9.9
CiteScore
7.1
Impact Factor
Volume 51 Issue 10
Oct.  2024
Turn off MathJax
Article Contents
Abstract
References
Article Navigation >  Journal of Genetics and Genomics  > 2024  >  51(10): 1111-1120

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
  •  

    a. State Key Laboratory of Respiratory Disease, National Clinical Research Center for Respiratory Disease, National Center for Respiratory Medicine, Department of Allergy and Clinical Immunology, Guangdong Provincial Key Laboratory of Allergy & Clinical Immunology, Guangzhou Institute of Respiratory Health, The First Affiliated Hospital, Guangzhou Medical University, Guangzhou, Guangdong 510182, China;

  •  

    b. State Key Laboratory of Respiratory Disease Allergy Division at Shenzhen University, Shenzhen Key Laboratory of Allergy and Immunology, Shenzhen University, Shenzhen, Guangdong 518055, China

Funds:

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
    Abstract
  • 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.
    • FullText(HTML)
    • References(39)
  • 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.
    • Relative Articles

  • Relative Articles

    [1]Qiang Huang, Chaoliang Wen, Shuang Gu, Yuchen Jie, Guangqi Li, Yiyuan Yan, Chuanyao Tian, Guiqin Wu, Ning Yang. Synergy of gut microbiota and host genome in driving heterosis expression of chickens[J]. Journal of Genetics and Genomics, 2024, 51(10): 1121-1134. doi: 10.1016/j.jgg.2024.06.011
    [2]Boxun Zhang, Xuan Zhang, Zhen Luo, Jixiang Ren, Xiaotong Yu, Haiyan Zhao, Yitian Wang, Wenhui Zhang, Weiwei Tian, Xiuxiu Wei, Qiyou Ding, Haoyu Yang, Zishan Jin, Xiaolin Tong, Jun Wang, Linhua Zhao. Microbiome and metabolome dysbiosis analysis in impaired glucose tolerance for the prediction of progression to diabetes mellitus[J]. Journal of Genetics and Genomics, 2024, 51(1): 75-86. doi: 10.1016/j.jgg.2023.08.005
    [3]Qiao Meng, Jing Ning, Jingjing Lu, Jing Zhang, Ming Zu, Jing Zhang, Xiurui Han, Huiling Zheng, Yueqing Gong, Xinyu Hao, Ying Xiong, Fang Gu, Wenling Han, Weiwei Fu, Jun Wang, Shigang Ding. Cmtm4 deficiency exacerbates colitis by inducing gut dysbiosis and S100a8/9 expression[J]. Journal of Genetics and Genomics, 2024, 51(8): 811-823. doi: 10.1016/j.jgg.2024.03.009
    [4]Han Du, Zhongtao Du, Liang Wang, Hong Wang, Mingjun Jia, Chunge Zhang, Yun Liu, Cheng Zhang, Ya Zhang, Ruifeng Zhang, Shuang Zhang, Ning Zhang, Zhenghai Ma, Chen Chen, Wenjun Liu, Hui Zeng, George F. Gao, Xiaotong Hou, Yuhai Bi. Fulminant myocarditis induced by SARS-CoV-2 infection without severe lung involvement: insights into COVID-19 pathogenesis[J]. Journal of Genetics and Genomics, 2024, 51(6): 608-616. doi: 10.1016/j.jgg.2024.02.007
    [5]Chensi Yao, Xiaowen Gou, Chuanxi Tian, Lijuan Zhou, Rui Hao, Li Wan, Zeyu Wang, Min Li, Xiaolin Tong. Key regulators of intestinal stem cells: diet, microbiota, and microbial metabolites[J]. Journal of Genetics and Genomics, 2023, 50(10): 735-746. doi: 10.1016/j.jgg.2022.12.002
    [6]Changxu Chen, Xin Wang, Zeli Zhang. Humoral and cellular immunity against diverse SARS-CoV-2 variants[J]. Journal of Genetics and Genomics, 2023, 50(12): 934-947. doi: 10.1016/j.jgg.2023.10.003
    [7]Li Xu, Qiankun Zhang, Xiaowei Dou, Yipeng Wang, Jianwei Wang, Yong Zhou, Xingyin Liu, Jing Li. Fecal microbiota transplantation from young donor mice improves ovarian function in aged mice[J]. Journal of Genetics and Genomics, 2022, 49(11): 1042-1052. doi: 10.1016/j.jgg.2022.05.006
    [8]Xuezhen Liu, Miaoyan Shen, Han Yan, Pinpin Long, Haijing Jiang, Yizhi Zhang, Lue Zhou, Kuai Yu, Gaokun Qiu, Handong Yang, Xiulou Li, Xinwen Min, Meian He, Xiaomin Zhang, Hyungwon Choi, Chaolong Wang, Tangchun Wu. Alternations in the gut microbiota and metabolome with newly diagnosed unstable angina[J]. Journal of Genetics and Genomics, 2022, 49(3): 240-248. doi: 10.1016/j.jgg.2021.11.009
    [9]Zhengtu Li, Yinhu Li, Linghua Li, Xiaoneng Mo, Shaoqiang Li, Mingzhou Xie, Yangqing Zhan, Ye Lin, Zhun Li, Min Xie, Zhaoming Chen, Airu Zhu, Ruosu Ying, Le Yu, Jincun Zhao, Shuai Cheng Li, Weiping Cai, Feng Ye. Alteration of the respiratory microbiome in COVID-19 patients with different severities[J]. Journal of Genetics and Genomics, 2022, 49(3): 258-261. doi: 10.1016/j.jgg.2021.11.002
    [10]Chunbing Liu, Jingyang Hu, Yajiang Wu, David M. Irwin, Wu Chen, Zhigang Zhang, Li Yu. Comparative study of gut microbiota from captive and confiscated-rescued wild pangolins[J]. Journal of Genetics and Genomics, 2021, 48(9): 825-835. doi: 10.1016/j.jgg.2021.07.009
    [11]Zhiyao Lv, Rui Dai, Haoran Xu, Yongxin Liu, Bo Bai, Ying Meng, Haiyan Li, Xiaofeng Cao, Yang Bai, Xianwei Song, Jingying Zhang. The rice histone methylation regulates hub species of the root microbiota[J]. Journal of Genetics and Genomics, 2021, 48(9): 836-843. doi: 10.1016/j.jgg.2021.06.005
    [12]You Yu, Fangqing Zhao. Microbiota-gut-brain axis in autism spectrum disorder[J]. Journal of Genetics and Genomics, 2021, 48(9): 755-762. doi: 10.1016/j.jgg.2021.07.001
    [13]Suxian Lin, Tao Zhang, Lingxiao Zhu, Kun Pang, Saisai Lu, Xin Liao, Senhong Ying, Lixia Zhu, Xin Xu, Jinyu Wu, Xiaobing Wang. Characteristic dysbiosis in gout and the impact of a uric acid-lowering treatment, febuxostat on the gut microbiota[J]. Journal of Genetics and Genomics, 2021, 48(9): 781-791. doi: 10.1016/j.jgg.2021.06.009
    [14]Yeqiong Li, Yuwei Zhou, Pei Wang, Tao Tao, Lisha Wei, Ye Wang, Wei Wang, Yanyan Zheng, Zhihui Jiang, Tiantian Qiu, Wei Zhao, Jie Sun, Xin Chen, Xue-Na Zhang, Min-Sheng Zhu. LIMK2 is required for membrane cytoskeleton reorganization of contracting airway smooth muscle[J]. Journal of Genetics and Genomics, 2021, 48(6): 452-462. doi: 10.1016/j.jgg.2021.04.014
    [15]Rong Xu, Pengcheng Liu, Tao Zhang, Qunfu Wu, Mei Zeng, Yingying Ma, Xia Jin, Jin Xu, Zhigang Zhang, Chiyu Zhang. Progressive deterioration of the upper respiratory tract and the gut microbiomes in children during the early infection stages of COVID-19[J]. Journal of Genetics and Genomics, 2021, 48(9): 803-814. doi: 10.1016/j.jgg.2021.05.004
    [16]Qingrui Huang, Jiawei Zeng, Jinghua Yan. COVID-19 mRNA vaccines[J]. Journal of Genetics and Genomics, 2021, 48(2): 107-114. doi: 10.1016/j.jgg.2021.02.006
    [17]Paul D. Hartley, Richard L. Tillett, David P. AuCoin, Joel R. Sevinsky, Yanji Xu, Andrew Gorzalski, Mark Pandori, Erin Buttery, Holly Hansen, Michael A. Picker, Cyprian C. Rossetto, Subhash C. Verma. Genomic surveillance of Nevada patients revealed prevalence of unique SARS-CoV-2 variants bearing mutations in the RdRp gene[J]. Journal of Genetics and Genomics, 2021, 48(1): 40-51. doi: 10.1016/j.jgg.2021.01.004
    [18]Wanglong Gou, Yuanqing Fu, Liang Yue, Geng-Dong Chen, Xue Cai, Menglei Shuai, Fengzhe Xu, Xiao Yi, Hao Chen, Yi Zhu, Mian-Li Xiao, Zengliang Jiang, Zelei Miao, Congmei Xiao, Bo Shen, Xiaomai Wu, Haihong Zhao, Wenhua Ling, Jun Wang, Yu-Ming Chen, Tiannan Guo, Ju-Sheng Zheng. Gut microbiota, inflammation, and molecular signatures of host response to infection[J]. Journal of Genetics and Genomics, 2021, 48(9): 792-802. doi: 10.1016/j.jgg.2021.04.002
    [19]Xiaojuan Tan, Lin Liu, Shili Liu, Dongting Yang, Yikun Liu, Shuang Yang, Aiqun Jia, Nan Qin. Genome of Staphylococcus xylosus and Comparison with S. aureus and S. epidermidis[J]. Journal of Genetics and Genomics, 2014, 41(7): 413-416. doi: 10.1016/j.jgg.2014.03.007
    [20]Ya-juan Li, Bing Hu. Establishment of Multi-Site Infection Model in Zebrafish Larvae for Studying Staphylococcus aureus Infectious Disease[J]. Journal of Genetics and Genomics, 2012, 39(9): 521-534. doi: 10.1016/j.jgg.2012.07.006
    • Supplements(0)
    • Cited By

  • Cited by

    Periodical cited type(1)

    1. Lin, M., Xu, T., Li, J. et al. Annual advances in clinical studies of chronic cough (2024) | 慢性咳嗽年度进展2024. Chinese Journal of Tuberculosis and Respiratory Diseases, 2025, 48(2): 164–169.

    Other cited types(0)

  • Created with Highcharts 5.0.7Amount of accessChart context menuAbstract Views, HTML Views, PDF Downloads StatisticsAbstract ViewsHTML ViewsPDF Downloads2024-082024-092024-102024-112024-122025-012025-022025-032025-042025-052025-062025-0701234
    Created with Highcharts 5.0.7Chart context menuAccess Class DistributionFULLTEXT: 28.6 %FULLTEXT: 28.6 %META: 71.4 %META: 71.4 %FULLTEXTMETA
    Created with Highcharts 5.0.7Chart context menuAccess Area DistributionReserved: 14.3 %Reserved: 14.3 %United States: 85.7 %United States: 85.7 %ReservedUnited States

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索
    Get Citation
    PDF

    Article Metrics

    Article has an altmetric score of 1
    Article views (4) PDF downloads (0) Cited by (1)
    Proportional views
    Related

    Editorial Office

    Journal of Genetics and Genomics

    京ICP备09063187号-12

    No.1, West Beichen Road, Chaoyang District, Beijing 100101, P.R.China

    +86-10-64806528+86-10-64807786jgg@genetics.ac.cn

    Supported by: Beijing Renhe Information Technology Co. Ltd  

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return