Pathogenesis of bat rabies in a natural reservoir: Comparative susceptibility of the straw-colored fruit bat (Eidolon helvum) to three strains of Lagos bat virus

PLoS Neglected Tropical Diseases

Volumn 12, Issue 3, 2018, Pages

  Suu Ire, Richard ^a,b,c,d   Begeman, Lineke ^e   Banyard, Ashley C ^f   Breed, Andrew C ^f   Drosten, Christian ^g   Eggerbauer, Elisa ^h   Freuling, Conrad M ^h   Gibson, Louise ^a   Goharriz, Hooman ^f   Horton, Daniel L ⁱ   Jennings, Daisy ^f   Kuzmin, Ivan V ^j   Marston, Denise ^f   Ntiamoa Baidu, Yaa ^b   Riesle Sbarbaro, Silke ^a,k   Selden, David ^f   Wise, Emma L ^f   Kuiken, Thijs ^e   Fooks, Anthony R ^f   Müller, Thomas ^h   Wood, James L N ^k   Cunningham, Andrew A ^a   more..

^a INSTITUTE OF ZOOLOGY   (United Kingdom)

^b UNIVERSITY OF GHANA   (Ghana)

^c Ministry of Food and Agriculture Ghana   (Ghana)

^d Wildlife Division of the Forestry Commission   (Ghana)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f VETERINARY LABORATORIES AGENCY   (United Kingdom)

^g HUMBOLDT UNIVERSITY   (Germany)

^h FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

ⁱ UNIVERSITY OF SURREY   (United Kingdom)

^j University of Texas Medical Branch School of Medicine   (United States)

^k UNIVERSITY OF CAMBRIDGE   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; CONTROLLED STUDY; EIDOLON HELVUM; FLUORESCENT ANTIBODY TECHNIQUE; FLYING FOX; IMMUNOHISTOCHEMISTRY; LAGOS BAT VIRUS; LYSSAVIRUS; NONHUMAN; RABIES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEREOTAXIC SURGERY; VIRUS STRAIN; VIRUS TRANSMISSION; ANIMAL; BAT; BLOOD; BRAIN; CLASSIFICATION; DISEASE CARRIER; HOST PATHOGEN INTERACTION; NERVE CELL; PATHOLOGY; PHYSIOLOGY; VETERINARY; VIROLOGY;

VIRUS ANTIBODY;

ANIMALS; ANTIBODIES, VIRAL; BRAIN; CHIROPTERA; DISEASE RESERVOIRS; HOST-PATHOGEN INTERACTIONS; IMMUNOHISTOCHEMISTRY; LYSSAVIRUS; NEURONS; RABIES;

EID: 85045117272     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0006311     Document Type: Article

References (73)

1. Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, et al. Estimating the global burden of endemic canine rabies. PLoS Negl Trop Dis. 2015;9: e0003709. doi: 10.1371/journal.pntd.0003709 25881058
2. Messenger SL, Smith JS, Orciari LA, Yager PA, Rupprecht CE, Emerging pattern of rabies deaths and increased viral infectivity. Emerg Infect Dis. 2003;9: 151–154. doi: 10.3201/eid0902.020083 12603983
3. De Serres G, Dallaire F, Côte M, Skowronski DM, Bat rabies in the United States and Canada from 1950 through 2007: human cases with and without bat contact. Clinical Infectious Diseases. 2008;46: 1329–1337. doi: 10.1086/586745 18419432
4. Petersen BW, Rupprecht CE, Tkachev S, Human rabies epidemiology and diagnosis. In: Non-flavivirus encephalitis. NY: InTech; 2011. pp. 247–78
5. Leslie MJ, Messenger S, Rohde RE, Smith J, Cheshier R, Hanlon C, et al. Bat-associated rabies virus in skunks. Emerg Infect Dis. 2006;12: 1274–1277. doi: 10.3201/eid1208.051526 16965714
6. Daoust PY, Wandeler AI, Casey GA, Cluster of rabies cases of probable bat origin among red foxes in Prince Edward Island, Canada. J Wildl Dis. 1996;32: 403–406. doi: 10.7589/0090-3558-32.2.403 8722290
7. 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. e1002786. doi: 10.1371/journal.ppat.1002786 22737076
8. Dacheux L, Larrous F, Mailles A, Boisseleau D, Delmas O, Biron C, et al. European bat lyssavirus transmission among cats, Europe. Emerg Infect Dis. 2009;15: 280–284. doi: 10.3201/eid1502.080637 19193273
9. Müller T, Johnson N, Freuling CM, Fooks AR, Selhorst T, Vos A, Epidemiology of bat rabies in Germany. Arch Virol. 2007;152: 273–288. doi: 10.1007/s00705-006-0853-5 17066249
10. Tjørnehøj K, Fooks AR, Agerholm JS, Rønsholt L, Natural and experimental infection of sheep with European bat lyssavirus type-1 of Danish bat origin. J Comp Pathol. 2006;134: 190–201. doi: 10.1016/j.jcpa.2005.10.005 16545840
11. Markotter W, Kuzmin I, Rupprecht CE, Randles J, Sabeta CT, Wandeler AI, et al. Isolation of Lagos bat virus from water mongoose. Emerg Infect Dis. 2006;12: 1913–1918. doi: 10.3201/eid1212.060514 17326944
12. Mebatsion T, Cox JH, Frost JW, Isolation and characterization of 115 street rabies virus isolates from Ethiopia by using monoclonal antibodies: Identification of 2 isolates as Mokola and Lagos bat viruses. J Infect Dis. 1992;166: 972–977. 1402044
13. Shinwari MW, Annand EJ, Driver L, Warrilow D, Harrower B, Allcock RJN, et al. Australian bat lyssavirus infection in two horses. Vet Microbiol. 2014;173:224–31. doi: 10.1016/j.vetmic.2014.07.029 25195190
14. Banyard AC, Evans JS, Rong Luo T, Fooks AR, Lyssaviruses and bats: Emergence and zoonotic threat. Viruses. 2014;6: 2974–2990. doi: 10.3390/v6082974 25093425
15. Banyard AC, Hayman D, Johnson N, McElhinney L, Fooks AR, Jackson AC, Bats and Lyssaviruses. In: Advances in Virus Research. London: Academic Press; 2011. pp. 239–289. doi: 10.1016/B978-0-12-387040-7.00012-3 21601050
16. Allendorf SD, Cortez A, Heinemann MB, Appolinário Harary CM, Antunes JMAP, Peres MG, et al. Rabies virus distribution in tissues and molecular characterization of strains from naturally infected non-hematophagous bats. Virus Res. 2012;165: 119–125. doi: 10.1016/j.virusres.2012.01.011 22349147
17. Banyard AC, Johnson N, Voller K, Hicks D, Nunez A, Hartley M, et al. Repeated detection of European bat lyssavirus type 2 in dead bats found at a single roost site in the UK. Arch Virol. 2009;154: 1847–1850. doi: 10.1007/s00705-009-0504-8 19841859
18. Hooper PT, Fraser GC, Foster RA, Storie GJ, Histopathology and immunohistochemistry of bats infected by Australian bat lyssavirus. Aust Vet J. 1999;77: 595–599. 10561795
19. Schatz J, Teifke JP, Mettenleiter TC, Aue A, Stiefel D, Müller T, et al. Lyssavirus distribution in naturally infected bats from Germany. Vet Microbiol. 2014;169:33–41. doi: 10.1016/j.vetmic.2013.12.004 24440375
20. Baer GM, Bales GL, Experimental rabies infection in the Mexican freetail bat. J Infect Dis. 1967;1: 82–90.
21. Freuling C, Vos A, Johnson N, Kaipf I, Denzinger A, Neubert L, et al. Experimental infection of serotine bats (Eptesicus serotinus) with European bat lyssavirus type 1a. J Gen Virol. 2009;90: 2493–2502. doi: 10.1099/vir.0.011510-0 19515825
22. Johnson N, Vos A, Neubert L, Freuling C, Mansfield KL, Kaipf I, et al. Experimental study of European bat lyssavirus type-2 infection in Daubenton’s bats (Myotis daubentonii). J Gen Virol. 2008;89: 2662–2672. doi: 10.1099/vir.0.2008/003889-0 18931061
23. McColl KA, Chamberlain T, Lunt RA, Newberry KM, Middleton D, Westbury HA, Pathogenesis studies with Australian bat lyssavirus in grey-headed flying foxes (Pteropus poliocephalus). Aust Vet J. 2002;80: 636–641. 12465817
24. Aguilar-Setien A, Loza-Rubio E, Salas-Rojas M, Brisseau N, Cliquet F, Pastoret PP, et al. Salivary excretion of rabies virus by healthy vampire bats. Epidemiol Infect. 2005;133: 517–522. doi: 10.1017/s0950268805003705 15966107
25. Almeida MF, Martorelli LFA, Aires CC, Sallum PC, Durigon EL, Massad E, Experimental rabies infection in haematophagous bats Desmodus rotundus. Epidemiol Infect. 2005;133: 523–527. doi: 10.1017/s0950268804003656 15962559
26. Davis AD, Jarvis JA, Pouliott C, Rudd RJ, Rabies virus infection in Eptesicus fuscus bats born in captivity (naïve bats). PLoS One. 2013;8. e64808. doi: 10.1371/journal.pone.0064808 23741396
27. Davis AD, Gordy PA, Bowen RA, Unique characteristics of bat rabies viruses in big brown bats (Eptesicus fuscus). Arch Virol. 2013;158: 809–820. doi: 10.1007/s00705-012-1551-0 23208279
28. Davis AD, Jarvis JA, Pouliott CE, Morgan SMD, Rudd RJ, Susceptibility and pathogenesis of little brown bats (Myotis lucifugus) to heterologous and homologous rabies viruses. J Virol. 2013;87: 9008–9015. doi: 10.1128/JVI.03554-12 23741002
29. Fooks AR, Johnson N, Müller T, Vos A, Mansfield K, Hicks D, et al. Detection of high levels of European bat lyssavirus type-1 viral RNA in the thyroid gland of experimentally-infected Eptesicus fuscus bats. Zoonoses Public Health. 2009;56: 270–277. doi: 10.1111/j.1863-2378.2008.01203.x 19497087
30. Franka R, Johnson N, Müller T, Vos A, Neubert L, Freuling C, et al. Susceptibility of North American big brown bats (Eptesicus fuscus) to infection with European bat lyssavirus type 1. J Gen Virol. 2008;89: 1998–2010. doi: 10.1099/vir.0.83688-0 18632972
31. Hughes GJ, Kuzmin IV, Schmitz A, Blanton J, Manangan J, Murphy S, et al. Experimental infection of big brown bats (Eptesicus fuscus) with Eurasian bat lyssaviruses Aravan, Khujand, and Irkut virus. Arch Virol. 2006;151: 2021–2035. doi: 10.1007/s00705-005-0785-0 16705370
32. Jackson FR, Turmelle AS, Farino DM, Franka R, McCracken GF, Rupprecht CE, Experimental rabies virus infection of big brown bats (Eptesicus fuscus). J Wildl Dis. 2008;44: 612–621. doi: 10.7589/0090-3558-44.3.612 18689646
33. Kuzmin IV, Franka R, Rupprecht CE, Experimental infection of big brown bats (Eptesicus fuscus) with West Caucasian bat virus (WCBV). Dev Biol. 2008;131: 327–337.
34. Moreno JA, Baer GM, Experimental rabies in the vampire bat. Am J Trop Med Hyg. 1980;29: 254–259. 7369444
35. Pawan JL, Rabies in the vampire bat of Trinidad, with special reference to the clinical course and the latency of infection. Ann Trop Med Parasitol. 1936;30: 401–422.
36. Sims RA, Allen R, Sulkin SE, Studies on the pathogenesis of rabies in insectivorous bats. III. Influence of the gravid state. J Infect Dis. 1963;112: 17–27. 13977575
37. Stamm DD, Kissling RE, Eidson ME, Experimental rabies infection in insectivorous bats. J Infect Dis. 1956;98: 10–14. 13295618
38. Sulkin SE, Krutzsch PH, Allen R, Wallis C, Studies on the pathogenesis of rabies in insectivorous bats. I. Role of brown adipose tissue. J Exp Med. 1959;110: 369–388. 13835624
39. Sulkin SE, Allen R, Sims R, Krutzsch PH, Kim C, Studies on the pathogenesis of rabies in insectivorous bats: II. Influence of environmental temperature. J Exp Med. 1960;112: 595–617. 19867178
40. Van der Poel WHM, Van der Heide R, Van Amerongen G, Van Keulen LJM, Wellenberg GJ, Bourhy H, et al. Characterisation of a recently isolated lyssavirus in frugivorous zoo bats. Arch Virol. 2000;145: 1919–1931. 11043951
41. 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: 2360–2366. doi: 10.1099/vir.0.020073-0 20519458
42. Hayman DTS, Fooks AR, Rowcliffe JM, McCrea R, Restif O, Baker KS, et al. Endemic Lagos bat virus infection in Eidolon helvum. Epidemiol Infect. 2012;140: 2163–2171. doi: 10.1017/S0950268812000167 22370126
43. Swanepoel R, Barnard BJ, Meredith CD, Bishop GC, Brückner GK, Foggin CM, et al. Rabies in southern Africa. Onderstepoort J Vet Res. 1993;60: 325–46. 7777317
44. Peel AJ, Sargan DR, Baker KS, Hayman DTS, Barr JA, Crameri G, et al. Continent-wide panmixia of an African fruit bat facilitates transmission of potentially zoonotic viruses. Nat Commun. 2013;4. doi: 10.1038/ncomms3770 24253424
45. Kamins AO, Restif O, Ntiamoa-Baidu Y, Suu-Ire R, Hayman DTS, Cunningham AA, et al. Uncovering the fruit bat bushmeat commodity chain and the true extent of fruit bat hunting in Ghana, West Africa. Biol Conserv. 2011;144: 3000–8. doi: 10.1016/j.biocon.2011.09.003 22514356
46. Malerczyk C, Selhorst T, Tordo N, Moore S, Müller T, Antibodies induced by vaccination with purified chick embryo cell culture vaccine (PCECV) cross-neutralize non-classical bat lyssavirus strains. Vaccine. 2009;27: 5320–5. doi: 10.1016/j.vaccine.2009.06.095 19615958
47. Freuling CM, Binger T, Beer M, Adu-Sarkodie Y, Schatz J, Fischer M, et al. Lagos bat virus transmission in an Eidolon helvum bat colony, Ghana. Virus Research. 2015;210: 42–45. doi: 10.1016/j.virusres.2015.07.009 26191622
48. Boulger LR, Porterfield JS, Isolation of a virus from Nigerian fruit bats. Trans R Soc Trop Med Hyg. 1958;52: 421–424. 13592882
49. Swanepoel R, Coetzer JAW, Thomson GR, Tustin RC, Rabies. In: Infectious diseases of livestock with special reference to Southern Africa. Cape Town: Oxford University Press; 1994. pp. 493–552.
50. Percy DH, Bhatt PN, Tignor GH, Shope RE, Experimental infection of dogs and monkeys with two rabies serogroup viruses, Lagos bat and Mokola (IbAn 27377): gross pathologic and histopathologic changes. Vet pathol. 1973;10: 534–549. doi: 10.1177/030098587301000607 4214315
51. Tignor GH, Shope RE, Gershon RK, Waksman BH, Immunopathologic aspects of infection with Lagos bat virus of the rabies serogroup. J Immunol. 1974;112: 260–265. 4590821
52. Markotter W, Van Eeden C, Kuzmin IV, Rupprecht CE, Paweska JT, Swanepoel R, et al. Epidemiology and pathogenicity of African bat lyssaviruses. Dev Biol. 2008;131: 317–325.
53. Markotter W, Kuzmin IV, Rupprecht CE, Nel LH, Lagos bat virus virulence in mice inoculated by the peripheral route. Epidemiol Infect. 2009;137: 1155–1162. doi: 10.1017/S0950268808001945 19144249
54. Kgaladi J, Nel LH, Markotter W, Comparison of pathogenic domains of rabies and African rabies-related lyssaviruses and pathogenicity observed in mice. Onderstepoort J Vet Res. 2013. doi: 10.4102/ojvr.v80i1.511 23718883
55. Baker KS, Suu-Ire R, Barr J, Hayman DTS, Broder CC, Horton DL, et al. Viral antibody dynamics in a chiropteran host. J Anim Ecol. 2014;83: 415–428. doi: 10.1111/1365-2656.12153 24111634
56. King AA, Meslin FX, Kaplan MM, Koprowski H, Cell culture of rabies virus. In: Laboratory techniques in rabies. Geneva: World Health Organization; 1996. pp. 114–122.
57. Heaton PR, Johnstone P, McElhinney LM, Cowley R, O’Sullivan E, Whitby JE, Heminested PCR assay for detection of six genotypes of rabies and rabies-related viruses. J Clin Microbiol. 1997;35: 2762–2766. 9350729
58. Hayman DTS, Banyard AC, Wakeley PR, Harkess G, Marston D, Wood JLN, et al. A universal real-time assay for the detection of Lyssaviruses. J Virol Methods. 2011;177: 87–93. doi: 10.1016/j.jviromet.2011.07.002 21777619
59. McElhinney LM, Marston DA, Brookes SM, Fooks AR, Effects of carcase decomposition on rabies virus infectivity and detection. J Virol Methods. 2014;207: 110–113. doi: 10.1016/j.jviromet.2014.06.024 25010791
60. Zimmer K, Wiegand D, Manz D, Frost JW, Reinacher M, Frese K, Evaluation of five different methods for routine diagnosis of rabies. J Vet Med B Infect Dis Vet Public Health. 1990;37: 392–400.
61. Jackson AC, Fu ZF, Jackson AC, Pathogenesis. In: Rabies: scientific basis of the disease and its management. Amsterdam: Academic Press; 2013. pp. 299–349.
62. Lodmell DL, Dimcheff DE, Ewalt LC, Viral RNA in the bloodstream suggests viremia occurs in clinically ill rabies-infected mice. Virus Res. 2006;116: 114–118. doi: 10.1016/j.virusres.2005.09.004 16242805
63. Preuss MAR, Faber ML, Tan GS, Bette M, Dietzschold B, Weihe E, et al. Intravenous inoculation of a bat-associated rabies virus causes lethal encephalopathy in mice through invasion of the brain via neurosecretory hypothalamic fibers. PLoS Pathog. 2009;5. e1000485doi: 10.1371/journal.ppat.1000485 19543379
64. Kuzmin IV, Rupprecht CE, Wang LF, Cowled C, Bat lyssaviruses. In: Bats and viruses. Hoboken: John Wiley & Sons; 2015. pp. 47–97.
65. Artois M, Bourhy H, Müller T, Selhorst T, Smith GC, Gavier-Widen D, Duff JP, Meredith A, Lyssavirus infections. In: Infectious diseases of wild mammals and birds in Europe. Oxford: Wiley-blackwell; 2012. pp. 86–98.
66. Hooper PT, Lunt RA, Gould AR, Samaratunga H, A new lyssavirus—the first endemic rabies-related virus recognized in Australia. Bull Inst Pasteur. 1997;95: 209–218.
67. Smart NL, Charlton KM, The distribution of challenge virus standard rabies virus versus skunk street rabies virus in the brains of experimentally infected rabid skunks. Acta Neuropathol. 1992;84: 501–508. 1462765
68. Hicks DJ, Nunez A, Healy DM, Brookes SM, Johnson N, Fooks AR, Comparative pathological study of the murine brain after experimental infection with classical rabies virus and European bat lyssaviruses. J Comp Pathol. 2009;140: 113–126. doi: 10.1016/j.jcpa.2008.09.001 19111840
69. Aloisi F, Ria F, Adorini L, Regulation of T-cell responses by CNS antigen-presenting cells: different roles for microglia and astrocytes. Immunol Today. 2000;21: 141–147. 10689302
70. Weller RO, Pathology of cerebrospinal fluid and interstitial fluid of the CNS: significance for Alzheimer disease, prion disorders and multiple sclerosis. J Neuropathol Exp Neurol. 1998;57: 885–894. 9786239
71. Kuzmin IV, Niezgoda M, Franka R, Agwanda B, Markotter W, Beagley JC, et al. Lagos bat virus in Kenya. J Clin Microbiol. 2008;46: 1451–1461. doi: 10.1128/JCM.00016-08 18305130
72. Charlton KM, Casey GA, Campbell JB, Experimental rabies in skunks: effects of immunosuppression induced by cyclophosphamide. Can J Comp Med. 1984;48: 72–77. 6370390
73. Charlton KM, Casey GA, Campbell JB, Experimental rabies in skunks: immune response and salivary gland infection. Comp Immunol Microbiol Infect Dis. 1987;10: 227–35. 3427891