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Cyst(e)ine imbalance and its effect on methionine precursor utilization in chicks

Department of Animal Sciences and Division of Nutritional Sciences, University of Illinois at Urbana-Champaign, Urbana 61801

	Abstract

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Five 9- or 12-d chick growth bioassays were done in batteries using 2 Met-deficient diets: a purified AA-based diet containing (by analysis, as-fed) 20.3% CP, 0.12% Met, and 0.05% cyst(e)ine; and an AA-fortified corn-peanut meal diet containing (by analysis, as-fed) 19.0% CP, 0.22% Met, and 0.23% cyst(e) ine. Feed-grade DL-Met (DL-M; 99%) was compared with feed-grade DL-OH-Met, Ca (OH-M; 84%). When the purified diet was modified to contain 0.12% Met and 0.20% or greater cyst(e)ine, slope-ratio assays involving graded dosing of DL-M (0, 404, 808, and 1,212 mg of DL-M/kg) or isosulfurous levels of OH-M resulted in linear (P < 0.01) BW gain and G:F responses. Multiple linear regression analysis (BW gain vs. supplemental sulfur intake, R² = 0.98) resulted in a mean bioefficacy estimate of 78.1% for OH-M vs. DL-M (equivalent to 65.6% on a supplemental compound basis). In assay 3, the purified diet was modified to be equally deficient in Met and cyst(e)ine [i.e., 0.12% Met, 0.12% cyst(e)ine]. When this diet was supplemented with either 404 mg of DL-M/kg or 476 mg of OH-M/kg, BW gain and G:F responded (P < 0.01) markedly to either compound, and differences between DL-M and OH-M were not significant (P > 0.10). Assays 4 and 5 used the corn-peanut meal basal diet containing 0.22% total Met and 0.23% total cyst(e)ine. In both assays, addition of either 465 mg of DL-M/kg or 554 mg of OH-M/kg resulted in increased (P < 0.01) BW gain and G:F, regardless of dietary cyst(e)ine concentration. In the absence of excess cyst(e)ine, BW gain responses to DL-M and OH-M were similar, but when 0.10% excess cyst(e)ine was provided as L-cystine or feather meal, DL-M responses tended to exceed those of OH-M. Moreover, this small excess of dietary cyst(e)ine, regardless of source, depressed (P < 0.01) feed intake and BW gain when added to the basal diet. Overall, these results suggest that excess dietary cyst(e)ine, when included in Met-deficient diets, has the potential to be both anorexigenic and pernicious to OH-M utilization.

Key Words: bioefficacy • chick • cysteine • hydroxy methionine • methionine

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
A debate regarding the precise bioefficacy of Met precursor compounds has embroiled the field of nonruminant nutrition for more than 4 decades. The plethora of peer-reviewed swine and poultry data suggests that the relative bioefficacy (isosulfurous basis) of DLhydroxy methionine (OH-M) may be as low as 80% or as great as 100%, relative to DL-methionine (DL-M) under various experimental conditions (Jansman et al., 2003). Whereas emphasis has traditionally been placed on repetition of bioefficacy studies, much less research has been conducted to elucidate factors responsible for differences in bioefficacy estimates.

Without a doubt, the use of purified or chemically defined diets has been instrumental in quantifying biological responses to Met precursor compounds (Baker, 1976, 2006), partly because these diets can be made severely deficient in sulfur AA (SAA). The use of purified diets allows maximal control over dietary variables, thus facilitating the study of factors affecting biological utilization of Met precursors. We have identified dietary cyst(e)ine content, and perhaps the ratio of dietary cyst(e)ine to Met, as factors that may help to explain observed differences in bioefficacy of DL-M vs. OH-M (Dilger and Baker, 2007). Dietary cyst(e)ine concentration was chosen as a potentially confounding factor (Baker, 1976, 1986) on the basis that OH-M elicited greater growth responses when supplemented in cyst(e) ine-deficient diets than in Met-deficient diets (Katz and Baker, 1975; Christensen and Anderson, 1980; Boebel and Baker, 1982). Because virtually all corn-soybean meal-based poultry diets are supplemented with Met precursors, predominantly OH-M and DL-M, characterizing factors affecting their utilization is paramount from both an economic and a production-oriented per-spective. Thus, the primary objectives of the studies reported herein were to 1) determine the bioefficacy of OH-M relative to DL-M in support of chick growth, and 2) evaluate the impact of dietary Cys concentration on utilization of these Met precursors.

	MATERIALS AND METHODS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
General Procedures

All experimental procedures were approved by the University of Illinois Animal Care and Use Committee.

Five studies were conducted using male chicks (New Hampshire male x Columbian female) obtained from the University of Illinois Poultry Farm. Chicks were housed in thermostatically controlled starter batteries with raised-wire flooring in an environmentally controlled room with continuous lighting. From hatch to d 7 posthatch, chicks were fed a typical corn-soybean meal starter diet that provided 23% CP (as-fed) and was adequate in all dietary nutrients (NRC, 1994). After an overnight fast, chicks were weighed, wing-banded, and randomized to dietary treatments on d 8, such that the mean initial pen weights and BW distributions were similar among treatments.

The experimental basal diets (Table 1) were fed for a 9-d period (d 8 to 17 posthatch) in assays 1, 3, 4, and 5, and for a 12-d period (d 8 to 20 posthatch) in assay 2. Experimental diets and tap water were freely available to chicks at all times. Body weight of individual chicks and pen feed intakes were measured at the termination of each bioassay. Body weight gain, feed intake, and G:F were calculated for each replicate pen of chicks.

The purified basal diet contained 0.12% Met and 0.05% cyst(e)ine, making it severely deficient in SAA relative to dietary requirements of ~0.3% digestible Met and ~0.3% digestible Cys (NRC, 1994). The cornpeanut meal diet contained analyzed total concentrations of 0.22% Met and 0.23% cyst(e)ine. Other AA in the basal diets were in excess of the true digestible AA requirements of young chicks (NRC, 1994). When fully fortified with SAA, these experimental diets have been shown to allow chick growth rates similar to those obtained with a typical 23% CP corn-soybean meal diet (unpublished data).

In all instances, DL-M and OH-M were supplemented at isosulfurous levels, assuming purity values of 99% for feed-grade DL-M and 84% for feed-grade OH-M for assays 1, 2, and 3. Purity values for feed-grade DL-M were assumed to be 100% rather than 99% for assays 4 and 5 based on previous work from our laboratory (Dilger and Baker, 2007). Comparing isosulfurous doses is the most accurate and valid approach to compare DL-M and OH-M, because DL-OH-Met (Ca) contains 2 mol of DL-OH-Met/mol of Ca. Thus, it is not appropriate to compare DL-M and DL-OH-Met (Ca) on an isomolar basis. When making comparisons on an isosulfurous basis, if OH-M were 100% bioefficacious, chick growth would not be different between diets supplemented with DL-M and OH-M. In addition, Cys was supplemented as L-cystine in all instances, with the understanding that L-Cys and L-cystine are equally efficacious on a weight or concentration basis when provided as low-level supplements to cyst(e)ine-deficient diets (Graber and Baker, 1971; Baker, 2006). Supplementation of crystalline SAA was always made at the expense of cornstarch.

Assay 1 The objective of this 9-d assay was to quantify the bioefficacy of OH-M relative to DL-M based on chick growth performance by using standard slope-ratio procedures. The purified basal diet (Table 1) was supplemented with 0, 404.0, or 808.1 mg of DL-M/kg or isosulfurous levels of OH-M. Additionally, 0.15% L-cystine was added to increase the total dietary cyst(e) ine concentration to 0.20%. Growth performance was quantified by using 5 replicate pens of 4 chicks (mean initial BW, 92 g).

Assay 2 Similar to assay 1, this chick assay sought to quantify the bioefficacy of OH-M relative to DL-M over a 12-d feeding period by using standard slope-ratio procedures. The purified basal diet (Table 1) was supplemented with 0, 404.0, 808.1, or 1,212.1 mg of DL-M/ kg or isosulfurous levels of OH-M. Additionally, 0.35% L-cystine was added to increase the total dietary cyst(e) ine concentration to 0.40%. Growth performance was quantified by using 5 replicate pens of 3 chicks (mean initial BW, 107 g).

Assay 3 The objective of this 9-d bioassay was to determine the effect of a low dietary cyst(e)ine concentration on the qualitative assessment of Met precursor utilization. The purified basal diet (Table 1) was supplemented with 0.07% L-cystine, resulting in a total dietary cyst(e)ine concentration of 0.12% (equal to the analyzed concentration of total Met in the basal diet). This total cyst(e)ine concentration was low compared with concentrations used in assays 1 (0.20%) and 2 (0.40%). Additionally, DL-M (404.0 mg/kg) or an isosul-furous level of OH-M (476.2 mg/kg) was added to the basal diet. Growth performance was quantified by using 8 replicate pens of 3 chicks (mean initial BW, 100 g).

Assays 4 and 5 These 9-d chick bioassays were conducted to further elucidate the effect of dietary cyst(e)ine concentration on utilization of Met precursor compounds by using a diet based on intact protein sources. The corn-peanut meal basal diet (Table 1) contained 0.22% Met and 0.23% cyst(e)ine, and was supplemented with 465.0 mg of DL-M/kg or an isosulfurous level of OH-M (553.6 mg/kg). Purity of feed-grade DL-M was assumed to be 100% in assays 4 and 5, as described earlier. Thus, 465.0 mg of DL-M/kg was compared with 553.6 mg of OH-M/kg, assuming the latter was 84% OH-M. Additionally, the basal diet was supplemented with 0.10% bioavailable cyst(e)ine from L-cystine (assay 4) or feather meal (assay 5). Feather meal (analyzed 84.1% CP, as-fed) and synthetic sources of SAA were supplemented at the expense of cornstarch.

Assays 4 and 5 each used a 3 x 2 factorial arrangement of dietary treatments: 3 levels of added Met (unsupplemented, 465.0 mg of DL-M/kg, or 553.6 mg of OH-M/ kg), and 2 levels of added cyst(e)ine [unsupplemented and 0.10% L-cystine (assay 4) or 0.10% bioavailable cyst(e)ine provided by feather meal (assay 5)]. The concentration of bioavailable cyst(e)ine originating from feather meal (assay 5) was based on analyzed contents of cyst(e)ine plus lanthionine. In this respect, feather meal was analyzed to contain 0.51% Met, 4.50% cyst(e) ine, and 1.31% lanthionine, as-fed). Methionine originating from feather meal was assumed to be used as Met per se, without transsulfuration to Cys, because of the Met-deficient nature of the basal diet. Using an approach described by Baker et al. (1981), we assumed 48.6% Cys bioavailability in feather meal (when accounting for cyst(e)ine plus lanthionine), and calculated that 3.54% feather meal was required to supply 0.10% bioavailable cyst(e)ine.

Statistical Analysis and Calculations All data were subjected to ANOVA using the GLM procedure (SAS Inst. Inc., Cary, NC). Data were analyzed by using pen means with procedures appropriate for a completely randomized design. Data are presented as mean values with pooled SEM estimates, and significance was set at an level of 0.05. Where applicable, linear and quadratic responses were evaluated by using single df contrasts.

In assays 1 and 2, the relative bioefficacy of Met precursor compounds was evaluated by using standard slope-ratio methodology (Sasse and Baker, 1973; Littell et al., 1997). Briefly, growth performance criteria (dependent variables) were regressed on supplemental sulfur intake (independent variable) from Met precursor compounds in a multiple linear regression analysis using the GLM procedure of SAS. Relative bioefficacy was then evaluated by dividing the response slope of OH-M by the response slope obtained for the standard Met compound (DL-M) and multiplying by 100.

	RESULTS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Assay 1

Daily BW gain, daily feed intake, and G:F were improved (P < 0.001) by supplementation of either DL-M or OH-M to the Met-deficient basal diet (Table 2). Additionally, supplementation of DL-M resulted in greater responses (P < 0.001) in growth performance compared with OH-M when included in the purified basal diet containing 0.20% total cyst(e)ine. Multiple linear regression analysis using daily BW gain as the dependent variable resulted in a bioefficacy estimate of 77.5% for OH-M relative to DL-M. A similar bioefficacy estimate of 76.4% was obtained when using G:F as the dependent variable. The R² values for multiple linear regression based on daily BW gain and G:F were 0.98 and 0.96, respectively.

This assay was similar to assay 1, except that the purified basal diet contained 0.40% total cyst(e)ine. Growth performance criteria were improved (P < 0.001) by supplementation of Met precursor compounds, and addition of DL-M elicited greater (P < 0.001) growth responses than OH-M (Table 3). Consequently, an interaction (P < 0.001) between Met precursor source and level was observed for all growth criteria. Supplementation of Met precursor compounds to the Metdeficient diet containing 0.40% total cyst(e)ine elicited linear improvements (P < 0.001) in growth criteria, and quadratic effects were not detectable. Multiple linear regression analysis using daily BW gain and G:F as dependent variables resulted in bioefficacy estimates of 78.7 and 80.3%, respectively, for OH-M relative to DL-M. The R² values for multiple linear regression based on daily BW gain and G:F were 0.97 and 0.93, respectively.

Total dietary cyst(e)ine concentrations in assay 1 and 2 were 0.20 and 0.40%, respectively, which were high compared with total Met concentrations. In contrast, this assay balanced total dietary Met and cyst(e) ine concentrations in the purified basal diet. Similar to assays 1 and 2, all growth performance criteria were improved (P < 0.001) by Met precursor supplementation (Table 4). However, no differences (P > 0.44) between DL-M and OH-M were observed for growth criteria when chicks were fed the diets containing an equal deficiency of Met and cyst(e)ine.

These assays further tested the hypothesis that dietary cyst(e)ine concentration differentially affects utilization of Met precursor compounds. Overall, supplementation with Met precursor compounds improved (P < 0.001) growth performance, but there was also evidence to suggest differential responses (P < 0.05) between DL-M and OH-M (Tables 5 and 6). For instance, in the absence of supplemental cyst(e)ine, DL-M and OH-M resulted in similar improvements in daily BW gain (58 and 45% mean improvements over the un-supplemented basal diet in assays 4 and 5, respectively). However, with 0.10% excess L-cystine in assay 4, DL-M still improved daily BW gain to 18.7 g/d, whereas OH-M improved BW gain to only 16.5 g/d. Similarly, in the presence of 0.10% bioavailable cyst(e)ine provided by feather meal in assay 5, DL-M supplementation improved BW gain to 12.0 g/d, whereas OH-M improved BW gain to only 10.0 g/d.

	DISCUSSION

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For more than 40 yr (Scott et al., 1966), controversy has surrounded the issue of Met precursor utilization, with emphasis placed on comparing DL-2-amino-4-(methylthio)butyric acid (i.e., DL-M) and DL-2-hydroxy- 4-(methylthio)butyric acid (i.e., OH-M). The scientific names are intentionally used here to highlight the fact that these Met precursor compounds differ only in the chemical group attached to the -carbon. Both DL-M and OH-M are considered Met precursors because animals possess the enzymes necessary to convert these compounds into L-Met [Figure 1; cf. Gordon (1965) and Dibner and Knight (1984)]. The controversy surrounding these Met precursors stems, in part, from differences in their metabolic conversion to L-Met. Even after considerable research, an explanation for the variability in bioefficacy estimates obtained among independent laboratories has remained elusive. Thus, it is imperative that factors affecting the absorption and metabolism of DL-M and OH-M be identified.

View larger version (21K): [in this window] [in a new window]   Figure 1. Metabolic pathways of Met precursor compounds. Enzyme names are as follows: A) D-amino acid oxidase (EC 1.4.3.3); B) L--hydroxy acid oxidase (EC 1.1.3.15); C) D-2-hydroxy acid dehydrogenase (EC 1.1.99.6); D) general transaminase (e.g., EC 2.6.1.5 or EC 2.6.1.57).

Data from assays 1 and 2 suggested that OH-M bio-efficacy was 78.1% (ranging from 76 to 81%) relative to DL-M when supplemented on an isosulfurous basis. When accounting for the moisture and impurities associated with the OH-M product used herein (assuming 84% bioactivity), OH-M relative bioefficacy averaged 65.6% on a compound basis. These estimates are slightly greater than recently reported values (Jansman et al., 2003); regardless, we provide evidence that OH-M bioefficacy is different from 100% relative to DL-M when basal diets contain excess cyst(e)ine relative to a Met deficiency.

The primary difference between assays 1 and 2 was the total dietary cyst(e)ine concentrations of the Met-deficient basal diet, yet 0.40% of total dietary cyst(e)ine resulted in the same bio-efficacy estimates as when the diet contained 0.20% total cyst(e)ine. In addition, it is especially intriguing that chick BW gain was decreased over a 12-d period with 0.40% total dietary cyst(e)ine (assay 2) compared with BW gain over a 9-d period with 0.20% total dietary cyst(e)ine (assay 1). Thus, it may be inferred from these data that excess dietary cyst(e)ine, or differentially expressed as a high dietary cyst(e)ine:Met ratio, is not only detrimental to chick growth (Dilger and Baker, 2007), but may also reduce utilization of OH-M in young chicks.

On realizing the potentially detrimental effect of dietary cyst(e)ine concentration on OH-M utilization, we designed assay 3 to investigate OH-M bioefficacy by using a purified basal diet that was equally deficient in Met and cyst(e)ine (0.12% of each). Data from this bio-assay clearly showed that DL-M and OH-M supported chick growth equally well, and there was no evidence to suggest a difference in efficacy when these compounds were supplemented on an isosulfurous basis. Thus, in our 2 concluding assays, we tested the effects of supplemental cyst(e)ine concentration and cyst(e) ine source on the bioefficacy of OH-M relative to DL-M. It was again evident that DL-M and OH-M supported chick growth equally well when added to the Met- and cyst(e)ine-deficient corn-peanut meal diet. Thus, on the basis of supplemental dietary cyst(e)ine concentration alone, we provide evidence to suggest that utilization of OH-M may be negatively affected in young chicks. Whether this effect results from detriments in absorption or metabolic conversion is yet to be determined.

In addition to cyst(e)ine concentration, cyst(e)ine source may have an impact on Met precursor utilization in young chicks. Feather meal was chosen as an intact protein source of cyst(e)ine because of its unique nutritional profile and relatively common use in the poultry industry. Far exceeding other protein-furnishing ingredients, feather meal typically contains as much as 10 times more total cyst(e)ine than Met (Liu et al., 1989; Han and Parsons, 1990; NRC, 1994; Wang and Parsons, 1997). As a result of this poor SAA pattern (i.e., poor protein quality), it is generally accepted that inclusion of feather meal should be limited to no more than 5% in a practical corn-soybean meal diet fed to broiler chickens (Baker et al., 1981). However, even lower feather meal inclusion rates may be necessary under certain dietary circumstances, as evidenced by the data in Table 6. In this respect, excess dietary cyst(e) ine, abnormally high dietary cyst(e)ine:Met ratios, or both may lead to nutritional imbalances (Featherston and Rogler, 1978; Sell et al., 1980; Dilger and Baker, 2007) or direct toxic effects in young chicks (Dilger et al., 2007). In our study, we used 3.54% feather meal to supply 0.10% bioavailable cyst(e)ine [i.e., when accounting for Cys, cystine, and lanthionine (Baker et al., 1981)].

Although not statistically significant, the interaction between cyst(e)ine supplementation and Met source in assays 4 and 5 was intriguing (Tables 5 and 6). Chick BW gain caused by supplemental DL-M was unaffected by addition of L-cystine, whereas excess cyst(e)ine provided by feather meal reduced the benefit of DL-M by 17%. However, the benefit of supplemental OH-M was reduced in the presence of either L-cystine (9%) or feather meal (31%). Additionally, whereas L-cystine reduced feed intake by 15% in diets containing no supplemental Met, feather meal caused a reduction of 27% in feed intake. This reinforces the concept that either a high cyst(e)ine:Met ratio or excess dietary cyst(e)ine per se have profound negative effects on voluntary feed intake (Dilger and Baker, 2007). The observation that 3.54% feather meal appeared to have a greater impact on growth performance than L-cystine may have resulted from 1) underestimation of the amount of bioavailable cyst(e)ine provided by feather meal, or 2) undetermined factors present in feather meal that may affect Met-precursor utilization. Although speculative, we cannot eliminate the possibility that either a specific cyst(e)ine-related compound (e.g., lanthionine) or the abnormal cyst(e)ine:Met ratio present in feather meal were to blame. More research is necessary to elucidate these, and other, factors that may affect utilization of Met-precursor compounds when included in practical Met-deficient diets.

Elucidating the link between excess cyst(e)ine and reduced OH-M utilization is difficult. It is tempting to speculate that either L--hydroxy acid oxidase or D-2-hydroxy acid dehydrogenase, or both (Figure 1), are directly affected by dietary cyst(e)ine concentration, but we are unable to find supporting evidence for this in the literature. Alternatively, under conditions of excess cyst(e)ine and deficient Met, OH-M may be less efficient than DL-M in allowing Cys to be utilized (along with Met) for protein synthesis. On the other hand, when dietary cyst(e)ine relative to Met is either more deficient or equally deficient, OH-M appears to be effectively converted to L-Met and subsequently converted via transsulfuration to L-Cys. Regardless of the underlying mechanism, OH-M is an important Met precursor compound, and studies investigating the effects of cyst(e)ine on these OH-M-related enzymes are warranted.

Our results showing that excess dietary cyst(e)ine may be detrimental to OH-M utilization in young chicks may also extend to swine. Although anecdotal, recent swine bioefficacy studies suggest that variability in dietary cyst(e)ine concentrations may affect OH-M efficacy. Using N-balance and an SAA-deficient practical diet containing 0.21% total Met and 0.40% total cyst(e) ine, Kim et al. (2006) reported OH-M bioefficacy of 64% relative to DL-M when compared on a compound basis. However, Yi et al. (2006) used growth performance of pigs fed a basal diet with 0.24% Met and 0.26% cyst(e) ine and reported OH-M bioefficacy of 111% relative to DL-M when compared on a compound basis. In the work of Kim et al. (2006), both DL-M and OH-M would have been used to supply only Met, but in the work of Yi et al. (2006), both Met precursor compounds would have been used to supply not only Met but also Cys. Thus, it appears from cross-species data that the dietary cyst(e) ine concentration of experimental diets may aid in explaining differences in bioefficacy estimates of Met precursor compounds. Additional research is clearly needed to characterize this potentially significant effect.

In conclusion, we provide evidence that the bioefficacy of OH-M is approximately 78% relative to DL-M when compared on an isosulfurous basis, or 66% when compared on a compound basis, in young chicks fed purified diets singly deficient in Met and containing excess cyst(e)ine. However, we were unable to detect meaningful differences between OH-M and DL-M in terms of growth performance when either the purified or practical basal diet was made equally deficient in Met and cyst(e)ine. Moreover, addition of 0.10% excess bioavailable cyst(e)ine from either L-cystine or feather meal reduced the beneficial effect of supplemental OH-M to a greater extent than for DL-M. Thus, our data suggest that OH-M utilization is more sensitive than DL-M to dietary cyst(e)ine concentration, even though OH-M and DL-M share a common transamination path-way beyond the initial stereospecific conversion of D- Met and D- and L-OH-Met to the keto analog of Met.

¹ Corresponding author: rdilger2{at}uiuc.edu

Received for publication November 6, 2007. Accepted for publication March 28, 2008.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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