The respiratory microbiome: an underappreciated player in the human response to inhaled pollutants?

Annals of Epidemiology

Volumn 26, Issue 5, 2016, Pages 355-359

  Adar, Sara D ^a   Huffnagle, Gary B ^b   Curtis, Jeffrey L ^b,c  

^a UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

Air pollution; Gut; Inhaled irritants toxicants; Respiratory microbiome; Smoking; Susceptibility

Indexed keywords

IRRITANT AGENT;

AIR POLLUTION; BACTERIAL COLONIZATION; BACTEROIDETES; CHRONIC LUNG DISEASE; DISEASE COURSE; DISEASE EXACERBATION; DISEASE PREDISPOSITION; ENVIRONMENTAL EXPOSURE; HUMAN; IMMUNE RESPONSE; INHALATION; LUNG LAVAGE; MICROBIAL COMMUNITY; MICROBIOME; NONHUMAN; POLLUTANT; PRIORITY JOURNAL; RESPIRATORY MICROBIOME; REVIEW; SPUTUM; VERRUCOMICROBIA; AIR POLLUTANT; ENVIRONMENTAL MONITORING; FEMALE; HEALTH STATUS; MALE; MICROBIOLOGY; MICROFLORA; PATHOPHYSIOLOGY; PHYSIOLOGY; RESPIRATORY SYSTEM; RESPIRATORY TRACT DISEASE; RISK ASSESSMENT;

AIR POLLUTANTS; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL MONITORING; FEMALE; HEALTH STATUS; HUMANS; MALE; MICROBIOTA; RESPIRATORY SYSTEM; RESPIRATORY TRACT DISEASES; RISK ASSESSMENT;

EID: 84965028206     PISSN: 10472797     EISSN: 18732585     Source Type: Journal    
DOI: 10.1016/j.annepidem.2016.03.010     Document Type: Review

References (78)

1. [1] Brunekreef, B., Holgate, S.T., Air pollution and health. Lancet 360:9341 (2002), 1233–1242.
2. [2] Lim, S.S., Vos, T., Flaxman, A.D., Goodarz, D., Shibuya, K., Adair-Rohani, H., et al. A comparative risk assessment of burden of disease and injury attributable to 67 risk factors and risk factor clusters in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:9859 (2013), 2224–2260.
3. [3] Laden, F., Schwartz, J., Speizer, F.E., Dockery, D.W., Reduction in fine particulate air pollution and mortality—extended follow-up of the Harvard six cities study. Am J Respir Crit Care Med 173:6 (2006), 667–672.
4. [4] Jones, M., Barnoya, J., Stranges, S., Losonczy, L., Navas-Acien, A., Cardiovascular events following smoke-free legislations: an updated systematic review and meta-analysis. Curr Environ Health Rep 1:3 (2014), 239–249.
5. [5] Pope, C.A., Ezzati, M., Dockery, D.W., Fine particulate air pollution and life expectancy in the United States. N Engl J Med 360:4 (2009), 376–386.
6. [6] Correia, A.W., Pope, C.A., Dockery, D.W., Wang, Y., Ezzati, M., Dominici, F., Effect of air pollution control on life expectancy in the United States: an analysis of 545 U.S. Counties for the period from 2000 to 2007. Epidemiology 24:1 (2013), 23–31.
7. [7] Bell, M.L., Zanobetti, A., Dominici, F., Evidence on vulnerability and susceptibility to health risks associated with short-term exposure to particulate matter: a systematic review and meta-analysis. Am J Epidemiol 178 (2013), 865–876.
8. [8] Sacks, J.D., Stanek, L.W., Luben, T.J., Johns, D.O., Buckley, B.J., Brown, J.S., et al. Particulate matter-induced health effects: who is susceptible?. Environ Health Perspect 119:4 (2011), 446–454.
9. [9] Cho, I., Blaser, M.J., The Human Microbiome: At the interface of health and disease. Nat Rev Genet 13:4 (2012), 260–270.
10. [10] Van de Wiele, T., Vanhaecke, L., Boeckaert, C., Peru, K., Headley, J., Verstraete, W., et al. Human colon microbiota transform polycyclic aromatic hydrocarbons to estrogenic metabolites. Environ Health Perspect 113 (2005), 6–10.
11. [11] Vanhaecke, L., Van Hoof, N., Van Brabandt, W., Soenen, B., Heyerick, A., De Kimpe, N., et al. Metabolism of the food-associated carcinogen 2-amino-1-methyl-6-phenylimidazo [4, 5-b] pyridine by human intestinal microbiota. J Agric Food Chem 54:9 (2006), 3454–3461.
12. [12] Tuohy, K.M., Hinton, D.J., Davies, S.J., Crabbe, M.J., Gibson, G.R., Ames, J.M., Metabolism of Maillard reaction products by the human gut microbiota–implications for health. Mol Nutr Food Res 50:9 (2006), 847–857.
13. [13] Hilty, M., Burke, C., Pedro, H., Cardenas, P., Bush, A., Bossley, C., et al. Disordered microbial communities in asthmatic airways. PLoS One, 5(1), 2010, e8578.
14. [14] Erb-Downward, J.R., Thompson, D.L., Han, M.K., Freeman, C.M., McCloskey, L., Schmidt, L.A., et al. Analysis of the lung microbiome in the “healthy” smoker and in COPD. PLoS One, 6(2), 2011, e16384.
15. [15] Beck, J.M., Young, V.B., Huffnagle, G.B., The microbiome of the lung. Transl Res 160:4 (2012), 258–266.
16. [16] Dickson, R.P., Martinez, F.J., Huffnagle, G.B., The role of the microbiome in exacerbations of chronic lung diseases. Lancet 384:9944 (2014), 691–702.
17. [17] Huang, Y.J., Charlson, E.S., Collman, R.G., Colombini-Hatch, S., Martinez, F.D., Senior, R.M., The role of the lung microbiome in health and disease. A National Heart, Lung, and Blood Institute workshop report. Am J Respir Crit Care Med 187:12 (2013), 1382–1387.
18. [18] Dickson, R.P., Huffnagle, G.B., The lung microbiome: new principles for respiratory bacteriology in health and disease. PLoS Pathog, 11(7), 2015, e1004923.
19. [19] Lighthart, B., Mini-review of the concentration variations found in the alfresco atmospheric bacterial populations. Aerobiologia 16:1 (2000), 7–16.
20. [20] Dickson, R.P., Erb-Downward, J.R., Freeman, C.M., McCloskey, L., Beck, J.M., Huffnagle, G.B., et al. Spatial variation in the healthy human lung microbiome and the adapted island model of lung biogeography. Ann Am Thorac Soc 12:6 (2015), 821–830.
21. [21] Dickson, R.P., Erb-Downward, J.R., Freeman, C.M., Walker, N., Scales, B.S., Beck, J.M., et al. Changes in the lung microbiome following lung transplantation include the emergence of two distinct Pseudomonas species with distinct clinical associations. PLoS One, 9(5), 2014, e97214.
22. [22] Charlson, E.S., Bittinger, K., Haas, A.R., Fitzgerald, A.S., Frank, I., Yadav, A., et al. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 184:8 (2011), 957–963.
23. [23] Bassis, C.M., Erb-Downward, J.R., Dickson, R.P., Freeman, C.M., Schmidt, T.M., Young, V.B., et al. Analysis of the upper respiratory tract microbiotas as the source of the lung and gastric microbiotas in healthy individuals. MBio, 6(2), 2015, e00037.
24. [24] Hayashi, H., Sakamoto, M., Benno, Y., Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiol Immunol 46:8 (2002), 448–535.
25. [25] Huang, Y.J., Nelson, C.E., Brodie, E.L., Desantis, T.Z., Baek, M.S., Liu, J., et al. Airway microbiota and bronchial hyperresponsiveness in patients with suboptimally controlled asthma. J Allergy Clin Immunol 127:2 (2011), 372–381 e371–373.
26. [26] Marri, P.R., Stern, D.A., Wright, A.L., Billheimer, D., Martinez, F.D., Asthma-associated differences in microbial composition of induced sputum. J Allergy Clin Immunol 131:2 (2013), 346–352 e343.
27. [27] Goleva, E., Jackson, L.P., Harris, J.K., Robertson, C.E., Sutherland, E.R., Hall, C.F., et al. The effects of airway microbiome on corticosteroid responsiveness in asthma. Am J Respir Crit Care Med 188:10 (2013), 1193–1201.
28. [28] Huang, Y.J., Kim, E., Cox, M.J., Brodie, E.L., Brown, R., Wiener-Kronish, J.P., et al. A persistent and diverse airway microbiota present during chronic obstructive pulmonary disease exacerbations. OMICS 14:1 (2010), 9–59.
29. [29] Segal, L.N., Alekseyenko, A.V., Clemente, J.C., Kulkarni, R., Wu, B., Chen, H., et al. Enrichment of lung microbiome with supraglottic taxa is associated with increased pulmonary inflammation. Microbiome, 1(1), 2013, 19.
30. [30] Green, B.J., Wiriyachaiporn, S., Grainge, C., Rogers, G.B., Kehagia, V., Lau, L., et al. Potentially pathogenic airway bacteria and neutrophilic inflammation in treatment resistant severe asthma. PLoS One, 9(6), 2014, e100645.
31. [31] Rogers, G.B., Zain, N.M., Bruce, K.D., Burr, L.D., Chen, A.C., Rivett, D.W., et al. A novel microbiota stratification system predicts future exacerbations in bronchiectasis. Ann Am Thorac Soc 11:4 (2014), 496–503.
32. [32] Weiss, B., Bujanover, Y., Yahav, Y., Vilozni, D., Fireman, E., Efrati, O., Probiotic supplementation affects pulmonary exacerbations in patients with cystic fibrosis: a pilot study. Pediatr Pulmonol 45:6 (2010), 536–540.
33. [33] Russell, S.L., Gold, M.J., Hartmann, M., Willing, B.P., Thorson, L., Wlodarska, M., et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep 13:5 (2012), 440–447.
34. [34] USEPA. Integrated Science Assessment for Particulate Matter. 2009, NCEA-RTP Office, Research Triangle Park, NC EPA/600/R-08/139F.
35. [35] Brook, R.D., Rajagopalan, S., Pope, C.A., Brook, J.R., Bhatnagar, A., Diez-Roux, A.V., et al. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 121 (2010), 2331–2378.
36. [36] Adar, S.D., Adamkiewicz, G., Gold, D.R., Schwartz, J., Coull, B.A., Suh, H., Ambient and microenvironmental particles and exhaled nitric oxide before and after a group bus trip. Environ Health Perspect 115:4 (2007), 507–512.
37. [37] Dubowsky, S.D., Suh, H., Schwartz, J., Coull, B.A., Gold, D.R., Diabetes, obesity, and hypertension may enhance associations between air pollution and markers of systemic inflammation. Environ Health Perspect 114:7 (2006), 992–998.
38. [38] Mirabelli, M.C., Golan, R., Greenwald, R., Raysoni, A.U., Holguin, F., Kewada, P., et al. Modification of traffic-related respiratory response by asthma control in a population of car commuters. Epidemiology 26 (2015), 546–555.
39. [39] Zanobetti, A., Schwartz, J., Are diabetics more susceptible to the health effects of airborne particles?. Am J Respir Crit Care Med 164:5 (2001), 831–833.
40. [40] Zanobetti, A., Schwartz, J., Cardiovascular damage by airborne particles: are diabetics more susceptible?. Epidemiology 13:5 (2002), 588–592.
41. [41] Zanobetti, A., Schwartz, J., Are diabetics more susceptible to CVD health effects of airborne particles? Results from four cities. Epidemiology, 13(4), 2002, S168.
42. [42] Lu, K., Abo, R.P., Schlieper, K.A., Graffam, M.E., Levine, S., Wishnok, J.S., et al. Arsenic exposure perturbs the gut microbiome and its metabolic profile in mice: an integrated metagenomics and metabolomics analysis. Environ Health Perspect 122:3 (2014), 284–291.
43. [43] Ley, R.E., Turnbaugh, P.J., Klein, S., Gordon, J.I., Microbial ecology: human gut microbes associated with obesity. Nature 444:7122 (2006), 1022–1023.
44. [44] Bervoets, L., Van Hoorenbeeck, K., Kortleven, I., Van Noten, C., Hens, N., Vael, C., et al. Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog, 5, 2013, 10.
45. [45] Zarrinpar, A., Loomba, R., Review article: the emerging interplay among the gastrointestinal tract, bile acids and incretins in the pathogenesis of diabetes and non-alcoholic fatty liver disease. Aliment Pharmacol Ther 36:10 (2012), 909–921.
46. [46] Choi, J.J., Eum, S.Y., Rampersaud, E., Daunert, S., Abreu, M.T., Toborek, M., Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environ Health Perspect 121:6 (2013), 725–730.
47. [47] Silver, S., Phung, L.T., Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:2 (2005), 599–608.
48. [48] Van de Wiele, T., Gallawa, C.M., Kubachka, K.M., Creed, J.T., Basta, N., Dayton, E.A., et al. Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ Health Perspect 118:7 (2010), 1004–1009.
49. [49] DCR, S.S., Alava, P., Zekker, I., Du Laing, G., Van de Wiele, T., Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. Environ Health Perspect 122:8 (2014), 817–822.
50. [50] Youngji, C., David, I.K., Joel, A.M., Jeffrey, D.B., Stephanie, A.S., The effects of a depleted gut microbiome on ozone induced airway hyperresponsiveness and inflammation in mice. Am J Respir Crit Care Med, 189, 2014, A6390.
51. [51] Arrieta, M.C., Stiemsma, L.T., Amenyogbe, N., Brown, E.M., Finlay, B., The intestinal microbiome in early life: health and disease. Front Immunol, 5, 2014, 427.
52. [52] Delima, S.L., McBride, R.K., Preshaw, P.M., Heasman, P.A., Kumar, P.S., Response of subgingival bacteria to smoking cessation. J Clin Microbiol 48:7 (2010), 2344–2349.
53. [53] Kumar, P.S., Matthews, C.R., Joshi, V., de Jager, M., Aspiras, M., Tobacco smoking affects bacterial acquisition and colonization in oral biofilms. Infect Immun 79:11 (2011), 4730–4738.
54. [54] Biedermann, L., Zeitz, J., Mwinyi, J., Sutter-Minder, E., Rehman, A., Off, S.J., et al. Smoking cessation induces profound changes in the composition of the intestinal microbiota in humans. PLoS One, 8(3), 2013, e59260.
55. [55] Morris, A., Beck, J.M., Schloss, P.D., Campbell, T.B., Crothers, K., Curtis, J.L., et al. Comparison of the respiratory microbiome in healthy nonsmokers and smokers. Am J Respir Crit Care Med 187:10 (2013), 1067–1075.
56. [56] Chen, J., Bittinger, K., Charlson, E.S., Hoffman, C., Lewis, J., Wu, G.D., et al. Associating microbiome composition with environmental covariates using generalized UniFrac distances. Bioinformatics 28:16 (2012), 2106–2113.
57. [57] Straus, W.L., Plouffe, J.F., File, T.M., Lipman, H.B., Hackman, B.H., Salstrom, S.J., et al. Risk factors for domestic acquisition of Legionnaires disease. Arch Intern Med 156:15 (1996), 1685–1692.
58. [58] Arcavi, L., Benowitz, N.L., Cigarette smoking and infection. Arch Intern Med 164:20 (2004), 2206–2216.
59. [59] Smith, K.R., Samet, J.M., Romieu, I., Bruce, N., Indoor air pollution in developing countries and acute lower respiratory infections in children. Thorax 55:6 (2000), 518–532.
60. [60] Aronson, M.D., Weiss, S.T., Ben, R.L., Komaroff, A.L., Association between cigarette smoking and acute respiratory tract illness in young adults. JAMA 248:2 (1982), 181–183.
61. [61] Bensenor, I.M., Cook, N.R., Lee, I.M., Chown, M.J., Hennekens, C.H., Buring, J.E., et al. Active and passive smoking and risk of colds in women. Ann Epidemiol 11:4 (2001), 225–231.
62. [62] Stampfli, M.R., Anderson, G.P., How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat Rev Immunol 9:5 (2009), 377–384.
63. [63] Marcy, T.W., Merrill, W.W., Cigarette smoking and respiratory tract infection. Clin Chest Med 8:3 (1987), 381–391.
64. [64] Erickson, J.J., Gilchuk, P., Hastings, A.K., Tollefson, S.J., Johnson, M., Downing, M.B., et al. Viral acute lower respiratory infections impair CD8+ T cells through PD-1. J Clin Invest 122:8 (2012), 2967–2982.
65. [65] Molyneaux, P.L., Mallia, P., Cox, M.J., Footitt, J., Willis-Owen, S.A., Homola, D., et al. Outgrowth of the bacterial airway microbiome after rhinovirus exacerbation of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 188:10 (2013), 1224–1231.
66. [66] McKendry, R.T., Spalluto, C.M., Burke, H., Nicholas, B., Cellura, D., Al-Shamkhani, A., et al. Dysregulation of anti-viral function of CD8+T cells in the COPD lung: role of the PD1/PDL1 axis. Am J Respir Crit Care Med 193 (2016), 642–651.
67. [67] Jervis-Bardy, J., Leong, L.E., Marri, S., Smith, R.J., Choo, J.M., Smith-Vaughan, H.C., et al. Deriving accurate microbiota profiles from human samples with low bacterial content through post-sequencing processing of Illumina MiSeq data. Microbiome, 3, 2015, 19.
68. [68] Salter, S.J., Cox, M.J., Turek, E.M., Calus, S.T., Cookson, W.O., Moffatt, M.F., et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol, 12, 2014, 87.
69. [69] Biesbroek, G., Sanders, E.A., Roeselers, G., Wang, X., Caspers, M.P.M., Trzcinski, K., et al. Deep sequencing analyses of low density microbial communities: working at the boundary of accurate microbiota detection. PLoS One, 7(3), 2012, e32942.
70. [70] Willner, D., Daly, J., Whiley, D., Grimwood, K., Wainwright, C.E., Hugenholtz, P., Comparison of DNA extraction methods for microbial community profiling with an application to pediatric bronchoalveolar lavage samples. PLoS One, 7(4), 2012, e34605.
71. [71] Mestecky, J., The common mucosal immune system and current strategies for induction of immune responses in external secretions. J Clin Immunol 7:4 (1987), 265–276.
72. [72] Ichinohe, T., Pang, I.K., Kumamoto, Y., Peaper, D.R., Ho, J.H., Murray, T.S., et al. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A 108:13 (2011), 5354–5359.
73. [73] Yasui, H., Kiyoshima, J., Hori, T., Reduction of influenza virus titer and protection againstinfluenza virus infection in infant mice fed Lactobacillus Casei Shirota. Clin Diagn Lab Immunol 11:4 (2004), 675–679.
74. [74] Huang, Y.J., Boushey, H.A., The microbiome in asthma. J Allergy Clin Immunol 135:1 (2015), 25–30.
75. [75] Trompette, A., Gollwitzer, E.S., Yadava, K., Sichelstiel, A.K., Sprenger, N., Ngom-Bru, C., et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 20:2 (2014), 159–166.
76. [76] De Brouwere, K., Buekers, J., Cornelis, C., Schlekat, C.E., Oller, A.R., Assessment of indirect human exposure to environmental sources of nickel: oral exposure and risk characterization for systemic effects. Sci Total Environ 419 (2012), 25–36.
77. [77] Salim, S.Y., Kaplan, G.G., Madsen, K.L., Air pollution effects on the gut microbiota: a link between exposure and inflammatory disease. Gut Microbes 5:2 (2014), 215–219.
78. [78] Kish, L., Hotte, N., Kaplan, G.G., Vincent, R., Tso, R., Ganzle, M., et al. Environmental particulate matter induces murine intestinal inflammatory responses and alters the gut microbiome. PLoS One, 8(4), 2013, e62220.