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Effect of Chronic Heat Exposure on Fat Deposition and Meat Quality in Two Genetic Types of Chicken¹

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

² Corresponding author: wenj{at}iascaas.net.cn or zhanghf6565{at}vip.sina.com

	ABSTRACT

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The effects of chronic heat stress on growth, proportion of carcass and fat deposition, and meat quality were investigated in 2 genetic types of chickens. One hundred and eight 5-wk-old male chickens from a commercially fast-growing strain (Arbor Acres, AA) and a locally slow-growing species (Beijing You chicken, BJY) were kept in the following conditions: constant optimal ambient temperature at 21°C and ad libitum feeding (21AL), constant high ambient temperature at 34°C and ad libitum feeding (34AL), and constant optimal ambient temperature 21°C and pair-fed to the 34AL chickens (21PF). The results showed that feed intakes were decreased by heat exposure in both type of chickens at 8 wk of age (P < 0.001). At 34°C, AA broilers exhibited greatly decreased weight gain (22.38 vs. 61.45 g/d for 21AL) and lower breast proportion compared with 21AL, while the relevant indices of BJY chickens were not affected in hot condition. Abdominal fat deposition of BJY chickens was enhanced by heat exposure (P < 0.05). Fat deposition of AA broilers was decreased in heat-exposed and pair-fed chickens. Abdominal and intermuscular fat deposition in 34AL birds, however, were enhanced compared with 21PF birds (P < 0.01). The L* values, drip loss, initial pH, and shear force of breast meat in BJY chickens were not affected by treatments. In AA birds, chronic heat stress increased L* values and drip loss compared with 21AL, but pH and shear force were not affected by treatments. The results from this study indicated that the impact of heat stress was breed dependent and that BJY chickens showed higher resistance to high ambient temperature, which could be related to their increased feed efficiency and deposition of abdominal fat under heat exposure.

Key Words: heat exposure • chicken • meat quality • fat deposition

	INTRODUCTION

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Genetic selection for broiler performance over the last few decades has led to tremendous improvements in growth (McKay et al., 2000; Deeb and Cahaner, 2002). However, this growth potential has been achieved under optimal conditions and may not occur under suboptimal environmental conditions. High ambient temperature has been recognized as one of the major environmental factors influencing poultry production. Continuous selection for increased growth rate may have increased sensitivity of broilers to high ambient temperature (Cahaner et al., 1995). The effects of heat exposure on growth rate, feed intake, and meat yield of commercial broilers have been well documented (Yalcin et al., 2001). Seasonal heat-stress has been reported to accelerate postmortem glycolytic metabolism leading to biochemical changes in muscle and the production of pale, exudative meat characteristics in chickens and turkeys (McKee and Sams, 1997; Sandercock et al., 2001). These detrimental effects are exacerbated in older birds (Sandercock et al., 2001).

Chronic exposure of growing pigs to a high ambient temperature is associated with enhanced lipid metabolism in the liver and the adipose tissue (Kouba et al., 1999, 2001). As a consequence, plasma triglyceride uptake and storage is facilitated in the adipose tissues, which results in greater fatness (Kouba et al., 2001). Increased fatness in long-term heat-exposed pigs was accompanied by the changes in the distribution of adipose tissues: a shift of body fat toward internal sites (Le Dividich et al., 1998) and an increased weight of flare fat and increased ratio of flare fat:back fat + flare fat were reported (Kouba et al., 2001). The change in fat distribution in these heat-exposed pigs would appear to increase heat loss and represented an adaptation to high ambient temperature (Le Dividich et al., 1998; Kouba et al., 2001). Heat-exposed chickens also exhibit enhanced fat deposition (Ain Baziz et al., 1990, 1996; Geraert et al., 1996). The relationship between the change of fat deposition and the adaptation to high ambient temperature of chickens has not been reported.

Behavioral, physiological, and metabolic responses to aversive situations depend on genetic background and prior experience of the animals (Terlouw, 2004). The negative effect on growth rate was found to be greater in broilers with a higher genetic potential for growth rate than in broilers with lower growth rates (Cahaner and Leenstra, 1992). The objective of the present study was to evaluate the effects of excessive heat exposure on carcass composition, fat deposition, and meat quality in 2 breeds of chickens reared in China. A commercial breed of chickens (Arbor Acres, AA) were compared with a slow-growing local species (Beijing You, BJY), which has highly acceptable texture and flavor characteristics and is resistant to suboptimal growth conditions.

	MATERIALS AND METHODS

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Animals and Management
Two hundred 1-d-old male chickens from commercial AA broiler (from a commercial hatchery, Huadu Broiler Company, Beijing, China) and BJY stocks (from Institute of Animal Science of Chinese Academy of Agricultural Sciences, which is a BJY chicken conservation organization in Beijing, China) were reared in floor pens for up to 5 wk of age. Ambient temperature was gradually decreased from 32°C at 1 d to 21°C at 3 wk of age (rate of decrease: 3°C during the first week, 4°C during the second and the third weeks).

At wk 5, 108 broilers from each species with similar BW (AA broiler, 1,377 ± 62 g; BJY chicken, 412 ± 25 g) were transferred to 3 temperature-controlled chambers, where all chickens were equally distributed to 3 treatments for 6 replicates of 6 chickens each: ambient temperature of 21°C with ad libitum access to feed (21AL); ambient temperature of 34°C and fed ad libitum (34AL); and ambient temperature of constant 21°C and pair-fed to the amount consumed by the 34AL group (21PF). Relative humidity was maintained at 50 ± 5%.

A complete starter diet with 21.5% CP and 3,022 kcal/kg of ME from 0 to 3 wk, and a grower diet with 19.3% CP and 3,093 kcal/kg of ME from 4 to 8 wk were used. Continuous light and unlimited water were provided throughout the experiment.

Slaughter and Dissection Procedure
Feed intake was measured daily at 0900 h. Live weights were recorded after a 12-h feed withdrawal at 5 and 8 wk of age. At 8 wk of age and following a 12-h period of feed deprivation, 18 birds of each treatment were killed by bleeding from a single neck cut, which severed the right carotid artery and jugular vein. After bleeding, birds were scalded in water at 60°C for 45 s prior to defeathering, evisceration, and tissue sample collection.

Abdominal fat, composed of fat tissues surrounding the proventriculus and gizzard lying against the inside abdominal wall and around the cloaca, was collected as described by Ain Baziz et al. (1996). Subcutaneous fat and intermuscular fat were taken from the leg according to Ricard et al. (1983) and Ain Baziz et al. (1996). The subcutaneous fat included the skin and associated subcutaneous fat of thigh and drumstick, and the fat associated with the sartorius muscle. The skin and subcutaneous fat were removed carefully by lifting it and slowly scraping the undersurface with a scalpel according to Bochno et al. (2004). The fat associated with the sartorius muscle was taken off carefully using a forceps according to the method of Ricard et al. (1983). Intermuscular fat of leg mainly existed in the thigh region, and the fat located between the individual muscles of the thigh was collected carefully as outlined by Ricard et al. (1983).

Breast muscle and leg were removed, according to the standard method of dissection as described by Jensen (1984). Carcass, dissected fat and muscle tissues, and legs were weighed.

Meat Quality Measurements
Muscle samples were collected from the left side of the pectoral major muscle for the assessment of drip loss and shear force. The entire left side of the pectoral minor muscle was measured for color determination. The upper one-third of the pectoral major muscle from the right side was used for pH measurement. The pH values were determined 15 min postslaughter (initial pH, pHi) and after chilling for 24 h at 4°C in self-sealed plastic bags (ultimate pH, pH_u), using a portable pH meter (IQ150, IQ Scientific Instruments Inc., Carlsbad, CA) equipped with a stainless electrode (pH57-SS).

The color measurement was made by a spectrocolorimeter (model WSC-S, Shanghai Shenguang Ltd., China) using the CIELAB system (L* = lightness; a* = redness; b* = yellowness). Each sample was scored on 3 different areas. Drip loss was determined by the filter paper method of Kauffman et al. (1986). The left breast was weighed and placed in plastic bags and freely suspended using steel wire hook at 4°C. Muscle contact with the inside surface of the bag was kept to a minimum. Muscle samples were wiped and weighed 24 h later to evaluate the drip loss, which was expressed as a percentage of the initial muscle weight.

Shear force was measured using a universal Warner-Bratzler testing machine (G. R. Electric Manufacturing Co., Manhattan, KS). Muscle samples were stored at 4°C for 24 h and were then individually cooked in a water bath at 80°C in plastic bags to an internal temperature of 70°C. The samples then were removed and chilled to room temperature. Strips [1.0 cm (width) x 0.5 cm (thickness) x 2.5 cm (length)] parallel to the muscle fiber were prepared from the medial portion of the meat and sheared vertically (Molette et al., 2003). Shear force was expressed in kilograms.

Statistical Analysis
Results are presented as means with their standard deviations. The data were classified by treatment and replicate, and the data from all replicates were pooled into a completely randomized block design. The data were subjected to ANOVA to determine the effect of treatments on traits using the GLM procedure of SAS software (SAS Institute, 1989). Data from indices of meat quality under different treatments were subjected to correlation analysis to determine the link between the characteristics of meat. Mortality data was subjected to ² analysis.

	RESULTS

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Growth Performance
Effects of heat exposure on feed intake, BW gain, and final body weight are presented in Table 1. In the case of AA broilers, feed intake, final BW, and weight gain of heat-exposed birds (34AL) were significantly lower than those obtained for the 21AL group (P < 0.001), but feed:gain ratio of 34AL group was significantly higher than those of the 21AL group (P < 0.05). Heat-exposed chickens had lower weight gain than that of pair-fed birds (P < 0.05).

During the growth phase in the temperature-controlled rooms, the mortality of AA broilers was 36, 8.3, and 5.6% in 34AL, 21AL, and 21PF groups, respectively. All of the BJY groups survived the experimental feeding period.

Proportion of Carcass, Muscle, and Fat Tissues
The proportion of carcass, breast muscle, and abdominal fat in BW and the proportion of subcutaneous fat and intermuscular fat in the leg are presented in Table 2. When the AA broilers were compared with the 21AL group, high temperature exposure increased carcass percentage (P < 0.01) and leg proportion (P < 0.05), but decreased breast proportion. At 21°C, the proportions of carcass, breast, and leg were not affected by feed restriction. With ad libitum feeding, heat stress resulted in decreased fat content of birds. For example, subcutaneous fat and intermuscular fat deposition decreased significantly (P < 0.01), whereas abdominal fat decreased slightly (P > 0.05). At the same feeding level, heat stress enhanced abdominal fat and intermuscular fat deposition (34AL vs. 21PF; P < 0.01). In BJY chickens, high temperature had no effect on carcass, breast, and leg proportions when compared with the control group (21AL). Feed restriction decreased breast and leg proportion (P < 0.05) compared with the other 2 treatments. Abdominal fat pad was enhanced significantly in heat-exposed birds (34AL vs. 21PF; P < 0.05), whereas subcutaneous fat and intermuscular fat deposition had no difference among different treatments (P > 0.05).

	DISCUSSION

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Feed efficiency under hot conditions differs somewhat between mammals and birds. Feed to weight gain ratio is enhanced in hot conditions in chickens (Howlider and Rose, 1989; Ain Baziz et al., 1996). On the other hand, an improvement in feed efficiency was often observed in rats and pigs under heat exposure (Christon et al., 1984; Rinaldo and Le Dividich, 1991). Ain Baziz et al. (1996) considered that birds adapted to hot conditions somewhat differently than mammals, suggesting changes in regulation. In the present study, the feed efficiency of heat-stressed AA broilers was decreased, in line with the above reports on chickens. On the other hand, the results obtained for BJY chickens were more in line with those reported for pigs. Therefore, the results in the present work suggested that the regulatory mechanism of BJY chickens at high ambient temperature was different to that functioning in AA broilers. The results also showed that BJY chickens had a higher feed efficiency, which would account for the maintenance of growth under hot conditions.

The proportion of carcass under hot conditions increased in AA broilers. Ain Baziz et al. (1996) reported similar results for chickens held at a constant temperature of 32°C. These findings could be explained by reduced feather proportion to improve heat losses (Geraert et al., 1996). In the present study, heat-exposed AA broilers also had significantly reduced breast muscle proportion, which meant that meat yield of AA broilers was decreased by heat exposure. The carcass, breast, and leg proportion of BJY chickens did not change under the constant heat stress at 34°C, which strengthened the conclusion that BJY chickens had higher resistance to high ambient temperature.

The present results also showed that AA broilers exposed to heat stress had slightly decreased abdominal fat deposition (1.57 vs. 1.35%, P > 0.05) and significantly decreased subcutaneous fat (13.76 vs. 11.08%, P < 0.05) as well as intermuscular fat deposition (0.43 vs. 0.35%, P < 0.05) compared with 21AL. On the other hand, Ain Baziz et al. (1996) and Geraert et al. (1996) observed that enhanced fat deposition under chronic heat exposure conditions. Other workers (Smith, 1993; Smith and Teeter, 1993) also reported a significant decrease in fat deposition due to heat stress. The differences reported above could be related to the age of the animal, the model of heat stress (constant or cyclic), the method used to measure the fat index (abdominal fat was generally used as the single fatness index), and chicken breed. At 21°C, fat deposition of AA broilers decreased significantly due to feed restriction (P < 0.01). The effect of feed restriction was more pronounced than that induced by heat exposure. Therefore, fat deposition in AA broilers was enhanced by high ambient temperature at the same feeding level. For BJY chicken in this study, heat exposure enhanced abdominal fat deposition significantly. Enhanced abdominal fat deposition seems to have an advantage under hot conditions. Le Dividich et al. (1998) reported that high ambient temperature increased abdominal fat in pigs, and Kouba et al. (2001) found flare fat was increased in pigs under heat exposure. These increased amounts of internal fat in pigs could reduce thermal insulation, which was useful to adapt to high ambient temperature. The enhanced abdominal fat deposition in BJY chickens is probably an adaptive regulation under hot conditions; the more dietary energy was stored as fat, the lower heat produced, thus less heat needed to be dispersed.

In summary, BJY chickens and AA broilers responded differently to heat stress in relation to growth, meat quality, and proportion of carcass, muscle, and fat deposition. The findings suggest that the impact of heat stress could be breed dependent, and the local, slow-growing chickens had higher resistance and adaptability to hot conditions. By comparing to pair-fed birds, it can be deduced that the impact of heat exposure on the growth, carcass and muscle proportion, and fat deposition in the 2 breeds of birds may be related to the direct effect of high ambient temperature and not be associated with the decreased feed intake induced by heat exposure.

Stress reactions prior to slaughter may influence ante and postmortem muscle metabolism, and consequently, the rate and extent of glycogen breakdown, pH decline, and drip loss. The effect is principally due to variations in adenosinetriphosphatase activity and muscle glycogen reserve (Terlouw, 2004). Seasonal heat stress accelerates postmortem metabolism and biochemical changes in the muscle, which produces a faster pH decline, lower ultimate pH, and higher L* values in turkey meat (McKee and Sams, 1997). But acute heat stress appeared to have no effect upon breast meat color in broilers (Sandercock et al., 2001) and turkeys (Froning et al., 1978). In the present study, heat-exposed AA broilers had higher L* values than the controls (21AL). The results of enhanced L* values in heat-stressed AA broilers are in agreement with the report of McKee and Sams (1997), which showed that chronic heat stress increased the lightness in muscle. The BJY chickens in the present trial did not exhibit significant changes of L* values under any of the 3 treatments. The impact of stress response on meat quality is not inevitable. Terlouw (2004) indicated that production of meat with normal ultimate pH does not necessarily mean that animals have not been stressed. In the present study, high mortality and decreased growth, carcass, and breast muscle yield during heat exposure indicated that the treatment did indeed cause physiological stress in AA broilers, even though the resulting meat did have normal pH.

Drip loss was greater in muscles from heat-exposed AA broilers in this study. This result was in accord with most reports (McKee and Sams, 1997; Sandercock et al., 2001). Warriss and Brown (1987) suggested that pHi is the most important factor in determining drip loss in porcine muscle. In the present study, pHi exhibited a negative correlation to drip loss in AA broilers under hot conditions (r = –0.7826), which may partly support the Warriss and Brown hypothesis

Shear force of heat-exposed AA broilers increased slightly but not significantly. Tenderness of meat is considered to be strongly related to pHu (Watanabe et al., 1996); however, this close relationship was not observed in this study. A positive correlation between drip loss and shear force was observed in this study (r = 0.9770 in 21PF AA broilers; and r = 0.8907 in 21AL BJY chickens). Neither drip loss or shear force of BJY chickens was affected by the treatments.

The data showed that chronic heat exposure had negative effects on growth performance, breast yield, and meat quality in AA broilers, but had no significant influence on growth and meat quality in the local, slow-growing chickens. The possible mechanism of high adaptability to hot conditions of BJY chickens might be associated with their increased feed efficiency and abdominal fat deposition in high ambient temperature.

	FOOTNOTES

 
¹ Supported by grant 2004CB11750-6 and 2004CB11750-7 from the National Basic Research Program of China.

Received for publication July 17, 2006. Accepted for publication March 7, 2007.

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