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Depletion of selenium in blood, liver and muscle from beef heifers previously fed forages containing high levels of selenium
Science of the Total Environment 536 (2015) 603–608
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Depletion of selenium in blood, liver and muscle from beef heifers previously fed forages containing high levels of selenium Sharon E. Benes a, Peter H. Robinson b,⁎, Grace S. Cun a,b a b
Department of Plant Science, California State University, Fresno, CA 93740, USA Department of Animal Science, University of California, Davis, CA 95616, USA
H I G H L I G H T S
G R A P H I C A L
• Se level depletion from blood, liver, muscle in heifers previously on Se-enriched forages • Se levels decreased but that in liver was more than in whole blood, with muscle lowest • Low body weight gains the first 82 d of feeding but increased substantially afterwards • Grazing forages containing high levels of Se can successfully produce Se-enriched beef
Concentration of Se (mg/kg wet weight) in muscle tissue from beef heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for 165 d and were fed a low Se diet for 209 d. Concentration of Se in muscle tissue remained higher in heifers that grazed TWG except at 209 d, compared to heifers that grazed CWR.
a r t i c l e
a b s t r a c t
i n f o
Article history: Received 14 March 2015 Received in revised form 20 July 2015 Accepted 21 July 2015 Available online 4 August 2015 Editor: D. Barcelo Keywords: Selenium toxicity Selenium enriched beef Drainage water Irrigation Salinity Selenium copper interaction
A B S T R A C T
Beef heifers which had grazed ‘Jose’ tall wheatgrass (TWG; Thinopyrum ponticum var. ‘Jose’; 10 heifers) and creeping wildrye (CWR; Leymus triticoides var. ‘Rio’; 10 heifers) with high levels of Se (N2 mg/kg DM) due to growth in saline soils, accumulated high Se levels in blood, liver and muscle (Juchem et al., 2012). We determined the decrease in Se levels in blood, liver and muscle from these heifers, particularly the decrease of Se in muscle, in order to determine the maximum feeding length of a low Se diet (LSeD) required sustaining Se-enriched beef. Immediately after grazing, all heifers were fed a LSeD containing b 0.30 mg/kg DM for 209 d. Blood, liver and muscle samples, as well as body weight (BW), were collected at the beginning and end of the LSeD feeding period and at intermediate times. After grazing, CWR and TWG heifers had similar BW, but TWG heifers had higher levels of Se in whole blood (1.19 versus 0.81 mg/L), liver (2.67 versus 2.12 mg/kg wet weight (WW)), and muscle tissue (0.87 versus 0.63 mg/kg WW) than CWR heifers. The Se levels decreased with exposure time to the LSeD and, at 82 d of feeding the LSeD, Se levels were 77 (liver), 49 (blood) and 31% (muscle) lower. The BW gains for both groups were ~ 0.5 kg/d during the first 82 d of feeding, but increased thereafter. Levels of Cu in serum (0.28 versus 0.50 mg/L) and liver (1.14 versus 22.9 mg/kg WW) were lower at the end of grazing in TWG heifers,
Abbreviations: ADF, acid detergent fiber with residual ash; aNDFom, neutral detergent fiber exclusive of residual ash; BW, body weight; Cu, copper; CP, crude protein; CWR, creeping wild rye; DM, dry matter; LSeD, low Se diet; SJV, San Joaquin Valley; TWG, tall wheatgrass; WW, wet weight. ⁎ Corresponding author at: Department of Animal Science, 2203 Meyer Hall, Davis, CA 95616, USA. E-mail address: [email protected] (P.H. Robinson).
http://dx.doi.org/10.1016/j.scitotenv.2015.07.096 0048-9697/© 2015 Elsevier B.V. All rights reserved.
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and suggested a potential Cu deficiency. Grazing forages with high Se levels can result in Se-enriched beef, but a LSeD feeding period of b82 d is required to maintain enrichment. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The western San Joaquin Valley (SJV) of California (USA) is an important agricultural area, but salinity and drainage problems have challenged sustainability of its agricultural production (Letey et al., 2002). Saline soils unsuitable for salt sensitive crops generate income through production of salt tolerant forages, and agricultural drainage water can be a water source for such production systems (Suyama et al., 2007b). The potential of saline soils irrigated with drainage water for forages that have adequate dry matter (DM) production and forage quality has been demonstrated (Suyama et al., 2007a), but high levels of elements such as Se and S remained a concern (Suyama et al., 2007b; Robinson et al., 2004; Grattan et al., 2004a). Selenium plays an important role in animal and human well-being and health as an essential nutrient, and natural antioxidant, as well as a potentially toxic element. Limited evidence demonstrates the health promoting properties of Se in humans, such as anticarcinogenic properties (Clark et al., 1996; Reid et al., 2002; Vogt et al., 2003; Waters et al., 2003) and positive impacts on reproductive health (Krsnjavi et al., 1992; Boitani and Puglisi, 2008). The most common option to increase Se intake by humans is Se supplementation tablets. While production of Se-enriched beef (Knowles et al., 2004) is an option, since beef is already a source of dietary Se, the Se concentration of beef products varies by geographical origin (Finley et al., 1996). In 2007, the average red meat consumption in the United States was 85 g/person/d (Daniel et al., 2011), and Finley et al. (1996) calculated that daily intakes of Se from beef in the USA are regional and range from 40 to 100 μg/d. One study supplemented month old calves with 0.3 mg/kg dietary Se for 2 mo and increased the Se concentration in striated muscles from 0.092 to 0.263 μg/g (Pavlata et al., 2001). Fisinin et al. (2009) calculated that 100 g of such a Se-enriched beef would provide 40 to 50% of the USDA recommended daily Se allowance. Consumption of Se-enriched beef is also a safe option since, in order to reach an intake of 400 μg/d, the maximum safe dietary intake, a person would have to consume N1 kg of meat/d for 13 d. We addressed limitations of forage production on saline soils to grow beef cattle, and its potential to create cattle with Se-enriched beef (Juchem et al., 2012). Because body weight (BW) gains of cattle that grazed high Se CWR and TWG were limited by forage nutrient density, a confinement period after grazing is required to achieve industry standard BW, marbling and subcutaneous carcass fat cover. However a standard low Se finishing diet will reduce the Se concentration in the beef, and so any Se-enriched beef premium would be lost. Data on rates of Se depletion in blood, liver and muscle of beef heifers consuming Se-enriched forages is very limited. We hypothesized that Se depletion in muscle tissue would be slow enough that an appropriate finishing period would maintain a substantive Se enrichment level in beef. Thus the objective was to determine the extent of Se depletion within blood, liver and muscle from beef heifers that were previously Se loaded due to grazing forages containing high Se levels (i.e., N2 mg/kg DM; Juchem et al., 2012) and the time necessary to sustain elevated levels of Se in muscle. In addition, due to the results, this study discusses the Se/Cu interaction in blood serum and liver.
triticoides var. ‘Rio’) that contained high levels of Se (N2 mg/kg DM), due to growth in saline soils, accumulated high Se levels in blood, liver and muscle (Expt. 2 of Juchem et al., 2012). Twenty of these 23 heifers (10 from each forage group) were selected to investigate Se depletion when fed a low Se finishing diet. The two heifer groups (i.e., CWR and TWG) had similar BW at the beginning of the study, 325 and 315 kg respectively, and were ~ 14 mo old when they were moved to a feedlot ~20 km from the grazing site in Red Rock Ranch located southwest of Five Points (CA, USA). All heifers were housed in a drylot of ~ 30 m width and 20 m depth, with 30 head spaces at the feed bunk, and had continuous access to fresh water. All heifers were dewormed at the beginning of the feeding phase with 0.5 mg of moxidectin/kg of BW utilizing a pour-on formulation (CYDECTIN® Pour-On, Fort Dodge Animal Health, Fort Dodge, IA, USA), and were fed alfalfa hay during the first 25 d. A total mixed ration (Table 1) containing a low Se level (b0.30 mg/kg DM; LSeD) was then fed for 20 to 30 g/kg refusals, and formulated to meet, or exceed, requirements of growing heifers for a BW gain of 1.1 kg/d (NRC, 2000).
2.2. Sample collection 2.2.1. Feed samples, blood and body weight Feed ingredient samples were collected from every load into premarked plastic bags and stored at room temperature until chemical analysis (Table 1). One load of mineral mixture was fed during the study, but two samples were analyzed for its mineral composition. Blood was collected from the jugular vein into evacuated tubes (Vacutainer®, Becton Dickinson, Franklin Lakes, NJ, USA), whereas EDTA was the anticoagulant for Se determination in whole blood (BD Hemogard™, 10.8 mg of K2EDTA). Samples for serum mineral levels (BD Hemogard™) were collected at 1, 82, 137 and 209 d and centrifuged at 1500 ×g for 10 min at 5 °C. Whole blood samples were Table 1 Chemical composition (g/kg 105 °C DMa) of ingredients and calculated composition of the total mixed ration (TMR) fed to the growing heifers.
n DM, g/kg CP Fat aNDF d Ash P Ca Mg S K Na Cl Zn, mg/kg Mn, mg/kg Fe, mg/kg Cu, mg/kg Se, mg/kg a
2. Materials and methods 2.1. Cattle, housing and diets Angus beef heifers which had grazed ‘Jose’ tall wheatgrass (TWG; Thinopyrum ponticum var. ‘Jose’) and creeping wildrye (CWR; Leymus
Hay, Alfalfa
Straw, wheat
Corn grain, rolled
Almond, hulls
Mineral mixtureb
TMRc
5 916 170 17.8 359 144 1.50 26.30 2.90 3.16 14.2 3.28 8.80 22.8 63.2 1040 76.4 0.23
3 937 40.4 10.8 677 178 0.50 3.20 2.00 1.70 21.4 1.99 11.50 14.9 62.0 1627 37.3 0.14
1 905 11.3 53.4 168 97 4.97 7.40 3.19 1.94 6.1 0.09 0.60 60.4 37.6 1671 43.0 0.18
2 897 45.9 13.4 460 77 2.00 2.70 1.20 0.45 31.2 0.22 1.10 14.2 22.3 1408 44.0 0.04
2 898 69.0 33.0 106 125 5.30 20.80 2.50 1.86 4.2 21.36 0.90 157.9 88.5 216 278.5 0.24
– 737 95.2 28.2 304 122 2.89 16.73 2.68 2.28 13.3 4.13 4.84 47.3 54.2 1180 85.8 0.19
Dry matter. The mineral mixture contained 811 g of ground corn/kg on an as fed basis. c Calculated chemical composition of total mixed ration (TMR) based on analyzed chemical composition of individual ingredients. The TMR contained (g/kg DM): 451 g alfalfa hay, 41.5 g wheat straw, 264 g rolled corn grain, 125 g almond hulls, and 118 g mineral mixture. Fresh water was added at 260 g/kg of DM to increase the moisture content. d Neutral detergent fiber assayed with a heat stable amylase, expressed exclusive of residual ash. b
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drawn at 1, 24, 42, 82, 137 and 209 d of the feeding period, followed by recording individual animal BW. Whole blood and serum samples were stored at 5 °C until submission to the California Animal Health and Food Safety Laboratory (Davis, CA, USA).
Optek Corporation, Franklin, MA, USA) according to Martin et al. (1987). After precipitation of proteins in serum, protein free supernatants were analyzed for Cu ICP-AES (spectrometer listed above) as described by Melton et al. (1990).
2.2.2. Liver and muscle biopsies Liver and muscle samples were collected by biopsy (Juchem et al., 2012). Briefly, the surgical field was cleaned, thoroughly disinfected, local anesthesia administered and liver samples biopsied with a biopsy needle (Sontec Instruments, Inc., Englewood, CO, USA) and an ultrasound unit with a 3.5 MHz convectional mechanical probe (WED-200A, Well.D Electronics Co., Ltd, Shenzhen, China). The biopsy needle was introduced into the abdominal cavity through an incision of ~ 3 cm and positioned cranio-ventrally towards the elbow on the opposite flank of the animal, deep enough to reach the liver. Samples from the semitendinosus muscle were collected from the right rear leg utilizing a scalpel and curved haemostatic forceps (Juchem et al., 2012). Incisions for sampling liver and muscle were closed with an interrupted cruciate and simple continuous suture patterns, respectively. Liver samples were individually stored in plastic micro tubes and kept in ice until submitted to the California Animal Health and Food Safety Laboratory for analyses. Before each biopsy, heifers received an intramuscular injection of penicillin (22,000 IU/kg BW), except for the last sampling where 2 mg/kg BW of Ceftiofur Hydrochloride (Excenel® RTU, Pfizer, New York, NY, USA) was used in order to avoid antibiotic residues in the beef. All animal procedures are fully compliant with laws of the USA and the State of California, as well as animal protocols of the University of California at Davis (CA, USA).
2.4. Statistical analysis
2.3. Analytical methods 2.3.1. Feeds and diets Feed samples were assayed for organic and mineral chemical composition. Moisture at 105 °C was determined gravimetrically (Reuter et al., 1986), neutral detergent fiber was as described by Van Soest et al. (1991) utilizing sodium sulphite, a heat stable amylase, and is expressed without residual ash (aNDFom), acid detergent fiber (ADF) was according to AOAC (2000; #973.18) and is expressed with residual ash. Lignin(sa) was determined by the sulfuric acid procedure (Robertson and Van Soest, 1981), and ash was determined as the residue after heating to 550 °C for 8 h. Total fat was determined by extraction with ether (AOAC, 2000; #930.39). Feed samples were digested in nitric acid/hydrogen peroxide microwave digestion system and the contents of P, S, Ca, Mg, Na, B, Zn, Mn, Fe and Cu were quantified utilizing atomic absorption spectrometry or inductively coupled plasma atomic emission spectrometry (ICP-AES; Sah and Miller, 1992; Meyer and Keliher, 1992). Samples were extracted with 20 g/L acetic acid for K and Cl determinations, whereas K levels were determined by atomic emission spectrometry (Johnson and Ulrich, 1959) and Cl by a chloridometer (Johnson and Ulrich, 1959). Samples were extracted with nitric/perchloric acid digestion/dissolution and determined by vapor generation using ICP-AES (Tracy and Moeller, 1990) for determination of total Se content in feeds. Total N was determined by the Dumas method (LECO FP-528; AOAC (2002; #990.03)). 2.3.2. Blood, serum and tissues Liver and muscle tissues were digested in a solution of nitric, sulfuric and perchloric acids at 350 °C, followed by reduction with 5 M HCl at 95 °C. The Se levels were by hydride vapor generation inductively coupled plasma spectrometer (FISONS, Accuris Model, Thermo Optek Corporation, Franklin, MA, USA) as described by Tracy and Moeller (1990). Whole blood Se Levels were by ICP-AES as described previously (Tracy and Moeller, 1990). Liver tissues were digested with nitric acid at 180 °C and subsequently analyzed for Cu by ICP-AES (FISONS, Accuris Model, Thermo
The CWR and TWG grazing treatments had been applied before this feeding period began and were discontinued as the heifers were moved to the common LSeD. However because tissue Se levels were biologically different between the two forage groups at this time, and it was likely that the initial level of Se could affect Se depletion, the prior treatment was maintained in the statistical model. Thus the effect of ‘treatment’ represents two scenarios of Se load rather than a residual grazing effect per se, and we do not consider it to be related to Se content from the two forages grazed by these heifers in Juchem et al. (2012). Data were analyzed as repeated measures utilizing the PROC MIXED procedure of SAS (2002) with the experimental unit (heifers) as a random effect as this covariance structure was the most appropriate based on its lowest Bayesian Information Criterion. The model included effects of heifer, time (fixed), forage (fixed) and the forage by time interaction. Differences P ≤ 0.05 were considered significant, and 0.05 b P ≤ 0.10 were considered a tendency to a difference. 3. Results 3.1. Diet and animal performance Feed ingredients in the LSeD varied in levels of Se (Table 1), but the LSeD contained 0.19 mg/kg DM as well as 95.2 g/kg CP, 304 g/kg aNDF, 16.7 g/kg Ca, 2.9 g/kg P and levels of other macro and micro minerals (Table 1) that met or exceeded requirements of growing heifers (NRC, 2000). Heifers were fed 12 to 15 kg of TMR/d (DM) for 209 d to b30 g/kg refusals. Heifers that had previously grazed CWR or TWG had similar BW at the start of LSeD feeding, 325 and 315 kg (±10.4 SEM), respectively. Despite differences in initial Se levels in liver and blood between CWR and TWG heifers, their BW and BW gains were similar (Fig. 1). After 209 d of feeding the LSeD, CWR and TWG heifers weighed 525 and 491 kg (±25.1; Fig. 1). 3.2. Concentration of Cu in serum and liver Serum (0.50 versus 0.28 mg/L) and liver (22.9 versus 1.1 mg/kg WW) Cu levels (Juchem et al., 2012) were higher (P b 0.05) at the start of LSeD feeding for heifers which had previously grazed CWR versus TWG. Serum Cu levels after 209 d of feeding the low Se, Cu adequate, diet
Fig. 1. Body weight (BW; kg) from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for 165 d. Body weight gain was similar (P = 0.72; Pooled SEM = 12.52) in heifers that had previously grazed CWR or TWG and were then fed a low Se diet for 209 d.
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were higher than at its start, but similar for heifers which had previously grazed CWR versus TWG (0.67 versus 0.70 mg/L; Table 2). Levels of Cu in liver had converged by 209 d, and were also similar (14.2 versus 17.4 mg/kg WW; Table 2) in the previously grazed CWR versus TWG heifers. 3.3. Concentration of Se in blood, liver and muscle The Se levels in whole blood (1.19 versus 0.81 mg/L), liver (2.7 versus 2.1 mg/kg WW) and muscle (0.87 versus 0.63 mg/kg WW) at the beginning of the low Se feeding period were higher (P b 0.01) in heifers that had grazed TWG versus those that had grazed CWR (Figs. 2, 3, 4) because TWG had a higher Se content at the end of grazing (Juchem et al., 2012). The Se levels decreased in blood, liver and muscle with time of feeding the LSeD (Figs. 2, 3, 4), although the extent of the decrease differed, particularly in muscle. Indeed the liver Se levels depleted faster than blood or muscle and, after feeding the LSeD for only 24 d the Se levels reduced (P b 0.01) 60 and 65% in liver (0.85 versus 0.93 mg/kg WW), and 21 and 22% in blood (0.63 versus 0.92 mg/L) in heifers previously grazed CWR or TWG, respectively. In muscle, levels of Se 82 d after feeding the LSeD (0.85 versus 0.93 mg/kg WW) was only reduced by 32 and 30% in heifers that had grazed CWR and TWG, respectively. Despite the rapid decline in liver and blood Se levels, blood Se levels at the end of the low Se feeding period were higher than levels measured at the beginning of the grazing season (i.e., before grazing the high Se TWG and CWR; Juchem et al., 2012) in blood (0.32 versus 0.10 mg/L), liver (0.62 versus 0.23 mg/kg WW), and muscle (0.42 versus 0.06 mg/kg WW). 4. Discussion It is well documented that Se is an essential mineral for health and reproduction of mammals, and supplementing Se at suboptimal levels, and/or factors which limit Se absorption, have been associated with poor reproductive performance. However, unlike most minerals, Se has a narrow safety margin between essentiality and toxicity. 4.1. Animal performance and micro minerals Beef production systems in the USA typically utilize grazing to provide feed for replacement heifers, pregnant cows and calves until weaning. However 6 to 12 mo old calves are fed energy dense diets until slaughter at 14 to 18 mo. We had previously used 6 mo old weaned heifers to evaluate the BW gain potential of CWR and TWG forages containing high levels of Se under grazing conditions (Juchem et al., 2012) because such animals are suitable for such production systems. Findings from that study demonstrated that TWG can support BW gains of 0.5 kg/d if the CP content in the forage is not limiting, whereas CWR supported slightly lower BW gains (Juchem et al., 2012). Forages such as CWR and TWG grown in saline soils in the west side of SJV of California may have excess Se and can contain imbalanced micro-mineral levels (Grattan et al., 2004b; Suyama et al., 2007b) relative to the requirements of growing beef cattle (NRC, 2000). In fact, these forages
Table 2 Concentration of Cu in serum (mg/L) and liver (mg/kg wet weight) from heifers which had previously grazed creeping wildrye (CWR) or tall wheatgrass (TWG) for 165 d, and were then fed a low Se, Cu adequate, diet for 209 d.
Serum Liver 1
CWR
TWG
SEM
Forage
0.67 14.2
0.70 17.4
0.034 2.72
0.44 0.42
1
1
Forage ∗ time b0.01 b0.01
P values for the effects of forage and the interaction of forage by time.
Fig. 2. Concentration of Se (mg/L) in whole blood from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for a 165 d and were then fed a low Se diet for 209 d. Heifers that had previously grazed TWG (dashed line) had higher concentration of Se up to 82 d of feeding (forage by day interaction; P b 0.01), however concentration of Se in whole blood decreased over time for heifers fed either forages (day effect; P b 0.01). Pooled SEM = 0.52.
had low levels of Cu (b 7 mg/kg forage DM), Mg (b0.10 mg/kg forage DM), Zn (b30 mg/kg forage DM), and high levels of Mo (N5 mg/kg forage DM) and S (0.4 mg/kg forage DM; Juchem et al., 2012). Thus the heifers that started this LSeD feeding period had very high Se levels in blood and liver, but were deficient in Cu. The high levels of dietary Mo (N 5 mg/kg DM) and S (N 0.2%), which decrease rumen Cu absorption, likely caused the Cu deficiency. Generally, growing cattle that are underfed for a period of time and changed to a more nutrient dense diet demonstrate compensatory growth (i.e., BW gains are higher than those predicted based on nutrient requirements). However, this was not the case here and potential compensatory gains only occurred after 138 d of feeding the low Se diet when heifers gained 1.78 and 1.74 kg/d after previously grazing CWR or TWG, respectively. Despite the adequate LSeD nutrient levels during the 209 d LSeD feeding period, the diet (and its low Se level) should have supported BW gains of 1.1 kg/d (NRC, 2000) as voluntary DM intake was not depressed, but the heifers had modest BW gains (i.e., 0.28 and 0.38 kg/d for heifers that had grazed CWR or TWG, respectively) during the first 80 d of LSeD feeding. That BW gains increased with time of feeding the LSeD, but were still lower than anticipated based on diet nutrient composition, may have been related to the
Fig. 3. Levels of Se (mg/kg wet weight) in liver samples from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for a 165 d and were fed a low Se diet for 209 d. Levels of Se in wet liver were higher for heifers that grazed TWG (P b 0.05; interaction of forage by day) at beginning of the feeding period and at 82 d after feeding, however both groups of heifers (i.e., CWR and TWG) showed the largest depletion in Se from liver during the first 24 d of exposure to a low Se diet. Pooled SEM = 0.049.
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4.2. Se depletion in whole blood and liver
Fig. 4. Concentration of Se (mg/kg wet weight) in muscle tissue from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for 165 d and were fed a low Se diet for 209 d. Concentration of Se in muscle tissue remained higher in heifers that grazed TWG (forage by day interaction; P b 0.05; Pooled SEM = 0.021) except at 209 d, compared to heifers that grazed CWR.
declining tissue levels of Se and/or increasing levels of Cu. Although it is tempting to associate the decrease in Se level in blood and liver over time (Figs. 2 and 3) with the increases in the extent of BW gain (Fig. 1), the literature provides no support for such an association. Feeding diets containing up to 10 mg/kg of Se from sodium selenite (an inorganic Se source) to wether lambs for a period of 52 wks increased the Se concentration in liver to as high as 20 mg/kg of dry liver, but BW gains were similar across all levels of sodium selenite supplementation (Cristaldi et al., 2005). Similar findings were reported by Lawler et al. (2004) who supplemented steers with 2.8 mg Se/kg in an organic or inorganic form for 126 d and found BW gain and DM intake were similar to the control group, which were fed a diet containing only 0.38 mg Se/kg. Limited research exists on Cu and Se interactions, but indicates that high Cu intakes induce signs of Se deficiency in chicks (Jensen, 1975). However mammalian research suggests that increasing Se intake does not alter Cu metabolism (Miller and Groziak, 1997). While Se levels in blood and liver decreased with time of feeding, the Cu concentration in serum increased for both CWR and TWG heifers. Researchers have found bovine herds with low liver Cu levels and a high incidence of Cu deficiency, but that it is not uncommon for a high proportion of animals to have “normal” serum Cu levels (Hall and ZoBell, 2010). Since most body Cu is stored in the liver, it is liver Cu levels which give a true reflection of the Cu status of the animal. The magnitude of BW gains were higher in the last third of our feeding period suggests that increasing Cu status may have been associated with the improved BW gains. In contrast, despite the large difference in Cu levels in serum and liver among the CWR and TWG heifers at the beginning of the study, BW gains did not differ between the forage groups (Fig. 1). It is possible that high levels of S accumulation in liver and whole blood, known to depress voluntary feed intake and BW gain, could have been one of the reasons that heifers took longer to express their full BW gain potential. Excess dietary S in ruminants has been shown to interfere with absorption of some trace minerals, particularly Cu, Mo and Se (reviewed by Kandylis, 1984). Because of confounded mineral levels in tissues over time, and possible interactions of high Se levels with other minerals, the delay to enhanced animal performance after heifers were moved from high Se pastures to the LSeD cannot be clearly explained, particularly because we did not anticipate such findings and so the experimental design did not contemplate such a comparison. However, findings suggest that if BW gains are to be optimized during a confinement phase that follows grazing Se-enriched forages, supplementation of minerals, except Se, should be included, to at least alleviate the effects observed in our study.
Levels of Se decreased with time after grazing (P b 0.01) which would be expected from animals that had been previously consuming a Se enriched diet, and Se depletion from blood, liver and muscle differed. At the end of grazing, liver levels of Se were 25% higher in TWG versus CWR heifers but, after 20 d of eating the LSeD, both groups had similar liver Se thereby demonstrating that mobilization of Se accumulated in liver occurred quickly. The Se concentration in blood decreased at a slow rate, likely because Se mobilized within liver and muscle continuously entered the blood pool. Stockdale and Gill (2011) found blood Se concentrations were slow to react after the exclusion of Se-enriched pellets in the diets of dairy cows. And since Se in whole blood responds slowly to changes in Se concentration as most Se is incorporated into red blood cells during erythropoiesis, there is a lag in blood Se. A full whole blood response to a dietary Se supplementation or depletion may therefore require a time span equal to the average life span of the red blood cell, which in cattle is 90 to 120 d (Stowe and Herdt, 1992). At 81 d of post-grazing, levels of Se were reduced by 77% in liver, 49% in blood, but only 31% in muscle. These results are consistent with Juniper et al. (2008) who reported the Se depletion rate in lamb tissue was fastest in liver and the slowest in skeletal muscle after Se supplementation. At 81 d of post grazing, liver Se levels had reached their lowest level while blood Se only reached its lowest level after 137 d of feeding the low Se diet. There were no differences in the levels of Se within the liver and blood between heifers that had previously grazed CWR or TWG. 4.3. Depletion of Se in muscle and implications Major food sources of Se in the American diet are breads, grains and meats (National Institutes of Health, 2013). Attempts to improve the nutritional value of foods for human consumption, such as raising micronutrient levels in milk and meat (Knowles et al., 2004), have been considered as delivery systems for health-promoting nutrients in geographical areas with micronutrient deficiencies. Benefits of utilizing geographical areas naturally high in Se to produce Se-enriched beef has been previously suggested (Hintze et al., 2001; Lawler et al., 2004). 5. Conclusions Our findings partially support our initial hypothesis, as time of feeding a low Se diet was an important factor in determining the concentration of Se in muscle of beef heifers previously loaded with Se. However even after 209 d of exposure to low levels of dietary Se, muscle Se levels were elevated making this a suitable system to produce Se-enriched beef from low value crops grown on saline degraded soils. However forages grown under these conditions can limit performance due to mineral imbalances and, in some cases, suboptimum CP contents, which may have limited the performance of heifers subsequently fed energy dense diets post-grazing. Acknowledgments The authors greatly appreciate the logistical support, animal facilities and equipment provided by John Diener and staff from Red Rock Ranch in Five Points, CA (USA) to conduct this research. We are also thankful to Dr. John Maas (University of California Veterinary Medicine Extension) for his technical support and kindness in lending us his surgical materials for liver and muscle biopsies. The authors acknowledge the technical and scientific inputs of Dr. S. Juchem. This research was funded through Proposition 204 Agricultural Drainage Program (agreement #4600007357) administrated by the California Department of Water Resources and the California State University Agricultural Research Initiative (CSU-ARI, grant #07-1-001-13).
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emission spectrometry. Revision 1.3. U.S. Environmental Protection Agency, Office of Research and Development, Environmental Monitoring and Support Laboratory, Washington, DC, USA. Melton, L.A., Tracy, M.L., Moller, G., 1990. Screening trace elements and electrolytes in serum by inductively-coupled plasma emission spectrometry. Clin. Chem. 36, 247–250. Meyer, G.A., Keliher, P.N., 1992. An overview of analysis by inductively coupled plasmaatomic emission spectrometry. In: Montaser, A., Golightly, D.W. (Eds.), Inductively Coupled Plasmas in Analytical Atomic Spectrometry. VCH Publishers Inc., New York, NY, USA, pp. 473–505. Miller, G.D., Groziak, S.M., 1997. Essential and nonessential mineral interactions. In: Massaro, E.J. (Ed.), Handbook of Human Toxicology. CRC Press LLC, Boca Raton, FL, USA, pp. 369–408. National Institutes of Health, U.S. Department of Health and Human Services, 2013. Selenium. Office of Dietary Supplements, Bethesda, MD, USA. National Research Council (NRC), 2000. Nutrient Requirements of Beef Cattle. 7th edition. National Academy of Science, Washington, DC, USA. Pavlata, L., Pechova, A., Becvar, O., Illek, J., 2001. Selenium status in cattle at slaughter: analyses of blood, skeletal muscle, and liver. Acta Vet. Brno 70, 277–284. Reid, M.E., Duffield-Lillico, A.J., Garland, L., Turnbull, B.W., Clark, L.C., Marshall, J.R., 2002. Selenium supplementation and lung cancer incidence: an update of the nutritional prevention of cancer trial. Cancer Epidemiol. Biomark. Prev. 11, 1285–1291. Reuter, D.J., Robinson, J.B., Peverill, K.I., Price, G.H., 1986. Guidelines for collecting, handling and analyzing plant materials. In: Reuter, D.J., Robinson, J.B. (Eds.), Plant Analysis an Interpretation Manual. Inkata Press, Melbourne, Australia, pp. 20–35. Robertson, J.B., Van Soest, P.J., 1981. The detergent system of analysis and its application to human foods. In: James, W.P.T., Theander, O. (Eds.), The Analysis of Dietary Fiber in Foods. Marcel Dekker, New York, NY, USA, pp. 123–142. Robinson, P.H., Grattan, S.R., Getachew, G., Grieve, C.M., Poss, J.A., Suarez, D.L., Benes, S.E., 2004. Biomass accumulation and potential nutritive value of some forages irrigated with saline-sodic drainage water. Anim. Feed Sci. Technol. 111, 175–189. Sah, R.N., Miller, R.O., 1992. Spontaneous reaction for acid dissolution of biological tissues in closed vessels. Anal. Chem. 64, 230–233. SAS, 2002. User's Guide: Statistics. Version 7th edition. SAS Inst., Inc., Cary, NC, USA. Stockdale, C.R., Gill, H.S., 2011. Effect of duration and level of supplementation of diets of lactating dairy cows with selenized yeast on selenium concentrations in milk and blood after the withdrawal of supplementation. J. Dairy Sci. 94, 2351–2359. Stowe, H.D., Herdt, T.H., 1992. Clinical assessment of selenium status of livestock. J. Anim. Sci. 70, 3928–3933. Suyama, H., Benes, S.E., Robinson, P.H., Grattan, S.R., Grieve, C.M., Getachew, G., 2007a. Forage yield and quality under irrigation with saline-sodic drainage water: greenhouse evaluation. Agric. Water Manag. 88, 159–172. Suyama, H., Benes, S.E., Robinson, P.H., Getachew, G., Grattan, S.R., Grieve, C.M., 2007b. Productivity and quality of forages under long-term irrigation with saline-sodic drainage water on the Westside San Joaquin Valley. Anim. Feed Sci. Technol. 135, 329–345. Tracy, M.L., Moeller, G., 1990. Continuous flow vapor generation for inductively coupled argon plasma spectrometric analysis. Part 1: selenium. J. Assoc. Off. Anal. Chem. 73, 404–410. Van Soest, P.J., Robertson, J.B., Lewis, B.A., 1991. Methods for dietary fiber, neutral detergent fiber and non-starch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597. Vogt, T.M., Ziegler, R.G., Graubard, B.I., Swanson, C.A., Greenberg, R.S., Schoenberg, J.B., Swanson, G.M., Hayes, R.B., Mayne, S.T., 2003. Serum selenium and risk of prostate cancer in U.S. blacks and whites. Int. J. Cancer 103, 664–670. Waters, D.J., Shen, S., Cooley, D.M., Bostwick, D.G., Qian, J., Combs Jr., G.F., Glickman, L.T., Oteham, C., Schlittler, D., Morris, J.S., 2003. Effects of dietary selenium supplementation on DNA damage and apoptosis in canine prostate. J. Natl. Cancer Inst. 95, 237–241.
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Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv
Depletion of selenium in blood, liver and muscle from beef heifers previously fed forages containing high levels of selenium Sharon E. Benes a, Peter H. Robinson b,⁎, Grace S. Cun a,b a b
Department of Plant Science, California State University, Fresno, CA 93740, USA Department of Animal Science, University of California, Davis, CA 95616, USA
H I G H L I G H T S
G R A P H I C A L
• Se level depletion from blood, liver, muscle in heifers previously on Se-enriched forages • Se levels decreased but that in liver was more than in whole blood, with muscle lowest • Low body weight gains the first 82 d of feeding but increased substantially afterwards • Grazing forages containing high levels of Se can successfully produce Se-enriched beef
Concentration of Se (mg/kg wet weight) in muscle tissue from beef heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for 165 d and were fed a low Se diet for 209 d. Concentration of Se in muscle tissue remained higher in heifers that grazed TWG except at 209 d, compared to heifers that grazed CWR.
a r t i c l e
a b s t r a c t
i n f o
Article history: Received 14 March 2015 Received in revised form 20 July 2015 Accepted 21 July 2015 Available online 4 August 2015 Editor: D. Barcelo Keywords: Selenium toxicity Selenium enriched beef Drainage water Irrigation Salinity Selenium copper interaction
A B S T R A C T
Beef heifers which had grazed ‘Jose’ tall wheatgrass (TWG; Thinopyrum ponticum var. ‘Jose’; 10 heifers) and creeping wildrye (CWR; Leymus triticoides var. ‘Rio’; 10 heifers) with high levels of Se (N2 mg/kg DM) due to growth in saline soils, accumulated high Se levels in blood, liver and muscle (Juchem et al., 2012). We determined the decrease in Se levels in blood, liver and muscle from these heifers, particularly the decrease of Se in muscle, in order to determine the maximum feeding length of a low Se diet (LSeD) required sustaining Se-enriched beef. Immediately after grazing, all heifers were fed a LSeD containing b 0.30 mg/kg DM for 209 d. Blood, liver and muscle samples, as well as body weight (BW), were collected at the beginning and end of the LSeD feeding period and at intermediate times. After grazing, CWR and TWG heifers had similar BW, but TWG heifers had higher levels of Se in whole blood (1.19 versus 0.81 mg/L), liver (2.67 versus 2.12 mg/kg wet weight (WW)), and muscle tissue (0.87 versus 0.63 mg/kg WW) than CWR heifers. The Se levels decreased with exposure time to the LSeD and, at 82 d of feeding the LSeD, Se levels were 77 (liver), 49 (blood) and 31% (muscle) lower. The BW gains for both groups were ~ 0.5 kg/d during the first 82 d of feeding, but increased thereafter. Levels of Cu in serum (0.28 versus 0.50 mg/L) and liver (1.14 versus 22.9 mg/kg WW) were lower at the end of grazing in TWG heifers,
Abbreviations: ADF, acid detergent fiber with residual ash; aNDFom, neutral detergent fiber exclusive of residual ash; BW, body weight; Cu, copper; CP, crude protein; CWR, creeping wild rye; DM, dry matter; LSeD, low Se diet; SJV, San Joaquin Valley; TWG, tall wheatgrass; WW, wet weight. ⁎ Corresponding author at: Department of Animal Science, 2203 Meyer Hall, Davis, CA 95616, USA. E-mail address: [email protected] (P.H. Robinson).
http://dx.doi.org/10.1016/j.scitotenv.2015.07.096 0048-9697/© 2015 Elsevier B.V. All rights reserved.
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and suggested a potential Cu deficiency. Grazing forages with high Se levels can result in Se-enriched beef, but a LSeD feeding period of b82 d is required to maintain enrichment. © 2015 Elsevier B.V. All rights reserved.
1. Introduction The western San Joaquin Valley (SJV) of California (USA) is an important agricultural area, but salinity and drainage problems have challenged sustainability of its agricultural production (Letey et al., 2002). Saline soils unsuitable for salt sensitive crops generate income through production of salt tolerant forages, and agricultural drainage water can be a water source for such production systems (Suyama et al., 2007b). The potential of saline soils irrigated with drainage water for forages that have adequate dry matter (DM) production and forage quality has been demonstrated (Suyama et al., 2007a), but high levels of elements such as Se and S remained a concern (Suyama et al., 2007b; Robinson et al., 2004; Grattan et al., 2004a). Selenium plays an important role in animal and human well-being and health as an essential nutrient, and natural antioxidant, as well as a potentially toxic element. Limited evidence demonstrates the health promoting properties of Se in humans, such as anticarcinogenic properties (Clark et al., 1996; Reid et al., 2002; Vogt et al., 2003; Waters et al., 2003) and positive impacts on reproductive health (Krsnjavi et al., 1992; Boitani and Puglisi, 2008). The most common option to increase Se intake by humans is Se supplementation tablets. While production of Se-enriched beef (Knowles et al., 2004) is an option, since beef is already a source of dietary Se, the Se concentration of beef products varies by geographical origin (Finley et al., 1996). In 2007, the average red meat consumption in the United States was 85 g/person/d (Daniel et al., 2011), and Finley et al. (1996) calculated that daily intakes of Se from beef in the USA are regional and range from 40 to 100 μg/d. One study supplemented month old calves with 0.3 mg/kg dietary Se for 2 mo and increased the Se concentration in striated muscles from 0.092 to 0.263 μg/g (Pavlata et al., 2001). Fisinin et al. (2009) calculated that 100 g of such a Se-enriched beef would provide 40 to 50% of the USDA recommended daily Se allowance. Consumption of Se-enriched beef is also a safe option since, in order to reach an intake of 400 μg/d, the maximum safe dietary intake, a person would have to consume N1 kg of meat/d for 13 d. We addressed limitations of forage production on saline soils to grow beef cattle, and its potential to create cattle with Se-enriched beef (Juchem et al., 2012). Because body weight (BW) gains of cattle that grazed high Se CWR and TWG were limited by forage nutrient density, a confinement period after grazing is required to achieve industry standard BW, marbling and subcutaneous carcass fat cover. However a standard low Se finishing diet will reduce the Se concentration in the beef, and so any Se-enriched beef premium would be lost. Data on rates of Se depletion in blood, liver and muscle of beef heifers consuming Se-enriched forages is very limited. We hypothesized that Se depletion in muscle tissue would be slow enough that an appropriate finishing period would maintain a substantive Se enrichment level in beef. Thus the objective was to determine the extent of Se depletion within blood, liver and muscle from beef heifers that were previously Se loaded due to grazing forages containing high Se levels (i.e., N2 mg/kg DM; Juchem et al., 2012) and the time necessary to sustain elevated levels of Se in muscle. In addition, due to the results, this study discusses the Se/Cu interaction in blood serum and liver.
triticoides var. ‘Rio’) that contained high levels of Se (N2 mg/kg DM), due to growth in saline soils, accumulated high Se levels in blood, liver and muscle (Expt. 2 of Juchem et al., 2012). Twenty of these 23 heifers (10 from each forage group) were selected to investigate Se depletion when fed a low Se finishing diet. The two heifer groups (i.e., CWR and TWG) had similar BW at the beginning of the study, 325 and 315 kg respectively, and were ~ 14 mo old when they were moved to a feedlot ~20 km from the grazing site in Red Rock Ranch located southwest of Five Points (CA, USA). All heifers were housed in a drylot of ~ 30 m width and 20 m depth, with 30 head spaces at the feed bunk, and had continuous access to fresh water. All heifers were dewormed at the beginning of the feeding phase with 0.5 mg of moxidectin/kg of BW utilizing a pour-on formulation (CYDECTIN® Pour-On, Fort Dodge Animal Health, Fort Dodge, IA, USA), and were fed alfalfa hay during the first 25 d. A total mixed ration (Table 1) containing a low Se level (b0.30 mg/kg DM; LSeD) was then fed for 20 to 30 g/kg refusals, and formulated to meet, or exceed, requirements of growing heifers for a BW gain of 1.1 kg/d (NRC, 2000).
2.2. Sample collection 2.2.1. Feed samples, blood and body weight Feed ingredient samples were collected from every load into premarked plastic bags and stored at room temperature until chemical analysis (Table 1). One load of mineral mixture was fed during the study, but two samples were analyzed for its mineral composition. Blood was collected from the jugular vein into evacuated tubes (Vacutainer®, Becton Dickinson, Franklin Lakes, NJ, USA), whereas EDTA was the anticoagulant for Se determination in whole blood (BD Hemogard™, 10.8 mg of K2EDTA). Samples for serum mineral levels (BD Hemogard™) were collected at 1, 82, 137 and 209 d and centrifuged at 1500 ×g for 10 min at 5 °C. Whole blood samples were Table 1 Chemical composition (g/kg 105 °C DMa) of ingredients and calculated composition of the total mixed ration (TMR) fed to the growing heifers.
n DM, g/kg CP Fat aNDF d Ash P Ca Mg S K Na Cl Zn, mg/kg Mn, mg/kg Fe, mg/kg Cu, mg/kg Se, mg/kg a
2. Materials and methods 2.1. Cattle, housing and diets Angus beef heifers which had grazed ‘Jose’ tall wheatgrass (TWG; Thinopyrum ponticum var. ‘Jose’) and creeping wildrye (CWR; Leymus
Hay, Alfalfa
Straw, wheat
Corn grain, rolled
Almond, hulls
Mineral mixtureb
TMRc
5 916 170 17.8 359 144 1.50 26.30 2.90 3.16 14.2 3.28 8.80 22.8 63.2 1040 76.4 0.23
3 937 40.4 10.8 677 178 0.50 3.20 2.00 1.70 21.4 1.99 11.50 14.9 62.0 1627 37.3 0.14
1 905 11.3 53.4 168 97 4.97 7.40 3.19 1.94 6.1 0.09 0.60 60.4 37.6 1671 43.0 0.18
2 897 45.9 13.4 460 77 2.00 2.70 1.20 0.45 31.2 0.22 1.10 14.2 22.3 1408 44.0 0.04
2 898 69.0 33.0 106 125 5.30 20.80 2.50 1.86 4.2 21.36 0.90 157.9 88.5 216 278.5 0.24
– 737 95.2 28.2 304 122 2.89 16.73 2.68 2.28 13.3 4.13 4.84 47.3 54.2 1180 85.8 0.19
Dry matter. The mineral mixture contained 811 g of ground corn/kg on an as fed basis. c Calculated chemical composition of total mixed ration (TMR) based on analyzed chemical composition of individual ingredients. The TMR contained (g/kg DM): 451 g alfalfa hay, 41.5 g wheat straw, 264 g rolled corn grain, 125 g almond hulls, and 118 g mineral mixture. Fresh water was added at 260 g/kg of DM to increase the moisture content. d Neutral detergent fiber assayed with a heat stable amylase, expressed exclusive of residual ash. b
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drawn at 1, 24, 42, 82, 137 and 209 d of the feeding period, followed by recording individual animal BW. Whole blood and serum samples were stored at 5 °C until submission to the California Animal Health and Food Safety Laboratory (Davis, CA, USA).
Optek Corporation, Franklin, MA, USA) according to Martin et al. (1987). After precipitation of proteins in serum, protein free supernatants were analyzed for Cu ICP-AES (spectrometer listed above) as described by Melton et al. (1990).
2.2.2. Liver and muscle biopsies Liver and muscle samples were collected by biopsy (Juchem et al., 2012). Briefly, the surgical field was cleaned, thoroughly disinfected, local anesthesia administered and liver samples biopsied with a biopsy needle (Sontec Instruments, Inc., Englewood, CO, USA) and an ultrasound unit with a 3.5 MHz convectional mechanical probe (WED-200A, Well.D Electronics Co., Ltd, Shenzhen, China). The biopsy needle was introduced into the abdominal cavity through an incision of ~ 3 cm and positioned cranio-ventrally towards the elbow on the opposite flank of the animal, deep enough to reach the liver. Samples from the semitendinosus muscle were collected from the right rear leg utilizing a scalpel and curved haemostatic forceps (Juchem et al., 2012). Incisions for sampling liver and muscle were closed with an interrupted cruciate and simple continuous suture patterns, respectively. Liver samples were individually stored in plastic micro tubes and kept in ice until submitted to the California Animal Health and Food Safety Laboratory for analyses. Before each biopsy, heifers received an intramuscular injection of penicillin (22,000 IU/kg BW), except for the last sampling where 2 mg/kg BW of Ceftiofur Hydrochloride (Excenel® RTU, Pfizer, New York, NY, USA) was used in order to avoid antibiotic residues in the beef. All animal procedures are fully compliant with laws of the USA and the State of California, as well as animal protocols of the University of California at Davis (CA, USA).
2.4. Statistical analysis
2.3. Analytical methods 2.3.1. Feeds and diets Feed samples were assayed for organic and mineral chemical composition. Moisture at 105 °C was determined gravimetrically (Reuter et al., 1986), neutral detergent fiber was as described by Van Soest et al. (1991) utilizing sodium sulphite, a heat stable amylase, and is expressed without residual ash (aNDFom), acid detergent fiber (ADF) was according to AOAC (2000; #973.18) and is expressed with residual ash. Lignin(sa) was determined by the sulfuric acid procedure (Robertson and Van Soest, 1981), and ash was determined as the residue after heating to 550 °C for 8 h. Total fat was determined by extraction with ether (AOAC, 2000; #930.39). Feed samples were digested in nitric acid/hydrogen peroxide microwave digestion system and the contents of P, S, Ca, Mg, Na, B, Zn, Mn, Fe and Cu were quantified utilizing atomic absorption spectrometry or inductively coupled plasma atomic emission spectrometry (ICP-AES; Sah and Miller, 1992; Meyer and Keliher, 1992). Samples were extracted with 20 g/L acetic acid for K and Cl determinations, whereas K levels were determined by atomic emission spectrometry (Johnson and Ulrich, 1959) and Cl by a chloridometer (Johnson and Ulrich, 1959). Samples were extracted with nitric/perchloric acid digestion/dissolution and determined by vapor generation using ICP-AES (Tracy and Moeller, 1990) for determination of total Se content in feeds. Total N was determined by the Dumas method (LECO FP-528; AOAC (2002; #990.03)). 2.3.2. Blood, serum and tissues Liver and muscle tissues were digested in a solution of nitric, sulfuric and perchloric acids at 350 °C, followed by reduction with 5 M HCl at 95 °C. The Se levels were by hydride vapor generation inductively coupled plasma spectrometer (FISONS, Accuris Model, Thermo Optek Corporation, Franklin, MA, USA) as described by Tracy and Moeller (1990). Whole blood Se Levels were by ICP-AES as described previously (Tracy and Moeller, 1990). Liver tissues were digested with nitric acid at 180 °C and subsequently analyzed for Cu by ICP-AES (FISONS, Accuris Model, Thermo
The CWR and TWG grazing treatments had been applied before this feeding period began and were discontinued as the heifers were moved to the common LSeD. However because tissue Se levels were biologically different between the two forage groups at this time, and it was likely that the initial level of Se could affect Se depletion, the prior treatment was maintained in the statistical model. Thus the effect of ‘treatment’ represents two scenarios of Se load rather than a residual grazing effect per se, and we do not consider it to be related to Se content from the two forages grazed by these heifers in Juchem et al. (2012). Data were analyzed as repeated measures utilizing the PROC MIXED procedure of SAS (2002) with the experimental unit (heifers) as a random effect as this covariance structure was the most appropriate based on its lowest Bayesian Information Criterion. The model included effects of heifer, time (fixed), forage (fixed) and the forage by time interaction. Differences P ≤ 0.05 were considered significant, and 0.05 b P ≤ 0.10 were considered a tendency to a difference. 3. Results 3.1. Diet and animal performance Feed ingredients in the LSeD varied in levels of Se (Table 1), but the LSeD contained 0.19 mg/kg DM as well as 95.2 g/kg CP, 304 g/kg aNDF, 16.7 g/kg Ca, 2.9 g/kg P and levels of other macro and micro minerals (Table 1) that met or exceeded requirements of growing heifers (NRC, 2000). Heifers were fed 12 to 15 kg of TMR/d (DM) for 209 d to b30 g/kg refusals. Heifers that had previously grazed CWR or TWG had similar BW at the start of LSeD feeding, 325 and 315 kg (±10.4 SEM), respectively. Despite differences in initial Se levels in liver and blood between CWR and TWG heifers, their BW and BW gains were similar (Fig. 1). After 209 d of feeding the LSeD, CWR and TWG heifers weighed 525 and 491 kg (±25.1; Fig. 1). 3.2. Concentration of Cu in serum and liver Serum (0.50 versus 0.28 mg/L) and liver (22.9 versus 1.1 mg/kg WW) Cu levels (Juchem et al., 2012) were higher (P b 0.05) at the start of LSeD feeding for heifers which had previously grazed CWR versus TWG. Serum Cu levels after 209 d of feeding the low Se, Cu adequate, diet
Fig. 1. Body weight (BW; kg) from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for 165 d. Body weight gain was similar (P = 0.72; Pooled SEM = 12.52) in heifers that had previously grazed CWR or TWG and were then fed a low Se diet for 209 d.
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were higher than at its start, but similar for heifers which had previously grazed CWR versus TWG (0.67 versus 0.70 mg/L; Table 2). Levels of Cu in liver had converged by 209 d, and were also similar (14.2 versus 17.4 mg/kg WW; Table 2) in the previously grazed CWR versus TWG heifers. 3.3. Concentration of Se in blood, liver and muscle The Se levels in whole blood (1.19 versus 0.81 mg/L), liver (2.7 versus 2.1 mg/kg WW) and muscle (0.87 versus 0.63 mg/kg WW) at the beginning of the low Se feeding period were higher (P b 0.01) in heifers that had grazed TWG versus those that had grazed CWR (Figs. 2, 3, 4) because TWG had a higher Se content at the end of grazing (Juchem et al., 2012). The Se levels decreased in blood, liver and muscle with time of feeding the LSeD (Figs. 2, 3, 4), although the extent of the decrease differed, particularly in muscle. Indeed the liver Se levels depleted faster than blood or muscle and, after feeding the LSeD for only 24 d the Se levels reduced (P b 0.01) 60 and 65% in liver (0.85 versus 0.93 mg/kg WW), and 21 and 22% in blood (0.63 versus 0.92 mg/L) in heifers previously grazed CWR or TWG, respectively. In muscle, levels of Se 82 d after feeding the LSeD (0.85 versus 0.93 mg/kg WW) was only reduced by 32 and 30% in heifers that had grazed CWR and TWG, respectively. Despite the rapid decline in liver and blood Se levels, blood Se levels at the end of the low Se feeding period were higher than levels measured at the beginning of the grazing season (i.e., before grazing the high Se TWG and CWR; Juchem et al., 2012) in blood (0.32 versus 0.10 mg/L), liver (0.62 versus 0.23 mg/kg WW), and muscle (0.42 versus 0.06 mg/kg WW). 4. Discussion It is well documented that Se is an essential mineral for health and reproduction of mammals, and supplementing Se at suboptimal levels, and/or factors which limit Se absorption, have been associated with poor reproductive performance. However, unlike most minerals, Se has a narrow safety margin between essentiality and toxicity. 4.1. Animal performance and micro minerals Beef production systems in the USA typically utilize grazing to provide feed for replacement heifers, pregnant cows and calves until weaning. However 6 to 12 mo old calves are fed energy dense diets until slaughter at 14 to 18 mo. We had previously used 6 mo old weaned heifers to evaluate the BW gain potential of CWR and TWG forages containing high levels of Se under grazing conditions (Juchem et al., 2012) because such animals are suitable for such production systems. Findings from that study demonstrated that TWG can support BW gains of 0.5 kg/d if the CP content in the forage is not limiting, whereas CWR supported slightly lower BW gains (Juchem et al., 2012). Forages such as CWR and TWG grown in saline soils in the west side of SJV of California may have excess Se and can contain imbalanced micro-mineral levels (Grattan et al., 2004b; Suyama et al., 2007b) relative to the requirements of growing beef cattle (NRC, 2000). In fact, these forages
Table 2 Concentration of Cu in serum (mg/L) and liver (mg/kg wet weight) from heifers which had previously grazed creeping wildrye (CWR) or tall wheatgrass (TWG) for 165 d, and were then fed a low Se, Cu adequate, diet for 209 d.
Serum Liver 1
CWR
TWG
SEM
Forage
0.67 14.2
0.70 17.4
0.034 2.72
0.44 0.42
1
1
Forage ∗ time b0.01 b0.01
P values for the effects of forage and the interaction of forage by time.
Fig. 2. Concentration of Se (mg/L) in whole blood from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for a 165 d and were then fed a low Se diet for 209 d. Heifers that had previously grazed TWG (dashed line) had higher concentration of Se up to 82 d of feeding (forage by day interaction; P b 0.01), however concentration of Se in whole blood decreased over time for heifers fed either forages (day effect; P b 0.01). Pooled SEM = 0.52.
had low levels of Cu (b 7 mg/kg forage DM), Mg (b0.10 mg/kg forage DM), Zn (b30 mg/kg forage DM), and high levels of Mo (N5 mg/kg forage DM) and S (0.4 mg/kg forage DM; Juchem et al., 2012). Thus the heifers that started this LSeD feeding period had very high Se levels in blood and liver, but were deficient in Cu. The high levels of dietary Mo (N 5 mg/kg DM) and S (N 0.2%), which decrease rumen Cu absorption, likely caused the Cu deficiency. Generally, growing cattle that are underfed for a period of time and changed to a more nutrient dense diet demonstrate compensatory growth (i.e., BW gains are higher than those predicted based on nutrient requirements). However, this was not the case here and potential compensatory gains only occurred after 138 d of feeding the low Se diet when heifers gained 1.78 and 1.74 kg/d after previously grazing CWR or TWG, respectively. Despite the adequate LSeD nutrient levels during the 209 d LSeD feeding period, the diet (and its low Se level) should have supported BW gains of 1.1 kg/d (NRC, 2000) as voluntary DM intake was not depressed, but the heifers had modest BW gains (i.e., 0.28 and 0.38 kg/d for heifers that had grazed CWR or TWG, respectively) during the first 80 d of LSeD feeding. That BW gains increased with time of feeding the LSeD, but were still lower than anticipated based on diet nutrient composition, may have been related to the
Fig. 3. Levels of Se (mg/kg wet weight) in liver samples from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for a 165 d and were fed a low Se diet for 209 d. Levels of Se in wet liver were higher for heifers that grazed TWG (P b 0.05; interaction of forage by day) at beginning of the feeding period and at 82 d after feeding, however both groups of heifers (i.e., CWR and TWG) showed the largest depletion in Se from liver during the first 24 d of exposure to a low Se diet. Pooled SEM = 0.049.
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4.2. Se depletion in whole blood and liver
Fig. 4. Concentration of Se (mg/kg wet weight) in muscle tissue from heifers that had previously grazed creeping wildrye (CWR; solid line) or tall wheatgrass (TWG; dashed line) for 165 d and were fed a low Se diet for 209 d. Concentration of Se in muscle tissue remained higher in heifers that grazed TWG (forage by day interaction; P b 0.05; Pooled SEM = 0.021) except at 209 d, compared to heifers that grazed CWR.
declining tissue levels of Se and/or increasing levels of Cu. Although it is tempting to associate the decrease in Se level in blood and liver over time (Figs. 2 and 3) with the increases in the extent of BW gain (Fig. 1), the literature provides no support for such an association. Feeding diets containing up to 10 mg/kg of Se from sodium selenite (an inorganic Se source) to wether lambs for a period of 52 wks increased the Se concentration in liver to as high as 20 mg/kg of dry liver, but BW gains were similar across all levels of sodium selenite supplementation (Cristaldi et al., 2005). Similar findings were reported by Lawler et al. (2004) who supplemented steers with 2.8 mg Se/kg in an organic or inorganic form for 126 d and found BW gain and DM intake were similar to the control group, which were fed a diet containing only 0.38 mg Se/kg. Limited research exists on Cu and Se interactions, but indicates that high Cu intakes induce signs of Se deficiency in chicks (Jensen, 1975). However mammalian research suggests that increasing Se intake does not alter Cu metabolism (Miller and Groziak, 1997). While Se levels in blood and liver decreased with time of feeding, the Cu concentration in serum increased for both CWR and TWG heifers. Researchers have found bovine herds with low liver Cu levels and a high incidence of Cu deficiency, but that it is not uncommon for a high proportion of animals to have “normal” serum Cu levels (Hall and ZoBell, 2010). Since most body Cu is stored in the liver, it is liver Cu levels which give a true reflection of the Cu status of the animal. The magnitude of BW gains were higher in the last third of our feeding period suggests that increasing Cu status may have been associated with the improved BW gains. In contrast, despite the large difference in Cu levels in serum and liver among the CWR and TWG heifers at the beginning of the study, BW gains did not differ between the forage groups (Fig. 1). It is possible that high levels of S accumulation in liver and whole blood, known to depress voluntary feed intake and BW gain, could have been one of the reasons that heifers took longer to express their full BW gain potential. Excess dietary S in ruminants has been shown to interfere with absorption of some trace minerals, particularly Cu, Mo and Se (reviewed by Kandylis, 1984). Because of confounded mineral levels in tissues over time, and possible interactions of high Se levels with other minerals, the delay to enhanced animal performance after heifers were moved from high Se pastures to the LSeD cannot be clearly explained, particularly because we did not anticipate such findings and so the experimental design did not contemplate such a comparison. However, findings suggest that if BW gains are to be optimized during a confinement phase that follows grazing Se-enriched forages, supplementation of minerals, except Se, should be included, to at least alleviate the effects observed in our study.
Levels of Se decreased with time after grazing (P b 0.01) which would be expected from animals that had been previously consuming a Se enriched diet, and Se depletion from blood, liver and muscle differed. At the end of grazing, liver levels of Se were 25% higher in TWG versus CWR heifers but, after 20 d of eating the LSeD, both groups had similar liver Se thereby demonstrating that mobilization of Se accumulated in liver occurred quickly. The Se concentration in blood decreased at a slow rate, likely because Se mobilized within liver and muscle continuously entered the blood pool. Stockdale and Gill (2011) found blood Se concentrations were slow to react after the exclusion of Se-enriched pellets in the diets of dairy cows. And since Se in whole blood responds slowly to changes in Se concentration as most Se is incorporated into red blood cells during erythropoiesis, there is a lag in blood Se. A full whole blood response to a dietary Se supplementation or depletion may therefore require a time span equal to the average life span of the red blood cell, which in cattle is 90 to 120 d (Stowe and Herdt, 1992). At 81 d of post-grazing, levels of Se were reduced by 77% in liver, 49% in blood, but only 31% in muscle. These results are consistent with Juniper et al. (2008) who reported the Se depletion rate in lamb tissue was fastest in liver and the slowest in skeletal muscle after Se supplementation. At 81 d of post grazing, liver Se levels had reached their lowest level while blood Se only reached its lowest level after 137 d of feeding the low Se diet. There were no differences in the levels of Se within the liver and blood between heifers that had previously grazed CWR or TWG. 4.3. Depletion of Se in muscle and implications Major food sources of Se in the American diet are breads, grains and meats (National Institutes of Health, 2013). Attempts to improve the nutritional value of foods for human consumption, such as raising micronutrient levels in milk and meat (Knowles et al., 2004), have been considered as delivery systems for health-promoting nutrients in geographical areas with micronutrient deficiencies. Benefits of utilizing geographical areas naturally high in Se to produce Se-enriched beef has been previously suggested (Hintze et al., 2001; Lawler et al., 2004). 5. Conclusions Our findings partially support our initial hypothesis, as time of feeding a low Se diet was an important factor in determining the concentration of Se in muscle of beef heifers previously loaded with Se. However even after 209 d of exposure to low levels of dietary Se, muscle Se levels were elevated making this a suitable system to produce Se-enriched beef from low value crops grown on saline degraded soils. However forages grown under these conditions can limit performance due to mineral imbalances and, in some cases, suboptimum CP contents, which may have limited the performance of heifers subsequently fed energy dense diets post-grazing. Acknowledgments The authors greatly appreciate the logistical support, animal facilities and equipment provided by John Diener and staff from Red Rock Ranch in Five Points, CA (USA) to conduct this research. We are also thankful to Dr. John Maas (University of California Veterinary Medicine Extension) for his technical support and kindness in lending us his surgical materials for liver and muscle biopsies. The authors acknowledge the technical and scientific inputs of Dr. S. Juchem. This research was funded through Proposition 204 Agricultural Drainage Program (agreement #4600007357) administrated by the California Department of Water Resources and the California State University Agricultural Research Initiative (CSU-ARI, grant #07-1-001-13).
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