Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin

ABSTRACT Infections are relatively rare following cutaneous surgical procedures, despite the potential for wound exposure to pathogens both during surgery and throughout the healing process. Although gut commensals are believed to reduce the risk of intestinal infections, an analogous role for skin...

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Main Authors: Sameer Gupta, Alexandra J. Poret, David Hashemi, Amarachi Eseonu, Sherry H. Yu, Jonathan D'Gama, Victor A. Neel, Tami D. Lieberman
Format: Article
Language:English
Published: American Society for Microbiology 2023-02-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.03300-22
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author Sameer Gupta
Alexandra J. Poret
David Hashemi
Amarachi Eseonu
Sherry H. Yu
Jonathan D'Gama
Victor A. Neel
Tami D. Lieberman
author_facet Sameer Gupta
Alexandra J. Poret
David Hashemi
Amarachi Eseonu
Sherry H. Yu
Jonathan D'Gama
Victor A. Neel
Tami D. Lieberman
author_sort Sameer Gupta
collection DOAJ
description ABSTRACT Infections are relatively rare following cutaneous surgical procedures, despite the potential for wound exposure to pathogens both during surgery and throughout the healing process. Although gut commensals are believed to reduce the risk of intestinal infections, an analogous role for skin commensals has not been described. In fact, the microbiome of normally healing surgical skin wounds has not yet been profiled using culture-independent techniques. We characterized the wound microbiome in 53 patients who underwent skin cancer surgery and healed without signs or symptoms of infection. A week after surgery, several bacterial species displayed significant differences in relative abundance when compared to control, nonoperated skin from the same patient. The relative abundance of the most common bacterium found on intact skin, Cutibacterium acnes, was reduced in wounds 5-fold. Staphylococcus aureus, a frequent cause of postoperative skin infections, was enriched 6.4-fold in clinically noninfected wounds, suggesting active suppression of pathogenicity. Finally, members of the Corynebacterium genus were the dominant organism in postoperative wounds, making up 37% of the average wound microbiome. The enrichment of these bacteria in normally healing wounds suggests that they might be capable of providing colonization resistance. Future studies focused on the biological and clinical significance of the wound microbiome may shed light on normal wound healing and potential therapeutic opportunities to mitigate infection risk. IMPORTANCE Commensal bacteria on skin may limit the ability of pathogenic bacteria to cause clinically significant infections. The bacteria on healing acute wounds, which might provide such a protective effect, have not been described using culture-independent approaches in the absence of antibiotics. We compare the microbiome of wounds a week after skin cancer removal surgery with intact skin from the same patient. We find that the potentially pathogenic species S. aureus is common on these healing wounds despite the absence of symptoms or signs of infection. We report that bacteria often considered as potential skin probiotics, including Staphylococcus epidermidis, do not reach high relative abundance in wound microbiomes. In contrast, specific members of the Corynebacterium genus, rarely associated with infections, were significantly enriched in healing wounds compared to intact skin. Future work is needed to see if Corynebacterium species or derivatives thereof could be employed to lower the risk of wound infection.
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spelling doaj.art-1fe5f458fbd6456e981ead9270d318272023-02-14T14:15:50ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.03300-22Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact SkinSameer Gupta0Alexandra J. Poret1David Hashemi2Amarachi Eseonu3Sherry H. Yu4Jonathan D'Gama5Victor A. Neel6Tami D. Lieberman7Department of Dermatology, MGH, Boston, Massachusetts, USAInstitute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USADepartment of Dermatology, MGH, Boston, Massachusetts, USADepartment of Dermatology, MGH, Boston, Massachusetts, USADepartment of Dermatology, MGH, Boston, Massachusetts, USADepartment of Dermatology, MGH, Boston, Massachusetts, USADepartment of Dermatology, MGH, Boston, Massachusetts, USAInstitute for Medical Engineering and Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USAABSTRACT Infections are relatively rare following cutaneous surgical procedures, despite the potential for wound exposure to pathogens both during surgery and throughout the healing process. Although gut commensals are believed to reduce the risk of intestinal infections, an analogous role for skin commensals has not been described. In fact, the microbiome of normally healing surgical skin wounds has not yet been profiled using culture-independent techniques. We characterized the wound microbiome in 53 patients who underwent skin cancer surgery and healed without signs or symptoms of infection. A week after surgery, several bacterial species displayed significant differences in relative abundance when compared to control, nonoperated skin from the same patient. The relative abundance of the most common bacterium found on intact skin, Cutibacterium acnes, was reduced in wounds 5-fold. Staphylococcus aureus, a frequent cause of postoperative skin infections, was enriched 6.4-fold in clinically noninfected wounds, suggesting active suppression of pathogenicity. Finally, members of the Corynebacterium genus were the dominant organism in postoperative wounds, making up 37% of the average wound microbiome. The enrichment of these bacteria in normally healing wounds suggests that they might be capable of providing colonization resistance. Future studies focused on the biological and clinical significance of the wound microbiome may shed light on normal wound healing and potential therapeutic opportunities to mitigate infection risk. IMPORTANCE Commensal bacteria on skin may limit the ability of pathogenic bacteria to cause clinically significant infections. The bacteria on healing acute wounds, which might provide such a protective effect, have not been described using culture-independent approaches in the absence of antibiotics. We compare the microbiome of wounds a week after skin cancer removal surgery with intact skin from the same patient. We find that the potentially pathogenic species S. aureus is common on these healing wounds despite the absence of symptoms or signs of infection. We report that bacteria often considered as potential skin probiotics, including Staphylococcus epidermidis, do not reach high relative abundance in wound microbiomes. In contrast, specific members of the Corynebacterium genus, rarely associated with infections, were significantly enriched in healing wounds compared to intact skin. Future work is needed to see if Corynebacterium species or derivatives thereof could be employed to lower the risk of wound infection.https://journals.asm.org/doi/10.1128/spectrum.03300-2216S RNACorynebacteriumhuman microbiomeinfectious diseaseskin microbiome
spellingShingle Sameer Gupta
Alexandra J. Poret
David Hashemi
Amarachi Eseonu
Sherry H. Yu
Jonathan D'Gama
Victor A. Neel
Tami D. Lieberman
Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin
Microbiology Spectrum
16S RNA
Corynebacterium
human microbiome
infectious disease
skin microbiome
title Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin
title_full Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin
title_fullStr Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin
title_full_unstemmed Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin
title_short Cutaneous Surgical Wounds Have Distinct Microbiomes from Intact Skin
title_sort cutaneous surgical wounds have distinct microbiomes from intact skin
topic 16S RNA
Corynebacterium
human microbiome
infectious disease
skin microbiome
url https://journals.asm.org/doi/10.1128/spectrum.03300-22
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