Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro

Strategies are sought to reduce the carriage and dissemination of zoonotic pathogens and antimicrobial-resistant microbes within food-producing animals and their production environment. Thymol (an essential oil) is a potent bactericide in vitro but in vivo efficacy has been inconsistent, largely due...

Full description

Bibliographic Details
Main Authors: Robin C. Anderson, Gizem Levent, Branko T. Petrujkić, Roger B. Harvey, Michael E. Hume, Haiqi He, Kenneth J. Genovese, Ross C. Beier, Toni L. Poole, Tawni L. Crippen, David J. Nisbet
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-09-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2021.751266/full
_version_ 1819099044530618368
author Robin C. Anderson
Gizem Levent
Gizem Levent
Branko T. Petrujkić
Branko T. Petrujkić
Roger B. Harvey
Michael E. Hume
Haiqi He
Kenneth J. Genovese
Ross C. Beier
Toni L. Poole
Tawni L. Crippen
David J. Nisbet
author_facet Robin C. Anderson
Gizem Levent
Gizem Levent
Branko T. Petrujkić
Branko T. Petrujkić
Roger B. Harvey
Michael E. Hume
Haiqi He
Kenneth J. Genovese
Ross C. Beier
Toni L. Poole
Tawni L. Crippen
David J. Nisbet
author_sort Robin C. Anderson
collection DOAJ
description Strategies are sought to reduce the carriage and dissemination of zoonotic pathogens and antimicrobial-resistant microbes within food-producing animals and their production environment. Thymol (an essential oil) is a potent bactericide in vitro but in vivo efficacy has been inconsistent, largely due to its lipophilicity and absorption, which limits its passage and subsequent availability in the distal gastrointestinal tract. Conjugation of thymol to glucose to form thymol-β-d-glucopyranoside can decrease its absorption, but in vivo passage of effective concentrations to the lower gut remains suboptimal. Considering that contemporary swine diets often contain 5% or more added fat (to increase caloric density and reduce dustiness), we hypothesized that there may be sufficient residual fat in the distal intestinal tract to sequester free or conjugated thymol, thereby limiting the availability and subsequent effectiveness of this biocide. In support of this hypothesis, the anti-Salmonella Typhimurium effects of 6 mM free or conjugated thymol, expressed as log10-fold reductions of colony-forming units (CFU) ml−1, were diminished 90 and 58%, respectively, following 24-h in vitro anaerobic fecal incubation (at 39°C) with 3% added vegetable oil compared to reductions achieved during culture without added oil (6.1 log10 CFU ml−1). The antagonistic effect of vegetable oil and the bactericidal effect of free and conjugated thymol against Escherichia coli K88 tested similarly were diminished 86 and 84%, respectively, compared to reductions achieved in cultures incubated without added vegetable oil (5.7 log10 CFU ml−1). Inclusion of taurine (8 mg/ml), bile acids (0.6 mg/ml), or emulsifiers such as polyoxyethylene-40 stearate (0.2%), Tween 20, or Tween 80 (each at 1%) in the in vitro incubations had little effect on vegetable oil-caused inhibition of free or conjugated thymol. Based on these results, it seems reasonable to suspect that undigested lipid in the distal gut may limit the effectiveness of free or conjugated thymol. Accordingly, additional research is warranted to learn how to overcome obstacles diminishing bactericidal activity of free and conjugated thymol in the lower gastrointestinal tract of food-producing animals.
first_indexed 2024-12-22T00:40:37Z
format Article
id doaj.art-3ab7fac7bacd4a78822043093f4a3719
institution Directory Open Access Journal
issn 2297-1769
language English
last_indexed 2024-12-22T00:40:37Z
publishDate 2021-09-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Veterinary Science
spelling doaj.art-3ab7fac7bacd4a78822043093f4a37192022-12-21T18:44:42ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692021-09-01810.3389/fvets.2021.751266751266Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In VitroRobin C. Anderson0Gizem Levent1Gizem Levent2Branko T. Petrujkić3Branko T. Petrujkić4Roger B. Harvey5Michael E. Hume6Haiqi He7Kenneth J. Genovese8Ross C. Beier9Toni L. Poole10Tawni L. Crippen11David J. Nisbet12United States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesDepartment of Veterinary Pathobiology, Texas A&M University, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesDepartment of Nutrition and Botany, Faculty of Veterinary Medicine, University of Belgrade, Belgrade, SerbiaUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesUnited States Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, TX, United StatesStrategies are sought to reduce the carriage and dissemination of zoonotic pathogens and antimicrobial-resistant microbes within food-producing animals and their production environment. Thymol (an essential oil) is a potent bactericide in vitro but in vivo efficacy has been inconsistent, largely due to its lipophilicity and absorption, which limits its passage and subsequent availability in the distal gastrointestinal tract. Conjugation of thymol to glucose to form thymol-β-d-glucopyranoside can decrease its absorption, but in vivo passage of effective concentrations to the lower gut remains suboptimal. Considering that contemporary swine diets often contain 5% or more added fat (to increase caloric density and reduce dustiness), we hypothesized that there may be sufficient residual fat in the distal intestinal tract to sequester free or conjugated thymol, thereby limiting the availability and subsequent effectiveness of this biocide. In support of this hypothesis, the anti-Salmonella Typhimurium effects of 6 mM free or conjugated thymol, expressed as log10-fold reductions of colony-forming units (CFU) ml−1, were diminished 90 and 58%, respectively, following 24-h in vitro anaerobic fecal incubation (at 39°C) with 3% added vegetable oil compared to reductions achieved during culture without added oil (6.1 log10 CFU ml−1). The antagonistic effect of vegetable oil and the bactericidal effect of free and conjugated thymol against Escherichia coli K88 tested similarly were diminished 86 and 84%, respectively, compared to reductions achieved in cultures incubated without added vegetable oil (5.7 log10 CFU ml−1). Inclusion of taurine (8 mg/ml), bile acids (0.6 mg/ml), or emulsifiers such as polyoxyethylene-40 stearate (0.2%), Tween 20, or Tween 80 (each at 1%) in the in vitro incubations had little effect on vegetable oil-caused inhibition of free or conjugated thymol. Based on these results, it seems reasonable to suspect that undigested lipid in the distal gut may limit the effectiveness of free or conjugated thymol. Accordingly, additional research is warranted to learn how to overcome obstacles diminishing bactericidal activity of free and conjugated thymol in the lower gastrointestinal tract of food-producing animals.https://www.frontiersin.org/articles/10.3389/fvets.2021.751266/fullantibiotic alternativeSalmonellaE. colithymolthymol-β-d-glucopyranoside
spellingShingle Robin C. Anderson
Gizem Levent
Gizem Levent
Branko T. Petrujkić
Branko T. Petrujkić
Roger B. Harvey
Michael E. Hume
Haiqi He
Kenneth J. Genovese
Ross C. Beier
Toni L. Poole
Tawni L. Crippen
David J. Nisbet
Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro
Frontiers in Veterinary Science
antibiotic alternative
Salmonella
E. coli
thymol
thymol-β-d-glucopyranoside
title Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro
title_full Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro
title_fullStr Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro
title_full_unstemmed Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro
title_short Antagonistic Effects of Lipids Against the Anti-Escherichia coli and Anti-Salmonella Activity of Thymol and Thymol-β-d-Glucopyranoside in Porcine Gut and Fecal Cultures In Vitro
title_sort antagonistic effects of lipids against the anti escherichia coli and anti salmonella activity of thymol and thymol β d glucopyranoside in porcine gut and fecal cultures in vitro
topic antibiotic alternative
Salmonella
E. coli
thymol
thymol-β-d-glucopyranoside
url https://www.frontiersin.org/articles/10.3389/fvets.2021.751266/full
work_keys_str_mv AT robincanderson antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT gizemlevent antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT gizemlevent antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT brankotpetrujkic antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT brankotpetrujkic antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT rogerbharvey antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT michaelehume antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT haiqihe antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT kennethjgenovese antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT rosscbeier antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT tonilpoole antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT tawnilcrippen antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro
AT davidjnisbet antagonisticeffectsoflipidsagainsttheantiescherichiacoliandantisalmonellaactivityofthymolandthymolbdglucopyranosideinporcinegutandfecalculturesinvitro