Reestablishment of recipient-associated microbiota in the lung allograft is linked to reduced risk of bronchiolitis obliterans syndrome

American Journal of Respiratory and Critical Care Medicine

Volumn 187, Issue 6, 2013, Pages 640-647

  Willner, Dana L ^a   Hugenholtz, Philip ^a   Yerkovich, Stephanie T ^a,b   Tan, Maxine E ^a,b   Daly, Joshua N ^a   Lachner, Nancy ^a   Hopkins, Peter M ^a,b   Chambers, Daniel C ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b THE PRINCE CHARLES HOSPITAL   (Australia)

Author keywords

Bronchiolitis obliterans syndrome; Lung transplantation; Microbiome

Indexed keywords

RNA 16S;

ADULT; ARTICLE; ASPERGILLUS; BRONCHIOLITIS OBLITERANS; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CYSTIC FIBROSIS; FEMALE; GENE AMPLIFICATION; HUMAN; LONGITUDINAL STUDY; LUNG LAVAGE; LUNG TRANSPLANTATION; MAJOR CLINICAL STUDY; MALE; MICROBIAL COMMUNITY; MICROFLORA; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PYROSEQUENCING; RECIPIENT; RISK FACTOR; STREPTOCOCCUS; VEILLONELLA;

ADULT; ASPERGILLUS FUMIGATUS; BRONCHIOLITIS OBLITERANS; BRONCHOALVEOLAR LAVAGE FLUID; CYSTIC FIBROSIS; DNA, BACTERIAL; FEMALE; HUMANS; LUNG; LUNG TRANSPLANTATION; MALE; METAGENOME; MIDDLE AGED; PRINCIPAL COMPONENT ANALYSIS; PSEUDOMONAS; RISK ASSESSMENT; RISK FACTORS; STREPTOCOCCUS; SYNDROME; TRANSPLANTATION, HOMOLOGOUS; VEILLONELLA;

EID: 84875148797     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201209-1680OC     Document Type: Article

References (43)

1. Orens JB, Garrity ER Jr. General overview of lung transplantation and review of organ allocation. Proc Am Thorac Soc 2009;6:13-19.
2. Christie JD, Edwards LB, Kucheryavaya AY, Benden C, Dipchand AI, Dobbels F, Kirk R, Rahmel AO, Stehlink J, Hertz MI. The Registry of the International Society for Heart and Lung Transplantation: 29th Adult Lung and Heart-Lung Transplant Report - 2012. J Heart Lung Transplant 2012;31:1073-1086.
3. Hayes D Jr. A review of bronchiolitis obliterans syndrome and therapeutic strategies. J Cardiothorac Surg 2011;6:92.
4. Vos R, Vanaudenaerde BM, Geudens N, Dupont LJ, Van Raemdonck DE, Verleden GM. Pseudomonal airway colonisation: risk factor for bronchiolitis obliterans syndrome after lung transplantation? Eur Respir J 2008;31:1037-1045.
5. Gupta MR, Valentine VG, Walker JE Jr, Lombard GA, LaPlace SG, Seoane L, Taylor DE, Dhillon GS. Clinical spectrum of gram-positive infections in lung transplantation. Transpl Infect Dis 2009;11:424-431.
6. Glanville AR, Gencay M, Tamm M, Chhajed P, Plit M, Hopkins P, Aboyoun C, Roth M, Malouf M. Chlamydia pneumoniae infection after lung transplantation. J Heart Lung Transplant 2005;24:131-136.
7. Gottlieb J, Mattner F, Weissbrodt H, Dierich M, Fuehner T, Strueber M, Simon A, Welte T. Impact of graft colonization with gram-negative bacteria after lung transplantation on the development of bronchiolitis obliterans syndrome in recipients with cystic fibrosis. Respir Med 2009; 103:743-749.
8. Walter S, Gudowius P, Bosshammer J, Römling U, Weissbrodt H, Schürmann W, von der Hardt H, Tümmler B. Epidemiology of chronic Pseudomonas aeruginosa infections in the airways of lung transplant recipients with cystic fibrosis. Thorax 1997;52:318-321.
9. Botha P, Archer L, Anderson RL, Lordan J, Dark JH, Corris PA, Gould K, Fisher AJ. Pseudomonas aeruginosa colonization of the allograft after lung transplantation and the risk of bronchiolitis obliterans syndrome. Transplantation 2008;85:771-774.
10. Nunley DR, Grgurich W, Iacono AT, Yousem S, Ohori NP, Keenan RJ, Dauber JH. Allograft colonization and infections with Pseudomonas in cystic fibrosis lung transplant recipients. Chest 1998;113:1235-1243.
11. Guss AM, Roeselers G, Newton IL, Young CR, Klepac-Ceraj V, Lory S, Cavanaugh CM. Phylogenetic and metabolic diversity of bacteria associated with cystic fibrosis. ISME J 2011;5:20-29.
12. Willner D, Haynes MR, Furlan M, Schmieder R, Lim YW, Rainey PB, Rohwer F, Conrad D. Spatial distribution of microbial communities in the cystic fibrosis lung. ISME J 2011;6:471-474.
13. Charlson ES, Bittinger K, Haas AR, Fitzgerald AS, Frank I, Yadav A, Bushman FD, Collman RG. Topographical continuity of bacterial populations in the healthy human respiratory tract. Am J Respir Crit Care Med 2011;184:957-963.
14. Charlson ES, Diamond JM, Bittinger K, Fitzgerald AS, Yadav A, Haas AR, Bushman FD, Collman RG. Lung-enriched organisms and aberrant bacterial and fungal respiratory microbiota following lung transplant. Am J Respir Crit Care Med 2012;186:536-545.
15. Willner D, Hugenholtz P, Tan ME, Yerkovich ST, Hopkins PM, Chambers DC. Distinct microbial signatures of healthy and failing lung allografts. J Heart Lung Transplant 2012;31:S32.
16. Estenne M, Maurer JR, Boehler A, Egan JJ, Frost A, Hertz M, Mallory GB, Snell GI, Yousem S. Bronchiolitis obliterans syndrome 2001: an update of the diagnostic criteria. J Heart Lung Transplant 2002;21: 297-310.
17. Stewart S, Fishbein MC, Snell GI, Berry GJ, Boehler A, Burke MM, Glanville A, Gould FK, Magro C, Marboe CC, et al. Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection. J Heart Lung Transplant 2007;26:1229-1242.
18. Willner D, Daly J, Whiley D, Grimwood K, Wainwright CE, Hugenholtz P. Comparison of DNA extraction methods for microbial community profiling with an application to pediatric bronchoalveolar lavage samples. PLoS ONE 2012;7:e34605.
19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-336.
20. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27:2194-2200.
21. Li W, Fu L, Niu B, Wu S, Wooley J. Ultrafast clustering algorithms for metagenomic sequence analysis. Brief Bioinform 2012;13:656-668.
22. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012;6:610-618.
23. Hamady M, Lozupone C, Knight R. Fast UniFrac: facilitating highthroughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 2009;4:17-27.
24. Dixon P. VEGAN, a package of R functions for community ecology. J Veg Sci 2003;14:927-930.
25. Lozupone C, Lladser ME, Knights D, Stombaugh J, Knight R. UniFrac: an effective distance metric for microbial community comparison. ISME J 2011;5:169-172.
26. Stressmann FA, Rogers GB, van der Gast CJ, Marsh P, Vermeer LS, Carroll MP, Hoffman L, Daniels TW, Patel N, Forbes B, et al. Long-term cultivation-independent microbial diversity analysis demonstrates that bacterial communities infecting the adult cystic fibrosis lung show stability and resilience. Thorax 2012;67:867-873.
27. Moree WJ, Phelan VV, Wu CH, Bandeira N, Cornett DS, Duggan BM, Dorrestein PC. Interkingdom metabolic transformations captured by microbial imaging mass spectrometry. Proc Natl Acad Sci USA 2012; 109:13811-13816.
28. Delhaes L, Monchy S, Fréalle E, Hubans C, Salleron J, Leroy S, Prevotat A, Wallet F, Wallaert B, Dei-Cas E, et al. The airway microbiota in cystic fibrosis: a complex fungal and bacterial community-implications for therapeutic management. PLoS ONE 2012;7:e36313.
29. Zhao J, Schloss PD, Kalikin LM, Carmody LA, Foster BK, Petrosino JF, Cavalcoli JD, VanDevanter DR, Murray S, Li JZ, et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc Natl Acad Sci USA 2012;109:5809-5814.
30. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM, Wolfgang MC. The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS ONE 2012;7:e45001.
31. Charlson ES, Bittinger K, Chen J, Diamond JM, Li H, Collman RG, Bushman FD. Assessing bacterial populations in the lung by replicate analysis of samples from the upper and lower respiratory tracts. PLoS ONE 2012;7:e42786.
32. Blondeau K, Mertens V, Vanaudenaerde BA, Verleden GM, Van Raemdonck DE, Sifrim D, Dupont LJ. Gastro-oesophageal reflux and gastric aspiration in lung transplant patients with or without chronic rejection. Eur Respir J 2008;31:707-713.
33. Atkins BZ, Petersen RP, Daneshmand MA, Turek JW, Lin SS, Davis RD Jr. Impact of oropharyngeal dysphagia on long-term outcomes of lung transplantation. Ann Thorac Surg 2010;90:1622-1628.
34. Mertens V, Blondeau K, Van Oudenhove L, Vanaudenaerde B, Vos R, Farre R, Pauwels A, Verleden G, Van Raemdonck D, Sifrim D, et al. Bile acids aspiration reduces survival in lung transplant recipients with BOS despite azithromycin. Am J Transplant 2011;11:329-335.
35. Nakajima T, Palchevsky V, Perkins DL, Belperio JA, Finn PW. Lung transplantation: infection, inflammation, and the microbiome. Semin Immunopathol 2011;33:135-156.
36. Bianconi I, Milani A, Cigana C, Paroni M, Levesque RC, Bertoni G, Bragonzi A. Positive signature-tagged mutagenesis in Pseudomonas aeruginosa: tracking patho-adaptive mutations promoting airways chronic infection. PLoS Pathog 2011;7:e1001270.
37. Cigana C, Curcurù L, Leone MR, Ieranò T, Lorè NI, Bianconi I, Silipo A, Cozzolino F, Lanzetta R, Molinaro A, et al. Pseudomonas aeruginosa exploits lipid A and muropeptides modification as a strategy to lower innate immunity during cystic fibrosis lung infection. PLoS ONE 2009;4:e8439.
38. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR, D'Argenio DA, Miller SI, Ramsey BW, Speert DP, Moskowitz SM, et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci USA 2006;103:8487-8492.
39. Lorè NI, Cigana C, De Fino I, Riva C, Juhas M, Schwager S, Eberl L, Bragonzi A. Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS ONE 2012;7:e35648.
40. Mainz JG, Hentschel J, Schien C, Cramer N, Pfister W, Beck JF, Tümmler B. Sinonasal persistence of Pseudomonas aeruginosa after lung transplantation. J Cyst Fibros 2012;11:158-161.
41. Leung M-K, Rachakonda L, Weill D, Hwang PH. Effects of sinus surgery on lung transplantation outcomes in cystic fibrosis. Am J Rhinol 2008;22:192-196.
42. Hansen SK, Rau MH, Johansen HK, Ciofu O, Jelsbak L, Yang L, Folkesson A, Jarmer HØ, Aanæs K, von Buchwald C, et al. Evolution and diversification of Pseudomonas aeruginosa in the paranasal sinuses of cystic fibrosis children have implications for chronic lung infection. ISME J 2012;6:31-45.
43. Johansen HK, Aanaes K, Pressler T, Nielsen KG, Fisker J, Skov M, Høiby N, von Buchwald C. Colonisation and infection of the paranasal sinuses in cystic fibrosis patients is accompanied by a reduced PMN response. J Cyst Fibros 2012;11:525-531.