Diseases and causes of death in European bats: Dynamics in disease susceptibility and infection rates

PLoS ONE

Volumn 6, Issue 12, 2011, Pages

  Mühldorfer, Kristin ^a   Speck, Stephanie ^b   Kurth, Andreas ^c   Lesnik, René ^c   Freuling, Conrad ^d   Müller, Thomas ^d   Kramer Schadt, Stephanie ^a   Wibbelt, Gudrun ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b BUNDESWEHR INSTITUTE OF MICROBIOLOGY   (Germany)

^c ROBERT KOCH INSTITUTE   (Germany)

^d FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; AUTOPSY; BACTERIAL INFECTION; BACTERIUM EXAMINATION; BAT; CARCASS; CAUSE OF DEATH; CONTROLLED STUDY; DISEASE TRANSMISSION; FEMALE; GERMANY; HISTOPATHOLOGY; INFECTION RATE; INFECTION RISK; INFECTION SENSITIVITY; INJURY; MALE; NONHUMAN; PARASITE EXAMINATION; PARASITOSIS; PREVALENCE; RISK FACTOR; SEASONAL VARIATION; SPECIES DIFFERENCE; VESPERTILIONIDAE; VIRUS EXAMINATION; VIRUS INFECTION; ANIMAL; ANIMAL DISEASE; DISEASE PREDISPOSITION; MORTALITY; NUCLEOTIDE SEQUENCE; VIROLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); MAMMALIA; VESPERTILIONIDAE;

PRIMER DNA;

ANIMAL DISEASES; ANIMALS; BASE SEQUENCE; CAUSE OF DEATH; CHIROPTERA; DISEASE SUSCEPTIBILITY; DNA PRIMERS; GERMANY;

EID: 84555203660     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029773     Document Type: Article

References (66)

1. Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, et al. (2008) The status of the world's land and marine mammals: diversity, threat and knowledge. Science 322: 225-230.
2. Kunz TH, de Torrez EB, Bauer D, Lobova T, Fleming TH, (2011) Ecosystem services provided by bats. Ann N Y Acad Sci 1223: 1-38.
3. Mickleburgh SP, Hutson AM, Racey PA, (2002) A review of the global conservation status of bats. Oryx 36: 18-34.
4. Wibbelt G, Moore MS, Schountz T, Voigt CC, (2010) Emerging diseases in Chiroptera: why bats? Biol Lett 6: 438-440.
5. Wibbelt G, Speck S, Field H, (2009) Methods for assessing diseases in bats. In: Kunz TH, Parsons S, editors. Ecological and Behavioral Methods for the Study of Bats. 2nd Edition The Johns Hopkins University Press pp. 775-794.
6. Halpin K, Young PL, Field HE, Mackenzie JS, (2000) Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81: 1927-1932.
7. Chua KB, Koh CL, Hooi PS, Wee KF, Khong JH, et al. (2002) Isolation of Nipah virus from Malaysian Island flying-foxes. Microbes Infect 4: 145-151.
8. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, et al. (2005) Fruit bats as reservoirs of Ebola virus. Nature 438: 575-576.
9. Li W, Shi Z, Yu M, Ren W, Smith C, et al. (2005) Bats are natural reservoirs of SARS-like coronaviruses. Science 310: 676-679.
10. Wong S, Lau S, Woo P, Yuen K-Y, (2007) Bats as a continuing source of emerging infections in humans. Rev Med Virol 17: 67-91.
11. Towner JS, Amman BR, Sealy TK, Carroll SAR, Comer JA, et al. (2009) Isolation of genetically diverse Marburg viruses from Egyptian fruit bats. PLoS Pathog 5: e1000536.
12. Kuzmin IV, Bozick B, Guagliardo SA, Kunkel R, Shak JR, et al. (2011) Bats, emerging infectious diseases, and the rabies paradigm revisited. Emerging Health Threats Journal 4: 7159.
13. Simpson VR, (2000) Veterinary advances in the investigation of wildlife diseases in Britain. Res Vet Sci 69: 11-16.
14. Daffner B, (2001) Causes of morbidity and mortality in British bat species and prevalence of selected zoonotic pathogens. Thesis for MSc in Wild Animal Health, University of London.
15. Duignan P, Horner G, O'Keefe J, (2003) Infectious and emerging diseases of bats, and health status of bats in New Zealand. Surveillance 30: 15-18.
16. Hajkova P, Pikula J, (2007) Veterinary treatment of evening bats (Vespertilionidae) in the Czech Republic. Vet Rec 161: 139-140.
17. Harris SL, Brookes SM, Jones G, Hutson AM, Racey PA, et al. (2006) European bat lyssaviruses: distribution, prevalence and implications for conservation. Biol Conserv 131: 193-210.
18. Müller T, Johnson N, Freuling CM, Fooks AS, Selhorst T, et al. (2007) Epidemiology of bat rabies in Germany. Arch Virol 152: 273-288.
19. Gloza-Rausch F, Ipsen A, Seebens A, Göttsche M, Panning M, et al. (2008) Detection and prevalence patterns of group I coronaviruses in bats, northern Germany. Emerg Infect Dis 14: 626-631.
20. Rihtaric D, Hostnik P, Steyer A, Grom J, Toplak I, (2010) Identification of SARS-like coronavirus in horseshoe bats (Rhinolophus hipposideros) in Slovenia. Arch Virol 155: 507-514.
21. Evans NJ, Bown K, Timofte D, Simpson VR, Birtles RJ, (2009) Fatal borreliosis in bat caused by relapsing fever spirochete, United Kingdom. Emerg Infect Dis 15: 1331-1333.
22. Mühldorfer K, Wibbelt G, Haensel J, Riehm J, Speck S, (2010) Yersinia species isolated from bats, Germany. Emerg Infec Dis 16: 578-580.
23. Mühldorfer K, Schwarz S, Fickel J, Wibbelt G, Speck S, (2011) Genetic diversity of Pasteurella species isolated from European vespertilionid bats. Vet Microbiol 149: 163-171.
24. Wibbelt G, Kurth A, Yasmum N, Bannert M, Nagel S, et al. (2007) Discovery of herpesviruses in bats. J Gen Virol 88: 2651-2655.
25. Sonntag M, Mühldorfer K, Speck S, Wibbelt G, Kurth A, (2009) New adenovirus in bats, Germany. Emerg Infect Dis 15: 2052-2055.
26. Mühldorfer K, Speck S, Wibbelt G, (2011) Diseases in free-ranging bats from Germany. BMC Vet Res 7: 61.
27. Gaisler J, Zukal J, Rehak Z, Homolka M, (1998) Habitat preference and flight activity of bats in a city. J Zool Lond 244: 439-445.
28. O'Shea TJ, Neubaum DJ, Neubaum MA, Cryan PM, Ellison LE, et al. (2011) Bat ecology and public health surveillance for rabies in an urbanizing region of Colorado. Urban Ecosystem DOI 10.1007/s11252-011-0182-7.
29. Bisping W, Amtsberg G, (1988) Colour Atlas for the Diagnosis of Bacterial Pathogens in Animals. Paul Parey Scientific Publishers. Berlin, Hamburg.
30. Brenner DJ, Krieg NR, Staley JT, (2005) Bergey's Manual of Systematic Bacteriology. 2nd Edition. Springer, New York.
31. Sánchez-Seco MP, Rosario D, Domingo C, Hernández L, Valdés K, et al. (2005) Generic RT-nested-PCR for detection of flaviviruses using degenerated primers and internal control followed by sequencing for specific identification. J Virol Methods 126: 101-109.
32. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V, et al. (2006) Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 12: 838-840.
33. de Souza Luna LK, Heiser V, Regamey N, Panning M, Drexler JF, et al. (2007) Generic detection of coronaviruses and differentiation at the prototype strain level by reverse transcription-PCR and nonfluorescent low-density microarray. J Clin Microbiol 45: 1049-1052.
34. Spackman E, Senne DA, Myers TJ, Bulaga JL, Garber LP, et al. (2002) Development of a real-time reverse transcriptase PCR assay for type A influenza virus and the avian H5 and H7 hemagglutinin subtypes. J Clin Microbiol 40: 3256-3260.
35. Dean D, Abelseth MK, (1996) The fluorescent antibody test. In: Meslin FX, Kaplan MM, Koprowski H, editors. Laboratory Techniques in Rabies. 4th Edition World Health Organization pp. 88-95.
36. Webster WA, Casey GA, (1996) Virus isolation in neuroblastoma cell culture. In: Meslin FX, Kaplan MM, Koprowski H, editors. Laboratory Techniques in Rabies. 4th Edition World Health Organization pp. 96-103.
37. Schneider LG, Barnard BJH, Schneider HP, (1985) Application of monoclonal antibodies for epidemiological investigations and oral vaccination studies. In: Kuwert E, Mérieux C, Koprowski H, Bögel K, editors. Rabies in the Tropics Springer, Berlin pp. 47-59.
38. Linacre A, Lee JC, (2005) Species determination: the role and use of the cytochrome b gene. Methods Mol Biol 297: 45-52.
39. Kaňuch P, Hájková P, Řehák Z, Bryja J, (2007) A rapid PCR-based test for species identification of two cryptic bats Pipistrellus pipistrellus and P. pygmaeus and its application on museum and dropping samples. Acta Chirop 9: 277-282.
40. Akaike H, (1973) Information theory as an extension of the maximum likelihood principle. In: Petrov BN, Csaki F, editors. Second International Symposium on Information Theory Akademiai Kiado, Budapest, UK pp. 267-281.
41. Bradley CA, Altizer S, (2007) Urbanization and the ecology of wildlife diseases. Trends Ecol Evol 22: 95-102.
42. Christe P, Arlettaz R, Vogel P, (2000) Variation of intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol Lett 3: 207-212.
43. Zahn A, Rupp D, (2004) Ectoparasite load in European vespertilionid bats. J Zool Lond 262: 383-391.
44. Lučan RK, (2006) Relationships between the parasitic mite Spinturnix andegavinus (Acari: Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera: Vespertilionidae): seasonal, sex- and age-related variation in infestation and possible impact of the parasite on the host condition and roosting behavior. Folia Parasitol 53: 147-152.
45. Christe P, Glaizot O, Evanno G, Bruyndonckx N, Devevey G, et al. (2007) Host sex and ectoparasites choice: preference for, and higher survival on female host. J Anim Ecol 76: 703-710.
46. Plowright RK, Field HE, Smith C, Divljan A, Palmer C, et al. (2008) Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus). Proc Biol Sci 275: 861-869.
47. 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.
48. Ciechanowsky M, Zaja{ogonek}c T, Zielińska A, Dunajski R, (2010) Seasonal activity patterns of seven vespertilionid bat species in Polish lowlands. Acta Theriol 55: 301-314.
49. Bouma HR, Carey HV, Kroese FGM, (2010) Hibernation: the immune system at rest? J Leukoc Biol 88: 619-624.
50. Peterson JW, (1996) Bacterial Pathogenesis. In: Baron S, editors. Medical Microbiology. 4th Edition Galveston (TX) University of Texas Medical Branch at Galveston. Chapter 7.
51. Talan DA, Citron DM, Abrahamian FM, Moran GJ, Goldstein EJC, (1999) Bacteriologic analysis of infected dog and cat bites. N Engl J Med 340: 85-92.
52. Dacheux L, Larrous F, Mailles A, Boisseleau D, Delmas O, et al. (2009) European bat lyssavirus transmission among cats, Europe. Emerg Infect Dis 15: 280-284.
53. Johnson N, Vos A, Freuling C, Tordo N, Fooks AR, et al. (2010) Human rabies due to lyssavirus infection of bat origin. Vet Microbiol 142: 151-159.
54. Freuling C, Grossmann E, Conraths F, Schameitat A, Kliemt J, et al. (2008) First isolation of EBLV-2 in Germany. Vet Microbiol 131: 26-34.
55. Freuling C, Beer M, Conraths FJ, Finke S, Hoffmann B, et al. (2011) Novel lyssavirus in Natterer's bat, Germany. Emerg Infect Dis 17: 1519-1522.
56. Kuzmin IV, Rupprecht CE, (2007) Bat rabies. In: Jackson AC, Wunner W, editors. Rabies 2nd Edition Academic Press, New York pp. 259-307.
57. Thiry E, Vercouter M, Dubuisson J, Barrat J, Sepulchre C, et al. (1988) Serological survey of herpesvirus infections in wild ruminants of France and Belgium. J Wildl Dis 24: 268-273.
58. Schrenzel MD, Tucker TA, Donovan TA, Busch MDM, Wise AG, et al. (2008) New hosts for equine herpesvirus 9. Emerg Infect Dis 14: 1616-1619.
59. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, et al. (2010) Host phylogeny constrains cross-species emergence of rabies virus in bats. Science 329: 676-679.
60. Hart BL, (1992) Behavioral adaptations to parasites: an ethological approach. J Parasitol 78: 256-265.
61. ter Hofstede HM, Fenton MB, (2005) Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. J Zool Lond 266: 333-340.
62. Patterson BD, Dick CW, Dittmar K, (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23: 177-189.
63. Pearce RD, O'Shea TJ, (2007) Ectoparasites in an urban population of big brown bats (Eptesicus fuscus) in Colorado. J Parasitol 93: 518-530.
64. Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, et al. (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25: 362-371.
65. Aguirre LF, Herrel A, Van Damme R, Matthysen E, (2003) The implications of food hardness for diet in bats. Funct Ecol 17: 201-212.
66. Feldhamer GA, Carter TC, Whitaker JO Jr, (2009) Prey consumed by eight species of insectivorous bats from Southern Illinois. Am Midl Nat 162: 43-51.