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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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BackgroundResultMicrobiome dysbiosis in cancer: Exploring therapeutic strategies to counter the disease
Sharma, V., Singh, M. P., Kumar, V., Yadav, M. K., Sehrawat, N., Sharma, D. K., & Sharma, A. K. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.07.006 · Cited by 49
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BackgroundRespiratory microbiota and lower respiratory tract disease
Lanaspa, M., Bassat, Q., Medeiros, M. M., & Muñoz‐Almagro, C. (2017) · Expert Review of Anti-infective Therapy · doi:10.1080/14787210.2017.1349609 · Cited by 48
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Chung, K. F. (2017) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201702-138aw · Cited by 48
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Yi, B., Dalpke, A. H., & Boutin, S. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.548613 · Cited by 44
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BackgroundDumont-Leblond, N., Veillette, M., Racine, C., Joubert, P., & Duchaine, C. (2021) · PLoS ONE · doi:10.1371/journal.pone.0249832 · Cited by 49
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“However, bacterial DNA was commonly detected in lower respiratory tract, despite at a low-biomass (5 e 8.25 log copies/mL) 39,40 .”
BackgroundInfluentialThe respiratory microbiome and nontuberculous mycobacteria: an emerging concern in human health
Thornton, C. S., Mellett, M., Jarand, J. M., Barss, L., Field, S. K., & Fisher, D. A. (2021) · European Respiratory Review · doi:10.1183/16000617.0299-2020 · Cited by 44
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Host–microbe interactions in distal airways: relevance to chronic airway diseases
Martin, C., Burgel, P., Lepage, P., Andréjak, C., Jacques de, B. L. I. C., BOURDIN, A. A., Brouard, J., Chanez, P., Dalphin, J., Deslée, G., et al. (2015) · European Respiratory Review · doi:10.1183/09059180.00011614 · Cited by 48
Protected sampling is preferable in bronchoscopic studies of the airway microbiome
Grønseth, R., Drengenes, C., Wiker, H. G., Tangedal, S., Xue, Y., Husebø, G. R., Svanes, Ø., Lehmann, S., Aardal, M. E., Hoang, T., et al. (2017) · ERJ Open Research · doi:10.1183/23120541.00019-2017 · Cited by 48
Smoking is associated with quantifiable differences in the human lung DNA virome and metabolome
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Metagenome and Metatranscriptome Profiling of Moderate and Severe COPD Sputum in Taiwanese Han Males
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“The lack of significant differences between the moderate and severe COPD samples is similar to the study by Erb-Downward et al [41], in which high variations between different lungs tissue samples and individuals were found.”
ResultLung Microbiome in Idiopathic Pulmonary Fibrosis and Other Interstitial Lung Diseases
Amati, F., Stainer, A., Mantero, M., Gramegna, A., Simonetta, E., Suigo, G., Voza, A., Nambiar, A. M., Cariboni, U., Oldham, J. M., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020977 · Cited by 47
“Moreover, considerable topographic heterogeneity has been observed in the bacterial communities of lung patients with end-stage diseases [24,25].”
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“Previous studies using 16S ribosomal RNA microarray comparing the lung microbiome of smokers with non-smokers have reported either no differences, 34,35 or a higher abundance of Veillonella and Megasphaera with a decrease in Haemophilus .”
Lung antimicrobial proteins and peptides: from host defense to therapeutic strategies
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“The functional role and implications of the lung microbiota are unknown at this point, but this is a promising avenue for future investigations, particularly given the recent literature that has linked microbiota in the lung with healthy or diseased lung (Blainey et al., 2012; Erb-Downward et al., 2011; Hilty et al.,…”
BackgroundMartinez, C. H., & Han, M. K. (2012) · Medical Clinics of North America · doi:10.1016/j.mcna.2012.02.007 · Cited by 46
“independent techniques are limited, a predominance of Pseudomonas species in patients with more impaired lung function in COPD has been reported.(30)”
Polymicrobial community‐acquired pneumonia: An emerging entity
Cillóniz, C., Čivljak, R., Nicolini, A., & Torres, A. (2015) · Respirology · doi:10.1111/resp.12663 · Cited by 46
Host-microbiome interactions in acute and chronic respiratory infections
Taylor, S., Wesselingh, S. L., & Rogers, G. B. (2016) · Cellular Microbiology · doi:10.1111/cmi.12589 · Cited by 46
Comparing microbiota profiles in induced and spontaneous sputum samples in COPD patients
Tangedal, S., Aanerud, M., Grønseth, R., Drengenes, C., Wiker, H. G., Bakke, P. S., & Eagan, T. (2017) · Respiratory Research · doi:10.1186/s12931-017-0645-3 · Cited by 46
“Different airways regions have been shown to harbor different communities [30, 31], possibly partly due to different ventilation-circulation ratios in the lower and upper parts of the lungs, and possibly due to differences between proximal and distal airways.”
BackgroundExacerbation induces a microbiota shift in sputa of COPD patients
Jubinville, É., Veillette, M., Milot, J., Maltais, F., Comeau, A., Lévesque, R. C., & Duchaine, C. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194355 · Cited by 45
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“Reduced microbial diversity in lower airways is linked to inflammatory phenotypes of the airways [53–55], which could increase both systemic inflammation and arterial stiffness that occur during ageing [23, 48].”
BackgroundRole of pulmonary microorganisms in the development of chronic obstructive pulmonary disease
Liu, J., Ran, Z., Wang, F., Xin, C., Xiong, B., & Song, Z. (2020) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2020.1830748 · Cited by 46
“In addition, several pioneering studies using next-generation sequencing techniques in metagenomics have con- firmed the role of pulmonary microorganisms in the occurrence and development of COPD (Erb-Downward et al. 2011; Moffatt and Cookson 2017).”
BackgroundMicrobiome in the pathogenesis of cystic fibrosis and lung transplant-related disease
Cribbs, S. K., & Beck, J. M. (2016) · Translational research · doi:10.1016/j.trsl.2016.07.022 · Cited by 48
“respiratory tract, raising the issue of contamination (12-14).”
BackgroundKotlyarov, S. N., & Котлярова, А. А. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22147634 · Cited by 50
Airway microbiome-immune crosstalk in chronic obstructive pulmonary disease
Kayongo, A., Robertson, N. M., Siddharthan, T., Ntayi, M. L., Ndawula, J. C., Sande, O. J., Bagaya, B. S., Kirenga, B., Mayanja‐Kizza, H., Joloba, M. L., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1085551 · Cited by 50
Microbial communities in swine lungs and their association with lung lesions
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“…et al., 2011), investigation of the microbial communities at different developmental stages (Kostric et al., 2018) and exploration of the lung microbiome in disease states (Hilty et al., 2010; Erb-Downward et al., 2011; Guss et al., 2011; Huang et al., 2011; Scher et al., 2016).”
BackgroundMethodInfluentialMycobiome in the Lower Respiratory Tract – A Clinical Perspective
Krause, R., Moissl-Eichinger, C., Halwachs, B., Gorkiewicz, G., Berg, G., Valentin, T., Prattes, J., Högenauer, C., & Zollner-Schwetz, I. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02169 · Cited by 43
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Microbial communities present in the lower respiratory tract of clinically healthy birds in Pakistan
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“culture-independent analyses in other hosts have reported distribution of characteristic organisms in the lower respiratory tract (Erb-Downward et al., 2011; Charlson et al., 2011).”
BackgroundLung cancer: a new frontier for microbiome research and clinical translation
Mur, L. A. J., Huws, S., Cameron, S. J. S., Lewis, P. D., & Lewis, K. E. (2018) · ecancermedicalscience · doi:10.3332/ecancer.2018.866 · Cited by 42
Lung and Gut Microbiome in COPD
Karakasidis, E., Kotsiou, O. S., & Gourgoulianis, K. I. (2023) · Journal of Personalized Medicine · doi:10.3390/jpm13050804 · Cited by 46
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Development of a Stable Lung Microbiome in Healthy Neonatal Mice
Kostrić, M., Milger, K., Krauss‐Etschmann, S., Engel, M., Vestergaard, G., Schloter, M., & Schöler, A. (2017) · Microbial Ecology · doi:10.1007/s00248-017-1068-x · Cited by 45
Lung Microbiome Participation in Local Immune Response Regulation in Respiratory Diseases
Lira-Lucio, J. A., Falfán‐Valencia, R., Ramírez‐Venegas, A., Buendía-Roldán, I., Rojas‐Serrano, J., Mejía, M. E., & Pérez-Rubio, G. (2020) · Microorganisms · doi:10.3390/microorganisms8071059 · Cited by 45
“It has been observed that there is a positive correlation between the years of cigarette smoking and taxa of the phylum Firmicutes (genera Veillonella and Megasphaera) and the genus Prevotella, while this variable is inversely associated with the taxon Proteobacteria (genera Eikenella and Haemophilus) [24].”
BackgroundRelationship between intestinal microbiota, diet and biological systems: an integrated view
Ferreira, R. D. S., Mendonça, L. A. B. M., Ribeiro, C. F. A., Calças, N. C., Guimarães, R. D. C. A., do Nascimento, V. A., Freitas, K. D. C., Carvalho, C. M. E., de Castro, A. P., & Franco, O. L. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1836605 · Cited by 46
“In the microbiota of the normal respiratory tract are found Bacteroidetes (including genus Prevotella sp.), Firmicutes (including genus Streptococcus sp. and Veillonella sp.), Proteobacteria and Actinobacteria (Dickson et al. 2015; Erb-Downward et al. 2011; Morris et al. 2013).”
BackgroundThe Effects of Corticosteroids on the Respiratory Microbiome: A Systematic Review
Hartmann, J. E., Albrich, W. C., Dmitrijeva, M., & Kahlert, C. R. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.588584 · Cited by 42
Peel, A. M., Wilkinson, M., Sinha, A., Loke, Y. K., Fowler, S. J., & Wilson, A. M. (2020) · Respiratory Medicine · doi:10.1016/j.rmed.2020.105984 · Cited by 40
“Change in the metabolome reflects change in underlying cellular activity(4) - disease pathophysiology can alter the relative concentrations of metabolites produced, or produce metabolites which are absent in health(5) - metabolomics is thus gaining traction as a means of biomarker discovery in disease(6).”
The Airway Microbiome-IL-17 Axis: a Critical Regulator of Chronic Inflammatory Disease
Mannion, J. M., McLoughlin, R. M., & Lalor, S. J. (2022) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-022-08928-y · Cited by 42
“Streptococcus, Haemophilus, Moraxella, Pseudomonas, Fusobacterium and Porphyromonas taxa are also commonly identified in this dynamic community that results from microaspiration of bacteria and other microbes in oropharyngeal secretions, and ongoing outward movement through mucociliary clearance and the cough reflex […”
BackgroundInfluentialAsthma-COPD Overlap in Clinical Practice (ACO_CP 2023): Toward Precision Medicine
Alsayed, A. R., Abu‐Samak, M., & Alkhatib, M. (2023) · Journal of Personalized Medicine · doi:10.3390/jpm13040677 · Cited by 40
“It is worth mentioning that the community structures specific to each patient, which showed a predominance of one or a few microbial genera, were in line with previous studies on COPD patients [32,37,38].”
ResultChronic Obstructive Pulmonary Disease (COPD): Developments in Pharmacological Treatments
Singh, D., Higham, A., Mathioudakis, A. G., & Beech, A. S. (2025) · Drugs · doi:10.1007/s40265-025-02188-8 · Cited by 51
Update on lung transplantation: programmes, patients and prospects
Kotsimbos, T. C., Williams, T. J., & Anderson, G. P. (2012) · European Respiratory Review · doi:10.1183/09059180.00006312 · Cited by 43
The microbiome of the nasopharynx
Flynn, M. F., & Dooley, J. S. G. (2021) · Journal of Medical Microbiology · doi:10.1099/jmm.0.001368 · Cited by 44
“Sterile dissection of healthy smokers' lungs have confirmed this microbiome, distinct from the oral cavity or nasopharynx, and more robust models of sterile sampling and controls for lavage contamination and oropharyngeal sampling confirm specifically lungenriched organisms [67, 68].”
BackgroundThe microbiome of the human lower airways: a next generation sequencing perspective
Aho, V. T. E., Pereira, P. A. B., Haahtela, T., Pawankar, R., Auvinen, P., & Koskinen, K. (2015) · World Allergy Organization Journal · doi:10.1186/s40413-015-0074-z · Cited by 47
“A recent study reported that although antibiotic treatment of P. aeruginosa infected CF patients with pulmonary exacerbations initially caused a drop in the relative abundance of Pseudomonas and an overall increase in alpha diversity (measured with the Shannon diversity index), the microbial communities reverted to th…”
BackgroundInfluentialThe Role of the Microbiome in Driving RA-Related Autoimmunity
Rooney, C. M., Mankia, K. S., & Emery, P. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.538130 · Cited by 41
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“This was not unexpected as species of Pseudomonas are ubiquitous in aquatic and terrestrial environments and have been hypothesized to be a part of the core pulmonary bacterial microbiome [58].”
BackgroundInfluentialEngel, M., Endesfelder, D., Schloter-Hai, B., Kublik, S., Granitsiotis, M. S., Boschetto, P., Stendardo, M., Barta, I., Döme, B., Deleuze, J., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180859 · Cited by 40
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The Human Respiratory Microbiome: Implications and Impact
Mitchell, A. B., & Glanville, A. R. (2018) · Seminars in Respiratory and Critical Care Medicine · doi:10.1055/s-0037-1617441 · Cited by 38
Thiruvengadam, M., Subramanian, U., Venkidasamy, B., Thirupathi, P., Samynathan, R., Shariati, M. A., Ребезов, М. Б., Chung, I., & Rengasamy, K. R. R. (2021) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2021.1954874 · Cited by 40
Severe viral respiratory infections: are bugs bugging?
Vissers, M., de Groot, R., & Ferwerda, G. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.93 · Cited by 39
“A ‘‘core airway microbiota’’ has been described in healthy subjects, containing predominantly Pseudomonas, Streptococcus, Prevotella, Fusobacterium, Haemophilus, Veillonella, and Porphyromonas.(40) However, other studies have been more sceptical.”
BackgroundSibley, C. D., Church, D. L., Surette, M. G., Dowd, S. E., & Parkins, M. D. (2012) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-012-1614-x · Cited by 38
“Whereas studies of the microbiome of the gastrointestinal tract [31, 32], superficial wounds [8, 10, 33–35], and lower airways of patients with chronic respiratory disease [14, 16, 36] must contend with the issue of external environmental contamination of samples, pyogenic infections represent invasion into normally s…”
BackgroundCelli, B. R. (2012) · Proceedings of the American Thoracic Society · doi:10.1513/pats.201107-039ms · Cited by 38
The lung and gut microbiome: what has to be taken into consideration for cystic fibrosis?
Héry-Arnaud, G., Boutin, S., Cuthbertson, L., Elborn, J. S., & Tunney, M. M. (2018) · Journal of Cystic Fibrosis · doi:10.1016/j.jcf.2018.11.003 · Cited by 37
Hosgood, H. D., Mongodin, E. F., Wan, Y., Hua, X., Rothman, N., Hu, W., Vermeulen, R. C. H., Seow, W. J., Rohan, T. E., Xu, J., et al. (2019) · Environmental and Molecular Mutagenesis · doi:10.1002/em.22291 · Cited by 37
“For example, bacterial communities have been detected in both lung tissues and bronchoalveolar lavage samples of smokers and nonsmokers (Erb-Downward et al., 2011; Beck et al., 2012; Dickson et al., 2013a, 2013b).”
BackgroundD’Anna, S. E., Balbi, B., Cappello, F., Carone, M., & Stefano, A. D. (2016) · International Journal of COPD · doi:10.2147/copd.s93398 · Cited by 38
“and could be either an “effect” of the lung inflammation or, in part, a “cause” of disease onset and progression.(21)”
A Study in Balance: How Microbiomes Are Changing the Shape of Environmental Health
Betts, K. S. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.119-a340 · Cited by 37
Smoking related environmental microbes affecting the pulmonary microbiome in Chinese population
Liu, X., Sun, W., Ma, W., Wang, H., Xu, K., Zhao, L., & He, Y. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.154652 · Cited by 36
Mackay, A. J., & Hurst, J. R. (2012) · Medical Clinics of North America · doi:10.1016/j.mcna.2012.02.008 · Cited by 38
Use of bronchoalveolar lavage to assess the respiratory microbiome: signal in the noise
Twigg, H. L., Morris, A., Ghedin, E., Curtis, J. L., Huffnagle, G. B., Crothers, K. A., Campbell, T., Flores, S. C., Fontenot, A. P., Beck, J. M., et al. (2013) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(13)70117-6 · Cited by 39
Possible role of anaerobes in the pathogenesis of nontuberculous mycobacterial infection
Yamasaki, K., Mukae, H., Kawanami, T., Fukuda, K., Noguchi, S., Akata, K., Naito, K., Oda, K., Ogoshi, T., Nishida, C., et al. (2015) · Respirology · doi:10.1111/resp.12536 · Cited by 36
Microbiome in chronic obstructive pulmonary disease
Monsó, E. (2017) · Annals of Translational Medicine · doi:10.21037/atm.2017.04.20 · Cited by 39
“This change is associated with an increase in the regional heterogeneity of the respiratory microbiome, identifiable through microbiome analyses of bronchial biopsies (5).”
BackgroundResultde la Rosa, D., López-Campos, J. L., Navarrete, B. A., Rubio, M. C., Cantón, R., Rivero, J. L. G., Carro, L. M., Fuster, C. O., & Martínez‐García, M. Á. (2020) · Archivos de Bronconeumología · doi:10.1016/j.arbr.2020.08.006 · Cited by 38
Shen, D., Guo, Z., Huang, K., Dai, P., Jin, X., Li, Y., & Li, C. (2021) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2021.126710 · Cited by 38
Non-infectious Pulmonary Diseases and HIV
Triplette, M., Crothers, K. A., & Attia, E. F. (2016) · Current HIV/AIDS Reports · doi:10.1007/s11904-016-0313-0 · Cited by 36
Nguyen, M. T., Sharma, A., Wu, W., Gomi, R., Sung, B., Hospodsky, D., Angenent, L. T., & Worgall, S. (2016) · The ISME Journal · doi:10.1038/ismej.2016.76 · Cited by 36
“In general, the relative distribution of phyla within each sample was found to be similar to the human respiratory microbiomes from oropharyngeal or BAL samples (Hilty et al., 2010; Erb-Downward et al., 2011; Sze et al, 2012).”
BackgroundMa, Q., Huang, D.-Y., Zhang, H., Wang, S., & Chen, X.-F. (2017) · International Immunopharmacology · doi:10.1016/j.intimp.2017.09.024 · Cited by 36
Sung, J. Y., Hwang, Y., Shin, M. H., Park, M. S., Lee, S. H., Yong, D., & Lee, K. (2017) · Annals of Laboratory Medicine · doi:10.3343/alm.2018.38.2.110 · Cited by 38
“Although the 2012 Human Microbiome Project did not include the lower respiratory tract in its surveys, advances in sequencing technology have revealed a diverse population of non-routinely cultured bacteria in the lung, which has traditionally been thought to be sterile [2-5].”
BackgroundThe Potential for Topical Probiotic Treatment of Chronic Rhinosinusitis, a Personal Perspective
Cervin, A. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00530 · Cited by 37
“The microbiome of the airway has been less investigated, but it there have been suggestions that there is a healthy airway core microbiome (Erb-Downward et al., 2011), however most researchers still find it difficult to distinguish between healthy and diseased by analyzing the microbiome only…”
BackgroundWong, L. M., Shende, N., Li, W. T., Castaneda, G., Apostol, L., Chang, E. Y., & Ongkeko, W. M. (2020) · Cancers · doi:10.3390/cancers12061447 · Cited by 37
“One study found over nine genera of bacteria in the lungs [5,6].”
BackgroundImpact of micro‐environmental changes on respiratory tract infections with intracellular bacteria
Shima, K., Coopmeiners, J., Graspeuntner, S., Dalhoff, K., & Rupp, J. (2016) · FEBS Letters · doi:10.1002/1873-3468.12353 · Cited by 36
Airway microbiome in adult survivors of extremely preterm birth: the EPICure study
Rofael, S., McHugh, T. D., Troughton, R., Beckmann, J., Spratt, D. A., Marlow, N., & Hurst, J. R. (2018) · European Respiratory Journal · doi:10.1183/13993003.01225-2018 · Cited by 37
Toraldo, D. M., & Conte, L. (2019) · Journal of Clinical Medicine Research · doi:10.14740/jocmr3875 · Cited by 36
“The healthy lung microbiota contains lots of commensal bacteria coming from and shared with the upper respiratory tract and these new results led the nowadaysaccepted knowledge that lower airways contain a consortium that can vary among individuals and across regions [43-45].”
BackgroundBrennan, M., McDonnell, M. J., Harrison, M. J., Duignan, N., O'Regan, A. W., Murphy, D. M., Ward, C., & Rutherford, R. M. (2022) · Respiratory Research · doi:10.1186/s12931-022-01947-5 · Cited by 34
“evaluated the bacterial microbiome in both current and non-smokers [63].”
BackgroundGarcía-Núñez, M., Martí, S., Puig, C., Pérez‐Brocal, V., Millares, L., Santos, S., Ardanuy, C., Moyá, A., Liñares, J., & Monsó, E. (2017) · Future Microbiology · doi:10.2217/fmb-2016-0127 · Cited by 37
Lipinksi, J. H., Ranjan, P., Dickson, R. P., & O’Dwyer, D. N. (2024) · The Journal of Immunology · doi:10.4049/jimmunol.2300716 · Cited by 37
Cystic Fibrosis Transmembrane Conductance Regulator: Roles in Chronic Obstructive Pulmonary Disease
Dransfield, M., Rowe, S., Vogelmeier, C. F., Wedzicha, J. A., Criner, G. J., Han, M. K., Martínez, F. J., & Calverley, P. (2022) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202109-2064tr · Cited by 38
Andersen, S. B., Egelund, G. B., Jensen, A. V., Petersen, P. T., Rohde, G. G. U., & Ravn, P. (2016) · Scandinavian Journal of Infectious Diseases · doi:10.1080/23744235.2016.1253860 · Cited by 34
Dóra, D., Szőcs, E., Soós, Á., Halasy, V., Somodi, C., Mihucz, A., Rostás, M., Mógor, F., Lohinai, Z., & Nagy, N. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1434804 · Cited by 33
“However, the complexity of sampling, particularly from the lung where invasive procedures are often required, poses challenges to accurately characterizing its microbiome (218 – 222).”
Immune system dynamics in response to Pseudomonas aeruginosa biofilms
Sahu, A., & Ruhal, R. (2025) · npj Biofilms and Microbiomes · doi:10.1038/s41522-025-00738-2 · Cited by 37
“Although P. aeruginosa infections are less frequent in COPD compared to CF or non-CF bronchiectasis (NCFB), their prevalence rises from 4% to 13% in individuals with severe airway obstruction 64,65 .”
Herr, C., Han, G., Li, D., Tschernig, T., Dinh, Q. T., Beißwenger, C., & Bals, R. (2015) · Experimental and Toxicologic Pathology · doi:10.1016/j.etp.2015.01.002 · Cited by 33
Inflammatory bowel diseases, chronic liver diseases and the lung
Rodriguez‐Roisin, R., Bartolome, S., Huchon, G., & Krowka, M. J. (2016) · European Respiratory Journal · doi:10.1183/13993003.00647-2015 · Cited by 33
Bouillon, A., Ferreira, M. S. V., Awad, S. A., Richter, J., Hochhaus, A., Kunzmann, V., Dengler, J. B., Janssen, J. J. W. M., Ossenkoppele, G. J., Westerweel, P. E., et al. (2018) · Blood Advances · doi:10.1182/bloodadvances.2018017772 · Cited by 32
The Cryptococcus neoformans Titan Cell: From In Vivo Phenomenon to In Vitro Model
Zhou, X., & Ballou, E. R. (2018) · Current Clinical Microbiology Reports · doi:10.1007/s40588-018-0107-9 · Cited by 31
pldist: ecological dissimilarities for paired and longitudinal microbiome association analysis
Plantinga, A., Chen, J., Jenq, R. R., & Wu, M. C. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz120 · Cited by 32
Ren, Y., Su, H., She, Y., Dai, C., Xie, D., Narrandes, S., Huang, S.-J., Chen, C., & Xu, W. W. (2019) · Translational Lung Cancer Research · doi:10.21037/tlcr.2019.06.11 · Cited by 32
Lung microbiome in human immunodeficiency virus infection
Twigg, H. L., Weinstock, G. M., & Knox, K. S. (2016) · Translational research · doi:10.1016/j.trsl.2016.07.008 · Cited by 33
The transient but not resident (TBNR) microbiome: a Yin Yang model for lung immune system
Saeedi, P., Salimian, J., Ahmadi, A., & Fooladi, A. A. I. (2015) · Inhalation Toxicology · doi:10.3109/08958378.2015.1070220 · Cited by 31
The Bergen COPD microbiome study (MicroCOPD): rationale, design, and initial experiences
Grønseth, R., Haaland, I., Wiker, H. G., Martinsen, E. M. H., Leiten, E. O., Husebø, G. R., Svanes, Ø., Bakke, P. S., & Eagan, T. (2014) · European Clinical Respiratory Journal · doi:10.3402/ecrj.v1.26196 · Cited by 31
“For instance, the study by Erb-Downward found evidence of reduced diversity of the lung microbiota in patients with advanced COPD (8), whereas Pragman et al.”
BackgroundInfluentialProbiotic strategies for treatment of respiratory diseases
Nagalingam, N. A., Cope, E. K., & Lynch, S. V. (2013) · Trends in Microbiology · doi:10.1016/j.tim.2013.04.008 · Cited by 32
Comparison of inflammatory markers in induced and spontaneous sputum in a cohort of COPD patients
Tangedal, S., Aanerud, M., Persson, L. J. P., Brokstad, K. A., Bakke, P. S., & Eagan, T. (2014) · Respiratory Research · doi:10.1186/s12931-014-0138-6 · Cited by 32
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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