Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel

Abstract Chronic non-healing wounds significantly strain modern healthcare systems, affecting 1–2% of the population in developed countries with costs ranging between $28.1 and $96.8 billion annually. Additionally, it has been established that chronic wounds resulting from comorbidities, such as per...

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Main Authors: Ayushi D. Sharma, Evan H. Jarman, Krutika Kuppalli, Matthew J. Murphy, Michael T. Longaker, Geoffrey Gurtner, Paige M. Fox
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-024-54477-z
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author Ayushi D. Sharma
Evan H. Jarman
Krutika Kuppalli
Matthew J. Murphy
Michael T. Longaker
Geoffrey Gurtner
Paige M. Fox
author_facet Ayushi D. Sharma
Evan H. Jarman
Krutika Kuppalli
Matthew J. Murphy
Michael T. Longaker
Geoffrey Gurtner
Paige M. Fox
author_sort Ayushi D. Sharma
collection DOAJ
description Abstract Chronic non-healing wounds significantly strain modern healthcare systems, affecting 1–2% of the population in developed countries with costs ranging between $28.1 and $96.8 billion annually. Additionally, it has been established that chronic wounds resulting from comorbidities, such as peripheral vascular disease and diabetes mellitus, tend to be polymicrobial in nature. Treatment of polymicrobial chronic wounds with oral and IV antibiotics can result in antimicrobial resistance, leading to more difficult-to-treat wounds. Ideally, chronic ulcers would be topically treated with antibiotic combinations tailored to the microbiome of a patient’s wound. We have previously shown that a topical collagen-rich hydrogel (cHG) can elute single antibiotics to inhibit bacterial growth in a manner that is nontoxic to mammalian cells. Here, we analyzed the microbiology of cultures taken from human patients diagnosed with diabetes mellitus suffering from chronic wounds present for more than 6 weeks. Additionally, we examined the safety of the elution of multiple antibiotics from collagen-rich hydrogel in mammalian cells in vivo. Finally, we aimed to create tailored combinations of antibiotics impregnated into cHG to successfully target and treat infections and eradicate biofilms cultured from human chronic diabetic wound tissue. We found that the majority of human chronic wounds in our study were polymicrobial in nature. The elution of multiple antibiotics from cHG was well-tolerated in mammalian cells, making it a potential topical treatment of the polymicrobial chronic wound. Finally, combinations of antibiotics tailored to each patient’s microbiome eluted from a collagen-rich hydrogel successfully treated bacterial cultures isolated from patient samples via an in vitro assay.
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spelling doaj.art-159be1bad20245bc98dda61117d359502024-03-10T12:11:26ZengNature PortfolioScientific Reports2045-23222024-03-0114111010.1038/s41598-024-54477-zSuccessful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogelAyushi D. Sharma0Evan H. Jarman1Krutika Kuppalli2Matthew J. Murphy3Michael T. Longaker4Geoffrey Gurtner5Paige M. Fox6Division of Plastic & Reconstructive Surgery, Department of Surgery, Stanford University School of MedicineDivision of Plastic & Reconstructive Surgery, Department of Surgery, Stanford University School of MedicineDivision of Plastic & Reconstructive Surgery, Department of Surgery, Stanford University School of MedicineDivision of Plastic & Reconstructive Surgery, Department of Surgery, Stanford University School of MedicineDivision of Plastic & Reconstructive Surgery, Department of Surgery, Stanford University School of MedicineDepartment of Surgery, The University of Arizona College of MedicineDivision of Plastic & Reconstructive Surgery, Department of Surgery, Stanford University School of MedicineAbstract Chronic non-healing wounds significantly strain modern healthcare systems, affecting 1–2% of the population in developed countries with costs ranging between $28.1 and $96.8 billion annually. Additionally, it has been established that chronic wounds resulting from comorbidities, such as peripheral vascular disease and diabetes mellitus, tend to be polymicrobial in nature. Treatment of polymicrobial chronic wounds with oral and IV antibiotics can result in antimicrobial resistance, leading to more difficult-to-treat wounds. Ideally, chronic ulcers would be topically treated with antibiotic combinations tailored to the microbiome of a patient’s wound. We have previously shown that a topical collagen-rich hydrogel (cHG) can elute single antibiotics to inhibit bacterial growth in a manner that is nontoxic to mammalian cells. Here, we analyzed the microbiology of cultures taken from human patients diagnosed with diabetes mellitus suffering from chronic wounds present for more than 6 weeks. Additionally, we examined the safety of the elution of multiple antibiotics from collagen-rich hydrogel in mammalian cells in vivo. Finally, we aimed to create tailored combinations of antibiotics impregnated into cHG to successfully target and treat infections and eradicate biofilms cultured from human chronic diabetic wound tissue. We found that the majority of human chronic wounds in our study were polymicrobial in nature. The elution of multiple antibiotics from cHG was well-tolerated in mammalian cells, making it a potential topical treatment of the polymicrobial chronic wound. Finally, combinations of antibiotics tailored to each patient’s microbiome eluted from a collagen-rich hydrogel successfully treated bacterial cultures isolated from patient samples via an in vitro assay.https://doi.org/10.1038/s41598-024-54477-z
spellingShingle Ayushi D. Sharma
Evan H. Jarman
Krutika Kuppalli
Matthew J. Murphy
Michael T. Longaker
Geoffrey Gurtner
Paige M. Fox
Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel
Scientific Reports
title Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel
title_full Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel
title_fullStr Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel
title_full_unstemmed Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel
title_short Successful topical treatment of human biofilms using multiple antibiotic elution from a collagen-rich hydrogel
title_sort successful topical treatment of human biofilms using multiple antibiotic elution from a collagen rich hydrogel
url https://doi.org/10.1038/s41598-024-54477-z
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