J. Anim. Sci. 2005. 83:900-907
© 2005 American Society of Animal Science
Preslaughter handling effects on pork quality and glycolytic potential in two muscles differing in fiber type composition
E. Hambrecht*,1,
J. J. Eissen*,
D. J. Newman
,
C. H. M. Smits*,
M. W. A. Verstegen
and
L. A. den Hartog*,
* 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
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Abstract
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The objective of the present experiment was to investigate the effects of transportation, lairage, and preslaughter stressor treatment on glycolytic potential and pork quality of the glycolytic longissimus and the oxidative supraspinatus (SSP) or serratus ventralis (SV) muscles. In a 2 x 2 x 2 factorial design, 384 pigs were assigned randomly either to 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. Muscle samples were taken from the LM at 135 min and from the SSP at 160 min postmortem for determination of the glycolytic potential and rate of glycolysis. At 23 h postmortem, pork quality was assessed in the LM and the SV. Effects of transport and lairage conditions were similar in both muscle types. Long transport increased (P < 0.01) the glycolytic potential and muscle lactate concentrations compared with short transport. Both long transportation and short lairage decreased (P < 0.01) redness (a* values) and yellowness (b* values) of the LM and SV. In combination with short lairage, long transport decreased (P < 0.05) pork lightness (lower L* values), and electrical conductivity was increased (P < 0.05) after long transport. Several interactions between stress level and muscle type (P < 0.001) were observed. High preslaughter stress decreased (P < 0.001) muscle glycogen in both the LM and SSP, but this decrease was greater in the LM. Lactate concentrations were increased (P < 0.001) only in the LM by high preslaughter stress. Increases in ultimate pH (P < 0.001) and decreases in a* values (P < 0.01) were greatest in the SV, whereas increases in electrical conductivity (P < 0.001) were greatest in the LM. The lack of interactions among transportation, lairage, and muscle type was attributed to the relatively minor differences in stress among treatments. It was concluded that, in glycolytic muscle types such as the LM, the high physical and psychological stress levels associated with stress in the immediate preslaughter period have a greater effect on the water-holding capacity of the meat and may promote PSE development. Conversely, oxidative muscle types tend to have higher ultimate pH values and produce DFD pork in response to intense physical activity and/or high psychological stress levels preslaughter.
Key Words: Glycogen • Meat Quality • Muscle Type • Pigs • Preslaughter Handling • Stress
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Introduction
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Various stages during preslaughter handling, such as transportation (Pérez et al., 2002a
; Leheska et al., 2003), lairage (Milligan et al., 1998; Pérez et al., 2002b), and stress immediately before slaughter (van der Wal et al., 1999; Hambrecht et al., 2004b) were shown to affect pork quality. Most of the effects have been attributed to alterations in the rate and extent of pH decline postmortem, which in turn are related to muscle glycolytic potential (an estimate of muscle glycogen in vivo) and a stress-induced increase in glycolysis. Due to its size and accessibility, the LM is the most frequently assessed muscle; however, muscles consist of various fiber types that can be classified on the basis of their contractile and metabolic properties into slow-twitch oxidative and fast-twitch glycolytic types, as well as an intermediate type (Solomon and Dunn, 1988). "Oxidative" compared with "glycolytic" muscle fibers have a lower glycolytic potential (Monin et al., 1987; Fernandez et al., 1994), lower glycolytic capacity (Vøllestad et al., 1992), higher sensitivity to epinephrine (Górski, 1978; Fernandez et al., 1995b), and a lower threshold force, resulting in earlier recruitment at low-intensity exercise (Køpke et al., 1984; Lacourt and Tarrant, 1985). It can be expected that muscles, depending on their fiber-type composition, react differently to the physical and psychological stressors associated with preslaughter handling. Therefore, the objective of the present experiment was to investigate whether the response to various levels of physical and psychological stress caused by transportation, lairage, and preslaughter stressor treatments are dependent on the metabolic type of the muscle.
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Materials and Methods
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The Animal Care and Ethics Committee of the University of Nijmegen, The Netherlands, approved the experimental protocol.
Animals and Experimental Design
All pigs were commercial Yorkshire x (Large White x Landrace), halothane-free endproducts of the Hypor pig breeding company (Regina, Canada). In a completely randomized design, equal numbers of barrows and gilts (n = 384) were assigned to one of eight treatments in a 2 x 2 x 2 factorial arrangement, with two types of transport (short and smooth vs. long and rough), two lairage durations (long [considered optimal] vs. short [considered suboptimal]), and two stress levels immediately before slaughter (minimal or high). 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 subsequent weeks. Transport types and preslaughter 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 from a total 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 for all pigs was 0.45 m2/100 kg BW. Pigs of the first two treatments (minimal and high preslaughter stress pigs of the long transport treatment) were loaded and driven for 2 h on minor roads with frequent roundabouts and speed bumps, resulting in the truck changing speed, stopping, and starting periodically. Meanwhile, pigs of the other two treatments (minimal and high preslaughter stress pigs of the short transport treatment) were loaded on a second, larger but otherwise similar truck (double deck, all pigs were 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, on 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 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 135 min postmortem, when carcasses had passed from the rapid-chilling tunnel into the cooler, muscle samples were taken from the LM at the last rib, and at 160 min postmortem, another sample was taken from the supraspinatus muscle (SSP) 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 fraction was neutralized with 10 M KOH. Lactate in the supernatant fraction was determined spectrophotometrically with lactate dehydrogenase and NAD (Bergmeyer, 1974). Glycogen in the supernatant fraction was enzymatically hydrolyzed to glucose by incubation with amyloglucosidase (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 fraction was neutralized with 10 M KOH. Glucose was determined spectrophotometrically by the hexokinase method (Bergmeyer, 1974). The concentrations of glucose-6-phosphate and glucose were not separately determined but are included in the glycogen determination. The glycolytic potential was calculated as the sum of 2 x [glycogen] + [lactate] (Monin and Sellier, 1985).
Measurements
At 23 h postmortem, various cuts of the left carcass side were fabricated for final meat quality assessment. Measurements were taken in the LM at the level of the third lumbar vertebra and in the center of the serratus ventralis muscle (SV). Ultimate pH was measured using a portable pH meter (Portamess 911 pH, Knick Elektronische Messgeräte, Berlin, Germany) equipped with a probe-type glass electrode (LoT406, Mettler Toledo, Switzerland), and electrical conductivity was measured using the LF-Star (Ingenieurbüro Matthäus, Nobitz, Germany). Objective color (L*, a*, and b*) was measured on a freshly cut surface 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.
Statistical Analyses
Data were analyzed as a completely randomized design with treatments in a 2 x 2 x 2 factorial arrangement using 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 least squares means were adjusted according to the Tukey-Kramer method to ensure the overall significance level of P 
0.05. The model included the fixed effects of muscle type, transport conditions, lairage duration, and stressor level, as well as all two-way interactions, and the random effect of slaughter day nested within lairage.
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Results
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Results of the muscle metabolites and meat quality measurements for the two muscles are presented in Table 1, whereas the effects of the various preslaughter treatments on muscle metabolites and pork quality attributes of both muscles are presented in Tables 2, 3, and 4. In the LM, representing a glycolytic muscle type, both muscle metabolites and pork quality attributes were measured. Because the SV was not accessible for sampling in the intact carcass side, for the oxidative muscle type, metabolites were measured in the SSP and pork quality attributes in the SV muscle.
Muscle type affected (P < 0.05) all traits (Table 1
). Electrical conductivity, however, did not differ (P = 0.336) for either the LM or the SV. The LM was associated with a higher glycolytic potential, increased lactate formation during the first 135 min postmortem, and a higher residual glycogen level compared with the oxidative SSP muscle (P < 0.001). Regarding pork quality attributes, the LM was paler (higher L* value), less red (lower a* value), more yellow (higher b* value), and exhibited a lower ultimate pH than the SV muscle (P < 0.001).
Transportation had a similar effect on both muscle types (Table 2). Increasing the length and roughness of transport resulted in increased (P < 0.01) glycolytic potential due to increased (P < 0.001) lactate production, but residual glycogen levels were unaffected (P > 0.85). Pork from long and rough transported pigs was less red (P < 0.01) and less yellow (P < 0.001). Yet, lightness (L*) for both the LM and the SV was only affected by the transport treatment when lairage duration was short (transport x lairage interaction, P < 0.05; Table 5), with long vs. short transportation resulting in a darker (P < 0.05) muscle color (results not shown). Independent from muscle type or any other treatment, the long transport treatment decreased water-holding capacity as indicated by increased (P < 0.05) electrical conductivity values. Ultimate pH tended to be higher (P = 0.077) after long vs. short transport.
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Table 5. Least squares means for muscle metabolites and pork quality attributes presented for each muscle separatelya
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Decreasing the duration of lairage from 3 h to less than 45 min tended to decrease both glycolytic potential (P = 0.083) and residual glycogen levels (P = 0.063; Table 3). Short lairage duration had no effect on the LM lactate concentrations, whereas lactate content of the SSP was decreased (P < 0.05) by short lairage (lairage x muscle interaction, P < 0.05; Table 5). Short, compared with long, lairage led to a darker (P < 0.01), less red (P < 0.05), and less yellow (P < 0.05) pork color (Table 3). The decrease in redness (a*) seemed to be greater in the SV than in the LM (lairage x muscle interaction, P < 0.05; Table 5). Lairage did not affect (P > 0.05) ultimate pH (Table 3); however, lairage affected electrical conductivity response to the high stressor treatment, with short vs. long lairage resulting in a numerically larger, stress-induced increase in electrical conductivity in both the LM and SV (lairage x stress interaction, P < 0.05; results not shown).
Stressor level affected all traits that were measured but many of the effects depended on the type of muscle. In both muscle types, glycolytic potential was decreased (P < 0.001) by the high stressor treatment (Table 4). The decrease in residual glycogen in the LM was greater than in the SSP (stress x muscle interaction, P < 0.001; Table 5). In the LM, the decreased glycogen levels were reflected in an increased lactate formation, but there was no effect on lactate formation in the SSP (stress x muscle interaction, P < 0.001; Table 5). Independent of muscle type, pork color was darker (P < 0.001) and less yellow (P < 0.001) after high vs. minimal preslaughter stress (Table 4). Redness (a*) of pork was unaffected in the LM but, in the SV, redness was decreased (P < 0.01) by the high stressor treatment (stress x muscle interaction, P < 0.001; Table 5). In both the LM and SV, there was an increase (P < 0.05) in ultimate pH noted, but this increase seemed to be greater in the SV than the LM (stress x muscle interaction, P < 0.001; Table 5). In contrast, electrical conductivity was increased more in the LM than in the SV (stress x muscle interaction, P < 0.001; Table 5). Moreover, the minimal stressor treatment resulted in the lowest conductivity value in the LM compared with all other measurements; however, the high preslaughter stressor treatment caused a higher electrical conductivity than the minimal stressor treatment in both the LM and SV, as well as the high stressor treatment in the SV.
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Discussion
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In the present experiment, the LM and SV were chosen for pork quality assessment based on their metabolic and contractile properties, economical importance, and susceptibility to quality problems. Muscle glycolytic potential was measured in the LM, predominantly containing fast-twitch glycolytic fibers, and the SSP, a muscle of the shoulder containing a high portion of slow-twitch oxidative muscle fibers similar to the SV (Ruusunen et al., 1988; Warriss et al., 1990; Bee et al., 1999). For simplicity, the SV and SSP muscles will be referred to as oxidative in the discussion of results, whereas the LM will be referred to as glycolytic. The SSP muscle was chosen for determination of glycolytic potential because, as opposed to the SV muscle, this muscle was accessible for sampling in the intact carcass side early postmortem.
Few studies have assessed both glycolytic potential and pork quality beyond ultimate pH in muscles other than the LM. Generally, differences in the present experiment between the LM and the SSP and the SV are in agreement with several studies showing that, compared with glycolytic muscles, oxidative muscles have a lower glycolytic potential (Monin et al., 1987; Fernandez et al., 1994), a darker color (Warner et al., 1993; Brewer et al., 2001), and a higher ultimate pH (Barton-Gade and Olsen, 1987; Monin et al., 1987; Warner et al., 1993). Additionally, Warner et al. (1993) reported less exudate for oxidative than glycolytic muscles, which contradicts the results of the current study, which showed similar electrical conductivity values (a measure for water-holding capacity) for both the SV and LM. However, Warner et al. (1993) selected carcasses with a wide range in pork quality, including more than 20% with an initial muscle pH of less than 5.8 (less than 1% of carcasses in the present study had initial LM pH values less than 5.8; results not shown).
The focus of the present study was the difference in responses to preslaughter handling treatments rather than the differences between the two different muscle types. The transport, lairage, and stressor treatments were chosen to result in various psychological and physical stress levels (Bradshaw et al., 1996; Pérez et al., 2002b; Hambrecht et al., 2004b) that are frequently encountered in commercial practice.
Effects of Transport
The physical activity and psychological stress that is associated with transportation varies depending on the type of transport. Transport, in general, was shown to be stressful for pigs (Becker et al., 1985; Geverink et al., 1998), and even more so in rough, as opposed to smooth, journeys (Bradshaw et al., 1996). As a result, both the physical activity and the psychological stress level were probably higher in the long and rough vs. the short and smooth transport treatment. Oxidative muscle fibers are preferentially recruited at low intensity exercise levels (Køpke et al., 1984; Lacourt and Tarrant, 1985). Because the physical activity level associated with transport is probably low, the long and rough transport treatment was expected to decrease glycogen to a larger extent in the oxidative muscle, as demonstrated in sheep by Monin and Gire (1980). In the present study, however, both the SSP and the LM reacted similarly to the transport treatments, with no glycogen depletion detected in long-transport pigs; nonetheless, long and rough transportation increased lactate formation, resulting in increased glycolytic potential. This is in apparent contradiction with the ultimate pH values, which tended to be increased after long transport. Karlsson et al. (1994) observed differences in ultimate muscle pH in pigs with similar glycogen levels; however, the glycogen depletion pattern among fibers was different, suggesting that glycogen distribution within a muscle and not total muscle glycogen concentration affect pork quality.
Effects of Lairage
Lairage is not a stress factor itself but is meant to provide a rest for pigs to recover from the stress associated with transportation. Prolonged lairage may promote fighting among pigs, however, and lead to energy depletion (Warriss, 2003). The tendency toward a slight increase in muscle glycogen level in the present study indicates that pigs rested during lairage. There are some indications that glycogen replenishment during recovery from physical exercise depends on muscle fiber type in rats (Górski et al., 1978; McLane and Holloszy, 1979) and man (Fairchild et al., 2003). In the present study, however, no differences in glycogen repletion during lairage were observed in the LM and SSP. The physical activity associated with either of the transport treatments was probably too low to induce different patterns of glycogen depletion and replenishment in muscles differing in metabolic type. Effects on pork quality were probably mediated by differences in the psychological stress level and not by differences in physical activity associated with the various transportation and lairage combinations. Secretion of epinephrine in response to a stressor can lead to both glycogen depletion and increased glycolysis (Fernandez et al., 1995a; Jensen et al., 1999). Oxidative muscle fibers are characterized by greater vascularisation and higher ß-adrenergic receptor density (Essén-Gustavsson et al., 1992; Jensen et al., 1995) and are, therefore, more sensitive to epinephrine. Yet, similar to physical activity, psychological stress levels related to the transportation and lairage treatments were probably too low to exert different effects on the two muscle types.
Effects of Preslaughter Stress
The high preslaughter stressor treatment was previously shown to be associated with a high level of both physical activity and psychological stress, causing dramatic effects on pork quality (Hambrecht et al., 2004a,b). In agreement with the previously mentioned differences in epinephrine sensitivity and responses to physical activity, effects of this preslaughter stressor treatment are dependent on the muscle type. Although a large increase in lactate concentration was noted only in the LM, it cannot be concluded that the high stressor treatment did not lead to a higher rate of lactate formation in the oxidative muscles. At 160 min postmortem, when SSP muscle samples were taken, almost the entire SSP glycogen stores had been converted into lactate. To assess whether lactate production rate was also increased in the SSP in response to high preslaughter stress, muscle samples should have been taken at an earlier time. This is supported by electrical conductivity values, which were increased in both the LM and the SV. The increase was more than twice as large in the LM (+59.4%) compared with the SV (+22.4%). The SV, on the other hand, was more sensitive to high preslaughter stress regarding pork color. Additionally, the SV showed a greater increase in ultimate pH than the LM, which is in agreement with studies demonstrating a larger pH-increasing effect of preslaughter stress on oxidative than glycolytic muscles (Warriss et al., 1995; Brown et al., 1998). Barton-Gade and Olsen (1987) compared stress-susceptible pigs with stress-resistant pigs, and found an increased incidence of PSE in glycolytic muscles such as the LM, whereas oxidative muscles, including the SV, showed an increased incidence of the DFD condition.
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Implications
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Increasing duration and roughness of transportation, as well as shortening lairage time, affected both the glycolytic longissimus muscle from the loin and the oxidative supraspinatus and serratus ventralis in a similar manner. However, the considerably higher physical and psychological stress level associated with preslaughter handling may promote pale, soft, and exudative pork development in predominantly glycolytic muscles, whereas oxidative muscles may develop dark, firm, and dry pork.
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 June 3, 2004.
Accepted for publication December 17, 2004.
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Abstract
Introduction
