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© 2005 The American Society for Nutritional Sciences J. Nutr. 135:1732-1737, July 2005

Nutrient Requirements

Magnesium Proteinate Is More Protective than Magnesium Oxide in Heat-Stressed Quail

N. Sahin1, M. Onderci, K. Sahin*, G. Cikim{dagger} and O. Kucuk**

Veterinary Control and Research Institute, * Department of Animal Nutrition, Faculty of Veterinary Science, {dagger} Department of Biochemistry, Sarahatun Hospital, 23100, Elazig, Turkey, and ** Karmanos Cancer Institute, Wayne State University, Detroit, MI

1To whom correspondence should be addressed. E-mail: nsahinkm{at}yahoo.com.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
We evaluated the effects of dietary supplementation with Mg-oxide and Mg-proteinate on performance; nutrient digestibilities; malondialdehyde (MDA) concentrations in serum, liver, and thigh meat; and serum cholesterol and triacylglycerol concentrations in Japanese quail (Coturnix coturnix japonica) exposed to high ambient temperature. The birds (n = 360; 10 d old) were randomly assigned to 12 treatment groups consisting of 6 replicates of 5 birds each in a 2 x 2 x 3 factorial arrangement (temperature, Mg source, Mg level). Birds were maintained in temperature-controlled rooms at 22°C for 24 h/d or 34°C for 8 h/d (0900–1700 h) and fed a basal diet or that diet supplemented with 1 or 2 g Mg-oxide or Mg-proteinate/kg of diet. Heat exposure decreased (P = 0.0001) live weight gain, feed intake, feed efficiency, and carcass weight in quail fed the basal diet. A linear increase in feed intake (P = 0.008) and body weight (P = 0.001), and improvements in feed efficiency (P = 0.001), carcass weight (P < 0.0001), digestibility of dry matter, organic matter, crude protein, and ether extract were found in Mg-supplemented, heat-stressed quail. The effects of Mg-proteinate were greater than those of Mg-oxide (P ≤ 0.0001). Serum Mg (P = 0.001) concentration increased, whereas the concentration of MDA in serum (P = 0.0001), liver (P = 0.04), and thigh meat (P = 0.0001) and serum triglyceride and cholesterol concentrations decreased linearly (P = 0.001) with the level of Mg in the diet. Interactions between dietary Mg source, temperature, and level of supplementation (P ≤ 0.05) were found for several variables. Results of the present study suggest that supplementation with Mg-proteinate is more protective than Mg-oxide in reducing the negative effects of heat stress in quail.

KEY WORDS: • magnesium • oxidative stress • performance • quail

High ambient temperature has adverse effects including decreased feed intake, egg production, live weight gain, nutrient digestibility, and feed efficiency in poultry (1–3). Increased mineral excretion is one of the major consequences of heat distress. Belay and Teeter (4) reported lower rates of phosphorus, potassium, sodium, magnesium, sulfur, manganese, copper, and zinc retention in broilers raised at high cycling ambient temperatures (24–35°C) compared with those housed at 24°C. Stress causes secretion of epinephrine and corticosteroids and results in Mg loss in animals and humans (5,6). Donoghue et al. (7) reported that Mg-aspartate supplementation increased the body weight of broilers during heat stress (HS).2

Magnesium plays a role in >300 fundamental enzymatic reactions, including the transfer of phosphate groups, the acylation of coenzyme A in the initiation of fatty acid oxidation, and the hydrolysis of phosphate and pyrophosphate. In addition, it functions in the activation of amino acids, the synthesis and degradation of DNA, and has a key role in neurotransmission and immune function (8). Although few reports about the effects of Mg on poultry meat quality and stability against peroxidation have been published, it was shown that dietary magnesium supplementation of pigs reduces the effects of stress by reducing plasma cortisol and catecholamine concentrations (9,10) and magnesium supplementation may be a viable option for improving meat quality (11,12). The adverse effects of HS on Mg metabolism are becoming increasingly important because they raise environmental concerns. Dietary modifications offer a practical way to alleviate the effect of high environmental temperature on poultry performance. Organic Mg sources such as Mg citrate are more bioavailable than inorganic Mg sources such as MgO and Mg-mica (13–15). The objective of this study was to evaluate the effects of 1 inorganic and 1 organic Mg source, Mg-oxide and Mg-proteinate, on growth, digestibility, and hepatic and meat lipid peroxidation in Japanese quail reared under HS (34°C).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Animals and dietary treatments. Japanese quail (Coturnix coturnix Japonica; n = 360; 10 d old) provided by a commercial company, were used in the study. The experiment was in accordance with animal welfare and ethics and was conducted at the Veterinary Control and Research Institute of Elazig, Turkey. The birds were randomly assigned to 12 treatment groups consisting of 6 replicates of 5 birds each in a 2 x 2 x 3 factorial arrangement of treatments. The first factor was the temperature; the birds were kept in cages in temperature-controlled rooms at 22°C for 24 h [thermoneutral (TN) groups] or 34°C for 8 h/d (0900–1700 h) followed by 22°C for 16 h [heat stress (HS) groups] at 10 d of age. To avoid acclimation, a cycling heat exposure was used. The second factor was Mg source, either Mg-oxide or Mg-proteinate. The third factor was the level of supplementation of Mg-oxide or Mg-proteinate to the diet (0, 1, or 2 g Mg/kg of diet). The birds were fed a starter diet until 21 d of age followed by a grower diet from d 21 to 42. Ingredients and chemical composition of the basal diet are shown in Table 1. The basal diet was formulated using NRC (16) guidelines and contained 22.53 or 19.64 g protein/100 g diet for the starter and grower periods, respectively, with 12.97 MJ (3.10 Mcal) metabolizable energy/kg diet. Quail consumed feed and fresh water ad libitum.


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  		TABLE 1 Ingredients and nutrient composition of diets

 
Feed intake and body weights were recorded at weekly intervals and used to calculate weight gain and feed efficiency of the birds. For carcass evaluations at 42 d, 12 birds were randomly chosen from each group (2/replicate) for slaughter. The birds were not deprived of feed before slaughter; heads were removed and carcasses were cleaned by removing feathers (wet), feet, and visceral organs. Cold carcass weights were calculated after carcasses were kept at 4°C for 18 h. Cold carcass yield was calculated as cold carcass weight divided by body weight at slaughter.

    Sample collection and laboratory analyses. During the last week of the experiment, 60 birds (6 birds from each group; 1/replicate) were placed in individual battery cages for collection of excrement to measure nutrient digestibility [dry matter (DM), organic matter (OM), crude protein (CP), and ether extract (EE)]. The composite excrement samples were oven-dried at 60°C for 48 h, then were ground and subsampled (1 g) for chemical analysis. Digestibility of nutrients was measured using Cr2O3 as described by Petry and Rapp (17). To estimate protein digestibility, excrement N was analyzed chemically according to the method of Terpstra and De Hart (18).

On the last day of the experiment, blood, liver, and thigh samples from different birds (2/replicate) were randomly chosen from each treatment. Blood samples were centrifuged at 3000 x g for 10 min; sera were collected and serum and tissue samples were stored at –70°C until processing. Serum, liver, and thigh meat malondialdehyde (MDA) concentrations were determined (19). Serum triglyceride and cholesterol concentrations were measured using a biochemical analyzer (Olympus AU-600). Chemical analyses of the diets and excrement samples were performed using international procedures of the AOAC (20). Serum concentrations of Mg were measured at specific wavelengths using an atomic absorption spectrometer (Shimadzu AA-660). Calibrations for the Mg assay were conducted with a series of mixtures containing graded concentrations of standard solutions.

    Statistical analyses. The data were analyzed using the General Linear Model procedures of SAS software (21) with the main effects of temperature (T), Mg source (S), and Mg level (L). Least-square treatment means were compared if a significant F statistic (5% level) was detected by analysis of variance. Linear and quadratic polynomial contrasts were used to evaluate the effect of different levels of Mg sources.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Heat exposure decreased (P = 0.0001) performance in quail fed the basal diet (Table 2). Mg supplementation as either Mg-oxide or Mg-proteinate at different levels improved feed intake (P = 0.008), body weight gain (P = 0.001), feed efficiency (P = 0.001), and carcass weight (P = 0.0001) and yield (P = 0.001) in HS quail (Table 2). The increases in feed intake, body weight, feed efficiency, and carcass weight were linear with the amount of Mg supplemented. Variables other than cold carcass weight had temperature x Mg source interactions (P ≤ 0.05). Variables other than feed efficiency had temperature x level interactions (P ≤ 0.02). There were no source x level or temperature x source x level interactions (Table 2).


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  		TABLE 2 Effects of magnesium source and level on performance of heat-stressed quail1

 
Digestibilities of nutrients (DM, OM, CP, and EE) were increased by the supplementation of Mg-oxide and Mg-proteinate (P ≤ 0.0001) in both the TN and HS groups, with the greater effects in the latter (Table 3). Greater improvement was seen in the performance and digestibility variables after Mg-proteinate supplementation (P ≤ 0.0001) than after Mg-oxide. There were few interactions among temperature, source, and level for these variables.


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  		TABLE 3 Effects of magnesium source supplementation on nutrient digestibilities in Japanese quails reared under heat stress1

 
As dietary Mg-oxide and Mg-proteinate supplementation increased in all groups (Table 4), serum Mg (P = 0.001) concentration increased, whereas concentrations of serum (P = 0.0001), liver (P = 0.04), and thigh meat (P = 0.0001) MDA and serum triglyceride and cholesterol concentrations decreased linearly (P = 0.001). Temperature affected serum MDA and Mg concentrations (P = 0.0001). There was an interaction between temperature and source for MDA and triglyceride concentrations, and between temperature and level of supplementation for MDA and Mg levels. There was no source x level or temperature x source x level interactions. Supplementation with Mg improved performance, digestibility of nutrients and carcass quality and the effects of Mg-proteinate were significantly greater than those of Mg-oxide in HS quail.


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  		TABLE 4 Effects of magnesium source supplementation on tissue and serum metabolites in Japanese quails reared under heat stress1

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Magnesium (Mg) activates numerous enzymes in the central pathways of intermediary cellular metabolism (22). In animals, Mg supplementation has traditionally been used as a precautionary treatment to prevent metabolic disorders associated with Mg deficiency (23). Mg requirements of poultry do not exceed 0.6 g/kg dry matter (16); however, stressors increase this requirement. Recent information showed that Mg supplementation may reduce the consequences of stress in animals (10,24) and have beneficial effects on meat quality (12,24). Heat stress is of major concern for the poultry industry because it results in decreased feed intake, poor growth performance and digestion of nutrients, and high mortality (25–29). Excretion of minerals such as Mg, Zn, Cu, and Mn increases under conditions of HS (4). The reduction in feed consumption and the increase in excretion of minerals have adverse effects on poultry performance, health status, and antioxidant concentrations.

In the present study, Mg supplementation had a greater effect on birds kept under HS more than on those reared at TN temperatures. Supplementation partially restored feed intake, body weight gain, feed efficiency, and carcass weight and yield in Japanese quail kept under conditions of HS (34°C) (Table 2). The reduced gain, feed efficiency, and poor carcass weight and yield of heat-exposed birds might be due to a reduction in feed intake and impairment in utilization of nutrients. Gaal et al. (15) reported that Mg supplementation increased weight gain and egg production, and improved the quality of breeding eggs and hatching yield. Although Mg supplementation above recommended levels increased egg production in laying hens (30–32) and mean egg weight (30), Mg-Mica supplementation did not affect the growth performance of swine and cattle kept under TN conditions (13,33). On the other hand, Donoghue et al. (7) reported the Mg-aspartate-hydrochloride reduced body weight loss in heat-stressed hens. Environmental stress increases the secretion of catecholamines, and Mg was shown to reduce the release of the catecholamines norepinephrine and epinephrine (10).

High ambient temperatures suppress nutrient digestibility in broilers by decreasing digestibility of amino acids (34) and the activities of trypsin, chymotrypsin, and amylase (35). Apparent digestibility results for nutrients in the present study agree with findings of Gaal et al. (15) and support the benefits of supplementing dietary Mg (Table 3) because this increased the digestibility of nutrients, partially restoring the negative effects of the stress in Japanese quail. Activation of several enzymes in intermediary metabolism requires Mg, and extracellular/intracellular Mg concentrations would increase enzyme activities. The result of increased activity would be increased ATP production from energy substrates and improved energy utilization (22).

Stress conditions including high ambient temperatures cause increased oxygen radicals, possibly by the disruption of the electron transport assemblies of the membranes (36), and lower the concentrations of antioxidant vitamins and minerals such as vitamins A, C, and E, as well as Zn and Mg in serum (3,37). Heat-induced reactive oxygen species formation may be the factor that causes molecular changes in DNA, proteins, lipids, and other biological molecules (38). The lower levels of the vitamins and minerals may be due to decreased feed intake and the breakdown of these vitamins and minerals by the products of oxidative stress; it may also be the result of increased excretion under stress conditions. Mg deficiency causes increased lipid peroxidation of hepatic tissue and thigh meat and this can be inhibited by Mg supplementation. Parallel to the observations in the study by Guo et al. (14) in which the TBARS value of the thigh meat was decreased as the proteinate Mg supplementation increased, in the present study, significantly lower hepatic and muscle concentrations of MDA were observed in birds receiving Mg supplementation, with the Mg-proteinate producing the higher values. Although in vivo studies reveal that Mg can inhibit peroxidation in animal tissues (39,40), the mechanism by which antioxidants act has not been clarified. Mg may play a very important role in the activation of some enzymes involved in the redox reactions. Magnesium may also attenuate free radical production. It may directly prevent the production of free radicals or it may facilitate the scavenging of free radicals (41). Afanas’ev et al. (42) showed that Mg inhibits reduced NADPH oxidase, an enzyme that produces superoxide radical. Guo et al. (14) reported that supplemental Mg in both the proteinate and oxide forms significantly elevated the activity of hepatic catalase and improved antiperoxidation capacity of broilers. To determine the effect of Mg, Mg-deficient diets also were tried. Dickens et al. (43) showed that Mg deficiency increased cytotoxicity to oxyradicals compared with Mg-rich endothelial cells, indicating that Mg may also protect the endothelial cell from oxyradical injury.

Increased concentrations of blood glucose, triglyceride, and cholesterol are another consequence of heat exposure; supplementation of antioxidant vitamins and minerals decreased these elevated levels (3). Magnesium deficiency also was shown to increase LDL and reduce HDL in rats (44), and an Mg-deficient diet increased serum triglyceride and cholesterol concentrations (45,46). In the present study, a stress-induced elevation in the serum levels of triglyceride and cholesterol was prevented by dietary Mg supplementation. Similarly, Rasic et al. (47) reported that Mg supplementation lowers serum cholesterol and triglyceride levels in rats. Reduction in plasma lipid content in the presence of high serum Mg levels occurs via an increase in the disposal of lipids, but not into fatty acid depots (48).

In conclusion, HS conditions caused significant detrimental effects in Japanese quail, and dietary Mg supplementation offers a feasible way to reduce the losses in performance of Japanese quails reared under HS.


   FOOTNOTES
 
2 Abbreviations used: CP, crude protein; DM, dry matter; EE, ether extract; HS, heat stress; MDA, malondialdehyde; OM, organic matter; TN, thermoneutral. Back

Manuscript received 7 March 2005. Initial review completed 7 April 2005. Revision accepted 18 April 2005.


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