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Article

Boron Supplementation of a Semipurified Diet for Weanling Pigs Improves Feed Efficiency and Bone Strength Characteristics and Alters Plasma Lipid Metabolites^{1 ,2 ,3}

Todd A. Armstrong, Jerry W. Spears⁴, Thomas D. Crenshaw^* and Forrest H. Nielsen

Department of Animal Science and Interdepartmental Nutrition Program, North Carolina State University, Raleigh, NC 27695-7621; ^* Department of Animal Sciences, University of Wisconsin, Madison, WI 53706; and U.S. Department of Agriculture, Agriculture Research Service, Grand Forks Human Nutrition Research Center, Grand Forks, ND 58202-9034

⁴To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Two experiments were conducted to determine effects of dietary boron (B) on performance, plasma minerals and metabolites, and bone characteristics in young pigs. In Experiment 1, 48 pigs (24 males, 24 females; 21 d old) were allotted to pens, which were randomly assigned to one of the following dietary treatments: 1) control (natural ingredient diet; 6.7 mg B/kg diet), 2) control + 5 mg B/kg diet and 3) control + 15 mg B/kg diet. Boron was supplemented as sodium borate. In Experiment 2, 48 pigs (24 males, 24 females; 21 d old) were assigned to the same treatments described in Experiment 1; however, the basal diet was a semipurified diet (0.98 mg B/kg diet). Diets were fed for 40 d; on d 40, blood samples were obtained for determination of plasma mineral and metabolite concentrations. Femurs were harvested from 8 pigs per treatment on d 40 for determination of mechanical properties, ash and lipid percentage. In Experiment 1, B did not affect performance, plasma minerals or metabolites or bone properties. In Experiment 2, B supplementation improved (P < 0.05) the gain:feed ratio and increased plasma cholesterol and triglyceride concentrations. There was a treatment x sex interaction (P < 0.05) in Experiment 2 for bone lipid to be lower and bending moment to be higher, with the response occurring in male pigs. Other dependent variables in Experiment 2 were not affected by treatment. In conclusion, B supplementation of a low B diet elicited responses of physiologic importance to pigs. However, B supplementation of a natural ingredient diet did not elicit a response.

KEY WORDS: • boron • bone • cholesterol • triglycerides • pigs

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Boron (B) was first reported to be essential for plant growth in the early 1920s (Warrington 1923 ), and today B is accepted as an essential element for vascular plant growth (Loomis and Durst 1992 ). However, the essentiality of this ultratrace element in animal nutrition is unclear. Early reports indicated that B supplementation of potassium-deficient rats enhanced survival and increased liver glycogen (Skinner and McHargue 1945 ); however, Follis (1947) was unable to duplicate these findings. The study of B essentiality in animal nutrition was limited until the report that supplemental B stimulated growth and partially corrected leg abnormalities in cholecalciferol-deficient chicks (Hunt and Nielsen 1981 ).

Boron appears to function in bone mineralization and structure. The addition of B and other ultratrace elements to a chick trace mineral premix increased tibial bone ash percentage and reduced the incidence of tibial dyschondroplasia (Edwards 1987 ). Supplementing B to natural ingredient and semipurified diets increased bone ash percentage in broiler chicks (Elliot and Edwards 1992 , Qin and Klandorf 1991 ). In addition to increasing the percentage of ash, B supplementation to chick diets increased tibial breaking load (Rossi et al. 1993 ) and shear fracture energy of the femur, tibia and radius (Wilson and Ruszler 1997 and 1998 ).

Nielsen et al. (1987) reported that supplemental B increased serum testosterone and estradiol concentrations in postmenopausal women. Low B culture conditions have resulted in abnormal development and increased malformations in Xenopus embryos (Fort et al. 1998 , 1999a and 1999b ). In addition, adult frogs maintained in a low B environment had increased numbers of necrotic eggs and abnormal gastrulation of embryos (Fort et al. 1998 ). A deficiency of B impaired embryonic development in rodents (Lanoue et al. 1998 ), and B supplementation stimulated growth of trout (Eckhert 1998 ) and zebrafish (Rowe et al. 1998 , Rowe and Eckhert 1999 ). To our knowledge, no studies have reported physiologic responses of pigs to dietary supplementation of B. These studies were conducted to examine the effects of B supplementation of a natural ingredient or a semipurified basal diet on bone characteristics, plasma minerals and metabolites, and growth in young pigs.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Animal care and feeding.

Two experiments were conducted, utilizing 96 (Experiment 1, n = 48; Experiment 2, n = 48) 21-d-old castrated male and prepubertal female crossbred (Landrace x Yorkshire) x (Hampshire x Duroc) pigs. In each experiment, pigs were allotted to pens on the basis of sex, weight and litter origin. Pens were randomly assigned to receive one of three dietary treatments as follows: 1) control (0 mg supplemental B/kg diet), 2) 5 mg supplemental B/kg diet or 3) 15 mg supplemental B/kg diet. In each experiment, pigs were housed four per pen (two males and two females per pen) with four replicate pens per treatment. Boron was supplemented as sodium borate decahydrate (Na₂B₄O₇·10H₂O; 11.34% B; Sigma Chemical, St. Louis, MO).

In Experiment 1, the basal diet consisted primarily of ground corn, dehulled soybean meal and dried whey (Table 1 ). This basal diet was calculated to contain 20.3% crude protein (CP),⁵ 1.25% lysine, and 14.2 MJ/kg metabolizable energy (ME). In Experiment 2, a semipurified basal diet was formulated utilizing feedstuffs primarily of animal origin, with the exception of cornstarch (Table 2 ). These feedstuffs were chosen in an attempt to formulate a diet low in B (Hunt 1997a ). This basal diet was calculated to contain 15.9% CP, 1.28% lysine and 16.0 MJ/kg ME. The basal diets for both experiments were formulated to meet or exceed the requirements for all nutrients (NRC 1998 ).

Plasma metabolites.

Venous blood samples were obtained from the jugular vein of one half of the pigs in each pen (one randomly chosen male and female per pen) on d 40 to evaluate plasma macromineral concentrations (calcium, magnesium and phosphorus), serum B concentrations (Experiment 2 only), plasma alkaline phosphatase (ALP) activity, and plasma total cholesterol and triglyceride concentrations. Blood for serum B analysis was collected by using a 5-mL syringe and a 20-gauge needle, and transferred to polypropylene tubes to avoid B contamination with borosilicate glassware. Blood for analysis of other plasma metabolites was collected in heparinized trace mineral–free Vacutainer tubes (Becton Dickinson, Franklin Lakes, NJ). Serum and plasma were obtained by centrifugation (1670 x g) of the blood samples at 5°C for 30 min.

Plasma inorganic phosphorus concentrations were determined colorimetrically from the absorbance at 400 nm (Spectronic 1001, Bausch and Lomb, Rochester, NY), after deproteinization with 0.61 mol/L trichloroacetic acid (TCA) and resuspension with vanadomolybdate reagent. Plasma calcium and magnesium concentrations were determined by flame atomic absorption spectrophotometry (Shimadzu, AA-6701F, Kyoto, Japan) after dilution with 0.02 mol/L lanthium chloride (LaCl₃). Serum and basal diet B concentrations were determined using an inductively coupled argon plasma atomic emission spectrometer (Varian Liberty II, Varian, Sugarland, TX) with a detection limit for B of 3 µg B/L as described by Hunt (1997b) . The stock standard was Specpure boric acid (1000 mg B/L; Alfa Aesar, Ward Hill, MA), with calibration standards diluted from this stock. The reference standard for the basal diet analysis was National Institute of Standards and Technology, Standard Reference Material Program 1515 apple leaves (Gaithersburg, MD). The reference standard for the plasma analysis was Utak Blue plasma (Utak Laboratories, Valencia, CA).

Plasma ALP activity was analyzed kinetically by measuring the absorbance at 405 nm of p-nitrophenol produced from the hydrolysis of p-nitrophenyl phosphate using a commercial kit (procedure no. 245; Sigma Diagnostics, St. Louis, MO). Plasma total cholesterol concentrations were determined enzymatically using a commercial kit (procedure no. 352; Sigma Diagnostics), which is a modified method of Allain et al. (1974) . Triglyceride concentrations were determined by measuring the absorbance of formazin at 500 nm after enzymatic reactions using a commercial kit (procedure no. 336; Sigma Diagnostics).

Bone characteristics.

Right and left femurs were obtained from the same pigs from which venous blood samples were obtained (one randomly chosen male and one randomly chosen female per pen) on d 40. Femurs were transported to the laboratory, where muscle and connective tissue were removed. Bones were kept moist, length and weight of the femurs were determined, and bones were frozen at -20°C until mechanical properties and bone ash content were determined. Left femurs were used for the measurement of maximum load after the frozen bones had equilibrated to room temperature (23°C).

Bone mechanical properties were determined from the load-deformation curve generated from a three-point bending test (ASAE Standard S459 1992 ) using an Instron Universal Testing Instrument (Model 1122, Instron, Canton, MA) and the Instron Series IX Automated Materials Testing System Software (version 4.05). The crosshead speed was constant at 10 mm/min. Bending moment, a measure of the force applied to a bone adjusted for the distance over which it is applied (Crenshaw et al. 1981a and 1981b ), was calculated from the following formula: bending moment = (F x L)/4, where F is a measure of the maximum load (kN) and L is the distance between the bottom two fulcra (mm).

At the point of fracture, 3- to 4-mm cross sections were obtained from the shaft of the femur. The cross sections were machined to a thickness of 1 mm, and trabecular bone and marrow were removed. From this cross section, the moment of inertia was determined for the cortical bone. Moment of inertia is a measure of the area distribution around the axis of the center load in the direction of the applied force (Turner and Burr 1993 ). Moment of inertia takes into account both the size and the shape of an object. The thin cross sections were placed on a light table, and the image was digitized with video analysis using the Optimas software (OPTIMAS, version 3.10, Media Cybernetics, Bothell, WA) as described by Vidal (1995) . The moment of inertia parallel to the applied force through the centroid was calculated from the digitized image using the SLICE program (Nagurka and Hayes 1980 ). Total, cortical and medullary areas were also determined from the SLICE program.

Bone stress takes into account both bending moment and moment of inertia. Stress was calculated from the following equation: stress = (F x L x C)/(4 x MI), where F is the measure of the maximum load (N) from the load-deformation curve, L is the length (mm) between the bottom two fulcra supports for the bone during the mechanical test, C (mm) is the radius of the femur cross section, and MI is the moment of inertia (mm⁴) derived from SLICE.

The percentage of bone ash was expressed on a fat-free basis. Cross sections (3–4 mm) of the right femur were weighed and dried for 18 h at 100°C. The bone sections were again weighed, wrapped in filter paper (Fisher Scientific P8, 09–795D, Pittsburgh, PA), placed in a side-arm Soxhlet extraction apparatus, extracted with petroleum ether for 48 h and allowed to air dry under a hood for 48 h. Bone sections were dried at 100°C for 18 h and weighed. The percentage of bone lipid was calculated on the basis of weight loss after solvent extraction of dry bone. The percentage of bone ash was calculated after heating the cross sections of bone in a muffle furnace at 700°C for 48 h. Bone ash was dissolved with heat in 5 mL of 6 mol/L HCl and brought to 50 mL with deionized water. Bone ash calcium and magnesium concentrations were determined by flame atomic absorption spectrophotometry after a 1:250 dilution with 0.02 mol/L LaCl₃. Bone ash copper and zinc concentrations were determined by flame atomic absorption spectrophotometry. Bone ash phosphorus was determined colorimetrically using a commercial kit (procedure no. 670; Sigma Diagnostics) after a 1:61 dilution with deionized water.

Statistical analysis.

Statistical analyses of data were performed by ANOVA using the General Linear Models procedure of SAS (1988) . Pen was considered the experimental unit for animal performance data. Animal was considered the experimental unit for plasma mineral, metabolite and bone characteristic data. The model for average daily gain, average daily feed intake and feed efficiency contained dietary treatment. The model for plasma minerals and metabolites and bone variables contained dietary treatment, sex and treatment x sex interaction. When the treatment x sex interaction was significant (P < 0.05), individual df were partitioned; however, when the treatment x sex interaction was not significant (P > 0.05), data were pooled and presented across sex. Body weights and bone weights were used as covariates in the analyses of bone. Body weight was used as a covariate in the analyses of bone weights, bone lengths and bone mineral concentrations. Significance was declared at a P-value 0.05. Means for each dependent variable were separated using the Least Significant Difference test.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The B concentration of the natural ingredient basal diet in Experiment 1 was 6.7 mg B/kg diet (Table 1) . The semipurified basal diet in Experiment 2 contained 0.98 mg B/kg diet (Table 2) .

Experiment 1.

Boron supplementation had no affect on average daily gain, average daily feed intake or gain:feed ratio in pigs fed the natural ingredient diet (Table 3 ). Plasma calcium, magnesium and phosphorus concentrations were not different among treatments (Table 4 ). Also, ALP activity and plasma total cholesterol and triglyceride concentrations were not affected by B supplementation (Table 4) .

The addition of B to the semipurified basal diet did not affect average daily gain or average daily feed intake (Table 3) . However, the addition of 5 mg B/kg diet improved (P < 0.05) the gain:feed ratio compared with the control and 15 mg B/kg diet treatments.

Plasma calcium, magnesium and phosphorus concentrations were not different among treatments, and ALP activity was not affected by B supplementation (Table 4) . Serum B concentrations increased (P < 0.002) in a dose-responsive manner to dietary B supplementation of the semipurified basal diet (Fig. 1 ). This dose-dependent increase in serum B was present for both male and female pigs in Experiment 2.

View larger version (11K): [in this window] [in a new window]   Figure 1. Serum boron concentrations in weanling pigs fed the semipurified basal diet supplemented with 0, 5 or 15 mg B/kg basal diet. Means (n = 8) and pooled SEM with different letters differ (P < 0.002).

A treatment x sex interaction (P < 0.05) was present for bone lipid percentage (Table 5) . The male pigs supplemented with 5 and 15 mg B/kg diet had a lower (P < 0.05) percentage of bone lipid compared with the male controls. There was no difference in bone lipid percentage for the female pigs. Weight and length of the right and left femurs were not affected by dietary treatment (Table 5) . The fat-free bone ash percentage was not different among treatments, and the concentrations of calcium, phosphorus, magnesium, copper and zinc in the fat-free bone ash were not affected by B supplementation (Table 5) .

A treatment x sex interaction (P < 0.05) was present for maximum bending moment (Table 6) . Maximum bending moment was higher (P < 0.05) in male pigs supplemented with 5 mg B/kg diet. The male pigs supplemented with 15 mg B/kg diet had maximum bending moments that were not different from male control pigs or male pigs supplemented with 5 mg B/kg diet. There was no difference in maximum bending moment for the female pigs. Total, cortical and medullary areas were not affected by B supplementation (Table 6) . The area moment of inertia and bone stress also were not affected by B supplementation (Table 6) .

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
To our knowledge, this is the first study demonstrating the biological importance of B in pigs. These data reveal that physiologic concentrations of supplemental B to a low B semipurified diet can affect serum lipid metabolites and bone mechanical properties. However, in Experiment 1, no responses to B supplementation were detected in any of the dependent variables. We hypothesized that the B requirement of the pigs was met because the natural ingredient basal diet contained 6.7 mg B/kg (Table 1) . Plant legumes such as soybeans and soybean protein by-products are known to be high in B content (Hunt 1997a ).

The daily gain, daily feed intake and feed efficiency were similar between Experiments 1 and 2 (Table 3) . However, pigs consuming the semipurified basal diet supplemented with 5 mg B/kg diet had an improved gain:feed ratio compared with the other two treatments (Table 3) . Naghii and Samman (1996) reported that body weight gain increased at lower doses of B supplementation in rats, with no change at the highest concentration of supplemental B. Previous research has demonstrated improvements in performance variables with B supplementation, but these responses were associated with other nutritional stressors, such as calcium, cholecalciferol, magnesium or potassium deficiencies (Hunt and Nielsen 1981 , Hunt 1996 , Nielsen 1996 ).

Boron supplementation has been shown to affect the concentration of steroid hormones in circulation and their production in vitro. Nielsen et al. (1987) first reported that B supplementation to postmenopausal women increased the serum concentrations of 17ß-estradiol and testosterone. Naghii and Samman (1997) found that B supplementation increased plasma estradiol concentrations and tended to increase plasma testosterone concentrations in men. In addition, testicular homogenates from rats fed supplemental B incubated with androstenedione produced higher concentrations of testosterone than testicular homogenates from rats fed low B diets (Naghii and Samman 1996 ). Androstenedione is an immediate precursor to testosterone in the steroid hormone synthesis pathway (Hadley 1996 ).

Because gonadal steroid hormones are derived from cholesterol and these pigs were either castrated or in the prepubertal period, plasma total cholesterol concentrations were measured in this study. Adrenal and testicular steroid production relies upon cholesterol from extracellular LDL delivered in plasma or serum as the primary substrate (Hadley 1996 ). However, follicular fluid steroids of the ovary are produced from cholesterol delivered from extracellular lipoproteins (as with adrenal and testicular steroids), preformed cholesterol stored in the ovarian cell or cholesterol synthesized de novo in the ovarian cell (Gore-Langton and Armstrong 1994 ). The increase in total plasma cholesterol concentrations in pigs supplemented with 5 mg B/kg diet may be consistent with earlier data that indicate an increase in circulating gonadal steroid hormone concentrations. However, the gilts used in these experiments were in the prepubertal period with relatively low estrogen concentrations, and the barrows were castrated male pigs and lacked endogenous testosterone production.

In Experiment 2, pigs supplemented with 15 mg B/kg diet had increased plasma triglyceride concentrations. Boron supplementation caused an increase in serum triglyceride concentrations in chicks (Hunt and Herbel 1993 ) and rats (Hunt and Herbel 1992 ) during a vitamin D deficiency. In addition, fasting serum triglyceride concentrations were increased by B supplementation in postmenopausal women (Nielsen et al. 1992 ). The relationship between B supplementation and the increase in circulating triglyceride concentrations is unclear; however, Hunt (1996) stated that this increase may be indicative of a shift in the distribution of endogenous fuels.

This study is the first report demonstrating a change in bone lipid percentage with B supplementation in pigs. However, Seal and Weeth (1980) reported that the femurs of rats consuming drinking water containing 150 or 300 mg B/L had a lower fat content. In addition, there is considerable evidence linking B to bone mineralization, structure and strength. Boron supplementation partially corrected leg abnormalities in cholecalciferol-deficient chicks (Hunt and Nielsen 1981 ). Hunt (1989) also reported that B supplementation to cholecalciferol-deficient chicks tended to correct the malformations of marrow sprouts of bone. Boron injected in ovo into turkey eggs increased the tibial length and bone ash percentage (King et al. 1993 ), and bone ash percentage in mature broiler chickens was increased by B supplementation (Elliot and Edwards 1992 , Qin and Klandorf 1991 ).

Bone ash percentage was not affected in these studies, nor were the macromineral concentrations of the bone ash. The percentage of bone that was lipid increased and the percentage of bone that was ash was unchanged; therefore, it is hypothesized that the protein content of the bone may be affected by B supplementation.

The supplementation of 5 mg B/kg diet to the semipurified basal diet increased the maximum bending moment of the femur. This is in agreement with other literature demonstrating that B supplementation increased tibial breaking load (Rossi et al. 1993 ) and increased shear fracture energy of the femur, tibia and radius (Wilson and Ruszler 1997 and 1998 ) in chicks. Vertebral resistance to a crushing force was increased by B supplementation in rats (Chapin et al. 1997 and 1998 ).

A treatment x sex interaction existed for bone lipid percentage and maximum bending moment. In both dependent variables, the male pigs showed a response to B supplementation, whereas the female pigs did not. These data agree with those of Rossi et al. (1993) in which male broilers supplemented with 5 mg B/kg diet had higher body weights than male broilers receiving the control diet with no supplemental B. The supplementation of B did not influence the body weights of the female broilers (Rossi et al. 1993 ). In addition, Rossi et al. (1993) reported that tibias from male broilers supplemented with 5 mg B/kg diet had increased breaking load; however, no tibias from female broilers were tested. Current data indicate a response in bone lipid percentage and maximum bending moment in male pigs fed supplemental B.

In conclusion, when B was supplemented to a low B semipurified basal diet (0.98 mg B/kg diet), it appeared that B was of nutritional importance to pigs. These data agree with previously reported work with B supplementation, and suggest that pigs may provide a useful model for defining and understanding the role of B in human and animal nutrition. However, the supplementation of B to a natural ingredient basal diet (6.7 mg B/kg diet) had no effect on any of the dependent variables measured. This may be due to the high B content of the feedstuffs used in the basal diet for Experiment 1. However, one cannot rule out the fact that the differences in response to supplemental B were due in part to the difference in the ingredient composition of the two basal diets.

	ACKNOWLEDGMENTS

 
We thank Akey, Lewisburg, OH for supplying the vitamin and trace mineral premix. Appreciation is extended to Karen Lloyd, Terry Engle, Cody Wright, Tom Steffel, Curtis Powell, Steve Wagner, Elaine Wood, Timothy Seaboch and Debra Schneider for technical assistance.

	FOOTNOTES

 
¹ Presented in part at the 91st Annual Meeting of the American Society of Animal Science, July 21–23, 1999, Indianapolis, IN [Armstrong, T. A., Spears, J. W. & Stikeleather, L. F. (1999) Effect of boron supplementation on bone characteristics and plasma mineral concentrations in young pigs. J. Anim. Sci. 77 (suppl. 1): 196 (abs.)].

² Mention of a trademark or proprietary product does not constitute a guarantee or warranty of the product by the U.S. Department of Agriculture and does not imply its approval to the exclusion of other products that may also be suitable.

³ The U.S. Department of Agriculture, Agricultural Research Service, Northern Plains Area, is an equal opportunity/affirmative action employer and all agency services are available without discrimination.

⁵ Abbreviations used: ALP, alkaline phosphatase; CP, crude protein; ME, metabolizable energy; TCA, trichloroacetic acid.

Manuscript received January 24, 2000. Initial review completed March 2, 2000. Revision accepted June 9, 2000.

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				N. A. Bakken and C. D. Hunt Dietary Boron Decreases Peak Pancreatic In Situ Insulin Release in Chicks and Plasma Insulin Concentrations in Rats Regardless of Vitamin D or Magnesium Status J. Nutr., November 1, 2003; 133(11): 3577 - 3583. [Abstract] [Full Text] [PDF]

				T. A. Armstrong and J. W. Spears Effect of boron supplementation of pig diets on the production of tumor necrosis factor-{alpha} and interferon-{gamma} J Anim Sci, October 1, 2003; 81(10): 2552 - 2561. [Abstract] [Full Text] [PDF]

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