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The effects of essential oils on inactivation of Listeria monocytogenes in Rainbow Trout cooked with sous‐vide

Journal of Food Processing and Preservation

August 2021
45(11)

DOI:10.1111/jfpp.15878

Authors:

Fatma Öztürk

Izmir Kâtip Çelebi University

Hatice Gündüz

Izmir Kâtip Çelebi University

Goknur Surengil

Isparta University of Applied Sciences

In this study was investigated combined effect of 4 different natural antimicrobial essential oil (Rosemary, Coriander, Basil and Laurel) and 2 different cooking temperatures (50 and 55 °C) on inactivating of Listeria monocytogenes in rainbow trout. The products prepared with this technology were stored at +4 °C for 36 days and the number of L. monocytogenes was determined. As a result of this study, laurel essential oil was found to be effective on L. monocytogenes invitro whereas coriander essential oil was found to be effective on L. monocytogenes in sous‐vide applied trout. In addition, coriander essential oil addition (2 times more than the MIC value) and 7 min sous‐vide application in 55 °C was effective for the inhibition of L. monocytogenes in sous‐vide applied trouts. Consequently, the findings indicated that the use of coriender essential oil in sous‐vide trout fillets was effective to ensure of L. monocytogenes control.

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https://doi.org/10.1111/jfpp.15878

1 | INTRODUCTION

Sous- vide which means “under vacuum,” and sous- vide process-

ing is defined as “raw materials or raw materials with intermediate

foods that are cooked under controlled conditions of tempera-

ture and time inside heat- stable vacuumized pouches.” Sous- vide

processing prevents evaporative losses of moisture and volatile

components during the cooking of foods. It also retains the color

and texture properties of the product and limits the risk of cross-

contamination during storage. In this way, delicious and nutritious

products are obtained (Baldwin, 2012; Schellekens, 1996; Sun

et al., 2019).

Although Sous- vide Technology offers products with enhancing

nutritional value, high quality and extended shelf life, pathogen mi-

croorganisms may grow that can cause health hazards due to low

temperature applied to products in a short time. Therefore, the

temperature- time parameters and the use of antimicrobials are very

important in the cooking process (Church, 1998).

Most of the essential oils and their components exhibit antibac-

terial properties and these are used for the inhibition of pathogenic

Received:24July2019

Revised:8M arch2021

Accepted:1August2021

DOI: 10.1111/jfpp.15878

ORIGINAL ARTICLE

The effects of essential oils on inactivation of Listeria

monocytogenes in rainbow trout cooked with sous- vide

Fatma Öztürk1 | Hatice Gündüz1 | Göknur Sürengil1,2

1Department of Fisheries and Fish

Processing Technology, Faculty of Fisheries,

Izmir Katip Celebi University, Izmir, Turkey

2Department of Fishing and Processing

Technology,FacultyofEğirdirFisheries,

University of Isparta Applied Sciences,

Isparta, Turkey

Correspondence

Fatma Öztürk, Faculty of Fisheries,

Department of Fisheries and Fish Processing

Technology, Izmir Katip Celebi University,

Izmir, Turkey.

Email: fatma.ozturk@ikc.edu.tr

Funding information

İzmirKatipÇelebiUniversity,Grant/Award

N u m b e r :  2 0 1 6 - G A P - S U Ü F - 0 0 1 8

Abstract

This study investigated the combined effect of four different natural antimicrobial

essential oil (Rosemary, Coriander, Basil and Laurel) and two different cooking tem-

peratures (50℃ and 55℃) on inactivating of Listeria monocytogenes in rainbow trout.

The products prepared with this technology were stored at +4℃ for 36 days and the

number of L. monocytogenes was determined. As a result of this study, laurel essential

oil was found to be effective on L. monocytogenes invitro whereas coriander essen-

tial oil was found to be effective on L. monocytogenes in sous- vide applied trout. In

addition, coriander essential oil addition (2 times more than the minimum inhibition

concentration value) and 7 min sous- vide application in 55℃ was effective for the

inhibition of L. monocytogenes in sous- vide applied trouts. Consequently, the findings

indicated that the use of coriander essential oil in sous- vide trout fillets was effective

to ensure of L. monocytogenes control.

Practical applications

Sous- vide technology is a long- term cooking method in vacuum- packed food at low

temperatures. Thanks to this application, since the products are cooked in vacuum

packaging, the unique aroma and nutritional components of the foods are not lost.

This technology offers products with high nutritional value, quality, and high shelf

life. Although it is more advantageous than traditional cooking methods, if the ap-

plied temperature is low and the time is insufficient, pathogenic microorganisms de-

velop and pose a threat to health. For this reason, the temperature- time parameters

and the use of antimicrobials used in cooking are of great importance. In this re-

search, it was determined that the development of Listeria monocytogenes in seafood

was prevented by using essential oils with sous- vide technology.

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ÖZTÜRK e T al.

bacteria in foods (Amoroso et al., 2019; Burt, 2004). Increasing con-

sumer demand for the use of natural antimicrobials instead of chem-

ical antimicrobial agents has led to the widespread use of essential

oilsasadditivesinfoods(Gouveiaetal.,2017).

Many studies have focused on the quality of vegetables, meat and

meat products prepared with sous- vide technology (Alahakoon et al.,

2018, 2019; Ismail et al., 2019; Martínez- Hernández et al., 2013;

Muñoz et al., 2017; Oliveira et al., 2013; Rinaldi et al., 2013, 2014).

The effects of different temperature- time combinations on physical,

chemical and microbiological quality parameters were investigated

in the studies conducted on the use of this technology in seafood

(Cetinkaya et al., 2015; Gonzalez-Fandos et al., 2004, 2005; Mol

et al., 2012). In another study, the effect of lemon juice on the qual-

ity of whiting fish cooked in a vacuum was determined (Cosansu

et al., 2013). However, there are few studies on the inactivation of

Listeria monocytogenes in products prepared with sous- vide (Ben

Embarek & Huss, 1993; Bolton et al., 200 0; Hansen & Knochel, 2001;

Nyatı,2000).L. monocytogenes is one of the high temperature resis-

tant foodborne pathogens which is also capable of developing during

refrigeration temperature. Therefore, the development of heat-

resistant L. monocytogenes in sous- vide products, which are mild heat

treated and stored in the cold, is a concern (Hansen & Knochel, 2001).

It is known that the effect of essential oils in the control of patho-

genic microorganisms in foods is very important and there are many

researches on this subject (Abdollahzadeh et al., 2014; Azeredo

et al., 2011; Da Silveira et al., 2014; De Medeiros Ba rbosa et al., 2016;

Dussaultetal.,2014;Ghabraieetal.,2016;Gilletal.,2002;Gutierrez

et al., 2008; Khalil et al., 2018; Mazzarrino et al., 2015; Ouibrahim

et al., 2013; Pesavento et al., 2015; Tosun et al., 2018). However,

only a few studies have been performed on the use of essential oils

on the inactivation of L. monocytogenes, which is a significant prob-

lem in foods that are ready- to- eat products and processed at low

temperatures-timeswithsous-videapplication(Gouveiaetal.,2016,

2017). No studies have been conducted to use the essential oils in

the control of L. monocytogenes in the seafood applied sous- vide.

The aim of this study was to investigate the effect of antimicrobial

essential oils and different temperature applications on the inactiva-

tion of L. monocytogenes in vacuum- packed cooked trout fillets. For

this purpose, rosemary, coriander, basil, and laurel essential oils were

added to the trout fi llets and vacuum p acked, then cooked at different

temperatures (50℃ and 55℃) in a stability time (7 min). After cook-

ing, the cooled products were stored at +4℃ and L. monocytogenes

counts were determined on 0, 1, 3, 6, 9, 12, 15, 22, 29, and 36 days.

2 | MATERIALS AND METHODS

2.1 | Material

2.1.1 | Fishmaterialandessentialoils

Rainbow trout fillets (approximately, 40 fillets) were purchased from

a fish processing plant in Turkey, and they were transferred to the

laboratory (for sous- vide application and analysis) in polystyrene

boxes containing ice. Rosemary (Rosmarinus officinalis), coriander

(Coriandrum sativum), basil (Ocimum basilicum), and laurel (Laurus no-

bilis) essential oils were obtained from a commercial company.

2.1.2 | Testmicroorganismsandmedia

In the study, the strain of L. monocytogenes ATCC 7644 was obtained

from a commercial company. Tryptic Soy Broth (TSB, Merck), Tryptic

Soy Agar ( TSB, Merck), Müller Hilton Agar (MHA , Merck), and Müller

Hilton Broth (MHB, Merck) media were used for the activation of

bacteria and measurement of the antibacterial activity of essential

oils.

2.2 | Methods

2.2.1 | Determinationofbiochemicalcompositionof

essential oils

GC-MSanalysiswasperformedtodeterminethemaincomponents

of essenti al oils. GC-MS assays we re perfor med using the A gilent

5975CS eries GC-MSD sy stem (7890A GC an d 5975Cine rt MSD)

equipped with HP- 5MS capillary (30 m × 0.25 mm, film thickness

0.50 µm). The sample injection volume was 1 µl. The initial oven tem-

perature was programmed at 60℃, in 3 degree increments, the final

temperature was brought to 260℃ and terminated. MS transfer line

temperature was set at 230℃. The MS system was operated in scan

mode with a mass range of 40– 400 m/z. Helium was used as carrier

gas. The inlet temperature was 250℃.

2.2.2 | Preparationofbacterialinoculum

Stock cultures of L. monocytogenes in liquid form were maintained

at−20± 2℃ in TSB medium containing glycerol (20%; v/v). For ex-

periments, 100 µl of stock cultures were transferred to 10 ml of TSB

medium and incubated at 30℃ for 24 hr to activate the bacteria.

The active bacterial cultures were transferred to centrifuge tubes at

10 ml each and centrifuged for 15 min at 6,000 rpm (Hermle Z206A).

Cell pellets suspended using physiological saline (PSW ) were washed

twice again by centrifugation. After centrifugation, PSW was added

to the pellet fraction obtained and the cell densities were adjusted to

0.5 Mcfarland (108 CFU/ml) turbidity so the bacteria inoculum was

prepared for the experiments.

2.2.3 | Determinationofantibacterialeffectsof

essential oils

Disk diffusion method (Kirby- Bauer method)

Disc diffusion method was used to determine the antibacterial activ-

ity of essential oils. Active cultures of L. monocytogenes ATCC 7644

were adjusted to 0.5 Mcfarland standard density by diluting with

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ÖZTÜRK e T al.

sterile PSW. In this way, the prepared bacterial inoculum was applied

to petri dishes containing MHA by means of sterile swab rod. 20 µl of

essential oil was impregnated into sterile empty discs placed in petri

dishes. Sterile 10% DMSO (Dimethyl Sulphoxide) was used as a neg-

ative control. Sulphamethoxazole/trimethoprim (SXT, 25 µg), ampi-

cillin (AMP; 10 µg) and erythromycin (E, 15 µg) discs were used as

positive controls. The medium was incubated at 30℃ for 24– 48 hr.

After the incubation, the zone diameters were determined and anti-

bacterial activity was determined.

Minimum inhibition concentration (MIC) and minimum bactericidal

concentration (MBC)

MIC and MBC were used to determine the in vitro activity of essen-

tial oils. MIC values of essential oils were determined by the macro

dilution method (Baron & Finegold, 1990). The lowest essential

oil concentration without microbial growth was evaluated by MIC

value. Stock solutions of essential oils (100 mg/ml) were prepared

using 10% DMSO. 570 µl of MHB was transferred to each of the

15 sterile test tubes. Two- fold serial dilutions were made by add-

ing 600 µl of the stock solution of essential oils to the first tube,

and added dilutions with essential oils. L. monocytogenes ATCC 7644

strain was added to 30 µl of 106 log CFU/g on each dilution tube and

incubated at 30℃ for 24 hr (Oke et al., 2009). After incubation, the

bacterial development of the tubes was evaluated visually also the

final dilution without development was accepted as MIC value. In

addition, after incubation each dilution tube was transferred to ster-

ile cuvettes, then the absorbance values were evaluated the 543 nm

wavelength by spectrophotometer. The visually determined MIC

value was compared and verified with the MIC value determined by

the optical density. 600 µl MHB + 600 µl essential oil as negative

control; 600 µl MHB + 30 µl bacteria and 600 µl MHB + 600 µl 10%

DMSO containing tubes were used as positive control. Trials were

performed as two replicates for each essential oils (Oke et al., 2009).

The lowest concentration of non- reproduction was determined

as MBC by sowing to the PALCAM Agar from the determined

MIC concentration and their upper concentrations (García-Díez

et al., 2017; Hu et al., 2012).

2.2.4 | Determinationoftheeffectofsous-vide

technology and essential oil supplementation on

L. monocytogenes in fish fillets

Preparation of sous- vide fish fillets

L. monocytogenes were grown in TSB medium at 30℃ for 24 hr. The

active cultures were centrifuged for 15 min at 6,000 rpm. The cell

pellets were adjusted to 0.5 Mcfarland (108 CFU/ml) standard den-

sity by diluting with PSW. Fish fillets were cut into pieces weighing

10 g each. Each piece was inoculated with 500 µl of a 108 CFU/ml

of L. monocytogenes. The inoculated samples were kept at 4℃ for

10 min for the attachment of pathogens. The inoculated samples

with L. monocytogenes were divided into five groups as control (not

essential oil), rosemary added, coriander added, basil added, and lau-

rel added. Then, 100 µl of essential oil (two times the concentration

of MIC) was added to the these fish fillets. Then the prepared fish

fillets were vacuum packaged and cooked at 50 and 55℃ for 7 min.

Pasteurized packets were quickly cooled to 0℃– 1℃ in an iced water

tank and stored at 4℃. The counts of L. monocytogenes was deter-

mined on days 0, 1, 3, 6, 9, 12, 15, 22, 29, and 36 of the storage.

Determination of L. monocytogenes

Ten grams of fish were homogenized using 90 ml Maximum Recovery

Diluent. The homogenisation was diluted to 105 dilutions (with a

1/10 dilution rate). 0.1 ml of the appropriate dilutions were applied

into PALCAM Agar medium and incubation at 30℃ for 24– 48 hr. At

the end of the incubation colonies were counted and the number of

bacteria was determined as log CFU/g.

2.2.5 | Statisticalanalysis

The data obtained from the study were analyzed using ANOVA

(variance analysis). The results were evaluated by Tukey Multiple

Comparison Test. SPSS package programme was used to test

whether there was a difference between the experimental groups

(IBM SPSS 2012).

3 | RESULTS AND DISCUSSION

3.1 | Chemical composition of essential oils

The main components of the essential oils used in the study were

determined by GC-MS method. The percentages of the chemical

components of basil, coriander, rosemary, and laurel essential oils

are summarized in Table 1. As a result of this study, it was deter-

mined that the main components of rosemary essential oil (R. of-

ficinalis L) were eucalyptol (51.31%) and α-pinene(15.06%).Gouveia

et al. (2017) described the main compounds in rosemary essential

oil as eucalyptol (13.05%), camphor (8.93%), verbenone (8.58%),

endo-borneol (7.87%),anda-pinene (6.78%). Ghabraie et al. (2016)

reported that the major components of this essential oil were

1.8- cineole (44.48%), a- pinene (12.45%), and camphor (10.70%).

Teixeira et al. (2013) stated that rosemary essential oil is rich in cam-

phor, eucal yptol, and bor nylacetate. Gu tierrez et al. ( 2008) deter-

mined that the main components of this oil were eucalyptol (39.6%),

camphor (19%), a- pinene (4.8%). Jordán et al. (2013) found that the

main components of R. officinalis essential oils obtained from differ-

ent ecological bioclimatic fields were a- pinene, camphene, eucalyp-

tol, and camphor. In this study, the main components of rosemary

essential oil have been generally similar to other studies. However,

the percentage of eucalyptol compound was determined to be

higher than the other studies.

As a result of this study, it was determined that the main com-

ponents of Laurel (L. nobilis) were eucalyptol (62.84%) α- terpinenyl

acetate (6.32%), α- pinene (4.47%), terpinen- 4- ol (3.73%), β- pinene

(3.37%), and linalool (2.08%). Ramos et al. (2012) described the main

compounds in L. nobilis as eucalyptol (27.2%), α- terpinenyl acetate

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ÖZTÜRK e T al.

TABLE 1 Chemicalcomposition(%)ofbasil,coriander,laurel,androsemaryessentialoils,determinedbyGC-MS

Component name

Basil Coriander Rosemary Laurel

% % % %

Alpha- citral 0.32 – – –

Alpha- muurolene – – 0.04 0.13

Alpha- pinene 0.08 6.21 15.06 4.47

Alpha- copaene – – 0.13 –

Alpha- thujene – – – 0.36

Alpha- phellandrene – – 0.07 0.50

Alpha- terpineol – 0.38 – 0.50

Alpha- terpinyl acetate – – – 6.32

Beta- bisabolene 0.04 – 0.05 0.06

Beta- citral 0.57 – – –

Beta- myrcene 0.03 0.78 1.08 0.72

Beta- pinene 0.06 0.46 0.98 3.37

Beta- ocimene 0.10 – – 0.46

(+)- 2- bornanone – 5.74 4.49 –

Bornyl acetate – – 1.15 –

Camphene – 1.01 4.37 0.04

Camphene hydrate – – 0.86 –

3- carene – – 0.19 –

(+)- 3- carene – 0.03 0.16 –

(+)- 4- carene – – 0.13 0.74

Caryophyllene 0.36 – 3.89 0.29

Caryophyllene oxide – – 0.19 0.06

Cis- beta- farnesene 0.12 – – –

Cis- 2- p- menthen- 1- ol – – – 0.14

Decane 0.03 0.04 0.04 –

Delta- terpineol acetate – – – 0.27

D- limonene 0.08 2.74 2.68 –

Endo- borneol – 0.22 4.88 –

Estragole 75.56 – – –

Eucalyptol 0.32 0.05 51.33 62.84

Eugenol – – – 0.18

(E)- beta- farnesene 0.08 – – –

Fenchol – – 0.09 –

Gamma-elemene – – – 0.10

Gamma-muurolene – – 0.09 –

Gamma-terpinene – 4.01 0.03 1.35

Geraniol – 1.05 – –

Geranylacetate – 2.17 – –

Germacrene-D 0.18 – – 0.04

Ho- trienol – 0.18 – –

Humulene 1.60 – 0.58 0.58

Humulene 0.19 – – –

Linalool 18.97 70.09 0.35 2.08

Levo- menthol 0.32 – – –

(Continues)

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ÖZTÜRK e T al.

(10.2%), linalool (8.4%), methyleugenol (5.4%), sabinene (4.0%),

and car vacrol (3.2%). Similarly Ghabraie et al. (2016), found high

amounts of 1.8- cineole (48.1%), a- terpineol (6.8%), sabinene (6.4%),

a- pinene (6.3%), and b- pinene (5.8%) compounds in L. nobilis. Da

Silveira et al. (2014) stated that the main components of Laurel were

1.8- cineole (35.50%) and linalool (14.10%).

It was determined that the main components of coriander (C. sa-

tivum) were linalool (70.09%), α- pinene (6.21%) and (+)- 2- bornanone

(5.74%). Similar to our work; Khalil et al. (2018) and Delaquis

et al. (2002) reported that the main content of coriander essential

oil was linalool and α- pinene. Miri and Djenane (2018) described

the main compounds in coriander as linalool (78.86%). Unlike this

studies, Teixeira et al. (2013) stated that the main composition of

this essential oil was 3- carene and γ-terpinene.Gilletal.(2002)re-

ported that the main compound of this was linalool (% 25.86) and

(E)- 2- decenal (20.22%).

As a result of this study, it was determined that the main compo-

nents of basil (O. basilicum) estragole (methylchavicol) (75.56%) and

linalool (18.97%). Similarly, Teixeira et al. (2013) found that the main

componentofbasil essential oil was methylchavicoland Gutierrez

et al. (2008) determined that the main component of this essential

oillinalool(42.3%),estragole(26.9%)andeucalyptol(8.1%).Soković

et al. (2010) stated that the main composition of this essential oil was

linalool (69.3%).

The results of the research show that there are differences in

the main components and amounts of rosemary, basil, coriander

and laurel essential oils. These differences are thought to depend

on the geographic conditions of the plants, climate and harvest sea-

son. In addition, the use of different parts of plants and different

extraction applications may have caused these differences (Azeredo

et al., 2011; Gach kar et al., 20 07;Go uveia et al., 2017; Nezhad ali

et al., 2014; Teixeira et al., 2013).

3.2 | Antibacterial effect of essential oils

In this study, the disk diffusion method was used to determine an-

tibacterial activities of essential oils on L. monocytogenes. The anti-

bacterial activity of the essential oils against L. monocytogenes are

presented in Table 2. According to disc diffusion results, laurel, cori-

ander, and rosemary essential oils were found to be more effective

than basil oil (p < .05).

Mazzarrino et al. (2015) evaluated the activity level of antimi-

crobial agents according to the zone diameters determined by the

disk diffusion test. According to this evaluation, those inhibition

zone “<12 mm” were evaluated as having weak antimicrobial effect;

“>12.1 mm” were evaluated as having medium antimicrobial effect;

“>20 mm” were evaluated as having strong antimicrobial effect. In

the study conducted by us, it was determined that essential oils of

laurel (31.75 mm), rosemary (30.5 mm), and coriander (20.50 mm)

had strong antimicrobial effect; basil essential oil (14.25 mm) had

strong medium antimicrobial effect.

Ouibrahim et al. (2013) reported that the inhibition zones against

20 bacteria they tested were 8.4– 22.4 mm for laurel; 8.4– 16.4 mm

Component name

Basil Coriander Rosemary Laurel

% % % %

Mesitylene 0.03 – 0.04 –

Methyleugenol – – – 0.61

Myrtenyl acetate – 0.08 – –

3- octanone – – 0.07 –

P- cymene 0.03 3.62 3.80 2.70

Pinocarvone – – – 0.08

Prenylacetone 0.10 – – –

Sabinene – – – 5

Sabinene hydrate – – – 0.15

Α- Sabinene – 0.20 – –

Terpineol 0.12 3.10 1.60

Terpinen- 4- ol – 0.17 0.08 3.73

Terpinolene – – – 0.26

Α- Terpinolen – 0.73 – 0.5

Terpinene- 1- ol – – – 0.27

Trans- alpha- bergamotene 0.56 – – –

Trans- linalool oxide 0.06 – – –

Trans- 4- metoxycinnamaldehyde 0.03 – – –

Note: – , not detected.

TABLE 1 (Continued)

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ÖZTÜRK e T al.

for rosemary and 7– 19.9 mm for basil. Teixeira et al. (2013) stated

that the inhibition zone for rosemary, basil and coriander essential

oils against L. monocytogenes were 8, 9, and 16 mm, respectively.

Ghabraieetal.(2016)foundthattheinhibitionzoneagainstL. mono-

cytogenes was less than 10 mm for laurel essential oil; was 11.2 mm

for rosemary essential oil. Similarly, Tural and Turhan (2017) found

that the inhibition zone for rosemary essential oil was higher than

the laurel essential oil. Pesavento et al. (2015) reported that the inhi-

bition zone for rosemary essential oil was 16.3 mm against L. mono-

cytogenes. In addition, the researchers stated that Cinnamomum

zeylanicum (24 mm), Origanum vulgare (19.7), and Thymus vul-

garis (33.5) essential oils were more effective than rosemary oil.

Mazzarrino et al. (2015) stated that rosemary essential oil had a

low (<12 mm) and medium (>12.1 mm) antimicrobial effect against

L. monocytogenes. Jordán et al. (2013) reported that the inhibition

zone for different chemotypes of rosemary essential oil against L.

monocytogenes varied between 20.9 and 22.8 mm.

Cherrat et al. (2014) reported that the inhibition zone of laurel

essential oil against different strains of L. monocytogenes ranged

from 14.0– 32.5. Millezi et al. (2012) found that the inhibition zones

for laurel essential oil at different concentrations (5%– 50%) on

L. monocytogenes ranged between 1.0 and 5.67 mm.

Although the essential oils used in most of the studies were

identical, the antimicrobial effect on L. monocytogenes was differ-

ent. It has been reported that the antimicrobial effect of essential

oils changes depending on the type and amount of the components

contained in the essential oils, the extraction method, the inoculum

ratio and the growth phase of the bacteria (Burt, 2004; Tajkarimi

et al., 2010; Tosun et al., 2018).

3.3 | MIC and MBC of essential oils

MIC and MBC values of basil, coriander, laurel, and rosemary essen-

tial oils against L. monocytogenes are given in Table 3. As a result of

this study, MIC values fo r L. monocytogenes were 6.25 m g/ml for basil

and laurel essential oils; 12.50 mg/ml for essential oils of rosemary

and coriander essential oils. MIC is an effective method to compare

the antibacterial effect of essential oils and to determine the con-

centrationwithoutbacterialgrowth(Gouveiaetal.,2017).

Gouveia etal. (2017) found that the MIC forL. monocytogenes

was 62.5 µl/ml for rosemary essential oil. Azeredo et al. (2011) de-

termined the MIC value as 20 µl/ml. Another study was carried out

by De Medeiros Barbosa et al. (2016) and a MIC value of 5 µl/ml was

obtained. Jordán et al. (2013) concluded that the MIC of different

chemotypes of this essential oil for L. monocytogenes was smaller

than 0.5 µl/ml.

Da Silveira et al. (2014) reported that the MIC of laurel essen-

tial oil for two different strains of L. monocytogenes (L. monocyto-

genes ATCC 19117, L. monocytogenes serotype 2 ATCC 19112) was

1.25– 2.5 g/L. The results obtained by the researchers indicate

that the laurel essential oil is more effective on L. monocytogenes

than Salmonella typhimurium, Staphylococcus aureus, Bacillus cereus,

Pseudomonas aeruginosa.

Cherrat et al. (2014) found that the MIC of laurel essential oil

for different strains of L. monocytogenes was between 0.5– 1.0 µl/L.

Ramos et al. (2012) found that MIC value of this essential oil is

1.1mg/ml.Ghabraieetal.(2016)reportedthattheMICofL. mono-

cytogenes was 4,380 ppm for rosemary essential oil and was greater

than 10,000 ppm for laurel essential oil. Dussault et al. (2014) stated

that the MIC of L. monocytogenes was 2,500 ppm for laurel essential

oil and was greater than 5,000 ppm for coriander and rosemary es-

sential oils. Teixeira et al. (2 013) reported that the coriande r essential

oil for L. monocytogenes had the lowest MIC value, followed by rose-

mary and basil essential oils (MICCoriander < MICRosemary < MICBasil).

Oussalah et al. (2007) reported that the concentration of 0.8% (vol/

vol) of coriander essential oil was effective on L. monocytogenes.

As a result of the studies conducted by different researchers,

it was obser ved that the MIC values of essential oils differed from

each other. It is thought that this difference may be related to the

different strains of L. monocytogenes used, the composition of the

essential oils and different types of solvents in the oils (Djenane

etal., 2011;Gouveia et al., 2017). According todisc diffusionand

TABLE 2 Antibacterial activity of basil, coriander, laurel, and

rosemary essential oils against Listeria monocytogenes, using paper

disc- diffusion method, inhibition zones in mm

Essential oils

Inhibition zone

diameter (mm)

Coriander 20.5 ± 0.71c

Rosemary 30.5 ± 0.71a

Basil 14.5 ± 0.71d

Laurel 31.5 ± 2.12a

Ampicillin (AMP; 10 µg) 25.0 ± 0.0b

Erythromycin (E, 15 µg) 16.0 ± 0.0d

Sulphamethoxazole/trimethoprim (SXT, 25 µg) 18.0 ± 0.0cd

Note: Different letters are significantly different from each other

(p < .05).

TABLE 3 Minimal inhibitory concentration (MIC, mg/ml) and

minimal bactericidal concentration (MBC, mg/ml) of basil, coriander,

laurel, and rosemary essential oils against Listeria monocytogenes

Essential oils

Analysis of antibacterial

activitya L. monocytogenes

Coriander MIC (mg/ml) 12.50

MBC (mg/ml) 12.50→(0.403abs)

Rosemary MIC (mg/ml) 12.50

MBC (mg/ml) 12.50→(0.152abs)

Basil MIC (mg/ml) 6.250

MBC (mg/ml) 6.250→(0.045abs)

Laurel MIC (mg/ml) 6.250

MBC (mg/ml) 6.250→(0.015abs)

aMinimum inhibition concentration (MIC; mg/ml), Minimum bactericidal

concentration (MBC; mg/ml ve abs; absorbans).

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ÖZTÜRK e T al.

MIC results, it was found that the essential oil with the highest anti-

microbial effect on L. monocytogenes was laurel oil.

3.4 | Inactivation of L. monocytogenes in fish fillets

The change in the number of L. monocytogenes during storage period

in trout fillets added of basil, coriander, laurel, and rosemary essen-

tial oils and applied to sous- vide at 50℃ and 55℃ for 7 min was

given in Figure 1a,b. The number of L. monocytogenes in the group

applied to coriander essential oil and applied to sous- vide at 50℃’de

was found to be lower than the control group (p < .05). Although the

number of L. monocytogenes in the group added of coriander essen-

tial oil lower than other groups added of essential oils, this difference

was not statistically significant (p > .05).

In the trout fillets treated with sous- vide at 55℃, the number

of L. monocytogenes was found to be lower than the control group.

Especially, it was determined that the difference in the group added

of coriander essential oil was statistically significant (p < .05). After

sous- vide processing (0 day), the number of L. monocytogenes in

the group added of coriander essential oil was found to be 3.01 log

CFU/g lower than the control group. The difference between these

groups continued until the 9th day of storage (p < .05).

In this study, the combined effect of essential oil and tempera-

ture applications on the inactivation of L. monocytogenes in fish

fillets cooked with sous- vide technology was investigated. The num-

ber of L. monocytogenes was found to be lower in the groups which

were applied sous- vide at 50℃ and added with essential oil. The

number of L. monocytogenes was found to be lower than 1.06, 0.67,

0.57, and 0.17 log CFU/g in the group containing coriander, rose-

mary, basil, and laurel essential oil compared to the control group not

containing essential oil, respectively. At the beginning of storage, it

was observed that essential oils had a high antimicrobial effect and

lost their effectiveness in the later days of storage.

In groups that applied sous- vide at 55℃, the number of

L.monocytogenes detected was 5.09 log CFU/g in the control group

on day 0. This number was decreased 3.01, 1.53, 1.82, and 1.11 log

CFU/g with the addition of coriander, rosemary, basil, and laurel es-

sential oils, respectively.

As a result of this study carried out by us, it was determined that

the antibacterial effect of essential oils in sous- vide application per-

formed at 55℃ was higher than essential oils in sous- vide application

performed 50℃. It has been determined that higher temperature ap-

plication increases the effect of essential oils on L. monocytogenes

and a synergistic effect occurs. In addition, it was observed that

coriander essential oil had a higher antimicrobial effect than other

essential oils in both temperature applications.

Gouveia e t al. (2017) reporte d that the rosemar y essential oi l

added at 1.25% to the meat product they applied sous- vide showed

higher antilisterial activity on the number of L. monocytogenes than

the thyme essential oil. Karyotis et al. (2017) reported that the

D- value on the number of L. monocytogenes in marinated chicken

breast meat applied sous- vide was determined 54.81 min for 55℃

and 10.39 min for 60℃. Bolton et al. (2000) reported that the

D- value on the number of L. monocytogenes in the vacuum cooked in

the meat samples were determined between 0.15 and 36.1.

Jafari et al. (2017), investigated alone effect and combination

effect of rosemary extract and chitosan on L. monocytogenes inoc-

ulated Huso huso fillets. At the end of the study, it was determined

that the combined use of rosemary extract and chitosan showed the

most effective antimicrobial effect against L. monocytogenes. Raeisi

et al. (2016) found that the use of rosemary essential oil with dif-

ferent antimicrobials (C. zeylanicum and nisin) against L. monocyto-

genes in chicken meat samples is more effective than the use of this

oil alone. Oliveira et al. (2013) investigated the effect of essential

oils in edible gelatin packaging on L. monocytogenes in fresh meat

products. The researchers stated that the number of L. monocyto-

genes was lower 0.42, 1.21, and 0.70 log CFU/g in the gelatin with

the addition of rosemary essential oil compared to the control group

at the 1st, 48th, and 96th hours. Haskaraca et al. (2019) investigated

the effect of 0.5% and 1% grapefruit seed extract on L. monocyto-

genes in the sous- vide process at 57.5℃, 60℃, 62.5℃, and 65℃.

Researchers have determined that the sous- vide procedure applied

to 5 7. 5℃, 60℃, 62.5℃, and 65℃ requires a processing time of 140,

62.38, 14.45, and 6.84 min to reduce the number of L. monocyto-

genes to 4 log CFU/g. Tosun et al. (2018) investigated the effect of

essential oils on the development of L. monocytogenes in untreated

salmon fillets at +2℃. The researchers initially found the number of

FIGURE 1 Listeria monocytogenes (log CFU/g) changes in (a) 50℃ and (b) 55℃ for 7 min sous- vide applied trout fillets at +4℃

8 of 10

ÖZTÜRK e T al.

L. monocytogenes at 4.75, 4.77, and 4.80 log CFU/g for rosemary, co-

riander and control groups and this number was to be 4.67, 4.73, and

4.95 log CFU/g at the end of the 96th hour, respectively. At the end

of the study, the researchers stated that the group that added es-

sential oil had a lower number of L. monocytogenes compared to the

control group. However, they reported that there was no statistically

significant difference between the groups with added essential oil.

In the studies reported, different results have been obtained re-

garding antibacterial effects of essential oils. It is possible to explain

these differences by different L. monocytogenes strains and different

content of the essential oils used in the experiments (Abdollahzadeh

etal.,2014;Gouveiaetal.,2017).

4 | CONCLUSION

In this study, while coriander, laurel, and rosemary essential oils were

found to be effective according to disc diffusion results, coriander

essential oil was found to be the most effective essential oil on

L. monocytogenes in sous- vide applied trout. Coriander essential oil

addition (2 times more than the MIC value) and 7 min sous- vide ap-

plication in 55℃ was effective for the inhibition of L. monocytogenes

in sous- vide applied trouts. According to our results, the sous- vide

packaging in association with coriander essential oil was confirmed

as a good application for the quality preservation of trout. This study

shows that, sous- vide technology was used as a functional cooking

method in seafood, which will ensure pathogen control by use of es-

sential oils, so these foods will be safely and ready- to- eat.

ACKNOWLEDGMENT

This study has been supported by İzmir Katip Çelebi University

Scientific Research Project Coordination (Project number:

2 0 1 6 - G A P - S U Ü F - 0 0 1 8 ) .

CONFLICT OF INTEREST

The authors have declared no conflicts of interest for this article.

AUTHOR CONTRIBUTIONS

Fatma Öztürk: Investigation. Hatice Gündüz: Investigation. Göknur

Sürengil: Investigation.

DATA AVAIL ABI LIT Y S TATEMENT

The data that support the findings of this study are available from

the corresponding author upon reasonable request.

ORCID

Fatma Öztürk https://orcid.org/0000-0003-4763-3801

Hatice Gündüz https://orcid.org/0000-0002-9899-8635

Göknur Sürengil https://orcid.org/0000-0002-4560-7856

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The demand for safe, high-quality meat products drives the need for effective antimicrobial solutions to combat bacterial contamination, a significant health and economic concern. Synthetic preservatives face increasing scrutiny, leading to interest in natural alternatives such as coriander (Coriandrum sativum L.). Known for its culinary and medicinal uses, coriander essential oils, particularly linalool and pinene, exhibit strong antimicrobial properties against a wide range of pathogens. This review examines the phytochemical composition and antimicrobial mechanisms of coriander, and its practical applications in meat preservation through a One Health perspective, which addresses the interconnectedness of human, animal, and environmental health. Coriander offers unique benefits such as a milder flavor and cost-effectiveness. Despite challenges, including variability in antimicrobial efficacy and sensory impacts, its safety profile and regulatory status support its use. Future research should optimize extraction methods, explore synergies with other preservatives, and evaluate long-term safety and efficacy. Coriander is a viable natural solution for improving food safety and quality in the meat industry, aligning with One Health objectives by promoting sustainable practices and reducing health risks across the food production continuum.

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FOOD BIOPROCESS TECH

The effect of pulsed electric fields (0.7 and 1.5 kV/cm, specific energy 90–100 kJ/kg) processing followed by post–pulsed electric field (PEF) ageing ( 0, 3, 7, 14 days) on the safety and quality attributes of sous vide–processed (60 °C/12 or 24 h) beef briskets was assessed. Ageing did not significantly reduce the hardness of sous vide–processed meat except for those PEF treated either at 0.7 kV/cm followed by sous vide processing for 12 h or at 1.5 kV/cm followed by sous vide processing for 24 h. Post-PEF ageing time had no effect on the collagen solubility of sous vide–processed meat. The effect of PEF treatment on hardness was much greater than the effect of ageing time, and sous vide processing time. Sous vide processing (12 or 24 h) for all treatments reduced both aerobic and lactic acid bacteria numbers to below the detection limit. Initial peptide concentrations during in vitro peptic digestibility were significantly (P < 0.05) different between some treatments; however no significant (P > 0.05) differences were observed in digestion rates between any treatment. Ageing of PEF-treated meat for a few days prior to sous vide processing may improve tenderness; however, these gains in quality may be offset by a greater total water loss and an increase in lipid oxidation.

Optimisation of Sous Vide Processing Parameters for Pulsed Electric Fields Treated Beef Briskets

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Nov 2018
FOOD BIOPROCESS TECH

The goal of this research was to optimise sous vide processing parameters for beef briskets, previously treated with pulsed electric fields (PEF), to enhance meat tenderness while maintaining other quality attributes such as water holding capacity, colour, and collagen solubility. PEF-treated briskets (electric field strength 1.5 kV/cm; specific energy of 90–100 kJ/kg) were subjected to various sous vide temperature and time combinations for the process optimisation using response surface methodology. Sous vide temperature was found to significantly reduce the shear force of PEF-treated meat while time significantly reduced its hardness. In addition, beef briskets processed by PEF prior to sous vide processing showed less variation owing to a reduction in the effect of biological variation on the parameters tested. According to the response optimiser prediction, sous vide processing at 60 °C for 24 h resulted in optimal quality and tenderness. Scanning electron microscopy (SEM) revealed that PEF-treated meat showed evidence of pore formation in connective tissue and polarised-sensitive optical coherence topography (PS-OCT) revealed that the collagen matrix of PEF-treated meat had a reduced birefringence capacity compared to non-PEF-treated meat, which indicated a breakdown of the collagen.

Evaluation of Protective Impact of Algerian Cuminum cyminum L. and Coriandrum sativum L. Essential Oils on Aspergillus flavus Growth and Aflatoxin B1 Production

Article

Full-text available

Feb 2018

Background and objective: Aflatoxin B1 (AFB1) is a highly toxic and carcinogenic metabolite produced by Aspergillus species on food and agricultural commodities. The aim of this investigation was to evaluate the inhibition of growth Aspergillus flavus E73 (A. flavus E73) and AFB1 production by Cuminum cyminum L. (C. cyminum L.) and Coriandrum sativum L. (C. sativum L.) essential oils (EOs) as well their antioxidant and phytotoxicity activities. Methodology: The C. cyminum L. and C. sativum L. EOs were extracted by hydrodistillation. The chemical profile of EOs was identified by GC-MS, antifungal activity was assessed by poisoned food technique and in term Minimal Inhibitory Concentration (MIC) and minimal fungicidal concentration (MFC) and antiaflatoxin effect by broth medium. The antioxidant activity of EOs was determined by DPPH free radical scavenging assay, β-carotene bleaching test and total phenolic content by Folin-Ciocalteu. Phytotoxicity of C. cyminum L. and C. sativum L. EOs were determined for varieties of wheat. The results were analyzed by analysis of variance (one way ANOVA). Results: The GS/MS analysis showed that the major components of C. cyminum L. EO were cuminaldehyde (65.98%), o-cymene (18.40%) and C. sativum L. EO was mainly consisted of linalool (78.86%). The results showed that both the EOs could inhibit the growth of A. flavus E73 in the range of 24.27-84.90% for C. cyminum and 15.09-65.00% for C. sativum. During antiaflatoxin investigation, the oils exhibited noticeable inhibition on dry mycelium weight and synthesis of AFB1 by A. flavus E73. EOs of C. cyminum L. and C. sativum L. revealed complete inhibition of AFB1 at 1.25 and 1.5 mg mL-1, respectively. EOs exhibited inhibitory influence against some fungi. The IC50 values of C. cyminum L. and C. sativum L. EOs were 494.93 and 756.43 μg mL-1, respectively, while, β-carotene/linoleic acid bleaching was 47.68 and 29.29% , respectively. Total phenolic content of C. cyminum L. and C. sativum L. were 10.66 and 6.2 μg mg-1. Additionally, the EOs were non-phytotoxic on the two verities of wheat seeds. Conclusion: The C. cyminum L. and C. sativum L EOs could be good alternative to protect foods.

Chemical composition and antimicrobial activity of the essential oils of selected Apiaceous fruits

Article

Full-text available

Mar 2018

Antimicrobial properties of plants essential oils are continuously investigated to use them as potential drug candidates to overcome the problem of microbial drug resistance. The aim of this research is to study the antimicrobial effects of the essential oils of ten Apiaceous fruits [Pimpinella anisum L. (anise), Carum carvi L. (caraway), Apium graveolens L. (celery), Coriandrum sativum L. (coriander), Cuminum cyminum L. (cumin), Anethum graveolens L. (dill), Foeniculum vulgare L. (fennel), Petroselinum crispum L. (pasley), Daucus carota L. var. sativus (yellow carrot) and Daucus carota L. var. boissieri (red carrot)]. Results of agar-well diffusion method revealed that the maximum inhibition zones were obtained with cumin, coriander and caraway oils against the standard bacterial strains Escherichia coli, Bordetella bronchiseptica followed by Staphylococcus aureus. Results of viable count time-kill method revealed that coriander oil had the highest antimicrobial activity with more than 99.99% killing of the exposed cells of the standard E. coli and Bordetella bronchiseptica standard strains. GC/MS was carried out to identify the chemical composition of the most active oils. The percentage of identified compounds by GC/MS was 92.5%, 99.43% and 98.66% for cumin, coriander and caraway oils, respectively. Monoterpenes were the most abundant components in the three oils.

Texture, color and sensory evaluation of sous-vide cooked beef steaks processed using high pressure processing as method of microbial control

Article

Dec 2018
LWT-FOOD SCI TECHNOL

The effects of high pressure processing (HPP; 450 MPa for 15 min and 600 MPa for 10 min) and sous vide (SV) cooking time on the texture, color, and sensory characteristics of beef strip steaks were studied. Control treatments (no HPP) were SV cooked for 180 min while HPP treated steaks (450 MPa or 600 MPa) were SV cooked for 45 min or 120 min. SV cooking did not change (P > 0.05) the redness of HPP samples compared to control. There were significant (P < 0.05) differences between SV control and SV HPP samples regarding tenderness. SV control steaks were rated higher (P < 0.05) for tenderness juiciness and overall liking than SV HPP, but not differently (P > 0.05) for taste and aftertaste liking from SV 450 MPa. These results indicate HPP treatment with shorter sous vide cooking times can have some negative impact on quality and sensory characteristics of beef steaks, but still may be potentially accepted by consumers with optimized pressure and time.

Nutritional values of potato slices added with rosemary essential oil cooked in sous vide bags

Article

Nov 2018

The sous vide packaging method, in association with rosemary essential oil (REO), was confirmed as a good strategy for the quality preservation of sliced potatoes over refrigerated storage until 11 days. Looking at vegetables as sources of phytochemicals together with the benefits of sous vide cooking method validated by several studies, taking into account the increasing interest in early crop variety and their nutritional value and considering that potatoes must be cooked to be eaten, the potato slices treated with peanut oil and with the addition of REO were monitored on ascorbic acid, total polyphenols content and antioxidant activity. Results demonstrated that the presence of REO have no “a direct” effect on the nutritional content of cooked samples, but it was probably linked with the protection of such compounds. The ascorbic acid (AsAc) was better preserved (24.7 ± 4.06 mg/100 g DM) and values were kept nearest to the raw tubers having moderate loss with a maximum of 20% in Erika. Total polyphenol content (TPC) was well maintained after cooking, ranging from 337 to 257 mg/100 g DM, of course the varieties with the highest content were able to save a high amount of the compound studied, and the antioxidant activity (AA) calculated showed a loss mean value of 48% among cultivars. Hence, we can conclude that potato slices treated with REO, packaged in sous vide bags and cooked at 105 ± 5 °C for 15 min, retain nearly all the nutritive compounds considered in our study. The most suitable cultivar identified to be stored as fresh cut potato slices with the addition of REO in sous vide bags and then cooked, was Elodie: it was able to save the highest nutritive values among cultivars studied holding AsAc and TPC content as well as the smaller reduction in AA from the fresh material.

The Effects of Grapefruit Seed Extract on the Thermal Inactivation of Listeria monocytogenes in Sous-vide Processed Döner Kebabs

Article

Jul 2018
FOOD CONTROL

The heat resistance (57.5–65 °C) of Listeria monocytogenes in vacuum packaged, cook-in-bag, döner kebabs that included 0.5 or 1% grapefruit seed extract (GSE) was determined. The packages were processed to an internal temperature of 57.5, 60, 62.5 or 65 °C in 1 h, held for a predetermined period of time, and then, ice chilled. The surviving cell population was determined by plating diluted samples onto tryptic soy agar overlaid with 10 ml of modified Oxford agar. Survivor curves were fitted to an equation based on the Weibull distribution using the USDA Integrated Pathogen Modeling Program 2013 software tool. The Weibull model consistently offered more accurate fit to all survivor curves based on the smaller root mean square error (<0.46). The times to 4-log reduction were 140, 62.38, 14.45 and 6.84 min at 57.5, 60, 62.5, and 65 °C, respectively. Supplementing döner kebab with 0.5–1% GSE rendered the pathogen more sensitive to the lethal effect of heat. The results provide the food industry with an option to supplement 0.5–1% GSE in sous vide processed döner kebab, that ensures adequate degree of protection against L. monocytogenes and at the same time, provide energy conservation and quality products.

Effects of essential oils on the survival of Salmonella Enteritidis and Listeria monocytogenes on fresh Atlantic salmons (Salmo salar) during storage at 2 ± 1 °C

Article

Nov 2017

In this study, the effects of coriander, garlic, rosemary, and orange peel oils on the survival of Salmonella Enteritidis and Listeria monocytogenes were examined 2 ± 1 °C during storage of inoculated fresh Atlantic salmon samples (96 hr). At the end of storage population decrease in Salmonella Enteritidis was significantly lower (p < .05) in the essential oil groups compared with control group. Salmonella Enteritidis count of rosemary oil treated group was higher than (p < .05) other groups (coriander, garlic, and orange peel oils) at the end of storage. Essential oils decreased the population of L. monocytogenes while the population in untreated samples were higher at the end of storage period (p < .05). Results of this study indicated that treatment of salmon fish samples with essential oils may be an effective natural antimicrobial application to control Salmonella Enteritidis and L. monocytogenes. Practical applications In the present study, it was concluded that essential oils had an antimicrobial effect Salmonella Enteritidis and Listeria monocytogenes. Use of essential oils during storage of fish or fish products may play an important role against Salmonella Enteritidis and L. monocytogenes. Essential oils are easily applicable and a cheaper method. The results of this experiment propose that addition of essential oils to fish flesh can be recommended to seafood processors and fish market retailers.

ANTIMICROBIAL AND ANTIOXIDANT PROPERTIES OF THYME (Thymus vulgaris L.), ROSEMARY (Rosmarinus officinalis L.) AND LAUREL (Lauris nobilis L.) ESSENTIAL OILS AND THEIR MIXTURES

Article

Jan 2017

The effects of essential oils on inactivation of Listeria monocytogenes in Rainbow Trout cooked with sous‐vide

Abstract

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