Combine Effects of Essential Oils and Packaging on Smoked Rainbow Trout Stored 4°C

Combine Effects of Essential Oils and Packaging on Smoked

Rainbow Trout Stored 4°C

By P

ınar Oğuzhan Yıldız*

The Faculty of Engineering, Food Engineering Department, Ardahan University, Ardahan, 7500, Turkey

In this study, the effect of essential oils (thyme and clove) and packaging treatments (vacuum and modified atmosphere) on the storage of hot smoked rainbow trout (Oncorhynchus mykiss)fillets over a period of 120 days at 4°C was investigated. Fillets were subjected to microbiological (total aerobic mesophilic bacte-ria, psychrotrophic bactebacte-ria, lactic acid bactebacte-ria, yeast and mould), chemical analyses (pH, thiobarbituric acid reactive substances and total volatile base nitrogen) and quality testing throughout the storage period. Difference in microbiological and chemical changes between samples was found to be significant (p < 0.05) during storage period. Sensory evaluation showed significant differences between the samples, and V2 and M2 samples were assessed as the most acceptable products by the panellists. In conclusion, essential oils treatment to hot smoking had a positive effect on shelf life of rainbow trout, especially clove oil showed more positive effect when compared with thyme oil. Copyright © 2015 John Wiley & Sons, Ltd.

Received 16 July 2014; Revised 27 August 2015; Accepted 1 September 2015

KEY WORDS:Oncorhynchus mykiss; hot smoked; shelf life; essential oil; packaging

INTRODUCTION

Microorganisms can grow in the muscle tissue of aquatic products because of their high-nutrient con-tent. So the conservation and handling of aquatic products are very important.1One of the conservation processes of aquatic products is smoking.2Smoking is one of the oldest methods of food preservation and widely used infish processing.3,4The shelf life of smokedfish products depends largely on the initial bacterial contamination level of the raw material; the water holding capacity (aw) of brined and pre-dried tissues; the activation of putrefactive microflora by heat treatment; the amount of smoke components that penetrate the product; and the temperature, air humidity and oxygen levels during storage.5,6The three following methods are used to smokefish: the traditional method of combustion at a low temperature (cold smoking≤30°C) or at a high temperature (hot smoking ≥60°C), a high-voltage electrostatic field to accelerate smoke deposition or a liquid smoked-fish flavorant. Hot smoking is a pasteurizing process, the preservative effect of which depends on the composition and preparation of raw material, temperature, relative humidity, density and composition of the smoke and the smoking time.7There are different stages of hot smoking process: salting (brining), drying, heating and smoking.8The salting process is itself a preservation technique that is performed before many processing techniques (smoking, drying and marinating) are used. Salting is the first step of thefish-smoking process and is primarily used to partially dehydrate the tissue. Bacterial activity is largely prevented by high salt concentrations, and a high salt concentration prevents the growth of microflora that spoils fish, thus significantly increasing its shelf life.9NaCl is an essential ingredient in processed meat products because it affects the water-holding capacity, prevents microbial growth,

* Correspondence to: Pınar Oğuzhan Yildiz, The Faculty of Engineering, Food Engineering Department, Ardahan University, Ardahan, Turkey.

E-mail: pinaroguzhan@ardahan.edu.tr

Packag. Technol. Sci. 2015; 28: 987–997 Published online in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/pts.2177

reduces water activity, facilitates the solubilization of certain proteins and enhances the flavour of processed meats by conferring a typical salty taste.10Modified atmosphere packaging (MAP) is a form of packaging that removes air from the package and replaces the air with a single gas or a mixture of gases. The gaseous atmosphere changes continuously during storage because of the respiration of the product, biochemical changes and the slow permeation of gases through the packaging material.6,11 MAP offers multiple advantages to thefish industry and the consumer. Various atmospheres have been examined infish packaging.12–21Vacuum packaging is also a type of MAP because air is removed from the package and is not replaced. However, MAP is an increasingly popular food preservation technique. MAP is a preservation method used to extend the shelf life offish and fish products.6,22 The application of essential oils (EOs) has proven to be an effective preservation method that extends the shelf life of fresh foods.16,22–26EOs are aromatic, oily liquids that are obtained from plant material. Extracts from oregano, thyme, rosemary, clove, sage and mint are among the EOs used to both im-prove the sensory characteristics and extend the shelf life of foods. A number of EOs and some of their components have been reported to have antimicrobial activity against a wide range of spoilage and pathogenic bacteria.27,28Very little information is available about the combined effects of EOs and dif-ferent packaged type on smoked rainbow trout. The aim of this study was to determine the combined effects of EOs (thyme and clove) and packaging type (vacuum and MAP) on the shelf life of refriger-ated (4°C) hot-smoked rainbow trout fillets by evaluating microbiological, chemical and sensory parameters.

MATERIALS AND METHODS Preparing samples

Hot-smokedfish was prepared from rainbow trout (Oncorhynchus mykiss). Rainbow trout (250 ± 25 g) was obtained from the Ataturk University Agricultural College Fisheries Department’s rainbow trout breeding and research centre. The freshfish samples were carried to the laboratory and washed with tap water. The study was conducted using two replicates per test condition. A total of 104fish samples were eviscerated, stored until rigour had resolved and thenfilleted, yielding a total of 208 fillets.29The treatments included the following: C1 (control samples: vacuum packaged and hot smoked), C2 (control samples: modified atmosphere packaged and hot smoked), V1 [vacuum packaged with 1% (v/w) thyme EO added and hot smoked], M1 [modified atmosphere packaged with 1% (v/w) thyme EO added and hot smoked], V2 [vacuum packaged with 1% (v/w) clove EO added and hot smoked] and M2 [modified atmosphere packaged with 1% (v/w) clove EO added and hot smoked]. Each group included 52fillets.

Brine salting, essential oil treatments and smoking process

The salting and essential oil application processes were performed simultaneously. The rainbow trout fillets were immersed in brine (20% NaCl) at a ratio of 1 : 1 (w/w) for 1 h. Thyme and clove EOs were added to the two lots offilleted samples in appropriate volumes to cover both sides of each fillet using a micropipette to achievefinal concentrations of 0.1 and 1% (v/wt) EO. Undiluted thyme and clove essential oils were applied using a micropipette. In all treatments (described later), the antimicrobials were massaged onto the product to obtain an even distribution of the oil using glovedfingers to avoid cross-contamination of the samples and the transmission of microorganisms. Then thefillets were dried at 30°C for 30 min. After drying,fish were transferred to the smokehouse (Aqua Tech R 137/12). Samples were smoked at 50°C, 60°C, 70°C and 80°C for a total of 2 h for a period of 30 min. Thefillets were packaged by applying a vacuum or a modified atmosphere (50% CO2+ 50% N2).

Vacuum and modified atmosphere packaging

Allfilleted samples including the control were packaged in 15 × 25 cm thick polyethylene/polyamide (three-seal bags GB 70) obtained from Südpack Verpackungen GmbH and Co. (Ochsenhausen, Germany), having an O2permeability of 40 cm3/(m2.day.atm) at 23°C, an N2 permeability of cm3/

(m2.day.atm) at 23°C, CO2permeability of 145 cm3/(m2.day.atm) at 23°C and a water vapour

perme-ability of<3 g (m2.day.atm) at 23°C. After the application of EOs and the packaging treatments were complete, the rainbow trout fillets were stored under refrigeration (4 ± 1°C) and were subjected to microbiological [total aerobic mesophilic bacteria (TMAB), psychrotrophic bacteria, lactic acid bacteria (LAB), yeast and mould], chemical [pH, thiobarbituric acid-reactive substances (TBARS) and total volatile base-nitrogen (TVB-N)] and sensory analyses. The microbiological and chemical analyses were performed 0, 10, 20, 30, 40, 50, 60, 70, 80, 90, 100, 110 and 120 days of storage. Microbiological analysis

A sample (25 g) was taken from each fillet, transferred aseptically to a stomacher bag containing 225 ml of 0.1% peptone water and was homogenized for 60 s using a Stomacher blender (Lab Stom-acher Blender 400-BA 7021 Seward Medical, UK) at room temperature. For microbial analyses, 0.1 ml samples of serial dilutions (1 : 10, diluent: 0.1% peptone water) were inoculated on agar plates. The TMAB and total psychrotrophic aerobic bacteria (TPAB) numbers were determined using plate count agar (Merck 1.05463.0500) plates that were incubated at 30°C for 2 days or at 10°C for 7 days, respectively. The number of LAB was determined using Man Rogosa Sharpe agar (Oxoid CM0361) plates that were incubated at 30°C for 2 days. The number of yeasts and moulds was determined using Rose Bengal Chloramphenicol agar (Merck 1.00467.0500) plates that were incubated at 25°C for 5 days.

Chemical analysis

The TVB-N content was determined using the distillation method reported by Malle and Tao.30For TVB-N, fish muscle (40 g) was homogenized with 6% trichloroacetic acid (80 ml) in Ultra-Turrax. The homogenates were filtered through a filter paper Whatman No. 1, and 25 ml of the filtrate was taken. Five millilitres 10% NaOH was added to the filtrate and distilled. The distillate was titrated 0.1 N H2SO4. The TVB-N contents were expressed as mg/100 g offish muscle. The TBARS content

was determined as reported by Lemon31and Kilic and Richards.32 Fish muscle (12 g) was homoge-nized with 7.5% trichloroacetic acid, 0.1% ethylenediaminetetraacetic acid and 0.1% propyl gallate for 15–20 s in an Ultra-Turrax. The mixture was filtered through a Whatman No. 1 filter paper (Whatman®Schleicher&Schuell CAT No:1001 125). Three millilitres of thefiltrate was taken. Three millilitres 0.02 M thiobarbituric acid (TBA) was added to the filtrate. The mixture was heated in boiling water bath (100°C) for 40 min, then cooled. The absorbance at 530 nm was measured with a spectrophotometer (Shimadzu Corporation, Japan). The TBARS content was expressed asμmol of malondialdehyde (MDA)/kg of fish muscle. The pH was determined according to the method of Gokalp et al.33 The pH values were recorded by using a Schott model pH metre (Schott, Lab Star pH) after homogenization of each 10 gfish muscle sample in 100 ml distilled water.

Sensory evaluation

Sensory analysis of rainbow trout was performed by a panel offive experienced panellists.34The qual-ity of the rainbow troutfillets was assessed based on the appearance, taste and odour characteristics using a 5-point descriptive scale. A score of 5 indicated‘very good’ quality, a score of 4.0 indicated ‘good’ quality, a score of 3.0 ‘normal’ quality, a score of 2.0 ‘bad’ quality and a score of 1.0 denoted ‘very bad’. All of the samples were stored at 4°C until the sensory analyses were performed. The sam-ples for sensory evaluation were fried in oil in a teflon pan for 10 min and cooled to room temperature. Statistical analysis

The experiments were replicated twice on two separate occasions using different fish samples. The analyses were performed in duplicate for each experimental replicate. All of the data obtained in this study were subjected to analysis of variance, followed by Duncan’s multiple range test to determine if difference between the mean values was significant at α = 0.05 using SPSS software (SPSS 17.0; Chicago, IL, USA).35

RESULTS AND DISCUSSION Microbiological changes

The changes in the TMAB content of the refrigerated rainbow troutfillets in vacuum packaging or MAP during the storage period are shown in Figure 1a. Microbiological counts infillets were found to be significant (p < 0.05) during storage time. On the initial day (day 0), the TMAB content (Figure 1a) of the rainbow trout fillets was 2.00 log cfu/g. The TMAB contents of C1, C2 and V1 rainbow trout fillets exceeded 7 log cfu/g, which is considered the upper limit for acceptable TMAB levels in fresh marine species36on days 50, 70 and 110 of storage, respectively. This limit was not exceeded throughout storage in M1, V2 and M2. At the end of the 120 day storage period, the TMAB levels in C1, C2, V1, M1, V2 and M2 had reached 11.9, 11.2, 7.95, 6.48, 6.03 and 5.00 cfu/g, respectively. Initially (day 0), psychrotrophic bacteria content (Figure 1b) of the rainbow troutfillets was 2.00 log cfu/g. The psychrotrophic bacteria levels in C1, C2, V1 and M1 rainbow trout fillets exceeded 7 log cfu/g, which is considered the upper limit of acceptability of psychrotrophic bacteria in fresh marine species,36 on days 50, 80, 100 and 120 of storage, respec-tively. This limit was not exceeded throughout storage in V2 and M2. At the end of the storage pe-riod, the levels of psychrotrophic bacteria in C1, C2, V1, M1, V2 and M2 had reached 12.1, 11.7, 8.36, 7.05, 6.27 and 5.25 log cfu/g, respectively. Microbial growth and lipid oxidation are factors that affect the shelf life and, consequently, consumers’ acceptance of fresh fish and meat.36 The control group exhibited the highest bacterial counts, and the groups treated with thyme and clove EOs exhibited the lowest bacterial counts, indicating that thyme and clove EOs have a high level of antimicrobial activity. The combination of MAP and clove oil treatment might have a synergistic effect, hindering microbial growth and decreasing the final counts of spoilage microorganisms in rainbow trout. The rate of bacterial growth in the MAP samples was lower than that in the vacuum-packaged samples, most likely because of the presence of CO2 gas in the packaging.

Carbon dioxide can effectively inhibit the growth of TMAB and TPAB. Similar results were observed by several researchers.16,37–41 Erkan16 reported that thyme and garlic oil treatment was effective in eliminating the growth total aerobicflora. Likewise, Emir Coban and Ozpolat41reported that rosemary extract was effective in controlling the growth of bacteria. Chouliara et al.42observed that 1% oregano oil and air packaging treatment reduced the growth of aerobic bacteria in chicken meat. Ozyılmaz43 found that thyme essential oil reduced the growth of psychrotrophic bacteria. Mahmoud44reported that various EOs reduced growth TMAB and TPAB. Mejlhom and Dalgaard45 reported that the combined use of MAP and oregano oil in the preservation of codfillets retarded the growth of aerobic microorganisms during refrigeration storage (2°C).

Lactic acid bacteria are facultative anaerobic bacteria that can grow under both anaerobic and aero-bic conditions.46The initial LAB content (Figure 1c) on day 0 was 2.00 log cfu/g. At the end of the storage period, the LAB contents of C1, C2, V1, M1, V2 and M2 were 11.0, 10.2, 7.16, 6.95, 5.87 and 4.73 log cfu/g, respectively. Similar findings were reported by Schulze,39 Emir Coban40 and Mahmoud et al.44Giatrakou et al.24and Kykkidou et al.47reported that thyme–oregano oil treatment was effective in eliminating the growth of total viable count (TVC) and LAB in modified atmosphere packaged fish under refrigerated storage. Pournis et al.13 Stamatis and Arkoudelos20 and Kostaki48 observed that thyme oil treatment did not reduce the growth of LAB.

The yeast and mould levels (Figure 1d) were 2.00 log cfu/g on day 0. At the end of the storage pe-riod, C1, C2, V1, M1, V2 and M2 contained 7.95, 7.24, 4.63, 4.34, 3.63 and 3.20 log cfu/g yeast and mould, respectively. These results showed the antifungal activity of EOs. Similarly, yeast and mould (day 0) counts have been reported for hot smoked rainbow trout.40,41Ozyılmaz,43Rasooli and Owlia49 and Karaman et al.50observed that thyme treatment reduced yeast–mould counts.

Chemical changes

Total volatile base-nitrogen. The amount of TVB-N is an important criterion in determining fresh-ness offish and fish products because generally, TVB-N values increase according to progression of spoilage process.51TVB-N consists of TMA and ammonia with the effect of the bacteria and endog-enous enzymes infish. TVB-N value increases depending on the storage period in preservation fish

Figure 1. (a) Total aerobic mesophilic bacteria counts; (b) psychrotrophic bacteria; (c) lactic acid bacteria counts; and (d) yeast and mould changes of treatment with thyme and clove essential oil (1% v/w) hot smoking rainbow trout fillets during cold storage in vacuum and modified atmosphere

andfish products.16,52–55In rating the quality of freshfish, the term ‘very good’ corresponds to a TVB-N value of up to 25 mg/100 g,‘good’ to values of up to 30 mg/100 g and ‘marketable’ to values of up to 35 mg/100 g, whereas‘spoiled’ denotes an unacceptable product corresponding to TVB-N values of more than 35 mg/100 g..56Initially (day 0), the TVB-N values (Figure 2a) of the rainbow troutfillets were 18.1, 17.5, 15.6, 15.1, 14.2 and 12.4 mg N 100/g for C1, C2, V1, M1, V2 and M2, respectively. The TVB-N values of the C1, C2, V1, M1, V2 and M2 rainbow troutfillets exceeded 25 mg/100 g, which is considered as the upper acceptable TVB-N limit for rainbow trout29 on days 20, 30, 70, 80, 80 and 90 of storage, respectively. The TVB-N values of all of the groups increased during the storage period. TVB-N values in control groups were higher than that in EO-treated groups. These in-creases in the TVB-N value can be explained by proteolysis driven by the enzymatic and microbial activity of the samples. Values similar to our TVB-N data have been reported for rainbow trout.16 Goulas and Kontominas17 found that TVB-N of treatment thyme oil is lower than that of the non-treatment sample. Very little information is available in the literature on the effect of EOs

Figure 2. (a) Total volatile base-nitrogen; (b) thiobarbituric acid reactive substances; and (c) pH changes of treatment with thyme and clove essential oil (1% v/w) rainbow troutfillets during cold

on the TVB-N production infish. The inhibition of TVB-N production in smoked rainbow trout samples may be attributed to the effects of MAP and/or with the combined synergistic effect of thyme and rosemary oil, the latter known to possess antibacterial properties because of its phenolic (carvacrol and thymol) and organosulfur (allicin) constituents.28

Lipid oxidation. Lipid oxidation is one of the factors that cause product spoilage. Rancidity, a foul taste and a yellow colour might develop during the oxidation of fresh fish or fish products, partic-ularly those with high lipid content.57 Lipid oxidation is a major quality problem, particularly in fatty marine species. This process leads to the development of off-odours and off-tastes known as oxidative rancidity in edible oils and fat-containing foods. TBA is a secondary breakdown product of lipid oxidation and is widely used as an indicator of the degree of lipid oxidation, which can be assessed by measuring MDA content. MDA is formed through hydroperoxides, which are the initial reaction products of polyunsaturated fatty acids and oxygen.58–61In food suitable for consumption, the TBA values might reach the upper limit of 7 to 8 mg of MDA kg-1;31,54,62in‘perfect material’, the TBA value should be less than 3 mg of MDA/kg, and in‘good material’, the TBA value should be no more than 5 mg of MDA/kg. The TBA values indicate the degree of rancidity of products, and values greater than 3–4 mg of MDA/kg indicate a loss of product quality.63 The TBARS values of the rainbow trout fillets (Figure 2b) were 2.55, 2.59, 2.08, 1.82, 1.59 and 1.17 μmol MDA/kg ini-tially and were 17.5, 15.1, 10.3, 9.81, 5.85 and 4.80μmol/kg at the end of the storage period for C1, C2, V1, M1, V2 and M2, respectively. These values increased in all groups during the storage period. TBARS values in EO-treated groups were lower than control groups. Lower production TBARS index in EO-treated samples may be due to the antioxidant properties of EO. These results showed the antioxidant characteristics of EOs. Similar results have been obtained in the literature on the effective antioxidant activity of EOs in rainbow trout16,40 and pike.41 Fernandez-Lopez et al.64 found that TBA values in EO-treated groups were lower than control groups. Serdaroğlu and Felekoğlu65 observed that rosemary and onion extract inhibited the TBA. The use of thyme oil to protect muscle foods against oxidation has been reported in the literature. Mariutti et al.66and Erkan and Bilen67found that garlic oil and thyme oil were effective means of controlling lipid oxidation in chicken and fish meat, as reflected in TBARS values.

pH. The pH of freshfish flesh is approximately neutral. In the post-mortem period, the decomposition of nitrogenous compounds leads to an increase in the pH of thefish flesh, which indicates a loss of quality.68The pH value offish meat generally ranges from 5.7 to 6.6. Fresh fish has a neutral pH value, and after death, upon the formation of lactic acid, the pH value mightfirst fall, and then rise as spoilage develops over prolonged storage.69The pH values of the rainbow troutfillets (Figure 2c) were 6.29, 6.37, 5.83, 5.59, 5.65 and 5.52 initially and 6.84, 6.77, 6.44, 6.36, 6.28 and 6.25 at the end of the stor-age period for C1, C2, V1, M1, V2 and M2, respectively. Similarly, pH values have been reported for rainbow trout.16,40The pH values of the MAP groups were lower than those of the vacuum-packed samples, which might be explained by the formation of carbonic acid from the conversion of carbon dioxide in the MAP samples.

Sensory changes. The results of the sensory evaluation (appearance, taste and odour) of the smoked rainbow trout samples are presented in Figure 3a–c. A significant difference (p < 0.05) was found to be between the samples for appearance, taste and odour during storage time. The sensory scores for each sample indicated‘good quality’ after processing. However, the scores for the C1 and C2 samples had particularly decreased by the end of the storage period, which can be explained by the increase in microbial growth and TVB-N values. Similar results have been reported in other recent stud-ies.16,40,41,61,70–72The taste of the C1, C2, V1, V2 and M1 was scored as ‘spoiled’ by the panellists after 50, 60, 90 and 110 days, whereas groups M2 continued to be scored as good quality after 120 days. The appearance and odour of clove extract were much stronger in groups V2 and M2 than in groups V1 and M1. Smoke and the most intense odour of clove (M2) were scored by the panellists as very good odour quality (5 points). These results showed that samples with high clove oil have ac-ceptable overall scores, because of the limiting effect of thyme on microbiological activity and TVB-N value and the positive attributes of clove flavour. V2 and M2 samples were assessed as the most acceptable products by the panellists.

In conclusion, EOs treatment to hot smoking had a positive effect on the shelf life of rainbow trout, especially clove oil showed more positive effect when compared with thyme oil. In the present study, usage of these EOs in smokedfish showed that EOs have a positive effect on the product’s chemical, microbial and sensory attributes. Overall, the combined use of clove EO (1%, v/w) and MAP exerted a synergistic effect, extending the shelf life of rainbow troutfillets. According to the results of TMAB analyses, shelf life of rainbow troutfillets was estimated as 50, 70 and 110 days for C1, C2 and V1 respectively. M1, V2 and M2 samples did not exceed 7 log cfu/g after 120 days of storage.

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