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Article ; Online: Relationship between iron bioavailability and Salmonella Typhimurium fitness in raw and pasteurized liquid whole egg.

Guillén, Silvia / Cebrián, Guillermo

2022 Volume 104, Page(s) 104008

Abstract: Salmonella: Enteritidis growth rates in liquid whole egg have been shown to be dependent on the initial inoculum dose and on the egg product's thermal history. This study's objective is to obtain further insight into the mechanisms underlying both ... ...

Abstract	Salmonella: Enteritidis growth rates in liquid whole egg have been shown to be dependent on the initial inoculum dose and on the egg product's thermal history. This study's objective is to obtain further insight into the mechanisms underlying both phenomena. First we verified that Salmonella Typhimurium ATCC 14028s cells displayed the behavior already described for S. Enteritidis cells. Then, we carried out supplementation assays by adding different concentrations of egg-white antimicrobial proteins, iron, or siderophores to the egg samples (raw or pasteurized liquid whole egg, depending on the assay). These experiments revealed that addition of lysozyme (at the concentration at which it is present in liquid whole egg) did not affect Salmonella growth in pasteurized liquid whole egg, but that ovotransferrin as well as Ex-FABP caused a significant (p < 0.05) reduction in Salmonella growth rates in whole egg pasteurized at 70 °C for 1.5 min. Furthermore, we observed that the inactivation of ovotransferrin was dependent on treatment intensity within the range studied. On the other hand, addition of iron or siderophores to raw or low temperature (60 °C/3.5 min) pasteurized liquid whole egg increased the growth rate of Salmonella cells inoculated at a low initial dose. The concentration of these supplements required to reach the growth rate of cells inoculated at a high dose was lower for pasteurized than for raw egg. Finally, growth of a set of deletion mutants in genes coding for proteins related to different iron uptake systems, along with supplementation assays using spent medium revealed the key role of salmochelin in growth of S. Typhimurium in raw whole egg. In summary, our results strongly suggest that iron bioavailability determines the fitness (growth rates) of Salmonella cells in liquid whole egg. Thus, the higher the intensity of the thermal treatment applied to liquid egg, the more iron would be available, a phenomenon that would be linked to the denaturation of iron and/or siderophore binding egg proteins. Further work is still required to fully elucidate why lower Salmonella initial doses lead to lower growth rates, but it can be hypothesized that this might be related to a lower amount of siderophores being released to the medium (especially salmochelin), which would also limit iron bioavailability.
MeSH term(s)	Biological Availability ; Eggs ; Iron ; Salmonella typhimurium
Chemical Substances	Iron (E1UOL152H7)
Language	English
Publishing date	2022-02-23
Publishing country	England
Document type	Journal Article
ZDB-ID	50892-5
ISSN	1095-9998 ; 0740-0020
ISSN (online)	1095-9998
ISSN	0740-0020
DOI	10.1016/j.fm.2022.104008
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Article: Relationship between iron bioavailability and Salmonella Typhimurium fitness in raw and pasteurized liquid whole egg

Guillén, Silvia / Cebrián, Guillermo

Food microbiology. 2022 June, v. 104

2022

Abstract: Enteritidis growth rates in liquid whole egg have been shown to be dependent on the initial inoculum dose and on the egg product's thermal history. This study's objective is to obtain further insight into the mechanisms underlying both phenomena. First ... ...

Abstract	Enteritidis growth rates in liquid whole egg have been shown to be dependent on the initial inoculum dose and on the egg product's thermal history. This study's objective is to obtain further insight into the mechanisms underlying both phenomena. First we verified that Salmonella Typhimurium ATCC 14028s cells displayed the behavior already described for S. Enteritidis cells. Then, we carried out supplementation assays by adding different concentrations of egg-white antimicrobial proteins, iron, or siderophores to the egg samples (raw or pasteurized liquid whole egg, depending on the assay). These experiments revealed that addition of lysozyme (at the concentration at which it is present in liquid whole egg) did not affect Salmonella growth in pasteurized liquid whole egg, but that ovotransferrin as well as Ex-FABP caused a significant (p < 0.05) reduction in Salmonella growth rates in whole egg pasteurized at 70 °C for 1.5 min. Furthermore, we observed that the inactivation of ovotransferrin was dependent on treatment intensity within the range studied. On the other hand, addition of iron or siderophores to raw or low temperature (60 °C/3.5 min) pasteurized liquid whole egg increased the growth rate of Salmonella cells inoculated at a low initial dose. The concentration of these supplements required to reach the growth rate of cells inoculated at a high dose was lower for pasteurized than for raw egg. Finally, growth of a set of deletion mutants in genes coding for proteins related to different iron uptake systems, along with supplementation assays using spent medium revealed the key role of salmochelin in growth of S. Typhimurium in raw whole egg. In summary, our results strongly suggest that iron bioavailability determines the fitness (growth rates) of Salmonella cells in liquid whole egg. Thus, the higher the intensity of the thermal treatment applied to liquid egg, the more iron would be available, a phenomenon that would be linked to the denaturation of iron and/or siderophore binding egg proteins. Further work is still required to fully elucidate why lower Salmonella initial doses lead to lower growth rates, but it can be hypothesized that this might be related to a lower amount of siderophores being released to the medium (especially salmochelin), which would also limit iron bioavailability.
Keywords	Salmonella Typhimurium ; bioavailability ; denaturation ; egg albumen ; eggs ; food microbiology ; inoculum ; iron ; liquid egg products ; liquids ; lysozyme ; pasteurization ; raw eggs ; siderophores ; temperature
Language	English
Dates of publication	2022-06
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	50892-5
ISSN	1095-9998 ; 0740-0020
ISSN (online)	1095-9998
ISSN	0740-0020
DOI	10.1016/j.fm.2022.104008
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Article ; Online: Modelling the low temperature growth boundaries of Salmonella Enteritidis in raw and pasteurized egg yolk, egg white and liquid whole egg: Influence of the initial concentration.

Guillén, Silvia / Domínguez, Lara / Mañas, Pilar / Álvarez, Ignacio / Carrasco, Elena / Cebrián, Guillermo

International journal of food microbiology

2024 Volume 414, Page(s) 110619

Abstract: Salmonella is the most frequently reported cause of foodborne outbreaks with known origin in Europe, with eggs and egg products standing out as the most frequent food source (when it was known). The growth and survival of Salmonella in eggs and egg ... ...

Abstract	Salmonella is the most frequently reported cause of foodborne outbreaks with known origin in Europe, with eggs and egg products standing out as the most frequent food source (when it was known). The growth and survival of Salmonella in eggs and egg products have been extensively studied and, recently, it has been reported that factors such as the initial concentration and thermal history of the egg product can also influence its growth capability. Therefore, the objective of this study was to define the boundary zones of the growth/no growth domain of Salmonella Enteritidis (4 strains) as a function of temperature (low temperature boundary) and the initial concentration in different egg products. A series of polynomial logistic regression equations were successfully adjusted, allowing the study of these factors and their interaction on the probability of growth of S. Enteritidis in these products. Results obtained indicate that the minimum growth temperatures of Salmonella Enteritidis are higher in egg white (9.5-18.3 °C) than in egg yolk (7.1-7.8 °C) or liquid whole egg (7.2-7.9 °C). Results also demonstrate that in raw liquid whole egg and raw and pasteurized egg white, the minimum growth temperature of Salmonella Enteritidis does depend on the initial concentration. Similarly, the previous thermal history of the egg product only influenced the minimum growth temperature in some of them. On the other hand, large differences in the minimum growth temperatures among strains were observed in some products (up to approx. 6 °C in egg white). Finally, it should be noted that none of the strains grew at 5 °C under any of the conditions assayed. Therefore, storage of egg products (particularly whole liquid egg and egg yolk) below this temperature might be regarded/proposed as a good management approach. Our experimental approach has allowed us to provide a more accurate prediction of S. Enteritidis minimum growth temperatures in egg products by taking into account additional factors (initial concentration and thermal history) while also providing a quantification of the intra-specie variability. This would be of high relevance for improving the safety of egg products.
MeSH term(s)	Animals ; Salmonella enteritidis ; Egg Yolk ; Temperature ; Egg White ; Eggs ; Food Microbiology ; Colony Count, Microbial ; Chickens
Language	English
Publishing date	2024-02-06
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	87122-9
ISSN	1879-3460 ; 0168-1605
ISSN (online)	1879-3460
ISSN	0168-1605
DOI	10.1016/j.ijfoodmicro.2024.110619
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Article ; Online: Effect of the Application of Ultrasound to Homogenize Milk and the Subsequent Pasteurization by Pulsed Electric Field, High Hydrostatic Pressure, and Microwaves

Astráin-Redín, Leire / Skipnes, Dagbjørn / Cebrián, Guillermo / Álvarez-Lanzarote, Ignacio / Rode, Tone Mari

Foods. 2023 Mar. 29, v. 12, no. 7

2023

Abstract: The efficacy of applying ultrasound (US) as a system to homogenize emulsions has been widely demonstrated. However, research has not yet shown whether the effect achieved by homogenizing milk with US is modified by subsequent pasteurization treatments ... ...

Abstract	The efficacy of applying ultrasound (US) as a system to homogenize emulsions has been widely demonstrated. However, research has not yet shown whether the effect achieved by homogenizing milk with US is modified by subsequent pasteurization treatments that use new processing technologies such as pulsed electric fields (PEF), microwaves (MW), and high hydrostatic pressure (HPP). The aim of this study was, therefore, to optimize the application of US for milk homogenization and to evaluate the effect of PEF, HPP, and MW pasteurization treatments on the sensorial, rheological, and microbiological properties of milk throughout its shelf life. To homogenize whole milk, a continuous US system (20 kHz, 0.204 kJ/mL, 100%, 40 °C) was used, and different ultrasonic intensities (0.25, 0.5, and 1.0 kJ/mL) were evaluated. The optimal ultrasonic treatment was selected on the basis of fat globule size distribution and pasteurization treatments by MW (5800 W, 1.8 L/min), PEF (120 kJ/kg, 20 kV/cm) and HPP (600 MPa, 2 min, 10 °C) was applied. The ultrasound intensity that achieved the highest reduction in fat globule size (0.22 ± 0.02 µm) and the most homogeneous distribution was 1.0 kJ/mL. Fat globule size was smaller than in commercial milk (82% of volume < 0.5 µm for US milk versus 97% of volume < 1.2 µm for commercial milk). That size was maintained after the application of the different pasteurization treatments, and the resulting milk had better emulsion stability than commercial milk. After 28 days of storage, no differences in viscosity (4.4–4.9 mPa s) were observed. HPP pasteurization had the greatest impact on color, leading to higher yellowness values than commercial milk. Microbial counts did not vary significantly after 28 days of storage, with counts below 10² CFU/mL for samples incubated at 15 °C and at 37 °C. In summary, the homogenization of milk obtained by US was not affected by subsequent pasteurization processes, regardless of the technology applied (MW, PEF, or HPP). Further research is needed to evaluate these procedures’ effect on milk’s nutritional and functional properties.
Keywords	color ; emulsions ; high pressure treatment ; homogenization ; pasteurization ; pulsed electric fields ; shelf life ; ultrasonic treatment ; ultrasonics ; viscosity ; whole milk
Language	English
Dates of publication	2023-0329
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article ; Online
ZDB-ID	2704223-6
ISSN	2304-8158
ISSN	2304-8158
DOI	10.3390/foods12071457
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Evaluation of Pulsed Electric Fields (PEF) Parameters in the Inactivation of Anisakis Larvae in Saline Solution and Hake Meat

Abad, Vanesa / Alejandre, Marta / Hernández-Fernández, Elena / Raso, Javier / Cebrián, Guillermo / Álvarez-Lanzarote, Ignacio

Foods. 2023 Jan. 06, v. 12, no. 2

2023

Abstract: Larvae of the nematode family Anisakidae are capable of causing parasitic infections in humans associated with the consumption of fishery products, leading to intestinal syndromes and allergic reactions. Anisakidae larvae are widely distributed ... ...

Abstract	Larvae of the nematode family Anisakidae are capable of causing parasitic infections in humans associated with the consumption of fishery products, leading to intestinal syndromes and allergic reactions. Anisakidae larvae are widely distributed geographically, with rates of parasitism close to 100% in certain fish species. Methods need to be established for their inactivation and elimination, especially in fishery products that are to be consumed raw, pickled, or salted, or which have been insufficiently treated to kill the parasite. Many strategies are currently available (such as freezing and heat treatment), but further ones, such as pulsed electric fields (PEF), have hardly been investigated until now. This study focuses on the experimental evaluation of the efficacy of PEF in the inactivation of Anisakis spp. larvae in terms of electric field strength, specific energy, and pulse width, as well as on the evaluation of the quality of fish samples after PEF treatment. Results show that viability of Anisakis was highly dependent on field strength and specific energy. Pulse width exerted a considerable influence at the lowest field strengths tested (1 kV/cm). Central composite design helped to define a PEF treatment of 3 kV/cm and 50 kJ/kg as the one capable of inactivating almost 100% of Anisakis present in pieces of hake, while affecting the investigated quality parameters (moisture, water holding capacity, and cooking loss) to a lesser extent than freezing and thawing. These results show that PEF could serve as an alternative to traditional freezing processes for the inactivation of Anisakis in fish.
Keywords	Anisakis ; electric field ; fisheries ; hake ; heat treatment ; intestines ; meat ; parasites ; parasitism ; sodium chloride ; specific energy ; viability
Language	English
Dates of publication	2023-0106
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article ; Online
ZDB-ID	2704223-6
ISSN	2304-8158
ISSN	2304-8158
DOI	10.3390/foods12020264
Database	NAL-Catalogue (AGRICOLA)

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Article: Evaluation of Pulsed Electric Fields (PEF) Parameters in the Inactivation of

Abad, Vanesa / Alejandre, Marta / Hernández-Fernández, Elena / Raso, Javier / Cebrián, Guillermo / Álvarez-Lanzarote, Ignacio

Foods (Basel, Switzerland)

2023 Volume 12, Issue 2

Abstract: Larvae of the nematode ... ...

Abstract	Larvae of the nematode family
Language	English
Publishing date	2023-01-06
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2704223-6
ISSN	2304-8158
ISSN	2304-8158
DOI	10.3390/foods12020264
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Article: Effect of the Application of Ultrasound to Homogenize Milk and the Subsequent Pasteurization by Pulsed Electric Field, High Hydrostatic Pressure, and Microwaves.

Astráin-Redín, Leire / Skipnes, Dagbjørn / Cebrián, Guillermo / Álvarez-Lanzarote, Ignacio / Rode, Tone Mari

Foods (Basel, Switzerland)

2023 Volume 12, Issue 7

Abstract	The efficacy of applying ultrasound (US) as a system to homogenize emulsions has been widely demonstrated. However, research has not yet shown whether the effect achieved by homogenizing milk with US is modified by subsequent pasteurization treatments that use new processing technologies such as pulsed electric fields (PEF), microwaves (MW), and high hydrostatic pressure (HPP). The aim of this study was, therefore, to optimize the application of US for milk homogenization and to evaluate the effect of PEF, HPP, and MW pasteurization treatments on the sensorial, rheological, and microbiological properties of milk throughout its shelf life. To homogenize whole milk, a continuous US system (20 kHz, 0.204 kJ/mL, 100%, 40 °C) was used, and different ultrasonic intensities (0.25, 0.5, and 1.0 kJ/mL) were evaluated. The optimal ultrasonic treatment was selected on the basis of fat globule size distribution and pasteurization treatments by MW (5800 W, 1.8 L/min), PEF (120 kJ/kg, 20 kV/cm) and HPP (600 MPa, 2 min, 10 °C) was applied. The ultrasound intensity that achieved the highest reduction in fat globule size (0.22 ± 0.02 µm) and the most homogeneous distribution was 1.0 kJ/mL. Fat globule size was smaller than in commercial milk (82% of volume < 0.5 µm for US milk versus 97% of volume < 1.2 µm for commercial milk). That size was maintained after the application of the different pasteurization treatments, and the resulting milk had better emulsion stability than commercial milk. After 28 days of storage, no differences in viscosity (4.4-4.9 mPa s) were observed. HPP pasteurization had the greatest impact on color, leading to higher yellowness values than commercial milk. Microbial counts did not vary significantly after 28 days of storage, with counts below 10
Language	English
Publishing date	2023-03-29
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2704223-6
ISSN	2304-8158
ISSN	2304-8158
DOI	10.3390/foods12071457
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Article: Relationship between growth ability, virulence, and resistance to food-processing related stresses in non-typhoidal Salmonellae

Guillén, Silvia / Marcén, María / Fau, Ester / Mañas, Pilar / Cebrián, Guillermo

International journal of food microbiology. 2022 Jan. 16, v. 361

2022

Abstract: The ability of Salmonella to resist and adapt to harsh conditions is one of the major features that have made this microorganism such a relevant health hazard. However, the impact of these resistance responses on other aspects of Salmonella physiology, ... ...

Abstract	The ability of Salmonella to resist and adapt to harsh conditions is one of the major features that have made this microorganism such a relevant health hazard. However, the impact of these resistance responses on other aspects of Salmonella physiology, such as virulence and growth ability, is still not fully understood. The objective of this study was to determine the maximum growth rates (in three different media), virulence (adhesion and invasion of Caco-2 cells), and other phenotypic characteristics (biofilm-forming ability and antimicrobial resistance) of 23 Salmonella strains belonging to different serovars, and to compare them with their previously determined stress resistance parameters. Significant differences (p < 0.05) in growth rates, virulence, and biofilm-forming ability were found among the 23 strains studied. Nevertheless, whereas less than 3-fold change between the lowest and the highest growth rate was observed, the percentage of cells capable of invading Caco-2 cells varied more than 100-fold, that to form biofilms more than 30-fold, and the antibiotic MICs varied up to 512-fold, among the different strains. Results indicate that those strains with the highest cell adhesion ability were not always the most invasive ones and suggest that, in general terms, a higher stress resistance did not imply a reduced growth ability (rate). Similarly, no association between stress resistance and biofilm formation ability (except for acid stress) or antibiotic resistance (with minor exceptions) was found. Our data also suggest that, in Salmonella, acid stress resistance would be associated with virulence, since a positive correlation of that trait with adhesion and a negative correlation with invasion was found. This study contributes to a better understanding of the physiology of Salmonella and the relationship between bacterial stress resistance, growth ability, and virulence. It also provides new data regarding intra-specific variability of a series of phenotypic characteristics of Salmonella that are relevant from the food safety perspective.
Keywords	Salmonella ; acid tolerance ; adhesion ; antibiotic resistance ; antibiotics ; biofilm ; cell adhesion ; food microbiology ; food processing ; food safety ; health hazards ; intraspecific variation ; phenotype ; physiology ; serotypes ; stress tolerance ; virulence
Language	English
Dates of publication	2022-0116
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	87122-9
ISSN	1879-3460 ; 0168-1605
ISSN (online)	1879-3460
ISSN	0168-1605
DOI	10.1016/j.ijfoodmicro.2021.109462
Database	NAL-Catalogue (AGRICOLA)

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Article: Differences in resistance to different environmental stresses and non-thermal food preservation technologies among Salmonella enterica subsp. enterica strains

Guillén, Silvia / Marcén, María / Mañas, Pilar / Cebrián, Guillermo

Food research international. 2020 June, v. 132

2020

Abstract: In this work the resistance of 15 strains belonging to 11 serovars of Salmonella enterica subsp. enterica to several different environmental stresses (acid, hydrogen peroxide, NaCl and heat) and non-thermal food preservation technologies (HHP, PEF, UV) ... ...

Abstract	In this work the resistance of 15 strains belonging to 11 serovars of Salmonella enterica subsp. enterica to several different environmental stresses (acid, hydrogen peroxide, NaCl and heat) and non-thermal food preservation technologies (HHP, PEF, UV) was determined and compared. Results obtained showed that differences in resistance among strains, quantified as 2D-values, varied less than 2.4-fold for all agents, including heat if S. senftenberg 775W is excluded from the analysis. These results also indicate that variability in resistance among strains of the same serovar was comparable to inter-serovar variability. Salmonella strains that were the most resistant to a given stress were not more resistant to other types of stress. Nevertheless, a positive correlation was observed between the resistance of Salmonella strains to oxidative and osmotic stress, as well as between UV and PEF resistance. These results would be especially helpful in defining safe food preservation processes and might be very useful for improving quantitative microbiological risk assessments of Salmonella in food products.
Keywords	Salmonella enterica subsp. enterica ; food preservation ; foods ; heat ; hydrogen peroxide ; osmotic stress ; risk assessment ; serotypes ; sodium chloride
Language	English
Dates of publication	2020-06
Publishing place	Elsevier Ltd
Document type	Article
ZDB-ID	1111695-x
ISSN	1873-7145 ; 0963-9969
ISSN (online)	1873-7145
ISSN	0963-9969
DOI	10.1016/j.foodres.2020.109042
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Article ; Online: Differences in resistance to different environmental stresses and non-thermal food preservation technologies among Salmonella enterica subsp. enterica strains.

Guillén, Silvia / Marcén, María / Mañas, Pilar / Cebrián, Guillermo

Food research international (Ottawa, Ont.)

2020 Volume 132, Page(s) 109042

Abstract	In this work the resistance of 15 strains belonging to 11 serovars of Salmonella enterica subsp. enterica to several different environmental stresses (acid, hydrogen peroxide, NaCl and heat) and non-thermal food preservation technologies (HHP, PEF, UV) was determined and compared. Results obtained showed that differences in resistance among strains, quantified as 2D-values, varied less than 2.4-fold for all agents, including heat if S. senftenberg 775W is excluded from the analysis. These results also indicate that variability in resistance among strains of the same serovar was comparable to inter-serovar variability. Salmonella strains that were the most resistant to a given stress were not more resistant to other types of stress. Nevertheless, a positive correlation was observed between the resistance of Salmonella strains to oxidative and osmotic stress, as well as between UV and PEF resistance. These results would be especially helpful in defining safe food preservation processes and might be very useful for improving quantitative microbiological risk assessments of Salmonella in food products.
MeSH term(s)	Drug Resistance, Bacterial/drug effects ; Food Handling ; Food Microbiology ; Food Preservation ; Hot Temperature ; Hydrogen Peroxide ; Osmotic Pressure ; Oxidation-Reduction ; Risk Assessment ; Salmonella/physiology ; Stress, Physiological
Chemical Substances	Hydrogen Peroxide (BBX060AN9V)
Language	English
Publishing date	2020-01-30
Publishing country	Canada
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1111695-x
ISSN	1873-7145 ; 0963-9969
ISSN (online)	1873-7145
ISSN	0963-9969
DOI	10.1016/j.foodres.2020.109042
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