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Effects and interactions of gallic acid, eugenol and temperature on thermal inactivation of Salmonella spp. in ground chicken
Abstract
The combined effects of heating temperature (55 to 65 °C), gallic acid (0 to 2.0%), and eugenol (0 to 2.0%) on thermal inactivation of Salmonella in ground chicken were assessed. Thermal death times were determined in bags submerged in a heated water bath maintained at various set temperatures, following a central composite design. The recovery medium was tryptic soy agar supplemented with 0.6% yeast extract and 1% sodium pyruvate. D-values were analyzed by second-order response surface regression for temperature, gallic acid, and eugenol. The observed D-values for chicken with no gallic acid or eugenol at 55, 57.5, 60, 62.5, and 65 °C were 21.85, 5.43, 2.83, 0.58, and 0.26 min, respectively. A second-order polynomial model developed to inactivate Salmonella was found to be significant (p < 0.0001) with a R² = 0.95 and a no significant lack of fit (p > 0.1073). Efficacy of the additives in increasing the sensitivity of the pathogen to heat was concentration dependent. The model developed in this study can be used by processors to design appropriate thermal process to inactivate Salmonella in chicken products used in the study and thereby, ensuring an adequate degree of protection against risks associated with the pathogen.
... The cost of detection, prevention and treatment of Salmonella related diseases has increased the economic burden of industrialized and developing countries (Crump et al., 2008). Among the over 2600 serotypes of Salmonella, Salmonella Typhimurium and Salmonella Enteritidis are the most common serotypes associated with human infection, which can lead to a variety of diseases (López-Romero et al., 2018). Antibiotics, such as fluoroquinolones and cephalosporin are commonly used in the treatment of Salmonella infection. ...
... Genomic DNA extraction was carried out by boiling method as described previously, with modifications (López-Romero et al., 2018) with modifications. 1.5 mL of the stationary phase S. enterica culture were harvested by centrifugation at 12,000 g for 2 min (Thermo Fisher Scientific, Shanghai, China). ...
Salmonella enterica is a foodborne pathogen that can cause zoonotic diseases. The aggravation of antibiotic resistant S. enterica has drawn wide attention. Understanding the behavior of antibiotic-resistant pathogens along food chain is important to risk assessment. The objective of this study was to describe the growth and survival characteristics of S. enterica strains and evaluate the correlation with the strains’ antibiotic resistance phenotypes. Strains isolated from food (n=16), clinic (n=8) and standard strain (n=2) of various antibiotic resistant phenotypes were selected, of which half strains were S. Typhimurium and half were S. Enteritidis. The growth parameters under different temperatures (25, 30, 35°C) were obtained by time-to-detection (TTD) method, the survival characteristics were evaluated by the viability after exposed to heat (55, 57.5, 60°C) and acid (HCl, pH=3.0). It was observed that the antibiotic-resistant strains were more heat sensitive than antibiotics-sensitive ones, although the difference was significant only at 57.5°C. The multi-antibiotics resistant strains showed significant higher acid resistance than antibiotics resistant ones. No significant differences were observed on growth and inactivation characteristics between strains of different origins or serotypes. This study provides useful information for understanding the correlation of antibiotic resistance phenotypes with growth and survival characteristics in S. enterica.
... In most of the articles, a D 90 or T 90 value (the time required to reduce the population by 90%) was reported (Spinks et al., 2006;Weiss and Hammes, 2005;Lang and Smith, 2008;Juneja et al., 2009;Soupir. et al., 2008;Stopforth et al., 2008;Aitken et al., 2007;Osaili et al., 2007;Aitken et al., 2005;Kenney and Beuchat, 2004;Juneja and Novak, 2003;Al-Holy et al., 2009;Tomat et al., 2015;Huertas et al., 2015;Elving et al., 2014;Juneja et al., 2012;Juneja et al., 2010a;Sharma et al., 2009;Kharel et al., 2018;Forghani et al., 2018;López-Romero et al., 2018;Karyotis et al., 2017;Vasan et al., 2013;Nygaard et al., 2012;Limcharoenchat et al., 2019;Linden and Murphy, 2017;Juneja et al., 2014;Luchansky et al., 2013;Syamaladevi et al., 2016;Burch and Thomas, 1998;Villa-Rojas et al., 2013;Palumbo et al., 1995). If this value was not reported, we calculated it using regression curves based on data reported in the paper. ...
... If this value was not reported, we calculated it using regression curves based on data reported in the paper. The majority of the data (61%) originated from experiments in food matrices (Palumbo et al., 1995;Osaili et al., 2007;Weiss and Hammes, 2005;Kenney and Beuchat, 2004;Juneja and Novak, 2003;Al-Holy et al., 2009;Tomat et al., 2015;Huertas et al., 2015;Mataragas et al., 2015;Juneja et al., 2012;Vidaček et al., 2011;Neetoo and Chen, 2011;Juneja et al., 2010a;Juneja et al., 2010b;Sharma et al., 2009;Kharel et al., 2018;Forghani et al., 2018;Taormina, 2014;López-Romero et al., 2018;Chandrakash and Davey, 2017;Karyotis et al., 2017;Park and Kang, 2013;Park et al., 2017;Shah et al., 2017;Syamaladevi et al., 2016;Becker et al., 2015;Weiss and Hammes, 2003;Luchansky et al., 2013;Vasan et al., 2013;Nygaard et al., 2012;Limcharoenchat et al., 2019;Kottapalli et al., 2019;Jeong et al., 2017;Cálix-lara et al., 2015;Juneja et al., 2014;Wiegand et al., 2009;McCann et al., 2006;Retzlaff et al., 2004;Juneja et al., 2009;Sow et al., 2011;Hosseini et al., 2017), though there were also data that originated from experiments in water, wastewater, compost, sludge, and other biosolids. A breakdown of the different matrices associated with the final extracted data table is shown in Fig. 2a. ...
Heat treatment, or thermal disinfection, is one of the simplest disinfection methods, and is widely used in the water, sanitation, and food sectors, especially in low resource settings. Pathogen reductions achieved during heat treatment are influenced by a combination of temperature and exposure time. The objective of this paper was to construct updated time-temperature pathogen inactivation curves to define “safety zones” for the reduction of four pathogen groups (bacteria, viruses, protozoan (oo)cysts, and helminth eggs) during heat treatment in a variety of matrices. A systematic review and meta-analysis were conducted to determine the times needed to achieve specified levels of pathogen reduction at different temperatures. Web of Science was searched using a Boolean string to target studies of heat treatment and pasteurization systems that exposed pathogens in water, wastewater, biosolids, soil, or food matrices to temperatures between 20 °C and 95 °C. Data were extracted from tables or figures and regression was used to assess the relationship between time and temperature. Our findings indicate that the temperatures and times needed to achieve a 1-log10 reduction of all pathogen groups are likely higher and longer, respectively, than previously reported. The type of microorganism and the matrix significantly impact T90 values reported at different temperatures. At high temperatures, the time-temperature curves are controlled by thermally stable viruses such as hepatitis A virus. Data gaps include the lack of data on protozoa, and the lack of data on all pathogen groups at low temperatures, for long exposure times, and with high log10 reductions. The findings from this study can be used by engineers, food safety specialists for the planning and design of engineered water, sanitation, and food pasteurization and treatment systems.
... in control samples without herbal extract. In previous studies, the z-values of Salmonella in chicken meat ranged from 5.34 to 8.88 C (Aviles et al., 2022;Juneja, Eblen, & Ransom, 2001;Karyotis et al., 2017;López-Romero et al., 2018;Mazzotta, 2000;Murphy et al., 2004;Osaili et al., 2006). Therefore, the z value of S. ...
Thermal death kinetics of Salmonella Enteritidis in ground chicken in the presence of ribwort, sorrel and yarrow extracts mixture (1%) was investigated by fitting the inactivation curves to the log–linear and Weibull models. The thermal inactivation curves were fitted well to both models (r² ≥ 0.94). The times required for 4–log reduction in the S. Enteritidis population were shortened by 47–64% in ground chicken supplemented with the herbal extract mixture (p < 0.05). The 4–log reduction times calculated using the Weibull model were 0.13–13.6% longer than those extrapolated with the log–linear model. The z values in the ground chicken samples with and without herbal extract were 5.08°C (r² = 0.97) and 5.57°C (r²= 0.94), respectively. The results suggest that the mixture of these extracts increased the thermal sensitivity of S. Enteritidis significantly at tested temperatures. In addition, using the Weibull model to calculate thermal death kinetics may reduce the underestimation of the thermal reduction times.
Practical applications
This research aimed to investigate the effects of an herbal extract mixture consisting of ribwort, sorrel, and yarrow on the thermal resistance of Salmonella Enteritidis in ground chicken. While these plants are recognized for their antimicrobial and antioxidant properties, there are not many studies conducted to explore their effects on foodborne pathogens in the food matrix. As far as we know, this is the first study that examines the impact of these plants on the thermal resistance of S. Enteritidis in ground chicken. We determined the thermal death kinetics of S. Enteritidis in ground chicken with and without the herbal extract mixture using curve fitting to log‐linear and Weibull models. The findings of this study could help the food industry to develop cooking conditions for Salmonella‐free chicken products.
... These findings indicate that the presence of Salmonella in the gut may negatively influence the overall health of the falcons by affecting the capacity to build and maintain protein mass, which is essential for flighted birds that engage in long-distance migrations. Moreover, small aromatic compounds such as gallic acid, 3-phenylpropionic acid, nicotinic acid, 4-methylcatechol, 3-hydroxycinnamate and their derivatives are known antimicrobials [80][81][82][83][84] and are known to have Salmonella inhibitory effects in humans [85]. The falcons in our study that harbored high levels of Salmonella showed enrichment of functional pathways that degrade these antimicrobial compounds. ...
The gut microbiome is increasingly being appreciated as a master regulator of animal health. However, avian gut microbiome studies commonly focus on birds of economic importance and the gut microbiomes of raptors remain underexplored. Here we examine the gut microbiota of 29 captive falcons—raptors of historic importance—in the context of avian evolution by sequencing the V4 region of the 16S rRNA gene. Our results reveal that evolutionary histories and diet are significantly associated with avian gut microbiota in general, whereas diet plays a major role in shaping the falcon gut microbiota. Multiple analyses revealed that gut microbial diversity, composition, and relative abundance of key diet-discriminating bacterial genera in the falcon gut closely resemble those of carnivorous raptors rather than those of their closest phylogenetic relatives. Furthermore, the falcon microbiota is dominated by Firmicutes and contains Salmonella at appreciable levels. Salmonella presence was associated with altered functional capacity of the falcon gut microbiota as its abundance is associated with depletion of multiple predicted metabolic pathways involved in protein mass buildup, muscle maintenance, and enrichment of antimicrobial compound degradation, thus increasing the pathogenic potential of the falcon gut. Our results point to the necessity of screening for Salmonella and other human pathogens in captive birds to safeguard both the health of falcons and individuals who come in contact with these birds.
... Both EU and CAR NE were stable for 1 month, except for a diameter increase of about 15-20 nm which might be negligible as shown in Fig. 2C. This infinitesimal increase in particle size might result from the superior resistance of PGU to gravitational separation and Ostwald ripening [29,30], and this droplet diameter variation has already been reported even for stable EO NE [31,48]. ...
The ultrasonically processed Eugenol (EU) and Carvacrol (CAR) nanoemulsions (NE) were successfully optimized via response surface methodology (RSM) to achieve broad spectrum antimicrobial efficacy. These NE were prepared using 2 % (w/w) purity gum ultra (i.e., succinylated starch), 10 % (v/v) oil phase, 80 % (800 W) sonication power, and 10 min of processing time as determined via RSM. The second order Polynomial method was suitable to RSM with a co-efficient of determination >0.90 and a narrow polydispersity index (PDI) ranging 0.12–0.19. NE had small droplet sizes (135.5–160 nm) and low volatility at high temperatures. The EU & CAR entrapment and heat stability (300 °C) confirmed by Fourier transform infrared spectroscopy (FTIR) and thermogravimetric analysis (TGA). Further, the volatility of EU & CAR NE was 18.18 ± 0.13 % and 12.29 ± 0.11 % respectively, being lower than that of bulk/unencapsulated EU & CAR (i.e., 23.48 ± 0.38 % and 19.11 ± 0.08 %) after 2 h at 90 °C. Interestingly, both EU & CAR NE showed sustained release behaviour till 48 h. Their digest could inhibit Salmonella typhimurium (S. typhimurium) via membrane disruption and access to cellular machinery as evident from SEM images. Furthermore, in-vivo bio-accessibility of EU & CAR in mice serum was up to 80 %. These cost-effective and short-processed EU/CAR NE have the potential as green preservatives for food industry.
... It has been documented that consumption of foods rich in GA, induced hypoglycemia and attenuate the health hazard effects in obese individuals (36). GA has been implicated as antioxidant (34), antibacterial (21) and antitumor (23) agents. In addition to its protection against myocardial infarction (19). ...
This study was aimed to explore the role of gallic acid (GA) in ameliorating in reducing adverse effects of cadmium chloride (CdCl2) on antioxidant status and lipid profile in adult male rats. Twenty-eight (28) adult male rats were divided randomly into four equal groups; they were daily handled for 30 days, as follows: control group (C), received tap water only. (G1), received 100ppm of CdCl2 in drinking tap water, animals in proceeding groups were given in addition to CdCl2 in drinking water the following: intraperitoneal injection of GA 100 mg/kg. daily (G2 group) and the combination of GA and CdCl2 were given to rats in group (G3) in the same pattern. At the end of the experiment, fasting blood samples were collected and serum was isolated for measuring of antioxidant status and lipid profile. The results showed that administration CdCl2 (G1 group) caused a case of dyslipidemia illustrated by significant elevation in serum cholesterol concentration in lipoprotein low density lipoprotein-cholesterol (LDL-C) and very low-density lipoprotein-cholesterol (VLDL-C), total cholesterol (TC), triglyceride (TAG) and non-HDL-C accompanied with significant decrease in cholesterol of high density lipoprotein (HDL-C) concentrations. The results also revealed a significant elevation in lipid indices including, coronary risk index (CRI), and cardiovascular risk index (CVRI) in CdCl2 exposed rats. While significant elevation in malondialdehyde (MDA) and reduction in (GSH) concentrations observed in the same group comparing to gallic acid and control group, indicating a case of oxidative stress. The current results also recorded that intraperitoneal injection of GA against CdCl2 caused amelioration of all previously estimated parameters.
... Carvacrol (CR) is a primary phenolic compound in oregano essential oil and possesses proven antimicrobial properties against Salmonella (Burt, 2004;Kollanoor Johny et al., 2010a,b;Moore-Neibel et al., 2012;Oladunjoye et al., 2013;Nair et al., 2014Nair et al., , 2015. Eugenol (EG) is the primary active compound in clove oil, and its antimicrobial efficacy against Salmonella has been previously demonstrated (Burt, 2004;Kollanoor Johny et al., 2010a,b;Nair et al., 2014;Kollanoor Johny et al., 2017;L opez-Romero et al., 2018;Ruengvisesh et al., 2019). However, limited studies have been conducted using these PDAs to control Salmonella during organic poultry processing. ...
Organic poultry constitutes a sizeable segment of the American organic commodities market. However, processors have limited strategies that are safe, effective, and approved for improving the microbiological safety of products. In this study, the efficacy of 3 plant-derived antimicrobials (PDAs), eugenol (EG), carvacrol (CR), and β-resorcylic acid (BR) was evaluated against Salmonella on organic chicken wings and carcasses. Wings inoculated with Salmonella (6 log10 CFU/wing) were treated with or without the treatments (BR [0.5%, 1% w/v], EG [0.5%, 1% v/v], CR [0.5%, 1% v/v], chlorine [CL; 200 ppm v/v], or peracetic acid [PA; 200 ppm v/v]) applied for 2 min at 54°C (scalding study) or 30 min at 4°C (chilling study). Homogenates and treatment water were evaluated for surviving Salmonella. Six wings or carcasses per treatment were analyzed in each study. All treatments, except CL and 0.5% BR in the scalding study, yielded significant reductions of Salmonella on wings compared to the positive control (PC-Salmonella inoculated samples not treated with antimicrobials). To follow, carcasses inoculated with Salmonella (higher inoculum [106 CFU/carcass] or lower inoculum [104 CFU/carcass]) and immersed in antimicrobials (CR 1% [v/v] and industry controls [CL {200 ppm}, or PA [200 ppm]) for 30 min at 4°C were stored until analysis. For the higher inoculum study, 1% CR resulted in a 3.9 log10 CFU/g reduction of Salmonella on the carcass on d 0 compared to PC (P < 0.05); however, CL yielded no reduction. On d 3, CR and PA resulted in 0.9 and 1.2 log10 CFU/g reduction of Salmonella, respectively (P < 0.05). For the lower inoculum study, consistent Salmonella reductions were obtained with CR and PA (1.4-2.1 log10 CFU/g) on d 0 and 7. High reductions of Salmonella in processing water were obtained in all studies. CR effectively controls Salmonella on wings and carcasses and in processing water immediately after application. Follow-up studies on the organoleptic characteristics of PDA-treated chicken carcasses are necessary.
... VA-containing food upon a thermal treatment had greater antioxidant and antimicrobial potential compared to non-VA-treated foods (Mourtzinos et al., 2009). EU up to 2%, along with up to 2% gallic acid, decreased the thermal resistance of Salmonella spp. in ground chicken compared to the control (López-Romero et al., 2018). Further studies using different EOs and various cooking methods are needed to develop more concrete conclusions. ...
The combined inhibitory effect of essential oils (EOs) with meat-based marinades has not been fully studied. Therefore, the present study aimed to gauge the effect of a yogurt-based marinade when individually combined with three EOs, namely eugenol (EU), vanillin (VA) or β-resorcylic acid (BR) on camel meat cubes inoculated with Listeria monocytogenes, Salmonella spp., and Escherichia coli O157:H7 during storage. Fresh camel meat cubes of 10 g were inoculated with bacteria and dipped in the mixture of marinade and EO. Overall, the study had 6 EO treatments (EU 0.5%, EU 1%, VA 0.5%, VA 1%, BR 0.5%, BR 1%) and two controls (meat without marinade and marinated meat). Treated meat cubes were stored at 4°C or 10°C for 1, 4 and 7 d. Adding only marinade to the camel meat at 10°C decreased the pathogens by 0.8 – 2.4 log CFU/g. At 10°C, BR decreased L. monocytogenes, E. coli O157:H7 and Salmonella spp. by 2.0, 1.5 and 1.3 log CFU/g, while EU caused a decrease (p < 0.05) of 1.9, 1.2 and 0.9 log CFU/g, respectively. Similarly, VA caused a reduction in these microorganisms of 1.3, 1.1 and 1.0 log CFU/g, respectively (p < 0.05). The combination of marinade and EO resulted in a decrease of the pathogens ranging from 0.9 – 1.4 and 2.8 – 3.7 log CFU/g at 4 and 10°C, respectively. The antimicrobial efficacy of EO alone or when combined with marinade was higher at 10°C than at 4°C with all three pathogens at both 0.5% and 1%. Overall, EOs were found to enhance the microbial safety of camel meat. In addition, they are antimicrobials that occur naturally, require minimum investment and may prove to be a great asset for marinated camel meat producers.
... These findings indicate that the presence of Salmonella in the gut may negatively influence the overall health of the falcons by affecting the capacity to build and maintain protein mass, which is essential for flighted birds that engage in long-distance migrations. Moreover, small aromatic compounds such as gallic acid, 3-phenylpropionic acid, nicotinic acid, 4-methylcatechol, 3-hydroxycinnamate and their derivatives are known antimicrobials (67)(68)(69)(70)(71) and are known to have Salmonella inhibitory effects in humans (72). The falcons in our study that harbored high levels of Salmonella showed enrichment of functional pathways that degrade these antimicrobial compounds. ...
The gut microbiome is increasingly being appreciated as a master regulator of animal health. However, most avian gut microbiome studies have focused on birds of economic importance while the gut microbiomes of raptors remain underexplored. Here we examine the gut microbiota of 29 samples from four Falco species including hybrid birds— raptors of historic importance —in the context of avian evolution by sequencing the 16S rDNA V4 region. Our results reveal that evolutionary histories and diet are significantly associated with avian gut microbiota in general, whereas diet plays a major role in shaping the falcon gut microbiota. Multiple analyses revealed that gut microbial diversity, composition, and abundance of key diet-discriminating bacterial genera in the falcon gut closely resemble those of carnivorous raptors rather than those of their closest phylogenetic relatives. Furthermore, the falcon microbiota is dominated by Firmicutes and consists of Salmonella at appreciable levels. Salmonella presence may potentially alter the functional capacity of the falcon gut microbiota as its abundance is associated with depletion of multiple predicted metabolic pathways involved in protein mass buildup, muscle maintenance, and enrichment of antimicrobial compound degradation, thus increasing the pathogenic potential of the falcon gut and presents a potential risk to human health.
Author Summary in Arabic
... Eugenol, the main component of clove oil, is one of the most investigated natural compound for its significant antimicrobial activity. The efficacy of eugenol applications in the poultry meat model has been noted by recent studies, in addition to findings from in vitro studies (Alanazi et al., 2018;López-Romero et al., 2018;Nair et al., 2014). Besides eugenol, the activity of eugenol derivatives was evaluated against foodborne pathogens (Friedman et al., 2002;Hyldgaard et al., 2015). ...
Poultry is one of the fastest growing industries due to advantages in land use, rapid production and advances in feed technology. The rising trend in the consumption of poultry meat over the last 50 years has also increased concerns about food safety. Campylobacter jejuniis the leading bacterial cause of gastroenteritis, the foremost cause of foodborne deaths. Despite significant progress in food safety methology, the genusCampylobacter remains a common foodborne pathogen in poultry. Increasing consumer demands for natural products require the discovery of new antimicrobials to ensure the safety of poultry meat. Recent studies have revealed that eugenol acts with antimicrobial activity on a wide variety of foodborne microorganisms. Eugenol is generally recognized as safe and is a promising preservative for the food industry. However, specific applications of eugenol need to be identified and validated to clarify the role of the food preservative in poultry meat safety.
... The response surface model has been widely used as a tool to predict bacterial inactivation during complicated treatment conditions. López-Romero et al. (2018) The comparison of experimental and response surface model predicted reduction of Salmonella and E. faecium was shown in Fig. 4. The response surface models provide favorable predictions for both Salmonella and E. faecium with the RMSE of 0.48 and 0.45 log CFU/g, respectively. From the predicted reduction curves, it can also be observed that larger inactivation is achieved at higher temperature and RH levels. ...
This research investigated the effect of temperature and relative humidity (RH) conditions during ethylene oxide (EtO) fumigation for inactivation of Salmonella and Enterococcus faecium NRRL B-2354 on whole black pepper-corns. Black peppercorn samples were inoculated with a five-strain Salmonella cocktail or E. faecium inoculum. EtO (735.3 mg/L) fumigation was conducted at different treatment temperatures (46, 53, and 60 • C) and different RH levels (30,40, and 50%) for the inactivation of inoculated black peppercorn samples with different exposure times (2-180 min). The temperature, RH, and exposure time exhibit significant linear effects on microbial inactivation. Bacterial inactivation during EtO fumigation was described by the Weibull model with the R 2 > 0.70 and RMSE < 0.20 log CFU/g at all conditions. The concave upward trend of the Weibull model indicated a tailing effect. The inactivation data were also used to develop the response surface model as a function of temperature, RH, and exposure time to predict the reduction of Salmonella or E. faecium on whole black peppercorn during EtO fumigation. The developed models predicted log reductions with RMSE of 0.48 and 0.45 log CFU/g for Salmonella andE. faecium, respectively. Technical information for developing and validating EtO fumigation for whole black peppercorn could be estimated based on the developed model.
... The phenolic acids evaluated in this study have been previously noted by other researchers, primarily for their roles as antioxidants, documented use as food preservatives, and antimicrobial potential against Gram-negative bacterial pathogens [32]. GA, PA and VA specifically have been shown to inhibit the growth of Pseudomonas spp., Listeria monocytogenes, Mannheimia haemolytica, Pasteurella multocida, Escherichia coli and some strains of Salmonella spp., as well as being able to reduce the pathogenicity of other bacteria such as Proteus mirabilis [33][34][35][36]. However, the effectiveness against ST, specifically, has not been consistently documented, in addition to the mechanisms of action underlying the molecular interactions that precede cell death remaining poorly understood. ...
Salmonella enterica serovar Typhimurium (ST) remains a major infectious agent in the USA, with an increasing antibiotic resistance pattern, which requires the development of novel antimicrobials capable of controlling ST. Polyphenolic compounds found in plant extracts are strong candidates as alternative antimicrobials, particularly phenolic acids such as gallic acid (GA), protocatechuic acid (PA) and vanillic acid (VA). This study evaluates the effectiveness of these compounds in inhibiting ST growth while determining changes to the outer membrane through fluorescent dye uptake and scanning electron microscopy (SEM), in addition to measuring alterations to virulence genes with qRT-PCR. Results showed antimicrobial potential for all compounds, significantly inhibiting the detectable growth of ST. Fluorescent spectrophotometry and microscopy detected an increase in relative fluorescent intensity (RFI) and red-colored bacteria over time, suggesting membrane permeabilization. SEM revealed severe morphological defects at the polar ends of bacteria treated with GA and PA, while VA-treated bacteria were found to be mid-division. Relative gene expression showed significant downregulation in master regulator hilA and invH after GA and PA treatments, while fliC was upregulated in VA. Results suggest that GA, PA and VA have antimicrobial potential that warrants further research into their mechanism of action and the interactions that lead to ST death.
... The phenolic acids evaluated in this study have been previously noted by other researchers, primarily for their roles as antioxidants, documented use as food preservatives, and antimicrobial potential against Gram-negative bacterial pathogens [32]. GA, PA and VA specifically have been shown to inhibit the growth of Pseudomonas spp., Listeria monocytogenes, Mannheimia haemolytica, Pasteurella multocida, Escherichia coli and some strains of Salmonella spp., as well as being able to reduce the pathogenicity of other bacteria such as Proteus mirabilis [33][34][35][36]. However, the effectiveness against ST, specifically, has not been consistently documented, in addition to the mechanisms of action underlying the molecular interactions that precede cell death remaining poorly understood. ...
... It has been shown that in addition to its immunomodulatory effect [59], scopoletin reduces the intracellular survival of Salmonella Typhi within U937 human macrophage cell line [60]. Gallic acid has in addition to its in vitro and in vivo antibacterial effect against Salmonella Typhimurium [61,62], an antioxidant activity. These compounds related properties corroborate the findings of Sokoudjou et al. [20] who reported that the ability of the extract of Canarium schweinfurthii to cure salmonellosis in broilers could be explained by its ability to directly kill Salmonella and/or boost the immune system of the host. ...
... It has been shown that in addition to its immunomodulatory effect [59], scopoletin reduces the intracellular survival of Salmonella Typhi within U937 human macrophage cell line [60]. Gallic acid has in addition to its in vitro and in vivo antibacterial effect against Salmonella Typhimurium [61,62], an antioxidant activity. These compounds related properties corroborate the findings of Sokoudjou et al. [20] who reported that the ability of the extract of Canarium schweinfurthii to cure salmonellosis in broilers could be explained by its ability to directly kill Salmonella and/or boost the immune system of the host. ...
Background
Bacteria belonging to the Salmonella genus are major concern for health, as they are widely reported in many cases of food poisoning. The use of antibiotics remains a main stream control strategy for avian salmonellosis as well as typhoid and paratyphoid fevers in humans. Due to the growing awareness about drug resistance and toxicities, the use of antibiotics is being discouraged in many countries whilst advocating potent benign alternatives such as phyto-based medicine. The objective of this work was to isolate, characterise the bioactive compounds of Canarium schweinfurthii ; and evaluate their anti-salmonellal activity.
Methods
The hydro-ethanolic extract of Canarium schweinfurthii was fractionated and tested for their anti-salmonellal activity. The most active fractions (i.e. chloroform and ethyl acetate partition fractions) were then explored for their phytochemical constituents. Fractionation on normal phase silica gel column chromatography and size exclusion chromatography on Sephadex LH-20 led to the isolation of four compounds (maniladiol, scopoletin, ethyl gallate and gallic acid) reported for the first time in Canarium schweinfurthii .
Results
Result indicated that scopoletin and gallic acid had greater activity than the crude extracts and partition fractions. Among the isolated compounds, scopoletin showed the highest inhibitory activity with a MIC of 16 μg/ml against Salmonella Typhimurium and Salmonella Enteritidis.
Conclusions
The overall results of this study indicates that the hydro-ethanolic extract as well as some of isolated compounds have interesting anti-salmonellal activities that could be further explored for the development of potent therapy for salmonellosis. Furthermore, the study adds credence to the folkloric applications of the plant.
... Similarly, a study on chickens displayed a synergistic effect of GA and eugenol in reducing the heat lethality of Salmonella spp. (121). ...
Gallic acid (GA) is a naturally occurring polyphenol compound present in fruits, vegetables, and herbal medicines. According to previous studies, GA has many biological properties, including antioxidant, anticancer, anti-inflammatory, and antimicrobial properties. GA and its derivatives have multiple industrial uses, such as food supplements or additives. Additionally, recent studies have shown that GA and its derivatives not only enhance gut microbiome (GM) activities, but also modulate immune responses. Thus, GA has great potential to facilitate natural defense against microbial infections and modulate the immune response. However, the exact mechanisms of GA acts on the GM and immune system remain unclear. In this review, first the physicochemical properties, bioavailability, absorption, and metabolism of GA are introduced, and then we summarize recent findings concerning its roles in gastrointestinal health. Furthermore, the present review attempts to explain how GA influences the GM and modulates the immune response to maintain intestinal health.
... Eug, often in forms of clove essential oil, is a natural phenolic compound extracted from Myrtaceae plants. Owning to its antimicrobial and antioxidant properties, recent studies reported the use of Eug in food, pharmaceuticals, nutraceuticals, cosmetics, and active packagings (Devi et al. 2010;Baskaran et al. 2010;Chatterjee and Bhattacharjee 2013;Abbaszadeh et al. 2014;Guerreiro et al. 2016;Requena et al. 2017;Resende et al. 2017;Navikaite-Snipaitiene et al. 2018;Wan et al. 2018;Ribes et al. 2019;Cheng et al. 2019;López-Romero et al. 2018;Ju et al. 2020;Li et al. 2020;Jia et al. 2020). However, practical applications of Eug depend on sustained slowrelease delivery systems, which prolongs bacteriostasis and increases bioavailability Cheng et al. (2011);Zhu et al. (2016). ...
This study aimed to develop self-assembled gelatin-chitosan (Gel-CS) nanocapsules as a water-soluble delivery system for alcohol-soluble compounds. Eugenol (Eug) selected as the model molecule for its high solubility in alcohol and insolubility in water. The study also examined different reaction conditions and reagent loading ratios to optimize eugenol-embedded gelatin-chitosan nanocapsules (Eug-Gel-CS NPs) formation. The optimal loading ratio of Gel, CS, and Eug was 3:1:2, which yielded an average particle size of 229.09 nm and an encapsulation efficiency of 50.69%. The morphological characteristics of Eug-Gel-CS NPs were further demonstrated by transmission electron microscopy. The prepared Eug-Gel-CS NPs also exhibited potential controlled-release properties in aqueous phase with the in vitro release percentage of 69.47 ± 1.24% over 36 h. This nanocapsule system may provide a platform to expand the potential applications of Eug in food and nutrition.
... heat resistance in ground chicken. GA and eugenol efficacy in rendering the pathogen more sensitive to the lethal effect of heat were concentration dependent (López-Romero et al., 2018), and Sorrentino et al. (2018) reported the antimicrobial activity of GA against food-related Pseudomonas strains and its use as a biocontrol tool to improve the shelf life of fresh black truffles. ...
... Degala et al. (13) reported the potential hurdle effect of lemongrass oil and UV-C treatment for inactivation of Escherichia coli K-12 on goat meat surfaces. López-Romero et al. (26) successfully utilized plant phytochemicals, gallic acid, and eugenol for inhibition of Salmonella in ground chicken. Probiotic lactic acid bacteria (LAB) have also been used as an effective strategy for suppression of several food spoilage microorganisms (2,17). ...
Second-generation functional foods based on nonconventional matrices such as fruits, vegetables, and cereals demand high-quality food products with an extended shelf life. The aim of this work was to evaluate the protective efficiency of probiotic strain Lactobacillus rhamnosus GG incorporated into two phenolic-rich fruit matrices, sea buckthorn juice (SBT) and apple juice (APJ) both supplemented with whey protein concentrate (WPC), during refrigerated storage (4°C). The protective potential after a cold chain break (at 10 and 20°C) was also evaluated. The efficiency of L. rhamnosus GG substantially depended on the matrix components. L. rhamnosus GG in SBT+WPC inhibited Enterobacter aerogenes and Staphylococcus aureus by 1 log CFU/mL within 7 days of refrigerated storage compared with less inhibition of E. aerogenes and S. aureus by 0.75 and 0.83 log CFU/mL, respectively, by L. rhamnosus GG in APJ+WPC. Principal component analysis clustered L. rhamnosus GG in SBT+WPC as the most efficient matrix based on its ability to inhibit both E. aerogenes and S. aureus. The rheological parameters of the WPC-supplemented L. rhamnosus GG matrices were also evaluated. The consistency index and flow behavior index were derived from shear experiments. All juice matrices had shear-thinning properties. The pseudoplastic behavior of the juices increased with the addition of WPC and L. rhamnosus GG.
HIGHLIGHTS
Bacillus cereus is a foodborne pathogen widely distributed in the large-scale catering industry and produces spores. The study explored the antibacterial activity, potential mechanism of eugenol against B. cereus, and spores with germination rate. The minimum inhibitory concentration (MIC; 0.6 mg/mL) of eugenol to six B. cereus strains was compared with the control; B. cereus treated with eugenol had a longer lag phase. Eugenol at a concentration of more than 1/2MIC decreased viable B. cereus (∼5.7 log colony-forming unit [CFU]/mL) counts below detectable limits within 2 h, and eugenol of 3MIC reduced B. cereus (∼5.9 log CFU/mL) in skim milk below detectable limits within 30 min. The pH values of skim milk were unaffected by the addition of eugenol. The ΔE values below 2 show that the color variations of skim milk were not visible to the human eye. For sensory evaluation, eugenol did not significantly affect the color or structural integrity of the skim milk. It had a negative impact on the flavor and general sensory acceptance of the treated milk. Eugenol hyperpolarized B. cereus cell membrane, decreased intracellular ATP concentration, and increased intracellular reactive oxygen species contents and extracellular malondialdehyde contents, resulting in the cell membrane of B. cereus being damaged and permeabilized, and cell morphology being changed. In addition, according to the viable count, confocal laser scanning microscopy, and spore morphology changes, eugenol reduced the germination rate of B. cereus spores. These findings suggest that eugenol can be used as a new natural antibacterial agent to control B. cereus and spores in the food production chain.
The purpose of this study was to identify the effect of amalgam UV lamp-activated gallic acid on the inactivation of foodborne pathogens (Escherichia coli O157:H7, Salmonella enterica serovar Typhimurium, and Listeria monocytogenes). When the bactericidal effect of amalgam UV lamp-activated gallic acid was compared with that of conventional low-pressure (LP) Hg UV lamp-activated gallic acid, the reduction levels of all three foodborne pathogens were significantly higher by amalgam UV lamp-activated gallic acid than LP lamp-activated gallic acid. Bactericidal mechanism was investigated using four reactive oxygen species (ROS) scavengers (mannitol, sodium pyruvate, trion, and sodium azide) and a wider range of ROS was produced by amalgam lamp-activated gallic acid than LP lamp-activated gallic acid. It is assumed that dual-wavelength (185 and 254 nm) emission characteristics of amalgam lamp generate a wider range of ROS. When applied to cherry tomato samples, amalgam lamp-activated gallic acid reduced levels of pathogens to a significantly greater level than LP lamp-activated gallic acid. These results indicate that amalgam lamp-activated gallic acid can effectively control foodborne pathogens in the food processing industry.
In this study, black peppercorns and cumin seeds were inoculated with a five-serotype cocktail of Salmonella or its surrogate Enterococcus faecium NRRL B-2354. The inoculated samples (ca. 10⁷ CFU/g) were treated by ClO2 gas at different gas concentrations (5, 10, and 15 mg/L) and relative humidities (60, 70, and 80%) at room temperature (25 °C) at five gas exposure times (60, 120, 180, 240, 300 min). More than 5-log reduction of Salmonella was achieved in both spices with 300 min of ClO2 gas treatment at 15 mg/L and 80% RH. The corresponding values for E. faecium were 4.36 and 4.17 log CFU/g in black peppercorns and cumin seeds, respectively, which were significant lower than Salmonella (p < 0.05). Gas concentration, RH, and exposure time showed significantly positive linear associations with Salmonella inactivation. E. faecium appears a suitable surrogate for Salmonella and can be used for future process validations using comparable conditions.
Persistence, thermal resistance, and survival of Salmonella in low moisture foods (LMF) have resulted in several foodborne illness outbreaks. Both existing and novel pasteurization technologies need to be validated for microbial safety of LMF. In this dissertation, a framework for using radio frequency (RF) heating to enhance microbial safety of milk powders and egg white powder was established. Thermal inactivation kinetics of Salmonella in milk powders were determined to guide the dairy industry for identifying thermal processing conditions for pasteurization. Storage time showed no effect on the thermal resistance of Salmonella, which can simplify the process validation study in the industry. Hot air-assisted RF heating followed by holding at high temperatures in a convective oven was developed and validated for pasteurization of milk powders. Continuous RF processing was evaluated for pasteurization of egg white powder (EWP), which can provide> 6.7 log reduction for Salmonella after RF-assisted thermal processing of EWP at 80°C for 2 h. Ethylene oxide (EtO) and chlorine dioxide (ClO2) gaseous technologies were evaluated as non-thermal pasteurization for improving microbial safety of spices. A response surface model was developed as a function of temperature, relative humidity, and exposure time to predict the reduction of Salmonella or Enterococcus faecium NRRL B-2354 on whole black peppercorn during EtO fumigation, which can guide the spice industry in determining the process conditions for pasteurization. The effects of gas concentration, RH, and exposure time on Salmonella and E. faecium on whole black peppercorn and cumin seeds during ClO2 gaseous treatment were evaluated which can provide technical information for implementation of this technology. E. faecium was found to be a suitable surrogate for Salmonella during both thermal (RF) and non-thermal (EtO and ClO2) of dairy powders and spices, respectively. Therefore, the food industry can use E. faecium to replace Salmonella for conducting the industrial process validation. Advisors: Drs. Jeyamkondan Subbiah and Mary-Grace Danao
The present study was aimed at developing a mathematical model to predict the growth of Salmonella in ground chicken in the presence of the background microflora. Ground chicken was inoculated with a cocktail of S. Typhimurium and S. Enteritidis and incubated at various isothermal temperatures (8-33 °C). Salmonella grew at all temperatures, except at 8 °C, while the background microflora could grow under all conditions. The observed growth data of both Salmonella and background microflora at temperatures between 12 and 33 °C were analyzed simultaneously to develop the predictive growth models. The Huang-Jameson effect (HJE) model and Huang-Lotka-Volterra (HLV) model were used to describe the growth and interaction between Salmonella and background microflora. The Huang square-root model was used to evaluate the effect of temperature on the growth rates and lag times of Salmonella and background microflora. A one-step analysis method was used to directly build the tertiary models and to determine the kinetic parameters from the growth curves.
The minimum growth temperature (Tmin) for Salmonella estimated by both the HJE and HLV models was 7.2 °C. The Tmin for background flora determined by HJE and HLV model was 1.3 and 1.8 °C, respectively. Under competition, the growth rate of Salmonella could be lower or higher than that of the native microbiota, depending on the storage temperature. Above 16.8 °C, Salmonella grew faster than the background microflora.
With relatively low value of RMSE (0.3 log CFU/g), the HJE and HLV models could both successfully describe the growth of Salmonella and native microflora and the interaction between the two. Although the Akaike Information Criterion (AIC) value of the HJE model (−349.1) was slightly smaller than that of the HLV model (−339.4), both models were practically equal in accuracy for predicting the competitive growth of Salmonella and background flora in ground chicken. The HJE model and kinetic parameters were validated using separate isothermal and dynamic growth data. The validation results indicated the competition model was accurate. The RMSE of the predictions was only 0.3 log CFU/g. Overall, the residual errors of predictions followed a normal distribution, with more than 86% of them were within ±0.5 log CFU/g. The results from this study may be useful for microbial risk assessments of Salmonella and shelf-life prediction of ground chicken.
Consumers' preferences for cleaner label products require the food industry to replace synthetic preservatives with natural substitutes. Therefore, the synergistic inhibitory effect of eugenol and citral (SEC) on Aspergillus niger was explored. On this basis, the antimicrobial sachet containing SEC was developed and its application potential in bread preservation was evaluated. The content of reactive oxygen species (ROS) and malondialdehyde (MDA) showed that SEC could significantly induce lipid peroxidation in cell membranes, in which citral played a leading role. The permeation experiments of SEM, TEM, propyl iodide and fluorescein diacetate showed that SEC could destroy the integrity of the cell membrane. Eugenol contributed more than citral. The OD260 and the relative conductivity of the SEC group increased by 5.2 and 4.1 times, respectively, after 8 h. Finally, the shelf life experiment of bread showed that the antimicrobial sachets containing SEC could significantly prolong the shelf life of bread without producing unpleasant odour.
Silk fibroin is widely used in the medical field as an electrospinning material, but there are few reports on the application of silk fibroin nanofibers encapsulating antibacterial essential oil as active antibacterial packaging in food. This study aims to fabricate cold plasma treated thyme essential oil (TO)/silk fibroin (SF) nanofibers to inhibit Salmonella Typhimurium in poultry meat. Firstly, antimicrobial activity and mechanism of TO against Salmonella Typhimurium was assessed. Subsequently, viscoelastic properties of spinning solutions and properties of nanofibers which included nanofibers stability, hydration, barrier and mechanical properties were studied to screen good performance nanofibers. Further, cold plasma was applied to implement the surface modification of TO/SF nanofibers. The results showed that the TO release amount of plasma-TO/SF nanofibers improved obviously after cold plasma treatment, leading to higher antibacterial activity of plasma-TO/SF nanofibers than TO/SF nanofibers. After plasma-TO/SF nanofibers treatment, the number of Salmonella Typhimurium in chicken meat and duck meat decreased by 6.1 and 6.06 Log CFU/g compared with control group at 25 °C, respectively. Overall, this study indicated that plasma-TO/SF nanofibers membrane was an effective antimicrobial packaging to increase shelf life of foods, which had a broad prospect in the field of food preservation.
The heat resistance data on Listeria monocytogenes in culture media and foods are summarized. Most heat resistance data for foods have been obtained in dairy, meat, poultry, and egg products. Limited data have been published on seafood, fruits, and vegetables. The methodologies employed have evolved over time; hence data from earlier experiments are not directly comparable to more recent studies. Many factors influence the heat resistance of L. monocytogenes. Variation exists among different strains in their ability to withstand heat treatment. In addition, heat resistance is influenced by age of the culture, growth conditions, recovery media, and characteristics of foods such as salt content, aw, acidity, and the presence of other inhibitors. Listeriae are more heat resistant than most other nonspore-forming foodborne pathogens, and thus, processing recommendations based on data from experiments with Salmonella spp, or pathogenic Escherichia coli may not be sufficient to eliminate similar numbers of L. monocytogenes. The data provided in this review may prove useful for food processors in determining appropriate times and temperatures for producing foods free of vegetative pathogens.
Chitosan-based active films were developed by incorporation of carvacrol (10 g/L), pomegranate peel extract (PPE, 10 g/L) and carvacrol + PPE (10 g/L of each) and their physical, antioxidant and antimicrobial properties were investigated. Incorporation of carvacrol and carvacrol + PPE into the films significantly decreased the water vapor permeability, tensile strength and percentage of elongation at break. Incorporation of carvacrol, PPE and carvacrol + PPE into the films decreased the transparency, but significantly increased the total phenol content and antioxidant activity. All the films, with the exception of PPE-incorporated film, exhibited antibacterial activity against Escherichia coli and Staphylococcus aureus. In addition, the antibacterial activity against Staphylococcus aureus of the film incorporated with carvacrol + PPE was moderately higher than that incorporated with carvacrol or PPE alone, suggesting a synergistic action between carvacrol and PPE.
Bacterial resistance has been increasingly reported worldwide and is one of the major causes of failure in the treatment of infectious diseases. Natural-based products, including plant secondary metabolite (phytochemicals) may be used to surpass or reduce this problem. The objective of this study was to determine the antibacterial effect and mode of action of selected essential oils (EOs) components: carveol, carvone, citronellol and citronellal against Escherichia coli and Staphylococcus aureus. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) were assessed for the selected EOs components. Moreover, physicochemical bacterial surface characterization, bacterial surface charge, membrane integrity and K+ leakage assays were carried out to investigate the antimicrobial mode of action of EOs components. Citronellol was the most effective molecule against both pathogens, followed by citronellal, carveol and carvone. Changes in the hydrophobicity, surface charge and membrane integrity with the subsequent K+ leakage from E. coli and S. aureus were observed after exposure to EOs. This study demonstrates that the selected EOs have significant antimicrobial activity against the bacteria tested, acting on the cell surface and causing the disruption of the bacterial membrane. Moreover, these molecules are interesting alternatives to conventional antimicrobials for the control of microbial infections.
This paper serves as an overview of various aspects of thermal processing. Heat processing of foods has a long history and is still one of the most important preservation methods. To guarantee microbiological safety and stability, large safety margins are often applied in traditional heat processes. Because of the need for more fresh like foods, there is a need for milder preservation methods without compromising on safety and stability. The review deals with heat resistance data and mathematical models that describe heat inactivation. The effects of food composition are not yet fully clear and more knowledge of the cell physiology of the target microorganism could be of help in predicting the effects of food constituents. Finally, special attention has been paid to biological time temperature indicators to enable proper process calculations.
O efeito inibitório do eugenol, o principal constituinte do óleo essencial de cravo, foi avaliado sobre o crescimento e produção de listeriolisina O (LLO) por Listeria monocytogenes. O efluxo de íons potássio das células também foi determinado após 24 h de incubação em solução tampão, contendo eugenol. Concentrações de 100, 300 e 500 µg mL-1 de eugenol promoveram a inibição do crescimento de L. monocytogenes e, em concentrações acima de 800 µg mL-1, constatou-se um efeito bactericida. O crescimento de L. monocytogenes na presença de eugenol resultou na inibição de 80 a 100% da produção de LLO. O efluxo de K+ promovido pelo eugenol indicou que a membrana celular foi afetada. Estes resultados indicam a efetividade do eugenol para o controle do crescimento e da produção de LLO por L. monocytogenes.
Abstract The increased resistance of pathogenic microorganisms is frequently attributed to the extreme and inadequate use of antibiotics and transmission of resistance within and between individuals. To counter the emergence of resistant microorganisms, considerable resources have been invested in the search for new antimicrobials. Plants synthesize a diverse array of secondary metabolites (phytochemicals) known to be involved in defense mechanisms, and in the last few years it is recognized that some of these molecules have health beneficial effects, including antimicrobial properties. In this study, the mechanism of action of gallic (GA) and ferulic (FA) acids, a hydroxybenzoic acid and a hydroxycinnamic acid, was assessed on Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, and Listeria monocytogenes. The targets of antimicrobial action were studied using different bacterial physiological indices: minimum inhibitory concentration (MIC), minimum bactericidal concentration (MBC), membrane permeabilization, intracellular potassium release, physicochemical surface properties, and surface charge. It was found that FA and GA had antimicrobial activity against the bacteria tested with MIC of 500 μg/mL for P. aeruginosa, 1500 μg/mL for E. coli, 1750 μg/mL for S. aureus, and 2000 μg/mL for L. monocytogenes with GA; 100 μg/mL for E. coli and P. aeruginosa, 1100 μg/mL and 1250 μg/mL for S. aureus and L. monocytogenes, respectively, with FA. The MBC for E. coli was 2500 μg/mL (FA) and 5000 (GA), for S. aureus was 5000 μg/mL (FA) and 5250 μg/mL (GA), for L. monocytogenes was 5300 μg/mL (FA) and 5500 μg/mL (GA), and 500 μg/mL for P. aeruginosa, with both phytochemicals. GA and FA led to irreversible changes in membrane properties (charge, intra and extracellular permeability, and physicochemical properties) through hydrophobicity changes, decrease of negative surface charge, and occurrence of local rupture or pore formation in the cell membranes with consequent leakage of essential intracellular constituents. The overall study emphasizes the potential of plant-derived molecules as a green and sustainable source of new broad spectrum antimicrobial products.
Estimates of foodborne illness can be used to direct food safety policy and interventions. We used data from active and passive surveillance and other sources to estimate that each year 31 major pathogens acquired in the United States caused 9.4 million episodes of foodborne illness (90% credible interval [CrI] 6.6–12.7 million), 55,961 hospitalizations (90% CrI 39,534–75,741), and 1,351 deaths (90% CrI 712–2,268). Most (58%) illnesses were caused by norovirus, followed by nontyphoidal Salmonella spp. (11%), Clostridium perfringens (10%), and Campylobacter spp. (9%). Leading causes of hospitalization were nontyphoidal Salmonella spp. (35%), norovirus (26%), Campylobacter spp. (15%), and Toxoplasma
gondii (8%). Leading causes of death were nontyphoidal Salmonella spp. (28%), T.
gondii (24%), Listeria
monocytogenes (19%), and norovirus (11%). These estimates cannot be compared with prior (1999) estimates to assess trends because different methods were used. Additional data and more refined methods can improve future estimates.
Salmonella is one of the most extensively characterized bacterial pathogens and is a leading cause of bacterial gastroenteritis. Despite this, we are only just beginning to understand at a molecular level how Salmonella interacts with its mammalian hosts to cause disease. Studies during the past decade on the genetic basis of virulence of Salmonella have significantly advanced our understanding of the molecular basis of the host-pathogen interaction, yet many questions remain. In this review, we focus on the interaction of enterocolitis-causing salmonellae with the intestinal mucosa, since this is the initiating step for most infections caused by Salmonella. Animal and in vitro cell culture models for the interaction of these bacteria with the intestinal epithelium are reviewed, along with the bacterial genes that are thought to affect this interaction. Lastly, recent studies on the response of epithelial cells to Salmonella infection and how this might promote diarrhea are discussed.
An improved method of sample preparation was used in a microplate assay to evaluate the bactericidal activity levels of 96 essential oils and 23 oil compounds against Campylobacter jejuni, Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella enterica obtained from food and clinical sources. Bactericidal activity (BA50) was defined as the percentage of the sample in the assay mixture that resulted in a 50% decrease in CFU relative to a buffer control. Twenty-seven oils and 12 compounds were active against all four species of bacteria. The oils that were most active against C. jejuni (with BA50 values ranging from 0.003 to 0.009) were marigold, ginger root, jasmine, patchouli, gardenia, cedarwood, carrot seed, celery seed, mugwort, spikenard, and orange bitter oils; those that were most active against E. coli (with BA50 values ranging from 0.046 to 0.14) were oregano, thyme, cinnamon, palmarosa, bay leaf, clove bud, lemon grass, and allspice oils; those that were most active against L monocytogenes (with BA50 values ranging from 0.057 to 0.092) were gardenia, cedarwood, bay leaf, clove bud, oregano, cinnamon, allspice, thyme, and patchouli oils; and those that were most active against S. enterica (with BA50 values ranging from 0.045 to 0.14) were thyme, oregano, cinnamon, clove bud, allspice, bay leaf, palmarosa, and marjoram oils. The oil compounds that were most active against C. jejuni (with BA50 values ranging from 0.003 to 0.034) were cinnamaldehyde, estragole, carvacrol, benzaldehyde, citral, thymol, eugenol, perillaldehyde, carvone R, and geranyl acetate; those that were most active against E. coli (with BA50 values ranging from 0.057 to 0.28) were carvacrol, cinnamaldehyde, thymol, eugenol, salicylaldehyde, geraniol, isoeugenol, citral, perillaldehyde, and estragole; those that were most active against L monocytogenes (with BA50 values ranging from 0.019 to 0.43) were cinnamaldehyde, eugenol, thymol, carvacrol, citral, geraniol, perillaldehyde, carvone S, estragole, and salicylaldehyde; and those that were most active against S. enterica (with BA50 values ranging from 0.034 to 0.21) were thymol, cinnamaldehyde, carvacrol, eugenol, salicylaldehyde, geraniol, isoeugenol, terpineol, perillaldehyde, and estragole. The possible significance of these results with regard to food microbiology is discussed.
Flavonoids are ubiquitous in photosynthesising cells and are commonly found in fruit, vegetables, nuts, seeds, stems, flowers, tea, wine, propolis and honey. For centuries, preparations containing these compounds as the principal physiologically active constituents have been used to treat human diseases. Increasingly, this class of natural products is becoming the subject of anti-infective research, and many groups have isolated and identified the structures of flavonoids possessing antifungal, antiviral and antibacterial activity. Moreover, several groups have demonstrated synergy between active flavonoids as well as between flavonoids and existing chemotherapeutics. Reports of activity in the field of antibacterial flavonoid research are widely conflicting, probably owing to inter- and intra-assay variation in susceptibility testing. However, several high-quality investigations have examined the relationship between flavonoid structure and antibacterial activity and these are in close agreement. In addition, numerous research groups have sought to elucidate the antibacterial mechanisms of action of selected flavonoids. The activity of quercetin, for example, has been at least partially attributed to inhibition of DNA gyrase. It has also been proposed that sophoraflavone G and (-)-epigallocatechin gallate inhibit cytoplasmic membrane function, and that licochalcones A and C inhibit energy metabolism. Other flavonoids whose mechanisms of action have been investigated include robinetin, myricetin, apigenin, rutin, galangin, 2,4,2'-trihydroxy-5'-methylchalcone and lonchocarpol A. These compounds represent novel leads, and future studies may allow the development of a pharmacologically acceptable antimicrobial agent or class of agents.
The heat resistance of Campylobacter jejuni strains AR6 and L51 and the heat resistance of Campylobacter coli strains DR4 and L6 were measured over the temperature range from 50 to 60 degrees C by two methods. Isothermal measurements yielded D55 values in the range from 4.6 to 6.6 min and z values in the range from 5.5 to 6.3 degrees C. Dynamic measurements using differential scanning calorimetry (DSC) during heating at a rate of 10 degrees C/min yielded D55 values of 2.5 min and 3.4 min and z values of 6.3 degrees C and 6.5 degrees C for AR6 and DR4, respectively. Both dynamic and isothermal methods yielded mean D55 values that were substantially greater than those reported previously (0.75 to 0.95 min). DSC analysis of each strain during heating at a rate of 10 degrees C/min yielded a complex series of overlapping endothermic peaks, which were assigned to cell wall lipids, ribosomes, and DNA. Measurement of the decline in the numbers of CFU in calorimetric samples as they were heated showed that the maximum rate of cell death occurred at 56 to 57 degrees C, which is close to the value predicted mathematically from the isothermal measurements of D and z (61 degrees C). Both estimates were very close to the peak m1 values, 60 to 62 degrees C, which were tentatively identified with unfolding of the 30S ribosome subunit, showing that cell death in C. jejuni and C. coli coincided with unfolding of the most thermally labile regions of the ribosome. Other measurements indicated that several essential proteins, including the alpha and beta subunits of RNA polymerase, might also unfold at the same time and contribute to cell death.
In the United States, multidrug-resistant phenotypes of Salmonella enterica serotype Newport (commonly referred to as MDR-AmpC) have emerged in animals and humans and have become a major public health
problem. Although pulsed-field gel electrophoresis (PFGE) is the current “gold standard” typing method for Salmonella, multilocus sequence typing (MLST) may be more relevant to investigations exploring evolutionary and population biology relationships.
In this study, 81 Salmonella enterica serotype Newport isolates from humans, food animals, and retail foods were examined for antimicrobial susceptibility and
characterized using PFGE and MLST of seven genes, aroC, dnaN, hemD, hisD, purE, sucA, and thrA. Forty-nine percent of the isolates were resistant to nine or more of the tested antimicrobials. Salmonella isolates displayed resistance most often to sulfamethoxazole (57%), streptomycin (56%), tetracycline (56%), ampicillin (52%),
and ceftiofur (49%) and, to a lesser extent, to kanamycin (19%), trimethoprim-sulfamethoxazole (17%), and gentamicin (11%).
A total of 43 PFGE patterns were generated using XbaI, indicating a genetically diverse population. The largest PFGE cluster
contained isolates from clinically ill swine, cattle, and humans. MLST resulted in 12 sequence types (STs), with one type
encompassing 62% of the strains. Ten new sequence types and one novel allele type were identified. Furthermore, MLST typing
showed that strains closely related by PFGE clustered in major STs, whereas more distantly related strains were separated
into two clusters by PFGE. The results of this study demonstrated that the MLST scheme employed here clustered S. enterica serovar Newport isolates in distinct molecular populations, and strain discrimination was enhanced by combining PFGE, antimicrobial
susceptibility, and MLST results.
Presents the latest research in the control of foodborne pathogens. Emphasizes traditional and emerging techniques as well as current applications for the inactivation of microorganisms to reduce illness and enhance food safety and quality.
The influence of mild heat pretreatment on the bactericidal action of nisin, carvacrol and thymol on stationary and exponential phase cells of two Bacillus cereus strains was studied. Carvacrol or thymol concentrations of 0.3 mmol/L had no bactericidal effect on unheated, and a minor effect on heated B. cereus cells either in stationary or exponential growth phases. Nisin (0.15 mg/mL) alone decreased the viable counts in all cases (unheated and heated cells in stationary and exponential phase) although the two strains tested showed different sensitivity to this natural antimicrobial between them. When carvacrol or thymol were combined with nisin, it resulted in a greater loss of viability of heated cells than when nisin was applied alone. There was a synergistic effect of nisin and both essential oils with a mild heat pretreatment on the viability of B. cereus cells. This study pointed out the potential use of nisin alone and in combination with carvacrol or thymol applied after a mild heat pretreatment for preservation of minimally processed foods.
This study investigated the antimicrobial activity of 3 natural (thymol, carvacrol, and gallic acid) and 2 synthetic [butylated hydroxyanisole (BHA) and octyl gallate] phenolic compounds, individually and in binary combinations, on 4 dairy isolates of Enterococcus faecalis with different virulence factors (β-hemolytic, gelatinase, or trypsin activities; acquired resistance to erythromycin or tetracycline; and natural resistance to gentamicin). A checkerboard technique and a microdilution standardized method were used. All compounds individually tested exhibited antimicrobial activity against E. faecalis, with minimal inhibitory concentrations (MIC) ranging from 30 μg/mL (octyl gallate) to 3,150 μg/mL (gallic acid), although no significant differences were detected among strains to each phenolic compound. Carvacrol in combination with thymol or gallic acid, and gallic acid combined with octyl gallate showed partial synergistic inhibition of all E. faecalis strains. The most effective combinations were thymol + carvacrol and gallic acid + octyl gallate, as the MIC for each of these compounds was reduced by 67 to 75% compared with their respective individual MIC. These results highlight the possibility of using combinations of these phenolic compounds to inhibit the growth of potential virulent or spoilage E. faecalis strains by reducing the total amount of additives used in dairy foods.
We investigated the combined effect of three internal temperatures (57.5, 60, and 62.5°C) and different concentrations (0 to 3.0wt/wt.%) of sodium chloride (NaCl) and apple polyphenols (APP), individually and in combination, on the heat-resistance of a five-strain cocktail of Listeria monocytogenes in ground beef. A complete factorial design (3×4×4) was used to assess the effects and interactions of heating temperature, NaCl, and APP. All 48 combinations were tested twice, to yield 96 survival curves. Mathematical models were then used to quantitate the combined effect of these parameters on heat resistance of the pathogen. The theoretical analysis shows that compared with heat alone, the addition of NaCl enhanced and that of APP reduced the heat resistance of L. monocytogenes measured as D-values. By contrast, the protective effect of NaCl against thermal inactivation of the pathogen was reduced when both additives were present in combination, as evidenced by reduction of up to ~68% in D-values at 57.5°C; 65% at 60°C; and 25% at 62.5°C. The observed high antimicrobial activity of the combination of APP and low salt levels (e.g., 2.5% APP and 0.5% salt) suggests that commercial and home processors of meat could reduce the salt concentration by adding APP to the ground meat. The influence of the combined effect allows a reduction of the temperature of heat treatments as well as the salt content of the meat. Meat processors can use the predictive model to design processing times and temperatures that can protect against adverse effects of contaminated meat products. Additional benefits include reduced energy use in cooking, and the addition of antioxidative apple polyphenols may provide beneficial health affects to consumers.
This paper proposes a review of some alternative approaches for food stabilisation and shelf life prolonging (based on the use of natural compounds and/or non-thermal techniques). After a brief description of food structure implication on the way of using the alternative approaches, two paragraphs summarise the topics of natural molecules (essential oils, lysozyme, lactoferrin and lactoperoxidase system, fatty acids, chitosan) and non-thermal approaches (high hydrostatic and homogenisation pressures, pulsed electric fields, high power ultrasound and irradiation). Finally, the last sections deal with the use of combined hurdles (along with the proposal of three possible modes of action of a multi-target preservation), the mathematical approaches for shelf life evaluating and some critical issues to be addressed in the future for a real scaling up of the proposed techniques.
Traditional antimicrobials have been extensively used for many years. However, consumers are currently demanding wholesome, fresh-like, and safe foods without addition of chemically synthesized preservatives. The application of novel natural antimicrobials to assure safety of fresh-cut fruits and unpasteurized juices while preventing quality loss is a promising alternative. The effectiveness of these natural substances added to fruit derivatives has been studied by different researchers. Antimicrobials of animal (lactoperoxidase, lysozyme, and chitosan), plant (essential oils, aldehydes, esters, herbs, and spices), and microbial origin (nisin) can be used to effectively reduce pathogenic and spoilage microorganisms in fresh-cut fruits and fruit juices. Nevertheless, the use of these compounds at a commercial level is still limited due to several factors such as impact on sensory attributes or, in some cases, regulatory issues concerning their use. Therefore, extensive research on the effects of each antimicrobial on food sensory characteristics is still needed so that antimicrobial substances of natural origin can be regarded as feasible alternatives to synthetic ones.
The chemical composition of essential oils isolated from the aerial parts by hydrodistillation of Turkish Tanacetum aucheranum and Tanacetum chiliophyllum var. chiliophyllum were analyzed by GC–MS. The oils contain similar major components. The major components of T. aucheranum oil were 1,8-cineole (23.8%), camphor (11.6%), terpinen-4-ol (7.2%), α-terpineol (6.5%), borneol (3.8%), (E)-thujone (3.2%), epi-α-cadinol (3.1%), and artemisia ketone (3.0%). Camphor (17.9%), 1,8-cineole (16.6%) and borneol (15.4%) were found to be predominant constituents in the oil of T. chiliophyllum. It is interesting to find that ester derivatives of dihydro-α-cyclogeranic acid (2,2,6-trimethylcyclohexylcarboxylate), dihydro-α-cyclogeranyl hexanoate (10.1%), dihydro-α-cyclogeranyl pentanoate (3.0%), dihydro-α-cyclogeranyl butanoate (2.1%) and dihydro-α-cyclogeranyl propionate (1.2%) are firstly found as chemotaxonomically important components in T. chiliophyllum oil. From these, dihydro-α-cyclogeranyl hexanoate was isolated on silica gel column chromatography and its structure was confirmed by spectroscopic methods. This is the first report on the occurrence of ester derivatives of dihydro-α-cyclogeranic acid in essential oils of Tanacetum species. The oils were also characterized to have relatively high amounts of oxygenated monoterpenes. Results of the antifungal testing by microbial growth inhibition assays showed that the oils completely inhibit the growth of 30 phytopathogenic fungi. However, their growth inhibition effects were lower than commercial benomyl. The oils tested for antibacterial activity against 33 bacterial strains showed a considerable antibacterial activity over a wide spectrum. Herbicidal effects of the oils on seed germination of Amaranthus retroflexus, Chenopodium album and Rumex crispus were also determined and the oils completely inhibited the seed germination and seedling growth of the plants.
Different extracts of Caesalpinia mimosoides Lamk. (Leguminosae) were tested against eight human pathogenic bacteria and six fungal strains by the disc diffusion method. Among these extracts, the aqueous and the ethanolic extracts showed potent activity against some tested microorganisms. Subsequently, the latter extract was fractionated by means of Sephadex LH-20 column chromatography. A bioactive substance, responsible for the antimicrobial property was separated, and its structure was assigned as a known compound, gallic acid, by extensive chromatographic and spectroscopic analyses.
The Centers for Disease Control and Prevention (CDC) recently revised their estimates for the annual number of foodborne illnesses; 48 million Americans suffer from domestically acquired foodborne illness associated with 31 identified pathogens and a broad category of unspecified agents. Consequently, economic studies based on the previous estimates are now obsolete. This study was conducted to provide improved and updated estimates of the cost of foodborne illness by adding a replication of the 2011 CDC model to existing cost-of-illness models. The basic cost-of-illness model includes economic estimates for medical costs, productivity losses, and illness-related mortality (based on hedonic value-of-statistical-life studies). The enhanced cost-of-illness model replaces the productivity loss estimates with a more inclusive pain, suffering, and functional disability measure based on monetized quality-adjusted life year estimates. Costs are estimated for each pathogen and a broader class of unknown pathogens. The addition of updated cost data and improvements to methodology enhanced the performance of each existing economic model. Uncertainty in these models was characterized using Monte Carlo simulations in @Risk version 5.5. With this model, the average cost per case of foodborne illness was $1,626 (90% credible interval [CI], $607 to $3,073) for the enhanced cost-of-illness model and $1,068 (90% CI, $683 to $1,646) for the basic model. The resulting aggregated annual cost of illness was $77.7 billion (90% CI, $28.6 to $144.6 billion) and $51.0 billion (90% CI, $31.2 to $76.1 billion) for the enhanced and basic models, respectively.
Naturally occurring antimicrobial compounds could be applied as food preservatives to protect food quality and extend the shelf life of foods and beverages. These compounds are naturally produced and isolated from various sources, including plants, animals and microorganisms, in which they constitute part of host defense systems. Many naturally occurring compounds, such as nisin, plant essential oils, and natamycin, have been widely studied and are reported to be effective in their potential role as antimicrobial agents against spoilage and pathogenic microorganisms. Although some of these natural antimicrobials are commercially available and applied in food processing, their efficacy, consumer acceptance and regulation are not well defined. This manuscript reviews natural antimicrobial compounds with reference to their applications in food when applied individually or in combination with other hurdles. It also reviews the mechanism of action of selected natural antimicrobials, factors affecting their antimicrobial activities, and future prospects for use of natural antimicrobials in the food industry.
Interactions of monolaurin, eugenol (phenolic compound) and sodium citrate (chelator) on the growth of six organisms including common meat spoilage (Lactobacillus curvatus, Lactobacillus sake, Leuconostoc mesenteroides, Brochothrix thermosphacta) and pathogenic (Escherichia coli O157:H7 and Listeria monocytogenes) organisms were investigated. The combinations of 100 to 250 ppm monolaurin with 500 and 1000 ppm eugenol, and 0.2 and 0.4% sodium citrate were more effective than each component separately. More than one combination prevented detectable growth of each organism. Lactic acid bacteria (LAB) and E. coli O157:H7 were most resistant and L. monocytogenes and B. thermosphacta most sensitive to control by the chosen combinations. The presence of sodium citrate was necessary to yield potent inhibition of Lb. curvatus and Lb. sake growth by the monolaurin and eugenol combinations.
To evaluate the antibacterial activity of eugenol and its mechanism of bactericidal action against Salmonella typhi.
The antibacterial activity was checked by disc-diffusion method, MIC, MBC, time course assay and pH sensitivity assay. The chemo-attractant property of eugenol was verified by chemotaxis assay. The mode of action of eugenol was determined by crystal violet assay, measurement of release of 260 nm absorbing material, SDS-PAGE, FT-IR spectroscopy, AFM and SEM.
Treatment with eugenol at their MIC (0.0125%) and MBC (0.025%) reduced the viability and resulted in complete inhibition of the organism. Eugenol inactivated Salmonella typhi within 60 min exposure. The chemo-attractant property of eugenol combined with the observed high antibacterial activity at alkaline pH favors the fact that the compound can work more efficiently when given in vivo. Eugenol increased the permeability of the membrane, as evidenced by crystal violet assay. The measurement of release of 260 nm absorbing intracellular materials, SDS-PAGE, SEM and AFM analysis confirmed the disruptive action of eugenol on cytoplasmic membrane. The deformation of macromolecules in the membrane, upon treatment with eugenol was verified by FT-IR spectroscopy.
The results suggest that the antibacterial activity of eugenol against Salmonella typhi is due to the interaction of eugenol on bacterial cell membrane.
Heat resistance of Lactobacillus bulgaricus in skimmed milk at 62 degrees, 64 degrees, 65 degrees and 66 degrees C was studied. The response to increasing temperatures in this range was not linear, with temperatures at 65 degrees C and above giving a lower survival rate than would be predicted from experiments at lower temperatures. To identify sites of injury at these temperatures, chemical markers were used. Heating at 64 degrees C and below resulted in damage to the cytoplasmic membrane. At temperatures of 65 degrees C and above chemical markers also indicated damage in the cell wall and proteins. Using differential scanning calorimetry analysis of whole cells of Lact. bulgaricus seven main peaks were observed (1-51, m1-61, m2-73, n-80, p-89, q-100, r-112 degrees C). Three of these peaks (l(r), m(r) and p(r)) were the result of reversible reactions. Analysis of cell fractions identified the cell structure involved in giving rise to each of the three reversible peaks; l(r), cell membrane lipids, m(r), ribosomes, and p(r), DNA. The evidence presented in this paper shows that irreversible reactions in the cell ribosomes are a critical site of damage in Lact. bulgaricus during heat stress in liquid media at 65 degrees C and above.
This study investigates the antimicrobial activity and mode of action of two natural products, eugenol and thymol, a commonly utilized biostatic agent, triclocarban (TCC), and two surfactants, didecyldimethylammonium chloride (DDDMAC) and C10-C16 alkyldimethyl amine N-oxides (ADMAO).
Methods used included: determination of minimum inhibitory concentrations (MICs), lethal effect studies with suspension tests and the investigation of sub-MIC concentrations on growth of E. coli, Staph. aureus and Ps. aeruginosa using a Bioscreen microbiological analyser. Leakage of intracellular constituents and the effects of potentiating agents were also investigated. Only DDDMAC was bactericidal against all of the organisms tested. Eugenol, thymol and ADMAO showed bacteriostatic and bactericidal activity, but not against Ps. aeruginosa. TCC was only bacteristatic against Staph. aureus, but like the other agents, it did affect the growth of the other organisms in the Bioscreen experiments. All of the antimicrobial agents tested were potentiated by the permeabilizers to some extent and leakage of potassium was seen with all of the agents except TCC.
DDDMAC was bactericidal against all organisms tested and all compounds had some bacteriostatic action. Low level static effects on bacterial growth were seen with sub-MIC concentrations. Membrane damage may account for at least part of the mode of action of thymol, eugenol, DDDMAC and ADMAO.
The ingredients evaluated demonstrated a range of bactericidal and bacteriostatic properties against the Gram-negative and -positive organisms evaluated and the membrane (leakage of intracellular components) was implicated in the mode of action for most (except TCC). Sub-MIC levels of all ingredients did induce subtle effects on the organisms which impacted bacterial growth, even for those which had no true inhibitory effects.
The increasing consumer demand for 'fresh-like' foods has led to much research effort in the last 20 years to develop new mild methods for food preservation. Nonthermal methods allow micro-organisms to be inactivated at sublethal temperatures thus better preserving the sensory, nutritional and functional properties of foods. The aim of this review is to provide an overview of the microbiological aspects of the most relevant nonthermal technologies for microbial inactivation currently under study, including irradiation, high hydrostatic pressure, pulsed electric field and ultrasound under pressure. Topics covered are the mechanisms of inactivation, sensitivity of different microbial groups and factors affecting it and kinetics of inactivation.
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