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- Cardinal parameter meta-regression models describing Listeria monocytogenes growth in brothPublication . Silva, Beatriz Nunes; Cadavez, Vasco; Teixeira, José; Ellouze, Mariem; Gonzales-Barron, UrsulaListeria monocytogenes has a high case-fatality rate, substantial research has been devoted to estimate its growth rate under different conditions of temperature, pH and water activity (aw). In this study, published findings on L. monocytogenes growth in broth were extracted and unified by constructing meta-regression models based on cardinal models for (i) temperature (CM[T]), (ii) temperature and pH (CM[T][pH]), and (iii) temperature, pH and aw (CM[T][pH][aw]). After assessing all the sources retrieved between 1988 until 2017, forty-nine primary studies were considered appropriate for inclusion. Apart from the modelling variables, study characteristics such as: type of broth (BHI, TSB, TPB), reading method (colony-forming-units, CFU; or binary-dilution optical density methods, OD), inoculum concentration and strain serotype, were also extracted. Meta-regressions based on CM[T] and CM[T][pH] were fitted on subsets of the 2009 growth rate measures and revealed that type of broth and reading method significantly modulated the cardinal parameter estimates. In the most parsimonious CM[T][pH][aw] meta-regression model, whereby the variability due to type of broth was extracted in a nested random-effects structure, the optimum growth rate μopt of L. monocytogenes was found to be lower when measured as CFU (0.947 log CFU/h; SE = 0.094 log CFU/h) than when measured as OD (1.289 log CFU/h; SE = 0.092 log CFU/h). Such a model produced the following cardinal estimates: Tmin = -1.273 °C (SE = 0.179 °C), Topt = 37.26 °C (SE = 0.688 °C), Tmax = 45.12 °C (SE = 0.013 °C), pHmin = 4.303 (SE = 0.014), pHopt = 7.085 (SE = 0.080), pHmax = 9.483 (SE = 0.080), aw min = 0.894 (SE = 0.002) and awopt = 0.995 (SE = 0.001). Integrating the outcomes from numerous L. monocytogenes growth experiments, this meta-analysis has estimated pooled cardinal parameters that can be used as reference values in quantitative risk assessment studies.
- Dynamic modelling to describe the effect of plant extracts and customised starter culture on Staphylococcus aureus survival in goat's raw milk soft cheesePublication . Silva, Beatriz Nunes; Coelho-Fernandes, Sara; Teixeira, José António; Cadavez, Vasco; Gonzales-Barron, UrsulaThis study characterises the effect of a customised starter culture (CSC) and plant extracts (lemon balm, sage, and spearmint) on Staphylococcus aureus (SA) and lactic acid bacteria (LAB) kinetics in goat's raw milk soft cheeses. Raw milk cheeses were produced with and without the CSC and plant extracts, and analysed for pH, SA, and LAB counts throughout ripening. The pH change over maturation was described by an empirical decay function. To assess the effect of each bio-preservative on SA, dynamic Bigelow-type models were adjusted, while their effect on LAB was evaluated by classical Huang models and dynamic Huang-Cardinal models. The models showed that the bio-preservatives decreased the time necessary for a one-log reduction but generally affected the cheese pH drop and SA decay rates (logD(ref) = 0.621-1.190 days; controls: 0.796-0.996 days). Spearmint and sage extracts affected the LAB specific growth rate (0.503 and 1.749 ln CFU/g day(-1); corresponding controls: 1.421 and 0.806 ln CFU/g day(-1)), while lemon balm showed no impact (p > 0.05). The Huang-Cardinal models uncovered different optimum specific growth rates of indigenous LAB (1.560-1.705 ln CFU/g day(-1)) and LAB of cheeses with CSC (0.979-1.198 ln CFU/g day(-1)). The models produced validate the potential of the tested bio-preservatives to reduce SA, while identifying the impact of such strategies on the fermentation process.
- In vitro antimicrobial activity of extracts and essential oils of Cinnamomum, Salvia, and Menthaspp. against foodborne pathogens: a meta‐analysis studyPublication . Ezzaky, Youssef; Elmoslih, Abdelkhaleq; Silva, Beatriz Nunes; Bonilla‐Luque, Olga María; Possas, Arícia; Valero, Antonio; Cadavez, Vasco; Gonzales-Barron, Ursula; Achemchem, FouadEssential oils (EOs) are a class of natural products that exhibit potent antimicrobial properties against a broad spectrum of bacteria. Inhibition diameters (IDs) and minimum inhibitory concentrations (MICs) are the typical measures of antimicrobial activity for extracts and EOs obtained from Cinnamomum, Salvia, and Mentha species. This study used a meta-analytical regression analysis to investigate the correlation between ID and MIC measurements and the variability in antimicrobial susceptibility tests. By utilizing pooled ID models, this study revealed significant differences in foodborne pathogens’ susceptibility to extracts, which were dependent on both the plant species and the methodology employed (p < .05). Cassia showed the highest efficacy against Salmonella spp., exhibiting a pooled ID of 26.24 mm, while cinnamon demonstrated the highest efficacy against Bacillus cereus, with a pooled ID of 23.35 mm. Mint extract showed the greatest efficacy against Escherichia coli and Staphylococcus aureus. Interestingly, cinnamon extract demonstrated the lowest effect against Shiga toxin-producing E. coli, with a pooled ID of only 8.07 mm, whereas its EOs were the most effective against this bacterial strain. The study found that plant species influenced the MIC, while the methodology did not affect MIC measurements (p > .05). An inverse correlation between ID and MIC measurements was identified (p < .0001). These findings suggest that extracts and EOs obtained from Cinnamomum, Salvia, and Mentha spp. have the potential to inhibit bacterial growth. The study highlights the importance of considering various factors that may influence ID and MIC measurements when assessing the effectiveness of antimicrobial agents.
- Chemical profiles and bioactivities of polyphenolic extracts of Lavandula stoechas L., Artemisia dracunculus L. and Ocimum basilicum LPublication . Silva, Beatriz Nunes; Cadavez, Vasco; Caleja, Cristina; Pereira, Eliana; Calhelha, Ricardo C.; Molina, Adriana K.; Finimundy, Tiane C.; Kostić, Marina; Soković, Marina; Teixeira, José António; Barros, Lillian; Gonzales-Barron, UrsulaThis study assessed the chemical profiles and bioactivities of the infusions, decoctions and hydroethanolic extracts of tarragon, basil and French lavender. The extracts were chemically characterised (HPLC-DAD-ESI/MS) and their bioactivities were evaluated in vitro. All extracts revealed antimicrobial, antifungal and antioxidant properties. French lavender extracts showed higher total phenolic content, regardless of the extraction method used, and antioxidant and antitumour capacities, but no anti-inflammatory action. All basil and two of the tarragon extracts revealed anti-inflammatory power. Thus, tarragon, basil and French lavender extracts may be considered for inclusion in foods, as preservatives or functional ingredients. Nonetheless, further studies must be conducted to evaluate the pharmacokinetic parameters of the bioactive compounds.
- Mild heat treatment and biopreservatives for artisanal raw milk cheeses: reducing microbial spoilage and extending shelf-life through thermisation, plant extracts and lactic acid bacteriaPublication . Silva, Beatriz Nunes; Teixeira, José António; Cadavez, Vasco; Gonzales-Barron, UrsulaThe microbial quality of raw milk artisanal cheeses is not always guaranteed due to the possible presence of pathogens in raw milk that can survive during manufacture and maturation. In this work, an overview of the existing information concerning lactic acid bacteria and plant extracts as antimicrobial agents is provided, as well as thermisation as a strategy to avoid pasteurisation and its negative impact on the sensory characteristics of artisanal cheeses. The mechanisms of antimicrobial action, advantages, limitations and, when applicable, relevant commercial applications are discussed. Plant extracts and lactic acid bacteria appear to be effective approaches to reduce microbial contamination in artisanal raw milk cheeses as a result of their constituents (for example, phenolic compounds in plant extracts), production of antimicrobial substances (such as organic acids and bacteriocins, in the case of lactic acid bacteria), or other mechanisms and their combinations. Thermisation was also confirmed as an effective heat inactivation strategy, causing the impairment of cellular structures and functions. This review also provides insight into the potential constraints of each of the approaches, hence pointing towards the direction of future research.
- Meta-analysis of antimicrobial activity of Allium, Ocimum, and Thymus spp. confirms their promising application for increasing food safetyPublication . Bonilla-Luque, Olga María; Silva, Beatriz Nunes; Ezzaky, Youssef; Possas, Arícia; Achemchem, Fouad; Cadavez, Vasco; Gonzales-Barron, Ursula; Valero, AntonioBiopreservation strategies such as the use of Mediterranean plant extracts to ensure food safety are promising to deal with the emergence of antimicrobial resistances and the overreliance on food chemical additives. In the last few decades, antimicrobial susceptibility testing (AST) for evaluating the in vitro antibacterial potential of plant extracts against the most relevant foodborne pathogens has been widely reported in the literature. The current meta-analysis aimed to summarise and analyse the extensive evidence available in the literature regarding the in vitro antimicrobial capability of Allium, Ocimum and Thymus spp. extracts against foodborne pathogens. A systematic review was carried out to gather data on AST results of these extracts against Listeria monocytogenes, Staphylococcus aureus, Salmonella spp., Escherichia coli and Bacillus cereus, including inhibition diameters (ID) and minimum inhibitory concentrations (MIC). A total of 742 records were gathered from a raw collection of 2,065 articles. Weighted mixed-effect linear models were adjusted to data to obtain pooled ID, pooled MIC and the relationship between both model estimations and observations. The pooled results revealed B. cereus as the most susceptible bacteria to Allium sativum (pooled ID = 20.64 ± 0.61 mm) by diffusion methods and S. aureus (pooled MIC = 0.146 mg/mL) by dilution methods. Diffusion methods did not yield conclusive results for Ocimum spp. extracts; however, the lowest pooled MIC was obtained for S. aureus (0.263 mg/mL). Among the foodborne pathogens evaluated, B. cereus showed the highest sensitivity to Thymus spp. extracts by both diffusion and dilution methods (pooled ID = 28.90 ± 2.34 mm and MIC = 0.075 mg/mL). The methodology used for plant extraction was found to not significantly affect MIC values (p > 0.05). Overall, the antimicrobial effectiveness of the studied extracts against Gram-positive and Gram-negative bacteria was demonstrated. Finally, the robustness of the meta-regression model was confirmed, also revealing an inversely proportional correlation between the ID and MIC measurements (p < 0.0001). These results provide a robust scientific basis on the factors affecting the in vitro antimicrobial efficacy of extracts from Mediterranean plants. They also provide valuable information for stakeholders involved in their industrial application in food, including producers, regulatory agencies and consumers which demand green-labelled foods.
- Meta-analysis of in vitro antimicrobial capacity of extracts and essential oils of Syzygium aromaticum, Citrus L. and Origanum L.: contrasting the results of different antimicrobial susceptibility methodsPublication . Silva, Beatriz Nunes; Bonilla-Luque, Olga María; Possas, Arícia; Ezzaky, Youssef; Elmoslih, Abdelkhaleq; Teixeira, José António; Achemchem, Fouad; Valero, Antonio; Cadavez, Vasco; Gonzales-Barron, UrsulaDiffusion methods, including agar disk-diffusion and agar well-diffusion, as well as dilution methods such as broth and agar dilution, are frequently employed to evaluate the antimicrobial capacity of extracts and essential oils (EOs) derived from Origanum L., Syzygium aromaticum, and Citrus L. The results are reported as inhibition diameters (IDs) and minimum inhibitory concentrations (MICs), respectively. In order to investigate potential sources of variability in antimicrobial susceptibility testing results and to assess whether a correlation exists between ID and MIC measurements, meta-analytical regression models were built using in vitro data obtained through a systematic literature search. The pooled ID models revealed varied bacterial susceptibilities to the extracts and in some cases, the plant species and methodology utilised impacted the measurements obtained (p < 0.05). Lemon and orange extracts were found to be most effective against E. coli (24.4 ± 1.21 and 16.5 ± 0.84 mm, respectively), while oregano extracts exhibited the highest level of effectiveness against B. cereus (22.3 ± 1.73 mm). Clove extracts were observed to be most effective against B. cereus and demonstrated the general trend that the well-diffusion method tends to produce higher ID (20.5 ± 1.36 mm) than the disk-diffusion method (16.3 ± 1.40 mm). Although the plant species had an impact on MIC, there is no evidence to suggest that the methodology employed had an effect on MIC (p > 0.05). The ID–MIC model revealed an inverse correlation (R2 = 47.7%) and highlighted the fact that the extract dose highly modulated the relationship (p < 0.0001). The findings of this study encourage the use of extracts and EOs derived from Origanum, Syzygium aromaticum, and Citrus to prevent bacterial growth. Additionally, this study underscores several variables that can impact ID and MIC measurements and expose the correlation between the two types of results.
- Meta-regression models describing the effects of essential oils and added lactic acid bacteria on pathogen inactivation in cheesePublication . Silva, Beatriz Nunes; Cadavez, Vasco; Teixeira, José; Gonzales-Barron, UrsulaBiopreservatives such as plant-based antimicrobials and bacteriocinogenic starter cultures have been proposed as hurdles to increase microbiological safety of a variety of products, including cheese, and numerous studies have reported their pathogen inhibitory properties. For that reason, the objective of this meta-analysis was to summarise the inactivation of Listeria monocytogenes (LM), Staphylococcus aureus (SA) and Salmonella spp. (SS) in cheese attained by added lactic acid bacteria (LAB) and essential oils (EOs); and to compare the inhibitory effectiveness by application mode and specific antimicrobial. After systematic review, 1810 observations on log reduction data and study characteristics were extracted from 53 studies. Comparing among the factual methods of application of antimicrobials (in milk, cheese surface and incorporated in films), meta-regression models pointed out that addition of EOs to milk renders, as a whole, the lowest inhibitory effect against LM, SA and SS in the finished product; whereas for added LAB, incorporation in milk prompts a faster inactivation of LM than onto cheese surface. Lemon balm, sage and basil EOs showed the best inhibitory outcomes against LM and SA; whereas clove, oregano and bay EOs presented the highest bactericidal effect against SS. For a given increase in EO concentration, the application on cheese surface provides the greatest inhibitory effect against LM and SS, while EO-embedded films lead to a more rapid inactivation during maturation/storage. The experimental practice of inoculating the antimicrobial in cheese mixture should no longer be employed in challenge studies, since the meta-regression models have demonstrated that this application method biases the results, overestimating or underestimating the inhibitory effects of EOs or added LAB, respectively. This meta-analysis has also emphasised the need to further investigate the relationship between pathogen's inoculum size and their concentrations in time.
- In vitro antimicrobial activity of extracts and essential oils of Cinnamomum, Salvia, and Menthaspp. against foodborne pathogens: a meta‐analysis studyPublication . Ezzaky, Youssef; Elmoslih, Abdelkhaleq; Silva, Beatriz Nunes; Bonilla‐Luque, Olga M.; Possas, Arícia; Valero, Antonio; Cadavez, Vasco; Gonzales-Barron, Ursula; Achemchem, FouadGenetic analysis of the honey bee spermathecal content can be particularly useful to provide an estimate of the genetic diversity and purity of the surrounding populations. Here we compared the concentration and quality of DNA extracted from queen spermatheca using four commercial kits to determine the best method to obtain DNA suitable for single nucleotide polymorphism genotyping by next-generation sequencing. The four kits were tested with different adjustments in the lysis incubation time, use of RNA-carrier, elution conditions and number of re-elutions. Only the use of QIAamp DNA Microkit with 3 h of lysis incubation, the addition of RNA-carrier and multiple re-elutions produced a DNA concentration over the required threshold.
- Lactic acid bacteria from artisanal raw goat milk cheeses: technological properties and antimicrobial potentialPublication . Silva, Beatriz Nunes; Fernandes, Nathália; Carvalho, Laís; Faria, Ana Sofia; Teixeira, José António; Rodrigues, Carina; Gonzales-Barron, Ursula; Cadavez, VascoIn cheese-making, a starter culture composed of adequately chosen lactic acid bacteria (LAB) may be suitable to ensure the rapid acidification of milk, improve textural and sensory characteristics, and avoid pathogen proliferation. In this work, 232 LAB isolates collected from artisanal goat’s raw milk cheeses produced in Portugal were evaluated for their antimicrobial capacity (at 10 and 37°C), as well as their acidifying and proteolytic properties. Among the 232 isolates, at least 98% of those isolated in De Man- Rogosa-Sharpe (MRS) agar presented antagonism against Listeria monocytogenes, Salmonella Typhimurium, or Staphylococcus aureus, whereas less than 28.1% of M17-isolated LAB showed antagonism against these pathogens. M17-isolated LAB displayed better results than MRS ones in terms of acidifying capacity. As for the proteolytic assay, only 2 MRS isolates showed casein hydrolysis capacity. Principal component analyses and molecular characterization of a subset of selected isolates were conducted to identify those with promising capacities and to correlate the identified LAB genera and species with their antimicrobial, acidifying, and/or proteolytic properties. Lactococcus strains were associated with the highest acidifying capacity, whereas Leuconostoc and Lacticaseibacillus strains were more related to antimicrobial capacities. Leuconostoc mesenteroides, Lactococcus lactis, and Lacticaseibacillus paracasei were the predominant organisms found. The results of this work highlight various strains with pathogen inhibition capacity and suitable technological properties to be included in a customized starter culture. In future work, it is necessary to appropriately define the starter culture and implement it in the cheese-making process to evaluate if the in-vitro capacities are observable in a real food system.
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