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International Journal of Food Microbiology
journal homepage: www.elsevier.com/locate/ijfoodmicro
Investigating the infuence of organic acid marinades, storage temperature
and time on the survival/inactivation interface of Salmonella on chicken
breast fllets
Anastasia E. Lytou
a
, Konstantinos Tzortzinis
a
, Panagiotis N. Skandamis
b
,
George-John E. Nychas
a,
⁎
, Efstathios Z. Panagou
a
a
Laboratory of Microbiology and Biotechnology of Foods, Department of Food Science and Human Nutrition, Faculty of Foods, Biotechnology and Development,
Agricultural University of Athens (AUA), Iera Odos 75, Athens 11855, Greece
b
Laboratory of Food Quality Control & Hygiene, Department of Food Science and Human Nutrition, Faculty of Foods, Biotechnology and Development, Agricultural
University of Athens (AUA), Iera Odos 75, Athens 11855, Greece
ARTICLEINFO
Keywords:
Inactivation probability
Acidic marination
Serotype persistence
Poultry meat
Pathogenic bacteria
ABSTRACT
The aim of this work was to study the infuence of lemon and vinegar marinades on Salmonella inoculated on
chicken fllets and stored under diferent storage temperatures for nine days in the presence of indigenous
microbiota. In addition to this, model development for the determination of the inactivation boundaries and the
prediction of pathogens response was attempted. The diferent acid concentrations in the marinades, the type of
acid, the storage temperature as well as the duration of storage impacted the levels of pathogens and background
fora. The higher tested concentrations (2% and 4% v/v for acetic and citric acid) were more efective against
Salmonella and spoilage microorganisms than the lower ones (0.5 and 1% v/v for acetic and citric acid), while
the intermediate concentrations (1, 1.5 and 2, 3% v/v for acetic and citric acid, respectively) presented dif-
ferentiations of particular interest to the microbial responses to acidic stress. The aforementioned parameters
also diferentiated Salmonella serovars persistence and spoilage microorganisms dominance. Regarding model
development, the probability of inactivation of Salmonella was satisfactorily predicted particularly in the case of
acetic acid marination while in model validation, the majority of the vinegar marinated samples were correctly
classifed, whereas, in case of lemon marination, a higher number of misclassifcations was observed, indicating
a partial weakness of the model to predict the pathogens response at interface concentrations.
1. Introduction
Salmonella is recognized as one of the most prevalent foodborne
pathogens linked to several outbreaks. In 2016, a number of 94,530
confrmed salmonellosis cases were reported by the European Union.
Although infections caused by Salmonella have been declining since
2008, in recent years (2012–2016) this decreasing trend has been sta-
bilized. Specifcally in 2016, the number of reported cases has been
slightly increased according to the European Centre for Disease
Prevention and Control (ECDC) and the European Food Safety
Authority (EFSA) (EFSA, 2017). The most widespread serovar of the
pathogen is Salmonella enterica subsp. enterica ser. Enteritidis or Sal-
monella Enteritidis in short (Brenner et al., 2000) followed by Salmo-
nella Typhimurium, Salmonella Infantis and Salmonella Derby (EFSA,
2017). Among the products with the highest level of non-compliance
with Salmonella food safety criteria are ready-to-cook poultry meat
preparations, including marinated chicken products (EFSA, 2017).
Marination is a food preparation process that could contribute to the
mitigation of this issue by using marinades containing ingredients with
antimicrobial activity. Previous studies have reported the efectiveness
of several marinades that contained wine, soy sauce, essential oils or
spices mixtures on decreasing either pathogen population such as
Salmonella (Rhoades et al., 2013; Pathania et al., 2010; Nisiotou et al.,
2013) and Campylobacter (Isohanni et al., 2010; Zakarienė et al., 2015)
or extending the shelf life (Kargiotou et al., 2011; Karam et al., 2019).
Marinade formulations containing organic acids could also have a sig-
nifcant impact on growth, inhibition or even inactivation of spoilage
and pathogenic microorganisms of meat, while at the same time bal-
ancing the odor and favor due to the presence of a variety of other
ingredients, resulting in desirable fnal products (Birk et al., 2010; Yang
https://doi.org/10.1016/j.ijfoodmicro.2019.03.019
Received 30 September 2018; Received in revised form 8 February 2019; Accepted 29 March 2019
⁎
Corresponding author.
E-mail address: gjn@aua.gr (G.-J.E. Nychas).
International Journal of Food Microbiology 299 (2019) 47–57
Available online 01 April 2019
0168-1605/ © 2019 Elsevier B.V. All rights reserved.
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