Community-acquired respiratory coinfection in critically ill patients with pandemic 2009 influenza A(H1N1) virus
Open accessAbstract
Background Little is known about the impact of community-acquired respiratory coinfection in patients with pandemic 2009 influenza A(H1N1) virus infection.Methods This was a prospective, observational, multicenter study conducted in 148 Spanish ICUs.Results Severe respiratory syndrome was present in 645 ICU patients. Coinfection occurred in 113 (17.5%) of patients. Streptococcus pneumoniae (in 62 patients [54.8%]) was identified as the most prevalent bacteria. Patients with coinfection at ICU admission were older (47.5±15.7 vs 43.8±14.2 years, P<.05) and presented a higher APACHE (Acute Physiology and Chronic Health Evaluation) II score (16.1±7.3 vs 13.3±7.1, P<.05) and Sequential Organ Failure Assessment (SOFA) score (7.0±3.8 vs 5.2±3.5, P<.05). No differences in comorbidities were observed. Patients who had coinfection required vasopressors (63.7% vs 39.3%, P<.05) and invasive mechanical ventilation (69% vs 58.5%, P<.05) more frequently. ICU length of stay was 3 days longer in patients who had coinfection than in patients who did not (11 [interquartile range, 5-23] vs 8 [interquartile range 4-17], P=.01). Coinfection was associated with increased ICU mortality (26.2% vs 15.5%; OR, 1.94; 95% CI, 1.21-3.09), but Cox regression analysis adjusted by potential confounders did not confirm a significant association between coinfection and ICU mortality.Conclusions During the 2009 pandemics, the role played by bacterial coinfection in bringing patients to the ICU was not clear, S pneumoniae being the most common pathogen. This work provides clear evidence that bacterial coinfection is a contributor to increased consumption of health resources by critical patients infected with the virus and is the virus that causes critical illness in the vast majority of cases.
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?
Bacterial co-infection was detected in ~30% of cases in the 2009 H1N1 pandemic, with high mortality rates despite administration of appropriate antibiotics.
“Bacterial co-infection was also detected in ~30% of cases in the 2009 H1N1 pandemic, with high mortality rates despite administration of appropriate antibiotics”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [15]
In the Spanish ICU study, S pneumoniae was identified as the most prevalent bacteria (54·8%).
“S pneumoniae was identified as the most prevalent bacteria (54·8%).”
From Bacterial and viral infections associated with influenza (2013) · cites this paper as [36]
In a prospective observational multicenter study of 645 patients with confirmed H1N1 pandemic influenza in 148 Spanish ICUs, co-infection occurred in 113 (17·5%) of patients.
“A prospective, observational, multicenter study conducted in 148 Spanish intensive care units (ICU) and with 645 patients, all of whom had confirmed H1N1 pandemic influenza infection showed that co‐infection occurred in 113 (17·5%) of patients.”
From Bacterial and viral infections associated with influenza (2013) · cites this paper as [36]
In the Spanish ICU study, Cox regression analysis adjusted by potential confounders did not confirm a significant association between co-infection and ICU mortality.
“but Cox regression analysis adjusted by potential confounders did not confirm a significant association between co‐infection and ICU mortality.”
From Bacterial and viral infections associated with influenza (2013) · cites this paper as [36]
In the Spanish ICU study, co-infection was associated with increased ICU mortality (26·2% versus 15·5%).
“Co‐infection was associated with increased ICU mortality (26·2% versus 15·5%)”
From Bacterial and viral infections associated with influenza (2013) · cites this paper as [36]
Cites
Knaus, W. A., Draper, E. A., Wagner, D. P., & Zimmerman, J. E. (1985) · Critical Care Medicine · doi:10.1097/00003246-198510000-00009 · Cited by 15,333 · see citing works
APACHE II-A Severity of Disease Classification System
Knaus, W. A., Draper, E. A., Wagner, D. P., & Zimmerman, J. E. (1986) · Critical Care Medicine · doi:10.1097/00003246-198608000-00028 · Cited by 13,379 · see citing works
Vincent, J. L., Moreno, R., Takala, J., Willatts, S., De Mendonça, A., Bruining, H., Reinhart, C. K., Suter, P. M., & Thijs, L. G. (1996) · Intensive Care Medicine · doi:10.1007/bf01709751 · Cited by 11,674 · see citing works
Bellomo, R., Ronco, C., Kellum, J. A., Mehta, R. L., Palevsky, P. M., & workgroup, T. A. (2004) · Critical Care · doi:10.1186/cc2872 · Cited by 6,769 · see citing works
Mandell, L. A., Wunderink, R. G., Anzueto, A., Bartlett, J. G., Campbell, G. D., Dean, N. C., Dowell, S. F., File, T. M., Musher, D. M., Niederman, M. S., et al. (2007) · Clinical Infectious Diseases · doi:10.1086/511159 · Cited by 6,182 · see citing works
(2005) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200405-644st · Cited by 5,870 · see citing works
Voriconazole versus Amphotericin B for Primary Therapy of Invasive Aspergillosis
Herbrecht, R., Denning, D. W., Patterson, T. F., Bennett, J. E., Greene, R. E., Oestmann, J.-W., Kern, W. V., Marr, K. A., Ribaud, P., Lortholary, O., et al. (2002) · New England Journal of Medicine · doi:10.1056/nejmoa020191 · Cited by 3,304 · see citing works
Practice Guidelines for the Management of Community-Acquired Pneumonia in Adults
Bartlett, J. G., Dowell, S. F., Mandell, L. A., File, T. M., Musher, D. M., & Fine, M. J. (2000) · Clinical Infectious Diseases · doi:10.1086/313954 · Cited by 2,277 · see citing works
Morens, D. M., Taubenberger, J. K., & Fauci, A. S. (2008) · The Journal of Infectious Diseases · doi:10.1086/591708 · Cited by 1,625 · see citing works
Critically Ill Patients With 2009 Influenza A(H1N1) Infection in Canada
Kumar, A. (2009) · JAMA · doi:10.1001/jama.2009.1496 · Cited by 1,425 · see citing works
H1N1 2009 influenza virus infection during pregnancy in the USA
Jamieson, D. J., Honein, M. A., Rasmussen, S. A., Williams, J. L., Swerdlow, D. L., Biggerstaff, M., Lindstrom, S., Louie, J. K., Christ, C. M., Bohm, S. R., et al. (2009) · The Lancet · doi:10.1016/s0140-6736(09)61304-0 · Cited by 1,340 · see citing works
Pneumonia 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
Critical Care Services and 2009 H1N1 Influenza in Australia and New Zealand
The ANZIC Influenza Investigators (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0908481 · Cited by 1,002 · see citing works
Guidelines for the management of adult lower respiratory tract infections
Woodhead, M. A., Blasi, F., Ewig, S., Huchon, G., Leven, M., Ortqvist, A., Schaberg, T., Torres, A., van der Heijden, G. J. M. G., & Verheij, T. J. (2005) · European Respiratory Journal · doi:10.1183/09031936.05.00055705 · Cited by 891 · see citing works
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
Influenza-Associated Deaths among Children in the United States, 2003–2004
Bhat, N., Wright, J. G., Broder, K. R., Murray, E. L., Greenberg, M. E., Glover, M. J., Likos, A. M., Posey, D. L., Klimov, A., Lindstrom, S. E., et al. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa051721 · Cited by 648 · see citing works
The 1918 Influenza Pandemic: Insights for the 21st Century
Morens, D. M., & Fauci, A. S. (2007) · The Journal of Infectious Diseases · doi:10.1086/511989 · Cited by 536 · see citing works
BTS Guidelines for the Management of Community Acquired Pneumonia in Adults
British Thoracic Society Standards of Care Committee in collaboration with and endorsed by the Royal College of Physicians of London, Royal College of General Practitioners, British Geriatrics Society, British Lung Foundation, British Infection Society, & B (2001) · Thorax · doi:10.1136/thx.56.suppl_4.iv1 · Cited by 506 · see citing works
Intensive care adult patients with severe respiratory failure caused by Influenza A (H1N1)v in Spain
Rello, J., Rodríguez, A. H., Ibañez, P., Socías, L., Cebrián, J., Marques, A., Guerrero, J. E., Ruiz‐Santana, S., Márquez, E., Nogal-Saez, F. D., et al. (2009) · Critical Care · doi:10.1186/cc8044 · Cited by 441 · see citing works
Self-citationTo, K. K., Hung, I. F., Li, I. W. S., Lee, K., Koo, C., Yan, W., Liu, R. W., Ho, K., Chu, K., Watt, C., et al. (2010) · Clinical Infectious Diseases · doi:10.1086/650581 · Cited by 417 · see citing works
The 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
Brundage, J. F. (2006) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(06)70466-2 · Cited by 386 · see citing works
Severe Community-acquired Pneumonia Due to <i>Staphylococcus aureus</i> , 2003–04 Influenza Season
Hageman, J. C., Uyeki, T. M., Francis, J. S., Jernigan, D. B., Wheeler, J. G., Bridges, C. B., Barenkamp, S. J., Sievert, D. M., Srinivasan, A., Doherty, M. C., et al. (2006) · Emerging infectious diseases · doi:10.3201/eid1206.051141 · Cited by 379 · see citing works
Th1 and Th17 hypercytokinemia as early host response signature in severe pandemic influenza
Bermejo-Martín, J. F., de Lejarazu, R. O., Pumarola, T., Rello, J., Almansa, R., Ramírez, P., Martín‐Loeches, I., Varillas‐Delgado, D., Gallegos, M. C., Arbeloa, C. S., et al. (2009) · Critical Care · doi:10.1186/cc8208 · Cited by 373 · see citing works
Self-citationEpidemiology of fatal cases associated with pandemic H1N1 influenza 2009.
Vaillant, L., La Ruche, G., Tarantola, A., Barboza, P., & for the epidemic intelligence team at InVS (2009) · Eurosurveillance · doi:10.2807/ese.14.33.19309-en · Cited by 348 · see citing works
Streptococcus pneumoniae coinfection is correlated with the severity of H1N1 pandemic influenza
Palacios, G., Hornig, M., Cisterna, D., Savji, N., Bussetti, A. V., Kapoor, V., Hui, J., Tokarz, R., Briese, T., Baumeister, E., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008540 · Cited by 275 · see citing works
BTS Guidelines for the Management of Community Acquired Pneumonia in Adults.
(2001) · Europe PMC (PubMed Central) · doi:10.1136/thorax.56.suppl_4.iv1 · Cited by 272 · see citing works
Pandemic 2009 Influenza A in Argentina: A Study of 337 Patients on Mechanical Ventilation
Estenssoro, E., Ríos, F. G., Apezteguía, C., Reina, R., Neira, J., Ceraso, D. H., Orlandi, C., Valentini, R., Tiribelli, N., Brizuela, M., et al. (2010) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/201001-0037oc · Cited by 230 · see citing works
Bruneel, F., Hocqueloux, L., Alberti, C., Wolff, M., Chevret, S., Bédos, J.-P., Durand, R., Le Bras, J., Régnier, B., & Vachon, F. (2003) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.200206-631oc · Cited by 207 · see citing works
Microbiological Testing and Outcome of Patients With Severe Community-Acquired Pneumonia
Rello, J., Bodí, M. A., Mariscal, D., et al. (2003) · CHEST Journal · doi:10.1378/chest.123.1.174 · Cited by 167 · see citing works
Self-citationClinical characteristics of paediatric H1N1 admissions in Birmingham, UK
Hackett, S. J., Hill, L. F., Patel, J., Ratnaraja, N., Ifeyinwa, A., Farooqi, M., Nusgen, U., Debenham, P., Gandhi, D. K., Makwana, N., et al. (2009) · The Lancet · doi:10.1016/s0140-6736(09)61511-7 · Cited by 139 · see citing works
Rello, J., Esandi, M., Mariscal, D., Gallego, M., Domingo, C., & Vallés, J. (1998) · Clinical Infectious Diseases · doi:10.1086/517672 · Cited by 118 · see citing works
Self-citationThe value of routine microbial investigation in community-acquired pneumonia
Woodhead, M. A., Arrowsmith, J. E., Chamberlain-Webber, R., et al. (1991) · Respiratory Medicine · doi:10.1016/s0954-6111(06)80103-4 · Cited by 111 · see citing works
Walter, N. D., Taylor, T. H., Shay, D. K., Thompson, W., Brammer, L., Dowell, S. F., & Moore, M. R. (2009) · Clinical Infectious Diseases · doi:10.1086/649208 · Cited by 105 · see citing works
Immunokinetics in severe pneumonia due to influenza virus and bacteria coinfection in mice.
Seki, M., Yanagihara, K., Higashiyama, Y., Fukuda, Y., Kaneko, Y., Ohno, H., Miyazaki, Y., Hirakata, Y., Tomono, K., Kadota, J., et al. (2004) · European Respiratory Journal · doi:10.1183/09031936.04.00126103 · Cited by 103 · see citing works
SEPAR Working Group on Community-Acquired Pneumonia, & Assembly, T. A. R. I. (. (2005) · Archivos de Bronconeumología · doi:10.1016/s1579-2129(06)60222-x · Cited by 38 · see citing works
A Comparison of Group A Streptococcus Versus Streptococcus pneumoniae Pneumonia
Kaabi, N. A. M. A., Solh, Z., Pacheco, S., et al. (2006) · The Pediatric Infectious Disease Journal · doi:10.1097/01.inf.0000243198.63255.c1 · Cited by 32 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis.
Klein, E. Y., Monteforte, B., Gupta, A., Jiang, W., May, L., Hsieh, Y., & Dugas, A. (2016) · Influenza and Other Respiratory Viruses · doi:10.1111/irv.12398 · Cited by 574 · 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
Rice, T. W., Rubinson, L., Uyeki, T. M., Vaughn, F. L., John, B. B., Miller, R. R., Higgs, E., Randolph, A. G., Smoot, B. E., & Thompson, B. T. (2012) · Critical Care Medicine · doi:10.1097/ccm.0b013e3182416f23 · Cited by 391 · see citing works
Bacterial Coinfection in Influenza: A Grand Rounds Review
Chertow, D. S., & Memoli, M. J. (2013) · JAMA · doi:10.1001/jama.2012.194139 · Cited by 390 · see citing works
MacIntyre, C. R., Chughtai, A. A., Barnes, M., Ridda, I., Seale, H., Toms, R., & Heywood, A. (2018) · BMC Infectious Diseases · doi:10.1186/s12879-018-3548-0 · Cited by 323 · see citing works
Bacterial and viral infections associated with influenza
Joseph, C., Togawa, Y., & Shindo, N. (2013) · Influenza and Other Respiratory Viruses · doi:10.1111/irv.12089 · Cited by 250 · see citing works
Weinberger, D. M., Simonsen, L., Jordan, R., Steiner, C., Miller, M., & Viboud, C. (2012) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir749 · Cited by 132 · see citing works
The impact of bacterial and viral co‐infection in severe influenza
Blyth, C. C., Webb, S. A. R., Kok, J., Dwyer, D. E., van Hal, S. J., Foo, H., Ginn, A. N., Kesson, A. M., Seppelt, I., Iredell, J. R., et al. (2013) · Influenza and Other Respiratory Viruses · doi:10.1111/j.1750-2659.2012.00360.x · Cited by 117 · see citing works
Bacterial co-infection with H1N1 infection in patients admitted with community acquired pneumonia
Cillóniz, C., Ewig, S., Menéndez, R., Ferrer, M., Polverino, E., Reyes, S., Gabarrús, A., Marcos, M. A., Cordoba, J., Mensa, J., et al. (2012) · Journal of Infection · doi:10.1016/j.jinf.2012.04.009 · Cited by 94 · see citing works
Muscedere, J., Ofner, M., Kumar, A., Long, J., Lamontagne, F., Cook, D., McGeer, A., Chant, C., Marshall, J., Jouvet, P., et al. (2013) · Chest · doi:10.1378/chest.12-1861 · Cited by 40 · see citing works
- Authors
- Martín-Loeches, I., Sanchez-Corral, A., Diaz, E., Granada, R. M., Zaragoza, R., Villavicencio, C., Albaya, A., Cerdá, E., Catalán, R. M., Luque, P., Paredes, A., Navarrete, I., Rello, J., & Rodríguez, A.
- Affiliations
- Vall d'Hebron Hospital Universitari (ES)
- Bellvitge University Hospital (ES)
- Hospital Universitario Doctor Peset (ES)
- Centro de Investigación Biomédica en Red de Enfermedades Respiratorias (ES)
- Hospital Universitario de Guadalajara (ES)
- Hospital Clínico Universitario Lozano Blesa (ES)
- Hospital Universitario Virgen de las Nieves (ES)
- Universitat Autònoma de Barcelona (ES)
- Venue
- Chest
- Publisher
- Elsevier BV
- Published
- 2011-03
- Volume
- 139
- Issue
- 3
- Pages
- 555-562
- ISSN
- 0012-3692 (ISSN-L)
- OpenAlex
- W2166978186
- Semantic Scholar
- 194814586299f696be1cd83ce20b3464f6763f3e
- Cited by
- 203
- References
- 37
- Citations by year
- 2026: 1 · 2025: 12 · 2024: 11 · 2023: 28 · 2022: 20 · 2021: 30 · 2020: 8 · 2019: 4 · 2018: 10 · 2017: 7 · 2016: 11 · 2015: 11 · 2014: 4 · 2013: 13 · 2012: 16
- FWCI
- 10.71
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- CHEST Journal (publishedVersion)
- PubMed (publishedVersion)
- Acceda (Universidad de Las Palmas de Gran Canaria) (submittedVersion)
- RUNA. Repositorio Institucional del Sergas (Servicio Gallego de Salud (SERGAS)) (submittedVersion, other-oa)
- 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
- 2009 H1N1 pandemic, influenza A (H1N1) virus, bacterial co-infection, Streptococcus pneumoniae, community-acquired respiratory tract infections, critically ill patients, intensive care unit, ICU mortality, mechanical ventilation, vasopressors, ICU length of stay, health resource utilization
- MeSH terms
- Adult, Female, Humans, Influenza, Human, Intensive Care Units, Male, Middle Aged, Prospective Studies, Regression Analysis, Respiration, Artificial, Respiratory Tract Infections, Retrospective Studies, Spain, Comorbidity, Prevalence, Critical Illness, Community-Acquired Infections, Influenza A Virus, H1N1 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