Influenza enhances host susceptibility to non-pulmonary invasive Streptococcus pyogenes infections

References

• Morens DM, Fauci AS. The 1918 influenza pandemic: insights for the 21st century. J Infect Dis. 2007;195(7):1018–11. doi: 10.1086/511989
   PubMed Web of Science ®Google Scholar
• Brundage JF, Shanks GD. Deaths from bacterial pneumonia during 1918-19 influenza pandemic. Emerg Infect Dis. 2008;14(8):1193–1199. doi: 10.3201/eid1408.071313
   PubMed Web of Science ®Google Scholar
• Chien YW, Klugman KP, Morens DM. Bacterial pathogens and death during the 1918 influenza pandemic. N Engl J Med. 2009;361(26):2582–2583. doi: 10.1056/NEJMc0908216
   PubMed Web of Science ®Google Scholar
• Birge E, Havens L. A comparison of the bacteriology of pneumonia, antemortem and postmortem. N Y Med J. 1919;109:544–545.
   Google Scholar
• McCullers JA. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol. 2014;12(4):252–262. doi: 10.1038/nrmicro3231
   PubMed Web of Science ®Google Scholar
• McCullers JA. Insights into the interaction between influenza virus and pneumococcus. Clin Microbiol Rev. 2006;19(3):571–582. doi: 10.1128/CMR.00058-05
   PubMed Web of Science ®Google Scholar
• Metzger DW, Sun K. Immune dysfunction and bacterial coinfections following influenza. J Immunol. 2013;191(5):2047–2052. doi: 10.4049/jimmunol.1301152
   PubMed Web of Science ®Google Scholar
• Rynda-Apple A, Robinson KM, Alcorn JF, et al. Influenza and bacterial superinfection: illuminating the immunologic mechanisms of disease. Infect Immun. 2015;83(10):3764–3770. doi: 10.1128/IAI.00298-15
   PubMed Web of Science ®Google Scholar
• Michelow IC, Olsen K, Lozano J, et al. Epidemiology and clinical characteristics of community-acquired pneumonia in hospitalized children. Pediatrics. 2004;113(4):701–707. doi: 10.1542/peds.113.4.701
   PubMed Web of Science ®Google Scholar
• Berkley JA, Munywoki P. Viral etiology of severe pneumonia among Kenyan infants and children. JAMA. 2010;303(20):2051–2057. doi: 10.1001/jama.2010.675
   PubMed Web of Science ®Google Scholar
• Olsen SJ, Thamthitiwat S, Chantra S, et al. Incidence of respiratory pathogens in persons hospitalized with pneumonia in two provinces in Thailand. Epidemiol Infect. 2010;138(12):1811–1822. doi: 10.1017/S0950268810000646
   PubMed Web of Science ®Google Scholar
• Hammitt LL, Kazungu S, Morpeth SC, et al. A preliminary study of pneumonia etiology among hospitalized children in Kenya. Clinl Infect Dis. 2012;54(Suppl 2):S190–9. doi: 10.1093/cid/cir1071
   PubMedGoogle Scholar
• Chen CJ, Lin P-Y, Tsai M-H, et al. Etiology of community-acquired pneumonia in hospitalized children in northern Taiwan. Pediatr Infect Dis J. 2012;31(11):e196–201. doi: 10.1097/INF.0b013e31826eb5a7
   PubMed Web of Science ®Google Scholar
• Techasaensiri B, Techasaensiri C, Mejías A, et al. Viral coinfections in children with invasive pneumococcal disease. Pediatr Infect Dis J. 2010;29(6):519–523. doi: 10.1097/INF.0b013e3181cdafc2
   PubMed Web of Science ®Google Scholar
• Peltola VT, McCullers JA. Respiratory viruses predisposing to bacterial infections: role of neuraminidase. Pediatr Infect Dis J. 2004;23(1 Suppl):S87–97. doi: 10.1097/01.inf.0000108197.81270.35
   PubMed Web of Science ®Google Scholar
• Peltola V, Heikkinen T, Ruuskanen O, et al. Temporal association between rhinovirus circulation in the community and invasive pneumococcal disease in children. Pediatr Infect Dis J. 2011;30(6):456–461. doi: 10.1097/INF.0b013e318208ee82
   PubMed Web of Science ®Google Scholar
• Herrera AL, Suso K. Binding host proteins to the M protein contributes to the mortality associated with influenza-Streptococcus pyogenes superinfections. Microbiology. 2017;163(10):1445–1456. doi: 10.1099/mic.0.000532
   PubMed Web of Science ®Google Scholar
• Herrera AL, Faal H, Moss D, et al. The Streptococcus pyogenes fibronectin/tenascin-binding protein PrtF.2 contributes to virulence in an influenza superinfection. Sci Rep. 2018;8(1):12126. doi: 10.1038/s41598-018-29714-x
   PubMedGoogle Scholar
• Herrera AL, Huber VC, Chaussee MS. The association between invasive group a streptococcal diseases and viral respiratory tract infections. Front Microbiol. 2016;7:342. doi: 10.3389/fmicb.2016.00342
   PubMed Web of Science ®Google Scholar
• de Gier B, Woudt SHS, van Sorge NM, et al. Associations between common respiratory viruses and invasive group a streptococcal infection: a time-series analysis. influenza and other respiratory viruses. Influenza Other Respir Viruses. 2019 Sep;13(5):453–458. [cited 2019 Jun 25] doi: 10.1111/irv.12658
   PubMed Web of Science ®Google Scholar
• Zakikhany K, Degail MA, Lamagni T, et al. Increase in invasive Streptococcus pyogenes and Streptococcus pneumoniae infections in England, December 2010 to January 2011. Euro Surveill. 2011;16(5): doi: 10.2807/ese.16.05.19785-en
   PubMedGoogle Scholar
• Parola P, Colson P, Dubourg G, et al. Letter to the editor. Group a streptococcal infections during the seasonal influenza outbreak 2010/11 in South East England. Euro Surveill. 2011;16(11): doi: 10.2807/ese.16.11.19816-en
   Google Scholar
• Tasher D, Stein M, Simões EAF, et al. Invasive bacterial infections in relation to influenza outbreaks, 2006–2010. Clin Infect Dis. 2011;53(12):1199–1207. doi: 10.1093/cid/cir726
   PubMed Web of Science ®Google Scholar
• Glans H, Rönnbäck K, Berggren I, et al. [Increase in serious infections due to group a streptococci]. Lakartidningen. 2013;110(22):1094–1097.
   PubMedGoogle Scholar
• Jean C, Louie J, Glaser C, et al. Invasive group a streptococcal infection concurrent with 2009 H1N1 influenza. Clin Infect Dis. 2010;50(10):e59–62. doi: 10.1086/652291
   PubMed Web of Science ®Google Scholar
• Aebi T, Weisser M. Co-infection of influenza B and streptococci causing severe pneumonia and septic shock in healthy women. 2010; 10:308.
   Google Scholar
• Allard R, Couillard M, Pilon P, et al. Invasive bacterial infections following influenza: a time-series analysis in Montréal, Canada, 1996-2008. influenza other Respir viruses. Influenza Other Respir Viruses. 2012;6(4):268–275. doi: 10.1111/j.1750-2659.2011.00297.x
   PubMed Web of Science ®Google Scholar
• Scaber J, Saeed S, Ihekweazu C, et al. Group a streptococcal infections during the seasonal influenza outbreak 2010/11 in South East England. Euro Surveill. 2011;16(5): doi: 10.2807/ese.16.05.19780-en
   PubMedGoogle Scholar
• Lee SE, Eick A, Bloom MS, et al. Influenza immunization and subsequent diagnoses of group a streptococcus-illnesses among U.S. Army trainees, 2002–2006. Vaccine. 2008;26(27–28):3383–3386. doi: 10.1016/j.vaccine.2008.04.041
   PubMed Web of Science ®Google Scholar
• Turner PV, Brabb T, Pekow C, et al. Administration of substances to laboratory animals: routes of administration and factors to consider. J Am Assoc Lab Anim Sci. 2011;50(5):600–613.
   PubMed Web of Science ®Google Scholar
• Herrera AL, Van Hove C, Hanson M, et al. Immunotherapy targeting the Streptococcus pyogenes M protein or streptolysin O to treat or prevent influenza a superinfection. PLoS One. 2020;15(6):e0235139. doi: 10.1371/journal.pone.0235139
   PubMed Web of Science ®Google Scholar
• Chaussee MS, Sandbulte HR, Schuneman MJ, et al. Inactivated and live, attenuated influenza vaccines protect mice against influenza: Streptococcus pyogenes super-infections. Vaccine. 2011;29(21):3773–3781. doi: 10.1016/j.vaccine.2011.03.031
   PubMed Web of Science ®Google Scholar
• Klonoski JM, Hurtig HR, Juber BA, et al. Vaccination against the M protein of Streptococcus pyogenes prevents death after influenza virus: S. pyogenes super-infection. Vaccine. 2014;32(40):5241–5249. doi: 10.1016/j.vaccine.2014.06.093
   PubMed Web of Science ®Google Scholar
• Klonoski JM, Watson T, Bickett TE, et al. Contributions of influenza virus hemagglutinin and host immune responses toward the severity of influenza virus: Streptococcus pyogenes superinfections. Viral Immunol. 2018;31(6):457–469. doi: 10.1089/vim.2017.0193
   PubMed Web of Science ®Google Scholar
• de Gier B, Vlaminckx BJM, Woudt SHS, et al. Associations between common respiratory viruses and invasive group a streptococcal infection: a time-series analysis. Influenza Other Respir Viruses. 2019;13(5):453–458. doi: 10.1111/irv.12658
   PubMed Web of Science ®Google Scholar
• Ochi F, Tauchi H, Jogamoto T, et al. Sepsis and pleural empyema caused by Streptococcus pyogenes after influenza a virus infection. Case Rep Pediatr. 2018;2018:1–4. doi: 10.1155/2018/4509847
   Web of Science ®Google Scholar
• Guy R, Henderson KL, Coelho J, et al. Increase in invasive group a streptococcal infection notifications, England, 2022. Euro Surveill. 2023;28(1): doi: 10.2807/1560-7917.ES.2023.28.1.2200942
   PubMedGoogle Scholar
• Aleith J, Brendel M, Weipert E, et al. Influenza a virus exacerbates group a Streptococcus infection and thwarts anti-bacterial inflammatory responses in murine macrophages. Pathogens. 2022;11(11):1320. doi: 10.3390/pathogens11111320
   PubMed Web of Science ®Google Scholar
• Jamieson AM, Yu S, Annicelli CH, et al. Influenza virus-induced glucocorticoids compromise innate host defense against a secondary bacterial infection. Cell Host Microbe. 2010;7(2):103–114. doi: 10.1016/j.chom.2010.01.010
   PubMed Web of Science ®Google Scholar
• Tisoncik JR, Korth MJ, Simmons CP, et al. Into the eye of the cytokine storm. Microbiol Mol Biol Rev. 2012;76(1):16–32. doi: 10.1128/MMBR.05015-11
   PubMed Web of Science ®Google Scholar
• Ellis GT, Davidson S, Crotta S, et al. TRAIL + monocytes and monocyte-related cells cause lung damage and thereby increase susceptibility to influenza– S treptococcus pneumoniae coinfection. EMBO Rep. 2015;16(9):1203–1218. doi: 10.15252/embr.201540473
   PubMed Web of Science ®Google Scholar
• Kirby AC, Raynes JG, Kaye PM. The role played by tumor necrosis factor during localized and systemic infection with Streptococcus pneumoniae. J Infect Dis. 2005;191(9):1538–1547. doi: 10.1086/429296
   PubMed Web of Science ®Google Scholar
• Hussell T, Pennycook A, Openshaw PJ. Inhibition of tumor necrosis factor reduces the severity of virus-specific lung immunopathology. Eur J Immunol. 2001;31(9):2566–2573. doi: 10.1002/1521-4141(200109)31:9<2566:AID-IMMU2566>3.0.CO;2-L
   PubMed Web of Science ®Google Scholar
• La Gruta NL, Kedzierska K, Stambas J, et al. A question of self-preservation: immunopathology in influenza virus infection. Immunol Cell Biol. 2007;85(2):85–92. doi: 10.1038/sj.icb.7100026
   PubMed Web of Science ®Google Scholar
• Marcos-Ramiro B, García-Weber D, Millán J. TNF-induced endothelial barrier disruption: beyond actin and rho. Thromb Haemost. 2014;112(6):1088–1102. doi: 10.1160/th14-04-0299
   PubMed Web of Science ®Google Scholar
• Stegemann S, Dahlberg S, Kröger A, et al. Increased susceptibility for superinfection with Streptococcus pneumoniae during influenza virus infection is not caused by TLR7-mediated lymphopenia. PLoS One. 2009;4(3):e4840. doi: 10.1371/journal.pone.0004840
   PubMed Web of Science ®Google Scholar
• Astry CL, Jakab GJ. Influenza virus-induced immune complexes suppress alveolar macrophage phagocytosis. J Virol. 1984;50(2):287–292. doi: 10.1128/jvi.50.2.287-292.1984
   PubMed Web of Science ®Google Scholar
• Jakab GJ. Immune impairment of alveolar macrophage phagocytosis during influenza virus pneumonia. Am Rev Respir Dis. 1982;126(5):778–782. doi: 10.1164/arrd.1982.126.5.778
   PubMedGoogle Scholar
• Warr GA, Jakab GJ. Alterations in lung macrophage antimicrobial activity associated with viral pneumonia. Infect Immun. 1979;26(2):492–497. doi: 10.1128/iai.26.2.492-497.1979
   PubMed Web of Science ®Google Scholar
• Sun K, Metzger DW. Inhibition of pulmonary antibacterial defense by interferon-gamma during recovery from influenza infection. Nat Med. 2008;14(5):558–564. doi: 10.1038/nm1765
   PubMed Web of Science ®Google Scholar
• Beres SB, Sylva GL, Barbian KD, et al. Genome sequence of a serotype M3 strain of group a Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A. 2002;99(15):10078–10083. doi: 10.1073/pnas.152298499
   PubMed Web of Science ®Google Scholar
• Muller MP, Low DE. Clinical and epidemiologic features of group a streptococcal pneumonia in Ontario, Canada. Arch Intern Med. 2003;163(4):467–472. doi: 10.1001/archinte.163.4.467
   PubMedGoogle Scholar
• Huber VC, Thomas PG, McCullers JA. A multi-valent vaccine approach that elicits broad immunity within an influenza subtype. Vaccine. 2009;27(8):1192–1200. doi: 10.1016/j.vaccine.2008.12.023
   PubMed Web of Science ®Google Scholar
• Sanders CJ, Johnson B. Intranasal influenza infection of mice and methods to evaluate progression and outcome. Methods Mol Biol. 2013;1031:177–188.
   PubMedGoogle Scholar
• Trammell RA, Toth LA. Markers for predicting death as an outcome for mice used in infectious disease research. Comp Med. 2011;61(6):492–498.
   PubMed Web of Science ®Google Scholar
• Bouvier NM, Lowen AC. Animal models for influenza virus pathogenesis and transmission. Viruses. 2010;2(8):1530–1563. doi: 10.3390/v20801530
   PubMed Web of Science ®Google Scholar
• Herrera AL, Callegari EA, Chaussee MS, et al. The Streptococcus pyogenes signaling peptide SpoV regulates streptolysin O and enhances survival in murine blood. J Bacteriol. 2021;203(11). doi: 10.1128/JB.00586-20
   PubMed Web of Science ®Google Scholar