Bacterial microbiota of the upper respiratory tract and childhood asthma

Journal of Allergy and Clinical Immunology

Volumn 139, Issue 3, 2017, Pages 826-834.e13

  Depner, Martin ^a   Ege, Markus J ^a,b   Cox, Michael J ^c   Dwyer, Sarah ^c   Walker, Alan W ^d   Birzele, Lena T ^a   Genuneit, Jon ^e   Horak, Elisabeth ^f   Braun Fahrländer, Charlotte ^g,h   Danielewicz, Hanna ⁱ   Maier, Raina M ^j   Moffatt, Miriam F ^c   Cookson, William O ^c   Heederik, Dick ^k   von Mutius, Erika ^a,b   Legatzki, Antje ^a  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b German Center for Lung Research (DZL)   (Germany)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e UNIVERSITY OF ULM   (Germany)

^f INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^g SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^h UNIVERSITY OF BASEL   (Switzerland)

ⁱ WROCLAW MEDICAL UNIVERSITY   (Poland)

^j UNIVERSITY OF ARIZONA   (United States)

^k UTRECHT UNIVERSITY   (Netherlands)

more..

Author keywords

16S rRNA gene; Asthma; childhood; microbiota; nose; throat; upper respiratory tract

Indexed keywords

RNA 16S; BACTERIAL DNA;

ARTICLE; ASTHMA; BACTERIAL COLONIZATION; BACTERIAL FLORA; BACTERIAL LOAD; CHILD; CONTROLLED STUDY; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MALE; MICROBIAL COMMUNITY; MICROBIAL DIVERSITY; MORAXELLA; NONHUMAN; NOSE; PRIORITY JOURNAL; PYROSEQUENCING; RURAL AREA; TAXONOMY; THROAT; UPPER RESPIRATORY TRACT; AGRICULTURAL LAND; BACTERIUM; CLASSIFICATION; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; MICROFLORA; PHARYNX;

ASTHMA; BACTERIA; CHILD; DNA, BACTERIAL; FARMS; FEMALE; HUMANS; MALE; MICROBIOTA; NOSE; PHARYNX; RNA, RIBOSOMAL, 16S;

EID: 84994155175     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.05.050     Document Type: Article

References (48)

1. Blaser, M., Bork, P., Fraser, C., Knight, R., Wang, J., The microbiome explored: recent insights and future challenges. Nat Rev Microbiol 11 (2013), 213–217.
2. Petersen, C., Round, J.L., Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol 16 (2014), 1024–1033.
3. 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 (2013), 1193–1201.
4. Hilty, M., Burke, C., Pedro, H., Cardenas, P., Bush, A., Bossley, C., et al. Disordered microbial communities in asthmatic airways. PLoS One, 5, 2010, e8578.
5. 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 (2013), 1382–1387.
6. 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 (2013), 346–352 e1-3.
7. 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, 2014, e100645.
8. Huang, Y.J., Nariya, S., Harris, J.M., Lynch, S.V., Choy, D.F., Arron, J.R., et al. The airway microbiome in patients with severe asthma: associations with disease features and severity. J Allergy Clin Immunol 136 (2015), 874–884.
9. 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 (2011), 957–963.
10. Togias, A., Rhinitis and asthma: evidence for respiratory system integration. J Allergy Clin Immunol 111 (2003), 1171–1183.
11. Bisgaard, H., Hermansen, M.N., Buchvald, F., Loland, L., Halkjaer, L.B., Bonnelykke, K., et al. Childhood asthma after bacterial colonization of the airway in neonates. N Engl J Med 357 (2007), 1487–1495.
12. Teo, S.M., Mok, D., Pham, K., Kusel, M., Serralha, M., Troy, N., et al. The infant nasopharyngeal microbiome impacts severity of lower respiratory infection and risk of asthma development. Cell Host Microbe 17 (2015), 704–715.
13. Genuneit, J., Buchele, G., Waser, M., Kovacs, K., Debinska, A., Boznanski, A., et al. The GABRIEL advanced surveys: study design, participation and evaluation of bias. Paediatr Perinat Epidemiol 25 (2011), 436–447.
14. Illi, S., Depner, M., Genuneit, J., Horak, E., Loss, G., Strunz-Lehner, C., et al. Protection from childhood asthma and allergy in Alpine farm environments—the GABRIEL advanced studies. J Allergy Clin Immunol 129 (2012), 1470–1477.e6.
15. Cardenas, P.A., Cooper, P.J., Cox, M.J., Chico, M., Arias, C., Moffatt, M.F., et al. Upper airways microbiota in antibiotic-naive wheezing and healthy infants from the tropics of rural Ecuador. PLoS One, 7, 2012, e46803.
16. Claesson, M.J., O'Sullivan, O., Wang, Q., Nikkila, J., Marchesi, J.R., Smidt, H., et al. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One, 4, 2009, e6669.
17. Fierer, N., Hamady, M., Lauber, C.L., Knight, R., The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci U S A 105 (2008), 17994–17999.
18. Sim, K., Cox, M.J., Wopereis, H., Martin, R., Knol, J., Li, M.S., et al. Improved detection of bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. PLoS One, 7, 2012, e32543.
19. Quince, C., Lanzen, A., Davenport, R.J., Turnbaugh, P.J., Removing noise from pyrosequenced amplicons. BMC Bioinform, 12, 2011, 38.
20. Edgar, R.C., Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26 (2010), 2460–2461.
21. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7 (2010), 335–336.
22. 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.
23. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, et al. vegan: Community Ecology Package. R package version 2.0-10. 2013. Available at: https://cran.r-project.org/web/packages/vegan/index.html. Accessed August 19, 2016.
24. Chen J. GUniFrac: Generalized UniFrac distances. R package version 1.0. 2012.
25. Lozupone, C., Lladser, M.E., Knights, D., Stombaugh, J., Knight, R., UniFrac: an effective distance metric for microbial community comparison. ISME J 5 (2011), 169–172.
26. R-Development-Core-Team. R: A Language and Environment for Statistical Computing. 2008, R Foundation for Statistical Computing, Vienna, Austria.
27. McMurdie, P.J., Holmes, S., phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, 2013, e61217.
28. Costello, E.K., Lauber, C.L., Hamady, M., Fierer, N., Gordon, J.I., Knight, R., Bacterial community variation in human body habitats across space and time. Science 326 (2009), 1694–1697.
29. Frank, D.N., Feazel, L.M., Bessesen, M.T., Price, C.S., Janoff, E.N., Pace, N.R., The human nasal microbiota and Staphylococcus aureus carriage. PLoS One, 5, 2010, e10598.
30. Lemon, K.P., Klepac-Ceraj, V., Schiffer, H.K., Brodie, E.L., Lynch, S.V., Kolter, R., Comparative analyses of the bacterial microbiota of the human nostril and oropharynx. MBio, 1, 2010 e00129-10.
31. Oh, J., Conlan, S., Polley, E.C., Segre, J.A., Kong, H.H., Shifts in human skin and nares microbiota of healthy children and adults. Genome Med, 4, 2012, 77.
32. Park, H., Shin, J.W., Park, S.G., Kim, W., Microbial communities in the upper respiratory tract of patients with asthma and chronic obstructive pulmonary disease. PLoS One, 9, 2014, e109710.
33. Segata, N., Haake, S.K., Mannon, P., Lemon, K.P., Waldron, L., Gevers, D., et al. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol, 13, 2012, R42.
34. Yan, M., Pamp, S.J., Fukuyama, J., Hwang, P.H., Cho, D.Y., Holmes, S., et al. Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host Microbe 14 (2013), 631–640.
35. Bassis, C.M., Tang, A.L., Young, V.B., Pynnonen, M.A., The nasal cavity microbiota of healthy adults. Microbiome, 2, 2014, 27.
36. Tlaskalova-Hogenova, H., Stepankova, R., Hudcovic, T., Tuckova, L., Cukrowska, B., Lodinova-Zadnikova, R., et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett 93 (2004), 97–108.
37. Bisgaard, H., Hermansen, M.N., Bonnelykke, K., Stokholm, J., Baty, F., Skytt, N.L., et al. Association of bacteria and viruses with wheezy episodes in young children: prospective birth cohort study. BMJ, 341, 2010, c4978.
38. Biesbroek, G., Tsivtsivadze, E., Sanders, E.A.M., Montijn, R., Veenhoven, R.H., Keijser, B.J.F., et al. Early respiratory microbiota composition determines bacterial succession patterns and respiratory health in children. Am J Respir Crit Care Med 190 (2014), 1283–1292.
39. de Vries, S.P., Bootsma, H.J., Hays, J.P., Hermans, P.W., Molecular aspects of Moraxella catarrhalis pathogenesis. Microbiol Mol Biol Rev 73 (2009), 389–406.
40. Castro-Nallar, E., Shen, Y., Freishtat, R.J., Perez-Losada, M., Manimaran, S., Liu, G., et al. Integrating microbial and host transcriptomics to characterize asthma-associated microbial communities. BMC Med Genomics, 8, 2015, 50.
41. Abrahamsson, T.R., Jakobsson, H.E., Andersson, A.F., Bjorksten, B., Engstrand, L., Jenmalm, M.C., Low gut microbiota diversity in early infancy precedes asthma at school age. Clin Exp Allergy 44 (2014), 842–850.
42. Hoen, A.G., Li, J., Moulton, L.A., O'Toole, G.A., Housman, M.L., Koestler, D.C., et al. Associations between gut microbial colonization in early life and respiratory outcomes in cystic fibrosis. J Pediatr 167 (2015), 138–147 e1-3.
43. Abreu, N.A., Nagalingam, N.A., Song, Y., Roediger, F.C., Pletcher, S.D., Goldberg, A.N., et al. Sinus microbiome diversity depletion and Corynebacterium tuberculostearicum enrichment mediates rhinosinusitis. Sci Transl Med, 4, 2012, 151ra124.
44. Ege, M.J., Mayer, M., Normand, A.C., Genuneit, J., Cookson, W.O., Braun-Fahrlander, C., et al. Exposure to environmental microorganisms and childhood asthma. N Engl J Med 364 (2011), 701–709.
45. Normand, A.C., Sudre, B., Vacheyrou, M., Depner, M., Wouters, I.M., Noss, I., et al. Airborne cultivable microflora and microbial transfer in farm buildings and rural dwellings. Occup Environ Med 68 (2011), 849–855.
46. von Hertzen, L., Hanski, I., Haahtela, T., Natural immunity: biodiversity loss and inflammatory diseases are two global megatrends that might be related. EMBO Rep 12 (2011), 1089–1093.
47. Claesson, M.J., O'Sullivan, O., Wang, Q., Nikkila, J., Marchesi, J.R., Smidt, H., et al. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS One, 4, 2009, e6669.
48. Sim, K., Cox, M.J., Wopereis, H., Martin, R., Knol, J., Li, M.S., et al. Improved detection of bifidobacteria with optimised 16S rRNA-gene based pyrosequencing. PLoS One, 7, 2012, e32543.