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Effects of High Temperature on Multiple Parameters of Broilers In Vitro and In Vivo¹

Institute of Animal Science, Chinese Academy of Agricultural Science, State Key Laboratory of Animal Nutrition, Beijing, 100094, China

² Corresponding author: mhzhang{at}iascaas.net.cn

	ABSTRACT

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The effects of high temperature on multiple parameters of broilers were evaluated both in vitro and in vivo. In the in vitro study, the bilateral musculus fibularis longus muscles of 8 broilers were isolated and incubated at either 41.5 or 44.5°C. The greater incubation temperature increased mitochondrial H₂O₂ production by 28.0% (P < 0.0001), malondialdehyde concentration by 16.8% (P = 0.0368), and lactate concentration by 33.0% (P < 0.0001) and decreased mitochondrial Ca²⁺-ATPase activity by 19.6% (P = 0.0001). In the in vivo study, 180 four-week-old broilers were kept in 3 controlled-environment chambers for 3 wk. High temperature increased mitochondrial H₂O₂ production (P < 0.05) in liver, malondialdehyde concentration in liver and breast muscle, and lactate concentration in breast muscle (P < 0.05). In addition, it inhibited mitochondrial Ca²⁺-ATPase activity in muscle and liver (P < 0.05). High temperature also significantly decreased initial pH and increased L*, drip loss, and shear force of broiler breast muscle.

Key Words: high temperature • mitochondrial hydrogen peroxide • calcium-ATPase • broiler • breast meat quality

	INTRODUCTION

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The reported incidence of pale, soft, and exudative (PSE) meat in commercial poultry plants has been as high as 40 to 47% (Owens et al., 2000a; Woelfel et al., 2002) and has been increasing. Reducing the incidence of PSE meat is a major challenge for the poultry industry.

High ambient temperature increases the likelihood of meat becoming PSE. Consequently, the incidence of PSE poultry meat is greater in summer than in winter (McCurdy et al., 1996). Sustained heat stress significantly decreases initial pH (pH_i) and water-holding capacity (WHC) and increases the color L* (lightness) value of turkey breast muscles (McKee and Sams, 1997; Owens et al., 2000b). Similar effects on poultry meat have been observed under acute or short-term preslaughter heat stress (Northcutt et al., 1994; Sandercock et al., 2001).

Heat stress increases lipid peroxidation in broilers (Altan et al., 2000) and laying hens (Bollengier-Lee et al., 1998; Whitehead et al., 1998). Mujahid et al. (2005) showed that mitochondrial superoxide radical production in chicken skeletal muscle increases under acute heat stress. In vitro studies have indicated that reactive oxygen species (ROS) influence the calcium release channel or Ca²⁺-ATPase activity (Castilho et al., 1996; Kourie, 1998; Lounsbury et al., 2000) and induce Ca²⁺ overload in smooth muscle of the human intestine (Bielefeldt et al., 1997), in heart cells of rats (Kaminishi et al., 1989) and in PC₁₂, a neurosecretory cell line (Wang and Joseph, 2000). In turn, Ca²⁺ overload leads to increased glycolysis through activation of adenosine monophosphate-activated protein kinase and to increased lactate production (Hardie, 2003). In another study, broiler erythrocytes produced more lactate when loaded with Ca²⁺ (Imaeda, 2000). Accumulation of lactate in postmortem muscle induced a rapid decline in muscle pH when carcass temperature was high, resulting in extensive protein denaturation, with the meat showing ultimate PSE characteristics (Warriss and Brown, 1987). Thus, it is likely that high temperature leads to increased ROS, which in turn causes deregulated intracellular Ca²⁺ levels, resulting in a series of other metabolic changes that ultimately affect meat quality. However, no single report has thus far systematically documented the effects of heat stress on ROS production, Ca²⁺ regulation, malondialdehyde (MDA), and lactate content at the same time. We believe that gathering such information is an important first step in establishing the mechanisms by which poultry meat quality is affected by heat stress. Here we address this issue and present our findings from both in vivo and in vitro experiments.

	MATERIALS AND METHODS

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Birds and Husbandry

Arbor Acres broilers purchased from a local breeding company were reared in electrically heated batteries from d 1, following the procedures described in the Arbor Acres Broilers Husbandry Manual. For in vitro studies, 8 two-week-old birds were used. For in vivo studies, 180 four-week-old birds were randomly allocated to 3 treatment groups: a high-temperature group, a control group, and a paired-feeding group. Each group consisted of 6 replicates, and each replicate was a cage with 10 birds. The high-temperature group was housed in a controlled-environment chamber with daily high cyclic temperature from 28 to 34°C and ad libitum feeding. The other groups were housed in 2 controlled-environment chambers at 22°C; one group was fed ad libitum (control group) and the other was subject to pair-feeding with the high-cyclic group (paired-feeding group). All controlled-environment chambers were kept at 50% RH, and the trial lasted 3 wk.

Blood samples were taken by venipuncture (brachial vein) from12 birds in each group at 35, 42, and 49 d of age (experiment 2). On d 49, twelve birds from each group were killed by exsanguination, and the liver and breast were isolated quickly and placed directly into liquid nitrogen to isolate mitochondria and to allow later determination of lipid peroxidation and lactate content. Eighteen birds in each group were killed as part of a commercial program (hang shackles, exsanguination, defeathering, evisceration) to measure breast meat quality.

Muscle Isolation and Incubation

Muscles were isolated and incubated as described by Sandercock and Mitchell (2004), with modifications. Briefly, eight 2-wk-old birds were anesthetized by intraperitoneal injection of pentobarbital (100 mg/kg of BW). The bilateral musculus fibularis longus muscles were carefully excised with intact tendons and immediately placed in ice-cold saline solution (0.9%), weighed, and fixed to a stainless-steel clip to maintain the resting length. The muscles were first preincubated at 41.5°C for 20 min in 15 mL of gassed (95% O₂ and 5% CO₂) Krebs-Henseleit physiological saline solution (pH 7.4 and with 5.5 mM glucose). The paired muscles from each bird were randomized among treatments and controls. Eight muscles were incubated in medium at 41.5°C as a control group, and the others were incubated in medium at 44.5°C as a treatment group. All muscles were incubated for 2 h, with gassing every 30 min. The muscles were then placed into liquid nitrogen, and 5 mL of medium from each incubation was collected and frozen at –20°C for creatine kinase (CK) and lactate dehydrogenase (LDH) activity determination.

Isolation of Mitochondria

Muscle mitochondria were isolated by differential centrifugation as described by Thakar and Ashmore (1975), with modifications. Briefly, the muscles were first minced and incubated at 4°C for 5 min in an isolation buffer (100 mM sucrose, 50 mM Tris-HCl, 5 mM MgCl₂, 10 mM EDTA, and 0.18 M KCl, pH 7.4) containing 1 mM adenosine triphosphate (A-3377, Sigma, St. Louis, MO), 0.2% BSA (738238, Roche, Basel, Switzerland), and 1 mg/mL of Nagarse (9014-01-1, Sigma), with a muscle-to-medium ratio of 1:10 (g:mL). For the in vitro study, 0.2 g of muscle from each animal was processed, whereas for the in vivo study, 2 g of muscle from each animal was used. The mixture was then gently homogenized using either a glass homogenizer (5 passages; in vitro samples) or a tissue grinder (10,000 cycles/min, 15 s, model T18, IKA Corp., Guangzhou, China; in vivo samples). Next, the homogenate was incubated for an additional 5 min on ice with stirring, after which an equal volume of isolation medium (containing BSA and adenosine triphosphate but no Nagarse) was added, and the homogenate was homogenized again. The final homogenate was centrifuged at 480 x g for 10 min, and the supernatant was centrifuged once again at 8,700 x g for 10 min. The resultant mitochondrial pellet was resuspended in medium containing 300 mM mannitol, 10 mM KH₂PO₄, and 10 mM Tris-HCl, pH 7.4.

Hepatic mitochondria were isolated by differential centrifugation as described by Cawthon et al. (1999), with modifications. Briefly, 1 g of liver was placed in 10 mL of isolation medium [220 mM mannitol, 70 mM sucrose, 2 mM N-2-hydroxyethyl piperazine-N'-ethanesulfonic acid (HEPES), 0.2 mg/mL of BSA, and 1 mM ethylene glycol tetraacetic acid, pH 7.4], minced, and homogenized with a tissue grinder (10,000 cycles/min, twice for 15 s). The homogenate was then centrifuged twice for 10 min at 1,300 x g, and the supernatant was centrifuged again at 8,700 x g for 10 min. The final mitochondrial pellet was resuspended in medium containing 220 mM mannitol, 70 mM sucrose, and 2 mM HEPES, pH 7.4. Mitochondrial protein concentrations were determined using the Coomassie Brilliant Blue G-250 reagent (27816, Fluka, Buchs, Switzerland) with BSA as a standard.

Determination of Mitochondrial H₂O₂ Production and Ca²⁺-ATPase Activity

Production of H₂O₂ was determined as described by Garait et al. (2005), with modifications. Briefly, the following components were sequentially added to an incubation chamber: 2.5 mL of incubation buffer (145 mM KCl, 30 mM HEPES, 15 mM KH₂PO₄, 3mM MgCl₂, and 0.1mM ethylene glycol tetraacetic acid), 100 µL of mitochondrial suspension or H₂O₂ standard, 100 µL of superoxide dismutase (600 U/mL), 100 µL of horseradish peroxidase (180 U/mL; P6782, Sigma), and 100 µL of 15 mM homovanillic acid (H1252, Sigma). The reaction was started by adding 100 µL of 300 mM succinate, and the mixture was incubated at 37°C. The fluorescence intensity was taken at the 0- and 30-min time points using a fluorescence spectrophotometer (Hitachi 850, Hitachi Ltd., Tokyo, Japan) with an excitation wavelength of 315 nm and an emission wavelength of 425 nm. Mitochondrial Ca²⁺-ATPase activity was determined following Anand et al. (1977).

Biochemical Analyses

All biochemical analyses were performed using commercial colorimetric diagnostic kits from the Jiancheng Biochemical Institute (Nanjing, China). The following kits were used: A032 for CK, A020 for LDH, A003 for MDA, and A019–2 for lactate.

Breast Meat Quality Evaluation

When birds were killed as part of a commercial program, the left pectoralis muscle was immediately isolated and cut into 6 parts within 15 min postmortem: 2 parts were placed directly in liquid nitrogen for pH_i determination, 2 parts were placed in plastic bags and kept at 4°C for 24 h for ultimate pH determination, and 2 parts were weighted and covered with self-sealing plastic bags and hung at 4°C for 24 h. At 24 h postmortem, these 2 fillets were reweighed, and drip loss was calculated. Muscle pH was determined using the iodoacetate method described by Sams and Janky (1986) with a pH meter (model pHSJ-4A, Shanghai Precision and Scientific Instrument Co., Shanghai, China) equipped with a combination-probe glass electrode (model E-201-C, Shanghai Precision and Scientific Instrument Co.).

The right pectoralis muscle was isolated and placed in a plastic bag at 4°C for 24 h. At 24 h postmortem, 3 fillets were cut from the right pectoralis muscle, and meat color (lightness, L*; redness, a*; and yellowness, b* values) was measured on the cut surface of each fillet using a colorimeter (model MSC-S, Shanghai Precision and Scientific Instrument Co.). A new cut was made on the fillet before each L* value measurement to avoid any surface changes caused by contact with water or air. The remaining muscle was heated in a plastic bag in a water bath at 80°C for 30 min. After cooling at room temperature, shear force was measured in triplicate as described by Gwartney et al. (1992) with a shear device (G. R. Electric Manufacturing Co., Manhattan, KS)

Statistical Analyses

The experiments were conducted in a completely randomized fashion. There were 8 replicates for in vitro study and 6 replicates for in vivo study. A paired Student’s t-test was applied to data collected from the in vitro study using the univariate procedure of SAS (SAS Institute Inc., Cary, NC). The general linear models procedure of SAS (SAS Institute Inc.) was applied to data collected from in vivo studies for variant analysis. Duncan’s multiple range test was applied to evaluate the differences among means, and P < 0.05 was considered significant.

	RESULTS AND DISCUSSION

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Mitochondrial H₂O₂ Production and Lipid Peroxidation

Under in vitro conditions, high temperature increased mitochondrial H₂O₂ production (P < 0.0001) by 28% and MDA concentration (P = 0.0368) by 28.0% in musculus fibularis longus muscles (Table 1). Under in vivo conditions, high temperature increased mitochondrial H₂O₂ production (P < 0.05) and MDA concentrations in liver tissues and breast muscles compared with the normal-temperature controls (i.e., the control and pair-feeding groups; Table 2). There were no significant differences for the 2 parameters between the control and the pair-feeding groups (P > 0.05; Table 2), indicating that the increased mitochondrial H₂O₂ production and MDA concentrations were not a result of the reduced food intake under high-temperature conditions.

Via the Fenton reaction, H₂O₂ reacts with mitochondrial Fe²⁺ to produce the highly reactive hydroxyl radical (OH·), which in turn can cause lipid peroxidation and increased MDA concentrations (Bhuyan et al., 1986). Thus, the increased mitochondrial H₂O₂ production was consistent with the increased MDA concentration in livers and breast muscles of broilers under high temperature conditions.

Mitochondrial Ca²⁺-ATPase Activity and Lactate Content

As shown in Tables 1 and 3, under in vitro conditions, high temperature inhibited mitochondrial Ca²⁺-ATPase activity by 17.9% (P = 0.0001) and elevated lactate concentration by 33.0% (P < 0.0001) in musculus fibularis longus muscles. Under in vivo conditions, high temperature inhibited mitochondrial Ca²⁺-AT-Pase activity in breast muscle (P < 0.05), but not in the liver, as compared with the pair-feeding group (Table 4). Compared with the control group, high temperature inhibited mitochondrial Ca²⁺-ATPase activity (P < 0.05) in both liver and muscle (Table 4). Lactate levels were greater in the high-temperature group than in the control group (P < 0.05) and slightly greater than in the pair-feeding group (Table 4). In contrast, no significant differences in the 2 parameters were observed between the control group and the pair-feeding group, indicating that the observed differences between the high-temperature group and the 2 control groups were not caused by differences in food intake.

Losses of CK and LDH

As shown in Table 3, in the in vitro system, high temperature increased LDH (P = 0.0009) and CK activities (P = 0.0114) in the incubation medium. Similarly, in the in vivo system, high temperature increased plasma LDH (P < 0.05) and CK activities (P < 0.05; Table 4).

Skeletal muscle is the major source of CK and LDH, and 99% of CK in plasma is derived from muscle. One consequence of Ca²⁺ overload is leakage of CK from skeletal muscle (Mitchell et al., 1999; Sandercock and Mitchell, 2003, 2004). Increased plasma CK, as observed here, is likely indicative of increased Ca²⁺ concentration in the skeletal muscle, which in turn is indicative of inhibition of mitochondrial Ca²⁺-ATPase activity by high-temperature-induced ROS upregulation.

In the in vivo system, a significant difference in CK levels was again observed between the 2 control groups, but not in LDH levels. One possibility for this difference is that restrictions on food intake in the pair-feeding group may have downregulated the overall metabolic rate, resulting in decreased plasma CK levels. Indeed, Hocking et al. (1998) noted that food restriction reduces plasma CK activity in turkeys.

Meat Quality of Breast Muscles

As shown in Table 5, high temperature decreased breast muscle pH_i (P < 0.05), and this can be regarded as a natural outcome of the observed lactate increase in breast muscle. This finding is consistent with previous studies (McKee and Sams, 1997; Sandercock et al., 2001), in which high temperature decreased the breast muscle pH_i of broilers and turkeys.

It has been suggested that in pork, rapid declines in pH while the carcass temperature is still high can result in muscle protein denaturation and influence meat color and WHC (Warriss and Brown, 1987; Offer, 1991; Santos et al., 1994). Our results are consistent with this scenario; however, no consensus has been reached as to whether muscle protein denaturation induces changes in the color and WHC of poultry meat. According to Van Laack et al. (2000), compared with normal-colored breast meat, the sarcoplasmic protein solubility of pale-colored breast meat was significantly reduced, yet no difference was observed in total protein solubility. The authors thus argued that protein denaturation was not a key factor in the low WHC of the pale breast meat from broilers. Similarly, Van Laack et al. (2000) reported that the total protein from chicken muscles was not prone to denaturation. In contrast, according to Barbut et al. (2005), the levels of salt-soluble proteins of broiler PSE meat were lower than those of normal meat, and the heavy myosin chain was also denatured. In line with this, similar observations have been reported for turkey (Rathgeber et al., 1999).

In summary, the results of this study show that high temperature conditions significantly increase mitochondrial ROS production, inhibit Ca²⁺-ATPase activity, increase lactate content and CK and LDH losses from muscle, decrease pH_i, and increase the L* value, drip loss, and shear force of poultry breast meat. These results support our hypothesis that increased ROS production is the key event by which heat stress exerts its multiple effects. High temperatures may increase levels of ROS and thereby inhibit Ca²⁺-ATPase activity. This leads to an elevated free-Ca²⁺ load that results in increased lactate concentration and decreased muscle pH_i, which ultimately result in the decline in meat quality. However, this hypothesis needs to be evaluated rigorously in the future.

	ACKNOWLEDGMENTS

 
We thank J. Zhang (University of Dundee, Dundee, UK) for proofreading an earlier draft of this manuscript. This work was funded by grant 2004CB11750–7 to M. Zhang from the National Basic Science Program of China.

	FOOTNOTES

 
¹ Supported by grant 2004CB11750-7 from National Basic Research Program of China.

Received for publication August 25, 2007. Accepted for publication April 13, 2008.

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