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Endocrine, blood metabolite, and meat quality changes in goats as influenced by short-term, preslaughter stress¹

Agricultural Research Station, Fort Valley State University, Fort Valley, GA 31030

² Correspondence:
1005 State University Dr. (phone: 478 827 3085; fax: 478 825 6376; E-mail:
govindak{at}mail.fvsu.edu).

	Abstract

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The purpose of this study was to determine the effects of short-term, preslaughter stress on physiological responses and meat quality in goats of different age groups. The goats (n = 28) were classified into young (6 to 12 mo of age) and old (24 to 30 mo of age) groups, feed deprived overnight, and slaughtered at three different times (replicates). On each slaughter day, goats were either subjected to a 2-h transportation stressor (TS) or remained unstressed in holding pens (NS) before slaughter. Blood samples were collected via jugular venipuncture from TS and NS goats at 2, 1, and 0 h before slaughter. Muscle glycogen and pH were measured on samples from longissimus muscle (LM) collected at 15 min and 24 h postmortem, and instrumental measures of meat color were obtained on the LM after a 24-h chilling period at 4°C. The TS goats had higher plasma cortisol (P < 0.01) and glucose (P < 0.05) concentrations than NS goats. The rates of increase in plasma cortisol, glucose, and nonesterified fatty acid concentrations were greater in TS than in NS goats (stressor treatment x blood sampling time, P < 0.01). Muscle glycogen concentrations were greater (P < 0.05) in NS than in TS goats and higher (P < 0.01) in old vs. young goats; however, pH measured at 15 min and 24 h postmortem was not (P > 0.05) influenced by stressor treatment. Water-holding capacity of meat was not (P > 0.05) influenced by stressor treatment. Older goats had lower (P < 0.01) L* values and greater (P < 0.01) a* and chroma values than the younger goats. The a* and chroma values of loin cuts from young goat carcasses were lower in the TS than NS treatment groups, but this effect was absent in the old goat carcasses (stressor treatment x age, P < 0.05). Cooking loss percentages and shear force values for loin chops aged for 7 d were not (P < 0.05) affected by stressor treatment; however, old goats produced tougher (P < 0.01) loin chops than young goats. These results indicate that short-term preslaughter transport can cause noticeable changes in stress responses and muscle metabolism in goats.

Key Words: Goats • Meat Quality • Slaughter • Stress

	Introduction

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Livestock preslaughter management procedures invariably result in increased production of catecholamines and glucocorticoids in the animal. Stress causes metabolic changes that can in turn adversely affect meat quality in small ruminants (Ashmore et al., 1972; Apple et al., 1995).

Concentrations of plasma cortisol, glucose, and creatine kinase are useful indicators of stress and muscle damage in goats (Kannan et al., 2000). Moreover, Heiman et al. (1997) reported that hypothalamic-pituitary-adrenal axis activity was inhibited by leptin in response to stress. Meat animals are normally housed without feed in abattoir holding pens before slaughter, primarily to decrease fecal contamination of carcasses (Gregory and Grandin, 1998). Plasma triiodothyronine (T₃) and tetraiodothyronine (T₄) concentrations may be altered due to prolonged feed deprivation in goats (Gomez-Pasten et al., 1999), and feed deprivation stress may also elevate plasma urea nitrogen (PUN; Kannan et al., 2000) and NEFA levels in goats (Kouakou et al., 1999). In regard to meat quality, the important metabolic changes due to preslaughter stress are depletion of glycogen and the consequent inability of muscles to develop adequate acidity levels postmortem (Gregory and Grandin, 1998). Dark muscle color is a common condition encountered when animals are exposed to situations that deplete muscle glycogen levels prior to slaughter (Lawrie, 1966). Characterized by an elevated postmortem pH, dark muscle incidences negatively impact economic returns (Smith et al., 1992).

Data are very limited on physiological responses to stress in goats. No published information is available on the effects of preslaughter stress on meat quality in goats. Therefore, the objective of this experiment was to determine the effects of short-term preslaughter stress on physiological responses and meat quality characteristics in dairy goats of different age groups.

	Materials and Methods

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Animals and Treatments
Twenty-eight castrated male Alpine goats, classified as either young (6 to 12 mo old, average weight of 22.1 kg) or old (24 to 30 mo old, average weight of 53.6 kg), were slaughtered on three different days (replicate) during a 3-wk period in the month of September. The weather conditions were identical on experiment days. The maximal temperatures on the three slaughter days were between 28 and 30°C, and the minimal temperatures were between 17 and 20°C. The number of goats slaughtered was 4, 4, and 6 from each age group, during wk -1, 2, and 3, respectively. Feed was withheld overnight prior to slaughter, and goats were subjected to one of two treatments: held overnight (12 h) without mixing young and old animals in holding pens until slaughter (NS) or held in home pens as groups and subjected to a 2-h transportation (approximately 130 km) just prior to slaughter (TS) to simulate preslaughter stress. The home pens and holding pens at the slaughter plant had similar pen dimensions and environmental conditions and were located approximately 100 m apart. A livestock trailer with internal floor dimensions of 4.5 x 1.8 m was used to transport animals. To avoid confounding the effect of time of slaughter with that of treatment, the order of slaughter was alternated between treatments.

Blood Sampling and Analysis
Blood samples were collected by trained personnel using disposable Vacutainer needles and tubes containing 81 µL of 15% EDTA solution to assess the physiological stress responses. Blood samples were collected from both treatment groups simultaneously at 2, 1, and 0 h prior to slaughter (time), which corresponded with sampling just prior to transportation of the TS goats, 1 h after beginning of transportation, and immediately after the 2-h transportation, respectively. The blood tubes were placed on ice until plasma was separated (<3 h). The samples were centrifuged at 1,000 x g for 20 min, and then the plasma was pipetted into different aliquots and stored at -40°C until analysis.

Plasma cortisol concentrations were analyzed using a Coat-A-Count (Diagnostic Products Corp., Los Angeles, CA) RIA kit, as described by Kannan et al. (2000). The sensitivity of the assay was 2.0 ng/mL. Intra- and interassay CV were 4.8 and 6.4%, respectively. Plasma T₃ and T₄ concentrations were also determined using Coat-A-Count (Diagnostic Products Corp.) RIA kits. The sensitivity of the T₃ assay was 7 ng/dL and intra- and interassay CV were 5.9 and 6.3%, respectively. The sensitivity of the T₄ assay was 2.5 ng/mL, and the intra- and interassay CV were 3.3 and 8.1%, respectively. Plasma leptin concentrations were analyzed using a multispecies leptin RIA kit (Linco Research, St. Louis, MO). The assay was validated for parallelism and recovery for goats in our laboratories as described by Kannan et al. (2000). The sensitivity of the leptin assay was 1.0 ng/mL, and intra- and interassay CV were 3.6 and 8.7%, respectively.

Plasma glucose, creatine kinase, and PUN concentrations were analyzed using commercially available diagnostic kits (Sigma Diagnostics, St. Louis, MO). Plasma NEFA levels were analyzed using a commercial kit manufactured by Wako Chemicals (Richmond, VA).

Meat Sampling and Analysis
Goats were stunned using a captive bolt pistol and then slaughtered using standard procedures. The dressed carcasses were stored at 2°C for 24 h before fabrication. Muscle samples were collected at 15 min and 24 h postmortem from longissimus muscle (LM) from the right side of each carcass for assessment of muscle pH and glycogen concentrations. At 15 min and 24 h postmortem, muscle samples were taken from the loin region of the LM, individually wrapped in aluminum foil, quick frozen in liquid nitrogen, and stored immersed in liquid nitrogen until glycogen analysis. Moreover, muscle pH was assessed at each sampling time on duplicate samples using the iodoacetate-KCl homogenate procedure (Bendall, 1973). Glycogen concentrations were analyzed from duplicate samples using the iodine-binding procedure described by Dreiling et al. (1987).

Each carcass was split along the vertebral column into left and right halves and then sliced into 2.5-cm loin/rib chops using a band saw. To the furthest extent possible, the cuts were carefully made such that the cut surfaces were at right angles to the axes of LM fibers. One chop from the posterior end of the loin region from left side of each carcass was allotted for water-holding capacity (WHC) assessment. Water-holding capacity was measured on duplicate muscle samples at 24 h postmortem, following the filter paper press method of Wierbicki and Deatherage (1958), and expressed as percentage of free water. The Commission Internationale de l’E’clairage (CIE, 1976) L*, a*, and b* color coordinate values were measured on the cut surfaces of loin chops from left side of each carcass after a 30-min bloom time at 4°C using a Minolta Chromameter (model CR-200, Minolta, Japan) with illuminant D65 as the light source. This instrument has a color-measuring area with a diameter of 1.1 cm and was calibrated using a Minolta calibration plate (L* = 97.4, a* = 0.3, b* = 1.7). Hue angle was calculated as tan^-1(b/a), whereas chroma (a measure of color vividness) was calculated as (a² + b²)1/2 (Francis and Clydesdale, 1975; Hunter and Harold, 1987).

To avoid the effect of prerigor muscle sampling and possible sarcomere shortening, only the loin/rib chops from the left side of each carcass were used for shear value determinations. The chops were vacuum-packed and aged at 2°C for 7 d postmortem for assessing Warner-Bratzler shear force (WBSF) values. A minimum of three chops was used for shear value determinations. At the end of aging time the cuts were frozen and stored at -30°C until (<1 mo) assessment of tenderness. The cuts were thawed at 4°C and cooked according to the procedures described by Kannan et al. (2002a). Cooked samples were wrapped in aluminum foil and cooled at 4°C overnight before core removal. The cuts were allowed to come to room temperature by removing them from the refrigerator and placing them on a laboratory countertop for 2 h, and then 1-cm diameter cores were removed parallel to muscle fiber orientation (Kannan et al., 2002a). Two cores were taken from each chop and WBSF values were assessed using a TA-XT2 texture analyzer (Texture Technologies Corp., Scarsdale, NY), with the samples being sheared at right angles to the orientation of muscle fibers using a Warner-Bratzler shear attachment (Texture Technologies Corp.). The instrument was set with a 25-kg load cell and a crosshead speed of 200 mm/min. Chops were weighed before and after cooking to calculate cooking loss percentage.

Statistical Analysis
The hormone and blood metabolite data were analyzed as randomized complete block design (RCB) with repeated measures using GLM procedures in SAS (SAS Inst., Inc., Cary, NC). Animals were blocked by slaughter day, and the experimental unit for blood data was the individual animal. Age of goat was included as an independent variable in the analysis in addition to stressor treatment and sampling time. Muscle pH and glycogen data were analyzed as a RCB split-plot design with factorial treatment arrangement using MIXED procedures in SAS. The whole-plot factors were stressor treatment and age of goat, and were tested with replicate x stressor treatment x age of goat as the error term. The subplot factors were meat sampling time and its interactions. These factors were tested with residual error. Chops were the experimental units for collecting meat quality data. Cooking loss, shear value, WHC, and color data were analyzed as RCB design with stressor treatment, age of goat, and stressor treatment x age of goat as fixed effects. When significant by ANOVA at P < 0.05, the means were separated by LSD test.

	Results

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There was a stressor treatment x blood sampling time (P < 0.01) interaction effect on plasma cortisol concentrations (Table 1). The cortisol concentrations increased with increasing transportation time, but the levels did not change significantly during corresponding times in NS goats. Young goats had higher (P < 0.05) plasma cortisol concentrations than older ones. Plasma leptin, T₃, and T₄ concentrations were not (P > 0.05) affected by any of the independent factors studied.

View larger version (43K): [in this window] [in a new window]   Figure 1. Effects of short-term preslaughter transportation stress on A) pH (stressor treatment x age of goat x meat sampling time, P < 0.05; age of goat, P < 0.01; meat sampling time, P < 0.01) and B) glycogen concentrations (stressor treatment x age of goat x meat sampling time, P < 0.06; stressor treatment, P < 0.05; age of goat, P < 0.01; meat sampling time, P < 0.01) in longissimus muscle samples from male goat carcasses (n = 14 per stress treatment at each sampling time).

View larger version (43K): [in this window] [in a new window]   Figure 2. Effects of short-term preslaughter transportation stress on A) L* values (age of goat, P < 0.01), B) a* values (stressor treatment x age of goat, P < 0.05; age of goat, P < 0.01), and C) chroma values (stressor treatment x age of goat, P < 0.05; age of goat, P < 0.01) of loin chops (longissimus muscle) from male goat carcasses (n = 14 per stress treatment).

View larger version (38K): [in this window] [in a new window]   Figure 3. Effects of short-term preslaughter transportation stress on Warner-Bratzler shear force (WBSF) values (age of goat, P < 0.01) of loin/rib chops (longissimus muscle) in male goat carcasses (n = 14 per stress treatment).

	Discussion

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The magnitudes of cortisol and glucose responses in older goats were greater compared with young goats, which resulted in significant age main effects. King et al. (1991) also observed that cortisol responses to stressors were greater in older calves (167 d) compared with those in younger ones (78 d).

The increase in NEFA levels in the NS goats during the 2 h prior to slaughter was very minimal compared to that in the TS goats. By contrast, Warris et al. (1990) reported lower plasma FFA in transported sheep. During prolonged exercise, FFA are the major source of energy for muscles (Gregory and Grandin, 1998; Brody, 1999). Plasma NEFA levels can also increase due to feed deprivation (Kouakou et al., 1999); however, the increase in NEFA levels in the TS goats is more likely due to physical activity rather than feed deprivation. Both TS and NS goats were subjected to the same duration of feed deprivation. In the present study, the objective of experimentally stressing one group of goats was achieved as evidenced by elevated cortisol, glucose, and NEFA concentrations.

In response to stress and muscle damage, creatine kinase from skeletal muscles is released into blood (Addis et al., 1974; Tripp and Schmitz, 1982; Lumeij et al., 1988). Plasma creatine kinase activity was higher in the NS group of goats than the TS group before the initiation of transportation stress, and levels in the unstressed goats remained elevated compared to those of transported goats throughout transportation. Additionally, transportation failed to elicit an increase in plasma creatine kinase activity, regardless of age group. In a previous study with Spanish goats (Kannan et al., 2000), our laboratory found that after encountering a physical stress, creatine kinase activity increases in circulation after a 2-h lag time. Moreover, we found that vigorous physical activity, such as herding, loading, and unloading procedures, were more important in determining plasma creatine kinase activity than transportation itself (Kannan et al., 2000). Creatine kinase activity also indicates the extent of muscular activity (Wilson et al., 1990) and damage during hauling and holding. Although the young and older animals were not mixed in the holding pens, the NS goats appeared to have undergone more muscular activity than the TS goats.

Plasma cortisol concentrations were higher in the NS goats than TS goats at 2 h prior to slaughter. The NS goats were moved to the holding pens at the slaughter plant the previous night, whereas the TS goats remained in their home pens until 2 h prior to slaughter. The novelty of the slaughter plant holding pens would have resulted in elevated stress responses in the NS goats. Kannan et al. (2002b) observed that novelty of environment during preslaughter holding may be a more potent stressor than feed deprivation in goats.

The average initial LM pH was similar in both young and old goats, but the mean ultimate pH was higher in young vs. old goats. The higher ultimate pH in the LM of young goats corresponds with their lower glycogen content compared with that of old goats. Although overall glycogen concentrations were higher in the LM of NS vs. TS goats, LM glycogen differences were only noted in young goats at 15 min postmortem. The lower glycogen content in TS goats did not affect ultimate pH; thus, transportation for 2 h, under the conditions of this study, may not have been sufficient to elicit a change in the ultimate pH of the LM. Apple et al. (1994) reported that subjecting lambs to treadmill exercise at a speed of 5.6 km/h reduced LM glycogen content, but did not alter pH measured at 48 h postmortem. Although their study involved only physical stressors, the results suggested that there could be preslaughter situations where the ultimate pH of meat may not be affected in spite of a significant preslaughter glycogenolysis.

Different types of stressors may elicit varying degrees of responses in animals. In cattle, exercise is not an adequate stimulus for increasing ultimate pH greater than 6.0 (Lawrie, 1958). However, mixing unfamiliar bulls prior to slaughter has been reported to be severe enough to result in inferior meat quality (McVeigh and Tarrant, 1981). Exercise, as well as the release of epinephrine during stress, can cause glycogen breakdown in muscles (Gregory and Grandin, 1998).

Transportation not only includes physical stress, but also emotional stress caused by loading and unloading, noise, vibration, and social disruption. As evidenced by changes in muscle metabolism, young goats are probably more susceptible to these factors, although increases in circulating cortisol and glucose concentrations were noticeably less in young goats compared with older ones. In the present experiment, 2 h of transportation prior to slaughter was sufficient to cause enough stress to effect glycogenolysis in LM of young goats, but not in older goats. There have been conflicting reports on the effect of age on muscle pH in small ruminants. Although Madruga et al. (1999) observed that slaughter age had a significant effect on goat muscle pH measured at 24 h postmortem, McGeehin et al. (2001) failed to note differences in the pH of lamb LM due to age. The conflicting published reports may be partially explained by the observation that pH varies considerably among different goat muscles. Kannan et al. (2001) found that the triceps brachii had higher pH values than either the semimembranosus or longissimus muscle.

Meat from older goats appeared darker (lower L*) and redder (higher a*) than the LM from young goats in the present study. The darker color of older animals is more than likely a response to increased myoglobin content (Lawrie, 1979) because pigment concentration in goat LM has been shown to increase with age (Dhanda et al., 1999). Furthermore, transported young goats had lower a* and chroma values than unstressed young goats, but transportation had no effect on these color values in the old goats. Perhaps, the LM of old goats was such a dark red that short-term transportation was unable to produce any further change in muscle color. Again, results of the present study indicate that meat quality may be affected by short-duration transportation more readily in young goats than in older animals.

Transportation stress causes depletion of muscle glycogen and results in formation of dark-cutting meat in sheep (Warriss et al., 1990), primarily due to the release of catecholamines (Tarrant, 1989). Adrenocortical response to transportation stress seems to be similar in sheep and goats (Greenwood and Shutt, 1992), yet quality changes characteristic of dark-cutting meat were absent in the present study, probably because the stress imposed was not chronic and intense enough. There was no effect of transportation on the ultimate pH, WHC, or cooking loss of LM. Moreover, Bray et al. (1989) reported that subjecting sheep to different physical stressors did not influence the L*a*b* values of LM.

Muscle with a greater ultimate pH (>6.0) has been reported to result in a more tender meat during aging than that with a lower ultimate pH (Marsh, 1983; Watanabe et al., 1996). Increased tenderness as the ultimate pH of meat rises from 6.0 to 7.0 is attributed to greater calpain activity (Watanabe et al., 1996). The ultimate pH of meat from young goats in our study was 6.24 and 6.11 in the LM of TS and NS groups, respectively. It is not clear if the increased tenderization rate noticed in transported young goats compared with unstressed young goats was due to the ultimate pH because the difference was very small (0.13 pH unit). Prolongation of a high ultimate pH-status in muscles due to antemortem depletion of glycogen has been reported to result in tender meat (Marsh, 1983; Apple et al., 1995). However, severe prolonged stress in animals has been reported to induce dark-cutting meat, which should be minimized to improve overall meat quality.

In conclusion, short-term preslaughter transport can cause significant changes in the stress responses of goats (increased plasma concentrations of cortisol, glucose, and NEFA). Additionally, muscle glycogen concentrations decreased due to transportation of goats, with a more pronounced effect in young vs. older goats, although the magnitudes of cortisol and glucose responses to stressor treatment were greater in older goats. Preslaughter stress can also affect the color of meat from younger goats. The effects of stress on meat quality are more pronounced in younger animals than in older ones. However, short-term preslaughter stress does not seem to produce conditions similar to dark-cutting meat in male dairy goats.

	Implications

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Under commercial situations, meat animals are normally held in holding pens after transport before slaughter, but goats are typically slaughtered immediately on arrival at the abattoir. Results from this study reveal that short-duration transportation before slaughter produces significant changes in stress responses, muscle metabolism, and meat quality. Furthermore, the effects of short-term preslaughter stress on muscle quality are more pronounced in young goats than older goats. Meat quality changes in goats when exposed to stressors for longer periods before slaughter could be evaluated in future studies.

	Footnotes

 
¹ This research was supported by the Agricultural Research Station at FVSU. The authors would like to thank S. Wang, N. Evans-Moye, and O. Samples for technical assistance. Acknowledgements are also due to L. Brown and R. Buckner for assistance with animal handling and blood sampling.

Received for publication June 8, 2002. Accepted for publication February 18, 2003.

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