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Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs
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Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs Fathy A. Khalafalla, Fatma H.M. Ali, Abdel-Rahim H.A. Hassan* Food Hygiene Department, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef, 62512, Egypt
article info
abstract
Article history:
The present study was preformed to evaluate the effect of dip treatments by thyme
Received 6 August 2014
(Thymus vulgaris) extract (0.5%) and rosemary (Rosmarinus officinalis) extract (1.5%) on
Accepted 2 January 2015
the quality and shelf life of Nile tilapia (Orechromis niloticus) fillets during refrigerated
Available online xxx
storage at 2 ± 1 C. The control (untreated) and treated groups were examined periodically at day zero and every 3 days (0, 3, 6, 9, 12, 15, 18, ....) during refrigeration until apparent
Keywords:
decomposition of each group, with sensory, physicochemical and microbiological
Thyme
methods. The obtained results showed that thyme extract has strong antimicrobial and
Rosemary
antioxidant activity and can maintain the quality parameters and extend the shelf life of
Nile tilapia
refrigerated Nile tilapia fillets for 9 days longer than control one, while rosemary extract
Microbiological
had efficient antioxidant activity with weak antimicrobial action. Copyright 2015, Beni-Suef University. Production and hosting by Elsevier B.V. This is an open
TBA
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/
TVB-N
4.0/).
1.
Introduction
About one-third of the world's food production is lost annually as a result of microbial spoilage (Lund et al., 2000). The high levels of moisture, free amino acids and polyunsaturated fatty acids, and nutrient content, in addition to high amount of naturally present autolytic enzymes and high pH render fish an easily perishable product, often going bad within a short period under refrigerated conditions (Cakli et al., 2007). Spoilage of fish results from changes brought about by biological reactions such as oxidation of lipids, the activities of the fish muscular enzymes, and the metabolic activities of
microorganisms. Enzymatic and chemical reactions are usually responsible for the initial loss of freshness whereas microbial activity is responsible for the obvious spoilage and thereby establishes product shelf life (Arashisara et al., 2004). Increasing demand for high quality ready-to-cook fish products with extended shelf-life has initiated the development of several innovative techniques to keep quality attributes as long as possible and yield safe products (Maftoonazad and Badii, 2009). Due to modern trends consumers adopt towards the consumption of minimally processed foodstuffs containing no chemical preservatives, lightly preserved food products with natural additives have become popular. Thyme and rosemary extracts come to fulfill part of the increasing
* Corresponding author. Tel.: þ20 822327982; fax: þ20 822322066. E-mail address: [email protected] (A.-R.H.A. Hassan). Peer review under the responsibility of Beni-Suef University. http://dx.doi.org/10.1016/j.bjbas.2015.02.005 2314-8535/Copyright 2015, Beni-Suef University. Production and hosting by Elsevier B.V. This is an open access article under the CC BYNC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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demand for products with a ‘‘green image’’, being obtained exclusively from plant materials, that possess antibacterial, antioxidant, antiviral and antimycotic properties (Holley and Patel, 2005). The use of rosemary and thyme as natural preservatives in food industry has been reported previously by several studies (Cadun et al., 2008; Harpaz et al., 2003; Kostaki et al., 2009; Mahmoud et al., 2004; Marino et al., 1999; Offord et al., 1997; Szczepanik and Stodonik, 2003). Rosemary plant (Rosmarinus officinalis) contains certain compounds such as carnosol and carnosic acid, with high antioxidant activity, and others with minor activity (Offord et al., 1997). Carvacrol and thymol (extracted from thyme) are hydrophobic compounds that dissolve in the hydrophobic domain of cytoplasmic membrane. They cause increasing in the permeability to ATP that results in lethal damage to the bacterial cell (Burt, 2004). In the present study the antibacterial and antioxidant activities of thyme and rosemary extracts as natural food preservatives were evaluated by dipping for quality improvement and shelf-life extension of aerobically packaged Nile tilapia fillets during refrigerated storage by examining the sensory, physicochemical and microbiological attributes.
2.
Materials and methods
2.1.
Preparation of fish fillets
About 100 Nile tilapia (Orechromis niloticus) fish samples (of average weight ¼ 350e500 gm) were purchased from a fish market in Beni-Suef City, Egypt at the same day of harvesting. Each sample was gutted, deheaded, cleaned and filleted into two pieces of about 100 g weight for each piece. Then the samples were wrapped in sterile polyethylene bags and directly transferred to the laboratory in sterile icebox for further preparation within 2 h after purchasing.
2.2.
Thyme and rosemary extraction
The extraction of active ingredients from dry thyme (Thymus vulgaris) and rosemary (Rosmarinus officinalis) plant was done according to the technique developed by Tandon and Rane (2008). In brief; the dried plant material was size reduced with milling using hammer mill. Extraction of the plant material was carried out by immersion in absolute methanol for three days with agitation using automatic shaker. Then filtration through a piece of gauze to remove solid plant particles was done, the extract was re-filtered through filter paper to remove fine or colloidal particles from the extract. The enriched extract was concentrated by evaporation of the solvent with heating in water bath at 65 C until solid mass was obtained. Finally Drying the extract by spreading under shaded area till complete dryness, then stored in the refrigerator until using. Thyme extract was used for preparation of 0.5% (w/v) solution and rosemary extract was used for preparation of 1.5% (w/v) solution in distilled water of 4 C.
2.3.
Dipping of fish fillets into plant extracts
The samples were divided into 3 groups; the 1st was untreated control (C), while the 2nd group was dipped into rosemary extract 1.5%/10 min (R), and the 3rd was dipped into thyme extract 0.5%/15 min (T) inside a refrigerator, then the dipping solution was discarded.
2.4.
Packaging and storage
Treated fish fillets samples were labeled and aerobically packaged as triplicates inside fiber dishes, then stored at 2 ± 1 C inside the refrigerator. The treated groups were subjected to sensory, physicochemical and microbiological assessment at day zero (within 2 h after treatment) then periodically every three days until decomposition (0, 3rd, 6th, 9th, 12th, 18th … ..).
2.5.
Chemicals and reagents
TBA reagent was composed of 0.2883 g of 0.02 M 2-Thiobarbituric acid (C4H4N2O2S, Sigma Aldrich) in 100 mL of 90% glacial acetic acid (ADWIC, Egypt). 125 ug of Butylated Hydroxy Toluene (BHT) (C15H24O CN, Sigma Aldrich)/g of flesh were used to prevent autoxidation during the heating step of TBA-RS determination. Screened methyl red indicator was composed of 0.016 g methyl red and 0.083 g bromocreasol green in 100 mL ethanol for determination of TVB-N. Magnesium oxide (Mg O) was purchased from (LOBA, India) and N/10 Sulphuric acid (H2SO4) was from (ADWIC, Egypt). While peptone water was purchased from (MAST, UK), Lauryl Sulphate Tryptose broth from (HIMEDIA, India), and Standard plate count agar and Brilliant Green Bile Lactose broth from (Biolife, Italy).
2.6.
Sensory evaluation
The sensory assessment was performed using the scoring test developed by Neuman et al. (1983) (Table 1). Five panelists were used to evaluate the sensory attributes of fillets samples. The fillets samples were blind-coded by special codes; the panelists were not informed about the experimental approach. They were asked to give a score for each of colour, odour & consistency while the fillets were raw. Then the samples without salt and spices were fried using high quality sunflower oil, cooled to 50 C then served to the panelists to complete the evaluation of the sensory attributes. The
Table 1 e : The scoring table for sensory evaluation of fish fillets designed by Neuman et al. (1983).* Overall acceptability equals 20; 5 for each of (appearance, odour, texture and flavour) of fish fillets. Score* 20 18.2e19.9 15.2e18.1 11.2e15.1 7.2e11.1 4.0e7.1
Grade Excellent Very good Good Middle Poor Spoiled
Acceptability Acceptable
Limit of acceptability Unacceptable
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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panelists were asked to wash their mouths with warm water between samples.
2.7.
Physicochemical analysis
2.7.1.
pH
The pH determination was done according to the method recommended by Korkeala et al. (1986). Briefly; ten grams of fish fillet was homogenized for about 2 min with an equal mass of distilled water in a food blender (Arnica Quick, China). After washing with distilled water (pH 7) at 26 C; the electrode of pH-meter (350 Jenway pH meter, UK) was introduced into the test portion and the temperature correction system was set to the temperature of the test portion. The pH was directly read from the scale on the instrument of the nearest 0.05 pH unit when constant value has been reached.
2.8.
Microbiological examination
2.8.1.
Preparation of the samples
Preparation of the fish fillets samples was carried out according to the muscle maceration technique recommended by ICMSF (1986). Ten grams of fish fillet were removed using sterile scalpel and forceps and transmitted to a sterile homogenizer flask containing 90 mL of 0.1% sterile peptone water. The contents were homogenized at 2000 r.p.m. for 2.5 min using a sterile homogenizer (MPW 302, Universal Laboratory Aid, Poland).
2.8.2.
Thiobarbituric acid-reactive substances (TBA-RS)
For determination of TBA-RS, the technique developed by Taraldgis et al. (1960) with additional modification of Pikul et al. (1983) was used. Briefly, ten grams of fillets sample were blended with 50 mL of distilled water in food blender/2 min. The mixture was quantitatively transferred to Kjeldahl flask by washing with additional 47.5 mL of distilled water. Then, 2.5 mL of 4 N Hcl solution were added to bring pH 1.5. Antioxidant (BHT) and anti pumping stones were added. Apparatus and heat flasks were assembled at the highest heat obtainable on the kjeldahl distillation apparatus. Five mL of the mixed distillate were pipetted into 50 mL glass stoppered tube and 5 mL of TBA reagent were added. The tubes were stoppered and their contents were mixed, and immersed in a boiling water bath for 35 min. A distilled water-TBA reagent (blank) was treated the same as the samples. After heating, be cooled under tap water for 10 min. A portion was transferred to a cuvette and the optical density of sample (D) was determined against the blank at a wavelength of 538 nm of the spectrophotometer. Calculation : TBAvalue ¼D7:8ðmg malondialdehydeðMDAÞ =kg fleshÞ
2.7.3.
Bacteriological techniques
Aerobic plate count (APC) at 35 C and coliforms MPN (3 tubes method) were performed according to the techniques recommended by AOAC (1990).
2.8.3. 2.7.2.
3
Aeromonas/Pseudomonas count
The technique recorded by Pireson et al. (1970) was applied. Briefly, 100 mL of homogenate was aseptically transferred to the surface of Glutamate starch phenol red agar medium (GSP, Merck Millipore, USA) and then spread by a sterile glass spreader. Inoculated plates were incubated at 25 C for 3 days. All pink colonies were counted as Pseudomonas while yellow colonies were counted as Aeromonas. Calculation: Pseudomonas count=g ¼ No: of colonies dilution factor 10 Aeromonas count=g ¼ No: of colonies dilution factor 10
2.9.
Statistical analysis
Data were subjected to analysis of variances (one wayANOVA) according to Knapp and Miller (1992) using (SPSS Statistics 17.0) software program. Data was expressed as mean values (n ¼ 3) with standard error. Differences among the mean values of the various treatments were determined by the least significant difference (LSD) test, and the significance was defined at P < 0.05.
Total volatile basic nitrogen (TVB-N)
TVB-N (mg N/100 g) was measured according to the method recommended by FAO (1986). One hundred mL of distilled water was added to 10 g of the minced fish fillet in a food blender and homogenized for two minutes. Sample was washed into distillation flask with a further 200 mL of water. Two grams magnesium oxide and two drops of antifoaming agent were added. The mixture was boiled for 10 min and distilled for exactly 25 min, using the same rate of heating, into 25 ml of 2% boric acid solution with few drops of screened methyl red indicator in a 500 ml flask. The heating was stopped and the condenser washed down with distilled water. Then, the contents of the flask were titrated with 0.1 N H2SO4 (titer) and 25 mL of 2% boric acid solution were also titrated against 0.1 N H2SO4 (blank). Calculation : Total volatile base ðmg N=100 g fleshÞ ¼ 14 ðtiter blankÞ
3.
Results and discussion
3.1.
Sensory evaluation
Sensory evaluation is the most popular way of assessing the freshness of fish. It is fast, simple, and provides immediate quality information (Reineccius, 1990). The data illustrated in Fig. 1 conclude the changes in the sensory attributes of control and treated fish fillets samples during refrigerated storage at 2 ± 1 C. The average scores of sensory attributes (overall acceptability) provided by the panelists at day zero were excellent (20 ± 0.0) for control (C) and thyme treated (T) samples, while it was very good (18.8 ± 0.06) for rosemary treated (R) samples. Low scores given to (R) group could be attributed to yellow discoloration and rosemary odour observed in fillets samples, this is in accordance with that reported by Hsieh et al. (2001). The overall acceptability for all samples
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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decreased gradually with storage time until became 4.8 ± 0.61, 6.5 ± 0.28 and 5.3 ± 0.72 for C, R and T groups, to be below the lowest acceptability limit (7.2) according to the scoring table designed by Neuman et al. (1983) at 9th, 9th and 18th day of storage, respectively.
3.2.
Physicochemical analysis
3.2.1.
pH
Generally, the natural pH of live fish is just above 7.0, typically about 7.3, but this value falls markedly after death as the fish goes through rigor mortis and glycogen is converted to lactic acid. In most species, the post mortem pH is between 6.0 and 6.8. In the present study, a gradual increase in pH values with storage time from 6.2 ± 0.02, 6.2 ± 0.02 and 6.2 ± 0.01 at day zero has been observed to reach 7.16 ± 0.11, 7.23 ± 0.04 and 7.27 ± 0.01 at 9th, 9th and 18th day of refrigerated storage for C, R and T groups, respectively (Fig. 2). Similar results of pH values at day zero of chilled storage were recorded by Sallam et al. (2007) and Zambuchini et al. (2008), while Hernandez et al. (2009) reported higher pH values at day zero. Differences among the initial pH values than those reported in other studies may be due to the species, diet, and season, level of stress during the catch as well as type of muscle. pH values reported in the current study were significantly higher (p < 0.05) in C and R groups than T group. Higher pH values of the C and R groups could be attributed to the increase in volatile bases such as ammonia produced by either microbial or muscular enzymes (Li et al., 2012). As regards to the maximum acceptable limit of pH value (6.5) in fish and fish products recommended by EOS (2005), it was evident that C, R and T groups exceeded such limit at 6th, 6th and 12th day of storage, respectively, however, the samples still acceptable according to the sensory evaluation results. These results are in accor€ dance with that recorded by Ozyurt et al. (2009) that pH values above 7.1 are indicative of decomposition in fish. In this regard, Newton and Gell (1981) reported that pH value of fish
Fig. 1 e The changes in overall acceptability (total score of the sensory attributes) of control and treated fish fillets samples during refrigerated storage The error bars represent the SD of three replicates (n ¼ 3).
Fig. 2 e The changes in pH of control and treated fish fillets samples during refrigerated storage The error bars represent the SD of three replicates (n ¼ 3).
varies from 5.8 to 7.2 depending on struggling at the time of harvesting but the normal variation is 5.8e6.5.
3.2.2.
TBA-RS
TBA value is an index of lipid oxidation measuring malondialdehyde (MDA) content. MDA formed through hydroperoxides, which are the initial reaction product of polyunsaturated fatty acids with oxygen (Fernandez et al., 1997). In the current study, the initial TBA-RS values of C, R and T groups increased progressively (p < 0.05) with storage time from 0.093 ± 0.04, 0.036 ± 0.013 and 0.04 ± 0.008 at day zero until the last time of examination before spoilage, when a decline in all groups has been observed to reach 0.796 ± 0.07, 0.316 ± 0.021 and 0.313 ± 0.008 mg MDA/Kg at 9th, 9th and 18th day of refrigerated storage, respectively (Fig. 3A). That decline could be attributed to production of secondary lipid oxidation products from MDA, this phenomena was also observed by Aubourg (1993). TBA-RS values of C group were significantly higher (p < 0.05) than treated groups in each occasion of examination. Similar results of TBA-RS values at day zero of chilled storage with progressive increase with storage duration were obtained by Goulas and Kontominas (2007) and Hernandez et al. (2009), while higher initial values than obtained in this study was recorded by Selmi and Sadok (2008). The antioxidant activity of rosemary extract was previously reported by Offord et al. (1997) who mentioned that rosemary plant (Rosmarinus officinalis) contains certain compounds such as carnosol and carnosic acid, with high antioxidant activity. Moreover the antioxidant activity of thyme extract was previously mentioned by Marino et al. (1999) who reported that thyme extract is a potential natural antimicrobial and antioxidant agent, as it contains high concentrations of phenolic compounds including carvacrol, thymol, p-cymene and g-terpinene. Concerning the permissible limit of TBA value in fish and fish products (4.5 mg MDA/kg) recommended by EOS (2005); neither treated groups nor control one exceeded such limit in any occasion of examination even after showed objectionable odours and flavours; these results substantiate
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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Fig. 3 e The changes in Thiobarbituric acid reactive substances TBA-RS (A) and total volatile basic nitrogen TVB-N (B) of control and treated fish fillets samples during refrigerated storage The error bars represent the SD of three replicates (n ¼ 3).
the hypothesis reported by Connell (1990) who stated that TBA values of 1e2 mg MDA/kg of fish flesh are usually regarded as the limit beyond which fish will normally develop an objectionable odour and taste. The antioxidant properties of rosemary extract were previously recorded by Cadun et al. (2008); Szczepanik and Stodonik (2003); and Tironi et al. (2010), while the antioxidant properties of thyme extract were previously reported by Kostaki et al. (2009).
3.2.3.
TVB-N
The Commission of the European Community (1995) stated that TVB-N critical limits of 25, 30 and 35 mg N/100 g were established for different groups of fish species and have been proposed as an upper acceptability limit for spoilage initiation for fresh fish. Values of TVB-N in all groups are illustrated in Fig. 3B. At day zero TVB-N of C, R and T groups were 7.23 ± 0.46, 7.93 ± 0.40 and 7.00 ± 0.80 mg N/100 g. Similar results were detected by Chan-Yin et al. (2002) and Sallam et al. (2007). Higher values of TVB-N at day zero of chilled storage were reported by Goulas and Kontominas (2007) and Kilinc and Cakli (2004), while lower values were achieved by € Ozogul et al. (2004). Differences in TVB-N values than reported by others could be attributed to that TVB-N value is affected by species, catching season and region, age and sex of the fish. There was a progressive increase (p < 0.05) in TVBN values with storage duration in all groups to reach 30.56 ± 0.40, 29.86 ± 1.23 and 32.66 ± 1.23 mg N/100 g at 9th, 9th and 18th day of refrigerated storage in C, R and T groups, respectively. Such increase may be due to ammonia production in the fish flesh during storage as a result of microbial and muscular enzymes activities. TVB-N values were significantly higher (p < 0.05) in C and R groups than T group in most examination occasions (Fig. 3B), which indicating that rosemary extract has a poor effect on microbial and enzymatic activities, this hypothesis is substantiated by the high APC in control and R treated samples, this agrees with that reported by Gutierrez et al. (2008). Regarding the permissible limits of TVB-N in fish recommended by EOS (2005) and Commission of the European Community (1995), it is clear from Fig. 3B that 30 mg N/100 g approximately was
reached by C, R and T groups at 9th, 9th and 18th day of storage life, respectively.
3.3.
Microbiological examination
3.3.1.
Aerobic plate count (APC)
About one-third of the world's food production is lost annually as a result of microbial spoilage. Microbial activity is responsible for spoilage of most fresh and of several lightly preserved seafoods. Possibly, for this reason, the total number of microorgansims, named total viable counts (TVC) or aerobic plate counts (APC), have been used in mandatory seafood standards in some European Countries, Japan and USA (Lund et al., 2000). In this respect, ICMSF (1986) stated that the upper acceptability limit of total viable bacterial count in fresh fish is 7 log10 CFU/g flesh, and 6 log10 CFU/g is the maximum permissible limit of APC recommended by EOS (2005) in chilled fish. The changes in APC with storage time in all groups were concluded in Fig. 4A. The initial APC (2.3 103 ± 9.77 102, 6.9 102 ± 9.4 10 and 4 102 ± 1.5 102 CFU/g) increased progressively (p < 0.05) with storage time to final values of 2.4 107 ± 2.05 107, 8.2 106 ± 2.6 105 and 1.1 106 ± 1.7 105 CFU/g at 9th, 9th and 18th day of refrigerated storage (time of production of off odours and taste by the sensory evaluation) in C, R and T groups, respectively. Similar results were reported by Fu and Labuza (1993) and Zambuchini et al. (2008). In this regard, Fu and Labuza (1993) found that the duration of refrigerated storage (0 C) of fish had a significant (P < 0.05) effect on bacterial count, which tended to increase as the storage duration increased. Furthermore, Hernandez et al. (2009) mentioned that the initial mesophilic count in commercial-sized meagre fillets was 3.11 log10 CFU/g, which increased to reach 11.2 log10 CFU/ g, at 18th day of chilled storage. APC in T group was significantly (p < 0.05) lower than other groups in each occasion of examination which indicates the high antimicrobial activities of thyme extract. This is substantiate the hypothesis reported by Burt (2004) that carvacrol and thymol (extracted from thyme) are hydrophobic compounds that dissolve in the
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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Fig. 4 e The changes in aerobic plate count APC (A) and Coliforms MPN (B) of control and treated fish fillets samples during refrigerated storage (n ¼ 3).
hydrophobic domain of cytoplasmic membrane, they increase the permeability to ATP that results in lethal damage to the bacterial cell. According to the permissible limit of APC in chilled fish (106 CFU/g) recommended by EOS (2005), it was evident from Fig. 4A that all groups exceeded such limit at the day when it became unacceptable by the sensory evaluation results. Regarding the upper acceptability limit recommended by ICMSF (1986) for total viable count in fresh fish (7 log10 CFU/g flesh), it could be observed that C group exceeded such limit at 9th day of storage, while such limit has not exceeded by treated groups until time of spoilage. € In this respect, Ozogul et al. (2004) mentioned that when the aerobic plate count reaches 106 CFU/g or mL in a food product, it is assumed to be at, or near, spoilage. Furthermore, Parallel Food Testing in the European Union (1995) stated that in a recent European study by consumers, fish was assumed “not to be in a good enough condition to be stored for long” when total plate count were 106 CFU/g. The antimicrobial activities of thyme extracts were previously reported by Fan and Chen (2001); Ismail et al. (2012); Mahmoud et al. (2004) andNzeako et al. (2006).
3.3.2.
Coliforms MPN
The initial coliforms MPN in C, R and T groups increased gradually from 4.1 10 ± 2.68 10, 2.8 10 ± 2 10 and 2.7 10 ± 1.1 10 to final values of 2.3 103 ± 2.64 102,
2.9 103 ± 8.3±102 and 1.5 103 ± 3.3 102 bacteria/g at 9th, 9th and 18th day of refrigerated storage, respectively (Fig. 4B). At zero and 3rd day of storage, there was no significant difference (p < 0.05) in coliforms MPN between groups, while at 6th day of storage, C group was significantly higher (p < 0.05) than treated groups, as well as at 9th day, C and R groups were significantly higher (p < 0.05) than T group in coliforms MPN. The inhibitory effect of thyme against coliform group of bacteria was previously reported by Harpaz et al. (2003); Hernandez et al. (2009) and Mahmoud et al. (2004). In this respect; the National Academy of Science (1985) reported that coliform group of bacteria in fish and fishery products has been considered important in microbiological analysis on account of their significance as indicator organisms for pin pointing the unhygienic conditions during catching, handling, processing and distribution ().
3.3.3.
Aeromonas and Pseudomonas counts
Aeromonas spp. are considered emerging food borne pathogens that are associated with septicemia, gastroenteritis, enterocolitis and wound infection in humans (Janda, 1991; Isonhood and Drake, 2002). While Pseudomonads are a good spoilage index in fishes and a marker for fish deterioration, furthermore they have to be the specific spoilage organism (SSO) in ice-stored tropical freshwater fish (Gram et al., 1990). In the present study, Fig. 5A and B clarifies the changes in Aeromonas and Pseudomonas counts in all groups during
Fig. 5 e The changes in Aeromonas (A) and Pseudomonas (B) counts of control and treated fish fillets samples during refrigerated storage (n ¼ 3). Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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refrigerated storage. The initial Aeromonas counts in C and R groups increased gradually with storage time from <102 ± 3.7 10 and <102 ± 3.5 10 CFU/g to reach final values of 3.2 102 ± 2.18 10 and 4.0 102 ± 4.8 10 CFU/g at 9th day of storage, respectively. While in T group still <102 CFU/g until 12th day of storage then increased to reach a final value of 2.1 102 ± 7.6 10 at 18th day of storage. Quiet similar results were obtained by Hernandez et al. (2009); Jay (1986); Mahmoud et al. (2004). Regarding Pseudomonas counts, it was noticed that the initial counts in C and R groups increased gradually with storage time from 1.3 102 ± 2.96 10 and 1.2 102 ± 6.4 10 CFU/g to final values of 1.5 103 ± 5.92 102 and 3.1 103 ± 2.6 102 CFU/g, respectively. In T group Pseudomonas count still <102 CFU/g until 12th day of storage then increased to a final value of 9.5 102 ± 4.8 102 CFU/g at 18th day of storage. The poor antibacterial activity of rosemary extract was previously reported by Hernandez et al. (2009) and Szczepanik and Stodonik (2003).
4.
Conclusion
From the previously mentioned data, it could be concluded that the dipping of Nile tilapia fillets into thyme extract before refrigeration can retain the quality attributes and extend the shelf life for about 9 days more than control during refrigerated storage at 2 ± 1 C. The antimicrobial and antioxidant activities of thyme extract were recorded without any adverse effect on the sensory acceptability of the treated fillets. Rosemary extract was reported to has an antioxidant activity with clear reduction in the TBA-RS value in treated fillets than control group, while it has no antimicrobial activity, so it is recommended to be used with an antimicrobial agent for extension of shelf life.
references
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moluccensis) during storage in ice. Food Chem 2009;114:505e10. Parallel Food Testing in the European Union. Fish. London, UK: International Consumers Research & Testing Limited; 1995. Pikul J, Leszezynski DE, Kummersw F. Auto-oxidation by elimination of sample butylated hydroxytoulene addition before thiobarbituric acid assay for malonaldehyde in fat from chicken meat. J Agric Food Chem 1983;31:1338. Pireson MD, Thompson DLC, Ordal ZJ. Microbiological, sensory and pigment changes of aerobically and anaerobically packaged beef. J Food Technol 1970;24:1171. Reineccius G. Off-flavors in foods. Crit Rev Food Sci Nutr 1990;29:381e402. Sallam KI, Ahmed AM, Elgazzar MM, Eldaly EA. Chemical quality and sensory attributes of marinated Pacific saury (Cololabis saira) during vacuum-packaged storage at 4 C. Food Chem 2007;102:1061e70. Selmi S, Sadok S. The effect of natural antioxidant (Thymus vulgaris Linnaeus) on flesh quality of tuna (Thunnus thynnus (Linnaeus)) during chilled storage. Pan-Am J Aquat Sci 2008;3:36e45. Szczepanik G, Stodonik L. The effect of the composition of fatty acids of baltic fishes and frozen storage process on the antioxidant activity of aqueous extracts of rosemary and sage, as well as BHA and Endox. Acta Ichthyol Piscat 2003;xxxiii:57e74. Tandon S, Rane S. Decoction and hot continuous extraction techniques. In: Handa, et al., editors. Extraction technologies for medicinal and aromatic plants. Trieste, Italy: ICS-UNIDO; 2008. p. 93e106. Taraldgis BG, Walts BM, Younthan MT, Dugan LR. A distillation method for the quantitative determination of malonaldehyde in rancid foods. J Ame Oil Chem Soc 1960;37:44. Tironi VA, Tomas MC, Anon MC. Quality loss during the frozen storage of sea salmon (Pseudopercis semifasciata) Effect of rosemary (Rosmarinus officinalis L) extract. LebensmittelWissenschaft und-Technologie (LWT), Food Sci Technol 2010;43:263e72. Zambuchini B, Fiorini D, Verdenelli MC, Orpianesi C, Ballini R. Inhibition of microbiological activity during sole (Solea solea L) chilled storage by applying ellagic and ascorbic acids. Food Sci Technol 2008;41:1733e8.
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Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs Fathy A. Khalafalla, Fatma H.M. Ali, Abdel-Rahim H.A. Hassan* Food Hygiene Department, Faculty of Veterinary Medicine, Beni-Suef University, Beni-Suef, 62512, Egypt
article info
abstract
Article history:
The present study was preformed to evaluate the effect of dip treatments by thyme
Received 6 August 2014
(Thymus vulgaris) extract (0.5%) and rosemary (Rosmarinus officinalis) extract (1.5%) on
Accepted 2 January 2015
the quality and shelf life of Nile tilapia (Orechromis niloticus) fillets during refrigerated
Available online xxx
storage at 2 ± 1 C. The control (untreated) and treated groups were examined periodically at day zero and every 3 days (0, 3, 6, 9, 12, 15, 18, ....) during refrigeration until apparent
Keywords:
decomposition of each group, with sensory, physicochemical and microbiological
Thyme
methods. The obtained results showed that thyme extract has strong antimicrobial and
Rosemary
antioxidant activity and can maintain the quality parameters and extend the shelf life of
Nile tilapia
refrigerated Nile tilapia fillets for 9 days longer than control one, while rosemary extract
Microbiological
had efficient antioxidant activity with weak antimicrobial action. Copyright 2015, Beni-Suef University. Production and hosting by Elsevier B.V. This is an open
TBA
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/
TVB-N
4.0/).
1.
Introduction
About one-third of the world's food production is lost annually as a result of microbial spoilage (Lund et al., 2000). The high levels of moisture, free amino acids and polyunsaturated fatty acids, and nutrient content, in addition to high amount of naturally present autolytic enzymes and high pH render fish an easily perishable product, often going bad within a short period under refrigerated conditions (Cakli et al., 2007). Spoilage of fish results from changes brought about by biological reactions such as oxidation of lipids, the activities of the fish muscular enzymes, and the metabolic activities of
microorganisms. Enzymatic and chemical reactions are usually responsible for the initial loss of freshness whereas microbial activity is responsible for the obvious spoilage and thereby establishes product shelf life (Arashisara et al., 2004). Increasing demand for high quality ready-to-cook fish products with extended shelf-life has initiated the development of several innovative techniques to keep quality attributes as long as possible and yield safe products (Maftoonazad and Badii, 2009). Due to modern trends consumers adopt towards the consumption of minimally processed foodstuffs containing no chemical preservatives, lightly preserved food products with natural additives have become popular. Thyme and rosemary extracts come to fulfill part of the increasing
* Corresponding author. Tel.: þ20 822327982; fax: þ20 822322066. E-mail address: [email protected] (A.-R.H.A. Hassan). Peer review under the responsibility of Beni-Suef University. http://dx.doi.org/10.1016/j.bjbas.2015.02.005 2314-8535/Copyright 2015, Beni-Suef University. Production and hosting by Elsevier B.V. This is an open access article under the CC BYNC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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demand for products with a ‘‘green image’’, being obtained exclusively from plant materials, that possess antibacterial, antioxidant, antiviral and antimycotic properties (Holley and Patel, 2005). The use of rosemary and thyme as natural preservatives in food industry has been reported previously by several studies (Cadun et al., 2008; Harpaz et al., 2003; Kostaki et al., 2009; Mahmoud et al., 2004; Marino et al., 1999; Offord et al., 1997; Szczepanik and Stodonik, 2003). Rosemary plant (Rosmarinus officinalis) contains certain compounds such as carnosol and carnosic acid, with high antioxidant activity, and others with minor activity (Offord et al., 1997). Carvacrol and thymol (extracted from thyme) are hydrophobic compounds that dissolve in the hydrophobic domain of cytoplasmic membrane. They cause increasing in the permeability to ATP that results in lethal damage to the bacterial cell (Burt, 2004). In the present study the antibacterial and antioxidant activities of thyme and rosemary extracts as natural food preservatives were evaluated by dipping for quality improvement and shelf-life extension of aerobically packaged Nile tilapia fillets during refrigerated storage by examining the sensory, physicochemical and microbiological attributes.
2.
Materials and methods
2.1.
Preparation of fish fillets
About 100 Nile tilapia (Orechromis niloticus) fish samples (of average weight ¼ 350e500 gm) were purchased from a fish market in Beni-Suef City, Egypt at the same day of harvesting. Each sample was gutted, deheaded, cleaned and filleted into two pieces of about 100 g weight for each piece. Then the samples were wrapped in sterile polyethylene bags and directly transferred to the laboratory in sterile icebox for further preparation within 2 h after purchasing.
2.2.
Thyme and rosemary extraction
The extraction of active ingredients from dry thyme (Thymus vulgaris) and rosemary (Rosmarinus officinalis) plant was done according to the technique developed by Tandon and Rane (2008). In brief; the dried plant material was size reduced with milling using hammer mill. Extraction of the plant material was carried out by immersion in absolute methanol for three days with agitation using automatic shaker. Then filtration through a piece of gauze to remove solid plant particles was done, the extract was re-filtered through filter paper to remove fine or colloidal particles from the extract. The enriched extract was concentrated by evaporation of the solvent with heating in water bath at 65 C until solid mass was obtained. Finally Drying the extract by spreading under shaded area till complete dryness, then stored in the refrigerator until using. Thyme extract was used for preparation of 0.5% (w/v) solution and rosemary extract was used for preparation of 1.5% (w/v) solution in distilled water of 4 C.
2.3.
Dipping of fish fillets into plant extracts
The samples were divided into 3 groups; the 1st was untreated control (C), while the 2nd group was dipped into rosemary extract 1.5%/10 min (R), and the 3rd was dipped into thyme extract 0.5%/15 min (T) inside a refrigerator, then the dipping solution was discarded.
2.4.
Packaging and storage
Treated fish fillets samples were labeled and aerobically packaged as triplicates inside fiber dishes, then stored at 2 ± 1 C inside the refrigerator. The treated groups were subjected to sensory, physicochemical and microbiological assessment at day zero (within 2 h after treatment) then periodically every three days until decomposition (0, 3rd, 6th, 9th, 12th, 18th … ..).
2.5.
Chemicals and reagents
TBA reagent was composed of 0.2883 g of 0.02 M 2-Thiobarbituric acid (C4H4N2O2S, Sigma Aldrich) in 100 mL of 90% glacial acetic acid (ADWIC, Egypt). 125 ug of Butylated Hydroxy Toluene (BHT) (C15H24O CN, Sigma Aldrich)/g of flesh were used to prevent autoxidation during the heating step of TBA-RS determination. Screened methyl red indicator was composed of 0.016 g methyl red and 0.083 g bromocreasol green in 100 mL ethanol for determination of TVB-N. Magnesium oxide (Mg O) was purchased from (LOBA, India) and N/10 Sulphuric acid (H2SO4) was from (ADWIC, Egypt). While peptone water was purchased from (MAST, UK), Lauryl Sulphate Tryptose broth from (HIMEDIA, India), and Standard plate count agar and Brilliant Green Bile Lactose broth from (Biolife, Italy).
2.6.
Sensory evaluation
The sensory assessment was performed using the scoring test developed by Neuman et al. (1983) (Table 1). Five panelists were used to evaluate the sensory attributes of fillets samples. The fillets samples were blind-coded by special codes; the panelists were not informed about the experimental approach. They were asked to give a score for each of colour, odour & consistency while the fillets were raw. Then the samples without salt and spices were fried using high quality sunflower oil, cooled to 50 C then served to the panelists to complete the evaluation of the sensory attributes. The
Table 1 e : The scoring table for sensory evaluation of fish fillets designed by Neuman et al. (1983).* Overall acceptability equals 20; 5 for each of (appearance, odour, texture and flavour) of fish fillets. Score* 20 18.2e19.9 15.2e18.1 11.2e15.1 7.2e11.1 4.0e7.1
Grade Excellent Very good Good Middle Poor Spoiled
Acceptability Acceptable
Limit of acceptability Unacceptable
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panelists were asked to wash their mouths with warm water between samples.
2.7.
Physicochemical analysis
2.7.1.
pH
The pH determination was done according to the method recommended by Korkeala et al. (1986). Briefly; ten grams of fish fillet was homogenized for about 2 min with an equal mass of distilled water in a food blender (Arnica Quick, China). After washing with distilled water (pH 7) at 26 C; the electrode of pH-meter (350 Jenway pH meter, UK) was introduced into the test portion and the temperature correction system was set to the temperature of the test portion. The pH was directly read from the scale on the instrument of the nearest 0.05 pH unit when constant value has been reached.
2.8.
Microbiological examination
2.8.1.
Preparation of the samples
Preparation of the fish fillets samples was carried out according to the muscle maceration technique recommended by ICMSF (1986). Ten grams of fish fillet were removed using sterile scalpel and forceps and transmitted to a sterile homogenizer flask containing 90 mL of 0.1% sterile peptone water. The contents were homogenized at 2000 r.p.m. for 2.5 min using a sterile homogenizer (MPW 302, Universal Laboratory Aid, Poland).
2.8.2.
Thiobarbituric acid-reactive substances (TBA-RS)
For determination of TBA-RS, the technique developed by Taraldgis et al. (1960) with additional modification of Pikul et al. (1983) was used. Briefly, ten grams of fillets sample were blended with 50 mL of distilled water in food blender/2 min. The mixture was quantitatively transferred to Kjeldahl flask by washing with additional 47.5 mL of distilled water. Then, 2.5 mL of 4 N Hcl solution were added to bring pH 1.5. Antioxidant (BHT) and anti pumping stones were added. Apparatus and heat flasks were assembled at the highest heat obtainable on the kjeldahl distillation apparatus. Five mL of the mixed distillate were pipetted into 50 mL glass stoppered tube and 5 mL of TBA reagent were added. The tubes were stoppered and their contents were mixed, and immersed in a boiling water bath for 35 min. A distilled water-TBA reagent (blank) was treated the same as the samples. After heating, be cooled under tap water for 10 min. A portion was transferred to a cuvette and the optical density of sample (D) was determined against the blank at a wavelength of 538 nm of the spectrophotometer. Calculation : TBAvalue ¼D7:8ðmg malondialdehydeðMDAÞ =kg fleshÞ
2.7.3.
Bacteriological techniques
Aerobic plate count (APC) at 35 C and coliforms MPN (3 tubes method) were performed according to the techniques recommended by AOAC (1990).
2.8.3. 2.7.2.
3
Aeromonas/Pseudomonas count
The technique recorded by Pireson et al. (1970) was applied. Briefly, 100 mL of homogenate was aseptically transferred to the surface of Glutamate starch phenol red agar medium (GSP, Merck Millipore, USA) and then spread by a sterile glass spreader. Inoculated plates were incubated at 25 C for 3 days. All pink colonies were counted as Pseudomonas while yellow colonies were counted as Aeromonas. Calculation: Pseudomonas count=g ¼ No: of colonies dilution factor 10 Aeromonas count=g ¼ No: of colonies dilution factor 10
2.9.
Statistical analysis
Data were subjected to analysis of variances (one wayANOVA) according to Knapp and Miller (1992) using (SPSS Statistics 17.0) software program. Data was expressed as mean values (n ¼ 3) with standard error. Differences among the mean values of the various treatments were determined by the least significant difference (LSD) test, and the significance was defined at P < 0.05.
Total volatile basic nitrogen (TVB-N)
TVB-N (mg N/100 g) was measured according to the method recommended by FAO (1986). One hundred mL of distilled water was added to 10 g of the minced fish fillet in a food blender and homogenized for two minutes. Sample was washed into distillation flask with a further 200 mL of water. Two grams magnesium oxide and two drops of antifoaming agent were added. The mixture was boiled for 10 min and distilled for exactly 25 min, using the same rate of heating, into 25 ml of 2% boric acid solution with few drops of screened methyl red indicator in a 500 ml flask. The heating was stopped and the condenser washed down with distilled water. Then, the contents of the flask were titrated with 0.1 N H2SO4 (titer) and 25 mL of 2% boric acid solution were also titrated against 0.1 N H2SO4 (blank). Calculation : Total volatile base ðmg N=100 g fleshÞ ¼ 14 ðtiter blankÞ
3.
Results and discussion
3.1.
Sensory evaluation
Sensory evaluation is the most popular way of assessing the freshness of fish. It is fast, simple, and provides immediate quality information (Reineccius, 1990). The data illustrated in Fig. 1 conclude the changes in the sensory attributes of control and treated fish fillets samples during refrigerated storage at 2 ± 1 C. The average scores of sensory attributes (overall acceptability) provided by the panelists at day zero were excellent (20 ± 0.0) for control (C) and thyme treated (T) samples, while it was very good (18.8 ± 0.06) for rosemary treated (R) samples. Low scores given to (R) group could be attributed to yellow discoloration and rosemary odour observed in fillets samples, this is in accordance with that reported by Hsieh et al. (2001). The overall acceptability for all samples
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decreased gradually with storage time until became 4.8 ± 0.61, 6.5 ± 0.28 and 5.3 ± 0.72 for C, R and T groups, to be below the lowest acceptability limit (7.2) according to the scoring table designed by Neuman et al. (1983) at 9th, 9th and 18th day of storage, respectively.
3.2.
Physicochemical analysis
3.2.1.
pH
Generally, the natural pH of live fish is just above 7.0, typically about 7.3, but this value falls markedly after death as the fish goes through rigor mortis and glycogen is converted to lactic acid. In most species, the post mortem pH is between 6.0 and 6.8. In the present study, a gradual increase in pH values with storage time from 6.2 ± 0.02, 6.2 ± 0.02 and 6.2 ± 0.01 at day zero has been observed to reach 7.16 ± 0.11, 7.23 ± 0.04 and 7.27 ± 0.01 at 9th, 9th and 18th day of refrigerated storage for C, R and T groups, respectively (Fig. 2). Similar results of pH values at day zero of chilled storage were recorded by Sallam et al. (2007) and Zambuchini et al. (2008), while Hernandez et al. (2009) reported higher pH values at day zero. Differences among the initial pH values than those reported in other studies may be due to the species, diet, and season, level of stress during the catch as well as type of muscle. pH values reported in the current study were significantly higher (p < 0.05) in C and R groups than T group. Higher pH values of the C and R groups could be attributed to the increase in volatile bases such as ammonia produced by either microbial or muscular enzymes (Li et al., 2012). As regards to the maximum acceptable limit of pH value (6.5) in fish and fish products recommended by EOS (2005), it was evident that C, R and T groups exceeded such limit at 6th, 6th and 12th day of storage, respectively, however, the samples still acceptable according to the sensory evaluation results. These results are in accor€ dance with that recorded by Ozyurt et al. (2009) that pH values above 7.1 are indicative of decomposition in fish. In this regard, Newton and Gell (1981) reported that pH value of fish
Fig. 1 e The changes in overall acceptability (total score of the sensory attributes) of control and treated fish fillets samples during refrigerated storage The error bars represent the SD of three replicates (n ¼ 3).
Fig. 2 e The changes in pH of control and treated fish fillets samples during refrigerated storage The error bars represent the SD of three replicates (n ¼ 3).
varies from 5.8 to 7.2 depending on struggling at the time of harvesting but the normal variation is 5.8e6.5.
3.2.2.
TBA-RS
TBA value is an index of lipid oxidation measuring malondialdehyde (MDA) content. MDA formed through hydroperoxides, which are the initial reaction product of polyunsaturated fatty acids with oxygen (Fernandez et al., 1997). In the current study, the initial TBA-RS values of C, R and T groups increased progressively (p < 0.05) with storage time from 0.093 ± 0.04, 0.036 ± 0.013 and 0.04 ± 0.008 at day zero until the last time of examination before spoilage, when a decline in all groups has been observed to reach 0.796 ± 0.07, 0.316 ± 0.021 and 0.313 ± 0.008 mg MDA/Kg at 9th, 9th and 18th day of refrigerated storage, respectively (Fig. 3A). That decline could be attributed to production of secondary lipid oxidation products from MDA, this phenomena was also observed by Aubourg (1993). TBA-RS values of C group were significantly higher (p < 0.05) than treated groups in each occasion of examination. Similar results of TBA-RS values at day zero of chilled storage with progressive increase with storage duration were obtained by Goulas and Kontominas (2007) and Hernandez et al. (2009), while higher initial values than obtained in this study was recorded by Selmi and Sadok (2008). The antioxidant activity of rosemary extract was previously reported by Offord et al. (1997) who mentioned that rosemary plant (Rosmarinus officinalis) contains certain compounds such as carnosol and carnosic acid, with high antioxidant activity. Moreover the antioxidant activity of thyme extract was previously mentioned by Marino et al. (1999) who reported that thyme extract is a potential natural antimicrobial and antioxidant agent, as it contains high concentrations of phenolic compounds including carvacrol, thymol, p-cymene and g-terpinene. Concerning the permissible limit of TBA value in fish and fish products (4.5 mg MDA/kg) recommended by EOS (2005); neither treated groups nor control one exceeded such limit in any occasion of examination even after showed objectionable odours and flavours; these results substantiate
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
b e n i - s u e f u n i v e r s i t y j o u r n a l o f b a s i c a n d a p p l i e d s c i e n c e s x x x ( 2 0 1 5 ) 1 e8
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Fig. 3 e The changes in Thiobarbituric acid reactive substances TBA-RS (A) and total volatile basic nitrogen TVB-N (B) of control and treated fish fillets samples during refrigerated storage The error bars represent the SD of three replicates (n ¼ 3).
the hypothesis reported by Connell (1990) who stated that TBA values of 1e2 mg MDA/kg of fish flesh are usually regarded as the limit beyond which fish will normally develop an objectionable odour and taste. The antioxidant properties of rosemary extract were previously recorded by Cadun et al. (2008); Szczepanik and Stodonik (2003); and Tironi et al. (2010), while the antioxidant properties of thyme extract were previously reported by Kostaki et al. (2009).
3.2.3.
TVB-N
The Commission of the European Community (1995) stated that TVB-N critical limits of 25, 30 and 35 mg N/100 g were established for different groups of fish species and have been proposed as an upper acceptability limit for spoilage initiation for fresh fish. Values of TVB-N in all groups are illustrated in Fig. 3B. At day zero TVB-N of C, R and T groups were 7.23 ± 0.46, 7.93 ± 0.40 and 7.00 ± 0.80 mg N/100 g. Similar results were detected by Chan-Yin et al. (2002) and Sallam et al. (2007). Higher values of TVB-N at day zero of chilled storage were reported by Goulas and Kontominas (2007) and Kilinc and Cakli (2004), while lower values were achieved by € Ozogul et al. (2004). Differences in TVB-N values than reported by others could be attributed to that TVB-N value is affected by species, catching season and region, age and sex of the fish. There was a progressive increase (p < 0.05) in TVBN values with storage duration in all groups to reach 30.56 ± 0.40, 29.86 ± 1.23 and 32.66 ± 1.23 mg N/100 g at 9th, 9th and 18th day of refrigerated storage in C, R and T groups, respectively. Such increase may be due to ammonia production in the fish flesh during storage as a result of microbial and muscular enzymes activities. TVB-N values were significantly higher (p < 0.05) in C and R groups than T group in most examination occasions (Fig. 3B), which indicating that rosemary extract has a poor effect on microbial and enzymatic activities, this hypothesis is substantiated by the high APC in control and R treated samples, this agrees with that reported by Gutierrez et al. (2008). Regarding the permissible limits of TVB-N in fish recommended by EOS (2005) and Commission of the European Community (1995), it is clear from Fig. 3B that 30 mg N/100 g approximately was
reached by C, R and T groups at 9th, 9th and 18th day of storage life, respectively.
3.3.
Microbiological examination
3.3.1.
Aerobic plate count (APC)
About one-third of the world's food production is lost annually as a result of microbial spoilage. Microbial activity is responsible for spoilage of most fresh and of several lightly preserved seafoods. Possibly, for this reason, the total number of microorgansims, named total viable counts (TVC) or aerobic plate counts (APC), have been used in mandatory seafood standards in some European Countries, Japan and USA (Lund et al., 2000). In this respect, ICMSF (1986) stated that the upper acceptability limit of total viable bacterial count in fresh fish is 7 log10 CFU/g flesh, and 6 log10 CFU/g is the maximum permissible limit of APC recommended by EOS (2005) in chilled fish. The changes in APC with storage time in all groups were concluded in Fig. 4A. The initial APC (2.3 103 ± 9.77 102, 6.9 102 ± 9.4 10 and 4 102 ± 1.5 102 CFU/g) increased progressively (p < 0.05) with storage time to final values of 2.4 107 ± 2.05 107, 8.2 106 ± 2.6 105 and 1.1 106 ± 1.7 105 CFU/g at 9th, 9th and 18th day of refrigerated storage (time of production of off odours and taste by the sensory evaluation) in C, R and T groups, respectively. Similar results were reported by Fu and Labuza (1993) and Zambuchini et al. (2008). In this regard, Fu and Labuza (1993) found that the duration of refrigerated storage (0 C) of fish had a significant (P < 0.05) effect on bacterial count, which tended to increase as the storage duration increased. Furthermore, Hernandez et al. (2009) mentioned that the initial mesophilic count in commercial-sized meagre fillets was 3.11 log10 CFU/g, which increased to reach 11.2 log10 CFU/ g, at 18th day of chilled storage. APC in T group was significantly (p < 0.05) lower than other groups in each occasion of examination which indicates the high antimicrobial activities of thyme extract. This is substantiate the hypothesis reported by Burt (2004) that carvacrol and thymol (extracted from thyme) are hydrophobic compounds that dissolve in the
Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
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b e n i - s u e f u n i v e r s i t y j o u r n a l o f b a s i c a n d a p p l i e d s c i e n c e s x x x ( 2 0 1 5 ) 1 e8
Fig. 4 e The changes in aerobic plate count APC (A) and Coliforms MPN (B) of control and treated fish fillets samples during refrigerated storage (n ¼ 3).
hydrophobic domain of cytoplasmic membrane, they increase the permeability to ATP that results in lethal damage to the bacterial cell. According to the permissible limit of APC in chilled fish (106 CFU/g) recommended by EOS (2005), it was evident from Fig. 4A that all groups exceeded such limit at the day when it became unacceptable by the sensory evaluation results. Regarding the upper acceptability limit recommended by ICMSF (1986) for total viable count in fresh fish (7 log10 CFU/g flesh), it could be observed that C group exceeded such limit at 9th day of storage, while such limit has not exceeded by treated groups until time of spoilage. € In this respect, Ozogul et al. (2004) mentioned that when the aerobic plate count reaches 106 CFU/g or mL in a food product, it is assumed to be at, or near, spoilage. Furthermore, Parallel Food Testing in the European Union (1995) stated that in a recent European study by consumers, fish was assumed “not to be in a good enough condition to be stored for long” when total plate count were 106 CFU/g. The antimicrobial activities of thyme extracts were previously reported by Fan and Chen (2001); Ismail et al. (2012); Mahmoud et al. (2004) andNzeako et al. (2006).
3.3.2.
Coliforms MPN
The initial coliforms MPN in C, R and T groups increased gradually from 4.1 10 ± 2.68 10, 2.8 10 ± 2 10 and 2.7 10 ± 1.1 10 to final values of 2.3 103 ± 2.64 102,
2.9 103 ± 8.3±102 and 1.5 103 ± 3.3 102 bacteria/g at 9th, 9th and 18th day of refrigerated storage, respectively (Fig. 4B). At zero and 3rd day of storage, there was no significant difference (p < 0.05) in coliforms MPN between groups, while at 6th day of storage, C group was significantly higher (p < 0.05) than treated groups, as well as at 9th day, C and R groups were significantly higher (p < 0.05) than T group in coliforms MPN. The inhibitory effect of thyme against coliform group of bacteria was previously reported by Harpaz et al. (2003); Hernandez et al. (2009) and Mahmoud et al. (2004). In this respect; the National Academy of Science (1985) reported that coliform group of bacteria in fish and fishery products has been considered important in microbiological analysis on account of their significance as indicator organisms for pin pointing the unhygienic conditions during catching, handling, processing and distribution ().
3.3.3.
Aeromonas and Pseudomonas counts
Aeromonas spp. are considered emerging food borne pathogens that are associated with septicemia, gastroenteritis, enterocolitis and wound infection in humans (Janda, 1991; Isonhood and Drake, 2002). While Pseudomonads are a good spoilage index in fishes and a marker for fish deterioration, furthermore they have to be the specific spoilage organism (SSO) in ice-stored tropical freshwater fish (Gram et al., 1990). In the present study, Fig. 5A and B clarifies the changes in Aeromonas and Pseudomonas counts in all groups during
Fig. 5 e The changes in Aeromonas (A) and Pseudomonas (B) counts of control and treated fish fillets samples during refrigerated storage (n ¼ 3). Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005
b e n i - s u e f u n i v e r s i t y j o u r n a l o f b a s i c a n d a p p l i e d s c i e n c e s x x x ( 2 0 1 5 ) 1 e8
refrigerated storage. The initial Aeromonas counts in C and R groups increased gradually with storage time from <102 ± 3.7 10 and <102 ± 3.5 10 CFU/g to reach final values of 3.2 102 ± 2.18 10 and 4.0 102 ± 4.8 10 CFU/g at 9th day of storage, respectively. While in T group still <102 CFU/g until 12th day of storage then increased to reach a final value of 2.1 102 ± 7.6 10 at 18th day of storage. Quiet similar results were obtained by Hernandez et al. (2009); Jay (1986); Mahmoud et al. (2004). Regarding Pseudomonas counts, it was noticed that the initial counts in C and R groups increased gradually with storage time from 1.3 102 ± 2.96 10 and 1.2 102 ± 6.4 10 CFU/g to final values of 1.5 103 ± 5.92 102 and 3.1 103 ± 2.6 102 CFU/g, respectively. In T group Pseudomonas count still <102 CFU/g until 12th day of storage then increased to a final value of 9.5 102 ± 4.8 102 CFU/g at 18th day of storage. The poor antibacterial activity of rosemary extract was previously reported by Hernandez et al. (2009) and Szczepanik and Stodonik (2003).
4.
Conclusion
From the previously mentioned data, it could be concluded that the dipping of Nile tilapia fillets into thyme extract before refrigeration can retain the quality attributes and extend the shelf life for about 9 days more than control during refrigerated storage at 2 ± 1 C. The antimicrobial and antioxidant activities of thyme extract were recorded without any adverse effect on the sensory acceptability of the treated fillets. Rosemary extract was reported to has an antioxidant activity with clear reduction in the TBA-RS value in treated fillets than control group, while it has no antimicrobial activity, so it is recommended to be used with an antimicrobial agent for extension of shelf life.
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Please cite this article in press as: Khalafalla FA, et al., Quality improvement and shelf-life extension of refrigerated Nile tilapia (Oreochromis niloticus) fillets using natural herbs, Beni-Suef University Journal of Basic and Applied Sciences (2015), http:// dx.doi.org/10.1016/j.bjbas.2015.02.005