Heat Stress on Meat Quality Status: History
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Contributor:
Bochra Bejaoui
,
Chaima Sdiri
,
Ikram Ben Souf
,
Imen Belhadj Slimen
,
Manel Ben Larbi
,
Sidrine Koumba
,
Naceur M’Hamdi
,
Patrick Martin

Heat stress is one of the most stressful events in livestock life, negatively impacting animal health, productivity, and product quality. 

  • heat stress
  • meat quality
  • product
  • muscle glycogenolysis

1. Introduction

Food quality is a very complex and broad concept that has changed rapidly in recent years. Recently, it has represented the set of all food properties that are closely related to physicochemical properties, texture, and taste that are acceptable and satisfying to consumers. Previous studies showed that consumers’ concerns about food quality have been increasing, in recent decades, particularly concerning the perceived healthiness of food [1][2][3]. Meat and various meat products are important sources of high-quality proteins, fats, and minerals as essential nutrients [4][5]. As animal welfare concerns grow and consumers become more conscious of food quality, there is an increasing focus on improving the quality, safety, and nutritional value of meat. Based on current knowledge, increasing global warming and climate change appear to pose a potential threat to food security in the coming decades [6][7]. Heat stress (HS) is one of the major impacts of climate change (CC) on livestock raised in both intensive and extensive production systems [8]. This is especially true given its negative impact on behavior, immune response, gut integrity, productivity, and meat quality [9]. Heat stress is a form of hyperthermia (elevated body temperature) in which the body’s physiological systems are unable to regulate body temperature within normal limits [8]. It is well known that, at temperatures higher than an animal’s thermoneutral zone, heat stress can affect animal welfare, performance, and product quality.

2. Heat Stress and Carcass Characteristics

Carcass and meat quality depend on both intrinsic and extrinsic factors. The intrinsic factors include species, breed, gender, age, and slaughter weight. The extrinsic factors include weaning, diet, and stress [10][11]. This latter can be attributed to the breeding conditions, the transport, or the environment. To maintain euthermia, heat-stressed animals activate some physiologic and metabolic adjustments at the expense of growth, reproductive, and productive aspects [12][13]. For this purpose, homeothermic animals reduce their feed intake to lower metabolic heat production [14]. However, such an adaptive response has implications on carcass characteristics in monogastric and ruminants as well. Carcass yield, carcass fat deposition, and intramuscular fat content were reported to be decreased in poultry [15][16], pigs [17][18], sheep [19], goats [20], and cattle [19][21]. A reduction in subcutaneous fat was also reported in pigs subjected to chronic HS, to enhance heat dissipation [22]. Holinger et al. [23] described that the carcass of heat-stressed pigs had reduced lean meat percentage and thicker backfat. The extent of changes indeed depends on the species, but it is known that the economic losses caused by carcass yield loss are great [24]. At the same time as fat content dropped, acetyl coenzyme A carboxylase enzyme, L (+) P-hydroxy acyl CoA dehydrogenase, and lipolytic enzyme activities were decreased [17][22]. Pearce et al. [17] demonstrated that this decrease is independent of heat stress-induced reductions in feed intake. Nevertheless, no significant effects on intramuscular fat were reported in broilers subjected to heat stress for 3 weeks [25] and heat-stressed goats for 1 month [11]. Similarly, Mader et al. [26] and Ponnampalam et al. [27] did not report any significant difference between chronic heat stress (1 week) and thermal neutral groups in subcutaneous fat in cattle and carcass fat scores in lambs. These findings may be attributed to the ability of the breeds to cope with heat stress conditions, and to the duration and severity of HS [11]. However, it is noteworthy to mention that although the carcass weight was significantly affected by heat stress-induced feed intake reduction, the impacts on carcass composition are confusing and need further investigation.

3. Heat Stress and Rapid pH Drop

After slaughter, skeletal muscle undergoes physical structural, and biochemical changes. These changes are triggered by the cession of blood flow and oxygen supply, and the scarcity of glucose resources. Under these conditions, and for postmortem homeostasis purposes, skeletal muscle metabolizes stored glycogen for adenosine triphosphate (ATP) synthesis and use [28]. Lactic acid and hydrogen ions (H+) are the endeavor products of several chemical reactions leading to the conversion of glycogen to lactic acid [15]. Since oxygen is lacking, the electron chain is interrupted and pyruvate can no longer enter the mitochondria [28][29]. Hence, lactic acid and H+ accumulate, resulting in pH lowering [30]. pH is widely recognized as one of the most accepted indicators of meat quality. Any homeostatic disturbance of postmortem metabolism (e.g., such as rapid pH drop and lower pHu) leads to meat quality defects such as pale, soft, and exudative (PSE) meat, high ultimate pH (pHu) meat (dark, firm, and dry (DFD) meat) and dark-cutting in ruminants [30]. Several studies associated heat stress with a high glycolysis rate and rapid pH decline, resulting in serious damage to skeletal muscle. In broilers under short-term heat stress (36 °C, 1 h), AMP-activated protein kinase (AMPk) activity at 1 h postmortem was greater than that of broilers under thermal neutral (25 °C) conditions [31]. This was also the case with broilers exposed to chronic HS [32]. Moreover, broilers transported during summer (32–42 °C) registered a higher adenosine monophosphate/adenosine triphosphate (AMP/ATP) ratio, increased AMPK, and lower pHu value [33][34]. It is worth noticing that some authors did not register any significant decline in ultimate pH muscle in broilers [35][36].
During and after slaughtering, HS stimulates anaerobic glycolysis within the muscles. The hydrolysis of ATP governed primarily by pyruvate kinase and lactate dehydrogenase in anaerobic conditions then escalates. More pyruvate is converted to lactate leading to an accumulation of H+ and lactic acid [37][38]. The result is a rapid pH drop which lowers the water-holding capacity and is at the origin of PSE meat [39][40]. In ruminants, heat stress results in pHu values greater than 5.8, a normal pHu muscle value [41][42]. This finding may be attributed to the effect of the cortisol hormone, which increases under HS conditions. As a result, antemortem skeletal muscle glycogen content is noteworthy reduced and postmortem glycolytic enzyme activity is enhanced [42]. Contrarily, in chickens, heat stress does not affect the antemortem glycogen content [35]. Postmortem glycolytic enzyme activity and pH drops are then faster and greater. Interestingly, some authors demonstrated that high ambient temperature and/or long-term heat exposure may not necessarily have adverse effects on muscle pH and meat quality [33][43]. This could be explained by animals’ adaptation to heat stress [43]. However, rapid pH drops and meat quality damage seem to be associated with short-term exposure to acute ambient temperatures [40][42].

4. Meat Color and Water Holding Capacity

Besides its detrimental effects on feed intake and growth rate, heat stress was reported to impact physicochemical properties such as color, texture, WHC, and organoleptic properties such as softness, consistency, flavor, and odor in chicken and pork [44][45][46]. Protein denaturation is a result of HS exposure before slaughtering. As proteins are involved in the WHC of meat, each protein damage impedes its ability to bind water. The cumulative effect leads to an impaired WHC marked by high drip and cooking loss [47]. In this trend, numerous studies reported increased values of heat loss and shear force in heat-stressed meat-type broilers [15].
In chickens and pigs, muscles consist of fast-twitching fibers [39][40]. These fibers rely mainly on anaerobic glycolysis [48]. Exposure to stressful ambient temperatures before slaughtering allows for augmented carcass temperature [49], accelerated glycolysis rate, increased H+ and lactic acid levels, and elevated protein degradation rate. Consequently, PSE conditions are developed [50]. PSE meat is poorly processed meat, more dry and brittle, and has a poor texture, higher lightness, and lower sensory score [37][39][51] due to its hindered WHC and protein extractability [52][53]. In ruminants, increased pHu values under heat stress conditions negatively affect the shrinkage of the myofilament lattice leading to darker meat color. Many meat quality defects were reported, including higher light absorption, less light scattering, higher oxygen consumption, lower WHC, and increased toughness [41][45][54][55]. However, it seems that these meat quality attributes may be influenced by the duration of heat stress exposure, and the extent of the ambient temperature [27][33][56].

5. Impacts of Heat Stress on Muscle Biochemical and Chemical Properties

It is known that ruminants, pigs, and poultry are highly vulnerable to HS due to their rapid metabolism and growth, high production, and species-specific characteristics such as rumen fermentation, transpiration, and skin insulation [57]. Numerous studies have documented how HS affects muscles [58][59]. According to Sula et al. [60], HS results in myocyte fibers that are homogenously eosinophilic, hypereosinophilic, and fragmented. It has been reported that chronic HS would increase the production of lactate in muscle and affect the meat quality. Therefore, acute HS before slaughter accelerates muscle glycogenolysis and increases lactate concentrations in early postmortem slaughter while carcasses are still warm [53]. The result is PSE meat characterized by a decreased WHC, jointly reported in poultry [61][62], but also found recently in cattle [63][64]. Contrarily, animals under chronic HS have diminished muscle glycogen stores, leading to lower lactic acid generation, leading to DFD meat with a higher ultimate pH in ruminants [65], but also in pigs [66]. Additionally, HS effects primarily involve autonomic responses due to the activation of the autonomic nervous system (ANS), which is regulated by catecholamines (adrenaline and norepinephrine) (Table 1). This includes increased respiration and heart rate, increased body temperature, and the redistribution of blood flow from the intestine to the skin for thermoregulation, hence energy utilization from body stores [67] promotes muscle glycogenolysis and inhibits energy storage [65][68]. Both acute and chronic HS cause increases in plasma glucocorticoid concentrations via the activation of the hypothalamic–pituitary–adrenal (HPA) axis. Nevertheless, acute HS leads to increased glucocorticoids more than chronic HS [69]. Glucocorticoids enhance heat loss through vasodilation [70] and increase proteolysis and altered lipid metabolism; proteolysis occurs because of an increased rate of myofibrillar protein degradation in skeletal muscle as mediated by the following mechanisms: the Ca2+-dependent-ubiquitin–proteasome, and autophagy–lysosome system [71][72][73] (Table 1).
HS stimulates the hypothalamic–pituitary–adrenal system in poultry, increases the concentration of the circulating hormone corticosterone [74], and has profound effects on protein and lipid metabolism, body composition, and meat quality [75]. Imiku et al. [16] and Lu et al. [76] provided evidence that HS is associated with chemical alterations in chicken meat. High levels of the hormone corticosterone (glucocorticoid) increase fat accumulation in the abdomen, neck, and thighs [77][78][79], but boosted protein degradation and skeletal muscle breakdown [75], potentially via the expression of fatty acid transport protein and the insulin receptor in the pectoralis major [79]. The exposure of animals to HS is related to an elevation in the expression of heat shock proteins in ruminants and pigs [12][80][81], most notably the small alpha βcrystallin (αβC) heat shock protein (sHSP). Heat shock proteins are key components of living muscle that regulate the cytoskeleton and control cell maintenance [82].
In rabbits, HS affects the amount of myoglobin in the muscle, which leads to a decrease in the pigment content of the meat [83].
Table 1. Effects of heat stress on biochemical and chemical parameters of the muscle.
Origin Chemical Class Sub-Class References
Pigs Steroid hormones Glucocorticoids [70]
Carbohydrates Glycogen [62]
Organic acid Lactic acid [53]
Ruminants Protein Myofibrillar protein [72]
alpha βcrystallin (αβC) heat shock protein (sHSP) and HSP27 [12][80][81]
Steroid hormones Glucocorticoids [70]
Organic acid Lactic acid [62]
Carbohydrates Glycogen
Lipid Volatile fatty acids
Broiler Hormone Corticosterone [74]
Insulin [79]
Protein alpha βcrystallin (αβC) heat shock protein (sHSP) and HSP27 [12][78][80][81]
Organic acid Lactic acid [54]
Steroid hormones Glucocorticoids [70]
Lipid Fatty acid [78]
Rabbit Organic acid Lactic acid [4]
Lipids - [84]
Proteins - [84]
Metalloprotein Myoglobin [83]

This entry is adapted from the peer-reviewed paper 10.3390/molecules28083332

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