Sensory and chemical assessment of silver pomfret(Pampus argenteus)treated with Ginkgo biloba leaf extract treatment during storage in ice

Weiqing Ln,Xu Che,Qioling Xu,Ting Wng,Ruoyun Du,Jing Xie,*,Min Hou,Hn Lei

aCollege of Food Science&Technology,Shanghai Ocean University,Shanghai 201306,China

bShanghai Engineering Research Center of Aquatic Product Processing&Preservation,Shanghai 201306,China

1.Introduction

Silver pomfret(Pampus argenteus),a species of butter fish,is one of the most economically important aquatic fish species distributed along the coast of China from the Bohai Sea to the East China and South China Seas.It is one of the most popular fish species in China and possesses high economical,nutritive,and edible value.Pomfret,rich with unsaturated fatty acids and microelements,such as selenium and magnesium,which protect against hyperlipidemia,high cholesterol,coronary atherosclerosis,and other cardiovascular diseases(Liu,Li,&Li,2002;Zhao et al.,2011).The demand of pomfret has increased during recent years,evenwith the decline of pomfret production due to over fishing and ecological changes(Yang,Li,&Yue,2006).As with most aquatic products,the influence of geography,climate,seasons,and other factors cause pomfret to spoil easily during processing and storage.

Plants have developed advanced defense mechanisms and several kinds of plant secondary metabolites which are the main source of antimicrobials and other pharmaceuticals(Cowan,1999;Li&Vederas,2009;Zhao,Davis,&Verpoorte,2005).Fan,Chi,and Zhang(2008)found that tea polyphenols dip could extend the shelf life of silver carp during storage in ice,which indicated that tea polyphenols dip is successful in either a more quickly lowered bacterial population or reduced the ability of bacteria for oxidative deamination of non-protein nitrogen fraction.Fan et al.(2009)also used 0.1%tea polyphenols on silvercarp byimpregnating treatment and stored during partial freezing.The results concluded that K value of tea polyphenols group and the control group appeared similar change trend.Ginkgo biloba is one of these endemic plants in China and its leaves have a wide distribution and rich resources.G.biloba leaves have both water-soluble and ethanol-soluble flavonoids with antioxidation effect,which making it better to act on the samples and inhibit the oxidase activity.G.biloba leaf extract(GBLE),rich with active components,such as flavonoids and terpene trilactones,is appreciated for its anti-allergic,antimicrobial,and antioxidant properties,which positively affect health(Balasundram,Sundram,&Samman,2006;Martins et al.,2011;Mendel&Youdim,2004).While GBLE has been widely used in the production of health products and functional beverages recently,its use as a natural food preservative has seldom been reported.It is this utilization of GBLE that is of great significance with high economic and social benefits.Anggo,Ma'ruf,Swastawati,and Rianingsih(2015)suggested that several natural antioxidants in GBLE mayhave an effect for slowingdown the degradation speed of fish muscle by endogenous enzymes or the growth of microorganisms during storage.The effectiveness of GBLE for inhibiting microorganism growth of seafood has not been reported previously,but other botanical preservatives had the similar results in this research(Abdollahi,Rezaei,&Farzi,2014).We evaluated the potential effects of GBLE on the quality and shelf-life of pomfret during refrigerated storage in ice,and evaluated the optimal concentration of GBLE by measuring the evaluation indexes.

2.Materials and methods

2.1.Ginkgo biloba leaf extract preparation

Ginkgo biloba leaves were obtained in October 2015 at Shanghai Ocean University.Fresh leaves without leaf stalk were washed with distilled water for 5 min and then dried at 65°C for 5-10 h until the moisture content was lower than 10%and then were ground with a high-speed disintegrating machine(Yongkang,type HC-500T2,Zhejiang,China).This powder of Ginkgo biloba leaves was then sifted through a 60 mesh sieve(bore diameter=250μm).Fifty grams of Ginkgo biloba leaf powder were extracted with 1 L ethanol solvent(60%,v/v)via ultrasonic extraction at 60°C for 40 min(Du,Xie,Wang,Che,&Lan,2015).This extract was diluted in distilled water to final concentrations of 2.5 mg/mL,5.0 mg/mL,and 10.0 mg/mL.

2.2.Sample preparation

Fresh pomfret(Pampus argenteus)samples were purchased directly from the local market(Luchao Harbor,Shanghai,China)in October 2015,with mean weights varying from 200 to 250 g and mean body lengths from 15 to 19 cm.Thirty-two fish samples,which were divided into 4 lots(about 8 samples for each group),were transported 30 min to the laboratory with ice.Untreated pomfret were represented as the control group(CK)and were washed with distilled water.Samples treated with different concentrations of GBLE(2.5 mg/mL,5.0 mg/mL,and 10.0 mg/mL)were designed as sample GBLE1,GBLE2 or GBLE3 respectively.Treated whole fish samples were dipped for 5 min in each concentration of the GBLE solution.All samples were packed in Polyethylenebag and stored in a refrigerator at 4± 1°C with ice.

2.3.Quality evaluation design

Assessments of quality(Fig.1)were determined using an array of analyses at 3-day intervals over 18 days.Each analysis was repeated three times with three fishes,with the averages of each replicate used to measure the overall quality of fish.

2.4.Physical analysis

2.4.1.L*,a*and b*values

Colour is one of the key parameters used to evaluate the quality of aquatic products and the typically essential factor for deciding the acceptance of aquatic products by consumers(Jo et al.,2014).The colour of pomfret samples were measured with a colorimeter(CR-400,Konica Minolta(China)Investment Ltd.Shanghai,China)in the reflectance mode which was calibrated with a white standard plate at room temperature.Colour was expressed in L*,a*and b*values,representing for lightness/whiteness,redness/greenness,and yellowness/blueness,respectively.

2.4.2.Texture profile analyses(TPA)

TPA were conducted by using a TA-XT2i Texture Analyzer(Stable Micro System,Surrey,UK).Texture parameters(cohesiveness and springiness)were calculated as defined by Bourne(1978).All measurements were performed at ambient temperature(12-16°C).

2.4.3.pH

pH measurement is one of the most useful methods for physical quality of aquatic products,which is influenced by the variations in the concentrations of free hydrogen and hydroxyl ions because of the shifts in food redox equilibrium by microorganism or enzyme activity(Varlik,Baygar,Özden,Erkan,&Metin,2000).It is mainly affected by free carboxyl and amino groups in low-molecular-mass compounds and cellular macromolecules,such as proteins,nucleic acids,polysaccharides(Briones-Labarca,Perez-Won,Zamarca,Aguilera-Radic,&Tabilo-Munizaga,2012;Cruz-Romero,Kelly,&Kerry,2007).pH value was measured using a digital 320 pH metre(Mettler Toledo,Zurich,Switzerland)to demonstrate the hygienic standard of fish and other aquatic products according to GB/T 5009.45-2003.

2.5.Chemical analysis

2.5.1.Total volatile basic nitrogen(TVB-N)measurement

TVB-N is an important index for evaluating the quality of fish during storage,which is due to the activity of spoilage bacteria and endogenous enzymes primarily(Dembele,Wang,Sun,&Dong,2009).According to SCT 3103-2010,the level of TVB-N in freshly caught fish usually fluctuates between 5 and 20 mg N/100 g.A level of more than 30 mg N/100 g of muscle is usually considered as spoiled(Lakshmanan,2000).TVB-N values were determined with a Kjeltec 2300(FOSS,Hiller,Denmark)and expressed in mg nitrogen per 100 g fish sample.

2.5.2.K-value

Pomfret samples were pretreated by the method described by Ginson et al.(2013).Determination of ATP-related compounds were carried out by HPLC(LC-2010C HT,Shimadzu Corporation).The individual amounts of ATP and its related compounds were determined and calculated based on ATP,ADP,AMP,IMP,HxR,and Hx standards(Fan et al.,2008).The K-value was defined as follows:

where HxR,Hx,ATP,ADP,AMP,IMP are hypoxanthine riboside,hypoxanthine,adenosine triphosphate,adenosine diphosphate,adenosine monophosphate, and inosine monophosphate,respectively.

Variation of the K-value is relevant to several factors such as kinds of fish,stress during capture,processing mode,seasons,type of muscle and preserved conditions.According to Ehira and Uchiyama(1974),who set the rejection levels of K-value as 60%and lower than 20%as very fresh,with less than 50%as moderately fresh,and higher than 70%as decayed,High content of IMP is regarded as a main flavor contributor of flesh,especially the sweetness,meat flavors and creamy flavors of fresh fish.It suggested that the IMP measurement is a sufficient freshness index since it plays a major role in desirable odor and tastable in fresh fish(Li et al.,2011;Ocaˇna-Higuera et al.,2011).

Fig.1.Quality evaluation in pomfret samples with different treatment during storage in ice.

2.5.3.Thiobarbituric acid(TBA)measurement

TBA is an indicator of lipid oxidation level for measuring malondialdehyde(MDA)content(Khalafalla,Ali,&Hassan,2015).MDA formed through hydroperoxides,which are the initial reaction products of polyunsaturated fatty acids with oxygen(Fernandez,Perez-Alvarez,&Fernandez-Lopez,1997).TBA measurement was performed as described by Buege and Aust(1978).TBA value was expressed as mg of malonaldehyde/100 g of muscle sample and obtained by using as follows:

2.6.Microbiological analysis

Determination of the total viable count(TVC)in a food product is one of the simplest and widely used microbiological techniques.It was regarded that a quality criterion corresponding to 106CFU/g for TVC should be considered to discriminate between unspoiled and spoiled samples in this research,because 106CFU/g is the general microbiological safety guideline applied in food quality(Barbri et al.,2009).According to GB 47892-2010,25 g fish samples were transferred to a stomacher bag and 225 mL of 0.1%peptone water with salt(NaCl,0.85%,w/v)were added and homogenized for 60 s with a stomacher.Other decimal dilutions were obtained from this dilution and 1 mL of three dilutions was transferred in triplicate to Petri dishes containing 15 mL commercial plate count agar(Land-Bridge Technology Co.,Ltd,Beijing,China).TVC were determined by counting the number of colony-forming units after incubation at 30°C for 72 h(Li,Li,Hu,&Li,2013).

2.7.Amino acid analyses

Amino acid determinations were carried out by HPLC(waters corporation,USA).Amino acid standard solution used for calibration from Waters Atlantis T3 C18 AccqTag column(4.6×250 mm,5μm),mobile phase A was methanol solution,mobile phase B was 0.05 mol/L dipotassium hydrogen phosphate and potassium dihydrogen phosphate solution(1:1),including 9 mmol/L tetrabutylammonium hydroxide solution(pH=6.5).The flow rate was 0.9 mL/min with fluorescence detector.Injection volume for each sample was 20μL(Anggo et al.,2015).Je,Park,Jung,and Kim(2005)reported that glycine,lysine and alanine may also be responsible for the taste of pomfret.Other amino acids,such as lysine,arginine and tyrosine,are of great importance because they can be transformed into cadaverine,putrescine and tyramine,respectively(Ruiz-Capillas&Jim'enez-Colmenero,2005;Zaman,Abu Bakar,Jinap,&Bakar,2011).A downward trend in the contents of free amino acid may be due to the reason for the degradation to amines,volatile acids,and other nitrogenous matter as by-products of enzymatic degradation or bacterial metabolism(Ezzat,Zare,Karim,&Ghazali,2015).The operating column temperature was at 27°C and the absorbance was measured at 254 nm.

2.8.Electronic nose analyses

The volatile components in the headspace of the samples were measured using a sensor array system-electronic nose(Alpha M.O.S.,FOX4000.France).Two grams of minced pomfret flesh were put into 10 mL glass vials,which were sealed with a PTFE/silicone septum and a screw cap(Limbo,Sinelli,Torri,&Riva,2009).A calibration of the equipment was performed every two weeks to address possible sensor drift.Principle component analysis(PCA)of e-nose data generated by the sensors(Cozzolino,Cynkar,Dambergs,&Smith,2010;Tang et al.,2013)was used to discriminate between fresh and spoiled samples by using the XLSTAT software(Version 2012.2.01).PCA has been widely used to analyze the datum by electronic nose,it can reduce the dimensionality of original data and thus simplify the analysis without loss of original data(Kim,Kim,&Bang,2003;Zhao&Jiang,2006).

2.9.Statistical analysis

Data are expressed as mean values(n=3)accompanied by standard deviation.Analyses were performed with SPSS software(Version 13.0)(SPSS,Chicago,IL,USA)to detect significant differences between lots and periods of cold storage.One-way analysis of variance was used,the Tukey multiple comparison test was used to find the significant differences between lots.Significance level was set at 0.05.The figures are drawn by Origin software(Version Pro V8.5).

3.Results

3.1.L*,a*and b*

Samples treated by GBLE were remarkably bright in appearance compared to that of the control and samples with GBLE2 had higher L*in particular(Table 1).The average a*from all treated samples was not significantly different during the storage period.However,a comparatively large fluctuation of a*was shown(P＞0.05),It also indicated that b*of treated group was different from untreated one(P≥0.05).The b*of treated groups had the obvious rise from day 0 to day 3,This rise abated in weeks 6-9,before resuming again,while the GBLE1 treatment group maintained lower b*than that in samples of other groups from day 3(Table 2).

3.2.Texture profile analyses(TPA)

Springiness is an important indicator for the freshness of samples and the proportion of water content under certain conditions.As shown in Fig.2,springiness showed similar trends in each treatment group,but the springiness of the controlled group declined sharply after day 6 and was always lower than the treatment groups.The cohesiveness of CK group decreased drastically,especially from day 9 to day 12,compared to the steady decline exhibited by the treatment groups.

The results indicated that GBLE had an effect on springiness and cohesiveness with higher values.

3.3.pH and TVB-N

The initial pH of the fish samples was 7.07±0.01 and 7.80 at day 8,The pH of all treated group samples were lower than that of the control during storage,In the first 9 days of storage,the pH rose obviously.

The changes in TVB-N on pomfret during storage in ice were shown in Fig.3.The increase speed of TVB-N values in pomfret for GBLE treatment was lower than control samples were 10 mg N/100 g and showed obvious rising trend after 9th day.TVB-N of group CK was significantly higher than group GBLE1.

Likewise,microbial growth of pomfret samples were actively suppressed by GBLE and TVB-N values with storage duration in all groups reached 21.54±0.06,25.97±2.05,24.92±1.30 and 29.94±5.34 mg N/100 g at 9th,15th,12th,and 12th day of iced storage in CK,GBLE1,GBLE2,and GBLE3 groups respectively.The results showed that the level of TVB-N value in treated samples was lower than the control samples apparently and it could be a good indicator for quality evaluation of pomfret.

3.4.K-value

From Fig.4,the results show that values of HxR were found to be increased significantly(P＜0.05)during storage.Hx is concerned as an enhancer to off- flavors,which is used as an index of fish freshness.The pomfret was very fresh in initial storage and K-value was 9.86%.K-values in the untreated group increased continuously with storage time and reached 68.77%on the last day during ice storage.Treated groups showed the same trend as the control group,but with lower K-values during storage.GBLE1 had the lowest K-value(43.13%)on the 18th day.However,K-values in treated samples were lower than that of the control,which is consistent with the results of Fan et al.(2009).It also indicated that GBLE was efficient in inhibiting the degradation of ATP,maintaining the quality and prolonging the shelf life of samples.

3.5.TBA

The initial TBA values increased progressively during storage time from 0.195±0.041 mg/100 g at the first day and reached 0.605±0.116,0.460±0.066,0.523±0.022,and 0.601±0.011 mg/100 g through the 18th day,respectively(Fig.5).However,it showed a decline at 3rd day,TBA values of control group were generally higher than treated groups,especially the GBLE1 group.The results revealed that GBLE treated samples can extend the shelf life of pomfret by suppressing the lipid oxidation in fish.

3.6.Microbiological analyses

Total viable count(TVC)is an important indicator for quality assessment.The results of the bacterial analysis performed on the pomfret samples are presented in Fig.6.The initial TVC level was found to be 3.98 log10CFU/g.TVC showed a slight variation in the first 3 days,followed by a relevantly fast increase between day 3 and 9,and the curves showed a tendency to be stabilized during the last days of conservation finally.It was evident from Fig.6 that control group exceeded such limit between day 12 and day 15 when it became unacceptable by sensory evaluation results,while such limit has not exceeded by GBLE1 and GBLE2 groups until spoilage time.

TVC in treatment group was lower than control group which indicates the high antimicrobial activities of GBLE.

3.7.Composition and content of amino acid

It found that the major amino acids in marine fish were aspartate,glutamic acid,alanine,leucine,isoleucine,valine and lysine(Rabie,Simon-Sarkadi,Siliha,El-Seedy,&El Badawy,2009),while glutamic acid which is the critical role for umami taste in fish products(Peralta et al.,2008).

Table 1 Change of the colour in untreated and treated Pomfret samples during storage in ice.

Table 2 Amino acids content in each group during storage in ice(mg/g).

Fig.2.Changes of Cohesiveness and Springiness in pomfret samples with different GBLE treatment during storage in ice.Vertical error bars represent standard error of data from three replicate trials.

Fig.3.Changes of pH and TVB-N in pomfret samples with different GBLE treatment during storage in ice.Vertical error bars represent standard error of data from three replicate trials.

3.8.Electronic nose analysis

Fig.7 showed the plots of first and second principle components(PC1,PC2)of data derived from 18 sensors of electronic nose in control group and GBLE treated groups during ice storage.

The first two components,PC1 and PC2,captured 97.94%,98.07%,97.90%and 97.88%of data variance,with PC1 accounted 88.09%,90.37%,91.63%,99.43%at different groups and the discrimination indexes were 92,73,78,73 respectively.

4.Discussion

4.1.Colour analyses

The bright appearance of GBLE treated pomfret is caused by denaturation of myofibrillar and sarcoplasmic proteins(Jain,Pathare,&Manikantan,2007).A large fluctuation of a*value may be due to the change of heme displacement or release and indicate the change of a*value.The results may be due to the diluted GBLE,which is rich with flavonoids,had an influence on pomfret and resulted in the increase of yellow colour.

4.2.TPA analyses

Cohesiveness could reflect the magnitude of intercellular binding force.The result showed that GBLE could prevent water loss in samples and maintain its springiness during storage in ice,the quality of pomfret can be well kept during storage when treated with GBLE.Quality degeneration and bacterial reproduction would lead to the decline of cohesiveness and the decrease of intercellular binding force.It can be concluded that GBLE could maintain good quality and restrain bacterial growth from the change of cohesiveness.The pomfret death caused autolysis and then the muscle became softer and loss of elasticity,while the process could be accelerated by microbial activity(Olafsdottir et al.,2004).

Fig.4.Changes of K-value in pomfret skin and flesh with different GBLE treatment during storage in ice.Vertical error bars represent standard error of data from three replicate trials.

Fig.5.Changes of TBA in pomfret samples with different GBLE treatment during storage in ice.Vertical error bars represent standard error of data from three replicate trials.

Fig.6.Changes of TVC in pomfret samples with different GBLE treatment during storage in ice.Vertical error bars represent standard error of data from three replicate trials.

4.3.pH

The change of pH value may be caused by the growth of spoilage organisms leading to the accumulation of alkaline components such as ammonia and trimethylamine.which is consistent with the antimicrobial characteristics of GBLE,which is rich with flavonoids and can inhibit the growth of bacteria.The earlier research reported by Gould and Peters(1971)and Abbas,Mokhtar,Sapuan,and Mawlood(2005)found that the increase in pH during seafood storage is result from depletion of the tissues.The trends of pH value are together with the loss of texture due to depletion in the tissue of samples,which could be deteriorated finally(Jain et al.,2007).

4.4.TVB-N

This trivial decrease in initial time may be caused by the degradation of glycogen and the generation of free amino acids(Hong,Luo,Zhou,Bao,&Shen,2013),while the apparent increase in TVB-N during later period is more possibly initiated by microbial associations,autolytic activities and the complete microbial reduction of trimethylamino oxide to tetramethylammonium(Sallam,Ahmed,Elgazzar,&Eldaly,2007).Bacterial catabolism of amino acids in fish muscle leads to the accumulation of trimethylamine,dimethylamine,monoethylamine,ammonia and other volatile bases,which accompanied by increased curvilinearly or linearly as corruption progresses and produces peculiar smell to fish(Goulas&Kontominas,2007;Li et al.,2013).

4.5.K-value

Autolytic changes happen in fish muscle after death and before microbial spoilage begin which result in the generation of diverse compounds and are usually considered as an effective indicator of fish freshness.The concentrations of adenosine triphosphate(ATP)and its degradation products are most widely used to reflect freshness and shelf-life of aquatic products(Li et al.,2011;Mohan,Ravishankar,Srinivasa Gopal,&Ashok Kumar,2009;Ocană-Higuera et al.,2011).The lower K-value in treatment samples were considered as the result from decomposition of inosine monophosphate(IMP),as the outcome of 5-nucleotidase activity(Li et al.,2013).Therefore,the relatively lower K-value could be explained by the effect of GBLE to minimize the activity of 5-nucleotidase and slower the degradation of ATP(Fan et al.,2009).

4.6.TBA

The changes of TBA value could be attributed to the generation of secondary lipid oxidation products from MDA.Similar result was also found by Aubourg(1993).The continuous increase in TBA value during ice storage could be ascribed to the partial dehydration of pomfret,the denaturation of fish muscle and the accumulated oxidation of unsaturated fatty acids.

Fig.7.PCA in pomfret samples with different treatment during storage in ice.

4.7.Microbiological analyses

GBLE is a potentially natural antimicrobial and antioxidant agent,as it contains high concentrations of ginkgetin,isoginkgetin,bilobetin,isorhamnrtin and ginkgolic acid.(Fan et al.,2008).The result of TVC is in accordance with the result by Burt(2004)who found carvacrol and thymol(extracted from thyme)are hydrophobic compounds that dissolve in the hydrophobic domain of cytoplasmic membrane,results in lethal damage to the bacterial cell.Ozogul et al.(2010)also reported that rosemary extract could improve the shelf life of sardine fillets by decreasing TVC for 7 days.

4.8.Content of amino acid and electronic nose analysis

It indicated that there was an obvious separation between the samples from different groups during storage.The conclusion of amino acid contents of pomfret samples indicated that pomfret treated with GBLE can be more fresh than untreated samples.Therefore the change occurred from day 9 to day 12 of control group,a little change occurred from day 12 to day 15 and a big change from day 15 to day 18 of other three GBLE groups in the production of volatile components.In particular,samples were distributed along PC1 according to different groups and storage time(Tang et al.,2013).From the amino acid composition analyze,it was found that the trend of taste amino acid content in three GBLE treatment groups changed in day 12,from no distinct tendency to rising slowly and being stable finally.However,in the control group,the amino acid content had a steep rise from day 9 and kept increasing.The analysis of amino acid composition and electronic nose were in accordance with sensory evaluation.The results showed that different GBLE had an obvious influence on the flavor of pomfret.

5.Conclusions

Varying concentrations of GBLE often enhanced the longevity of pomfret quality during cold storage.GBLE treatment inhibited lipid oxidation,protein degradation and microorganism growth effectively,which also kept the parameters of texture and the sensory characteristics within acceptable limits during ice storage and extended the shelf-life of pomfret.The samples with GBLE1(2.5 mg/mL GBLE)prolonged the shelf-life of pomfret from 8 to 15 d and was the best for the preservation of pomfret during storage in ice.

Conflict of interest statement

We declare that we have no conflict of interest.

Acknowledgement

The study was financially supported by China Agriculture Research System(CARS-47),Shanghai promote agriculture by applying scientific&technological advances projects(2015No.4-12),Ability promotion project of Shanghai Municipal Science and Technology Commission Engineering Center(16DZ2280300);Shanghai Professional Technology Service Platform on Cold Chain Equipment Performance and Energy Saving Evaluation(17DZ2293400).

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