Estimation of Bioavailability of DL-Methionine Hydroxy Analogue Relative to DL-Methionine in Layers with Exponential and Slope-Ratio Models
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1 Estimation of Bioavailability of DL-Methionine Hydroxy Analogue Relative to DL-Methionine in Layers with Exponential and Slope-Ratio Models Z. Liu,* A. Bateman,* M. Bryant,* A. Abebe, and D. Roland*,1 *Department of Poultry Science and Department of Statistics, Auburn University, Auburn, Alabama ABSTRACT An experiment was conducted using molted hens to estimate the bioavailability of DL-methionine hydroxy analogue-free acid (MHA-FA) relative to DL-methionine (DLM). In this experiment, 5 supplemental levels (0.012, 0.024, 0.036, 0.048, and 0.060%) of DLM or equimolar concentrations of MHA-FA were added to a basal diet containing 14.97% protein and 0.27% methionine. The low protein diet was used to increase the sensitivity of laying hens to methionine deficiency. Feed consumption, egg production, egg mass, and egg weight increased (P < 0.05), and feed conversion decreased (P < 0.05) when DLM or MHA-FA was added to the basal diet for some supplemental methionine levels. There was no difference (P > 0.05) in feed consumption between hens fed DLM and hens fed MHA-FA. Regression analysis showed that the bioavailability of MHA-FA relative to DLM on a molar basis was 88.7% (egg production), 88.0% (egg mass), and 84.6% (egg weight) with the exponential model, and was 89.7% (egg production), 89.6% (egg mass), and 86.8% (egg weight) with the slope-ratio model. The average bioavailability of MHA-FA relative to DLM was 88% on a molar basis. (Key words: bioavailability, DL-methionine, layer, methionine hydroxy analogue, regression model) 2004 Poultry Science 83: INTRODUCTION Methionine is generally the first limiting amino acid in commercial laying hen diets, and is commonly supplemented as 2 sources, dry DL-methionine (DLM) or liquid DL-methionine hydroxy analogue-free acid (MHA-FA). Knowledge about the relative bioavailability of these 2 sources is necessary for successful poultry production. Currently, there is limited information regarding the use of laying hens to determine relative bioavailability, and some of the results were inconsistent due to large variation in hens performances (Reid et al., 1982; Van Weerden and Schutte, 1984; Scott, 1987; Harms and Russell, 1994; Danner and Bessei, 2002). Therefore, there are still ongoing discussions about the bioavailability of MHA-FA relative to DLM in laying hens. The objective of this experiment was to determine the bioavailability of MHA-FA relative to DLM with exponential and slope-ratio models, which are appropriate statistical methods according to Littell et al. (1997) Poultry Science Association, Inc. Received for publication December 9, Accepted for publication April 4, To whom correspondence should be addressed: roland1@ auburn.edu. MATERIALS AND METHODS The basal diet used in the 2 experiments was formulated to meet nutrient requirements for Hy-Line Variety W-36 (Anonymous, 2000), with the exception of total protein and amino acid content (Table 1). The ME content for the basal diet was 2,863 kcal/kg. Five supplemental levels of methionine (0.012, 0.024, 0.036, 0.048, and 0.060%) were added to the basal diet, and the diets were fed for 12 wk. Equimolar amounts of DLM (99.7%) and MHA-FA (88%) were added to diets for comparison. The experimental design is shown in Table 2. To ensure the diets were properly mixed, feed samples were chemically analyzed (AOAC, 1990) and, except for the feed sample of the treatment with % added MHA-FA, the results (Table 3) indicated that the experiment was based on graded supplemental levels of DLM and MHA- FA as expected. In this experiment, 1,760 Hy-Line W-36 hens (the first phase of the second cycle, 69 wk old) were randomly allocated into 440 cages ( cm) with 4 birds per cage. Five adjoining cages consisted of a group, and the resulting 88 groups were randomly assigned to 11 dietary treatments. Replicates were equally distributed into upper and lower cage levels to minimize the effect of cage level. All hens were housed in a house with controlled temperature (day and night temperatures at Abbreviation Key: DLM = DL-methionine; MHA-FA = DL-methionine hydroxy analogue-free acid. 1580
2 BIOAVAILABILITY OF METHIONINE SOURCES 1581 TABLE 1. Composition and calculated analysis of experimental basal diet Ingredient (%) Corn (CP, 8%) Soybean meal (CP, 48%) Limestone 7.07 Hard shell 2.00 Dicalcium phosphate 1.66 Poultry oil 0.97 NaCl 0.42 Vitamin premix Mineral premix Calculated analysis CP, % ME, kcal/kg 2,863 Total phosphorus, % 0.59 Available phosphorus, % 0.40 Ca, % 4.00 Na, % 0.18 Methionine, % 0.27 Methionine + cysteine, % 0.51 Lysine, % 0.75 Tryptophan, % Provided per kilogram of diet: vitamin A (retinyl acetate), 8,000 IU; cholecalciferol, 2,200 ICU; vitamin E (DL-α-tocopheryl acetate), 8 IU; vitamin B 12, 0.02 mg; riboflavin, 5.5 mg; D-calcium pantothenic acid, 13 mg; niacin, 36 mg; choline, 50 mg; folic acid, 0.5 mg; vitamin B 1 (thiamin mononitrate), 1 mg; pyridoxine, 2.2 mg; D-biotin, 0.05 mg; vitamin K (menadione sodium bisulfate complex), 2 mg. 2 Provided per kilogram of diet: manganous oxide, 65 mg; iodine (ethylene diamine dihydriodide), 1 mg; ferrous carbonate, 55 mg; copper oxide, 6 mg; zinc oxide, 55 mg; sodium selenite, 0.3 mg. approximately 30 and 18 C, respectively), ventilation, and lighting (16L:8D), but without controlled relative humidity. All birds had ad libitum access to feed and water. Egg production was recorded daily, feed consumption and egg weight were recorded weekly, and egg specific gravity was recorded monthly. Egg weight and egg specific gravity were measured using all eggs produced during 2 consecutive days. Egg specific gravity was determined by the flotation method as described by Holder and Bradford (1979). Mortality was recorded daily and feed consumption was calculated accordingly. Body weight was obtained by weighing 4 birds per replicate at the end of the experiment. Egg mass and feed TABLE 2. Experimental design Met + Met + Addition Cys Cys/Lys of Met source Met source (%) ratio (%) Basal DLM DLM DLM DLM DLM MHA-FA MHA-FA MHA-FA MHA-FA MHA-FA DLM = DL-methionine (calculated as 99.7%). 2 MHA-FA = DL-methionine hydroxy analogue-free acid (calculated as 88%). conversion were calculated from egg production, egg weight, and feed consumption. Data were analyzed using the GLM procedure of SAS/STAT (SAS Institute, 2000) to determine if a methionine level effect existed. The means were separated with Fisher LSD methods. Exponential analysis was used with the nonlinear procedure (PROC NLIN) in SAS/STAT software for the dependent variables (feed consumption, egg production, egg mass, and egg weight) to determine the bioavailability of MHA-FA relative to DLM. The statistical model was: Y=a+b (1 e (c x 1 +d x 2 ) )+e where y = response (feed consumption, egg production, egg mass, egg weight, or feed conversion), a = intercept (the minimum performance), b = asymptotic response, a + b = common asymptote (the maximum performance), c = steepness coefficient for DLM, d = the steepness coefficient for MHA-FA, and e = the random error. According to Littell et al. (1997), the bioavailability of MHA-FA compared with DLM was given by d/c, the ratio of regression coefficients. To determine the bioavailability of MHA-FA relative to DLM, slope-ratio analysis was also used with the GLM procedure in SAS/ STAT software. The statistical model was: y=a+b x 1 +c x 2 +e where y = response (feed consumption, egg production, egg mass, egg weight, or feed conversion), a = intercept (the minimum performance), b = slope for DLM, c = slope for MHA-FA, and e = the random error. The bioavailability of MHA-FA compared with DLM was given by c/b, the ratio of regression coefficients. RESULTS In this experiment, total mortality was 1.82% (32 of 1,760 hens) during the 84-d experimental period. Mortality was not affected (P > 0.05) by treatment (data not shown). Feed Consumption Feed consumption increased in response to the 5 supplemental methionine levels. The lowest feed consumption was 68.2 g/hen per d at zero supplemental methionine level, and the highest feed consumption was 76.8 g/hen per d for DLM, and 79.4 g/hen per d for MHA-FA at 0.060% supplemental methionine level (Table 4). The asymptotic response was 14.3 g, demonstrating an improvement of 20.9% in feed consumption (Figure 1). The slope-ratio model showed that with every 0.01% of methionine supplementation, there were improvements in feed consumption of 1.54 g for DLM and 1.53 g for MHA-FA. There was no difference (P > 0.05) in feed consumption of hens fed DLM compared with those fed MHA-FA.
3 1582 LIU ET AL. TABLE 3. Chemical analysis of feed samples Content of Content of Met Met+Cys additional additional DLM 3 MHA-FA 4 Treatment Content 1 AA in CP 2 Content AA in CP (%) (%) Basal < % DLM % DLM % DLM % DLM % DLM % MHA-FA <0.01 < % MHA-FA < % MHA-FA < % MHA-FA < % MHA-FA < Amino acids were expressed as a percentage of diet and the figures were standardized to a DM content of 88%. 2 Amino acids were expressed as a percentage of dietary CP. 3 DLM = DL-methionine. 4 MHA-FA = DL-methionine hydroxy analogue-free acid. 5 The feed sample for this treatment may have been incorrectly taken or analyzed. This sample should have no added synthetic methionine, but should have methionine hydroxy analogue-free acid. Egg Production Egg production responded positively to the 5 supplemental methionine levels. Egg production at the zero supplemental methionine level was 50.0%. The highest egg production was 61.1% at the 0.048% supplemental level for DLM and 61.7% at the 0.060% supplemental level for MHA-FA (Table 4). The exponential model showed that the asymptotic response was 20.5%, indicating an improvement of 41.3% (Figure 2). The sloperatio model showed that with every 0.01% of methionine supplementation, there was an improvement in egg production of 1.93% with DLM and 1.73% with MHA-FA. Analysis based on egg production indicated the bioavailability of MHA-FA compared with DLM was 88.7% or 89.7% with the exponential model or with slope-ratio model, respectively, on a molar basis. Egg Mass An improvement in egg mass by the supplemental methionine was obtained (Table 4). Egg mass at the zero supplemental methionine level was g. The highest egg mass was g at the 0.048% supplemental level for DLM and g at the 0.060% supplemental level for MHA-FA. The exponential model showed that the asymptotic response was g, demonstrating an improvement of 71.3% (Figure 3). The slope-ratio model showed that with every 0.01% of methionine supplementation, there was an improvement in egg mass of 1.50 g with DLM and 1.34 g with MHA-FA. Analysis based on egg mass indicated the bioavailability of MHA- FA relative to DLM was 88.0% or 89.6% with the exponential or slope-ratio model, respectively, on a molar basis. TABLE 4. Feed consumption, egg production, egg mass, and egg weight of laying hens fed graded levels of DLM and MHA-FA Feed Egg Egg Egg Added level consumption production mass weight Source (%) (g) (%) (g) (g) Basal ± 2.0 d 50.0 ± 2.0 e ± 1.12 f ± 0.40 e DLM ± 1.2 cd 51.0 ± 1.6 de ± 0.96 ef ± 0.29 d DLM ± 2.1 cd 54.8 ± 1.7 cd ± 0.90 de ± 0.25 cd DLM ± 2.2 a 59.9 ± 1.9 ab ± 1.25 abc ± 0.28 ab DLM ± 1.4 a 61.1 ± 2.0 a ± 1.05 ab ± 0.37 a DLM ± 1.2 ab 60.9 ± 1.0 ab ± 0.79 ab ± 0.55 a MHA-FA ± 0.9 cd 54.9 ± 1.6 cd ± 0.90 de ± 0.16 de MHA-FA ± 1.7 bcd 54.9 ± 0.8 cd ± 0.60 de ± 0.52 d MHA-FA ± 0.6 abc 58.7 ± 1.2 abc ± 0.67 bc ± 0.34 b MHA-FA ± 1.2 abc 56.6 ± 0.6 bc ± 0.27 cd ± 0.38 bc MHA-FA ± 1.4 a 61.7 ± 1.2 a ± 0.81 a ± 0.47 a a e Mean ± SEM in a column without a common superscript differ significantly (P < 0.05). 1 DLM = DL-methionine. 2 MHA-FA = DL-methionine hydroxy analogue-free acid.
4 BIOAVAILABILITY OF METHIONINE SOURCES 1583 FIGURE 1. Influence of methionine source on feed consumption. Panel A: exponential model; panel B: slope-ratio model. Values in brackets indicate the 95% confidence interval. DLM = DL-methionine; MHA- FA = DL-methionine hydroxy analogue-free acid. FIGURE 2. Bioavailability of MHA-FA compared to DLM based on egg production. A: Exponential model, B: Slope-ratio model. Values in brackets indicate the 95% confidence interval. DLM = DL-methionine; MHA-FA = DL-methionine hydroxy analogue-free acid. Egg Weight Egg weight responded positively to the 5 supplemental methionine levels (Table 4). Egg weight of the hens fed the basal diet was g. The highest egg weight was g at the 0.048% supplemental level for DLM, and g at the 0.060% supplemental level for MHA- FA. The exponential model showed that the asymptotic response was g, indicating an improvement of 21.5% (Figure 4). The slope-ratio model showed that with every 0.01% of methionine supplementation, there was an improvement in egg weight of 0.65 g with DLM and 0.57 g with MHA-FA. Analysis based on egg weight indicated the bioavailability of MHA-FA relative to DLM was 84.6% or 86.8% with the exponential or sloperatio model, respectively, on a molar basis. Feed Conversion Feed conversion (grams of feed/grams of egg) also responded positively to the 5 supplemental methionine levels (Table 5). Feed conversion at the zero supplemental methionine level was The lowest feed conversions for DLM and MHA-FA were 2.50 and 2.61, respectively, at the 0.060% supplemental level. However, more variation was observed in feed conversion. When an attempt was made to analyze the data with the exponential model, the regression did not converge, so a bioavailability value based on feed conversion was not obtainable. Body weight and egg specific gravity were also recorded (Table 5), There was a positive improvement on BW by supplementing methionine, except for the highest supplemental methionine level for both DLM and MHA-FA. There was also a decrease in egg specific gravity after the first supplemental methionine level. The decrease in egg specific gravity that occurred as the supplemental methionine level increased was due to the increase in egg weight. When the exponential and sloperatio models were applied to the data, the regression curve and line could not be well fit, so the bioavailability values based on these 2 criteria were not obtainable. DISCUSSION Inconsistent conclusions regarding the bioavailability of MHA-FA relative to DLM were reported in previous studies conducted using laying hens. The inconsistent response could be due to low sensitivity, large variation, and different statistical methods (Reid et al., 1982; Van Weerden and Schutte, 1984; Scott, 1987; Harms and Russell, 1994; Danner and Bessei, 2002). In this research, molted birds and diets with a low protein level were used to increase sensitivity to methionine supplementation, as low protein diets are more deficient in methionine than high protein diets. More birds per treatment
5 1584 LIU ET AL. FIGURE 3. Bioavailability of MHA-FA compared to DLM based on egg mass. A: Exponential model, B: Slope-ratio model. Values in brackets indicate the 95% confidence interval. DLM = DL-methionine; MHA-FA = DLmethionine hydroxy analogue-free acid. FIGURE 4. Bioavailability of MHA-FA compared to DLM based on egg weight. A: Exponential model, B: Slope-ratio model. Values in brackets indicate the 95% confidence interval. DLM = DL-methionine; MHA-FA = DL-methionine hydroxy analogue-free acid. were used compared with previous studies to decrease variation of performances. There were also relatively small standard errors for most of the criteria compared with previous studies in laying hens, indicating that this trial was well conducted with a corn-soybean meal diet. According to our previous experiments (Bateman et al., 2003; Liu et al., 2003), it was difficult to detect differences between DLM and MHA-FA from simple comparisons at a certain supplemental methionine level. Because we could not detect differences between 2 methionine levels, which should be much greater than any potential difference between DLM and MHA-FA, any potential difference due to methionine sources could not be detected. Therefore, other statistical methods are more appropriate for the data analysis than just simple comparisons at a fixed supplemental methionine level. Littell et al. (1997) summarized the exponential and slope-ratio models for estimation of comparative bioavailability of nutrients. These models have been used by nutritionists for evaluating the bioavailability of nutrients, such as methionine (Thomas et al., 1991; Huyghebaert, 1993), phosphorus (Potter et al., 1995; Fernandes et al., 1999), and copper (Guo et al., 2001). These models are based on dose-response trials with several test substance levels. The bioavailability is estimated from the slope values and therefore the biased estimate at any given supplemental level is minimized. Data in this experiment were analyzed by exponential and slope-ratio models. The equimolar bioavailability values (88.7, 88.0, and 84.6% for egg production, egg mass, and egg weight, respectively) from the exponential model were slightly lower than the values (89.7, 89.6, and 86.8% for egg production, egg mass, and egg weight, respectively) from the slope-ratio model. There were no differences (P > 0.05) among these bioavailability values. When the goodness of fit for the 2 models was determined, the exponential model had slightly smaller standard errors than the slope-ratio model, indicating that the exponential model was fitted a little better. The R 2 values based on the exponential model (0.63 for egg production, 0.74 for egg mass, and 0.74 for egg weight) were also slightly greater than those based on the sloperatio model (0.62 for egg production, 0.73 for egg mass, and 0.74 for egg weight), indicating that exponential models were a little better than slope-ratio models. However, neither model was fitted well for feed conversion. This was in agreement with our previous study (Bateman et al., 2003; Liu et al. 2003), which showed there was a larger variation for feed conversion than for egg production, egg mass, and egg weight. Based on a 95% confidence interval, the bioavailability of MHA-FA was not shown to be significantly greater than 74% or less than 100% on a molar basis. Using confidence intervals of 80 or 90%, the results indicated that the bioavailability was significantly greater than 74% or less than 100% with some of the criteria. This result was in agreement with the previous studies (Reid et al., 1982; Van Weerden and Schutte, 1984; Scott, 1987; Harms and Russell, 1994; Danner and Bessei, 2002). The
6 BIOAVAILABILITY OF METHIONINE SOURCES 1585 TABLE 5. Feed conversion, body weight and egg specific gravity of laying hens fed graded levels of DLM and MHA-FA Added level Feed conversion Body weight Egg specific Product (%) (g/g) (kg) gravity Basal ± 0.16 a 1.35 ± 0.03 c ± a DLM ± 0.05 b 1.42 ± 0.04 abc ± a DLM ± 0.04 bcd 1.47 ± 0.04 ab ± a DLM ± 0.06 d 1.48 ± 0.02 ab ± abc DLM ± 0.05 d 1.48 ± 0.01 ab ± c DLM ± 0.02 d 1.39 ± 0.04 abc ± bc MHA-FA ± 0.09 cd 1.35 ± 0.03 c ± a MHA-FA ± 0.04 bc 1.38 ± 0.03 bc ± a MHA-FA ± 0.15 cd 1.40 ± 0.01 abc ± abc MHA-FA ± 0.15 bc 1.44 ± 0.03 abc ± abc MHA-FA ± 0.09 cd 1.41 ± 0.06 abc ± bc a d Mean ± SEM in a column without a common superscript differ significantly (P < 0.05). 1 DLM = DL-methionine. 2 MHA-FA = DL-methionine hydroxy analogue-free acid. average relative bioavailability of MHA-FA compared with DLM reported in those studies was 88% on a molar basis without the extreme large and small values. Our results showed that the bioavailability of MHA- FA relative to DLM on laying hens is 88% on a molar basis. There are few, if any, studies with laying hens concerning the mechanism of the digestion, absorption, and conversion of DLM and MHA-FA, but some research had been done with broilers. Some researchers (Lingens and Molnar, 1996; Maenz and Engele-Schaan, 1996a,b; Drew et al., 2003) reported that there was a lower absorption of MHA-FA than DLM. In addition, some studies (Saunderson, 1991; Van Weerden et al., 1992) provided evidence that oligomers of MHA-FA were absorbed less efficiently. In contrast, Knight and Dibner (1986) reported that the chick absorbed different methionine sources by different mechanisms but at similar rates. Likewise, Han et al. (1990) concluded that there was no difference between DLM and MHA-FA in true digestibility, and that the bioavailability difference was related to in vivo conversion. Gordon and Sizer (1965) reported that to use MHA-FA, an animal must convert it to a keto-acid first, and then transaminate the ketoacid to methionine. The exact metabolic processes that result in the bioavailability difference between DLM and MHA-FA remain unclear. REFERENCES AOAC Official Methods of Analysis. 15th ed. Association of Official Analytical Chemists, Washington, DC. Bateman, A., Z. Liu, M. M. Bryant, and D. A. Roland, Sr Relative bioefficacy of methionine hydroxy analog compared to DL-methionine. Southern Poultry Science Society (SPSS) Annual Meeting, Atlanta, GA. (Abstr.) Danner, E. E., and W. Bessei Effectiveness of liquid DLmethionine hydroxy analogue-free acid (DL-MHA-FA-FA) compared to DL-methionine on performance of laying hens. Arch. Gefluegelkd. 66: Drew, M. D., A. A. Van Kessel, and D. D. Maenz Absorption of methionine and 2-hydroxy-4-methylthiobutanoic acid in conventional and germ-free chickens. Poult. Sci. 82: Fernandes, J. I. M., F. R. Lima, C. X. Mendonca, Jr., I. Mabe, R. Albuquerque, and P. M. Leal Relative bioavailability of phosphorus in feed and agricultural phosphates for poultry. Poult. Sci. 78: Gordon, R. S., and I. W. Sizer Conversion of methionine hydroxy analogue to methionine in the chicks. Poult. Sci. 44: Guo, R., P. R. Henry, R. A. Holweda, J. Cao, R. C. Littell, R. D. Miles, and C. B. Ammerman Chemical characteristics and relative bioavailability of supplemental organic copper sources for poultry. J. Anim. Sci. 79: Han, Y., F. Castanon, C. M. Parsons, and D. M. Baker Absorption and bioavailability of DL-methionine hydroxy analog compared to DL-methionine. Poult. Sci. 69: Harms, R. H., and G. B. Russell A comparison of the bioavailability of DL-methionine and methionine hydroxy analogue acid for the commercial laying hen. J. Appl. Poult. Res. 3:1 6. Holder, D. P., and M. V. Bradford Relationship of specific gravity of chicken eggs to number of cracked eggs and percent shell. Poult. Sci. 58: Huyghebaert, G Comparison of DL-methionine and methionine hydroxy analogue-free acid in broilers by using multi-exponential regression models. Br. Poult. Sci. 34: Hy-Line International Hy-Line Variety W-36 Commercial Management Guide Hy-Line International, West Des Moines, IA. Knight, C. D., and J. J. Dibner Comparative absorption of 2-hydroxy-4-(methylthio)butanoic acid and L-methionine in the broiler chick. J. Nutr. 114: Lingens, G., and S. Molnar Studies on metabolism of broilers by using 14C-labelled DL-methionine and DL-methionine hydroxy analog Ca-salt. Arch. Anim. Nutr. 49: Littell, R. C., P. R. Henry, A. J. Lewis, and C. B. Ammerman Estimation of relative bioavailability of nutrients using SAS procedures. J. Anim. Sci. 75: Liu, Z., A. Bateman, M. M. Bryant, and D. A. Roland, Sr Response comparison of DL-methionine and methionine hydroxy analogue with milo-soybean diet using different regression models. Southern Poultry Science Society Annual Meeting (SPSS), Atlanta, GA. (Abstr.) Maenz, D. D., and C. M. Engele-Schaan. 1996a. Methionine and 2-hydroxy-4-methylthiobutanoic acid are transported by distinct Na+-dependent and H+-dependent systems in the brush border membrane of the chick intestinal epithelium. J. Nutr. 126:
7 1586 LIU ET AL. Maenz, D. D., and C. M. Engele-Schaan. 1996b. Methionine and 2-hydroxy-4-methylthiobutanoic acid are partially converted to nonabsorbed compounds during passage through the small intestine and heat exposure does not affect small intestinal absorption of methionine sources in broiler chicks. J. Nutr. 126: Potter, L. M., M. Potchanakorn, V. Ravindran, and E. T. Kornegay Bioavailability of phosphorus in various phosphate sources using body weight and toe ash as response criteria. Poult. Sci. 74: Reid, B. L., A. Madrid, and R. M. Maiodrino Relative biopotency of three methionine sources for laying hens. Poult. Sci. 61: SAS Institute SAS/STAT User s Guide. SAS Institute Inc., Cary, NC. Saunderson, C. L Metabolism of methionine and its nutritional analogs. Poult. Int. 30: Scott, M. L Studies on the comparative utilization of synthetic sources of methionine activity in laying pullets. Nutr. Rep. Int. 36: Thomas, O. P., C. Tamplin, S. D. Crissey, E. Bossard, and A. Zuckerman An evaluation of methionine hydroxy analog free acid using a nonlinear (exponential) bioassay. Poult. Sci. 70: Van Weerden, E. J., and J. B. Schutte Comparison of DL-methionine, DL-methionine-Na, DL-methionine hydroxy analogue-ca, and DL-methionine hydroxy analoguefree acid with layers. Poult. Sci. 63: Van Weerden, E. J., J. B. Schutte, and H. L. Bertram Utilization of the polymers of methionine hydroxy analog free acid (MHA-FA-FA) in broiler chicks. Arch. Gefluegelkd. 56:63 68.
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