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Review

The impact of infection with COVID-19 on the respiratory microbiome: A narrative review

, , ORCID Icon &
Pages 1076-1087 | Received 14 Jan 2022, Accepted 10 Jun 2022, Published online: 28 Jun 2022

References

  • Heymann DL, Shindo N. COVID-19: what is next for public health? Lancet. 2020;395:542–545.
  • Ferreira-Santos D, Maranhão P, Monteiro-Soares M. Identifying common baseline clinical features of COVID-19: a scoping review. BMJ Open. 2020;10:e041079.
  • Chen N, Zhou M, Dong X, et al. Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet. 2020;395:507–513.
  • Piva S, Filippini M, Turla F, et al. Clinical presentation and initial management critically ill patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in Brescia, Italy. J Crit Care. 2020;58:29–33.
  • Quah P, Li A, Phua J. Mortality rates of patients with COVID-19 in the intensive care unit: a systematic review of the emerging literature. Crit Care. 2020;24:1–4.
  • Gilbert JA, Blaser MJ, Caporaso JG, et al. Current understanding of the human microbiome. Nat Med. 2018;24:392–400.
  • Ogunrinola GA, Oyewale JO, Oshamika OO, et al. The human microbiome and its impacts on health. Int J Microbiol 2020. 2020;2020:7. https://doi.org/10.1155/2020/8045646
  • Shang J, Ye G, Shi K, et al. Structural basis of receptor recognition by SARS-CoV-2. Nature. 2020;581:221–224.
  • Segal JP, Mak JWY, Mullish BH, et al. The gut microbiome: an under-recognised contributor to the COVID-19 pandemic? Therap Adv Gastroenterol. 2020;13:1756284820974914.
  • Srinath BS, Shastry RP, Kumar SB. Role of gut-lung microbiome crosstalk in COVID-19. Res Biomed Eng. 2020;38:181–191. https://doi.org/10.1007/s42600-020-00113-4
  • Gu S, Chen Y, Wu Z, et al. Alterations of the gut microbiota in patients with coronavirus disease 2019 or H1N1 influenza. Clin Infect Dis. 2020;71:2669–2678.
  • Rosell A, Monsó E, Soler N, et al. Microbiologic determinants of exacerbation in chronic obstructive pulmonary disease. Arch Intern Med. 2005;165:891–897.
  • Thorpe JE, Baughman RP, Frame PT, et al. Bronchoalveolar lavage for diagnosing acute bacterial pneumonia. J Infect Dis. 1987;155:855–861.
  • Wang L, Hao K, Yang T, et al. Role of the lung microbiome in the pathogenesis of chronic obstructive pulmonary disease. Chin Med J (Engl). 2017;130:2107.
  • Huffnagle GB, Dickson RP, Lukacs NW. The respiratory tract microbiome and lung inflammation: a two-way street. Mucosal Immunol. 2017;10:299–306.
  • Mathieu E, Escribano-Vazquez U, Descamps D, et al. Paradigms of lung microbiota functions in health and disease, particularly, in asthma. Front Physiol. 2018;9:1168.
  • Yagi K, Huffnagle GB, Lukacs NW, et al. The lung microbiome during health and disease. Int J Mol Sci. 2021;22:10872.
  • Sze MA, Dimitriu PA, Hayashi S, et al. The lung tissue microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2012;185:1073–1080.
  • Dickson RP, Huffnagle GB, Goldman WE. The lung microbiome: new principles for respiratory bacteriology in health and disease. PLoS Pathog. 2015;11(7):e1004923.
  • Dickson RP, Martinez FJ, Huffnagle GB. The role of the microbiome in exacerbations of chronic lung diseases. Lancet. 2014;384:691–702.
  • Frayman KB, Armstrong DS, Carzino R, et al. The lower airway microbiota in early cystic fibrosis lung disease: a longitudinal analysis. Thorax. 2017;72:1104–1112.
  • Feigelman R, Kahlert CR, Baty F, et al. Sputum DNA sequencing in cystic fibrosis: non-invasive access to the lung microbiome and to pathogen details. Microbiome. 2017;5:1–14.
  • Laguna TA, Wagner BD, Williams CB, et al. Airway microbiota in bronchoalveolar lavage fluid from clinically well infants with cystic fibrosis. PLoS One. 2016;11:e0167649.
  • Millares L, Ferrari R, Gallego M, et al. Bronchial microbiome of severe COPD patients colonised by pseudomonas aeruginosa. Eur J Clin Microbiol Infect Dis. 2014;33:1101–1111.
  • Lee S-W, Kuan C-S, Ls-H W, et al. Metagenome and metatranscriptome profiling of moderate and severe COPD sputum in Taiwanese Han males. PLoS One. 2016;11:e0159066.
  • Teo SM, Mok D, Pham K, et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe. 2015;17:704–715.
  • Durack J, Lynch SV, Nariya S, et al. Features of the bronchial bacterial microbiome associated with atopy, asthma, and responsiveness to inhaled corticosteroid treatment. J Allergy Clin Immunol. 2017;140:63–75.
  • Denner DR, Sangwan N, Becker JB, et al. Corticosteroid therapy and airflow obstruction influence the bronchial microbiome, which is distinct from that of bronchoalveolar lavage in asthmatic airways. J Allergy Clin Immunol. 2016;137:1398–1405.
  • Yan X, Yang M, Liu J, et al. Discovery and validation of potential bacterial biomarkers for lung cancer. Am J Cancer Res. 2015;5:3111.
  • Liu H, Tao L, Zhang J, et al. Difference of lower airway microbiome in bilateral protected specimen brush between lung cancer patients with unilateral lobar masses and control subjects. Int J Cancer. 2018;142:769–778.
  • Lee SH, Sung JY, Yong D, et al. Characterization of microbiome in bronchoalveolar lavage fluid of patients with lung cancer comparing with benign mass like lesions. Lung Cancer. 2016;102:89–95.
  • Han MK, Zhou Y, Murray S, et al. Lung microbiome and disease progression in idiopathic pulmonary fibrosis: an analysis of the COMET study. Lancet Respir Med. 2014;2:548–556.
  • Molyneaux PL, Cox MJ, Wells AU, et al. Changes in the respiratory microbiome during acute exacerbations of idiopathic pulmonary fibrosis. Respir Res. 2017;18:1–6.
  • Molyneaux PL, Maher TM. The role of infection in the pathogenesis of idiopathic pulmonary fibrosis. Eur Respir Rev. 2013;22:376–381.
  • Molyneaux PL, Cox MJ, Willis-Owen SAG, et al. The role of bacteria in the pathogenesis and progression of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2014;190:906–913.
  • Muhlebach MS, Zorn BT, Esther CR, et al. Initial acquisition and succession of the cystic fibrosis lung microbiome is associated with disease progression in infants and preschool children. PLoS Pathog. 2018;14:e1006798.
  • Byun MK, Chang J, Kim HJ, et al. Differences of lung microbiome in patients with clinically stable and exacerbated bronchiectasis. PLoS One. 2017;12:e0183553.
  • Wypych TP, Wickramasinghe LC, Marsland BJ. The influence of the microbiome on respiratory health. Nat Immunol. 2019;20:1279–1290.
  • Huang YJ, Nariya S, Harris JM, et al. The airway microbiome in patients with severe asthma: associations with disease features and severity. J Allergy Clin Immunol. 2015;136:874–884.
  • Sze MA, Dimitriu PA, Suzuki M, et al. Host response to the lung microbiome in chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 2015;192:438–445.
  • Weinberg F, Dickson RP, Nagrath D, et al. The lung microbiome: a central mediator of host inflammation and Metabolism in lung cancer patients? Cancers (Basel). 2021;13:13.
  • Liang H, Li X, Yu X, et al. Facts and fiction of the relationship between preexisting tuberculosis and lung cancer risk: a systematic review. Int J Cancer. 2009;125:2936–2944.
  • Zhang R, Chen L, Cao L, et al. Effects of smoking on the lower respiratory tract microbiome in mice. Respir Res. 2018;19:1–15.
  • Panzer AR, Lynch SV, Langelier C, et al. Lung microbiota is related to smoking status and to development of acute respiratory distress syndrome in critically ill trauma patients. Am J Respir Crit Care Med. 2018;197:621–631.
  • Gregory AC, Sullivan MB, Segal LN, et al. Smoking is associated with quantifiable differences in the human lung DNA virome and metabolome. Respir Res. 2018;19:1–13.
  • Steed E, Balda MS, Matter K. Dynamics and functions of tight junctions. Trends Cell Biol. 2010;20:142–149.
  • Invernizzi R, Lloyd CM, Molyneaux PL. Respiratory microbiome and epithelial interactions shape immunity in the lungs. Immunology. 2020;160:171–182.
  • Hall MW, Joshi I, Leal L, et al. Immune modulation in COVID-19: strategic considerations for personalized therapeutic intervention. Clin Infect Dis. 2020;74(1):144-148. doi:10.1093/cid/ciaa904.
  • Whitsett JA, Alenghat T. Respiratory epithelial cells orchestrate pulmonary innate immunity. Nat Immunol. 2015;16:27–35.
  • Tay MZ, Poh CM, Rénia L, et al. The trinity of COVID-19: immunity, inflammation and intervention. Nat Rev Immunol. 2020;20:363–374.
  • Ou X, Liu Y, Lei X, et al. Characterization of spike glycoprotein of SARS-CoV-2 on virus entry and its immune cross-reactivity with SARS-CoV. Nat Commun. 2020;11:1–12.
  • Cantuti-Castelvetri L, Ojha R, Pedro LD, et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science. 2020;370:856–860.
  • Santos LD, Antunes KH, Muraro SP, et al. TNF-Mediated alveolar macrophage necroptosis drives disease pathogenesis during respiratory syncytial virus infection. Eur Respir J. 2021;57:1–41.
  • Antunes KH, Fachi JL, de Paula R, et al. Microbiota-Derived acetate protects against respiratory syncytial virus infection through a GPR43-type 1 interferon response. Nat Commun. 2019;10:1–17.
  • Martin TR, Frevert CW. Innate immunity in the lungs. Proc Am Thorac Soc. 2005;2:403–411.
  • Zhou Z, Ren L, Zhang LI, et al. Overly exuberant innate immune response to SARS-CoV-2 infection. 2020. https://doi.org/10.2139/ssrn.3551623
  • Zhou Z, Ren L, Zhang L, et al. Heightened innate immune responses in the respiratory tract of COVID-19 patients. Cell Host Microbe. 2020;27:883–890.
  • Liao M, Liu Y, Yuan J, et al. Single-Cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat Med. 2020;26:842–844.
  • Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395:497–506.
  • Jamilloux Y, Henry T, Belot A, et al. Should we stimulate or suppress immune responses in COVID-19? Cytokine and anti-cytokine interventions. Autoimmun Rev. 2020;19:102567.
  • Li G, Fan Y, Lai Y, et al. Coronavirus infections and immune responses. J Med Virol. 2020;92:424–432.
  • Seif F, Khoshmirsafa M, Aazami H, et al. The role of JAK-STAT signaling pathway and its regulators in the fate of T helper cells. Cell Commun Signal. 2017;15:1–13.
  • Azkur AK, Akdis M, Azkur D, et al. Immune response to SARS‐CoV‐2 and mechanisms of immunopathological changes in COVID‐19. Allergy. 2020;75:1564–1581.
  • Pavel AB, Glickman JW, Michels JR, et al. Th2/th1 cytokine imbalance is associated with higher COVID-19 risk mortality. Front Genet. 2021;12:706902. doi:10.3389/fgene.2021.706902.
  • Mazzoni A, Maggi L, Capone M, et al. Cell‐mediated and humoral adaptive immune responses to SARS‐CoV‐2 are lower in asymptomatic than symptomatic COVID‐19 patients. Eur J Immunol. 2020;50:2013–2024.
  • Qin C, Zhou L, Hu Z, et al. Dysregulation of immune response in patients with coronavirus 2019 (COVID-19) in Wuhan, China. Clin Infect Dis. 2020;71:762–768.
  • Kalfaoglu B, Almeida-Santos J, Tye CA, et al. T-Cell hyperactivation and paralysis in severe COVID-19 infection revealed by single-cell analysis. Front Immunol. 2020;11:2605.
  • Consortium HMP. Structure, function and diversity of the healthy human microbiome. Nature. 2012;486:207.
  • Tian Y, Sun K, Meng T, et al. Gut microbiota may not be fully restored in recovered COVID-19 patients after 3-month recovery. Front Nutr. 2021;8:182.
  • Ferreira C, Viana SD, Reis F. Is gut microbiota dysbiosis a predictor of increased susceptibility to poor outcome of COVID-19 patients? an update. Microorganisms. 2021;9:53.
  • Chen J, Vitetta L. Modulation of gut microbiota for the prevention and treatment of COVID-19. J Clin Med. 2021;10:2903.
  • Yeoh YK, Zuo T, Lui G-Y, et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut. 2021;70:698–706.
  • Zuo T, Zhang F, Lui GCY, et al. Alterations in gut microbiota of patients with COVID-19 during time of hospitalization. Gastroenterology. 2020;159:944–955.
  • Zuo T, Liu Q, Zhang F, et al. Depicting SARS-CoV-2 faecal viral activity in association with gut microbiota composition in patients with COVID-19. Gut. 2021;70:276–284.
  • Khan M, Mathew BJ, Gupta P, et al. Gut dysbiosis and IL-21 response in patients with severe COVID-19. Microorganisms. 2021;9:1292.
  • Moreira-Rosário A, Marques C, Pinheiro H, et al. Gut microbiota diversity and C-Reactive protein are predictors of disease severity in COVID-19 patients. bioRxiv. 2021;12:705020. doi:10.3389/fmicb.2021.705020.
  • Luu M, Weigand K, Wedi F, et al. Regulation of the effector function of CD8+ T cells by gut microbiota-derived metabolite butyrate. Sci Rep. 2018;8:1–10.
  • Zhou Y, Shi X, Fu W, et al. Gut microbiota dysbiosis correlates with abnormal immune response in moderate COVID-19 patients with fever. J Inflamm Res. 2021;14:2619.
  • Tao W, Zhang G, Wang X, et al. Analysis of the intestinal microbiota in COVID-19 patients and its correlation with the inflammatory factor IL-18. Med Microecol. 2020;5:100023.
  • Haiminen N, Utro F, Seabolt E, et al. Functional profiling of COVID-19 respiratory tract microbiomes. Sci Rep. 2021;11:1–8.
  • Törnquist K, Asghar MY, Srinivasan V, et al. Sphingolipids as modulators of SARS-CoV-2 infection. Front Cell Dev Biol. 2021;9:1574.
  • Santos AF, Póvoa P, Paixão P, et al. Changes in glycolytic pathway in SARS-COV 2 infection and their importance in understanding the severity of COVID-19. Front Chem. 2021;9:685196. doi:10.3389/fchem.2021.685196.
  • Codo AC, Davanzo GG, de Brito Monteiro L, et al. Elevated glucose levels favor SARS-CoV-2 infection and monocyte response through a HIF-1α/glycolysis-dependent axis. Cell Metab. 2020;32:437–446.
  • Viciani E, Gaibani P, Castagnetti A, et al. Critically ill patients with COVID-19 show lung fungal dysbiosis with reduced microbial diversity in patients colonized with Candida spp. Int J Infect Dis. 2022;117:233–240.
  • Calderaro A, Buttrini M, Montecchini S, et al. Detection of SARS-CoV-2 and other infectious agents in lower respiratory tract samples belonging to patients admitted to intensive care units of a tertiary-care hospital, located in an epidemic area, during the Italian lockdown. Microorganisms. 2021;9:185.
  • Zhong H, Wang Y, Shi Z, et al. Characterization of respiratory microbial dysbiosis in hospitalized COVID-19 patients. Cell Discov. 2021;7:1–14.
  • Hoque MN, Sarkar M, Hasan M, et al. SARS-CoV-2 infection reduces human nasopharyngeal commensal microbiome with inclusion of pathobionts. Sci Rep. 2021;11:1–17.
  • Hoque MN, Rahman MS, Ahmed R, et al. Diversity and genomic determinants of the microbiomes associated with COVID-19 and non-COVID respiratory diseases. Gene Rep. 2021;23:101200.
  • Hoque MN, Akter S, Mishu ID, et al. Microbial co-infections in COVID-19: associated microbiota and underlying mechanisms of pathogenesis. Microb Pathog. 2021;156:104941.
  • Lin X, Gong Z, Xiao Z, et al. Novel coronavirus pneumonia outbreak in 2019: computed tomographic findings in two cases. Korean J Radiol. 2020;21:365–368.
  • Man WH, de Steenhuijsen Piters WAA, Bogaert D. The microbiota of the respiratory tract: gatekeeper to respiratory health. Nat Rev Microbiol. 2017;15:259–270.
  • Mostafa HH, Fissel JA, Fanelli B, et al. Metagenomic next-generation sequencing of nasopharyngeal specimens collected from confirmed and suspect COVID-19 patients. Mbio. 2020;11: 1- 13.
  • Zhang H, Ai J-W, Yang W, et al. Metatranscriptomic characterization of Coronavirus disease 2019 identified a host transcriptional classifier associated with immune signaling. Clin Infect Dis. 2021;73:376–385.
  • Han Y, Jia Z, Shi J, et al. The active lung microbiota landscape of COVID-19 patients. medRxiv. 2020;2008.2020.20144014. doi:10.1101/2020.08.20.20144014.
  • Lloréns-Rico V, Gregory AC, Van Weyenbergh J, et al. Clinical practices underlie COVID-19 patient respiratory microbiome composition and its interactions with the host. Nat Commun. 2021;12:1–12.
  • Tsitsiklis A, Zha B, Byrne A, et al. Impaired immune signaling and changes in the lung microbiome precede secondary bacterial pneumonia in COVID-19. Res Sq 2021. doi:10.21203/rs.3.rs-380803/v1.
  • Maes M, Higginson E, Pereira-Dias J, et al. Ventilator-Associated pneumonia in critically ill patients with COVID-19. Crit Care. 2021;25:1–11.
  • Kolhe R, Sahajpal NS, Vyavahare S, et al. Alteration in nasopharyngeal microbiota profile in aged patients with COVID-19. Diagnostics. 2021;11:1622.
  • Liu J, Liu S, Zhang Z, et al. Association between the nasopharyngeal microbiome and metabolome in patients with COVID-19. Synth Syst Biotechnol. 2021;6:135-143.
  • Zhang L, Fan Y, Su H, et al. Chlorogenic acid methyl ester exerts strong anti-inflammatory effects via inhibiting the COX-2/NLRP3/NF-κB pathway. Food Funct. 2018;9:6155–6164.
  • Gaibani P, Viciani E, Bartoletti M, et al. The lower respiratory tract microbiome of critically ill patients with COVID-19. Sci Rep. 2021;11:1–11.
  • Merenstein C, Liang G, Whiteside SA, et al. Signatures of COVID-19 severity and immune response in the respiratory tract microbiome. mBio. 2021;12:e01777-21. https://doi.org/10.1128/mBio.01777-21
  • Iebba V, Zanotta N, Campisciano G, et al. Profiling of oral microbiota and cytokines in COVID-19 patients. Front Microbiol. 2021; 12:671813. doi:10.3389/fmicb.2021.671813.
  • Soffritti I, D’-Accolti M, Fabbri C, et al. Oral microbiome dysbiosis is associated with symptoms severity and local immune/inflammatory response in COVID-19 patients: a cross-sectional study. Front Microbiol. 2021;12:1397.
  • Langford BJ, So M, Raybardhan S, et al. Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis. Clin Microbiol Infect. 2020;26:1622-1629.
  • Lansbury L, Lim B, Baskaran V, et al. Co-Infections in people with COVID-19: a systematic review and meta-analysis. J Infect. 2020;81:266–275.
  • Zhu X, Ge Y, Wu T, et al. Co-Infection with respiratory pathogens among COVID-2019 cases. Virus Res. 2020;285:198005.
  • Conte L, Toraldo DM. Targeting the gut–lung microbiota axis by means of a high-fibre diet and probiotics may have anti-inflammatory effects in COVID-19 infection. Ther Adv Respir Dis. 2020;14:1753466620937170.
  • Li J, Zhao J, Wang X, et al. Novel angiotensin-converting enzyme-inhibitory peptides from fermented bovine milk started by Lactobacillus helveticus KLDS. 31 and Lactobacillus casei KLDS. 105: purification, identification, and interaction mechanisms. Front Microbiol. 2019;10:2643.
  • Minato T, Nirasawa S, Sato T, et al. B38-CAP is a bacteria-derived ACE2-like enzyme that suppresses hypertension and cardiac dysfunction. Nat Commun. 2020;11:1–12.
  • Ceccarelli G, Borrazzo C, Pinacchio C, et al. Oral bacteriotherapy in patients with COVID-19: a retrospective cohort study. Front Nutr. 2021;7:341.
  • Kumova OK, Fike AJ, Thayer JL, et al. Lung transcriptional unresponsiveness and loss of early influenza virus control in infected neonates is prevented by intranasal Lactobacillus rhamnosus GG. PLoS Pathog. 2019;15:e1008072.
  • Eguchi K, Fujitani N, Nakagawa H, et al. Prevention of respiratory syncytial virus infection with probiotic lactic acid bacterium Lactobacillus gasseri SBT2055. Sci Rep. 2019;9:1–11.
  • Liu F, Ye S, Zhu X, et al. Gastrointestinal disturbance and effect of fecal microbiota transplantation in discharged COVID-19 patients. J Med Case Rep. 2021;15:1–9.
  • Biliński J, Winter K, Jasiński M, et al. Rapid resolution of COVID-19 after faecal microbiota transplantation. Gut. 2022;71:230–232.
  • Munshi R, Hussein MH, Toraih EA, et al. Vitamin D insufficiency as a potential culprit in critical COVID‐19 patients. J Med Virol. 2021;93:733–740.