Review Role of dietary zinc in heat-stressed poultry: A review K. Sahin,*1 N. Sahin,* O. Kucuk,† A. Hayirli,‡ and A. S. Prasad§ *Department of Animal Nutrition, Faculty of Veterinary Medicine, Firat University, 23119 Elazig, Turkey; †Emory University Winship Cancer Institute, Atlanta, GA 30322; ‡Department of Animal Nutrition, Faculty of Veterinary Medicine, Atatürk University, 25700 Erzurum, Turkey; and §Karmanos Cancer Institute, Wayne State University, Detroit, MI 48201 ABSTRACT High ambient temperatures compromise performance and productivity through reducing feed intake and decreasing nutrient utilization, growth rate, egg production, egg quality, and feed efficiency, which lead to economic losses in poultry. Environmental stress also leads to oxidative stress associated with a reduced antioxidant status in the bird in vivo, as reflected by increased oxidative damage and lowered plasma concentrations of antioxidant vitamins (e.g., vitamins E, A, and C) and minerals (e.g., Zn). Zinc has an important role in numerous biological processes in
avian and mammalian species. For instance, Zn is an essential component of many enzymes, and it has both structural and catalytic functions in metalloenzymes. Furthermore, dietary Zn is required for normal immune function as well as proper skeletal development and maintenance. One of the most important functions of Zn is related to its antioxidant role and its participation in the antioxidant defense system. This work compiles past and present information about the role of Zn in heat-stressed poultry health.
Key words: heat stress, zinc, poultry 2009 Poultry Science 88:2176–2183 doi:10.3382/ps.2008-00560
INTRODUCTION High ambient temperature is of great concern in all types of poultry operations. Feed intake (FI), BW, hatchability, mortality, carcass characteristics, and other important traits governing the prosperity of the industry are adversely affected by severe heat stress. Heat loss in poultry is limited due to feathering and the absence of sweat glands. When the temperature and RH exceed the comfort level of a bird, it loses the ability to efficiently dissipate heat. This leads to physiological changes that are accompanied by a change in hormonal status and a reduction in FI to reduce metabolic heat production (Teeter et al., 1985) and lower growth rate as well as reduce feed efficiency (Geraert et al., 1996). Many researchers have experimented with various temperature levels above what is considered thermoneutral (TN), and their reports have consistently shown negative effects on bird performance. In broilers exposed to an environmental temperature of 32°C, FI decreased by 14% compared with those kept at TN temperature. Heat stress also increases mineral excretion (El Husseiny and Creger, 1981), whereas it decreases serum ©2009 Poultry Science Association Inc. Received December 23, 2008. Accepted May 13, 2009. 1 Corresponding author:
[email protected]
and liver concentrations of vitamins (e.g., vitamin C, E, and A) and minerals (e.g., Fe, Zn, Se, and Cr; Feenster, 1985; Klasing, 1998; Sahin et al., 2001, 2002a,b, 2005; Sahin and Kucuk, 2003a,b). Moreover, mobilization of minerals and vitamins from tissues and their excretion (McDowell, 1989; Siegel, 1995) are increased under stress conditions, and consequently, stress may exacerbate a marginal vitamin and mineral deficiency or lead to increased mineral and vitamin requirements. El Husseiny and Creger (1981) reported that high environmental temperature decreased retention rates of Ca, Fe, K, Na, and Zn in broilers. Several studies have also shown that the environmental temperature may influence the immune response of poultry (Henken et al., 1982; Beard and Mitchell, 1987; Donker et al., 1990). The mechanism by which the environmental temperature may act as an immune suppressor is not fully understood. However, increased activity of the adrenal gland due to stress increases the level of serum corticosteroids, which cause suppression of cell proliferation factor, or interleukin-2 (Siegel, 1995). The role of dietary supplements such as vitamins for alleviating the effect of heat stress in poultry has been reviewed extensively (Sahin and Kucuk, 2003b). However, effects of Zn on performance, oxidative stress markers, and immunity in heat-stressed poultry remain rather limited. The objective of this article was to review studies dealing with the effect of Zn supplemen-
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Figure 1. Effects of environmental temperature on body heat regulation (Wiernusz, 1998). TN = thermoneutral.
tation to heat-stressed poultry with respect to its role in metabolic and antioxidant status, immune potency, and performance. Probable mechanisms of action of Zn in preventing or alleviating the heat stress will be discussed as well.
THE EFFECTS OF HEAT STRESS ON POULTRY As a general subjective term, stress is used to describe the sum of nonspecific responses or defense mechanisms of the body when confronted with abnormal or extreme demands. Several factors including environmental and nutritional abnormalities and disease conditions can trigger a state of stress that results in generation of a combination of behavioral, biochemical, and physiological adaptations. Animals have known zones of thermal comfort that vary by the species, the physiological status, the RH, the velocity of ambient air, and the degree of solar radiation (NRC, 1981). When the environmental temperature exceeds the TN zone, the animal is in the warm zone where thermoregulatory reactions are limited. Under this situation, when TN zone exceeds the upper critical temperature (the borderline of comfort zone), the animal is considered to be heat stressed (Figure 1). A negative balance between the net amount of energy flowing from the animal to its surrounding environment and the amount of heat energy produced by the animal generates heat stress. This imbalance is induced by several factors such as environmental factors (e.g., sunlight, thermal radiation, and air temperature), animal properties (e.g., rate of metabolism and moisture loss), and thermoregulatory mechanisms (e.g., conduction, radiation, convection, and evaporation). To ameliorate this, animals must lose heat by evaporative heat loss mechanisms such as sweating and panting. When animals fail to use these mechanisms to cool the body, then death is likely to occur (Ensminger et al., 1990).
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For poultry, the environmental TN (comfort) zone covers a temperature range between 18 and 22°C. Within the TN zone, animals are expected to have no problem in physical temperature regulation and the animal is not in discomfort (NRC, 1981; Ensminger et al., 1990). Birds in general have a greater challenge in maintaining homeothermic body temperature during heat stress than other animals due to the fact that poultry lack sweat glands and have relatively high body temperature (41.5°C), relying on evaporative cooling (panting) to keep themselves cool (Ensminger et al., 1990). High ambient temperature, which is defined as heat stress, has a highly detrimental effect on egg production in laying hens (Smith, 1974) and affects FI and daily gain in broiler chickens (Yalcin et al., 2001; Sahin and Kucuk, 2003a). Research on heat stress in laying hens indicates a consistent decrease in egg weight and shell thickness (Wolfenson et al., 1979, 2001; Emery et al., 1984). Heat stress during rapid growth has also been associated with undesirable meat characteristics (Sandercock et al., 2001). Bird mortality increases during heat stress (Bogin et al., 1996; De Basilio et al., 2001) and is greater near marketing time (McDougald and McQuistion, 1980; Arjona et al., 1990) as well as during transportation (Mitchell and Kettlewell, 1998). Literature on heat stress in turkeys relates primarily to mortality (Evans et al., 2000) and the association between heat stress and the incidence of pale, exudative meat (McKee and Sams, 1997; Owens et al., 2000). It is well established that heat stress can lead to a reduction in the defense mechanisms of birds or to a relative state of immunosuppression (Thaxton and Siegel, 1970). However, the mechanism by which a high environmental temperature may act as an immune suppressor is not fully understood. It is speculated that levels of serum corticosteroids increase as the result of the increased activity of the adrenal gland due to stress, which then causes suppression of cell proliferation factor or interleukin-2 (Siegel, 1995). The effect of the environmental temperature depends on the degree of habituation of the bird as well. In addition, heat stress causes molecular changes and has been shown to elevate inflammatory markers such as interleukin-6, c-reactive protein, and tumor necrosis factor (Etches et al., 1995; Hargreaves et al., 1996; Sahin et al., 2006a). Synthesizing antioxidant enzymes such as superoxide dismutase (SOD) and glutathione peroxidase is an important regulation, in terms of animal response to stress conditions. However, this response will be effective only if cofactors such as Se for glutathione peroxidase and Cu, Zn, and Mn for SOD are available (Underwood, 1977; McDowell, 1989). At the cellular level, elevated temperature and different stress factors such as chemical and physiological stress factors and radiation, toxins, viral infections, ethanol, arsenite, oxygenation after anoxia, or gene transfer increase the synthesis of heat shock proteins (HSP), also known as stress proteins. Increased HSP protect cells against the additional stress, via protecting the cells against harm-
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ful insults and making the cells resistant to apoptosis (Morimoto et al., 1997; Wang and Edens, 1998; Coronato et al., 1999). Constitutive expression of a major HSP, HSP70, mediates the protection against cell lysis induced by the toxic effect of NO, a reactive oxygen intermediate created through oxygen-derived free radical action (Bellmann et al., 1996).
METHODS TO ALLEVIATE THE ADVERSE EFFECTS OF HEAT STRESS Several methods to alleviate the negative effects of high environmental temperature on performance of poultry have been recommended. Environmental approaches aim at increasing the airflow over birds to increase heat loss via keeping birds in open-sided cages, increasing ventilation rates or using evaporative cooling systems in enclosed houses, and lowering stocking densities (NRC, 1981; Siegel, 1995; Teeter and Belay, 1996). Recommendations regarding housing, ventilation, and cooling systems are now issues that are probably applicable on a regional basis (Armstrong et al., 1999). Effects of heat stress can noticeably be ameliorated by acclimation (Yahav and Plavnik, 1999; Altan et al., 2000; Yalcin et al., 2001). Due to their impracticality and high cost, some of the aforementioned methods, however, cannot be applied, at least in some regions and farms. Instead, because of being practical, nutritional manipulation with its low cost is a common approach in poultry production (Austic, 1985; Leeson, 1986; Shane, 1988). Considerable attention has been paid to the role of nutrition in minimizing the effects of heat stress (Austic, 1985; Shane, 1988). Nutritional modifications of the poultry diet during the time of heat stress mainly covers energy, protein, and other specific nutrients for heat-stressed poultry. To alleviate marginal nutrient deficiencies that are considered the primary cause of economic losses associated with heat stress, Leeson (1986) recommended that nutrient density of the diet should be increased. Fat supplementation to increase energy density is associated with reduced dietary heat increment and an increase in energy consumption (Dale and Fuller, 1979). Decreasing protein concentration (Kubena et al., 1972) with concomitant improvement in amino acid balance has been recommended (Waldroup et al., 1976). Dietary vitamin (Moreng, 1980) and trace element fortification (Nollet et al., 2008) may also contribute to well-being and survival. Fresh and cool drinking water may also ameliorate the effects of heat stress (Teeter and Belay, 1996). In addition, drinking water may contain electrolyte solutions (Na, Cl, K, and NaHCO3) to provide the electrolytes and adjust the acid-base balance (Balnave and Zhang, 1993; Koelkebeck et al., 1993; Smith, 1994; Balnave and Muheereza, 1997). Mineral-enriched water was shown to improve shell quality in laying hens (Odom et al., 1986). Vitamin C was also shown to increase egg production, improve hatchability and fertil-
ity, and reduce egg breakage and mortality in laying hens raised in a hot environment (Sahin and Kucuk, 2003a). Antioxidant vitamins and minerals as a part of a nutritional manipulation tool are commonly added to the diets of birds reared under heat stress (Sahin and Kucuk, 2003a). An extensive review on antioxidant vitamins in heat-stressed poultry is available (Sahin and Kucuk, 2003a). Zinc is used in poultry diets because of its antistress effects. Moreover, its requirement increases and its retention decreases during stress (Bartlett and Smith, 2003; Sahin and Kucuk, 2003b).
ZINC Zinc is required for the activity of over 300 enzymes and participates in many enzymatic and metabolic functions in the body (Prasad and Kucuk, 2002). One of the most important functions of Zn is its participation in the antioxidant defense system. Zinc deficiency increases oxidative damage of cell membranes caused by free radicals (Oteiza et al., 1996; Salgueri et al., 2000; Prasad and Kucuk, 2002). The mechanism by which Zn exerts its antioxidant action is not well defined. However, it has been suggested that Zn increases the synthesis of metallothionein, a cystine-rich protein that acts as a free radical scavenger (Oteiza et al., 1996). Zinc is absorbed in the small intestine and an intestinal pool of Zn may be formed by binding the metal to the intestinal metallothionein or Zn may be transported by albumin in plasma to the liver (Prasad, 1993). More than one isoform of metallothionein is found in different tissues in animal species. Recently, a family of Zn transporters that play an important role in the regulation of Zn metabolism at the intracellular level in mammalians has been described. They structurally consist of 6 transmembrane domains, an intracellular histidine-rich region, and the amino and carboxy terminus, which resides intracellularly (Tako et al., 2005). On the other hand, a single isoform of metallothionein in the chicken has been found in liver, pancreas, kidney, and intestinal mucosa (McCormick, 1984; Sandoval et al., 1998; Cao et al., 2000). Metallothionein is synthesized in tissues in response to dietary Zn and can bind 7 atoms of Zn per molecule of protein, but they can also bind Cu with a higher affinity (Cousins and LeeAmbrose, 1992). The NRC (1994) recommends a level of 40 to 75 mg/ kg of Zn in various poultry diets. Several biochemical and different clinical manifestations of Zn deficiency have been reported. Blood Zn concentrations are lower, and the activity of several enzymes in metabolic pathways decrease in Zn-deficient animals. Zinc deficiency causes loss of appetite and reduced efficiency of feed utilization and thus leads to growth retardation (Ensminger et al., 1990). Feather development and structure are affected by Zn deficiency, and feather fraying is observed. Zinc deficiency also causes shortness and thickness in long bones of legs and wings. Scaling of
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the skin, especially on the feet, and mortality in severe cases are also observed (Ensminger et al., 1990). Zinc deficiency may cause severe economic loss by reducing egg production and hatchability as well. Embryos of Zn-deficient eggs have skeletal abnormalities, and the hatched chicks also might not be able to stand, eat, or drink (Van Campen and Scaife, 1967; Selling et al., 1975). Because many natural feed ingredients are marginally Zn-deficient, this micronutrient is commonly supplemented to diets for livestock and poultry. Trace mineral supplements have been increasingly used in the feed industry. Two of the most common inorganic Zn supplements for poultry diets are ZnO and ZnSO4 (Batal et al., 2001). However, recent research has shown that organic Zn sources may be more available to the chick than inorganic Zn sources (Kidd et al., 1996). Wedekind et al. (1992) reported that Zn from Zn-methionine, an organic source of Zn, is more bioavailable than Zn from ZnSO4 or ZnO.
Zn Supplementation in Heat-Stressed Poultry Performance and Productivity. Zinc deficiency in animals is characterized by decreased FI, decreased growth, low circulating levels of growth hormone (GH) and insulin-like growth factor-I, and decreased hepatic production of insulin-like growth factor-I, GH receptor, and GH binding protein (MacDonald, 2000). Zinc positively affects feed utilization through participating in the metabolism of carbohydrates, lipids, and proteins (MacDonald, 2000). Sahin and Kucuk (2003b) reported linear increases in FI and egg production and improved feed efficiency and egg quality upon ZnSO4 supplemention (30 and 60 mg/kg of diet) to quail reared under heat stress conditions. There are conflicting reports on the influence of Zn on performance in stressed birds. Bartlett and Smith (2003) reported that dietary Zn levels did not affect growth performance or plasma Zn concentration in broilers reared under heat stress, whereas Sahin et al. (2005) reported that ZnSO4 or Zn picolinate supplementation (30 or 60 mg/kg) improved performance and carcass quality in quails reared under heat stress temperature. Kucuk (2008) investigated the effect of Zn (30 mg/kg) and Mg supplementation on performance responses in heat-stressed quail and reported that FI, live weight gain, and hot and chilled dressing percentages were greatest with the combination of Zn and Mg supplementation. In a more comprehensive experiment, Kucuk et al. (2008) reported that feed conversion and egg production were improved when both Zn (30 mg/kg) and pyridoxine (8 mg/kg) were supplemented to laying hens. They reported that eggshell weights and Haugh units were also increased when both pyridoxine and Zn were supplemented. Roberson and Edwards (1994) reported that 15 to 30 mg/kg of Zn supplementation increased growth rate in broilers. Kim and Patterson (2004) evaluated the effects of ZnSO4 or
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ZnO supplementation of broiler diets on growth performance and loss of uric acid and total N from manure. They reported that the Zn treatments significantly reduced N loss in poultry manure, and ZnO could be a better Zn source to prevent N loss to the atmosphere without any detrimental effect on growth performance. A linear increase in FI and BW and improvement in feed efficiency and carcass weight were reported in Zn picolinate-supplemented quail reared under heat stress conditions (Sahin et al., 2005). Zinc is a component of the carbonic anhydrase enzyme, which is crucial for supplying the carbonate ions during eggshell formation. Inhibition of this enzyme results in lowered bicarbonate ion secretion and, consequently, greatly reduces eggshell weight (Nys et al., 2001). Dietary supplementation of 80 mg/kg of Zn (Moreng et al., 1992) or 100 mg/kg of Zn (Balnave and Zhang, 1993) as Zn-methionine was shown to improve eggshell weight and reduce shell defects in hens exposed to high temperatures. In a dose response study, we studied the effect of Zn and vitamin E supplementation in quail exposed to heat stress. Increasing supplemental Zn (0, 30, and 60 mg/kg) and vitamin E (0, 250, and 500 mg/kg) linearly increased FI intake, growth rate, and carcass quality (Sahin et al., 2006b). Positive effects of Zn supplementation under TN conditions have been reported. Ao et al. (2007) reported that dietary Zn supplementation linearly increased FI, weight gain, feed efficiency, plasma and liver Zn concentrations, tibia Zn content, and tibia ash weight in broilers kept under TN conditions. Burrell et al. (2004) showed that during the 45-d experimental period, addition of Zn to the basal diet with 0, 20, 40, and 80 mg/kg of Zn from ZnSO4 significantly increased BW gain in broilers reared under TN conditions but did not affect feed conversion or mortality. Nutrient Digestibility. High ambient temperatures are associated with suppressed nutrient digestibility in poultry (Wallis and Balnave, 1984; Sahin and Kucuk, 2003a). Larbier et al. (1993) observed that heat stress decreased protein digestibility. Bonnet et al. (1997) reported that the digestibility of proteins, fats, and starch decreased with exposure of broiler chickens to high temperatures. In addition, activities of trypsin, chymotrypsin, and amylase decrease significantly at a temperature of 32°C (Hai et al., 2000). Because Zn has a protective role on pancreatic tissue against oxidative damage, it may help the pancreas to function properly including secretions of digestive enzymes, thus improving digestibility of nutrients. In a dose response study, we studied the effect of Zn supplementation in quails exposed to heat stress. Increasing supplemental Zn (0, 30, and 60 mg/kg) linearly increased digestibility of DM, organic matter, CP, and ether extract (Sahin and Kucuk, 2003b). Onderci et al. (2003) also reported that supplemental Cr and Zn ameliorated the decrease in digestibility of DM, CP, and ether extract in laying hens reared under a low temperature.
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Antioxidant Status. Several studies demonstrated that heat stress causes an increased free radical production (Halliwell and Gutteridge, 1989) and lowers the concentrations of antioxidant vitamins and minerals such as E, C, A, and Zn in serum (Feenster, 1985; Sahin and Kucuk, 2003b; Sahin et al., 2005). Studies show that concentrations of malondialdehyde (MDA), an indicator of lipid peroxidation, in serum decrease with dietary Zn picolinate supplementation in heatstressed quail (Sahin et al., 2005; Kucuk, 2008). Sahin and Kucuk (2003b) reported that 30 or 60 mg/kg of Zn decreased serum and liver MDA levels in heat-stressed birds. In addition, Zn supplementation significantly increased serum concentrations of vitamins C and E and Zn in poultry. Onderci et al. (2003) also reported that 30 mg/kg of ZnSO4 and 400 μg/kg of Cr supplementation decreased serum MDA concentrations and increased the concentrations of vitamins C, E, and A in cold-stressed laying hens. Sahin et al. (2005) reported that serum vitamin C and E concentrations increased linearly, whereas MDA concentrations decreased linearly as dietary 30 or 60 mg/kg of ZnSO4 and Zn picolinate supplementation increased. In a similar experiment, Kucuk et al. (2003) reported that supplemental Zn resulted in an increased total serum protein but decreased glucose, cholesterol, and MDA concentrations in heat-stressed broiler chickens. In heat-stressed quail, Kucuk (2008) also showed that both Zn and Mg supplementations decreased plasma MDA levels. Zinc may play a key role in suppression of free radicals because it is a cofactor of the main antioxidative enzyme Cu-ZnSOD and it also inhibits the NADPH-dependent lipid peroxidation (Prasad and Kucuk, 2002). It prevents lipid peroxidation via inhibiting glutathione depletion as well (Prasad, 1997). Due to the ability to replace Fe and Cu from binding sites, Zn can compete with these transition metals to bind to the cell membrane and decrease the production of free radicals and thus exert a direct antioxidant action (Oteiza et al., 1996; Powell, 2000; Prasad and Kucuk, 2002). Zinc also induces production of metallothionein, which is an effective scavenger for hydroxyl radical. It has been suggested that Zn-metallothionein complexes in the islet cells provide protection against immune-mediated free radical attack (Salgueiro et al., 2000; Prasad and Kucuk, 2002). Another mode of action proposed for Zn as an antioxidant is its interaction with vitamin E. During Zn deficiency, probably due to defective formation of chylomicrons in the enterocyte, absorption of lipid-soluble vitamins such as E and A is impaired. Thus, some of the oxidative damage in Zn-deficient animals may be linked to the impaired vitamin E status during Zn deficiency, as in many cases, supplemental vitamin E seemed to prevent some of these lesions (Kim et al., 1998). For instance, in heat-stressed quail, it was shown that serum vitamin C, vitamin E, and Zn concentrations linearly increased, whereas MDA concentrations linearly decreased as dietary vitamin E (0, 250, and 500 mg/kg)
and Zn picolinate (0, 30, and 60 mg/kg) supplementation increased (Sahin et al., 2006b). Heat shock proteins are thought to play a role in cellular protection under high ambient temperature, with a proposed relationship between the development of thermotolerance and HSP synthesis, especially HSP70 (Lindquist and Craig, 1988). A lower HSP70 expression was observed in animals receiving therapeutic levels of Zn picolinate (30 and 60 mg/kg) and in quails reared under TN conditions (Sahin et al., 2009). Immunity. Numerous studies have evaluated the effects of heat stress on the immune responses in chickens. The heterophil-to-lymphocyte ratio has been used as a sensitive indicator of stress, including heat stress, among chicken populations (Gross and Siegel, 1983; Mashaly et al., 2004). An increased heterophilto-lymphocyte ratio was observed under high ambient temperature, which indicates a relationship between heat stress and nonspecific immune reactive cells (heterophil cells; McFarlane and Curtis, 1989; Mashaly et al., 2004). Thaxton et al. (1968) showed that a high environmental temperature (41 to 45°C) affected the specific humoral immune response in young chickens. Heat stress also caused a reduction in antibody production in broilers (Zulkifli et al., 2000) and laying hens (Mashaly et al., 2004). Zinc is an important element for all aspects of immunity (Chandra and Dayton, 1982; Sherman, 1992) and is critical for the integrity of the cells involved in the immune response (Dardenne et al., 1985). Zinc deficiency causes a decrease in cellular immunity (Prasad and Kucuk, 2002) and adversely affects thymus (Fraker et al., 1977), spleen (Luecke et al., 1978), and interleukin production (Dowd et al., 1986). Abnormal Tlymphocyte development is thought to be the primary consequence of Zn deficiency (Dardenne and Bach, 1993). Zinc deficiency causes an imbalance in functions of T helper-1 and T helper-2 cells (Shankar and Prasad, 1998). Although it was stated that supplementing the diet of broilers with Zn above 40 mg/kg recommended by the NRC (1994) enhances antibody production (Kidd et al., 1992), some reports showed no benefical effect (Stahl et al., 1989; Pimentel et al., 1991). For evaluation of the effect of Zn on performance and immune status during heat stress, Bartlett and Smith (2003) used male broilers raised in either a TN or high environment and fed low (34 mg/kg), adequate (68 mg/ kg), and high Zn diets (181 mg/kg) and found that heat stress caused a reduction in lymphoid organ weights, primary and secondary antibody responses, phagocytic ability of macrophages, and plasma Zn concentration; these responses increased at high Zn supplementation. Birds receiving high Zn under TN temperatures had higher total IgM and IgG antibody titers, indicating that the level of Zn in the diet and environmental conditions significantly influenced the immune response of broilers. Sunder et al. (2008) reported that the humoral and cell-mediated immune responses were significant-
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ly higher in broilers supplemented with 80 mg/kg or greater amounts of Zn than those supplemented with less than 80 mg/kg of Zn. The weights of bursa and spleen were higher at 40 mg/kg of Zn compared with lower levels. In conclusion, heat stress causes significant decreases in performance, productivity, nutrient utilization, and immune and antioxidant statuses, which result in increases in disease incidences and economic losses in poultry operations. Dietary manipulations are among the methods to alleviate these negative adverse effects of heat stress. Because it has several significant functions as well as antioxidant properties, Zn is one of the most important components of the poultry diet during times of heat stress.
REFERENCES Altan, O., A. Altan, I. Oguz, A. Pabuccuoglu, and S. Konyalioglu. 2000. Effects of heat stress on growth, some blood variables and lipid oxidation in broilers exposed to high temperature at an early age. Br. Poult. Sci. 41:489–493. Ao, T., J. L. Pierce, A. J. Pescatore, A. H. Cantor, K. A. Dawson, M. J. Ford, and B. L. Shafer. 2007. Effects of organic zinc and phytase supplementation in a maize-soybean meal diet on the performance and tissue zinc content of broiler chicks. Br. Poult. Sci. 48:690–695. Arjona, A. A., D. M. Denbow, and W. D. Weaver Jr. 1990. Neonatally induced thermotolerance. Comp. Biochem. Physiol. 95A:393–399. Armstrong, D. V., P. E. Hillman, M. J. Meyer, J. F. Smith, S. R. Stokes, and J. P. Harner. 1999. Heat stress management in freestall barns in the western U. S. Pages 87–98 in Proc. West. Dairy Manage. Conf., Las Vegas, NV. Kansas State University Agricultural Experiment Station and Cooperative Extension Service, Manhattan. Austic, R. E. 1985. Feeding poultry in hot and cold climates. Pages 123–136 in Stress Physiology in Livestock. Vol. 3. M. K. Yousef, ed. CRC Press, Boca Raton, FL. Balnave, D., and S. K. Muheereza. 1997. Improving eggshell quality at high temperatures with dietary sodium bicarbonate. Poult. Sci. 76:588–593. Balnave, D., and D. Zhang. 1993. Response of laying hens on saline drinking water to dietary supplementation with various Zn compounds. Poult. Sci. 72:603–609. Bartlett, J. R., and M. O. Smith. 2003. Effects of different levels of zinc on the performance and immunocompetence of broilers under heat stress. Poult. Sci. 82:1580–1588. Batal, A. B., T. M. Parr, and D. H. Baker. 2001. Zinc bioavailability in tetrabasic zinc chloride and the dietary zinc requirement of young chicks fed a soy concentrate diet. Poult. Sci. 80:87–90. Beard, C. W., and B. W. Mitchell. 1987. Influence of environmental temperatures on the serologic responses of broiler chickens to inactivated and viable Newcastle disease vaccines. Avian Dis. 31:321–326. Bellmann, K., M. Jaattela, D. Wissing, V. Burkart, and H. Kolb. 1996. Heat shock protein hsp70 overexpression confers resistance against nitric oxide. FEBS Lett. 5:185–188. Bogin, E., Y. Avidar, V. Pech-Waffenschmidt, Y. Doron, B. A. Israeli, and E. Kevhayev. 1996. The relationship between heat stress, survivability and blood composition of the domestic chicken. Eur. J. Clin. Chem. Biochem. 34:463–469. Bonnet, S., P. A. Geraert, M. Lessire, B. Carre, and S. Guillaumin. 1997. Effect of high ambient temperature on feed digestibility in broilers. Poult. Sci. 76:857–863. Burrell, A. L., W. A. Dozier, A. J. Davis, M. M. Compton, M. E. Freeman, P. F. Vendrell, and T. L. Ward. 2004. Responses of broilers to dietary zinc concentrations and sources in relation to environmental implications. Br. Poult. Sci. 45:225–263.
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Cao, J., P. R. Henry, R. Guo, R. A. Holwerda, J. P. Toth, R. C. Littell, R. D. Miles, and C. B. Ammerman. 2000. Chemical characteristics and relative bioavailability of supplemental organic zinc sources for poultry and ruminants. J. Anim. Sci. 78:2039–2054. Chandra, R. K., and D. H. Dayton. 1982. Trace element regulation of immunity and infection. Nutr. Res. 2:721–733. Coronato, S., W. Di Girolamo, M. Salas, O. Spinelli, and G. Laguens. 1999. Biology of heat shock proteins. Medicina (B. Aires) 59:477–486. Cousins, R. J., and L. M. Lee-Ambrose. 1992. Nuclear zinc uptake and interactions and metallothionein gene expression are influenced by dietary zinc in rats. J. Nutr. 122:56–64. Dale, N. M., and H. L. Fuller. 1979. Effects of diet composition on feed intake and growth of chicks under heat stress. Poult. Sci. 58:1529–1534. Dardenne, M., and J. M. Bach. 1993. Rationale for the mechanism of zinc interaction in the immune system. Pages 501–509 in Nutrient Modulation of the Immune Response. S. Cunningham-Rundles, ed. Marcel Dekker, New York, NY. Dardenne, M., W. Savino, S. Borrih, and J. F. Bach. 1985. A zinc dependent epitope of the molecule of thymulin, a thymic hormone. Proc. Natl. Acad. Sci. USA 82:7035–7038. De Basilio, V., M. Vilarino, S. Yahav, and M. Picard. 2001. Early age thermal conditioning and a dual feeding program for male broilers challenged by heat stress. Poult. Sci. 80:29–36. Donker, R. A., M. G. B. Nieuwland, and A. J. van der Zijpp. 1990. Heat-stress influences on antibody production in chicken lines selected for high and low immune responsiveness. Poult. Sci. 69:599–607. Dowd, P. S., J. Kelleher, and P. J. Guillou. 1986. T-lymphocyte subsets and interleukin-2 production in zinc-deficient rats. Br. J. Nutr. 55:59–69. El Husseiny, O., and C. R. Creger. 1981. Effect of ambient temperature on mineral retention and balance of the broiler chicks. Poult. Sci. 60(Suppl. 1):1651. (Abstr.) Emery, D. A., P. Vohra, R. A. Ernst, and S. R. Morrison. 1984. The effect of cyclic and constant ambient temperatures on feed consumption, egg production, egg weight, and shell thickness of heat. Poult. Sci. 63:2027–2035. Ensminger, M. E., J. E. Oldfield, and W. W. Heinemann. 1990. Pages 8–120 in Feeds and Nutrition. The Ensminger Publishing Company, Clovis, CA. Etches, R., J. M. John, and A. M. V. Gibbins. 1995. Behavioural, physiological, neuroendocrine and molecular responses to heat stress. Pages 31–65 in Poultry Production in Hot Climates. N. J. Daghir, ed. CAB International, Wallingford, UK. Evans, R. D., R. K. Edson, K. L. Watkins, J. L. Robertson, J. B. Meldrum, and M. N. Novilla. 2000. Turkey knockdown in successive flocks. Avian Dis. 44:730–736. Feenster, R. 1985. High temperatures decrease vitamin utilization. Misset Poult. 38:38–41. Fraker, P. J., S. M. Haas, and R. W. Leucke. 1977. Effect of zinc deficiency on the immune response of the young adult A/J mouse. J. Nutr. 107:1889–1895. Geraert, P. A., J. C. F. Padilha, and S. Guillaumin. 1996. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: Growth performance, body composition and energy retention. Br. J. Nutr. 75:195–204. Gross, W. B., and H. S. Siegel. 1983. Evaluation of the heterophil/ lymphocyte ratio as a measure of stress in chickens. Avian Dis. 27:972–978. Hai, L., D. Rong, and Z. Y. Zhang. 2000. The effect of thermal environment on the digestion of broilers. J. Anim. Physiol. Anim. Nutr. (Berl.) 83:57–64. Halliwell, B. E., and J. M. C. Gutteridge. 1989. Lipid peroxidation: A radical chain reaction. Pages 188–218 in Free Radicals in Biology and Medicine. 2nd ed. Oxford University Press, New York, NY. Hargreaves, M., P. Dillo, D. Angus, and M. Febbraio. 1996. Effect of fluid ingestion on muscle metabolism during prolonged exercise. J. Appl. Physiol. 80:363–366. Henken, A. M., A. M. J. Groote Schaarsberg, and M. G. B. Nieuwland. 1982. The effect of environmental temperature on im-
2182
Sahin et al.
mune response and metabolism of the young chicken. Poult. Sci. 62:51–58. Kidd, M. T., N. B. Anthony, L. A. Newberry, and S. R. Lee. 1992. Effect of supplemental zinc in either a corn-soybean or a milo and corn-soybean meal diet on the performance of young broiler breeders and their progeny. Poult. Sci. 72:1492–1499. Kidd, M. T., P. R. Ferket, and M. A. Qureshi. 1996. Zinc metabolism with special reference to its role in immunity. World’s Poult. Sci. J. 52:309–323. Kim, E. S., S. K. Noh, and S. I. Koo. 1998. Marginal zinc deficiency lowers the lymphatic absorption of α-tocopherol in rats. J. Nutr. 128:265–270. Kim, W. K., and P. H. Patterson. 2004. Effects of dietary zinc supplementation on broiler performance and nitrogen loss from manure . Poult. Sci. 83:34–38. Klasing, K. C. 1998. Comparative Avian Nutrition. University Press, Cambridge, UK. Koelkebeck, K. W., P. C. Harrison, and T. J. Madindou. 1993. Effect of carbonated drinking water on production performance and bone characteristics of laying hens exposed to high environmental temperatures. Poult. Sci. 72:1800–1803. Kubena, L. F., B. D. Lott, J. W. Deaton, F. N. Reece, and J. D. May. 1972. Body composition of chicks as influenced by environmental temperature and selected dietary factors. Poult. Sci. 51:517–522. Kucuk, O. 2008. Zinc in a combination with magnesium helps reducing negative effects of heat stress in quails. Biol. Trace Elem. Res. 123:144–153. Kucuk, O., A. Kahraman, I. Kurt, N. Yildiz, and A. C. Onmaz. 2008. A combination of zinc and pyridoxine supplementation to the diet of laying hens improves performance and egg quality. Biol. Trace Elem. Res. 126:165–175. Kucuk, O., N. Sahin, and K. Sahin. 2003. Supplemental zinc and vitamin A can alleviate negative effects of heat stress in broiler chickens. Biol. Trace Elem. Res. 94:225–235. Larbier, Z. M., A. M. Chagneau, and P. A. Geraert. 1993. Influence of ambient temperature on true digestibility of protein and amino acids of rapeseed and soybean meals in broilers. Poult. Sci. 72:289–295. Leeson, S. 1986. Nutritional considerations of poultry during heat stress. World’s Poult. Sci. J. 42:69–81. Luecke, R. W., C. E. Siminol, and P. J. Fraker. 1978. The effect of restricted dietary intake on the antibody mediated response of the zinc deficient A/J mouse. J. Nutr. 108:881–887. Lindquist, S., and E. A. Craig. 1988. The heat shock proteins. Annu. Rev. Genet. 22:631–637. MacDonald, R.S. 2000. The role of zinc in growth and cell proliferation. J. Nutr. 130(5S Suppl.):1500S–1508S. Mashaly, M. M., G. L. Hendricks, M. A. Kalama, A. E. Gehad, A. O. Abbas, and P. H. Patterson. 2004. Effect of heat stress on production parameters and immune responses of commercial laying hens. Poult. Sci. 83:889–894. McCormick, C. C. 1984. Induction and accumulation of metallothionein in liver and pancreas of chicks given oral zinc: A tissue comparison. J. Nutr. 114:191–203. McDougald, L. R., and T. E. McQuistion. 1980. Mortality from heat stress in broiler chickens influenced by anticoccidial drugs. Poult. Sci. 59:2421–2423. McDowell, L. R. 1989. Comparative aspects to human nutrition. Vitamin C, A and E. Pages 93–131 in Vitamins in Animal Nutrition. L. R. McDowell, ed. Academic Press, London, UK. McFarlane, J. M., and S. E. Curtis. 1989. Multiple concurrent stressors in chicks. 3. Effects on plasma corticosterone and the heterophil:lymphocyte ratio. Poult. Sci. 68:522–527. McKee, S. R., and A. R. Sams. 1997. The effect of seasonal heat stress on rigor development and the incidence of pale, exudative turkey meat. Poult. Sci. 76:1616–1620. Mitchell, M. A., and P. J. Kettlewell. 1998. Physiological stress and welfare of broiler chickens in transit: Solutions not problems. Poult. Sci. 77:1803–1814. Moreng, R. E. 1980. Temperature and vitamin requirements of the domestic fowl. Poult. Sci. 59:782–785.
Moreng, R. E., D. Balnave, and D. Zhang. 1992. Dietary zinc methionine effect on eggshell quality of hens drinking saline water. Poult. Sci. 71:1163–1167. Morimoto, R. I., M. P. Kline, D. N. Bimston, and J. J. Cotto. 1997. The heat-shock response: Regulation and function of heat-shock protein and molecular chaperones . Essays Biochem. 32:17–29. Nollet, L., G. Huyghebaert, and P. Spring. 2008. Effect of different levels of dietary organic (bioplex) trace minerals on live performance of broiler chickens by growth phases. J. Appl. Poult. Res. 17:109–115. NRC. 1981. Poultry. Pages 109–134 in Effect of Environment on Nutrient Requirements of Domestic Animals. National Academy Press, Washington, DC. NRC. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC. Nys, Y., J. Gautron, M. D. McKee, J. M. Garcia-Ruiz, and M. Hincke. 2001. Biochemical and functional characterization of eggshell matrix proteins. World’s Poult. Sci. J. 57:401–403. Odom, T. W., P. C. Harrison, and W. G. Bottje. 1986. Effects of thermal-induced respiratory alkalosis on blood ionised calcium in the domestic hen. Poult. Sci. 65:570–573. Onderci, M., N. Sahin, K. Sahin, and N. Kilic. 2003. The antioxidant properties of chromium and zinc: In vivo effects on digestibility, lipid peroxidation, antioxidant vitamins and some minerals under a low ambient temperature. Biol. Trace Elem. Res. 92:139–150. Oteiza, P. L., K. L. Olin, C. G. Fraga, and C. L. Keen. 1996. Oxidant defense systems in testes from Zn deficient rats. Proc. Soc. Exp. Biol. Med. 213:85–91. Owens, C. M., S. R. Mckee, N. S. Matthews, and A. R. Sams. 2000. The development of pale, exudative meat in two genetic lines of turkeys subjected to heat stress and its prediction by halothane screening. Poult. Sci. 79:430–435. Pimentel, J. L., M. E. Cook, and J. L. Greger. 1991. Immune response of chicks fed various levels of zinc. Poult. Sci. 70:947–954. Powell, S. R. 2000. The antioxidant properties of zinc. J. Nutr. 130:1447S–1454S. Prasad, A. S. 1993. Biochemistry of Zinc. Plenum Press, New York, NY. Prasad, A. S. 1997.The role of zinc in brain and nerve functions. Pages 95–111 in Metals and Oxidative Damage in Neurological Disorders. A. Connor, ed. Plenum Press, New York, NY. Prasad, A. S., and O. Kucuk. 2002. Zinc in cancer prevention. Cancer Metastasis Rev. 21:291–295. Roberson, K. D., and H. M. Edwards Jr.. 1994. Effects of 1,25 dihydroxycholecalciferol and phytase on zinc utilization in broiler chicks. Poult. Sci. 73:1312–1316. Sahin, K., and O. Kucuk. 2003a. Heat stress and dietary vitamin supplementation of poultry diets. Nutr. Abstr. Rev. Ser. B Livest. Feeds Feed. 73:41R–50R. Sahin, K., and O. Kucuk. 2003b. Zinc supplementation alleviates heat stress in laying Japanese quail. J. Nutr. 33:2808–2811. Sahin, K., O. Kucuk, N. Sahin, and M. Sari. 2002a. Effects of vitamin C and vitamin E on lipid peroxidation status, some serum hormone, metabolite, and mineral concentrations of Japanese quails reared under heat stress (34°C). Int. J. Vitam. Nutr. Res. 72:91–100. Sahin, K., M. Onderci, N. Sahin, T. A. Balci, M. F. Gursu, V. Juturu, and O. Kucuk. 2006a. Dietary arginine silicate inositol complex improves bone mineralization in quail. Poult. Sci. 85:486–492. Sahin, K., N. Sahin, M. Onderci, S. Yaralioglu, and O. Kucuk. 2001. Protective role of supplemental vitamin E on lipid peroxidation, vitamins E, A and some mineral concentrations of broilers reared under heat stress. Vet. Med. 46:140–144. Sahin, K., N. Sahin, S. Yaralioglu, and M. Onderci. 2002b. Protective role of supplemental vitamin E and selenium on lipid peroxidation, vitamin E, vitamin A, and some mineral concentrations of Japanese quails reared under heat stress. Biol. Trace Elem. Res. 85:59–70. Sahin, K., M. O. Smith, M. Onderci, N. Sahin, M. F. Gursu, and O. Kucuk. 2005. Supplementation of zinc from organic or inorganic
REVIEW source improves performance and antioxidant status of heat-distressed quail. Poult. Sci. 84:882–887. Sahin, K., M. Onderci, N. Sahin, F. Gulcu, N. Yildiz, M. Avci, and O. Kucuk. 2006b. Responses of quail to dietary vitamin E and zinc picolinate at different environmental temperatures. Anim. Feed Sci. Technol. 129:39–48. Sahin, N., M. Tuzcu, I. Ozercan, K. Sahin, A. S. Prasad, and O. Kucuk. 2009. Zinc picolinate in the prevention of leiomyoma in Japanese quail. J. Med. Food. In press. Salgueiro, M. J., M. Zubillaga, A. Lysionek, M. I. Sarabia, R. Caro, T. De Paoli, A. Hager, R. Weill, and J. Boccio. 2000. Zinc as essential micronutrient: A review. Nutr. Res. 20:737–755. Sandercock, D. A., R. R. Hunter, G. R. Nute, M. A. Mitchell, and P. M. Hocking. 2001. Acute heat stress-induced alterations in blood acid-base status and skeletal muscle membrane integrity in broiler chickens at two ages: Implications for meat quality. Poult. Sci. 80:418–425. Sandoval, M., P. R. Henry, X. G. Luo, R. C. Littell, R. D. Miles, and C. B. Ammerman. 1998. Performance and tissue zinc and metallothionein accumulation in chicks fed a high dietary level of zinc. Poult. Sci. 77:1354–1363. Selling, W., F. W. Ahnefeld, W. Dick, and L. Fodor. 1975. The biological significance of zinc. Anaesthesist 24:329–342. Shane, S. M. 1988. Factors influencing health and performance of poultry in hot climates. Crit. Rev. Poult. Biol. 1:247–267. Shankar, A. H., and A. S. Prasad. 1998. Zinc and immune function: The biological basis of altered resistance to infection. Am. J. Clin. Nutr. 68:447–463. Sherman, A. R. 1992. Zinc, copper and iron nutrition and immunity. J. Nutr. 122:604–609. Siegel, H. S. 1995. Stress, strains and resistance. Br. Poult. Sci. 36:3–22. Smith, A. J. 1974. Changes in the average weight and shell thickness of eggs produced by hens exposed to high environmental temperatures. A review. Trop. Anim. Health Prod. 6:237–244. Smith, M. O. 1994. Effects of electrolyte and lighting regimen on growth of heat-distressed broilers. Poult. Sci. 73:350–353. Stahl, J. L., M. E. Cook, M. L. Sunde, and J. L. Greger. 1989. Enhanced humoral immunity in progeny chicks from hens fed practical diets supplemented with zinc. Appl. Agric. Res. 4:86–89. Sunder, G. S., A. K. Panda, N. C. S. Gopinath, S. V. Rama Rao, M. V. L. N. Raju, M. R. Reddy, and C. V. Kumar. 2008. Effects of higher levels of zinc supplementation on performance, mineral availability, and immune competence in broiler chickens. J. Appl. Poult. Res. 17:79–86. Tako, E., P. R. Ferket, and Z. Uni. 2005. Changes in chicken intestinal zinc exporter mRNA expression and small intestinal functionality following intra-amniotic zinc-methionine administration. J. Nutr. Biochem. 16:339–346.
2183
Teeter, R. G., and T. Belay. 1996. Broiler management during acute stress. Anim. Feed Sci. Technol. 58:127–142. Teeter, R. G., M. O. Smith, F. N. Owens, S. C. Arp, S. Sangiah, and J. E. Breazile. 1985. Chronic heat stress and respiratory alkalosis: Occurrence and treatment in broiler chicks. Poult. Sci. 64:1060–1064. Thaxton, P., C. R. Sadler, and B. Glick. 1968. Immune response of chickens following heat exposure or injections with ACTH. Poult. Sci. 47:264–266. Thaxton, P., and H. S. Siegel. 1970. Immunodepression in young chickens by high environmental temperature. Poult. Sci. 49:202– 205. Underwood, E. J. 1977. Zinc: Intermediary metabolism. Pages 196– 242 in Trace Elements in Human and Animal Nutrition. 4th ed. Academic Press, New York, NY. Van Campen, D. R., and P. V. Scaife. 1967. Zinc interference with copper absorption in rats. J. Nutr. 91:473–476. Waldroup, P. W., R. J. Mitchell, J. R. Payne, Z. B. Johnson, and K. R. Hazen. 1976. Performance of chicks fed diets formulated to minimize excess levels of essential amino acids. Poult. Sci. 55:243–253. Wallis, I. R., and D. Balnave. 1984. The influence of environmental temperature, age and sex on the digestibility of amino acids in growing broiler chickens. Br. Poult. Sci. 25:401–407. Wang, S., and F. W. Edens. 1998. Heat conditioning induces heat shock proteins in broiler chickens and turkey poults. Poult. Sci. 77:1636–1645. Wedekind, K. J., A. E. Hortin, and D. H. Baker. 1992. Methodology for assessing zinc bioavailability: Efficacy estimates for zinc-methionine, zinc sulfate, and zinc oxide. J. Anim. Sci. 70:178–187. Wiernusz, C. 1998. Nutritional Therapies to Optimize Poultry Production During High Humidity and Ambient Temperature Exposure. Quarterly Publication of Cobb-Vantress Incorporated 6:2. Wolfenson, D., D. Bachrach, M. Maman, Y. Graber, and I. Rozenboim. 2001. Evaporative cooling of ventral regions of the skin in heat stressed laying hens. Poult. Sci. 80:958–964. Wolfenson, D., Y. F. Feri, N. Snapir, and A. Berman. 1979. Effect of diurnal or nocturnal heat stress on egg formation. Br. Poult. Sci. 20:167–174. Yahav, S., and I. Plavnik. 1999. Effect of early-stage thermal conditioning and food restriction on performance and thermotolerance of male broiler chickens. Br. Poult. Sci. 40:120–126. Yalcin, S., S. Ozkan, L. Turkmut, and P. B. Siegel. 2001. Responses to heat stress in commercial and local broiler stocks. 1. Performance traits. Br. Poult. Sci. 42:149–152. Zulkifli, I., M. T. Norma, D. A. Israf, and A. R. Omar. 2000. The effect of early age feed restriction on subsequent response to high environmental temperatures in female broiler chickens. Poult. Sci. 79:1401–1407.
