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ANIMAL NUTRITION |
Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, Canada S7N 5A8
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Abstract |
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 Top Abstract INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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0.74) by dietary treatment. Dietary treatment had no effect on endogenous production of urea N and its recycling to the GIT; however, across dietary treatments, endogenous production of urea N (45.8 to 50.9 g/d) exceeded N intake (42.3 to 47.9 g/d). Across dietary treatments, 30.6 to 38.5 g/d of urea N were recycled to the GIT, representing 0.67 to 0.74 of endogenous urea N production; however, 0.64 to 0.76 of urea N recycled to the GIT was returned to the ornithine cycle. In summary, although dietary treatment did not alter urea N kinetics, substantial amounts of hepatic urea N output were recycled to the GIT under the dietary conditions used in this study, and additional research is required to determine how this recycled urea N can be efficiently captured by bacteria within the GIT.
Key Words: nitrogen metabolism • processed barley • ruminally degradable protein • sheep • urea nitrogen recycling
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INTRODUCTION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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). Urea that is recycled to the GIT is an important source of N for microbial growth. Increasing dietary amounts of ruminally fermentable carbohydrate (RFC; Huntington, 1989; Rémond et al., 1996) or shifting carbohydrate digestion from the small intestine to the rumen via steam-flaking compared with dry-rolling of sorghum grain (Theurer et al., 2002) increased urea N transfer to the rumen, in addition to increasing N sequestration into microbial protein.
In ruminants fed low-N diets, a greater proportion of blood urea N is recycled to the GIT compared with animals fed adequate levels of N (Siddons et al., 1985; Marini et al., 2004). However, under practical feeding conditions, high-producing ruminants (e.g., dairy cows fed for high levels of milk yield) are usually fed high levels of dietary N (25.6 to 32.0 g of N/kg of DM; NRC, 2001) to adequately meet protein requirements. Marini and Van Amburgh (2003) demonstrated in Holstein heifers that, even at high levels of N intake (25.0 to 34.0 g of N/kg of DM), there was a wide range (29 to 42%) in the proportion of hepatic urea N output that was recycled to the GIT. Clearly, therefore, there is opportunity for manipulation of urea N recycling to the GIT, even in ruminants fed high-N diets, to improve N efficiency of ruminants. Because ruminal NH3-N concentration is negatively correlated with the rate of urea N transfer into the rumen (Kennedy and Milligan, 1980), the form of the N fed, particularly the proportion of ruminally degradable protein (RDP), is important because it determines how much N is directed toward ruminal NH3-N (Lapierre and Lobley, 2001). However, limited information is available on how concomitant changes in dietary content of RFC and RDP might influence urea N kinetics in ruminants fed high N diets.
Our hypothesis was that changes in the proportion of dietary N that is digested in the rumen (by varying dietary RDP level) would alter urea N recycling to the rumen, and that this effect would be more pronounced with more extensive barley grain processing, which would increase ruminal starch digestion and subsequently urea N recycling to the rumen and microbial N sequestration.
The objective of this study was to determine how interactions between dietary RDP level and RFC alter urea N transfer to the GIT and the utilization of this recycled urea N in lambs.
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MATERIALS AND METHODS |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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The lambs were cared for and handled in accordance with regulations of the Canadian Council on Animal Care (1993), and their use in this experiment was approved by the University of Saskatchewan Animal Care Committee.
Four Suffolk ram lambs (34.8 ± 0.5 kg of initial BW) were used in this study. The experiment used a 4 x 4 Latin square design with 21-d periods and a 2 x 2 factorial arrangement of dietary treatments. Each experimental period consisted of 14 d of dietary adaptation and 7 d of data collection. Throughout the experiment, lambs were housed at the Livestock Research Building (University of Saskatchewan) in a temperature-controlled environment (18 to 22°C). Lambs were housed in individual floor pens (during dietary adaptation) or in metabolism crates (during the 7-d data collection period) to facilitate total urine and feces collection. It was decided to use rapidly growing lambs as an experimental model because of their high N demands for rapid growth. Most previous research investigating regulatory mechanisms that impact urea N recycling in ruminants has been conducted using slow-growing ruminants, ruminants fed at low intakes, nonlactating cows, or low-producing lactating cows (Lapierre and Lobley, 2001), yet the productive state of the animal is important because it dictates biological N requirements.
Experimental Treatments and Feeding Management
The 4 dietary treatments were formulated by combining 2 factors, each with 2 levels. The dietary factors studied were 1) dry-rolled vs. pelleted barley as the principal source of RFC and 2) dietary levels of RDP of 60 vs. 70% (% of CP, DM basis). The ingredient and chemical composition for 4 concentrate mixtures used to formulate the experimental diets are presented in Table 1. Dietary levels of RDP were manipulated by changing inclusion levels of urea, canola meal, and corn gluten meal in concentrate mixtures. Barley grain obtained from one source was used for both dry-rolled and pelleted barley throughout the experiment. The dry-rolled barley was prepared by passing whole barley grains through large rollers (23 x 58 cm). For pelleting, whole barley grains were ground through a 6.35-mm screen in a hammer mill and then pelleted using a California pellet mill. Experimental diets were fed twice daily for ad libitum intake at 0900 and 1700 as total mixed rations (TMR), composed of 80% concentrate mixture and 20% barley silage (DM basis), which were hand mixed thoroughly just before feeding. Barley silage contained 35.5% DM and its chemical composition (DM basis) was 90.9% OM, 11.3% CP, 54.7% NDF, 35.8% ADF, and 3.42% ether extract.
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. Lambs had free access to water and were weighed weekly.
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Experimental lambs were moved from individual floor pens into individual metabolism crates on d 12 of each experimental period to allow acclimation before the initiation of data collection on d 15. During the 7-d data collection period, individual lamb feed intake was recorded daily. Samples of experimental TMR and orts were collected daily, stored at –20°C, and composited per lamb for each experimental period before chemical analysis.
On d 14 of each experimental period, lambs were fitted with temporary vinyl catheters (0.86-mm i.d. x 1.32-mm o.d.; Scientific Commodities Inc., Lake Havasu City, AZ) in the right and left jugular veins to allow for simultaneous isotope infusion and blood sampling. Urea transfer to the gastrointestinal tract and whole-body N balance were determined between d 15 and 21, as described by Lobley et al. (2000). Briefly, background samples of urine, feces, and blood were collected on d 14 to measure the natural abundance of 15N. Beginning on d 15 of each experimental period, double-labeled urea ([15N15N]-urea, 99.8 atom % 15N, Cambridge Isotope Laboratories, Andover, MA) prepared in 0.15 M sterile saline was infused continuously into a jugular vein at a rate of 1.2 mmol of N/d using a peristalitic pump (Model 60 rpm/7524-10, Masterflex L/S Microprocessor Pump Drive, Vernon Hills, IL) for 96 h (d 15 to 19).
Total feces and urine were collected daily between d 15 and 21 before the 0900 feeding to determine daily outputs. Feces were collected using fecal bags, which were fitted 2 d before the start of collection to allow acclimation. Bags were emptied daily at 0900 during total collection periods. Total daily fecal output for each lamb was mixed thoroughly, quantitatively transferred into a preweighed plastic container and weighed. A 25% subsample was taken daily and stored at –20°C. Urine was collected into sealed plastic containers placed below metabolic crates. Plastic containers had 40 mL of 12 M HCl to maintain the urine pH between 2 to 3 to prevent bacterial growth and the loss of ammonia. Total urine output was recorded daily. A 50-mL subsample of urine was collected daily (d 16 to 19) and stored at –20°C until analyzed for proportions of [15N15N]-, [14N15N]-, and [14N14N]-urea in urinary urea. In addition, a 2-mL subsample of urine was diluted with 8 mL of distilled water and stored at –20°C for later determination of urea N and purine derivatives (PD). All daily urinary output was composited by period and animal and stored at –20°C until analyzed for total N. Blood samples were collected daily from the contralateral jugular vein in vacutainers containing heparin just before the 0900 feeding. Blood samples were centrifuged at 1,500 x g for 15 min at 4°C, and the plasma obtained was stored at –20°C until analyzed for urea N.
Sample Analyses
At the end of the trial, frozen TMR, orts, and fecal subsamples were thawed overnight at room temperature and analyzed for DM by drying in an oven at 60°C for 48 h (AOAC, 1990; method 930.15). Dried TMR, orts, and feces were then ground through a 1-mm screen using a Christy-Norris mill (Christy and Norris Ltd., Chelmsford, UK). Ground TMR, orts, and feces samples were pooled per lamb for each experimental period and analyzed for OM by ashing at 600°C for at least 8 h, CP using the macro-Kjeldahl procedure (AOAC, 1990; method 990.03), ether extract (AOAC, 1990; method 920.39), ADF (AOAC, 1990), and NDF (Van Soest et al., 1991). Amylase and sodium sulfite were used for NDF determination. Dietary content of RDP in experimental TMR and ruminal starch degradation were determined using the in situ method, as described by Yu et al. (2003). Briefly, air-equilibrated experimental TMR samples (approximately 7 g) were weighed into nylon bags and incubated in the rumen of a steer fed barley silage for 2, 4, 8, 12, 24, and 48 h. The rumen incubation protocol, nylon bags, and washing and drying procedures for nylon bags were as described by Yu et al. (2003). Samples of TMR and nylon bag residues were analyzed for CP using the macro-Kjeldahl procedure (AOAC, 1990; method 990.03) and for total starch (AOAC, 1990; method 996.11) using a commercial kit (Total Starch Assay Kit, Megazyme International Ireland Ltd., Wicklow, Ireland). Rumen degradation characteristics of CP and starch were analyzed using the NLIN procedure (SAS Institute Inc., Cary, NC) using iterative least squares regression (Gauss-Newton method), as described by Yu et al. (2003).
Total N in pooled urine was determined using the macro-Kjeldahl procedure (AOAC, 1990). Daily dilute urine subsamples were pooled by lamb and experimental period and analyzed for allantoin and xanthine plus hypoxanthine (Chen and Gomes, 1992), and for uric acid by a quantitative enzymatic colorimetric method using a commercial kit (Stanbio Uric Acid Liquicolor Kit, Procedure No. 1045, Stanbio Laboratories, Boerne, TX). Total PD excretion per day was calculated as: allantoin + uric acid + xanthine plus hypoxanthine. Microbial nonammonia N supply was calculated based on total PD excretion in urine (Chen and Gomes, 1992), using BW measurements obtained on d 14. The ratio of purine N:total N in ruminal microbes was assumed constant at 11.6:100 (Chen and Gomes, 1992). Plasma urea N (PUN) and urinary urea N were determined by the diacetyl monoxime method of Marsh et al. (1957) using a commercial kit (Stanbio Urea Nitrogen Kit, Procedure No. 0580, Stanbio Laboratories).
To determine the proportions of [15N15N]-, [14N15N]-, and [14N14N]-urea in daily urine samples, urinary urea was isolated by applying urine containing 1.5 mg of urea N through prepacked cation exchange resin columns (AG-50W-x8 Resin, 100–200 mesh, H+ form, BioRad, Richmond, CA) as described by Archibeque et al. (2001). Previous studies have determined that this concentration of urea N was suitable to ensure sufficient amounts of gas for analysis, yet minimized the occurrence of non-monomolecular degradation of urea (Archibeque et al., 2001; Marini and Van Amburgh, 2003). After the urine was applied to the column, 7 mL of N-free water was applied to the columns, and the eluate discarded. Urea was then eluted by applying 20 mL of N-free water to the columns, which was collected into test tubes. The eluate was air-dried at 60°C, and urea was quantitatively transferred into 17- x 60-mm borosilicate glass tubes using three 1-mL rinses of N-free water. The urea samples were then freeze-dried and the proportions of [15N15N]-, [14N15N]-, and [14N14N]-urea in urinary urea were analyzed by isotope ratiomass spectrometry (Lobley et al., 2000) at the N-15 Analysis Laboratory, University of Illinois (Urbana-Champaign). Under the conditions of this assay, [14N14N]-, [14N15N]-, and [15N15N]-urea molecules should yield ions with mass/charge (m/z) values of 28, 29, and 30, respectively. To account for nonmonomolecular reactions, standards that were prepared from [15N15N]-urea (99.8 atom % 15N) and [14N14N]-urea (natural abundance urea; 0.364 atoms % 15N) were also analyzed and the necessary corrections for [14N15N]-urea that is produced by non-monomolecular reactions were then made (Lobley et al., 2000). Fecal samples collected daily (d 15 to 19) were analyzed for total 15N enrichment by combustion to N2 in an elemental analyzer and continuous flow isotope ratio-mass spectrometry, as described by Lobley et al. (2000).
Calculation of Urea N Kinetics
For all dietary treatments, enrichments of urinary [15N15N]-, [14N15N]-, and [14N14N]-urea, and fecal 15N attained isotopic plateau by 72 h (i.e., d 3) after the initiation of isotope infusion. Therefore, plateau enrichments over the last 72 to 96 h of isotope infusion were used in calculations of urea N kinetics according to the model of Lobley et al. (2000). In this model, a portion of urea N synthesized in the liver (urea N entry rate, UER) is lost via the urine (urinary urea N elimination, UUE) and the remainder enters the GIT (GIT entry rate, GER). The urea N entering the GIT (i.e., the GER) undergoes bacterial degradation liberating NH3. A portion of this NH3 is excreted in feces (urea N in feces, UFE), some is reabsorbed into portal blood and reenters the ornithine cycle in the liver (ROC), and the remainder is used for anabolic purposes (urea N utilized for anabolism, UUA; Lobley et al., 2000).
Statistical Analysis
All data were analyzed using PROC MIXED of SAS for a 4 x 4 Latin square design according to the following model: Y = µ + P + L + R + G + (R x G) + E, where Y is the dependent variable, µ is the overall mean, P is the effect of period, L is the effect of lamb, R is the effect of dietary RDP level, G is the effect of method of barley grain processing, R x G is the interaction between dietary RDP level and method of barley grain processing, and E is the residual error. All terms were considered fixed, except L and E, which were considered random. When there was a significant method of barley processing x level of RDP interaction, means were separated by Tukey’s honestly significant differences test. Treatment differences were considered significant when P < 0.05 and tendencies are discussed when 0.05 < P < 0.10.
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RESULTS AND DISCUSSION |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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The chemical compositions of experimental TMR fed to growing lambs are presented in Table 2
. The TMR were formulated to be isonitrogenous at 28.8 g of N/kg of DM (18.5% CP), and chemical analysis showed only marginal deviations in dietary N content across the TMR, with a CV of 1.9% (Table 2). Experimental TMR contained 60 and 70% RDP (as % of CP), or 11.1 and 13.1% (as % of DM; Table 3). The actual RDP levels as determined using the in situ technique indicated only marginal deviations from these intended dietary RDP contents (Table 2). The NRC (2001) recommendations for dietary RDP levels are 10.9 to 11.3% (as % of DM) for cows producing up to 40 kg/d of milk. However, Reynal and Broderick (2005) fed dairy cows diets with RDP levels ranging from 13.2 to 10.6% (as % of DM) and concluded that recommended levels of RDP should fall between 11.7 and 12.2%. The RDP levels that were tested in our study are comparable to that recommended RDP range. As expected, the in situ soluble CP fraction (P < 0.001), the degradation rate of the degradable CP fraction (P = 0.004), and effective CP degradability (P < 0.001) of the high-RDP diet were greater than that of the low-RDP diet; however, the degradable CP fraction was smaller (P < 0.001) for the high-RDP diet compared with the low-RDP diet (Table 3).
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). As expected, the in situ soluble starch fraction (P = 0.04), degradation rate of the degradable starch fraction (P = 0.03), and effective starch degradability (P = 0.02) of the TMR containing pelleted barley were greater than that of the TMR containing dry-rolled barley; however, the degradable starch fraction tended to be lower (P = 0.07) in the TMR containing pelleted barley compared with those containing dry-rolled barley. Data comparing ruminal starch digestion in ruminants fed dry-rolled or pelleted barley are scarce. Unpublished results from current research in our laboratory using ruminally cannulated dairy cows indicated that feeding pelleted barley increased ruminal starch digestion, decreased ruminal pH, and increased VFA concentrations compared with feeding dry-rolled barley (T. Mutsvangwa, unpublished data). We did not measure ruminal starch digestion in lambs used in the current study; however, based on the in situ ruminal starch digestion measurements, we can surmise that ruminal starch digestion was altered by barley grain processing. Intakes, N Balance, Urea N Kinetics, and Microbial Nonammonia N Supply
As expected, all experimental lambs gained weight (200 ± 3.5 g/d on average) during the experiment. Interactions between the level of dietary RDP and method of barley grain processing influenced N metabolism in lambs (Table 4). Lambs fed the high dietary RDP consumed 111 g/d more DM compared with those fed the low dietary RDP (P = 0.006); consequently, lambs fed the high dietary RDP consumed 4.2 g/d more N compared with those fed the low dietary RDP (P = 0.001). Compared with the high dietary RDP, excretion of fecal N (P = 0.002) and urinary N (P = 0.03) were 1.8 and 2.9 g/d lower, respectively, in lambs fed the low dietary RDP. The greater N intake (4.2 g/d) in lambs fed the high dietary RDP was similar to the extra N (4.7 g/d) that was voided in feces and urine. Nitrogen digestibility was greater (P = 0.04) in lambs fed dry-rolled barley compared with those fed pelleted barley. In addition, N digestibility was greater (P = 0.04) in lambs fed the low dietary RDP compared with those fed the high dietary RDP. Retained N was unaffected (P 0.74) by dietary treatment, and all experimental animals were in positive N balance. Previous research with lambs fed varying dietary N levels reported that N retention reached a plateau at dietary N contents around 28 g of N/kg of DM (Marini et al., 2004), which is equivalent to the dietary N content used in our study. Plasma urea N concentration was unaffected (P = 0.27) by barley processing, but it tended (P = 0.06) to be greater in lambs fed the low dietary RDP compared with those fed the high dietary RDP. Lambs fed high-concentrate diets with N contents comparable to those used in our study (27.2 g of N/kg of DM) had similar PUN concentrations (Dabiri and Thonney, 2004; Marini et al., 2004). The greater PUN concentration in lambs fed the low-RDP diet was unexpected, especially considering that these lambs had lower intake of ruminally fermentable N, which would have decreased postabsorptive NH3-N supply for hepatic ureagenesis; the reasons for this observation are unclear.
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; Marini and Van Amburgh, 2003; Marini et al., 2004) have clearly demonstrated that a greater proportion of hepatic urea N output is transferred to the GIT in ruminants fed low-N diets; however, under practical feeding conditions during lactation or growth, productive ruminants are rarely fed low-N diets. In Holstein heifers fed high-N diets, there was a wide range (29 to 42%) in the proportion of hepatic urea N output that was recycled to the GIT (Marini and Van Amburgh, 2003), indicating that even at high levels of N intake there is opportunity to enhance N efficiency of ruminants by manipulating the extent of urea N recycling to the GIT. Therefore, it is important to delineate regulatory mechanisms that dictate urea N transfer to the GIT and the subsequent fate of recycled urea N in ruminants fed high-N diets. In our study, dietary treatment did not alter (P 0.22) urea kinetics as measured by the intrajugular [15N15N]-urea infusion protocol (Table 5); however, urea N transfer to feces (UFE) was greater (P = 0.01) in lambs fed dry-rolled barley compared with those fed pelleted barley. Previous research showed that the proportion of GER lost via the feces is largely influenced by the supply of fermentable energy to the hind-gut (Thornton et al., 1970; Oncuer et al., 1990). In our study, we did not measure fermentable energy supply to the hind-gut, but, based on the in situ ruminal starch digestion, we can surmise that feeding dry-rolled barley compared with pelleted barley provided more fermentable energy to the hind-gut, thus a greater transfer of GER to the hind-gut and subsequent loss via the feces. Urea N transfer to feces tended (P = 0.08) to be greater in lambs fed the high dietary RDP compared with those fed the low dietary RDP. Fractional urea N transfers of the GER to feces ranged from 0.015 to 0.022 across diets, and this represented the smallest proportion of GER. Urea-N transfer to urine (i.e., UUE) was unaffected (P > 0.05) by dietary treatment (Table 5). Fractional urea-N transfers of the UER to urine were unaffected (P > 0.05) by dietary treatment and ranged from 0.26 to 0.33 (Table 5). In a previous study with lambs fed diets with similar N contents as in the current study, Lobley et al. (2000) reported UUE:UER ratios of 0.305 to 0.390, which are in agreement with UUE:UER ratios obtained in the present study. Across dietary treatments, hepatic urea production (UER) was 1.06 to 1.13 of N intake. In growing ruminants, hepatic output of urea N can exceed N intake under a variety of dietary conditions, and it is positively correlated with N intake. The UER:N intake ratios obtained in sheep by other researchers (0.77 to 0.95, Lobley et al., 2000; 0.73 to 0.99, Sunny et al., 2007) indicate that the UER:N intake ratio can vary considerably depending on dietary conditions. However, in these studies, N intakes (range of 14 to 22 g/d) were lower than in our study (42.3 to 47.9 g/d), and this difference might explain the greater UER:N intake ratios that we observed.
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). Even though urea N was transferred to all compartments of the GIT, it is generally assumed that a significant proportion of the GER is transferred to the rumen (Lobley et al., 2000). In ruminants, the proportion of hepatic urea N output that can be recycled to the GIT is influenced by several factors (Lapierre and Lobley, 2001) and can vary from 0.10 to 0.95 (Harmeyer and Martens, 1980). Various researchers, using sheep at N intakes ranging from 8.9 to 25 g/d (i.e., N intakes less than ours) observed that the GER:UER ratios ranged from 0.75 to 0.61 (Sarraseca et al., 1998; Lobley et al., 2000; Marini et al., 2004) and were negatively correlated with N intake. Another important factor influencing the GER:UER ratio appears to be blood concentrations of urea N (see Harmeyer and Martens, 1980). Recently, Sunny et al. (2007), using an intrajugular urea infusion protocol to increase blood urea N concentrations, clearly demonstrated that urea N transfer from blood to the GIT was elevated as blood urea N concentration increased. In our study, PUN concentrations (25.9 to 28.1 mg/dL) across dietary treatments were greater than reported in other studies (Lobley et al., 2000; Marini et al., 2004), so it is plausible that the greater GER:UER ratios observed, even with greater N intakes, could be attributable to the greater PUN concentrations.
The GER that was used for anabolic purposes (UUA) was unaffected by dietary treatment (Table 5). Across dietary treatments, 0.23 to 0.34 of GER was used for anabolic purposes (UUA; Table 5). A significant proportion (ranging from 0.64 to 0.76) of the GER was returned to the urea cycle (ROC; Table 5). The reasons for this observation are unclear, but it is possible that, because of the high N intakes, a limit of N utilization by ruminal microbes may already have been reached (Lobley et al., 2000). We had hypothesized that provision of additional RFC via grain processing would enhance urea N transfer to the GIT and, subsequently, its utilization for anabolic purposes. The lack of effect of grain processing suggests that energy supply did not limit utilization of the extra N provided via enhanced urea N recycling to the GIT, likely because of the high levels of concentrate fed.
Lambs fed the high dietary RDP consumed more OM compared with those fed the low dietary RDP (P = 0.006; Table 6). Because dietary OM was similar across treatments, differences in OM intake largely reflect differences in DMI that were observed due to dietary RDP level; however, OM total-tract digestibility was unaffected (P 0.10) by dietary treatment. Urinary output was unaffected (P 0.58) by dietary treatment (Table 6). Urinary excretion of allantoin, uric acid, xanthine + hypoxanthine, and total PD were unaffected (P > 0.05) by dietary treatment (Table 6), but there was a tendency (P = 0.06) for urinary allantoin excretion to be greater in lambs fed dry-rolled barley compared with those fed pelleted barley (Table 6). Microbial nonammonia N flow to the small intestine, which was estimated using urinary total PD excretion, was unaffected (P > 0.17) by dietary treatment (Table 6). Because diets were high in N, it is likely that N supply for microbial growth was not limiting.
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Footnotes |
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2 Corresponding author: tim.mutsvan{at}usask.ca
Received for publication February 6, 2007. Accepted for publication August 28, 2007.
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LITERATURE CITED |
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TopAbstractINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONLITERATURE CITED |
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