Effects of postmortem temperature on the physicochemical characteristics of prerigor Pekin duck breast muscles

Effects of postmortem temperature on the physicochemical characteristics of prerigor Pekin duck breast muscles J. H. Choi,∗ Y. S. Choi,† H. W. Kim,‡ D. H. Song,‡ and C. J. Kim‡,1 ∗

CJ CheilJedang Food R&D Center, Seoul, 152–051, Republic of Korea; † Food Processing Research Center, Korean Food Research Institute, Seongnam 463–746, Republic of Korea; and ‡ Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 143–701, Republic of Korea

Key words: duck, postmortem temperature, breast muscle 2015 Poultry Science 00:1–6 http://dx.doi.org/10.3382/ps/pev263

INTRODUCTION

the latter have what is necessary for fast and effective anaerobic metabolism, namely, high ATP-ase activity, a high content of creatine phosphate to replenish ATP from adenosine diphosphate (ADP), and greater stores of glycogen to sustain anaerobic glycolysis (Lawrie, 1992). Among the extrinsic factors, the temperature to which the muscles are exposed during the PM period affects the rate of PM glycolysis. In unrestrained muscles, shortening has long been known to occur when rigor mortis develops at about 37◦ C (high temperature rigor); but with the high rate of PM glycolysis at cool temperatures, cold shortening also occurs (Locker and Hagyard, 1963). As the temperature falls from 15 to 0◦ C, Ca2+ ions are released from the tubes of the sarcoplasmic reticulum whereby their concentration in the sarcoplasm rises 30- to 40-fold, causing a massive stimulation of the contractile ATP-ase of the myofibrils and, thus, their contraction (Davey and Gilbert, 1974). This phenomenon is more developed in white muscle than red muscle. Poultry generally have white muscle, but duck muscle is a source of red meat around the world. Because duck breast has higher levels of red muscle fiber compared to chicken, PM changes are different in duck than in chicken, according to Ali et al. (2007), who reported that duck breast meat contained more redness and less lightness. Also, cooking loss and shear force of duck

It is generally known that the muscle of mammals (beef, hog, and lamb) and poultry (chicken, turkey, duck, and geese) begins undergoing various biochemical changes, such as the depletion of adenosine triphosphate (ATP) and glycogen, under anaerobic conditions after slaughter (Hamm, 1977). Also, the various factors that affect the rate of postmortem (PM) glycolysis are both intrinsic (species, genotype, animal age, and type of muscle) and extrinsic (the circumstances during slaughter, the addition of salts, and the PM temperature). In particular, among intrinsic factors, the type of muscle is an important determinant of the rate of pH decrease postmortem (Lawrie, 1992). It has long been known that this rate is greater in white muscle than in red muscle. White muscles have differentiated over the course of evolution to undertake fast, intermittent, and largely anaerobic actions, whereas red muscles are adapted to carrying out slower, more continuous action that depends on the supply of oxygen in vivo. Red muscles contain a higher proportion of respiratory enzymes than white muscles, whereas

 C 2015 Poultry Science Association Inc. Received December 26, 2014. Accepted August 10, 2015. 1 Corresponding author: [email protected]

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increased, cooking loss of meat stored at each temperature increased significantly (P < 0.05) at 2 h, but storage temperature does not affect cooking loss of duck breast muscle. The shear force of breast meat at 24 h PM had the lowest value, but meat stored at 30◦ C increased at 2 h and decreased at 24 h PM. Meat stored at 15◦ C showed a longer sarcomere length than meat stored at 0 and 30◦ C. The rate of muscle shortening was high during the 2 h PM for meat at the 3 temperatures. It is concluded that the different temperatures in the range of 0 to 30◦ C affected the muscle shortening or meat quality of the duck breast meat.

ABSTRACT The effects of postmortem (PM) temperature on prerigor Pekin duck breast muscle quality were assessed. Breast meat was obtained from 90 ducks within 15 min PM and then divided into 3 storage temperature groups at 0, 15, and 30◦ C for 24 h PM. Results revealed that the meat stored at 0◦ C had a higher pH value than that stored at 30◦ C. The Rvalue tended to increase between 15 min, 2 h, and 24 h PM, whereas the water-holding capacity decreased significantly (P < 0.05) with increasing storage time. The drip loss of treatment in meat stored at 30◦ C was higher than in those stored at 0 and 15◦ C. As storage periods

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breast were higher compared to chicken breast during storage for 7 d. Storage conditions are the most important factor in meat physical characteristics. Recently, duck has become very popular in Korea, but the changes that occur in duck muscle after slaughter have not been researched widely. In particular, the temperature conditions during PM storage affect the physicochemical and sensory qualities of duck. Therefore, this study was conducted to evaluate the effects of storage temperature on the bio- and physicochemical characteristics of prerigor Pekin duck breast muscle.

Sample Collection A total of 90 Pekin ducks (Anas platyrhynchos, 42 ± 2 d of age and approximately 3.2 to 3.4 kg live weight) were obtained from a local poultry processor and transported to the Konkuk University Meat Science Laboratory. To minimize the effects of catching and handling, feed was removed 12 h prior to processing, but the ducks were allowed access to water until 2 h prior to processing (Alvarado and Sams, 2000; Kim et al., 2012). The ducks were stunned electrically at 50 V for 10 s and killed by bleeding from incision of a single unilateral neck for approx. 3 min. The duck carcasses (2.1 to 2.2 kg) were obtained within 15 min after slaughter, and then the breast muscle was immediately removed (pectoralis major). Each duck breast muscle was weighed (143.25 ± 9.33 g). The separated left and right muscles were randomly assigned, and each portion was packed in a polyethylene bag. The left portion was used to determine the pH, R-value, water-holding capacity (WHC), and sarcomere length, and the right portion was used to determine the drip loss, cooking loss, and shear force. The samples were placed at 0, 15, 30◦ C for 0.25, 0.5, 1, 2, 4, 6, 12, and 24 h. Following storage, as previously stated, their physicochemical properties were evaluated.

pH and R-value The pH of a sample was determined using a pH meter (Model 340, Mettler-Toledo GmbH, Schwerzenbach, Switzerland). The pH values were measured by blending a 5 g sample with 20 mL distilled water for 60 s in a homogenizer (Ultra-Turrax T25, Janke & Kunkel, Staufen, Germany). The R-value was determined using a slightly modified method of Koh et al. (1993). The sample was homogenized in 6% perchloric acid (HClO4 ) at 5,000 rpm for 90 s, then centrifuged at 3,000 × g for 10 min. Ten mL of the supernatant was taken, and its pH was adjusted with 2 M KOH to 6.0 to 6.5, then stored chilled for 60 min. Then it was filtrated with Whatman No. 1 filter paper, and 0.1 mL of the filtrated solution was mixed with 2.9 mL of 0.1 M phosphate buffer (pH 6.5), and

Drip and Cooking loss The drip and cooking loss were determined for 0.5, 1, 2, 4, 6, 1 2, and 24 h. Drip loss was calculated according to weight loss percentage compared with the weight before storage. After drip loss was determined, the samples were bagged in polyethylene bags and immersed in a 75◦ C water bath (Model 10–101, Daehan Co., Seoul, Korea) for 30 min and cooled at room temperature for 30 min. After cooling to room temperature, the bags were opened and free juice was drained. The cooked samples were blotted with a paper towel and weighed. Cooking loss was determined by weighing the meat before and after cooking.

Water-Holding Capacity (WHC) The WHC was determined in triplicate using a filter paper press method (Grau and Hamm, 1953). Briefly, 300 mg sample was weighed on Whatman No. 2 filter paper and pressed between two Plexiglas plates for 3 min. The areas of pressed water and sample were measured using a planimeter (KP-21, Koizumi, Nagaoka, Japan). The WHC was measured at 0.25, 0.5, 1, 2, 4, 6, 12, and 24 h and calculated as a ratio of the meat film area to the total area.

Sarcomere Length and Degree of Muscle Shrinkage Sarcomere length was determined by a method (Voyle, 1971) using helium-neon-laser diffraction (Model 212–2, Spectra-Physics, Santa Clara, CA, USA). At different PM times, 1 to 2 g muscle sample was carefully cut with a knife and immersed in 2% glutaraldehyde solution with 2% glucose in a 0.1 M phosphate buffer, with a pH of 7.0, at a temperature similar to that at which the muscles were incubated, and the sarcomere length was measured. The degree of muscle shrinkage was measured in relation to muscle length. Immediately after slaughter, the duck breast meat was pinned up in 3 cm lengths along the muscle fiber and the lengths of the contracted muscles were measured after 0.5, 1, 2, 4, 6, and 24 h.

Shear Force Measurement To determine the shear force, samples were cooked individually in plastic bags immersed in a 75◦ C water bath for 30 min. The cooked meats were cooled at room temperature for 30 min. The 30 samples from each treatment were cut to thicknesses of 1.5 cm along the muscle fiber. Shear force values were determined

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MATERIALS AND METHODS

then its absorbance at 250 and 260 nm was determined with a UV spectrophotometer (DU650, Beckman, Massachusetts, USA). Then the R-value of A250/A260 was calculated.

POSTMORTEM TEMPERATURE OF DUCK BREAST MUSCLE

using a Warner–Bratzler shear attachment on a texture analyzer (TA-XT2i, Stable Micro Systems Ltd., Surrey, UK). Test speeds were set at 2 mm/s. Data were collected and analyzed on the basis of the shear force values to obtain the maximum force required to shear through each sample.

Statistical Analysis

RESULTS AND DISCUSSION pH and R-value It is well known that pH, sarcomere length, and development of rigor affect the WHC by altering cellular and extracellular components (Honikel et al., 1986; Offer and Knight, 1988). Generally speaking, the rate and extent of PM pH decline are very important factors affecting meat quality (Fernandez et al., 2002). A rapid pH decline may induce protein denaturation, resulting in decreased tenderness and juiciness and less intense (or pale) muscle coloration. The changes in pH and R-value in duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM are presented in Figure 1. The pH value for meat stored at 0, 15, and 30◦ C was 6.63 at 15 min PM. At 2 h PM pH values were 6.27, 6.21, and 6.09, and at 24 h PM they were 6.03, 5.99, and 5.94, respectively. The rate of pH decline was high during the first 2 h PM for meat at the 3 temperatures, whereas from 2 to 24 h PM only a slight decline was observed. On the other hand, a significant difference was observed in pH values between the meat

Figure 1. Changes in pH (, , ) and R-value (, r, ) on duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM.

stored at 0◦ C and that stored at 30◦ C. This result is similar to that of Lesiak et al. (1996), who reported that the rate of pH decline was high during the first hour PM for all temperatures (0, 12, and 30◦ C) and a slight decline in pH from 3 to 24 h PM. The pH of turkey meat at 3 h PM was not significantly affected among the various temperature treatments. In addition, Ali et al. (2007) showed that the breast meat of duck (cherry berry) has pH values ranging from 6.6 at 15 min PM to 6.0 at 24 h PM. The R-value is used to measure the degree to which adenosine nucleotides are transformed into inosine nucleotides and to estimate indirectly PM rigor development (Khan and Frey, 1971). As rigor mortis develops, the R-value generally tends to increase. Papa and Fletcher (1988) reported that the R-value of broiler pectoralis major reaches 0.95 to 0.97 in 15 to 30 min PM, and reaches 1.2 to 1.3 in 2 to 4 h PM. In this experiment, the R-values of the meat stored at 0◦ C for 0.25, 2, and 24 h PM were 0.97, 1.11, and 1.26, respectively. There were significant differences in R-values between 15 min and 2 h PM (P < 0.05) and between 2 h and 24 h PM (P > 0.05). For the meat stored at 15◦ C, the R-values at 0.25, 2, and 24 h were 0.97, 1.12, and 1.25, respectively, and significant differences were observed among the various storage times (P < 0.05). In addition, the R-values of the meat stored at 30◦ C for 0.25, 2, and 24 h PM were 0.97, 1.13, and 1.28, respectively, and significant differences were observed among the various storage times (P < 0.05). But R-values did not differ significantly among the 3 temperature treatments (P > 0.05).

Water-Holding Capacity and Drip Loss The level of exudates in animals has been related to the extent of muscle shortening (Honikel et al., 1986), and the contraction of myofibrils results in a greater proportion of free water that can be lost from meat (Marsh et al., 1972). The changes in WHC and drip loss in duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM are shown in Figure 2. WHC decreased significantly with increases in storage time (P < 0.05). In comparison with WHC at 0.25 h PM (52%), WHC at 2 and 24 h PM was reduced by 42 and 40% respectively for meat stored at 0◦ C, by 43 and 38% respectively for meat stored at 15◦ C, and by 40 and 37% respectively for meat stored at 30◦ C. In addition, WHC at 24 h PM was 22, 26, and 28% lower than that at 0.25 h PM for meat stored at 0, 15, and 30◦ C treatments, respectively. However, there were no significant differences between the 3 temperature treatments during storage periods. Kristensen and Purslow (2001) observed that the WHC of meat decreases from 3.9% water loss at 1 d PM to 11.9% at 3 d PM. Biswas et al. (2006) and Ali et al. (2007) showed that duck muscles have a lower WHC, greater cooking loss, and emulsion stability than chicken muscles.

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ANOVA was performed on all variables measured using the General Linear Model (GLM) procedure of the SAS statistical package (SAS Inst., 2002). Duncan’s multiple range test (P < 0.05) was used to determine the differences between treatment means. The CORR procedure of the SAS package was used to calculate the correlations between the storage temperature and the various parameters (pH, R-value, WHC, sarcomere length, cooking loss, and degree of muscle shrinkage) in duck breast muscles stored at 0, 15, and 30◦ C.

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Drip loss is a process generally involving the transfer of water from myofibrils to extracellular space; it is affected by structural features at several levels within the muscle tissue (Bertram et al., 2002). Drip loss is related to a contraction of PM muscle and deterioration of muscle proteins (Kristensen and Purslow, 2001; Melody et al., 2004). Drip losses rates in meat stored at 0, 15, and 30◦ C for 2 h PM were 0.89, 1.36, and 2.03%, and 4.16, 3.68, and 4.76% for 24 h, respectively. Significant differences were observed in results between 2 and 24 h PM and between meats stored at all storage temperatures (P < 0.05). Also, the drip loss in treatment involving storage at 30◦ C was higher than under storage at 0 and 15◦ C. These results are similar to those of Alvarado and Sams (2002), who found that the drip loss in muscles from turkey carcasses chilled at 30◦ C was significantly higher than that in those chilled at 0 and 10◦ C.

Cooking Loss and Shear Force The changes from cooking loss and shear force in duck breast muscle stored at 0, 15, and 30◦ C for 24 h PM are shown in Table 1. In this study, cooking loss at 15 min after slaughter was 17.0%. As storage periods increased, cooking loss in meat stored at each temperature significantly increased for 2 h but was not significantly different thereafter. Also, storage tempera-

Sarcomere Length and Degree of Muscle Shrinkage Sarcomere length is a good indicator of muscle shortening. The relationship between cold shortening and sarcomere length was first demonstrated clearly by

Table 1. Changes in cooking loss and shear force on duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM. Time after slaughter (h) ◦

Trait

Temp. ( C)

0.25

Cooking loss (%)

◦

1

0 C 15◦ C 30◦ C

17.00 ± 2.66 17.00 ± 2.66c 17.00 ± 2.66c

21.50 ± 3.10 21.20 ± 4.14b 21.72 ± 2.51b

25.71 ± 3.83 25.25 ± 2.60a 26.29 ± 3.27a

26.04 ± 2.44 26.22 ± 4.29a 27.37 ± 4.30a

26.22 ± 3.32 25.86 ± 3.37a 27.71 ± 2.51a

25.80 ± 3.10a 26.59 ± 3.51a 26.66 ± 4.74a

Shear force (kg)

0◦ C 15◦ C 30◦ C

8.02 ± 0.57 8.02 ± 0.57 8.02 ± 0.57

8.48 ± 0.57 8.31 ± 0.42 8.58 ± 0.29

8.57 ± 0.71 8.34 ± 0.64 8.60 ± 0.67

8.28 ± 0.68 8.12 ± 0.29 8.33 ± 0.50

8.20 ± 0.61 8.32 ± 0.64 8.31 ± 0.53

8.28 ± 0.50 8.08 ± 0.57 8.12 ± 0.55

c

2 b

6 a

Values are the mean ± standard deviation (n = 30). a–c Means in the same row with different superscripts differ significantly (P < 0.05).

12 a

24 a

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Figure 2. Changes in water-holding capacity (WHC) (, , ) and drip loss (DL) (, r, ) on duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM.

ture does not affect cooking loss in duck breast muscle. Geesink et al. (2000) observed that cooking loss in longissimus muscle of lamb was not affected by initial temperature treatment (16 h, 5 to 35◦ C). McKee and Sams (1998) observed that a PM storage temperature of 40◦ C increased the cooking loss in turkey breast fillets compared to 0◦ C treatment. However, the differences between these results were probably due to materials used, genetic factors, and experimental design. Tenderness is one of the major factors affecting consumer acceptance of meat products. In addition, duck muscle is generally perceived by consumers as being tough (Smith and Fletcher, 1992). Davey et al. (1967) also reported that shortening of up to 20% did not appear to affect shear force values, but further shortening significantly increased shear force values. In this study, the shear force for meat stored at 0◦ C increased from 7.62 kg at 15 min after slaughter to 8.77 kg at 2 h, and was significantly different (P < 0.05). Shear force then decreased to 7.26 kg at 24 h PM (P < 0.05). For meat stored at 30◦ C, the shear force increased at 2 h (9.00, P < 0.05) but decreased at 24 h PM (7.52, P < 0.05). Wyche and Goodwin (1974) reported that the shear force of broiler meat over 24 h increased gradually until 4 h PM and thereafter decreased until 8 h PM, then increased again slightly but not significantly. Likewise, the shear force did not change significantly when pectoralis major meat was individually stored at 4, 20, and 40◦ C for 6 h and then stored at 4◦ C for 18 h (Molette et al., 2003). McKee and Sams (1998) found no significant differences between 0 and 20◦ C or between 20 and 40◦ C, but they did find significant differences between broiler breast meat stored at 0◦ C and that stored at 40◦ C. Ali et al. (2007) found that cooking loss and shear force was higher in duck breast compared to chicken breast for the duration of storage times (7 d). In particular, they found that the shear force decreased rapidly in duck breast compared to chicken breast.

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POSTMORTEM TEMPERATURE OF DUCK BREAST MUSCLE

Rigor shortening can be minimized if prerigor muscle is stored at 10 to 15◦ C during rigor development. Rigor shortening of approximately 28 to 32% was observed in all treatments of our study. The rate of muscle shortening was high during the first 2 h PM for meat at the 3 temperatures, whereas from 2 to 24 h PM there was only a slight decline.

Correlation Analysis

Herring et al. (1965), who showed the direct relationship between sarcomere length, fiber diameter, and toughness. Muscle contraction is induced by the release of Ca2+ ions from the sarcoplasmic reticulum into the myofibrillar space. Sarcomere is the contractile unit of myofibrils, and sarcomere lengths shorten during muscle contraction (Honikel et al., 1986). In this study, sarcomere length was determined in order to evaluate the contractile state of the prerigor duck pectoralis major muscles. The changes in sarcomere length and muscle shrinkage in duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM are shown in Figure 3. At 15 min PM, pectoralis major muscles exhibited a resting sarcomere length of 1.92 ± 0.12 μm. The sarcomere of duck breast meat stored at 0, 15 and 30◦ C shrank continuously until 24 h PM. For meat stored at 0◦ C, sarcomere lengths for meat stored for 2 and 24 h PM were, respectively, 24 and 37% shorter than at 15 min PM, and those for meat stored at 30◦ C for 2 and 24 h PM were, respectively, 20 and 40% shorter than at 15 min PM. On the other hand, for meat stored at 15◦ C, sarcomere lengths for meat stored for 2 and 24 h PM were, respectively, 15 and 30% shorter than at 15 min PM. This indicated that sarcomere length had shrunk slightly at 15◦ C compared with that at 0 and 30◦ C. The reports of Papa and Fletcher (1988) and Dunn et al. (1995) on sarcomere length in poultry measured under similar PM storage conditions showed that the shrinkage of sarcomere length at 0◦ C was more severe.

Table 2. Relationship between storage temperature and measurements in duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM. Traits Storage temperature pH R-value WHC Sarcomere length Cooking loss

pH

R-value

− 0.59

a

a

0.77 − 0.52a

WHC

Sarcomere length

− 0.61 0.44 − 0.73a

− 0.65 0.60a − 0.82a 0.65a

Highly statistically significant at P < 0.001. WHC: water-holding capacity.

a

a

a

Cooking loss a

0.53 − 0.26 0.67a − 0.59a − 0.70a

Muscle shrinkage 0.52a − 0.40 0.73a − 0.76a − 0.69a 0.68a

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Figure 3. Changes in sarcomere length (SL) (, , ) and muscle shrinkage (MS) (, r, ) on duck breast muscle stored at 0, 15, or 30◦ C for 24 h PM.

Table 2 shows the relationship between storage temperature and parameters in duck breast muscle stored at 0, 15, and 30◦ C. Most of the correlation coefficients between storage temperature and parameters of breast meat were significant. In particular, storage temperature was very positively correlated with R-value, cooking loss, and degree of muscle shrinkage, whereas it was negatively correlated with pH, WHC, and sarcomere length. The R-value was negatively correlated with pH, WHC, and sarcomere length but positively correlated with cooking loss and degree of muscle shrinkage. Additionally, WHC was negatively correlated with cooking loss and muscle shrinkage and positively correlated with sarcomere length. The relationships between pH and meat quality in poultry meats (turkey, chicken, and duck) have been studied quite extensively (Fletcher, 1999; Van Laack et al., 2000). In addition, Dunn et al. (1995) found a strong negative correlation between shear force and sarcomere length in chicken breast meat, emphasizing that sarcomere shortening was a major contributor to toughness in carcasses chilled at −12 and 0◦ C. Also, Lesiak et al. (1996) reported a significant correlation between PM temperature and storage time in both breast and leg muscles for turkey breast where drip loss was least at 0 and 12◦ C and greatest at 30◦ C. Sams and Janky (1991) stated that chilling has a greater effect on slowing the rate of rigor mortis development in red fibers compared with white fibers. Duck breast muscle with red fiber shows slower muscle shortening than chicken and turkey with white muscle. This is because duck carcasses are covered with thick skin and fat layers under the skin (Smith et al., 1976; Dolezal et al., 1982). The results of this study indicated that in the meat of big livestock, such as beef and pork, cold shortening is distinct from heat

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shortening in general (Hertzman et al., 1993), whereas there is little difference between the two in the meat of small livestock, such as poultry (Wyche and Goodwin, 1974). The results of this study, therefore, cannot be similar to results from big livestock. In conclusion, the different temperatures in the range of 0 to 30◦ C affected muscle shortening or meat quality of duck breast meat. In particular, duck breast meat was more susceptible to hot shortening at 30◦ C than cold shortening at 0◦ C.

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