Predicting disease severity and viral spread of h5n1 influenza virus in ferrets in the context of natural exposure routes

Journal of Virology

Volumn 90, Issue 4, 2016, Pages 1888-1897

  Edenborough, Kathryn M ^a   Lowther, Suzanne ^b   Laurie, Karen ^a   Yamada, Manabu ^b,c   Long, Fenella ^b   Bingham, John ^b   Payne, Jean ^b   Harper, Jennifer ^b   Haining, Jessica ^b   Arkinstall, Rachel ^b   Gilbertson, Brad ^a   Middleton, Deborah ^b   Brown, Lorena E ^a  

^a PETER DOHERTY INSTITUTE FOR INFECTION AND IMMUNITY   (Australia)

^b CSIRO   (Australia)

^c NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM INFECTION; CEREBROSPINAL FLUID; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FERRET; INFLUENZA A (H5N1); LIVER; LUNG; LYMPH NODE; MALE; NONHUMAN; OLFACTORY EPITHELIUM; PANCREAS; PREDICTION; PRIORITY JOURNAL; SEROCONVERSION; SMALL INTESTINE; SPLEEN; SURVIVAL RATE; TRACHEA; TURBINATE; UPPER RESPIRATORY TRACT INFECTION; VIRAL RESPIRATORY TRACT INFECTION; VIREMIA; VIRUS TRANSMISSION; ANIMAL; DISEASE MODEL; DISEASE TRANSMISSION; INFLUENZA A VIRUS (H5N1); MORTALITY; MUSTELA PUTORIUS FURO; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; RISK ASSESSMENT; SURVIVAL ANALYSIS; TRANSMISSION; VIROLOGY;

ANIMALS; DISEASE MODELS, ANIMAL; DISEASE TRANSMISSION, INFECTIOUS; FEMALE; FERRETS; INFLUENZA A VIRUS, H5N1 SUBTYPE; MALE; ORTHOMYXOVIRIDAE INFECTIONS; RISK ASSESSMENT; SURVIVAL ANALYSIS;

EID: 84958068669     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01878-15     Document Type: Article

References (56)

1. Dinh PN, Long HT, Tien NT, Hien NT, Mai le TQ, Phong le H, Tuan le V, Van Tan H, Nguyen NB, Van Tu P, Phuong NT, World Health Organization/Alert and Response Network Avian Influenza Investigation Team in Vietnam. 2006. Risk factors for human infection with avian influenza A H5N1, Vietnam, 2004. Emerg Infect Dis 12:1841-1847. http://dx.doi.org/10.3201/eid1212.060829.
2. Chotpitayasunondh T, Ungchusak K, Hanshaoworakul W, Chunsuthiwat S, Sawanpanyalert P, Kijphati R, Lochindarat S, Srisan P, Suwan P, Osotthanakorn Y, Anantasetagoon T, Kanjanawasri S, Tanupattarachai S, Weerakul J, Chaiwirattana R, Maneerattanaporn M, Poolsavathitikool R, Chokephaibulkit K, Apisarnthanarak A, Dowell SF. 2005. Human disease from influenza A (H5N1), Thailand, 2004. Emerg Infect Dis +11: 201-209. http://dx.doi.org/10.3201/eid1102.041061.
3. Mounts AW, Kwong H, Izurieta HS, Ho Y, Au T, Lee M, Buxton Bridges C, Williams SW, Mak KH, Katz JM, Thompson WW, Cox NJ, Fukuda K. 1999. Case-control study of risk factors for avian influenza A (H5N1) disease, Hong Kong, 1997. J Infect Dis 180:505-508. http://dx.doi.org/10.1086/314903.
4. Zhou L, Liao Q, Dong L, Huai Y, Bai T, Xiang N, Shu Y, Liu W, Wang S, Qin P, Wang M, Xing X, Ly J, Chen RY, Feng Z, Yang W, Uyeki T, Yu H. 2009. Risk factors for human illness with avian influenza A (H5N1) virus infection in China. J Infect Dis 199:1726-1734. http://dx.doi.org/10.1086/599206.
5. Van Kerkhove MD, Ly S, Holl D, Guitian J, Mangtani P, Ghani AC, Vong S. 2008. Frequency and patterns of contact with domestic poultry and potential risk of H5N1 transmission to humans living in rural Cambodia. Influenza Other Respir Viruses 2:155-163. http://dx.doi.org/10.1111/j.1750-2659.2008.00052.x.
6. Van Kerkhove MD, Mumford E, Mounts AW, Bresee J, Ly S, Bridges CB, Otte J. 2011. Highly pathogenic avian influenza (H5N1): pathways of exposure at the animal-human interface, a systematic review. PLoS One 6:e14582. http://dx.doi.org/10.1371/journal.pone.0014582.
7. Rabinowitz P, Perdue M, Mumford E. 2010. Contact variables for exposure to avian influenza H5N1 virus at the human-animal interface. Zoonoses Public Health 57:227-238. http://dx.doi.org/10.1111/j.1863-2378.2008.01223.x.
8. WHO. 2015. Cumulative number of confirmed human cases of avian influenza A/(H5N1) reported to WHO, 2003-2015. http://www.who.int/influenza/human_animal_interface/EN_GIP_20150623cumulative NumberH5N1cases.pdf?ua=1. Accessed 13 July 2015.
9. Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P. 2005. Influenza A H5N1 replication sites in humans. Emerg Infect Dis 11:1036-1041. http://dx.doi.org/10.3201/eid1107.041313.
10. Shinde V, Hanshaoworakul W, Simmerman JM, Narueponjirakul U, Sanasuttipun W, Kaewchana S, Areechokechai D, Ungchusak K, Fry AM. 2011. A comparison of clinical and epidemiological characteristics of fatal human infections with H5N1 and human influenza viruses in Thailand, 2004-2006. PLoS One 6:e14809. http://dx.doi.org/10.1371/journal.pone.0014809.
11. Puthavathana P, Sangsiriwut K, Korkusol A, Pooruk P, Auewarakul P, Pittayawanganon C, Sutdan D, Kitphati R, Sawanpanyalert P, Phommasack B, Bounlu K, Ungchusak K. 2009. Avian influenza virus (H5N1) in human, Laos. Emerg Infect Dis 15:127-129. http://dx.doi.org/10.3201/eid1501.080524.
12. Zhou JJ, Fang DY, Fu J, Tian J, Zhou JM, Yan HJ, Liang Y, Jiang LF. 2009. Infection and replication of avian influenza H5N1 virus in an infected human. Virus Genes 39:76-80. http://dx.doi.org/10.1007/s11262-009-0365-y.
13. Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, Shortridge KF, Cheung PT, To WK, Ho ET, Sung R, Cheng AF. 1998. Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351:467-471. http://dx.doi.org/10.1016/S0140-6736(98)01182-9.
14. Yu H, Gao Z, Feng Z, Shu Y, Xiang N, Zhou L, Huai Y, Feng L, Peng Li Z, Xu C, Li J, Hu C, Li Q, Xu X, Liu X, Liu Z, Xu L, Chen Y, Luo H, Wei L, Zhang X, Xin J, Guo J, Wang Q, Yuan Z, Zhou L, Zhang K, Zhang W, Yang J, Zhong X, Xia S, Li L, Cheng J, Ma E, He P, Lee SS, Wang Y, Uyeki TM, Yang W. 2008. Clinical characteristics of 26 human cases of highly pathogenic avian influenza A (H5N1) virus infection in China. PLoS One 3:e2985. http://dx.doi.org/10.1371/journal.pone.0002985.
15. Ku AS, Chan LT. 1999. The first case of H5N1 avian influenza infection in a human with complications of adult respiratory distress syndrome and Reye's syndrome. J Paediatr Child Health 35:207-209. http://dx.doi.org/10.1046/j.1440-1754.1999.t01-1-00329.x.
16. Zhang Z, Zhang J, Huang K, Li KS, Yuen KY, Guan Y, Chen H, Ng WF. 2009. Systemic infection of avian influenza A virus H5N1 subtype in humans. Hum Pathol 40:735-739. http://dx.doi.org/10.1016/j.humpath.2008.08.015.
17. To KF, Chan PK, Chan KF, Lee WK, Lam WY, Wong KF, Tang NL, Tsang DN, Sung RY, Buckley TA, Tam JS, Cheng AF. 2001. Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 63:242-246. http://dx.doi.org/10.1002/1096-9071(200103)63:3<242::AID-JMV1007>3.0.CO;2-N.
18. Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J, Hemphill M, Rowe T, Shaw M, Xu X, Fukuda K, Cox N. 1998. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393-396. http://dx.doi.org/10.1126/science.279.5349.393.
19. de Jong MD, Bach VC, Phan TQ, Vo MH, Tran TT, Nguyen BH, Beld M, Le TP, Truong HK, Nguyen VV, Tran TH, Do QH, Farrar J. 2005. Fatal avian influenza A (H5N1) in a child presenting with diarrhea followed by coma. N Engl J Med 352:686-691. http://dx.doi.org/10.1056/NEJMoa044307.
20. Sirinonthanawech N, Uiprasertkul M, Suptawiwat O, Auewarakul P. 2011. Viral load of the highly pathogenic avian influenza H5N1 virus in infected human tissues. J Med Virol 83:1418-1423. http://dx.doi.org/10.1002/jmv.22146.
21. Gao R, Dong L, Dong J, Wen L, Zhang Y, Yu H, Feng Z, Chen M, Tan Y, Mo Z, Liu H, Fan Y, Li K, Li CK, Li D, Yang W, Shu Y. 2010. A systematic molecular pathology study of a laboratory confirmed H5N1 human case. PLoS One 5:e13315. http://dx.doi.org/10.1371/journal.pone.0013315.
22. de Jong MD, Hien TT. 2006. Avian influenza A (H5N1). J Clin Virol 35:2-13. http://dx.doi.org/10.1016/j.jcv.2005.09.002.
23. Buchy P, Mardy S, Vong S, Toyoda T, Aubin JT, Miller M, Touch S, Sovann L, Dufourcq JB, Richner B, Tu PV, Tien NT, Lim W, Peiris JS, Van der Werf S. 2007. Influenza A/H5N1 virus infection in humans in Cambodia. J Clin Virol 39:164-168. http://dx.doi.org/10.1016/j.jcv.2007.04.010.
24. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJD, Chau TNB, Hoang DM, Van Vinh Chau N, Khanh TH, Dong VC, Qui PT, Van Cam B, Ha DQ, Guan Y, Peiris JSM, Chinh NT, Hien TT, Farrar J. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12:1203-1207. http://dx.doi.org/10.1038/nm1477.
25. Gu J, Xie Z, Gao Z, Liu J, Korteweg C, Ye J, Lau LT, Lu J, Gao Z, Zhang B, McNutt MA, Lu M, Anderson VM, Gong E, Yu AC, Lipkin WI. 2007. H5N1 infection of the respiratory tract and beyond: a molecular pathology study. Lancet 370:1137-1145. http://dx.doi.org/10.1016/S0140-6736(07)61515-3.
26. Liem NT, Tung CV, Hien ND, Hien TT, Chau NQ, Long HT, Hien NT, Mai Le, Taylor QWR, Wertheim H, Farrar J, Khang DD, Horby P. 2009. Clinical features of human influenza A (H5N1) infection in Vietnam: 2004-2006. Clin Infect Dis 48:1639-1646. http://dx.doi.org/10.1086/599031.
27. White NJ, Webster RG, Govorkova EA, Uyeki TM. 2009. What is the optimal therapy for patients with H5N1 influenza? PLoS Med 6:e1000091. http://dx.doi.org/10.1371/journal.pmed.1000091.
28. Schunemann H, Hill S, Kakad M, Bellamy R, Uyeki T, Hayden F, Yazdanpanah Y, Beigel J, Chotpitayasunondh T, Del Mar C, Farrar J, Hien T, Ozbay B, Sugaya N, Fukuda K, Shindo N, Stockman L, Vist G, Croisier A, Nagjdaliyev A, Roth C, Thomson G, Zucker H, Oxman A. 2007. WHO rapid advice guidelines for pharmacological management of sporadic human infection with avian influenza A (H5N1) virus. Lancet Infect Dis 7:21-31. http://dx.doi.org/10.1016/S1473-3099(06)70684-3.
29. Zitzow LA, Rowe T, Morken T, Shieh WJ, Zaki S, Katz JM. 2002. Pathogenesis of avian influenza A (H5N1) viruses in ferrets. J Virol 76: 4420-4429. http://dx.doi.org/10.1128/JVI.76.9.4420-4429.2002.
30. Govorkova EA, Rehg JE, Krauss S, Yen HL, Guan Y, Peiris M, Nguyen TD, Hanh TH, Puthavathana P, Long HT, Buranathai C, Lim W, Webster RG, Hoffmann E. 2005. Lethality to ferrets of H5N1 influenza viruses isolated from humans and poultry in 2004. J Virol 79:2191-2198. http://dx.doi.org/10.1128/JVI.79.4.2191-2198.2005.
31. Long J, Vela E, Stark G, Jones K, Miller S, Bigger J. 2012. Early indicators of disease in ferrets infected with a high dose of avian influenza H5N1. Sci Rep 2:972. http://dx.doi.org/10.1038/srep00972.
32. Abdel-Ghafar A-N, Chotpitayasunondh T, Gao Z, Hayden FG, Nguyen DH, de Jong MD, Naghdaliyev A, Peiris JSM, Shindo N, Soeroso S, Uyeki TM. 2008. Update on avian influenza A (H5N1) virus infection in humans. N Engl J Med 358:261-273. http://dx.doi.org/10.1056/NEJMra0707279.
33. Uyeki TM. 2009. Human infection with highly pathogenic avian influenza A (H5N1) virus: review of clinical issues. Clin Infect Dis 49:279-290. http://dx.doi.org/10.1086/600035.
34. Plourde JR, Pyles JA, Layton RC, Vaughan SE, Tipper JL, Harrod KS. 2012. Neurovirulence of H5N1 infection in ferrets is mediated by multifocal replication in distinct permissive neuronal cell regions. PLoS One 7:e46605. http://dx.doi.org/10.1371/journal.pone.0046605.
35. Peng BH, Yun N, Chumakova O, Zacks M, Campbell G, Smith J, Smith J, Linde S, Linde J, Paessler S. 2012. Neuropathology of H5N1 virus infection in ferrets. Vet Microbiol 156:294-304. http://dx.doi.org/10.1016/j.vetmic.2011.11.025.
36. Bodewes R, Kreijtz JH, van Amerongen G, Fouchier RA, Osterhaus AD, Rimmelzwaan GF, Kuiken T. 2011. Pathogenesis of influenza A/H5N1 virus infection in ferrets differs between intranasal and intratracheal routes of inoculation. Am J Pathol 179:30-36. http://dx.doi.org/10.1016/j.ajpath.2011.03.026.
37. Shinya K, Makino A, Hatta M, Watanabe S, Kim JH, Hatta Y, Gao P, Ozawa M, Le QM, Kawaoka Y. 2011. Subclinical brain injury caused by H5N1 influenza virus infection. J Virol 85:5202-5207. http://dx.doi.org/10.1128/JVI.00239-11.
38. Yamada M, Bingham J, Payne J, Rookes J, Lowther S, Haining J, Robinson R, Johnson D, Middleton D. 2012. Multiple routes of invasion of wild-type clade 1 highly pathogenic avian influenza H5N1 virus into the central nervous system (CNS) after intranasal exposure in ferrets. Acta Neuropathol 124:505-516. http://dx.doi.org/10.1007/s00401-012-1010-8.
39. Wang X, Zhao J, Tang S, Ye Z, Hewlett I. 2010. Viremia associated with fatal outcomes in ferrets infected with avian H5N1 influenza virus. PLoS One 5:e12099. http://dx.doi.org/10.1371/journal.pone.0012099.
40. Shinya K, Makino A, Tanaka H, Hatta M, Watanabe T, Le MQ, Imai H, Kawaoka Y. 2011. Systemic dissemination of H5N1 influenza A viruses in ferrets and hamsters after direct intragastric inoculation. J Virol 85:4673-4678. http://dx.doi.org/10.1128/JVI.00148-11.
41. Middleton D, Rockman S, Pearse M, Barr I, Lowther S, Klippel J, Ryan D, Brown L. 2009. Evaluation of vaccines for H5N1 influenza virus in ferrets reveals the potential for protective single-shot immunization. J Virol 83:7770-7778. http://dx.doi.org/10.1128/JVI.00241-09.
42. Gustin KM, Belser JA, Wadford DA, Pearce MB, Katz JM, Tumpey TM, Maines TR. 2011. Influenza virus aerosol exposure and analytical system for ferrets. Proc Natl Acad Sci U S A 108:8432-8437. http://dx.doi.org/10.1073/pnas.1100768108.
43. Lipatov AS, Kwon YK, Pantin-Jackwood MJ, Swayne DE. 2009. Pathogenesis of H5N1 influenza virus infections in mice and ferret models differs according to respiratory tract or digestive system exposure. J Infect Dis 199:717-725. http://dx.doi.org/10.1086/596740.
44. Moore IN, Lamirande EW, Paskel M, Donahue D, Qin J, Subbarao K. 2014. Severity of clinical disease and pathology in ferrets experimentally infected with influenza viruses is influenced by inoculum volume. J Virol 88:13879-13891. http://dx.doi.org/10.1128/JVI.02341-14.
45. WHO. 2011. WHO Global Influenza Surveillance Network: manual for the laboratory diagnosis and virological surveillance of influenza. WHO Press, Geneva, Switzerland. http://whqlibdoc.who.int/publications/2011/9789241548090_eng.pdf.
46. Reed L, Muench H. 1938. A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493-497.
47. Wibawa H, Bingham J, Nuradji H, Lowther S, Payne J, Harper J, Wong F, Lunt R, Junaidi A, Middleton D, Meers J. 2013. The pathobiology of two Indonesian H5N1 avian influenza viruses representing different clade 2.1 sublineages in chickens and ducks. Comp Immunol Microbiol Infect Dis 36:175-191. http://dx.doi.org/10.1016/j.cimid.2012.12.001.
48. Tate MD, Ioannidis LJ, Croker B, Brown LE, Brooks AG, Reading PC. 2011. The role of neutrophils during mild and severe influenza virus infections of mice. PLoS One 6:e17618. http://dx.doi.org/10.1371/journal.pone.0017618.
49. Schrauwen EJ, Herfst S, Leijten LM, van Run P, Bestebroer TM, Linster M, Bodewes R, Kreijtz JH, Rimmelzwaan GF, Osterhaus AD, Fouchier RA, Kuiken T, van Riel D. 2012. The multibasic cleavage site in H5N1 virus is critical for systemic spread along the olfactory and hematogenous routes in ferrets. J Virol 86:3975-3984. http://dx.doi.org/10.1128/JVI.06828-11.
50. Vong S, Ly S, Van Kerkhove MD, Achenbach J, Holl D, Buchy P, Sorn S, Seng H, Uyeki TM, Sok T, Katz JM. 2009. Risk factors associated with subclinical human infection with avian influenza A (H5N1) virus-Cambodia, 2006. J Infect Dis 199:1744-1752. http://dx.doi.org/10.1086/599208.
51. van den Brand JMA, Stittelaar KJ, van Amerongen G, Reperant L, de Waal L, Osterhaus ADME, Kuiken T. 2012. Comparison of temporal and spatial dynamics of seasonal H3N2, pandemic H1N1 and highly pathogenic avian influenza H5N1 virus infections in ferrets. PLoS One 7:e42343. http://dx.doi.org/10.1371/journal.pone.0042343.
52. Krammer F, Hai R, Yondola M, Tan GS, Leyva-Grado VH, Ryder AB, Miller MS, Rose JK, Palese P, García-Sastre A, Albrecht RA. 2014. Assessment of influenza virus hemagglutinin stalk-based immunity in ferrets. J Virol 88:3432-3442. http://dx.doi.org/10.1128/JVI.03004-13.
53. Chutinimitkul S, Bhattarakosol P, Srisuratanon S, Eiamudomkan A, Kongsomboon K, Damrongwatanapokin S, Chaisingh A, Suwannakarn K, Chieochansin T, Theamboonlers A, Poovorawan Y. 2006. H5N1 influenza A virus and infected human plasma. Emerg Infect Dis 12:1041-1043. http://dx.doi.org/10.3201/eid1206.060227.
54. England R, Homer J, Knight L, Ell S. 1999. Nasal pH measurement: a reliable and repeatable parameter. Clin Otolaryngol 24:67-68. http://dx.doi.org/10.1046/j.1365-2273.1999.00223.x.
55. Linster M, van Boheemen S, de Graaf M, Schrauwen EJA, Lexmond P, Mänz B, Bestebroer TM, Baumann J, van Riel D, Rimmelzwaan GF, Osterhaus ADME, Matrosovich M, Fouchier RAM, Herfst S. 2014. Identification, characterization, and natural selection of mutations driving airborne transmission of A/H5N1 virus. Cell 157:329-339. http://dx.doi.org/10.1016/j.cell.2014.02.040.
56. Watanabe Y, Arai Y, Daidoji T, Kawashita N, Ibrahim MS, El-Gendy Eel D, Hiramatsu H, Kubota-Koketsu R, Takagi T, Murata T, Takahashi K, Okuno Y, Nakaya T, Suzuki Y, Ikuta K. 2015. Characterization of H5N1 influenza virus variants with hemagglutinin mutations isolated from patients. mBio 6(2):e00081-15. http://dx.doi.org/10.1128/mBio.00081-15.