- Email: [email protected]
The effect of seasonal heat stress on rigor development and the incidence of pale, exudative turkey meat
The Effect of Seasonal Heat Stress on Rigor Development and the Incidence of Pale, Exudative Turkey Meat S. R. MCKEE and A. R. SAMS1 Department of Poultry Science, Texas A&M University System, College Station, Texas 77843-2472 remaining intact Pectoralis muscle was harvested, aged on ice for 23 h, and analyzed for drip loss and cook loss. Percentage mortality and carcass weights were not significantly different between treatments. By 15 min post-mortem, the HS birds exhibited a faster pH decline and had higher R-values that persisted through 24 h. The HS birds were also paler in color and exhibited increased drip loss and cook loss when compared to controls; however, expressible moisture was not different between treatments. In addition, the HS birds had a higher frequency of abnormal birds than controls when birds were grouped as normal (L* < 53) or abnormal (L* > 53).
(Key words: heat stress, turkey meat, pale soft exudative meat, rigor mortis development) 1997 Poultry Science 76:1616–1620
INTRODUCTION During the early summer season, the turkey industry reports substantial losses in yield due to formed turkey breast products with poor water-holding capacity, poor texture, and pale color. These meat characteristics are consistent with those observed in pale, soft, and exudative (PSE) pork. In pork, genetic selection for heavier, leaner muscling has resulted in animals that are genetically susceptible to various ante-mortem and postmortem stressors, which induce physiological and biochemical changes in the muscle that result in the development of PSE meat characteristics (Cassens et al., 1975). More specifically, Briskey (1964) postulated that the low pH resulting from rapid metabolism early (prior to chilling) post-mortem when combined with high carcass temperatures caused extensive protein denaturation in the muscle. The loss of protein functionality due to extensive protein denaturation is considered to be the primary factor associated with the development of PSE meat characteristics (Warris and Brown 1987; Fernandez et al., 1994; Santos et al., 1994). Heat stress has long been recognized as one of the prominent environmental elements influencing meat
Received for publication December 9, 1996. Accepted for publication June 22, 1997. 1To whom correspondence should be addressed.
quality (Thomas et al., 1966; Howe et al., 1968; Aberle et al., 1969; Wood and Richards, 1975; Northcutt et al., 1994). Many studies have focused on resulting meat quality from heat stress applications just prior to slaughter. Sayre et al. (1963) reported stress-susceptible pigs that were subjected to heat stress (42 to 45 C for 20 to 60 min) prior to slaughter developed PSE meat characteristics. Northcutt et al. (1994) found that chickens that were subjected to heat (40 to 41 C for 1 h) and preconditioned (3 d at 35 to 36 C for 3 h) exhibited PSE meat characteristics. However, Northcutt (1994) found that turkeys subjected to 30 C for 1 h had lower initial pH after slaughter than controls, but they did not differ in lightness or water-holding capacity from the controls. In addition, Froning et al. (1978) found that turkeys exposed to immediate preslaughter heat stress did not exhibit PSE meat characteristics. Researchers have not studied the effect of a sustained seasonal heat stress on turkey meat quality and the development of PSE meat characteristics; however, industry reports of PSE turkey meat increase in early summer with the onset of prolonged high temperatures. In addition, Santos et al. (1994) stated that the percentage of PSE pork carcasses doubles during the summer months and attributes this to higher environmental temperatures and relative humidity. Therefore, the objective of this study was to evaluate meat characteristics of turkeys that had been subjected to a sustained,
1616
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
ABSTRACT Heat stress is one of the prominent antemortem stressors that elicits pale, soft, and exudative meat characteristics in stress-susceptible pigs. Industry reports of exudative turkey meat increase in the early summer with the onset of prolonged high temperatures. To study the effect of seasonal heat exposure on turkeys, 122 17-wk-old Nicholas tom turkeys were subjected in January either to growth temperatures of 16/24 C (night/day) (control) or to elevated temperatures of 32/ 38 C (night/day) (heat-stressed, HS). Turkeys were processed at 21 wk of age in a manner simulating commercial conditions. Pectoralis muscle samples were taken at 15 min (prechill), 2 h (postchill), and 24 h and analyzed for R-value, pH, and color. At 2 h, the
SEASONAL HEAT STRESS AND RIGOR MORTIS DEVELOPMENT IN TURKEYS
seasonal heat stress that was modeled after the normal temperature changes observed in the climate of the southern U.S. during the transition from spring to summer. The reports of turkey PSE meat diminish during the latter part of the summer as birds have become acclimated to the heat and are smaller in body size. Therefore, the timing of this heat application during the growth cycle was important, because it appears that heavier body weight is a factor in the way growing strains of birds respond to environmental heat stress (Bohren et al., 1982).
MATERIALS AND METHODS
2Model SS-36-SS, Brower Corp., Houghton, IA 52631. 3Model SP3055, Brower Corp., Houghton, IA 52631. 4Minolta Chroma Meter Model CR-200, Minolta Corp., Ramsay,
NJ 07446. 5Binder clips, Acco USA Inc., Wheeling, IL 60090-6070. 6Blodggett Zepharie G-1 speed, Blodggett Oven Co., Burlington, VT 05402.
fluctuation in humidity from night to day and from day to day than between the heat stress and control environments. Furthermore, Reece et al. (1972) reported that birds that had been acclimated to heat stress were not affected by relative humidity. Mortality was monitored and recorded twice daily. At 21 wk of age (after 4 wk in the temperature environments), the turkeys in the three replicated groups were processed on 3 separate processing d with a total of 41, 44, and 37 turkeys being killed on Days 1, 2, and 3, respectively. Following a 12-h period of feed withdrawal on each processing day, turkeys were hung on shackles and killed by bleeding for 90 s from a single neck cut severing the right carotid artery and jugular vein. Birds were not electrically stunned prior to exsanguination because this type of stunning has been reported to retard rigor mortis development, and this study required rigor to develop without any conflicting factors (Papinaho and Fletcher, 1995). After bleeding, birds were subscalded2 at 63 C for 45 s, defeathered in a rotary drum3 picker for 35 s, and manually eviscerated. At 15 min post-mortem, birds were weighed and banded and tissue samples were taken for biochemical analyses. A lengthwise incision was made in the skin covering the right breast muscle in preparation for sampling. Muscle tissue samples were cut (20 × 80 × 30 mm) parallel to the muscle fiber from the right Pectoralis of each carcass at 15 min (prechill), 2 h (postchill), and 24 h post-mortem. Pectoralis muscle samples were cut at least 30 mm apart from the previous sample area. Muscle samples for biochemical analyses were placed in labeled plastic bags, placed directly into liquid nitrogen, and stored at –75 C until analyzed (< 1 mo). Pectoralis muscle samples for determination of expressible moisture were placed in a plastic bag, aged on ice until 24 h post-mortem, and then analyzed using the press method described by Urbin et al. (1962). Immediately after the samples were removed, lightness (L*value) was evaluated4 in triplicate on the cut surface of the remaining breast muscle. Location of sampling in the Pectoralis muscle was randomized between carcasses and sampling times to account for any variation within the muscle. Carcasses were placed in a manually agitated tap water-ice slush after the 15 min sampling period. The skin covering the breast was clamped5 after sampling to minimize water contact with the muscle. After sampling at 2 h post-mortem for biochemical analyses, both breast muscles were removed. The left, undisturbed breast muscle was weighed and both the left and right breast muscles were placed into 8.46 L zip seal, perforatedplastic bags and then stored on ice for an additional 22 h. Following the 22 h storage, right fillets were sampled for biochemical analyses and left fillets were reweighed in order to determine drip loss. Left fillets were baked on racks in foil covered aluminum pans in an air convection oven6 at 177 C to an internal temperature of 76 C. Cooked fillets were reweighed for cook loss determination. Tissue samples at 15 min, 2 h, and 24 h post-mortem were used for the measurement of R-value and pH. The
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
A total of 132 Nicholas toms (12 wk of age) were obtained from a commercial grower. Birds were transported (< 160 km) to the Texas A&M University Poultry Research Center, where they were equally divided into three replicate groups. The turkeys were housed in litter-covered floor pens and consumed a commercial ration (20% crude protein and 3,080 kcal ME/kg) ad libitum. The birds were provided a 5-wk period to acclimate to their new housing and recover from transportation. At 17 wk of age, the birds in each replicate were divided into equal groups and placed into either an environment that simulated seasonal heat exposure or a control environment (day/night temperature 24/16 C). These environments were created by partitioning the birds into separate growing areas having 12 3.05 × 1.83 m pens in each section with each area having its own heating controls and windows for exposure to the natural outside environment. The heatstressed birds were exposed to increasing environmental temperatures over a 3-d period to a final day/night temperature of 38/32 C. To produce a stressfully hot environment for the heat-stressed birds, as well as to avoid a cold-stress environment for the control birds (the study began in January), supplemental heating from a forced air natural gas heaters (47,445 kJ) was provided as needed to achieve and maintain the desired temperatures. Additional gas heaters were positioned throughout the elevated-temperature environment. Ceiling fans were positioned between pens to circulate air and minimize temperature differences within and between pens. To regulate the heat, temperature was monitored and recorded twice daily at the level of the birds’ head in the center of each growing area. Relative humidity was also monitored and recorded twice daily; however, no attempt was made to regulate or equalize humidity. It was determined that there was a much greater
1617
1618
MCKEE AND SAMS
RESULTS AND DISCUSSION There was no difference in mortality (7.14% for heat stressed vs 4.29% for controls) or carcass weights (13.06 kg for heat-stressed vs 16.27 kg for controls) between the two treatment groups. Heat stress has been associated with increased mortality (Phelps, 1990); however, the birds in the current study were acclimated to the elevated temperatures over a 3-d period. Acclimation has been previously shown to reduce mortality related to heat stress (Reece et al., 1972). Although bird weight was not affected by the applied heat stress in the current study, chronic heat stress has been shown to result in a 20% reduction in growth rate in fast-growing strains of poultry (Bohren et al., 1981). Bohren et al. (1982) reported that although preconditioning or acclimation increased the survival rate of fast-growing strains of heat stressed poultry, it did not improve growth performance. The R-value is an indirect measure of ATP depletion in the muscle. During rigor mortis development, ATP in the muscle is depleted and R-value increases (Calkins et al., 1982). The R-value data presented in Figure 1 indicate that by 15 min post-mortem, the heat-stressed birds had significantly higher R-values than controls; this trend persisted through 24 h post-mortem. These results indicated that the seasonal heat stress application accelerated ATP depletion, thereby hastening the onset of rigor mortis. Moreover, Pietrzak et al. (1994) reported that turkeys characterized as PSE due to rapid postmortem metabolism, pale color, and poor water-holding capacity exhibited lower ATP levels by 20 min postmortem than the group with slower post-mortem metabolism. The effects of seasonal heat stress on post-mortem pH decline are shown in Figure 2. The decline in pH is a
FIGURE 1. The effect of seasonal heat stress on R-values (ratio of Abs260:Abs250) in turkey Pectoralis. Means (n = 61 per mean) within level of post-mortem time with different superscripts are significantly different (P < 0.05).
result of the breakdown of glycogen to lactic acid during post-mortem glycolysis, thereby resulting in the accumulation of lactic acid in the muscle (Lawrie, 1991). Results in Figure 2 illustrate that as early as 15 min postmortem, the heat-stressed birds exhibit a significantly lower pH than the controls. The accelerated pH decline in the heat stress birds persisted through 24 h postmortem. Ma and Addis (1973) and Vanderstoep and Richards (1974) have demonstrated that maximum differences in post-mortem pH decline between fast and slow glycolyzing turkeys occurred within 1 h postmortem, decreasing thereafter during post-mortem aging. Although the current study did not measure the pH
FIGURE 2. The effect of seasonal heat stress on pH decline in turkey Pectoralis. Means (n = 61 per mean) within level of post-mortem time with different superscripts are significantly different (P < 0.05).
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
R-value, the ratio of inosine to adenosine, is an indication of adenosine triphosphate (ATP) depletion in the muscle and was determined using the method described by Thompson et al. (1987). The post-mortem pH of samples was determined using the iodoacetate method described by Sams and Janky (1986). Mortality and carcass weight data was subjected to chi-square analysis. The rest of the data were classed by treatment and replication and the remaining parameters were subjected to ANOVA using the General Linear Models procedure (SAS Institute, 1985). Because no interaction was detected between treatment and replication, the data from all replicates were pooled into a completely randomized block design with post-mortem time as the blocking factor. The residual mean square was used as the error term and treatment means were compared utilizing the F test (SAS Institute, 1985). Frequencies of abnormal (L* value > 53) and normal (L* value < 53) birds in each treatment were subjected to chi-square analysis. Significance for all data was determined using P < 0.05.
1619
SEASONAL HEAT STRESS AND RIGOR MORTIS DEVELOPMENT IN TURKEYS
was selected to be more conservative than the L*value criteria used by Barbut (1993) in identifying abnormally pale meat. This result suggests that the heat may have caused sufficient stress to trigger the development of the PSE-like condition in the muscle. Ante-mortem stressors such as mixing, breeding, and heat have previously been reported to trigger the PSE condition in swine (Louis et al., 1993). Data in Table 1 indicates the extent to which heat stress influenced drip loss, cook loss, expressible moisture of turkey breast fillets. Heat stress significantly increased drip loss and cook loss but appeared to have no effect on expressible moisture. The increased drip loss and cook loss were expected because they are directly associated with protein functionality in the muscle. Santos et al. (1994) postulated that the early development of rigor mortis in PSE pork meat combined with high carcass temperatures caused the denaturation of muscle sarcoplasmic and contractile proteins, which resulted in meat with poor water-holding capacity, which was reflected by higher drip loss and cooking losses. Moreover, Warris and Brown (1987) found that the early post-mortem pH decline from 30 min to 1 h was determined to be the most important factor in determining the degree of protein denaturation and resulting exudate in meat. However, the fact that there was no difference in expressible moisture between treatments was not expected because changes in expressible moisture usually follow a similar trend to changes observed in drip loss and cook loss. In this study, samples for expressible moisture were collected and analyzed at 24 h post-mortem possibly after much of the expressible moisture had been lost to drip. Earlier (15 min and 2 h) samples may have been more meaningful in determining changes in expressible moisture between treatments over time. In conclusion, the current study suggested that the seasonal heat stress accelerated post-mortem metabolism and biochemical changes in the muscle, which produced pale, exudative meat characteristics in tom turkeys.
ACKNOWLEDGMENTS The authors gratefully acknowledge the donation of the turkeys used in this study by Plantation Foods of Waco, TX 76705.
TABLE 1. The effect of seasonal heat stress on drip loss, cook loss, and expressible moisture in turkey Pectoralis
FIGURE 3. The effect of seasonal heat stress on L* value in turkey Pectoralis. Means (n = 61 per mean) within level of post-mortem time with different superscripts are significantly different (P < 0.05).
Environmental treatments
Parameters
Pooled SEM
Heat-stressed Control
Drip loss, % Cook loss, % Expressible moisture, %
0.08 0.51 0.62
0.44a 24.56a 22.02
0.06b 19.08b 25.23
a,bMeans (n = 61 per mean) within each row with no common superscript differ significantly (P < 0.05).
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
at 1 h post-mortem, overall pH decline did follow a similar trend to that observed by Ma and Addis (1973) and Vanderstoep and Richards (1974). Specifically, maximum pH differences between heat-stressed and control birds were observed as early as 15 min postmortem and persisted through 2 h post-mortem, after which the differences in pH began to decrease. The results from the current study indicate that the turkeys exposed to seasonal heat stress exhibited accelerated post-mortem glycolysis compared to the birds raised in the control environment. It is the rapid decline in pH early post-mortem, while carcass temperatures are still high, that can result in extensive protein denaturation, which affects the color and water-holding capacity of the meat (Warris and Brown, 1987). Accelerated rigor mortis development occurring with poor water-holding capacity and light color is indicative of PSE meat (Cassens et al., 1975; Fox et al., 1980; Warris and Brown, 1987). Lawrie (1991) attributed the pale color meat to the denaturation of sarcoplasmic proteins, which causes increased light scattering in the muscle. The lightness (as indicated by L*values) of turkey breast fillets of both heat-stressed and control birds are illustrated in Figure 3. At 15 min, 2 h, and 24 h, heatstressed birds exhibited greater L*values than the controls. These results agree with those of Barbut (1993) and Pietrzak et al. (1994), who reported that turkeys exhibiting a rapid pH decline had significantly higher L* values than the slower glycolyzing group. In addition, van Hoof (1979) reported that the pale color in poultry meat is associated with low pH and concluded that poultry is susceptible to a PSE condition similar to that previously described in pork. In the current study, the heat stress treatment significantly (P < 0.01) increased the percentage of birds that would be classified as PSElike (36.9 vs 10.5%) according to the criterion of 24 h L*values greater than 53 being PSE-like. This criterion
1620
MCKEE AND SAMS
REFERENCES
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
Aberle, E. D., N. W. Thomas, J. M. Howe, and P. T. Arroyo, 1969. Environmental influence on high energy phosphate metabolites in porcine muscles. J. Food Sci. 34:600–603. Barbut, S., 1993. Colour measurements for evaluating the pale soft exudative (PSE) occurrence in turkey meat. Food Res. Int. 26:39–43. Bohren, B. B., J. R. Carson, and J. C. Rogler, 1981. Response to selection in two temperatures for fast and slow growth to nine weeks of age. Genetics 97:443–450. Bohren, B. B., J. C. Rogler, and J. R. Carson, 1982. Survival under heat stress of lines selected for fast and slow growth at two temperatures. Poultry Sci. 61:1804–1808. Briskey, E. J., 1964. Etiological status and associated studies of pale, soft, exudative porcine musculature. Adv. Food Res. 13:89–105. Calkins, C. R., T. R. Dutson, G. C. Smith, and Z. L. Carpenter, 1982. Concentrations of creatine phosphate, adenine nucleotides and their derivatives in electrically stimulated and nonstimulated beef muscle. J. Food Sci. 47:1350–1353. Cassens, R. G., D. N. Marple, and G. Eikelenboom, 1975. Animal physiology and meat quality. Adv. Food Res. 21: 71–155. Fernandez, X., A. Forslid, and E. Tornberg, 1994. The effect of high post-mortem temperature on the development of pale, soft and exudative pork: Interaction with ultimate pH. Meat Sci. 37:133–147. Froning, G. W., A. S. Babji, and F. B. Mather, 1978. The effect of preslaughter temperature, stress struggle anesthetization on color and textural characteristics of turkey muscle. Poultry Sci. 57:630–633. Fox, J. D., S. A. Wolffram, J. D. Kemp, and B. E. Langlois, 1980. Physical, chemical, sensory, and microbiological properties and shelf life of PSE and normal pork chops. J. Food Sci. 45:786–790. Howe, J. M., N. W. Thomas, P. B. Addis, and M. D. Judge, 1968. Temperature acclimation and its effects on porcine muscle properties in two humidity environments. J. Food Sci. 33:235–238. Lawrie, R. A., 1991. Pages 56–60, 188, and 206 in: Meat Science. 5th ed. Pergamon Press, New York, NY. Louis, F., W. E. Rempel, and J. R. Mickelson, 1993. Porcine stress syndrome: Biochemical and genetic basis of this inherited syndrome of skeletal muscle. Pages 89–95 in: Proceedings from the Reciprocal Meat Conference. Vol. 46. National Meat and Livestock Board, Chicago, IL. Ma, R. T.-I., and P. B. Addis, 1973. The association of struggle during exsanguination to glycolysis, protein solubility, and shear in turkey pectoralis muscle. J. Food Sci. 38: 995–997.
Northcutt, J. K., 1994. Influence of antemortem treatment on postmortem muscle properties of poultry meat. Ph.D. dissertation, North Carolina State University, Raleigh NC. Northcutt, J. K., E. A. Foegeding, and F. W. Edens, 1994. Water-holding properties of thermally preconditioned chicken breast and leg meat. Poultry Sci. 73:308–316. Papinaho, P. A., and D. L. Fletcher, 1995. Effects of electrical stunning duration on postmortem rigor development and broiler breast meat tenderness. J. Muscle Foods 6:1–8. Phelps, A., 1990. Improved bird performance possible at high temperatures. Feedstuffs 62:12, 17. Pietrzak, M., M. L. Greaser, and A. A. Sosniki, 1994. Effect of rapid onset of rigor mortis on protein functionality in turkey breast muscle. Poultry Sci. 73(Suppl. 1):194. (Abstr.) Reece, F. N., J. W. Deaton, and L. F. Kubena, 1972. Effects of high temperature and humidity on heat prostration of broiler chickens. Poultry Sci. 51:2021–2025. Sams, A. R., and D. M. Janky, 1986. The influence of brine chilling on tenderness of hot boned chill-boned and ageboned broiler fillets. Poultry Sci. 65:1316–1321. Santos C., L. C. Roserio, H. Goncalves, and R. S. Melo, 1994. Incidence of different pork quality categories in a Portuguese slaughterhouse: A survey. Meat Sci. 38: 279–287. SAS Institute, 1985. SAS/STAT Guide for Personal Computers. Version 6th Edition. SAS Institute Inc., Cary, NC. Sayre, R. N., E. J. Briskey, and W. G. Hoekstra, 1963. Alteration of postmortem changes in porcine muscle by preslaughter heat treatment and diet modification. J. Food Sci. 28: 292–297. Thomas, N. W., P. B. Addis, H. R. Hohnson, R. D. Howard, and M. D. Judge, 1966. Effects of environmental temperature and humidity during growth on muscle properties of two porcine breeds. J. Food Sci. 31:309–312. Thompson, L. D., M. D. Janky, and S. A. Woodward, 1987. Tenderness and physical characteristics of broiler breast fillets harvested at various times from post-mortem electrically stimulated carcasses. Poultry Sci. 66:1158–1167. Urbin M. C., D. A. Zessin, and G. D. Wilson, 1962. Observation on a method of determining water-binding properties of meat. J. Anim. Sci. 21:9. Vanderstoep, J., and J. F. Richards, 1974. Post-mortem glycolytic and physical changes in turkey breast meat. Can. Inst. Food Sci. Technol. J. 7:120–124. van Hoof, J., 1979. Influence of ante- and peri-mortem factors on biochemical and physical characteristics of turkey breast muscle. Vet. Q. 1:29–36. Warris, P. D., and S. N. Brown, 1987. The relationship between initial pH, reflectance and exudation in pig muscle. Meat Sci. 20:65–72. Wood, D. G., and J. F. Richards, 1975. Effect of some antemortem stressors on post-mortem aspects of chicken broiler pectoralis muscle. Poultry Sci. 54:528–531.
(Key words: heat stress, turkey meat, pale soft exudative meat, rigor mortis development) 1997 Poultry Science 76:1616–1620
INTRODUCTION During the early summer season, the turkey industry reports substantial losses in yield due to formed turkey breast products with poor water-holding capacity, poor texture, and pale color. These meat characteristics are consistent with those observed in pale, soft, and exudative (PSE) pork. In pork, genetic selection for heavier, leaner muscling has resulted in animals that are genetically susceptible to various ante-mortem and postmortem stressors, which induce physiological and biochemical changes in the muscle that result in the development of PSE meat characteristics (Cassens et al., 1975). More specifically, Briskey (1964) postulated that the low pH resulting from rapid metabolism early (prior to chilling) post-mortem when combined with high carcass temperatures caused extensive protein denaturation in the muscle. The loss of protein functionality due to extensive protein denaturation is considered to be the primary factor associated with the development of PSE meat characteristics (Warris and Brown 1987; Fernandez et al., 1994; Santos et al., 1994). Heat stress has long been recognized as one of the prominent environmental elements influencing meat
Received for publication December 9, 1996. Accepted for publication June 22, 1997. 1To whom correspondence should be addressed.
quality (Thomas et al., 1966; Howe et al., 1968; Aberle et al., 1969; Wood and Richards, 1975; Northcutt et al., 1994). Many studies have focused on resulting meat quality from heat stress applications just prior to slaughter. Sayre et al. (1963) reported stress-susceptible pigs that were subjected to heat stress (42 to 45 C for 20 to 60 min) prior to slaughter developed PSE meat characteristics. Northcutt et al. (1994) found that chickens that were subjected to heat (40 to 41 C for 1 h) and preconditioned (3 d at 35 to 36 C for 3 h) exhibited PSE meat characteristics. However, Northcutt (1994) found that turkeys subjected to 30 C for 1 h had lower initial pH after slaughter than controls, but they did not differ in lightness or water-holding capacity from the controls. In addition, Froning et al. (1978) found that turkeys exposed to immediate preslaughter heat stress did not exhibit PSE meat characteristics. Researchers have not studied the effect of a sustained seasonal heat stress on turkey meat quality and the development of PSE meat characteristics; however, industry reports of PSE turkey meat increase in early summer with the onset of prolonged high temperatures. In addition, Santos et al. (1994) stated that the percentage of PSE pork carcasses doubles during the summer months and attributes this to higher environmental temperatures and relative humidity. Therefore, the objective of this study was to evaluate meat characteristics of turkeys that had been subjected to a sustained,
1616
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
ABSTRACT Heat stress is one of the prominent antemortem stressors that elicits pale, soft, and exudative meat characteristics in stress-susceptible pigs. Industry reports of exudative turkey meat increase in the early summer with the onset of prolonged high temperatures. To study the effect of seasonal heat exposure on turkeys, 122 17-wk-old Nicholas tom turkeys were subjected in January either to growth temperatures of 16/24 C (night/day) (control) or to elevated temperatures of 32/ 38 C (night/day) (heat-stressed, HS). Turkeys were processed at 21 wk of age in a manner simulating commercial conditions. Pectoralis muscle samples were taken at 15 min (prechill), 2 h (postchill), and 24 h and analyzed for R-value, pH, and color. At 2 h, the
SEASONAL HEAT STRESS AND RIGOR MORTIS DEVELOPMENT IN TURKEYS
seasonal heat stress that was modeled after the normal temperature changes observed in the climate of the southern U.S. during the transition from spring to summer. The reports of turkey PSE meat diminish during the latter part of the summer as birds have become acclimated to the heat and are smaller in body size. Therefore, the timing of this heat application during the growth cycle was important, because it appears that heavier body weight is a factor in the way growing strains of birds respond to environmental heat stress (Bohren et al., 1982).
MATERIALS AND METHODS
2Model SS-36-SS, Brower Corp., Houghton, IA 52631. 3Model SP3055, Brower Corp., Houghton, IA 52631. 4Minolta Chroma Meter Model CR-200, Minolta Corp., Ramsay,
NJ 07446. 5Binder clips, Acco USA Inc., Wheeling, IL 60090-6070. 6Blodggett Zepharie G-1 speed, Blodggett Oven Co., Burlington, VT 05402.
fluctuation in humidity from night to day and from day to day than between the heat stress and control environments. Furthermore, Reece et al. (1972) reported that birds that had been acclimated to heat stress were not affected by relative humidity. Mortality was monitored and recorded twice daily. At 21 wk of age (after 4 wk in the temperature environments), the turkeys in the three replicated groups were processed on 3 separate processing d with a total of 41, 44, and 37 turkeys being killed on Days 1, 2, and 3, respectively. Following a 12-h period of feed withdrawal on each processing day, turkeys were hung on shackles and killed by bleeding for 90 s from a single neck cut severing the right carotid artery and jugular vein. Birds were not electrically stunned prior to exsanguination because this type of stunning has been reported to retard rigor mortis development, and this study required rigor to develop without any conflicting factors (Papinaho and Fletcher, 1995). After bleeding, birds were subscalded2 at 63 C for 45 s, defeathered in a rotary drum3 picker for 35 s, and manually eviscerated. At 15 min post-mortem, birds were weighed and banded and tissue samples were taken for biochemical analyses. A lengthwise incision was made in the skin covering the right breast muscle in preparation for sampling. Muscle tissue samples were cut (20 × 80 × 30 mm) parallel to the muscle fiber from the right Pectoralis of each carcass at 15 min (prechill), 2 h (postchill), and 24 h post-mortem. Pectoralis muscle samples were cut at least 30 mm apart from the previous sample area. Muscle samples for biochemical analyses were placed in labeled plastic bags, placed directly into liquid nitrogen, and stored at –75 C until analyzed (< 1 mo). Pectoralis muscle samples for determination of expressible moisture were placed in a plastic bag, aged on ice until 24 h post-mortem, and then analyzed using the press method described by Urbin et al. (1962). Immediately after the samples were removed, lightness (L*value) was evaluated4 in triplicate on the cut surface of the remaining breast muscle. Location of sampling in the Pectoralis muscle was randomized between carcasses and sampling times to account for any variation within the muscle. Carcasses were placed in a manually agitated tap water-ice slush after the 15 min sampling period. The skin covering the breast was clamped5 after sampling to minimize water contact with the muscle. After sampling at 2 h post-mortem for biochemical analyses, both breast muscles were removed. The left, undisturbed breast muscle was weighed and both the left and right breast muscles were placed into 8.46 L zip seal, perforatedplastic bags and then stored on ice for an additional 22 h. Following the 22 h storage, right fillets were sampled for biochemical analyses and left fillets were reweighed in order to determine drip loss. Left fillets were baked on racks in foil covered aluminum pans in an air convection oven6 at 177 C to an internal temperature of 76 C. Cooked fillets were reweighed for cook loss determination. Tissue samples at 15 min, 2 h, and 24 h post-mortem were used for the measurement of R-value and pH. The
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
A total of 132 Nicholas toms (12 wk of age) were obtained from a commercial grower. Birds were transported (< 160 km) to the Texas A&M University Poultry Research Center, where they were equally divided into three replicate groups. The turkeys were housed in litter-covered floor pens and consumed a commercial ration (20% crude protein and 3,080 kcal ME/kg) ad libitum. The birds were provided a 5-wk period to acclimate to their new housing and recover from transportation. At 17 wk of age, the birds in each replicate were divided into equal groups and placed into either an environment that simulated seasonal heat exposure or a control environment (day/night temperature 24/16 C). These environments were created by partitioning the birds into separate growing areas having 12 3.05 × 1.83 m pens in each section with each area having its own heating controls and windows for exposure to the natural outside environment. The heatstressed birds were exposed to increasing environmental temperatures over a 3-d period to a final day/night temperature of 38/32 C. To produce a stressfully hot environment for the heat-stressed birds, as well as to avoid a cold-stress environment for the control birds (the study began in January), supplemental heating from a forced air natural gas heaters (47,445 kJ) was provided as needed to achieve and maintain the desired temperatures. Additional gas heaters were positioned throughout the elevated-temperature environment. Ceiling fans were positioned between pens to circulate air and minimize temperature differences within and between pens. To regulate the heat, temperature was monitored and recorded twice daily at the level of the birds’ head in the center of each growing area. Relative humidity was also monitored and recorded twice daily; however, no attempt was made to regulate or equalize humidity. It was determined that there was a much greater
1617
1618
MCKEE AND SAMS
RESULTS AND DISCUSSION There was no difference in mortality (7.14% for heat stressed vs 4.29% for controls) or carcass weights (13.06 kg for heat-stressed vs 16.27 kg for controls) between the two treatment groups. Heat stress has been associated with increased mortality (Phelps, 1990); however, the birds in the current study were acclimated to the elevated temperatures over a 3-d period. Acclimation has been previously shown to reduce mortality related to heat stress (Reece et al., 1972). Although bird weight was not affected by the applied heat stress in the current study, chronic heat stress has been shown to result in a 20% reduction in growth rate in fast-growing strains of poultry (Bohren et al., 1981). Bohren et al. (1982) reported that although preconditioning or acclimation increased the survival rate of fast-growing strains of heat stressed poultry, it did not improve growth performance. The R-value is an indirect measure of ATP depletion in the muscle. During rigor mortis development, ATP in the muscle is depleted and R-value increases (Calkins et al., 1982). The R-value data presented in Figure 1 indicate that by 15 min post-mortem, the heat-stressed birds had significantly higher R-values than controls; this trend persisted through 24 h post-mortem. These results indicated that the seasonal heat stress application accelerated ATP depletion, thereby hastening the onset of rigor mortis. Moreover, Pietrzak et al. (1994) reported that turkeys characterized as PSE due to rapid postmortem metabolism, pale color, and poor water-holding capacity exhibited lower ATP levels by 20 min postmortem than the group with slower post-mortem metabolism. The effects of seasonal heat stress on post-mortem pH decline are shown in Figure 2. The decline in pH is a
FIGURE 1. The effect of seasonal heat stress on R-values (ratio of Abs260:Abs250) in turkey Pectoralis. Means (n = 61 per mean) within level of post-mortem time with different superscripts are significantly different (P < 0.05).
result of the breakdown of glycogen to lactic acid during post-mortem glycolysis, thereby resulting in the accumulation of lactic acid in the muscle (Lawrie, 1991). Results in Figure 2 illustrate that as early as 15 min postmortem, the heat-stressed birds exhibit a significantly lower pH than the controls. The accelerated pH decline in the heat stress birds persisted through 24 h postmortem. Ma and Addis (1973) and Vanderstoep and Richards (1974) have demonstrated that maximum differences in post-mortem pH decline between fast and slow glycolyzing turkeys occurred within 1 h postmortem, decreasing thereafter during post-mortem aging. Although the current study did not measure the pH
FIGURE 2. The effect of seasonal heat stress on pH decline in turkey Pectoralis. Means (n = 61 per mean) within level of post-mortem time with different superscripts are significantly different (P < 0.05).
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
R-value, the ratio of inosine to adenosine, is an indication of adenosine triphosphate (ATP) depletion in the muscle and was determined using the method described by Thompson et al. (1987). The post-mortem pH of samples was determined using the iodoacetate method described by Sams and Janky (1986). Mortality and carcass weight data was subjected to chi-square analysis. The rest of the data were classed by treatment and replication and the remaining parameters were subjected to ANOVA using the General Linear Models procedure (SAS Institute, 1985). Because no interaction was detected between treatment and replication, the data from all replicates were pooled into a completely randomized block design with post-mortem time as the blocking factor. The residual mean square was used as the error term and treatment means were compared utilizing the F test (SAS Institute, 1985). Frequencies of abnormal (L* value > 53) and normal (L* value < 53) birds in each treatment were subjected to chi-square analysis. Significance for all data was determined using P < 0.05.
1619
SEASONAL HEAT STRESS AND RIGOR MORTIS DEVELOPMENT IN TURKEYS
was selected to be more conservative than the L*value criteria used by Barbut (1993) in identifying abnormally pale meat. This result suggests that the heat may have caused sufficient stress to trigger the development of the PSE-like condition in the muscle. Ante-mortem stressors such as mixing, breeding, and heat have previously been reported to trigger the PSE condition in swine (Louis et al., 1993). Data in Table 1 indicates the extent to which heat stress influenced drip loss, cook loss, expressible moisture of turkey breast fillets. Heat stress significantly increased drip loss and cook loss but appeared to have no effect on expressible moisture. The increased drip loss and cook loss were expected because they are directly associated with protein functionality in the muscle. Santos et al. (1994) postulated that the early development of rigor mortis in PSE pork meat combined with high carcass temperatures caused the denaturation of muscle sarcoplasmic and contractile proteins, which resulted in meat with poor water-holding capacity, which was reflected by higher drip loss and cooking losses. Moreover, Warris and Brown (1987) found that the early post-mortem pH decline from 30 min to 1 h was determined to be the most important factor in determining the degree of protein denaturation and resulting exudate in meat. However, the fact that there was no difference in expressible moisture between treatments was not expected because changes in expressible moisture usually follow a similar trend to changes observed in drip loss and cook loss. In this study, samples for expressible moisture were collected and analyzed at 24 h post-mortem possibly after much of the expressible moisture had been lost to drip. Earlier (15 min and 2 h) samples may have been more meaningful in determining changes in expressible moisture between treatments over time. In conclusion, the current study suggested that the seasonal heat stress accelerated post-mortem metabolism and biochemical changes in the muscle, which produced pale, exudative meat characteristics in tom turkeys.
ACKNOWLEDGMENTS The authors gratefully acknowledge the donation of the turkeys used in this study by Plantation Foods of Waco, TX 76705.
TABLE 1. The effect of seasonal heat stress on drip loss, cook loss, and expressible moisture in turkey Pectoralis
FIGURE 3. The effect of seasonal heat stress on L* value in turkey Pectoralis. Means (n = 61 per mean) within level of post-mortem time with different superscripts are significantly different (P < 0.05).
Environmental treatments
Parameters
Pooled SEM
Heat-stressed Control
Drip loss, % Cook loss, % Expressible moisture, %
0.08 0.51 0.62
0.44a 24.56a 22.02
0.06b 19.08b 25.23
a,bMeans (n = 61 per mean) within each row with no common superscript differ significantly (P < 0.05).
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
at 1 h post-mortem, overall pH decline did follow a similar trend to that observed by Ma and Addis (1973) and Vanderstoep and Richards (1974). Specifically, maximum pH differences between heat-stressed and control birds were observed as early as 15 min postmortem and persisted through 2 h post-mortem, after which the differences in pH began to decrease. The results from the current study indicate that the turkeys exposed to seasonal heat stress exhibited accelerated post-mortem glycolysis compared to the birds raised in the control environment. It is the rapid decline in pH early post-mortem, while carcass temperatures are still high, that can result in extensive protein denaturation, which affects the color and water-holding capacity of the meat (Warris and Brown, 1987). Accelerated rigor mortis development occurring with poor water-holding capacity and light color is indicative of PSE meat (Cassens et al., 1975; Fox et al., 1980; Warris and Brown, 1987). Lawrie (1991) attributed the pale color meat to the denaturation of sarcoplasmic proteins, which causes increased light scattering in the muscle. The lightness (as indicated by L*values) of turkey breast fillets of both heat-stressed and control birds are illustrated in Figure 3. At 15 min, 2 h, and 24 h, heatstressed birds exhibited greater L*values than the controls. These results agree with those of Barbut (1993) and Pietrzak et al. (1994), who reported that turkeys exhibiting a rapid pH decline had significantly higher L* values than the slower glycolyzing group. In addition, van Hoof (1979) reported that the pale color in poultry meat is associated with low pH and concluded that poultry is susceptible to a PSE condition similar to that previously described in pork. In the current study, the heat stress treatment significantly (P < 0.01) increased the percentage of birds that would be classified as PSElike (36.9 vs 10.5%) according to the criterion of 24 h L*values greater than 53 being PSE-like. This criterion
1620
MCKEE AND SAMS
REFERENCES
Downloaded from http://ps.oxfordjournals.org/ at Universite Laval on June 20, 2014
Aberle, E. D., N. W. Thomas, J. M. Howe, and P. T. Arroyo, 1969. Environmental influence on high energy phosphate metabolites in porcine muscles. J. Food Sci. 34:600–603. Barbut, S., 1993. Colour measurements for evaluating the pale soft exudative (PSE) occurrence in turkey meat. Food Res. Int. 26:39–43. Bohren, B. B., J. R. Carson, and J. C. Rogler, 1981. Response to selection in two temperatures for fast and slow growth to nine weeks of age. Genetics 97:443–450. Bohren, B. B., J. C. Rogler, and J. R. Carson, 1982. Survival under heat stress of lines selected for fast and slow growth at two temperatures. Poultry Sci. 61:1804–1808. Briskey, E. J., 1964. Etiological status and associated studies of pale, soft, exudative porcine musculature. Adv. Food Res. 13:89–105. Calkins, C. R., T. R. Dutson, G. C. Smith, and Z. L. Carpenter, 1982. Concentrations of creatine phosphate, adenine nucleotides and their derivatives in electrically stimulated and nonstimulated beef muscle. J. Food Sci. 47:1350–1353. Cassens, R. G., D. N. Marple, and G. Eikelenboom, 1975. Animal physiology and meat quality. Adv. Food Res. 21: 71–155. Fernandez, X., A. Forslid, and E. Tornberg, 1994. The effect of high post-mortem temperature on the development of pale, soft and exudative pork: Interaction with ultimate pH. Meat Sci. 37:133–147. Froning, G. W., A. S. Babji, and F. B. Mather, 1978. The effect of preslaughter temperature, stress struggle anesthetization on color and textural characteristics of turkey muscle. Poultry Sci. 57:630–633. Fox, J. D., S. A. Wolffram, J. D. Kemp, and B. E. Langlois, 1980. Physical, chemical, sensory, and microbiological properties and shelf life of PSE and normal pork chops. J. Food Sci. 45:786–790. Howe, J. M., N. W. Thomas, P. B. Addis, and M. D. Judge, 1968. Temperature acclimation and its effects on porcine muscle properties in two humidity environments. J. Food Sci. 33:235–238. Lawrie, R. A., 1991. Pages 56–60, 188, and 206 in: Meat Science. 5th ed. Pergamon Press, New York, NY. Louis, F., W. E. Rempel, and J. R. Mickelson, 1993. Porcine stress syndrome: Biochemical and genetic basis of this inherited syndrome of skeletal muscle. Pages 89–95 in: Proceedings from the Reciprocal Meat Conference. Vol. 46. National Meat and Livestock Board, Chicago, IL. Ma, R. T.-I., and P. B. Addis, 1973. The association of struggle during exsanguination to glycolysis, protein solubility, and shear in turkey pectoralis muscle. J. Food Sci. 38: 995–997.
Northcutt, J. K., 1994. Influence of antemortem treatment on postmortem muscle properties of poultry meat. Ph.D. dissertation, North Carolina State University, Raleigh NC. Northcutt, J. K., E. A. Foegeding, and F. W. Edens, 1994. Water-holding properties of thermally preconditioned chicken breast and leg meat. Poultry Sci. 73:308–316. Papinaho, P. A., and D. L. Fletcher, 1995. Effects of electrical stunning duration on postmortem rigor development and broiler breast meat tenderness. J. Muscle Foods 6:1–8. Phelps, A., 1990. Improved bird performance possible at high temperatures. Feedstuffs 62:12, 17. Pietrzak, M., M. L. Greaser, and A. A. Sosniki, 1994. Effect of rapid onset of rigor mortis on protein functionality in turkey breast muscle. Poultry Sci. 73(Suppl. 1):194. (Abstr.) Reece, F. N., J. W. Deaton, and L. F. Kubena, 1972. Effects of high temperature and humidity on heat prostration of broiler chickens. Poultry Sci. 51:2021–2025. Sams, A. R., and D. M. Janky, 1986. The influence of brine chilling on tenderness of hot boned chill-boned and ageboned broiler fillets. Poultry Sci. 65:1316–1321. Santos C., L. C. Roserio, H. Goncalves, and R. S. Melo, 1994. Incidence of different pork quality categories in a Portuguese slaughterhouse: A survey. Meat Sci. 38: 279–287. SAS Institute, 1985. SAS/STAT Guide for Personal Computers. Version 6th Edition. SAS Institute Inc., Cary, NC. Sayre, R. N., E. J. Briskey, and W. G. Hoekstra, 1963. Alteration of postmortem changes in porcine muscle by preslaughter heat treatment and diet modification. J. Food Sci. 28: 292–297. Thomas, N. W., P. B. Addis, H. R. Hohnson, R. D. Howard, and M. D. Judge, 1966. Effects of environmental temperature and humidity during growth on muscle properties of two porcine breeds. J. Food Sci. 31:309–312. Thompson, L. D., M. D. Janky, and S. A. Woodward, 1987. Tenderness and physical characteristics of broiler breast fillets harvested at various times from post-mortem electrically stimulated carcasses. Poultry Sci. 66:1158–1167. Urbin M. C., D. A. Zessin, and G. D. Wilson, 1962. Observation on a method of determining water-binding properties of meat. J. Anim. Sci. 21:9. Vanderstoep, J., and J. F. Richards, 1974. Post-mortem glycolytic and physical changes in turkey breast meat. Can. Inst. Food Sci. Technol. J. 7:120–124. van Hoof, J., 1979. Influence of ante- and peri-mortem factors on biochemical and physical characteristics of turkey breast muscle. Vet. Q. 1:29–36. Warris, P. D., and S. N. Brown, 1987. The relationship between initial pH, reflectance and exudation in pig muscle. Meat Sci. 20:65–72. Wood, D. G., and J. F. Richards, 1975. Effect of some antemortem stressors on post-mortem aspects of chicken broiler pectoralis muscle. Poultry Sci. 54:528–531.