Viral-bacterial co-infections in the respiratory tract

Lauren O Bakaletz, Lauren O Bakaletz

Abstract

Preceding or concurrent viral respiratory tract infection can predispose to secondary bacterial co-infection throughout the airway. The mechanisms by which viruses promote these superinfections are diverse and replete. Whereas we understand much as to how viruses damage the airway and dysregulate both innate and acquired immune responses which, in turn, supports bacterial growth, adherence and invasion into normally sterile sites within the respiratory tract, new information regarding these co-infections is being gained from recent advances in microbiome research and our enhanced appreciation of the contribution of bacterial biofilms, among others. The advanced understanding obtained by continued research efforts in all aspects of viral-bacterial co-infections of the respiratory tract will allow us to devise novel approaches for disease prevention as well as to develop more effective therapeutics.

Copyright © 2016 Elsevier Ltd. All rights reserved.

References

    1. Ballinger M.N., Standiford T.J. Postinfluenza bacterial pneumonia: host defenses gone awry. J Interferon Cytokine Res. 2010;30:643–652.
    1. Rothberg M.B., Haessler S.D., Brown R.B. Complications of viral influenza. Am J Med. 2008;121:258–264.
    1. Rynda-Apple A., Robinson K.M., Alcorn J.F. Influenza and bacterial superinfection: illuminating the immunologic mechanisms of disease. Infect Immun. 2015;83:3764–3770.
    2. Discussion of immunological mechanisms of influenza-induced susceptibility to bacterial pneumonia.

    1. Falsey A.R., Becker K.L., Swinburne A.J., Nylen E.S., Formica M.A., Hennessey P.A., Criddle M.M., Peterson D.R., Baran A., Walsh E.E. Bacterial complications of respiratory tract viral illness: a comprehensive evaluation. J Infect Dis. 2013;208:432–441.
    1. Marom T., Alvarez-Fernandez P.E., Jennings K., Patel J.A., McCormick D.P., Chonmaitree T. Acute bacterial sinusitis complicating viral upper respiratory tract infection in young children. Pediatr Infect Dis J. 2014;33:803–808.
    1. Brook I. Acute sinusitis in children. Pediatr Clin North Am. 2013;60:409–424.
    1. Autio T.J., Tapiainen T., Koskenkorva T., Narkio M., Lappalainen M., Nikkari S., Hemmila H., Koskela K.A., Koskela M., Koivunen P. The role of microbes in the pathogenesis of acute rhinosinusitis in young adults. Laryngoscope. 2015;125:E1–E7.
    1. Pettigrew M.M., Gent J.F., Pyles R.B., Miller A.L., Nokso-Koivisto J., Chonmaitree T. Viral–bacterial interactions and risk of acute otitis media complicating upper respiratory tract infection. J Clin Microbiol. 2011;49:3750–3755.
    1. Marom T., Nokso-Koivisto J., Chonmaitree T. Viral–bacterial interactions in acute otitis media. Curr Allergy Asthma Rep. 2012;12:551–558.
    1. Bakaletz L.O. Immunopathogenesis of polymicrobial otitis media. J Leukoc Biol. 2010;87:213–222.
    1. Alho O.P. Nasal airflow, mucociliary clearance, and sinus functioning during viral colds: effects of allergic rhinitis and susceptibility to recurrent sinusitis. Am J Rhinol. 2004;18:349–355.
    1. Rodrigues F., Foster D., Nicoli E., Trotter C., Vipond B., Muir P., Goncalves G., Januario L., Finn A. Relationships between rhinitis symptoms, respiratory viral infections and nasopharyngeal colonization with Streptococcus pneumoniae, Haemophilus influenzae and Staphylococcus aureus in children attending daycare. Pediatr Infect Dis J. 2013;32:227–232.
    1. Thorburn K., Harigopal S., Reddy V., Taylor N., van Saene H.K. High incidence of pulmonary bacterial co-infection in children with severe respiratory syncytial virus (RSV) bronchiolitis. Thorax. 2006;61:611–615.
    1. Lehtinen P., Jartti T., Virkki R., Vuorinen T., Leinonen M., Peltola V., Ruohola A., Ruuskanen O. Bacterial coinfections in children with viral wheezing. Eur J Clin Microbiol Infect Dis. 2006;25:463–469.
    1. Asner S., Waters V., Solomon M., Yau Y., Richardson S.E., Grasemann H., Gharabaghi F., Tran D. Role of respiratory viruses in pulmonary exacerbations in children with cystic fibrosis. J Cyst Fibros. 2012;11:433–439.
    1. Wat D., Gelder C., Hibbitts S., Cafferty F., Bowler I., Pierrepoint M., Evans R., Doull I. The role of respiratory viruses in cystic fibrosis. J Cyst Fibros. 2008;7:320–328.
    1. Papi A., Bellettato C.M., Braccioni F., Romagnoli M., Casolari P., Caramori G., Fabbri L.M., Johnston S.L. Infections and airway inflammation in chronic obstructive pulmonary disease severe exacerbations. Am J Respir Crit Care Med. 2006;173:1114–1121.
    1. De Serres G., Lampron N., La Forge J., Rouleau I., Bourbeau J., Weiss K., Barret B., Boivin G. Importance of viral and bacterial infections in chronic obstructive pulmonary disease exacerbations. J Clin Virol. 2009;46:129–133.
    1. Ko F.W., Chan K.P., Hui D.S., Goddard J.R., Shaw J.G., Reid D.W., Yang I.A. Acute exacerbation of COPD. Respirology. 2016;21:1152–1165.
    1. Molyneaux P.L., Mallia P., Cox M.J., Footitt J., Willis-Owen S.A., Homola D., Trujillo-Torralbo M.B., Elkin S., Kon O.M., Cookson W.O. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2013;188:1224–1231.
    1. Bakaletz L.O. Developing animal models for polymicrobial diseases. Nat Rev Microbiol. 2004;2:552–568.
    1. Hraiech S., Papazian L., Rolain J.M., Bregeon F. Animal models of polymicrobial pneumonia. Drug Des Dev Ther. 2015;9:3279–3292.
    2. Describes animal models developed to study polymicrobial pneumonia.

    1. McCullers J.A. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol. 2014;12:252–262.
    1. Peltola V.T., Boyd K.L., McAuley J.L., Rehg J.E., McCullers J.A. Bacterial sinusitis and otitis media following influenza virus infection in ferrets. Infect Immun. 2006;74:2562–2567.
    1. Li N., Ren A., Wang X., Fan X., Zhao Y., Gao G.F., Cleary P., Wang B. Influenza viral neuraminidase primes bacterial coinfection through TGF-beta-mediated expression of host cell receptors. Proc Natl Acad Sci U S A. 2015;112:238–243.
    2. Describes mechanism by which influenza viral neuraminidase promotes increased bacterial receptor availability.

    1. Nakamura S., Davis K.M., Weiser J.N. Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J Clin Invest. 2011;121:3657–3665.
    1. Iverson A.R., Boyd K.L., McAuley J.L., Plano L.R., Hart M.E., McCullers J.A. Influenza virus primes mice for pneumonia from Staphylococcus aureus. J Infect Dis. 2011;203:880–888.
    1. Smith A.M., Adler F.R., Ribeiro R.M., Gutenkunst R.N., McAuley J.L., McCullers J.A., Perelson A.S. Kinetics of coinfection with influenza A virus and Streptococcus pneumoniae. PLoS Pathog. 2013;9:e1003238.
    1. Avadhanula V., Rodriguez C.A., Devincenzo J.P., Wang Y., Webby R.J., Ulett G.C., Adderson E.E. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J Virol. 2006;80:1629–1636.
    1. Novotny L.A., Bakaletz L.O. Intercellular adhesion molecule 1 serves as a primary cognate receptor for the Type IV pilus of nontypeable Haemophilus influenzae. Cell Microbiol. 2016;18:1043–1055.
    1. Van Ewijk B.E., Wolfs T.F., Aerts P.C., Van Kessel K.P., Fleer A., Kimpen J.L., Van der Ent C.K. RSV mediates Pseudomonas aeruginosa binding to cystic fibrosis and normal epithelial cells. Pediatr Res. 2007;61:398–403.
    1. Hament J.M., Aerts P.C., Fleer A., Van Dijk H., Harmsen T., Kimpen J.L., Wolfs T.F. Enhanced adherence of Streptococcus pneumoniae to human epithelial cells infected with respiratory syncytial virus. Pediatr Res. 2004;55:972–978.
    1. Esposito S., Zampiero A., Terranova L., Ierardi V., Ascolese B., Daleno C., Prada E., Pelucchi C., Principi N. Pneumococcal bacterial load colonization as a marker of mixed infection in children with alveolar community-acquired pneumonia and respiratory syncytial virus or rhinovirus infection. Pediatr Infect Dis J. 2013;32:1199–1204.
    1. Wolter N., Tempia S., Cohen C., Madhi S.A., Venter M., Moyes J., Walaza S., Malope-Kgokong B., Groome M., du Plessis M. High nasopharyngeal pneumococcal density, increased by viral coinfection, is associated with invasive pneumococcal pneumonia. J Infect Dis. 2014;210:1649–1657.
    1. Lijek R.S., Weiser J.N. Co-infection subverts mucosal immunity in the upper respiratory tract. Curr Opin Immunol. 2012;24:417–423.
    1. Braciale T.J., Sun J., Kim T.S. Regulating the adaptive immune response to respiratory virus infection. Nat Rev Immunol. 2012;12:295–305.
    1. Robinson K.M., Kolls J.K., Alcorn J.F. The immunology of influenza virus-associated bacterial pneumonia. Curr Opin Immunol. 2015;34:59–67.
    2. Describes mechanisms by which influenza viral infection alters the immune response to secondary bacterial infection.

    1. Kash J.C., Taubenberger J.K. The role of viral, host, and secondary bacterial factors in influenza pathogenesis. Am J Pathol. 2015;185:1528–1536.
    2. Comprehensive review of viral, host and bacterial factors that contribute to superinfection post influenza.

    1. Ghoneim H.E., Thomas P.G., McCullers J.A. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol. 2013;191:1250–1259.
    1. Sun K., Metzger D.W. Influenza infection suppresses NADPH oxidase-dependent phagocytic bacterial clearance and enhances susceptibility to secondary methicillin-resistant Staphylococcus aureus infection. J Immunol. 2014;192:3301–3307.
    1. Mehta D., Petes C., Gee K., Basta S. The role of virus infection in eeregulating the cytokine response to secondary bacterial infection. J Interferon Cytokine Res. 2015;35:925–934.
    1. Davidson S., Maini M.K., Wack A. Disease-promoting effects of type I interferons in viral, bacterial, and coinfections. J Interferon Cytokine Res. 2015;35:252–264.
    1. McGillivary G., Mason K.M., Jurcisek J.A., Peeples M.E., Bakaletz L.O. Respiratory syncytial virus-induced dysregulation of expression of a mucosal beta-defensin augments colonization of the upper airway by non-typeable Haemophilus influenzae. Cell Microbiol. 2009;11:1399–1408.
    1. Murray J.F. Epidemiology of human immunodeficiency virus-associated pulmonary disease. Clin Chest Med. 2013;34:165–179.
    1. Vittor A.Y., Garland J.M., Gilman R.H. Molecular diagnosis of TB in the HIV positive population. Ann Glob Health. 2014;80:476–485.
    1. Pawlowski A., Jansson M., Skold M., Rottenberg M.E., Kallenius G. Tuberculosis and HIV co-infection. PLoS Pathog. 2012;8:e1002464.
    1. Al-Omari A., Aljamaan F., Alhazzani W., Salih S., Arabi Y. Cytomegalovirus infection in immunocompetent critically ill adults: literature review. Ann Intensive Care. 2016;6:110.
    1. Rota P.A., Moss W.J., Takeda M., de Swart R.L., Thompson K.M., Goodson J.L. Measles. Nat Rev Dis Primers. 2016;2:16049.
    1. Chattoraj S.S., Ganesan S., Jones A.M., Helm J.M., Comstock A.T., Bright-Thomas R., LiPuma J.J., Hershenson M.B., Sajjan U.S. Rhinovirus infection liberates planktonic bacteria from biofilm and increases chemokine responses in cystic fibrosis airway epithelial cells. Thorax. 2011;66:333–339.
    1. Chao Y., Marks L.R., Pettigrew M.M., Hakansson A.P. Streptococcus pneumoniae biofilm formation and dispersion during colonization and disease. Front Cell Infect Microbiol. 2014;4:194.
    2. Characterizes virus-mediated release of bacteria from an established biofilm and resultant increased virulence phenotype.

    1. Pettigrew M.M., Marks L.R., Kong Y., Gent J.F., Roche-Hakansson H., Hakansson A.P. Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection. Infect Immun. 2014;82:4607–4619.
    1. Hennigar S.R., McClung J.P. Nutritional immunity: starving pathogens of trace minerals. Am J Lifestyle Med. 2016;10:170–173.
    1. Siegel S.J., Roche A.M., Weiser J.N. Influenza promotes pneumococcal growth during coinfection by providing host sialylated substrates as a nutrient source. Cell Host Microbe. 2014;16:55–67.
    1. Hendricks M.R., Lashua L.P., Fischer D.K., Flitter B.A., Eichinger K.M., Durbin J.E., Sarkar S.N., Coyne C.B., Empey K.M., Bomberger J.M. Respiratory syncytial virus infection enhances Pseudomonas aeruginosa biofilm growth through dysregulation of nutritional immunity. Proc Natl Acad Sci U S A. 2016;113:1642–1647.
    2. Novel observation as to how RSV promotes biofilm formation by a predominant respiratory tract pathogen due to increased release of transferrin.

    1. Lynch S.V. Viruses and microbiome alterations. Ann Am Thorac Soc. 2014;11(Suppl. 1):S57–S60.
    1. Pettigrew M.M., Gent J.F., Revai K., Patel J.A., Chonmaitree T. Microbial interactions during upper respiratory tract infections. Emerg Infect Dis. 2008;14:1584–1591.
    1. Ruohola A., Pettigrew M.M., Lindholm L., Jalava J., Raisanen K.S., Vainionpaa R., Waris M., Tahtinen P.A., Laine M.K., Lahti E. Bacterial and viral interactions within the nasopharynx contribute to the risk of acute otitis media. J Infect. 2013;66:247–254.
    1. Brealey J.C., Sly P.D., Young P.R., Chappell K.J. Viral bacterial co-infection of the respiratory tract during early childhood. FEMS Microbiol Lett. 2015:362.
    2. Current view of the clinical significance of viral–bacterial co-infections in young children.

    1. Bellinghausen C., Gulraiz F., Heinzmann A.C., Dentener M.A., Savelkoul P.H., Wouters E.F., Rohde G.G., Stassen F.R. Exposure to common respiratory bacteria alters the airway epithelial response to subsequent viral infection. Respir Res. 2016;17:68.
    1. Nguyen D.T., Louwen R., Elberse K., van Amerongen G., Yuksel S., Luijendijk A., Osterhaus A.D., Duprex W.P., de Swart R.L. Streptococcus pneumoniae enhances human respiratory syncytial virus infection in vitro and in vivo. PLoS ONE. 2015;10:e0127098.
    1. Gulraiz F., Bellinghausen C., Bruggeman C.A., Stassen F.R. Haemophilus influenzae increases the susceptibility and inflammatory response of airway epithelial cells to viral infections. FASEB J. 2015;29:849–858.
    1. Norhayati M.N., Ho J.J., Azman M.Y. Influenza vaccines for preventing acute otitis media in infants and children. Cochrane Database Syst Rev. 2015 CD010089.
    1. Deng J.C. Viral–bacterial interactions-therapeutic implications. Influenza Other Respir Viruses. 2013;7(Suppl. 3):24–35.
    1. Jamieson A.M., Pasman L., Yu S., Gamradt P., Homer R.J., Decker T., Medzhitov R. Role of tissue protection in lethal respiratory viral–bacterial coinfection. Science. 2013;340:1230–1234.
    1. Damjanovic D., Lai R., Jeyanathan M., Hogaboam C.M., Xing Z. Marked improvement of severe lung immunopathology by influenza-associated pneumococcal superinfection requires the control of both bacterial replication and host immune responses. Am J Pathol. 2013;183:868–880.

Source: PubMed

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