. Public Health Rep 83: 303-316.
3. Trimarchi CV, Debbie JG (1977) Naturally occurring rabies virus and neutralizing antibody in two species of insectivorous bats of New York State. J Wildl Dis 13: 366-369.
4. Salas-Rojas M, Sanchez-Hernandez C, Romero-Almaraz MDL, Schnell GD, Schmid RK, et al. (2004) Prevalence of rabies and LPM paramyxovirus antibody in non-hematophagous bats captured in the Central Pacific coast of Mexico. Trans R Soc Trop Med Hyg 98: 577-584. (Pubitemid 39345158)
5. Steece R, Altenbach JS (1989) Prevalence of rabies antibodies in the Mexican free-tailed bat (Tadarida brasiliensis mexicana) at Lava Cave, New Mexico. J Wildl Dis 25: 490-496.
6. Schatz J, Fooks AR, McElhinney L, Horton D, Echevarria J, et al. (2013) Bat rabies surveillance in Europe. Zoonoses Public Health 60: 22-34.
7. Brookes SM, Aegerter JN, Smith GC, Healy DM, Jolliffe T, et al. (2005) Prevalence of antibodies to European Bat Lyssavirus type-2 in Scottish bats. Emerg Infect Dis 11: 572-578. (Pubitemid 40462907)
8. Harris SL, Aegerter JN, Brookes SM, McElhinney LM, Jones G, et al. (2009) Targeted surveillance for European bat lyssaviruses in English bats (2003-06). J Wildl Dis 45: 1030-1041.
9. Serra-Cobo J, Amengual B, Abellán C, Bourhy H (2002) European bat Lyssavirus infection in Spanish bat populations. Emerg Infect Dis 8: 413-420. (Pubitemid 34415205)
10. Serra-Cobo J, López-Roig M, Seguí M, Sánchez LP, Nadal J, et al. (2013) Ecological factors associated with European bat Lyssavirus seroprevalence in Spanish bats. PLoS One 8(5): e64467. doi:10.1371/journal.pone.0064467.
11. Vázquez-Morón S, Juste J, Ibáñez C, Ruiz-Villamor E, Avellón A, et al. (2008) Endemic circulation of European bat lyssavirus type 1 in serotine bats, Spain. Emerg Infect Dis 14: 1263-1266.
12. Perez-Jorda JL, Ibáñez C, Muñoz-Cervera M, Téllez A (1995) Lysaavirus in Eptesicus serotinus (Chiroptera: Vespertilionidae). J Wildl Dis 31: 372-377.
13. Amengual B, Bourhy H, López-Roig M, Serra-Cobo J (2007) Temporal dynamics of European bat lyssavirus type 1 and survival of Myotis myotis bats in natural colonies. PLoS One 2(6): e566. doi:10.1371/journal.pone.0000566.
14. Pape WJ, Fitzsimmons TD, Hoffman RE (1999) Risk for rabies transmission from encounters with bats, Colorado, 1977-1996. Emerg Infect Dis 5: 433-437. (Pubitemid 29289458)
15. Mondul AM, Krebs JW, Childs JE (2003) Trends in national surveillance for rabies among bats in the United States (1993-2000). J Am Vet Med Assoc 222: 633-639. (Pubitemid 36258995)
16. Patyk K, Turmelle A, Blanton JD, Rupprecht CE (2012) Trends in National Surveillance Data for Bat Rabies in the United States: 2001-2009. Vector Borne Zoonotic Dis 12: 666-673.
17. Shankar V, Bowen RA, Davis AD, Rupprecht CE, O'Shea TJ (2004) Rabies in a captive colony of big brown bats (Eptesicus fuscus). J Wildl Dis 40: 403-413. (Pubitemid 39342308)
18. Jackson FR, Turmelle AS, Farino DM, Franka R, McCracken GF, et al. (2008) Experimental rabies virus infection of big brown bats (Eptesicus fuscus). J Wildl Dis 44: 612-621.
19. 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: 2360-2366.
20. Davis AD, Rudd RJ, Bowen RA (2007) Effects of aerosolized rabies virus exposure on bats and mice. J. Infect Dis 195: 1144-1150. (Pubitemid 46543445)
21. Davis A, Gordy P, Rudd R, Jarvis JA, Bowen RA (2012) Naturally acquired rabies virus infections in wild-caught bats. Vector Borne Zoonotic Dis 12: 55-60.
22. Davis AD, Gordy PA, Bowen RA (2013) Unique characteristics of bat rabies viruses in big brown bats (Eptesicus fuscus). Arch Virol 158: 809-820.
23. Neubaum DJ, O'Shea TJ, Wilson KR (2006) Autumn migration and selection of rock crevices as hibernacula by big brown bats in Colorado. J Mammal 87: 470-479. (Pubitemid 43902242)
24. Neubaum DJ, Wilson KR, O'Shea TJ (2007) Urban maternity roost selection by big brown bats in north-central Colorado. J Wildl Manage 71: 728-736.
25. O'Shea TJ, Neubaum DJ, Neubaum MA, Cryan PM, Ellison LE, et al. (2011a) Bat ecology and public health surveillance for rabies in an urbanizing region of Colorado. Urban Ecosystems 14: 665-697.
26. O'Shea TJ, Ellison LE, Neubaum DJ, Neubaum MA, Reynolds CA, et al. (2010) Recruitment in a Colorado population of big brown bats: breeding probabilities, litter size, and first-year survival. J Mammal 91: 418-428.
27. O'Shea TJ, Ellison LE, Stanley TR (2011b) Adult survival and population growth rate in Colorado big brown bats (Eptesicus fuscus). J Mammal 92: 433-443.
28. Neubaum MA, Douglas MR, Douglas ME, O'Shea TJ (2007) Molecular ecology of the big brown bat (Eptesicus fuscus): genetic and natural history variation in a hybrid zone. J Mammal 88: 1230-1238. (Pubitemid 350005046)
29. Turmelle AS, Allen LC, Jackson FR, Kunz TH, Rupprecht CE, et al. (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: 165-175.
30. Schmid-Hempel P (2003) Variation in immune defiance as a question of evolutionary ecology. Proc R Soc Lond B Biol Sci 270: 357-366.
31. Hawley DM, Altizer SM (2011) Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct Ecol 25: 48-60.
32. Ellison LE, O'Shea TJ, Neubaum DJ, Bowen RA (2007) Factors influencing movement probabilities of big brown bats (Eptesicus fuscus) in buildings. Ecol Appl 17: 620-627. (Pubitemid 46607419)
33. Cryan PM, Stricker CA, Wunder MB (2012) Evidence of cryptic individual specialization in an opportunistic insectivorous bat. J Mammal 93: 381-389.
34. Shankar V, Orciari LA, De Mattos C, Kuzmin IV, Pape WJ, et al. (2005) Genetic divergence of rabies viruses from bat species of Colorado, USA. Vector Borne Zoonotic Dis 5: 330-341. (Pubitemid 43192872)
35. George DB, Webb CT, Farnsworth ML, O'Shea TJ, Bowen RA, et al. (2011) Host and viral ecology determine bat rabies seasonality and maintenance. Proc Natl Acad Sci USA 108: 10208-10213.
36. Colorado Climate Center (2013) Drought resources. Available: http://ccc.atmos.colostate.edu/palmerindex.php. Accessed 20 February 2013.
37. National Climatic Data Center (2013) Palmer drought severity index. Available: http://www.ncdc.noaa.gov/paleo/drought/drght-pdsi.html. Accessed 20 February 2013.
38. Snider EA (2009) Post-fire insect communities and roost selection by western long-eared myotis (Myotis evotis) in Mesa Verde National Park, Colorado. Master's thesis, Colorado State University, Fort Collins, CO.
39. Frick WF, Reynolds DS, Kunz TH (2010) Influence of climate and reproductive timing on demography of little brown Myotis lucifugus. J Anim Ecol 79: 128-136.
40. O'Shea TJ, Cryan PM, Snider PE, Valdez EW, Ellison LE, et al. (2011) Bats of Mesa Verde National Park, Colorado: composition, reproduction, and roosting habits. Monogr West N Am Nat 5: 1-19.
41. Colorado Climate Center (2006) Available: http://ccc.atmos.colostate.edu. /dataaccess.php. Accessed 22 February 2006.
42. O'Shea TJ, Ellison LE, Stanley TR (2004) Survival estimation in bats: Historical overview, critical appraisal, and suggestions for new approaches. In: Thompson WL, editor. Sampling rare or elusive species: Concepts, designs, and techniques for estimating population parameters. Washington, DC: Island Press. 297-336.
43. Sheffield SR, Shaw JH, Heidt GA, McClenaghan LR (1992) Guidelines for the protection of bat roosts. J Mammal 73: 707-710.
44. Wimsatt J, O'Shea TJ, Ellison LE, Pearce RD, Price VR (2005) Anesthesia and blood sampling of wild big brown bats (Eptesicus fuscus) with an assessment of impacts on survival. J Wildl Dis 41: 87-95. (Pubitemid 40652050)
45. Anthony ELP (1988) Age determination in bats. In: Kunz TH, editor. Ecological and behavioral methods for the study of bats. Washington, DC: Smithsonian Institution. pp. 47-58.
46. Ellison LE, O'Shea TJ, Wimsatt J, Pearce RD, Bowen RA (2007) A comparison of conventional capture versus PIT reader techniques for estimating survival and capture probabilities of big brown bats. Acta Chiropt 9: 149-160. (Pubitemid 47376498)
47. Kunz TH (2003) Censusing bats: challenges, solutions, and sampling biases. In: O'Shea TJ, Bogan MA, editors. Monitoring trends in bat populations of the United States and territories: problems and prospects. US Geol Survey Info Technol Rep ITR-2003-003. 9-19.
48. Willis CKR, Brigham RM (2004) Roost switching, roost sharing and social cohesion: forest-dwelling big brown bats, Eptesicus fuscus, conform to the fission-fusion model. Anim Behav 68: 495-505. (Pubitemid 39464505)
49. Ellison LE, O'Shea TJ, Wimsatt J, Pearce RD, Neubaum DJ, et al. (2006) Sampling blood from big brown bats (Eptesicus fuscus) in the field with and without anesthesia: Impacts on survival. J Wildl Dis 42: 849-852. (Pubitemid 46231854)
50. Bowen RA, O'Shea TJ, Shankar V, Neubaum MA, Neubaum DJ, et al. (2013) Prevalence of neutralizing antibodies to rabies virus in serum of seven species of insectivorous bats from Colorado and New Mexico. J Wildl Dis 49: 367-374.
51. th ed. Geneva: World Health Organization. 200-208.
52. th edition. World Geneva: Health Organization. pp. 88-93.
53. Smith JS (1996) New aspects of rabies with emphasis on epidemiology, diagnosis, and prevention of the disease in the United States. Clin Microbiol Rev 9: 166-176.
54. Newcombe RG (1998) Two-sided confidence intervals for the single proportion: Comparison of seven methods. Stat Med 17: 857-872.
55. Marascuilo LA (1966) Large-sample multiple comparison. Psychol Bull 65: 280-290.
56. SAS Institute Inc (2008) SAS/STATH® 9.2 User's Guide. Cary, NC: SAS Institute Inc.
57. Sulkin SE, Allen R, Sims R, Singh KV (1966) Studies of arthropod-borne virus infections in Chiroptera. IV. The immune response of the big brown bat (Eptesicus f. fuscus) maintained at various environmental temperatures to experimental Japanese b encephalitis virus infection. Am J Trop Med Hyg 15: 418-427.
58. Burton RS, Reichman OJ (1999) Does immune challenge affect torpor duration? Funct Ecol 13: 232-237. (Pubitemid 29266997)
59. Prendergast BJ, Freeman DA, Zucker I, Nelson RJ (2002) Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels. Am J Physiol Regul Integr Comp Physiol 282: R1054-R1062. (Pubitemid 34664557)
60. Canale CI, Henry PY (2011) Energetic costs of the immune response and torpor use in a primate. Funct Ecol 25: 557-565.
61. Vieira P, Rajewsky K (1988) The half-lives of serum immunoglobulins in adult mice. Eur J Immunol 18: 313-316. (Pubitemid 18078861)
62. Sigounas G, Harindranath N, Donadel G, Notkins AL (1994) Half-life of polyreactive antibodies. J Clin Immunol 14: 134-140. (Pubitemid 24108800)
63. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach. New York: Springer. p 514.
64. Arnold TD (2010) Uninformative parameters and model selection using Akaike's information criterion. J Wildl Manage 74: 1175-1178.
65. Burnham KP, Anderson DR, White GC, Brownie C, Pollock KP (1987) Design and analysis of methods for fish survival experiments based on release-recapture. Monogr Am Fish Soc 5: 1-437.
66. Kurta A, Baker RH (1990) Eptesicus fuscus. Mammalian Species 356: 1-10.
67. Bode AV, Sejvar JJ, Pape WJ, Campbell GL, Marfin AA (2006) West Nile virus disease: a descriptive study of 228 patients hospitalized in a 4-county region of Colorado in 2003. Clin Infect Dis 42: 1234-1240.
68. Bolling BG, Moore CG, Anderson SL, Blair CD, Beaty BJ (2007) Entomological studies along the Colorado Front Range during a period of intense West Nile virus activity. J Am Mosq Control Assoc 23: 37-46. (Pubitemid 46775971)
69. Colorado Mosquito Control (2004) 2004 Annual Report City of Fort Collins Mosquito Control Program. Available: http://fcgov.com/westnile/pdf/ annualreport04. Accessed 20 February 2013.
70. O'Shea TJ, Johnston JJ (2009) Environmental contaminants and bats: Investigating exposure and effects. In: Kunz TH, Parsons S, editors. Behavioral and ecological methods for the study of bats. Baltimore, MD: Johns Hopkins University Press. pp. 500-528.
71. Constantine DG (1988) Health precautions for bat researchers. In: Kunz TH, editor. Ecological and behavioral methods for the study of bats. Washington, DC: Smithsonian Institution Press. pp. 491-528.
72. Turmelle AS, Allen LC, Schmidt-French BA, Jackson FR, Kunz TH, et al. (2010) Response to vaccination with a commercial inactivated rabies vaccine in a captive colony of Brazilian free-tailed bats (Tadarida brasiliensis). J Zoo Wildl Med 41: 140-143.
73. Messenger SL, Rupprecht CE, Smith JS (2003) Bats, emerging virus infections, and the rabies paradigm In: Kunz TH, Fenton MB editors. Bat ecology. Chicago, IL: University of Chicago Press. pp. 622-679.
74. Pearce RD, O'Shea TJ, Shankar V, Rupprecht CE (2007) Lack of association between ectoparasite intensities and rabies virus neutralizing antibody seroprevalence in wild big brown bats (Eptesicus fuscus), Fort Collins, Colorado. Vector Borne Zoonotic Dis 7: 489-495.
75. Niezgoda M, Hanlon CA, Rupprecht CE (2002) Animal rabies. In: Jackson AC, Wunner WH, editors. Rabies. New York: Academic Press. pp. 163-218.
76. Baker ML, Schountz T, Wang LF (2013) Antiviral immune responses of bats: a review. Zoonoses Public Health 60: 104-116.
77. Silberman DM, Wald MR, Genaro AM (2003) Acute and chronic stress exert opposing effects on antibody responses associated with changes in stress hormone regulation of T-lymphocyte reactivity. J Neuroimmunol 144: 53-60. (Pubitemid 37329929)
78. Murray SE, Lallman HR, Heard AD, Rittenberg MB, Stenzel-Poore MP (2001) A genetic model of stress displays decreased lymphocytes and impaired antibody responses without altered susceptibility to Streptococcus pneumonia. J Immunol 167: 691-698. (Pubitemid 32660821)
79. Lewanzik D, Kelm DH, Greiner S, Dehnhard M, Voigt CC (2012) Ecological correlates of cortisol levels in two bat species with contrasting feeding habits. Gen Comp Endocrinol 177: 104-112.
80. Allen LC, Turmelle AS, Widmaier EP, Hristov NI, McCracken GF, et al. (2010) Variation in physiological stress between bridge- and cave-roosting Brazilian free-tailed bats. Conserv Biol 25: 374-381.
81. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21: 55-89. (Pubitemid 32266068)
82. Baker MR, Gobush KS, Vynne CH (2013) Review of factors influencing stress hormones in fish and wildlife. J Nature Conserv 21: 309-318.
83. Demas GE (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45: 173-180.
84. Fair JM, Whitaker SJ (2008) Avian cell-mediated immune response to drought. Wilson J Ornithol 120: 813-819.
85. King JM, Bradshaw SG (2010) Stress in an Island kangaroo? The Barrow Island euro, Macropus robustus isabellinus . Gen Comp Endocrinol 167: 60-67.
86. Rhodes M (2007) Roost fidelity and fission-fusion dynamics of white-striped free-tailed bats (Tadarida australis). J Mammal 88: 1252-1260.
87. Frick WF, Rainey WE, Pierson ED (2007) Potential effects of environmental contamination on Yuma myotis demography and population growth. Ecol Appl 17: 1213-1222. (Pubitemid 351328154)
88. Abad-Gomez JM, Gutiérrez JS, Villegas A, Sánchez- Guzmán JM, Navedo JG, et al. (2013) Time course and metabolic costs of a humoral immune response in the little ringed plover Charadrius dubius. Physiol Biochem Zool 86: 354-360.
89. Seager R, Ting M, Held I, Kushnir Y, Lu J, et al. (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316: 1181-1184. (Pubitemid 46877478)
90. Barnett TP, Pierce DW, Hidalgo HG, Bonfils C, Santer BD, et al. (2008) Human-induced changes in the hydrology of the western United States. Science 319: 1080-1083. (Pubitemid 351300787)
91. McAfee SA, Russell JL (2008) Northern annular mode impact on spring climate in the western United States. Geophys Res Lett 35: 1-5.