Viral–bacterial co-infections in the respiratory tract

Current Opinion in Microbiology

Volumn 35, Issue , 2017, Pages 30-35

  Bakaletz, Lauren O ^a  

^a THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZITHROMYCIN; DEXAMETHASONE;

ADAPTIVE IMMUNITY; ANTIBIOTIC THERAPY; ANTIVIRAL THERAPY; BACTERIAL COLONIZATION; BACTERIAL SUPERINFECTION; BACTERIUM ADHERENCE; BIOFILM; DISEASE PREDISPOSITION; HUMAN; IMMUNOREGULATION; INNATE IMMUNITY; MIXED INFECTION; NONHUMAN; PLANKTON; RESPIRATORY SYSTEM; RESPIRATORY TRACT INFECTION; REVIEW; SUPERINFECTION; ANIMAL; BACTERIAL INFECTION; COMPLICATION; IMMUNOLOGY; INFLUENZA; MICROBIOLOGY; MICROFLORA; MOUSE; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; VIROLOGY; VIRUS INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; BACTERIAL INFECTIONS; COINFECTION; HUMANS; IMMUNITY, INNATE; INFLUENZA, HUMAN; MICE; MICROBIOTA; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY SYSTEM; RESPIRATORY TRACT INFECTIONS; VIRUS DISEASES;

EID: 85001946084     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2016.11.003     Document Type: Review

References (65)

1. 1 Ballinger, M.N., Standiford, T.J., Postinfluenza bacterial pneumonia: host defenses gone awry. J Interferon Cytokine Res 30 (2010), 643–652.
2. 2 Rothberg, M.B., Haessler, S.D., Brown, R.B., Complications of viral influenza. Am J Med 121 (2008), 258–264.
3. 3• Rynda-Apple, A., Robinson, K.M., Alcorn, J.F., Influenza and bacterial superinfection: illuminating the immunologic mechanisms of disease. Infect Immun 83 (2015), 3764–3770 Discussion of immunological mechanisms of influenza-induced susceptibility to bacterial pneumonia.
4. 4 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 208 (2013), 432–441.
5. 5 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 33 (2014), 803–808.
6. 6 Brook, I., Acute sinusitis in children. Pediatr Clin North Am 60 (2013), 409–424.
7. 7 Autio, T.J., Tapiainen, T., Koskenkorva, T., Narkio, M., Lappalainen, M., Nikkari, S., Hemmila, H., Koskela, K.A., Koskela, M., Koivunen, P., et al. The role of microbes in the pathogenesis of acute rhinosinusitis in young adults. Laryngoscope 125 (2015), E1–E7.
8. 8 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 49 (2011), 3750–3755.
9. 9 Marom, T., Nokso-Koivisto, J., Chonmaitree, T., Viral–bacterial interactions in acute otitis media. Curr Allergy Asthma Rep 12 (2012), 551–558.
10. 10 Bakaletz, L.O., Immunopathogenesis of polymicrobial otitis media. J Leukoc Biol 87 (2010), 213–222.
11. 11 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 18 (2004), 349–355.
12. 12 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 32 (2013), 227–232.
13. 13 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 61 (2006), 611–615.
14. 14 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 25 (2006), 463–469.
15. 15 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 11 (2012), 433–439.
16. 16 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 7 (2008), 320–328.
17. 17 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 173 (2006), 1114–1121.
18. 18 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 46 (2009), 129–133.
19. 19 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 21 (2016), 1152–1165.
20. 20 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., et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 188 (2013), 1224–1231.
21. 21 Bakaletz, L.O., Developing animal models for polymicrobial diseases. Nat Rev Microbiol 2 (2004), 552–568.
22. 22• Hraiech, S., Papazian, L., Rolain, J.M., Bregeon, F., Animal models of polymicrobial pneumonia. Drug Des Dev Ther 9 (2015), 3279–3292 Describes animal models developed to study polymicrobial pneumonia.
23. 23 McCullers, J.A., The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol 12 (2014), 252–262.
24. 24 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 74 (2006), 2562–2567.
25. 25•• 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 112 (2015), 238–243 Describes mechanism by which influenza viral neuraminidase promotes increased bacterial receptor availability.
26. 26 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 121 (2011), 3657–3665.
27. 27 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 203 (2011), 880–888.
28. 28 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, 9, 2013, e1003238.
29. 29 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 80 (2006), 1629–1636.
30. 30 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 18 (2016), 1043–1055.
31. 31 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 61 (2007), 398–403.
32. 32 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 55 (2004), 972–978.
33. 33 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 32 (2013), 1199–1204.
34. 34 Wolter, N., Tempia, S., Cohen, C., Madhi, S.A., Venter, M., Moyes, J., Walaza, S., Malope-Kgokong, B., Groome, M., du Plessis, M., et al. High nasopharyngeal pneumococcal density, increased by viral coinfection, is associated with invasive pneumococcal pneumonia. J Infect Dis 210 (2014), 1649–1657.
35. 35 Lijek, R.S., Weiser, J.N., Co-infection subverts mucosal immunity in the upper respiratory tract. Curr Opin Immunol 24 (2012), 417–423.
36. 36 Braciale, T.J., Sun, J., Kim, T.S., Regulating the adaptive immune response to respiratory virus infection. Nat Rev Immunol 12 (2012), 295–305.
37. 37•• Robinson, K.M., Kolls, J.K., Alcorn, J.F., The immunology of influenza virus-associated bacterial pneumonia. Curr Opin Immunol 34 (2015), 59–67 Describes mechanisms by which influenza viral infection alters the immune response to secondary bacterial infection.
38. 38• Kash, J.C., Taubenberger, J.K., The role of viral, host, and secondary bacterial factors in influenza pathogenesis. Am J Pathol 185 (2015), 1528–1536 Comprehensive review of viral, host and bacterial factors that contribute to superinfection post influenza.
39. 39 Ghoneim, H.E., Thomas, P.G., McCullers, J.A., Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol 191 (2013), 1250–1259.
40. 40 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 192 (2014), 3301–3307.
41. 41 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 35 (2015), 925–934.
42. 42 Davidson, S., Maini, M.K., Wack, A., Disease-promoting effects of type I interferons in viral, bacterial, and coinfections. J Interferon Cytokine Res 35 (2015), 252–264.
43. 43 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 11 (2009), 1399–1408.
44. 44 Murray, J.F., Epidemiology of human immunodeficiency virus-associated pulmonary disease. Clin Chest Med 34 (2013), 165–179.
45. 45 Vittor, A.Y., Garland, J.M., Gilman, R.H., Molecular diagnosis of TB in the HIV positive population. Ann Glob Health 80 (2014), 476–485.
46. 46 Pawlowski, A., Jansson, M., Skold, M., Rottenberg, M.E., Kallenius, G., Tuberculosis and HIV co-infection. PLoS Pathog, 8, 2012, e1002464.
47. 47 Al-Omari, A., Aljamaan, F., Alhazzani, W., Salih, S., Arabi, Y., Cytomegalovirus infection in immunocompetent critically ill adults: literature review. Ann Intensive Care, 6, 2016, 110.
48. 48 Rota, P.A., Moss, W.J., Takeda, M., de Swart, R.L., Thompson, K.M., Goodson, J.L., Measles. Nat Rev Dis Primers, 2, 2016, 16049.
49. 49 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 66 (2011), 333–339.
50. 50•• 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, 4, 2014, 194 Characterizes virus-mediated release of bacteria from an established biofilm and resultant increased virulence phenotype.
51. 51 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 82 (2014), 4607–4619.
52. 52 Hennigar, S.R., McClung, J.P., Nutritional immunity: starving pathogens of trace minerals. Am J Lifestyle Med 10 (2016), 170–173.
53. 53 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 16 (2014), 55–67.
54. 54•• 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 113 (2016), 1642–1647 Novel observation as to how RSV promotes biofilm formation by a predominant respiratory tract pathogen due to increased release of transferrin.
55. 55 Lynch, S.V., Viruses and microbiome alterations. Ann Am Thorac Soc 11:Suppl. 1 (2014), S57–S60.
56. 56 Pettigrew, M.M., Gent, J.F., Revai, K., Patel, J.A., Chonmaitree, T., Microbial interactions during upper respiratory tract infections. Emerg Infect Dis 14 (2008), 1584–1591.
57. 57 Ruohola, A., Pettigrew, M.M., Lindholm, L., Jalava, J., Raisanen, K.S., Vainionpaa, R., Waris, M., Tahtinen, P.A., Laine, M.K., Lahti, E., et al. Bacterial and viral interactions within the nasopharynx contribute to the risk of acute otitis media. J Infect 66 (2013), 247–254.
58. 58•• 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 Current view of the clinical significance of viral–bacterial co-infections in young children.
59. 59 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, 17, 2016, 68.
60. 60 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, 10, 2015, e0127098.
61. 61 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 29 (2015), 849–858.
62. 62 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.
63. 63 Deng, J.C., Viral–bacterial interactions-therapeutic implications. Influenza Other Respir Viruses 7:Suppl. 3 (2013), 24–35.
64. 64 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 340 (2013), 1230–1234.
65. 65 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 183 (2013), 868–880.