The frequency of influenza and bacterial coinfection: a systematic review and meta-analysis

Influenza and other Respiratory Viruses

Volumn 10, Issue 5, 2016, Pages 394-403

  Klein, Eili Y ^a,b   Monteforte, Bradley ^c   Gupta, Alisha ^d   Jiang, Wendi ^b   May, Larissa ^e   Hsieh, Yu Hsiang ^a   Dugas, Andrea ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Center for Disease Dynamics Economics and Policy   (United States)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

^d ALLEGHENY GENERAL HOSPITAL   (United States)

^e GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

antibiotic resistance; bacterial coinfection; influenza; meta analysis; MRSA; Streptococcus Pneumoniae

Indexed keywords

BACTERIAL INFECTION; DISEASE SEVERITY; ESCHERICHIA COLI; HAEMOPHILUS INFLUENZAE; HUMAN; INFECTION RATE; INFECTION RISK; INFLUENZA; KLEBSIELLA PNEUMONIAE; MIXED INFECTION; MORAXELLA CATARRHALIS; MYCOPLASMA PNEUMONIAE; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STREPTOCOCCUS PNEUMONIAE; STREPTOCOCCUS PYOGENES; SYSTEMATIC REVIEW;

EID: 84978701081     PISSN: 17502640     EISSN: 17502659     Source Type: Journal    
DOI: 10.1111/irv.12398     Document Type: Review

References (65)

1. Thompson WW, Shay DK, Weintraub E et al. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 2003; 289:179–186.
2. Metersky ML, Masterton RG, Lode H, File TM Jr, Babinchak T. Epidemiology, microbiology, and treatment considerations for bacterial pneumonia complicating influenza. Int J Infect Dis 2012; 16:e321–e331.
3. Morens DM, Taubenberger JK, Fauci AS. Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness. J Infect Dis 2008; 198:962–970.
4. Masiá M, Padilla S, Antequera P, Ramos JM, Ruiz M, Gutiérrez F. Predictors of pneumococcal co-infection for patients with pandemic (H1N1) 2009. Emerg Infect Dis 2011; 17:1475.
5. Blyth CC, Webb SA, Kok J et al. The impact of bacterial and viral co-infection in severe influenza. Influenza Other Respir Viruses 2013; 7:168–176.
6. Cillóniz C, Ewig S, Menéndez R et al. Bacterial co-infection with H1N1 infection in patients admitted with community acquired pneumonia. J Infect 2012; 65:223–230.
7. Paddock CD, Liu L, Denison AM et al. Myocardial injury and bacterial pneumonia contribute to the pathogenesis of fatal influenza B virus infection. J Infect Dis 2012; 205:895–905.
8. Wilson WJ, Steer P. Bacteriological and pathological observations on influenza as seen in France during 1918. Br Med J 1919; 1:634–635.
9. Louria DB, Blumenfeld HL, Ellis JT, Kilbourne ED, Rogers DE. Studies on influenza in the pandemic of 1957-1958. II. Pulmonary complications of influenza. J Clin Invest 1959; 38:213.
10. Harford CG, Leidler V, Hara M. Effect of the lesion due to influenza virus on the resistance of mice to inhaled pneumococci. J Exp Med 1949; 89:53–68.
11. McCullers JA. Insights into the Interaction between Influenza Virus and Pneumococcus. Clin Microbiol Rev 2006; 19:571–582.
12. Van-Tam J, Sellwood C. Pandemic Influenza. Boston: CABI, 2012.
13. Chertow DS, Memoli MJ. Bacterial coinfection in influenza: a grand rounds review. JAMA 2013; 309:275–282.
14. Wang X-Y, Kilgore PE, Lim KA et al. Influenza and bacterial pathogen coinfections in the 20th century. Interdiscip Perspect Infect Dis 2011; 2011:146376.
15. Centers for Disease Control Prevention. Severe methicillin-resistant Staphylococcus aureus community-acquired pneumonia associated with influenza–Louisiana and Georgia, December 2006-January 2007. MMWR Morb Mortal Wkly Rep 2007; 56:325–329.
16. Centers for Disease Control Prevention. Severe coinfection with seasonal influenza A (H3N2) virus and Staphylococcus aureus–Maryland, February-March 2012. MMWR Morb Mortal Wkly Rep 2012; 61:289–291.
17. Randolph AG, Vaughn F, Sullivan R et al. Critically ill children during the 2009–2010 influenza pandemic in the United States. Pediatrics 2011; 128:e1450–e1458.
18. Reed C, Kallen AJ, Patton M et al. Infection with community-onset Staphylococcus aureus and influenza virus in hospitalized children. Pediatr Infect Dis J 2009; 28:572–576.
19. Liberati A, Altman DG, Tetzlaff J et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 2009; 339:b2700. doi: 10.1136/bmj.b2700.
20. National Collaborating Centre for Methods and Tools. Quality Assessment Tool for Quantitative Studies. Vol Updated 13 April. Hamilton. ON: McMaster University, 2010; 2008.
21. Thomas BH, Ciliska D, Dobbins M, Micucci S. A process for systematically reviewing the literature: providing the research evidence for public health nursing interventions. Worldviews Evid Based Nurs 2004; 1:176–184. 179p.
22. Deeks J, Dinnes J, D'Amico R, Sowden A, Sakarovitch C. Evaluating non-randomised intervention studies. Health Technol Assess 2003; 7:186.
23. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315:629–34.
24. Vittinghoff E, Glidden DV, Shiboski SC, McCulloch CE. Regression Methods in Biostatistics: Linear, Logistic, Survival, and Repeated Measures Models. New York: Springer, 2005.
25. R: A language and environment for statistical computing[computer program]. Vienna, Austria: R Foundation for Statistical Computing; 2013.
26. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327:557–560.
27. Thompson SG, Higgins JPT. How should meta-regression analyses be undertaken and interpreted? Stat Med 2002; 21:1559–1573.
28. Ahn S, Kim WY, Kim SH et al. Role of procalcitonin and C-reactive protein in differentiation of mixed bacterial infection from 2009 H1N1 viral pneumonia. Influenza Other Respi Viruses 2011; 5:398–403.
29. Bender JM, Ampofo K, Gesteland P et al. Influenza virus infection in infants less than three months of age. Pediatr Infect Dis J 2010; 29:6–9.
30. Bjarnason A, Thorleifsdottir G, Love A et al. Severity of influenza A 2009 (H1N1) pneumonia is underestimated by routine prediction rules. Results from a prospective, population-based study. PLoS ONE 2012; 7:e46816.
31. Carr SB, Adderson EE, Hakim H, Xiong X, Yan X, Caniza M. Clinical and demographic characteristics of seasonal influenza in pediatric patients with cancer. Pediatr Infect Dis J 2012; 31:e202–e207.
32. Choi SH, Hong SB, Ko GB et al. Viral infection in patients with severe pneumonia requiring intensive care unit admission. Am J Respir Crit Care Med 2012; 186:325–332.
33. Cordero E, Perez-Romero P, Moreno A et al. Pandemic influenza A(H1N1) virus infection in solid organ transplant recipients: impact of viral and non-viral co-infection. Clin Microbiol Infect 2012; 18:67–73.
34. Cuquemelle E, Soulis F, Villers D et al. Can procalcitonin help identify associated bacterial infection in patients with severe influenza pneumonia? A multicentre study. Intensive Care Med 2011; 37:796–800.
35. Dave BM. Clinical data of h1n1 infected patients, 2012–2013. Indian J Crit Care Med 2014; 18(Suppl 13):S25.
36. Falsey AR, Becker KL, Swinburne AJ et al. Bacterial complications of respiratory tract viral illness: a comprehensive evaluation. J Infect Dis 2013; 208:432–441.
37. Guervilly C, Coisel Y, Bothelo-Nevers E et al. High levels of procalcitonin and (greater-than or equal to) reactive protein during H1N1 illness. Intensive Care Med 2010; 36(Suppl 2):S138.
38. Hon KL, Leung E, Tang J et al. Premorbid factors and outcome associated with respiratory virus infections in a pediatric intensive care unit. Pediatr Pulmonol 2008; 43:275–280.
39. Ingram PR, Inglis T, Moxon D, Speers D. Procalcitonin and C-reactive protein in severe 2009 H1N1 influenza infection. Intensive Care Med 2010; 36:528–532.
40. Johansson N, Kalin M, Annika TL, Giske CG, Hedlund J. Etiology of Community-Acquired pneumonia: increased microbiological yield with new diagnostic methods. Clin Infect Dis 2010; 50:202–209.
41. Lopez-Delgado J, Rovira A, Esteve F et al. Thrombocytopenia as a mortality risk factor in acute respiratory failure in H1N1 influenza. Swiss Med Wkly 2013; 143:w13788.
42. Malato L, Llavador V, Marmier E et al. Pandemic influenza A(H1N1)2009: molecular characterisation and duration of viral shedding in intensive care patients in Bordeaux, south-west France, May 2009 to January 2010. Euro Surveill 2011; 16:19776.
43. Marcos M, Camps M, Pumarola T et al. The role of viruses in the aetiology of community-acquired pneumonia in adults. Antivir Ther 2006; 11:351–359.
44. Martin-Loeches I, Sanchez-Corral A, Diaz E et al. Community-acquired respiratory coinfection in critically iii patients with pandemic 2009 Influenza A(H1N1) Virus. Chest 2011; 139:555–562.
45. Mermond S, Berlioz-Arthaud A, Estivals M, Baumann F, Levenes H, Martin PM. Aetiology of community-acquired pneumonia in hospitalized adult patients in New Caledonia. Trop Med Int Health 2010; 15:1517–1524.
46. Nguyen T, Kyle UG, Jaimon N et al. Coinfection with Staphylococcus aureus increases risk of severe coagulopathy in critically ill children with influenza A (H1N1) virus infection. Crit Care Med 2012; 40:3246–3250.
47. Schnell D, Gits-Muselli M, Canet E et al. Burden of respiratory viruses in patients with acute respiratory failure. J Med Virol 2014; 86:1198–1202.
48. Sohn CH, Ryoo SM, Yoon JY et al. Comparison of clinical features and outcomes of hospitalized adult patients with novel influenza A (H1N1) pneumonia and other pneumonia. Acad Emerg Med 2013; 20:46–53.
49. Torres JP, Labrana Y, Ibanez C et al. Frequency and clinical outcome of respiratory viral infections and mixed viral-bacterial infections in children with cancer, fever and neutropenia. Pediatr Infect Dis J 2012; 31:889–893.
50. Van Gageldonk-Lafeber AB, Wever PC, Van DL et al. The aetiology of community-acquired pneumonia and implications for patient management. Neth J Med 2013; 71:418–425.
51. Vieira RA, Diniz EM, Vaz FA. Clinical and laboratory study of newborns with lower respiratory tract infection due to respiratory viruses. J Matern Fetal Neonatal Med 2003; 13:341–350.
52. von Baum H, Schweiger B, Welte T et al. How deadly is seasonal influenza-associated pneumonia? The German Competence Network for Community-Acquired Pneumonia. Eur Respir J 2011; 37:1151–1157.
53. Yan XX, Xu HB, Liu Y et al. Influenza a (H1n1) virus complicated with bacteria infection. Respirology 2011; 16(Suppl 2):60.
54. Zhang Q, Ji W, Guo Z, Bai Z, MacDonald NE. Risk factors and outcomes for pandemic H1N1 influenza compared with seasonal influenza in hospitalized children in China. Can J Infect Dis Med Microbiol 2012; 23:199–203.
55. Brundage JF. Interactions between influenza and bacterial respiratory pathogens: implications for pandemic preparedness. Lancet Infect Dis 2006; 6:303–312.
56. Gonzales R, Bartlett JG, Besser RE et al. Principles of appropriate antibiotic use for treatment of acute respiratory tract infections in adults: background, specific aims, and methods. Ann Emerg Med 2001; 37:690–697.
57. Metlay JP, Camargo CA, MacKenzie T et al. Cluster-randomized trial to improve antibiotic use for adults with acute respiratory infections treated in emergency departments. Ann Emerg Med 2007; 50:221–230.
58. Fiore AE, Fry A, Shay D, et al. Antiviral agents for the treatment and chemoprophylaxis of influenza—Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2011; 60:1–24.
59. Dugas AF, Monteforte B, Puri A, Awad M, Hsieh Y-H, Rothman R. ED compliance with influenza antiviral recommendations. Am J Emerg Med 2014; 32:1550–1552.
60. Dugas AF, Valsamakis A, Atreya MR et al. Clinical diagnosis of influenza in the ED. Am J Emerg Med 2015; 33:770–775.
61. Jain S, Self WH, Wunderink RG et al. Community-acquired pneumonia requiring hospitalization among U.S. adults. N Engl J Med 2015; 373:415–427.
62. McCullers JA. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Micro 2014; 12:252–262.
63. Harper SA, Bradley JS, Englund JA et al. Seasonal influenza in adults and children—diagnosis, treatment, chemoprophylaxis, and institutional outbreak management: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 2009; 48:1003–1032.
64. Klein EY, Sun L, Smith DL, Laximarayan R. The changing epidemiology of methicillin-resistant Staphylococcus aureus in the United States: A national observational study. Am J Epidemiol 2013; 177:666–674.
65. Thompson WW, Shay DK, Weintraub E et al. Influenza-associated hospitalizations in the United States. JAMA 2004; 292:1333–1340.