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J. Anim. Sci. 2005. 83:2434-2439
© 2005 American Society of Animal Science

ANIMAL NUTRITION

Influence of dietary manganese on performance, lipid metabolism, and carcass composition of growing and finishing steers1,2

L. R. Legleiter, J. W. Spears3 and K. E. Lloyd

Department of Animal Science and Interdepartmental Nutrition Program, North Carolina State University, Raleigh 27695-7621


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 Implications
 Literature Cited
 
A study was conducted to determine the effect of dietary Mn on performance of growing and finishing steers, and to evaluate the effect of pharmacological concentrations of Mn on lipid metabolism and subsequent carcass quality in steers. One hundred twenty Angus cross steers were blocked by BW and origin and assigned randomly to one of six treatments (four replicate pens per treatment) providing 0 (control), 10, 20, 30, 120, or 240 mg of supplemental Mn/kg of DM from MnSO4. Steers were fed a corn silage-based growing diet for 84 d, and then switched to a corn-based finishing diet for an average of 112 d. The control growing diet analyzed 29 mg of Mn/kg of DM, whereas the control finishing diet analyzed 8 mg of Mn/kg of DM. Jugular blood samples were obtained on d 56 of the growing and finishing phase for plasma Mn and glucose analysis. Final BW, DMI, ADG, and G:F did not differ (P = 0.38 to P = 0.98) across treatments during growing and finishing phases. Plasma Mn concentrations were not affected by treatment; however, liver and LM Mn at slaughter increased linearly (P = 0.02 and 0.002, respectively) with increasing dietary Mn. Plasma glucose concentrations did not differ (P = 0.90) among treatments. Serum nonesterified fatty acid concentrations tended (P = 0.10) to decrease linearly with increasing dietary Mn on d 56 of the finishing phase. Longissimus muscle lipid concentration was affected quadratically (P = 0.08) by dietary Mn. Muscle lipid seemed to increase slightly when steers were fed 30 or 120 mg of Mn/kg of DM, but decreased with the addition of 240 mg of Mn/kg of DM. Carcass characteristics were not affected by dietary Mn. Manganese concentrations of 29 and 8 mg/kg of DM in the growing and finishing diets, respectively, were adequate for maximizing performance of growing and finishing steers in this experiment. Supplementing physiological or pharmacological concentrations of Mn affected lipid metabolism; however, this did not result in altered carcass characteristics.

Key Words: Cattle • Growth • Lipid Metabolism • Manganese


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 Implications
 Literature Cited
 
The Mn requirement for growing cattle is listed as 20 mg of Mn/kg of DM (NRC, 1996Go). The requirement is based on limited research (Bentley and Phillips, 1951Go; Rojas et al., 1965Go). To our knowledge, the requirement for Mn has not been evaluated for growing or finishing steers in confinement. In addition, little research has focused on the biological role(s) of Mn in cattle.

Manganese has been shown to influence lipid metabolism in several studies using mice and rats as models. Baly et al. (1990)Go demonstrated that isolated adipocytes from Mn-deficient rats had decreased uptake of glucose, decreased insulin receptors, and decreased triglyceride synthesis compared with rats fed adequate Mn. High dietary Mn has been shown to be insulinomimetic and to increase glucose uptake by isolated rat adipocytes (Ueda et al., 1984Go; Baquer et al., 2003Go).

Smith and Crouse (1984)Go established that i.m. fat preferentially utilizes glucose as an acetyl unit precursor, whereas s.c. adipose primarily utilizes acetate for lipogenesis in cattle. Schoonmaker et al. (2003)Go stimulated increased serum insulin and glucose in early-weaned steers by providing a high-concentrate finishing diet ad libitum, and subsequently increased ultrasound measured i.m. fat at 218 d of age. The effect of dietary Mn on lipid metabolism in cattle has not been evaluated.

The present study was conducted to evaluate the effect of dietary Mn on the performance and tissue Mn concentrations of growing and finishing steers. The effects of physiological and pharmacological concentrations of Mn on lipid metabolism and subsequent carcass characteristics also were evaluated.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 Implications
 Literature Cited
 
Animal and Experimental Design
One hundred twenty Angus cross steers (248 kg initial BW) were used in this study. All care, handling, and sampling procedures were approved by the North Carolina State University Animal Care and Use Committee before the initiation of the experiment. Upon arrival, cattle were vaccinated for protection against infectious bovine rhinotracheitis, bovine viral diarrhea (I and II), parainfluenza-3, bovine respiratory syncitial virus, (Titanium 5, AgriLabs, St. Joseph, MO) and Clostridial organisms (Vision 7, Intervet, Millsboro, DE). Cattle also were treated for internal and external parasites (Bovimec, Virbac, Fort Worth, TX). Steers were weighed on two consecutive days at the start of the growing study. Steers were stratified by BW and origin into four blocks and assigned randomly to one of six treatments within each block. Treatments consisted of control (no supplemental Mn), 10, 20, 30, 120, or 240 mg of supplemental Mn/kg of DM. Supplemental Mn was provided from MnSO4·H2O (Sulfamex, Veracruz, Mexico). Diets were formulated to meet or exceed all nutrient requirements with the exception of Mn (NRC, 1996Go). For the growing phase, steers were fed a corn silage-based diet (Table 1Go; control growing diet contained 29.2 mg of Mn/kg of DM) once daily in amounts adequate to allow ad libitum intake. After d 84, steers were gradually switched to a high-concentrate finishing diet (Table 1Go; control finishing diet contained 8.1 mg of Mn/kg of DM) over a 7-d period, and implanted with Synovex-Plus (Fort Dodge Animal Health, Fort Dodge, IA). Treatments and feeding regimen remained the same as in the growing phase. Steers were housed in groups of five in covered, slotted-floor pens (3 x 4 m) with concrete feed bunks.


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  		Table 1. Ingredient composition of basal diets
 
All steers were weighed every 28 d, and jugular blood samples were collected from four steers per treatment on d 0 and from eight steers per treatment (two steers per pen) on d 56 of both the growing and finishing phases. Blood was collected into heparinized tubes specifically designed for trace mineral analysis (Vacutainer 9735, Becton Dickinson, Franklin Lakes, NJ) for Mn determination. Blood for glucose analysis was collected into tubes containing potassium oxalate and sodium fluoride (Vacutainer 6470, Becton Dickinson). On d 56 of the finishing phase, a blood sample also was collected into a tube with no additive (Vacutainer 6431, Becton Dickinson) for serum NEFA determination. Blood samples were transported on ice back to the laboratory and centrifuged at 1,200 x g at 4°C for 20 min. Plasma and serum were removed following centrifugation and frozen at –20°C until analysis.

Steers were slaughtered by weight block after receiving the high-concentrate finishing diets for 104 to 132 d. Before slaughter, steers were scanned by placing an ultrasound probe (Aloka 210, Corometrics Medical Systems, Wallingford, CT) over the LM between the 12th and 13th ribs, for 12th-rib fat thickness. Final weights were obtained on two consecutive days to ensure animals were slaughtered at a similar BW and 12th-rib fat thickness across all blocks. Steers were then transported approximately 320 km to a commercial abattoir and slaughtered after an overnight period of feed withdrawal. Hot carcass weights were recorded, and liver samples collected immediately after slaughter. Fat depth over the LM (between the 12th and 13th ribs), estimated percentage of KPH, LM area, bone maturity, marbling score, and USDA yield and quality grades were determined by a certified USDA grader 48 h after slaughter. After carcass grading, a LM sample encompassing the entire surface area of the LM at the interface of the 12th and 13th ribs was sliced from the right side of the carcass (approximate weight, 150 g). Muscle samples were obtained from three of the four blocks (two steers·treatment–1·block–1). Samples were placed in plastic bags, chilled on dry ice for transport to the laboratory, and frozen until analysis for total lipid, moisture, and Mn concentrations.

Analytical Procedures
Plasma samples were prepared for Mn analysis using a modified version of the wet ashing procedure described by Johnson et al. (1991)Go. One milliliter of plasma was digested in 6 mL of trace mineral grade nitric acid (Fisher Scientific, Fair Lawn, NJ). After boiling off the nitric acid, 2 mL of 30% hydrogen peroxide (Fisher Scientific) was added and again boiled off. After cooling, 1 mL of 5% nitric acid was used to reconstitute the dried sample. Feed, liver, and LM samples for analysis of Mn were prepared using a microwave digestion (Mars 5, CEM Corp., Matthews, NC) procedure described by Gengelbach et al. (1994)Go. Manganese in plasma and LM was determined by flameless atomic absorption spectrophotometry, whereas Mn in feed and liver was analyzed using flame atomic absorption spectrophotometry (GFA-6500, Shimadzu Scientific Instruments, Kyoto, Japan). Plasma glucose was determined by a membrane-immobilized glucose oxidase enzyme coupled to an electrochemical sensor (model 2700 select biochemical analyzer, Yellow Springs Instrument Co. Inc., Yellow Springs, OH). Serum NEFA concentrations were determined using the Wako NEFA C test kit (Wako Chemicals USA, Inc., Richmond, VA). To determine muscle lipid content, LM samples were thoroughly ground after removal of all external fat. Total lipid was extracted using the chloroform methanol lipid extraction procedure (Bligh and Dyer, 1959Go).

Statistical Analyses
Data were analyzed as a randomized complete block design using ANOVA from the GLM procedure of SAS (SAS Inst., Inc., Cary, NC). Pen was the experimental unit for all data and effects were considered significant at P < 0.05. The model included effects due to treatment and block. Treatment means were tested for linear, quadratic, and cubic effects using contrast statements for unequally spaced treatments. Additional analyses were conducted using two pairwise comparisons: control vs. 120 and 240 mg of Mn/kg of DM; and control vs. 20 mg of Mn/kg of DM.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
Implications
 Literature Cited
 
Dietary Mn did not affect ADG, DMI, or G:F during the growing or finishing phases (Table 2Go). Treatments with 0 to 30 mg of supplemented Mn/kg of DM provided concentrations of Mn within the physiological range and were intended to test the effects of Mn on performance. Because corn silage was relatively high in Mn, the control diet in the growing phase contained 29 mg of Mn/kg of DM, which is above the NRC (1996)Go recommended requirement of 20 mg of Mn/kg of DM for growing cattle. Results of the present study indicate that 29 mg of Mn/kg of DM was at least adequate in Mn, based on performance, for growing cattle. Because the control growing diet Mn concentration exceeded the NRC (1996)Go recommendation, this experiment could not determine whether the current NRC (1996)Go requirement is adequate. The control finishing diet in our study analyzed 8.1 mg of Mn/kg of DM, primarily due to the low Mn concentration in corn. In the finishing phase, cattle fed the control diet performed equally as well as cattle receiving 20 mg of Mn/kg of DM or greater, suggesting the requirement for Mn in finishing cattle may be lower than the NRC (1996)Go recommendation.


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  		Table 2. Effects of dietary Mn on performance of steers in the growing and finishing phasea
 
The supplemental Mn concentrations considered pharmacological did not negatively affect performance during the growing or finishing phase. Addition of 1,000 mg of Mn/kg of DM to diets of growing calves for 100 d did not affect performance (Cunningham et al., 1966Go); however, addition of 2,460 mg of Mn/kg of DM decreased gain and feed intake by growing calves (Cunningham et al., 1966Go).

Plasma Mn concentrations on d 56 of each of the growing and finishing phases were not affected by dietary Mn concentration (Table 3Go). Liver Mn concentration increased (P = 0.02; R2 = 0.515) linearly with increasing dietary Mn, ranging from 12.1 in controls to 15.1 mg/kg (DM basis) in steers supplemented with 240 mg of Mn/kg of DM. Likewise, LM Mn concentrations increased (P = 0.002; R2 = 0.690) linearly with increasing dietary Mn. Despite the increase in LM Mn concentration with increasing dietary Mn, muscle Mn concentration remained low (<0.50 mg/kg) in all treatment groups. Liver and LM Mn concentrations were greater (P = 0.03 and 0.006, respectively) in steers receiving the pharmacological concentrations (120 and 240 mg/kg) of Mn than those in the control treatment (Table 3Go). Supplementing grazing sheep with 250 or 500 mg of Mn/d increased concentrations of Mn in liver but not in kidney and heart (Grace, 1973Go). However, lambs receiving 4,000 mg of Mn/kg of DM had increased concentrations of Mn in liver, kidney, heart, spleen, brain, and muscle (Watson et al., 1973Go), whereas lambs receiving 300 and 3,000 mg of Mn/kg of DM had increased concentrations of Mn in heart, liver, pancreas, pituitary, adrenal, and bile (Ivan and Hidiroglou, 1980Go).


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  		Table 3. Effects of dietary Mn on plasma and tissue Mn and blood metabolites
 
Plasma glucose concentrations were not affected by dietary Mn during the growing or finishing phases (Table 3Go). Manganese has been shown to increase gluconeogenesis in vitro (Rognstad, 1981Go; Tolbert et al., 1981Go) due to its integral role in pyruvate carboxylase, a Mn metalloenzyme, and phosphoenolpyruvate carboxykinase, a Mn-activated enzyme (Baly et al., 1985Go). The effect of supplemental Mn above the dietary requirement on gluconeogenesis and circulating levels of glucose in ruminants is not known.

Nonesterified fatty acids were not measured during the growing phase; however, serum NEFA tended (P = 0.10; R2 = 0.319) to decrease linearly as supplemental Mn increased from 0 to 240 mg/kg of DM in the finishing phase. This finding suggests that increasing dietary Mn may have decreased lipolysis or increased uptake of NEFA from blood. Although not entirely understood, Mn has been shown to increase catecholamine release (Powis et al., 1996Go) and synthesis (Chandra and Shukla, 1981Go). A Mn-induced increase in catecholamine concentration should have resulted in increased lipolysis and subsequent NEFA concentrations (Stich and Berlan, 2004Go). Although catecholamine concentrations were not measured in the present study, results do not indicate that dietary Mn caused an increase in catecholamine concentrations that resulted in increased lipolysis.

Hot carcass weight, LM area, 12th-rib fat, KPH, dressing percent, and yield grade were not affected by treatment (Table 4Go). Carcass quality was not affected by dietary Mn, as marbling scores and quality grades were similar across treatments. Muscle lipid content tended (P = 0.08; R2 = 0.446) to respond in a quadratic fashion as dietary Mn increased. Muscle lipid seemed to increase slightly when 30 or 120 mg of Mn/kg of DM was supplemented, but it decreased with the addition of 240 mg of Mn/kg of DM.


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  		Table 4. Effects of dietary Mn on carcass characteristics of finished steers
 
Combining the concepts of Mn increasing the uptake of glucose by isolated adipocytes (Ueda et al., 1984Go; Baquer et al., 2003Go) and i.m. adipocytes preferentially utilizing glucose (Smith and Crouse, 1984Go), the potential for dietary Mn in the physiological or pharmacological range to increase i.m. fat seems plausible. The trend for decreased NEFA concentrations and increased LM lipid content with a concomitant increase in liver and LM Mn concentrations suggests that lipid metabolism was affected by dietary Mn; however, the Mn-induced changes in lipid metabolism did not result in alterations in carcass characteristics. It is likely that the in vitro Mn concentrations required to achieve insulinomimetic effects in isolated rat adipocytes were greater than peripheral Mn concentrations achieved in our study. Lack of an effect of Mn on carcass characteristics in the present study may have been the result of homeostatic mechanisms limiting peripheral Mn concentrations from reaching levels adequate to achieve an insulinomimetic effect. Homeostatic regulation of Mn in the body is primarily a function of increased biliary excretion (Hall and Symonds, 1981Go); however, the percentage of dietary Mn absorbed from the small intestine also seems to decrease in calves fed high dietary Mn (Abrams et al., 1977Go). Manganese is removed from blood very efficiently by the liver (Gibbons et al., 1976Go), as indicated by similar plasma Mn concentrations across all treatments, and subsequently excreted in the bile. Biliary excretion of Mn can increase up to 200-fold in cattle in response to Mn loading (Hall and Symonds, 1981Go). Morever, due to ruminal fermentation, the availability of absorbed glucose may have limited peripheral tissue uptake, even in the event that Mn concentrations were great enough to have an insulinomimetic effect.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 Implications
Literature Cited
 
Current manganese requirements for growth in the growing phase seem to be adequate, whereas requirements for manganese in the finishing phase may be less than what is currently recommended. The performance by growing and finishing steers was not affected by dietary manganese concentrations far in excess of recommended requirements. Although supplementing manganese at pharmacological concentrations seemed to affect lipid metabolism, this effect did not result in improved carcass quality.


   Footnotes
 
1 Use of trade names in this publication does not imply endorsement by the North Carolina Agric. Res. Serv. or criticism of similar products not mentioned. Back

2 Appreciation is extended to G. Shaeffer, E. Baird, H. Stahlhut, S. Hansen, J. Dickerson, and J. Woodlief for assistance in sampling and animal care. Back

3 Correspondence: Campus Box 7621 (phone: 919-515-4008; fax: 919-515-4463; e-mail: Jerry_Spears{at}ncsu.edu).

Received for publication February 25, 2005. Accepted for publication July 11, 2005.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 Implications
 Literature Cited
 


Abrams, E., J. W. Lassiter, W. J. Miller, M. W. Neathery, R. P. Gentry, and D. M. Blackmon. 1977. Effect of normal and high manganese diets on the role of bile in manganese metabolism of calves. J. Anim. Sci. 45:1108–1113.

Baly, D. L., C. L. Keen, and L. S. Hurley. 1985. Pyruvate carboxylase and phosphoenolpyruvate carboxykinase activity in developing rats: Effect of manganese deficiency. J. Nutr. 115:872–879.

Baly, D. L., J. S. Schneiderman, and A. L. Garcia-Welsh. 1990. Effect of manganese deficiency on insulin binding, glucose transport and metabolism in rat adipocytes. J. Nutr. 120:1075–1079.

Baquer, N. Z., M. Sinclair, S. Kunjara, U. Yadav, and P. McLean. 2003. Regulation of glucose utilization and lipogenesis in adipose tissue of diabetic and fat fed animals: Effects of insulin and manganese. J. Biosci. 28:215–221.[Medline]

Bentley, O. G., and P. H. Phillips. 1951. The effect of low manganese rations upon dairy cattle. J. Dairy Sci. 34:396–403.[Abstract/Free Full Text]

Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911–917.

Chandra, S. V., and G. S. Shukla. 1981. Effect of manganese on synthesis of brain catecholamines in growing rats. Acta Pharmacol. Toxicol. 48:349–354.[Medline]

Cunningham, G. N., M. B. Wise, and E. R. Barrick. 1966. Effect of high dietary levels of manganese on the performance and blood constituents of calves. J. Anim. Sci. 25:532–538.[Abstract/Free Full Text]

Gengelbach, G. P., J. D. Ward, and J. W. Spears. 1994. Effect of dietary copper, iron, and molybdenum on growth and copper status of beef cows and calves. J. Anim. Sci. 72:2722–2727.[Abstract]

Gibbons, R. A., S. N. Dixon, K. Hallis, A. M. Russell, B. F. Sansom, and H. W. Symonds. 1976. Manganese metabolism in cows and goats. Biochim. Biophys. Acta 444:1–10.[Medline]

Grace, N. D. 1973. Effect of high dietary manganese levels on the growth rate and the level of mineral elements in the plasma and soft tissue of sheep. N. Z. J. Agric. Res. 16:177–180.

Hall, E. D., and H. W. Symonds. 1981. The maximum capacity of the bovine liver to excrete manganese in bile, and the effects of a manganese load on the rate of excretion of copper, iron and zinc in bile. Br. J. Nutr. 45:605–611.[Medline]

Ivan, M., and M. Hidiroglou. 1980. Effect of dietary manganese on growth and manganese metabolism in sheep. J. Dairy Sci. 63:385–390.

Johnson, P. E., G. I. Lykken, and E. D. Korynta. 1991. Absorption and biological half-life in humans of intrinsic and extrinsic 54Mn tracers from foods of plant origin. J. Nutr. 121:711–717.

NRC. 1996. Nutrient Requirements of Beef Cattle. 7th ed. Natl. Acad. Press, Washington, DC.

Powis, D. A., K. J. O’Brien, S. M. Harrison, P. E. Jarvie, and P. R. Dunkley. 1996. Manganese can substitute for calcium in causing catecholamine secretion but not for increasing tyrosine hydroxylase phosphorylation in bovine adrenal chromaffin cells. Cell Calcium 19:419–429.[Medline]

Rognstad, R. 1981. Manganese effects on gluconeogenesis. J. Biol. Chem. 256:1608–1610.[Abstract/Free Full Text]

Rojas, M. A., I. A. Dyer, and W. A. Cassatt. 1965. Manganese deficiency in the bovine. J. Anim. Sci. 24:664–667.

Schoonmaker, J. P., M. J. Cecava, D. B. Faulkner, F. L. Fluharty, H. N. Zerby, and S. C. Loerch. 2003. Effect of source of energy and rate of growth on performance, carcass characteristics, ruminal fermentation, and serum glucose and insulin of early-weaned steers. J. Anim. Sci. 81:843–855.[Abstract/Free Full Text]

Smith, S. B., and J. D. Crouse. 1984. Relative contributions of acetate, lactate and glucose to lipogenesis in bovine intramuscular and subcutaneous adipose tissue. J. Nutr. 114:792–800.

Stich, V., and M. Berlan. 2004. Physiological regulation of NEFA availability: Lipolysis pathway. Proc. Nutr. Soc. 63:369–374.[Medline]

Tolbert, M. E., J. A. Kamalu, and G. D. Draper. 1981. Effects of cadmium, zinc, copper, and manganese on hepatic parenchymal cell gluconeogenesis. J. Environ. Sci. Health B. 16:575–585.[Medline]

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