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Meat Science 76 (2007) 604610
www.elsevier.com/locate/meatsci
Department of Food and Nutritional Sciences, University College Cork, National University of Ireland, Western Road, Cork, Ireland
Abstract
The eect of grape seed extract (GSE) and bearberry (BB), on lipid oxidation (TBARS, mg malondialdehyde (MDA)/kg muscle),
colour (CIE a redness value), pH, microbial status (log10CFU colony forming units/g pork) and sensorial properties of cooked pork
patties was investigated. GSE (01000 lg/g muscle) and BB (01000 lg/g muscle) were added to raw pork (M. longissimus dorsi) patties
which were stored in modied atmosphere packs (MAP) (75% O2:25% CO2) for up to 12 days at 4 C. Cooked pork patties were stored in
MAP (70% N2:30% CO2) for up to 4 days at 4 C. Mesophilic plate counts and pork pH were unaected by GSE and BB. GSE and BB
addition decreased (P < 0.05) lipid oxidation (TBARS) in raw pork patties on days 9 and 12 of storage, relative to controls. Antioxidant
activity of GSE and BB was observed in cooked pork patties demonstrating the thermal stability of GSE and BB. The a redness values
of raw and cooked pork patties marginally increased with increasing GSE concentration. The sensory properties of cooked pork patties
were unaected by GSE and BB addition. Results obtained demonstrate the potential for using health promoting nutraceuticals in meat
and meat products.
2007 Elsevier Ltd. All rights reserved.
Keywords: Natural antioxidants; Grape seed extract; Bearberry extract; Lipid oxidation; Pork
0309-1740/$ - see front matter 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.meatsci.2007.01.021
R. Carpenter et al. / Meat Science 76 (2007) 604610 605
Flavonoids are the most abundant and potent group of GSE and BB on meat quality parameters merits
plant phenolic compounds and act as antioxidants (Rice- investigation.
Evans & Miller, 1996). Grape seeds from grape juice and The objective of the present study was to assess the eect
wine processing can be separated, extracted, dried and of health promoting plant extracts, GSE and BB, on lipid
puried into GSE which contains phenolic compounds oxidation, colour, pH, microbial status and organoleptic
(Lau & King, 2003). Clinical data has shown that the anti- properties of raw and cooked pork patties during chilled
oxidant potential of grape seed is twenty and fty fold storage.
greater than vitamins E and C, respectively (Shi, Yu, Poh-
orly, & Kakuda, 2003) arising from increased levels of pol- 2. Materials and methods
yphenol proanthocyanidins and oligomers of avan-3-ol
units, especially catechin and epicatechin present in GSE 2.1. Reagents
(Yilmaz & Toledo, 2004). The antioxidant activity of
GSE has been reported in a variety of test systems (Jayap- All chemicals used were AnalaR grade obtained from
rakasha, Singh, & Sakariah, 2001) including cooked beef British Drug House, Poole, Dorset, UK; Sigma Chemical
(Ahn, Grun, & Fernando, 2002) and turkey (Lau et al., Co. Ltd, Poole, Dorset, UK and Rathburn Chemical Co.
2003; Mielnik, Olsen, Vogt, Adeline, & Skrede, 2006). Ltd, Walkerburn, Peableshire, Scotland. Grape seed
The antimicrobial properties of GSE against gram positive extract (GSE, 85% oligopolysaccharides) and bearberry
and gram negative bacteria has been reported previously (BB) extract (Uva Ursi, 20% arbutin) were obtained from
(Jayaprakasha, Selvi, & Sakariah, 2003). GSE eectively Guinness Chemical (Ireland) Ltd, Clonminam Industrial
reduced the numbers of E. coli and S. typhimurium and Estate, Portlaoise, Co. Laois, Ireland. Fresh pork (M. Lon-
retarded growth of L. monocytogenes and A. hydrophila gissimus dorsi) was obtained from Ballyburden Meat Pro-
in cooked ground beef (Ahn, Grun, & Mustapha, 2007). cessors, Ballincollig, Co. Cork, Ireland.
From a health perspective, GSE has been shown to act
as a anticarcinogenic (Roy et al., 2002) and cardio-protec- 2.2. Total polyphenol content of GSE and BB
tive agent (Shaee, Carbonneau, Urban, Descomps, &
Leger, 2003). The concentration of phenolic compounds in GSE and
BB, also known as Uva Ursi, is a member of the ever- BB was determined by the Folin-Ciocalteau method as
green heath family. Traditionally, the astringent leaves described by Singleton and Rossi (1965). GSE and BB were
have been used in the treatment of bladder infections and dissolved in distilled water, and to 1 ml of sample, 5 ml of
other aictions of the urinary tract. The scientic literature Folin-Ciocalteau reagent (diluted 1:10 with distilled water)
contains less information regarding the antioxidant poten- was added. After 5 mins, 4 ml of a sodium carbonate solu-
tial of BB compared to GSE, however antioxidant activity tion (7.5%) was added to each tube. The tubes were incu-
of BB has been reported in cooked pork (Pegg, Amarowicz, bated for 2 h at room temperature and the absorbance
& Barl, 2001). The antioxidant properties of BB (Amar- determined spectrophotometrically (DU 640 UV/Vis
owicz, Pegg, Rahimi-Moghaddam, Barl, & Weil, 2004) spectrophotometer, Beckman Coulter, CA, USA) against
are most likely attributed to the glycoside arbutin fraction a reagent blank at 740 nm. The total polyphenol content
present (Annuk et al., 1999). BB extract displays potential was calculated using gallic acid as a standard and results
antimicrobial benets with respect to food-associated bac- were expressed as gallic acid equivalents (GAE) (g GAE/
teria when used in combination with nisin (Dykes, Amar- 100 g extract).
owicz, & Pegg, 2003). Furthermore, aqueous extracts of
BB have been shown to alter the ability of E. coli (Turi, 2.3. Antioxidant addition and pork packaging
Turi, Anuuk, & Arak, 1999) and H. pylori (Annuk et al.,
1999) to cause infection. GSE and BB were found to be most eective against oxi-
Lipid oxidation is a major quality deteriorative process dative stress in vitro at concentrations of 50 lg/ml and
in muscle foods resulting in a variety of breakdown 10 lg/ml, respectively (Carpenter et al., 2006). Therefore
products which produce o-odours and avours in order to evaluate the eects of GSE and BB in a meat
(Faustman & Cassens, 1990). Muscle foods are also suscep- system, a range of increasing concentrations, including
tible to microbial contamination leading to foodborne ill- the above stated values for GSE and BB, were added to
nesses. In addition, colour changes are also an important minced pork. Pork samples were minced twice through a
factor inuencing the quality and acceptability of meat plate with 4 mm holes (Model P114L, Talsa, Valencia,
and meat products. Currently, there is a growing interest Spain) following the removal of all external fat and connec-
in the use of natural antimicrobial agents and antioxidants tive tissue. Following mincing, raw pork was assigned to
derived from plant sources. The use of plant derived one of the following thirteen treatments: untreated pork
nutraceuticals may aord meat processors the opportunity (control); pork plus increasing amounts of GSE: 50 lg
to develop novel meat products with enhanced nutritional GSE/g muscle (GSE 50); 100 lg/g muscle (GSE 100);
and health benets, improved shelf-life, quality and prole. 200 lg/g muscle (GSE 200); 300 lg/g muscle (GSE 300);
Therefore the inuence of selected nutraceuticals such as 400 lg/g muscle (GSE 400); 1000 lg/g muscle (GSE
606 R. Carpenter et al. / Meat Science 76 (2007) 604610
1000); or increasing amounts of BB: 10 lg BB/g muscle diameter measuring area, and a data processor (DP-301).
(BB 10); 20 lg/g muscle (BB 20); 40 lg/g muscle (BB 40); The chroma meter was calibrated on the CIE colour space
60 lg/g muscle (BB 60); 80 lg/g muscle (BB 80) and system using a white tile. The L value represents lightness
1000 lg/g muscle (BB 1000). GSE and BB were added to and a and b values represent redness and yellowness,
raw pork samples at 1000 lg/g pork to determine if such respectively. Colour measurements were made on days 0,
levels exerted any pro-oxidant activity. GSE and BB were 3, 6, 9 and 12 for raw pork samples and days 0, 2 and 4
dissolved in distilled water (5% v/w), immediately added for cooked pork samples.
to raw minced pork and mixed vigorously.
Minced pork containing GSE or BB was formed into 2.7. pH measurements
patties (80 g portions) using a meat former (Ministeak bur-
ger maker, O.L Smith Co. Ltd., Italy), placed in low oxy- Pork samples (10 g) were homogenised (1 min,
gen permeable (<1 cm3/m2/24 h/atSTP) polystyrene/ 24,000 rpm) in 90 ml distilled water using an Ultra Turrax
ethylvinylalcohol/polyethylene trays and using modied T25 homogeniser (Janke and Kunkel, IKA-Labortechnik,
atmosphere packaging (MAP) technology, ushed with GmbH and Co., Staufen, Germany). Also, GSE and BB
75% O2: 25% CO2 using a vacuum-sealing unit (VS 100, (10 g) were dissolved in 90 ml distilled water. The pH of
Gustav Muller and Co. KG, Bad Homburg, Germany) the pork homogenates, GSE and BB were measured at
equipped with a gas mixer (Witt-Gasetechnik GmbH and 20 C using a pHm 201 portable pH meter (Radiometer,
Co. KG, Witten, Germany). Trays were covered and Copenhagen, Denmark). The pH of the raw pork samples
heat-sealed using a low oxygen permeable (3 cm3/m2/ was recorded on days 0, 3, 6, 9 and 12 of storage.
24 h/atSTP) laminated barrier lm with a polyolen heat
sealable layer. All MAP samples were stored for up to 12 2.8. Microbiological analysis
days under uorescent lighting conditions (approximately
660 lx) at 4 C. Pork samples (10 g) were transferred into stomacher
bags, diluted with 90 ml of ringers solution and stomached
2.4. Cooking and packaging for 2 min in a Stomacher-400 (Steward Stomacher 400 Lab
Blender, London, UK) resulting in a 10 1 dilution used for
Minced pork was assigned to one of the following ve analysis. Serial dilutions were prepared and 0.1 ml aliquots
treatments: untreated pork (control); pork plus increasing from each dilution were plated onto standard plate count
amounts of GSE: 400 lg GSE/g muscle (GSE 400); agar (PCA). The plates were incubated at 30 C for 48 h
1000 lg/g muscle (GSE 1000); or increasing amounts of to determine mesophilic counts on days 0, 3, 6, 9 and 12
BB: 80 lg BB/g muscle (BB 80) and 1000 lg/g muscle of storage. Results were expressed as log10CFU (colony
(BB 1000). Samples were formed into 80 g pork patties as forming units)/g pork.
described above and cooked in a fan-assisted oven (Model
10 GN1/1, Zanussi Professional, Conegliano, Italy) at 2.9. Sensory evaluation
180 C until an internal meat temperature of 72 C was
reached and subsequently held at 180 C for a further A trained sensory panel of 810 researchers, Depart-
8 min. Following cooling, cooked patties were packaged ment of Food and Nutritional Sciences, University College
as described above, packs were ushed with 70% N2: 30% Cork, evaluated cooked pork patties after 0, 2 and 4 days
CO2 and stored for up to 4 days under uorescent lighting of chilled storage at 4 C. Each of the 5 patties were sliced
conditions (approximately 660 lx) at 4 C. into 8 pieces, placed on paper plates and served to panel-
ists. Panelists were asked to evaluate sample colour, a-
2.5. Measurement of lipid oxidation vour, texture, juiciness and o-avours on a 10-point
descriptive hedonic scale ranging from extremely desirable
Lipid oxidation was measured by the 2-thiobarbituric (1) to undesirable (10).
acid distillation method of Tarladgis, Watts, and Youna-
than (1960) as modied by Ke, Ackman, Linke, and Nash 2.10. Statistical analysis
(1977). Results were expressed as 2-thiobarbituric acid
reactive substances (TBARS) in mg malondialdehyde All analyses were performed in duplicate. A full
(MDA)/kg muscle. TBARS values were measured on days repeated measures ANOVA was conducted to investigate
0, 3, 6, 9, 12 for raw pork samples and on days 0, 2 and 4 the eects of antioxidant concentration, time and their
for cooked pork samples. interactions. The concentration assigned to the pork patties
represented the between-subjects factor. The eect of
2.6. Colour determination time was measured using the within-subjects factor.
Tukeys test was used to adjust for multiple comparisons
Surface colour measurements were determined using a between treatment means. The analysis was carried out
CR-300 Chroma Meter (Minolta Co., Osaka, Japan) which using SPSS 11.0 for Windows (SPSS, Chicago, IL, USA)
consisted of a measuring head (CR-300), with an 8 mm software package.
R. Carpenter et al. / Meat Science 76 (2007) 604610 607
3. Results and discussion pathogens such as E. coli and H. pylori (Annuk et al.,
1999).
3.1. Total polyphenol content of GSE and BB
3.3. Lipid stability of raw pork patties containing added GSE
The total polyphenol content of GSE and BB was and BB
86.5 g 1.15 GAE/100 g and 57.4 g 1.73 GAE/100 g,
respectively. Caillet, Salmieri, and Lacroix (2006) reported The presence of GSE and BB in raw pork patties signif-
that GSE contained 80.7 g GAE/100 g which is similar to icantly decreased (P < 0.05) lipid oxidation on days 9 and
the polyphenol content of GSE used in the present study. 12 of storage compared to the controls (Table 1). A signif-
To date, the scientic literature contained no data referring icant (P < 0.05) antioxidant concentration time interac-
to the polyphenol content of BB extract. tion was observed for both GSE and BB. Lau et al.
(2003) reported antioxidant activity of GSE at a concentra-
3.2. pH and microbial status of raw pork patties containing tion of 1000 lg/g (GSE polyphenol content of 85.4 g GAE/
added GSE and BB 100 g) in uncooked poultry. The highest concentration of
GSE and BB employed in our study (1000 lg/g) did not
The pH of raw pork patties decreased from 5.7 to 5.5 exert any pro-oxidant activity in raw pork and was shown
over the 12 day storage period and were unaected by to be four times more eective in reducing lipid oxidation
the addition of GSE and BB whose pH values were 3.84 when compared to lower concentrations (50 lg GSE/g
and 4.71, respectively. This pH range is comparable to that muscle and 20 lg BB/g muscle). By contrast, in a previ-
previously reported (5.45.8) for post-mortem muscle ously reported study, b-carotene demonstrated a pro-oxi-
(Faustman et al., 1990). The mesophilic plate counts ran- dant eect at 50 lg/g, while at lower concentrations
ged from 3.32 log10 cfu/g to 3.61 log10 cfu/g, and did not (10 lg/g) acted as an antioxidant in broiler meat (Ruiz,
signicantly increase over the 12 day storage period. This Perez-Vendrell, & Esteve-Garca, 1999). Plant-extracted
may be partly due to the antimicrobial eect of carbon antioxidants can exhibit pro-oxidant activity at low con-
dioxide (25%) in the modied atmosphere packs. Meso- centrations and antioxidant activity above a certain level
philic counts obtained are similar to previously reported (Wanasundara & Shahidi, 1998). Conversely, an antioxi-
values for raw pork (Houben, Eikelenboom, & Hoving- dant eect at low concentrations and pro-oxidant activity
Bolink, 1998). Graded addition of GSE and BB did not at higher concentrations can also occur (Pryzbylski, Lee,
signicantly eect or improve the microbial status of pork & Eskin, 1998). Although an antioxidant eect was evident
patties relative to the controls (data not shown). This is in at 400 lg GSE/g muscle and 80 lg BB/g muscle, the use of
contrast to previous reports where the antimicrobial 1000 lg/g muscle of each extract did not oer any further
properties of GSE were demonstrated in ground beef protection against lipid oxidation compared to the lower
(Ahn, Grun, & Mustapha, 2004) and extracts of BB (1:10 levels (Table 1). Overall, lipid stability increased with
aqueous infusion) exhibited protection against food increasing concentrations of GSE and BB.
Table 1
Eect of grape seed extract (GSE) and bearberry (BB) on lipid oxidation (TBARS) in raw pork patties stored in modied atmosphere packs (75% O2: 25%
CO2) at 4 C
Treatment1 Day 0 Day 3 Day 6 Day 9 Day 12
* * * a
Control 0.15 0.02 0.33 0.04 0.38 0.01 0.58 0.09 0.91 0.01a
GSE 50 0.14 0.03 0.29 0.09 0.31 0.02 0.31 0.01b 0.35 0.02b
GSE 100 0.11 0.01 0.23 0.03 0.30 0.08 0.33 0.05b 0.29 0.01bd
GSE 200 0.12 0.01 0.19 0.04 0.31 0.12 0.28 0.04b 0.24 0.01cd
GSE 300 0.09 0.01 0.17 0.04 0.22 0.05 0.19 0.04b 0.24 0.01cd
GSE 400 0.09 0.01 0.17 0.07 0.16 0.03 0.16 0.02b 0.16 0.02e
GSE 1000 0.09 0.01 0.10 0.06 0.14 0.03 0.11 0.03b 0.09 0.01e
BB 10 0.14 0.05* 0.29 0.05* 0.37 0.13* 0.46 0.11ac 0.43 0.11b
BB 20 0.10 0.01 0.22 0.07 0.36 0.12 0.32 0.04ad 0.40 0.01b
BB 40 0.09 0.02 0.17 0.01 0.26 0.04 0.23 0.05bcd 0.27 0.03b
BB 60 0.10 0.04 0.17 0.06 0.16 0.05 0.19 0.02bcd 0.23 0.04b
BB 80 0.07 0.03 0.13 0.03 0.14 0.02 0.17 0.01bcd 0.21 0.02b
BB 1000 0.10 0.03 0.11 0.02 0.16 0.03 0.11 0.03bcd 0.10 0.03b
TBARS, mg malondialdehyde/kg muscle.
abcde
Within each day (each antioxidant type compared to the control) mean values ( SEM) in the same column bearing dierent superscripts are
signicantly dierent, P < 0.05.
1
GSE or BB, lg/g muscle.
*
No signicance, P > 0.05.
608 R. Carpenter et al. / Meat Science 76 (2007) 604610
3.4. Lipid stability of cooked pork patties containing added BB reduced lipid oxidation during the cooking process
GSE and BB (day 0 TBARS). These results demonstrate the thermal sta-
bility of GSE and BB.
After 0, 2 and 4 days of refrigerated storage, GSE GSE and BB demonstrated a pronounced antioxidant
(400 lg/g, 1000 lg/g) inhibited (P < 0.05) TBARS forma- eect in raw and cooked pork during chilled storage. The
tion, compared to controls, in cooked pork patties held mechanism of the protective eect of GSE on lipid oxida-
in MAP (Table 2). Mielnik et al. (2006) reported that tion may be due to the presence of a number of oligomer
GSE (0, 400, 800 and 1600 lg/g) signicantly improved procyanidins, such as catechin and epicatechin (Yilmaz
the oxidative stability of cooked turkey meat. Similarly, et al., 2004), which possess a greater antioxidant potential
the antioxidant eect of GSE was also demonstrated in than monomer components (Llopiz et al., 2004). BB is
cooked ground beef (200, 500 and 1000 lg/g) (Ahn et al., reported to contain a vast array of hydroquinone deriva-
2002). The addition of BB (80 lg/g, 1000 lg/g) signicantly tives, such as arbutin, tannins, avonoids, triterpenes and
(P < 0.05) reduced lipid oxidation in cooked pork patties. phenolcarboxylic acids (Annuk et al., 1999) which confer
These ndings are in agreement with a similar study (Pegg antioxidant activity. Since a number of polyphenolic com-
et al., 2001) whereby, BB was shown to protect against pounds are present in GSE and BB, the antioxidant poten-
lipid oxidation in cooked minced pork at levels of 100, tial demonstrated in the present study may also be due to
200 and 500 lg/g. GSE and BB addition, at the upper limit the additive and synergistic eects of the individual com-
of 1000 lg/g, resulted in a 5-fold (day 2) and 9-fold (day 4) pounds present.
decrease in lipid oxidation compared to controls and anti-
oxidant potency increased (P < 0.05) with increasing GSE 3.5. Colour stability of raw pork patties containing added
and BB concentration (Table 2). In addition, GSE and GSE and BB
Table 3
Eect of grape seed extract (GSE) and bearberry (BB) on the surface redness (a value) of raw pork patties stored in modied atmosphere packs (75% O2:
25% CO2) at 4 C
Treatment1 Day 0 Day 3 Day 6 Day 9 Day 12
* * * *
Control 11.19 0.16 9.69 0.44 8.90 0.63 7.81 0.55 7.04 0.49*
GSE 50 11.39 0.28 9.62 0.41 9.04 0.24 7.98 0.75 7.54 0.54
GSE 100 11.28 0.21 9.73 0.29 9.30 0.34 8.09 0.65 7.68 0.49
GSE 200 11.37 0.25 9.88 0.30 9.23 0.33 8.50 0.53 7.84 0.37
GSE 300 11.45 0.16 10.03 0.30 9.23 0.26 8.39 0.52 7.89 0.28
GSE 400 11.25 0.08 10.04 0.25 9.74 0.26 8.65 0.49 8.08 0.34
GSE 1000 11.34 0.11 10.09 0.19 9.85 0.21 8.81 0.24 8.19 0.24
BB 10 11.13 0.57* 10.10 0.35* 8.77 0.45* 8.40 0.49* 7.39 0.52*
BB 20 11.11 0.12 9.74 0.37 9.04 0.40 8.31 0.48 7.56 0.34
BB 40 11.90 0.12 9.73 0.62 9.09 0.44 8.56 0.50 7.95 0.24
BB 60 10.99 0.20 9.74 0.35 9.03 0.54 8.41 0.52 7.78 0.29
BB 80 10.96 0.25 9.36 0.34 9.20 0.52 7.97 0.50 7.65 0.23
BB 1000 10.95 0.20 9.45 0.28 9.25 0.31 8.13 0.42 7.84 0.20
CIE a redness value (mean SEM).
1
GSE or BB, lg/g muscle.
*
No signicance, P > 0.05.
R. Carpenter et al. / Meat Science 76 (2007) 604610 609
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