title: Bacterial and viral co-infections complicating severe influenza: Incidence and impact among 507 U.S. patients, 2013-14.
abstract: Influenza acts synergistically with bacterial co-pathogens. Few studies have described co-infection in a large cohort with severe influenza infection.
  
  
  
  To describe the spectrum and clinical impact of co-infections.
  
  
  
  Retrospective cohort study of patients with severe influenza infection from September 2013 through April 2014 in intensive care units at 33 U.S. hospitals comparing characteristics of cases with and without co-infection in bivariable and multivariable analysis.
  
  
  
  Of 507 adult and pediatric patients, 114 (22.5%) developed bacterial co-infection and 23 (4.5%) developed viral co-infection. Staphylococcus aureus was the most common cause of co-infection, isolated in 47 (9.3%) patients. Characteristics independently associated with the development of bacterial co-infection of adult patients in a logistic regression model included the absence of cardiovascular disease (OR 0.41 [0.23-0.73], p=0.003), leukocytosis (>11K/μl, OR 3.7 [2.2-6.2], p<0.001; reference: normal WBC 3.5-11K/μl) at ICU admission and a higher ICU admission SOFA score (for each increase by 1 in SOFA score, OR 1.1 [1.0-1.2], p=0.001). Bacterial co-infections (OR 2.2 [1.4-3.6], p=0.001) and viral co-infections (OR 3.1 [1.3-7.4], p=0.010) were both associated with death in bivariable analysis. Patients with a bacterial co-infection had a longer hospital stay, a longer ICU stay and were likely to have had a greater delay in the initiation of antiviral administration than patients without co-infection (p<0.05) in bivariable analysis.
  
  
  
  Bacterial co-infections were common, resulted in delay of antiviral therapy and were associated with increased resource allocation and higher mortality.
authors.affiliation: Department of Medicine, University of Chicago, Chicago, IL, United States. Electronic address: Nirav.Shah@uchospitals.edu.
authors.forename: Nirav S
authors.initials: NS
authors.lastname: Shah
authors.affiliation: Department of Medicine, University of Chicago, Chicago, IL, United States.
authors.forename: Jared A
authors.initials: JA
authors.lastname: Greenberg
authors.affiliation: Department of Medicine, University of Chicago, Chicago, IL, United States.
authors.forename: Moira C
authors.initials: MC
authors.lastname: McNulty
authors.affiliation: Department of Medicine, University of Michigan Medical School, Ann Arbor, MI, United States.
authors.forename: Kevin S
authors.initials: KS
authors.lastname: Gregg
authors.affiliation: Department of Medicine, University of Michigan Medical School, Ann Arbor, MI, United States.
authors.forename: James
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authors.lastname: Riddell
authors.affiliation: Department of Medicine, The Ohio State University Wexner Medical Center, Columbus, OH, United States.
authors.forename: Julie E
authors.initials: JE
authors.lastname: Mangino
authors.affiliation: Department of Medicine, The Ohio State University Wexner Medical Center, Columbus, OH, United States.
authors.forename: Devin M
authors.initials: DM
authors.lastname: Weber
authors.affiliation: Department of Medicine, The Ohio State University Wexner Medical Center, Columbus, OH, United States; Department of Biomedical Informatics, The Ohio State University Wexner Medical Center, Columbus, OH, United States.
authors.forename: Courtney L
authors.initials: CL
authors.lastname: Hebert
authors.affiliation: Department of Family Medicine, University of Colorado Denver, Denver, CO, United States.
authors.forename: Natalie S
authors.initials: NS
authors.lastname: Marzec
authors.affiliation: Department of Medicine, University of Colorado Denver, Denver, CO, United States.
authors.forename: Michelle A
authors.initials: MA
authors.lastname: Barron
authors.affiliation: Department of Medicine, Vidant Medical Center, Greenville, NC, United States.
authors.forename: Fredy
authors.initials: F
authors.lastname: Chaparro-Rojas
authors.affiliation: Department of Medicine, Baylor College of Medicine, Houston, TX, United States.
authors.forename: Alejandro
authors.initials: A
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authors.affiliation: Department of Medicine, Baylor College of Medicine, Houston, TX, United States.
authors.forename: Vagish
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authors.affiliation: Department of Medicine, University of Iowa Hospitals and Clinics, Iowa City, IA, United States.
authors.forename: Kunatum
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authors.affiliation: Department of Medicine, University of Iowa Hospitals and Clinics, Iowa City, IA, United States.
authors.forename: Sandra
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authors.lastname: Cobb
authors.affiliation: Department of Medicine, University of Iowa Hospitals and Clinics, Iowa City, IA, United States.
authors.forename: Loreen
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authors.lastname: Herwaldt
authors.affiliation: Department of Pediatrics, University of California San Diego and Rady Children's Hospital San Diego, San Diego, CA, United States.
authors.forename: Vanessa
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authors.lastname: Raabe
authors.affiliation: Department of Pediatrics, University of California San Diego and Rady Children's Hospital San Diego, San Diego, CA, United States.
authors.forename: Christopher R
authors.initials: CR
authors.lastname: Cannavino
authors.affiliation: Department of Medicine, University of Nebraska Medical Center, Omaha, NE, United States.
authors.forename: Andrea Green
authors.initials: AG
authors.lastname: Hines
authors.affiliation: Department of Medicine, University of Nebraska Medical Center, Omaha, NE, United States.
authors.forename: Sara H
authors.initials: SH
authors.lastname: Bares
authors.affiliation: Department of Medicine, Loyola University Medical Center, Maywood, IL, United States; Department of Medicine, Edward Hines VA Hospital, Maywood, IL, United States.
authors.forename: Philip B
authors.initials: PB
authors.lastname: Antiporta
authors.affiliation: Department of Pharmacy, Loyola University Medical Center, Maywood, IL, United States.
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authors.lastname: Scardina
authors.affiliation: Department of Pharmacy, Edward Hines VA Hospital, Maywood, IL, United States.
authors.forename: Ursula
authors.initials: U
authors.lastname: Patel
authors.affiliation: Department of Medicine, Loyola University Medical Center, Maywood, IL, United States; Department of Medicine, Edward Hines VA Hospital, Maywood, IL, United States.
authors.forename: Gail
authors.initials: G
authors.lastname: Reid
authors.affiliation: Department of Medicine, University of Texas Southwestern Medical Center, Dallas, TX, United States.
authors.forename: Parvin
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authors.lastname: Mohazabnia
authors.affiliation: Department of Medicine, University of Texas Southwestern Medical Center, Dallas, TX, United States.
authors.forename: Suresh
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authors.lastname: Kachhdiya
authors.affiliation: Department of Medicine, University of Texas Southwestern Medical Center, Dallas, TX, United States.
authors.forename: Binh-Minh
authors.initials: BM
authors.lastname: Le
authors.affiliation: Department of Medicine, Montefiore Medical Center/Albert Einstein College of Medicine, Bronx, NY, United States.
authors.forename: Connie J
authors.initials: CJ
authors.lastname: Park
authors.affiliation: Department of Medicine, Montefiore Medical Center/Albert Einstein College of Medicine, Bronx, NY, United States.
authors.forename: Belinda
authors.initials: B
authors.lastname: Ostrowsky
authors.affiliation: Department of Medicine, University of Chicago, Chicago, IL, United States; Department of Medicine, Northshore University HealthSystem, Evanston, IL, United States.
authors.forename: Ari
authors.initials: A
authors.lastname: Robicsek
authors.affiliation: Department of Medicine, Northshore University HealthSystem, Evanston, IL, United States.
authors.forename: Becky A
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authors.affiliation: Department of Pediatrics, University of Chicago, Chicago, IL, United States.
authors.forename: Jeanmarie
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authors.affiliation: Department of Pediatrics, University of Chicago, Chicago, IL, United States.
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authors.initials: MM
authors.lastname: Bhatti
authors.affiliation: Department of Medicine, University of Illinois at Chicago, Chicago, IL, United States; Department of Medicine, Jesse Brown VA Medical Center, Chicago, IL, United States.
authors.forename: Stockton
authors.initials: S
authors.lastname: Mayer
authors.affiliation: Department of Medicine, University of Illinois at Chicago, Chicago, IL, United States; Department of Medicine, Jesse Brown VA Medical Center, Chicago, IL, United States.
authors.forename: Monica
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authors.lastname: Sikka
authors.affiliation: Department of Medicine, University of Illinois at Chicago, Chicago, IL, United States; Department of Medicine, Jesse Brown VA Medical Center, Chicago, IL, United States.
authors.forename: Ivette
authors.initials: I
authors.lastname: Murphy-Aguilu
authors.affiliation: Department of Medicine, Community Care Networks, Inc., Munster, IN, United States.
authors.forename: Priti
authors.initials: P
authors.lastname: Patwari
authors.affiliation: Department of Medicine, University of California San Diego, San Diego, CA, United States.
authors.forename: Shira R
authors.initials: SR
authors.lastname: Abeles
authors.affiliation: Department of Medicine, University of California San Diego, San Diego, CA, United States.
authors.forename: Francesca J
authors.initials: FJ
authors.lastname: Torriani
authors.affiliation: Department of Medicine, Methodist Hospitals, Merrillville, IN, United States.
authors.forename: Zainab
authors.initials: Z
authors.lastname: Abbas
authors.affiliation: Department of Medicine, Methodist Hospitals, Merrillville, IN, United States.
authors.forename: Sophie
authors.initials: S
authors.lastname: Toya
authors.affiliation: Department of Medicine, University of Miami/Jackson Health System, Miami, FL, United States.
authors.forename: Katherine
authors.initials: K
authors.lastname: Doktor
authors.affiliation: Department of Medicine, University of Miami/Jackson Health System, Miami, FL, United States.
authors.forename: Anindita
authors.initials: A
authors.lastname: Chakrabarti
authors.affiliation: Department of Medicine, University of Miami/Jackson Health System, Miami, FL, United States.
authors.forename: Susanne
authors.initials: S
authors.lastname: Doblecki-Lewis
authors.affiliation: Department of Medicine, VA San Diego/University of California San Diego, San Diego, CA, United States.
authors.forename: David J
authors.initials: DJ
authors.lastname: Looney
authors.affiliation: Department of Medicine, University of Chicago, Chicago, IL, United States; Department of Pediatrics, University of Chicago, Chicago, IL, United States.
authors.forename: Michael Z
authors.initials: MZ
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mesh_terms: D000293:Adolescent; D000328:Adult; D000368:Aged; D001424:Bacterial Infections / Q000453:epidemiology*; D002648:Child; D002675:Child, Preschool; D060085:Coinfection / Q000453:epidemiology* / Q000382:microbiology / Q000821:virology; D003422:Critical Care; D005260:Female; D006801:Humans; D015994:Incidence; D007223:Infant; D007231:Infant, Newborn; D007251:Influenza, Human / Q000382:microbiology* / Q000821:virology*; D008297:Male; D008875:Middle Aged; D012189:Retrospective Studies; D013203:Staphylococcal Infections / Q000453:epidemiology; D016019:Survival Analysis; D014777:Virus Diseases / Q000453:epidemiology*; D055815:Young Adult
keywords: Co-infection; ICU; Influenza A (H1N1) pdm09; MRSA; Severe influenza; Staphylococcus aureus