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Maastricht University, Department of Surgery, Nutrition and Toxicology Research Institute Maastricht (NUTRIM), 6200 MD Maastricht, The Netherlands
3To whom correspondence should be addressed. E-mail: nep.deutz{at}ah.unimaas.nl.
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • dietary protein • stable isotopes • urea • protein turnover • protein quality
In response to food intake, metabolism changes from a catabolic to an anabolic state due to inhibition of protein breakdown and increased net protein synthesis (1). A large part of this protein gain accumulates in the gut and is referred to as the labile protein pool (2). This pool provides essential amino acids to the body’s free amino acid pool during the postabsorptive phase when protein in this pool is in turn broken down (3,4).
Both the amount and the quality of protein in the diet are important in determining the magnitude of change in protein metabolism with food intake. With an increasing protein content in the diet and increased plasma amino acid levels, whole-body endogenous protein breakdown is more markedly inhibited and protein synthesis is stimulated, although the latter occurs to a lesser extent and is dependent on the amount of protein ingested (5–8). Moreover, the nutritional value of dietary protein is related to both the bioavailability of ingested nitrogen and amino acids and the efficiency of their metabolic utilization to meet nitrogen and amino acid requirements for growth and renewal of body proteins (9–13). Protein digestibility and naturally occurring growth-depressing or antinutritional factors in proteins affect both the bioavailability of nitrogen and amino acids (14,15), and postprandial protein kinetics (16). Moreover, metabolic utilization depends on the composition of the meal with respect to the presence or absence of (in)dispensable essential amino acids and carbohydrates in the meal (1,17–19). For example, an isoleucine-deficient blood meal or a protein meal without carbohydrates reduces gut protein synthesis and increases liver urea production (17,18).
Compared with casein, soy protein is deficient in the essential amino acids methionine and lysine and contains less BCAA. Moreover, the bioavailability of soy protein is further impaired by the presence of endogenous inhibitors of digestive enzymes (e.g., trypsin inhibitors), and the poor digestibility of raw soybean [see (20) for review]. An oro-ileal digestibility for soy protein isolate of 91% was reported in the literature (21); this is slightly lower than the 95% found for milk protein concentrate (22).
Recently, we observed in pigs that liver urea production and net production of essential amino acids by the portal drained viscera were higher with soy than with casein protein. To assess these production rates, stable isotopes of urea, phenylalanine, and valine were used in a multicatheterized pig model (23). The design of this pig study, however, is not applicable in humans, and a different methodology to study the splanchnic area is therefore required. In humans, whole-body retention of dietary nitrogen was lower with soy (24), which was associated with more rapid intestinal absorption of dietary nitrogen from soy, increased transfer to urea, and reduced uptake by the peripheral area. In addition, net postprandial protein utilization, calculated from the true ileal digestibility of nitrogen and the true percentage of ingested nitrogen retained in the organism, was reported to be 78% for soy protein and 85% for milk protein (21,22), with the latter containing casein (
80%) and whey proteins.
The present study, which involved studying metabolic variables as measures of the nutritional value of dietary proteins in humans, was designed to test the hypothesis that the quality of the ingested protein affects whole-body and splanchnic protein metabolism. Stable isotope techniques were used to compare whole-body protein kinetics and urea production rates of casein and soy protein meals. The double-labeled infusion technique (25,26) was used to test differences between casein and soy on the splanchnic level with respect to leucine extraction and protein synthesis.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1200 mL enteral nutrition (based on a 75-kg subject) was supplied during the study. The test meals were adjusted with mineral salts to balance the mineral differences in the protein sources. The test meals supplied 8.3 mg N/(kg BW · h) and 140 mg maltodextrin/(kg BW · h), resulting in 2016 kJ (480 kcal)/(kg BW · 8 h) and 0.42 g protein/(kg BW · 8 h) (26 En% protein) for a 75-kg person. Protein content of the meals is based on the daily protein requirement of 0.83 g protein/kg BW (9), which we considered equivalent to 16-h continuous intake. The meal therefore represents continuous moderate nitrogen infusion. The infusion rates of glucose and amino acids with the test meals are listed in Table 3 (not all amino acids listed). The protein composition of CAPM comprised a 1:1:1 mixture of commercially available French, Dutch, and Danish sodium caseinates. The protein composition of SOPM comprised a mixture of soy protein concentrate (Danpro S) and soy protein isolate (Supro 590). All meals were prepared during the evening before the experimental day. To ensure a complete dissolution of the proteins and to prevent bacterial growth, the meals were kept at 4°C until use.
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2H5-phenylalanine and 2H2-tyrosine are used to calculate whole-body protein metabolism; 2H4-tyrosine is used to prime the 2H4-tyrosine pool for measuring phenylalanine hydroxylation. 2H3-leucine and 13C-leucine are used to calculate splanchnic leucine extraction and endogenous leucine production. 15N2-urea is used for calculation of whole-body urea production.
Analysis of blood. Blood samples were collected in prechilled, heparinized tubes (Becton Dickinson Vacutainer system), immediately put on ice, and subsequently centrifuged at 4°C for 10 min at 3120 x g to obtain plasma. For amino acid analysis, plasma was deproteinized with sulfosalicylic acid (5%). For analysis of urea, glucose, lactate, acetate, pyruvate, and glycerol, plasma was deproteinized with trichloroacetic acid (5%). All samples were stored at –80°C until further analysis.
Plasma concentrations of amino acids were analyzed using an HPLC technique, after precolumn derivatization with o-phthaldialdehyde (30). Amino acid and urea enrichments were calculated as tracer:tracee ratios (TTR) and were analyzed by using a fully automated LC-MS (Thermoquest LCQ) (31). For urea enrichment, a newly developed method using reversed-phase LC in combination with an ion-trap spectrometer was applied (van Eijk, unpublished). Plasma glucose, lactate, acetate, pyruvate, urea, and glycerol were analyzed using a fully automated HPLC system (Pharmacia) application note number 5411, Alltech catalog (column IOA-1000, 300 x 7.8 mm, mobile phase 0.01 mol/L H2SO4, flow 0.3 mL/min, 60°C, refractive index detection).
Calculations. We used a single-pool model for calculation of protein turnover. The model parameters used in the protocol are based on the assumption that there is an isotopic, but not necessarily a physiologic steady state (32). These isotopic steady-state conditions were obtained from a 60-min tracer infusion in the postabsorptive state (2-way ANOVA) (Fig. 2). During enteral nutrition, tracer steady state was reached again from 60 min of food intake, which did not differ between the subjects consuming CAPM or SOPM (2-way ANOVA) (Fig. 2). For the calculations of whole-body rate of appearance (Ra)urea during the postabsorptive state and during enteral feeding, a one-pool model nonsteady-state equation of Steele, modified for use with stable isotopes (33) was applied.
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Splanchnic leucine extraction (SPELeu) represents the fraction (in %) of ingested leucine, taken up by the gut and liver during its first pass and metabolized via oxidation or protein synthesis (25,26), calculated as (1):
 | (1) |
where Ra2H3-Leu and Ra13C-Leu represent whole-body Ra of leucine calculated from i.v. 2H3-Leu and i.g. 13C-Leu isotopes, respectively.
The absolute splanchnic extraction of Leu from the meal [in nmol/(kg FFM · min)] can be calculated by multiplying SPELeu by the infusion rate of Leu with the meal.
Whole-body Ra of leucine, not coming from dietary leucine [endogenous leucine (Raend-Leu)] is calculated from (2) and (3), and indicates whole-body protein breakdown:
 | (2) |
 | (3) |
Whole-body Ra of phenylalanine, not coming from dietary protein [endogenous phenylalanine (Raend-Phe)], is estimated accordingly, using an estimated SPEPhe of 58% based on previous observations in the fed state (36).
 | (4) |
 | (5) |
Statistical analysis. Results are expressed as means ± SEM. Postabsorptive baseline values of arterial and arterialized blood were compared using paired samples t test and were not significantly different. Because postabsorptive baseline arterialized data had more missing values, we used arterial values as baseline. Postabsorptive baseline values between the 2 enteral protein meal groups were compared using independent-samples t tests. The meal-induced change in whole-body protein metabolism, splanchnic metabolism, and urea synthesis was calculated by subtracting the baseline values. Repeated-measures ANOVA was subsequently used to test changes during enteral feeding. A 2-way ANOVA was performed to compare meal and time differences (baseline values and values during the first 4 h and last 4 h of enteral feeding). When a time effect was observed, a Bonferroni test was used for post hoc analysis. Missing values, due mainly to occlusion of catheters during the experiment, were replaced by the series mean at the specific time for the specific protein meal, to make paired analyses possible. Urea kinetics (Ra) were calculated for n = 8 in the CAPM group and n = 7 in the SOPM group. SPSS software was used (SPSS for Windows version 7.5, SPSS). Statistical significance of differences was defined as a 2-tailed P < 0.05.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Tyr) increased significantly during enteral food intake, but the rates differed from postabsorptive values only during the last 4 h of enteral food intake (P < 0.01). The increase did not differ between the CAPM and SOPM groups (P = 0.13). The ratio, QPheTyr/Raphe, which represents the percentage of total phenylalanine that enters the route of hydroxylation, tended to be higher in subjects that consumed SOPM than in those that consumed CAPM (P = 0.06). The ratios tended to increase over time (P = 0.08), with ratios of 0.123 ± 0.012 and 0.111 ± 0.016 in the postabsorptive state, 0.120 ± 0.010 and 0.127 ± 0.010 during the first 4 h, and 0.136 ± 0.010 and 0.147 ± 0.005 during the last 4 h of CAPM and SOPM intake, respectively. Whole-body protein synthesis rate increased during enteral feeding (Fig. 4B), and the increase (difference from postabsorptive values) tended to be higher in the CAPM group than in the SOPM group during the last 4 h of the enteral feeding period (P = 0.09).
Net protein breakdown occurred during the postabsorptive period, but this changed to net protein synthesis during enteral food intake (Fig. 4C; P < 0.001 vs. baseline). The increase was greater in the subjects that consumed CAPM compared with those that consumed SOPM (P < 0.02).
Splanchnic leucine extraction. Splanchnic leucine extraction (SPELeu) was higher (P < 0.05) in the postabsorptive state (49 ± 5 and 39 ± 5% for CAPM and SOPM, respectively) than during enteral food intake (32 ± 3 and 35 ± 2% at T1–4 h for CAPM and SOPM, respectively). Although the percentage SPELeu did not differ between subjects that consumed CAPM and those that consumed SOPM, the absolute values of SPELeu (Fig. 5) were significantly higher in the subjects that consumed CAPM than in those that consumed SOPM throughout the feeding period (P < 0.01).
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Urine production during the 8-h study did not differ between the subjects that consumed CAPM (1234 ± 95 mL) and SOPM (1152 ± 123 mL).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Normal metabolic responses to food intake (casein)
Plasma concentrations and whole-body protein kinetics.
For most amino acids, changes in the arterial plasma level are related to the amino acid composition of the meal, except for those amino acids that are substantially metabolized in the splanchnic area. As an example, glutamine, of which 65% is extracted in the splanchnic area (37–39), is partially converted to citrulline (40), and this explains the rise in plasma citrulline.
Endogenous whole-body protein breakdown was reduced by food intake, as indicated by the 20% reduction of endogenous leucine release into the circulation. Together with the increase in phenylalanine hydroxylation, this observation reflects the normal change from a catabolic to an anabolic state and is in agreement with previous observations (1).
Whole-body urea kinetics.
We observed a decrease in whole-body urea synthesis with food intake, in contrast to the increase that we observed previously in growing pigs (23). The discrepancy is probably due to less reduction of endogenous protein breakdown in growing animals. The urea tracer technique that we used (41) cannot discriminate between urea production from endogenous amino acids and from dietary amino acids, but measures the total rate of urea production in the body. Although urea production from endogenous amino acids probably is decreased due to the change from a catabolic to an anabolic state, food intake increases the portal amino acids flux to the liver and as such stimulates urea production, in line with increased urea synthesis from 15N-labeled protein meals (42). Because urea synthesis from dietary nitrogen depends on the nitrogen content of the meal, which in our study was a continuous moderate nitrogen infusion [8.3 mg N/(kg BW · h), equivalent to 0.4 g protein/(kg BW · 8h); the daily protein requirement is defined at 0.83 g protein/(kg BW · d) (9)], this relatively low nitrogen content may have minimized the increase in urea synthesis from the diet in combination with the reduction in body protein catabolism. Taken together, these factors explain the decrease in urea production that we observed in our study.
Splanchnic metabolism.
Splanchnic extraction of leucine decreased from 45% in the postabsorptive state to 34% with food intake in our study, in line with previous studies (25,36,43,44). Whether the increased amount of extracted leucine with casein intake is used for splanchnic protein synthesis or whether it is transaminated or irreversibly lost (25) cannot be concluded directly from our data because this requires 13KIC and 13CO2 measurements. However, the depression of urea formation and the increase of net protein synthesis suggest a favorable effect on splanchnic protein metabolism.
The importance of the splanchnic area in protein anabolism after consumption of a meal, the last probably on the order of 50% of total intake, was described by us (18,23) and by others (24,45,46) previously, and has been related to the high protein turnover in this area (17,47). Moreover, the splanchnic region modulates the availability of amino acids for extra-splanchnic amino acids (48). Although the double-labeled tracer technique cannot discriminate between intestinal and liver metabolism, the liver uses a major part of extracted amino acids for protein synthesis (44), quantitatively equal to mucosal protein synthesis (45). This so-called labile protein pool in the splanchnic area could play an important role in the postabsorptive phase when renewed breakdown of this labile pool provides essential amino acids to the body free amino acid pool (4).
Differences between casein and soy protein
Plasma concentrations and whole-bodyprotein kinetics. The changes in plasma amino acid levels in the subjects consuming casein and soy meals largely reflected the different amino acid composition of the meals. The change in arterial concentration was less pronounced than expected from the differences in meal composition only for glycine, in agreement with previous studies (23,49). The difference in plasma citrulline between subjects consuming CAPM and those consuming SOPM could be related to the higher glutamine content of CAPM and subsequent intestinal conversion of glutamine to citrulline (40) (see above).
Protein breakdown did not differ between subjects consuming casein protein and those consuming soy protein. However, a larger part of phenylalanine was hydrolyzed during soy protein consumption, which may point to increased oxidation of soy protein, whereas net protein synthesis was lower in the subjects who consumed soy protein. Thus, a substantially larger degree of oxidation and less net protein synthesis with soy protein intake suggest that the biological value of soy protein is less than that of casein protein.
Our data on whole-body protein metabolism of soy and casein agree with previous findings comparing a high vegetable protein diet with a high animal protein diet (50), or low and high milk protein diets. Amino acids, in particular, are main acute regulators in the mechanism of the postprandial changes in protein and amino acid metabolism and are main determinants of protein synthesis (1,6).
Whole-body urea kinetics. During soy consumption, urea synthesis and plasma urea concentrations (first 4 h) were higher than during the same period after consumption of casein. This may indicate increased breakdown from dietary soy amino acids to urea because body protein breakdown was similar in subjects who ate both meals. This is consistent with observations reported after consumption of a bolus of soy and milk protein (24,51). A higher biological value of the meal (such as for casein compared with soy protein) may in general result in less urea production, suggested by comparison of milk protein alone and milk protein supplemented with sucrose (higher biological value) (22). Although urea production decreases during enteral feeding, the pattern of changes in urea concentrations differs from urea production. This seeming discrepancy probably reflects the fact that concentration is not determined only by urea production.
Splanchnic metabolism. The absolute splanchnic extraction of leucine from SOPM was lower than from CAPM. This is in line with previous observations in pigs (23), where CAPM resulted in increased gut protein synthesis. Whether increased splanchnic protein extraction with CAPM in our study also indicates increased protein synthesis was not measured directly, but may be indicated by the fact that on the whole-body level, net protein synthesis was higher with CAPM.
In general, it appears that changes in whole-body protein metabolism in subjects who consumed soy protein are more transitory than changes induced by casein protein. In contrast, more long-term effects on protein metabolism were present in subjects who consumed CAPM. As a consequence, a rapid amino acid delivery to the liver from SOPM and a slow and more continuous supply of amino acids from CAPM may have occurred, with increased transfer to urea and subsequent reduced uptake by the peripheral area when SOPM was consumed (24,51). These differential effects are probably due to the different behaviors of the 2 proteins in the intestine and mirror the slow and fast protein concept (16,51), which makes soy a "fast" protein and casein a very "slow" protein. This could also explain why, during our continuous food intake protocol, most differences between the subjects groups where found during the first hours after the start of food intake, when the response reflects bolus meal intake.
We as well as others have suggested that the degree to which protein in a meal is digested, absorbed, and immediately reutilized for protein synthesis in the gut, determines protein quality. This process "protects" meal protein–derived amino acids from immediate release into the portal vein and potential degradation in the liver to urea. The findings in this study, including a lower net protein synthesis and higher ureagenesis after a soy-containing meal, confirm earlier findings in pigs, and suggest that casein has a higher biological value than soy protein. The stable isotope techniques as used in this study provide a physiologic model that can be used to compare metabolic effects in subjects after consumption of diets of different protein composition or to study effects of protein diets in conditions of net protein catabolism, such as protein-energy malnutrition, renal disease, sepsis, and traumatic injury.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported by a grant from the European Dairy Association (Brussels, Belgium).
4 Abbreviations used: BW, body weight, CAPM, casein protein meal, FFM, fat-free mass; PB, protein breakdown; QPheTyr, hydroxylation of phenylalanine; Ra, rate of appearance; Rd, rate of disappearance; SOPM, soy protein meal; SPE, splanchnic extraction; TTR, tracer-tracee ratio.
Manuscript received 30 August 2004. Initial review completed 21 October 2004. Revision accepted 2 March 2005.
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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