Bacterial sinusitis and otitis media following influenza virus infection in ferrets
Abstract
Streptococcus pneumoniae is the leading cause of otitis media, sinusitis, and pneumonia. Many of these infections result from antecedent influenza virus infections. In this study we sought to determine whether the frequency and character of secondary pneumococcal infections differed depending on the strain of influenza virus that preceded bacterial challenge. In young ferrets infected with influenza virus and then challenged with pneumococcus, influenza viruses of any subtype increased bacterial colonization of the nasopharynx. Nine out of 10 ferrets infected with H3N2 subtype influenza A viruses developed either sinusitis or otitis media, while only 1 out of 11 ferrets infected with either an H1N1 influenza A virus or an influenza B virus did so. These data may partially explain why bacterial complication rates are higher during seasons when H3N2 viruses predominate. This animal model will be useful for further study of the mechanisms that underlie viral-bacterial synergism.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Animal models have confirmed that viral infection, particularly influenza, increases bacterial colonization rates in the URT, enhancing the risk of secondary bacterial infections.
“Animal models have similarly confirmed that viral infection, particularly influenza, increases bacterial colonization rates in the URT, enhancing the risk of secondary bacterial infections”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [99]
Cites
Principles and Practice of Infectious Diseases.
(1991) · Annals of Internal Medicine · doi:10.7326/0003-4819-114-9-818_5 · Cited by 12,045 · see citing works
Evolution and ecology of influenza A viruses
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., & Kawaoka, Y. (1992) · Microbiological Reviews · doi:10.1128/mr.56.1.152-179.1992 · Cited by 4,739 · see citing works
Mortality Associated With Influenza and Respiratory Syncytial Virus in the United States
Thompson, W. W., Shay, D. K., Weintraub, E., Brammer, L., Cox, N., Anderson, L. J., & Fukuda, K. (2003) · JAMA · doi:10.1001/jama.289.2.179 · Cited by 3,673 · see citing works
Efficacy, safety and immunogenicity of heptavalent pneumococcal conjugate vaccine in children
BLACK, S. B., Shinefield, H. R., FIREMAN, B. H., Lewis, E. M., Ray, P., Hansen, J. R., Elvin, L., ENSOR, K. M., Hackell, J. G., Siber, G. R., et al. (2000) · The Pediatric Infectious Disease Journal · doi:10.1097/00006454-200003000-00003 · Cited by 2,293 · see citing works
Efficacy of a Pneumococcal Conjugate Vaccine against Acute Otitis Media
Eskola, J., Kilpi, T. M., PALMU, A. A. I., Jokinen, J., Eerola, M., Haapakoski, J., Herva, E., Takala, A. K., Käyhty, H. M., Karma, P. H., et al. (2001) · New England Journal of Medicine · doi:10.1056/nejm200102083440602 · Cited by 1,454 · see citing works
A novel influenza A virus mitochondrial protein that induces cell death
Chen, W., Calvo, P. A., Malide, D. A., Gibbs, J. S., Schubert, U., Bačík, I., Basta, S., O’Neill, R. E., Schickli, J. H., Palese, P., et al. (2001) · Nature Medicine · doi:10.1038/nm1201-1306 · Cited by 1,037 · see citing works
Epidemiology and Clinical Characteristics of Community-Acquired Pneumonia in Hospitalized Children
Michelow, I. C., Olsen, K. D., Lozano, J., Rollins, N. K., Duffy, L. B., Ziegler, T. T., Kauppila, J., Leinonen, M., & McCracken, G. H. (2004) · PEDIATRICS · doi:10.1542/peds.113.4.701 · Cited by 709 · see citing works
Management of Community-Acquired Pneumonia in the Era of Pneumococcal Resistance
Heffelfinger, J. D. (2000) · Archives of Internal Medicine · doi:10.1001/archinte.160.10.1399 · Cited by 612 · see citing works
The impact of influenza epidemics on mortality: introducing a severity index.
Simonsen, L., Clarke, M. J., Williamson, G. D., Stroup, D. F., Arden, N. H., & Schonberger, L. B. (1997) · American Journal of Public Health · doi:10.2105/ajph.87.12.1944 · Cited by 587 · see citing works
A role for Streptococcus pneumoniae in virus-associated pneumonia
Madhi, S. A., Klugman, K. P., & The Vaccine Trialist Group (2004) · Nature Medicine · doi:10.1038/nm1077 · Cited by 565 · see citing works
Dowell, S. F., Butler, J. C., Giebink, G. S., Jacobs, M. R., Jernigan, D. B., Musher, D. M., Rakowsky, A., & Schwartz, B. (1999) · The Pediatric Infectious Disease Journal · doi:10.1097/00006454-199901000-00002 · Cited by 505 · see citing works
The Impact of Influenza Epidemics on Hospitalizations
Simonsen, L., Fukuda, K., Schonberger, L. B., & Cox, N. J. (2000) · The Journal of Infectious Diseases · doi:10.1086/315320 · Cited by 476 · see citing works
McCullers, J. A., & Rehg, J. E. (2002) · The Journal of Infectious Diseases · doi:10.1086/341462 · Cited by 423 · see citing works
Self-citationThe global impact of influenza on morbidity and mortality
Simonsen, L. (1999) · Vaccine · doi:10.1016/s0264-410x(99)00099-7 · Cited by 401 · see citing works
Role of Neuraminidase in Lethal Synergism between Influenza Virus and Streptococcus pneumoniae
McCullers, J. A., & Bartmess, K. C. (2003) · The Journal of Infectious Diseases · doi:10.1086/368163 · Cited by 384 · see citing works
Self-citationSinusitis of the Maxillary Antrum
Evans, F. O., Sydnor, J. B., Moore, W. E., Moore, G. R. W., Manwaring, J. L., Brill, A. H., Jackson, R. T., Hanna, S., Skaar, J. S., Holdeman, L. V., et al. (1975) · New England Journal of Medicine · doi:10.1056/nejm197510092931502 · Cited by 379 · see citing works
Klein, J. O. (2000) · Vaccine · doi:10.1016/s0264-410x(00)00271-1 · Cited by 312 · see citing works
Respiratory viruses predisposing to bacterial infections: role of neuraminidase.
PELTOLA, V. T., & MCCULLERS, J. A. (2004) · Pediatric Infectious Disease Journal · doi:10.1097/01.inf.0000108197.81270.35 · Cited by 290 · see citing works
Self-citationO’Brien, K. L., Walters, M. I., Sellman, J. S., Quinlisk, P., Regnery, H. L., Schwartz, B., & Dowell, S. F. (2000) · Clinical Infectious Diseases · doi:10.1086/313772 · Cited by 280 · see citing works
Influenza A and B Virus Infections in Children
Peltola, V. T., Ziegler, T. T., & Ruuskanen, O. (2003) · Clinical Infectious Diseases · doi:10.1086/345909 · Cited by 276 · see citing works
Self-citationBurden of Influenza in Children in the Community
Heikkinen, T., Silvennoinen, H., Peltola, V. T., Ziegler, T. T., Vainionpää, R., Vuorinen, T., Kainulainen, L., Puhakka, T., Jartti, T. T., Toikka, P., et al. (2004) · The Journal of Infectious Diseases · doi:10.1086/424527 · Cited by 272 · see citing works
Self-citationImportance of Respiratory Viruses in Acute Otitis Media
Heikkinen, T., & Chonmaitree, T. (2003) · Clinical Microbiology Reviews · doi:10.1128/cmr.16.2.230-241.2003 · Cited by 258 · see citing works
Epidemiological evidence of an early wave of the 1918 influenza pandemic in New York City
Olson, D. R., Simonsen, L., Edelson, P. J., & Morse, S. S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408290102 · Cited by 254 · see citing works
Francis, K. P., Yu, J., Bellinger-Kawahara, C., Joh, D., Hawkinson, M. J., Xiao, G., Purchio, T. F., Caparon, M. G., Lipsitch, M., & Contag, P. R. (2001) · Infection and Immunity · doi:10.1128/iai.69.5.3350-3358.2001 · Cited by 250 · see citing works
Etiology and Antimicrobial Therapy of Acute Maxillary Sinusitis
Hamory, B. H., Sande, M. A., Sydnor, A., Seale, D. L., & Gwaltney, J. M. (1979) · The Journal of Infectious Diseases · doi:10.1093/infdis/139.2.197 · Cited by 226 · see citing works
Gibbs, J. S., Malide, D. A., Hornung, F., Bennink, J. R., & Yewdell, J. W. (2003) · Journal of Virology · doi:10.1128/jvi.77.13.7214-7224.2003 · Cited by 224 · see citing works
Influenza virus neuraminidase contributes to secondary bacterial pneumonia.
Peltola, V. T., Murti, K. G., & McCullers, J. A. (2005) · The Journal of Infectious Diseases · doi:10.1086/430954 · Cited by 219 · see citing works
Self-citationThe 1918 Spanish influenza:integrating history and biology
Reid, A. H., Taubenberger, J. K., & Fanning, T. G. (2001) · Microbes and Infection · doi:10.1016/s1286-4579(00)01351-4 · Cited by 170 · see citing works
Effect of Antiviral Treatment on the Outcome of Secondary Bacterial Pneumonia after Influenza
McCullers, J. A. (2004) · The Journal of Infectious Diseases · doi:10.1086/421525 · Cited by 163 · see citing works
Self-citationOtitis Media: The Chinchilla Model1
Giebink, G. S. (1999) · Microbial Drug Resistance · doi:10.1089/mdr.1999.5.57 · Cited by 111 · see citing works
DIFFERING VIRULENCE OF H1N1 AND H3N2 INFLUENZA STRAINS
Wright, P. F., Thompson, J., & Karzon, D. T. (1980) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a113053 · Cited by 106 · see citing works
Community-acquired influenza C virus infection in children
Moriuchi, H., Katsushima, N., Nishimura, H., Nakamura, K., & Numazaki, Y. (1991) · The Journal of Pediatrics · doi:10.1016/s0022-3476(05)80489-5 · Cited by 62 · see citing works
Trends and Epidemics of Influenza and Pneumonia, 1918-1951
Collins, S. D., & Lehmann, J. (1951) · Public Health Reports (1896-1970) · doi:10.2307/4587915 · Cited by 54 · see citing works
Vaccines for otitis media: proposals for overcoming obstacles to progress
Murphy, T. F., Bakaletz, L. O., Kyd, J. M., Watson, B., & Klein, D. L. (2005) · Vaccine · doi:10.1016/j.vaccine.2004.12.014 · Cited by 34 · see citing works
Novotny, L. A., Mason, K. M., & Bakaletz, L. O. (2004) · Infection and Immunity · doi:10.1128/iai.73.1.609-611.2005 · Cited by 26 · see citing works
Coates, D. M., Sweet, C., & Smith, H. C. (1986) · Journal of General Virology · doi:10.1099/0022-1317-67-3-419 · Cited by 20 · see citing works
Collins, S. D. (1945) · Public Health Reports (1896-1970) · doi:10.2307/4585317 · Cited by 18 · see citing works
A ferret model of synergism between influenza virus and Streptococcus pneumoniae
Peltola, V. T., Rehg, J. E., & McCullers, J. A. (2004) · International Congress Series · doi:10.1016/j.ics.2004.02.023 · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Insights into the Interaction between Influenza Virus and Pneumococcus
McCullers, J. A. (2006) · Clinical Microbiology Reviews · doi:10.1128/cmr.00058-05 · Cited by 846 · see citing works
Self-citationThe fundamental link between pneumococcal carriage and disease
Simell, B., Auranen, K. J., Käyhty, H. M., Goldblatt, D., Dagan, R., O’Brien, K. L., & for the Pneumococcal Carriage Group (PneumoCarr) (2012) · Expert Review of Vaccines · doi:10.1586/erv.12.53 · Cited by 633 · see citing works
Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia.
Hanada, S., Pirzadeh, M., Carver, K. Y., & Deng, J. C. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02640 · Cited by 495 · see citing works
McAuley, J. L., Hornung, F., Boyd, K. L., Smith, A. M., McKeon, R., Bennink, J., Yewdell, J. W., & McCullers, J. A. (2007) · Cell Host & Microbe · doi:10.1016/j.chom.2007.09.001 · Cited by 389 · see citing works
Self-citationThe ferret as a model organism to study influenza A virus infection
Belser, J. A., Katz, J. M., & Tumpey, T. M. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.007823 · Cited by 364 · see citing works
Bacterial co‐infections with SARS‐CoV ‐2
Mirzaei, R., Goodarzi, P., Asadi, M., Soltani, A., Aljanabi, H. A. A., Jeda, A. S., Dashtbin, S., Jalalifar, S., Mohammadzadeh, R., Teimoori, A., et al. (2020) · IUBMB Life · doi:10.1002/iub.2356 · Cited by 292 · see citing works
McCullers, J. A., McAuley, J. L., Browall, S., Iverson, A. R., Boyd, K. L., & Henriques Normark, B. (2010) · The Journal of Infectious Diseases · doi:10.1086/656333 · Cited by 218 · see citing works
Self-citationViral–bacterial co-infections in the respiratory tract
Bakaletz, L. O. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2016.11.003 · Cited by 207 · see citing works
Kinetics of Coinfection with Influenza A Virus and Streptococcus pneumoniae
Smith, A. M., Adler, F. R., Ribeiro, R. M., Gutenkunst, R. N., McAuley, J., McCullers, J. A., & Perelson, A. S. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003238 · Cited by 195 · 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
Ferret models of viral pathogenesis
Enkirch, T., & von Messling, V. (2015) · Virology · doi:10.1016/j.virol.2015.03.017 · Cited by 156 · see citing works
The human microbiome and COVID-19: A systematic review
Yamamoto, S., Saito, M., Tamura, A., Prawisuda, D., Mizutani, T., & Yotsuyanagi, H. (2021) · PLoS ONE · doi:10.1371/journal.pone.0253293 · Cited by 146 · see citing works
Secondary Bacterial Infections in Influenza Virus Infection Pathogenesis
Smith, A. M., & McCullers, J. A. (2014) · Current topics in microbiology and immunology · doi:10.1007/82_2014_394 · Cited by 135 · see citing works
Self-citationOpatowski, L., Baguelin, M., & Eggo, R. M. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1006770 · Cited by 126 · see citing works
Complexities in Ferret Influenza Virus Pathogenesis and Transmission Models
Belser, J. A., Eckert, A. M., Tumpey, T. M., & Maines, T. R. (2016) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00022-16 · Cited by 113 · see citing works
Novel Strategy to Prevent Otitis Media Caused by Colonizing Streptococcus pneumoniae
McCullers, J. A., Karlström, Å., Iverson, A., Loeffler, J. M., & Fischetti, V. A. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030028 · Cited by 110 · see citing works
Self-citationViral and Bacterial Co-Infections in the Lungs: Dangerous Liaisons
Oliva, J., & Terrier, O. (2021) · Viruses · doi:10.3390/v13091725 · Cited by 107 · see citing works
Karlström, Å., Boyd, K. L., English, B. K., & McCullers, J. A. (2008) · The Journal of Infectious Diseases · doi:10.1086/596051 · Cited by 104 · see citing works
Self-citationEtiology and Impact of Coinfections in Children Hospitalized With Community-Acquired Pneumonia
Nolan, V. G., Arnold, S. R., Bramley, A. M., Ampofo, K., Williams, D. J., Grijalva, C. G., Self, W. H., Anderson, E. J., Wunderink, R. G., Edwards, K. M., et al. (2017) · The Journal of Infectious Diseases · doi:10.1093/infdis/jix641 · Cited by 98 · see citing works
Self-citationAnimal models for the preclinical evaluation of candidate influenza vaccines
Bodewes, R., Rimmelzwaan, G. F., & Osterhaus, A. D. M. E. (2009) · Expert Review of Vaccines · doi:10.1586/erv.09.148 · Cited by 96 · see citing works
Short, K. R., Habets, M. N., Hermans, P. W. M., & Diavatopoulos, D. A. (2012) · Future Microbiology · doi:10.2217/fmb.12.29 · Cited by 95 · see citing works
In-vivo monitoring of infectious diseases in living animals using bioluminescence imaging
Avci, P., Karimi, M., Sadasivam, M., Antunes-Melo, W. C., Carrasco, E., & Hamblin, M. R. (2017) · Virulence · doi:10.1080/21505594.2017.1371897 · Cited by 93 · see citing works
Chinchilla as a robust, reproducible and polymicrobial model of otitis media and its prevention
Bakaletz, L. O. (2009) · Expert Review of Vaccines · doi:10.1586/erv.09.63 · Cited by 81 · see citing works
The role of influenza in the severity and transmission of respiratory bacterial disease
Mina, M. J., & Klugman, K. P. (2014) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(14)70131-6 · Cited by 78 · see citing works
Bhowmick, R., Maung, N. H. T., Hurley, B. P., Ghanem, E. N. B., Gronert, K., McCormick, B. A., & Leong, J. M. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300522 · Cited by 76 · see citing works
Cameron, M. J., Kelvin, A. A., Leon, A. J., Cameron, C., Ran, L., Xu, L., Chu, Y.-K., Danesh, A., Yuan, F., Li, Q., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045842 · Cited by 68 · see citing works
Influenza-Induced Inflammation Drives Pneumococcal Otitis Media
Short, K. R., Reading, P. C., Brown, L. E., Pedersen, J., Gilbertson, B. P., Job, E. R., Edenborough, K. M., Habets, M. N., Zomer, A., Hermans, P. W. M., et al. (2013) · Infection and Immunity · doi:10.1128/iai.01278-12 · Cited by 65 · see citing works
Preventing and Treating Secondary Bacterial Infections with Antiviral Agents
McCullers, J. A. (2011) · Antiviral Therapy · doi:10.3851/imp1730 · Cited by 64 · see citing works
Self-citationMoore, H. C., Jacoby, P., Taylor, A., Harnett, G. B., Bowman, J. M., Riley, T. V., Reuter, K., Smith, D. W., & Lehmann, D. (2010) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0b013e3181d067cb · Cited by 64 · see citing works
Hu, Y., Lee, P., Hsueh, P., Lu, C., Chang, L., Huang, L., Chang, T., & Chen, J. (2021) · Scientific Reports · doi:10.1038/s41598-020-79680-6 · Cited by 59 · see citing works
Bacterial and Parasitic Diseases of Parrots
Doneley, B. (2009) · Veterinary Clinics of North America Exotic Animal Practice · doi:10.1016/j.cvex.2009.06.009 · Cited by 55 · see citing works
Short, K. R., von Köckritz‐Blickwede, M., Langereis, J. D., Chew, K. Y., Job, E. R., Armitage, C. W., Hatcher, B., Fujihashi, K., Reading, P. C., Hermans, P. W. M., et al. (2013) · Infection and Immunity · doi:10.1128/iai.01104-13 · Cited by 55 · see citing works
Bacterial Factors Required for Transmission of Streptococcus pneumoniae in Mammalian Hosts
Rowe, H. M., Karlsson, E. A., Echlin, H., Chang, T., Wang, L., van Opijnen, T., Pounds, S. B., Schultz‐Cherry, S., & Rosch, J. W. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2019.04.012 · Cited by 54 · see citing works
Dimmock, N. J., Dove, B. K., Scott, P. D., Meng, B., Taylor, I., Cheung, L., Hallis, B., Marriott, A. C., Carroll, M. W., & Easton, A. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049394 · Cited by 53 · see citing works
Innate immunity and chronic rhinosinusitis: What we have learned from animal models
London, N. R., & Lane, A. P. (2016) · Laryngoscope Investigative Otolaryngology · doi:10.1002/lio2.21 · Cited by 52 · see citing works
Influenza Virus Induces Bacterial and Nonbacterial Otitis Media
Short, K. R., Diavatopoulos, D. A., Thornton, R. B., Pedersen, J., Strugnell, R. A., Wise, A. K., Reading, P. C., & Wijburg, O. L. C. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir618 · Cited by 51 · see citing works
Influenza vaccination and Guillain–Barré syndrome: Reality or fear
Babazadeh, A., Afshar, Z. M., Javanian, M., Mohammadnia‐Afrouzi, M., Karkhah, A., Masrour-Roudsari, J., Sabbagh, P., Koppolu, V., Vasigala, V. R., & Ebrahimpour, S. (2019) · Journal of Translational Internal Medicine · doi:10.2478/jtim-2019-0028 · Cited by 51 · see citing works
Huang, S. S. H., Banner, D., Degousée, N., Leon, A. J., Xu, L., Paquette, S. G., Kanagasabai, T., Yuan, F., Rubino, S., Rubin, B. B., et al. (2012) · Journal of Virology · doi:10.1128/jvi.01456-12 · Cited by 51 · see citing works
Bacterial and Parasitic Diseases of Ferrets
Powers, L. V. (2009) · Veterinary Clinics of North America Exotic Animal Practice · doi:10.1016/j.cvex.2009.06.001 · Cited by 45 · see citing works
Vimalanathan, S., Schoop, R., Suter, A., & Hudson, J. B. (2017) · Virus Research · doi:10.1016/j.virusres.2017.03.006 · Cited by 44 · see citing works
Yano, H., Okitsu, N., Hori, T., Watanabe, O., Kisu, T., Hatagishi, E., Suzuki, A. K., Okamoto, M., Ohmi, A., Suetake, M., et al. (2008) · Acta Oto-Laryngologica · doi:10.1080/00016480802032777 · Cited by 44 · see citing works
Sialidase‐Based Anti–Influenza Virus Therapy Protects against Secondary Pneumococcal Infection
Hedlund, M., Aschenbrenner, L. M., Jensen, K. A., Larson, J. L., & Fang, F. (2010) · The Journal of Infectious Diseases · doi:10.1086/651170 · Cited by 42 · see citing works
Biology and Diseases of Ferrets
Mayer, J., Marini, R. P., & Fox, J. G. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-409527-4.00014-6 · Cited by 43 · see citing works
The Unexpected Impact of Vaccines on Secondary Bacterial Infections Following Influenza
Smith, A. M., & Huber, V. C. (2017) · Viral Immunology · doi:10.1089/vim.2017.0138 · Cited by 36 · see citing works
Banner, D., & Kelvin, A. A. (2012) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.2666 · Cited by 33 · see citing works
Host-microbe interactions in chronic rhinosinusitis biofilms and models for investigation
Vanderpool, E. J., & Rumbaugh, K. P. (2023) · Biofilm · doi:10.1016/j.bioflm.2023.100160 · Cited by 24 · see citing works
Brown, K. M., Sage, V. L., French, A. J., Jones, J. E., Padovani, G. H., Avery, A. J., Myerburg, M. M., Schultz‐Cherry, S., Rosch, J. W., Hiller, N. L., et al. (2022) · FEMS Microbes · doi:10.1093/femsmc/xtac007 · Cited by 19 · see citing works
5. Microbiology and Immunology
Barenkamp, S. J., Ogra, P. L. O., Bakaletz, L. O., Chonmaitree, T., Heikkinen, T., Hurst, D. S., Kawauchi, H., Kurono, Y., Leiberman, A., Murphy, T. F., et al. (2005) · Annals of Otology Rhinology & Laryngology · doi:10.1177/00034894051140s109 · Cited by 19 · see citing works
Kiupel, M., & Perpiñán, D. (2014) · doi:10.1002/9781118782699.ch20 · Cited by 18 · see citing works
Oladokun, S., & Sharif, S. (2024) · Animal Microbiome · doi:10.1186/s42523-024-00308-5 · Cited by 18 · see citing works
Pathogen Replication, Host Inflammation, and Disease in the Upper Respiratory Tract
Mina, M. J., & Klugman, K. P. (2013) · Infection and Immunity · doi:10.1128/iai.01460-12 · Cited by 16 · see citing works
Zhang, H. (2008) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkn026 · Cited by 16 · see citing works
Klonoski, J. M., Watson, T., Bickett, T. E., Svendsen, J. M., Gau, T. J., Britt, A., Nelson, J. T., Schlenker, E. H., Chaussee, M. S., Rynda‐Apple, A., et al. (2018) · Viral Immunology · doi:10.1089/vim.2017.0193 · Cited by 15 · see citing works
Agnihothram, S., Basco, M. D. S., Mullis, L. B., Foley, S. L., Hart, M. E., Sung, K., & Azevedo, M. S. P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144911 · Cited by 14 · see citing works
Animal Models of Human Viral Diseases
Ruiz, S. I., Zumbrun, E. E., & Nalça, A. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-415894-8.00038-5 · Cited by 13 · see citing works
Carreño-Flórez, G. P., Kocak, B. R., Hendricks, M. R., Melvin, J. A., Mar, K. B., Kosanovich, J. L., Cumberland, R. L., Delgoffe, G. M., Shiva, S., Empey, K. M., et al. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011719 · Cited by 13 · see citing works
Animal Models of Human Viral Diseases
Ruiz, S. I., Zumbrun, E. E., & Nalça, A. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809468-6.00033-4 · Cited by 13 · see citing works
Grieves, J. L., Jurcisek, J. A., Quist, B., Durbin, R. K., Peeples, M. E., Durbin, J. E., & Bakaletz, L. O. (2010) · PubMed Central · Cited by 12 · see citing works
Kiupel, M., Desjardins, D. R., Lim, A., Bolin, C. A., Johnson-Delaney, C. A., Resau, J. H., Garner, M. M., & Bolin, S. R. (2012) · Emerging infectious diseases · doi:10.3201/eid1811.120072 · Cited by 11 · see citing works
Tantawy, A. A. G., Barakat, M. M. A., Adly, A. A. M., Ebeid, F. S. E., Elshamaa, M. F., & Yassin, M. (2015) · Pediatric Hematology and Oncology · doi:10.3109/08880018.2015.1013230 · Cited by 11 · see citing works
Influenza virus infection: don't forget the role of the mucociliary system!
Duez, J.-M., Sixt, N., & Péchinot, A. (2008) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkn468 · Cited by 11 · see citing works
A comparative analysis of carbon dioxide displacement rates for euthanasia of the ferret
Fitzhugh, D. C., Parmer, A., Shelton, L. J., & Sheets, J. T. (2008) · Lab Animal · doi:10.1038/laban0208-81 · Cited by 10 · see citing works
Barron, H. W., & Rosenthal, K. L. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-6621-7.00006-3 · Cited by 9 · see citing works
COVID-19 and the Microbiome: The Gut-Lung Connection
Aan, F. J., Glibetić, N., Montoya‐Uribe, V., & Matter, M. L. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819265-8.00048-6 · Cited by 10 · see citing works
Can animal models really teach us anything about pneumonia? Pro
Orihuela, C. J., Maus, U. A., & Brown, J. (2020) · European Respiratory Journal · doi:10.1183/13993003.01539-2019 · Cited by 8 · see citing works
Lux, C. A., Douglas, R. G., Cho, D., Taylor, M. W., & Biswas, K. (2019) · Rhinology online · doi:10.4193/rhinol/19.015 · Cited by 8 · see citing works
Influenza Virus Antiviral Targets
Air, G. M., & Brouillette, W. J. (2014) · ASM Press eBooks · doi:10.1128/9781555815493.ch11 · Cited by 8 · see citing works
Yiu, L. K. W. (2015) · Journal of Pulmonary & Respiratory Medicine · doi:10.4172/2161-105x.1000245 · Cited by 7 · see citing works
Otolaryngological Complications in Patients Infected with the Influenza A (H1N1) Virus
Gutierrez, C., Nazar, G., & Torres, J. P. (2011) · Otolaryngology · doi:10.1177/0194599811425765 · Cited by 7 · see citing works
Development of an implantable PCL/alginate bilayer scaffold to prevent secondary infections
Baek, S., Park, H., Chen, K., Park, H., & Lee, D. (2020) · Korean Journal of Chemical Engineering · doi:10.1007/s11814-019-0459-8 · Cited by 6 · see citing works
Respiratory Diseases of Ferrets
Perpiñán, D. (2020) · Elsevier eBooks · doi:10.1016/b978-0-323-48435-0.00006-x · Cited by 6 · see citing works
Ferret TNF-α and IFN-γ Immunoassays
Ann, A., Banner, D., Danesh, A., Seneviratne, C., Ochi, A., & Joseph, D. (2012) · InTech eBooks · doi:10.5772/37193 · Cited by 5 · see citing works
Type I IFN Exhaustion is a Host Defence Protecting Against Secondary Bacterial Infections
Furuya, Y., & Müllbacher, A. (2013) · Scandinavian Journal of Immunology · doi:10.1111/sji.12107 · Cited by 5 · see citing works
Short, K. R., Habets, M. N., Payne, J., Reading, P. C., Diavatopoulos, D. A., & Wijburg, O. L. C. (2013) · Virology Journal · doi:10.1186/1743-422x-10-128 · Cited by 5 · see citing works
Mifsud, E. J., Farrukee, R., Hurt, A. C., Reading, P. C., & Barr, I. (2022) · FEMS Microbes · doi:10.1093/femsmc/xtac011 · Cited by 3 · see citing works
Ferrets as a Mammalian Model to Study Influenza Virus-Bacteria Interactions
Thakur, P. B., Mrotz, V., Maines, T. R., & Belser, J. A. (2023) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiad408 · Cited by 4 · see citing works
Complicated Head and Neck Infections Following Influenza Virus Infection in Children
Foster, C. E., & Kaplan, S. L. (2019) · The Pediatric Infectious Disease Journal · doi:10.1097/inf.0000000000002294 · Cited by 3 · see citing works
Wang, X., Cehn, M.-Q., Li, W., Fu, J., & Ye, X. (2021) · PubMed Central · doi:10.7499/j.issn.1008-8830.2011078 · Cited by 2 · see citing works
Acute sinusitis complicating infectious mononucleosis in an adolescent
Shkalim, V., Shoval, D. S., & Amir, J. (2007) · International Journal of Pediatric Otorhinolaryngology Extra · doi:10.1016/j.pedex.2007.06.001 · Cited by 2 · see citing works
Khalid, O. M., Omer, M. B., Kardman, S. E., & Yagi, H. I. (2022) · The Egyptian Journal of Otolaryngology · doi:10.1186/s43163-022-00316-9 · Cited by 2 · see citing works
Musa, M. D. (2023) · University of Thi-Qar Journal of Science · doi:10.32792/utq/utjsci/v10i1.930 · Cited by 2 · see citing works
Gouya, M. M., Tayeri, K., Akbari, H., Rezaei, F., Hemmati, P., & Soroush, M. (2018) · PubMed Central · Cited by 1 · see citing works
Novel strategies to prevent and treat experimental pneumococcal disease
Ross, K. (2010) · Enlighten: Theses (The University of Glasgow) · Cited by 1 · see citing works
POSSIBLE MECHANISMS UNDERLYING BACTERIAL-VIRAL INTERACTIONS IN RESPIRATORY DISEASES: A REVIEW
Oluwayelu, D. O., & Adebiyi, A. I. (2015) · African Journal of Infectious Diseases · doi:10.21010/ajid.v9i2.5
Eshaghi, A., Blair, J., Burton, L., Choi, K. W., Lima, C. D., McGeer, A., Low, D. E., Mazzulli, T., & Drews, S. J. (2009) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2008.10.014
Larsen, A. R., Skov, R. L., Henriksen, A. S., Jarlier, V., Bernard, P., O'Connell, B. C., Williams, Z., & Denton, M. (2008) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkn503
Neurologische Erkrankungen beim Frettchen - eine Literaturübersicht
Sulimma, L. (2014)
The role of viruses in chronic rhinosinusitis
Goggin, R. K. (2020) · Adelaide Research & Scholarship (AR&S) (University of Adelaide)
Murdoch, D. R. (2009) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1142023.599142
The Evolution and Complications of the Influenza During Covid-19 Pandemic
Iancu, M. A., Baltă, M. D., Eremia, I. A., Popovici, C., & Kozma, A. (2023) · Annals of the Academy of Romanian Scientists Series on Biological Sciences · doi:10.56082/annalsarscibio.2023.2.49
Alqaissi, E., Alotaibi, F. S., Ramzan, M. S., & Algarni, A. (2024) · Journal of Intelligent & Fuzzy Systems · doi:10.3233/jifs-233381
RetractedMcCullers, J. A. (2025) · Elsevier eBooks · doi:10.1016/b978-0-323-82763-8.00191-6
Self-citationPerez, A. C. (2014) · WakeSpace Scholarship (Wake Forest University)
A murine sinonasal infection model recapitulates key features of clinical chronic rhinosinusitis
Vanderpool, E. J., & Rumbaugh, K. P. (2026) · Journal of Medical Microbiology · doi:10.1099/jmm.0.002152
Propach, C., Hönemann, M., Vučinić, V., Frille, A., Berthold, T., Bergs, S., Maier, M., & Pietsch, C. (2026) · BMC Infectious Diseases · doi:10.1186/s12879-026-14377-1
- Authors
- Peltola, V. T., Boyd, K. L., McAuley, J. L., Rehg, J. E., & McCullers, J. A.
- Affiliations
- Departments of Infectious Diseases
- St. Jude Children's Research Hospital (US)
- Pathology
- Corresponding author
- McCullers, Jonathan A.
- Venue
- Infection and Immunity
- Publisher
- American Society for Microbiology
- Published
- 2006-05
- Volume
- 74
- Issue
- 5
- Pages
- 2562-2567
- ISSN
- 0019-9567 (ISSN-L)
- 1098-5522
- OpenAlex
- W2156265358
- Cited by
- 95
- References
- 38
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 5 · 2019: 4 · 2018: 4 · 2017: 5 · 2016: 3 · 2015: 6 · 2014: 6 · 2013: 8 · 2012: 8
- FWCI
- 4.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Infection and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Lebanese Syrian Associated Charities
- Academy of Finland
- National Institutes of Health (1k08ai049178-01)
- National Institute of Allergy and Infectious Diseases (AI-54802, AI-49178, R21AI054802)
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Pneumonia and Respiratory Infections
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Keywords
- Streptococcus pneumoniae, influenza virus, secondary bacterial infection, sinusitis, otitis media, ferrets, H1N1 influenza, influenza B, nasopharyngeal carriage, animal models
- MeSH terms
- Animals, Disease Models, Animal, Ferrets, Nasal Mucosa, Orthomyxoviridae Infections, Influenza B virus, Otitis Media, Pneumococcal Infections, Sinusitis, Influenza A Virus, H1N1 Subtype, Influenza A Virus, H3N2 Subtype
About these checks
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
