Introduction
Many factors have been noted that affect poultry production in tropical and subtropical areas, for instance, indigenous breed types, quality of available feed resources, price of raw materials, and hygiene/biosecurity problems (Renaudeau et al., Reference RENAUDEAU, COLLIN, YAHAV, DE BASILIO, GOURDINE and COLLIER2012). In addition, climatic conditions are a major limiting factor for production efficiency in these regions. Tropical and subtropical regions are characterised by high ambient temperatures which imposes heat stress on poultry. The long-term genetic selection in poultry for increased production performance has led to higher metabolic body heat generation and has enhanced susceptibility to heat stress (Narinç et al., Reference NARINÇ, ERDOĞAN, TAHTABIÇEN and AKSOY2016). Heat stress, derived from a negative balance of energy cycle, results when the net amount of energy flowing from the bird's body to its surrounding environment is less than the amount of heat energy produced by the bird (Lara and Rostagno, Reference LARA and ROSTAGNO2013). In this case, body temperature, respiration rate, heart rate and rectal temperature increases which in turn affects feed intake and production efficiency of birds (Zaboli et al., Reference ZABOLI, RAHIMI, SHARIATMADARI, TORSHIZI, BAGHBANZADEH and MEHRI2017), hence the economics of production are adversely affected. The frequency of high-temperature days is expected to increase with climate change and the trend of global warming, so mitigating the negative impact of heat stress on poultry production will be an important task for the researchers and the industry at large. Strategies for coping with the impact of heat stress on animals mainly focus on three aspects. First, the physical cooling measures, such as increasing ventilation, lowering stocking density, water temperature for drinking and reducing lighting intensity, among others (Renaudeau et al., Reference RENAUDEAU, COLLIN, YAHAV, DE BASILIO, GOURDINE and COLLIER2012). Second, breeding for heat-resistant related genes (Lin et al., Reference LIN, JIAO, BUYSE and DECUYPERE2006b). Third, changing nutrition (energy, protein, amino acids, etc.), feeding methods (Gous and Morris, Reference GOUS and MORRIS2005) and nutritional additives (Habibian et al., Reference HABIBIAN, SADEGHI, GHAZI and MOEINI2015; Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). This paper summarises the current knowledge regarding heat stress, as well as the main effective strategies to alleviate heat stress in poultry (main about broilers and laying hens) production.
Impact of heat stress on poultry production
In recent years, heat stress has drawn greater public attention because of its detrimental impacts, especially for high-metabolic and productive poultry in tropical, subtropical and arid regions. However, ambient temperature plays a major role in heat stress. Charles and Walker (Reference CHARLES and WALKER2002) have concluded that the optimum temperature for growing broilers and laying hens is likely to be 18-22°C and 19-22°C, respectively. Interestingly, Payne (Reference PAYNE1966) demonstrated that fluctuating environmental temperature regimes, particularly between 15-30°C, are associated with an increased total egg mass compared with that obtained from any constant environmental temperature regime. Previous research has shown that, in laying hens, the optimum may be as high as 23-27°C as long as the feed composition has been adjusted to take account of the lower intake that occurs at that temperature (Marsden and Morris, Reference MARSDEN and MORRIS1987). This gap in temperature probably results from long-term breeding for performance, which has enhanced their susceptibility to heat stress. When the ambient temperature was elevated beyond 32°C after four weeks post-hatch, the chickens showed remarkable impacts of heat stress, which in turn, imposed negative consequences on productivity. In the U.S., total annual economic losses attributable to heat stress across livestock production industry is between $ 1.69-2.36 billion out of which $128-165 million is lost from the poultry industry (St-Pierre et al., Reference ST-PIERRE, COBANOV and SCHNITKEY2003).
Heat stress is characterised by a decreased in feed intake, body weight, feed efficiency and reduced metabolic rate (Quinteiro-Filho et al., Reference QUINTEIRO-FILHO, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SAKAI, SA, FERREIRA and PALERMO-NETO2010; Reference QUINTEIRO-FILHO, GOMES, PINHEIRO, RIBEIRO, FERRAZ-DE-PAULA, ASTOLFI-FERREIRA, FERREIRA and PALERMO-NETO2012a; Kamel et al., Reference KAMEL, AHMED, MEHAISEN, MASHALY and ABASS2017). In addition, the poor performance of birds under heat stress is usually accompanied by increasing mortality and a drop in the yield of broilers (Syafwan et al., Reference SYAFWAN, KWAKKEL and VERSTEGEN2011). Syafwan et al. (Reference SYAFWAN, KWAKKEL and VERSTEGEN2011) reported that an increase ambient temperature from 21.1 to 32.2°C caused a drop in feed intake and body weight by 9.5% and 14.3% per bird/day respectively from post-hatch to 42 days of age. Likewise, when temperature rose from 32.2 to 37.8°C, further decreases in feed intake and body weight by 9.9% and 21.2% per bird/day, were observed when compared to the birds subjected to ambient temperature of 21.1°C.
In a recent report, broiler chickens subjected to cycling heat stress caused a significant reduction in feed intake (-8.6%), body weight gain (-15.4%), and poor feed conversion ratio (+8.5%) at 42 days of age (Safdari-Rostamabad et al., Reference SAFDARI-ROSTAMABAD, HOSSEINI-VASHAN, PERAI and SARIR2017). Kamel et al. (Reference KAMEL, AHMED, MEHAISEN, MASHALY and ABASS2017) reported that broilers exposed to chronic heat stress during 21-42 days of age had significantly reduced body weight and feed intake, whereas, the FCR was significantly increased. In another study, heat stress was shown to cause a significant reduction of body weight gain (-11.5%), feed intake (-5.8%), and weight gain: feed consumption ratio (-6.3%) during 22-42 days of Arbor Acres broilers (Wan et al., Reference WAN, JIANG, ZHONG, LU, ZHANG and WANG2017a). Other studies have shown similar effects of heat stress on growth performance of broilers (Niu et al., Reference NIU, LIU, YAN and LI2009; Imik et al., Reference IMIK, OZLU, GUMUS, ATASEVER, URCAR and ATASEVER2012a; Habibian et al., Reference HABIBIAN, GHAZI and MOEINI2013). Interestingly, it is noteworthy that the stocking density, temperature of the water and noise pollution also play major roles in restricting performance, as well as animal welfare (Estevez, Reference ESTEVEZ2007).
Apart from the impact on feed intake and body weight gain, heat stress has been reported to cause great changes in broilers meat quality, generating pale, soft and exudative meat (PSE meat) (Tankson et al., Reference TANKSON, VIZZIER-THAXTON, THAXTON, MAY and CAMERON2001). Chronic heat stress increases the production of lactate in the muscle, which in turn accelerates pH decline and subsequently affects the broilers meat quality (Zhang et al., Reference ZHANG, JIA, ZUO, ZHANG, LEI, REN and FENG2012). Moreover, Hashizawa et al. (Reference HASHIZAWA, KUBOTA, KADOWAKI and FUJIMURA2013) conducted a chronic heat stress trial and found out that broilers subjected to 30°C for 10 days has tougher breast meat. Zhang et al. (Reference ZHANG, ZHAO, WANG, YANG, CHEN and GENG2017) and Lu et al. (Reference LU, WEN and ZHANG2007) found that heat stress was detrimental to broiler meat quality, in particular drip loss, meat colour and pH value. In fact, heat stress reduced protein synthesis in breast muscle while inducing protein degradation in thigh muscle (Zuo et al., Reference ZUO, XU, ABDULLAHI, MA, ZHANG and FENG2015). Another study showed that broilers exposed to chronic heat stress had decreased protein gain (-54%) and lower protein retention efficiency (-46%) (Geraert et al., Reference GERAERT, PADILHA and GUILLAUMIN1996). Interestingly, the impact of high ambient temperature on meat quality was a derivative of heat stress which induced oxidative damage to skeletal muscle, and increased reactive oxygen species (ROS), reactive nitrogen species (RNS) production and muscle MDA concentrations, which caused undesirable changes in meat characteristics (Azad et al., Reference AZAD, KIKUSATO, ZULKIFLI and TOYOMIZU2013; Liu et al., Reference LIU, HE, XIE, YANG, LI and ZOU2014).
High ambient temperatures can cause huge economic losses in the laying hen industry. Heat stress is probably one of the most frequent challenges in poultry production, contributing to reproductive problems, poor egg quality, and impaired skeletal integrity of the hens (Sahin et al., Reference SAHIN, ONDERCI, BALCI, CIKIM, SAHIN and KUCUK2007). Moreover, feed intake, eggshell strength and percentage, egg mass and production were reported to be more sensitive to heat stress than other performance traits (Mignon-Grasteau et al., Reference MIGNON-GRASTEAU, MORERI, NARCY, ROUSSEAU, RODENBURG, TIXIER-BOICHARD and ZERJAL2015). Decreased feed intake was the main effect on production, leading to changes in other traits, like egg production and quality, dietary digestibility, serum protein and calcium content (Ebeid et al., Reference EBEID, SUZUKI and SUGIYAMA2012). In recent study (Attia et al., Reference ATTIA, ABD, ABEDALLA, BERIKA, AL-HARTHI, KUCUK, SAHIN and ABOU-SHEHEMA2016), the birds kept at 38°C environmental temperature had daily feed intake reduction of 5.9% and body weight of 24.7%, resulting into about 12.8% decrease in egg mass. Song et al. (Reference SONG, LIU, SHEIKHAHMADI, JIAO and LIN2012) reported that 24 weeks old laying hens subjected heat stress had decreased daily feed intake of about 52.9 g/bird, 5.5g less in average egg mass, with a reduction of 15.8% in egg production, and 37.7% poorer feed conversion rate. Additionally, Ebeid et al. (Reference EBEID, SUZUKI and SUGIYAMA2012) found that egg weight, eggshell thickness and percentage, and eggshell density were negatively affected by high ambient temperature, i.e. 3.55% lower egg weight, 9.3% thinner eggshell, 9.9% less eggshell weight, 6.7% less percent of shell compared to total egg and a reduction of 7.8% in eggshell density. However, it is difficult to draw a general and a definite conclusion about the effect of heat on production performance, as these studies have been conducted under varying experimental conditions, intensity and duration of the heat, birds of age, genetic background and using various experimental designs.
A meta-analysis on heat stress in laying hens concluded that shell strength, daily feed intake, egg mass, and hen-day egg production were more sensitive to heat stress than the other traits as they dropped by 9.0 to 22.6% between thermo-neutrality (15 to 20°C) and heat stress (30 to 35°C) (Mignon-Grasteau et al., Reference MIGNON-GRASTEAU, MORERI, NARCY, ROUSSEAU, RODENBURG, TIXIER-BOICHARD and ZERJAL2015). Reduced egg quality and production can be largely mediated by a decrease in available dietary calcium, because when feed intake decreases during heat stress, this limits dietary calcium ingestion and absorption (Quinteiro-Filho et al., Reference QUINTEIRO-FILHO, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SAKAI, SA, FERREIRA and PALERMO-NETO2010).
Effect of heat stress on behaviour and physiology
Exposure of birds to high temperature alters their behaviour and physiological homeostasis in an attempt to reduce body temperature by thermoregulation. Different species of birds react similarly to heat stress (Lara and Rostagno, Reference LARA and ROSTAGNO2013). Birds subjected to high environmental temperatures beyond their comfort zone spend less time feeding, walking or moving but spend more time drinking, resting and panting, as well as lifting their wings away from the body to expose the lightly feathered apteria under the wings in order to promote heat transfer to the environment (Mack et al., Reference MACK, FELVER-GANT, DENNIS and CHENG2013). Panting is among the behaviour exhibited by hens under heat stress because it increases evaporative cooling. However, constant panting increases water lost through evaporation under high ambient temperature conditions, as well as having higher carbon dioxide levels and altered pH in blood, which in turn, increases the risk of respiratory alkalosis (Calder and Schmidt-Nielsen, Reference CALDER and SCHMIDT-NIELSEN1968). This results in diminished egg quality and thinner eggshells as alkalosis hampers blood bicarbonate availability for egg shell mineralisation and decrease free calcium concentrations in the blood. In a similar way to panting, increased drinking is the mostly effective way of controlling heat loss by evaporation of water from the lungs (Mahmoud et al., Reference MAHMOUD, ABDEL-RAHMAN, DARWISH, APPLEGATE and CHENG2015). Recent studies showed that birds under high ambient temperature spent more time sitting, panting and drinking and less time walking and feeding, resulting in decreased egg and meat production (Mahmoud et al., Reference MAHMOUD, ABDEL-RAHMAN, DARWISH, APPLEGATE and CHENG2015; Mack et al., Reference MACK, FELVER-GANT, DENNIS and CHENG2013).
Physiological reasons behind the impaired production performance of broilers during heat stress remain poorly understood. Exposure of chickens to extreme heat stress induces the activity of neuroendocrine system, resulting in the hypothalamic-pituitary-adrenal (HPA) axis activation, leading to acceleration of the hypothalamus and pituitary secretion of corticotropin-releasing hormone (CRH) and adrenocorticotropic hormone (ACTH), respectively. Following on from this, ACTH stimulates the synthesis and release of steroids via promoting cholesterol transformation to the glucocorticoid hormone corticosterone (CORT), and consequently, elevates plasma CORT concentrations (Quinteiro-Filho et al., Reference QUINTEIRO-FILHO, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SAKAI, SA, FERREIRA and PALERMO-NETO2010; Reference QUINTEIRO-FILHO, RODRIGUES, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SA, FERREIRA and PALERMO-NETO2012b; Fraisse and Cockrem, Reference FRAISSE and COCKREM2006). Plasma CORT level is an effective heat stress indicator in chicken, and many studies used the significant difference of CORT as standard confirmation for the success of heat stress models in animals (Rimoldi et al., Reference RIMOLDI, LASAGNA, SARTI, MARELLI, COZZI, BERNARDINI and TEROVA2015; Zhang et al., Reference ZHANG, ZHAO, WANG, YANG, CHEN and GENG2017; Delezie et al., Reference DELEZIE, SWENNEN, BUYSE and DECUYPERE2007). In recent decades, clinical applications of glucocorticoids have outpaced the mechanistic understanding of the immunosuppressive properties, and the research into glucocorticoid-mediated regulation of the immune system continues to be an intense field of investigation (Cain and Cidlowski, Reference CAIN and CIDLOWSKI2017).
Besides the adrenal hormones, thyroid hormones are important to maintain homeostasis in animals. For example, triiodothyronine (T3) and thyroxine (T4) and their ratio, have an important role in temperature regulation in chickens by regulating basal metabolic rate. T3 is the primary ligand of the nuclear thyroid hormone receptor, which forms a complex with the retinoid X receptor or occasionally with itself as a homodimer (Ikeda et al., Reference IKEDA, RHEE and CHIN1994). Many studies have demonstrated that serum concentrations of T3 consistently decline in a high temperature environment (Star et al., Reference STAR, DECUYPERE, PARMENTIER and KEMP2008; Mack et al., Reference MACK, FELVER-GANT, DENNIS and CHENG2013; Elnagar et al., Reference ELNAGAR, SCHEIDELER and BECK2010). The decline in T3 concentrations upon high temperature exposure decreases heat production, which increases survivability of birds (Bogin et al., Reference BOGIN, AVIDAR, PECH-WAFFENSCHMIDT, DORON, ISRAELI and KEVKHAYEV1996). One of the mechanisms that induce thermo-tolerance involves the regulation of heat production through changes in circulating thyroid hormones concentrations, especially T3. The ability to reduce plasma T3 concentrations, especially during a thermal challenge, suggests an improvement in thermo-tolerance (Raghebian et al., Reference RAGHEBIAN, SADEGHI and AMINAFSHAR2016; Yahav et al., Reference YAHAV, COLLIN, SHINDER and PICARD2004). T4 is widely recognised as a prohormone, being deiodinated into the active form, T3, in the target cells. Moreover, local T3 availability is regulated by thyroid hormones transport proteins as well as by iodothyronine deiodinases, which catalyse the conversion of T4 to T3 (Williams and Bassett, Reference WILLIAMS and BASSETT2011). However, previous studies on plasma T4 concentrations have shown it is difficult to reach a consensus under high temperature conditions, whether for an increase (Elnagar et al., Reference ELNAGAR, SCHEIDELER and BECK2010), decrease (Attia et al., Reference ATTIA, ABD, ABEDALLA, BERIKA, AL-HARTHI, KUCUK, SAHIN and ABOU-SHEHEMA2016) or no alteration (Xie et al., 2015; Wan et al., Reference WAN, JIANG, ZHONG, LU, ZHANG and WANG2017a; Mack et al., Reference MACK, FELVER-GANT, DENNIS and CHENG2013). In actual production, heat stress often does not occur in isolation, being generally accompanied by other factors, like limited space and poor ventilation, as well flock density in transit, which may affect the stress response. Moreover, other studies reported that serum alanine aminotransferase (ALT) and aspartate aminotransferase (AST) activities were increased in birds under heat stress (Hosseini-Vashan et al., Reference HOSSEINI-VASHAN, GOLIAN and YAGHOBFAR2016; Wan et al., Reference WAN, ZHANG, HE, BAI, ZHANG and WANG2017b). Elevated activities of ALT and AST in serum are indicators of liver damage (Nyblom et al., Reference NYBLOM, BERGGREN, BALLDIN and OLSSON2004). Therefore, animals experiencing endocrine disorders may have accompanying liver damage under heat stress.
Heat stress induced oxidative stress
More recently, the involvement of heat in inducing oxidative stress has received attention from researchers (Lin et al., Reference LIN, DECUYPERE and BUYSE2006a; Liu et al., Reference LIU, HE, XIE, YANG, LI and ZOU2014; Mujahid et al., Reference MUJAHID, YOSHIKI, AKIBA and TOYOMIZU2005). Oxidative stress reflects the imbalance between pro-oxidant and anti-oxidant systems, defined as the presence of reactive species, such as ROS, RNS and reactive chlorine species, in excess of the available antioxidant capacity of animal cells (Halliwell and Whiteman, Reference HALLIWELL and WHITEMAN2004). ROS are by-products of oxygen metabolism, having one unpaired electron derived from molecular oxygen. Small concentrations of ROS are important stimulators and modulators of cellular signalling and consequently cell behaviour (Droge, Reference DROGE2002; Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). Uncontrolled increases in ROS and RNS concentrations can lead to free radical mediated chain reactions which indiscriminately target several biologically cellular macromolecules, such as proteins (Griffiths, Reference GRIFFITHS2000), lipids (Yang et al., Reference YANG, SHARMA, SHARMA, AWASTHI and AWASTHI2003), polysaccharides (Kaur and Halliwell, Reference KAUR and HALLIWELL1994) and nucleic acids, both DNA and RNA (Davies, Reference DAVIES1995; Richter et al., Reference RICHTER, PARK and AMES1988), induces the intrinsic pathway of apoptosis.
Mitochondria are the chief organelles of oxygen metabolism, consuming approximately 85-90% of the oxygen in the cell (Belhadj Slimen et al., Reference BELHADJ SLIMEN, NAJAR, GHRAM, DABBEBI, BEN MRAD and ABDRABBAH2014) and most cellular energy is derived from the process of oxidative phosphorylation (Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). Heat stress increases mitochondrial superoxide anion levels, which is the first by-product of the one electron reduction of oxygen (Kikusato et al., Reference KIKUSATO, YOSHIDA, FURUKAWA and TOYOMIZU2015; Mujahid et al., Reference MUJAHID, SATO, AKIBA and TOYOMIZU2006). This reaction occurs at specific sites of the electron transport chain (ETC) which is a key source of superoxide anion during heat stress (Kikusato et al., Reference KIKUSATO, RAMSEY, AMO and TOYOMIZU2010). Heat stress has been shown to cause a reduction in expression of superoxide dismutase 1 (SOD-1) mRNA, and decrease cytoplasmic SOD protein and enzyme activity, resulting in the increase of ROS generation (Lee et al., Reference LEE, CHO, JEOUNG, SOH, CHO, BAE, CHUNG, LEE and LEE2004). Moreover, hyperthermia leads to an overproduction of transition metal ions, which can elicit an electron flow to oxygen, thus forming superoxide anions or peroxide (H2O2) (Agarwal and Prabakaran, Reference AGARWAL and PRABAKARAN2005; Belhadj et al., Reference BELHADJ, NAJAR, GHRAM and ABDRRABBA2016). The superoxide anion is extremely reactive and does not diffuse easily through the cell membrane. Studies have demonstrated that this anion is the precursor of most ROS. Heat stress has been shown to increase H2O2 and hydroxyl radicals (Zhao et al., Reference ZHAO, FUJIWARA and KONDO2006; Kikusato and Toyomizu, Reference KIKUSATO and TOYOMIZU2013). Most cell are equipped with SOD, such as Mn-SOD located in the matrix and Cu/Zn-SOD located in the intermembrane or cytosol space to reduce superoxide to H2O2, and promote dangerous hydroxyl radical production (Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). Due to the diffusion capacities, H2O2 is the major ROS, acting as a second messenger in oxidation signalling pathways (Wood et al., Reference WOOD, POOLE and KARPLUS2003).
NO is a highly reactive free radical, which is important in cell signalling and metabolism. NO can directly reflect the level of oxidative stress, resulting from the breakdown of arginine to citrulline in a reaction catalysed by the nitric oxide synthase enzymes (NOS), which is nicotinamide adenine dinucleotide phosphate (NADPH)-dependent. Interestingly, superoxide anions can react with nitric oxide (NO) to produce peroxynitrite, which is a powerful oxidant, leading to SOD inactivation (Steinmann et al., Reference STEINMANN, MOOSMANN, SCHIMMEL, GERHARDUS and BAUER2004).
In order to maintain the balance of ROS, the cell must have its own antioxidant system, particularly in the mitochondria. The mitochondrial antioxidant system includes two major groups: enzymatic antioxidants comprising SOD, catalase (CAT) and glutathione superoxide dismutase (GSH-Px) (Tan et al., Reference TAN, YANG, FU, FENG and ZHANG2010; Lin et al., Reference LIN, DECUYPERE and BUYSE2006a; Altan et al., Reference ALTAN, PABUCCUOGLU, ALTAN, KONYALIOGLU and BAYRAKTAR2003), and low molecular weight non-enzymatic antioxidants main including GSH, uric acid and vitamins (Azad et al., Reference AZAD, KIKUSATO, MAEKAWA, SHIRAKAWA and TOYOMIZU2010; Torki et al., Reference TORKI, ZANGENEH and HABIBIAN2014; Attia et al., Reference ATTIA, ABD, ABEDALLA, BERIKA, AL-HARTHI, KUCUK, SAHIN and ABOU-SHEHEMA2016). However, the balance of antioxidant systems is disturbed under heat stress, leading to increased ROS and decreased or inhibited antioxidant enzyme activity and expression (Lin et al., Reference LIN, DECUYPERE and BUYSE2006a; Azad et al., Reference AZAD, KIKUSATO, MAEKAWA, SHIRAKAWA and TOYOMIZU2010). Under acute heat stress, inducing the antioxidant system to respond to the increased ROS leads to the sharp increases in the activities of antioxidant enzymes such as CAT, SOD and GSH-Px to protect the cell (Lin et al., Reference LIN, DECUYPERE and BUYSE2006a; Tan et al., Reference TAN, YANG, FU, FENG and ZHANG2010). However, variation of the activities of antioxidant enzymes have been shown in chronic heat stress. Liu et al. (Reference LIU, HE, XIE, YANG, LI and ZOU2014) found that subjecting birds to chronic heat stress at 37±2°C decreased GSH-Px, CAT and SOD activities in serum of black-boned chickens. Zhang et al. (Reference ZHANG, ZHAO, WANG, YANG, CHEN and GENG2017) reported that serum GSH-Px and CAT activities were decreased in animals kept under 33°C cyclic heat stress, while Pamok et al. (Reference PAMOK, AENGWANICH and KOMUTRIN2009) found that exposing broilers to a constant chronic heat stress at 38±2°C for 21 d led to an increase in GSH-Px activity in erythrocytes. Acute heat stress induces mitochondrial substrate oxidation and stimulates ETC activation, resulting in excessive superoxide production, which worsens the oxidative stress situation by down-regulation of the avian uncoupling protein (avUCP). This ultimately causes mitochondrial dysfunction and tissue damage. Remarkably, the antioxidant enzyme (SOD, CAT, GSH-Px) activities are upregulated. In comparison, chronic heat stress leads to decreasing of metabolic oxidative capacity, up-regulation of UCPs, and depletion of antioxidant reserves due to inhibition of antioxidant enzyme activities (Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). Thus, differences in antioxidant enzyme activity mostly depend on the kinds of heat stress condition, tissue, species and other interplaying roles. Heat stress exacerbates the reaction of mitochondrial ETC, causing ROS overproduction leading to oxidative stress (Miova et al., Reference MIOVA, DIMITROVSKA, DINEVSKA-KJOVKAROVSKA, ESPLUGUES and APOSTOLOVA2016), including induced mitochondrial protein oxidation, lipid peroxidation and DNA damage (Belhadj Slimen et al., Reference BELHADJ SLIMEN, NAJAR, GHRAM, DABBEBI, BEN MRAD and ABDRABBAH2014), contributing to cell apoptosis (Green and Kroemer, Reference GREEN and KROEMER2004).
Effect of heat stress on immune responses
Animals exposed to high temperatures can have changes in the function of organs and tissues involved in neuroendocrine system, anti-oxidation system and immune system. Indeed, these adverse stressors are known to induce immunosuppression and to increase the animals’ susceptibility to infectious diseases (Quinteiro-Filho et al., Reference QUINTEIRO-FILHO, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SAKAI, SA, FERREIRA and PALERMO-NETO2010; Reference QUINTEIRO-FILHO, RODRIGUES, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SA, FERREIRA and PALERMO-NETO2012b; Kamel et al., Reference KAMEL, AHMED, MEHAISEN, MASHALY and ABASS2017) . For instance, exposure to heat stress decreased the relative weights of thymus and bursa in broilers (Jahanian and Rasouli, Reference JAHANIAN and RASOULI2015); and caused lower relative weights of liver, spleen and bursa of Fabricius in Pekin ducks (Zhu et al., Reference ZHU, JIANG and WU2014; Calefi et al., Reference CALEFI, DE SIQUEIRA, NAMAZU, COSTOLA-DE-SOUZA, HONDA, FERREIRA, QUINTEIRO-FILHO, DA and PALERMO-NETO2016) and broilers (Calefi et al., Reference CALEFI, DE SIQUEIRA, NAMAZU, COSTOLA-DE-SOUZA, HONDA, FERREIRA, QUINTEIRO-FILHO, DA and PALERMO-NETO2016). Another study found that all organs weights (include thymus, spleen, bursa, liver) were reduced significantly when birds were exposed to heat stress (Habibian et al., Reference HABIBIAN, GHAZI, MOEINI and ABDOLMOHAMMADI2014), as well as some cortex and medulla areas of lymphocytes in the bursa (Lara and Rostagno, Reference LARA and ROSTAGNO2013). The heterophil to lymphocyte (H/L) ratio is a reliable index for evaluating stress in poultry (Schmidt et al., Reference SCHMIDT, FURLONGER, LAPIERRE, MACDOUGALL-SHACKLETON and MACDOUGALL-SHACKLETON2012; Habibian et al., Reference HABIBIAN, GHAZI, MOEINI and ABDOLMOHAMMADI2014). Several studies have concluded that heat stress caused a significant increase in H/L ratio (Akhavan-Salamat and Ghasemi, Reference AKHAVAN-SALAMAT and GHASEMI2016; Gitoee et al., Reference GITOEE, SADEGHI and KARIMI2018; Hosseini-Vashan et al., Reference HOSSEINI-VASHAN, GOLIAN and YAGHOBFAR2016), due to lower numbers of lymphocytes and higher numbers of heterophils. Moreover, heat stress was associated with an increase in endotoxins such as lipopolysaccharide (LPS) from the digestive system entering the bloodstream (Alhenaky et al., Reference ALHENAKY, ABDELQADER, ABUAJAMIEH and AL-FATAFTAH2017). This is an indication that heat stress caused damage to the mucosal barrier as revealed by increased mucosal permeability in birds (Abdelqader et al., Reference ABDELQADER, ABUAJAMIEH, HAMMAD and AL-FATAFTAH2017), a major contributor for the propagation of the inflammatory response, which then lead to heterophil infiltration and lymphocyte reduction.
Heat stress causes impairment of the immune system in hens (Khan et al., Reference KHAN, LAUDADIO and TUFARELLI2012) and reduces antibody production (Niu et al., Reference NIU, LIU, YAN and LI2009). Hosseini-Vashan et al. (Reference HOSSEINI-VASHAN, GOLIAN and YAGHOBFAR2016) observed that heat stressed broilers had lower levels of circulating antibodies and decreased IgG levels during a secondary humoral response. Bartlett and Smith (Reference BARTLETT and SMITH2003) demonstrated that heat stress reduced the level of IgG and IgM in broilers, and suggested that suppression of antibody response levels could be as a result of lower feed intake, thereby providing less energy for proper development of these responses.
The central nervous system (CNS) modulates immune responses, which is mediated by a complex network of signals that interplays across the nervous, endocrine and immune systems. However, stress alters immune function which include the two major pathways, the HPA and the sympathetic-adrenal medullary (SAM) axes, resulting in the production of glucocorticoid hormones and catecholamine (Padgett and Glaser, Reference PADGETT and GLASER2003; Lara and Rostagno, Reference LARA and ROSTAGNO2013). Many different immune cells such as lymphocytes, monocytes or macrophages and granulocytes have receptors for glucocorticoid and catecholamine. These can cause changes in cellular trafficking, proliferation, cytokine secretion, antibody production and cytolytic activity. For instance, glucocorticoid receptor binds cortisol which interferes with the function of NF-kB, regulating the activity of cytokine-producing immune cells (Padgett and Glaser, Reference PADGETT and GLASER2003). Quinteiro-Filho et al. (Reference QUINTEIRO-FILHO, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SAKAI, SA, FERREIRA and PALERMO-NETO2010) reported that heat-stressed broiler chicks (kept at 31 and 36°C) had high serum corticosterone levels, low weight gains and peritoneal macrophage activity. Stressors via corticosterone inhibits antibody production by B cells (Kiecolt-Glaser et al., Reference KIECOLT-GLASER, LOVING, STOWELL, MALARKEY, LEMESHOW, DICKINSON and GLASER2005), whereas, Quinteiro-Filho et al. (Reference QUINTEIRO-FILHO, CALEFI, CRUZ, ALOIA, ZAGER, ASTOLFI-FERREIRA, PIANTINO, SHARIF and PALERMO-NETO2017) observed a decreased in IgA plasmatic levels, probably due to the high temperature causing a sustained high level of corticosterone, which induces long lysis reaction in cells and reduced Ig synthesis (Tang and Chen, Reference TANG and CHEN2016). Another study (Quinteiro-Filho et al., Reference QUINTEIRO-FILHO, RODRIGUES, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SA, FERREIRA and PALERMO-NETO2012b) reported that acute heat stress decreased macrophage phagocytosis in the chickens’ jejunum. Additionally, heat stress affects the level of cytokine, for instance, Starkie et al. (Reference STARKIE, HARGREAVES, ROLLAND and FEBBRAIO2005) found heat stress induced higher level of stimulated cells that were positive for TNF-α and IL-1α. Xu et al. (Reference XU, LI, HUANG, HE and TIAN2014) reported that heat stress increased TNF-α and IL-4, decreased IFN-γ and IL-2 in chickens. Generally, the changes in plasma and tissue levels of cytokines, reflects a shift in immunity from a predominately helper T cell, type 1 (Th1) to a helper T cell, type 2 (Th2) (Heled et al., Reference HELED, FLEISCHMANN and EPSTEIN2013). The shift is accompanied by elevated levels of IL-4, which inhibits the activation of Th1 cells that partially leads to a reduction of the secretion of IL-2 (Lu et al., Reference LU, WANG, LIN, CHU and LIN2004). Moreover, the pathological changes of immune organs caused by heat stress indirectly leads to T and B lymphocyte damage (Tang and Chen, Reference TANG and CHEN2016), and Khajavi et al. (Reference KHAJAVI, RAHIMI, HASSAN, KAMALI and MOUSAVI2003) noted a decrease in CD4+ and CD8+ cells in chickens subjected to 39ºC for seven hours per day between 35 to 41 days of age.
It has been established that an animal's innate immune system detects the presence of microbial infection through germ line-encoded pattern recognition receptors (PPRs). Toll-like receptors (TLRs) have the capacity for PRRs recognition for a wide range of pathogen-associated molecular patterns (PAMPs), and likewise play a central role in initiating innate immune response of specific signalling (Kawai and Akira, Reference KAWAI and AKIRA2009). Under environmental stress conditions, due to the influences of the neuroendocrine and anti-oxidation systems, the expression of TLR is affected. Quinteiro-Filho et al. (Reference QUINTEIRO-FILHO, CALEFI, CRUZ, ALOIA, ZAGER, ASTOLFI-FERREIRA, PIANTINO, SHARIF and PALERMO-NETO2017) observed that TLR-2 expression, but not TLR-4 expression, was decreased in the spleen and caecal tonsils of heat stressed broiler chickens. Accordingly, the mRNA levels of TLR-4 were increased in the jejunum and ileum of heat stressed chickens (Varasteh et al., Reference VARASTEH, BRABER, AKBARI, GARSSEN and FINK-GREMMELS2015). Furthermore, higher levels of heat stress proteins (HSPs) mRNA expression were reported in broilers and laying hens under high environmental temperature conditions (Mahmoud et al., Reference MAHMOUD, EDENS, EISEN and HAVENSTEIN2004; Mack et al., Reference MACK, FELVER-GANT, DENNIS and CHENG2013; Liu et al., Reference LIU, HE, XIE, YANG, LI and ZOU2014; Xu et al., Reference XU, LI, HUANG, HE and TIAN2014; Wang et al., Reference WANG, YAN, HU, AMEN and CHENG2018). HSPs are a class of ATP-dependent molecular chaperone proteins involved in protein folding in response to cellular stress can be expressed in the nucleus, cytoplasm, endoplasmic reticulum and mitochondria of eukaryotic cells, induced by various environmental threats in addition to heat, such as oxidative stress, nutritional deprivation, exposure to toxins, and infectious agents (Muralidharan and Mandrekar, Reference MURALIDHARAN and MANDREKAR2013). Depending on the extra- and/or intra-cellular location and the type of immune cells, HSPs can exert an inflammatory immune activating signal for host defence against infection or an anti-inflammatory immunosuppressive signal to prevent excessive inflammation (Kaul and Thippeswamy, Reference KAUL and THIPPESWAMY2011).
Nutritional interventions to alleviate the negative consequences of heat stress
Heat stress is a major environmental stressor that has a negative effect on performance, nutrient availability, immunity, and welfare of poultry, particularly in hot climates and during the summer season in temperate regions. It influences broiler physiological function by inducing multiple disturbances, such as immune dysregulation, endocrine disorders and oxidative damage, which results in poor growth, increased mortality, and economic losses (Quinteiro-Filho et al., Reference QUINTEIRO-FILHO, RODRIGUES, RIBEIRO, FERRAZ-DE-PAULA, PINHEIRO, SA, FERREIRA and PALERMO-NETO2012b; Hosseini-Vashan et al., Reference HOSSEINI-VASHAN, GOLIAN and YAGHOBFAR2016). Up until now, various strategies have been applied to alleviate heat stress in animals. Several extensive reviews of strategies include physical cooling measures (Renaudeau et al., Reference RENAUDEAU, COLLIN, YAHAV, DE BASILIO, GOURDINE and COLLIER2012), breeding for heat-resistant related genes (Lin et al., Reference LIN, JIAO, BUYSE and DECUYPERE2006b), and the nutritional strategies (Gous and Morris, Reference GOUS and MORRIS2005; Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). However, physical cooling measures can increase fixed costs of production (Gous and Morris, Reference GOUS and MORRIS2005), and genetic selection is a relatively long process. In contrast, nutritional strategies and supplements can be utilised to reduce the effects of heat stress and these are more advantageous and convenient without changing the basal structure of the diet. Diet formulations need to maintain water balance, nutrients and electrolytes intake and/or satisfy specific needs during heat stress such as vitamins and minerals (Renaudeau et al., Reference RENAUDEAU, COLLIN, YAHAV, DE BASILIO, GOURDINE and COLLIER2012), which regulates the balance of electrolyte and ETC. Moreover, studies have shown that some phytochemicals can directly regulate the oxidation induced by heat stress (Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016).
vitamins
Vitamin A, C and E have been used to reduce the negative effects of environmental stress in poultry due to such benefits as anti-stress, anti-oxidant and enhancement of immune function, and because heat stress decreases feed intake that has repercussions on the intake of micronutrients (Lin et al., Reference LIN, JIAO, BUYSE and DECUYPERE2006b; Renaudeau et al., Reference RENAUDEAU, COLLIN, YAHAV, DE BASILIO, GOURDINE and COLLIER2012). Vitamin A is an effective antioxidant that slows down the lipid peroxidation process via breaking the chain reactions involved and can reduce associated membrane deterioration (Abd El-Hack et al., Reference ABD EL-HACK, MAHROSE, ASKAR, ALAGAWANY, ARIF, SAEED, ABBASI, SOOMRO, SIYAL and CHAUDHRY2017). Lin et al. (Reference LIN, WANG, SONG, XIE and YANG2002) reported that high (9000 IU/kg in feed) levels of vitamin A had a beneficial effect on feed intake and egg production in layers under heat stress. Hung et al. (Reference HUNG, TU and WANG2007) indicated that vitamins and/or minerals added in various doses and combinations to diets decreased superoxide and nitric oxide production. Moreover, vitamin C (ascorbic acid) is essential for body temperature regulation (Panda et al., Reference PANDA, RAMARAO, RAJU and CHATTERJEE2008). Ascorbic acid alleviates the negative effects of heat stress on metabolic processes and hence, enhances production and boosts immunity (Attia et al., Reference ATTIA, HASSAN and QOTA2009; Chand et al., Reference CHAND, NAZ, KHAN, KHAN and KHAN2014). Dietary supplementation with vitamin C and chromium elevates the levels of the antioxidant GSH-Px which protects cells against damage (Perai et al., Reference PERAI, KERMANSHAHI, NASSIRI and ZARBAN2014). It has been reported that lymphocytes increased in birds fed diets supplemented with vitamin C because it protects lymphocytes against damage by free radicals during heat stress (Rafiee et al., Reference RAFIEE, MAZHARI, GHOREISHI and ESMAEILIPOUR2016). Other studies concluded that supplementation with vitamin E is an effective strategy during heat stress in poultry, owing to its lipid soluble antioxidant activity, as it has a major role in the elimination of free radicals in the membranes of cells and subcellular organs exposed to excessive heat (Imik et al., Reference IMIK, ATASEVER, URCAR, OZLU, GUMUS and ATASEVER2012b). However, vitamin E cannot be synthesised in poultry, which must be supplied in feed to meet nutritional requirements. Dietary supplementation of vitamin E caused an increase in lymphocyte percentage and a decrease in both heterophil percentage and H/L ratio (Habibian et al., Reference HABIBIAN, GHAZI, MOEINI and ABDOLMOHAMMADI2014). Vitamin E improves immunocompetence directly by acting on the immune cells or indirectly by stimulating the neuroendocrine and metabolic systems under heat stress conditions (Khan et al., Reference KHAN, NAZ, NIKOUSEFAT and TUFARELLI2011). Providing optimum levels of vitamin E has been associated with improved growth performance and antioxidant status under heat stress in poultry (Rehman et al., Reference REHMAN, CHAND and KHAN2017; Khan et al., Reference KHAN, NAZ, NIKOUSEFAT and TUFARELLI2011). Thus, dietary supplementation with single or a combination of vitamins (mostly vitamin C and E) may improve heat tolerance ability and animal performance during heat stress.
minerals
Some antioxidant minerals, including chromium (Cr), zinc (Zn) and selenium (Se) are used to prevent the effects of environmental heat stress. Cr was found to be active in chromodulin, a cofactor of insulin, and appears to affect carbohydrate and lipid metabolism via the action of the insulin signalling pathway (Vincent, Reference VINCENT2000). Insulin has been shown to regulate fat metabolism, cholesterol utilisation, energy production and muscle tissue deposition, mostly through increased glucose and amino acid uptake into the muscle cells (Torki et al., Reference TORKI, ZANGENEH and HABIBIAN2014). Cr is thought to be essential for activating certain oxidative enzymes and for stabilisation of proteins (Rao et al., Reference RAO, RAJU, PANDA, POONAM, MURTHY and SUNDER2012), reducing lipid peroxidation and modulating the expression of stress-related nuclear transcription factors (Orhan et al., Reference ORHAN, AKDEMIR, SAHIN, TUZCU, KOMOROWSKI, HAYIRLI and SAHIN2012). Thus, many studies have reported that supplemental dietary Cr can improve production, feed efficiency and eggshell strength and weight, particularly in birds reared under heat stress conditions (Attia et al., Reference ATTIA, ABD, ABEDALLA, BERIKA, AL-HARTHI, KUCUK, SAHIN and ABOU-SHEHEMA2016; Gitoee et al., Reference GITOEE, SADEGHI and KARIMI2018; Torki et al., Reference TORKI, ZANGENEH and HABIBIAN2014). Cr has beneficial effects on immune response, resulting in a significant increase in antibody response, improve H/L, and higher relative weights of thymus and spleen in broilers reared under heat stress (Ghazi et al., Reference GHAZI, HABIBIAN, MOEINI and ABDOLMOHAMMADI2012). Interestingly, Rao et al. (Reference RAO, PRAKASH, RAJU, PANDA, KUMARI and REDDY2016) reported that broilers supplemented with organic forms of Se, Cr and Zn (0.30, 2 and 40 mg/kg, respectively) either alone or in combination significantly improved the growth performance and anti-oxidant responses (reduced lipid peroxidation and increased SOD) reared in open-sided poultry house under cyclic heat stress. Zn is an essential bio-element with a fundamental role in maintaining the integrity of cells and promoting biochemical processes. It is a major component of various proteins (many enzymes) that regulate immunity, cellular proliferation, reproduction, nervous system function, and provides defence against free radicals (Cao et al., Reference CAO, LI, LI, WANG and LI2015). Chand et al. (Reference CHAND, NAZ, KHAN, KHAN and KHAN2014) reported that supplementation of Zn or vitamin C alone or in combination improved performance and increased peripheral blood total leucocytes numbers, lymphocytes, and monocytes of broilers reared under heat stress. Zhu et al. (Reference ZHU, LI, LU, ZHANG, JI, LIN, LIU, ODLE and LUO2017) supplemented maternal diets with different sources of Zn and reported improved hatch chick quality and survivability of offspring and alleviated the negative effect of maternal heat stress on growth performance of offspring during the starter period. In addition, diets containing organic Zn improved hatchability and offspring meat quality.
Se is used for alleviating the negative effects of heat stress in poultry, and been discussed in extensive reviews (Habibian et al., Reference HABIBIAN, SADEGHI, GHAZI and MOEINI2015). Se is a key point of some enzymes, such as Se-dependent glutathione peroxidases, which plays an important role in the cellular antioxidant defence systems (Habibian et al., Reference HABIBIAN, GHAZI, MOEINI and ABDOLMOHAMMADI2014). It acts as an essential element for the integrity of the cells involved in the immune response (Singh et al., Reference SINGH, SODHI and KAUR2006). For instance, dietary supplementation with Se-yeast improved body weight, FCR, decreased mortality and imparted resistance to oxidative stress of broilers under heat stress (Mahmoud and Edens, Reference MAHMOUD and EDENS2005). Xu and Tian (Reference XU and TIAN2015) showed that Se ameliorated the oxidative injury in different immune organs and generally increased the levels of SOD and GPx and decreased MDA in heat-stressed chickens. Additionally, feeding organic Se alone or combination with vitamin E to heat stressed cockerels, enhanced the GSH-Px activity and total antioxidant capacity in the seminal plasma (Ebeid, Reference EBEID2012). With regards to immunocompetence, Niu et al. (Reference NIU, LIU, YAN and LI2009) found that heat stress caused a reduction in lymphoid organ weights, inhibited primary and secondary antibody responses, and decreased phagocytic ability of macrophages. However, high Se inclusion improved total IgM and IgG antibody titres under heat stress, indicating that Se can alleviate the deleterious effects of heat stress. High concentrations of Se in broiler feed showed an improved antibody titre in a secondary response under heat stress conditions (Habibian et al., Reference HABIBIAN, GHAZI, MOEINI and ABDOLMOHAMMADI2014).
phytochemicals
Phytochemicals are defined as any product derived from plants containing secondary plant metabolites as active principles, including dried material, extracts, essential oils or pure isolated compounds (Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). The commercial product Resveratrol (400 or 600 mg/kg feed) attenuated the heat stress-induced overexpression of Hsp27, Hsp70, and Hsp90 mRNA in the bursa of Fabricius and spleen and increased the low expression of Hsp27 and Hsp90 mRNA in the thymus, causing a linear increase in antioxidant enzyme activities and improved growth performance of black-boned chickens (Liu et al., Reference LIU, HE, XIE, YANG, LI and ZOU2014). Moreover, black-boned chickens subjected to cyclical heat stress and supplemented with Resveratrol (400 mg/kg) had improved intestinal morphology and jejunum mucosa injuries were alleviated by modulating the mRNA and protein expression of HSPs, epithelial growth and transcription factors (Liu et al., Reference LIU, FU, YAN, XIE, LI, YU, HE and HE2016). Proper expression of HSPs is fundamental to the protective effect on the heat stress response, and acts as signal sensors of cellular stress to mediate both the innate immune and adaptive immune response (Hickman-Miller and Hildebrand, Reference HICKMAN-MILLER and HILDEBRAND2004). Sahin et al. (Reference SAHIN, ORHAN, TUZCU, ALI, SAHIN and HAYIRLI2010) reported that a plant essential oil, Epigallocatechin-3-gallate alleviated oxidative stress in heat-stressed quail and showed positive effects on oxidative status parameters in serum through inhibiting NF-κB expression and activating Nrf2 expression, which were activated and suppressed in the heat stress environment. Similarly, Hosseini-Vashan et al. (Reference HOSSEINI-VASHAN, GOLIAN and YAGHOBFAR2016) published a report on dried tomato pomace supplementation (5%) which ameliorated the negative effects in heat stressed broilers on SOD, CAT and GSH-Px activity, lipid peroxidation, enhanced the secondary response by increased total antibodies and decreased the ratio of H/L. Moreover, research conducted by Rafiee et al. (Reference RAFIEE, MAZHARI, GHOREISHI and ESMAEILIPOUR2016) showed that lemon verbena powder (1%) significantly decreased heterophyl by 15.55% and increased lymphocytes by 4.51%, which lead to improved performance data in birds exposed to an ambient temperature of 35±2°C for 8 h daily between 25 and 42 days of age.
Wan et al. (Reference WAN, JIANG, ZHONG, LU, ZHANG and WANG2017a; Reference WAN, ZHANG, HE, BAI, ZHANG and WANG2017b) demonstrated that broilers fed enzymatically treated Artemisia annua L. (0.75-1.25 g/kg feed) supplemented diets had improved growth performance, as well as GSH concentration and increased antioxidant enzymes activities of SOD, CAT and GSH-Px. Similar results were reported by Song et al. (Reference SONG, CHENG, ZHANG and WANG2017). Xu et al. (Reference XU, LI, CAO, LI, TIAN and HUANG2017) showed that the polysaccharide of Atractylodes macrocephala Koidz (200 mg/kg feed) could relieve heat stress-induced immune dysfunction in chicken spleens via reducing oxidative stress, enhancing mitochondria function and inhibiting apoptosis. Interestingly, a study (Heidarisafar et al., Reference HEIDARISAFAR, SADEGHI, KARIMI and AZIZI2016) showed that feeding apple peel waste up to 50 g/kg in broilers from 28 to 49 days of age increased HDL and decreased LDL cholesterol in serum, as apple skin is a rich source of polyphenolic compounds containing antioxidant compounds. Dietary supplementation with turmeric or cinnamon compensated for decreased pH and dry matter values due to heat stress to some extent, and thiobarbituric acid reactive substances and ROS or RNS scavenging activity were reduced, as a result alleviating the effects of heat stress on meat quality (Kanani et al., Reference KANANI, DANESHYAR, ALIAKBARLU and HAMIAN2017).
However, the negative effects of such diets supplementation for poultry under high heat stress have been seen in some studies (Lin et al., Reference LIN, JIAO, BUYSE and DECUYPERE2006b; Renaudeau et al., Reference RENAUDEAU, COLLIN, YAHAV, DE BASILIO, GOURDINE and COLLIER2012; Akbarian et al., Reference AKBARIAN, MICHIELS, DEGROOTE, MAJDEDDIN, GOLIAN and DESMET2016). Due to differences in age, physiological stage, stocking density, diet composition, and doses, the effects in animals under heat stress vary and sometimes have shown unanticipated effects. Care need to be taken regarding the use of such ingredients in poultry diets to ensure beneficial outcomes for heat stressed birds.
Conclusions
Heat stress negatively impacts the performance of broilers in tropical and subtropical areas and in temperate countries during summer months, which results in large economic losses for poultry producers. Heat stress disturbs the balance of metabolism, changes behaviour, induces oxidative stress, suppresses the immune system and induced changes in the endocrine system. This enhances the susceptibility of an animal to various diseases and may impair welfare and production. In addition, heat stress induces changes in the activities of neuroendocrine system, such as activation of the HPA axis which results into elevated CORT causing negative regulation of metabolism and immune response. This stimulates the CNS in which the combined action reduces daily gain, feed intake and increases FCR.
Nutritional intervention through supplementation of vitamins, minerals and phytochemicals is a potential avenue to reduce or offset the negative impact of high temperature conditions. These have been proven to be effective via the balance of electrolytes, regulation of the activity of ETC, anti-oxidative capacity or clearing of ROS directly; regulating the synthesis of key metabolic enzymes. Further research is still needed as heat stress influences hormone concentrations in animals as this may have a deleterious effect on food safety as a result of high concentrations of hormonal residues in animal products.
Conflict of interest
There is no conflict of interest.
Acknowledgments
This work was supported by the National Natural Science Foundation of China (Grant No.: 31672444).
