Effects of Supplemental Boron on Growth Performance and Meat

Article pubs.acs.org/JAFC

Effects of Supplemental Boron on Growth Performance and Meat Quality in African Ostrich Chicks Wei Wang, Ke Xiao, Xinting Zheng, Daiyun Zhu, Zhi Yang, Juan Tang, Pengpeng Sun, Jing Wang, and Kemei Peng* College of Animal Science and Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, People’s Republic of China ABSTRACT: To investigate the effects of boron on growth performance and meat quality, 10-day-old Africa ostrich chicks were randomly divided into 6 groups with 6 replicates in each group. For 80 days, birds in the treatments were fed the same basal diet but given different concentrations of boron-supplemented water. The highest final BW (33.4 ± 0.30 kg), ADFI (376 ± 1.83 g), and ADG (224 ± 1.01 g) appeared in the group receiving 160 mg/L boron (group 4). 160 mg/L boron also decreased drip loss (2.20 ± 0.59), cooking loss (35.3 ± 1.14), and elevated pH value (6.13 ± 0.28) of meat (P < 0.05). Ostrich chicks in the 640 mg/L treatment group (group 6) had the lowest final BW (30.8 ± 1.05 kg) and ADG (208 ± 0.74 g) (P < 0.05). The highest ash (1.35 ± 0.01%) and pH (6.18 ± 0.03) and the lowest protein (20.4 ± 1.74%), drip loss (2.10 ± 0.76%), cooking loss (35.0 ± 0.41%), C18:1 (28.2 ± 0.65%), and C18:3ω3 (2.60 ± 0.51%) appeared in group 6 (P < 0.05) as well. Overall, the optimum concentration of 160 mg/L supplemental boron improved ostrich growth performance and meat quality; however, high concentrations of boron decreased both performance and meat quality. KEYWORDS: boron, African ostrich chicks, growth performance, meat quality

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INTRODUCTION Boron (B) is abundant in water, air, and soil, acts as a Lewis acid, and has characteristics between those of metals and nonmetals.1 Boron is an essential trace element for plants,2 humans, and animals.3,4 It is known that boron performs functions in mineral metabolism, immune response, and the endocrine system,5 and that a low boron intake impairs bone health, brain function, and the immune response.6 In chicks, the addition of dietary boron mitigated negative effects of vitamin D3 deficiency.7 Diets supplemented with 60−120 ppm boron significantly improved broiler growth rate and feed conversion ratio.8 However, boron may be toxic at high doses. Wilson and Ruszler9 fed white leghorn layers with 400 mg/kg dietary boron, resulting in decreased body weight, food consumption, egg weight, and egg production of the birds. Sabuncuoglu et al.10 reported that a subacute dose of 400 mg/kg/day administered orally to rats produced histopathological changes in kidney tissue. Cheng et al.11 added boron to the daily drinking water of ostrich chicks for reducing the incidence of tibial fractures; the results showed that the perimeter, length, weight, and ash content of ostrich tibias were increased significantly with increasing dosages of boron, demonstrating that boron was helpful for ostrich chick’s bone development. Their findings suggested that there was an essential linkage between boron and growth and development of ostriches. Ostrich farming is a rapidly growing industry throughout the world, and ostriches are becoming an important source of meat for humans.12 Ostrich meat is characterized, relative to meat from other species, by a low intramuscular lipid content, a favorable fatty acids profile (PUFA/SFA and n-6/n-3 ratios), low sodium content, and high iron, selenium, and zinc contents.13 With the current tendency toward healthy food, ostrich meat can be viewed as the ideal meat type.14 However, to date, no research © 2014 American Chemical Society

has been conducted to quantify the effect of additional boron on growth performance and meat quality traits in ostriches. The present study investigated the effect of boron on performance and meat quality by applying different doses of boron to drinking water. This research provides a scientific basis for the correct application of boron in ostrich farming.

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MATERIALS AND METHODS

Chemicals. Boric acid was purchased from Sinopharm Chemical Reagent Co., Ltd. (Shanghai, China). Methanol, chloroform, ethyl alcohol, boron trifluoride, dichloromethane, normal hexane, absolute ether, absolute ethyl alcohol, potassium hydroxide, anhydrous sodium sulfate, and trichloromethane were purchased from Chemical Reagent Factory (Tianjing, China). The fatty acids methyl esters (FAMEs) and cholesterol standards were purchased from Sigma-Aldrich Chemical Co., Ltd. (St. Louis, MO). Purified water was supplied by Hangzhou Wahaha Group Co., Ltd. (Hangzhou, China). All reagents used were analytical grade without further purification. Experimental Animals and Breeding Management. Fifty African ostrich chicks (1-day-old) were obtained from a commercial ostrich farm located in Henan China, housed together, and fed with a standard diet. After 10 days, 36 healthy ostriches were selected with similar body sizes and randomly divided into 6 groups with 6 replicates in each group. For 80 days, boric acid was added to the bird’s drinking water (drinking water from the tap, the boron content was 0.11 μg/g, negligible) in different dosages for each treatment group (group 1, 0 mg/L; group 2, 40 mg/L; group 3, 80 mg/L; group 4, 160 mg/L; group 5, 320 mg/L; and group 6, 640 mg/L). Group 1 was the control group. Apart from the different concentrations of boron in the water, the ostriches were fed with the same basic diet. Feed and water were supplied ad libitum. Cleaning of sinks and mangers and disinfecting Received: Revised: Accepted: Published: 11024

April 15, 2014 October 26, 2014 November 2, 2014 November 2, 2014 dx.doi.org/10.1021/jf501789t | J. Agric. Food Chem. 2014, 62, 11024−11029

Journal of Agricultural and Food Chemistry

Article

and b* values; the average of the three readings was used in the statistical analysis. Drip loss (%) was determined according to the method described by Zhang et al.17 Briefly, the muscles were cut into 2 × 2 × 2 cm thick slices, weighed, and suspended in individual plastic bags. After storage for 24 h at 4 °C, the samples were removed from their individual bags, dried with absorbent paper, and weighed again. Drip loss was calculated as weight loss expressed as a percentage of the initial weight of the sample. Cooking loss (%) was determined by placing weighed samples of approximately 100 g into sealed plastic bags and immersing in water at 75 °C (for the sufficient heat penetration without causing excessive denaturation of the collagen present in the meat). Samples were then removed from the water; the bagged samples were allowed to cool in running water to ±25 °C, and then the samples were blotted dry with tissue paper and reweighed. Cooking losses were then calculated by measuring the weight difference before and after cooking, and values were expressed as a percentage of the fresh (uncooked) sample weight. Warner−Bratzler shear force (WBS) was determined on the same samples used for the cooking loss determination. Cooked muscle was cooled to room temperature, and three cylindrical cores were randomly removed from each cooked sample using a 1.27 cm diameter bore to determine Warner−Bratzler shear force values.18 The samples were cut parallel to the direction of the muscle fiber to measure the influence of the myofibrillar proteins. Maximum shear force values were recorded for each cylindrical core of cooked muscle (repeated three times), and the mean values attained from the three samples were used in the statistical analysis. A larger value (kg) indicated a greater shear force and therefore tougher meat. Meat Chemical Analyses. Chemical analyses were carried out on meat samples stored at −20 °C. Moisture, fat, protein, and ash contents were assessed according to AOAC standard techniques19 on minced meat samples after 24 h of thawing at 4 °C. For fatty acid composition, lipid was extracted according to the method used by Folch et al.20 on M. iliofibularis (5 g of ground meat), after which the lipids were analyzed for fatty acids. Fatty acids were quantified as methyl esters, prepared according to the method described by Butte.21 Methyl esters were separated on an Agilent model GC-6400 gas chromatograph equipped with a DB-23 capillary column (length 60 m, internal diameter 0.25 mm, film thickness 0.25 μm). The GC program was set to the following conditions: a helium flow rate of 1 mL/min, FID detector at 250 °C, split−splitless injector at 220 °C, and an injection volume of 0.5 mL. The fatty acid methyl esters (FAME) were identified by comparison of the retention times to those of the FAME standards. Fatty acids were expressed as a percentage of total methylated fatty acids. The determination of cholesterol was performed using the method of Duckett and Wagner.22 This method involved direct saponification of the samples and extraction of the unsaponifiable compounds with cyclohexane. Samples were separated using a Drug Three Mega bore column (10 m, 0.53 mm) maintained at a constant temperature of 285 °C, with the injector temperature set at 300 °C and detector temperature at 320 °C. Helium was the carrier gas (flow rate: 12 mL/ min). The content of cholesterol was quantified using regression equations obtained from cholesterol standards and then corrected using stigmasterol (50 μg/mL) as an internal standard; cholesterol content was expressed as mg/100 g of meat.

the farm and its surroundings was conducted daily. All experiments with ostriches were performed according to protocols approved by the Huazhong Agricultural University Animal Care and Utilization Committee. Experimental Diets and Nutrient Levels. The ostriches were fed with a blend of custom-made premix diet and pak choi based on their physiological needs, developmental stage, and breeding experience.15 Moreover, to aid in digestion, some sand must be added in sufficient but not excessive quantities.16 The nutrient composition of the diets and of each ingredient is reported in Table 1.

Table 1. Ingredients and Composition of the Basal Dietsa ingredients custom-made premix pak choi

content (g/kg)

chemical composition

670

crude protein

330

lysine cystine crude fiber crude fat methionine ash metabolic energy boron in premix boron in pakchoi

content (g/kg) 193 10.0 3.90 76.5 29.1 3.41 87.8 2.94 × 103 kcal 1.78 mg 2.45 mg

a

Supplied per kilogram of diet: 6.30 g of phosphorus, 14.7 g of calcium, 80.0 mg of manganese, 500 mg of magnesium, 11.0 mg of copper, 87.0 mg of zinc, 0.27 mg of selenium, 3.00 mg of iodine, 150 mg of ferrum, 12 000 IU of vitamin A, 3000 IU of vitamin D3, 3.50 mg of vitamin K, 100 IU of vitamin E, 3.50 mg of vitamin B1, 8.10 mg of vitamin B2, 4.00 mg of vitamin B6, 50.4 mg of niacin, 20.9 mg of pantothenic acid, 2.00 mg of folic acid, 0.20 mg of biotin, 1500 mg of choline, and 0.01 mg of vitamin B12. Sample Collection and Processing. At 90 days of age, the birds were weighed after a fasting period of 24 h, and cumulative weight gain and feed intake were determined. Using these values, cumulative feed to gain ratios were calculated. Following these measurements, the birds were electrically stunned and terminated in an ostrich abattoir. The iliofibularis muscles were removed from the left and right legs of each carcass, after removal of the external fat and the epimysium. The muscle samples of every ostrich were divided in two; one was kept at 4 °C until the completion of the physical analysis, and the other was frozen at −20 °C for further chemical analysis. Each sample was ground, homogenized, and vacuum-packed in plastic bags. Meat Physical Analyses. At 24 h post-mortem, meat pH was measured on the iliofibularis muscles with a Testo 205 pH meter (Testo AG, Germany), equipped with an insertion glass electrode (calibrated at pH 4.01 and 7.00 at the abattoir temperature). Three readings were made on each sample, and the mean was recorded. Meat color was measured on 4 cm thick muscle slices (cut 24 h post-mortem), according to the CIE L*a*b* color system (where L* measures relative lightness, a* measures relative redness, and b* measures relative yellowness) using a Colorgard System 2000 colorimeter (Pacific Scientific, Silver Spring, MD). Three measurements were taken per sample at random positions to determine L*, a*,

Table 2. Effect of Boron on Growth Performance of African Chicksa items final BW/kg ADFI/g ADG/g feed conversion

group 1 32.0 364 214 1.71

± ± ± ±

0.04 b 1.21 b 2.31 c 0.31

group 2 32.7 364 215 1.70

± ± ± ±

0.02 ab 0.94 b 1.02 bc 0.88

group 3 32.9 371 219 1.69

± ± ± ±

0.70 ab 2.25 ab 0.96 b 0.74

group 4 33.4 376 224 1.68

± ± ± ±

0.30 a 1.83 a 1.01 a 0.05

group 5 31.9 364 210 1.71

± ± ± ±

1.04 c 0.04 b 0.63 d 0.92

group 6 30.8 360 208 1.71

± ± ± ±

1.05 c 2.13 b 0.74 d 1.49

a

In the same row, values with different letters indicate significant differences (p < 0.05), while the same or no letters indicate no significant difference (p > 0.05). The same applies for all tables. 11025

dx.doi.org/10.1021/jf501789t | J. Agric. Food Chem. 2014, 62, 11024−11029


Article

Table 3. Mean Values (Mean ± Standard Deviation) for the Physical Meat Quality Parameters Measured in M. iliofibularis (Groups 1−6) parameter pH CIE L* CIE a* CIE b* drip loss (%) cooking loss (%) WBS (kg)

group 1 6.01 37.7 15.9 9.73 2.36 36.7 3.61

± ± ± ± ± ± ±

1.32 b 1.04 0.33 0.03 0.06 a 0.02 a 0.27

group 2 6.03 37.3 15.7 9.82 2.34 36.2 3.60

± ± ± ± ± ± ±

0.55 b 0.25 0.16 0.31 0.43 a 0.23 a 0.81

group 3 6.07 37.1 15.9 9.80 2.29 36.1 3.60

± ± ± ± ± ± ±

0.12 ab 1.44 0.64 0.52 1.06 ab 0.91 ab 0.93

Statistical Analysis. All of the samples were measured in triplicate; the average of the three values was used in the statistical analysis. Data were analyzed using the SPSS 17.0 software (SPSS Inc., Chicago, IL). A one-way analysis of variance (ANOVA) was used to evaluate the effects of different concentrations of boron on the performance and meat quality of the African ostrich chicks. Duncan’s multiple range tests were performed to denote differences between the groups when differences were significant (a probability level of 5% was considered significant (p < 0.05) for all tests). All values were expressed as the means ± standard deviations.

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group 4 6.13 37.0 16.0 9.61 2.20 35.3 3.59

± ± ± ± ± ± ±

0.28 a 0.83 0.03 1.31 0.59 b 1.14 b 0.19

group 5 6.15 36.6 16.0 9.91 2.14 35.2 3.58

± ± ± ± ± ± ±

1.17 a 0.52 0.06 0.42 1.04 b 0.06 bc 0.40

group 6 6.18 36.3 16.3 9.84 2.10 35.0 3.59

± ± ± ± ± ± ±

0.03 a 1.51 0.17 0.34 0.76 c 0.41 c 1.73

To the best of our knowledge, there are no reports of the effect of boron on physical meat quality parameters. The data clearly showed that the pH value of the meat was significantly increased by supplemental boron at 160, 320, and 640 mg/L (P < 0.05) (Table 3). The pH value of meat depends on the content of lactic acid in the muscles, and after the slaughter, muscle glycogen glycolysis is the main source of lactic acid.28 It is widely accepted that there is a close correlation between muscle pH values and glycogen.29 The high ultimate pH of the meat is a consequence of depleted muscular glycogen reserves prior to slaughter and greatly affects meat quality.30 Boron has a major role in controlling certain metabolic pathway processes using hydrolases or oxidoreductases.4,31 These enzymes need pyridine or flavin nucleotides (NAD+, NADP, or FAD) to promote the enzyme activity. Boron reversibly inhibits their activity by forming transition state analogs or competing for NAD or FAD.4,31 Boron can also inhibit NAD directly to affect enzyme activity.32−34 NAD is an important reaction substrate of glycolysis; boron inhibits the glycolytic pathway by acting on NAD, thus reducing the lactic acid content of muscle and increasing pH value. Geyikoğglu and Türkez35 reported that high boric acid doses (3.375 and 4.5 mmol B/kg b.wt.) caused decreased metabolite concentrations (glucose, glycogen, lactate, and ATP) in breast muscle of broiler chickens, thus increasing the muscle pH value. In the present study, the pH value of the meat was significantly increased by 160, 320, and 640 mg/L boron in the drinking water, which could be due to the additional boron reducing lactic acid and glycogen content in the muscles. The drip loss and cooking loss were significantly decreased by supplemental boron at 160, 320, and 640 mg/L (P < 0.05) (Table 3). Meat that has a higher pH has a stronger water holding capacity (WHC) and lower moisture loss.36 Lower drip loss and cooking loss were, therefore, expected for the samples of groups 4, 5, and 6. The results confirmed that the drip loss and cooking loss of these groups were significantly decreased as compared to those of the control group (P < 0.05). The significant increase in the ultimate pH of groups 4, 5, and 6 could account for this finding. There were no significant differences between treatments with regard to meat color or shear force values (P > 0.05) (Table 3). At a higher meat pH, protein can bind more strongly with water, allowing less free water; therefore, meat will be darker in color because there is less free water to reflect light.37 Although not significant, groups 4, 5, and 6 had lower L* values. Lanza et al.38 reported that there was a negative correlation (r = −0.41; P < 0.05) between shear force values and ultimate pH, but in this study, no significant changes were detected for the shear force values with increasing pH value, suggesting that the inclusion of boron in the drinking water of

RESULTS AND DISCUSSION

Growth Performance. The results of the growth performance of the birds are presented in Table 2. The final BW of the birds fed 160 mg/L boron was significantly higher than that of the control group (0 mg/L) (P < 0.05), and the addition of 320 and 640 mg/L boron significantly decreased the final BW of the ostrich chicks when compared to the other groups (P < 0.05). The ADFI of the birds was significantly increased by 160 mg/L supplemental boron in drinking water (P < 0.05); however, the other boron levels had no significant effect on ADFI. Adding 80 and 160 mg/L boron significantly increased the ADG of the birds, and 320 and 640 mg/L boron significantly decreased the ADG of the birds (P < 0.05). Boron had no effect on feed conversion. In the present study, final BW, ADFI, and ADG of the birds significantly increased (P < 0.05) with supplementation of boron at 160 mg/L level (Table 2). Similar results were obtained in broilers fed 60−120 mg/kg boron8 and hens fed 100 and 200 mg/kg boron.23 Final BW and ADG were depressed by the higher levels of boron (320 and 640 mg/L) (Table 2), agreeing with results obtained in broilers fed 300 mg/kg boron,8 layers fed 400 mg/kg boron,9,23 hens fed 400 mg/kg boron,24 and Japanese quails fed 10, 60, 120, and 240 mg/kg boron.25 However, there were no differences in feed conversion between the groups (Table 2). In previous studies, feed conversion was not affected by 80 mg/kg boron in broilers,26 by 5, 10, 50, 100, 200, and 400 mg/kg boron in the hens,24 or by 5 and 15 mg/kg boron in pigs.27 The results (Table 2) of this study indicated that 160 mg/L boron supplementation improved growth performance in ostrich chicks, but 320 and 640 mg/L boron supplementation inhibited growth performance. Physical Meat Quality Parameters. The effects of different concentrations of boron on the physical meat quality parameters of the ostrich chicks are reported in Table 3. The drip loss and cooking loss of meat were significantly decreased by supplemental boron at 160, 320, and 640 mg/L. Further, the addition of 160, 320, and 640 mg/L boron to drinking water significantly increased the pH value of the meat (p < 0.05). The color and WBS values of meats did not differ among the birds administered different boron levels (P > 0.05). 11026



Article

Table 4. Mean Values (Mean ± Standard Deviation) for the Chemical Meat Quality Parameters Measured in M. iliofibularis (Groups 1−6) parameter moisture (%) fat (%) protein (%) ash (%) FA (%) SFA C12:0 C14:0 C15:0 C16:0 C18:0 FA (%) MUFA C16:1 C18:1 C20:1 C22:1 FA (%) PUFA C18:2ω6 C18:3ω3 C20:2ω6 C20:5ω3 C22:6ω3 cholesterol (mg/100 g)

group 1

group 2

group 3

group 4

group 5

group 6

77.8 0.49 21.0 1.00

± ± ± ±

1.44 0.40 0.41 a 0.03 b

77.9 0.50 20.9 1.01

± ± ± ±

1.46 0.07 1.36 a 0.13 b

77.0 0.50 20.7 1.03

± ± ± ±

0.83 0.42 1.05 ab 0.24 ab

76.9 0.51 20.7 1.13

± ± ± ±

1.23 0.33 0.66 ab 0.08 ab

76.8 0.51 20.5 1.20

± ± ± ±

0.31 0.26 1.21 b 0.04 ab

76.8 0.52 20.4 1.35

± ± ± ±

1.20 0.03 1.74 c 0.01 a

0.04 1.06 0.23 21.7 14.9

± ± ± ± ±

0.02 0.04 0.01 0.72 0.01

0.04 1.03 0.23 21.6 14.9

± ± ± ± ±

0.03 0.01 0.02 0.34 0.03

0.04 1.01 0.23 21.9 14.9

± ± ± ± ±

0.13 0.01 0.23 0.21 0.21

0.05 1.12 0.24 22.0 14.8

± ± ± ± ±

0.42 0.42 0.33 0.10 0.03

0.04 1.10 0.23 21.1 14.9

± ± ± ± ±

0.07 0.72 0.11 0.02 0.01

0.05 1.07 0.23 21.2 15.0

± ± ± ± ±

0.53 0.18 0.21 0.81 0.03

6.13 29.8 0.31 5.77

± ± ± ±

0.32 0.33 a 0.05 0.01

6.13 29.0 0.31 5.74

± ± ± ±

0.02 0.04 a 0.04 0.02

6.14 28.8 0.30 5.74

± ± ± ±

0.07 0.30 a 0.13 0.05

6.13 28.7 0.30 5.71

± ± ± ±

0.11 0.14 a 0.12 0.13

6.14 28.4 0.29 5.79

± ± ± ±

0.43 0.17 ab 0.02 0.04

6.13 28.2 0.27 5.73

± ± ± ±

0.01 0.65 b 0.31 0.02

18.0 2.81 0.29 0.52 0.31 60.4

± ± ± ± ± ±

0.03 0.04 a 0.01 0.32 0.53 0.87

18.9 2.80 0.29 0.51 0.31 60.0

± ± ± ± ± ±

0.01 0.13 a 0.01 0.03 0.01 0.42

19.1 2.80 0.28 0.49 0.28 59.9

± ± ± ± ± ±

0.37 0.32 a 0.04 0.04 0.06 0.12

19.0 2.77 0.30 0.50 0.30 59.7

± ± ± ± ± ±

0.03 0.01 ab 0.45 0.90 0.42 1.33

18.0 2.71 0.27 0.48 0.29 59.7

± ± ± ± ± ±

0.32 0.03 ab 0.03 0.38 0.03 0.92

19.2 2.60 0.30 0.53 0.32 59.5

± ± ± ± ± ±

0.96 0.51 b 0.19 1.42 0.73 1.42

the high dose (640 mg/L) than at the low doses (0, 40, 80, 160, 320 mg/L). The ash content increased gradually due to the boron raising the mineral content of the muscle, but more research is needed to further quantify this. As mentioned above, boron can inhibit the activity of NAD,32−34 and, because serine proteases require pyridine or flavin nucleotides (NAD+, NADP, or FAD), boron can inhibit the activity of serine proteases. Serine proteases are one of the most abundant groups of proteolytic enzymes; they are involved in many physiological processes through the proteolytic activation of precursor proteins.41 The addition of boron inhibited the activity of serine proteases, so that macromolecule proteins cannot be broken down into smaller proteins, resulting in the relatively low protein content of the ostrich meat. This may be the cause of the decrease in muscle protein with increasing doses of boron supplementation. Hall et al. 42 reported that when boron was orally administered (8 mg/kg/day) to rats, daily for 14 days, TG levels and LDL cholesterol decreased. Basoglu et al.43 suggested that boron had positive effects on hepatic steatosis and visceral fat by affecting the lipid profile and reducing oxidative stress. The administration of sodium borate decreased concentrations of total cholesterol, triglyceride, high-density lipoprotein, lowdensity lipoprotein, and nonesterified fatty acids in the blood.3 Several studies have indicated that boron could improve lipid metabolic profiles. Until now, the research has only been conducted in serum; there is no literature reporting changes of lipid substances in the muscle when boron is administered. Our experiment showed that boron had no influence on the percentages of SFA and cholesterol in meat, but the proportion of C18:1 and C18:3ω3 significantly (P < 0.05) decreased at the highest dosage (640 mg/L). In conclusion, we investigated the effect of boron on the growth performance and meat quality of African ostrich chicks, and our results showed that additional boron improved these parameters, but a high dose of boron had a negative effect.

ostrich chicks does not have any effect on the tenderness of meat. Chemical Meat Quality Parameters. The effects of different levels of boron on chemical meat quality parameters of ostrich chicks are reported in Table 4. The parameters that differed in the current study were protein, ash, C18:1, and C18:3ω3; significantly lower protein was found in the treatments of 320 and 640 mg/L boron; lower C18:1 and C18:3ω3 were found with the dose of 640 mg/L boron, and higher ash was found with the 640 mg/L boron (p < 0.05) dose. No significant effects of the boron treatment for moisture, fat, SFA, or cholesterol of meat were found for any birds in the trial. The moisture of muscle was decreased with increasing dosages of the boron supplement in the drinking water, but no significant difference (P > 0.05) was observed between the treatment groups. Eren et al.25 reported that boron had no effect on the moisture of Japanese quail meat, which was consistent with our results. Eren et al.25 also reported that fat in the meat of male Japanese quails was increased with boron supplements of 10, 60, 120, 240 mg/kg, and in females, 120 and 240 mg/kg boron increased fat percentages in the meat (P < 0.05). In the present study, the fat of the muscle increased with increasing doses of boron, but it was not significant (P < 0.05). This trend for fat was similar to previous research. The ash content of muscle is representative of mineral and trace element content.39 Boron has a regulatory role in the metabolism of several minerals such as magnesium, phosphorus, molybdenum, and calcium.23 Shang et al.40 showed that the addition of boron in drinking water could improve the contents of iron and zinc in chicken meat. Similarly, Eren et al.25 reported that 240 mg/kg boron increased ash percentages in the meat of Japanese quails (P < 0.05). Our results also showed that ash of muscle was increased with increasing dosage of boron, and ash content was significantly (P < 0.05) higher at 11027



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(14) Majewska, D.; Jakubowska, M.; Ligocki, M.; Tarasewicz, Z.; Szczerbińska, D.; Karamucki, T.; Sales, J. Physicochemical characteristics, proximate analysis and mineral composition of ostrich meat as influenced by muscle. Food Chem. 2009, 117, 207−211. (15) Cilliers, S.; Hayes, J.; Chwalibog, A.; Sales, J.; Du Preez, J. Determination of energy, protein and amino acid requirements for maintenance and growth in ostriches. Anim. Feed Sci. Technol. 1998, 72, 283−293. (16) Liang, C. Z.; Yang, Y. J. Ostrich-Raising Management and Disease Control; Beijing Agricultural University Press: Beijing, 1996; pp 42− 56. (17) Zhang, W.; Xiao, S.; Lee, E. J.; Ahn, D. U. Consumption of oxidized oil increases oxidative stress in broilers and affects the quality of breast meat. J. Agric. Food Chem. 2010, 59, 969−974. (18) Jiang, Z.; Lin, Y.; Zhou, G.; Luo, L.; Jiang, S.; Chen, F. Effects of dietary selenomethionine supplementation on growth performance, meat quality and antioxidant property in yellow broilers. J. Agric. Food Chem. 2009, 57, 9769−9772. (19) AOAC. Official Methods of Analysis; Association of Official Analytical Chemists: Washington, DC, 2000. (20) Folch, J.; Lees, M.; Sloane-Stanley, G. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957, 226, 497−509. (21) Butte, W. Rapid method for the determination of fatty acid profiles from fats and oils using trimethylsulphonium hydroxide for transesterification. J. Chromatogr., A 1983, 261, 142−145. (22) Duckett, S. K.; Wagner, D. G. Effect of laidlomycin propionate on bovine longissimus muscle fatty acid and cholesterol content. J. Agric. Food Chem. 1997, 45, 1725−1728. (23) Wilson, J.; Ruszler, P. Effects of dietary boron supplementation on laying hens. Br. Poult. Sci. 1996, 37, 723−729. (24) Eren, M.; Uyanik, F.; Kücu̧ ̈kersan, S. The influence of dietary boron supplementation on egg quality and serum calcium, inorganic phosphorus, magnesium levels and alkaline phosphatase activity in laying hens. Res. Vet. Sci. 2004, 76, 203−210. (25) Eren, M.; Kocaoglu-Güclü, B.; Uyanik, F.; Karabulut, N. The effects of dietary boron supplementation on performance, carcass composition and serum lipids in Japanese quails. J. Anim. Vet. Adv. 2006, 5, 1105−8. (26) Elliot, M. A.; Edwards, H. M. Studies to determine whether an interaction exists among boron, calcium, and cholecalciferol on the skeletal development of broiler chickens. Poult. Sci. 1992, 71, 677− 690. (27) Armstrong, T.; Spears, J. Effect of dietary boron on growth performance, calcium and phosphorus metabolism, and bone mechanical properties in growing barrows. J. Anim. Sci. 2001, 79, 3120−3127. (28) Zhong, Q. Z.; Wang, D.; Lou, Y. J. Research development in effects of heat stress on meat quality of poultry. China Anim. Husb. Vet. Med. 2011, 38, 231−234. (29) Warriss, P. D. Meat Science: An Introductory Text; CABI Publishing: Wallingford, UK, 2010. (30) Silva, J.; Patarata, L.; Martins, C. Influence of ultimate pH on bovine meat tenderness during ageing. Meat Sci. 1999, 52, 453−459. (31) Hunt, C. D. Regulation of enzymatic activity. Biol. Trace Elem. Res. 1998, 66, 205−225. (32) Strittmatter, P. Reversible direct hydrogen transfer from reduced pyridine nucleotides to cytochrome b5 reductase. J. Biol. Chem. 1964, 239, 3043−3050. (33) Deitrich, R. A. Diphosphopyridine nucleotide-linked aldehyde dehydrogenase: III. Sulfhydryl characteristics of the enzyme. Arch. Biochem. Biophys. 1967, 119, 253−263. (34) Deal, W. C., Jr. Metabolic control and structure of glycolytic enzymes. IV. Nicotinamide adenine dinucleotide-dependent in vitro reversal of dissociation and possible in vivo control of yeast glyceraldehyde-3-phosphate dehydrogenase synthesis. Biochemistry 1969, 8, 2795−2805.

According to our results, 160 mg/L boron was the optimal dosage for growth performance and meat quality of African ostrich chicks.

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AUTHOR INFORMATION

Corresponding Author

*Tel.: 86-27-87286970. Fax: 86-27-87280408. E-mail: [email protected]. Funding

This study was supported by the National Natural Science Foundation of China no. 31272517. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Lingqiao Ma for her skillful assistance in conducting this experiment. ABBREVIATIONS USED BW, body weight; AOAC, Association of Official Analytical Chemists; ADFI, average daily feed intake; ADG, average daily gain; NAD, nicotinamide adenine dinucleotide; NADP, nicotinamide-adenine dinucleotide phosphate; FAD, flavin adenine dinucleotide; ATP, adenosine triphosphate; TG, triglyceride; LDL, low density lipoprotein; SFA, saturated fatty acid; MUFA, monounsaturated fatty acid; PUFA, polyunsaturated fatty acid

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REFERENCES

(1) Criste, R. D.; Grossu, D. V.; Scorei, R.; Duca, R. C.; Mitrut, M.; Ciurascu, C. New investigations on the effect of the dietary boron on broilers and layers: boron and food quality. Arch. Zootec. 2005, 8, 65− 78. (2) Mondy, N. I.; Munshi, C. B. Effect of boron on enzymic discoloration and phenolic and ascorbic acid contents of potatoes. J. Agric. Food Chem. 1993, 41, 554−556. (3) Kabu, M.; Civelek, T. Effects of propylene glycol, methionine and sodium borate on metabolic profile in dairy cattle during periparturient period. Rev. Med. Vet. (Toulouse, Fr.) 2012, 163, 419−430. (4) Hunt, C. D. Dietary boron: progress in establishing essential roles in human physiology. J. Trace Elem. Med. Biol. 2012, 26, 157−160. (5) Kabu, M.; Akosman, M. S. Biological effects of boron. Reviews of Environmental Contamination and Toxicology; Springer: New York, 2013; pp 57−75. (6) Nielsen, F. H. Is boron nutritionally relevant? Nutr. Rev. 2008, 66, 183−191. (7) Hunt, C. D.; Herbel, J. L.; Idso, J. P. Dietary boron modifies the effects of vitamin D3 nutrition on indices of energy substrate utilization and mineral metabolism in the chick. J. Bone Miner. Res. 1994, 9, 171−182. (8) Rossi, A.; Miles, R.; Damron, B.; Flunker, L. Effects of dietary boron supplementation on broilers. Poult. Sci. 1993, 72, 2124−2130. (9) Wilson, J.; Ruszler, P. Long term effects of boron on layer bone strength and production parameters. Br. Poult. Sci. 1998, 39, 11−15. (10) Tavil Sabuncuoglu, B.; Aribal Kocaturk, P.; Yaman, O.; Ozelci Kavas, G.; Tekelioglu, M. Effects of subacute boric acid administration on rat kidney tissue. Clin. Toxicol. 2006, 44, 249−253. (11) Cheng, J.; Peng, K.; Jin, E.; Zhang, Y.; Liu, Y.; Zhang, N.; Song, H.; Liu, H.; Tang, Z. Effect of additional boron on tibias of African ostrich chicks. Biol. Trace Elem. Res. 2011, 144, 538−549. (12) Sales, J.; Hayes, J. Proximate, amino acid and mineral composition of ostrich meat. Food Chem. 1996, 56, 167−170. ̇ (13) Ö zsaraç, N.; Kolsarici, N.; Demirok, E. A study on nutritional characteristics of ostrich meat. Electronic J. Food Technol. 2013, 8, 63− 68. 11028



Article

(35) Geyikoğglu, F.; Türkez, H. Acute toxicity of boric acid on energy metabolism of the breast muscle in broiler chickens. Biologia 2007, 62, 112−117. (36) Page, J.; Wulf, D.; Schwotzer, T. A survey of beef muscle color and pH. J. Anim. Sci. 2001, 79, 678−687. (37) Johnston, D.; Knight, M.; Ledward, D. A. The Chemistry of Muscle-Based Foods; The Royal Society of Chemistry: Thomas Graham House, Science Park, Cambridge, U.K., 1992; pp 128−139. (38) Lanza, M.; Fasone, V.; Galofaro, V.; Barbagallo, D.; Bella, M.; Pennisi, P. Citrus pulp as an ingredient in ostrich diet: effects on meat quality. Meat Sci. 2004, 68, 269−275. (39) Liu, X. Integrated Study on the Characters of Fish Meat; Xiamen University: Xiamen, 2007; pp 3−4. (40) Shang, Z. F.; Gu, Y. F.; Chen, H. L.; Yang, J. F.; Pu, X. M.; Zha, L.; Wu, Q. T.; Wang, Y. Influence of boron on content of copper, zinc, iron and manganese in chicken meat. Stud. Trace Elem. Health 2004, 11, 31−33. (41) Neurath, H. Evolution of proteolytic enzymes. Science 1984, 224, 350−357. (42) Hall, I.; Spielvogel, B.; Griffin, T.; Docks, E.; Brotherton, R. The effects of boron hypolipidemic agents on LDL and HDL receptor binding and related enzyme activities of rat hepatocytes, aorta cells and human fibroblasts. Res. Commun. Chem. Pathol. Pharmacol. 1989, 65, 297−317. (43) Basoglu, A.; Baspinar, N.; Ozturk, A. S.; Akalin, P. P. Effects of boron administration on hepatic steatosis, hematological and biochemical profiles in obese rabbits. Trace Elem. Electrolytes 2010, 27.

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Effects of Supplemental Boron on Growth Performance and Meat

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