Influence of age and body condition on astrovirus infection of bats in Singapore: An evolutionary and epidemiological analysis

One Health

Volumn 4, Issue , 2017, Pages 27-33

  Mendenhall, Ian H ^a   Skiles, Maggie M ^b   Neves, Erica Sena ^a   Borthwick, Sophie A ^a   Low, Dolyce H W ^a   Liang, Benjamin ^a   Lee, Benjamin P Y H ^c   Su, Yvonne C F ^a   Smith, Gavin J D ^a,d  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c National Parks Board   (Singapore)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bat borne virus; Eonycteris spelaea; Epidemiology; Phylogenetics; Pooling prevalence; Rhinolophus lepidus; Southeast Asia

Indexed keywords

ADULT; AGE; ARTICLE; ASTROVIRIDAE; ASTROVIRUS INFECTION; BANGLADESH; BAT; BODY CONSTITUTION; CHINA; EONYCTERIS SPELAEA; FECES ANALYSIS; FEMALE; GEOGRAPHIC DISTRIBUTION; JUVENILE ANIMAL; LAOS; MALE; NONHUMAN; PHYLOGENY; PTEROPUS GIGANTEUS; RHINOLOPHUS LEPIDUS; ROUSETTUS; SINGAPORE; VIRUS CELL INTERACTION; VIRUS DETECTION; VIRUS GENE; VIRUS SHEDDING; VIRUS TRANSMISSION;

EID: 85032205644     PISSN: None     EISSN: 23527714     Source Type: Journal    
DOI: 10.1016/j.onehlt.2017.10.001     Document Type: Article

References (64)

1. IUCN, Status Category Summary by Major Taxonomic Groups (Animals). 2016, International Union for Conservation of Nature.
2. Nunn, C.L., Altizer, S., Sechrest, W., Jones, K.E., Barton, R.A., Gittleman, J.L., Parasites and the evolutionary diversification of primate clades. Am. Nat. 164 (2004), S90–S103.
3. Morse, S.S., Mazet, J.A., Woolhouse, M., Parrish, C.R., Carroll, D., Karesh, W.B., Zambrana-Torrelio, C., Lipkin, W.I., Daszak, P., Prediction and prevention of the next pandemic zoonosis. Lancet 380 (2012), 1956–1965.
4. Rabaa, M.A., Tue, N.T., Phuc, T.M., Carrique-Mas, J., Saylors, K., Cotten, M., Bryant, J.E., Nghia, H.D., Cuong, N.V., Pham, H.A., Berto, A., Phat, V.V., Dung, T.T., Bao, L.H., Hoa, N.T., Wertheim, H., Nadjm, B., Monagin, C., van Doorn, H.R., Rahman, M., Tra, M.P., Campbell, J.I., Boni, M.F., Tam, P.T., van der Hoek, L., Simmonds, P., Rambaut, A., Toan, T.K., Van Vinh Chau, N., Hien, T.T., Wolfe, N., Farrar, J.J., Thwaites, G., Kellam, P., Woolhouse, M.E., Baker, S., The Vietnam initiative on zoonotic infections (VIZIONS): a strategic approach to studying emerging zoonotic infectious diseases. EcoHealth 12 (2015), 726–735.
5. Longdon, B., Hadfield, J.D., Webster, C.L., Obbard, D.J., Jiggins, F.M., Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathog., 7, 2011, e1002260.
6. Webby, R., Hoffmann, E., Webster, R., Molecular constraints to interspecies transmission of viral pathogens. Nat. Med. 10 (2004), S77–81.
7. Parrish, C.R., Holmes, E.C., Morens, D.M., Park, E.C., Burke, D.S., Calisher, C.H., Laughlin, C.A., Saif, L.J., Daszak, P., Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 72 (2008), 457–470.
8. Méndez, E., Murillo, A., Velázquez, R., Burnham, A., Arias, C.F., Replication cycle of astroviruses. Astrovirus Research, 2013, Springer, 19–45.
9. Bidin, M., Bidin, Z., Majnaric, D., Tisljar, M., Lojkic, I., Circulation and phylogenetic relationship of chicken and turkey-origin astroviruses detected in domestic ducks (Anas platyrhynchos domesticus). Avian. Pathol. 41 (2012), 555–562.
10. Pantin-Jackwood, M.J., Spackman, E., Woolcock, P.R., Phylogenetic analysis of Turkey astroviruses reveals evidence of recombination. Virus Genes 32 (2006), 187–192.
11. Cattoli, G., Chu, D.K.W., Peiris, M., Astrovirus Infections in Animal Mammalian Species, Astrovirus Research. 2013, Springer, 135–149.
12. Benedictis, P., Schultz-Cherry, S., Burnham, A., Cattoli, G., Astrovirus infections in humans and animals - molecular biology, genetic diversity, and interspecies transmissions. Infect. Genet. Evol., 11, 2011.
13. Koci, M.D., Schultz-Cherry, S., Avian astroviruses. Avian Pathol. 31 (2002), 213–227.
14. Clark, B., McKendrick, M., A review of viral gastroenteritis. Curr. Opin. Infect. Dis. 17 (2004), 461–469.
15. Li, L., Diab, S., McGraw, S., Barr, B., Traslavina, R., Higgins, R., Talbot, T., Blanchard, P., Rimoldi, G., Fahsbender, E., Page, B., Phan, T.G., Wang, C., Deng, X., Pesavento, P., Delwart, E., Divergent astrovirus associated with neurologic disease in cattle. Emerg. Infect. Dis. 19 (2013), 1385–1392.
16. Schlottau, K., Schulze, C., Bilk, S., Hanke, D., Hoper, D., Beer, M., Hoffmann, B., Detection of a novel bovine astrovirus in a cow with encephalitis. Transbound. Emerg. Dis. 63 (2016), 253–259.
17. Sun, N., Yang, Y., Wang, G.S., Shao, X.Q., Zhang, S.Q., Wang, F.X., Tan, B., Tian, F.L., Cheng, S.P., Wen, Y.J., Detection and characterization of avastrovirus associated with diarrhea isolated from minks in China. Food Environ. Virol. 6 (2014), 169–174.
18. Da Silva, S.E., Bonetti, A.M., Petrocelli, A.T., Ferrari, H.F., Luvizotto, M.C., Cardoso, T.C., Detection of Turkey astrovirus in young poults affected with poult enteritis complex in Brazil. J. Vet. Med. Sci. 70 (2008), 629–631.
19. Cattoli, G., Toffan, A., De Battisti, C., Salviato, A., Terregino, C., Capua, I., Astroviruses found in the intestinal contents of guinea fowl suffering from enteritis. Vet. Rec., 156, 2005, 220.
20. Mor, S.K., Chander, Y., Marthaler, D., Patnayak, D.P., Goyal, S.M., Detection and molecular characterization of porcine astrovirus strains associated with swine diarrhea. J. Vet. Diagn. Investig. 24 (2012), 1064–1067.
21. Bidin, M., Lojkic, I., Tisljar, M., Bidin, Z., Majnaric, D., Astroviruses associated with stunting and pre-hatching mortality in duck and goose embryos. Avian Pathol. 41 (2012), 91–97.
22. Bulbule, N.R., Mandakhalikar, K.D., Kapgate, S.S., Deshmukh, V.V., Schat, K.A., Chawak, M.M., Role of chicken astrovirus as a causative agent of gout in commercial broilers in India. Avian Pathol. 42 (2013), 464–473.
23. Candido, M., Alencar, A.L., Almeida-Queiroz, S.R., Buzinaro Mda, G., Munin, F.S., de Godoy, S.H., Livonesi, M.C., Fernandes, A.M., de Sousa, R.L., Molecular detection and phylogenetic analysis of bovine astrovirus in Brazil. Arch. Virol. 160 (2015), 1519–1525.
24. Phan, T.G., Vo, N.P., Boros, A., Pankovics, P., Reuter, G., Li, O.T., Wang, C., Deng, X., Poon, L.L., Delwart, E., The viruses of wild pigeon droppings. PLoS One, 8, 2013, e72787.
25. Chu, D.K., Leung, C.Y., Perera, H.K., Ng, E.M., Gilbert, M., Joyner, P.H., Grioni, A., Ades, G., Guan, Y., Peiris, J.S., Poon, L.L., A novel group of avian astroviruses in wild aquatic birds. J. Virol. 86 (2012), 13772–13778.
26. Grimaldi, W.W., Hall, R.J., White, D.D., Wang, J., Massaro, M., Tompkins, D.M., First report of a feather loss condition in Adelie penguins (Pygoscelis adeliae) on Ross Island, Antarctica, and a preliminary investigation of its cause. Emu 115 (2015), 185–189.
27. Mendenhall, I.H., Yaung, K.N., Joyner, P.H., Keatts, L., Borthwick, S., Neves, E.S., San, S., Gilbert, M., Smith, G.J., Detection of a novel astrovirus from a black-naped monarch (Hypothymis azurea) in Cambodia. Virol. J., 12, 2015, 182.
28. Zhou, P., Tachedjian, M., Wynne, J.W., Boyd, V., Cui, J., Smith, I., Cowled, C., Ng, J.H., Mok, L., Michalski, W.P., Mendenhall, I.H., Tachedjian, G., Wang, L.F., Baker, M.L., Contraction of the type I IFN locus and unusual constitutive expression of IFN-alpha in bats. PNAS 113 (2016), 2696–2701.
29. Sodhi, N.S., Koh, L.P., Brook, B.W., Ng, P.K.L., Southeast Asian biodiversity: an impending disaster. Trends Ecol. Evol. 19 (2004), 654–660.
30. Mendenhall, I.H., Borthwick, S., Neves, E.S., Low, D., Linster, M., Liang, B., Skiles, M., Jayakumar, J., Han, H., Gunalan, V., Lee, B.P., Okahara, K., Wang, L.F., Maurer-Stroh, S., Su, Y.C., Smith, G.J., Identification of a lineage D Betacoronavirus in cave nectar bats (Eonycteris Spelaea) in Singapore and an overview of lineage D reservoir ecology in SE Asian bats. Transbound. Emerg. Dis., 2016.
31. Mendenhall, I.H., Low, D., Neves, E.S., Anwar, A., Oh, S., Su, Y.C., Smith, G.J., Evidence of Canine Parvovirus Transmission to a Civet Cat (Paradoxurus musangus) in Singapore. 2016, One Health.
32. Chu, D.K., Poon, L.L., Guan, Y., Peiris, J.S., Novel astroviruses in insectivorous bats. J. Virol. 82 (2008), 9107–9114.
33. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., Drummond, A., Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 (2012), 1647–1649.
34. Stamatakis, A., Ludwig, T., Meier, H., RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21 (2005), 456–463.
35. Sergeant, E.S.G., Epitools Epidemiological Calculators. 2017, Ausvet Pty Ltd.
36. Green, A.J., Mass/length residuals: measures of body condition or generators of spurious results?. Ecology 82 (2001), 1473–1483.
37. Hamilton, L.C., Statistics With Stata: version 12. 2012, Cengage Learning.
38. Fischer, K., Pinho Dos Reis, V., Balkema-Buschmann, A., Bat astroviruses: towards understanding the transmission dynamics of a neglected virus family. Viruses, 9, 2017.
39. Hu, B., Chmura, A.A., Li, J., Zhu, G., Desmond, J.S., Zhang, Y., Zhang, W., Epstein, J.H., Daszak, P., Shi, Z., Detection of diverse novel astroviruses from small mammals in China. J. Gen. Virol. 95 (2014), 2442–2449.
40. Wu, Z., Ren, X., Yang, L., Hu, Y., Yang, J., He, G., Zhang, J., Dong, J., Sun, L., Du, J., Liu, L., Xue, Y., Wang, J., Yang, F., Zhang, S., Jin, Q., Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J. Virol. 86 (2012), 10999–11012.
41. Zhu, H.C., Chu, D.K., Liu, W., Dong, B.Q., Zhang, S.Y., Zhang, J.X., Li, L.F., Vijaykrishna, D., Smith, G.J., Chen, H.L., Poon, L.L., Peiris, J.S., Guan, Y., Detection of diverse astroviruses from bats in China. J. Gen. Virol. 90 (2009), 883–887.
42. Dufkova, L., Strakova, P., Sirmarova, J., Salat, J., Moutelikova, R., Chrudimsky, T., Bartonicka, T., Nowotny, N., Ruzek, D., Detection of diverse novel bat Astrovirus sequences in the Czech Republic. Vector Borne Zoonot. Dis. 15 (2015), 518–521.
43. Seltmann, A., Corman, V.M., Rasche, A., Drosten, C., Czirjak, G.A., Bernard, H., Struebig, M.J., Voigt, C.C., Seasonal fluctuations of astrovirus, but not coronavirus shedding in bats inhabiting human-modified tropical forests. EcoHealth 14 (2017), 272–284.
44. Lacroix, A., Duong, V., Hul, V., San, S., Davun, H., Omaliss, K., Chea, S., Hassanin, A., Theppangna, W., Silithammavong, S., Khammavong, K., Singhalath, S., Afelt, A., Greatorex, Z., Fine, A.E., Goldstein, T., Olson, S., Joly, D.O., Keatts, L., Dussart, P., Frutos, R., Buchy, P., Diversity of bat astroviruses in Lao PDR and Cambodia. Infect. Genet. Evol. 47 (2017), 41–50.
45. Drexler, J.F., Corman, V.M., Wegner, T., Tateno, A.F., Zerbinati, R.M., Gloza-Rausch, F., Seebens, A., Muller, M.A., Drosten, C., Amplification of emerging viruses in a bat colony. Emerg. Infect. Dis. 17 (2011), 449–456.
46. Hayman, D.T., Biannual birth pulses allow filoviruses to persist in bat populations. Proc. R. Soc. Lond. Biol. 282 (2015), 2014–2591.
47. Karlsson, E.A., Small, C.T., Freiden, P., Feeroz, M.M., Matsen, F.A.t., San, S., Hasan, M.K., Wang, D., Jones-Engel, L., Schultz-Cherry, S., Non-human primates harbor diverse mammalian and avian astroviruses including those associated with human infections. PLoS Pathog., 11, 2015, e1005225.
48. Fischer, K., Zeus, V., Kwasnitschka, L., Kerth, G., Haase, M., Groschup, M.H., Balkema-Buschmann, A., Insectivorous bats carry host specific astroviruses and coronaviruses across different regions in Germany. Infect. Genet. Evol. 37 (2016), 108–116.
49. Lau, S.K., Li, K.S., Tsang, A.K., Shek, C.T., Wang, M., Choi, G.K., Guo, R., Wong, B.H., Poon, R.W., Lam, C.S., Wang, S.Y., Fan, R.Y., Chan, K.H., Zheng, B.J., Woo, P.C., Yuen, K.Y., Recent transmission of a novel alphacoronavirus, bat coronavirus HKU10, from Leschenault's rousettes to pomona leaf-nosed bats: first evidence of interspecies transmission of coronavirus between bats of different suborders. J. Virol. 86 (2012), 11906–11918.
50. Mendenhall, I.H., Smith, G.J., Dhanasekaran, V., Ecological drivers of virus evolution: astrovirus as a case study. J. Virol.(JVI), 2015, 02971–02974.
51. Vijaykrishna, D., Smith, G.J., Zhang, J.X., Peiris, J.S., Chen, H., Guan, Y., Evolutionary insights into the ecology of coronaviruses. J. Virol., 2007, 4012–4020.
52. Hu, B., Ge, X., Wang, L.F., Shi, Z., Bat origin of human coronaviruses. Virol. J., 12, 2015, 221.
53. Guix, S., Caballero, S., Villena, C., Bartolome, R., Latorre, C., Rabella, N., Simo, M., Bosch, A., Pinto, R.M., Molecular epidemiology of astrovirus infection in Barcelona, Spain. J. Clin. Microbiol. 40 (2002), 133–139.
54. Kofstad, T., Jonassen, C.M., Screening of feral and wood pigeons for viruses harboring a conserved mobile viral element: characterization of novel Astroviruses and Picornaviruses. PLoS One, 6, 2011, e25964.
55. Larsen, P.F., Møller, S., Clausen, T., Hammer, A., Proceedings of the Xth International Scientific Congress in Fur Animal Production. 2012, Wageningen Academic Pub.
56. Grellet, A., De Battisti, C., Feugier, A., Pantile, M., Marciano, S., Grandjean, D., Cattoli, G., Prevalence and risk factors of astrovirus infection in puppies from French breeding kennels. Vet. Microbiol. 157 (2012), 214–219.
57. Fu, Y., Pan, M., Wang, X., Xu, Y., Xie, X., Knowles, N.J., Yang, H., Zhang, D., Complete sequence of a duck astrovirus associated with fatal hepatitis in ducklings. J. Gen. Virol. 90 (2009), 1104–1108.
58. Awe, O.O., Kang, K.I., Ibrahim, M., Ali, A., Elaish, M., Saif, Y.M., Lee, C.W., Age-related susceptibility of turkeys to enteric viruses. Avian Dis. 59 (2015), 207–212.
59. Calisher, C.H., Childs, J.E., Field, H.E., Holmes, K.V., Schountz, T., Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 19 (2006), 531–545.
60. Farrington, C.P., Whitaker, H.J., Estimation of effective reproduction numbers for infectious diseases using serological survey data. Biostatistics 4 (2003), 621–632.
61. Nunn, C.L., Jordan, F., McCabe, C.M., Verdolin, J.L., Fewell, J.H., Infectious disease and group size: more than just a numbers game. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 370, 2015.
62. Tan, K., Akbar, Z., Kunz, T., Roost selection and social organisation in Cynopterus horsfieldi (Chiroptera: Pteropodidae). Malay. Nat. J. 53 (1999), 295–298.
63. Hayman, D.T., Bowen, R.A., Cryan, P.M., McCracken, G.F., O'Shea, T.J., Peel, A.J., Gilbert, A., Webb, C.T., Wood, J.L., Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses Public Health 60 (2013), 2–21.
64. Heideman, P.D., Utzurrum, R.C., Seasonality and synchrony of reproduction in three species of nectarivorous Philippines bats. BMC Ecol. 3 (2003), 1–14.