Meta-Regression models describing the effects of essential oils and added lactic acid bacteria on pathogen inactivation in cheese
Introduction
Listeria monocytogenes (LM), Staphylococcus aureus (SA) and Salmonella spp. (SS) are some of the most common bacterial agents causing foodborne illnesses and are found in numerous food matrices, including different types of cheeses (Iannetti et al., 2016; Jackson et al., 2018; Rosengren et al., 2010; Kousta et al., 2010; Cremonesi et al., 2007; Almeida et al., 2007; Tekinşen and Özdemir, 2006; Cunha‐Neto et al., 2019; Elafify et al., 2019). A recent meta-analysis showed pooled prevalence of 12.8% for LM and 16% for SA in goat raw milk cheeses, while the prevalence of SS was lower (5.91%), but still concerning (Gonzales-Barron et al., 2017). LM and SS can cause illnesses even when in low numbers in any food product, including cheese (United States Food and Drug Administration 2003). On the other hand, a larger number of SA (above 105 log CFU/g) is required for this pathogen to be able to produce enterotoxins and impose a serious health threat (Duquenne et al., 2010). Nevertheless, SA imposes an important contamination issue since, even at low initial contamination levels, many factors can contribute to SA growth to a sufficiently high concentration that enables enterotoxin production in the curd/cheese (Paulin et al., 2012). Overall, soft and semi-soft cheeses made from different milk kinds and types (pasteurised, raw or low-heat-treated; and from cows, goats, sheep, etc.) sampled at retail level have revealed non-satisfactory results in terms of pathogen contamination by pathogens (EFSA and ECDC, 2018) thus underscoring the importance of improving the safety of cheeses to reduce the occurrence of pathogens.
Biopreservatives such as bacteriocinogenic lactic acid bacteria (LAB) used in starter cultures, and plant-based antimicrobials such as essential oils (EOs) are hurdles used to increase the microbiological safety of cheeses. The microbial inhibition offered by bacteriocinogenic LAB is mostly due to competition for substrates, production of antimicrobial substances (bacteriocins), production of organic acids that drop the pH during fermentation, and production of other non-proteinaceous compounds such as H2O2 (Tulini, 2014). The mechanism of action of EOs include a series of events on the cell surface, and, consequently, within the cytoplasm (Nazzaro et al., 2013). Modifications of membrane permeability and compromised transport of molecules can lead to degradation of the cell wall (damaging the cytoplasmic membrane), increased permeability (causing the leakage of cell contents), denaturation of enzymes and cellular proteins, loss of metabolites and ions (Nazzaro et al., 2013), and cytoplasm coagulation (Nazzaro et al., 2013; Gustafson et al., 1998).
Over the past years, several authors have performed challenge studies of foodborne pathogens inoculated in milk or cheese to assess the antimicrobial capacity of functional starter cultures or selected LAB (Ibrahim and Awad, 2018; Campagnollo et al., 2018; Atanasova et al., 2014) and plant-based antimicrobials (Artiga-Artigas et al., 2017; Wahba et al., 2010; Menon and Garg, 2001; Tehrani and Sadeghi, 2015; Dannenberg et al., 2016). Thus, a meta-analysis of the published results on the effect of antimicrobial biopreservatives will help evaluate their usefulness to control foodborne pathogens in cheeses (Xavier et al., 2014); and more specifically, compare the effectiveness of the different biopreservatives and modes of application. In this meta-regression study, the population is defined as cheeses with added lactic acid bacteria or essential oils, and the measured outcome is the mean log reduction of pathogens. This study aims to deliver an insight on the effects of biopreservation methods in cheese for the optimisation of these hurdle technologies to improve the safety of cheeses.
Section snippets
Data collection and description of the data set
Electronic literature search was carried out in Scopus, PubMed and Web of Science databases to find original and review articles, published since 2000, summarising biopreservation methods currently tested and/or applied in cheese-making and their efficiencies against pathogens. The search was done systematically and aimed to find quality studies validated by the scientific community.
The bibliographic searches were conducted by properly applying the AND and OR logical connectors to combine terms
Results and discussion
The results of the analysis of variance of the five meta-regression models adjusted are presented in Table 3. The EOs-SA model allowed for the inclusion of the highest number of moderating variables. The EOs-LM model does not contain inoculum level as fixed effect since this term reveal to be non-significant (p = 0.627). The EOs-SS model did not include storage temperature, nor inoculum level, as the first variable had only two levels (data was collected at either 4 or 10 °C) and the second
Conclusion
Literature data was used to build meta-analytical regression models capable of summarising the reduction in LM, SA and SS populations in cheese attained by added LAB and EOs; and elucidating inhibitory effectiveness by application mode and specific antimicrobial. These meta-regressions showed that the effectiveness of added LAB and EOs were regulated by storage temperature, exposure time, pathogen's inoculum size, antimicrobial concentration and method of application of the biopreservative
CRediT authorship contribution statement
Beatriz Nunes Silva: Data curation, Formal analysis, Investigation, Writing - original draft, Validation. Vasco Cadavez: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Writing - review & editing, Software, Resources, Supervision. José António Teixeira: Project administration, Writing - review & editing, Supervision. Ursula Gonzales-Barron: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project
Declaration of Competing Interests
None
Acknowledgements
The authors are grateful to EU PRIMA programme and the Portuguese Foundation for Science and Technology (FCT) for funding the ArtiSane Food project (PRIMA/0001/2018). This study was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UIDB/04469/2020 unit and BioTecNorte operation (NORTE-01–0145-FEDER-000004) funded by the European Regional Development Fund under the scope of Norte2020 - Programa Operacional Regional do Norte. Ms.
References (80)
- et al.
Smearing of soft cheese with Enterococcus faecium WHE 81, a multi-bacteriocin producer, against Listeria monocytogenes
Food Microbiol
(2009) - et al.
Control of Listeria monocytogenes in goat’s milk and goat’s Jben by the bacteriocinogenic Enterococcus faecium F58 strain
J. Food Prot.
(2006) Microbiological characterization of randomly selected Portuguese raw milk cheeses with reference to food safety
J. Food Prot.
(2007)- et al.
Control of Listeria monocytogenes in fresh cheese using protective lactic acid bacteria
Int. J. Food Microbiol.
(2014) - et al.
Meta-analysis of the incidence of foodborne pathogens in Portuguese meats and their products
Food Res. Int.
(2014) Effects of the essential oil from Origanum vulgare L. on survival of pathogenic bacteria and starter lactic acid bacteria in semihard cheese broth and slurry
J. Food Prot
(2016)- et al.
Soft cheese supplemented with black cumin oil: impact on food borne pathogens and quality during storage
Saudi J. Biol. Sci.
(2014) Listeria monocytogenes in ready-to-eat foods in Italy: prevalence of contamination at retail and characterisation of strains from meat products and cheese
Food Control
(2016)- et al.
An explanation for the effect of inoculum size on MIC and the growth/no growth interface
Int. J. Food Microbiol.
(2008) - et al.
Response surface models for the growth kinetics of Escherichia coli O157:H7
Food Microbiol.
(1993)