Pandemic Swine-Origin H1N1 Influenza A Virus Isolates Show Heterogeneous Virulence in Macaques
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The first influenza pandemic of the new millennium was caused by a newly emerged swine-origin influenza virus (SOIV) (H1N1). This new virus is characterized by a previously unknown constellation of gene segments derived from North American and Eurasian swine lineages and the absence of common markers predictive of human adaptation. Overall, human infections appeared to be mild, but an alarming number of young individuals presented with symptoms atypical for seasonal influenza. The new SOIV also showed a sustained human-to-human transmissibility and higher reproduction ratio than common seasonal viruses, altogether indicating a higher pathogenic potential for this newly emerged virus. To study the virulence of the SOIV, we used a recently established cynomolgus macaque model and compared parameters of clinical disease, virology, host responses, and pathology/histopathology with a current seasonal H1N1 virus. We here show that infection of macaques with two genetically similar but clinically distinct SOIV isolates from the early stage of the pandemic (A/Mexico/4108/2009 and A/Mexico/InDRE4487/2009) resulted in upper and lower respiratory tract infections and clinical disease ranging from mild to severe pneumonia that was clearly advanced over the mild infection caused by A/Kawasaki/UTK-4/2009, a current seasonal strain. Unexpectedly, we observed heterogeneity among the two SOIV isolates in virus replication, host transcriptional and cytokine responses, and disease progression, demonstrating a higher pathogenic potential for A/Mexico/InDRE4487/2009. Differences in virulence may explain more severe disease, as was seen with certain individuals infected with the emerged pandemic influenza virus. Thus, the nonhuman primate model closely mimics influenza in humans.
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In a macaque infection model, clinically distinct Mexican isolates of SOIV showed an increase in IL-6, TNF, and IL-1beta gene expression in the lungs and pronounced levels of IL-6 and MCP-1 in the plasma.
“In a macaque infection model, clinically distinct Mexican isolates of SOIV showed an increase in IL-6, TNF, and IL-1 gene expression in the lungs and pronounced levels of IL-6 and MCP-1 in the plasma (123).”
From Into the Eye of the Cytokine Storm (2012) · cites this paper as [123]
Cites
Emergence of a Novel Swine-Origin Influenza A (H1N1) Virus in Humans
Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0903810 · Cited by 3,047 · see citing works
Garten, R. J., Davis, C. T., Russell, C. A., Shu, B., Lindstrom, S., Balish, A. L., Sessions, W. M., Xu, X., Skepner, E., Deyde, V., et al. (2009) · Science · doi:10.1126/science.1176225 · Cited by 2,499 · see citing works
Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic
Smith, G. J. D., Vijaykrishna, D., Bahl, J., Lycett, S., Worobey, M., Pybus, O. G., Ma, S. K., Cheung, C. L., Raghwani, J., Bhatt, S., et al. (2009) · Nature · doi:10.1038/nature08182 · Cited by 2,250 · see citing works
Pandemic Potential of a Strain of Influenza A (H1N1): Early Findings
Fraser, C., Donnelly, C. A., Cauchemez, S., Hanage, W. P., Kerkhove, M. D. V., Hollingsworth, T. D., Griffin, J. T., Baggaley, R. F., Jenkins, H. E., Lyons, E., et al. (2009) · Science · doi:10.1126/science.1176062 · Cited by 1,909 · see citing works
Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia.
de Jong, M. D., Simmons, C. P., Thanh, T. T., Hien, V. M., Smith, G. J. D., Chau, T. N. B., Hoang, D. M., Van Vinh Chau, N., Khanh, T. H., Dong, V. C., et al. (2006) · Nature Medicine · doi:10.1038/nm1477 · Cited by 1,858 · see citing works
Emergence and pandemic potential of swine-origin H1N1 influenza virus
Neumann, G., Noda, T., & Kawaoka, Y. (2009) · Nature · doi:10.1038/nature08157 · Cited by 1,562 · see citing works
Self-citationMolecular Basis for High Virulence of Hong Kong H5N1 Influenza A Viruses
Hatta, M., Gao, P., Halfmann, P., & Kawaoka, Y. (2001) · Science · doi:10.1126/science.1062882 · Cited by 1,336 · see citing works
Self-citationPneumonia and Respiratory Failure from Swine-Origin Influenza A (H1N1) in Mexico
Perez-Padilla, R., de la Rosa-Zamboni, D., Ponce de Leon, S., Hernandez, M., Quiñones-Falconi, F., Bautista, E., Ramirez-Venegas, A., Rojas-Serrano, J., Ormsby, C. E., Corrales, A., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0904252 · Cited by 1,325 · see citing works
The Pathology of Influenza Virus Infections
Taubenberger, J. K., & Morens, D. M. (2008) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev.pathmechdis.3.121806.154316 · Cited by 1,111 · see citing works
Self-citationIn vitro and in vivo characterization of new swine-origin H1N1 influenza viruses
Itoh, Y., Shinya, K., Kiso, M., Watanabe, T., Sakoda, Y., Hatta, M., Muramoto, Y., Tamura, D., Sakai‐Tagawa, Y., Noda, T., et al. (2009) · Nature · doi:10.1038/nature08260 · Cited by 1,058 · see citing works
Self-citationAberrant innate immune response in lethal infection of macaques with the 1918 influenza virus.
Kobasa, D., Jones, S. M., Shinya, K., Kash, J. C., Copps, J., Ebihara, H., Hatta, Y., Hyun Kim, J., Halfmann, P., Hatta, M., et al. (2007) · Nature · doi:10.1038/nature05495 · Cited by 934 · see citing works
Self-citationSwine influenza A (H1N1) infection in two children--Southern California, March-April 2009.
Ginsberg, M. M., Hopkins, J., Maroufi, A., Dunne, G., Sunega, D. R., Giessick, J., McVay, P., Lopez, K., Kriner, P., Munday, S. W., et al. (2009) · PubMed · Cited by 840 · see citing works
Severe Respiratory Disease Concurrent with the Circulation of H1N1 Influenza
Chowell, G., Bertozzi, S., Colchero, M. A., López‐Gatell, H., Alpuche-Aranda, C. M., Hernández, M., & Miller, M. A. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0904023 · Cited by 685 · see citing works
Hayden, F. G., Fritz, R., Lobo, M. C., Alvord, W. G., Strober, W., & Straus, S. E. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1355 · Cited by 680 · see citing works
Transmission and Pathogenesis of Swine-Origin 2009 A(H1N1) Influenza Viruses in Ferrets and Mice
Maines, T. R., Jayaraman, A., Belser, J. A., Wadford, D. A., Pappas, C., Zeng, H., Gustin, K. M., Pearce, M. B., Viswanathan, K., Shriver, Z. H., et al. (2009) · Science · doi:10.1126/science.1177238 · Cited by 653 · see citing works
Lethal H5N1 influenza viruses escape host anti-viral cytokine responses
Seo, S. H., Hoffmann, E., & Webster, R. G. (2002) · Nature Medicine · doi:10.1038/nm757 · Cited by 652 · see citing works
Pathogenesis and Transmission of Swine-Origin 2009 A(H1N1) Influenza Virus in Ferrets
Munster, V. J., de Wit, E., van den Brand, J. M. A., Herfst, S., Schrauwen, E. J. A., Bestebroer, T. M., van de Vijver, D. A. M. C., Boucher, C. A., Koopmans, M., Rimmelzwaan, G. F., et al. (2009) · Science · doi:10.1126/science.1177127 · Cited by 599 · see citing works
Swine influenza A (H1N1) infection in two children--Southern California, March-April 2009.
(2009) · PubMed · Cited by 571 · see citing works
Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus
Kobasa, D., Takada, A., Shinya, K., Hatta, M., Halfmann, P., Theriault, S., Suzuki, H., Nishimura, H., Mitamura, K., Sugaya, N., et al. (2004) · Nature · doi:10.1038/nature02951 · Cited by 455 · see citing works
Self-citationPulmonary Pathologic Findings of Fatal 2009 Pandemic Influenza A/H1N1 Viral Infections
Gill, J. R., Sheng, Z.-M., Ely, S. F., Guinee, D. G., Beasley, M. B., Suh, J., Deshpande, C., Mollura, D. J., Morens, D. M., Bray, M., et al. (2010) · Archives of Pathology & Laboratory Medicine · doi:10.5858/134.2.235 · Cited by 426 · see citing works
Self-citationAdaptive strategies of the influenza virus polymerase for replication in humans
Mehle, A., & Doudna, J. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911915106 · Cited by 383 · see citing works
Baskin, C. R., Bielefeldt-Ohmann, H., Tumpey, T. M., Sabourin, P. J., Long, J. P., García-Sastre, A., Tolnay, A.-E., Albrecht, R., Pyles, J. A., Olson, P. H., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0813234106 · Cited by 361 · see citing works
Self-citationPathology of human influenza revisited
Kuiken, T., & Taubenberger, J. K. (2008) · Vaccine · doi:10.1016/j.vaccine.2008.07.025 · Cited by 359 · see citing works
Self-citationSalomon, R., Franks, J., Govorkova, E. A., Ilyushina, N. A., Yen, H.-L., Hulse-Post, D. J., Humberd, J., Trichet, M., Rehg, J. E., Webby, R. J., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20051938 · Cited by 348 · see citing works
Host Range Restriction and Pathogenicity in the Context of Influenza Pandemic
Neumann, G., & Kawaoka, Y. (2006) · Emerging infectious diseases · doi:10.3201/eid1206.051336 · Cited by 290 · see citing works
Self-citationPathogenesis of Influenza A (H5N1) Virus Infection in a Primate Model
Rimmelzwaan, G. F., Kuiken, T., van Amerongen, G., Bestebroer, T. M., Fouchier, R. A. M., & Osterhaus, A. D. M. E. (2001) · Journal of Virology · doi:10.1128/jvi.75.14.6687-6691.2001 · Cited by 248 · see citing works
Cillóniz, C., Shinya, K., Peng, X., Korth, M. J., Proll, S. C., Aicher, L. D., Carter, V. S., Chang, J. H., Kobasa, D., Feldmann, F., et al. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000604 · Cited by 210 · see citing works
Self-citationAnimal models for the study of influenza pathogenesis and therapy
Barnard, D. L. (2009) · Antiviral Research · doi:10.1016/j.antiviral.2008.12.014 · Cited by 178 · see citing works
Skoner, D. P., Gentile, D. A., Patel, A. V., & Doyle, W. J. (1999) · The Journal of Infectious Diseases · doi:10.1086/314823 · Cited by 152 · see citing works
Pappas, C., Aguilar, P. V., Basler, C. F., Solórzano, A., Zeng, H., Perrone, L. A., Palese, P., García‐Sastre, A., Katz, J. M., & Tumpey, T. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0711815105 · Cited by 151 · see citing works
Structure-based discovery of dengue virus protease inhibitors
Tomlinson, S. M., Malmstrom, R. D., Russo, A. T., Mueller, N. H., Pang, Y., & Watowich, S. J. (2009) · Antiviral Research · doi:10.1016/j.antiviral.2009.02.190 · Cited by 131 · see citing works
Baas, T., Baskin, C. R., Diamond, D. L., García-Sastre, A., Bielefeldt-Ohmann, H., Tumpey, T. M., Thomas, M. J., Carter, V. S., Teal, T. H., Van Hoeven, N., et al. (2006) · Journal of Virology · doi:10.1128/jvi.00851-06 · Cited by 121 · see citing works
Self-citationSevere seasonal influenza in ferrets correlates with reduced interferon and increased IL-6 induction
Svitek, N., Rudd, P. A., Obojes, K., Pillet, S., & von Messling, V. (2008) · Virology · doi:10.1016/j.virol.2008.02.035 · Cited by 113 · see citing works
Baskin, C. R., Bielefeldt‐Ohmann, H., García‐Sastre, A., Tumpey, T. M., Hoeven, N. V., Carter, V. S., Thomas, M. J., Proll, S. C., Solórzano, A., Billharz, R., et al. (2007) · Journal of Virology · doi:10.1128/jvi.00590-07 · Cited by 81 · see citing works
Self-citationNakajima, N., Hata, S., Sato, Y., Tobiume, M., Katano, H., Kaneko, K., Nagata, N., Kataoka, M., Ainai, A., Hasegawa, H., et al. (2010) · Japanese Journal of Infectious Diseases · doi:10.7883/yoken.63.67 · Cited by 72 · see citing works
Hartley, C. A., Reading, P. C., Ward, A. C., & Anders, E. M. (1997) · Archives of Virology · doi:10.1007/s007050050060 · Cited by 66 · see citing works
Rockx, B., Sheahan, T. P., Donaldson, E., Harkema, J. R., Sims, A. M., Heise, M. T., Pickles, R. J., Cameron, M. J., Kelvin, D. J., & Baric, R. S. (2007) · Journal of Virology · doi:10.1128/jvi.00505-07 · Cited by 63 · see citing works
Self-citationKobinger, G. P., Meunier, I., Patel, A. R., Pillet, S., Gren, J., Stebner, S., Leung, A., Neufeld, J., Kobasa, D., & von Messling, V. (2010) · The Journal of Infectious Diseases · doi:10.1086/651171 · Cited by 63 · see citing works
Self-citationPandemic 2009 H1N1 Influenza Virus Causes Diffuse Alveolar Damage in Cynomolgus Macaques
Herfst, S., van den Brand, J. M. A., Schrauwen, E. J. A., de Wit, E., Munster, V. J., van Amerongen, G., Linster, M., Zaaraoui‐Boutahar, F., van IJcken, W. F. J., Rimmelzwaan, G. F., et al. (2010) · Veterinary Pathology · doi:10.1177/0300985810374836 · Cited by 37 · see citing works
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Impagliazzo, A., Milder, F. J., Kuipers, H., Wagner, M. V., Zhu, X., Hoffman, R. M. B., van Meersbergen, R., Huizingh, J., Wanningen, P., Verspuij, J. W. A., et al. (2015) · Science · doi:10.1126/science.aac7263 · Cited by 591 · see citing works
van Doremalen, N., Bushmaker, T., & Munster, V. J. (2013) · Eurosurveillance · doi:10.2807/1560-7917.es2013.18.38.20590 · Cited by 580 · see citing works
A Role for Neutrophils in Viral Respiratory Disease
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Kash, J. C., Walters, K.-A., Davis, A. S., Sandouk, A., Schwartzman, L. M., Jagger, B. W., Chertow, D. S., Qi, L., Kuestner, R. E., Ozinsky, A., et al. (2011) · mBio · doi:10.1128/mbio.00172-11 · Cited by 143 · see citing works
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Shinya, K., Gao, Y., Cillóniz, C., Suzuki, Y., Fujie, M., Deng, G., Zhu, Q., Fan, S., Makino, A., Muramoto, Y., et al. (2012) · Journal of Virology · doi:10.1128/jvi.00365-12 · Cited by 98 · see citing works
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Self-citationMa, W., Belisle, S. E., Mosier, D. A., Li, X., Stigger-Rosser, E., Liu, Q., Qiao, C., Elder, J., Webby, R. J., Katze, M. G., et al. (2011) · Journal of Virology · doi:10.1128/jvi.05705-11 · Cited by 67 · see citing works
Self-citationJosset, L., Engelmann, F., Haberthur, K., Kelly, S. M., Park, B. S., Kawoaka, Y., García‐Sastre, A., Katze, M. G., & Messaoudi, I. (2012) · Journal of Virology · doi:10.1128/jvi.01571-12 · Cited by 66 · see citing works
Self-citationMitchell, H. D., Eisfeld, A. J., Stratton, K. G., Heller, N. C., Bramer, L., Wen, J., McDermott, J., Gralinski, L. E., Sims, A. M., Le, M. Q., et al. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00200 · Cited by 65 · see citing works
Self-citationOtte, A., Sauter, M., Alleva, L. M., Baumgarte, S., Klingel, K., & Gabriel, G. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.03.041 · Cited by 64 · see citing works
Josset, L., Belser, J. A., Pantin‐Jackwood, M. J., Chang, J. H., Chang, S. T., Belisle, S. E., Tumpey, T. M., & Katze, M. G. (2012) · Journal of Virology · doi:10.1128/jvi.00563-12 · Cited by 58 · see citing works
Self-citationMuramoto, Y., Shoemaker, J. E., Le, M. Q., Itoh, Y., Tamura, D., Sakai‐Tagawa, Y., Imai, H., Uraki, R., Takano, R., Kawakami, E., et al. (2014) · Journal of Virology · doi:10.1128/jvi.00907-14 · Cited by 53 · see citing works
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Self-citationTisoncik-Go, J., Belisle, S. E., Tchitchek, N., Tumpey, T. M., Ma, W., Richt, J. A., Safronetz, D., Feldmann, H., & Katze, M. G. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-627 · Cited by 48 · see citing works
Self-citationHiguera-Iglesias, A. L., Kudo, K., Manabe, T., Corcho-Berdugo, A., Baeza, A. C., Ramos, L. A., Gutiérrez, R. G., Zavala, M. E. M., Takasaki, J., Izumi, S., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021838 · Cited by 47 · see citing works
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Xu, L., Bao, L., Zhou, J., Wang, D., Deng, W., Lv, Q., Ma, Y., Li, F., Sun, H., Zhan, L., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020698 · Cited by 36 · see citing works
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Self-citationOtte, A., Sauter, M., Daxer, M. A., McHardy, A. C., Klingel, K., & Gabriel, G. (2015) · Journal of Virology · doi:10.1128/jvi.00665-15 · Cited by 24 · see citing works
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Griffin, E. F., & Tompkins, S. M. (2023) · Viruses · doi:10.3390/v15091959 · Cited by 24 · see citing works
Insight into structural diversity of influenza virus haemagglutinin
Cho, K. J., Lee, J., Hong, K. W., Kim, S.-H., Park, Y., Lee, J. Y., Kang, S., Kim, S., Yang, J. H., Kim, E.-K., et al. (2013) · Journal of General Virology · doi:10.1099/vir.0.051136-0 · Cited by 24 · see citing works
de Wit, E., Rasmussen, A. L., Feldmann, F., Bushmaker, T., Martellaro, C., Haddock, E., Okumura, A., Proll, S. C., Chang, J., Gardner, D., et al. (2014) · mBio · doi:10.1128/mbio.01331-14 · Cited by 23 · see citing works
Self-citationShoemaker, J. E., Fukuyama, S., Eisfeld, A. J., Muramoto, Y., Watanabe, S., Watanabe, T., Matsuoka, Y., Kitano, H., & Kawaoka, Y. (2012) · BMC Systems Biology · doi:10.1186/1752-0509-6-117 · Cited by 22 · see citing works
Self-citationArikata, M., Itoh, Y., Okamatsu, M., Maeda, T., Shiina, T., Tanaka, K., Suzuki, S., Nakayama, M., Sakoda, Y., Ishigaki, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037220 · Cited by 23 · see citing works
Olsen, R. J., Fittipaldi, N., Kachroo, P., Sanson, M. A., Long, S. W., Como-Sabetti, K. J., Valson, C., Cantu, C. C., Lynfield, R., Beneden, C. V., et al. (2014) · Journal of Clinical Microbiology · doi:10.1128/jcm.02164-14 · Cited by 22 · see citing works
Mooij, P., Grødeland, G., Koopman, G., Andersen, T. K., Mortier, D., Nieuwenhuis, I. G., Verschoor, E. J., Fagrouch, Z. C., Bogers, W. M. J. M., & Bogen, B. (2019) · Vaccine · doi:10.1016/j.vaccine.2018.12.049 · Cited by 22 · see citing works
Age-Related Pathology Associated with H1N1 A/California/07/2009 Influenza Virus Infection
Bissel, S. J., Carter, C. E., Wang, G., Johnson, S. K., Lashua, L. P., Kelvin, A. A., Wiley, C. A., Ghedin, E., & Ross, T. M. (2019) · American Journal Of Pathology · doi:10.1016/j.ajpath.2019.08.017 · Cited by 22 · see citing works
Camp, J. V., Chu, Y. K., Chung, D.-H., McAllister, R. C., Adcock, R. S., Gerlach, R. L., Wiemken, T. L., Peyrani, P., Ramírez, J. A., Summersgill, J. T., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056602 · Cited by 21 · see citing works
Iwatsuki‐Horimoto, K., Nakajima, N., Kiso, M., Takahashi, K., Ito, M., Inoue, T., Horiuchi, M., Okahara, N., Sasaki, E., Hasegawa, H., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00844 · Cited by 21 · see citing works
Self-citationOld World Monkeys and New Age Science: The Evolution of Nonhuman Primate Systems Virology
Palermo, R. E., Tisoncik-Go, J., Korth, M. J., & Katze, M. G. (2013) · ILAR Journal · doi:10.1093/ilar/ilt039 · Cited by 20 · see citing works
Self-citationRecently Emerged Swine Influenza A Virus (H2N3) Causes Severe Pneumonia in Cynomolgus Macaques
Richt, J. A., Rockx, B., Ma, W., Feldmann, F., Safronetz, D., Marzi, A., Kobasa, D., Strong, J. E., Kercher, L., Long, D., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039990 · Cited by 17 · see citing works
Self-citationEvaluation of Macaca radiata as a non-human primate model of Dengue virus infection
Kato, F., Ishida, Y., Kawakami, A., Takasaki, T., Saijo, M., Miura, T., & Hishiki, T. (2018) · Scientific Reports · doi:10.1038/s41598-018-21582-9 · Cited by 17 · see citing works
Watanabe, T., Imai, M., Watanabe, S., Shinya, K., Hatta, M., Li, C., Neumann, G., Ozawa, M., Hanson, A., Zhong, G., et al. (2012) · Journal of Virology · doi:10.1128/jvi.01214-12 · Cited by 16 · see citing works
Self-citation6th International Conference on Emerging Zoonoses
Kahn, R. E., Morozov, I., Feldmann, H., & Richt, J. A. (2012) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2012.01539.x · Cited by 16 · see citing works
Self-citationYang, P., Deng, J., Li, C., Zhang, P., Xing, L., Li, Z., Wang, W., Zhao, Y., Yan, Y., Gu, H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046184 · Cited by 16 · see citing works
Comparative Pathology of Animal Models for Influenza A Virus Infection
Kirk, N. M., Liang, Y., & Ly, H. (2023) · Pathogens · doi:10.3390/pathogens13010035 · Cited by 14 · see citing works
Antibody and inflammatory response‐mediated severity of pandemic 2009 (pH1N1) influenza virus
Tiwari, N., Kapoor, P., & Dhole, T. N. (2014) · Journal of Medical Virology · doi:10.1002/jmv.23877 · Cited by 15 · see citing works
Cytokine-Mediated Tissue Injury in Non-human Primate Models of Viral Infections
Manickam, C., Shah, S. V., Lucar, O. A., Ram, D. R., & Reeves, R. K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02862 · Cited by 15 · see citing works
Nieto, A., Pozo, F., Vidal‐García, M., Omeñaca, M., Casas, I., & Falcón, A. M. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00575 · Cited by 15 · see citing works
Boonnak, K., Paskel, M., Matsuoka, Y., Vogel, L., & Subbarao, K. (2012) · Vaccine · doi:10.1016/j.vaccine.2012.06.088 · Cited by 14 · see citing works
Ljungberg, K., McBrayer, A. C., Camp, J. V., Chu, Y.-K., Tapp, R. A., Noah, D. L., Grimes, S. D., Proctor, M., Liljeström, P., Jonsson, C. B., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040743 · Cited by 12 · see citing works
Małachowa, N., Freedman, B. A., Sturdevant, D. E., Kobayashi, S. D., Nair, V., Feldmann, F., Starr, T., Steele‐Mortimer, O., Kash, J. C., Taubenberger, J. K., et al. (2018) · mSphere · doi:10.1128/mspheredirect.00567-17 · Cited by 11 · see citing works
Self-citationFarrukee, R., Tai, C. M. K., Oh, D. Y., Anderson, D. E., Gunalan, V., Hibberd, M. L., Lau, G. Y.-F., Barr, I., von Messling, V., Maurer‐Stroh, S., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008592 · Cited by 12 · see citing works
Heterogeneous virulence of pandemic 2009 influenza H1N1 virus in mice
Farooqui, A., Leon, A. J., Lei, Y.-C., Wang, P., Huang, J., Tenorio, R., Dong, W., Rubino, S., Lin, J., Li, G., et al. (2012) · Virology Journal · doi:10.1186/1743-422x-9-104 · Cited by 12 · see citing works
Diseases of the Respiratory System
(2017) · Elsevier eBooks · doi:10.1016/b978-0-7020-5246-0.00012-7 · Cited by 12 · see citing works
Mansfield, K. G., Sasseville, V. G., & Westmoreland, S. V. (2013) · Veterinary Pathology · doi:10.1177/0300985813509386 · Cited by 11 · see citing works
Translational research on influenza virus infection using a nonhuman primate model
Itoh, Y. (2016) · Pathology International · doi:10.1111/pin.12385 · Cited by 11 · see citing works
Rivera, A., Barr, T., Rais, M., Engelmann, F., & Messaoudi, I. (2016) · Viral Immunology · doi:10.1089/vim.2015.0074 · Cited by 10 · see citing works
He, L., Wu, Q., Jiang, K., Duan, Z., Liu, J., Xu, H., Cui, Z., Gu, M., Wang, X., Liu, X., et al. (2014) · Archives of Virology · doi:10.1007/s00705-014-2009-3 · Cited by 8 · see citing works
Workshop report: Experimental animal models for universal influenza vaccines
D’Alessio, F., Koopman, G., Houard, S. A., Remarque, E. J., Stockhofe, N., & Engelhardt, O. G. (2018) · Vaccine · doi:10.1016/j.vaccine.2018.10.024 · Cited by 8 · see citing works
Broadbent, A., Santos, C. P., Paskel, M., Matsuoka, Y., Lu, J., Chen, Y., Jin, H., & Subbarao, K. (2014) · Vaccine · doi:10.1016/j.vaccine.2014.10.065 · Cited by 7 · see citing works
Jamshidnezhad, A., Hosseini, S. A., Marashic, S. M. H., Ghavamabadi, L. I., Mousavi, H., Zilae, M., & Dehaghi, B. F. (2021) · Work · doi:10.3233/wor-210463 · Cited by 7 · see citing works
Koopman, G., Mortier, D., Michels, S., Hofman, S., Fagrouch, Z. C., Remarque, E. J., Verschoor, E. J., Mooij, P., & Bogers, W. M. J. M. (2019) · Journal of General Virology · doi:10.1099/jgv.0.001251 · Cited by 6 · see citing works
Pathogenic analysis of the pandemic 2009 H1N1 influenza A viruses in ferrets
Tsuda, Y., Weisend, C. M., Martellaro, C., Feldmann, F., & Haddock, E. (2017) · Journal of Veterinary Medical Science · doi:10.1292/jvms.16-0619 · Cited by 5 · see citing works
Self-citation‘Omics Investigations of HIV and SIV Pathogenesis and Innate Immunity
Palermo, R. E., & FULLER, D. H. (2012) · Current topics in microbiology and immunology · doi:10.1007/82_2012_255 · Cited by 3 · see citing works
Self-citationMooij, P., Mortier, D., Stammes, M. A., Fagrouch, Z. C., Verschoor, E. J., Bogers, W. M. J. M., & Koopman, G. (2020) · Journal of General Virology · doi:10.1099/jgv.0.001489 · Cited by 3 · see citing works
Meunier, I., Morisseau, O., Garneau, É., Marois, I., Cloutier, A., & Richter, M. V. (2015) · PLoS ONE · doi:10.1371/journal.pone.0138055 · Cited by 2 · see citing works
Bovine Derived Clade 2.3.4.4b HPAI H5N1 Virus Causes Mild Disease and Limited Transmission in PigsPreprint
Feldmann, H., Rosenke, K., Bushmaker, T., Griffin, A., Okumura, A., Kaiser, F. K., Altynova, E. S., Yinda, C. K., Lewis, M. C., Leventhal, S. S., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-6567595/v1 · Cited by 2 · see citing works
Self-citationTranslational research on pandemic virus infection using nonhuman primate models
Ishigaki, H., & Itoh, Y. (2025) · Virology · doi:10.1016/j.virol.2025.110511 · Cited by 1 · see citing works
Maximova, V. A., Kirilov, K., Markov, S. S., & Ivanov, I. (2011) · Biotechnology & Biotechnological Equipment · doi:10.5504/bbeq.2011.0098 · Cited by 1 · see citing works
Virulence of the H1N1 2009 Pandemic Influenza Virus
Auewarakul, P. (2020) · DOAJ (DOAJ: Directory of Open Access Journals)
Cardeti, G., Cersini, A., Manna, G., Santis, P. D., Scicluna, M. T., Albani, A., Simula, M., Sittinieri, S., Santis, L. D., Liberato, C. D., et al. (2022) · BMC Veterinary Research · doi:10.1186/s12917-022-03506-y
Host Factor Experiment (IM009-R)
J. Craig Venter Institute, & University of Chicago (2012) · Influenza Research Database · doi:10.35094/w748-fz49
Host Factor Experiment (IM002-R)
J. Craig Venter Institute, & University of Chicago (2012) · Influenza Research Database · doi:10.35094/y02d-pt67
- Authors
- Safronetz, D., Rockx, B., Feldmann, F., Belisle, S. E., Palermo, R. E., Brining, D., Gardner, D., Proll, S. C., Marzi, A., Tsuda, Y., LaCasse, R. A., Kercher, L., York, A., Korth, M. J., Long, D., Rosenke, R., Shupert, W. L., Aranda, C. A., Mattoon, J. S., Kobasa, D., Kobinger, G., Li, Y., Taubenberger, J. K., Richt, J. A., Parnell, M., Ebihara, H., Kawaoka, Y., Katze, M. G., & Feldmann, H.
- Affiliations
- Laboratory of Virology (Hamilton, Montana)
- University of Washington (US)
- Rocky Mountain Veterinary Branch (Hamilton, Montana)
- Instituto de Diagnóstico y Referencia Epidemiológicos, Prolongación de Carpio No. 470, 3er Piso, Col. Santo Tomas, Delegación Muguel Hidalgo, Mexico City, CP 11340, Mexico
- Washington State University (US)
- Public Health Agency of Canada (CA)
- National Institutes of Health (US)
- Department of Diagnostic Medicine and Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, Kansas
- University of Wisconsin–Madison (US)
- ORCID
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2011-02
- Volume
- 85
- Issue
- 3
- Pages
- 1214-1223
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC3020514
- OpenAlex
- W2061904548
- Cited by
- 86
- References
- 39
- Citations by year
- 2025: 2 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 5 · 2019: 6 · 2018: 6 · 2017: 4 · 2016: 2 · 2015: 9 · 2014: 12 · 2013: 9 · 2012: 19
- FWCI
- 8.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Virology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
- Funders
- Division of Intramural Research, National Institute of Allergy and Infectious Diseases
- University of Washington
- Public Health Agency of Canada
- Public Health Agency
- National Institutes of Health (HHSN272200800060C, HHSN266200700010C, 8r24od011157-10)
- Japan Science and Technology Agency
- National Institute of Allergy and Infectious Diseases (HHSN266200700010C, HHSN272200800060C)
- National Center for Research Resources (R24RR016354, P51RR000166)
- Exploratory Research for Advanced Technology
- NHLBI Division of Intramural Research
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Keywords
- virulence, cynomolgus macaque model, nonhuman primate model, pneumonia, respiratory infections, host transcriptional response, cytokine response, viral replication, disease progression, histopathology
- MeSH terms
- Animals, Child, Preschool, Disease Models, Animal, Humans, Influenza, Human, Macaca, Male, Orthomyxoviridae Infections, Pneumonia, Viral, Respiratory Tract Infections, Severity of Illness Index, Genetic Variation, Virulence, Cytokines, Primate Diseases, Disease Progression, Gene Expression Profiling, Influenza A Virus, H1N1 Subtype
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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