Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.

BACKGROUND:Biofilm formation by Staphylococcus aureus is an important virulence attribute because of its potential to induce persistent antibiotic resistance, retard phagocytosis and either attenuate or promote inflammation, depending upon the disease syndrome, in vivo. This study was undertaken to...

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Main Authors: Jully Gogoi-Tiwari, Vincent Williams, Charlene Babra Waryah, Paul Costantino, Hani Al-Salami, Sangeetha Mathavan, Kelsi Wells, Harish Kumar Tiwari, Nagendra Hegde, Shrikrishna Isloor, Hesham Al-Sallami, Trilochan Mukkur
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC5271311?pdf=render
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author Jully Gogoi-Tiwari
Vincent Williams
Charlene Babra Waryah
Paul Costantino
Hani Al-Salami
Sangeetha Mathavan
Kelsi Wells
Harish Kumar Tiwari
Nagendra Hegde
Shrikrishna Isloor
Hesham Al-Sallami
Trilochan Mukkur
author_facet Jully Gogoi-Tiwari
Vincent Williams
Charlene Babra Waryah
Paul Costantino
Hani Al-Salami
Sangeetha Mathavan
Kelsi Wells
Harish Kumar Tiwari
Nagendra Hegde
Shrikrishna Isloor
Hesham Al-Sallami
Trilochan Mukkur
author_sort Jully Gogoi-Tiwari
collection DOAJ
description BACKGROUND:Biofilm formation by Staphylococcus aureus is an important virulence attribute because of its potential to induce persistent antibiotic resistance, retard phagocytosis and either attenuate or promote inflammation, depending upon the disease syndrome, in vivo. This study was undertaken to evaluate the potential significance of strength of biofilm formation by clinical bovine mastitis-associated S. aureus in mammary tissue damage by using a mouse mastitis model. METHODS:Two S. aureus strains of the same capsular phenotype with different biofilm forming strengths were used to non-invasively infect mammary glands of lactating mice. Biofilm forming potential of these strains were determined by tissue culture plate method, ica typing and virulence gene profile per detection by PCR. Delivery of the infectious dose of S. aureus was directly through the teat lactiferous duct without invasive scraping of the teat surface. Both bacteriological and histological methods were used for analysis of mammary gland pathology of mice post-infection. RESULTS:Histopathological analysis of the infected mammary glands revealed that mice inoculated with the strong biofilm forming S. aureus strain produced marked acute mastitic lesions, showing profuse infiltration predominantly with neutrophils, with evidence of necrosis in the affected mammary glands. In contrast, the damage was significantly less severe in mammary glands of mice infected with the weak biofilm-forming S. aureus strain. Although both IL-1β and TNF-α inflammatory biomarkers were produced in infected mice, level of TNF-α produced was significantly higher (p<0.05) in mice inoculated with strong biofilm forming S. aureus than the weak biofilm forming strain. CONCLUSION:This finding suggests an important role of TNF-α in mammary gland pathology post-infection with strong biofilm-forming S. aureus in the acute mouse mastitis model, and offers an opportunity for the development of novel strategies for reduction of mammary tissue damage, with or without use of antimicrobials and/or anti-inflammatory compounds for the treatment of bovine mastitis.
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spelling doaj.art-95c6201ac4ca43c4917c5c7e3d89744b2022-12-22T03:34:44ZengPublic Library of Science (PLoS)PLoS ONE1932-62032017-01-01121e017066810.1371/journal.pone.0170668Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.Jully Gogoi-TiwariVincent WilliamsCharlene Babra WaryahPaul CostantinoHani Al-SalamiSangeetha MathavanKelsi WellsHarish Kumar TiwariNagendra HegdeShrikrishna IsloorHesham Al-SallamiTrilochan MukkurBACKGROUND:Biofilm formation by Staphylococcus aureus is an important virulence attribute because of its potential to induce persistent antibiotic resistance, retard phagocytosis and either attenuate or promote inflammation, depending upon the disease syndrome, in vivo. This study was undertaken to evaluate the potential significance of strength of biofilm formation by clinical bovine mastitis-associated S. aureus in mammary tissue damage by using a mouse mastitis model. METHODS:Two S. aureus strains of the same capsular phenotype with different biofilm forming strengths were used to non-invasively infect mammary glands of lactating mice. Biofilm forming potential of these strains were determined by tissue culture plate method, ica typing and virulence gene profile per detection by PCR. Delivery of the infectious dose of S. aureus was directly through the teat lactiferous duct without invasive scraping of the teat surface. Both bacteriological and histological methods were used for analysis of mammary gland pathology of mice post-infection. RESULTS:Histopathological analysis of the infected mammary glands revealed that mice inoculated with the strong biofilm forming S. aureus strain produced marked acute mastitic lesions, showing profuse infiltration predominantly with neutrophils, with evidence of necrosis in the affected mammary glands. In contrast, the damage was significantly less severe in mammary glands of mice infected with the weak biofilm-forming S. aureus strain. Although both IL-1β and TNF-α inflammatory biomarkers were produced in infected mice, level of TNF-α produced was significantly higher (p<0.05) in mice inoculated with strong biofilm forming S. aureus than the weak biofilm forming strain. CONCLUSION:This finding suggests an important role of TNF-α in mammary gland pathology post-infection with strong biofilm-forming S. aureus in the acute mouse mastitis model, and offers an opportunity for the development of novel strategies for reduction of mammary tissue damage, with or without use of antimicrobials and/or anti-inflammatory compounds for the treatment of bovine mastitis.http://europepmc.org/articles/PMC5271311?pdf=render
spellingShingle Jully Gogoi-Tiwari
Vincent Williams
Charlene Babra Waryah
Paul Costantino
Hani Al-Salami
Sangeetha Mathavan
Kelsi Wells
Harish Kumar Tiwari
Nagendra Hegde
Shrikrishna Isloor
Hesham Al-Sallami
Trilochan Mukkur
Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.
PLoS ONE
title Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.
title_full Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.
title_fullStr Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.
title_full_unstemmed Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.
title_short Mammary Gland Pathology Subsequent to Acute Infection with Strong versus Weak Biofilm Forming Staphylococcus aureus Bovine Mastitis Isolates: A Pilot Study Using Non-Invasive Mouse Mastitis Model.
title_sort mammary gland pathology subsequent to acute infection with strong versus weak biofilm forming staphylococcus aureus bovine mastitis isolates a pilot study using non invasive mouse mastitis model
url http://europepmc.org/articles/PMC5271311?pdf=render
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