Pathogenesis of influenza and SARS-CoV-2 co-infection at the extremes of age: decipher the ominous tales of immune vulnerability

Kai-lin Mai , Wei-qi Pan , Zheng-shi Lin , Yang Wang , Zi-feng Yang

Advanced Biotechnology ›› 2025, Vol. 3 ›› Issue (1) : 5

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Advanced Biotechnology ›› 2025, Vol. 3 ›› Issue (1) : 5 DOI: 10.1007/s44307-025-00057-9
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Pathogenesis of influenza and SARS-CoV-2 co-infection at the extremes of age: decipher the ominous tales of immune vulnerability

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Abstract

The co-circulation of influenza and SARS-CoV-2 has led to co-infection events, primarily affecting children and older adults, who are at higher risk for severe disease. Although co-infection prevalence is relatively low, it is associated with worse outcomes compared to mono-infections. Previous studies have shown that the outcomes of co-infection depend on multiple factors, including viral interference, virus-host interaction and host response. Children and the elderly exhibit distinct patterns of antiviral response, which involve airway epithelium, mucociliary clearance, innate and adaptive immune cells, and inflammatory mediators. This review explores the pathogeneses of SARS-CoV-2 and influenza co-infection, focusing on the antiviral responses in children and the elderly. By comparing immature immunity in children and immune senescence in older adults, we aim to provide insights for the clinical management of severe co-infection cases.

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Kai-lin Mai, Wei-qi Pan, Zheng-shi Lin, Yang Wang, Zi-feng Yang. Pathogenesis of influenza and SARS-CoV-2 co-infection at the extremes of age: decipher the ominous tales of immune vulnerability. Advanced Biotechnology, 2025, 3(1): 5 DOI:10.1007/s44307-025-00057-9

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References

[1]

Achdout H, Vitner EB, Politi B, Melamed S, Yahalom-Ronen Y, Tamir H, et al.. Increased lethality in influenza and SARS-CoV-2 coinfection is prevented by influenza immunity but not SARS-CoV-2 immunity Nat Commun, 2021, 12(1): 5819.

[2]

Adams K, Tastad KJ, Huang S, Ujamaa D, Kniss K, Cummings C, et al.. Prevalence of SARS-CoV-2 and Influenza Coinfection and Clinical Characteristics Among Children and Adolescents Aged <18 Years Who Were Hospitalized or Died with Influenza - United States, 2021–22 Influenza Season MMWR Morb Mortal Wkly Rep, 2022, 71(50): 1589-1596.

[3]

Agrawal A, Gupta S. Impact of aging on dendritic cell functions in humans Ageing Res Rev, 2011, 10(3): 336-345.

[4]

Aksoy E, Albarani V, Nguyen M, Laes J-F, Ruelle J-L, De Wit D, et al.. Interferon regulatory factor 3-dependent responses to lipopolysaccharide are selectively blunted in cord blood cells Blood, 2007, 109(7): 2887-2893.

[5]

Aleebrahim-Dehkordi E, Molavi B, Mokhtari M, Deravi N, Fathi M, Fazel T, et al.. T helper type (Th1/Th2) responses to SARS-CoV-2 and influenza A (H1N1) virus: From cytokines produced to immune responses Transpl Immunol, 2022, 70: 101495.

[6]

Almanan M, Raynor J, Ogunsulire I, Malyshkina A, Mukherjee S, Hummel SA et al. IL-10-producing Tfh cells accumulate with age and link inflammation with age-related immune suppression. Sci Adv. 2020;6(31):eabb0806. https://doi.org/10.1126/sciadv.abb0806.

[7]

Atkin-Smith GK, Duan M, Chen W, Poon IKH. The induction and consequences of Influenza A virus-induced cell death Cell Death Dis, 2018, 9(10): 1002.

[8]

Baker PJ, Bohrer AC, Castro E, Amaral EP, Snow-Smith M, Torres-Juárez F, et al. The inflammatory microenvironment of the lung at the time of infection governs innate control of SARS-CoV-2 replication. BioRxiv . 2024. https://doi.org/10.1101/2024.03.27.586885.

[9]

Bartleson JM, Radenkovic D, Covarrubias AJ, Furman D, Winer DA, Verdin E. SARS-CoV-2, COVID-19 and the Ageing Immune System Nature Aging, 2021, 1(9): 769-782.

[10]

Benne CA, Kraaijeveld CA, van Strijp JA, Brouwer E, Harmsen M, Verhoef J, et al.. Interactions of surfactant protein A with influenza A viruses: binding and neutralization J Infect Dis, 1995, 171(2): 335-341.

[11]

Bolouri H, Speake C, Skibinski D, Long SA, Hocking AM, Campbell DJ, et al. The COVID-19 immune landscape is dynamically and reversibly correlated with disease severity. J Clin Invest. 2021;131(3). https://doi.org/10.1172/JCI143648.

[12]

Bonfante F, Costenaro P, Cantarutti A, Di Chiara C, Bortolami A, Petrara MR, et al. Mild SARS-CoV-2 infections and neutralizing antibody titers. Pediatrics. 2021;148(3). https://doi.org/10.1542/peds.2021-052173.

[13]

Brauning A, Rae M, Zhu G, Fulton E, Admasu TD, Stolzing A, et al. Aging of the immune system: focus on natural killer cells phenotype and functions. Cells. 2022;11(6). https://doi.org/10.3390/cells11061017.

[14]

Bunyavanich S, Do A, Vicencio A. Nasal Gene Expression of Angiotensin-Converting Enzyme 2 in Children and Adults JAMA, 2020, 323(23): 2427-2429.

[15]

Callaway E. COVID's future: mini-waves rather than seasonal surges Nature, 2023, 617(7960): 229-230.

[16]

Casanova JL, Abel L. From rare disorders of immunity to common determinants of infection: following the mechanistic thread Cell, 2022, 185(17): 3086-103.

[17]

Chason KD, Jaspers I, Parker J, Sellers S, Brighton LE, Hunsucker, SA, et al. Age-associated changes in the respiratory epithelial response to influenza infection. J Gerontol: Series A. 2018;73(12):1643–1650. https://doi.org/10.1093/gerona/gly126.

[18]

Chatta GS, Andrews RG, Rodger E, Schrag M, Hammond WP, Dale DC. Hematopoietic progenitors and aging: alterations in granulocytic precursors and responsiveness to recombinant human G-CSF, GM-CSF, and IL-3 J Gerontol, 1993, 48(5): M207-M212.

[19]

Cheemarla NR, Watkins TA, Mihaylova VT, Foxman EF. Viral Interference During Influenza A-SARS-CoV-2 Coinfection of the Human Airway Epithelium and Reversal by Oseltamivir J Infect Dis, 2024, 229(5): 1430-1434.

[20]

Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J, et al.. Inflammatory responses and inflammation-associated diseases in organs Oncotarget, 2018, 9(6): 7204-7218.

[21]

Cheng Y, Ma J, Wang H, Wang X, Hu Z, Li H, et al.. Co-infection of influenza A virus and SARS-CoV-2: A retrospective cohort study J Med Virol, 2021, 93(5): 2947-2954.

[22]

Chow EJ, Uyeki TM, Chu HY. The effects of the COVID-19 pandemic on community respiratory virus activity Nat Rev Microbiol, 2023, 21(3): 195-210.

[23]

Coates BM, Staricha KL, Wiese KM, Ridge KM. Influenza A Virus Infection, Innate Immunity, and Childhood JAMA Pediatr, 2015, 169(10): 956-963.

[24]

Corbett NP, Blimkie D, Ho KC, Cai B, Sutherland DP, Kallos A, et al.. Ontogeny of Toll-like receptor mediated cytokine responses of human blood mononuclear cells PLoS ONE, 2010, 5(11): e15041.

[25]

Costa, V.G.d., Gomes, A.J.C., Bittar, C., Geraldini, D.B., Previdelli da Conceição, P.J., Cabral, Á.S., et al. Burden of influenza and respiratory syncytial viruses in suspected COVID-19 patients: a cross-sectional and meta-analysis study. Viruses. 2023;15(3). https://doi.org/10.3390/v15030665.

[26]

Couceiro JN, Paulson JC, Baum LG. Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity Virus Res, 1993, 29(2): 155-165.

[27]

Dadashi M, Khaleghnejad S, Abedi Elkhichi P, Goudarzi M, Goudarzi H, Taghavi A, et al.. COVID-19 and influenza co-infection: a systematic review and meta-analysis Front Med, 2021, 8: 681469.

[28]

Danis B, George TC, Goriely S, Dutta B, Renneson J, Gatto L, et al.. Interferon regulatory factor 7-mediated responses are defective in cord blood plasmacytoid dendritic cells Eur J Immunol, 2008, 38(2): 507-517.

[29]

Dao TL, Hoang VT, Colson P, Million M, Gautret P. Co-infection of SARS-CoV-2 and influenza viruses: a systematic review and meta-analysis J Clin Virol Plus, 2021, 1(3): 100036.

[30]

Darbeheshti F, Mahdiannasser M, Uhal BD, Ogino S, Gupta S, Rezaei N. Interindividual immunogenic variants: susceptibility to coronavirus, respiratory syncytial virus and influenza virus Rev Med Virol, 2021, 31(6): e2234.

[31]

De Leeuw E, Hammad H. The role of dendritic cells in respiratory viral infection. Eur Respir Rev. 2024;33(172). https://doi.org/10.1183/16000617.0250-2023.

[32]

De Maeyer RPH, Chambers ES. The impact of ageing on monocytes and macrophages. Immunol Lett. 2021;230. https://doi.org/10.1016/j.imlet.2020.12.003.

[33]

De Maeyer RPH, van de Merwe RC, Louie R, Bracken OV, Devine OP, Goldstein DR, et al.. Blocking elevated p38 MAPK restores efferocytosis and inflammatory resolution in the elderly Nat Immunol, 2020, 21(6): 615-625.

[34]

Del Valle DM, Kim-Schulze S, Huang H-H, Beckmann ND, Nirenberg S, Wang B, et al.. An inflammatory cytokine signature predicts COVID-19 severity and survival Nat Med, 2020, 26(10): 1636-1643.

[35]

Di Cicco M, Kantar A, Masini B, Nuzzi G, Ragazzo V, Peroni D. Structural and functional development in airways throughout childhood: Children are not small adults Pediatr Pulmonol, 2021, 56(1): 240-251.

[36]

Diamond MS, Kanneganti TD. Innate immunity: the first line of defense against SARS-CoV-2 Nat Immunol, 2022, 23(2): 165-176.

[37]

Drew W, Wilson DV, Sapey E. Inflammation and neutrophil immunosenescence in health and disease: Targeted treatments to improve clinical outcomes in the elderly Exp Gerontol, 2018, 105: 70-77.

[38]

Ehre C, Worthington EN, Liesman RM, Grubb BR, Barbier D, O'Neal WK, et al.. Overexpressing mouse model demonstrates the protective role of Muc5ac in the lungs Proc Natl Acad Sci USA, 2012, 109(41): 16528-16533.

[39]

Esfehani RJ, Aelami MH, Kalat AR, Soleimanpour S, Pasdar Z, Khazaei M, et al.. SARS-CoV-2 Liability: The Hidden Mystery Behind Its Presentation in Children Adv Exp Med Biol, 2021, 1353: 225-241.

[40]

Eşki A, Öztürk GK, Çiçek C, Gülen F, Demir E. Is viral coinfection a risk factor for severe lower respiratory tract infection? A retrospective observational study Pediatr Pulmonol, 2021, 56(7): 2195-203.

[41]

Essaidi-Laziosi M, Alvarez C, Puhach O, Sattonnet-Roche P, Torriani G, Tapparel C, et al.. Sequential infections with rhinovirus and influenza modulate the replicative capacity of SARS-CoV-2 in the upper respiratory tract Emerg Microbes Infect, 2022, 11(1): 412-23.

[42]

Evren E, Ringqvist E, Willinger T. Origin and ontogeny of lung macrophages: from mice to humans Immunology, 2020, 160(2): 126-138.

[43]

Fage C, Hénaut M, Carbonneau J, Piret J, Boivin G. Influenza A(H1N1)pdm09 virus but not respiratory syncytial virus interferes with SARS-CoV-2 replication during sequential infections in human nasal epithelial cells. Viruses. 2022;14(2). https://doi.org/10.3390/v14020395.

[44]

Frasca D, Blomberg BB. Aging induces B cell defects and decreased antibody responses to influenza infection and vaccination Immun Ageing, 2020, 17(1): 37.

[45]

Garg I, Gangu K, Shuja H, Agahi A, Sharma H, Bobba A, et al. COVID-19 and influenza coinfection outcomes among hospitalized patients in the United States: a propensity matched analysis of national inpatient sample. Vaccines. 2022;10(12). https://doi.org/10.3390/vaccines10122159.

[46]

Georgountzou A, Papadopoulos NG. Postnatal Innate Immune Development: From Birth to Adulthood Front Immunol, 2017, 8: 957.

[47]

Grigg J, Riedler J, Robertson CF, Boyle W, Uren S. Alveolar macrophage immaturity in infants and young children Eur Respir J, 1999, 14(5): 1198-1205.

[48]

Grudzinska FS, Brodlie M, Scholefield BR, Jackson T, Scott A, Thickett DR, et al.. Neutrophils in community-acquired pneumonia: parallels in dysfunction at the extremes of age Thorax, 2020, 75(2): 164-171.

[49]

Guilmot A, Hermann E, Braud VM, Carlier Y, Truyens C. Natural killer cell responses to infections in early life J Innate Immun, 2011, 3(3): 280-288.

[50]

Harbeson D, Ben-Othman R, Amenyogbe N, Kollmann TR. Outgrowing the Immaturity Myth: The Cost of Defending From Neonatal Infectious Disease Front Immunol, 2018, 9: 1077.

[51]

Harris E. WHO Declares End of COVID-19 Global Health Emergency JAMA, 2023, 329(21): 1817.

[52]

Hartshorn KL, Webby R, White MR, Tecle T, Pan C, Boucher S, et al.. Role of viral hemagglutinin glycosylation in anti-influenza activities of recombinant surfactant protein D Respir Res, 2008, 9(1): 65.

[53]

Hashemi SA, Safamanesh S, Ghasemzadeh-Moghaddam H, Ghafouri M, Azimian A. High prevalence of SARS-CoV-2 and influenza A virus (H1N1) coinfection in dead patients in Northeastern Iran J Med Virol, 2021, 93(2): 1008-1012.

[54]

Heier I, Malmström K, Pelkonen AS, Malmberg LP, Kajosaari M, Turpeinen M, et al.. Bronchial response pattern of antigen presenting cells and regulatory T cells in children less than 2 years of age Thorax, 2008, 63(8): 703-709.

[55]

Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, et al. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2). https://doi.org/10.1016/j.cell.2020.02.052.

[56]

Isasi-Campillo M, Losada-Oliva P, Pérez-Gil J, Olmeda B, García-Ortega L. Pulmonary surfactant-derived antiviral actions at the respiratory surface Curr Opin Colloid Interface Sci, 2023, 66: 101711.

[57]

Jacob IB, Gemmiti A, Xiong W, Reynolds E, Nicholas B, Thangamani S, et al.. Human surfactant protein A inhibits SARS-CoV-2 infectivity and alleviates lung injury in a mouse infection model Front Immunol, 2024, 15: 1370511.

[58]

Jeican II, Gheban D, Mariș A, Albu S, Aluaș M, Siserman CV, et al. Flurona: the first autopsied case. Medicina (Kaunas, Lithuania). 2023;59(9). https://doi.org/10.3390/medicina59091616.

[59]

Jin K, Dai Z, Shi P, Li Y, Zhu C. Severe pneumonia with co-infection of H5N1 and SARS-CoV-2: a case report BMC Infect Dis, 2024, 24(1): 31.

[60]

Johansson C, Kirsebom FCM. Neutrophils in respiratory viral infections Mucosal Immunol, 2021, 14(4): 815-827.

[61]

Karron RA, Garcia Quesada M, Schappell EA, Schmidt SD, Deloria Knoll M, Hetrich MK, et al. Binding and neutralizing antibody responses to SARS-CoV-2 in very young children exceed those in adults. JCI Insight 2022;7(8). https://doi.org/10.1172/jci.insight.157963.

[62]

Kim EH, Nguyen TQ, Casel MAB, Rollon R, Kim SM, Kim YI, et al.. Coinfection with SARS-CoV-2 and influenza A virus increases disease severity and impairs neutralizing antibody and CD4+ T cell responses J Virol, 2022, 96(6): e0187321.

[63]

Kim MJ, Kim S, Kim H, Gil D, Han HJ, Thimmulappa RK, et al.. Reciprocal enhancement of SARS-CoV-2 and influenza virus replication in human pluripotent stem cell-derived lung organoids1 Emerg Microbes Infect, 2023, 12(1): 2211685.

[64]

Knoll R, Schultze JL, Schulte-Schrepping J. Monocytes and macrophages in COVID-19 Front Immunol, 2021, 12: 720109.

[65]

Kollmann TR, Crabtree J, Rein-Weston A, Blimkie D, Thommai F, Wang XY, et al. Neonatal innate TLR-mediated responses are distinct from those of adults. J Immunol (Baltimore, Md. : 1950). 2009;183(11):7150–7160. https://doi.org/10.4049/jimmunol.0901481.

[66]

Kollmann TR, Levy O, Montgomery RR, Goriely S. Innate immune function by Toll-like receptors: distinct responses in newborns and the elderly Immunity, 2012, 37(5): 771-783.

[67]

Krumbein H, Kümmel LS, Fragkou PC, Thölken C, Hünerbein BL, Reiter R, et al.. Respiratory viral co-infections in patients with COVID-19 and associated outcomes: a systematic review and meta-analysis Rev Med Virol, 2023, 33(1): e2365.

[68]

Kumar N, Sharma S, Barua S, Tripathi BN, Rouse BT. Virological and immunological outcomes of coinfections. Clin Microbiol Rev. 2018;31(4). https://doi.org/10.1128/CMR.00111-17.

[69]

Lee CH, Pinho MP, Buckley PR, Woodhouse IB, Ogg G, Simmons A, et al.. Potential CD8+ T cell cross-reactivity against SARS-CoV-2 conferred by other coronavirus strains Front Immunol, 2020, 11: 579480.

[70]

Li X, Li C, Zhang W, Wang Y, Qian P, Huang H. Inflammation and aging: signaling pathways and intervention therapies Signal Transduct Target Ther, 2023, 8(1): 239.

[71]

Lio D, Scola L, Crivello A, Colonna-Romano G, Candore G, Bonafè M, et al.. Gender-specific association between -1082 IL-10 promoter polymorphism and longevity Genes Immun, 2002, 3(1): 30-33.

[72]

Liu D, Leung K-Y, Lam H-Y, Zhang R, Fan Y, Xie X, et al.. Interaction and antiviral treatment of coinfection between SARS-CoV-2 and influenza in vitro Virus Res, 2024, 345: 199371.

[73]

Long JS, Mistry B, Haslam SM, Barclay WS. Host and viral determinants of influenza A virus species specificity Nat Rev Microbiol, 2019, 17(2): 67-81.

[74]

Ma S, Lai X, Chen Z, Tu S, Qin K. Clinical characteristics of critically ill patients co-infected with SARS-CoV-2 and the influenza virus in Wuhan China. Int J Infect Dis, 2020, 96: 683-7.

[75]

Maddux AB, Douglas IS. Is the developmentally immature immune response in paediatric sepsis a recapitulation of immune tolerance? Immunology. 2015;145(1). https://doi.org/10.1111/imm.12454.

[76]

Maltezou HC, Papanikolopoulou A, Vassiliu S, Theodoridou K, Nikolopoulou G, Sipsas NV. COVID-19 and respiratory virus co-infections: a systematic review of the literature. Viruses. 2023;15(4). https://doi.org/10.3390/v15040865.

[77]

Mazzoni A, Salvati L, Maggi L, Annunziato F, Cosmi L. Hallmarks of immune response in COVID-19: exploring dysregulation and exhaustion Semin Immunol, 2021, 55: 101508.

[78]

McAuley JL, Kedzierska K, Brown LE, Shanks GD. Host Immunological Factors Enhancing Mortality of Young Adults during the 1918 Influenza Pandemic Front Immunol, 2015, 6: 419.

[79]

Meade P, Kuan G, Strohmeier S, Maier HE, Amanat F, Balmaseda A, et al. Influenza virus infection induces a narrow antibody response in children but a broad recall response in adults. MBio. 2020;11(1). https://doi.org/10.1128/mBio.03243-19.

[80]

Mettelman RC, Allen EK, Thomas PG. Mucosal immune responses to infection and vaccination in the respiratory tract Immunity, 2022, 55(5): 749-780.

[81]

Mifsud EJ, Kuba M, Barr IG. Innate immune responses to influenza virus infections in the upper respiratory tract. Viruses. 2021;13(10). https://doi.org/10.3390/v13102090.

[82]

Moliva JI, Duncan MA, Olmo-Fontánez A, Akhter A, Arnett E, Scordo JM, et al.. The Lung Mucosa Environment in the Elderly Increases Host Susceptibility to Mycobacterium tuberculosis Infection J Infect Dis, 2019, 220(3): 514-523.

[83]

Moran TM, Isobe H, Fernandez-Sesma A, Schulman JL. Interleukin-4 causes delayed virus clearance in influenza virus-infected mice J Virol, 1996, 70(8): 5230-5235.

[84]

Munkholm M, Mortensen J. Mucociliary clearance: pathophysiological aspects Clin Physiol Funct Imaging, 2014, 34(3): 171-177.

[85]

Nagano A, Wakabayashi H, Maeda K, Kokura Y, Miyazaki S, Mori T, et al.. Respiratory Sarcopenia and Sarcopenic Respiratory Disability: Concepts, Diagnosis, and Treatment J Nutr Health Aging, 2021, 25(4): 507-515.

[86]

Narayanan M, Owers-Bradley J, Beardsmore CS, Mada M, Ball I, Garipov R, et al.. Alveolarization continues during childhood and adolescence: new evidence from helium-3 magnetic resonance Am J Respir Crit Care Med, 2012, 185(2): 186-191.

[87]

Nguyen M, Leuridan E, Zhang T, De Wit D, Willems F, Van Damme P, et al.. Acquisition of adult-like TLR4 and TLR9 responses during the first year of life PLoS ONE, 2010, 5(4): e10407.

[88]

Nguyen THO, Koutsakos M, van de Sandt CE, Crawford JC, Loh L, Sant S, et al.. Immune cellular networks underlying recovery from influenza virus infection in acute hospitalized patients Nat Commun, 2021, 12(1): 2691.

[89]

Nguyen L, McCord KA, Bui DT, Bouwman KM, Kitova EN, Elaish M, et al.. Sialic acid-containing glycolipids mediate binding and viral entry of SARS-CoV-2 Nat Chem Biol, 2022, 18(1): 81-90.

[90]

Nguyen THO, Rowntree LC, Chua BY, Thwaites RS, Kedzierska K. Defining the balance between optimal immunity and immunopathology in influenza virus infection Nat Rev Immunol, 2024.

[91]

Nicholls JM, Bourne AJ, Chen H, Guan Y, Peiris JSM. Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses Respir Res, 2007, 8(1): 73.

[92]

Oishi K, Horiuchi S, Minkoff JM, tenOever BR. The host response to influenza A virus interferes with SARS-CoV-2 replication during coinfection J Virol, 2022, 96(15): e0076522.

[93]

Pieren DKJ, Boer MC, de Wit J. The adaptive immune system in early life: the shift makes it count Front Immunol, 2022, 13: 1031924.

[94]

Pinky L, DeAguero JR, Remien CH, Smith AM. How interactions during viral-viral coinfection can shape infection kinetics. Viruses. 2023;15(6). https://doi.org/10.3390/v15061303.

[95]

Piret J, Boivin G. Viral Interference between Respiratory Viruses Emerg Infect Dis, 2022, 28(2): 273-281.

[96]

Prigge AD, Ma R, Coates BM, Singer BD, Ridge KM. Age-Dependent Differences in T-Cell Responses to Influenza A Virus Am J Respir Cell Mol Biol, 2020, 63(4): 415-423.

[97]

Quiñones-Parra SM, Clemens EB, Wang Z, Croom HA, Kedzierski L, McVernon J, et al.. A Role of Influenza Virus Exposure History in Determining Pandemic Susceptibility and CD8+ T Cell Responses J Virol, 2016, 90(15): 6936-6947.

[98]

Romero Starke K, Reissig D, Petereit-Haack G, Schmauder S, Nienhaus A, Seidler A. The isolated effect of age on the risk of COVID-19 severe outcomes: a systematic review with meta-analysis. BMJ Glob Health 2021;6(12). https://doi.org/10.1136/bmjgh-2021-006434.

[99]

Salminen A, Huuskonen J, Ojala J, Kauppinen A, Kaarniranta K, Suuronen T. Activation of innate immunity system during aging: NF-kB signaling is the molecular culprit of inflamm-aging Ageing Res Rev, 2008, 7(2): 83.

[100]

Schneider JL, Rowe JH, Garcia-de-Alba C, Kim CF, Sharpe AH, Haigis MC. The aging lung: Physiology, disease, and immunity Cell, 2021, 184(8): 1990-2019.

[101]

Scotta MC, Chakr VCBG, de Moura A, Becker RG, de Souza APD, Jones MH, et al.. Respiratory viral coinfection and disease severity in children: a systematic review and meta-analysis J Clin Virol, 2016, 80: 45-56.

[102]

Shannon I, White CL, Murphy A, Qiu X, Treanor JJ, Nayak JL. Differences in the influenza-specific CD4 T cell immunodominance hierarchy and functional potential between children and young adults Sci Rep, 2019, 9(1): 791.

[103]

Sievers BL, Cheng MTK, Csiba K, Meng B, Gupta RK. SARS-CoV-2 and innate immunity: the good, the bad, and the "goldilocks" Cell Mol Immunol, 2024, 21(2): 171-183.

[104]

Silva MG, Falcoff NL, Corradi GR, Di Camillo N, Seguel RF, Tabaj GC, et al.. Effect of age on human ACE2 and ACE2-expressing alveolar type II cells levels Pediatr Res, 2023, 93(4): 948-952.

[105]

Stockman LJ, Massoudi MS, Helfand R, Erdman D, Siwek AM, Anderson LJ, et al.. Severe acute respiratory syndrome in children Pediatr Infect Dis J, 2007, 26(1): 68-74.

[106]

Stocks J, Hislop A, Sonnappa S. Early lung development: lifelong effect on respiratory health and disease Lancet Respir Med, 2013, 1(9): 728-742.

[107]

Svyatchenko VA, Ternovoi VA, Lutkovskiy RY, Protopopova EV, Gudymo AS, Danilchenko NV, et al. Human adenovirus and influenza A virus exacerbate SARS-CoV-2 infection in animal models. Microorganisms. 2023;11(1). https://doi.org/10.3390/microorganisms11010180.

[108]

Thevaranjan N, Puchta A, Schulz C, Naidoo A, Szamosi JC, Verschoor CP, et al. Age-associated microbial dysbiosis promotes intestinal permeability, systemic inflammation, and macrophage dysfunction. Cell Host Microbe. 2017;21(4). https://doi.org/10.1016/j.chom.2017.03.002.

[109]

Tschernig T, de Vries VC, Debertin AS, Braun A, Walles T, Traub F, et al.. Density of dendritic cells in the human tracheal mucosa is age dependent and site specific Thorax, 2006, 61(11): 986-991.

[110]

Unione L, Moure MJ, Lenza MP, Oyenarte I, Ereño-Orbea J, Ardá A, et al. The SARS-CoV-2 spike glycoprotein directly binds exogeneous sialic acids: a NMR view. Angewandte Chemie (International Ed. In English). 2022;61(18):e202201432. https://doi.org/10.1002/anie.202201432.

[111]

Uyeki TM. Global epidemiology of human infections with highly pathogenic avian influenza A (H5N1) viruses. Respirology (Carlton, Vic.) 2008;13 Suppl 1:S2-S9. https://doi.org/10.1111/j.1440-1843.2008.01246.x.

[112]

Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: soldier in the fight against respiratory viruses Clin Microbiol Rev, 2011, 24(1): 210-229.

[113]

Villanueva JL, Solana R, Alonso MC, Peña J. Changes in the expression of HLA-class II antigens on peripheral blood monocytes from aged humans Dis Markers, 1990, 8(2): 85-91

[114]

Viveiros A, Gheblawi M, Aujla PK, Sosnowski DK, Seubert JM, Kassiri Z, et al.. Sex- and age-specific regulation of ACE2: Insights into severe COVID-19 susceptibility J Mol Cell Cardiol, 2022, 164: 13-16.

[115]

Wang S, Wang D. Co-circulation, Co-infection of SARS-CoV-2 and influenza virus, where will it go? Zoonoses. 2023;3(1). https://doi.org/10.15212/ZOONOSES-2023-0006.

[116]

Wang Y, Ma Q, Li M, Mai Q, Ma L, Zhang H, et al.. A decavalent composite mRNA vaccine against both influenza and COVID-19 Mbio, 2024, 15(9): e0066824.

[117]

Wang Z, Li S, Huang B. Alveolar macrophages: Achilles' heel of SARS-CoV-2 infection Signal Transduct Target Ther, 2022, 7(1): 242.

[118]

Welsh RM, Fujinami RS. Pathogenic epitopes, heterologous immunity and vaccine design Nat Rev Microbiol, 2007, 5(7): 555-563.

[119]

Wlodarczyk MF, Kraft AR, Chen HD, Kenney LL, Selin LK. Anti-IFN-γ and peptide-tolerization therapies inhibit acute lung injury induced by cross-reactive influenza A-specific memory T cells. J Immunol (Baltimore, Md. : 1950). 2013;190(6):2736–2746. https://doi.org/10.4049/jimmunol.1201936.

[120]

Xia S, Zhang X, Zheng S, Khanabdali R, Kalionis B, Wu J, et al.. An Update on Inflamm-Aging: Mechanisms, Prevention, and Treatment J Immunol Res, 2016, 2016: 8426874.

[121]

Yan X, Li K, Lei Z, Luo J, Wang Q, Wei S. Prevalence and associated outcomes of coinfection between SARS-CoV-2 and influenza: a systematic review and meta-analysis Int J Infect Dis, 2023, 136: 29-36.

[122]

Yang J, Gong Y, Zhang C, Sun J, Wong G, Shi W, et al. Co-existence and co-infection of influenza A viruses and coronaviruses: public health challenges. Innovation (Cambridge (Mass.)). 2022;3(5):100306. https://doi.org/10.1016/j.xinn.2022.100306.

[123]

You D, Ripple M, Balakrishna S, Troxclair D, Sandquist D, Ding L, et al. Inchoate CD8+ T cell responses in neonatal mice permit influenza-induced persistent pulmonary dysfunction. J Immunol (Baltimore, Md. : 1950). 2008;181(5):3486–3494.

[124]

Yu M, Charles A, Cagigi A, Christ W, Österberg B, Falck-Jones S, et al.. Delayed generation of functional virus-specific circulating T follicular helper cells correlates with severe COVID-19 Nat Commun, 2023, 14(1): 2164.

[125]

Yuan C, Ma Z, Xie J, Li W, Su L, Zhang G, et al.. The role of cell death in SARS-CoV-2 infection Signal Transduct Target Ther, 2023, 8(1): 357.

[126]

Yue H, Zhang M, Xing L, Wang K, Rao X, Liu H, et al.. The epidemiology and clinical characteristics of co-infection of SARS-CoV-2 and influenza viruses in patients during COVID-19 outbreak J Med Virol, 2020, 92(11): 2870-2873.

[127]

Yunis J, Short KR, Yu D. Severe respiratory viral infections: T-cell functions diverging from immunity to inflammation Trends Microbiol, 2023, 31(6): 644-656.

[128]

Zanin M, Baviskar P, Webster R, Webby R. The Interaction between Respiratory Pathogens and Mucus Cell Host Microbe, 2016, 19(2): 159-168.

[129]

Zanin M, Marathe B, Wong S-S, Yoon S-W, Collin E, Oshansky C, et al.. Pandemic Swine H1N1 Influenza Viruses with Almost Undetectable Neuraminidase Activity Are Not Transmitted via Aerosols in Ferrets and Are Inhibited by Human Mucus but Not Swine Mucus J Virol, 2015, 89(11): 5935-5948.

[130]

Zarkoob H, Allué-Guardia A, Chen YC, Garcia-Vilanova A, Jung O, Coon S, et al.. Modeling SARS-CoV-2 and influenza infections and antiviral treatments in human lung epithelial tissue equivalents Commun Biol, 2022, 5(1): 810.

[131]

Zhang AJ, Lee ACY, Chan JFW, Liu F, Li C, Chen Y, et al.. Coinfection by severe acute respiratory syndrome coronavirus 2 and influenza A(H1N1)pdm09 virus enhances the severity of pneumonia in golden Syrian hamsters Clin Infect Dis, 2021, 72(12): e978-92.

[132]

Zheng J, Chen F, Wu K, Wang J, Li F, Huang S, et al.. Clinical and virological impact of single and dual infections with influenza A (H1N1) and SARS-CoV-2 in adult inpatients PLoS Negl Trop Dis, 2021, 15(11): e0009997.

[133]

Zheng X, Wang H, Su Z, Li W, Yang D, Deng F, et al.. Co-infection of SARS-CoV-2 and influenza virus in early stage of the COVID-19 epidemic in Wuhan, China J Infect, 2020, 81(2): e128-9.

[134]

Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al.. A Novel Coronavirus from Patients with Pneumonia in China, 2019 N Engl J Med, 2020, 382(8): 727-733.

Funding

National Natural Science Foundation of China(82361168672)

National Natural Science Foundation of China(82174053)

National Natural Science Foundation of China(82341099)

Science and Technology Development Fund of Macau SAR, China(FDCT0111/2023/AFJ)

Science and Technology Development Fund of Macau SAR, China(005/2022/ALC)

Science and Technology Development Fund of Macau SAR, China(0045/2021/A)

Open Project of State Key Laboratory of Respiratory Disease(SKLRD-OP-202209)

Self-supporting Program of Guangzhou Laboratory(SRPG22-007)

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