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Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease

Vibrio vulnificus is known to cause necrotizing soft tissue infections (NSTIs). However, the pathogenic mechanism causing cellulitis, necrotizing fasciitis, muscle necrosis, and rapidly developing septicemia in humans have not been fully elucidated. Here, we report a multilayer analysis of tissue da...

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Autores principales: Yamazaki, Kohei, Kashimoto, Takashige, Kado, Takehiro, Yoshioka, Kazuki, Ueno, Shunji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8957983/
https://www.ncbi.nlm.nih.gov/pubmed/35350614
http://dx.doi.org/10.3389/fmicb.2022.849600
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author Yamazaki, Kohei
Kashimoto, Takashige
Kado, Takehiro
Yoshioka, Kazuki
Ueno, Shunji
author_facet Yamazaki, Kohei
Kashimoto, Takashige
Kado, Takehiro
Yoshioka, Kazuki
Ueno, Shunji
author_sort Yamazaki, Kohei
collection PubMed
description Vibrio vulnificus is known to cause necrotizing soft tissue infections (NSTIs). However, the pathogenic mechanism causing cellulitis, necrotizing fasciitis, muscle necrosis, and rapidly developing septicemia in humans have not been fully elucidated. Here, we report a multilayer analysis of tissue damage after subcutaneous bacterial inoculation as a murine model of V. vulnificus NSTIs. Our histopathological examination showed the progression of cellulitis, necrotizing fasciitis, and muscle necrosis worsening as the infection penetrated deeper into the muscle tissue layers. The increase in vascular permeability was the primary cause of the swelling and congestion, which are acute signs of inflammation in soft tissue and characteristic of human NSTIs. Most importantly, our sequential analysis revealed for the first time that V. vulnificus not only spreads along the skin and subcutaneous tissues or fascia but also invades deeper muscle tissues beyond the fascia as the crucial process of its lethality. Also, increased vascular permeability enabled V. vulnificus to proliferate in muscle tissue and enter the systemic circulation, escalating the bacterium’s lethality. Our finding may yield important clinical benefits to patients by helping physicians understand the impact of surgical debridement on the patient’s quality of life. Furthermore, this study provides a promising system to accelerate studies of virulence factors and eventually help establish new therapies.
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spelling pubmed-89579832022-03-28 Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease Yamazaki, Kohei Kashimoto, Takashige Kado, Takehiro Yoshioka, Kazuki Ueno, Shunji Front Microbiol Microbiology Vibrio vulnificus is known to cause necrotizing soft tissue infections (NSTIs). However, the pathogenic mechanism causing cellulitis, necrotizing fasciitis, muscle necrosis, and rapidly developing septicemia in humans have not been fully elucidated. Here, we report a multilayer analysis of tissue damage after subcutaneous bacterial inoculation as a murine model of V. vulnificus NSTIs. Our histopathological examination showed the progression of cellulitis, necrotizing fasciitis, and muscle necrosis worsening as the infection penetrated deeper into the muscle tissue layers. The increase in vascular permeability was the primary cause of the swelling and congestion, which are acute signs of inflammation in soft tissue and characteristic of human NSTIs. Most importantly, our sequential analysis revealed for the first time that V. vulnificus not only spreads along the skin and subcutaneous tissues or fascia but also invades deeper muscle tissues beyond the fascia as the crucial process of its lethality. Also, increased vascular permeability enabled V. vulnificus to proliferate in muscle tissue and enter the systemic circulation, escalating the bacterium’s lethality. Our finding may yield important clinical benefits to patients by helping physicians understand the impact of surgical debridement on the patient’s quality of life. Furthermore, this study provides a promising system to accelerate studies of virulence factors and eventually help establish new therapies. Frontiers Media S.A. 2022-03-08 /pmc/articles/PMC8957983/ /pubmed/35350614 http://dx.doi.org/10.3389/fmicb.2022.849600 Text en Copyright © 2022 Yamazaki, Kashimoto, Kado, Yoshioka and Ueno. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Yamazaki, Kohei
Kashimoto, Takashige
Kado, Takehiro
Yoshioka, Kazuki
Ueno, Shunji
Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease
title Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease
title_full Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease
title_fullStr Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease
title_full_unstemmed Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease
title_short Increased Vascular Permeability Due to Spread and Invasion of Vibrio vulnificus in the Wound Infection Exacerbates Potentially Fatal Necrotizing Disease
title_sort increased vascular permeability due to spread and invasion of vibrio vulnificus in the wound infection exacerbates potentially fatal necrotizing disease
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8957983/
https://www.ncbi.nlm.nih.gov/pubmed/35350614
http://dx.doi.org/10.3389/fmicb.2022.849600
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