Exhaled aerosol transmission of pandemic and seasonal H1N1 influenza viruses in the ferret

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Koster, Frederick ^a   Gouveia, Kristine ^a   Zhou, Yue ^a   Lowery, Kristin ^b   Russell, Robert ^a   MacInnes, Heather ^a   Pollock, Zemmie ^a   Layton, R Colby ^a   Cromwell, Jennifer ^b   Toleno, Denise ^b   Pyle, John ^a   Zubelewicz, Michael ^a   Harrod, Kevin ^a   Sampath, Rangarajan ^b   Hofstadler, Steven ^b   Gao, Peng ^a   Liu, Yushi ^a   Cheng, Yung Sung ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b Analytical Services Laboratory   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; VIRUS RNA;

2009 H1N1 INFLUENZA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXPIRED AIR; FERRET; INFECTION SENSITIVITY; INFLUENZA VIRUS A H1N1; MALE; MUCOSA INFLAMMATION; NONHUMAN; PARTICLE SIZE; QUANTITATIVE ANALYSIS; SEASONAL INFLUENZA; SECONDARY ORGANIC AEROSOL; VIRUS STRAIN; VIRUS TRANSMISSION; WEIGHT REDUCTION; AEROSOL; ANIMAL; DISEASE TRANSMISSION; EXHALATION; HUMAN; LUNG; METABOLISM; NEBULIZER; ORTHOMYXOVIRUS INFECTION; PANDEMIC; PATHOGENICITY; PHYSIOLOGY; SEASON; SPECIES DIFFERENCE; TIME; VIROLOGY; VIRUS LOAD;

ANIMALIA; MUSTELA; ORTHOMYXOVIRIDAE;

AEROSOLS; ANIMALS; EXHALATION; FERRETS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; LUNG; MALE; NEBULIZERS AND VAPORIZERS; ORTHOMYXOVIRIDAE INFECTIONS; PANDEMICS; RNA, VIRAL; SEASONS; SPECIES SPECIFICITY; TIME FACTORS; VIRAL LOAD;

EID: 84859259700     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033118     Document Type: Article

References (54)

1. Thompson MG, Shay DK, Zhou H, Bridges CB, Cheng PY, et al. (2010) Updated estimates of mortality associated with seasonal influenza through the 2006-2007 influenza season. MMWR 59: 1057-1062.
2. Bautista E, Chotpitayasunondh T, Gao Z, Harper SA, Shaw M, et al. (2010) Clinical Aspects of pandemic 2009 influenza A (H1N1) virus infection. N Engl J Med 362: 1708-1717.
3. Taubenberger JK, (2006) The origin and virulence of the 1918 "Spanish" influenza virus. Proc Am Philos Soc 150: 86-112.
4. Webster RG, Govorkova EA, (2006) H5N1 influenza - Continuing evolution and spread. New Engl J Med 355: 2174-2177.
5. Goldfrank L, Liverman C, (2007) Preparing for an influenza pandemic: Personal protective equipment for healthcare Workers. The National Academies Press. Washington, D.
6. Vukotich CJ Jr, Coulborn RM, Aragon TJ, Baker MG, Burrus BB, et al. (2010) Findings, gaps, and future direction for research in nonpharmaceutical interventions for pandemic influenza. Emerg Infect Dis 16:e2.www.cdc.gov/EID/content/16/4/e2.htm.
7. Edwards DA, Man JC, Brand P, Katstra JP, Sommerer K, et al. (2004) Inhaling to mitigate exhaled bioaerosols. Proc Nat Acad Sci U S A 101: 17383-17388.
8. Roy CJ, Milton DK, (2004) Airborne transmission of communicable infection - the elusive pathway. New Engl J Med 350: 1710-1711.
9. Brankston G, Gitterman L, Hirji Z, Lemieux C, Gardam M, (2007) Transmission of influenza A in human beings. Lancet Infectious Disease 7: 257-265.
10. Lemieux C, Brankston G, Gitterman L, Hirji Z, Gardam M, (2007) Questioning aerosol transmission of influenza. Emerging Infect Dis 13: 173-174.
11. Tellier R, (2006) Review of aerosol transmission of influenza A virus. Emerging Infect Dis 12: 1657-1662.
12. Tellier R, (2009) Aerosol transmission of influenza A virus: a review of new studies. J Roy Soc Interface 6: S783-S790.
13. Fraser C, Donnelly CA, Cauchemez S, Hanage WP, Van Kerkhove MD, et al. (2009) Pandemic potential of a strain of influenza A (H1N1): Early Findings. Science 324: 1557-1561.
14. Yang Y, Sugimoto JD, Halloran ME, Basta NE, Chao DL, et al. (2009) The transmissibility and control of pandemic influenza A (H1N1) virus. Science 326: 729-733.
15. White LF, Wallinga J, Finelli L, Reed C, Riley S, et al. (2009) Estimation of the reproductive number and the serial interval in early phase of the 2009 influenza A/H1N1 pandemic in the USA. Influenza Other Resp Viruses 3: 267-276.
16. Balcan D, Hu H, Goncalves B, Bajardi P, Poletto C, et al. (2009) Seasonal transmission potential and activity peaks of the new influenza A (H1N1): a Monte Carlo likelihood analysis based on human mobility. BMC Med 10: 7-45.
17. Truscott J, Fraser C, Hinsley W, Cauchemez S, Donnelly C, et al. (2009) Quantifying the transmissibility of human influenza and its seasonal variation in temperate regions. PLoS Currents 2: RRN1125.
18. White LF, Pagano M, (2008) Transmissibility of the influenza virus in the 1918 pandemic. PLoS ONE 3: e1498.
19. Greenbaum JA, Kotturi MF, Kim Y, Oseroff C, Vaughan K, et al. (2009) Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci U S A 106: 20365-20370.
20. Belser JA, Maines TR, Tumpey TM, Katz JM, (2010) Influenza A virus transmission: contributing factors and clinical implications. Expert Rev Mol Med 12: e39.
21. Herlocher ML, Elias S, Truscon R, Harrison S, Mindell D, et al. (2001) Ferrets as a transmission model for influenza: sequence changes in HA1 of type A (H3N2) virus. J Infect Dis 184: 542-546.
22. Whitley RJ, (2010) Of ferrets and humans: influenza pathogenesis. J Infect Dis 201: 976-977.
23. Yen H-L, Herlocher LM, Hoffmann E, Mastrosovich MN, Monto AS, et al. (2005) Neuraminidase inhibitor-resistant influenza viruses may differ substantially in fitness and transmissibility. Antimicrob Agents Chemother 49: 4075-4084.
24. Steel J, Lowen AC, Mubareka S, Palese P, (2009) Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathog 5: e1000252.
25. Van Hoeven N, Pappas C, Belser JA, Maines TR, Zeng H, et al. (2009) Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc Nat Acad Sci USA 106: 3366-3371.
26. Sorrell EM, Wan H, Araya Y, Song H, Perez DR, (2009) Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Nat Acad Sci USA 106: 7565-7570.
27. Herfst S, Chutinimitkul S, Ye J, de Wit E, Munster VJ, et al. (2010) Introduction of virulence markers in PB2 of pandemic swine-origin influenza virus does not result in enhanced virulence or transmission. J Virol 84: 3752-3758.
28. Maines T, Chen L-M, Matsuoka Y, Chen H, Rowe T, et al. (2006) Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103: 12121-12126.
29. Maines TR, Jayaraman A, Belser JA, Wadford DA, Pappas C, et al. (2009) Transmission and pathogenesis of swine-origin 2009 A (H1N1) influenza viruses in ferrets and mice. Science 325: 484-487.
30. Munster VJ, de Wit E, van den Brand JM, Herfst S, Schrauwen EJA, et al. (2009) Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 325: 481-483.
31. Gustin KM, Belser JA, Wadford DA, Pearce MB, Katz JM, et al. (2011) Influenza virus aerosol exposure and analytical system for ferrets. Proc Natl Acad Sci U S A 108: 8432-8437.
32. MacInnes H, Zhou Y, Gouveia K, Cromwell J, Lowery K, et al. (2011) Transmission of aerosolized seasonal H1N1 influenza A to ferrets. PLoS ONE 6: e24448.
33. Sampath R, Russell KL, Massire C, Eshoo MW, Harpin V, et al. (2007) Global Surveillance of Emerging Influenza Virus Genotypes by Mass Spectrometry. PLoS ONE; 2: e489.
34. Deyde VM, Sampath R, Garten RJ, Blair PJ, Myers CA, et al. (2010) Genomic signature-based identification of influenza A viruses using RT-PCR/electrospray ionization mass spectrometry (ESI-MS) technology. PLoS ONE 5: e13293.
35. Boyd RL, Mangos JA, (1981) Pulmonary mechanics of the normal ferret. J Appl Physiol Respirat Environ Exercise Physiol 50: 799-804.
36. Vinegar A, Sinnett EE, Kosch PC, (1982) Respiratory mechanics of a small carnivore: the ferret. J Appl Physiol Respirat Environ Exercise Physiol 52: 832-837.
37. Lednicky JA, Hamilton SB, Tuttle RS, Sosna WA, Daniels DE, et al. (2010) Ferrets develop fatal influenza after inhaling small particle aerosols of highly pathogenic avian influenza virus A/Vietnam/1203/2004 (H5N1). Virol J 7: 231.
38. Gubareva, LV, McCullers JA, Bethell RC, Webster RG, (1998) Characterization of influenza A/HongKong/156/97 (H5N1) virus in a mouse model and protective effect of zanamivir on H5N1 infection in mice. J Infect Dis 178: 1592-1596.
39. Lowen AC, Mubareka S, Tumpey TM, Garcia-Sastre A, Palese P, (2006) the guinea pig as a transmission model for human influenza viruses. Proc Nat Acad Sci U S A 103: 9988-9992.
40. Alford RH, Kasel JA, Gerone PJ, Knight V, (1966) Human influenza resulting from aerosol inhalation. Proc Soc Exp Biol Med 122: 800-804.
41. Couch RB, Cate TR, Douglas RG Jr, Gerone PJ, Knight V, (1966) Effect of route of inoculation on experimental respiratory viral disease in volunteers and evidence for airborne transmission. Bacteriol Rev 30: 517-529.
42. Tuttle RS, Sosna WA, Daniels DE, Hamilton SB, Lednicky JA, (2010) Design, assembly, and validation of a nose-only inhalation exposure system for studies of aerosolized viable influenza H5N1 virus in ferrets. Virol J 7: 135.
43. Cox CS, (1987) The Aerobiological Pathway of Microorganisms. Chichester John Wiley & Sons.
44. Lowen AC, Mubareka S, Steel J, Palese P, (2007) Influenza virus transmission is dependent on relative humidity and temperature. PLoS PATHOGENS 3: 1470-1476.
45. Steel J, Staeheli P, Mubareka S, Garcia-Sastre A, Palese P, et al. (2010) Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J Virol 84: 21-26.
46. Steel J, Palese P, Lowen AC, (2011) Transmission of a 2009 pandemic influenza virus shows a sensitivity to temperature and humidity similar to that of an H3N2 seasonal strain. J Virol 85: 1400-1402.
47. Lindsley WG, Blachere FM, Thewlis RE, Vishnu A, Davis KA, et al. (2010) Measurements of airborne influenza virus in aerosol particles from human coughs. PLoS ONE 5: e15100.
48. Fabian P, McDevitt JJ, Houseman EA, Milton DK, (2009) Airborne influenza virus detection with four aerosol samplers using molecular and infectivity assays: considerations for a new infectious virus aerosol sampler. Indoor Air 19: 433-441.
49. Fabian P, McDevitt JJ, DeHaan WH, Fung ROP, Cowling BJ, et al. (2008) Influenza virus in human exhaled breath: an observational study. PLoS ONE 3: e2691.
50. Wie Z, McEvoy M, Razinkov V, Polozova A, Li E, et al. (2007) Biophysical characterization of influenza virus subpopulations using field flow fractionation and multiangle light scattering: Correlation of particle counts, size distribution and infectivity. J Virol Meth 144: 122-132.
51. Ngunjiri JM, Sekellick MJ, Marcus PI, (2008) Clonogenic assay of type A influenza viruses reveals noninfectious cell-killing (apoptosis-inducing) particles. J Virol 82: 2673-2680.
52. Marcus PI, Ngunjiri JM, Sekellick MJ, (2009) Dynamics of biologically active subpopulations of influenza virus: Plaque-forming, non-infectious cell-killing, and defective-interfering particles. J Virol 83: 8122-8130.
53. Rowe T, Leon AJ, Crevar CJ, Carter DM, Xu L, et al. (2010) Modeling host responses in ferrets during A/California/07/2009 influenza infection. Virology 401: 257-265.
54. Mitchell H, Levin D, Forrest S, Beauchemin C, Tipper J, et al. (2011) Higher replication efficiency of 2009 (H1N1) pandemic influenza than those of seasonal and avian strains: kinetics from epithelial cell culture and computational modeling. J Virol 85: 1125-1135.