Lipids, pH, and Their Interaction Affect the Inhibitory Effects of Carvacrol against Salmonella Typhimurium PT4 and Escherichia coli O157:H7

Abstract

Although carvacrol (CAR) is considered an alternative antimicrobial for use in food, few is known about the influence of food-related parameters on its inhibitory effects against pathogens. This study assessed the influence of different amounts of proteins, using beef extract (BE) as a protein-rich source, lipids (LIP), using sunflower oil as a LIP-rich source, and pH values or their interaction on the inhibitory effects of CAR against Salmonella Typhimurium PT4 (ST) and Escherichia coli O157:H7 (EC). The specific maximum growth rate (μmax) and lag phase duration (λ) of the test pathogens when exposed to CAR in media with different amounts of BE (4, 6, and 8 g/100 mL), LIP (3.75, 5, and 6.25 mL/100 mL), and pH values (5, 5.5, and 6) were determined. The viable counts of the tested pathogens in media that promoted the highest and lowest μmax in the presence of CAR were monitored during 24 h. The lowest μmax of ST and EC exposed to 2.4 μL/mL (-1.29 and -0.82 log CFU/mL/h, respectively) or 4.8 μL/mL CAR (-1.44 and -2.17 log CFU/mL/h, respectively) were observed in media with the highest LIP amount (6.25 mL/100 mL) and pH value (pH 6). For both SE and EC, the longest λ (> 2 h) was verified in media where these pathogens showed the lowest μmax. These data indicate that the concomitant increase in LIP amounts and pH values affected positively the CAR inhibitory effects against the target pathogens. CAR (2.4 or 4.8 μL/mL) failed to inhibit the increase in ST and EC counts in media where the highest μmax values were previously observed. On the contrary, CAR inhibited the increase of ST counts (final counts 5 log CFU/mL) and decreased the EC counts (final counts 3.5 log CFU/mL) in media where the lowest μmax values were observed. These results show that the inhibitory effects of CAR on ST and EC in food matrices could be affected as a function of the interaction of LIP amounts and pH values.

Modeling Salmonella ( S . Typhimurium ATCC14028, ATCC 13311, S . Typhi ATCC 19430, and S. enterica ) and Listeria ( L. monocytogenes Scott A, ATCC 7644, and CDBB‐B‐1426) cocktails’ survival under the effects of pH, protein, and essential oil concentration

“…In our case, it was observed that for Salmonella cocktails, the efficacy of oregano EO increased at a higher pH (6.5). A similar behavior was observed by Carvalho et al (2018), who reported that increasing pH values (6.0, as opposed to 5.0 or 5.5) in combination with an increase in lipids (6.25 ml/100 ml as opposed to 3.75 or 5.00 ml/100 ml) had a positive effect on the inhibitory effects of carvacrol against S . Typhimurium and E. coli .…”

“…Even when EOs have been proven useful for the control of pathogenic bacteria in vitro, their effectiveness in food products may be hindered by the interaction of their constituents with food matrix components and/or physicochemical parameters (Boskovic et al, 2013; de Carvalho et al, 2015; Firouzi, Shekarforoush, Nazer, Borumand, & Jooyandeh, 2007; Gill, Delaquis, Russo, & Holley, 2002; Gutierrez, Barry‐Ryan, & Bourke, 2009; Hyldgaard et al, 2012; Tassou, Drosinos, & Nychas, 1995; Tserennadmid et al, 2010; Veldhuizen, Creutzberg, Burt, & Haagsman, 2007). In this viewpoint, food model media, where components and parameters can be controlled, are useful to investigate the interaction of EOs with given food components, and thus, give a quick assessment of the type of food products where an EO can be utilized (Carvalho, de Jesus Medeiros, Chaves, de Souza, & Magnani, 2018; Hyldgaard et al, 2012). Previous studies suggest that lipid concentrations above 5% will have strong effects on the effectiveness of essential oils or their components on bacterial growth.…”

“…Previous studies suggest that lipid concentrations above 5% will have strong effects on the effectiveness of essential oils or their components on bacterial growth. Some authors have observed an enhancement of effectiveness at levels between 5.00 and 6.25 ml/100 ml (Carvalho et al, 2018), while others report a negative influence on the antimicrobial activity of essential oils at even higher lipid concentrations: 10% (Gutierrez, Barry‐Ryan & Bourke, 2008), 26% (Singh, Singh, Bhunia, & Singh, 2003), and 50% (Chen, Golden, Critzer, & Davidson, 2015). Since, according data taken from PROFECO (2016; 2013), the lipid content of commercial and economical turkey hams sold in Mexico is in average 3.2 ± 1.3 and 3.0 ± 1.2 g/100 g, respectively; it was decided to not consider lipid content for the present study.…”

Modeling dependence of growth inhibition of Salmonella Typhimurium and Listeria monocytogenes by oregano or thyme essential oils on the chemical composition of minced pork

“…A common suggestion is that the increased fat content decreases the efficiency of EOs as they dissolve in fat, not affecting the bacteria that reside in the aqueous phase of food (Burt, 2004). This hypothesis has been supported by the results of several studies involving a laboratory medium with sunflower oil (Carvalho, de Jesus Medeiros, Chaves, de Souza, & Magnani, 2018; Gutierrez et al, 2008) and pork fat (García‐Díez et al, 2017), a comparison of low‐fat and high‐fat cheeses (Smith‐Palmer, Stewart, & Fyfe, 2001), fish (Mejlholm & Dalgaard, 2002) and hot dogs (Singh, Singh, Bhunia, & Singh, 2003). However, no complex study has been conducted to elucidate the extent to which the fat content decreases the antimicrobial effect of EOs in meat.…”

Efficacy assessment of various natural and organic antimicrobials against Escherichia coli O157:H7, Salmonella enteritidis and Listeria monocytogenes

“…Our work confirmed a different degree of inhibition against tested strains. In 2018, a recent study supported this opinion describing that different physical, chemical factors, and their interaction influence the inhibitive effect of the natural antimicrobial compound against salmonella Typhimurium PT4 and E. coli O157:H7 (Carvalho et al 2018).…”