Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken

Salmonella is a foodborne pathogen of animal and public health significance. Considering the disadvantages of antibiotics or chemical preservatives traditionally used to eliminate this pathogen, attention has shifted, in recent years, toward biocontrol agents such as bacteriophages, used either sepa...

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Main Authors: Narges Torkashvand, Haniyeh Kamyab, Parisa Aarabi, Ahmad Reza Shahverdi, Mohammad Amir Karimi Torshizi, Mohammad Reza Khoshayand, Zargham Sepehrizadeh
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-11-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1505805/full
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author Narges Torkashvand
Haniyeh Kamyab
Haniyeh Kamyab
Parisa Aarabi
Ahmad Reza Shahverdi
Ahmad Reza Shahverdi
Mohammad Amir Karimi Torshizi
Mohammad Reza Khoshayand
Mohammad Reza Khoshayand
Zargham Sepehrizadeh
Zargham Sepehrizadeh
author_facet Narges Torkashvand
Haniyeh Kamyab
Haniyeh Kamyab
Parisa Aarabi
Ahmad Reza Shahverdi
Ahmad Reza Shahverdi
Mohammad Amir Karimi Torshizi
Mohammad Reza Khoshayand
Mohammad Reza Khoshayand
Zargham Sepehrizadeh
Zargham Sepehrizadeh
author_sort Narges Torkashvand
collection DOAJ
description Salmonella is a foodborne pathogen of animal and public health significance. Considering the disadvantages of antibiotics or chemical preservatives traditionally used to eliminate this pathogen, attention has shifted, in recent years, toward biocontrol agents such as bacteriophages, used either separately or in combination to prevent food contamination. However, extensive use of phage-based biocontrol agents in the food industry requires further studies to ensure their safety and efficacy. In the present study, we investigated the effectiveness and safety of phage cocktail, a phage cocktail comprising three pre-characterized Salmonella phages (vB_SenS_TUMS_E4, vB_SenS_TUMS_E15 and vB_SenS_TUMS_E19). First, we performed an MTT [3-(4,5-dimethylthiazol-2-yl)-2,5 diphenyl tetrazolium bromide] assay on a human foreskin fibroblast cell line, in which the resulting high cell viability revealed the safety of the phage cocktail. Next, we performed a time-kill assay in which a 4 Log decline in bacterial levels was detected. Additionally, we utilized a colorimetric method to evaluate the anti-biofilm activity of phage cocktail, in which it proved more efficacious compared to the MIC and MBEC levels of the antibiotic control. Then, we assessed the ability of phage cocktail to eradicate Salmonella in different food samples, where it considerably reduced the bacterial count regardless of the temperature (4°C and 25°C). Lastly, we used broiler chickens as an animal model to measure the growth-promoting activity of phage cocktail. Salmonella-infected chickens orally treated with modified phage cocktail demonstrated no mortality and a significant increase in weight gain compared to the untreated group (p ≤ 0.0002). The study presents a novel research evaluating the effectiveness and safety of a phage cocktail as a biocontrol agent against Salmonella in various contexts, including biofilms, food products, and broiler chickens. This multifaceted approach underscores the promising role of phage therapy as a sustainable biocontrol strategy in food safety and public health contexts.
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spelling doaj-art-bf235cddce8b4d67bccc2135aeb99e682025-08-20T02:07:24ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-11-011510.3389/fmicb.2024.15058051505805Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chickenNarges Torkashvand0Haniyeh Kamyab1Haniyeh Kamyab2Parisa Aarabi3Ahmad Reza Shahverdi4Ahmad Reza Shahverdi5Mohammad Amir Karimi Torshizi6Mohammad Reza Khoshayand7Mohammad Reza Khoshayand8Zargham Sepehrizadeh9Zargham Sepehrizadeh10Department of Pharmaceutical Biotechnology, Faculty of Pharmacy and Biotechnology Research Center, Tehran University of Medical Sciences, Tehran, IranDepartment of Pharmaceutical Biotechnology, Faculty of Pharmacy and Biotechnology Research Center, Tehran University of Medical Sciences, Tehran, IranFaculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IranFaculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IranDepartment of Pharmaceutical Biotechnology, Faculty of Pharmacy and Biotechnology Research Center, Tehran University of Medical Sciences, Tehran, IranFaculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IranDepartment of Poultry Sciences, Faculty of Agriculture, Tarbiat Modares University, Tehran, IranFaculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IranDepartment of Food and Drug Control, Faculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IranDepartment of Pharmaceutical Biotechnology, Faculty of Pharmacy and Biotechnology Research Center, Tehran University of Medical Sciences, Tehran, IranFaculty of Pharmacy, Tehran University of Medical Sciences, Tehran, IranSalmonella is a foodborne pathogen of animal and public health significance. Considering the disadvantages of antibiotics or chemical preservatives traditionally used to eliminate this pathogen, attention has shifted, in recent years, toward biocontrol agents such as bacteriophages, used either separately or in combination to prevent food contamination. However, extensive use of phage-based biocontrol agents in the food industry requires further studies to ensure their safety and efficacy. In the present study, we investigated the effectiveness and safety of phage cocktail, a phage cocktail comprising three pre-characterized Salmonella phages (vB_SenS_TUMS_E4, vB_SenS_TUMS_E15 and vB_SenS_TUMS_E19). First, we performed an MTT [3-(4,5-dimethylthiazol-2-yl)-2,5 diphenyl tetrazolium bromide] assay on a human foreskin fibroblast cell line, in which the resulting high cell viability revealed the safety of the phage cocktail. Next, we performed a time-kill assay in which a 4 Log decline in bacterial levels was detected. Additionally, we utilized a colorimetric method to evaluate the anti-biofilm activity of phage cocktail, in which it proved more efficacious compared to the MIC and MBEC levels of the antibiotic control. Then, we assessed the ability of phage cocktail to eradicate Salmonella in different food samples, where it considerably reduced the bacterial count regardless of the temperature (4°C and 25°C). Lastly, we used broiler chickens as an animal model to measure the growth-promoting activity of phage cocktail. Salmonella-infected chickens orally treated with modified phage cocktail demonstrated no mortality and a significant increase in weight gain compared to the untreated group (p ≤ 0.0002). The study presents a novel research evaluating the effectiveness and safety of a phage cocktail as a biocontrol agent against Salmonella in various contexts, including biofilms, food products, and broiler chickens. This multifaceted approach underscores the promising role of phage therapy as a sustainable biocontrol strategy in food safety and public health contexts.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1505805/fullbiocontrolphage cocktailSalmonellabiofilmfood productsbroiler chickens
spellingShingle Narges Torkashvand
Haniyeh Kamyab
Haniyeh Kamyab
Parisa Aarabi
Ahmad Reza Shahverdi
Ahmad Reza Shahverdi
Mohammad Amir Karimi Torshizi
Mohammad Reza Khoshayand
Mohammad Reza Khoshayand
Zargham Sepehrizadeh
Zargham Sepehrizadeh
Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken
Frontiers in Microbiology
biocontrol
phage cocktail
Salmonella
biofilm
food products
broiler chickens
title Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken
title_full Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken
title_fullStr Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken
title_full_unstemmed Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken
title_short Evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of Salmonella in biofilm, food products, and broiler chicken
title_sort evaluating the effectiveness and safety of a novel phage cocktail as a biocontrol of salmonella in biofilm food products and broiler chicken
topic biocontrol
phage cocktail
Salmonella
biofilm
food products
broiler chickens
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1505805/full
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