Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia

Frontiers in Immunology

Volumn 9, Issue NOV, 2018, Pages

  Hanada, Shigeo ^a,b   Pirzadeh, Mina ^a,c   Carver, Kyle Y ^a,c   Deng, Jane C ^a,c  

^a UNIVERSITY OF MICHIGAN   (United States)

^b TORANOMON HOSPITAL   (Japan)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

bacterial pneumonia; gut microbiome; host microbe interaction; influenza; respiratory viral infection; viral bacterial interaction

Indexed keywords

INTERLEUKIN 17; LIPOTEICHOIC ACID; RNA 16S; TOLL LIKE RECEPTOR; TRANSCRIPTOME; TUMOR NECROSIS FACTOR;

ACTINOBACTERIA; ANTIBODY PRODUCTION; AUTOIMMUNITY; BACTERIAL PNEUMONIA; BACTEROIDETES; CELL MIGRATION; DISEASE SEVERITY; DYSBIOSIS; ECOLOGICAL NICHE; FIRMICUTES; GASTROINTESTINAL TRACT; GENE EXPRESSION; HOST RESISTANCE; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLAMMATION; INTESTINE FLORA; INTESTINE MUCOSA; LONGITUDINAL STUDY; MESENTERIC LYMPH NODE LYMPHOCYTE; METAGENOMICS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MICROBIAL COMMUNITY; MICROBIAL GROWTH; MICROBIOME; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PROTEOBACTERIA; RESPIRATORY SYSTEM; REVIEW; RISK FACTOR; STREPTOCOCCUS PNEUMONIAE; VIRAL RESPIRATORY TRACT INFECTION; COMPLICATION; IMMUNOLOGY; INNATE IMMUNITY; MICROFLORA; MIXED INFECTION; RESPIRATORY TRACT INFECTION; VIRUS INFECTION;

COINFECTION; DYSBIOSIS; GASTROINTESTINAL MICROBIOME; HOST MICROBIAL INTERACTIONS; HUMANS; IMMUNITY, INNATE; MICROBIOTA; PNEUMONIA, BACTERIAL; RESPIRATORY TRACT INFECTIONS; VIRUS DISEASES;

EID: 85057424206     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2018.02640     Document Type: Review

References (144)

1. Brundage JF. Interactions between influenza and bacterial respiratory pathogens: Implications for pandemic preparedness. Lancet Infect Dis. (2006) 6:303-12. doi: 10.1016/S1473-3099(06)70466-2 PubMed Abstract | CrossRef Full Text | Google Scholar
2. Chien Y-W, Klugman KP, Morens DM. Bacterial pathogens and death during the 1918 influenza pandemic. N Engl J Med. (2009) 361:2582-3. doi: 10.1056/NEJMc0908216 PubMed Abstract | CrossRef Full Text | Google Scholar
3. Johnson NPAS, Mueller J. Updating the accounts: Global mortality of the 1918-1920 "Spanish" influenza pandemic. Bull Hist Med. (2002) 76:105-15. doi: 10.1353/bhm.2002.0022 PubMed Abstract | CrossRef Full Text | Google Scholar
4. McCullers JA. Insights into the interaction between influenza virus and pneumococcus. Clin Microbiol Rev. (2006) 19:571-82. doi: 10.1128/CMR.00058-05 PubMed Abstract | CrossRef Full Text | Google Scholar
5. Morens DM, Fauci AS. The 1918 influenza pandemic: Insights for the 21st century. J Infect Dis. (2007) 195:1018-28. doi: 10.1086/511989 PubMed Abstract | CrossRef Full Text | Google Scholar
6. 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) 198:962-70. doi: 10.1086/591708 PubMed Abstract | CrossRef Full Text | Google Scholar
7. Taubenberger JK. The origin and virulence of the 1918 "Spanish" influenza virus. Proc Am Philos Soc. (2006) 150:86-112. Available online at: Http://www.jstor.org/stable/4598974 PubMed Abstract | Google Scholar
8. Bisno AL, Griffin JP, Van Epps KA, Niell HB, Rytel MW. Pneumonia and Hong Kong influenza: A prospective study of the 1968-1969 epidemic. Am J Med Sci. (1971) 261:251-63. PubMed Abstract | Google Scholar
9. Hers JF, Masurel N, Mulder J. Bacteriology and histopathology of the respiratory tract and lungs in fatal Asian influenza. Lancet (1958) 2:1141-3. PubMed Abstract | Google Scholar
10. Oswald NC, Shooter RA, Curwen MP. Pneumonia complicating Asian influenza. Br Med J. (1958) 2:1305-11. PubMed Abstract | Google Scholar
11. Cillóniz C, Ewig S, Menéndez R, Ferrer M, Polverino E, Reyes S, et al. Bacterial co-infection with H1N1 infection in patients admitted with community acquired pneumonia. J Infect. (2012) 65:223-30. doi: 10.1016/j.jinf.2012.04.009 PubMed Abstract | CrossRef Full Text | Google Scholar
12. Gill JR, Sheng Z-M, Ely SF, Guinee DG, Beasley MB, Suh J, et al. Pulmonary pathologic findings of fatal 2009 pandemic influenza A/H1N1 viral infections. Arch Pathol Lab Med. (2010) 134:235-43. doi: 10.1043/1543-2165-134.2.235 PubMed Abstract | CrossRef Full Text | Google Scholar
13. Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, et al. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med. (2009) 361:1935-44. doi: 10.1056/NEJMoa0906695 PubMed Abstract | CrossRef Full Text | Google Scholar
14. Kumar A, Zarychanski R, Pinto R, Cook DJ, Marshall J, Lacroix J, et al. Critically ill patients with 2009 influenza A(H1N1) infection in Canada. JAMA (2009) 302:1872-9. doi: 10.1001/jama.2009.1496 PubMed Abstract | CrossRef Full Text | Google Scholar
15. Martín-Loeches I, Sanchez-Corral A, Diaz E, Granada RM, Zaragoza R, Villavicencio C, et al. Community-acquired respiratory coinfection in critically ill patients with pandemic 2009 influenza A(H1N1) virus. Chest (2011) 139:555-62. doi: 10.1378/chest.10-1396 PubMed Abstract | CrossRef Full Text | Google Scholar
16. Palacios G, Hornig M, Cisterna D, Savji N, Bussetti AV, Kapoor V, et al. Streptococcus pneumoniae coinfection is correlated with the severity of H1N1 pandemic influenza. PLoS ONE (2009) 4:e8540. doi: 10.1371/journal.pone.0008540 PubMed Abstract | CrossRef Full Text | Google Scholar
17. Shieh W-J, Blau DM, Denison AM, Deleon-Carnes M, Adem P, Bhatnagar J, et al. 2009 pandemic influenza A (H1N1): Pathology and pathogenesis of 100 fatal cases in the United States. Am J Pathol. (2010) 177:166-75. doi: 10.2353/ajpath.2010.100115 PubMed Abstract | CrossRef Full Text | Google Scholar
18. Domínguez-Cherit G, Lapinsky SE, Macias AE, Pinto R, Espinosa-Perez L, de la Torre A, et al. Critically Ill patients with 2009 influenza A(H1N1) in Mexico. JAMA (2009) 302:1880-7. doi: 10.1001/jama.2009.1536 PubMed Abstract | CrossRef Full Text | Google Scholar
19. Honda K, Littman DR. The microbiome in infectious disease and inflammation. Annu Rev Immunol. (2012) 30:759-95. doi: 10.1146/annurev-immunol-020711-074937 PubMed Abstract | CrossRef Full Text | Google Scholar
20. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature (2012) 486:207-14. doi: 10.1038/nature11234 CrossRef Full Text | Google Scholar
21. Rosshart SP, Vassallo BG, Angeletti D, Hutchinson DS, Morgan AP, Takeda K, et al. Wild mouse gut microbiota promotes host fitness and improves disease resistance. Cell (2017) 171:1015-28.e13. doi: 10.1016/j.cell.2017.09.016 PubMed Abstract | CrossRef Full Text | Google Scholar
22. Beaman BL, Gershwin ME, Scates SS, Ohsugi Y. Immunobiology of germfree mice infected with Nocardia asteroides. Infect Immun (1980) 29:733-43. PubMed Abstract | Google Scholar
23. Inagaki H, Suzuki T, Nomoto K, Yoshikai Y. Increased susceptibility to primary infection with Listeria monocytogenes in germfree mice may be due to lack of accumulation of L-selectin+ CD44+ T cells in sites of inflammation. Infect Immun. (1996) 64:3280-7. PubMed Abstract | Google Scholar
24. Oliveira MR, Tafuri WL, Afonso LCC, Oliveira MAP, Nicoli JR, Vieira EC, et al. Germ-free mice produce high levels of interferon-gamma in response to infection with Leishmania major but fail to heal lesions. Parasitology (2005) 131:477-88. doi: 10.1017/S0031182005008073 PubMed Abstract | CrossRef Full Text | Google Scholar
25. Osborne LC, Monticelli LA, Nice TJ, Sutherland TE, Siracusa MC, Hepworth MR, et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science (2014) 345:578-82. doi: 10.1126/science.1256942 PubMed Abstract | CrossRef Full Text | Google Scholar
26. Splichal I, Rychlik I, Gregorova D, Sebkova A, Trebichavsky I, Splichalova A, et al. Susceptibility of germ-free pigs to challenge with protease mutants of Salmonella enterica serovar Typhimurium. Immunobiology (2007) 212:577-82. doi: 10.1016/j.imbio.2007.05.001 PubMed Abstract | CrossRef Full Text | Google Scholar
27. Tanaka K, Sawamura S, Satoh T, Kobayashi K, Noda S. Role of the indigenous microbiota in maintaining the virus-specific CD8 memory T cells in the lung of mice infected with murine cytomegalovirus. J Immunol. (2007) 178:5209-16. doi: 10.4049/jimmunol.178.8.5209 PubMed Abstract | CrossRef Full Text | Google Scholar
28. Reese TA, Bi K, Kambal A, Filali-Mouhim A, Beura LK, Bürger MC, et al. Sequential infection with common pathogens promotes human-like immune gene expression and altered vaccine response. Cell Host Microbe (2016) 19:713-9. doi: 10.1016/j.chom.2016.04.003 PubMed Abstract | CrossRef Full Text | Google Scholar
29. Beura LK, Hamilton SE, Bi K, Schenkel JM, Odumade OA, Casey KA, et al. Normalizing the environment recapitulates adult human immune traits in laboratory mice. Nature (2016) 532:512-6. doi: 10.1038/nature17655 PubMed Abstract | CrossRef Full Text | Google Scholar
30. Cummings JH. Fermentation in the human large intestine: Evidence and implications for health. Lancet (1983) 1:1206-9. PubMed Abstract | Google Scholar
31. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly-Y M, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science (2013) 341:569-73. doi: 10.1126/science.1241165 PubMed Abstract | CrossRef Full Text | Google Scholar
32. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature (2013) 504:451-5. doi: 10.1038/nature12726 PubMed Abstract | CrossRef Full Text | Google Scholar
33. Goverse G, Molenaar R, Macia L, Tan J, Erkelens MN, Konijn T, et al. Diet-derived short chain fatty acids stimulate intestinal epithelial cells to induce mucosal tolerogenic dendritic cells. J Immunol. (2017) 198:2172-81. doi: 10.4049/jimmunol.1600165 CrossRef Full Text | Google Scholar
34. Mariño E, Richards JL, McLeod KH, Stanley D, Yap YA, Knight J, et al. Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes. Nat Immunol. (2017) 18:552-562. doi: 10.1038/ni.3713 CrossRef Full Text | Google Scholar
35. Haase S, Haghikia A, Wilck N, Müller DN, Linker RA. Impacts of microbiome metabolites on immune regulation and autoimmunity. Immunology (2018) 154:230-8. doi: 10.1111/imm.12933 PubMed Abstract | CrossRef Full Text | Google Scholar
36. Kalina U, Koyama N, Hosoda T, Nuernberger H, Sato K, Hoelzer D, et al. Enhanced production of IL-18 in butyrate-treated intestinal epithelium by stimulation of the proximal promoter region. Eur J Immunol. (2002) 32:2635-43. doi: 10.1002/1521-4141(200209)32:9 < 2635::AID-IMMU2635>3.0.CO;2-N PubMed Abstract | CrossRef Full Text | Google Scholar
37. Schauber J, Svanholm C, Termén S, Iffland K, Menzel T, Scheppach W, et al. Expression of the cathelicidin LL-37 is modulated by short chain fatty acids in colonocytes: Relevance of signalling pathways. Gut (2003) 52:735-41. doi: 10.1136/gut.52.5.735 PubMed Abstract | CrossRef Full Text | Google Scholar
38. Schauber J, Iffland K, Frisch S, Kudlich T, Schmausser B, Eck M, et al. Histone-deacetylase inhibitors induce the cathelicidin LL-37 in gastrointestinal cells. Mol Immunol. (2004) 41:847-54. doi: 10.1016/j.molimm.2004.05.005 PubMed Abstract | CrossRef Full Text | Google Scholar
39. Klaasen HL, Van der Heijden PJ, Stok W, Poelma FG, Koopman JP, Van den Brink ME, et al. Apathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune system of mice. Infect Immun. (1993) 61:303-6. PubMed Abstract | Google Scholar
40. Talham GL, Jiang HQ, Bos NA, Cebra JJ. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun. (1999) 67:1992-2000. PubMed Abstract | Google Scholar
41. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell (2009) 139:485-98. doi: 10.1016/j.cell.2009.09.033 PubMed Abstract | CrossRef Full Text | Google Scholar
42. Gaboriau-Routhiau V, Rakotobe S, Lécuyer E, Mulder I, Lan A, Bridonneau C, et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity (2009) 31:677-89. doi: 10.1016/j.immuni.2009.08.020 PubMed Abstract | CrossRef Full Text | Google Scholar
43. Wang J, Li F, Wei H, Lian Z-X, Sun R, Tian Z. Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation. J Exp Med. (2014) 211:2397-410. doi: 10.1084/jem.20140625 PubMed Abstract | CrossRef Full Text | Google Scholar
44. Deriu E, Boxx GM, He X, Pan C, Benavidez SD, Cen L. Influenza Virus Affects Intestinal Microbiota and Secondary Salmonella Infection in the Gut through Type I Interferons. PLoS Pathog. (2016) 12:e1005572. doi: 10.1371/journal.ppat.1005572 PubMed Abstract | CrossRef Full Text | Google Scholar
45. Bartley JM, Zhou X, Kuchel GA, Weinstock GM, Haynes L. Impact of age, caloric restriction, and influenza infection on mouse gut microbiome: An exploratory study of the role of age-related microbiome changes on influenza responses. Front Immunol. (2017) 8:1164. doi: 10.3389/fimmu.2017.01164 PubMed Abstract | CrossRef Full Text | Google Scholar
46. Yildiz S, Mazel-Sanchez B, Kandasamy M, Manicassamy B, Schmolke M. Influenza A virus infection impacts systemic microbiota dynamics and causes quantitative enteric dysbiosis. Microbiome (2018) 6:9. doi: 10.1186/s40168-017-0386-z PubMed Abstract | CrossRef Full Text | Google Scholar
47. Groves HT, Cuthbertson L, James P, Moffatt MF, Cox MJ, Tregoning JS. Respiratory disease following viral lung infection alters the murine gut microbiota. Front Immunol. (2018) 9:182. doi: 10.3389/fimmu.2018.00182 PubMed Abstract | CrossRef Full Text | Google Scholar
48. Wu J, Meng Z, Jiang M, Zhang E, Trippler M, Broering R, et al. Toll-like receptor-induced innate immune responses in non-parenchymal liver cells are cell type-specific. Immunology (2010) 129:363-74. doi: 10.1111/j.1365-2567.2009.03179.x PubMed Abstract | CrossRef Full Text | Google Scholar
49. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: Human gut microbes associated with obesity. Nature (2006) 444:1022-3. doi: 10.1038/4441022a PubMed Abstract | CrossRef Full Text | Google Scholar
50. Ruiz A, Cerdó T, Jáuregui R, Pieper DH, Marcos A, Clemente A, et al. One-year calorie restriction impacts gut microbial composition but not its metabolic performance in obese adolescents. Environ Microbiol. (2017) 19:1536-51. doi: 10.1111/1462-2920.13713 CrossRef Full Text | Google Scholar
51. Ichinohe T, Pang IK, Kumamoto Y, Peaper DR, Ho JH, Murray TS, et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci USA. (2011) 108:5354-9. doi: 10.1073/pnas.1019378108 PubMed Abstract | CrossRef Full Text | Google Scholar
52. Abt MC, Osborne LC, Monticelli LA, Doering TA, Alenghat T, Sonnenberg GF, et al. Commensal bacteria calibrate the activation threshold of innate antiviral immunity. Immunity (2012) 37:158-70. doi: 10.1016/j.immuni.2012.04.011 PubMed Abstract | CrossRef Full Text | Google Scholar
53. Oh JZ, Ravindran R, Chassaing B, Carvalho FA, Maddur MS, Bower M, et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity (2014) 41:478-92. doi: 10.1016/j.immuni.2014.08.009 PubMed Abstract | CrossRef Full Text | Google Scholar
54. Gauguet S, D'Ortona S, Ahnger-Pier K, Duan B, Surana NK, Lu R, et al. Intestinal Microbiota of Mice Influences Resistance to Staphylococcus aureus Pneumonia. Infect Immun. (2015) 83:4003-14. doi: 10.1128/IAI.00037-15 PubMed Abstract | CrossRef Full Text | Google Scholar
55. Schuijt TJ, Lankelma JM, Scicluna BP, de Sousa e Melo F, Roelofs JJTH, de Boer JD, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut (2016) 65:575-83. doi: 10.1136/gutjnl-2015-309728 PubMed Abstract | CrossRef Full Text | Google Scholar
56. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med. (2010) 16:228-31. doi: 10.1038/nm.2087 PubMed Abstract | CrossRef Full Text | Google Scholar
57. de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, et al. Probiotic bacteria reduced duration and severity but not the incidence of common cold episodes in a double blind, randomized, controlled trial. Vaccine (2006) 24:6670-4. doi: 10.1016/j.vaccine.2006.05.048 CrossRef Full Text | Google Scholar
58. Vouloumanou EK, Makris GC, Karageorgopoulos DE, Falagas ME. Probiotics for the prevention of respiratory tract infections: A systematic review. Int J Antimicrob Agents (2009) 34:197.e1-10. doi: 10.1016/j.ijantimicag.2008.11.005 PubMed Abstract | CrossRef Full Text | Google Scholar
59. Steed AL, Christophi GP, Kaiko GE, Sun L, Goodwin VM, Jain U, et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science (2017) 357:498-502. doi: 10.1126/science.aam5336 PubMed Abstract | CrossRef Full Text | Google Scholar
60. Maeda N, Nakamura R, Hirose Y, Murosaki S, Yamamoto Y, Kase T, et al. Oral administration of heat-killed Lactobacillus plantarum L-137 enhances protection against influenza virus infection by stimulation of type I interferon production in mice. Int Immunopharmacol. (2009) 9:1122-5. doi: 10.1016/j.intimp.2009.04.015 PubMed Abstract | CrossRef Full Text | Google Scholar
61. Hori T, Kiyoshima J, Shida K, Yasui H. Augmentation of cellular immunity and reduction of influenza virus titer in aged mice fed Lactobacillus casei strain Shirota. Clin Diagn Lab Immunol. (2002) 9:105-8. doi: 10.1128/CDLI.9.1.105-108.2002 PubMed Abstract | CrossRef Full Text | Google Scholar
62. Wu S, Jiang Z-Y, Sun Y-F, Yu B, Chen J, Dai C-Q, et al. Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza A virus infection. Curr Microbiol. (2013) 67:414-22. doi: 10.1007/s00284-013-0380-z PubMed Abstract | CrossRef Full Text | Google Scholar
63. Trompette A, Gollwitzer ES, Pattaroni C, Lopez-Mejia IC, Riva E, Pernot J, et al. Dietary fiber confers protection against flu by shaping Ly6c- patrolling monocyte hematopoiesis and CD8+ T cell metabolism. Immunity (2018) 48:992-1005.e8. doi: 10.1016/j.immuni.2018.04.022 PubMed Abstract | CrossRef Full Text | Google Scholar
64. Sun K, Metzger DW. Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med. (2008) 14:558-64. doi: 10.1038/nm1765 PubMed Abstract | CrossRef Full Text | Google Scholar
65. Shahangian A, Chow EK, Tian X, Kang JR, Ghaffari A, Liu SY, et al. Type I IFNs mediate development of postinfluenza bacterial pneumonia in mice. J Clin Invest. (2009) 119:1910-20. doi: 10.1172/JCI35412 PubMed Abstract | CrossRef Full Text | Google Scholar
66. Brown RL, Sequeira RP, Clarke TB. The microbiota protects against respiratory infection via GM-CSF signaling. Nat Commun. (2017) 8:1512. doi: 10.1038/s41467-017-01803-x PubMed Abstract | CrossRef Full Text | Google Scholar
67. Frank DN, Feazel LM, Bessesen MT, Price CS, Janoff EN, Pace NR. The human nasal microbiota and Staphylococcus aureus carriage. PLoS ONE (2010) 5:e10598. doi: 10.1371/journal.pone.0010598 PubMed Abstract | CrossRef Full Text | Google Scholar
68. Lemon KP, Klepac-Ceraj V, Schiffer HK, Brodie EL, Lynch SV, Kolter R. Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. MBio (2010) 1:e00129-10. doi: 10.1128/mBio.00129-10 PubMed Abstract | CrossRef Full Text | Google Scholar
69. Bassis CM, Tang AL, Young VB, Pynnonen MA. The nasal cavity microbiota of healthy adults. Microbiome (2014) 2:27. doi: 10.1186/2049-2618-2-27 PubMed Abstract | CrossRef Full Text | Google Scholar
70. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med. (2011) 184:957-63. doi: 10.1164/rccm.201104-0655OC PubMed Abstract | CrossRef Full Text | Google Scholar
71. Yi H, Yong D, Lee K, Cho Y-J, Chun J. Profiling bacterial community in upper respiratory tracts. BMC Infect Dis. (2014) 14:583. doi: 10.1186/s12879-014-0583-3 PubMed Abstract | CrossRef Full Text | Google Scholar
72. Ling Z, Liu X, Luo Y, Yuan L, Nelson KE, Wang Y, et al. Pyrosequencing analysis of the human microbiota of healthy Chinese undergraduates. BMC Genomics (2013) 14:390. doi: 10.1186/1471-2164-14-390 PubMed Abstract | CrossRef Full Text | Google Scholar
73. Allen EK, Koeppel AF, Hendley JO, Turner SD, Winther B, Sale MM. Characterization of the nasopharyngeal microbiota in health and during rhinovirus challenge. Microbiome (2014) 2:22. doi: 10.1186/2049-2618-2-22 PubMed Abstract | CrossRef Full Text | Google Scholar
74. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Falkowski NR, Huffnagle GB, et al. Bacterial topography of the healthy human lower respiratory tract. MBio (2017) 8:e02287-16. doi: 10.1128/mBio.02287-16 PubMed Abstract | CrossRef Full Text | Google Scholar
75. Abreu NA, Nagalingam NA, Song Y, Roediger FC, Pletcher SD, Goldberg AN, et al. Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Sci Transl Med. (2012) 4:151ra124. doi: 10.1126/scitranslmed.3003783 PubMed Abstract | CrossRef Full Text | Google Scholar
76. Bassis CM, Erb-Downward JR, Dickson RP, Freeman CM, Schmidt TM, Young VB, et al. Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. MBio (2015) 6:e00037. doi: 10.1128/mBio.00037-15 PubMed Abstract | CrossRef Full Text | Google Scholar
77. Venkataraman A, Bassis CM, Beck JM, Young VB, Curtis JL, Huffnagle GB, et al. Application of a neutral community model to assess structuring of the human lung microbiome. MBio (2015) 6:e02284-14. doi: 10.1128/mBio.02284-14 PubMed Abstract | CrossRef Full Text | Google Scholar
78. Morris A, Beck JM, Schloss PD, Campbell TB, Crothers K, Curtis JL, et al. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med. (2013) 187:1067-75. doi: 10.1164/rccm.201210-1913OC PubMed Abstract | CrossRef Full Text | Google Scholar
79. Segal LN, Alekseyenko AV, Clemente JC, Kulkarni R, Wu B, Gao Z, et al. Enrichment of lung microbiome with supraglottic taxa is associated with increased pulmonary inflammation. Microbiome (2013) 1:19. doi: 10.1186/2049-2618-1-19 PubMed Abstract | CrossRef Full Text | Google Scholar
80. Dickson RP, Erb-Downward JR, Freeman CM, McCloskey L, Beck JM, Huffnagle GB, Curtis JL. Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc. (2015) 12:821-30. doi: 10.1513/AnnalsATS.201501-029OC PubMed Abstract | CrossRef Full Text | Google Scholar
81. Rogers GB, Shaw D, Marsh RL, Carroll MP, Serisier DJ, Bruce KD. Respiratory microbiota: Addressing clinical questions, informing clinical practice. Thorax (2015) 70:74-81. doi: 10.1136/thoraxjnl-2014-205826 PubMed Abstract | CrossRef Full Text | Google Scholar
82. Rogers GB, Hoffman LR, Carroll MP, Bruce KD. Interpreting infective microbiota: The importance of an ecological perspective. Trends Microbiol. (2013) 21:271-6. doi: 10.1016/j.tim.2013.03.004 PubMed Abstract | CrossRef Full Text | Google Scholar
83. Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. (2005) 5:751-62. doi: 10.1016/S1473-3099(05)70295-4 PubMed Abstract | CrossRef Full Text | Google Scholar
84. Bogaert D, De Groot R, Hermans PWM. Streptococcus pneumoniae colonisation: The key to pneumococcal disease. Lancet Infect Dis. (2004) 4:144-54. doi: 10.1016/S1473-3099(04)00938-7 PubMed Abstract | CrossRef Full Text | Google Scholar
85. Wolter N, Tempia S, Cohen C, Madhi SA, Venter M, Moyes J, et al. High nasopharyngeal pneumococcal density, increased by viral coinfection, is associated with invasive pneumococcal pneumonia. J Infect Dis. (2014) 210:1649-57. doi: 10.1093/infdis/jiu326 PubMed Abstract | CrossRef Full Text | Google Scholar
86. Ishizuka S, Yamaya M, Suzuki T, Takahashi H, Ida S, Sasaki T, et al. Effects of rhinovirus infection on the adherence of Streptococcus pneumoniae to cultured human airway epithelial cells. J Infect Dis. (2003) 188:1928-39. doi: 10.1086/379833 PubMed Abstract | CrossRef Full Text | Google Scholar
87. Avadhanula V, Rodriguez CA, Devincenzo JP, Wang Y, Webby RJ, Ulett GC, et al. Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species- and cell type-dependent manner. J Virol. (2006) 80:1629-36. doi: 10.1128/JVI.80.4.1629-1636.2006 PubMed Abstract | CrossRef Full Text | Google Scholar
88. Wang JH, Kwon HJ, Jang YJ. Rhinovirus enhances various bacterial adhesions to nasal epithelial cells simultaneously. Laryngoscope (2009) 119:1406-11. doi: 10.1002/lary.20498 PubMed Abstract | CrossRef Full Text | Google Scholar
89. Safaeyan F, Nahaei MR, Seifi SJ, Kafil HS, Sadeghi J. Quantitative detection of Staphylococcus aureus, Streptococcus pneumoniae and Haemophilus influenzae in patients with new influenza A (H1N1)/2009 and influenza A/2010 virus infection. GMS Hyg Infect Control (2015) 10:Doc06. doi: 10.3205/dgkh000249 PubMed Abstract | CrossRef Full Text | Google Scholar
90. Hirano T, Kurono Y, Ichimiya I, Suzuki M, Mogi G. Effects of influenza A virus on lectin-binding patterns in murine nasopharyngeal mucosa and on bacterial colonization. Otolaryngol Head Neck Surg. (1999) 121:616-21. doi: 10.1016/S0194-5998(99)70068-9 PubMed Abstract | CrossRef Full Text | Google Scholar
91. McCullers JA, McAuley JL, Browall S, Iverson AR, Boyd KL, Henriques Normark B. Influenza enhances susceptibility to natural acquisition of and disease due to Streptococcus pneumoniae in ferrets. J Infect Dis. (2010) 202:1287-95. doi: 10.1086/656333 PubMed Abstract | CrossRef Full Text | Google Scholar
92. Wadowsky RM, Mietzner SM, Skoner DP, Doyle WJ, Fireman P. Effect of experimental influenza A virus infection on isolation of Streptococcus pneumoniae and other aerobic bacteria from the oropharynges of allergic and nonallergic adult subjects. Infect Immun. (1995) 63:1153-7. PubMed Abstract | Google Scholar
93. Wren JT, Blevins LK, Pang B, King LB, Perez AC, Murrah KA, et al. Influenza A virus alters pneumococcal nasal colonization and middle ear infection independently of phase variation. Infect Immun. (2014) 82:4802-12. doi: 10.1128/IAI.01856-14 PubMed Abstract | CrossRef Full Text | Google Scholar
94. Nakamura S, Davis KM, Weiser JN. Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J Clin Invest. (2011) 121:3657-65. doi: 10.1172/JCI57762 PubMed Abstract | CrossRef Full Text | Google Scholar
95. Diavatopoulos DA, Short KR, Price JT, Wilksch JJ, Brown LE, Briles DE, et al. Influenza A virus facilitates Streptococcus pneumoniae transmission and disease. FASEB J. (2010) 24:1789-98. doi: 10.1096/fj.09-146779 PubMed Abstract | CrossRef Full Text | Google Scholar
96. Vu HTT, Yoshida LM, Suzuki M, Nguyen HAT, Nguyen CDL, Nguyen ATT, et al. Association between nasopharyngeal load of Streptococcus pneumoniae, viral coinfection, and radiologically confirmed pneumonia in Vietnamese children. Pediatr Infect Dis J. (2011) 30:11-8. doi: 10.1097/INF.0b013e3181f111a2 PubMed Abstract | CrossRef Full Text | Google Scholar
97. Takase H, Nitanai H, Yamamura E, Otani T. Facilitated expansion of pneumococcal colonization from the nose to the lower respiratory tract in mice preinfected with influenza virus. Microbiol Immunol. (1999) 43:905-7. PubMed Abstract | Google Scholar
98. Tong HH, Fisher LM, Kosunick GM, DeMaria TF. Effect of adenovirus type 1 and influenza A virus on Streptococcus pneumoniae nasopharyngeal colonization and otitis media in the chinchilla. Ann Otol Rhinol Laryngol. (2000) 109:1021-7. doi: 10.1177/000348940010901106 PubMed Abstract | CrossRef Full Text | Google Scholar
99. Peltola VT, Boyd KL, McAuley JL, Rehg JE, McCullers JA. Bacterial sinusitis and otitis media following influenza virus infection in ferrets. Infect Immun. (2006) 74:2562-7. doi: 10.1128/IAI.74.5.2562-2567.2006 PubMed Abstract | CrossRef Full Text | Google Scholar
100. Edouard S, Million M, Bachar D, Dubourg G, Michelle C, Ninove L, et al. The nasopharyngeal microbiota in patients with viral respiratory tract infections is enriched in bacterial pathogens. Eur J Clin Microbiol Infect Dis. (2018) 37:172533. doi: 10.1007/s10096-018-3305-8 PubMed Abstract | CrossRef Full Text | Google Scholar
101. Verkaik NJ, Nguyen DT, de Vogel CP, Moll HA, Verbrugh HA, Jaddoe VWV, et al. Streptococcus pneumoniae exposure is associated with human metapneumovirus seroconversion and increased susceptibility to in vitro HMPV infection. Clin Microbiol Infect. (2011) 17:1840-4. doi: 10.1111/j.1469-0691.2011.03480.x PubMed Abstract | CrossRef Full Text | Google Scholar
102. DE Lastours V, Malosh R, Ramadugu K, Srinivasan U, Dawid S, Ohmit S, et al. Co-colonization by Streptococcus pneumoniae and Staphylococcus aureus in the throat during acute respiratory illnesses. Epidemiol Infect. (2016) 144:1-13. doi: 10.1017/S0950268816001473 CrossRef Full Text | Google Scholar
103. Ni K, Li S, Xia Q, Zang N, Deng Y, Xie X, et al. Pharyngeal microflora disruption by antibiotics promotes airway hyperresponsiveness after respiratory syncytial virus infection. PLoS ONE (2012) 7:e41104. doi: 10.1371/journal.pone.0041104 PubMed Abstract | CrossRef Full Text | Google Scholar
104. Wang J, Li F, Sun R, Gao X, Wei H, Li L-J, et al. Bacterial colonization dampens influenza-mediated acute lung injury via induction of M2 alveolar macrophages. Nat Commun. (2013) 4:2106. doi: 10.1038/ncomms3106 PubMed Abstract | CrossRef Full Text | Google Scholar
105. Langevin S, Pichon M, Smith E, Morrison J, Bent Z, Green R, et al. Early nasopharyngeal microbial signature associated with severe influenza in children: A retrospective pilot study. J Gen Virol. (2017) 98:2425-37. doi: 10.1099/jgv.0.000920 PubMed Abstract | CrossRef Full Text | Google Scholar
106. Lu H-F, Li A, Zhang T, Ren Z-G, He K-X, Zhang H, et al. Disordered oropharyngeal microbial communities in H7N9 patients with or without secondary bacterial lung infection. Emerg Microbes Infect. (2017) 6:e112. doi: 10.1038/emi.2017.101 CrossRef Full Text | Google Scholar
107. Tarabichi Y, Li K, Hu S, Nguyen C, Wang X, Elashoff D, et al. The administration of intranasal live attenuated influenza vaccine induces changes in the nasal microbiota and nasal epithelium gene expression profiles. Microbiome (2015) 3:74. doi: 10.1186/s40168-015-0133-2 PubMed Abstract | CrossRef Full Text | Google Scholar
108. Leung RK-K, Zhou J-W, Guan W, Li S-K, Yang Z-F, Tsui SK-W. Modulation of potential respiratory pathogens by pH1N1 viral infection. Clin Microbiol Infect. (2013) 19:930-5. doi: 10.1111/1469-0691.12054 PubMed Abstract | CrossRef Full Text | Google Scholar
109. Chaban B, Albert A, Links MG, Gardy J, Tang P, Hill JE. Characterization of the upper respiratory tract microbiomes of patients with pandemic H1N1 influenza. PLoS ONE (2013) 8:e69559. doi: 10.1371/journal.pone.0069559 PubMed Abstract | CrossRef Full Text | Google Scholar
110. Greninger AL, Chen EC, Sittler T, Scheinerman A, Roubinian N, Yu G, et al. A metagenomic analysis of pandemic influenza A (2009 H1N1) infection in patients from North America. PLoS ONE (2010) 5:e13381. doi: 10.1371/journal.pone.0013381 PubMed Abstract | CrossRef Full Text | Google Scholar
111. Jacoby P, Watson K, Bowman J, Taylor A, Riley TV, Smith DW, et al. Kalgoorlie Otitis Media Research Project Team. Modelling the co-occurrence of Streptococcus pneumoniae with other bacterial and viral pathogens in the upper respiratory tract. Vaccine (2007) 25:2458-64. doi: 10.1016/j.vaccine.2006.09.020 CrossRef Full Text | Google Scholar
112. van den Bergh MR, Biesbroek G, Rossen JWA, de Steenhuijsen Piters WAA, Bosch AATM, van Gils EJM, et al. Associations between pathogens in the upper respiratory tract of young children: Interplay between viruses and bacteria. PLoS ONE (2012) 7:e47711. doi: 10.1371/journal.pone.0047711 CrossRef Full Text | Google Scholar
113. Rosas-Salazar C, Shilts MH, Tovchigrechko A, Schobel S, Chappell JD, Larkin EK, et al. Differences in the nasopharyngeal microbiome during acute respiratory tract infection with human rhinovirus and respiratory syncytial virus in infancy. J Infect Dis. (2016) 214:1924-8. doi: 10.1093/infdis/jiw456 PubMed Abstract | CrossRef Full Text | Google Scholar
114. Bogaert D, Keijser B, Huse S, Rossen J, Veenhoven R, van Gils E, et al. Variability and diversity of nasopharyngeal microbiota in children: A metagenomic analysis. PLoS ONE (2011) 6:e17035. doi: 10.1371/journal.pone.0017035 PubMed Abstract | CrossRef Full Text | Google Scholar
115. Pérez-Losada M, Alamri L, Crandall KA, Freishtat RJ. Nasopharyngeal microbiome diversity changes over time in children with asthma. PLoS ONE (2017) 12:e0170543. doi: 10.1371/journal.pone.0170543 PubMed Abstract | CrossRef Full Text | Google Scholar
116. Hassoun A, Huff MD, Weisman D, Chahal K, Asis E, Stalons D, et al. Seasonal variation of respiratory pathogen colonization in asymptomatic health care professionals: A single-center, cross-sectional, 2-season observational study. Am J Infect Control (2015) 43:865-70. doi: 10.1016/j.ajic.2015.04.195 PubMed Abstract | CrossRef Full Text | Google Scholar
117. DeMuri GP, Gern JE, Eickhoff JC, Lynch SV, Wald ER. Dynamics of bacterial colonization with streptococcus pneumoniae, haemophilus influenzae, and moraxella catarrhalis during symptomatic and asymptomatic viral upper respiratory tract infection. Clin Infect Dis. (2018) 66:1045-53. doi: 10.1093/cid/cix941 PubMed Abstract | CrossRef Full Text | Google Scholar
118. Karppinen S, Teräsjärvi J, Auranen K, Schuez-Havupalo L, Siira L, He Q, et al. Acquisition and transmission of streptococcus pneumoniae are facilitated during rhinovirus infection in families with children. Am J Respir Crit Care Med. (2017) 196:1172-80. doi: 10.1164/rccm.201702-0357OC PubMed Abstract | CrossRef Full Text | Google Scholar
119. Hofstra JJ, Matamoros S, van de Pol MA, de Wever B, Tanck MW, Wendt-Knol H, et al. Changes in microbiota during experimental human Rhinovirus infection. BMC Infect Dis. (2015) 15:336. doi: 10.1186/s12879-015-1081-y PubMed Abstract | CrossRef Full Text | Google Scholar
120. Thors V, Christensen H, Morales-Aza B, Vipond I, Muir P, Finn A. The effects of live attenuated influenza vaccine on nasopharyngeal bacteria in healthy 2 to 4 year olds. a randomized controlled trial. Am J Respir Crit Care Med. (2016) 193:1401-9. doi: 10.1164/rccm.201510-2000OC PubMed Abstract | CrossRef Full Text | Google Scholar
121. Mina MJ, McCullers JA, Klugman KP. Live attenuated influenza vaccine enhances colonization of Streptococcus pneumoniae and Staphylococcus aureus in mice. MBio (2014) 5:e01040-13. doi: 10.1128/mBio.01040-13 PubMed Abstract | CrossRef Full Text | Google Scholar
122. Salk HM, Simon WL, Lambert ND, Kennedy RB, Grill DE, Kabat BF et al. Taxa of the nasal microbiome are associated with influenza-specific IgA response to live attenuated influenza vaccine. PLoS ONE (2016) 11:e0162803. doi: 10.1371/journal.pone.0162803 PubMed Abstract | CrossRef Full Text | Google Scholar
123. Planet PJ, Parker D, Cohen TS, Smith H, Leon JD, Ryan C, et al. Lambda interferon restructures the nasal microbiome and increases susceptibility to staphylococcus aureus superinfection. MBio (2016) 7:e01939-01915. doi: 10.1128/mBio.01939-15 PubMed Abstract | CrossRef Full Text | Google Scholar
124. Molyneaux PL, Mallia P, Cox MJ, Footitt J, Willis-Owen SAG, Homola D, et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med. (2013) 188:1224-31. doi: 10.1164/rccm.201302-0341OC PubMed Abstract | CrossRef Full Text | Google Scholar
125. Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: Soldier in the fight against respiratory viruses. Clin Microbiol Rev. (2011) 24:210-29. doi: 10.1128/CMR.00014-10 PubMed Abstract | CrossRef Full Text | Google Scholar
126. Pittet LA, Hall-Stoodley L, Rutkowski MR, Harmsen AG. Influenza virus infection decreases tracheal mucociliary velocity and clearance of Streptococcus pneumoniae. Am J Respir Cell Mol Biol. (2010) 42:450-60. doi: 10.1165/rcmb.2007-0417OC PubMed Abstract | CrossRef Full Text | Google Scholar
127. Smith CM, Kulkarni H, Radhakrishnan P, Rutman A, Bankart MJ, Williams G, et al. Ciliary dyskinesia is an early feature of respiratory syncytial virus infection. Eur Respir J. (2014) 43:485-96. doi: 10.1183/09031936.00205312 PubMed Abstract | CrossRef Full Text | Google Scholar
128. Abramson JS, Mills EL, Giebink GS, Quie PG. Depression of monocyte and polymorphonuclear leukocyte oxidative metabolism and bactericidal capacity by influenza A virus. Infect Immun. (1982) 35:350-5. PubMed Abstract | Google Scholar
129. Didierlaurent A, Goulding J, Patel S, Snelgrove R, Low L, Bebien M, et al. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory influenza infection. J Exp Med. (2008) 205:323-9. doi: 10.1084/jem.20070891 PubMed Abstract | CrossRef Full Text | Google Scholar
130. McNamee LA, Harmsen AG. Both influenza-induced neutrophil dysfunction and neutrophil-independent mechanisms contribute to increased susceptibility to a secondary Streptococcus pneumoniae infection. Infect Immun. (2006) 74:6707-21. doi: 10.1128/IAI.00789-06 PubMed Abstract | CrossRef Full Text | Google Scholar
131. Astry CL, Jakab GJ. Influenza virus-induced immune complexes suppress alveolar macrophage phagocytosis. J Virol. (1984) 50:287-292. PubMed Abstract | Google Scholar
132. Franke-Ullmann G, Pförtner C, Walter P, Steinmüller C, Lohmann-Matthes ML, Kobzik L, et al. Alteration of pulmonary macrophage function by respiratory syncytial virus infection in vitro. J Immunol. (1995) 154:268-80. PubMed Abstract | Google Scholar
133. Ghoneim HE, Thomas PG, McCullers JA. Depletion of alveolar macrophages during influenza infection facilitates bacterial superinfections. J Immunol. (2013) 191:1250-9. doi: 10.4049/jimmunol.1300014 PubMed Abstract | CrossRef Full Text | Google Scholar
134. Jakab GJ. Immune impairment of alveolar macrophage phagocytosis during influenza virus pneumonia. Am Rev Respir Dis. (1982) 126:778-82. doi: 10.1164/arrd.1982.126.5.778 PubMed Abstract | CrossRef Full Text | Google Scholar
135. Kleinerman ES, Daniels CA, Polisson RP, Snyderman R. Effect of virus infection on the inflammatory response. Depression of macrophage accumulation in influenza-infected mice. Am J Pathol. (1976) 85:373-82. PubMed Abstract | Google Scholar
136. Nickerson CL, Jakab GJ. Pulmonary antibacterial defenses during mild and severe influenza virus infection. Infect Immun. (1990) 58:2809-14. PubMed Abstract | Google Scholar
137. Uehara Y, Nakama H, Agematsu K, Uchida M, Kawakami Y, Abdul Fattah AS, et al. Bacterial interference among nasal inhabitants: Eradication of Staphylococcus aureus from nasal cavities by artificial implantation of Corynebacterium sp. J Hosp Infect. (2000) 44:127-33. doi: 10.1053/jhin.1999.0680 PubMed Abstract | CrossRef Full Text | Google Scholar
138. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature (2010) 465:346-9. doi: 10.1038/nature09074 PubMed Abstract | CrossRef Full Text | Google Scholar
139. Yan M, Pamp SJ, Fukuyama J, Hwang PH, Cho D-Y, Holmes S, et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe (2013) 14:631-40. doi: 10.1016/j.chom.2013.11.005 PubMed Abstract | CrossRef Full Text | Google Scholar
140. Kanmani P, Clua P, Vizoso-Pinto MG, Rodriguez C, Alvarez S, Melnikov V, et al. Respiratory commensal bacteria corynebacterium pseudodiphtheriticum improves resistance of infant mice to respiratory syncytial virus and streptococcus pneumoniae superinfection. Front Microbiol. (2017) 8:1613. doi: 10.3389/fmicb.2017.01613 PubMed Abstract | CrossRef Full Text | Google Scholar
141. Reddinger RM, Luke-Marshall NR, Hakansson AP, Campagnari AA. Host physiologic changes induced by influenza a virus lead to staphylococcus aureus biofilm dispersion and transition from asymptomatic colonization to invasive disease. MBio (2016) 7:CD007087. doi: 10.1128/mBio.01235-16 PubMed Abstract | CrossRef Full Text | Google Scholar
142. Pettigrew MM, Marks LR, Kong Y, Gent JF, Roche-Hakansson H, Hakansson AP. Dynamic changes in the Streptococcus pneumoniae transcriptome during transition from biofilm formation to invasive disease upon influenza A virus infection. Infect Immun. (2014) 82:4607-19. doi: 10.1128/IAI.02225-14 PubMed Abstract | CrossRef Full Text | Google Scholar
143. Marks LR, Davidson BA, Knight PR, Hakansson AP. Interkingdom signaling induces Streptococcus pneumoniae biofilm dispersion and transition from asymptomatic colonization to disease. MBio (2013) 4:e00438-13. doi: 10.1128/mBio.00438-13 PubMed Abstract | CrossRef Full Text | Google Scholar
144. Reddinger RM, Luke-Marshall NR, Sauberan SL, Hakansson AP, Campagnari AA. Streptococcus pneumoniae modulates staphylococcus aureus biofilm dispersion and the transition from colonization to invasive disease. MBio (2018) 9:e02089-17. doi: 10.1128/mBio.02089-17 PubMed Abstract | CrossRef Full Text | Google Scholar