International Journal of Food Science and Technology 2009, 44, 2021–2027
Original article Natural compounds to preserve fresh fish burgers Maria Rosaria Corbo,1,2 Barbara Speranza,1 Alfonso Filippone,1 Amalia Conte,1 Milena Sinigaglia,1,2 & Matteo Alessandro Del Nobile1,2* 1 Department of Food Science, University of Foggia, Via Napoli, 25 – 71100 Foggia, Italy 2 Istituto per la Ricerca e le Applicazioni Biotecnologiche per la Sicurezza e la Valorizzazione dei Prodotti Tipici e di Qualita`, Universita` degli Studi di Foggia, Via Napoli, 25 – 71100 Foggia, Italy (Received 16 March 2009; Accepted in revised form 21 May 2009)
Summary
Natural antimicrobial compounds to control the quality decay of a fresh fish burger were studied. In particular, thymol, lemon extract and grape fruit seed extract (GFSE), at 20, 40 and 80 ppm, have been tested against the main spoilage microorganisms inoculated in fish burgers stored at 5 C. The evolution of mesophilic and psychrotrophic bacteria was also monitored. The sensorial quality decay was determined by means of a panel test, which assessed odour, colour, texture, drip loss and general appearance during the storage period. Results show that all the active substances efficiently slowed down the growth of the spoilage microorganisms. In particular, GFSE was the most efficient against Photobacterium phosphoreum, Shewanella putrefaciens and mesophilic bacteria, whereas thymol was the most efficient against both psychrotrophic bacteria and Pseudomonas fluorescens. Microbial growth was the factor limiting fresh fish burger acceptability.
Keywords
Fish, grape fruit seed extract, lemon extract, shelf life, thymol.
Introduction
Fresh fish is a highly perishable product due to its biological composition. The loss of essentially fatty acids, fat-soluble vitamins and protein functionality, added to the production of potentially toxic reaction products, as biogenic amines, is the main results of the detrimental phenomena. The derived peptides and free amino acids represent a suitable substrate for microbial growth (Gram & Dalgaard, 2002). Moreover, microbial activity compromises the sensorial acceptability of packed and unpacked fresh fish due to the development of bacterial metabolites that produce off-odours and offflavour (Gram & Dalgaard, 2002). Besides the short shelf life, another barrier to fresh fish consumption is represented by the consideration of seafood product as a time-consuming meal. A strategic solution to promote the distribution of a product more suitable to the modern consumer demand could be represented by ready-to-cook fish products (Trondsen et al., 2003). The use of low temperature for fish storing cannot always prevent the quality loss because of some alter*Correspondent: Fax: +39 881 589 242; e-mail:
[email protected]
ations occurring also under chilled conditions (Gram & Dalgaard, 2002). Bio-preservation by bifidobacteria has been suggested to preserve the quality of fresh fish without affecting consumer safety (Altieri et al., 2005; Kim & Hearnsberger, 1995; Kim et al., 1995a). Vacuum packaging and modified atmosphere conditions are also reported to be effective in maintaining the hygienic, sanitary and sensory characteristics of perishable foods (Sivertsvik et al., 2002; Corbo et al., 2005). Due to increasing consumer demand for fresh and additive-free products, food science researches report a renewed interest in natural preservatives, as alternatives to synthetic compounds. A group of interesting active agents for food industry is represented by extracts from fruit and vegetables, as being unexplored, abundant and cheap sources of natural compounds (Tripathi & Dubey, 2004; Tulp & Bohlin, 2004). Plant origin extracts exert a very pronounced antimicrobial activity, even if their complexity and variability make it difficult to correlate their action to a specific component (Belletti et al., 2004; Conte et al., 2007b; c). Their antimicrobial activity is greatly due to the presence of high content of phenol derivatives and there is evidence that also minor components play a significant role in the whole antimicrobial effect (Lambert et al., 2001; Falcone et al., 2005). These natural preservatives are potentially able
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to extend the shelf life of food when used alone or in combination with other preservation techniques (Conte et al., 2007a). However, their applicability in foods remains little studied due to both the intrinsic properties of the food matrix and the storage conditions influencing bacterial sensitivity (Lo`pez-Malo et al., 2000; Nychas & Tassou, 2000). Mejlholm & Dalgaard (2002) found that oregano oil at 0.5 ll g)1 was effective against the spoilage organism Photobacterium phosphoreum on cod fillets. The spreading of natural oils on the surface of whole fish or using oils in a coating for shrimps appeared effective in inhibiting the respective natural spoilage flora (Ouattara et al., 2001; Harpaz et al., 2003). In this work a preliminary study aimed to assess the effectiveness of thymol, lemon extract and grape fruit seed extract (GFSE) in slowing down the microbial quality decay of refrigerated packaged fish burger is presented. In particular, their antimicrobial activity at 20, 40 and 80 ppm has been tested against the main spoilage microorganisms inoculated in fresh fish burger as well as on mesophilic and psychrotrophic bacteria. Odour, colour, texture, drip loss and general appearance were also monitored during storage to determine the sensorial quality decay kinetic of this new food product. Materials and methods
Raw material
Gilthead sea bream (Sparus auratus) from the Adriatic Sea was used as model food to test the effectiveness of antimicrobial compounds against the main fish spoilage microorganisms. Fish was purchased from Maricoltura Mattinatese (Mattinata, Foggia, Italy). Two months prior each experiment, gilthead were starved until catch; 300–400 g fishes were slaughtered by immersing in icecold water and kept in ice for less than 2 h until they were decapitated, cleaned and filleted. Strains and antimicrobial compounds
The three bacteria used as test organisms were P. fluorescens DSM50090, P. phosphoreum DSM15556 and S. putrefaciens DSM6067. All the strains were purchased from public collection and stocked at 4 C on slants of appropriate media as recommended by the producer (http://www.dsmz.de). Prior to use, stock cultures of all tested bacteria were left to grow in Nutrient Broth (Oxoid, Milan, Italy) at their optimal temperatures: 25 C for P. fluorescens and S. Putrefaciens and 10 C for P. phosphoreum. After 48 h, a cocktail of the three strains was prepared by mixing 5 mL of each exponentially growing culture. Inoculum for experiments was prepared by centrifugation of the obtained culture in an ALC 4239R centrifuge at 1300 g for 15 min at 4 C. The
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pellet was re-suspended in 15 mL of sterile physiological solution (0.85% NaCl) temperated at 4 C and the resulting cell suspension solution (9 log CFU mL)1 for each microorganism) was used as inoculum after opportune serial dilutions to reach 5 log CFU mL)1. The effects of three natural origin antimicrobial compounds, thymol (Sigma, Poole, UK), GFSE (Biocitro, Probena s.l, Zaragoza, Spain) and lemon extract (Spencer Food Industrial, Amsterdam, The Netherlands), tested in three concentrations (20, 40 and 80 ppm), were studied. For each compound, working active solutions of 500, 1000 and 2000 ppm were prepared; these concentrations were necessary to enable greater subsequent dilution of samples. To enhance its water solubility, thymol was dissolved in ethyl alcohol (95%) and then diluted with distilled water (50%, v ⁄ v), while GFSE and lemon extract, readily soluble in water, were dissolved in distilled water. All stock solutions were freshly prepared before use and sterilised by filtering through membranes (0.20 lm pore size; Minisart, Sartorius, Goettingen, Germany). Mini-burgers manufacture
Skin-off fillets were minced by a food processor (Multichef, Ariete, Firenze, Italy). The obtained minced fish was homogenised in a bowl mixer with a spiral dough hook during 5 min. For each treatment, an aliquot (40 mL kg)1) of the selected stock solution was added to obtain final concentrations of 20, 40 and 80 ppm, and then mixed again for 5 min. Mini-burgers were prepared by hand (25 g, 50–60 mm diameter) and the inoculum (about 3 log CFU mL)1) was performed in all of treated samples by spreading 0.1 mL of the prepared microbial cocktail. As control samples, burgers containing the same amount of distilled water (CONTROL) and samples containing 50% hydro-alcoholic solution (CONTROL ETHANOL) were also prepared and inoculated. The mini-burgers were packed in high-barrier plastic bags [Nylon ⁄ Polyethylene, 102 lm (Tecnovac, San Paolo D’Argon, Bergamo, Italy)] by means of S100Tecnovac equipment. The bags were 170 · 250 mm long with properties specified by the manufacturer as follows: CO2 and O2 permeability of 3.26 · 10)19 mol m m)2 s)1 Pa)1 and 9.23 · 10)19 mol m m)2 s)1 Pa)1, respectively, and water vapour transmission rate of 1.62 · 10)10 kg m)2 s)1. The samples were packaged in air and stored at 5 C. Microbiological analyses and determination of pH were made after 0, 1, 2, 3, 6, 8, 10 and 14 days, details of which are given below. Microbiological analyses
For microbiological analyses, mini-burgers (25 g) were diluted with 225 mL of 0.1% peptone water with salt (0.85% NaCl) in a Stomacher bag (Seward, London,
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UK) and homogenised for 1 min in a Stomacher Lab Blender 400 (Seward). Serial dilutions of fish homogenates were plated on the surface of the appropriate media in Petri dishes. The media and the conditions used were: plate count agar (PCA) incubated at 5 C for a week or 32 C for 48 h for psychrotrophic bacteria and total bacterial count, respectively; pseudomonas agar base (PAB), added with CFC Selective Supplement, incubated at 25 C for 48 h for P. fluorescens; spread plated chilled Iron Agar (IA), supplemented with 5 g L)1 NaCl, incubated at 10 C for 7 days for P. phosphoreum (luminous colonies were counted in a dark room); IA incubated at 25 C for three days for S. putrefaciens. All media were from Oxoid. The measurement of pH was performed on the first homogenised dilution of the fish samples during storage with a Crison pH meter model micro pH 2001 (Crison, Barcelona, Spain). Sensory evaluation
Samples were given three-digit codes and assessed by a five-member panel (researchers of the Department of Food Science, Faculty of Agricultural Science, University of Foggia) for colour, odour, texture, drip loss and general appearance on a five-point hedonic scale, on which a score of five represented attributed most liked; two represented attributes at an unacceptable border; and zero represented attributes most disliked (Altieri et al., 2005). Statistical analysis
All analyses were carried out in duplicate on two different batches. The average values and standard deviation were calculated. In fact, the data shown in the figures are the average of all repetitions, whereas the error bars are the standard deviation. The experimental data were elaborated as reported in the results and discussion section. The microbiological acceptability limit (MAL) values were submitted to one-way anova and Duncan’s test (P < 0.05) through the statistical package statistica 7.1 for Windows (Statsoft, Tulsa, OK, USA). Results and discussion
As reported above, the quality of packed fresh fish burger depends on several quality sub-indices, among which microbial and sensorial quality are the most important. The microbial quality decay of the developed fresh fish burger was determined by monitoring the viable cell concentration of S. putrefaciens, P. phosphoreum, P. fluorescens, mesophilic and psychrotrophic bacteria. The following sensorial attributes were also determined: odour, colour, texture, drip-loss and general appearance.
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Figure 1 Shewanella putrefaciens viable cell concentration in packaged fish burgers with 20, 40, and 80 ppm of thymol. The curves were obtained by fitting the eqn 1 to experimental data.
S. putrefaciens
As an example, Fig. 1 shows the evolution during storage at 5 C of S. putrefaciens viable cell concentration in fresh fish burger loaded with thymol at three different concentrations: 20, 40 and 80 ppm. The curves shown in the above figure were obtained by fitting the Gompertz equation as modified by Zwietering et al. (1990) to the experimental data: logðNðtÞÞ ¼ logðN0 Þ k A exp exp ðlmax 2:71Þ þ1 A kt þ A exp exp ðlmax 2:71Þ þ1 A
ð1Þ
where N(t) is the viable cell concentration (CFU g)1) at time t, N0 is the initial value of cell concentration (CFU g)1), A is related to the difference between the decimal logarithm of the initial value of cell concentration and the decimal logarithm of maximum bacteria growth attained at the stationary phase (CFU g)1), lmax is the maximal specific growth rate (Dlog[CFU g)1] ⁄ day), k is the lag time (day) and t is the time (day). As can be inferred from data shown in the above figure, eqn 1 satisfactorily describes the trend of experimental data. Analogous results were also obtained in the case of lemon extract and GFSE loaded samples. To quantitatively determine the effectiveness of the investigated antimicrobial compounds in slowing down the growth of the selected spoilage microorganisms, the time at which the viable cell concentration reached its acceptability limit was calculated according the to Gompertz equation, as re-parameterised by Corbo et al. (2006):
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logðNðtÞÞ ¼ logðNmax Þ k MAL þ1 A exp exp ðlmax 2:71Þ A kt þ A exp exp ðlmax 2:71Þ þ1 ð2Þ A where Nmax is the threshold value for the viable cell concentration (CFU g)1), and MAL is the microbiological acceptability limit (day) (i.e. the time at which log(N(t)) is equal to log(Nmax). The above expression has also been fitted to the experimental data. In particular, the fitting was run by setting the values of A, lmax and k as calculated in the previous step and using MAL as the sole new fitting parameter. Results on MAL values are reported in Table 1. In the specific case of S. putrefaciens the value of Nmax was set to 106 CFU g)1. As reported by Koutsoumanis & Nychas (2000), this cell concentration provokes the shelf life ending because it is strictly linked to the loss of sensory quality of fish. As can be seen in Table 1, at lowest antimicrobial compound concentration the MAL values do not differ, to a great extent, from the control samples. On the other hand, at medium and high thymol concentration an increase in the acceptability limit was detected. To highlight the differences in the efficacy of the investigated natural preservatives, Fig. 2 shows MAL values plotted as a function of the compound concentration. The curves shown in Fig. 2 were obtained by fitting an exponential function to the experimental data with the sole aim of highlighting their trend. As can be observed, thymol and lemon extract loaded samples show a similar trend: both of them have a down ward concavity, lemon extract being slightly more effective than thymol. On the other hand, GFSE shows an upward concavity. The maximum
MAL (day) Control Control ethanol GFSE (ppm) 20 40 80 Thymol (ppm) 20 40 80 Lemon (ppm) 20 40 80
Figure 2 MAL values obtained for S. putrefaciens plotted as a function
of antimicrobial compound concentration. The curves were obtained by fitting an exponential function to experimental data.
MAL value among the investigated antimicrobial compounds was detected with fish burger containing the highest GFSE concentration. P. phosphoreum
The evolution during storage at 5 C of P. phosphoreum viable cell concentration in fresh fish burgers loaded with the different active agents was similar to that shown in Fig. 1 for S. putrefaciens. As above, eqns 1 and 2 were fitted to the experimental data following the same fitting procedure. The value of Nmax for P. phosphoreum was set to 107 CFU g)1 as suggested by Dalgaard (1995), because it corresponds to cell load able to produce 30 mg-N-TMA 100 g)1 found in spoiled packed fish. The MAL values are also reported in Table 1. At the lowest compound concentration the loaded samples do not differ substantially from the control ones; whereas, Table 1 MAL values (mean ± SD) calculated for all microbial groups
Shewanella putrefaciens
Photobacterium phosphoreum
Total mesophilic bacteria
Total psychrotrophic bacteria
Pseudomonas fluorescens
2.02 ± 0.02A 1.93 ± 0.04B
2.77 ± 0.02A 2.68 ± 0.05A
2.60 ± 0.04A 2.62 ± 0.03A
2.75 ± 0.04C 2.36 ± 0.02D
2.01 ± 0.03A 1.84 ± 0.03C
1.92 ± 0.04B 2.04 ± 0.03A 2.83 ± 0.03C
2.68 ± 0.02A 2.90 ± 0.06B 4.42 ± 0.06G
2.87 ± 0.03A 3.01 ± 0.03B 3.24 ± 0.04E
2.87 ± 0.03A 3.01 ± 0.03B 3.24 ± 0.04E
1.80 ± 0.02C 2.00 ± 0.04A 2.48 ± 0.04F
2.09 ± 0.04A 2.26 ± 0.03D 2.45 ± 0.05E
4.03 ± 0.10F 3.16 ± 0.06D 3.77 ± 0.04C
2.93 ± 0.03C 3.40 ± 0.05E 3.26 ± 0.07B
3.15 ± 0.05E 3.81 ± 0.05G 4.70 ± 0.05H
2.07 ± 0.05A,B 2.19 ± 0.03E 2.64 ± 0.10D
2.21 ± 0.02D 2.45 ± 0.05E 2.49 ± 0.04E
2.88 ± 0.04B 3.67 ± 0.06E 3.79 ± 0.04C
2.92 ± 0.03C 3.26 ± 0.06B 3.25 ± 0.01B
3.00 ± 0.06B 2.92 ± 0.03A 3.62 ± 0.01F
2.07 ± 0.02A,B 2.12 ± 0.03B 2.63 ± 0.02D
Data in column with different superscript letters are significantly different (P < 0.05).
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at the middle and the highest concentration there are statistically significant differences between the MAL values of loaded and unloaded burgers. MAL calculated for burgers with thymol do not seem to depend to a great extent on the active compound concentration, the contrary is true for the other two compounds. In fact, the MAL increases with the concentration of either GFSE or lemon extract. By plotting MAL values as a function of the active agent, results similar to those obtained for S. putrefaciens are recorded for both samples with lemon extract and GFSE (data not shown). In particular, samples containing lemon extract show a downward concavity, whereas samples loaded with GFSE shows an upward concavity. Also in this case, the maximum MAL was detected for sample loaded with GFSE at 80 ppm. Mesophilic and psychrotrophic bacteria
The evolutions during storage of viable cell concentration of mesophilic and psychrotrophic bacteria in refrigerated fresh fish products were similar to those shown in Fig. 1 for S. putrefaciens. Also in this case eqns 1 and 2 were fitted to the experimental data following the same fitting procedure; results are also listed in Table 1. The value of Nmax for both microbial groups was set to 5 · 106 CFU g)1 (Altieri et al., 2005). Results obtained for mesophilic bacteria are similar to those obtained for the two above-discussed microorganisms. On the contrary, thymol seems to be the most effective compound in slowing down the growth of psychrotrophic bacteria, whereas GFSE appears the less effective. P. fluorescens
The evolution of P. fluorescens in the developed new fresh fish burger was similar to that shown in Fig. 1. Equations 1 and 2 were fitted to experimental data following the same fitting procedure and results are listed in Table 1. The value of Nmax for P. fluorescens was set to 106 CFU g)1 (Bishop & White, 1986). Figure 3 shows the MAL values plotted as a function
Figure 3 MAL values obtained for P. fluorescens plotted as a function of antimicrobial compound concentration. The curves were obtained by fitting an exponential function to experimental data.
of the active compound concentration. Also in this case there is a steady increase in the MAL value with the compound concentration. The MAL values do not change, to a great extent, with the type of active compound, even when the differences among the three substances are statistically significant. Table 2 shows the percentage MAL increase of packaged new fresh fish burgers, compared to control sample and calculated according to the following expression: MALA MALC 100 ð3Þ DMAL% ¼ MALC where DMAL% is the percentage MAL increase, MALA is the MAL value of the fresh fish burger loaded with the active compounds, MALC is the MAL value of the control sample. As can be inferred from the Table 2, DMAL% depends on the antimicrobial compound, on its concentration, and on the microorganism specie. In fact, DMAL% ranges between 0% and 70%. It is worth noting that among the antimicrobial compounds investigated in this work, GFSE was the most efficient against P. phosphoreum, S. putrefaciens, and mesophilic bacteria, whereas thymol was the most efficient against both
Table 2 Percentage MAL increase (DMAL%) of fresh fish burgers formulated with the three active compounds GFSE (ppm)
Ph. phosphoreum Sh. putrefaciens Mesophilic bacteria Psychrotrophic bacteria P. fluorescens
Thymol (ppm)
Lemon Extract (ppm)
20
40
80
20
40
80
20
40
80
No increase No increase 0.25 ± 1.50
4.54 ± 2.74 0.96 ± 2.26 5.20 ± 2.20
59.41 ± 2.87 40.46 ± 2.11 42.78 ± 3.21
45.55 ± 4.35 3.37 ± 1.58 12.54 ± 2.76
13.90 ± 2.85 12.24 ± 2.31 30.75 ± 2.85
36.00 ± 2.31 21.23 ± 2.65 25.35 ± 2.80
3.79 ± 1.84 9.37 ± 1.25 12.35 ± 2.10
32.59 ± 2.74 21.56 ± 3.32 25.43 ± 1.95
36.75 ± 2.11 23.65 ± 3.00 24.99 ± 2.22
4.43 ± 2.24
9.64 ± 2.36
17.90 ± 2.56
14.48 ± 2.64
38.63 ± 3.00
70.73 ± 3.63
9.06 ± 2.79
6.19 ± 2.33
31.63 ± 2.59
No increase
No increase
23.26 ± 2.10
3.09 ± 1.74
9.12 ± 2.58
31.61 ± 2.90
2.86 ± 1.30
5.43 ± 2.80
30.74 ± 2.31
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psychrotrophic bacteria and P. fluorescens. The above evidence suggests that GFSE and thymol could be advantageously combined to further slow down the growth of spoilage microorganisms. It is worth noting that pH was about 6.0 (data not shown), and it did not change much during storage, suggesting that the recorded antimicrobial activity has to be only ascribed to the investigated natural compounds. Sensorial quality decay
On fish, carvacrol is said to produce a ‘warmly pungent’ aroma (Kim et al., 1995b), thyme and oregano oils spread on whole Asian sea bass imparted herbal odour (Harpaz et al., 2003) and oregano oil on cod fillets produced a distinctive but pleasant flavour (Mejlholm & Dalgaard, 2002). In our conditions the used natural compounds had no ill effects on colour, odour, drip loss and texture. Figure 4 shows the fresh fish burger general appearance, as determined by panel test, plotted as a function of storage time for control and thymol loaded samples. Curves shown in this figure were drawn to highlight the trend of data. As can be inferred from Fig. 4, a different behaviour is observed between the control and the samples with thymol. Similar results were obtained for the other monitored attributes (data not shown). The sensorial acceptability limit (SAL) was taken as the latest storage time at which the packed product was still acceptable (i.e., none of monitored sensorial attributes has received a score below 2). Table 3 lists the SAL values obtained for the control and for the fish burgers loaded with the different antimicrobial compounds. As can be seen, for most of the samples the SAL value is higher than 14 days (i.e. the extension of the observation period), whereas for the control samples it is 6 days. However, Table 3 indicates that for all active samples an increase in the SAL value
Table 3 Sensory acceptability limit (SAL) values calculated for all fresh fish burgers Sample Control 20 ppm 40 ppm 80 ppm 20 ppm 40 ppm 80 ppm 20 ppm 40 ppm 80 ppm
thymol thymol thymol GFSE GFSE GFSE Lemon extract Lemon extract Lemon extract
SAL (day)
Restrictive sensory attribute
6 10 >14 >14 10 10 >14 >14 >14 >14
All attributes Odour — — Odour and general appearance Odour and general appearance — — — —
has been observed, if compared to the control. Moreover, by comparing the MAL and SAL values it can be inferred that microbial quality was the factor limiting fresh fish burger acceptability. Conclusions
All investigated compounds loaded at medium and high concentrations have found to be effective in slowing down the growth of the studied microorganisms, suggesting that they can be advantageously used to prolong the shelf life of fresh fish burger. Results also point out that GFSE and thymol are the most successful among the selected active natural preservatives in slowing down the growth of specific spoilage bacteria of marine temperate-water fish. Microbial proliferation was the factor limiting fresh fish burger acceptability suggesting that more efforts should be put forward to further slow down the growth of spoilage microorganisms. Acknowledgment
This work was financially supported by Ministero dell’Economia e delle Finanze, Ministero dell’Istruzione, dell’Universita` e delle Ricerca Scientifica e Tecnologica e l’Assessorato Bilancio e Programmazione Regione Puglia by the program ‘Accordo di Programma Quadro in Materia di Ricerca Scientifica della Regione Puglia - Progetto Esplorativo - Title: ‘Valorizzazione di pescato di basso valore commerciale attraverso trasformati ittici di IV gamma’. References
Figure 4 General appearance scores plotted as a function of storage time for control and thymol loaded samples. The curves were drawn to highlight the trend of experimental data.
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