Efficacy of peroxyacetic acid against Salmonella biofilms and as a decontaminant agent in poultry meat


Published: Jul 10, 2022
Keywords:
Biofilms Broiler meat Decontamination Peroxyacetic acid Salmonella
Bahar Onaran Acar
https://orcid.org/0000-0002-3515-7548
Gorkem Cengiz
https://orcid.org/0000-0001-9853-565X
Erman Gulendag
https://orcid.org/0000-0002-3335-7247
Muammer Goncuoglu
https://orcid.org/0000-0001-7245-1941
K. Serdar Diker
https://orcid.org/0000-0003-2150-5553
Abstract

We aimed to investigate the effect of the post-chilling Peroxyacetic Acid (PAA) application on chicken carcasses’ shelf life, PAA treatment on chicken neck skin samples contaminated with S. Enteritidis and S. Typhimurium serotypes, and its activity against single and mixed Salmonella biofilms. Initially, effects of the post-chilling PAA application on chicken carcasses’ shelf life was analyzed. Secondly, the effectiveness of PAA application in chicken neck skin samples which are experimentally contaminated was investigated. Then, biofilm forming capacity of Salmonella enterica serovars were determined, and PAA activity against single and mixed Salmonella biofilms was evaluated. According to the results, in all experimental groups at least 1 log cfu/g reduction was observed on the day of PAA application (0 hour), and we monitored significant decreases of Salmonella counts in all groups after both 100 and 200 ppm PAA treatments within the 6th hour. The combinations of PAA concentrations and duration of application used in the study were insufficient in terms of S. Typhimurium and S. Enteritidis counts in chicken neck skin samples; however, these treatments can be effective on extending the chicken meat’s shelf life. On the other hand, 200 ppm of PAA was effective in reducing S. Typhimurium and S. Enteritidis biofilms. As a mean of 4.8 log/ml reduction were detected against S. Enteritidis and S. Typhimurium biofilms. Moreover, we can conclude from statistical analysis that when biofilm is composed with more than one Salmonella, it is harder to reduce their counts with PAA treatments. However, there is a recommendation of EFSA (European Food Safety Authority) that PAA may be a decontamination agent in poultry production in the future, considering that PAA will not have toxic effects on human health. PAA studies on this subject will be of great importance in the future if it is passed to legislation.

Article Details
  • Section
  • Research Articles
Downloads
Download data is not yet available.
Author Biographies
Bahar Onaran Acar, Ankara University, Faculty of Veterinary Medicine
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Ankara University, 06110, Ankara
Gorkem Cengiz, Ankara University, Faculty of Veterinary Medicine
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Ankara University, 06110, Ankara
Erman Gulendag, Ankara University, Faculty of Veterinary Medicine
Department of Biostatistics, Faculty of Veterinary Medicine, Ankara University, 06110, Ankara
Muammer Goncuoglu, Ankara University, Faculty of Veterinary Medicine
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Ankara University, 06110, Ankara
K. Serdar Diker, Adnan Menderes University, Faculty of Veterinary Medicine

Department of Microbiolgy, Faculty of Veterinary Medicine, Adnan Menderes University, Aydin, Turkey

References
Alonso-Hernando A, Guevara-Franco JA, Alonso-Calleja C, Capita R (2013) Effect of the temperature of the dipping solution on the antimicrobial effectiveness of various chemical decontaminants against pathogenic and spoilage bacteria on poultry. J Food Protect 76(5): 833-842.
Anonymous (1991) ISO-International Standard Organization. Microbiology - General guidance for the enumeration of coliforms - Colony counttechnique 4832:1991(E).
Anonymous (2003a) FAO-Food and Agriculture Organization of the United Nations. Assuring Food Safety and Quality: Guidelines for Strengthening National Food Control Systems. FAO Food and Nutrition Paper 76. http://www.fao.org/3/a-y8705e.pdf [accessed 22 January 2021].
Anonymous (2003b) ISO-International Standard Organization. Microbiology of food and animal feding stuffs — Preparation of test samples, initial suspension and decimal dilutions for microbiological examination —Part 2: Specific rules for the preparation of meat and meat products 6887-2: 2003(E). https://www.iso.org/standard/29866.html [accessed 28 January 2021].
Anonymous (2003c) ISO-International Standard Organization. Microbiology of food and animal feding stuffs — Horizontal method for the enumeration of microorganisms —Colony-count technique at 30 °C 4833:2003(E). https://www.iso.org/standard/34524.html [accessed 28 January 2021].
Anonymous (2004) ISO-International Standard Organization.Microbiology of food and animal feding stuffs — Horizontal methods for the detection and enumeration of Enterobacteriaceae — Part 2:Colony-count method 21528-2:2004(E). https://www.iso.org/standard/34566.html [accessed 29 January 2021].
Anonymous (2007) EC/2007/646 Commission Regulation of 12 June 2007 implementing Regulation (EC) No 2160/2003 of the European Parliament and of the Council as regards a Community target for the reduction of the prevalence of Salmonella Enteritidis and Salmonella Typhimurium in broilers and repealing Regulation (EC) No 1091/2005. https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:02007R0646-20080701&from=en [accessed 29 January 2021].
Anonymous (2009) EC/2009/121 Council Decision of 18 December 2008 rejecting the proposal from the Commission for a Council Regulation implementing Regulation (EC) No. 853/2004 of the European Parliament and of the Council as regards the use of antimicrobial substances to remove surface contamination from poultry carcasses. https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32009D0121&from=EN [accessed 29 January 2021].
Anonymous (2014) EFSA. Scientific Opinion on the evaluation of the safety and efficacy of peroxyacetic acid solutions for reduction of pathogens on poultry carcasses and meat. EFSA J. 12(3):3599.
Anonymous (2016) CDC-Centers for Disease Control and Prevention. National Salmonella Surveillance 2016. Salmonella Serotypes Isolated from Animals and Related Sources. https://www.cdc.gov/nationalsurveillance/pdfs/salmonella-serotypes-isolated-animals-and-related-sources-508.pdf [accessed 29 January 2021].
Anonymous (2017) ISO-International Standard Organization. Microbiology of the food chain — Horizontal method for the detection, enumeration and serotyping of Salmonella — Part 1: Detection of Salmonella spp. 6579-1:2017 (E). https://www.iso.org/standard/56712.html [accessed 29 January 2021].
Anonymous (2019) USDA-FSIS. Safe And Suitable Ingredients Used In The Production Of Meat, Poultry, and Egg Products. Directive 7120.1 Rev. 52. https://www.fsis.usda.gov/wps/portal/fsis/topics/regulations/directives/7000-series/safe-suitable-ingredients-related-document [accessed 29 January 2021].
Antunes P, Mourão J, Campos J, Peixe L (2016) Salmonellosis: the role of poultry meat. Clin Microbiol Infect 22(2), 110-121.
Bauermeister, L. (2015) Evaluation of poultry meat safety and quality using peracetic acid in poultry chillers (Doctoral dissertation).
Chen XI, Bauermeister LJ, Hill GN, Singh M, Bilgili SF, McKee SR (2014) Efficacy of various antimicrobials on reduction of Salmonella and Campylobacter and quality attributes of ground chicken obtained from poultry parts treated in a postchill decontamination tank. J Food Protect 77(11):1882-1888.
Chylkova T, Cadena M, Ferreiro A, Pitesky M (2017) Susceptibility of Salmonella biofilm and planktonic bacteria to common disinfectant agents used in poultry processing. J Food Protect 80(7):1072-1079.
Davidson PM, Taylor TM, Schmidt SE (2013) Chemical preservatives and natural antimicrobial compounds. In: Food Microbiology. ASM Press, Washington: pp 765-801.
del Río E, Panizo-Morán M, Prieto M, Alonso-Calleja C, Capita R (2007) Effect of various chemical decontamination treatments on natural microflora and sensory characteristics of poultry. Int J Food Microbiol 115(3):268-280.
Diez-Garcia M, Capita R, Alonso-Calleja C (2012) Influence of serotype on the growth kinetics and the ability to form biofilms of Salmonella isolates from poultry. Food Microbiol 31(2):173-180.
Foster JW, Hall HK (1990) Adaptative acidification tolerance response of Salmonella Typhimurium. J Bacteriol 172:771-778.
González-Aguilar G, Ayala-Zavala JF, Chaidez-Quiroz C, Heredia JB, Castro-del Campo N (2012) 12 Peroxyacetic acid. In: Decontamination of fresh and minimally processed produce. Wiley-Blackwell, New Jersey: pp 215-223.
Iñiguez-Moreno M, Gutiérrez-Lomelí M, Guerrero-Medina PJ, Avila-Novoa MG (2018) Biofilm formation by Staphylococcus aureus and Salmonella spp. under mono and dual-species conditions and their sensitivity to cetrimonium bromide, peracetic acid and sodium hypochlorite. Brazilian J Microbiol 49(2):310-319.
Joseph B, Otta SK, Karunasagar I, Karunasagar I (2001) Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol 64(3):367-372.
Lianou A, Koutsoumanis KP (2012) Strain variability of the biofilm-forming ability of Salmonella enterica under various environmental conditions. Int J Food Microbiol 160(2):171-178.
Mani-Lopez E, Garcia H.S, Lopez-Malo A (2012) Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res Int 45:713-721.
Meredith H, Walsh D, McDowell DA, Bolton DJ (2013) An investigation of the immediate and storage effects of chemical treatments on Campylobacter and sensory characteristics of poultry meat. Int J Food Microbiol 166(2):309-315.
Moore A, Nannapaneni R, Kiess A, Sharma CS (2017) Evaluation of USDA approved antimicrobials on the reduction of Salmonella and Campylobacter in ground chicken frames and their effect on meat quality. Poultry Sci 96(7):2385-2392.
Nagel GM, Bauermeister LJ, Bratcher CL, Singh M, McKee SR (2013) Salmonella and Campylobacter reduction and quality characteristics of poultry carcasses treated with various antimicrobials in a post-chill immersion tank. Int J Food Microbiol 165:281–286.
Nguyen HDN, Yuk HG (2013) Changes in resistance of Salmonella Typhimurium biofilms formed under various conditions to industrial sanitizers. Food Control 29(1):236-240.
Park S, Harrison MA, Berrang ME (2017) Postchill antimicrobial treatments to control Salmonella, Listeria, and Campylobacter contamination on chicken skin used in ground chicken. J Food Prot 80(5):857-862.
Purnell G, James C, James SJ, Howell M, Corry JE (2014) Comparison of acidified sodium chlorite, chlorine dioxide, peroxyacetic acid and tri-sodium phosphate spray washes for decontamination of chicken carcasses. Food Bioprocess Technol 7(7):2093-2101.
Ramirez-Hernandez A, Brashears MM, Sanchez-Plata MX (2018) Efficacy of lactic acid, lactic acid–acetic acid blends, and peracetic acid to reduce Salmonella on chicken parts under simulated commercial processing conditions. J Food Protect 81(1):17-24.
Scott BR, Yang X, Geornaras I, Delmore RJ, Woerner DR, Reagan JO, Morgan JB, Belk KE (2015) Antimicrobial efficacy of a sulfuric acid and sodium sulfate blend, peroxyacetic acid, and cetylpyridinium chloride against Salmonella on inoculated chicken wings. J Food Protect 78(11):1967-1972.
Singh P, Hung YC, Qi H (2018) Efficacy of peracetic acid in inactivating foodborne pathogens on fresh produce surface. J Food Sci 83(2): 432-439.
Steenackers H, Hermans K, Vanderleyden J, De Keersmaecker SC (2012) Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Res Int 45(2):502-531.
Stepanović S, Ćirković I, Ranin L, S✓vabić‐Vlahović M (2004) Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 38(5):428-432.
Tamblyn KC, Conner DE (1997) Bactericidal activity of organic acids against Salmonella Typhimurium attached to broiler chicken skin? J Food Prot 60:629-633.
Tamblyn KC, Conner DE, Bilgili SF (1997) Utilization of the skin attachment model to determine the antibacterial efficacy of potential carcass treatments. Poult Sci 76:1318–1323.
Walsh RJ, White B, Hunker L, Leishman O, Hilgren J, Klein D (2018) Peracetic Acid and Hydrogen Peroxide Post-dip Decay Kinetics on Red Meat and Poultry. Food Prot Trends 38(2):96-103.
Young JF, Karlsson AH, Henckel P (2004) Water-holding capacity in chicken breast muscle is enhanced by pyruvate and reduced by creatine supplements. Poult Sci 83(3):400–405.
Zhang L, Garner LJ, McKee SR, Bilgili SF (2018) Effectiveness of several antimicrobials used in a postchill decontamination tank against Salmonella and Campylobacter on broiler carcass parts. J Food Prot 81(7):1134-1141.