The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype

Cold-smoked salmon is a ready-to-eat food product capable of supporting Listeria monocytogenes growth at refrigeration temperatures. While the FDA-approved antimicrobial nisin can be used to mitigate L. monocytogenes contamination, stresses associated with cold-smoked salmon and the associated proce...

Full description

Bibliographic Details
Main Authors: Ruixi Chen, Jordan William Skeens, Martin Wiedmann, Veronica Guariglia-Oropeza
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.930400/full
_version_ 1798002255537897472
author Ruixi Chen
Jordan William Skeens
Martin Wiedmann
Veronica Guariglia-Oropeza
author_facet Ruixi Chen
Jordan William Skeens
Martin Wiedmann
Veronica Guariglia-Oropeza
author_sort Ruixi Chen
collection DOAJ
description Cold-smoked salmon is a ready-to-eat food product capable of supporting Listeria monocytogenes growth at refrigeration temperatures. While the FDA-approved antimicrobial nisin can be used to mitigate L. monocytogenes contamination, stresses associated with cold-smoked salmon and the associated processing environments may reduce nisin efficacy. A previous study in our laboratory showed that, at high inoculation levels, pre-exposure of L. monocytogenes to sublethal concentrations of quaternary ammonium compounds had an overall detrimental effect on nisin efficacy. The objective of this study was to investigate the impact of nisin concentration and storage temperature on nisin efficacy against L. monocytogenes inoculated on salmon at natural contamination levels. Three L. monocytogenes strains were pre-grown in the presence of sublethal levels of benzalkonium chloride prior to inoculation at ~102 CFU/g on salmon slices that were pre-treated with either 0, 25, or 250 ppm nisin, followed by vacuum-packing and incubation at 4 or 7°C for up to 30 days. L. monocytogenes was enumerated on days 1, 15, and 30 using direct plating and/or most probable number methods. A hurdle model was constructed to describe the odds of complete elimination of L. monocytogenes on salmon and the level of L. monocytogenes when complete elimination was not achieved. Our data showed that (i) nisin efficacy (defined as L. monocytogenes reduction relative to the untreated control) was concentration-dependent with increased efficacy at 250 ppm nisin, and that (ii) 250 ppm nisin treatments led to a reduction in L. monocytogenes prevalence, independent of storage temperature and serotype; this effect of nisin could only be identified since low inoculation levels were used. While lower storage temperatures (i.e., 4°C) yielded lowered absolute L. monocytogenes counts on days 15 and 30 (as compared to 7°C), nisin efficacy did not differ between these two temperatures. Finally, the serotype 1/2b strain was found to be more susceptible to nisin compared with serotype 1/2a and 4b strains on samples incubated at 7°C or treated with 25 ppm nisin. This variation of nisin susceptibility across serotypes, which is affected by both the storage temperature and nisin concentration, needs to be considered while evaluating the efficacy of nisin.
first_indexed 2024-04-11T11:49:08Z
format Article
id doaj.art-d637ca6a6586440a9f547113c344f52b
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-11T11:49:08Z
publishDate 2022-09-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-d637ca6a6586440a9f547113c344f52b2022-12-22T04:25:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.930400930400The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotypeRuixi ChenJordan William SkeensMartin WiedmannVeronica Guariglia-OropezaCold-smoked salmon is a ready-to-eat food product capable of supporting Listeria monocytogenes growth at refrigeration temperatures. While the FDA-approved antimicrobial nisin can be used to mitigate L. monocytogenes contamination, stresses associated with cold-smoked salmon and the associated processing environments may reduce nisin efficacy. A previous study in our laboratory showed that, at high inoculation levels, pre-exposure of L. monocytogenes to sublethal concentrations of quaternary ammonium compounds had an overall detrimental effect on nisin efficacy. The objective of this study was to investigate the impact of nisin concentration and storage temperature on nisin efficacy against L. monocytogenes inoculated on salmon at natural contamination levels. Three L. monocytogenes strains were pre-grown in the presence of sublethal levels of benzalkonium chloride prior to inoculation at ~102 CFU/g on salmon slices that were pre-treated with either 0, 25, or 250 ppm nisin, followed by vacuum-packing and incubation at 4 or 7°C for up to 30 days. L. monocytogenes was enumerated on days 1, 15, and 30 using direct plating and/or most probable number methods. A hurdle model was constructed to describe the odds of complete elimination of L. monocytogenes on salmon and the level of L. monocytogenes when complete elimination was not achieved. Our data showed that (i) nisin efficacy (defined as L. monocytogenes reduction relative to the untreated control) was concentration-dependent with increased efficacy at 250 ppm nisin, and that (ii) 250 ppm nisin treatments led to a reduction in L. monocytogenes prevalence, independent of storage temperature and serotype; this effect of nisin could only be identified since low inoculation levels were used. While lower storage temperatures (i.e., 4°C) yielded lowered absolute L. monocytogenes counts on days 15 and 30 (as compared to 7°C), nisin efficacy did not differ between these two temperatures. Finally, the serotype 1/2b strain was found to be more susceptible to nisin compared with serotype 1/2a and 4b strains on samples incubated at 7°C or treated with 25 ppm nisin. This variation of nisin susceptibility across serotypes, which is affected by both the storage temperature and nisin concentration, needs to be considered while evaluating the efficacy of nisin.https://www.frontiersin.org/articles/10.3389/fmicb.2022.930400/fullListeria monocytogenesnisincold-smoked salmonantimicrobial concentrationserotype
spellingShingle Ruixi Chen
Jordan William Skeens
Martin Wiedmann
Veronica Guariglia-Oropeza
The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype
Frontiers in Microbiology
Listeria monocytogenes
nisin
cold-smoked salmon
antimicrobial concentration
serotype
title The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype
title_full The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype
title_fullStr The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype
title_full_unstemmed The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype
title_short The efficacy of nisin against Listeria monocytogenes on cold-smoked salmon at natural contamination levels is concentration-dependent and varies by serotype
title_sort efficacy of nisin against listeria monocytogenes on cold smoked salmon at natural contamination levels is concentration dependent and varies by serotype
topic Listeria monocytogenes
nisin
cold-smoked salmon
antimicrobial concentration
serotype
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.930400/full
work_keys_str_mv AT ruixichen theefficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT jordanwilliamskeens theefficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT martinwiedmann theefficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT veronicaguarigliaoropeza theefficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT ruixichen efficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT jordanwilliamskeens efficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT martinwiedmann efficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype
AT veronicaguarigliaoropeza efficacyofnisinagainstlisteriamonocytogenesoncoldsmokedsalmonatnaturalcontaminationlevelsisconcentrationdependentandvariesbyserotype