The development of pale, exudative meat in two genetic lines of turkeys subjected to heat stress and its prediction by halothane screening1

PROCESSING AND PRODUCTS The Development of Pale, Exudative Meat in Two Genetic Lines of Turkeys Subjected to Heat Stress and Its Prediction by Halothane Screening1 C. M. Owens,* S. R. Mckee,* N. S. Matthews,† and A. R. Sams*,2 *Department of Poultry Science and †Department of Small Animal Medicine and Surgery, Texas A&M University College Station, Texas 77843 the BODY strain, and there were no differences in readyto-cook yields between any treatments. The HAL+ HS birds had significantly lower muscle pH (0 h) and significantly higher L* values at 2 h postmortem compared with HAL– HS birds in the BREAST strain; however, there was no difference in L* value at 24 h postmortem. The HAL– HS birds had significantly lower muscle pH (0 h and 2 h) and significantly higher L* values at 2 h postmortem compared with HAL– controls in the BODY strain. The HAL– HS BREAST birds had significantly higher drip loss than HAL– controls. No differences in shear value were found among any treatments. The incidence of PSE (2-h L* values >52) was significantly higher in HAL+ HS birds (34.7%) compared with HAL– HS birds (13.4%). These results suggest that halothane sensitivity early in life is associated with HS susceptibility and the development of pale meat when birds are slaughtered at market age. These results also suggest that halothane screening may be better at predicting the development of PSE meat during HS in the strain selected for large breast yield rather than rapid overall growth.

ABSTRACT Previous research has indicated that seasonal-type heat stress (HS) can contribute to the development of pale, soft, exudative (PSE) meat in fast-growing turkeys and that halothane exposure may identify stresssusceptible animals. This study evaluated the ability of halothane screening to identify stress-susceptible birds prone to developing pale, exudative meat when reared to market age. Two lines of turkeys (n = 292), one selected for rapid overall growth (BODY) and the other for large breast muscle yield (BREAST), were exposed to 3% halothane for 5 min at 2 to 4 wk of age and were raised together until 16 wk of age. Approximately 10% of both BODY and BREAST birds were sensitive to halothane. Between 16 and 20 wk, all of the halothane sensitive (HAL+) and half of the halothane nonresponders (HAL–) were exposed to an HS environment of 30 to 36 C (night/day), whereas the other half of the HAL– birds were kept at an ambient temperature of 13 to 21 C (night/day). All birds were slaughtered at 20 wk of age, and samples were collected for pH, L* value, drip loss, cooking loss, and shear value. The BREAST strain had 5% greater breast percentage than

(Key words: pale, soft, exudative, halothane, heat stress, turkey, rigor) 2000 Poultry Science 79:430–435

man, 1995; D’Souza et al., 1998; Maribo et al., 1998). Pale, soft, exudative meat is the result of accelerated postmortem glycolysis, which results in a rapid postmortem decline in pH while carcass temperatures are still high. This combination can result in portein denaturation of the muscle that leads to pale meat color, decreased waterholding capacity, and poor texture (Penny, 1969; Warriss and Brown, 1987; Santos et al., 1994). In swine, PSE is associated with Porcine Stress Syndrome (PSS), which is similar to malignant hyperthermia (MH) in humans (Hall et al., 1966; Mitchell and Heffron, 1982; Harrison, 1994). Porcine Stress Syndrome and MH are inherited disorders caused by a defect in the calciumrelease channel (ryanodine receptor) in the sarcoplasmic reticulum (O’Brien, 1986). Porcine Stress Syndrome and

INTRODUCTION The occurrence of pale, soft, exudative (PSE) meat has become a growing problem for the turkey industry. This condition has been extensively studied in swine, but much is still unknown about the problem in poultry. Pale, soft, exudative meat in swine has been associated with rapid growth and antemortem and postmortem stressors, including environmental temperatures (too hot or cold), transportation, preslaughter handling practices, stunning methods, and chilling regimes (Cassens et al., 1975; Honikel, 1987; Offer, 1991; Backstrom and Kauff-

Received for publication June 7, 1999. Accepted for publication October 15, 1999. 1 This research was supported by a grant from the US Poultry and Egg Association. 2 To whom correspondence should be addressed: asams@poultry. tamu.edu.

Abbreviation Key: HAL+ = halothane sensitive; HAL– = halothane nonresponder; HS = heat stress; MH = malignant hyperthermia; PSE = pale, soft, exudative; PSS = Porcine Stress Syndrome.

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MH can be induced by stressful conditions as well as with anesthetics such as halothane or depolarizing agents such as succinylcholine in swine that are homozygous for the recessive PSS/MH gene (also known as the halothane gene). Muscle rigidity, increased body temperature, and increased lactic acid production can characterize the response to halothane (Michelson and Louis, 1993). Animals with PSS are prone to developing PSE meat. The swine industry has used halothane as a screening method for PSS to remove stress-susceptible animals from breeder populations, thereby reducing the incidence of PSE meat (Webb and Jordan, 1978). The halothane screening test has been successful in identifying pigs that are susceptible to stress and are prone to developing PSE. In addition, previous research has indicated that seasonal-type heat stress (HS) can contribute to the development of PSE in swine and turkeys (Santos et al., 1994; McKee and Sams, 1997). Therefore, the objective of this study was to evaluate the ability of halothane screening to identify stress-susceptible birds prone to developing PSE meat when reared to market age. Because rapid growth can increase stress susceptibility and the incidence of PSE (Ferket and Foegeding, 1994), two genetic lines of turkeys, selected for either rapid overall growth or large breast muscle yield, were evaluated to determine if they differed in the incidence of halothane sensitivity or PSE meat.

MATERIALS AND METHODS Two genetic lines of turkeys from Nicholas Turkey Breeding Farms were used in this study. One line was selected for overall rapid growth (BODY) and the other for large breast yield (BREAST). Hatching eggs were set and incubated for 28 d to hatch at the university’s poultry research farm. After hatching, poults were vent-sexed, wing-banded, and toe- and beak-trimmed. Poults were raised under normal brooding practices in brooder cages until 2 to 4 wk of age. Two hundred ninety-two 1- to 4wk old birds in two trials were challenged with halothane gas (Wheeler et al., 1997). Birds were placed in an airtight chamber (four to eight birds per group, depending on size) and were exposed to halothane gas at 3% for 5 min using an oxygen flow rate of 6 L/min. The 5-min timing began when a 3% halothane concentration was reached. The total exposure time was approximately 9 min. After exposure, turkeys were quickly removed and were subjectively evaluated for muscle rigidity in the leg muscles. If leg muscles were rigid, birds were classified as halothane sensitive (HAL+), and if muscles were flaccid, birds were classified as halothane nonresponders (HAL–). After halothane challenge, all birds were reared together until 16 wk on litter-covered concrete floors in 6× 9-m dark-out houses in ambient temperatures. These

3

Model SP3055, Brower Corp., Haughton, IA 52631. Model CR-200, Minolta Corp., Ramsey, NJ 07446. Model Zephaire-G, Blodgett Oven Co., Burlington, VT 05402.

4 5

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conditions were selected to reduce the stress on the birds until the HS treatment was applied. Birds were fed ad libitum using a commercial feeding schedule that met the nutritional requirements of the turkeys (NRC, 1994). Turkeys were then moved to a house with two separate growing areas with repeating 3.05- × 1.83-m pens (12 in each growing area) and were separated by strain, sex, and treatment. Birds were evenly distributed in pens (7 to 10 birds per pen) based on sex and strain. Males and females were placed in separate pens; however, strains of the same sex were grown together. All HAL+ and half of the HAL– birds were placed in an environment with elevated temperatures (30 to 36 C, night/day) for 4 wk (the HS treatment), whereas the remaining HAL– birds were kept at ambient temperatures (13 to 21 C, night/ day) for 4 wk. The elevated temperatures were achieved using forced air natural gas heaters and ceiling fans to circulate the air (McKee and Sams, 1997). Windows in the house were closed in the growing area where temperatures were elevated but were open in the growing area where birds were exposed to ambient temperatures. Temperature was recorded twice daily in both growing areas. At 20 wk, HAL– males and females of each strain from the HS treatment (HS) (n = 67) and control treatment (n = 75) and all HAL+ HS (n = 23) were slaughtered at the university’s pilot processing plant. Feed was withdrawn from turkeys for 12 h, and then they were transported to the holding room 1 h prior to slaughter. Preslaughter stunning was not used as it is not required for commercial poultry slaughter (Humane Slaughter Act of 1958). Furthermore, it is not universally practiced by commercial processors and has been shown to interfere with rigor mortis development (Murphy et al., 1988; Papinaho and Fletcher, 1995; Poole and Fletcher, 1998). Birds were killed by bleeding through a unilateral neck cut for 3 min. Birds were then individually subscalded (61 C, 45 s) and picked (rotary drum picker3; 30 s). Birds were manually eviscerated, and carcasses were chilled using a two-stage chilling system (12 C for 30 min the 4 C for 75 min). Breast fillets were deboned at 2 h postmortem and then aged on ice until 24 h postmortem. Muscle samples were collected from left fillets at 0, 2, and 24 h postmortem for pH determination using the iodoacetate method described by Jeacocke (1977) as modified by Sams and Janky (1986). After sample collection at 0 h (collected immediately after feather removal), breast skin surrounding the sample area was clipped together to prevent water in the chiller from contacting the breast muscle (McKee and Sams, 1997). Muscle samples were immediately frozen in liquid nitrogen and stored at –76 C until futher analysis. Color (L* value) was measured on the cut surface of the left fillets at 2 and 24 h postmortem using a Minolta colorimeter.4 After deboning (2 h), fillets were placed in closed-top sealable bags and were stored in a 4 C cooler overnight on ice. At 24 h postmortem, right fillets were placed in pans on raised wire racks, covered with aluminum foil and then cooked to an internal temperature of 76 C in a convection oven.5 AlloKramer shear analysis was conducted using the methods

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OWENS ET AL. TABLE 1. Muscle pH (0, 2, 24 h) and L* value (2, 24 h) of Pectoralis from two genetic lines (BODY or BREAST) of halothane-heat-stressed (HS) or nonheat-stressed (control) HS turkeys. BODY Measurement Breast percentage pH 0h 2h 24 h L* Value 2h 24 h Cooking loss percentage Shear value (kg/g)

1

BREAST 2

HS

Control a

1

HS

Control2

SEM

b

23.72 6.07b 5.89b 5.84

25.57 6.14a 5.97a 5.84

29.48 6.11 5.85 5.75y

30.31 6.08 5.81 5.66x

0.29 0.01 0.01 0.01

50.55a 53.71 18.23 7.56

49.31b 52.99 16.23 7.40

49.41 53.92 16.02 7.45

48.73 53.29 17.62 7.95

0.19 0.15 0.55 0.12

Means within BODY strain within sample time with no common superscript differ significantly (P < 0.05). Means within BREAST strain within sample time with no common superscript differ significantly (P < 0.05). 1 n = 67 per mean. 2 n = 75 per mean. a,b

x,y

described by Sams (1990) and McKee and Sams (1998) using an Instron Universal Testing machine.6 Weights of fillets before and after cooking were measured to determine cooking loss. Data were subjected to analysis of variance using the general linear model procedures of SAS (1985). Differences between means were determined using the least squares means procedure of SAS (1985) and a significance level of P < 0.05. The percentages of pale fillets (L * >52) in each treatment group were subjected to chi-square analysis to determine differences (P < 0.05). The effect of applied HS was analyzed by comparing HAL– control birds to HAL– HS birds. To determine if the halothane screening was effective in predicting birds prone to developing PSE meat, HAL+ HS birds were compared with HAL– HS birds. Because of an interaction in some parameters between strain and treatment, the strains were analyzed and are presented separately. The sexes were pooled within strain as there was no interaction or sex effect.

RESULTS AND DISCUSSION Halothane Response and Live Performance Approximately 10% of the turkeys screened with halothane responded to the treatment by showing signs of muscle rigidity in the legs. There was no significant difference in halothane response between the two strains (data not shown). In swine, the frequencies of halothane-positive reactions vary from 0 to 88%; however, most breeds range from 0 to 20% (Webb et al., 1982). Wheeler et al. (1997) reported that 2 to 15% of young turkeys challenged with halothane showed some response. Therefore, the 10% response in this study was consistent with this previous report. The BREAST strain had a greater (P < 0.05) breast percentage (29% vs. 24%) than the BODY strain. However, HS singificantly reduced breast percentage in the BODY strain but not in the BREAST strain (Table 1). 6

Model 1011, Instron Corp., Canton, MA 02021.

In addition, there were no significant effects of halothane response on breast percentages in either strain (Table 2).

Rigor Mortis Development Postmortem decline in muscle pH is due to an accumulation of lactic acid in the muscle during postmortem glycolysis (Khan and Nakamura, 1970). The application of HS accelerated rigor development in the BODY strain, as indicated by significantly lower pH values at 0 and 2 h postmortem, but caused no difference in muscle pH in the BREAST strain (Table 1). McKee and Sams (1997) reported that HS application 4 wk prior to slaughter accelerated rigor development in a fast-growing commercial strain of turkeys. Howe et al. (1968) reported that growing swine in an environment with fluctuating temperatures (21 and 32 C; 3 d at each temperature) resulted in a more rapid decline in postmortem pH compared with growing animals in an environment with a constant temperature of 27 C. In the BREAST strain, the HAL+ HS birds had significantly lower pH values at 0 h when compared with HAL– HS birds (Table 2). An acceleration of rigor development in halothane-positive swine is a common characteristic of these animals compared with halothane-negative animals (De Smet et al., 1993; Cheah et al., 1994; Klont and Lambooy, 1995). This finding suggests that the heat treatment caused a more rapid decline in muscle pH and that halothane was able to identify those animals (BREAST strain) susceptible to the accelerated rigor development. The fact that there was a difference in muscle pH of the BREAST strain between HAL+ HS and HAL– HS, but that there was no difference due to HS application (in the BREAST strain) suggests that halothane screening may be useful in identifying birds that are prone to accelerated rigor development when stressed.

Color Acceleration of rigor development, or rapid decline in pH, while carcass temperatures are still high can result in protein denaturation (Bendall and Wismer-Pedersen,

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HALOTHANE SCREENING FOR PALE, SOFT, EXUDATIVE MEAT IN TURKEYS TABLE 2. Muscle pH (0, 2, 24 h) and L* value (2, 24 h) of Pectoralis from two genetic lines (BODY or BREAST) of halothane + (HAL+) heat-stressed (HS) or halothane−(HAL−) heat-stressed (HS) turkeys. BODY 1

BREAST 2

1

Measurement

HAL+

HAL−

HAL+

HAL−2

SEM

Breast percentage pH 0h 2h 24 h L* Value 2h 24 h Cooking loss percentage Shear value (kg/g)

23.74 6.11 5.92 5.80

23.72 6.07 5.89 5.84

29.08 6.01y 5.76 5.72

29.48 6.11x 5.85 5.75

0.38 0.02 0.02 0.01

51.07 53.25 18.35 7.88

50.55 53.71 18.23 7.56

50.64x 53.13 18.80 8.09

49.41y 53.92 16.02 7.45

0.25 0.23 0.67 0.15

Means within BODY strain within sample time with no common superscript differ significantly (P < 0.05). Means within BREAST strain within sample time with no common superscript differ significantly (P < 0.05). 1 n = 23 per mean. 2 n = 67 per mean. a,b

x,y

1962; Penny 1969; Mitchell and Heffron, 1982; Offer, 1991). Protein damage in the muscle can lighten meat color and reduce water-holding capacity (Warriss and Brown, 1987; Santos et al., 1994), primary characteristics of PSE meat. The paleness of meat is a result of denatured sarcoplasmic proteins, which results in scattering of light (Bendall, 1973; Swatland, 1993). HS affected color in the BODY strain as indicated by significantly higher L* values (lightness) at 2 h postmortem when compared with nonHS BODY birds (Table 1); however, there was no difference between HAL+ HS and HAL– HS BODY birds (Table 2). This difference caused by HS was consistent with a report by McCurdy et al. (1996), who reported that turkey breast muscle had highest L* values in the summer season, which suggested that HS can contribute to the development of pale meat. There was no color difference due to HS in the BREAST strain (Table 1); however, the HAL+ HS BREAST birds had significantly higher L* values at 2 h when compared with HAL– HS BREAST birds (Table 2). The increased L* values at 2 h can be attributed to the more rapid decline in pH during early postmortem that was observed in each case. The trend of higher L* values associated with lower muscle pH in this study was consistent with Barbut (1993) who reported a significant correlation (r = –0.71, P < 0.01) between L* values and muscle pH. Warriss and Brown (1987) also reported similar relationships between pH and color. Although there were differences in L* values observed at 2 h, there were no differences observed at 24 h postmortem. This lack of difference could be attributed to color development that occurs over time. McCurdy et al. (1996) reported that 24h L* values of turkey breast were consistently higher than 3-h L* values (n = 4,500 fillets). However, the difference observed at 2 h postmortem in this study is important because it can be an early indication of a potential problem of PSE meat. It is important to note that at 2 h postmortem, the percentage of HAL+ HS birds (strains pooled) with L* values >52 (34.7% vs. 13.4%) was significantly higher than the percentage of HAL– HS birds with L* values >52 (Table 3). The HS application had no effect on this

percentage in the present study. McKee and Sams (1997) reported that HS application significantly increased the percentage of pale fillets when compared to controls. The fact that there were significantly more pale fillets in HAL+ HS birds compared with HAL–HS birds, but not significantly more in HAL–HS birds compared with HAL– nonHS birds, indicates that the halothane sensitivity predicted a tendency to develop PSE meat during HS. Therefore, the use of halothane may be useful to screen turkeys to identify those prone to developing PSE. In addition, 47% of the pale (L* >52) fillets (8/17, HAL+ pale/total pale) were from HAL+ turkeys. Halothane sensitivity in swine is related to a genetic mutation in the ryanodine receptor (calcium-release channel) protein (House et al., 1993; Vogeli et al., 1993). That 47% of the birds producing pale meat were HAL+ suggests that almost half of the pale meat incidence in the present study was related to a defective calcium channel protein. It follows that either the test is not 100% predictive or that the other half of the birds producing pale meat were influenced by other factors related to stress susceptibility (e.g., environment) independent of a ryanodine protein mutation. However, the relative influence of genetics and environment on the incidence of pale meat will depend on the genetics and conditions of each situation. This relationship will be particularly true as the incidence varies widely over time (McCurdy et al., 1996).

TABLE 3. Incidence of pale meat (L* value >52) from halothane + heat-stressed (HS), halothane − heat-stressed (HS), or halothane − nonheat-stressed (non-HS) turkeys. L * Value >52 Treatment

BODY

BREAST

Strains Combined

Halothane + HS Halothane − HS Halothane − Non-HS

5/7 (41.7%)a 5/30 (14.3%)b 2/34 (5.6%)b

3/8 (27.3%)a 4/28 (12.5%)a 4/35 (10.3%)a

8/15 (34.7%)a 9/58 (13.4%)b 6/69 (8.0%)b

a,b Means within columns with no common superscript differ significantly (P < 0.05).

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FIGURE 1. L* values of Pectoralis at 2 h from halothane + (HAL+) heat-stressed (HS) and halothane – (HAL–) heat-stressed (HS) turkeys.

The bimodal frequency histogram of 2-h L* values from the HAL+ turkeys suggests that there are two distinct subpopulations of birds with differing potentials for developing pale meat (Figure 1). The frequency of L* values from HAL–HS turkeys has an expected normal distribution.

Water-Holding Capacity Water-holding capacity is another important aspect of PSE meat and can be evaluated with cooking loss. No significant difference was observed in cooking loss in either strain due to HS (Table 1). There was no significant difference in cooking loss between HAL+ HS and HAL– HS turkeys in either strain (Table 2). Heat stress has been previously reported to increase drip loss and cooking loss (McKee and Sams, 1997). McKee and Sams (1998) reported increases in cooking loss only when carcasses were chilled above 20 C. It may be possible that the fast or long chilling system used in this study may have prevented some denaturation of the muscle proteins, resulting in little or no effect on cooking loss of the meat. Ma and Addis (1973) reported that cooking losses were not affected by muscle pH. Struggling turkeys (at time of slaughter) had significantly lower muscle pH than restrained turkeys, but there was no difference in cooking loss. Other factors, such as fillet size, surface exposure, and chiller water uptake can influence cooking loss. These factors may have contributed to the unexpected lack of differences in cooking loss observed in this study.

Texture Because texture is another quality of meat that can be affected in PSE meat, tenderness of turkey breast fillets was evaluated in this study. There were no differences in shear value when comparing HAL–HS with non-NS birds or HAL+ HS to HAL–HS in either strain (Tables 1 and 2). All shear values in this study were at or below 8 kg/g, which would be low enough to be considered moderately tender by consumers (Lyon and Lyon, 1990). This lack of a shear value difference is consistent with the results of McKee and Sams (1998) using a 0 or 20 C chilling temperature. Froning et al. (1978) also reported

no difference in shear values between HS and non-HS turkeys. Fox et al. (1980) reported that PSE pork chops had lower Warner-Bratzler shear values, although there was no difference in tenderness scores from a tasting panel compared with normal chops. Fox et al. (1980) also reported inconsistency among researchers in texture characteristics of PSE meat in which higher shear values and lower taste panel scores for tenderness have also been observed in PSE pork. These results indicate that the HS affected muscle pH and color of the halothane-positive birds more than the halothane-negative birds in the strain selected for large breast yield (BREAST). Therefore, these results suggest that the halothane sensitivity early in life may be associated with HS susceptibility and the development of PSE meat when birds are slaughtered at market age. These results also suggest that halothane may be better able to predict the development of PSE meat during HS in the strain selected for large breast yield rather than the strain selected for rapid overall growth.

ACKNOWLEDGMENTS The authors are grateful for the support of Nicholas Turkey Breeding Farms, Plantation Foods, and US Poultry and Egg Association.

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