Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 864

The DOI matches its Crossref record; 18 of the 18 references it cites were found in a registry or an index.

The wound microbiota: microbial mechanisms of impaired wound healing and infection

Uberoi, Aayushi, McCready-Vangi, Amelia, Grice, Elizabeth A.·2024·Nature Reviews Microbiology
DOI 10.1038/s41579-024-01035-z
Open this paper in CoChat — free account

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41579-024-01035-z

Cites

18 of 18 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 18 references

Research works printed but not linked: 173

  1. Shah, J. B. The history of wound care. J. Am. Col. Certif. Wound Spec. 3, 65–66 (2011).
  2. Broughton, G. II, Janis, J. E. & Attinger, C. E. A brief history of wound care. Plast. Reconstr. Surg. 117, 6S–11S (2006). · DOI · Paper page
  3. Sen, C. K. Human wounds and its burden: an updated compendium of estimates. Adv. Wound Care 8, 39–48 (2019). A comprehensive, regularly updated analysis of the economic and health burden of human wounds. · DOI · Paper page
  4. Nussbaum, S. R. et al. An economic evaluation of the impact, cost, and medicare policy implications of chronic nonhealing wounds. Value Health 21, 27–32 (2018). · DOI · Paper page
  5. Wang, G. et al. Bacteria induce skin regeneration via IL-1β signaling. Cell Host Microbe 29, 777–791.e6 (2021). Murine and human studies demonstrate the regenerative role of the microbiota. · DOI
  6. Uberoi, A. et al. Commensal microbiota regulates skin barrier function and repair via signaling through the aryl hydrocarbon receptor. Cell Host Microbe 29, 1235–1248.e8 (2021). · DOI · Paper page
  7. Flowers, L. & Grice, E. A. The skin microbiota: balancing risk and reward. Cell Host Microbe 28, 190–200 (2020). · DOI · Paper page
  8. Gardner, S. E. & Frantz, R. A. Wound bioburden and infection-related complications in diabetic foot ulcers. Biol. Res. Nurs. 10, 44–53 (2008). · DOI
  9. Swanson, T. et al. IWII Wound Infection in Clinical Practice consensus document: 2022 update. J. Wound Care 31, S10–S21 (2022). · DOI · Paper page
  10. Bowler, P. G., Duerden, B. I. & Armstrong, D. G. Wound microbiology and associated approaches to wound management. Clin. Microbiol. Rev. 14, 244–269 (2001). · DOI · Paper page
  11. Bartow-McKenney, C. et al. The microbiota of traumatic, open fracture wounds is associated with mechanism of injury. Wound Repair Regen. 26, 127–135 (2018). · DOI
  12. Fukuta, Y., Chua, H., Phe, K., Poythress, E. L. & Brown, C. A. Infectious diseases management in wound care settings: common causative organisms and frequently prescribed antibiotics. Adv. Skin Wound Care 35, 535–543 (2022). · DOI
  13. Gardner, S. E., Frantz, R. A. & Doebbeling, B. N. The validity of the clinical signs and symptoms used to identify localized chronic wound infection. Wound Repair Regen. 9, 178–186 (2001). · DOI · Paper page
  14. Cheong, J. Z. A. et al. Priority effects dictate community structure and alter virulence of fungal-bacterial biofilms. ISME J. 15, 2012–2027 (2021). · DOI
  15. Quinn, R. A. et al. Niche partitioning of a pathogenic microbiome driven by chemical gradients. Sci. Adv. 4, eaau1908 (2018). · DOI
  16. Walter, J., Maldonado-Gomez, M. X. & Martinez, I. To engraft or not to engraft: an ecological framework for gut microbiome modulation with live microbes. Curr. Opin. Biotechnol. 49, 129–139 (2018). · DOI · Paper page
  17. Mallon, C. A., Elsas, J. D. V. & Salles, J. F. Microbial invasions: the process, patterns, and mechanisms. Trends Microbiol. 23, 719–729 (2015). · DOI · Paper page
  18. Harris-Tryon, T. A. & Grice, E. A. Microbiota and maintenance of skin barrier function. Science 376, 940–945 (2022). · DOI · Paper page
  19. Cheung, G. Y. C., Bae, J. S. & Otto, M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 12, 547–569 (2021). · DOI · Paper page
  20. Parlet, C. P., Brown, M. M. & Horswill, A. R. Commensal staphylococci influence Staphylococcus aureus skin colonization and disease. Trends Microbiol. 27, 497–507 (2019). · DOI · Paper page
  21. Ding, X. et al. Challenges and innovation in treating chronic and acute wound infections: from basic science to clinical practice. Burns Trauma 10, tkac014 (2022). · DOI · Paper page
  22. Rahim, K. et al. Bacterial contribution in chronicity of wounds. Microb. Ecol. 73, 710–721 (2016). · DOI · Paper page
  23. Romano-Bertrand, S. et al. Dynamics of the surgical microbiota along the cardiothoracic surgery pathway. Front. Microbiol. 5, 787 (2014).
  24. Holder-Murray, J. et al. Time-dependent displacement of commensal skin microbes by pathogens at the site of colorectal surgery. Clin. Infect. Dis. 73, e2754–e2762 (2021). · DOI
  25. Gupta, S. et al. Cutaneous surgical wounds have distinct microbiomes from intact skin. Microbiol. Spectr. 11, e0330022 (2023). · DOI
  26. Wolcott, R. D. et al. Analysis of the chronic wound microbiota of 2,963 patients by 16S rDNA pyrosequencing. Wound Repair Regen. 24, 163–174 (2016). One of the largest studies to date profiling the microbiota of chronic wounds using molecular approaches. · DOI · Paper page
  27. Loesche, M. et al. Temporal stability in chronic wound microbiota is associated with poor healing. J. Invest. Dermatol. 137, 237–244 (2017). · DOI · Paper page
  28. Tipton, C. D. et al. Temporal dynamics of relative abundances and bacterial succession in chronic wound communities. Wound Repair Regen. 25, 673–679 (2017). · DOI
  29. Kalan, L. R. et al. Strain- and species-level variation in the microbiome of diabetic wounds is associated with clinical outcomes and therapeutic efficacy. Cell Host Microbe 25, 641–655.e5 (2019). Shotgun metagenomic study of diabetic foot ulcers identifies microbial features associated with healing outcomes, including strain-level diversity. · DOI · Paper page
  30. Sloan, T. J. et al. Examining diabetic heel ulcers through an ecological lens: microbial community dynamics associated with healing and infection. J. Med. Microbiol. 68, 230–240 (2019). · DOI
  31. Min, K. R. et al. Association between baseline abundance of Peptoniphilus, a Gram-positive anaerobic coccus, and wound healing outcomes of DFUs. PLoS ONE 15, e0227006 (2020). · DOI
  32. Verbanic, S., Shen, Y., Lee, J., Deacon, J. M. & Chen, I. A. Microbial predictors of healing and short-term effect of debridement on the microbiome of chronic wounds. NPJ Biofilms Microbiomes 6, 21 (2020). · DOI
  33. Citron, D. M., Goldstein, E. J., Merriam, C. V., Lipsky, B. A. & Abramson, M. A. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J. Clin. Microbiol. 45, 2819–2828 (2007). · DOI · Paper page
  34. Malone, M. et al. Next generation DNA sequencing of tissues from infected diabetic foot ulcers. EBioMedicine 21, 142–149 (2017). · DOI
  35. Dunyach-Remy, C. et al. Pressure ulcers microbiota dynamics and wound evolution. Sci. Rep. 11, 18506 (2021). · DOI
  36. Hannigan, G. D. et al. The human skin double-stranded DNA virome: topographical and temporal diversity, genetic enrichment, and dynamic associations with the host microbiome. mBio 6, e01578-15 (2015). · DOI · Paper page
  37. Verbanic, S., Deacon, J. M. & Chen, I. A. The chronic wound phageome: phage diversity and associations with wounds and healing outcomes. Microbiol. Spectr. 10, e0277721 (2022). · DOI
  38. Chellan, G. et al. Spectrum and prevalence of fungi infecting deep tissues of lower-limb wounds in patients with type 2 diabetes. J. Clin. Microbiol. 48, 2097–2102 (2010). · DOI
  39. Kalan, L. et al. Redefining the chronic-wound microbiome: fungal communities are prevalent, dynamic, and associated with delayed healing. mBio 7, e01058-16 (2016). · DOI · Paper page
  40. Barratt, J. L., Harkness, J., Marriott, D., Ellis, J. T. & Stark, D. Importance of nonenteric protozoan infections in immunocompromised people. Clin. Microbiol. Rev. 23, 795–836 (2010). · DOI
  41. Olaniyi, R., Pozzi, C., Grimaldi, L. & Bagnoli, F. Staphylococcus aureus-associated skin and soft tissue infections: anatomical localization, epidemiology, therapy and potential prophylaxis. Curr. Top. Microbiol. Immunol. 409, 199–227 (2017).
  42. Byrd, A. L. et al. Staphylococcus aureus and Staphylococcus epidermidis strain diversity underlying pediatric atopic dermatitis. Sci. Transl. Med. 9, eaal4651 (2017). · DOI · Paper page
  43. Foster, T. J., Geoghegan, J. A., Ganesh, V. K. & Hook, M. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat. Rev. Microbiol. 12, 49–62 (2014). · DOI · Paper page
  44. Foster, T. J. & Hook, M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol. 6, 484–488 (1998). · DOI · Paper page
  45. Thammavongsa, V., Kim, H. K., Missiakas, D. & Schneewind, O. Staphylococcal manipulation of host immune responses. Nat. Rev. Microbiol. 13, 529–543 (2015). · DOI · Paper page
  46. Falahee, P. C. et al. α-Toxin regulates local granulocyte expansion from hematopoietic stem and progenitor cells in Staphylococcus aureus-infected wounds. J. Immunol. 199, 1772–1782 (2017). · DOI
  47. Nakagawa, S. et al. Staphylococcus aureus virulent PSMα peptides induce keratinocyte alarmin release to orchestrate IL-17-dependent skin inflammation. Cell Host Microbe 22, 667–677.e5 (2017). · DOI · Paper page
  48. Sotto, A. et al. Virulence potential of Staphylococcus aureus strains isolated from diabetic foot ulcers a new paradigm. Diabetes Care 31, 2318–2324 (2008). · DOI
  49. Novick, R. P. et al. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J. 12, 3967–3975 (1993). · DOI · Paper page
  50. Morfeldt, E., Taylor, D., Vongabain, A. & Arvidson, S. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J. 14, 4569–4577 (1995). · DOI · Paper page
  51. Cheung, A. L., Koomey, J. M., Butler, C. A., Projan, S. J. & Fischetti, V. A. Regulation of exoprotein expression in Staphylococcus aureus by a locus (sar) distinct from agr. Proc. Natl Acad. Sci. USA 89, 6462–6466 (1992). · DOI · Paper page
  52. Cheung, A. L. et al. Diminished virulence of a sar–/agr– mutant of Staphylococcus aureus in the rabbit model of endocarditis. J. Clin. Invest. 94, 1815–1822 (1994). · DOI · Paper page
  53. Suligoy, C. M. et al. Mutation of Agr is associated with the adaptation of Staphylococcus aureus to the host during chronic osteomyelitis. Front. Cell. Infect. Microbiol. 8, 18 (2018). · DOI
  54. Bischoff, M. et al. Microarray-based analysis of the Staphylococcus aureus σB regulon. J. Bacteriol. 186, 4085–4099 (2004). · DOI · Paper page
  55. Bischoff, M., Entenza, J. M. & Giachino, P. Influence of a functional sigB operon on the global regulators sar and agr in Staphylococcus aureus. J. Bacteriol. 183, 5171–5179 (2001). · DOI · Paper page
  56. Tuchscherr, L. et al. Sigma factor SigB is crucial to mediate Staphylococcus aureus adaptation during chronic infections. PLoS Pathog. 11, e1004870 (2015). · DOI
  57. Jacquet, R. et al. Dual gene expression analysis identifies factors associated with Staphylococcus aureus virulence in diabetic mice. Infect. Immun. 87, e00163-19 (2019). · DOI
  58. Frees, D., Gerth, U. & Ingmer, H. Clp chaperones and proteases are central in stress survival, virulence and antibiotic resistance of Staphylococcus aureus. Int. J. Med. Microbiol. 304, 142–149 (2014). · DOI · Paper page
  59. Klopsfenstein, N., Hibbs, K., Blackman, A. & Serezani, C. H. Prostaglandin E2 production is required for phagocyte CXCR2-mediated skin host defense in obese and hyperglycemic mice. Preprint at bioRxiv https://doi.org/10.1101/2022.10.02.510554 (2022). · DOI
  60. Vitko, N. P., Grosser, M. R., Khatri, D., Lance, T. R. & Richardson, A. R. Expanded glucose import capability affords Staphylococcus aureus optimized glycolytic flux during infection. mBio 7, e00296-16 (2016). · DOI · Paper page
  61. de Oliveira, J. M. F. & Lisboa, L. D. Hospital-acquired infections due to Gram-negative bacteria. N. Engl. J. Med. 363, 1482–1483 (2010). · DOI
  62. Kirketerp-Moller, K. et al. Distribution, organization, and ecology of bacteria in chronic wounds. J. Clin. Microbiol. 46, 2717–2722 (2008). · DOI · Paper page
  63. Malone, M. et al. The prevalence of biofilms in chronic wounds: a systematic review and meta-analysis of published data. J. Wound Care 26, 20–25 (2017). · DOI · Paper page
  64. Zhao, G. et al. Delayed wound healing in diabetic (db/db) mice with Pseudomonas aeruginosa biofilm challenge: a model for the study of chronic wounds. Wound Repair Regen. 18, 467–477 (2010). · DOI · Paper page
  65. Gloag, E. S. et al. Pseudomonas aeruginosa interstrain dynamics and selection of hyperbiofilm mutants during a chronic infection. mBio 10, e01698-19 (2019). · DOI
  66. Morgan, S. J. et al. Bacterial fitness in chronic wounds appears to be mediated by the capacity for high-density growth, not virulence or biofilm functions. PLoS Pathog. 15, e1007511 (2019). · DOI
  67. Goldufsky, J. et al. Pseudomonas aeruginosa uses T3SS to inhibit diabetic wound healing. Wound Repair Regen. 23, 557–564 (2015). · DOI
  68. Turner, K. H., Everett, J., Trivedi, U., Rumbaugh, K. P. & Whiteley, M. Requirements for Pseudomonas aeruginosa acute burn and chronic surgical wound infection. PLoS Genet. 10, e1004518 (2014). This study uses murine models and transposon sequencing to discern the genetic requirements of acute and chronic wound fitness and virulence of P. aeruginosa. · DOI · Paper page
  69. Everett, J. et al. Arginine is a critical substrate for the pathogenesis of Pseudomonas aeruginosa in burn wound infections. mBio 8, e02160-16 (2017). · DOI
  70. Radzieta, M. et al. A multiomics approach to identify host-microbe alterations associated with infection severity in diabetic foot infections: a pilot study. NPJ Biofilms Microbiomes 7, 29 (2021). · DOI
  71. Roberts, S., Scott, J. R., Husmann, L. K. & Zurawski, C. A. Murine models of Streptococcus pyogenes infection.Curr. Protoc. Microbiol. https://doi.org/10.1002/9780471729259.mc09d05s02 (2006). · doi:10.1002/9780471729259.mc09d05s02
  72. Currie, B. J. Group A streptococcal infections of the skin: molecular advances but limited therapeutic progress. Curr. Opin. Infect. Dis. 19, 132–138 (2006). · DOI
  73. Siemens, N., Patenge, N., Otto, J., Fiedler, T. & Kreikemeyer, B. Streptococcus pyogenes M49 plasminogen/plasmin binding facilitates keratinocyte invasion via integrin-integrin-linked kinase (ILK) pathways and protects from macrophage killing. J. Biol. Chem. 286, 21612–21622 (2011). · DOI
  74. Ringdahl, U. et al. Molecular co-operation between protein PAM and streptokinase for plasmin acquisition by Streptococcus pyogenes. J. Biol. Chem. 273, 6424–6430 (1998). · DOI
  75. Vu, H. M. et al. Group A Streptococcus-induced activation of human plasminogen is required for keratinocyte wound retraction and rapid clot dissolution. Front. Cardiovasc. Med. 8, 667554 (2021). · DOI
  76. Towers, R. J. et al. Fibronectin-binding protein gene recombination and horizontal transfer between group A and G streptococci. J. Clin. Microbiol. 42, 5357–5361 (2004). · doi:10.1128/jcm.42.11.5357-5361.2004
  77. Mazade, M. A. & Edwards, M. S. Impairment of type III group B Streptococcus-stimulated superoxide production and opsonophagocytosis by neutrophils in diabetes. Mol. Genet. Metab. 73, 259–267 (2001). · DOI
  78. Di Palo, B. et al. Adaptive response of Group B Streptococcus to high glucose conditions: new insights on the CovRS regulation network. PLoS ONE 8, e61294 (2013). · DOI
  79. Keogh, R. A. et al. Group B Streptococcus adaptation promotes survival in a hyperinflammatory diabetic wound environment. Sci. Adv. 8, eadd3221 (2022). Dual-RNA sequencing approach to identify mechanisms of GBS pathogenesis in diabetic wound healing. · DOI
  80. Macdonald, K. E., Boeckh, S., Stacey, H. J. & Jones, J. D. The microbiology of diabetic foot infections: a meta-analysis. BMC Infect. Dis. 21, 770 (2021). · doi:10.1186/s12879-021-06516-7
  81. Dowd, S. E. et al. Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol. 8, 43 (2008). · DOI · Paper page
  82. Frick, I. M. et al. Identification of a novel protein promoting the colonization and survival of Finegoldia magna, a bacterial commensal and opportunistic pathogen. Mol. Microbiol. 70, 695–708 (2008). · DOI
  83. Karlsson, C. et al. SufA — a novel subtilisin-like serine proteinase of Finegoldia magna. Microbiology 153, 4208–4218 (2007). · DOI
  84. Karlsson, C. et al. SufA — a bacterial enzyme that cleaves fibrinogen and blocks fibrin network formation. Microbiology 155, 238–248 (2009). · DOI
  85. Karlsson, C. et al. SufA of the opportunistic pathogen Finegoldia magna modulates actions of the antibacterial chemokine MIG/CXCL9, promoting bacterial survival during epithelial inflammation. J. Biol. Chem. 284, 29499–29508 (2009). · DOI
  86. Murphy, E. C. & Frick, I. M. Gram-positive anaerobic cocci — commensals and opportunistic pathogens. FEMS Microbiol. Rev. 37, 520–553 (2013). · DOI · Paper page
  87. Neumann, A., Bjorck, L. & Frick, I. M. Finegoldia magna, an anaerobic Gram-positive bacterium of the normal human microbiota, induces inflammation by activating neutrophils. Front. Microbiol. 11, 65 (2020). · DOI
  88. Bjorck, L. Protein L. A novel bacterial cell wall protein with affinity for Ig L chains. J. Immunol. 140, 1194–1197 (1988). · DOI · Paper page
  89. de Chateau, M., Holst, E. & Bjorck, L. Protein PAB, an albumin-binding bacterial surface protein promoting growth and virulence. J. Biol. Chem. 271, 26609–26615 (1996). · DOI
  90. Nagy, E., Urbán, E. & Nord, C. E. Antimicrobial susceptibility of Bacteroides fragilis group isolates in Europe. Clin. Microbiol. Infect. 9, 475–488 (2003). · DOI
  91. Yekani, M. et al. Carbapenem resistance in Bacteroides fragilis: a review of molecular mechanisms. Anaerobe 76, 102606 (2022). · doi:10.1016/j.anaerobe.2022.102606
  92. Oyston, P. C. & Handley, P. S. Surface components of Bacteroides fragilis involved in adhesion and haemagglutination. J. Med. Microbiol. 34, 51–55 (1991). · doi:10.1099/00222615-34-1-51
  93. Wu, S., Lim, K. C., Huang, J., Saidi, R. F. & Sears, C. L. Bacteroides fragilis enterotoxin cleaves the zonula adherens protein, E-cadherin. Proc. Natl Acad. Sci. USA 95, 14979–14984 (1998). · DOI · Paper page
  94. Kaya, D., Aldirmaz Agartan, C. & Yucel, M. Fungal agents as a cause of surgical wound infections: an overview of host factors. Wounds 19, 218–222 (2007).
  95. Struck, M. F. & Gille, J. Fungal infections in burns: a comprehensive review. Ann. Burns Fire Disasters 26, 147–153 (2013).
  96. Gil, J., Solis, M., Higa, A. & Davis, S. C. Candida albicans infections: a novel porcine wound model to evaluate treatment efficacy. BMC Microbiol. 22, 45 (2022). · DOI
  97. von Muller, C. et al. Active neutrophil responses counteract Candida albicans burn wound infection of ex vivo human skin explants. Sci. Rep. 10, 21818 (2020). · DOI
  98. Alby, K. & Bennett, R. J. Stress-induced phenotypic switching in Candida albicans. Mol. Biol. Cell 20, 3178–3191 (2009). · DOI
  99. Schonherr, F. A. et al. The intraspecies diversity of C. albicans triggers qualitatively and temporally distinct host responses that determine the balance between commensalism and pathogenicity. Mucosal. Immunol. 10, 1335–1350 (2017). · DOI
  100. Pinto, A. M., Cerqueira, M. A., Banobre-Lopes, M., Pastrana, L. M. & Sillankorva, S. Bacteriophages for chronic wound treatment: from traditional to novel delivery systems. Viruses 12, 235 (2020). · DOI
  101. Secor, P. R. et al. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe 18, 549–559 (2015). · DOI · Paper page
  102. Rice, S. A. et al. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME J. 3, 271–282 (2009). · DOI · Paper page
  103. Sweere, J. M. et al. Bacteriophage trigger antiviral immunity and prevent clearance of bacterial infection. Science 363, eaat9691 (2019). Identification of phage-related mechanism that suppresses host immunity to P. aeruginosa infection. · DOI · Paper page
  104. Chong, K. K. L. et al. Enterococcus faecalis modulates immune activation and slows healing during wound infection. J. Infect. Dis. 216, 1644–1654 (2017). · DOI
  105. Orazi, G. & O’Toole, G. A. ‘It takes a village’: mechanisms underlying antimicrobial recalcitrance of polymicrobial biofilms. J. Bacteriol. 202, e00530-19 (2019). · DOI · Paper page
  106. Shumba, P., Mairpady Shambat, S. & Siemens, N. The role of streptococcal and staphylococcal exotoxins and proteases in human necrotizing soft tissue infections. Toxins 11, 332 (2019). · DOI
  107. Ovington, L. Bacterial toxins and wound healing. Ostomy Wound Manag. 49, 8–12 (2003).
  108. Caley, M. P., Martins, V. L. & O’Toole, E. A. Metalloproteinases and wound healing. Adv. Wound Care 4, 225–234 (2015). · DOI · Paper page
  109. Rippon, M. G., Westgate, S. & Rogers, A. A. Implications of endotoxins in wound healing: a narrative review. J. Wound Care 31, 380–392 (2022). · DOI
  110. Alhede, M. et al. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155, 3500–3508 (2009). · DOI · Paper page
  111. Rooijakkers, S. H. M. et al. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 6, 920–927 (2005). · DOI · Paper page
  112. de Haas, C. J. C. et al. Chemotaxis inhibitory protein of Staphylococcus aureus, a bacterial antiinflammatory agent. J. Exp. Med. 199, 687–695 (2004). · DOI · Paper page
  113. Campbell, A. E. et al. Variable staphyloxanthin production by Staphylococcus aureus drives strain-dependent effects on diabetic wound-healing outcomes. Cell Rep. 42, 113281 (2023). This study links S. aureus strain-level variation in the diabetic foot ulcer microbiome to a specific mechanism that impairs wound healing. · DOI
  114. von Eiff, C. et al. Intracellular persistence of Staphylococcus aureus small-colony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with Darier’s disease. Clin. Infect. Dis. 32, 1643–1647 (2001). · DOI · Paper page
  115. Read, T. D. & Massey, R. C. Characterizing the genetic basis of bacterial phenotypes using genome-wide association studies: a new direction for bacteriology. Genome Med. 6, 109 (2014). · DOI
  116. Sela, U., Euler, C. W., Correa da Rosa, J. & Fischetti, V. A. Strains of bacterial species induce a greatly varied acute adaptive immune response: the contribution of the accessory genome. PLoS Pathog. 14, e1006726 (2018). · DOI
  117. Deitsch, K. W., Lukehart, S. A. & Stringer, J. R. Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat. Rev. Microbiol. 7, 493–503 (2009). · DOI · Paper page
  118. Burke, F. M., McCormack, N., Rindi, S., Speziale, P. & Foster, T. J. Fibronectin-binding protein B variation in Staphylococcus aureus. BMC Microbiol. 10, 160 (2010). · DOI
  119. McCarthy, A. J. & Lindsay, J. A. Genetic variation in Staphylococcus aureus surface and immune evasion genes is lineage associated: implications for vaccine design and host-pathogen interactions. BMC Microbiol. 10, 173 (2010). · DOI · Paper page
  120. Beyene, R. T., Derryberry, S. L. Jr & Barbul, A. The effect of comorbidities on wound healing. Surg. Clin. North Am. 100, 695–705 (2020). · DOI · Paper page
  121. Sirobhushanam, S. et al. Staphylococcus aureus colonization is increased on lupus skin lesions and is promoted by IFN-mediated barrier disruption. J. Invest. Dermatol. 140, 1066–1074.e4 (2020). · DOI
  122. Gould, L. et al. Chronic wound repair and healing in older adults: current status and future research. J. Am. Geriatr. Soc. 63, 427–438 (2015). · DOI · Paper page
  123. Tipton, C. D. et al. Patient genetics is linked to chronic wound microbiome composition and healing. PLoS Pathog. 16, e1008511 (2020). A microbiome genome-wide association study identifies patient genetic determinants of the wound microbiome and healing responses. · DOI
  124. Margolis, D. J. et al. NOS1AP genetic variation is associated with impaired healing of diabetic foot ulcers and diminished response to healing of circulating stem/progenitor cells. Wound Repair Regen. 25, 733–736 (2017). · doi:10.1111/wrr.12564
  125. Chaney, S. B. et al. Histopathological comparisons of Staphylococcus aureus and Pseudomonas aeruginosa experimental infected porcine burn wounds. Wound Repair Regen. 25, 541–549 (2017). · DOI
  126. Lasa, I. & Solano, C. Polymicrobial infections: do bacteria behave differently depending on their neighbours? Virulence 9, 895–897 (2018). · doi:10.1080/21505594.2018.1426520
  127. Tan, C. A. Z. et al. Enterococcus faecalis antagonizes Pseudomonas aeruginosa growth in mixed-species interactions. J. Bacteriol. 204, e0061521 (2022). · DOI
  128. Radlinski, L. et al. Pseudomonas aeruginosa exoproducts determine antibiotic efficacy against Staphylococcus aureus. PLoS Biol. 15, e2003981 (2017). · DOI · Paper page
  129. Wong, J. J. et al. Escherichia coli BarA-UvrY regulates the pks island and kills staphylococci via the genotoxin colibactin during interspecies competition. PLoS Pathog. 18, e1010766 (2022). · DOI
  130. Antonic, V., Stojadinovic, A., Zhang, B., Izadjoo, M. J. & Alavi, M. Pseudomonas aeruginosa induces pigment production and enhances virulence in a white phenotypic variant of Staphylococcus aureus. Infect. Drug Resist. 6, 175–186 (2013).
  131. Alves, P. M. et al. Interaction between Staphylococcus aureus and Pseudomonas aeruginosa is beneficial for colonisation and pathogenicity in a mixed biofilm. Pathog. Dis. 76, 10 (2018). · DOI · Paper page
  132. DeLeon, S. et al. Synergistic interactions of Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro wound model. Infect. Immun. 82, 4718–4728 (2014). · DOI · Paper page
  133. Phalak, P. & Henson, M. A. Metabolic modelling of chronic wound microbiota predicts mutualistic interactions that drive community composition. J. Appl. Microbiol. 127, 1576–1593 (2019). · DOI
  134. Garcia-Perez, A. N. et al. From the wound to the bench: exoproteome interplay between wound-colonizing Staphylococcus aureus strains and co-existing bacteria. Virulence 9, 363–378 (2018). · DOI
  135. Ch’ng, J. H. et al. Heme cross-feeding can augment Staphylococcus aureus and Enterococcus faecalis dual species biofilms. ISME J. 16, 2015–2026 (2022). · DOI
  136. Allison, D. L. et al. Candida-bacteria interactions: their impact on human disease. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.VMBF-0030-2016 (2016). · DOI
  137. Kong, E. F. et al. Commensal protection of Staphylococcus aureus against antimicrobials by Candida albicans biofilm matrix. mBio https://doi.org/10.1128/mbio.01365-16 (2016). · DOI · Paper page
  138. Townsend, E. M. et al. Development and characterisation of a novel three-dimensional inter-kingdom wound biofilm model. Biofouling 32, 1259–1270 (2016). · DOI
  139. Abt, M. C., McKenney, P. T. & Pamer, E. G. Clostridium difficile colitis: pathogenesis and host defence. Nat. Rev. Microbiol. 14, 609–620 (2016). · DOI · Paper page
  140. Lipsky, B. A. et al. Antimicrobial stewardship in wound care: a position paper from the British Society for Antimicrobial Chemotherapy and European Wound Management Association. J. Antimicrob. Chemother. 71, 3026–3035 (2016). · DOI
  141. Limbago, B. M. et al. Report of the 13th vancomycin-resistant Staphylococcus aureus isolate from the United States. J. Clin. Microbiol. 52, 998–1002 (2014). · DOI
  142. Pallavali, R. R., Degati, V. L., Lomada, D., Reddy, M. C. & Durbaka, V. R. P. Isolation and in vitro evaluation of bacteriophages against MDR-bacterial isolates from septic wound infections. PLoS ONE 12, e0179245 (2017). · doi:10.1371/journal.pone.0179245
  143. Seppala, H., Klaukka, T., Lehtonen, R., Nenonen, E. & Huovinen, P. Outpatient use of erythromycin: link to increased erythromycin resistance in group A streptococci. Clin. Infect. Dis. 21, 1378–1385 (1995). · DOI
  144. Hahn, W. O., Werth, B. J., Butler-Wu, S. M. & Rakita, R. M. Multidrug-resistant Corynebacterium striatum associated with increased use of parenteral antimicrobial drugs. Emerg. Infect. Dis. 22, 1908–1914 (2016). · DOI
  145. Rudresh, S. M. et al. Non diphtheritic Corynebacteria: an emerging nosocomial pathogen in skin and soft tissue infection. J. Clin. Diagn. Res. 9, DC19–DC21 (2015).
  146. Rashid, R. et al. Comprehensive analysis of phospholipids and glycolipids in the opportunistic pathogen Enterococcus faecalis. PLoS ONE 12, e0175886 (2017). · DOI
  147. Lam, S. J. et al. Combating multidrug-resistant Gram-negative bacteria with structurally nanoengineered antimicrobial peptide polymers. Nat. Microbiol. 1, 16162 (2016). · DOI · Paper page
  148. Mekkawy, A. I. et al. In vitro and in vivo evaluation of biologically synthesized silver nanoparticles for topical applications: effect of surface coating and loading into hydrogels. Int. J. Nanomed. 12, 759–777 (2017). · DOI · Paper page
  149. Frydman, G. H. et al. Manuka honey microneedles for enhanced wound healing and the prevention and/or treatment of Methicillin-resistant Staphylococcus aureus (MRSA) surgical site infection. Sci. Rep. 10, 13229 (2020). · DOI
  150. Kot, B., Sytykiewicz, H., Sprawka, I. & Witeska, M. Effect of manuka honey on biofilm-associated genes expression during methicillin-resistant Staphylococcus aureus biofilm formation. Sci. Rep. 10, 13552 (2020). · DOI
  151. Barros Almeida, I. et al. Smart dressings for wound healing: a review. Adv. Skin Wound Care 34, 1–8 (2021). · DOI
  152. White, E. K. et al. Wound microbiota-mediated correction of matrix metalloproteinase expression promotes re-epithelialization of diabetic wounds. Preprint at bioRxiv https://doi.org/10.1101/2023.06.30.547263 (2023). · DOI
  153. Monaco, J. L. & Lawrence, W. T. Acute wound healing. An overview. Clin. Plast. Surg. 30, 1–12 (2003). · DOI · Paper page
  154. Korting, H. C., Schollmann, C. & White, R. J. Management of minor acute cutaneous wounds: importance of wound healing in a moist environment. J. Eur. Acad. Dermatol. Venereol. 25, 130–137 (2011). · DOI
  155. Li, J., Chen, J. & Kirsner, R. Pathophysiology of acute wound healing. Clin. Dermatol. 25, 9–18 (2007). · DOI · Paper page
  156. Clark, R. A. F. in Principles of Tissue Engineering 4th Edn (eds Lanza, R., Langer, R. & Vacanti, J.) 1595–1617 (Academic Press, 2014). · DOI
  157. Cross, W. W. III & Swiontkowski, M. F. Treatment principles in the management of open fractures. Indian J. Orthop. 42, 377–386 (2008). · doi:10.4103/0019-5413.43373
  158. Frykberg, R. G. & Banks, J. Challenges in the treatment of chronic wounds. Adv. Wound Care 4, 560–582 (2015). · DOI · Paper page
  159. Rowan, M. P. et al. Burn wound healing and treatment: review and advancements. Crit. Care 19, 243 (2015). · DOI · Paper page
  160. Grey, J. E., Harding, K. G. & Enoch, S. Venous and arterial leg ulcers. BMJ 332, 347–350 (2006). · DOI
  161. Mervis, J. S. & Phillips, T. J. Pressure ulcers: pathophysiology, epidemiology, risk factors, and presentation. J. Am. Acad. Dermatol. 81, 881–890 (2019). · DOI · Paper page
  162. Gardner, S. E. et al. Diagnostic validity of three swab techniques for identifying chronic wound infection. Wound Repair Regen. 14, 548–557 (2006). · DOI
  163. Franklin, M. J., Chang, C., Akiyama, T. & Bothner, B. New technologies for studying biofilms. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.MB-0016-2014 (2015). · DOI · Paper page
  164. Valm, A. M., Mark Welch, J. L. & Borisy, G. G. CLASI-FISH: principles of combinatorial labeling and spectral imaging. Syst. Appl. Microbiol. 35, 496–502 (2012). · DOI
  165. Dar, D., Dar, N., Cai, L. & Newman, D. K. Spatial transcriptomics of planktonic and sessile bacterial populations at single-cell resolution. Science 373, eabi4882 (2021). A high-resolution transcriptome-imaging approach reveals dynamic and spatial metabolic heterogeneity of P. aeruginosa in planktonic and biofilm cultures. · DOI · Paper page
  166. Eriksson, E. et al. Chronic wounds: treatment consensus. Wound Repair Regen. 30, 156–171 (2022). · DOI · Paper page
  167. Schultz, G. et al. Consensus guidelines for the identification and treatment of biofilms in chronic nonhealing wounds. Wound Repair Regen. 25, 744–757 (2017). · DOI · Paper page
  168. Moya-Lopez, J., Costela-Ruiz, V., Garcia-Recio, E., Sherman, R. A. & De Luna-Bertos, E. Advantages of maggot debridement therapy for chronic wounds: a bibliographic review. Adv. Skin Wound Care 33, 515–525 (2020). · doi:10.1097/01.asw.0000695776.26946.68
  169. Sibbald, R. G. et al. Wound bed preparation 2021. Adv. Skin Wound Care 34, 183–195 (2021). · DOI · Paper page
  170. Gomez-Ochoa, S. A. et al. Efficacy of phage therapy in preclinical models of bacterial infection: a systematic review and meta-analysis. Lancet Microbe 3, e956–e968 (2022). · DOI
  171. Valente, L., Prazak, J., Que, Y. A. & Cameron, D. R. Progress and pitfalls of bacteriophage therapy in critical care: a concise definitive review. Crit. Care Explor. 3, e0351 (2021). · DOI
  172. Lenzmeier, T. D. et al. Application of Lactobacillus gasseri 63 AM supernatant to Pseudomonas aeruginosa-infected wounds prevents sepsis in murine models of thermal injury and dorsal excision. J. Med. Microbiol. 68, 1560–1572 (2019). · DOI
  173. Surmeli, M., Macin, S., Akyon, Y. & Kayikcioglu, A. U. The protective effect of Lactobacillus plantarum against meticillin-resistant Staphylococcus aureus infections: an experimental animal model. J. Wound Care 28, S29–S34 (2019). · DOI

Cited by

See all 864

Metadata

Authors
Uberoi, A., McCready-Vangi, A., & Grice, E. A.
Venue
Nature Reviews Microbiology
Publisher
Springer Science and Business Media LLC
Published
2024-04-04
Volume
22
Issue
8
Pages
507-521
ISSN
  • 1740-1526 (ISSN-L)
  • 1740-1534
DOI
10.1038/s41579-024-01035-z
OpenAlex
W4393930924
Cited by
864
References
18
FWCI
61.70
Type
journal article
Language
en
Open access
closed
Licence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: The wound microbiota: microbial mechanisms of impaired wound healing and infection. https://app.cochat.ai/papers/10.1038/s41579-024-01035-z
The paper
Uberoi, A., McCready-Vangi, A., & Grice, E. A. (2024). The wound microbiota: microbial mechanisms of impaired wound healing and infection. Nature Reviews Microbiology. https://doi.org/10.1038/s41579-024-01035-z

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.