Effect of Heating Rate on Shortening of Prerigor Chicken Breast Muscle 1
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1 Effect of Heating Rate on Shortening of Prerigor Chicken Breast Muscle 1 H. A. ABUGROUN, 2 ' 3 J. C. FORREST, 3 J. S. MARKS, 4 and M. D. JUDGE 3 ' 5 Purdue Agricultural Experiment Station, West Lafayette, Indiana (Received for publication July 13,1984) ABSTRACT Experiments were conducted to evaluate the effects of various heating rates on prerigor chicken breast muscle (Pectoralis major). Heating rates from 2 C per 6 min to 2 C per 18 min (Experiment 1) gave similar results in percentages of myofibrillar, cooking, and total shortening. Myofibrillar shortening began at approximately 39 C and completed at 46 to 50 C, and cooking shortening began at 65 to 66 C, regardless of heating rate. Heat absorbed per gram of muscle sample to onset and completion of myofibrillar shortening, or to onset of cooking shortening, was not different for the various heating rates. A higher muscle temperature at both onset and completion of myofibrillar shortening was observed at the 2 C per 2 min heating rate than at the 2 C per 12 min heating rate (Experiment 2). At 2 C per 2 min, myofibrillar shortening was more extensive, occurred faster, and was coincident to the absorption of more heat per gram of muscle to onset and completion as compared to 2 C per 12 min. The results support the view that rapid heating (>2 C per 2 min) of prerigor muscle elicits extensive shortening caused by an active contraction. (Key words: prerigor muscle, chicken, heat shortening) INTRODUCTION There is a close relationship between myofibrillar contraction state and the tenderness of cooked meat (Locker, I960; Locker and Hagyard, 1963; Marsh and Leet, 1966; Herring et al, 1965; 1967). Muscle shortening greater than 40% has been associated with increased meat tenderness (Behnke et al, 1973; Marsh and Carse, 1974; Davey and Gilbert, 1975a; Hsieh et al, 1980). This improvement in tenderness results from the shattering of fiber structure in some areas as induced by extreme shortening in other areas. The fractured zones offer little resistance to cleavage by shearing force (Cia and Marsh, 1976). Little is known about the behavior of prerigor muscle at high temperatures. Marsh (1977) hypothesized that there is a critical heating rate above which tenderness of prerigor meat is improved. That concept suggests that, when heating is sufficiently rapid, denaturation of enzymes occurs before significant progress toward rigor onset takes place. 'Journal paper No Present address: Food Research Center, P.O. Box 213, Khartoum North, Sudan. 3 Department of Animal Science. "Department of Food Science. 5 To whom correspondence should be addressed Poultry Science 64: The purposes of this study were to determine the heating rate required to achieve muscle shortening greater than 40% and to ascertain if there is a critical heating rate that could arrest rigor mortis and avoid rigor shortening. Furthermore, the study was designed to quantitate muscle shortening due to the contractile mechanism (myofibrillar shortening) as well as that due to the shrinkage of collagen (cooking shortening) (Davey and Gilbert, 1974, 1975a). MATERIALS AND METHODS White Leghorn hens, approximately 52 weeks of age, were utilized. The Pectoralis major muscle was removed immediately after the birds were killed and strips of parallel fibers approximately 3.8 cm long and 1.5 cm 2 crosssectional area were prepared. Samples were held with clips placed at each end of the muscle strips at a constant 3 cm apart. The Myotron (Fig. 1), described by Forrest et al. (1969), was used in two experiments. Muscle samples were suspended in white paraffin oil in the inner chamber of a doublewalled glass vessel. Heated distilled water at 37 C was circulated through the enclosed space, surrounding the inner chamber, to control the temperature of the suspending medium. A ring was fitted in the bottom of the vessel to hold one end of the sample in a fixed position. The other end of the sample was held by a clamp 1315
2 1316 ABUGROUN ET AL. SCHEMATIC DRAWING OF THE MYOTRON TO RECORDER ISOTONIC--. MYOGRAPH >» TRANSDUCER TO CIRCULATOR MUSCLE SAMPLE PARAFFIN OIL FULCRUM rrrrrrrrrrrrrrrrrr ' ' I ' I ' ' I I I I ' ADJUSTABLE TEMP. CIRCULATOR c IT DOUBLE /WALL GLASS CHAMBER FIG. 1. Schematic drawing of the Myotron (Forrest et al., 1969). "yrrrrrrrrrrvrrrrr i i i i i,i rrr i MYOGRAPH HEAD COUNTER BALANCE attached to the lever arm assembly (Fig. 1). The inner chamber of the vessel was large enough to completely surround the muscle sample with the paraffin oil. The chambers were clamped to a screw mechanism so that their position could be adjusted to accommodate individual samples. Transducers were also mounted on screws for position adjustment. An aluminum lever 30 cm in length was used to transmit the deformation of the muscle to the transducer. A counterbalance weight and the transducer were attached to the lever opposite the sample. The lever on the side of the sample traveled twice the distance of the lever on the side of the counterbalance weight and transducer. A digital temperature recorder was used to monitor the internal muscle sample temperature during heating. The probe was inserted lengthwise at the center of the muscle sample. An E and M isotonic motion myograph was used to detect length changes in the muscles.
3 HEAT SHORTENING OF PRERIGOR MUSCLE 1317 The changes were recorded with an E and M physiograph recorder. The counter balance weight was sufficient to maintain a constant 15 X g net force on the muscle sample and its movement was measured by the myograph motion-detecting head. Shortening of the muscle sample was calculated as shortening percentage based on the initial sample length between the two muscle clips (3 cm). Experiment 1. The heating rates used in this experiment were 2 C per 6 min, 2 C per 9 min, 2 C per 12 min, 2 C per 15 min, and 2 C per 18 min. Because it was possible only to conduct three treatments at one time, the 2 C per 12 min was always used to identify any significant variation caused by day of heating. The treatments were applied to the samples after a 10-min delay from slaughter to ensure that no shortening occurred as a result of sample excision and preparation. The heating was terminated when the internal muscle sample temperature reached 85 C. This final temperature was determined from preliminary experiments in which no contraction of significance had occurred beyond 85 C. Two shortening phases were observed; the first one was termed myofibrillar shortening, and the second one was termed cooking shortening (Davey and Gilbert, 1974, 1975a). Several variables were measured including internal sample temperature at onset and completion of myofibrillar shortening and at onset of cooking shortening. Also included were percent myofibrillar shortening, percent cooking shortening, and percent total shortening. Energy was calculated as cumulative heat absorption (cal/g) required to begin myofibrillar shortening, to complete myofibrillar shortening, and to begin cooking shortening using the following equation: where: Q=C p (Ti-T 0 ) Q. = heat in calories absorbed by the muscle sample (cumulative heat absorption in cal/g), Tj[ = mean temperature at onset of myofibrillar shortening, or mean temperature at completion of myofibrillar shortening, or mean temperature at onset of cooking shortening, T 0 = mean internal temperature of muscle sample at the beginning of heating, and Cp = heat capacity of beef lean meat between 32 and 212 F (.82 cal'g -1 c"'; Ordinanz, 1946). Experiment 2. In preliminary experiments, heating rates ranging from.2 C per 2 min to 2 C per 15 min were used. It was found that 2 C per 2 min or faster heating rates gave similar results, but those results differed from results obtained using heating rates slower than 2 C per 2 min. Based on results of Experiment 1 and the preliminary experiments, Experiment 2 was designed. Heating rates of 2 C per 2 min, 2 C per 12 min, and a control (samples left suspended in oil at 37 C until rigor mortis was complete) were utilized. The experiment was terminated immediately after myofibrillar shortening. Accordingly, only variables related to myofibrillar shortening were measured, including the duration, rate, and extent of myofibrillar shortening. Shortening rate was expressed as the reduction in the initial muscle sample length per unit of time, i.e., the decrease in length of muscle sample in millimeters as a result of myofibrillar shortening was described by the duration of myofibrillar shortening in minutes. The time in minutes from onset to completion of myofibrillar shortening was recorded and analyzed. The other procedures, including energy calculations, were performed as described in Experiment 1. Statistical Analyses. Statistical analyses were performed on all data using analysis of variance and Newman-Keul's sequential range test to separate significantly different means (Anderson and McLean, 1974). RESULTS Experiment 1. Muscle shortening percent was the same in all the treatments used (Table 1). The myofibrillar, cooking, and total shortening were not significantly different (P>.05), nor did the muscle samples shorten extensively, in these treatments. Likewise, the various heating rates did not result in significant differences in the muscle temperature at onset and completion of myofibrillar shortening or at onset of cooking shortening (P>.05; Table 1). In all muscle samples, myofibrillar shortening began at relatively low muscle temperatures (approximately 39 C) and was completed when the muscle temperature was 46 to 50 C. Cooking shortening began at 65 to 66 C.
4 1318 ABUGROUNETAL. TABLE 1. Means and standard errors for shortening, temperature, and heat absorption of chicken breast muscle at different heating rates (Experiment I) 1 Independent variable 2/6 Rate of heating, 2 C/min Group 1 2/9 2/12 2/12 Group 2 2/15 2/18 SE Muscle shortening, % 3 Myofibrillar Cooking Total Muscle temperature, C At onset of myofibrillar shortening At completion of myofibrillar shortening At onset of cooking shortening Cumulative heat absorption, 4 cal/g To beginning of myofibrillar shortening 8.0 To completion of myofibrillar shortening 17.1 To beginning of cooking shortening Means in the same row are not significantly different (P>.05). 2 n = 6. 3 Percent of initial length. 4 Heat absorbed from beginning of heat treatment. The cumulative heat (cal/g) absorbed by the muscle samples to onset of myofibrillar shortening, to completion of myofibrillar shortening, and to onset of cooking shortening was not significantly different among the treatments (P>.05; Table 1). Moreover, the results indicate no significant variation over time. Experiment 2. The duration of myofibrillar shortening was significantly different among the treatments (P<.01) with the 2 C per 2 min rate having the shortest duration. A significantly greater percent myofibrillar shortening was observed at the 2 C per 2 min heating rate compared with the 2 C per 12 min rate or the control (P<.01; Table 2). The 2 C per 12 min rate caused a greater percent shortening compared with the control, but the difference was not significant (P>.05). The rate of myofibrillar shortening was also significantly different among the treatments (P<.01). The 2 C per 2 min heating rate resulted in a faster rate of shortening compared with the 2 C per 12 min rate or the control. Significant differences were observed between the muscle temperatures at onset and completion of myofibrillar shortening (P<.01; Table 2). In comparison with the slow heating rate of 2 C per 12 min or the control, the rapid heating rate of 2 C per 2 min ± ± ± 1.1 ±.4 ± 1.0 ± resulted in both onset and completion of myofibrillar shortening at significantly higher temperatures. Muscles heated at 2 C per 2 min absorbed a significantly greater amount of heat to onset and to completion of myofibrillar shortening compared with muscles heated at 2 C per 12 min (P<.01; Table 2). DISCUSSION Muscle shortening data from Experiment 1 show that 20 to 30 min elapsed from the time the treatments were applied until the onset of myofibrillar shortening (Fig. 2). Considering the 10-min delay, it appears that heating the muscle even at the rate of 2 C per 6 min is low enough for biochemical changes to occur. A prerigor muscle usually undergoes a series of biochemical reactions because it sustains many of the functions of living tissue until the onset of rigor mortis. These biochemical reactions continue in heated muscle, and lactic acid is produced until protein (enzyme) denaturation occurs (Bate-Smith and Bendall, 1949; Marsh, 1954; Davey and Gilbert, 1975b; Hamm et al, 1980). Biochemical reactions are generally favored by warm temperatures, so one would expect acidification due to lactic acid produc-
5 HEAT SHORTENING OF PRERIGOR MUSCLE 1319 TABLE 2. Means and standard errors for myofibrillar shortening, temperature, and heat absorption of chicken breast muscle at different heating rates (Experiment 2) Rate of heating, 1 C/min Independent variable 2/2 2/12 Control 2 SE Myofibrillar shortening Duration, 3 min 6.0* 37.3Y Z ±9.9 Extent," % 48.0 X 25.4Y 12.17Y Rate, mm/min 2.62 x.21y.04 z ±.30 Muscle temperature, C At onset of myofibrillar shortening 47.3 X 42.5 V 38.l z ±.6 At completion of myofibrillar shortening 52.6 X 48.8Y 38.l z ±.30 Cumulative heat absorption, 5 cal/g To beginning of myofibrillar shortening 17.l x 12.6 V To completion of myofibrillar shortening 21.5 X 17.8 V... ±.5 '"' Means in the same row bearing different superscripts are significantly different (P<.01). 'n = 6. 2 Constant 37 C. 3 Onset to completion of shortening. 4 Percent initial length. 5 Heat absorbed from beginning of heat treatment. tion in slowly heated muscles. As a result of these changes, most of the adenosine triphosphate (ATP) supply in the muscles was depleted, and the muscles eventually went into rigor mortis (Bate-Smith and Bendall, 1949). The time spent by the slowly heated samples in the warm oil before shortening was probably sufficient to reduce the excitability of the muscles (Fig. 2). Such reduction in excitability can affect muscle contraction, because the extent of excitability decreases with increasing postmortem time (Locker and Hagyard, 1963). Also, inactivation of the contractile system would result in termination of myofibrillar shortening. The warm temperature for a relatively long time would coagulate a considerable amount of myosin and eliminate ATPase activity, which, in turn, would limit the extent of muscle contraction (Greenstein and Edsall, 1940; Locker, 1956; Nimitz and Partmann, 1959; Cheng and Parrish, 1979). Hamm and Deatherage (1960) found that coagulation of the myofibrillar proteins begins between 30 and 40 C and is nearly completed at 55 C. The cooking shortening is believed to be caused by the shrinkage of collagen. Davey and Gilbert (1974) reported that cooking toughness develops in two distinct stages, the second of which occurs between 65 and 75 C and is accompanied by muscle shortening as a result of the shrinkage of connective tissue. Muscle samples in Experiment 1 did not differ in the extent or in the onset temperature (Fig. 2) of cooking shortening, because they were prepared from the same muscle (Pectoralis major) and were probably similar in connective tissue. The birds used in this experiment were of the same age and breed and were obtained from the same pen. Judge and Aberle (1982) reported that TIME FROM BEGINNING OF HEATING (hr) FIG. 2. The effect of heating rate on temperature and time of chicken breast muscle shortening (Experiment 1).
6 1320 ABUGROUN ET AL. 2 C/I2min Onset of Myofibrillar Shortening Completion of Myofibrillar Shortening TIME FROM BEGINNING OF HEATING (hr) FIG. 3. The effect of heating rate on temperature and time of chicken breast muscle shortening (Experiment 2). collagen shrinkage temperature varies with time postmortem and the age of the animal. There was no significant difference in the amount of heat abosorbed per unit of muscle in Experiment 1. As calculated, the amount of heat was proportional to the change in temperature of the muscle, but its source could have been from the heating medium or from exothermic reactions within the muscle. Experiment 2 shows that, at the heating rate of 2 C per 2 min, the muscle samples required less than half the time required by the slowly heated (2 C per 12 min) muscle samples to begin myofibrillar shortening (Fig. 3). We hypothesize that, at the rapid heating rate of 2 C per 2 min, the muscle membranes became stimulated or lost their integrity at 47 C. This stimulation or loss of integrity caused the release of calcium from the sarcoplasmic reticulum, and when calcium concentration increased in the sarcoplasm, it resulted in an extensive, active contraction. This explanation is substantiated by the observation that shortening always began at 47 C and was completed within 6 min at 5 3 C. It has been reported that 70% of the protein in the sarcoplasmic reticulum is the heat-labile ATPase, which is involved in calcium transport in and out of the sarcoplasmic reticulum (Greaser, 1974). Accordingly, one would expect the sarcoplasmic reticulum to be affected by the high temperature of the rapid heating rate so as to release most of its calcium at one time. The consistent observations obtained with the rapid heating rate show that some event must have triggered the myofibrillar shortening. The most likely cause of this shortening is the release of calcium. The above hypothesis is further supported by the following facts: At an early postmortem time, the muscle membrane is responsive to heat stimuli (Hsieh et al, 1980). The mechanism of postmortem shortening is believed to be similar to that of muscular contraction in vivo (Newbold and Harris, 1972). The onset and extent of rigor shortening is faster and greater respectively as calcium ions in the medium increase (Mobley, 1977; Izumi et al, 1978). A rapid heating rate, unlike a slow heating rate, produces less lactic acid, and hence, less decline in ph because of the adverse balance between acceleration of glycolysis and heat denaturation of the enzymes (Dransfield and Rhodes, 1975). Intensity of rigor tension decreases with decreasing ph (Izumi et al, 1978). Muscle heated at 2 C per 2 min absorbed a significantly greater amount of heat to onset and to completion of myofibrillar shortening, compared with muscle heated at 2 C per 12 min. Those differences are consistent with the contention that shortening is caused by different factors during slow and rapid heating i.e., ATPase depletion (slow heating) and calcium release (rapid heating). It is possible that the rapidly heated muscles did not absorb greater quantities of heat from the heating medium at onset and completion of shortening but, rather, produced their own heat by the exothermic reactions known to occur in rapidly heated prerigor muscle (Hamm et al, 1980). The results of the rapid-heating rate (2 C per 2 min) are in agreement with the findings of Whiting and Richard (1975). These authors cooked strips of prerigor chicken muscle using 80 C water and used a physiograph to monitor muscle shortening. They reported an extensive shortening of 47% that occurred at 30 min postmortem. They also observed two isometric tension peaks, the first of which occurred between 45 and 55 C but did not occur when aged muscle was used. From these experiments, it appears that postmortem shortening cannot be arrested, but its extent can be maximized or minimized depending on the heating rate applied. At high
7 HEAT SHORTENING OF PRERIGOR MUSCLE 1321 rates of heating (>2 C per 2 min), the heat may act as a stimulus to release calcium and elicit an extensive contraction. REFERENCES Anderson, V. L., and R. A. McLean, Design of Experiments. Marcel Dekker, Inc., New York, NY. Bate-Smith, E. C, and J. R. Bendall, Factors determining the time course of rigor mortis. J. Physiol. 110: Behnke, J. R., O. Fennema, and R. W. Halker, Quality changes in prerigor poultry at 3 C. J. FoodSci. 38: Cheng, C. S., and F. C. Parrish, Jr., Heat induced changes in myofibrillar proteins of bovine longissimus muscle. J. Food Sci. 44: Cia, G., and B. B. Marsh, Properties of beef cooked before rigor onset. J. Food Sci. 41: Davey, C. L., and K. V. Gilbert, Temperature dependent cooking toughness in beef muscle. J. Sci. Food Agric. 25: Davey, C. L., and K. V. Gilbert, 1975a. Cooking shortening and the toughening of beef. J. Food Technol. 10: Davey, C. L., and K. V. Gilbert, 1975b. Cold shortening and cooking changes in beef. J. Sci. Food Agric. 26: Dransfield, E., and D. N. Rhodes, Texture of beef M semitendinosus heated before, during and after development of rigor mortis. J. Sci. Food Agric. 26: Forrest, J. C, C. G. Haugh, and C. E. Allen, The myotron: An instrument for the study of physical properties of muscle under controlled conditions. Proc. Am. Soc. Agric. Eng., Chicago, IL, Paper No Greaser, M. L., Sarcoplasmic reticulum and its possible role in postmortem muscle. Pages in 27th Annu. Reciprocal Meat Conf. Am. Meat Sci. Assoc. Texas A & M Univ., College Station, TX. Greenstein, J. P., and J. Edsall, The effect of denaturing agents on myosin. 1. Sulfhydryl groups as estimated by porphyrindin titration. J. Biol. Chem. 133: Hamm, R., and F. E. Deatherage, Changes in hydration, solubility and charges of muscle proteins during heating of meat. Food Res. 25:587. Hamm, R., K. O. Honikel, A. Hamid, and C. Fischer, The influence of postmortem changes in bovine muscle on the water holding capacity of beef. 1. Postmortem storage of muscle at 20 C. Pages in Proc. 26th Eur. Mtg. Meat Res. Workers. Colorado Springs, CO. Herring, H. K., R. G. Cassens, and E. J. Briskey, Further studies on bovine muscle tenderness as influenced by carcass position, sarcomere length and fiber diameter. J. Food Sci. 30: Herring, H. K., R. G. Cassens, G. G. Suess, V. H. Brungardt, and E. J. Briskey, Tenderness and associated characteristics of stretched and contracted bovine muscles. J. Food Sci. 32: Hsieh, Y.P.C., D. P. Cornforth, and A. M. Pearson, Ultrastructural changes in pre- and postrigor beef muscle caused by conventional and microwave cookery. Meat Sci. 4: Izumi, K., T. Ito, and T. Fukazawa, Effects of ph, calcium ions and ATP on rigor contraction in glycerinated rabbit psoas muscle fibre. J. Food Sci. 43: Judge, M. D., and E. D. Aberle, Effects of choronological age and postmortem aging on thermal shrinkage temperature of bovine intramuscular collagen. J. Anim. Sci. 54: Locker, R. H., The dissociation of myosin by heat coagulation. Biochim. Biophys. Acta 20: Locker, R. H., Degree of muscular contraction as a factor in tenderness of beef. Food Res. 25: Locker, R. H., and C. J. Hagyard, A cold shortening effect in beef muscles. J. Sci. Food Agric. 14:787. Marsh, B. B., Rigor-mortis in beef. J. Sci. Food Agric. 5: Marsh, B. B., Temperature and post-mortem change. Energy use and meat quality. Pages in Proc. Meat Ind. Res. Conf. Am. Meat Inst. Found. Chicago, IL. Marsh, B. B., and W. A. Carse, Meat tenderness and sliding filament hypothesis. J. Food Technol. 9: Marsh, B. B., and N. G. Leet, Studies in meat tenderness. III. The effects of cold shortening on tenderness. J. Food Sci. 31: Mobley, B. A., Effect of calcium ions on rigor contraction in skinned frog muscle fibers. Biochim. Biophys. Acta 459: Newbold, R. P., and P. V. Harris, The effect of pre-rigor changes on meat tenderness. A review. J. Food Sci. 37: Nimitz, G., and W. Partmann, Uber die Hitzeinaktiviering des apyrase systems der Muskulatur. Z. Lebensm. Unters. Forsch. 109:121. Ordinanz, W. O., Specific heat of foods in cooking. Food Industry 18:1869. Whiting, R. C, and J. F. Richard, Thermally induced isometric tension and shortening of pre and postrigor chicken muscle. Can. Inst. Food Sci. Technol. J. 8(3): 168.
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