Gut–Lung Microbiota Interaction in COPD Patients: A Literature Review
Abstract
:1. Introduction
2. Characteristics of COPD
3. The Impact of COPD on the Intestinal Microflora
4. The Role of the Gastrointestinal Tract in the Immunity
5. The Mechanisms of Gut–Lung Interactions
6. Probiotics—Possible Components of Therapy?
7. Discussion
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Marchesi, J.R.; Ravel, J. The vocabulary of microbiome research: A proposal. Microbiome 2015, 3, 31. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Donaldson, G.P.; Lee, S.M.; Mazmanian, S.K. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 2016, 14, 20–32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gomaa, E.Z. Human gut microbiota/microbiome in health and diseases: A review. Antonie Van Leeuwenhoek 2020, 113, 2019–2040. [Google Scholar] [CrossRef] [PubMed]
- Illiano, P.; Brambilla, R.; Parolini, C. The mutual interplay of gut microbiota, diet and human disease. FEBS J. 2020, 287, 833–855. [Google Scholar] [CrossRef] [Green Version]
- Xu, H.; Wang, X.; Feng, W.; Liu, Q.; Zhou, S.; Liu, Q.; Cai, L. The gut microbiota and its interactions with cardiovascular disease. Microb. Biotechnol. 2020, 13, 637–656. [Google Scholar] [CrossRef] [Green Version]
- Jandhyala, S.M.; Talukdar, R.; Subramanyam, C.; Vuyyuru, H.; Sasikala, M.; Nageshwar Reddy, D. Role of the normal gut microbiota. World J. Gastroenterol. 2015, 21, 8787–8803. [Google Scholar] [CrossRef]
- Dang, A.T.; Marsland, B.J. Microbes, metabolites, and the gut–lung axis. Mucosal Immunol. 2019, 12, 843–850. [Google Scholar] [CrossRef] [Green Version]
- Zhou, D.; Wang, Q.; Liu, H. Coronavirus disease 2019 and the gut–lung axis. Int. J. Infect. Dis. 2021, 113, 300–307. [Google Scholar] [CrossRef]
- Budden, K.F.; Gellatly, S.L.; Wood, D.L.A.; Cooper, M.A.; Morrison, M.; Hugenholtz, P.; Hansbro, P.M. Emerging pathogenic links between microbiota and the gut–lung axis. Nat. Rev. Microbiol. 2017, 15, 55–63. [Google Scholar] [CrossRef]
- World Health Organization. The Top 10 Causes of Death. Available online: https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death (accessed on 9 December 2020).
- Barcik, W.; Boutin, R.C.T.; Sokolowska, M.; Finlay, B.B. The Role of Lung and Gut Microbiota in the Pathology of Asthma. Immunity 2020, 52, 241–255. [Google Scholar] [CrossRef]
- Hufnagl, K.; Pali-Schöll, I.; Roth-Walter, F.; Jensen-Jarolim, E. Dysbiosis of the gut and lung microbiome has a role in asthma. Semin. Immunopathol. 2020, 42, 75–93. [Google Scholar] [CrossRef] [Green Version]
- Thavamani, A.; Salem, I.; Sferra, T.; Sankararaman, S. Impact of Altered Gut Microbiota and Its Metabolites in Cystic Fibrosis. Metabolites 2021, 11, 123. [Google Scholar] [CrossRef]
- Coffey, M.J.; Nielsen, S.; Wemheuer, B.; Kaakoush, N.O.; Garg, M.; Needham, B.; Pickford, R.; Jaffe, A.; Thomas, T.; Ooi, C.Y. Gut Microbiota in Children With Cystic Fibrosis: A Taxonomic and Functional Dysbiosis. Sci. Rep. 2019, 9, 18593. [Google Scholar] [CrossRef] [Green Version]
- Yeoh, Y.K.; Zuo, T.; Lui, G.C.-Y.; Zhang, F.; Liu, Q.; Li, A.Y.; Chung, A.C.; Cheung, C.P.; Tso, E.Y.; Fung, K.S.; et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut 2021, 70, 698–706. [Google Scholar] [CrossRef]
- Yamamoto, S.; Saito, M.; Tamura, A.; Prawisuda, D.; Mizutani, T.; Yotsuyanagi, H. The human microbiome and COVID-19: A systematic review. PLoS ONE 2021, 16, e0253293. [Google Scholar] [CrossRef]
- WHO. Chronic Obstructive Pulmonary Disease (COPD). Available online: https://www.who.int/news-room/fact-sheets/detail/chronic-obstructive-pulmonary-disease-(copd) (accessed on 20 May 2022).
- Agustí, A.; Vogelmeier, C.; Faner, R. COPD 2020: Changes and challenges. Am. J. Physiol. Lung Cell. Mol. Physiol. 2020, 319, L879–L883. [Google Scholar] [CrossRef]
- Benjafield, A.; Tellez, D.; Barrett, M.; Gondalia, R.; Nunez, C.; Wedzicha, J.; Malhotra, A. An estimate of the European prevalence of COPD in 2050. Eur. Respir. J. 2021, 58, OA2866. [Google Scholar] [CrossRef]
- Labaki, W.W.; Rosenberg, S.R. Chronic Obstructive Pulmonary Disease. Ann. Intern. Med. 2020, 173, ITC17–ITC32. [Google Scholar] [CrossRef]
- Raftery, A.L.; Tsantikos, E.; Harris, N.L.; Hibbs, M.L. Links between Inflammatory Bowel Disease and Chronic Obstructive Pulmonary Disease. Front. Immunol. 2020, 11, 2144. [Google Scholar] [CrossRef]
- Barnes, P.J. Inflammatory mechanisms in patients with chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 2016, 138, 16–27. [Google Scholar] [CrossRef]
- López-Campos, J.L.; Tan, W.; Soriano, J.B. Global burden of COPD. Respirology 2016, 21, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Stolz, D. Chronic obstructive pulmonary disease risk: Does genetics hold the answer? Lancet Respir. Med. 2020, 8, 653–654. [Google Scholar] [CrossRef] [PubMed]
- Ekbom, A.; Brandt, L.; Granath, F.; Löfdahl, C.-G.; Egesten, A. Increased Risk of Both Ulcerative Colitis and Crohn’s Disease in a Population Suffering from COPD. Lung 2008, 186, 167–172. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.; Im, J.P.; Han, K.; Park, S.; Soh, H.; Choi, K.; Kim, J.; Chun, J.; Kim, J.S. Risk of inflammatory bowel disease in patients with chronic obstructive pulmonary disease: A nationwide, population-based study. World J. Gastroenterol. 2019, 25, 6354–6364. [Google Scholar] [CrossRef]
- Brassard, P.; Vutcovici, M.; Ernst, P.; Patenaude, V.; Sewitch, M.; Suissa, S.; Bitton, A. Increased incidence of inflammatory bowel disease in Québec residents with airway diseases. Eur. Respir. J. 2015, 45, 962–968. [Google Scholar] [CrossRef]
- Sin, D.D.; Sze, M.; Hogg, J.C. Bacterial microbiome of lungs in COPD. Int. J. Chronic Obstr. Pulm. Dis. 2014, 9, 229–238. [Google Scholar] [CrossRef] [Green Version]
- Jones, B.; Donovan, C.; Liu, G.; Gomez, H.M.; Chimankar, V.; Harrison, C.L.; Wiegman, C.H.; Adcock, I.M.; Knight, D.A.; Hirota, J.A.; et al. Animal models of COPD: What do they tell us? Respirology 2017, 22, 21–32. [Google Scholar] [CrossRef] [Green Version]
- García-Núñez, M.; Millares, L.; Pomares, X.; Ferrari, R.; Pérez-Brocal, V.; Gallego, M.; Espasa, M.; Moya, A.; Monsó, E. Severity-related changes of bronchial microbiome in chronic obstructive pulmonary disease. J. Clin. Microbiol. 2014, 52, 4217–4223. [Google Scholar] [CrossRef] [Green Version]
- O’Dwyer, D.N.; Dickson, R.P.; Moore, B.B. The Lung Microbiome, Immunity, and the Pathogenesis of Chronic Lung Disease. J. Immunol. 2016, 196, 4839–4847. [Google Scholar] [CrossRef] [Green Version]
- Shah, T.; Shah, Z.; Baloch, Z.; Cui, X. The role of microbiota in respiratory health and diseases, particularly in tuberculosis. Biomed. Pharmacother. 2021, 143, 112108. [Google Scholar] [CrossRef]
- Huang, Y.J.; Sethi, S.; Murphy, T.; Nariya, S.; Boushey, H.A.; Lynch, S.V. Airway Microbiome Dynamics in Exacerbations of Chronic Obstructive Pulmonary Disease. J. Clin. Microbiol. 2014, 52, 2813–2823. [Google Scholar] [CrossRef] [Green Version]
- Shukla, S.D.; Budden, K.F.; Neal, R.; Hansbro, P.M. Microbiome effects on immunity, health and disease in the lung. Clin. Transl. Immunol. 2017, 6, e133. [Google Scholar] [CrossRef]
- Ritchie, A.I.; Wedzicha, J.A. Definition, Causes, Pathogenesis, and Consequences of Chronic Obstructive Pulmonary Disease Exacerbations. Clin. Chest Med. 2020, 41, 421–438. [Google Scholar] [CrossRef]
- Li, J.; Sun, S.; Tang, R.; Qiu, H.; Huang, Q.; Mason, T.G.; Tian, L. Major air pollutants and risk of COPD exacerbations: A systematic review and meta-analysis. Int. J. Chronic Obstr. Pulm. Dis. 2016, 11, 3079–3091. [Google Scholar] [CrossRef] [Green Version]
- Ritchie, A.I.; Farne, H.A.; Singanayagam, A.; Jackson, D.J.; Mallia, P.; Johnston, S.L. Pathogenesis of Viral Infection in Exacerbations of Airway Disease. Ann. Am. Thorac. Soc. 2015, 12 (Suppl. 2), S115–S132. [Google Scholar] [CrossRef]
- Millares, L.; Ferrari, R.; Gallego, M.; Garcia-Nuñez, M.; Brocal, V.P.; Espasa, M.; Pomares, X.; Monton, C.; Moya, A.; Monsó, E. Bronchial microbiome of severe COPD patients colonised by Pseudomonas aeruginosa. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33, 1101–1111. [Google Scholar] [CrossRef] [Green Version]
- Qu, L.; Cheng, Q.; Wang, Y.; Mu, H.; Zhang, Y. COPD and Gut–Lung Axis: How Microbiota and Host Inflammasome Influence COPD and Related Therapeutics. Front. Microbiol. 2022, 13, 868086. [Google Scholar] [CrossRef]
- Wang, Z.; Bafadhel, M.; Haldar, K.; Spivak, A.; Mayhew, D.; Miller, B.E.; Tal-Singer, R.; Johnston, S.; Ramsheh, M.Y.; Barer, M.; et al. Lung microbiome dynamics in COPD exacerbations. Eur. Respir. J. 2016, 47, 1082–1092. [Google Scholar] [CrossRef] [Green Version]
- Sun, Z.; Zhu, Q.; Shen, Y.; Yan, T.; Zhou, X. Dynamic changes of gut and lung microorganisms during chronic obstructive pulmonary disease exacerbations. Kaohsiung J. Med. Sci. 2020, 36, 107–113. [Google Scholar] [CrossRef]
- George, S.N.; Garcha, D.S.; Mackay, A.J.; Patel, A.R.; Singh, R.; Sapsford, R.J.; Donaldson, G.C.; Wedzicha, J.A. Human rhinovirus infection during naturally occurring COPD exacerbations. Eur. Respir. J. 2014, 44, 87–96. [Google Scholar] [CrossRef]
- Tan, D.B.; Amran, F.S.; Teo, T.-H.; Price, P.; Moodley, Y.P. Levels of CMV-reactive antibodies correlate with the induction of CD28(null) T cells and systemic inflammation in chronic obstructive pulmonary disease (COPD). Cell. Mol. Immunol. 2016, 13, 551–553. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, J.; Liu, H.-Y.; Tan, X.-L.; Ji, Y.; Jiang, Y.-X.; Prabhakar, M.; Rong, Z.-H.; Zhou, H.-W.; Zhang, G.-X. Sputum Bacterial and Fungal Dynamics during Exacerbations of Severe COPD. PLoS ONE 2015, 10, e0130736. [Google Scholar] [CrossRef] [PubMed]
- Ding, K.; Chen, J.; Zhan, W.; Zhang, S.; Chen, Y.; Long, S.; Lei, M. Microbiome Links Cigarette Smoke-Induced Chronic Obstructive Pulmonary Disease and Dietary Fiber via the Gut-Lung Axis: A Narrative Review. COPD 2021, 19, 10–17. [Google Scholar] [CrossRef] [PubMed]
- Bowerman, K.L.; Rehman, S.F.; Vaughan, A.; Lachner, N.; Budden, K.F.; Kim, R.Y.; Wood, D.L.A.; Gellatly, S.L.; Shukla, S.D.; Wood, L.G.; et al. Disease-associated gut microbiome and metabolome changes in patients with chronic obstructive pulmonary disease. Nat. Commun. 2020, 11, 5886. [Google Scholar] [CrossRef]
- Chiu, Y.-C.; Lee, S.-W.; Liu, C.-W.; Lin, R.C.-J.; Huang, Y.-C.; Lan, T.-Y.; Wu, L.S.-H. Comprehensive profiling of the gut microbiota in patients with chronic obstructive pulmonary disease of varying severity. PLoS ONE 2021, 16, e0249944. [Google Scholar] [CrossRef]
- Donovan, C.; Liu, G.; Shen, S.; Marshall, J.E.; Kim, R.Y.; Alemao, C.A.; Budden, K.F.; Choi, J.P.; Kohonen-Corish, M.; El-Omar, E.M.; et al. The role of the microbiome and the NLRP3 inflammasome in the gut and lung. J. Leukoc. Biol. 2020, 108, 925–935. [Google Scholar] [CrossRef]
- Pinkerton, J.W.; Kim, R.Y.; Robertson, A.A.B.; Hirota, J.A.; Wood, L.G.; Knight, D.A.; Cooper, M.A.; O’Neill, L.A.J.; Horvat, J.C.; Hansbro, P.M. Inflammasomes in the lung. Mol. Immunol. 2017, 86, 44–55. [Google Scholar] [CrossRef]
- Huang, C.; Shi, G. Smoking and microbiome in oral, airway, gut and some systemic diseases. J. Transl. Med. 2019, 17, 225. [Google Scholar] [CrossRef] [Green Version]
- Lee, S.H.; Yun, Y.; Kim, S.J.; Lee, E.-J.; Chang, Y.; Ryu, S.; Shin, H.; Kim, H.-L.; Kim, H.-N.; Lee, J.H. Association between Cigarette Smoking Status and Composition of Gut Microbiota: Population-Based Cross-Sectional Study. J. Clin. Med. 2018, 7, 282. [Google Scholar] [CrossRef] [Green Version]
- Shanahan, E.R.; Shah, A.; Koloski, N.; Walker, M.M.; Talley, N.J.; Morrison, M.; Holtmann, G.J. Influence of cigarette smoking on the human duodenal mucosa-associated microbiota. Microbiome 2018, 6, 150. [Google Scholar] [CrossRef]
- Rogers, M.A.M.; Greene, M.T.; Saint, S.; Chenoweth, C.E.; Malani, P.N.; Trivedi, I.; Aronoff, D. Higher Rates of Clostridium difficile Infection among Smokers. PLoS ONE 2012, 7, e42091. [Google Scholar] [CrossRef]
- Taylor, C.T.; Colgan, S.P. Regulation of immunity and inflammation by hypoxia in immunological niches. Nat. Rev. Immunol. 2017, 17, 774–785. [Google Scholar] [CrossRef]
- Pral, L.P.; Fachi, J.L.; Corrêa, R.O.; Colonna, M.; Vinolo, M.A. Hypoxia and HIF-1 as key regulators of gut microbiota and host interactions. Trends Immunol. 2021, 42, 604–621. [Google Scholar] [CrossRef]
- Singhal, R.; Shah, Y.M. Oxygen battle in the gut: Hypoxia and hypoxia-inducible factors in metabolic and inflammatory responses in the intestine. J. Biol. Chem. 2020, 295, 10493–10505. [Google Scholar] [CrossRef]
- Adak, A.; Maity, C.; Ghosh, K.; Pati, B.R.; Mondal, K.C. Dynamics of predominant microbiota in the human gastrointestinal tract and change in luminal enzymes and immunoglobulin profile during high-altitude adaptation. Folia Microbiol. 2013, 58, 523–528. [Google Scholar] [CrossRef]
- Van Meijel, R.; Venema, K.; Canfora, E.; Blaak, E.; Goossens, G. Mild intermittent hypoxia exposure alters gut microbiota composition in men with overweight and obesity. Benef. Microbes 2022, 13, 355–363. [Google Scholar] [CrossRef]
- Marttinen, M.; Ala-Jaakkola, R.; Laitila, A.; Lehtinen, M.J. Gut Microbiota, Probiotics and Physical Performance in Athletes and Physically Active Individuals. Nutrients 2020, 12, 2936. [Google Scholar] [CrossRef]
- Jollet, M.; Nay, K.; Chopard, A.; Bareille, M.-P.; Beck, A.; Ollendorff, V.; Vernus, B.; Bonnieu, A.; Mariadassou, M.; Rué, O.; et al. Does Physical Inactivity Induce Significant Changes in Human Gut Microbiota? New Answers Using the Dry Immersion Hypoactivity Model. Nutrients 2021, 13, 3865. [Google Scholar] [CrossRef]
- Ramirez, J.; Guarner, F.; Fernandez, L.B.; Maruy, A.; Sdepanian, V.L.; Cohen, H. Antibiotics as Major Disruptors of Gut Microbiota. Front. Cell. Infect. Microbiol. 2020, 10, 572912. [Google Scholar] [CrossRef]
- Palleja, A.; Mikkelsen, K.H.; Forslund, S.K.; Kashani, A.; Allin, K.H.; Nielsen, T.; Hansen, T.H.; Liang, S.; Feng, Q.; Zhang, C.; et al. Recovery of gut microbiota of healthy adults following antibiotic exposure. Nat. Microbiol. 2018, 3, 1255–1265. [Google Scholar] [CrossRef]
- Kabbani, T.A.; Pallav, K.; Dowd, S.E.; Villafuerte-Galvez, J.; Vanga, R.R.; Castillo, N.E.; Hansen, J.; Dennis, M.; Leffler, D.A.; Kelly, C.P. Prospective randomized controlled study on the effects of Saccharomyces boulardii CNCM I-745 and amoxicillin-clavulanate or the combination on the gut microbiota of healthy volunteers. Gut Microbes 2017, 8, 17–32. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Burdet, C.; Grall, N.; Linard, M.; Bridier-Nahmias, A.; Benhayoun, M.; Bourabha, K.; Magnan, M.; Clermont, O.; D’Humières, C.; Tenaillon, O.; et al. Ceftriaxone and Cefotaxime Have Similar Effects on the Intestinal Microbiota in Human Volunteers Treated by Standard-Dose Regimens. Antimicrob. Agents Chemother. 2019, 63, e02244-18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Leffler, D.A.; Lamont, J.T. Clostridium difficile Infection. N. Engl. J. Med. 2015, 372, 1539–1548. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sabtu, N.; Enoch, D.A.; Brown, N.M. Antibiotic resistance: What, why, where, when and how? Br. Med. Bull. 2015, 116, 105–113. [Google Scholar] [CrossRef] [Green Version]
- Schepper, J.D.; Collins, F.; Rios-Arce, N.D.; Kang, H.J.; Schaefer, L.; Gardinier, J.D.; Raghuvanshi, R.; Quinn, R.A.; Britton, R.; Parameswaran, N.; et al. Involvement of the Gut Microbiota and Barrier Function in Glucocorticoid-Induced Osteoporosis. J. Bone Miner. Res. 2020, 35, 801–820. [Google Scholar] [CrossRef]
- Wang, M.; Zhu, Z.; Lin, X.; Li, H.; Wen, C.; Bao, J.; He, Z. Gut microbiota mediated the therapeutic efficacies and the side effects of prednisone in the treatment of MRL/lpr mice. Arthritis Res. Ther. 2021, 23, 240. [Google Scholar] [CrossRef]
- Mason, K.L.; Huffnagle, G.B.; Noverr, M.C.; Kao, J.Y. Overview of Gut Immunology. Adv. Exp. Med. Biol. 2008, 635, 1–14. [Google Scholar] [CrossRef]
- Tulic, M.K.; Piche, T.; Verhasselt, V. Lung-gut cross-talk: Evidence, mechanisms and implications for the mucosal inflammatory diseases. Clin. Exp. Allergy 2016, 46, 519–528. [Google Scholar] [CrossRef]
- McGhee, J.R.; Fujihashi, K. Inside the Mucosal Immune System. PLoS Biol. 2012, 10, e1001397. [Google Scholar] [CrossRef] [Green Version]
- Chelakkot, C.; Ghim, J.; Ryu, S.H. Mechanisms regulating intestinal barrier integrity and its pathological implications. Exp. Mol. Med. 2018, 50, 1–9. [Google Scholar] [CrossRef]
- Catalioto, R.-M.; Maggi, C.A.; Giuliani, S. Intestinal Epithelial Barrier Dysfunction in Disease and Possible Therapeutical Interventions. Curr. Med. Chem. 2011, 18, 398–426. [Google Scholar] [CrossRef]
- De Mey, J.R.; Freund, J.-N. Understanding epithelial homeostasis in the intestine: An old battlefield of ideas, recent breakthroughs and remaining controversies. Tissue Barriers 2013, 1, e24965. [Google Scholar] [CrossRef] [Green Version]
- Kagnoff, M.F. The intestinal epithelium is an integral component of a communications network. J. Clin. Investig. 2014, 124, 2841–2843. [Google Scholar] [CrossRef]
- Lueschow, S.R.; McElroy, S.J. The Paneth Cell: The Curator and Defender of the Immature Small Intestine. Front. Immunol. 2020, 11, 587. [Google Scholar] [CrossRef] [Green Version]
- Clevers, H.C.; Bevins, C.L. Paneth Cells: Maestros of the Small Intestinal Crypts. Annu. Rev. Physiol. 2013, 75, 289–311. [Google Scholar] [CrossRef]
- Badi, S.A.; Tarashi, S.; Fateh, A.; Rohani, P.; Masotti, A.; Siadat, S.D. From the Role of Microbiota in Gut-Lung Axis to SARS-CoV-2 Pathogenesis. Mediat. Inflamm. 2021, 2021, 6611222. [Google Scholar] [CrossRef]
- Dillon, A.; Lo, D.D. M Cells: Intelligent Engineering of Mucosal Immune Surveillance. Front. Immunol. 2019, 10, 1499. [Google Scholar] [CrossRef] [Green Version]
- Martinez, J.E.; Kahana, D.D.; Ghuman, S.; Wilson, H.P.; Wilson, J.; Kim, S.C.J.; Lagishetty, V.; Jacobs, J.P.; Sinha-Hikim, A.P.; Friedman, T.C. Unhealthy Lifestyle and Gut Dysbiosis: A Better Understanding of the Effects of Poor Diet and Nicotine on the Intestinal Microbiome. Front. Endocrinol. 2021, 12, 667066. [Google Scholar] [CrossRef]
- Weiss, G.A.; Hennet, T. Mechanisms and consequences of intestinal dysbiosis. Cell. Mol. Life Sci. 2017, 74, 2959–2977. [Google Scholar] [CrossRef] [Green Version]
- Wirusanti, N.I.; Baldridge, M.T.; Harris, V.C. Microbiota regulation of viral infections through interferon signaling. Trends Microbiol. 2022, 30, 778–792. [Google Scholar] [CrossRef]
- Bradley, K.C.; Finsterbusch, K.; Schnepf, D.; Crotta, S.; Llorian, M.; Davidson, S.; Fuchs, S.Y.; Staeheli, P.; Wack, A. Microbiota-Driven Tonic Interferon Signals in Lung Stromal Cells Protect from Influenza Virus Infection. Cell Rep. 2019, 28, 245–256.e4. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Steed, A.L.; Christophi, G.P.; Kaiko, G.E.; Sun, L.; Goodwin, V.M.; Jain, U.; Esaulova, E.; Artyomov, M.N.; Morales, D.J.; Holtzman, M.J.; et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science 2017, 357, 498–502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stefan, K.L.; Kim, M.V.; Iwasaki, A.; Kasper, D.L. Commensal Microbiota Modulation of Natural Resistance to Virus Infection. Cell 2020, 183, 1312–1324.e10. [Google Scholar] [CrossRef] [PubMed]
- Rittirsch, D.; Flierl, M.A.; Day, D.E.; Nadeau, B.A.; McGuire, S.R.; Hoesel, L.M.; Ipaktchi, K.; Zetoune, F.S.; Sarma, J.V.; Leng, L.; et al. Acute Lung Injury Induced by Lipopolysaccharide Is Independent of Complement Activation. J. Immunol. 2008, 180, 7664–7672. [Google Scholar] [CrossRef] [Green Version]
- Al Bander, Z.; Nitert, M.D.; Mousa, A.; Naderpoor, N. The Gut Microbiota and Inflammation: An Overview. Int. J. Environ. Res. Public Health 2020, 17, 7618. [Google Scholar] [CrossRef]
- Ghosh, S.S.; Wang, J.; Yannie, P.J.; Ghosh, S. Intestinal Barrier Dysfunction, LPS Translocation, and Disease Development. J. Endocr. Soc. 2020, 4, bvz039. [Google Scholar] [CrossRef] [Green Version]
- Lu, Y.-C.; Yeh, W.-C.; Ohashi, P.S. LPS/TLR4 signal transduction pathway. Cytokine 2008, 42, 145–151. [Google Scholar] [CrossRef]
- Palsson-McDermott, E.M.; O’Neill, L. Signal transduction by the lipopolysaccharide receptor, Toll-like receptor-4. Immunology 2004, 113, 153–162. [Google Scholar] [CrossRef]
- Kaluza, J.; Larsson, S.; Orsini, N.; Linden, A.; Wolk, A. Fruit and vegetable consumption and risk of COPD: A prospective cohort study of men. Thorax 2017, 72, 500–509. [Google Scholar] [CrossRef]
- Szmidt, M.K.; Kaluza, J.; Harris, H.R.; Linden, A.; Wolk, A. Long-term dietary fiber intake and risk of chronic obstructive pulmonary disease: A prospective cohort study of women. Eur. J. Nutr. 2020, 59, 1869–1879. [Google Scholar] [CrossRef]
- Jang, Y.O.; Kim, O.-H.; Kim, S.J.; Lee, S.H.; Yun, S.; Lim, S.E.; Yoo, H.J.; Shin, Y.; Lee, S.W. High-fiber diets attenuate emphysema development via modulation of gut microbiota and metabolism. Sci. Rep. 2021, 11, 7008. [Google Scholar] [CrossRef]
- Li, M.; Van Esch, B.C.A.M.; Wagenaar, G.T.M.; Garssen, J.; Folkerts, G.; Henricks, P.A.J. Pro- and anti-inflammatory effects of short chain fatty acids on immune and endothelial cells. Eur. J. Pharmacol. 2018, 831, 52–59. [Google Scholar] [CrossRef]
- Trompette, A.; Gollwitzer, E.S.; Pattaroni, C.; Lopez-Mejia, I.C.; Riva, E.; Pernot, J.; Ubags, N.; Fajas, L.; Nicod, L.P.; Marsland, B.J. Dietary Fiber Confers Protection against Flu by Shaping Ly6c−Patrolling Monocyte Hematopoiesis and CD8+ T Cell Metabolism. Immunity 2018, 48, 992–1005.e8. [Google Scholar] [CrossRef] [Green Version]
- Hartstra, A.V.; Bouter, K.E.; Bäckhed, F.; Nieuwdorp, M. Insights Into the Role of the Microbiome in Obesity and Type 2 Diabetes. Diabetes Care 2015, 38, 159–165. [Google Scholar] [CrossRef] [Green Version]
- Di Sabatino, A.; Cazzola, P.; Ciccocioppo, R.; Morera, R.; Biancheri, P.; Rovedatti, L.; Cantoro, L.; Vanoli, A.; Tinozzi, F.; Tinozzi, S.; et al. Efficacy of butyrate in the treatment of mild to moderate Crohn’s disease. Dig. Liver Dis. Suppl. 2007, 1, 31–35. [Google Scholar] [CrossRef]
- Vieira, R.D.S.; Castoldi, A.; Basso, P.J.; Hiyane, M.I.; Câmara, N.O.S.; Almeida, R.R. Butyrate Attenuates Lung Inflammation by Negatively Modulating Th9 Cells. Front. Immunol. 2019, 10, 67. [Google Scholar] [CrossRef]
- Salvi, P.S.; Cowles, R.A. Butyrate and the Intestinal Epithelium: Modulation of Proliferation and Inflammation in Homeostasis and Disease. Cells 2021, 10, 1775. [Google Scholar] [CrossRef] [PubMed]
- Lo, B.C.; Shin, S.B.; Hernaez, D.C.; Refaeli, I.; Yu, H.B.; Goebeler, V.; Cait, A.; Mohn, W.W.; Vallance, B.A.; McNagny, K.M. IL-22 Preserves Gut Epithelial Integrity and Promotes Disease Remission during Chronic Salmonella Infection. J. Immunol. 2019, 202, 956–965. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tedelind, S.; Westberg, F.; Kjerrulf, M.; Vidal, A. Anti-inflammatory properties of the short-chain fatty acids acetate and propionate: A study with relevance to inflammatory bowel disease. World J. Gastroenterol. 2007, 13, 2826–2832. [Google Scholar] [CrossRef]
- Wu, F.; Guo, X.; Zhang, J.; Zhang, M.; Ou, Z.; Peng, Y. Phascolarctobacterium faecium abundant colonization in human gastrointestinal tract. Exp. Ther. Med. 2017, 14, 3122–3126. [Google Scholar] [CrossRef]
- Ghavami, S.B.; Pourhamzeh, M.; Farmani, M.; Raftar, S.K.A.; Shahrokh, S.; Shpichka, A.; Aghdaei, H.A.; Hakemi-Vala, M.; Hossein-Khannazer, N.; Timashev, P.; et al. Cross-talk between immune system and microbiota in COVID-19. Expert Rev. Gastroenterol. Hepatol. 2021, 15, 1281–1294. [Google Scholar] [CrossRef]
- Antunes, K.H.; Fachi, J.L.; De Paula, R.; Da Silva, E.F.; Pral, L.P.; DOS Santos, A.; Dias, G.B.M.; Vargas, J.E.; Puga, R.; Mayer, F.Q.; et al. Microbiota-derived acetate protects against respiratory syncytial virus infection through a GPR43-type 1 interferon response. Nat. Commun. 2019, 10, 3273. [Google Scholar] [CrossRef] [Green Version]
- Nakajima, A.; Nakatani, A.; Hasegawa, S.; Irie, J.; Ozawa, K.; Tsujimoto, G.; Suganami, T.; Itoh, H.; Kimura, I. The short chain fatty acid receptor GPR43 regulates inflammatory signals in adipose tissue M2-type macrophages. PLoS ONE 2017, 12, e0179696. [Google Scholar] [CrossRef] [Green Version]
- Galvão, I.; Tavares, L.P.; Corrêa, R.O.; Fachi, J.L.; Rocha, V.; Rungue, M.; Garcia, C.; Cassali, G.; Ferreira, C.M.; Martins, F.; et al. The Metabolic Sensor GPR43 Receptor Plays a Role in the Control of Klebsiella pneumoniae Infection in the Lung. Front. Immunol. 2018, 9, 142. [Google Scholar] [CrossRef] [Green Version]
- Sencio, V.; Barthelemy, A.; Tavares, L.P.; Machado, M.G.; Soulard, D.; Cuinat, C.; Queiroz-Junior, C.M.; Noordine, M.-L.; Salomé-Desnoulez, S.; Deryuter, L.; et al. Gut Dysbiosis during Influenza Contributes to Pulmonary Pneumococcal Superinfection through Altered Short-Chain Fatty Acid Production. Cell Rep. 2020, 30, 2934–2947.e6. [Google Scholar] [CrossRef] [Green Version]
- Chen, G.Y.; Liu, M.; Wang, F.; Bertin, J.; Núñez, G. A Functional Role for Nlrp6 in Intestinal Inflammation and Tumorigenesis. J. Immunol. 2011, 186, 7187–7194. [Google Scholar] [CrossRef] [Green Version]
- Badi, S.A.; Moshiri, A.; Fateh, A.; Jamnani, F.R.; Sarshar, M.; Vaziri, F.; Siadat, S.D. Microbiota-Derived Extracellular Vesicles as New Systemic Regulators. Front. Microbiol. 2017, 8, 1610. [Google Scholar] [CrossRef] [Green Version]
- Badi, S.A.; Khatami, S.; Irani, S.; Siadat, S.D. Induction Effects of Bacteroides fragilis Derived Outer Membrane Vesicles on Toll Like Receptor 2, Toll Like Receptor 4 Genes Expression and Cytokines Concentration in Human Intestinal Epithelial Cells. Cell J. 2019, 21, 57–61. [Google Scholar] [CrossRef]
- Chelakkot, C.; Choi, Y.; Kim, D.-K.; Park, H.T.; Ghim, J.; Kwon, Y.; Jeon, J.; Kim, M.-S.; Jee, Y.-K.; Gho, Y.S.; et al. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Exp. Mol. Med. 2018, 50, e450. [Google Scholar] [CrossRef] [Green Version]
- Ashrafian, F.; Shahriary, A.; Behrouzi, A.; Moradi, H.R.; Raftar, S.K.A.; Lari, A.; Hadifar, S.; Yaghoubfar, R.; Badi, S.A.; Khatami, S.; et al. Akkermansia muciniphila-Derived Extracellular Vesicles as a Mucosal Delivery Vector for Amelioration of Obesity in Mice. Front. Microbiol. 2019, 10, 2155. [Google Scholar] [CrossRef]
- Shimada, Y.; Kinoshita, M.; Harada, K.; Mizutani, M.; Masahata, K.; Kayama, H.; Takeda, K. Commensal Bacteria-Dependent Indole Production Enhances Epithelial Barrier Function in the Colon. PLoS ONE 2013, 8, e80604. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sorgdrager, F.J.H.; Naudé, P.J.W.; Kema, I.P.; Nollen, E.A.; De Deyn, P.P. Tryptophan Metabolism in Inflammaging: From Biomarker to Therapeutic Target. Front. Immunol. 2019, 10, 2565. [Google Scholar] [CrossRef] [PubMed]
- Schirmer, M.; Smeekens, S.P.; Vlamakis, H.; Jaeger, M.; Oosting, M.; Franzosa, E.A.; Ter Horst, R.; Jansen, T.; Jacobs, L.; Bonder, M.J.; et al. Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity. Cell 2016, 167, 1125–1136.e8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Verdecchia, P.; Cavallini, C.; Spanevello, A.; Angeli, F. The pivotal link between ACE2 deficiency and SARS-CoV-2 infection. Eur. J. Intern. Med. 2020, 76, 14–20. [Google Scholar] [CrossRef]
- Fanos, V.; Pintus, M.C.; Pintus, R.; Marcialis, M.A. Lung microbiota in the acute respiratory disease: From coronavirus to metabolomics. J. Pediatr. Neonatal Individ. Med. (JPNIM) 2020, 9, e090139. [Google Scholar] [CrossRef]
- Hergott, C.B.; Roche, A.M.; Tamashiro, E.; Clarke, T.B.; Bailey, A.G.; Laughlin, A.; Bushman, F.D.; Weiser, J.N. Peptidoglycan from the gut microbiota governs the lifespan of circulating phagocytes at homeostasis. Blood 2016, 127, 2460–2471. [Google Scholar] [CrossRef] [Green Version]
- Zeng, M.Y.; Cisalpino, D.; Varadarajan, S.; Hellman, J.; Warren, H.S.; Cascalho, M.; Inohara, N.; Núñez, G. Gut Microbiota-Induced Immunoglobulin G Controls Systemic Infection by Symbiotic Bacteria and Pathogens. Immunity 2016, 44, 647–658. [Google Scholar] [CrossRef] [Green Version]
- Samuelson, D.R.; Welsh, D.A.; Shellito, J.E. Regulation of lung immunity and host defense by the intestinal microbiota. Front. Microbiol. 2015, 6, 1085. [Google Scholar] [CrossRef] [Green Version]
- Frank, K.M.; Zhou, T.; Moreno-Vinasco, L.; Hollett, B.; Garcia, J.G.N.; Wardenburg, J.B. Host Response Signature to Staphylococcus aureus Alpha-Hemolysin Implicates Pulmonary Th17 Response. Infect. Immun. 2012, 80, 3161–3169. [Google Scholar] [CrossRef] [Green Version]
- Gauguet, S.; D’Ortona, S.; Ahnger-Pier, K.; Duan, B.; Surana, N.K.; Lu, R.; Cywes-Bentley, C.; Gadjeva, M.; Shan, Q.; Priebe, G.P.; et al. Intestinal Microbiota of Mice Influences Resistance to Staphylococcus aureus Pneumonia. Infect. Immun. 2015, 83, 4003–4014. [Google Scholar] [CrossRef]
- Aujla, S.J.; Chan, Y.R.; Zheng, M.; Fei, M.; Askew, D.J.; Pociask, D.A.; Reinhart, T.A.; McAllister, F.; Edeal, J.; Gaus, K.; et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 2008, 14, 275–281. [Google Scholar] [CrossRef] [Green Version]
- Tsai, H.-C.; Velichko, S.; Hung, L.-Y.; Wu, R. IL-17A and Th17 Cells in Lung Inflammation: An Update on the Role of Th17 Cell Differentiation and IL-17R Signaling in Host Defense against Infection. Clin. Dev. Immunol. 2013, 2013, 267971. [Google Scholar] [CrossRef] [Green Version]
- Wolf, K.; Plano, G.V.; Fields, K.A. A protein secreted by the respiratory pathogen Chlamydia pneumoniae impairs IL-17 signalling via interaction with human Act1. Cell. Microbiol. 2009, 11, 769–779. [Google Scholar] [CrossRef] [Green Version]
- Flannigan, K.L.; Denning, T.L. Segmented filamentous bacteria-induced immune responses: A balancing act between host protection and autoimmunity. Immunology 2018, 154, 537–546. [Google Scholar] [CrossRef] [Green Version]
- Lécuyer, E.; Rakotobe, S.; Lengliné-Garnier, H.; Lebreton, C.; Picard, M.; Juste, C.; Fritzen, R.; Eberl, G.; McCoy, K.D.; Macpherson, A.J.; et al. Segmented Filamentous Bacterium Uses Secondary and Tertiary Lymphoid Tissues to Induce Gut IgA and Specific T Helper 17 Cell Responses. Immunity 2014, 40, 608–620. [Google Scholar] [CrossRef] [Green Version]
- Wang, F.; Liu, J.; Zhang, Y.; Lei, P. Association of Helicobacter pylori infection with chronic obstructive pulmonary disease and chronic bronchitis: A meta-analysis of 16 studies. Infect. Dis. (Lond.) 2015, 47, 597–603. [Google Scholar] [CrossRef]
- Sze, M.A.; Chen, Y.-W.R.; Tam, S.; Tashkin, D.; Wise, R.A.; Connett, J.E.; Man, S.P.; Sin, D.D. The relationship between Helicobacter pylori seropositivity and COPD. Thorax 2015, 70, 923–929. [Google Scholar] [CrossRef] [Green Version]
- Wan, L.Y.M.; Chen, Z.J.; Shah, N.P.; El-Nezami, H. Modulation of Intestinal Epithelial Defense Responses by Probiotic Bacteria. Crit. Rev. Food Sci. Nutr. 2016, 56, 2628–2641. [Google Scholar] [CrossRef]
- Nguyen, Q.V.; Chong, L.C.; Hor, Y.-Y.; Lew, L.-C.; Rather, I.A.; Choi, S.-B. Role of Probiotics in the Management of COVID-19: A Computational Perspective. Nutrients 2022, 14, 274. [Google Scholar] [CrossRef]
- Cruz, C.S.; Ricci, M.F.; Vieira, A.T. Gut Microbiota Modulation as a Potential Target for the Treatment of Lung Infections. Front. Pharmacol. 2021, 12, 724033. [Google Scholar] [CrossRef]
- Jung, Y.-J.; Lee, Y.-T.; Le Ngo, V.; Cho, Y.-H.; Ko, E.-J.; Hong, S.-M.; Kim, K.-H.; Jang, J.-H.; Oh, J.-S.; Park, M.-K.; et al. Heat-killed Lactobacillus casei confers broad protection against influenza A virus primary infection and develops heterosubtypic immunity against future secondary infection. Sci. Rep. 2017, 7, 17360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Belkacem, N.; Serafini, N.; Wheeler, R.; Derrien, M.; Boucinha, L.; Couesnon, A.; Cerf-Bensussan, N.; Boneca, I.G.; Di Santo, J.P.; Taha, M.-K.; et al. Lactobacillus paracasei feeding improves immune control of influenza infection in mice. PLoS ONE 2017, 12, e0184976. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Yeh, C.; Jin, Z.; Ding, L.; Liu, B.Y.; Zhang, L.; Dannelly, H.K. Prospective study of probiotic supplementation results in immune stimulation and improvement of upper respiratory infection rate. Synth. Syst. Biotechnol. 2018, 3, 113–120. [Google Scholar] [CrossRef] [PubMed]
- Morimoto, K.; Takeshita, T.; Nanno, M.; Tokudome, S.; Nakayama, K. Modulation of natural killer cell activity by supplementation of fermented milk containing Lactobacillus casei in habitual smokers. Prev. Med. 2005, 40, 589–594. [Google Scholar] [CrossRef]
- Reale, M.; Boscolo, P.; Bellante, V.; Tarantelli, C.; Di Nicola, M.; Forcella, L.; Li, Q.; Morimoto, K.; Muraro, R. Daily intake of Lactobacillus casei Shirota increases natural killer cell activity in smokers. Br. J. Nutr. 2012, 108, 308–314. [Google Scholar] [CrossRef] [Green Version]
- Salva, S.; Villena, J.; Alvarez, S. Immunomodulatory activity of Lactobacillus rhamnosus strains isolated from goat milk: Impact on intestinal and respiratory infections. Int. J. Food Microbiol. 2010, 141, 82–89. [Google Scholar] [CrossRef]
- Luoto, R.; Ruuskanen, O.; Waris, M.; Kalliomäki, M.; Salminen, S.; Isolauri, E. Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: A randomized, placebo-controlled trial. J. Allergy Clin. Immunol. 2014, 133, 405–413. [Google Scholar] [CrossRef]
- Anwar, F.; Altayb, H.N.; Al-Abbasi, F.A.; Al-Malki, A.L.; Kamal, M.A.; Kumar, V. Antiviral effects of probiotic metabolites on COVID-19. J. Biomol. Struct. Dyn. 2021, 39, 4175–4184. [Google Scholar] [CrossRef]
- Pu, F.; Guo, Y.; Li, M.; Zhu, H.; Wang, S.; Shen, X.; He, M.; Huang, C.; He, F. Yogurt supplemented with probiotics can protect the healthy elderly from respiratory infections: A randomized controlled open-label trial. Clin. Interv. Aging 2017, 12, 1223–1231. [Google Scholar] [CrossRef] [Green Version]
- Zeng, J.; Wang, C.-T.; Zhang, F.-S.; Qi, F.; Wang, S.-F.; Ma, S.; Wu, T.-J.; Tian, H.; Tian, Z.-T.; Zhang, S.-L.; et al. Effect of probiotics on the incidence of ventilator-associated pneumonia in critically ill patients: A randomized controlled multicenter trial. Intensive Care Med. 2016, 42, 1018–1028. [Google Scholar] [CrossRef]
- Shimizu, K.; Yamada, T.; Ogura, H.; Mohri, T.; Kiguchi, T.; Fujimi, S.; Asahara, T.; Ojima, M.; Ikeda, M.; Shimazu, T. Synbiotics modulate gut microbiota and reduce enteritis and ventilator-associated pneumonia in patients with sepsis: A randomized controlled trial. Crit. Care 2018, 22, 239. [Google Scholar] [CrossRef] [Green Version]
- Mortaz, E.; Adcock, I.M.; Ricciardolo, F.L.M.; Varahram, M.; Jammati, H.; Velayati, A.A.; Folkerts, G.; Garssen, J. Anti-Inflammatory Effects of Lactobacillus rahmnosus and Bifidobacterium breve on Cigarette Smoke Activated Human Macrophages. PLoS ONE 2015, 10, e0136455. [Google Scholar] [CrossRef] [Green Version]
- Aimbire, F.; Carvalho, J.L.; Fialho, A.K.; Miranda, M.; Albertini, R.; Keller, A. Role of probiotics Bfidobacterium breve and Lactobacillus rhmanosus on lung inflammation and airway remodeling in an experimental model of chronic obstructive pulmonary disease. Eur. Respir. J. 2019, 54, PA2452. [Google Scholar] [CrossRef]
- Vieira, A.T.; Rocha, V.M.; Tavares, L.; Garcia, C.C.; Teixeira, M.M.; Oliveira, S.C.; Cassali, G.D.; Gamba, C.; Martins, F.S.; Nicoli, J.R. Control of Klebsiella pneumoniae pulmonary infection and immunomodulation by oral treatment with the commensal probiotic Bifidobacterium longum 51A. Microbes Infect. 2016, 18, 180–189. [Google Scholar] [CrossRef]
- Brodin, P.; Davis, M.M. Human immune system variation. Nat. Rev. Immunol. 2017, 17, 21–29. [Google Scholar] [CrossRef]
- Gebrayel, P.; Nicco, C.; Al Khodor, S.; Bilinski, J.; Caselli, E.; Comelli, E.M.; Egert, M.; Giaroni, C.; Karpinski, T.M.; Loniewski, I.; et al. Microbiota medicine: Towards clinical revolution. J. Transl. Med. 2022, 20, 111. [Google Scholar] [CrossRef]
- Hou, K.; Wu, Z.-X.; Chen, X.-Y.; Wang, J.-Q.; Zhang, D.; Xiao, C.; Zhu, D.; Koya, J.B.; Wei, L.; Li, J.; et al. Microbiota in health and diseases. Signal Transduct. Target. Ther. 2022, 7, 135. [Google Scholar] [CrossRef]
- Yang, Q.; Liang, Q.; Balakrishnan, B.; Belobrajdic, D.P.; Feng, Q.-J.; Zhang, W. Role of Dietary Nutrients in the Modulation of Gut Microbiota: A Narrative Review. Nutrients 2020, 12, 381. [Google Scholar] [CrossRef] [Green Version]
- Leeming, E.R.; Johnson, A.J.; Spector, T.D.; Le Roy, C.I. Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration. Nutrients 2019, 11, 2862. [Google Scholar] [CrossRef] [Green Version]
- Boisseau, N.; Barnich, N.; Koechlin-Ramonatxo, C. The Nutrition-Microbiota-Physical Activity Triad: An Inspiring New Concept for Health and Sports Performance. Nutrients 2022, 14, 924. [Google Scholar] [CrossRef]
- Cella, V.; Bimonte, V.M.; Sabato, C.; Paoli, A.; Baldari, C.; Campanella, M.; Lenzi, A.; Ferretti, E.; Migliaccio, S. Nutrition and Physical Activity-Induced Changes in Gut Microbiota: Possible Implications for Human Health and Athletic Performance. Foods 2021, 10, 3075. [Google Scholar] [CrossRef] [PubMed]
- World Gastroenterology Organisation Global Guidelines. Probiotics and Prebiotics. Available online: https://www.worldgastroenterology.org/UserFiles/file/guidelines/probiotics-and-prebiotics-english-2017.pdf (accessed on 15 February 2017).
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Krumina, A.; Bogdanova, M.; Gintere, S.; Viksna, L. Gut–Lung Microbiota Interaction in COPD Patients: A Literature Review. Medicina 2022, 58, 1760. https://doi.org/10.3390/medicina58121760
Krumina A, Bogdanova M, Gintere S, Viksna L. Gut–Lung Microbiota Interaction in COPD Patients: A Literature Review. Medicina. 2022; 58(12):1760. https://doi.org/10.3390/medicina58121760
Chicago/Turabian StyleKrumina, Angelika, Marina Bogdanova, Sandra Gintere, and Ludmila Viksna. 2022. "Gut–Lung Microbiota Interaction in COPD Patients: A Literature Review" Medicina 58, no. 12: 1760. https://doi.org/10.3390/medicina58121760