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Institut National de la Recherche Agronomique (INRA), Unité de Physiologie de la Nutrition et du Comportement Alimentaire, Institut National Agronomique Paris-Grignon (INA-PG), 75231 Paris Cedex 05, France;
* Deutsches Institut für Ernährungsforschung-Potsdam (DIfE), Unit Protein Metabolism, 14558 Bergholz-Rehbrücke, Germany; and
Service de Gastroentérologie, Hôpital Avicenne, Bobigny, France
3To whom correspondence should be addressed. E-mail: gaudicho{at}inapg.fr.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • dietary protein • amino acids • postprandial metabolism • GC-C-IRMS • humans
We and others have recently shown that the postprandial nitrogen metabolism of intact dietary proteins differs after the ingestion of milk and soy protein, mainly because of the greater deamination of soy amino acids than of milk amino acids (AA) (1 –4 ), but also because of their differing capacity to support protein synthesis (5 ).
First, soy and milk differ in their amino acid composition, i.e., soy protein contains lower levels of methionine, branched-chain amino acids (BCAA), lysine and proline, and higher levels of aspartate, glycine, arginine and cystine than milk protein. In addition, soy proteins are less digestible than milk proteins on a nitrogen basis (1
,6
), and the digestibility of individual amino acids differs between these two proteins (7
). Threonine, in particular, reaches 93% digestibility in milk protein but only 89% in soy protein, whereas the values for valine are 96 and 92%, respectively. Moreover, individual amino acid availability for extraintestinal tissues is further reduced by amino acid uptake into portal-drained viscera (8
,9
). Consequently, it can be assumed that the pattern of amino acids reaching the liver is relatively more unbalanced with soy protein than with milk protein, which may result in higher postprandial deamination due to their limited utilization for protein synthesis (10
,11
). Second, the digestion and absorption kinetics of dietary proteins influence catabolic and anabolic activities at the whole-body level (12
) and in the liver (13
). Milk proteins contain caseins (
80%), which clot in the stomach during the course of digestion, and whey proteins, which are soluble and rapidly emptied from the stomach (14
,15
); in contrast, soy proteins are composed mainly of a soluble protein fraction. Despite these differences, the gastric emptying rates for soy and milk proteins have been found to be identical when measured on either a nitrogen or dry matter basis (16
–20
). However, few data (obtained in both rats and humans) are available to suggest that soy protein exhibits a higher intestinal transit rate than milk protein (13
,20
). Finally, the AA pattern of dietary proteins may have different effects on the secretion of insulin (21
); indeed, it has been shown that insulin secretion was positively correlated with plasma leucine, phenylalanine and arginine concentrations (22
,23
). Because the AA compositions of soy and milk proteins differ, variations in hormone secretions may occur with different protein sources, which, in turn, would be likely to influence the postprandial sparing of dietary amino acids (24
). Such hormonal differences between protein sources have been observed by some authors (23
,25
) but not by others, including our previous works in which we could not demonstrate any difference in insulin profile as a function of the nature of the protein ingested in a mixed meal, or any stimulation of insulin by the ingestion of protein alone (1
,3
,26
).
To better clarify the reasons for the differing postprandial deamination of soy and milk proteins, we traced the pattern of amino acids of dietary origin reaching the periphery, as well as the hormonal response induced by a single meal. For this purpose, healthy volunteers ingested a mixed meal containing 15N-labeled milk or soy proteins, after a 1-wk period of standardization to a protein intake of 1 g/(kg · d). The appearance of each 15N-AA was monitored in the serum using gas chromatography-combustion-isotope ratio mass spectrometry (GC-C-IRMS), and postprandial hormonal profiles were determined.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The study protocol was approved by the Institutional Review Board for Saint Germain-en-Laye (France). After obtaining their written, informed consent, 16 healthy volunteers (7 men and 9 women) were included in this study. Their mean age and body mass index were 28 ± 5 y and 21.4 ± 2.2 kg/m2, respectively (Table 1). Total body water (TBW) and the percentage of body fat were determined using multiple frequency Bio-Impedance Analysis (BIA); the vendor-provided equations were used for the calculations (Analycor 5w, Spengler, Cachan, France). During the week before the study, the subjects were asked to follow a controlled diet adjusted to their body weight, providing 138 kJ/(kg · d), 1 g protein/(kg · d), 4.5 g carbohydrates/(kg · d) and 1.2 g fat/(kg · d). The subjects were instructed to comply strictly with the specified meals and to weigh precisely the foods ingested. After this diet standardization period, they were asked to attend the Avicenne Hospital, Bobigny, France, on the morning of the study day, having fasted overnight, and were randomly assigned to one of the two experimental groups, i.e., soy or milk protein. The test meals represented one third of their daily energy intake, i.e., 46 kJ/kg, and had a standard nutrient composition, i.e., 15, 55 and 30% of total energy as protein, carbohydrate and fat, respectively (Table 1).
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Analytical procedures.
Total urea levels in the urine and serum, and creatinine levels in the urine were determined using an enzymatic method on a Dimension Automate (Dupont de Nemours, Les Ulis, France). Ammonia was measured in the urine by an enzymatic method using a clinical analyzer (Kone, Evry, France). Plasma glucose was measured by a glucose oxidase method (kit Glucose GOD-DP, Kone). Plasma hormones (insulin, glucagon) were measured by RIA (insulin: Bio-Rad, Marnes la Coquette, France; glucagon: Nichols, Paris, France).
For the determination of individual serum free AA concentrations, the protein fraction of 800 µL serum was precipitated with 40 µL of a sulfosalycilic acid solution (1 g/mL). After 1 h of precipitation at 4°C and centrifugation for 20 min at 3000 x g, the supernatant was removed and dried. It was then resuspended in a lithium citrate buffer (pH 2.2), filtered on 0.2-µm filters and injected into a HPLC system (Bio-tek Instruments, St Quentin en Yvelines, France) combined with a postcolumn ninhydrin derivatization. Separation was performed on cation exchange resin. All AA except proline (440 nm) were detected at 540 nm. 
-Aminobutyric acid was used as an internal standard.
The 15N-enrichment of individual AA was measured using gas chromatography/combustion/isotope ratio mass spectrometry (GC-C-IRMS) analysis. Free AA from serum samples were purified as previously described (27 ), and derivatized to N-pivaloyl-i-propyl AA esters. Briefly, the AA were treated with 1 mL of a thionylchloride and i-propanol solution. The mixture was heated for 30 min at 110°C and then dried under a gentle stream of nitrogen at 60°C and redissolved in pyridine (100 µL). After the addition of pivaloylchloride (100 µL), each solution was acylated for 30 min at 60°C, cooled and then 2 mL of dichloromethane was added. The solution was then passed through a silica gel column and the eluate dried in a gentle nitrogen stream at room temperature. The vials were covered and the derivatives kept refrigerated until GC-C-IRMS analysis; just before this procedure, the derivatized AA were resuspended in 50 µL ethyl acetate. The analysis was carried out on a Finnigan Delta S system (Thermoquest, Bremen, Germany) as previously described (28 ). A combustion interface allowed the production and purification of N2 gas from GC-separated compounds to enter the IRMS. An Ultra 2 capillary column (50 m, Hewlett-Packard, Waldbronn, Germany) was used to separate the AA. The carrier gas was He. A standard N2 gas (known isotopic composition) was introduced for calibration.
15N-enrichment in urinary and serum urea was measured by IRMS after extraction on cation-exchange resins, as previously described (1 ). Briefly, the serum urea was isolated after the precipitation of serum protein with sulfo-salicylic acid. The supernatant was buffered to pH 7 and urea was extracted on a cation-exchange resin (Biorad Dowex AG50-X8, mesh 100–200, Interchim, Montluçon, France) in the presence of urease. The resin containing urea-derived ammonia from serum was washed with distilled water and stored at 4°C. The pellet was dried, weighed and used for the determination of 15N-enrichment in the serum protein fraction. Urine samples (7 mL) were put on resins to extract ammonia. The supernatant was transferred on a second resin and kept at 30°C for 2 h with urease for urea hydrolysis. Before isotope determination, the resins were eluted with KHSO4 (2.5 mol/L). The 15N-enrichment was measured by isotopic ratio mass spectrometry (Optima, Fisons Instruments, Manchester, UK) coupled to the elemental analyzer (NA 1500 series 2, Fisons Instruments). A calibrated nitrogen gas was used as the reference to derive the 15N/14N ratio.
Calculations and statistics.
The time course of dietary N incorporation (Ndiet, expressed as a percentage of the ingested amount) into the different monitored body N pools (serum free AA, serum protein, serum and urinary urea) was calculated using the following equation:
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where Ntot is the N content of the pool (mmol N), APEs(t) is the 15N-enrichment above the baseline enrichment (expressed as atom % excess, APE) in the N pool sampled at time t, APEm is the 15N-enrichment of the meal (APE) and Nm is the N content of the meal (mmol N). Ntot in the serum protein pool was determined as the serum content of protein N, respectively, multiplied by the serum volume, estimated to be 5% of the body weight (29
). Body urea pool size was calculated as the product of the urea concentration and TBW, measured by BIA, which has been recognized as an accurate method for total body water determination in young, healthy adults (30
). A factor of 0.92 was used to take account of the plasma water content. For urinary urea, Ntot was calculated as the product of urinary urea N concentration and the volume of urine excreted. The transfer of dietary N to the urea pool (or dietary urea production, UPdiet) was evaluated from the dietary N excreted in the urinary urea for each 2-h interval, corrected for the change in the dietary N content of the body urea pool over the same period, as follows:
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where UU is urinary urea N from dietary origin and BU is body urea N from dietary origin. Dietary N retention, or net postprandial protein utilization, was derived from the amount of N ingested, minus the amount nonabsorbed at the intestinal level, i.e., 5 and 8.5% for milk protein and soy protein, respectively, as published previously (1 ,6 ), and minus the amount of urea produced for the 8-h period.
The appearance in the serum of dietary N-containing AA (AAdiet, in µmol/L) was calculated for each AA as follows:
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where AAtot (t) is the concentration of individual AA in the serum sample at time t (µmol/L), APEs(t) and APEm the 15N-enrichment excess of the individual sample and the meal, respectively. These values represented the quantity of individual AA carrying a nitrogen atom of dietary origin. For AA that do not transaminate (lysine and threonine), the amount of dietary N-containing AA directly reflected the amounts of dietary AA entering the systemic circulation.
Areas under the curve (AUC) for serum 15N-AA and hormones were computed. The results are expressed as mean ± SD. Group differences for single planned comparisons were tested using an unpaired t test. Comparisons of the time course of serum concentrations and of the incorporation of dietary N into the monitored N pools between the two groups were performed using a repeated-measures ANOVA (General Linear Model, SAS/STAT 6.03, SAS Institute, Cary, NC), in which the factors were the protein source, time and their interaction. When the protein source x time interaction was significant, Tukey’s post-hoc tests were applied. Differences were deemed significant when P < 0.05.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The postprandial plasma glucose profiles did not differ, and the AUC above baseline values were almost identical in both groups (Fig. 1 ). When normalized for baseline values, the insulin and glucagon postprandial profiles did not differ in the two groups.
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The temporal fate of both total AA and dietary N-containing AA in the different serum AA pools, including total (TAA), indispensable, dispensable, branched-chain (BCAA) and gluconeogenic (i.e., alanine, serine, glutamine, glutamate, glycine, threonine) AA, was monitored after the ingestion of a soy or milk protein meal. In each AA pool, AA concentrations rose significantly (time effect) and peaked 1–2 h after the ingestion of soy, whereas after the ingestion of milk, the rise was less pronounced and occurred later, as exemplified by the time course of total AA, BCAA and gluconeogenic AA (Fig. 2 ). The maximum total concentrations in the total AA pool occurred after 2 and 3 h, with values of 2923 ± 887 and 2446 ± 552 µmol/L after the soy and milk protein meal, respectively. There was a significant time x protein source interaction for both total and dietary N-containing AA in TAA, indispensable, dispensable, branched-chain and gluconeogenic AA pools (repeated-measures ANOVA), reflecting a global difference in the shape of the curves between groups. Moreover, for the different plasma AA pools, the postprandial rise in total AA concentrations could be explained mainly by the appearance of the dietary N-containing AA fraction, as illustrated by the specific course of leucine, proline or alanine (Fig. 3 ). For all AA (with the exception of proline), intake of the soy meal produced an earlier and higher peak value, usually 2 h after the meal, compared with the findings in the milk group. The protein source had a significant effect on serum AA concentrations for phenylalanine, arginine, glutamate and aspartate (higher global levels after soy than after milk protein ingestion). There was also a significant time x protein source interaction for almost all AA, except for alanine, histidine, glutamate, glycine and aspartate (not shown).
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There were few differences between the two groups in either the peak of dietary N-containing AA concentrations or the AUC in serum (Table 3). The only significant differences were observed for proline, which was found at double the amount in the milk group, and histidine, which reached a higher value after soy protein ingestion. There was a trend (0.05 < P < 0.1) toward lower dietary N-containing methionine and aspartate + asparagine AUC values after soy protein ingestion. However, there were major differences for almost all of the dietary N-containing AA in terms of their kinetics, characterized by their systematically earlier appearance in the serum after soy protein ingestion than after the milk protein meal. This difference was significant for leucine, methionine, threonine, valine, aspartate + asparagine, glutamate + glutamine, glycine and serine. When expressed as ratios between group results (milk:soy), the different accumulated appearances of dietary N-containing AA and initial AA levels in the ingested proteins were closely linked (Fig. 4 ). For instance, methionine was twice as abundant in the milk group as in the soy group, and the accumulated dietary N-containing methionine levels were also twice the values in the milk group compared with the soy group.
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The production of total urea (3.41 ± 0.93 and 3.61 ± 0.60 mmol N/kg body after soy or milk protein ingestion, respectively) and the time course of serum protein concentrations (36.1 ± 1.6 and 35.6 ± 1.9 mmol N/kg after soy or milk protein, respectively) did not differ over the 8 h period (not shown). The peak of dietary N urea production (Fig. 5 ) was earlier in the soy group than in the milk group (3 ± 1.1vs. 4.75 ± 1.0 h, respectively, P < 0.005). The protein source ingested had a significant effect on the time course of dietary N transfer to the urea produced (protein source x time interaction: P < 0.02, repeated measures ANOVA). Two hours after the meal, the levels of dietary N transferred to urea were higher after soy than after milk protein ingestion, reaching 7.9 ± 2.9 and 4.3 ± 1.9% of the N ingested, respectively; P < 0.02). The level of dietary N recovered in the urea pool over the 8-h period was 20.3 ± 4.1 and 21.6 ± 3.8% of the ingested amount in the milk and soy groups, respectively (P > 0.05) and dietary N retention reached 74.7 ± 4.1 and 69.9 ± 3.8% of the ingested amount in the milk and soy groups, respectively (P < 0.05). The incorporation of dietary N into serum protein (Fig. 5) was also higher in the soy group than in the milk group, and the protein type (P = 0.02) and protein source x time interaction (P = 0.04) had significant global effects (repeated-measures ANOVA).
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The present study confirms a difference in dietary N metabolism after soy and milk protein ingestion, as described earlier (1 ,6 ), and provides evidence of major differences between the two proteins in terms of the rate of appearance of "dietary" AA in the peripheral blood, which is representative of the digestion/absorption kinetics. The measurement of 15N-containing AA in the systemic circulation cannot exactly be considered to be dietary AA because of the transamination that occurs during the first-pass metabolism of AA, except in the case of threonine and lysine, which do not participate in transamination. Nevertheless, there was a close resemblance between the dietary protein and serum free dietary N-containing AA patterns, allowing us to draw conclusions concerning the differences between serum dietary N-containing AA in the two groups.
Our first conclusion is that the differences observed between the two proteins had an important kinetic component related to the intestinal rate of AA absorption. A nearly equivalent half-time of gastric emptying has been reported for milk and soy proteins (16 –20 ). However, this measure may not accurately account for the differential behaviors of milk protein fractions or differences in their kinetics, which are more likely to be seen at the intestinal level because the gastric emptying rate and intestinal transit time may be independently affected by dietary factors (31 ,32 ). Indeed, some differences between proteins seem to occur at the intestinal level, characterized by the more rapid transit of soy protein than that of casein, as has been shown in rats (20 ). In line with this, we recently found in humans that the intestinal half transit time of soy proteins was 50 min shorter than that of milk proteins in humans (13 ). A possible mechanism for such a difference may be the release from casein digestion of ß-casomorphin, which have been reported to modulate gastrointestinal motility (33 ,34 ), or a delay in the intestinal proteolysis of casein.
The reason for assuming that this kinetic difference influences the metabolic utilization of the two dietary proteins is that digestion and absorption kinetics determine the directions of dietary AA through the various metabolic pathways in organs. This is consistent with studies in both humans and animals comparing postprandial protein metabolism after the ingestion of casein (slow rate of absorption) or free AA/oligopeptides mimicking the composition of casein (fast rate of absorption) (35 –37 ). The rapid absorption of AA is associated with both enhanced AA catabolism and transiently higher protein synthesis at the whole-body level (12 ,35 ,36 ). Our results provide new evidence for an important role of the liver in this transient anabolic effect of fast protein, as illustrated by the higher incorporation of dietary N into serum protein after the ingestion of soy protein. The time-course of dietary N appearance in serum free AA, urea and serum protein was consistently always more rapid after the ingestion of soy than after that of milk protein. We have already reported in rats that an acute increase in protein intake resulted in a higher transfer of dietary N into plasma protein (38 ). In agreement with others (24 ), we conclude that a high influx of AA enhances both liver protein synthesis and deamination to prevent hyperaminoacidemia. This is also in line with the data obtained in rats showing a lower incorporation of lysine in the splanchnic zone after the ingestion of whole casein, compared with its corresponding crystalline AA mixture (37 ). Whether the moderate imbalance of indispensable AA from soy protein may also have contributed to their more marked deamination and incorporation into liver protein is difficult to predict from the present study and would require a study of soy protein supplemented with crystalline AA to reach the same level as total milk protein.
Apart from intestinal dynamics, the differences between soy and milk protein may have arisen from the combined influence of a relatively unbalanced AA composition in the soy protein and its lower digestibility, resulting in a less favorable pattern of AA reaching the periphery (7 ). Despite supposed differences in the pattern of absorbed AA entering the portal circulation after milk or soy protein ingestion, the absolute amounts of dietary AA appearing in the systemic circulation did not differ between groups, with the exception of a consistently higher level of dietary proline in the milk group because of its higher concentration in the meal. This lack of difference was due mainly to diminished power resulting from the large interindividual variability of circulating AA levels and the number of subjects in each group (n = 8). We would have expected some differences in the splanchnic first pass to have exacerbated differences in the AA composition pattern between milk and soy. However, the fact that the subjects had previously been adapted to a moderate level of protein [1 g/(kg · d)] was likely to attenuate differences in AA deamination/oxidation. At this level, the difference in dietary N retention between milk and soy protein was due mainly to differences in digestibility because AA catabolism was not activated, but at higher levels of protein habituation, the gap between the deamination of these proteins widens (unpublished data) (1 ,6 ).
Nevertheless, despite the absence of absolute differences in AA amounts in plasma, the dietary protein pattern was directly reflected by the circulating dietary AA pattern when expressed as ratios between groups. In this case, a direct influence of the AA composition of dietary protein on the indispensable AA available to the peripheral tissues for metabolic utilization and protein synthesis can be hypothesized, which is of particular interest with respect to AA such as BCAA. Human studies have shown that the composition of ingested AA mixtures has a direct influence on whole-body protein synthesis (39 ,40 ). Using compartmental modeling in humans, we showed that postprandial N retention was significantly higher in the peripheral N pools after milk protein ingestion than after soy protein, which could be interpreted as a more favorable pattern of AA available for peripheral protein synthesis in the case of milk protein ingestion (13 ). It is also consistent with the lower protein retention values observed in pigs fed a soybean protein–based diet compared with a casein-based diet (4 ).
Dietary proteins, through their AA composition and their specific insulinotropic effects, may influence insulin secretion. Because we know the role played by insulin in AA sparing (41 ), it was important to test this hypothesis. Arginine and leucine have been suspected of having the most potent insulinotropic effects (42 ,43 ). We found very similar hormonal responses to the acute ingestion of both the soy and milk meals, which is consistent with the findings of Lang et al. (26 ). Similarly, the study by van Loon and colleagues (22 ) did not demonstrate any differences in plasma insulin levels after the ingestion of casein or pea protein hydrolysates. In contrast, wheat ingestion induced a higher insulin response, suggesting an insulinotropic effect of glutamine. During our study, the glutamine intake was nearly identical in the soy and milk meals. Finally, as recently shown in humans, the degree of protein fractionation likely plays a predominant role in the modulation of postprandial insulin/glucagon release, independently of the protein source (23 ).
In conclusion, our study shows that the principal differences in postprandial metabolism between soy and milk protein are observed in terms of the time of appearance of dietary AA in the serum, presumably because of the different behavior of proteins in the intestine, with soy protein acting as a "fast" protein and milk protein as a "slow" protein. The massive influx of dietary AA into the liver appears to elicit a larger metabolic availability of AA in this organ, including both their incorporation into exported liver protein and their catabolism. In addition, we showed that the pattern of dietary AA reaching the periphery reflects mainly dietary protein composition and may participate in the lower level of protein retention. Elucidating whether these two important factors (rate of digestion and AA composition) interfere with each other under different nutritional conditions will constitute an interesting further step in the study of protein metabolism.
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FOOTNOTES |
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2 Present address: Research Institute for the Biology of Farm Animals, Research Unit Nutritional Physiology Oskar Kellner, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany.
4 Abbreviations used: AA, amino acid; APE, atom % excess; AUC, area under the curve; BIA, bioelectrical impedance analysis; GC-C-IRMS, gas chromatography-combustion-isotope ratio mass spectrometry; TBW, total body water.
Manuscript received 29 November 2002. Initial review completed 8 January 2003. Revision accepted 15 February 2003.
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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