PROCESSING, PRODUCTS, AND FOOD SAFETY

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1 PROCESSING, PRODUCTS, AND FOOD SAFETY Effects of constant and cyclic heat stress on muscle metabolism and meat quality of broiler breast fillet and thigh meat Z. Y. Zhang, 1 G. Q. Jia, 1 J. J. Zuo, Y. Zhang, J. Lei, L. Ren, and D. Y. Feng2 College of Animal Science of South China Agricultural University, Guangzhou , China ABSTRACT This study investigated the effects of constant and cyclic heat stress on muscle metabolism and meat quality of broiler breast fillet and thigh meat from 4 to 6 wk of age. Male Arbor Acres (AA) broilers (n = 270, 4 wk old) were raised under different temperature conditions: standard (temperature was 23 C); constant high temperature (temperature was 34 C); and cyclic high temperature (temperature was 36 C from 1000 h to 1600 h and 23 C from 1600 h to 1000 h). On d 42, broilers were stunned and sampled. The results showed that chronic high temperature significantly decreased the proportion of breast muscle and significantly increased the proportion of thigh muscle (P < 0.05). The moisture concentration was significantly higher in the breast muscle of the birds exposed to constant high temperature (P < 0.05), whereas the protein content was significantly lower (P < 0.05) and fat deposition was significantly higher (P < 0.05) in the breast muscle of the birds exposed to constant or diurnal cyclic high temperature than those grown under standard temperature. The breast and thigh muscle of the birds grown INTRODUCTION High ambient temperature has been recognized as one major environment factor influencing poultry production (Lin et al., 2006; Lu et al., 2007). The optimal temperature for performance is 19 to 22 C for laying hens and 18 to 22 C for growing broilers (Lin et al., 2006). When ambient temperature is higher than the thermoneutral temperature, heat stress may occur. This can lead to higher body temperature and thus heat burden. The adverse effects of heat stress include high mortality, decreased feed consumption, and lower BW gain in broiler chickens (Cooper and Washburn, 1998; Quinteiro-Filho et al., 2010). Heat stress has 2012 Poultry Science Association Inc. Received February 26, Accepted May 23, The first 2 authors contributed equally to this study. 2 Corresponding author: fengdy@scau.edu.cn under constant high temperature had significantly higher lightness, cook loss, and shear force (P < 0.05) and significantly lower initial ph (ph i ), ultimate ph (ph u ), and redness compared with those grown under standard temperature (P < 0.05). The ph i, ph u, and redness were significantly lower (P < 0.05) while the lightness and shear force were significantly higher for the breast muscle of the chickens raised under diurnal cyclic high temperature (P < 0.05) than those grown under standard temperature. In contrast, lightness and yellowness of thigh muscle were significantly higher (P < 0.05) in the chickens grown under diurnal cyclic high temperature than under standard temperature. Breast and thigh muscle of broilers exposed to constant high temperature produced higher (P < 0.05) lactic acid and pyruvate kinase activities than those exposed to the standard temperature. These results indicated that chronic heat stress significantly increased lactate production, reduced meat ph value by accelerating meat glycolysis, and eventually reduced meat quality. Key words: constant heat stress, cyclic heat stress, meat quality 2012 Poultry Science 91 : been considered as one of the significant environmental factors affecting meat quality, which could accelerate postmortem glycolytic metabolism, and result in pale, exudative meat characteristics in chickens (Northcutt et al., 1994; McCurdy et al., 1996; McKee and Sams, 1997; Sandercock et al., 2001). Acute heat stress has been proved to reduce the chicken meat quality (Froning et al., 1978; Northcutt et al., 1994; Holm and Fletcher, 1997; Petracci et al., 2001). It has been reported that the acute heat stress can increase lightness (L*) and decrease redness (a*) and yellowness (b*) in the breast muscle of broilers (McCurdy et al., 1996; Wynveen et al., 1999; Petracci et al., 2004; Akşit et al., 2006). This may be caused by the denaturation of sarcoplasmic proteins which results in scattering of light (McKee and Sams, 1997; Owens et al., 2000). Sandercock et al. (2001) speculated that acute heat stress could induce alterations in blood acid/ base status and disruptions in muscle membrane integ- 2931

2 2932 Zhang et al. rity, which may be associated with changes in ante- and postmortem breast muscle glycolytic metabolism, leading to alterations in meat characteristics. The majority of heat stress studies have investigated the effect of acute heat stress on broiler performance, physiological response, or meat quality, but only a few researchers have investigated the effect of chronic heat stress on the meat quality of broilers (Petracci et al., 2001; Lu et al., 2007; Quinteiro-Filho et al., 2012). Interestingly, Lu et al. (2007) observed that chronic heat stress increased breast meat lightness and drip loss of Arbor Acres (AA) broilers. This suggests that the chronic heat stress may reduce the broiler meat quality. The hypothesis of this research was that chronic heat stress would increase the production of lactate in muscle, which in turn increase the rate of ph decline and subsequently affect the broilers meat quality. Thus, the objective of the present study was to investigate the effect of 2 wk of heat stress (constant or diurnal cyclic high ambient temperature) on meat quality and muscle metabolism in AA broilers. MATERIALS AND METHODS Experimental Design In total, 500 one-day-old male AA broiler chicks were obtained from a commercial hatchery. The birds were fed with a complete starter diet containing 21% CP and 3,000 kcal/kg of ME between d 1 and 21 and a basal grower diet containing 19.7% CP and 3,140 kcal/ kg of ME between d 22 and 42. Birds had ad libitum access to feed and water and were subjected to a photoperiod of 22L:2D throughout the whole period of the study. This study was approved by the Animal Care and Use Committee of South China Agricultural University. Temperature was set at 32 C at 1 d of age and decreased gradually so as to reach about 23 C by 28 d of age. On d 29, 270 broilers with similar BW (1,299 ± 21 g) were transferred to 3 temperature-controlled chambers ( m), where all chickens were equally distributed to 3 treatments for 6 replicates with 270 colony cages ( cm). The temperature regimens applied to the chickens were 1) standard constant temperature at 23 C as standard; 2) constant high temperature at 34 C; and 3) diurnal cyclic temperature at 36 C from 1000 h to 1600 h and 23 C from 1600 h to 1000 h. Sample Collection On d 42, 2 birds from each replicate were randomly selected, stunned by an electrical stunner (40V: alternating current, 400 Hz for 5 s), and then slaughtered within 5 min via exsanguination from the left jugular vein. Within 15 min postmortem, the entire left pectoralis major (breast) and left satorius (thigh) of broilers were sampled and stored at 4 C for determination of ph, meat color, cook loss, shear force value, pyruvate acid, and lactic acid. The right breast and thigh muscle were sampled for determination of the content of moisture, protein, and fat. Chemical Composition Analysis The moisture, protein, and fat contents of samples were analyzed according to the official standard methods of analysis (AOAC, 1990). Moisture content was determined by heating samples in an oven at 85 C until constant weight. Protein content was measured using a micro-kjeldahl apparatus. Total lipids content was determined by ether extraction for 16 h. ph and Color Muscle ph was determined using a portable ph meter (Testo 205, Germany) at 45 min (initial ph; ph i ) and 24 h postmortem (ultimate ph; ph u ). The ph meter was calibrated using 2-point method against standard buffer solutions with ph values of 4.0 and 7.0. The ph value was expressed as the average of the 3 measurements. At 24 h postmortem, meat color was measured by the Chroma meter CR-410 (Minolta, Suita-shi, Japan). Color was measured on the dorsal side of the breast fillet at 3 locations and on 3 locations on the medial (bone) side of thigh. Color was reported in the CLE-LAB trichromatic system as L*, a*, and b* values. Cook Loss The muscles were stored at 4 C until 24 h postmortem, and then they were cooked in a water bath at 80 C in plastic bags to an internal temperature of 72 C for 30 min. The cooked samples were cooled in cold running tap water for 20 min before blotting and weighing. The mass changes were expressed as a percentage of initial mass. Shear Force Value Samples used for cooking loss analysis were also used to measure shear force. Shear force value was measured as described by Chen et al. (2007) using a digital meat tenderness meter (model C-LM3, Northeast Agricultural University, Harbin, China). Each sample was measured 3 times, and the average of 3 readings was used as the shear force value of the sample and was expressed in Newtons. Pyruvate Acid and Lactic Acid Samples of breast and thigh muscles were taken for analysis for the concentrations of pyruvate acid and lactic acid at 24 h after slaughter. The concentration of skeletal muscle pyruvate and lactic acids were mea-

3 CHRONIC HEAT STRESS IN BROILERS 2933 Table 1. Average BW and fillet weight of broilers on d 42 (n = 12) Item Treatment 1 42-d weight (g) 2,255 b 1,992 c 2,435 a 46.3 <0.001 Breast weight 2 (g) 217 b 165 c 241 a 7.4 <0.001 Thigh weight 2 (g) 169 a 151 b 170 a Cyclic = diurnal cyclic high temperature (temperature was 36 C from 1000 h to 1600 h and 23 C from Breast weight or thigh weight was one side of broilers. sured using commercially available colorimetric diagnostic kit (Nanjing Jiancheng Bioengineering Institute, Nanjing, China). Activities of Hexokinase, Pyruvate Kinase, and Lactate Dehydrogenase Samples of breast and thigh muscles were taken at 45 min postmortem for analysis for the activities of hexokinase, pyruvate kinase, and lactate dehydrogenase. Muscle hexokinase was assayed according to the method of Crabtree and Newsholme (1972) in which a reduction of NADP +, through a coupled reaction with glucose-6-phosphate dehydrogenase, is determined spectrophotometrically by measuring the increase in absorbance at 340 nm. Muscle pyruvate kinase was determined according to the method of Malcovati and Valentini (1982). The activity of muscle lactate dehydrogenase was used as the marker of glycolytic metabolism and determined by monitoring the rate of decrease in the absorbance of NADH following the reduction of pyruvate to lactate at 340 nm at 25 C. Statistical Analysis All data were subjected to a one-way ANOVA procedure of SPSS 19.0 for windows (SPSS Inc., Chicago, IL, 2010), and the differences among means were separated by Duncan s multiple range test. A probability value of less than 0.05 was described to be statistically significant. RESULTS Body Weight, Breast Weight, and Thigh Weight Table 1 shows BW, breast weight, and thigh weight of broilers on d 42. Heat exposure significantly affected average BW and breast weight of broilers (P < 0.05). Average BW of broilers in cyclic high temperature group and constant high temperature group had decreased by 8.1% (P < 0.05) and 18.2% (P < 0.05), respectively. Broilers in cyclic high temperature group had lower breast weight (P < 0.05) and similar thigh weight (P > 0.05) when compared with those in standard temperature group. Broilers from constant high temperature group had lower breast weight (P < 0.05) and thigh weight (P < 0.05) than those in standard temperature group. When muscle weights were expressed relative to BW (data not shown), the proportion of breast muscle from broilers in constant high temperature group or cyclic high temperature group was lower than that of broilers in standard temperature group (P < 0.05), whereas those of thigh muscle were higher (P < 0.05). Chemical Composition of Breast and Thigh Meat The chemical composition of breast and thigh meat is shown in Table 2. After 2 wk of heat exposure, breast meat composition was affected significantly by heat exposure, but not for thigh meat. Breast meat from birds in constant high temperature group had higher (P < 0.05) moisture and fat and lower (P < 0.05) protein content than those in standard temperature group. Breast meat from birds in diurnal cyclic high temperature group had lower (P < 0.05) protein content when compared with those in standard temperature group. Meat Quality High ambient temperature had a significant influence on meat quality (Table 3). The data on meat color showed that breast and thigh meat from broilers in constant high temperature group had higher (P < 0.05) L*, cook loss, and shear force value and lower (P < 0.05) ph i, ph u, and a* than those in standard temperature group. Breast muscle from broilers in diurnal cyclic high temperature group had higher (P < 0.05) L* and lower (P < 0.05) ph i, ph u, and a* than those in standard temperature group; thigh muscle from broilers in diurnal cyclic high temperature group had higher (P < 0.05) L*, b*, and lower a* than those in standard temperature group. Postmortem Glycolysis Changes The pyruvate and lactate concentrations are presented in Table 4. In the case of breast, the broilers

4 2934 Zhang et al. Table 2. The chemical composition of breast and thigh muscle (wet basis; n = 12) Item Treatment 1 Breast Moisture (%) b a b 0.20 <0.001 Protein (%) b c a 0.21 <0.001 Fat (%) 0.94 ab 0.98 a 0.80 b Thigh Moisture (%) Protein (%) Fat (%) Cyclic = diurnal cyclic high temperature (temperature was 36 C from 1000 h to 1600 h and 23 C from 1600 exposed to constant high temperature had higher lactic acid concentration in comparison with other groups, and broilers in diurnal cyclic high temperature group had a higher pyruvate concentration than the broilers in constant high temperature group or standard temperature group (P < 0.05). In the case of thigh, the broilers in constant high temperature group had higher pyruvate and lactic acid concentrations than the broilers in the other groups (P < 0.05), and no difference was observed between the birds in diurnal high temperature group and in standard temperature group. The data of HK, PK, and LDH are also shown in Table 4. The breast meat of the broilers in constant high temperature group had higher LDH and PK activities than those in standard temperature group (P < 0.05), and no significant difference was observed for HK activities among the treatments (P > 0.05). Meanwhile, Table 3. The meat quality of breasts and thighs (n = 12) Item 1 Treatment 2 the thigh meat of the broilers exposed to high temperature (constant high temperature group and diurnal cyclic high temperature group) had lower LDH and HK activities than those in standard temperature group (P < 0.05), and the broilers in constant high temperature group had a higher PK activity than those in other groups. DISCUSSION The effect of 2 wk of heat exposure on AA broilers was investigated. High ambient temperatures significantly affect broiler performance, especially between 4 and 6 wk of age (Geraert et al., 1996), so we used chickens in the finishing period (4 to 6 wk old). As expected, chronic heat stress had a negative effect on growth performance of broilers (data not shown), Breast ph i 6.25 b 6.21 b 6.36 a 0.01 <0.001 ph u 5.78 b 5.72 b 5.88 a Meat color L* b a c 0.49 <0.001 a* 14.1 b b a b* Cook loss (%) 9.43 ab a 8.58 b Shear force (N) a a b Thigh ph i 6.06 a 5.90 b 6.09 a 0.02 <0.001 ph u 5.87 a 5.81 b 5.88 a Meat color L* a a b 0.22 <0.001 a* b b a b* a a b Cook loss (%) b a b Shear force (N) b a b 0.56 < ph i = initial ph; ph u = ultimate ph; L* = lightness; a* = redness; b* = yellowness. 2 Cyclic = diurnal cyclic high temperature (temperature was 36 C from 1000 h to 1600 h and 23 C from 1600

5 CHRONIC HEAT STRESS IN BROILERS 2935 Table 4. Activities of 3 key enzymes of glycolysis and the products of glycolysis (n = 12) Item 1 Treatment 2 Breast Lactic acid (mmol/g protein) 0.94 b 1.04 a 0.86 b Pyruvate (μmol/mg protein) a c b 0.01 <0.001 LDH (U/g protein) 1, a 2, a 1, b PK (U/g protein) 1, ab 1, a 1, b HK (U/g protein) Thigh Lactic acid (mmol/g protein) 0.83 b 1.04 a 0.82 b 0.02 <0.001 Pyruvate (μmol/mg protein) b a b LDH (U/g protein) 2, c 2, b 2, a <0.001 PK (U/g protein) 2, ab 3, a 2, b HK (U/g protein) 8.46 c 9.48 b a 0.29 < HK = hexokinase; PK = pyruvate kinase; LDH = lactic dehydrogenase. 2 Cyclic = diurnal cyclic high temperature (temperature was 36 C from 1000 h to 1600 h and 23 C from 1600 similarly as previously reported (Geraert et al., 1996; Temim et al., 1998). Moreover, when expressed as a percentage of BW, chronic high temperature decreased the proportion of breast muscle and increased the proportion of thigh muscle. Temim et al. (2000) reported that the proportion of p. major was lower at 32 C than at 22 C, but those of the sartorius and gastrocnemius were higher. Reduced breast proportion and increased thigh proportion were also found by Ain Baziz et al. (1996). Breast meat of birds in diurnal cyclic high temperature and constant high temperature group showed a significant decrease in protein content than those in standard temperature group, which is in agreement with Geraert et al. (1996), who reported that high ambient temperature significantly decreased body protein content, protein gain, and protein retained:protein intake in broilers, suggesting that chronic heat stress changes protein metabolism, decreases protein synthesis, and increases catabolic rate. As it is reported, high environmental temperature decreased the muscle protein synthesis and accelerated protein breakdown (Yunianto et al., 1997). In finishing broiler chickens, chronic heat exposure induced a marked decrease in protein synthesis rates, as measured directly in different muscles; muscle protein turnover was lower under hot conditions than at thermoneutrality. At 32 C, protein synthesis was more susceptible than proteolysis, at least in the pectoralis major and the gastrocnemius muscles, which thereby reduced muscle protein deposition (Temim et al., 2000). It has been clearly demonstrated that heat stress lowers protein synthesis by changing ribosomal gene transcription (Jacob, 1995; Temim et al., 1998). Thus, we speculate that the high environmental temperature can lower the ribosomal capacity, lead to decreased rate of protein synthesis, and result in the reduction of the protein deposition. Excessive fat deposition in broilers is a worldwide concern. Environment is an important factor influencing fat deposition in birds (Sands and Smith, 1999). As it is reported, chronic exposure of broilers to a high ambient temperature is associated with enhanced abdominal, subcutaneous, and intermusclar fat deposits (Ain Baziz et al., 1996; Geraert et al., 1996). Our findings of AA broilers exposed to constant high temperature had significantly higher fat deposition in breast muscle compared with control standard group, which is similar to Howlider and Rose (1987). The increased fat deposition could be related to reduction in basal metabolism and physical activity (Howlider and Rose, 1987; Geraert et al., 1996). Preslaughter stressors such as heat stress, feed withdrawal, transport, and water deprivation may influence meat quality (Mota-Rojas et al., 2006). Preslaughter heat stress could accelerate rigor mortis development, which induces a faster ph decline, lower ph u, and higher L* value in turkey meat and leads to pale, exudative meat characteristics in chickens and turkeys (Northcutt et al., 1994; McKee and Sams, 1997), and these detrimental effects are exacerbated in older birds (Sandercock et al., 2001). In the present experiment, heat-exposed AA broilers had lower ph value, higher L*, and lower a* than the birds in standard temperature group; breast ph u were lower than those of thigh muscle, which could be explained by higher lactate concentrations in breast muscle (Table 3). Higher L* values in heat-stress AA broilers are in agreement with the reports of Lu and Zhang (2007) and McKee and Sams (1997), which showed that chronic heat stress increased the lightness in muscle. The results of decreased a* value indicated that there are more oxidized myoglobin in the heatexposed birds muscle (Mancini and Hunt, 2005). Water-holding properties are of great importance, because retention and gains or losses of water affect the weight and thus the economic value of chicken products. Additionally, the content and distribution of water within muscles may affect the visual appearance as well as tenderness and juiciness of meat. It was report-

6 2936 Zhang et al. ed that acute and chronic heat stresses cause the poor water-holding properties (McKee and Sams, 1997; Molette et al., 2003). Heat stress caused a high metabolic rate rigor mortis, resulting in pronounced protein denaturation (Channon et al., 2000; Deng et al., 2002). The severe protein denaturation affects the protein s ability to bind water and results in poor water-holding capacity (Klont et al., 1994), which was reflected by higher drip loss and cooking loss. There was a positive correlation between cook loss and drip loss (Woelfel et al., 2002). In our study, the broilers in constant high temperature group have higher meat cooking losses than those in the other group, which is similar to the result of Sandercock et al. (2001), who showed a higher drip loss for breast meat of heat-stress birds (32.5 C and RH of 67.1%). These findings were supported by the lower ph value and the more intramuscular fat content observed with the constant high temperature treatment. After exsanguination, circulatory failure cuts both nutrient and oxygen supply to the muscle cells. In an attempt to maintain homeostasis, which is energy consuming, the remaining glycogen and glucose is then anaerobically degraded, resulting in the accumulation of lactic acid (Pösö and Puolanne, 2005). In the present study, the birds in constant high temperature group had a higher lactic acid concentration than the birds in the other group, indicating that the meat of broilers in constant high temperature group had more glycogen converted to lactic acid. Glycolysis is a very important metabolic pathway in the postmortem period, and the key enzymes of anaerobic metabolism are HK, PEP, and PK. The main product of glycolysis is pyruvate, and LDH is a key enzyme in the conversion of pyruvate to lactate under anaerobic conditions in the muscle. Thus, we determined the activities of HK, PK, and LDH. The result showed that the thigh muscle of broilers in constant high temperature or diurnal cyclic high temperature group had higher HK activities than those in standard temperature group, indicating that preslaughter heat stress can mobilize more glucose to supply the energy by aerobic metabolism in the broilers. The muscle of broilers in constant high temperature or diurnal cyclic high temperature group had higher PK activities than those in standard temperature group, indicating that the muscle of broilers exposed to high temperature produced more pyruvate to convert lactate for providing energy than those of standard temperature group, which is consistent with the concentration of lactate (Table 3). The breast muscle of broilers in constant high temperature or diurnal cyclic high temperature group had higher LDH activities than birds in standard temperature group, which showed that the breast meat of broilers in constant high temperature or diurnal cyclic high temperature group had more pyruvate converted to lactate, leading to lower ph in the muscle and resulting in poor meat quality. In conclusion, the present results confirm that constant heat stress increased the production of lactate in muscle, which in turn increased the rate of ph decline and subsequently decreased the quality of breast and thigh meat. Cyclic heat stress also can decrease the quality of breast and thigh meat to a certain extent. Moreover, chronic heat stress decreased the proportion of breast muscle, increased the proportion of thigh muscle, and changed the breast chemical composition, characterized by more fat content and less protein concentration. REFERENCES Ain Baziz, H., P. A. Geraert, J. C. F. 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