Association between baseline abundance of Peptoniphilus, a Gram-positive anaerobic coccus, and wound healing outcomes of DFUs
Autoři:
Kyung R. Min aff001; Adriana Galvis aff001; Katherine L. Baquerizo Nole aff001; Rohita Sinha aff002; Jennifer Clarke aff002; Robert S. Kirsner aff001; Dragana Ajdic aff001
Působiště autorů:
Dr. Phillip Frost Department of Dermatology & Cutaneous Surgery, University of Miami, Miller School of Medicine, Miami, Florida, United States of America
aff001; Department of Statistics, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America
aff002
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0227006
Souhrn
Diabetic foot ulcers (DFUs) lead to nearly 100,000 lower limb amputations annually in the United States. DFUs are colonized by complex microbial communities, and infection is one of the most common reasons for diabetes-related hospitalizations and amputations. In this study, we examined how DFU microbiomes respond to initial sharp debridement and offloading and how the initial composition associates with 4 week healing outcomes. We employed 16S rRNA next generation sequencing to perform microbial profiling on 50 samples collected from 10 patients with vascularized neuropathic DFUs. Debrided wound samples were obtained at initial visit and after one week from two DFU locations, wound bed and wound edge. Samples of the foot skin outside of the wounds were also collected for comparison. We showed that DFU wound beds are colonized by a greater number of distinct bacterial phylotypes compared to the wound edge or skin outside the wound. However, no significant microbiome diversity changes occurred at the wound sites after one week of standard care. Finally, increased initial abundance of Gram-positive anaerobic cocci (GPAC), especially Peptoniphilus (p < 0.05; n = 5 subjects), was associated with impaired healing; thus, GPAC’s abundance could be a predictor of the wound-healing outcome.
Klíčová slova:
Actinobacteria – Anaerobic bacteria – Bacteria – diabetes mellitus – Microbiome – Shannon index – Tissue repair – Ulcers
Zdroje
1. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27(5):1047–53. doi: 10.2337/diacare.27.5.1047 15111519
2. Rathmann W, Giani G. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27(10):2568–9; author reply 9. doi: 10.2337/diacare.27.10.2568 15451946
3. Roglic G, World Health Organization. Global report on diabetes. Geneva, Switzerland: World Health Organization; 2016. 86 pages p.
4. Lebrun E, Kirsner RS. Frequent debridement for healing of chronic wounds. JAMA Dermatol. 2013;149(9):1059. doi: 10.1001/jamadermatol.2013.4959 23884509
5. Lebrun E, Tomic-Canic M, Kirsner RS. The role of surgical debridement in healing of diabetic foot ulcers. Wound Repair Regen. 2010;18(5):433–8. doi: 10.1111/j.1524-475X.2010.00619.x 20840517
6. Gregg EW, Li Y, Wang J, Burrows NR, Ali MK, Rolka D, et al. Changes in diabetes-related complications in the United States, 1990–2010. N Engl J Med. 2014;370(16):1514–23. doi: 10.1056/NEJMoa1310799 24738668
7. Gregg EW, Williams DE, Geiss L. Changes in diabetes-related complications in the United States. N Engl J Med. 2014;371(3):286–7. doi: 10.1056/NEJMc1406009 25014698
8. Reiber GE, Boyko EJ, Smith DG. Lower extremity foot ulcers and amputations in diabetes. Diabetes in America. 1995;2:409–27.
9. Davies CE, Hill KE, Wilson MJ, Stephens P, Hill CM, Harding KG, et al. Use of 16S ribosomal DNA PCR and denaturing gradient gel electrophoresis for analysis of the microfloras of healing and nonhealing chronic venous leg ulcers. J Clin Microbiol. 2004;42(8):3549–57. doi: 10.1128/JCM.42.8.3549-3557.2004 15297496
10. Grice EA, Kong HH, Conlan S, Deming CB, Davis J, Young AC, et al. Topographical and temporal diversity of the human skin microbiome. Science. 2009;324(5931):1190–2. doi: 10.1126/science.1171700 19478181
11. Cho I, Blaser MJ. The human microbiome: at the interface of health and disease. Nat Rev Genet. 2012;13(4):260–70. doi: 10.1038/nrg3182 22411464
12. Gontcharova V, Youn E, Sun Y, Wolcott RD, Dowd SE. A comparison of bacterial composition in diabetic ulcers and contralateral intact skin. Open Microbiol J. 2010;4:8–19. doi: 10.2174/1874285801004010008 20461221
13. Price LB, Liu CM, Melendez JH, Frankel YM, Engelthaler D, Aziz M, et al. Community analysis of chronic wound bacteria using 16S rRNA gene-based pyrosequencing: impact of diabetes and antibiotics on chronic wound microbiota. PLoS One. 2009;4(7):e6462. doi: 10.1371/journal.pone.0006462 19649281
14. Gardner SE, Hillis SL, Heilmann K, Segre JA, Grice EA. The neuropathic diabetic foot ulcer microbiome is associated with clinical factors. Diabetes. 2013;62(3):923–30. doi: 10.2337/db12-0771 23139351
15. Wolcott RD, Hanson JD, Rees EJ, Koenig LD, Phillips CD, Wolcott RA, et al. Analysis of the chronic wound microbiota of 2,963 patients by 16S rDNA pyrosequencing. Wound Repair Regen. 2016;24(1):163–74. doi: 10.1111/wrr.12370 26463872
16. Loesche M, Gardner SE, Kalan L, Horwinski J, Zheng Q, Hodkinson BP, et al. Temporal Stability in Chronic Wound Microbiota Is Associated With Poor Healing. J Invest Dermatol. 2017;137(1):237–44. doi: 10.1016/j.jid.2016.08.009 27566400
17. Kalan LR, Meisel JS, Loesche MA, Horwinski J, Soaita I, Chen X, et al. Strain- and Species-Level Variation in the Microbiome of Diabetic Wounds Is Associated with Clinical Outcomes and Therapeutic Efficacy. Cell Host Microbe. 2019;25(5):641–55 e5. doi: 10.1016/j.chom.2019.03.006 31006638
18. Brem H, Sheehan P, Rosenberg HJ, Schneider JS, Boulton AJ. Evidence-based protocol for diabetic foot ulcers. Plast Reconstr Surg. 2006;117(7 Suppl):193S–209S; discussion 10S-11S. doi: 10.1097/01.prs.0000225459.93750.29 16799388
19. Cha J, Falanga V. Stem cells in cutaneous wound healing. Clin Dermatol. 2007;25(1):73–8. doi: 10.1016/j.clindermatol.2006.10.002 17276204
20. Veves A, Falanga V, Armstrong DG, Sabolinski ML, Apligraf Diabetic Foot Ulcer S. Graftskin, a human skin equivalent, is effective in the management of noninfected neuropathic diabetic foot ulcers: a prospective randomized multicenter clinical trial. Diabetes Care. 2001;24(2):290–5. doi: 10.2337/diacare.24.2.290 11213881
21. Gardner SE, Haleem A, Jao YL, Hillis SL, Femino JE, Phisitkul P, et al. Cultures of diabetic foot ulcers without clinical signs of infection do not predict outcomes. Diabetes Care. 2014;37(10):2693–701. doi: 10.2337/dc14-0051 25011945
22. Gardner SE, Hillis SL, Frantz RA. Clinical signs of infection in diabetic foot ulcers with high microbial load. Biol Res Nurs. 2009;11(2):119–28. doi: 10.1177/1099800408326169 19147524
23. Edmonds M, Foster A. The use of antibiotics in the diabetic foot. Am J Surg. 2004;187(5A):25S–8S. doi: 10.1016/S0002-9610(03)00300-3 15147988
24. Gordon KA, Lebrun EA, Tomic-Canic M, Kirsner RS. The role of surgical debridement in healing of diabetic foot ulcers. Skinmed. 2012;10(1):24–6. 22324173
25. Cardinal M, Eisenbud DE, Armstrong DG, Zelen C, Driver V, Attinger C, et al. Serial surgical debridement: a retrospective study on clinical outcomes in chronic lower extremity wounds. Wound Repair Regen. 2009;17(3):306–11. doi: 10.1111/j.1524-475X.2009.00485.x 19660037
26. Sloan TJ, Turton JC, Tyson J, Musgrove A, Fleming VM, Lister MM, et al. Examining diabetic heel ulcers through an ecological lens: microbial community dynamics associated with healing and infection. J Med Microbiol. 2019;68(2):230–40. doi: 10.1099/jmm.0.000907 30624175
27. Tipton CD, Mathew ME, Wolcott RA, Wolcott RD, Kingston T, Phillips CD. Temporal dynamics of relative abundances and bacterial succession in chronic wound communities. Wound Repair Regen. 2017;25(4):673–9. doi: 10.1111/wrr.12555 28597990
28. Goldstein DE, Little RR, Lorenz RA, Malone JI, Nathan DM, Peterson CM, et al. Tests of glycemia in diabetes. Diabetes Care. 2003;26 Suppl 1:S106–8.
29. Nathan DM, Kuenen J, Borg R, Zheng H, Schoenfeld D, Heine RJ, et al. Translating the A1C assay into estimated average glucose values. Diabetes Care. 2008;31(8):1473–8. doi: 10.2337/dc08-0545 18540046
30. Kurd SK, Hoffstad OJ, Bilker WB, Margolis DJ. Evaluation of the use of prognostic information for the care of individuals with venous leg ulcers or diabetic neuropathic foot ulcers. Wound Repair Regen. 2009;17(3):318–25. doi: 10.1111/j.1524-475X.2009.00487.x 19660039
31. Margolis DJ, Gelfand JM, Hoffstad O, Berlin JA. Surrogate end points for the treatment of diabetic neuropathic foot ulcers. Diabetes Care. 2003;26(6):1696–700. doi: 10.2337/diacare.26.6.1696 12766096
32. Gardner SE, Frantz RA, Saltzman CL, Hillis SL, Park H, Scherubel M. Diagnostic validity of three swab techniques for identifying chronic wound infection. Wound Repair Regen. 2006;14(5):548–57. doi: 10.1111/j.1743-6109.2006.00162.x 17014666
33. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods. 2013;10(10):996–8. doi: 10.1038/nmeth.2604 23955772
34. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012;6(3):610–8. doi: 10.1038/ismej.2011.139 22134646
35. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2017.
36. Jari Oksanen FGB, Michael Friendly, Roeland Kindt, Pierre Legendre, Dan McGlinn, Peter R. Minchin, et al. vegan: Community Ecology Package. R package version 2.4–2 ed2017.
37. Mandal S, Van Treuren W, White RA, Eggesbo M, Knight R, Peddada SD. Analysis of composition of microbiomes: a novel method for studying microbial composition. Microb Ecol Health Dis. 2015;26:27663. 26028277
38. Kelly BJ, Gross R, Bittinger K, Sherrill-Mix S, Lewis JD, Collman RG, et al. Power and sample-size estimation for microbiome studies using pairwise distances and PERMANOVA. Bioinformatics. 2015;31(15):2461–8. doi: 10.1093/bioinformatics/btv183 25819674
39. Shade A, Handelsman J. Beyond the Venn diagram: the hunt for a core microbiome. Environ Microbiol. 2012;14(1):4–12. doi: 10.1111/j.1462-2920.2011.02585.x 22004523
40. Price LB, Liu CM, Frankel YM, Melendez JH, Aziz M, Buchhagen J, et al. Macroscale spatial variation in chronic wound microbiota: a cross-sectional study. Wound Repair Regen. 2011;19(1):80–8. 20946140
41. Frick IM, Karlsson C, Morgelin M, Olin AI, Janjusevic R, Hammarstrom C, et al. Identification of a novel protein promoting the colonization and survival of Finegoldia magna, a bacterial commensal and opportunistic pathogen. Mol Microbiol. 2008;70(3):695–708. doi: 10.1111/j.1365-2958.2008.06439.x 18808384
42. Funke G, Hutson RA, Bernard KA, Pfyffer GE, Wauters G, Collins MD. Isolation of Arthrobacter spp. from clinical specimens and description of Arthrobacter cumminsii sp. nov. and Arthrobacter woluwensis sp. nov. J Clin Microbiol. 1996;34(10):2356–63. 8880479
43. Funke G, Pagano-Niederer M, Sjoden B, Falsen E. Characteristics of Arthrobacter cumminsii, the most frequently encountered Arthrobacter species in human clinical specimens. J Clin Microbiol. 1998;36(6):1539–43. 9620373
44. Citron DM, Goldstein EJ, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol. 2007;45(9):2819–28. doi: 10.1128/JCM.00551-07 17609322
45. Dowd SE, Wolcott RD, Sun Y, McKeehan T, Smith E, Rhoads D. Polymicrobial nature of chronic diabetic foot ulcer biofilm infections determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One. 2008;3(10):e3326. doi: 10.1371/journal.pone.0003326 18833331
46. Mendes JJ, Marques-Costa A, Vilela C, Neves J, Candeias N, Cavaco-Silva P, et al. Clinical and bacteriological survey of diabetic foot infections in Lisbon. Diabetes Res Clin Pract. 2012;95(1):153–61. doi: 10.1016/j.diabres.2011.10.001 22019426
47. Malone M, Johani K, Jensen SO, Gosbell IB, Dickson HG, Hu H, et al. Next Generation DNA Sequencing of Tissues from Infected Diabetic Foot Ulcers. EBioMedicine. 2017.
48. Meisel JS, Hannigan GD, Tyldsley AS, SanMiguel AJ, Hodkinson BP, Zheng Q, et al. Skin Microbiome Surveys Are Strongly Influenced by Experimental Design. J Invest Dermatol. 2016;136(5):947–56. doi: 10.1016/j.jid.2016.01.016 26829039
49. Nelson MC, Morrison HG, Benjamino J, Grim SL, Graf J. Analysis, optimization and verification of Illumina-generated 16S rRNA gene amplicon surveys. PLoS One. 2014;9(4):e94249. doi: 10.1371/journal.pone.0094249 24722003
50. Funke G, von Graevenitz A, Clarridge JE 3rd, Bernard KA. Clinical microbiology of coryneform bacteria. Clin Microbiol Rev. 1997;10(1):125–59. 8993861
51. Pitcher DG, Malnick H. Identification of Brevibacterium from clinical sources. J Clin Pathol. 1984;37(12):1395–8. doi: 10.1136/jcp.37.12.1395 6392351
52. Rossau R, Kersters K, Falsen E, Jantzen E, Segers P, Union A, et al. Oligella, a New Genus Including Oligella-Urethralis Comb-Nov (Formerly Moraxella-Urethralis) and Oligella-Ureolytica Sp-Nov (Formerly Cdc Group Ive)—Relationship to Taylorella-Equigenitalis and Related Taxa. International Journal of Systematic Bacteriology. 1987;37(3):198–210.
53. Tena D, Fernandez C, Lago MR. Alcaligenes faecalis: an unusual cause of skin and soft tissue infection. Jpn J Infect Dis. 2015;68(2):128–30. doi: 10.7883/yoken.JJID.2014.164 25420652
54. Charles PG, Uckay I, Kressmann B, Emonet S, Lipsky BA. The role of anaerobes in diabetic foot infections. Anaerobe. 2015;34:8–13. doi: 10.1016/j.anaerobe.2015.03.009 25841893
55. Choi Y, Banerjee A, McNish S, Couch KS, Torralba MG, Lucas S, et al. Co-occurrence of Anaerobes in Human Chronic Wounds. Microb Ecol. 2019;77(3):808–20. doi: 10.1007/s00248-018-1231-z 30141127
56. Murphy EC, Frick IM. Gram-positive anaerobic cocci—commensals and opportunistic pathogens. FEMS Microbiol Rev. 2013;37(4):520–53. doi: 10.1111/1574-6976.12005 23030831
Článek vyšel v časopise
PLOS One
2020 Číslo 1
- Může hubnutí souviset s vyšším rizikem nádorových onemocnění?
- Polibek, který mi „vzal nohy“ aneb vzácný výskyt EBV u 70leté ženy – kazuistika
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
Nejčtenější v tomto čísle
- Severity of misophonia symptoms is associated with worse cognitive control when exposed to misophonia trigger sounds
- Chemical analysis of snus products from the United States and northern Europe
- Calcium dobesilate reduces VEGF signaling by interfering with heparan sulfate binding site and protects from vascular complications in diabetic mice
- Effect of Lactobacillus acidophilus D2/CSL (CECT 4529) supplementation in drinking water on chicken crop and caeca microbiome
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy