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Analysis of the lung microbiome in the “healthy” smoker and in COPD.
Open accessAbstract
Although culture-independent techniques have shown that the lungs are not sterile, little is known about the lung microbiome in chronic obstructive pulmonary disease (COPD). We used pyrosequencing of 16S amplicons to analyze the lung microbiome in two ways: first, using bronchoalveolar lavage (BAL) to sample the distal bronchi and air-spaces; and second, by examining multiple discrete tissue sites in the lungs of six subjects removed at the time of transplantation. We performed BAL on three never-smokers (NS) with normal spirometry, seven smokers with normal spirometry ("healthy smokers", HS), and four subjects with COPD (CS). Bacterial 16 s sequences were found in all subjects, without significant quantitative differences between groups. Both taxonomy-based and taxonomy-independent approaches disclosed heterogeneity in the bacterial communities between HS subjects that was similar to that seen in healthy NS and two mild COPD patients. The moderate and severe COPD patients had very limited community diversity, which was also noted in 28% of the healthy subjects. Both approaches revealed extensive membership overlap between the bacterial communities of the three study groups. No genera were common within a group but unique across groups. Our data suggests the existence of a core pulmonary bacterial microbiome that includes Pseudomonas, Streptococcus, Prevotella, Fusobacterium, Haemophilus, Veillonella, and Porphyromonas. Most strikingly, there were significant micro-anatomic differences in bacterial communities within the same lung of subjects with advanced COPD. These studies are further demonstration of the pulmonary microbiome and highlight global and micro-anatomic changes in these bacterial communities in severe COPD patients.
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“Under certain conditions, Streptococcus gordonii can attack host fibronectin, and subsequent cytokine production can induce inflammatory responses (Erb-Downward et al., 2011; Liu et al., 2018).”
From Oral Microbiome and SARS-CoV-2: Beware of Lung Co-infection (2020) · cites this paper as Erb-Downward et al., 2011
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Lung Microbiome for Clinicians. New Discoveries about Bugs in Healthy and Diseased Lungs
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Significance of Anaerobes and Oral Bacteria in Community-Acquired Pneumonia
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“Furthermore, information regarding bacteria obtained in the past several years using new molecular biology techniques (16S quantitative PCR followed by pyrosequencing) has highlighted the existence and possible clinical roles of the microbiota of the lower respiratory tract in patients with chronic obstructive pulmona…”
BackgroundMammen, M. J., & Sethi, S. (2016) · Respirology · doi:10.1111/resp.12732 · Cited by 153
Panzer, A. R., Lynch, S. V., Langelier, C., Christie, J. D., McCauley, K. E., Nelson, M. F., Cheung, C. K., Benowitz, N. L., Cohen, M. J. M., & Calfee, C. S. (2017) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201702-0441oc · Cited by 157
Multicenter comparison of lung and oral microbiomes of HIV-infected and HIV-uninfected individuals.
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“Although sampling during surgery can approach a gold standard (9, 10), this methodology is BAL Negative”
MethodResultSelf-citationThe lung tissue microbiota of mild and moderate chronic obstructive pulmonary disease
Pragman, A. A., Lyu, T., Baller, J. A., Gould, T. J., Kelly, R. F., Reilly, C. S., Isaacson, R. E., & Wendt, C. H. (2018) · Microbiome · doi:10.1186/s40168-017-0381-4 · Cited by 150
“Two prior studies have analyzed the lung tissue microbiota of end-stage COPD at the time of lung transplantation [3, 21].”
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“However, immunologic conditions of the nasal and lung mucosa are not identical because the nasal mucosa is continuously exposed to various microorganisms and aeroallergens,whereas the lungmucosa is only occasionally infectedwith a fewmicrobes.(4,5) In addition, the type, number, and immunologic function of barrier epi…”
Profiling of lung microbiota discloses differences in adenocarcinoma and squamous cell carcinoma
Gomes, S. C. V., Cavadas, B., Ferreira, J. C., Marques, P., Monteiro, C., Sucena, M., Sousa, C., Rodrigues, L. V., Teixeira, G., Pinto, P., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-49195-w · Cited by 146
Metataxonomic and Metagenomic Approaches vs. Culture-Based Techniques for Clinical Pathology
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Chen, Y., Feng, W., Ye, K., Guo, L., Xia, H., Guan, Y., Chai, L., Shi, W., Zhai, C., Wang, J., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.541092 · Cited by 142
“Evidences have shown that lungs are accompanied with the shift in microbial composition and diversity during diseases (Willner et al., 2009; Hilty et al., 2010; Erb-Downward et al., 2011; Cho and Blaser, 2012).”
BackgroundWang, Z., Singh, R., Miller, B. E., Tal‐Singer, R., Horn, S. V., Tomsho, L., Mackay, A. J., Allinson, J. P., Webb, A. J., Brookes, A. J., et al. (2017) · Thorax · doi:10.1136/thoraxjnl-2017-210741 · Cited by 147
Bronchial microbiome of severe COPD patients colonised by Pseudomonas aeruginosa
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“Although the sputum may be contaminated by bacterial flora of the oropharynx and the oral cavity, the microbiome composition that we have found in severe COPD patients is quite similar to that of previous reports in healthy controls and COPD patients based on the use of bronchial brushing and bronchoalveolar lavage fo…”
ResultWu, B. G., Sulaiman, I., Tsay, J.-C. J., Perez, L., Franca, B., Li, Y., Wang, J., Gonzalez, A. N., El-Ashmawy, M., Carpenito, J., et al. (2020) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202005-1596oc · Cited by 137
Carmody, L. A., Zhao, J., Kalikin, L. M., LeBar, W., Simon, R. H., Venkataraman, A., Schmidt, T. M., Abdo, Z., Schloss, P. D., & LiPuma, J. J. (2015) · Microbiome · doi:10.1186/s40168-015-0074-9 · Cited by 135
“Recent studies have demonstrated that microbial communities vary over the spatial landscape of the diseased lung [14-17].”
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The role of metagenomics in understanding the human microbiome in health and disease
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Topographic Diversity of the Respiratory Tract Mycobiome and Alteration in HIV and Lung Disease
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“Two previous studies examined the bacterial lung microbiome in HIV-uninfected individuals with advanced COPD and found profound changes in the microbiome associated with lung dysfunction (40, 41).”
BackgroundIntestinal barrier: A gentlemen’s agreement between microbiota and immunity
Caricilli, A. M. (2014) · World Journal of Gastrointestinal Pathophysiology · doi:10.4291/wjgp.v5.i1.18 · Cited by 137
Biomarkers of progression of chronic obstructive pulmonary disease (COPD).
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“In general, tobacco smoking in the absence of COPD does not appear to alter the lung microbiome, but severe COPD is associated with less population diversity of resident bacterial communities, although even this result seems dependent on whether BAL or airway tissue is being sampled (96,103,106).”
Cox, M. J., Turek, E. M., Hennessy, C., Mirza, G. K., James, P. L., Coleman, M., Jones, A., Wilson, R., Bilton, D., Cookson, W., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170622 · Cited by 130
Arthritis susceptibility and the gut microbiome
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“Recent studies have suggested that lungs, considered sterile before, harbor microbiota that changes with conditions like chronic obstructive pulmonary disease [56].”
BackgroundThe Human Microbiota and Asthma
Heul, A. V., Planer, J. D., & Kau, A. L. (2018) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-018-8719-7 · Cited by 133
“Further microbial community specialization to regions within the lung are also likely: lung explants and post-mortem analyses of patients with cystic fibrosis and chronic obstructive pulmonary disease have demonstrated that unique communities can be discerned between different segments of the lung [56, 57].”
BackgroundBacterial-Host Interactions: Physiology and Pathophysiology of Respiratory Infection
Håkansson, A., Orihuela, C. J., & Bogaert, D. (2018) · Physiological Reviews · doi:10.1152/physrev.00040.2016 · Cited by 129
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“These samples carry their own caveat --- they are most often obtained from patients with end---stage disease, which have been shown to contain significant regional differences in community composition, and severely reduced diversity (30, 70, 71).”
Bacterial microbiome of lungs in COPD
Sin, D. D., Sze, M. A., & Hogg, J. C. (2014) · International Journal of COPD · doi:10.2147/copd.s38932 · Cited by 125
“17 However, they showed that there was significant heterogeneity and diversity in the bacterial microbiota across different regions of the same lung.”
InfluentialRepertoire of intensive care unit pneumonia microbiota
Bousbia, S., Papazian, L., Saux, P., Forel, J. M., Auffray, J.-P., Martin, C., Raoult, D., & La Scola, B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032486 · Cited by 118
“Our study agrees with the recent literature and highlights the existence of a core pulmonary microbiota, confirming the non-sterility of the lung [15, 16] .”
BackgroundResultInfluentialBlainey, P. C., Milla, C. E., Cornfield, D. N., & Quake, S. R. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3004458 · Cited by 120
Alterations of fecal bacterial communities in patients with lung cancer.
Zhang, W., Zhao, S., Luo, J., Dong, X., Hao, Y., Li, H., Shan, L., Zhou, Y., Shi, H., Zhang, Z.-Y., et al. (2018) · Europe PMC (PubMed Central) · Cited by 128
Hogan, D. A., Willger, S. D., Dolben, E. L., Hampton, T. H., Stanton, B. A., Morrison, H. G., Sogin, M. L., Czum, J. M., & Ashare, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149998 · Cited by 123
“This observation was similar to a pattern detected in the analysis of an explanted lung affected with COPD in which P. aeruginosa was found in the upper middle bronchus, but Stenotrophomonas was found in the distal bronchus from the same lung [59].”
BackgroundResultInfluentialPneumonia in Patients with Chronic Obstructive Pulmonary Disease
Restrepo, M. I., Sibila, O., & Anzueto, A. (2018) · Tuberculosis & respiratory diseases · doi:10.4046/trd.2018.0030 · Cited by 127
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“Thereafter, a cytokine response could be induced to promote inflammation and further lead to carcinogenesis (48, 49).”
BackgroundGut Microbiota Predict Pulmonary Infiltrates after Allogeneic Hematopoietic Cell Transplantation
Harris, B., Morjaria, S. M., Littmann, E. R., Geyer, A. I., Stover, D. E., Barker, J. N., Giralt, S., Taur, Y., & Pamer, E. G. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201507-1491oc · Cited by 116
Evaluation of the airway microbiome in nontuberculous mycobacteria disease
Sulaiman, I., Wu, B. G., Li, Y., Scott, A. S., Malecha, P. W., Scaglione, B. D., Wang, J., Basavaraj, A., Chung, S., Bantis, K., et al. (2018) · European Respiratory Journal · doi:10.1183/13993003.00810-2018 · Cited by 112
Sputum Microbiota Associated with New, Recurrent and Treatment Failure Tuberculosis
Wu, J., Liu, W., He, L., Huang, F., Chen, J., Cui, P., Shen, Y., Zhao, J., Wang, W., Zhang, Y., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083445 · Cited by 116
“16S rRNA sequencing [8], demonstrating that the lung is not sterile contrary to previous belief.”
BackgroundResultA Brave New World: The Lung Microbiota in an Era of Change
Segal, L. N., & Blaser, M. J. (2014) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201306-189mg · Cited by 122
Mechanistic insight into the function of the microbiome in lung diseases
Ubags, N. D. J., & Marsland, B. J. (2017) · European Respiratory Journal · doi:10.1183/13993003.02467-2016 · Cited by 109
Chronic bronchial infection in COPD. Is there an infective phenotype?
Matković, Z., & Miravitlles, M. (2012) · Respiratory Medicine · doi:10.1016/j.rmed.2012.10.024 · Cited by 109
“106 Further studies are clearly needed to understand the role of these microbiomes in healthy individuals and patients with COPD. Figure 1 The impact of microbial infection on the pathogenesis of COPD, both in the stable state and in exacerbations.”
BackgroundDual Role of Toll-Like Receptors in Asthma and Chronic Obstructive Pulmonary Disease
Bezemer, G. F. G., Sagar, S., van Bergenhenegouwen, J., Georgiou, N., Garssen, J., Kraneveld, A. D., & Folkerts, G. (2012) · Pharmacological Reviews · doi:10.1124/pr.111.004622 · Cited by 110
“, 2002; Erb-Downward et al., 2011). Cigarette smoking and airway obstruction are related to increased bacterial colonization of the distal airways (Zalacain et al., 1999). As early as 1999, Hasday et al. (1999) showed that LPS is present in the main stream, and to a lesser extent in the side stream, of cigarette smoke.”
BackgroundBiologics and the lung: TSLP and other epithelial cell-derived cytokines in asthma
Mitchell, P. D., & O’Byrne, P. M. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.06.009 · Cited by 113
“Once thought of as a sterile environment in health, the distal airway and lung have been shown to host a wide variety of microbes, now referred to as lung microbiome (Baughman et al., 1987; Charlson et al., 2011; Erb-Downward et al., 2011).”
Zakharkina, T., Heinzel, E., Koczulla, R. A., Greulich, T., Rentz, K., Pauling, J. K., Baumbach, J., Herrmann, M., Grünewald, C., Dienemann, H., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068302 · Cited by 112
“Representatives of the common oral microbiome were found in COPD patients and less in healthy individuals [14,15].”
BackgroundInfluentialBacteria isolated from lung modulate asthma susceptibility in mice
Rémot, A., Descamps, D., Noordine, M.-L., Boukadiri, A., Mathieu, E., Robert, V., Riffault, S., Lambrecht, B. N., Langella, P., Hammad, H., et al. (2017) · The ISME Journal · doi:10.1038/ismej.2016.181 · Cited by 115
“A bacterial community has been described in healthy human lungs (Charlson et al., 2011; Erb-Downward et al., 2011).”
BackgroundSu, Y.-C., Jalalvand, F., Thegerström, J., & Riesbeck, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02530 · Cited by 114
The sputum microbiome is distinct between COPD and health, independent of smoking history
Haldar, K., George, L., Wang, Z., Mistry, V., Ramsheh, M. Y., Free, R. C., John, C., Reeve, N. F., Miller, B. E., Tal‐Singer, R., et al. (2020) · Respiratory Research · doi:10.1186/s12931-020-01448-3 · Cited by 108
Microbial communities in the respiratory tract of patients with interstitial lung disease
Garzoni, C., Brugger, S. D., Qi, W., Wasmer, S., Cusini, A., Dumont, P., Gorgievski-Hrisoho, M., Mühlemann, K., von Garnier, C., & Hilty, M. (2013) · Thorax · doi:10.1136/thoraxjnl-2012-202917 · Cited by 107
The microbiota in pneumonia: From protection to predisposition
Thibeault, C., Suttorp, N., & Opitz, B. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.aba0501 · Cited by 111
“J. R. Erb-Downward, D. L. Thompson, M. K. Han, C. M. Freeman, L. McCloskey, L. A. Schmidt, V. B. Young, G. B. Toews, J. L. Curtis, B. Sundaram, F. J. Martinez, G. B. Huffnagle, Analysis of the lung microbiome in the "healthy" smoker and in COPD.”
BackgroundResultInfluentialMicrobiomes other than the gut: inflammaging and age-related diseases
Santoro, A., Zhao, J., Wu, L. H., Carru, C., Biagi, E., & Franceschi, C. (2020) · Seminars in Immunopathology · doi:10.1007/s00281-020-00814-z · Cited by 106
Dual Transcriptomic Profiling of Host and Microbiota during Health and Disease in Pediatric Asthma
Pérez‐Losada, M., Castro‐Nallar, E., Bendall, M. L., Freishtat, R. J., & Crandall, K. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131819 · Cited by 106
“, the airway microbiome [1–4].”
Microbiota abnormalities in inflammatory airway diseases — Potential for therapy
Gollwitzer, E. S., & Marsland, B. J. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.08.002 · Cited by 100
“0 been demonstrated that there are variations in bacterial composition within the same lung, dependent on the location of the tissue sampling (Erb-Downward et al., 2011).”
BackgroundResultInfluentialHuang, Y. J., & Lynch, S. V. (2011) · Expert Review of Respiratory Medicine · doi:10.1586/ers.11.76 · Cited by 103
“A comparison of the lower airway microbiota among patients with COPD, ‘healthy’ smokers without evidence of COPD and nonsmoking controls was performed by analysis of bronchoalveolar lavage fluid collected from 14 subjects (four with COPD, seven smokers with normal spirometry, and three healthy nonsmokers) [87].”
BackgroundMethodThe biology of pulmonary exacerbations in bronchiectasis
Amati, F., Simonetta, E., Gramegna, A., Tarsia, P., Contarini, M., Blasi, F., & Aliberti, S. (2019) · European Respiratory Review · doi:10.1183/16000617.0055-2019 · Cited by 107
Case Studies of the Spatial Heterogeneity of DNA Viruses in the Cystic Fibrosis Lung
Willner, D. L., Haynes, M. R., Furlan, M., Hanson, N., Kirby, B. K., Lim, Y. W., Rainey, P. B., Schmieder, R., Youle, M., Conrad, D., et al. (2011) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2011-0253oc · Cited by 102
Barker, B. L., Haldar, K., Patel, H., Pavord, I. D., Barer, M. R., Brightling, C. E., & Bafadhel, M. (2014) · CHEST Journal · doi:10.1378/chest.14-0764 · Cited by 101
Fraczek, M. G., Chishimba, L., Niven, R. M., Bromley, M., Simpson, A., Smyth, L. J. C., Denning, D. W., & Bowyer, P. (2017) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2017.09.039 · Cited by 105
“5 (30-68) 49 (19-65) 24 (22-62) 29 (22-58) .”
COPD and Gut–Lung Axis: How Microbiota and Host Inflammasome Influence COPD and Related Therapeutics
Qu, L., Cheng, Q., Wang, Y., Mu, H., & Zhang, Y. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.868086 · Cited by 104
Park, H., Shin, J. W., Park, S.-G., & Kim, W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109710 · Cited by 101
“To date, the relationship between airway microbiota and chronic respiratory diseases has been investigated only in lower airway samples such as sputum and bronchoalveolar lavage (BAL) samples [17,18,19].”
BackgroundThe respiratory microbiome: an underappreciated player in the human response to inhaled pollutants?
Adar, S. D., Huffnagle, G. B., & Curtis, J. L. (2016) · Annals of Epidemiology · doi:10.1016/j.annepidem.2016.03.010 · Cited by 88
“recently, however, the use of culture-independent, sequence-based techniques has clearly shown that the lungs are not sterile [13,14].”
Jin, J., Gan, Y., Liu, H., Wang, Z., Yuan, J., Deng, T., Zhou, Y., Zhu, Y., Zhu, H. L., Yang, S., et al. (2019) · Lung Cancer · doi:10.1016/j.lungcan.2019.08.022 · Cited by 97
Necrotizing enterocolitis: The intestinal microbiome, metabolome and inflammatory mediators
Neu, J., & Pammi, M. (2018) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2018.08.001 · Cited by 100
Effect of Advanced HIV Infection on the Respiratory Microbiome
Twigg, H. L., Knox, K. S., Zhou, J. J., Crothers, K. A., Nelson, D. E., Toh, E. C., Day, R. B., Lin, H., Gao, X., Dong, Q., et al. (2016) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201509-1875oc · Cited by 98
“However, use of cultureindependent microbial detection methods, such as 16S ribosomal RNA (rRNA) gene sequencing, has strongly suggested that a lung microbiome is present, both in healthy (1–3) and diseased (1, 4, 5) populations.”
Contribution of the Mucosal Microbiota to Bovine Respiratory Health
Zeineldin, M. M., Lowe, J. F., & Aldridge, B. M. (2019) · Trends in Microbiology · doi:10.1016/j.tim.2019.04.005 · Cited by 107
Human Pharyngeal Microbiome May Play A Protective Role in Respiratory Tract Infections
Gao, Z., Kang, Y., Yu, J. M., & Ren, L. (2014) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2014.06.001 · Cited by 100
“In patients with chronic RTIs, the defending frontier retreats from the throat to the trachea or bronchia as indicated by increased number of microbial sequences found in bronchoalveolar lavage fluid (BALF) and sputum samples [27,29].”
BackgroundIdiopathic subglottic stenosis is associated with activation of the inflammatory IL‐17A/IL‐23 axis
Gelbard, A. H., Katsantonis, N., Mizuta, M., Newcomb, D. C., Rotsinger, J. E., Rousseau, B., Daniero, J. J., Edell, E. S., Ekbom, D. C., Kasperbauer, J. L., et al. (2016) · The Laryngoscope · doi:10.1002/lary.26098 · Cited by 97
Jerkic, S., Brinkmann, F., Calder, A. D., Casey, A. M. H., Dishop, M. K., Griese, M., Kurland, G., Niemitz, M., Nyilas, S., Schramm, D., et al. (2020) · Canadian Respiratory Journal · doi:10.1155/2020/5852827 · Cited by 96
The Oral-Lung Axis: The Impact of Oral Health on Lung Health
Gaeckle, N. T., Pragman, A. A., Pendleton, K. M., Baldomero, A. K., & Criner, G. J. (2020) · Respiratory Care · doi:10.4187/respcare.07332 · Cited by 98
“An early study of the lung microbiome in subjects with advanced COPD showed that distinct microbiota could be identified within the same lung lobe based on micro-anatomic differences.(23) Another study of lung tissue obtained at the time of lung extirpation during transplantation also revealed notable shifts in the mi…”
BackgroundThe microbiome: Composition and locations
Kennedy, M. S., & Chang, E. B. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.08.013 · Cited by 108
Three Clinically Distinct Chronic Pediatric Airway Infections Share a Common Core Microbiota
Gast, C., Cuthbertson, L., Rogers, G. B., Pope, C. E., Marsh, R. L., Redding, G. J., Bruce, K. D., Chang, A. B., & Hoffman, L. R. (2014) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201312-456oc · Cited by 94
Cui, L., Morris, A., Huang, L., Beck, J. M., Twigg, H. L., von Mutius, E., & Ghedin, E. (2014) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201402-052pl · Cited by 95
The Lung Microbiome and Its Role in Pneumonia
Wu, B. G., & Segal, L. N. (2018) · Clinics in Chest Medicine · doi:10.1016/j.ccm.2018.07.003 · Cited by 92
The impact of lung microbiota dysbiosis on inflammation
Yang, D., Xing, Y., Song, X., & Qian, Y. (2019) · Immunology · doi:10.1111/imm.13139 · Cited by 100
Lung Microbiome in Asthma: Current Perspectives
Loverdos, K., Bellos, G., Kokolatou, L., Vasileiadis, I., Giamarellos‐Bourboulis, E. J., Pecchiari, M., Koulouris, N. G., Koutsoukou, A., & Rovina, N. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8111967 · Cited by 91
“at least in part, due to the small sizes of the relevant studies, the presence of considerable inter-subject variability in lung microbiota composition has been documented in healthy individuals [44,52], so that, to date, it is not possible to define a typical (“normal”) lung microbiome.”
BackgroundLung tissue microbial profile in lung cancer is distinct from emphysema.
Liu, Y., O’Brien, J. L., Ajami, N. J., Scheurer, M. E., Amirian, E. S., Armstrong, G., Tsavachidis, S., Thrift, A. P., Jiao, L., Wong, M. C., et al. (2018) · Europe PMC (PubMed Central) · Cited by 92
Ren, L., Zhang, R., Rao, J. Y., Xiao, Y., Zhang, Z., Yang, B., Cao, D., Zhong, H., Ning, P., Shang, Y., et al. (2018) · mSystems · doi:10.1128/msystems.00199-18 · Cited by 90
Microbial burden and viral exacerbations in a longitudinal multicenter COPD cohort
Bouquet, J., Tabor, D. E., Silver, J. S., Nair, V., Tovchigrechko, A., Griffin, M. P., Esser, M. T., Sellman, B. R., & Jin, H. (2020) · Respiratory Research · doi:10.1186/s12931-020-01340-0 · Cited by 94
“The lung microbiome is also personal, with large interpatient variability [48].”
BackgroundSze, M. A., Abbasi, M., Hogg, J. C., & Sin, D. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110351 · Cited by 91
“between the total bacterial load and COPD [1,16,20].”
BackgroundMethodAnalysis of the association between host genetics, smoking, and sputum microbiota in healthy humans
Lim, M. Y., Yoon, H. S., Rho, M., Sung, J., Song, Y.-M., Lee, K., & Ko, G. (2016) · Scientific Reports · doi:10.1038/srep23745 · Cited by 89
“by directly affecting the airway environment 9 , at this time few studies have assessed the links between smoking and the airway microbiota 4,10–12 , and little is known regarding how smoking affects a normal balanced microbiota.”
Cell-associated bacteria in the human lung microbiome
Dickson, R. P., Erb‐Downward, J. R., Prescott, H. C., Martínez, F. J., Curtis, J. L., Lama, V. N., & Huffnagle, G. B. (2014) · Microbiome · doi:10.1186/2049-2618-2-28 · Cited by 90
Mariani, J., Favero, C., Spinazzè, A., Cavallo, D. M., Carugno, M., Motta, V., Bonzini, M., Cattaneo, A., Pesatori, A. C., & Bollati, V. (2017) · Environmental Research · doi:10.1016/j.envres.2017.12.016 · Cited by 90
“As a matter of fact, Proteobacteria is a normally dominant taxa in the lung and in the nasal microbiota of children (Erb-Downward et al., 2011; Oh et al., 2012).”
BackgroundHost-Microbiome Interaction in Lung Cancer
Dong, Q., Chen, E. S., Zhao, C. N., & Jin, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.679829 · Cited by 94
Chronic obstructive pulmonary disease subpopulations and phenotyping
Segal, L. N., & Martínez, F. J. (2018) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2018.02.035 · Cited by 97
“77 Importantly, this phenotype is associated with greater extent of dyspnea, greater frequency of exacerbations, greater airway obstruction, and increased airway wall thickening.”
Microbiome diversity in the sputum of patients with pulmonary tuberculosis
Krishna, P., Jain, A., & Bisen, P. S. (2016) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-016-2654-4 · Cited by 85
Longitudinal analysis of the lung microbiome in lung transplantation
Borewicz, K., Pragman, A. A., Kim, H. B., Hertz, M., Wendt, C. H., & Isaacson, R. E. (2012) · FEMS Microbiology Letters · doi:10.1111/1574-6968.12053 · Cited by 88
“Proteobacteria, Firmicutes, Fusobacteria, and Bacteroidetes (genera Pseudomonas, Streptococcus, Veillonella, Fusobacterium, Prevotella, and Porphyromonas) most frequently in healthy lungs (Erb-Downward et al., 2011).”
BackgroundInfluentialLung inflammation and disease: A perspective on microbial homeostasis and metabolism
Méndez, R., Banerjee, S., Bhattacharya, S. K., & Banerjee, S. (2018) · IUBMB Life · doi:10.1002/iub.1969 · Cited by 86
“It is known that variable region (V) 1–3 amplification has better taxonomic coverage, while V4–5 region has higher specificity of detection (10, 19).”
BackgroundGupta, S., Shariff, M., Chaturvedi, G., Sharma, A., Goel, N., Yadav, M., Mortensen, M. S., Sørensen, S. J., Mukerji, M., & Chauhan, N. S. (2021) · Scientific Reports · doi:10.1038/s41598-021-83524-2 · Cited by 82
Miyasaka, E. A., Feng, Y., Poroyko, V. A., Falkowski, N. R., Erb‐Downward, J. R., Gillilland, M. G., Summers, K. L., Huffnagle, G. B., & Teitelbaum, D. H. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1201746 · Cited by 83
“Bacterial DNA was extracted using established methods (24).”
MethodMöller, D. R., Koth, L. L., Maier, L. A., Morris, A., Drake, W. P., Rossman, M. D., Leader, J. K., Collman, R. G., Hamzeh, N. Y., Sweiss, N., et al. (2015) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201503-172ot · Cited by 82
Oral and Airway Microbiota in HIV-Infected Pneumonia Patients
Iwai, S., Fei, M., Huang, D., Fong, S., Subramanian, A., Grieco, K., Lynch, S. V., & Huang, L. (2012) · Journal of Clinical Microbiology · doi:10.1128/jcm.00278-12 · Cited by 82
“The number of phyla detected in this study appears to be inflated compared to the numbers obtained via sequence-based efforts by other studies of these niches (5, 9, 19), for a number of reasons.”
ResultMicrobiome of the Paranasal Sinuses: Update and Literature Review
Lee, J. T., Frank, D. N., & Ramakrishnan, V. R. (2016) · American Journal of Rhinology and Allergy · doi:10.2500/ajra.2016.30.4255 · Cited by 82
Characterization of the upper and lower respiratory tract microbiota in Piedmontese calves
Nicola, I., Cerutti, F., Grego, E., Bertone, I., Gianella, P., D’Angelo, A., Peletto, S., & Bellino, C. (2017) · Microbiome · doi:10.1186/s40168-017-0372-5 · Cited by 92
Manavathu, E. K., Vager, D. L., & Vazquez, J. A. (2014) · BMC Microbiology · doi:10.1186/1471-2180-14-53 · Cited by 80
Wang, L., Cheng, H. M., Wang, D., Zhao, B., Zhang, J., Cheng, L., Yao, P., Narzo, A. D., Shen, Y., Yu, J., et al. (2018) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2018.09.079 · Cited by 80
Airway Microbial Community Turnover Differs by BPD Severity in Ventilated Preterm Infants
Wagner, B. D., Sontag, M. K., Harris, J. K., Miller, J., Morrow, L. A., Robertson, C. E., Stephens, M., Poindexter, B. B., Abman, S. H., & Mourani, P. M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0170120 · Cited by 82
Facciponte, D. N., Bough, M. W., Seidler, D., Carroll, J. L., Ashare, A., Andrew, A. S., Tsongalis, G. J., Vaickus, L. J., Henegan, P. L., Butt, T. H., et al. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.07.226 · Cited by 81
“They discovered that the healthy lung microbiome consists primarily of Pseudomonas, Streptococcus, Prevotella, Fusobacterium, Haemophilus, Veillonella, and Porphyromonas (Erb-Downward et al. 2011).”
Background
Metadata
- Authors
- Erb-Downward, J. R., Thompson, D. L., Han, M. K., Freeman, C. M., McCloskey, L., Schmidt, L. A., Young, V. B., Toews, G. B., Curtis, J. L., Sundaram, B., Martinez, F. J., & Huffnagle, G. B.
- Affiliations
- University of Michigan (US)
- Corresponding author
- Huffnagle, Gary B.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-02-22
- Volume
- 6
- Issue
- 2
- Pages
- e16384
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3043049
- OpenAlex
- W2163401084
- Cited by
- 973
- References
- 42
- Citations by year
- 2026: 32 · 2025: 50 · 2024: 59 · 2023: 66 · 2022: 73 · 2021: 57 · 2020: 74 · 2019: 62 · 2018: 85 · 2017: 80 · 2016: 75 · 2015: 72 · 2014: 68 · 2013: 57 · 2012: 49
- FWCI
- 50.74
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Veterans Affairs (R01 HL082480)
- University of Michigan (UL1 RR024986)
- National Institutes of Health (n01hr46162-13-0-1)
- Michigan Institute for Clinical and Health Research (UL 1RR024986)
- University of Michigan Comprehensive Cancer Center (P30 CA46952, CA46952)
- National Heart, Lung, and Blood Institute (R01HL082480, N01HR046162, T32HL007749)
- National Cancer Institute (P30 CA 46952)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK070875, RR024986, R01DK070875)
- National Center for Research Resources (UL1RR024986)
- Topics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Chronic Obstructive Pulmonary Disease (COPD) Research
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- lung microbiome, chronic obstructive pulmonary disease, healthy smokers, bronchoalveolar lavage, lung tissue sampling, bacterial community diversity, core microbiome, Pseudomonas, Streptococcus, Prevotella, Fusobacterium, Haemophilus, Veillonella, Porphyromonas, lung transplantation
- MeSH terms
- Adult, Aged, Bronchoalveolar Lavage Fluid, Bronchoscopy, DNA, Bacterial, Female, Health, Humans, Lung, Male, Middle Aged, RNA, Ribosomal, 16S, Smoking, Sequence Analysis, DNA, Pulmonary Disease, Chronic Obstructive, Metagenome
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