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Volume 51 Issue 10
Oct.  2024
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Article Contents

Alteration of the airway microbiota is associated with the progression of post-COVID-19 chronic cough in adults: a prospective study

doi: 10.1016/j.jgg.2024.06.015
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This study was supported by the Guangdong Basic and Applied Basic Research Foundation (2022B1515120055) and the National Natural Science Foundation of China (82341060 and 82170024).

  • Received Date: 2024-05-06
  • Accepted Date: 2024-06-20
  • Rev Recd Date: 2024-06-20
  • Available Online: 2025-06-06
  • Publish Date: 2024-07-01
  • Cough is one of the most common symptoms observed in patients presenting with COVID-19, persisting for an extended duration following SARS-CoV-2 infection. We aim to describe the distribution of airway microbiota and explore its role in patients with post-COVID-19 chronic cough. A total of 57 patients experiencing persistent cough after infection were recruited during the Omicron wave of SARS-CoV-2 in China. Airway microbiota profiling is assessed in nasopharyngeal swab, nasal lavage, and induced sputum samples at 4 and 8 weeks after SARS-CoV-2 infection. Our findings reveal that bacterial families Staphylococcaceae, Corynebacteriaceae, and Enterobacteriaceae are the most prevalent in the upper airway, while Streptococcaceae, Lachnospiraceae, and Prevotellaceae emerge as the most prevalent bacterial families in the lower airway. An increase in the abundance of Staphylococcus in nasopharyngeal swab samples and of Streptococcus in induced sputum samples is observed after one month. Furthermore, the abundance of Staphylococcus identified in nasopharyngeal swab samples at the baseline period emerges as an insightful predictor for improvement in cough severity. In conclusion, dynamic alterations in the airway microbial composition may contribute to the post-COVID-19 chronic cough progression, while the compositional signatures of nasopharyngeal microbiota could reflect the improvement of this disease.
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  • Asseri, A.A., Khattab, N., Ezmigna, D., Awadalla, N.J., Daines, C.,Morgan, W., 2021. Diagnostic accuracy of nasopharyngeal swab cultures in children less than five years with chronic wet cough. Children 8, 1161.
    Baj, J., Karakula-Juchnowicz, H., Teresinski, G., Buszewicz, G., Ciesielka, M., Sitarz, R., Forma, A., Karakula, K., Flieger, W., Portincasa, P., et al., 2020. COVID-19: specific and non-specific clinical manifestations and symptoms: the current state of knowledge. J. Clin. Med. 9, 1753.
    Bock, J.M., Koszewski, I.J., Blumin, J.H., Toohill, R.J., Merati, A.L., Prieto, T.E.,Jaradeh, S.S., 2014. Surface-evoked laryngeal sensory action potential evaluation in neurogenic chronic cough. J. Voice 28, 624-630.
    Budding, A., Sieswerda, E., Wintermans, B.,Bos, M., 2020. An age dependent pharyngeal microbiota signature associated with SARS-CoV-2 infection. SSRN Electron. J., 3582780.
    Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.,Holmes, S.P., 2016. DADA2: high-resolution sample inference from illumina amplicon data. Nat. Methods 13, 581-583.
    Davison, V.E.,Sanford, B.A., 1981. Adherence of staphylococcus aureus to influenza a virus-infected madin-darby canine kidney cell cultures. Infect. Immun. 32, 118-126.
    De Maio, F., Posteraro, B., Ponziani, F.R., Cattani, P., Gasbarrini, A.,Sanguinetti, M., 2020. Nasopharyngeal microbiota profiling of SARS-CoV-2 infected patients. Biol. Proced. Online 22, 18.
    Dickson, R.P., Erb-Downward, J.R.,Huffnagle, G.B., 2015. Homeostasis and its disruption in the lung microbiome. Am. J. Physiol. Lung Cell Mol. Physiol. 309, L1047-L1055.
    Gao, M., Wang, H., Luo, H., Sun, Y., Wang, L., Ding, S., Ren, H., Gang, J., Rao, B., Liu, S., et al., 2021. Characterization of the human oropharyngeal microbiomes in SARS-CoV-2 infection and recovery patients. Adv. Sci. 8, e2102785.
    Giugliano, R., Sellitto, A., Ferravante, C., Rocco, T., D'Agostino, Y., Alexandrova, E., Lamberti, J., Palumbo, D., Galdiero, M., Vaccaro, E., et al., 2022. NGS analysis of nasopharyngeal microbiota in SARS-CoV-2 positive patients during the first year of the pandemic in the campania region of Italy. Microb. Pathog. 165, 105506.
    Grayson, K.M., Blevins, L.K., Oliver, M.B., Ornelles, D.A., Swords, W.E.,Alexander-Miller, M.A., 2017. Activation-dependent modulation of streptococcus pneumoniae-mediated death in human lymphocytes. Pathog. Dis. 75, ftx008.
    Guo, M.Y., Chen, H.K., Ying, H.Z., Qiu, F.S.,Wu, J.Q., 2021. The role of respiratory flora in the pathogenesis of chronic respiratory diseases. BioMed Res. Int. 2021, 6431862.
    Hare, K.M., Chang, A.B., Smith-Vaughan, H.C., Bauert, P.A., Spain, B., Beissbarth, J.,Grimwood, K., 2019. Do combined upper airway cultures identify lower airway infections in children with chronic cough? Pediatr. Pulmonol. 54, 907-913.
    Ioannidis, J.P.A., Zonta, F.,Levitt, M., 2023. Estimates of COVID-19 deaths in mainland China after abandoning zero COVID policy. Eur. J. Clin. Investig. 53, e13956.
    Ito, K.,Murphy, D., 2013. Application of ggplot2 to pharmacometric graphics. CPT Pharmacomet. Syst. Pharmacol. 2, e79.
    Jones, R.M., Hilldrup, S., Hope-Gill, B.D., Eccles, R.,Harrison, N.K., 2011. Mechanical induction of cough in idiopathic pulmonary fibrosis. Cough 7, 2.
    Lee, J.T., Kim, C.M.,Ramakrishnan, V., 2019. Microbiome and disease in the upper airway. Curr. Opin. Allergy Clin. Immunol. 19, 1-6.
    Li, Z., Li, Y., Li, L., Mo, X., Li, S., Xie, M., Zhan, Y., Lin, Y., Li, Z., Xie, M., et al., 2022. Alteration of the respiratory microbiome in COVID-19 patients with different severities. J. Genet. Genom. 49, 258-261.
    Lim, M.C., Taylor, R.M.,Naclerio, R.M., 1995. The histology of allergic rhinitis and its comparison to cellular changes in nasal lavage. Am. J. Respir. Crit. Care Med. 151, 136-144.
    Mallick, H., Rahnavard, A., McIver, L.J., Ma, S., Zhang, Y., Nguyen, L.H., Tickle, T.L., Weingart, G., Ren, B., Schwager, E.H., et al., 2021. Multivariable association discovery in population-scale meta-omics studies. PLoS Comput. Biol. 17, e1009442.
    Marsh, R.L., Smith-Vaughan, H.C., Chen, A.C.H., Marchant, J.M., Yerkovich, S.T., Gibson, P.G., Pizzutto, S.J., Hodge, S., Upham, J.W.,Chang, A.B., 2019. Multiple respiratory microbiota profiles are associated with lower airway inflammation in children with protracted bacterial bronchitis. Chest 155, 778-786.
    Mo, X., Jian, W., Su, Z., Chen, M., Peng, H., Peng, P., Lei, C., Chen, R., Zhong, N.,Li, S., 2020. Abnormal pulmonary function in COVID-19 patients at time of hospital discharge. Eur. Respir. J. 55, 2001217.
    Musuuza, J.S., Watson, L., Parmasad, V., Putman-Buehler, N., Christensen, L.,Safdar, N., 2021. Prevalence and outcomes of co-infection and superinfection with SARS-CoV-2 and other pathogens: a systematic review and meta-analysis. PLoS One 16, e0251170.
    Nusair, S., 2020. Abnormal carbon monoxide diffusion capacity in COVID-19 patients at time of hospital discharge. Eur. Respir. J. 56, 2001832.
    Ramsey, B.W., Wentz, K.R., Smith, A.L., Richardson, M., Williams-Warren, J., Hedges, D.L., Gibson, R., Redding, G.J., Lent, K.,Harris, K., 1991. Predictive value of oropharyngeal cultures for identifying lower airway bacteria in cystic fibrosis patients. Am. Rev. Respir. Dis. 144, 331-337.
    Romani, L., Del Chierico, F., Macari, G., Pane, S., Ristori, M.V., Guarrasi, V., Gardini, S., Pascucci, G.R., Cotugno, N., Perno, C.F., et al., 2022. The relationship between pediatric gut microbiota and SARS-CoV-2 infection. Front. Cell. Infect. Microbiol. 12, 908492.
    Rossi, G.A., Fanous, H.,Colin, A.A., 2020. Viral strategies predisposing to respiratory bacterial superinfections. Pediatr. Pulmonol. 55, 1061-1073.
    Rueca, M., Fontana, A., Bartolini, B., Piselli, P., Mazzarelli, A., Copetti, M., Binda, E., Perri, F., Gruber, C.E.M., Nicastri, E., et al., 2021. Investigation of nasal/oropharyngeal microbial community of COVID-19 patients by 16s rDNA sequencing. Int. J. Environ. Res. Public Health 18, 2174.
    Schult, D., Reitmeier, S., Koyumdzhieva, P., Lahmer, T., Middelhoff, M., Erber, J., Schneider, J., Kager, J., Frolova, M., Horstmann, J., et al., 2022. Gut bacterial dysbiosis and instability is associated with the onset of complications and mortality in COVID-19. Gut Microb. 14, 2031840.
    Scialo, F., Daniele, A., Amato, F., Pastore, L., Matera, M.G., Cazzola, M., Castaldo, G.,Bianco, A., 2020. ACE2: the major cell entry receptor for SARS-CoV-2. Lung 198, 867-877.
    Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S.,Huttenhower, C., 2011. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60.
    Sencio, V., Machelart, A., Robil, C., Benech, N., Hoffmann, E., Galbert, C., Deryuter, L., Heumel, S., Hantute-Ghesquier, A., Flourens, A., et al., 2022. Alteration of the gut microbiota following SARS-CoV-2 infection correlates with disease severity in hamsters. Gut Microbes 14, 2018900.
    Smith, A.M.,McCullers, J.A., 2014. Secondary bacterial infections in influenza virus infection pathogenesis. Curr. Top. Microbiol. Immunol. 385, 327-356.
    Song, W.J., Hui, C.K.M., Hull, J.H., Birring, S.S., McGarvey, L., Mazzone, S.B.,Chung, K.F., 2021. Confronting COVID-19-associated cough and the post-covid syndrome: role of viral neurotropism, neuroinflammation, and neuroimmune responses. Lancet Respir. Med. 9, 533-544.
    Ventero, M.P., Cuadrat, R.R.C., Vidal, I., Andrade, B.G.N., Molina-Pardines, C., Haro-Moreno, J.M., Coutinho, F.H., Merino, E., Regitano, L.C.A., Silveira, C.B., et al., 2021. Nasopharyngeal microbial communities of patients infected with SARS-CoV-2 that developed COVID-19. Front. Microbiol. 12, 637430.
    Wilkinson, T.M.A., Aris, E., Bourne, S., Clarke, S.C., Peeters, M., Pascal, T.G., Schoonbroodt, S., Tuck, A.C., Kim, V., Ostridge, K., et al., 2017. A prospective, observational cohort study of the seasonal dynamics of airway pathogens in the aetiology of exacerbations in COPD. Thorax 72, 919-927.
    Xiang, L., Zhou, T.J., Zhou, L.L., Luo, J., Qin, Z., You, J.Z., Jian, J., Zhao, Z.Y., Zhou, Y.S., Ye, Y.C., et al., 2019. Influenza a virus and streptococcus pneumonia coinfection potentially promotes bacterial colonization and enhances B lymphocyte depression and reduction. J. Biol. Regul. Homeost. Agents 33, 1437-1449.
    Yagi, K., Huffnagle, G.B., Lukacs, N.W.,Asai, N., 2021. The lung microbiome during health and disease. Int. J. Mol. Sci. 22, 10872.
    Yang, Z., Chen, Z., Lin, X., Yao, S., Xian, M., Ning, X., Fu, W., Jiang, M., Li, N., Xiao, X., et al., 2022. Rural environment reduces allergic inflammation by modulating the gut microbiota. Gut Microbes 14, 2125733.
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