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Negative effects of stress immediately before slaughter on pork quality are aggravated by suboptimal transport and lairage conditions

E. Hambrecht^*,1, J. J. Eissen^*, D. J. Newman, C. H. M. Smits^*, L. A. den Hartog^*, and M. W. A. Verstegen

^* Nutreco Swine Research Centre, Boxmeer, The Netherlands; and Department of Animal Science, University of Missouri, Columbia 65211-5300; and and Wageningen Institute of Animal Sciences, Wageningen University and Research Centre, The Netherlands

	Abstract

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The objectives of the present experiment were 1) to study the effects of transport conditions and lairage duration on stress level, muscle glycolytic potential, and pork quality; and 2) to investigate whether the negative effects of high stress immediately preslaughter are affected by preceding handling factors (transport and lairage). In a 2 x 2 x 2 factorial design, halothane-free pigs (n = 384) were assigned to either short (50 min) and smooth or long (3 h) and rough transport; long (3 h) or short (<45 min) lairage; and minimal or high preslaughter stress. Pigs were processed in eight groups (48 pigs per group) on various days at a commercial plant. Blood samples were taken at exsanguination to measure plasma cortisol and lactate concentrations. Muscle pH and temperature were measured at 30 and 40 min, respectively, and both were measured at 3 h, postmortem. A LM sample was taken 135 min postmortem to estimate glycogen content and rate of glycolysis. Pork quality attributes were assessed 23 h postmortem. Short transport increased cortisol when followed by short lairage (transport x lairage; P < 0.01). Long transport, but not lairage (P > 0.30), tended to increase (P = 0.06) muscle glycolytic potential. Long transport tended to increase (P = 0.08) electrical conductivity, and decreased a* (P < 0.01) and b* (P < 0.02) values. Decreasing lairage from 3 h to <45 min decreased (P < 0.05) the L* value, but it did not (P > 0.10) affect other pork quality traits. High stress decreased (P < 0.001) muscle glycolytic potential, and increased (P < 0.001) plasma lactate, cortisol, muscle temperature, rate of pH decline, and ultimate pH. Except for decreased (P < 0.001) b* values, pork color was not (P > 0.40) affected by high stress, but water-holding properties (measured by electrical conductivity, filter paper moisture, and drip loss) were impaired (P < 0.001) by high stress. Fiber optic-measured light scattering and Warner-Bratzler shear force were not (P > 0.12) affected by any treatment. Comparisons with the "optimal" handling (short transport, long lairage, and minimal stress) revealed that, with regard to water-holding properties, the negative effects of high stress were aggravated by suboptimal transport and lairage conditions. High stress alone increased electrical conductivity by 56%, whereas high stress in combination with short lairage led to an 88% increase. However, high preslaughter stress contributed most and was the major factor responsible for reductions in pork quality.

Key Words: Lairage • Meat Quality • Pigs • Stress • Transport

	Introduction

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The rate and extent of postmortem acidification in pork muscles largely determine ultimate meat quality (Wismer-Pedersen and Briskey, 1961; Briskey, 1964; Offer and Knight, 1988). van der Wal et al. (1999), Rosenvold et al. (2001), and Hambrecht et al. (2004b) found that preslaughter stress level and glycolytic potential (a measure for the in vivo muscle glycogen content present before slaughter) were closely related to these metabolic processes. In fact, both preslaughter stress and glycolytic potential explain a large portion of the variation in drip losses and pork color. Research has shown that genetic variation independent of the RN gene (Ciobanu et al., 2001; Oksbjerg et al., 2001), fasting (Eikelenboom et al., 1991; Wittman et al., 1994), transport (Becker et al., 1985; Geers et al., 1994; Leheska et al., 2003), and lairage (Honkavaara, 1989; Nanni Costa et al., 2002; Pérez et al., 2002b) may influence muscle glycolytic potential and/or stress level and, ultimately, pork quality. Hambrecht et al. (2004b) concluded that differences in any one, or several, of these factors may markedly affect muscle glycolytic potential, but which factor accounts for the greatest amount of variation in postmortem glycolysis is still largely unknown. Therefore, the present experiment was designed to study the effects of transport conditions and lairage duration on stress level, muscle glycolytic potential, and ultimate pork quality under controlled conditions. The objective was to test whether the negative effects of high stress immediately before slaughter were affected by preceding handling factors, such as transport and/or lairage.

	Materials and Methods

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The experimental protocol was approved by the Animal Care and Ethics Committee of the University of Nijmegen, The Netherlands.

Animals and Experimental Design
All pigs were commercial Yorkshire x (Large White x Landrace), and halothane-free endproducts of the Hypor pig breeding company (Regina, Canada). In a completely randomized design, barrows and gilts (n = 384) were assigned to one of eight treatments arranged in a 2 x 2 x 2 factorial design, with two types of transport (short and smooth or long and rough), two lairage durations (long or short), and two stress levels (minimal or high) immediately before slaughter. Eight groups of 48 pigs, all originating from the same commercial farm, were processed during 8 wk on various days. Long and short lairage alternated between one week and the next, whereas transport types and pre-slaughter stress levels were varied within the same slaughter day. The experiment took place from October to December. On six processing days, outdoor temperatures ranged between 5 and 12°C during the relevant periods of transport and lairage. On two consecutive slaughter occasions, outdoor temperatures fell below the freezing point (–4 to 0°C).

Preslaughter and Slaughter
All pigs were fed the same commercial diet in a liquid feeding system, and received their last meal 16 h before slaughter. Within each processing day, four groups of pigs, each group consisting of 12 pigs of three different pens (four pigs per pen out of a total of 12 pigs per pen), were assigned randomly in their home pen to either short and smooth or long and rough transport, and either minimal or high preslaughter stress. Loading density was 0.45 m²/100 kg BW for all pigs. Pigs in the first two treatments (minimal and high preslaughter stress after long transport) were loaded and driven for 2 h on minor roads, with frequent roundabouts and speed bumps, resulting in the truck changing speed and periodic stopping/starting. Meanwhile, pigs of the other two treatments (minimal and high preslaughter stress after short transport) were loaded on a second, larger, but otherwise similar, truck (double-deck truck with all pigs loaded onto the upper deck). After returning to the farm, the two groups of the long transport treatment were unloaded and reloaded onto the second truck, and transported together with the two groups of pigs of the short transport treatment to the processing plant. This transport was mostly smooth (paved, four-lane highways), and took approximately 50 min. After arrival, pigs were kept within their treatments separately in holding pens at a stocking density of 0.75 m²/100 kg BW. Pigs in the long lairage treatment received a 3-h rest before slaughter, whereas pigs that were subjected to the short lairage treatment were only rested for 30 to 45 min. Experimental pigs were the first to be slaughtered at 0630, which meant that, for the most part, lights were dimmed in lairage and there was little noise. All pigs were showered for approximately 10 min directly before they were led to the stunning area. Experimental stressor treatments were the same as those described by Hambrecht et al. (2004b). Pigs in the minimal stress group were guided to the stunning area without the use of electric goads and were handled as calmly as possible, whereas pigs in the high stressor treatments were forced, by yells and electric goads, to move back and forth four times in the corridor leading to the stunning area. Pigs were electrically stunned in a fully automated, head-to-heart stunning system (Midas, Stork, The Netherlands), and care was taken that all pigs were shackled using the right hind leg.

Sampling Procedures and Chemical Analyses
At exsanguination, a 9-mL blood sample was collected in a heparinized tube (Monovette LH, Sarstedt, Nümbrecht, Germany) from each pig for cortisol and lactate determinations. Blood samples were immediately put on ice and transported back to the laboratory, where samples were centrifuged for 10 min at 1,300 x g, and plasma (1.0 mL) was transferred to Eppendorf tubes and stored at –20°C until analysis. Plasma cortisol concentrations were determined as described by Erkens et al. (1998) using a solid-phase RIA kit (Coat-a-Count Cortisol TKCO, Diagnostic Products Corp., Apeldoorn, The Netherlands), whereas blood lactate concentrations were determined spectrophotometrically with lactate dehydrogenase and NAD (Bergmeyer, 1974).

At 135 min postmortem, when carcasses had passed from the rapid chilling tunnel into the cooler, muscle samples were taken from the left LM at the last rib for determination of the glycolytic potential. Samples were immediately frozen in liquid N and stored at –80°C until further analysis. Muscle lactate and glycogen were extracted by homogenizing the samples in 0.85 M perchloric acid. After centrifuging the suspension for 10 min at 1,500 x g, the supernatant fluid was neutralized with 10 M KOH. Lactate in the supernatant was determined spectrophotometrically with lactate dehydrogenase and NAD (Bergmeyer, 1974). Glycogen in the supernatant was enzymatically hydrolyzed to glucose by incubation with amyloglucosidase (Sigma A 7420, Sigma-Aldrich Chemie BV, Zwijndrecht, The Netherlands) in acetate buffer (pH 4.8) at 55°C for 2 h. After incubation, the supernatant fluid was neutralized with 10 M KOH, and glucose was determined spectrophotometrically by the hexokinase method (Bergmeyer, 1974). Concentrations of glucose-6-phosphate and glucose were not separately determined but were included in the glycogen determination. The glycolytic potential was calculated as the sum of 2 x [glycogen] + [lactate] (Monin and Sellier, 1985).

Measurements
The left carcass side was used for all measurements. Muscle pH and temperature were measured in the LM at the level of the third lumbar vertebra. At 30 min, 3 h, and 24 h postmortem, pH was measured with a portable pH meter (Portamess 911 pH, Knick Elektronische Messgeräte, Berlin, Germany) equipped with a probe-type glass electrode (LoT406; Mettler Toledo, Switzerland). To record temperatures, data loggers (Diligence EV N2002, Comark Instruments, Stevenage, U.K.) equipped with a food penetration probe (PX22L/C, Comark Instruments) were inserted in the LM at 40 min postmortem, and temperatures were recorded at 5-min intervals until 23 h postmortem; however, only data corresponding with the pH measurement times are reported.

At 23 h postmortem, loins were fabricated for final meat quality measurements. Objective color (L*, a*, and b*) was measured on a freshly cut surface at the height of the last lumbar vertebra after a 10-min blooming period with a Minolta portable chroma meter (model CR 210, Minolta, Osaka, Japan) equipped with a 50-mm aperture and using illuminant D65. Internal light scattering was measured using the fiber optic probe (TBL Fibres, Leeds, U.K.), and electrical conductivity was measured using the LF-Star (Ingenieurbüro Matthäus, Nobitz, Germany). Water-holding capacity of the LM was measured by two methods. Filter paper (45-mm diameter) was weighed, gently pressed on the caudal cut surface of the LM for 10 s, and subsequently reweighed to determine the absorbed moisture content. Additionally, a slice of the LM was placed with the cut surface facing down on a metal grid that was placed in a closed plastic container. Drip loss was determined as percentage of weight loss after 24 h of storage. A 2.5-cm LM slice was removed adjacent to the slice used for the drip loss measurement for determination of Warner Bratzler shear force. Samples were vacuum-packaged, heated in water at 75°C until an internal temperature of 70°C was reached. Samples were cooled in water until they had reached a temperature of approximately 20°C. Six 1-cm-diameter cores were removed parallel to the length of the muscle fiber and sheared once across the center using a TA-XT2 texture analyzer (Stable Micro Systems, Etten-Leur, The Netherlands). The mean shear force value for each LM slice was used for statistical analysis.

Statistical Analyses
Data were analyzed by the mixed-model procedure (Proc Mixed) of SAS (v. 8.02, SAS Inst., Inc., Cary, NC). Least squares means were generated by the LSMEANS statement. Tests of multiple comparisons of LSMEANS were adjusted according to the Tukey-Kramer method to ensure the overall significance level of P 0.05. The Tukey-Kramer adjustment controls the maximum-wise error rate, and represents a more conservative approach. The model applied included the fixed effects of transport type, lairage duration, and stress level, as well as their two-way interactions, and the random effect was slaughter day nested within lairage duration.

	Results

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Average hot carcass weight was 88.6 kg and lean yield was 56.7%, measured by the Hennessey Grading probe. None of the experimental treatments affected (P > 0.15) carcass yield traits (results not shown).

Plasma concentrations of cortisol and lactate, as well as muscle metabolites, are shown in Table 1. Both plasma cortisol and lactate were increased (P < 0.001) by the high stressor treatment, but were not affected by type of transportation (P > 0.45) or lairage duration (P > 0.20). Even though there were transport x stress (P = 0.013) and lairage x stress (P < 0.001) interactive effects on plasma lactate concentration, lactate concentrations were always higher in the plasma of pigs subjected to the high preslaughter stressor level compared with minimally handled pigs (results not shown). Furthermore, a transport x lairage interaction (P = 0.012) was detected for plasma lactate concentration, but plasma lactate concentrations did not differ (P = 0.146) among the transport and lairage treatment combinations (results not shown). Even though LM glycogen content was not affected (P = 0.62) by the long and rough transport, muscle lactate concentration was increased (P < 0.01) by longer, rougher transportation, resulting in greater (P = 0.06) glycolytic potentials (Table 1). Lairage had no (P > 0.15) effect on muscle metabolites. The high stressor treatment, on the other hand, clearly decreased (P < 0.001) muscle glycogen, and increased (P < 0.001) LM lactate concentrations, which was reflected by a decrease (P < 0.001) in glycolytic potential. Results of the temperature and pH measurements in the LM are shown in Table 2. Long and rough transport tended (P = 0.08) to lower pH at 30 min postmortem. There were no (P > 0.20) effects of lairage duration on LM pH or temperature. Even though transport and lairage treatments did not affect (P > 0.48) ultimate (24-h) pH values of the LM, the high stressor treatment decreased (P < 0.001) LM pH at both 30 min and 3 h postmortem, and increased (P < 0.001) ultimate (24-h) pH. Muscle temperature was increased (P < 0.001) by high preslaughter stress at both 40 min and 3 h postmortem. At 3 h postmortem, the stress-related increase was 1.9°C after long lairage, approximately twice that of pigs subjected to short lairage (lairage x stress; P = 0.042; results not shown).

	Discussion

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Effects of Transport
Differences between the two transport treatments were small and did not elicit major metabolic changes. The long transport treatment aimed at imposing a higher level of both physical and psychological stress on the pigs than the short transport treatment. This was done not just by increasing its duration, but by making the journey more unpleasant through frequent braking and accelerating and by selecting minor roads with bends, roundabouts, and speed bumps. In sheep (Ruiz-de-la-Torre et al., 2001) and pigs (Bradshaw et al., 1996), rough transport resulted in elevated cortisol concentrations; this was not observed, however, in the present experiment. During longer transports, animals have more time to adapt to transportation conditions after the stressful events, such as removal from their home pens, commingling, and loading onto trucks, and actually arrive in a better condition at the processing plant than after a short transport (Augustini and Fischer, 1982; Pérez et al., 2002a). In the present experiment, the last third of the transport was smooth for all pigs, which might have promoted a general habituation to transport in the long transport group. However, the tendency toward a more rapid postmortem acidification of muscle and an increased electrical conductivity for the long and rough transport treatment in combination with long lairage are clues that the long transport might have indeed imposed a somewhat higher stress level on the pigs. Although cortisol measurements do not support the assumption, this stressor must have been of a psychological rather than physical nature because glycolytic potential tended to be increased (and not decreased) by long and rough transport. Warriss et al. (1983) and Brown et al. (1999) found no effect of transport on muscle glycogen. During low-intensity exercise, fatty acids are the preferred source of energy (Romijn et al., 1993; Klein et al., 1994). In consequence, fat oxidation may have provided sufficient energy for physical movement occurring during transportation, which could explain the absence of an effect of transport on muscle glycogen stores. Conversely, Leheska et al. (2003) showed that transportation dramatically decreased antemortem glycogen reserves before slaughter. Differences between Leheska et al. (2003) and the current study might be related to the low environmental temperature of –10°C and the very low loading density in their study. In humans, the higher metabolic rate due to cold exposure increased carbohydrate oxidation almost sevenfold, whereas fat oxidation rose less than twofold (Vallerand and Jacobs, 1989). In the present study, an explanation for the somewhat higher glycolytic potential after long transport may be that pigs of the short transport treatment, left in their pens after the removal of the pigs for the long transport, became agitated by the unusual disturbance and actually became more active than their counterparts that were on transport. The effect of muscle glycogen on pork quality may be mediated, at least in part, by its relationship to ultimate pH (Leheska et al., 2003; Hambrecht et al., 2004b). In the present study, however, ultimate pH was not affected by the type of transport. Thus, the precise physiological effects of transport on pigs could not be conclusively described by measurements of plasma lactate, cortisol, and/or muscle glycolytic potential.

Effects of Lairage
Independent of the type of preceding transport, there were limited effects of decreasing lairage duration from 3 h to between 30 and 45 min, which is regarded as too short a time to allow pigs to recover from previous transport stress (De Smet et al., 1996; Milligan et al., 1998; Pérez et al., 2002b). The glycolytic potential was similar for both lairage durations. Generally, results of the present study indicate that lairage durations between 30 min and 3 h did not promote glycogen depletion or replenishment. There are few studies available that have measured muscle glycogen levels in response to various lairage durations. Honkavaara (1989), Fernandez et al. (1992), and Stalder et al. (1998) compared short (0 to 2.5 h) with long lairage durations (16 to 24 h), and found no effect or a decreasing effect of long lairage on muscle glycogen reserves.

Conversely, Warriss et al. (1999) demonstrated that the effect of lairage on muscle glycogen was nonlinear in broilers, and that prolonging lairage durations could abolish initial increases in muscle glycogen. The effects of lairage duration on pork quality, within the rather short ranges that were studied in the present experiment, were not likely mediated by the effects on glycolytic potential.

Effects of Stress
Results of the high preslaughter stressor treatment were very similar to those previously observed and discussed by Hambrecht et al. (2004a,b). Unlike other studies (van der Wal et al. 1999; Hambrecht et al., 2004b), but in agreement with D’Souza et al. (1998) and Channon et al. (2000), meat color seemed to be unaffected by stressor level. For all other traits, including plasma lactate and cortisol, muscle metabolites, pH, and temperature, as well as most pork quality attributes, the effects of preslaughter stress superseded the effects of any preceding treatment, such as transport and lairage.

Effects of Stress in Relation to Preceding Handling Factors
Single and combined effects of the three treatment factors on some of the most important pork quality attributes are displayed in Figure 1, whereas the effects on physiological variables are shown in Figure 2. Because some of the attributes show a far larger variation than others, changes caused by the variation of one or several treatment factors are expressed relative to the pooled standard deviation of the respective trait. Although the effects of short and smooth transport were not unequivocally positive, this treatment, with the 3 h of lairage and minimal stressor treatment combination, was selected to represent the zero-line as "optimal" preslaughter handling. As shown in Figure 1, the rough transport conditions and/or short lairage alone had little effect on pork quality. However, suboptimal transport and lairage conditions exacerbated the effects of high preslaughter stress, especially those traits related to water-holding properties. For example, the high stressor treatment alone increased electrical conductivity values by 1.1 SD (56%), compared with the "optimal" treatment; however, when, in addition, the lairage duration was shortened, the increase in electrical conductivity was 1.7 SD (88%). These findings were supported by the physiological variables presented in Figure 2. Compared with the effects of high stress alone, plasma lactate, cortisol, and muscle temperature were increased when concomitantly transport conditions were worsened and/or lairage duration decreased, which resulted in an increased rate of postmortem muscle acidification. In agreement with these findings, increases in plasma lactate, muscle temperature, and rate of early postmortem glycolysis have been associated with reductions in pork quality (Wismer-Pedersen and Briskey, 1961; Offer 1991; Hambrecht et al., 2004b).

View larger version (58K): [in this window] [in a new window]   Figure 1. Single and combined effects of preslaughter handling factors on various pork quality attributes. Absolute differences between means were divided by the pooled SD (SDp) of all treatment means for the respective attribute. Short (50 min) and smooth transport, long (3 h) lairage, and minimal stress before slaughter were regarded as "optimal" preslaughter treatment and represent the zero-line. Bars indicate deviation from this zero-line by the variation of only one treatment factor (long [3 h] and rough transport, short [<45 min] lairage, or high preslaughter stress) or the combined variation of several treatment factors. 24-h pH = ultimate pH (SDp = 0.11); EC = electrical conductivity (SDp = 3.04); 24-h DL = drip loss percent after storage for 24 h (SDp = 1.19); L* = a measure of lightness (SDp = 2.68); a* = a measure of redness (SDp = 1.10); b* = a measure of yellowness (SDp = 0.74). Within one attribute, least squares means of the corresponding bars that do not have a common letter differ, P <0.05.

View larger version (38K): [in this window] [in a new window]   Figure 2. Single and combined effects of preslaughter handling factors on plasma cortisol (pooled SD [SDp] = 24.68) and lactate concentrations (SDp = 5.02) measured at exsanguination, muscle temperature measured at 40 min postmortem (SDp = 1.08), as well as muscle lactate measured at 135 min postmortem (SDp = 14.18). Absolute differences between means were divided by the SDp of all treatment means for the respective attribute. Short (50 min) and smooth transport, long (3 h), short (<45 min) lairage, and minimal stress before slaughter were regarded as "optimal" preslaughter treatments and represent the zero-line. Bars indicate deviation from this zero-line by the variation of only one treatment factor (long [3 h] and rough transport, short [<45 min] lairage, or high preslaughter stress) or the combined variation of several treatment factors. Within one attribute, least squares means of the corresponding bars that do not have a common letter differ, P < 0.05.

	Implications

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Transport and lairage conditions, in the range that was investigated in the present study, had little influence on pork quality. However, when coinciding with high stress in the immediate preslaughter period, a long and rough transport, as well as too short a lairage duration, may aggravate negative effects of high pre-slaughter stress. The greatest improvements in pork quality can be achieved by decreasing stress in the immediate preslaughter period.

¹ Correspondence: P.O. Box 220, NL-5830 AE Boxmeer (phone: +31 (0) 485 589 742; fax: +31 (0) 485 568 183; e-mail: ellen.hambrecht{at}nutreco.com).

Received for publication April 9, 2004. Accepted for publication September 24, 2004.

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