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Article

Nutritional Value of [¹⁵N]-Soy Protein Isolate Assessed from Ileal Digestibility and Postprandial Protein Utilization in Humans¹

François Mariotti^*, Sylvain Mahé^*2, Robert Benamouzig, Catherine Luengo^*, Sophie Daré^*, Claire Gaudichon^* and Daniel Tomé^*

^* Institut National de la Recherche Agronomique, Unité de Nutrition Humaine et de Physiologie Intestinale, Institut National Agronomique Paris-Grignon, 75231 Paris Cédex 05, France and Service de Gastroentérologie, Hôpital Avicenne, 93009 Bobigny, France.

²To whom correspondence should be addressed.

	ABSTRACT

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The purpose of this work was to assess the true oro-ileal digestibility, and to concurrently quantify the deamination of absorbed dietary nitrogen to examine the postprandial nutritional value of a soy protein isolate (SPI) in humans. To assess bioavailability and bioutilization of SPI, 10 healthy volunteers ingested 30 g of SPI, intrinsically and uniformly [¹⁵N]-labeled, added with 100 g of sucrose and water up to a final volume of 500 mL. True ileal digestibility was assessed by the [¹⁵N]-dilution method for 8 h by means of a naso-intestinal intubation technique. To describe and quantify exogenous nitrogen deamination for the same time period, urine and plasma samples were collected. True oro-ileal digestibility of SPI nitrogen was 91%. The amount of absorbed SPI amino acids used for nonoxidative disposal, i.e., postprandial biological value, was 86% 8 h after meal ingestion. Hence, net postprandial protein utilization of SPI was 78%. Compared to previous data that were assessed under the same condition in humans, the nutritional value of SPI is 92% of that in milk protein concentrate.

KEY WORDS: • stable isotope • oxidation • plant protein • bioavailability • humans

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Among dietary proteins, soy protein isolate and concentrate are believed to have a high nutritional quality for humans (Erdman and Fordyce 1989 , Young 1991 ), but criteria to assess this quality are complex and still under discussion (Millward 1994 , Munro 1969 , Young and Pellett 1988 , Young et al. 1998 ). Studies of soy protein quality mainly include long-term balance studies in animals or humans fed different levels of protein (Beer et al. 1989 , Istfan et al. 1983 , Scrimshaw et al. 1983 , Wayler et al. 1983 , Young et al. 1984 ). This method's evaluation of dietary protein quality has been criticized (Millward and Pacy 1995 , Young 1986 , Young et al. 1981 ). Firstly, in long-term balance studies, the digestibility factor is assessed as fecal digestibility, although the intestinal flow of amino acid beyond the terminal ileum is an important route for the bacterial metabolic consumption of amino acids, which are consequently used for protein synthesis in the body. Therefore, ileal, rather than fecal, digestibility is probably the most critical biological parameter for amino acid or protein bioavailability. Secondly, this method does not consider the acute metabolic events that are concomitant with dietary protein ingestion, which are likely to be very critical in the deposition of dietary protein in tissues. The diurnal cycle of feeding and fasting periods results in postprandial dietary nitrogen gains and postabsorptive losses of body proteins, and in those conditions, the nitrogen retention that is calculated as the daily gain should be lower than the postprandial gain (Millward and Pacy 1995 ). To further evaluate soy protein quality, the aim of this study was to assess the true oro-ileal digestibility of [¹⁵N]-labeled soy protein isolate (SPI)³ and to describe and quantify the postprandial deamination of absorbed amino acids, and thus dietary nitrogen retained in the body, by concurrently measuring dietary oxidized nitrogen compounds in the blood and urine of humans.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Subjects.

The study was performed on 10, healthy volunteers (7 males and 3 females) ranging from 20 to 37 y (mean ± SD = 28 ± 5 y), weighing from 55 to 89 kg (mean ± SD = 65 ± 9 kg), and with a body mass index ranging from 19.6 to 27.5 kg·m^-2 (mean ± SD = 22.6 ± 2.6 kg·m^-2). The protocol was previously approved by the Ethical Committee of the St-Germain-en-Laye Hospital (St-Germain-en-Laye, France). After the experimental protocol had been explained in detail, all subjects gave their consent for their participation in the study. None of the subjects had a history of gastrointestinal surgery or suffered from gastrointestinal system disorders.

Diets.

Soy seeds (var. Chandor) were grown under controlled conditions, using K[¹⁵N]O₃ foliar spraying, by the INRA Unit (Unité de formation et de Recherche Génétique et Amélioration des Plantes, Montpellier, France). A soy protein isolate was purified by Nestec Research Center (Lausanne, Switzerland) from the intrinsically and uniformly [¹⁵N]-labeled soy seeds. Extraction and separation steps were carried out on a laboratory scale. First, beans were coarsely milled, and the native soyflour was then deoiled with hexane. The proteins were extracted from the defatted flour with water at neutral pH. After centrifugation (3500 x g for 30 min at 0°C), the supernatant was immediately acidified to pH 5.2 to precipitate the protein fraction. The protein coagulum was washed, neutralized (NaOH), sterilized (140°C for 40 s) to inactivate the trypsin inhibitors, lyophilized and then packaged. This SPI was composed of 90% of protein (N x 6.25), and its isotopic enrichment was 1.1606 atom-%. The experimental liquid meal (SPI meal) consisted of 30 g SPI (316 mmol N) and 100 g sucrose mixed with water for a final volume of 500 mL. The energy content of the experimental meal was 2294 kJ. The amino acid composition of the soy protein isolate was identified by amino acid analysis. Dry samples were hydrolyzed in vacuum tubes at 110°C for 24 h with 6 mol HCl/L using norleucine as the internal standard. Cysteine and methionine were oxidized with performic acid before hydrolysis at 110°C for 24 h with 6 mol HCl/L. The hydrolysates were analyzed on a Pharmacia LKB Alpha⁺ Analyzer (Pharmacia Biotech, Orsay, France) with a lithium buffer. Tryptophan was determined by a colorimetric method according to Spies (1967) .

Clinical protocol.

Volunteers were admitted to the hospital the morning before the study day. An intestinal tube was passed through the nose and led down the digestive tract, as previously described (Mahé et al. 1992 ). The intestinal tube was used 1) to perfuse phenol red (PSP), a nonabsorbable intestinal marker, into the ileum and 2) to collect intestinal samples by continuous suction 200 mm distally from the perfusion site. Volunteers had dinner at 2000 h and then fasted overnight. On the morning of the study, after the position of the tube had been checked by radioscopy, a catheter was inserted into a superficial forearm vein for blood sampling. Subjects were given a maximum of 5 min to drank a meal (316 mmol N). The postprandial sampling period lasted for 8 h. The test was performed while the subjects were at rest, and they were not allowed to ingest food or fluids until the end of the test. Intestinal aspirates were collected over ice and pooled in 30-min intervals, for 8 h, the first collection, taken before the meal, represented the initial period. The ileal effluents were freeze-dried, lyophilized and then analyzed for total nitrogen content and [¹⁵N] enrichment. Blood samples were collected every hour during the 8 h following meal ingestion, except between 1 and 4 h after the meal when additional samples were taken. A last blood sample was collected the next day at 0900 h. The plasma was immediately separated from whole blood by centrifugation (2500 x g for 20 min at 4°C) and kept frozen at -20°C until analysis. Urine was collected during 29 h (0–2, 2–4, 4–6, 6–8, 8–12, 12–20, 20–29 h), treated with thymol crystals and liquid paraffin as preservatives and stored at 4°C until further analysis.

Extraction of urea and ammonia in plasma and urine.

Urea and ammonia were isolated by using a batch method, as previously described (Gausserès et al. 1997 ). For urea extraction, 4 mL of plasma were added to 200 mg of solid, 5-sulfo-salicylic acid (Prolabo, Paris, France). After mixing, and then standing for 1 h at 4°C, the protein was pelleted at the bottom of the tube by centrifugation at 2400 x g for 25 min at 4°C, and the supernatant was collected. From the urine, ammonia was first extracted by using the Na/K form of the cation exchange resin (Dowex AG-50X8, Mesh 100–200, BioRad, Interchim, Montluçon, France) by the batch procedure. The supernatant fraction was collected for further urea extraction. The urea was extracted from both the plasma supernatant fraction and the ammonia-free urine fraction by converting it into ammonium by hydrolysis with urease (Sigma, Saint-Quentin-Fallavier, France) for 2 h at 30°C on the cation exchange resin. The resin was washed three times with distilled water and stored at 4°C. Before isotopic determination, ammonia and urea-derived ammonia were eluted from the washed resins by the addition of 2.5 mmol KH₂SO₄/L

Analytical Methods.

Total nitrogen content of the samples was determined by using an elemental nitrogen analyzer (NA 1500 series 2, Fisons Instruments, Manchester, UK) with atropine as the standard. Urea was assayed in both plasma and urine by an enzymatic method (urease/glutamate deshydrogenase) on a clinical analyzer (Dimension automate, Dupont de Nemours, Les Ulis, France). Ammonia in the urine was measured by an enzymatic method (glutamate deshydrogenase) on a clinical analyzer (Kone Automate, Kone, Evry, France). Creatinine content of a 24-h collection of urine was measured by using a direct colorimetric method on a clinical analyzer (Dimension automate, Dupont de Nemours). Glucose in the plasma was measured by a glucose oxidase method (kit glucose GOD-DP, Kone). Insulin in the plasma was measured by a radioimmunoassay method (kit INSI-PR, Cis Bio International, Gif-sur-Yvette, France). The isotopic N₂ enrichment (¹⁵N/¹⁴N) was determined by isotopic ratio mass spectrometry (IRMS). An aliquot was burned in an elementary analyzer (NA 1500 series 2, Fisons Instruments) at 1020°C interfaced with an isotope ratio mass spectrometer (Optima, Fisons Instruments). The ¹⁵N/¹⁴N ratios (m/z 28: m/z 29: m/z 30) were measured in reference to a calibrated ¹⁵N/¹⁴N nitrogen tank.

Calculations and statistical analysis.

An assessment of PSP dilution between the perfusion solution and collected samples, from the ileal perfusion technique, allows for the calculation of flow rates in the ileum (calculation of the average flux by 30 min), according to the following formula F_r = (PSP_p/PSP_s) x PSP_f, where F_r is the flow rate in the ileum (mL/min), PSP_p is the concentration of PSP in the perfusion (400 mg/L), PSP_s is the PSP concentration in the ileal samples (mg/mL) and PSP_f is the perfused PSP flow rate (1 mL/min). The fraction of exogenous nitrogen in the ileal samples was calculated from both the total nitrogen and the isotopic ¹⁵N/¹⁴N ratio. Exogenous nitrogen (N_exo-ileal mmol N) that transits through the terminal ileum, was thus calculated by using the equation N_exo-ileal = N_tot-ileal x E_dig/E_spi, where N_tot-ileal is the total nitrogen that transits through the terminal ileum and E_dig and E_spi are the ¹⁵N/¹⁴N ratio in the total nitrogen in the sample and in the [¹⁵N]-SPI, respectively. Exogenous nitrogen incorporated in the body urea pool (N_exo-urea mmol N) was calculated according to the formula N_exo-urea = N_tot-urea x E_urea/E_spi, where N_tot-urea is the nitrogen present in body urea pool and E_urea is the ¹⁵N/¹⁴N ratio in the plasma urea. N_tot-urea was calculated as the product of the plasma urea concentration and its volume of distribution with the assumption that urea was distributed throughout the total body water. Total body water was estimated by using the equation of Watson et al. (1980) . The exogenous nitrogen incorporated in urinary nitrogen (N_exo-urinary mmol N) was calculated according to the formula N_exo-urinary = N_tot-urinary x E_urinary/E_spi, where N_tot-urinary is the quantity of urinary nitrogen (in the form of either total urea or ammonia nitrogen), and E_urinary is the ¹⁵N/¹⁴N ratio in urinary nitrogen (in the form of either total urea or ammonia nitrogen). The postprandial biological value (PBV) and net postprandial protein utilization (NPPU) were calculated according to the formula

where N_meal is the amount of nitrogen ingested. Different model curves were used in the postprandial period to fit the experimental quantities of (1) cumulative exogenous nitrogen transiting at the terminal ileum; (2) exogenous nitrogen excreted in the urine as total nitrogen, urea, or ammonia; (3) exogenous urea present in the body; and (4) [¹⁵N]-labeled SPI deamination. For (1) and (2), the curve is in the form

in which t is time and a, b, c and d are regression-estimated constants. For (3), the curve is in the form

in which t is time, and , ß and t₀ are regression estimated constants. For (4), because cumulative soy protein deamination was assumed to be the sum of cumulative total nitrogen excreted in the urine and nitrogen retained in total body water, the adjustment curve is given by the sum of the two fitted equations (2 + 3)

Curve fittings of the experimental data were performed by using Sigma Plot 5.0 (Jandel Corporation, SPSS Sciences Software GmbH, Erkrath, Germany). Curve studies were computed by using an algebraic calculation software (MapleV, release 4, Waterlow Maple, Adept Scientific, Herts, UK). Results were expressed as means ± SD. To estimate the differences between the initial values and the absorptive values within the period, a statistical analysis was performed by using a Student's t-test (Proc Means, SAS/STAT Version 6.03, SAS Institute, Cary, NC). A probability of P < 0.05 was considered significant.

	RESULTS

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Glycemia and insulinemia.

The concentrations of glucose and insulin in the plasma after the ingestion of SPI meal were measured (Fig. 1 ). Glycemia significantly increased from 5.1 ± 0.3 mmol/L in initial period to 6.9 ± 1.4 mmol/L at 30 min and returned to the fasting level at 4 h. Insulinemia concomitantly and significantly increased to a maximal value of 249.1 ± 200.4 pmol/L at 30 min and then returned to the initial value (45.6 ± 19.4 pmol/L) at 5 h.

View larger version (16K): [in this window] [in a new window]   Figure 1. (A) Glucose and (B) insulin concentrations in the plasma of humans after ingestion of a [15N]-labeled soy protein isolate meal. Values are means + SD, n = 10. * Significantly different from the initial value (t-test, P < 0.05).

Figure 2 represents the cumulative, exogenous nitrogen at the terminal ileum during an 8-h period after meal ingestion. A substantial amount of exogenous nitrogen was detected at 2 h. At 8 h, the total exogenous nitrogen that was transited through the terminal ileum was 28.6 ± 6.9 mmol. Under these conditions, taking into account the quantity of nitrogen ingested (316 mmol), the overall true oro-ileal digestibility of SPI was 90.9 ± 2.2%. Regression-estimated constants showed that the plateau was reached at 417 min and that the asymptotic value is 28.2 mmol N.

View larger version (15K): [in this window] [in a new window]   Figure 2. Cumulative exogenous nitrogen in the ileum of human volunteers during 8 h after ingestion of a [15N]-labeled soy protein isolate meal. Values are means + SD, n = 10. The experimental values can be fitted to a sigmoidal curve according to the relation y = b/(1 + exp[c(t-a)]) + d, in which t is time, and a, b, c and d are regression-estimated constants: a = 152.45, b = 31.92, c = -0.014 and d = -3.72 (R2 = 0.9966). * Significantly different from zero (t-test, P < 0.05)

Figure 3 represents the exogenous part of cumulative urinary excretion of total nitrogen, urea and ammonia. Exogenous nitrogen in total nitrogen, urea nitrogen and ammonia nitrogen pools was significantly recovered after the first urine collection (2 h). The exogenous urea represented the major fraction of total nitrogen, and cumulative recoveries exhibited identical shapes. The fitted cumulative quantities of exogenous nitrogen excreted in the urine in the form of total nitrogen, urea and ammonia had asymptotic values of 73.7 mmol N for total, 68.1 mmol N for urea and 1.1 mmol N for ammonia exogenous nitrogen. The experimental recovery of total, urea and ammonia exogenous nitrogen after 29 h was 61.2 ± 9.8, 57.7 ± 10.4 and 1.1 ± 0.2 mmol N, respectively. Both total and urea exogenous nitrogen excretions had not reached their asymptotic value at 29 h, unlike ammonia exogenous nitrogen.

View larger version (15K): [in this window] [in a new window]   Figure 3. Cumulative exogenous nitrogen recovered in human urine as (A) total nitrogen, (B) urea or (C) ammonia after ingestion of a [15N]-labeled soy protein isolate meal. The experimental values of cumulative urinary exogenous nitrogen can be fitted to a sigmoidal curve according to the equation y = b/(1 + exp[c(t-a)]) + d, in which t is time, and a, b, c and d are regression-estimated constants: for total nitrogen a = 7.61, b = 110.65, c = -0.096 and d = -36.95 (R2=0.9979); for urea nitrogen a = 8.62, b = 97.38, c = -0.1037 and d = -29.23 (R2=0.9979); and for ammonia nitrogen a = -56.15, b = 539.69, c = -0.1102 andd = -538.58 (R2 = 0.9946). Values are means + SD, n = 10. All means were significantly different from zero (t-test, P < 0.05)

View larger version (18K): [in this window] [in a new window]   Figure 4. Evolution as a function of time of the [15N]-labeled soy protein isolate meal deamination measured from the quantity of exogenous nitrogen incorporated in the urea pool of the body and in the total nitrogen pool in urine of human volunteers. The exogenous urea present in the body can be fitted to a curve according to the relationy = exp(-0.5[ln(t/t0)/ß]2), in which t is time, and , ß and t0 are regression-estimated constants; for body urea nitrogen = 20.42, ß = 1.09 and t0=5.89 (R2 = 0.9959). Values are means + SD, n = 10. All means are significantly different from zero (t-test, P < 0.05).

From the amount of dietary nitrogen absorbed, and from the amount deaminated, the PBV and the NPPU of soy protein isolate in humans could be determined (Table 1 ). A chemical score of 1.01 was calculated from the amino acid composition of SPI in comparison to the FAO/WHO (1990 ) indispensable amino acid reference pattern (Table 2 ).

	DISCUSSION

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A true oro-ileal digestibility of 91% was determined for SPI, and to our knowledge, there is no other study relating to true oro-ileal digestibility of soy protein in humans. For comparison, the corrected-apparent fecal digestibility (derived from nitrogen balance studies) of soy protein isolate ranges from 92 to 98% and is similar to the digestibility of beef (98%), egg (97–98%), and milk protein (95–98%) (Scrimshaw et al. 1983 , Wayler et al. 1983 , Young et al. 1984 ). These results take into account nitrogen absorbed in the colon, which is considered to be of poor nutritional importance (Rowan et al. 1994 ), but only partially take into account endogenous secretions by using a constant average factor, whereas endogenous secretions are influenced by the nature of the meal (Corring et al. 1989 ). In humans, a true fecal digestibility of a soy protein isolate was found to be 97% (Kayser et al. 1992 ). Sandstrom (1986 ), found apparent ileal digestibility of meat protein, in human ileostomy subjects, to be significantly reduced by a partial replacement of soy isolate and underscored the discre-pancy between ileal and fecal digestibility studies. In cannulated dogs, the apparent ileal digestibility of soy isolate is 83–87% (Zhao et al. 1997 ), whereas a recent study on pigs with a postvalve-T-cecum cannula and using [¹⁵N]-leucine labeling of endogenous nitrogen exhibited a higher true ileal digestibility of a soy concentrate of 97% (Grala et al. 1998 ). When compared to data from similar studies, this SPI diges-tibility of 91% is slightly higher than that of pea flour protein (89%) (Gausserès et al. 1996 ), but lower than that of milk protein concentrate (95%) (Gaudichon et al. 1999 ). Trypsin inhibitors, present in large quantity in raw soybeans impair the bioavailability of soy proteins. Through their processing into isolate, the content of trypsin inhibitors decreases (Anderson and Wolf 1995 ), but usually (and in the SPI used in this experiment) a heat treatment is added to the process to remove almost all of the trypsin inhibitor activity from the final product. With appropriate heat treatment, bioavailability of SPI is high, although lower than milk protein concentrate.

¹⁵N labeling enables not only the quantification and description of the amount of dietary nitrogen becoming available for metabolic action, but also the quantification and description of its bioutilization. Serial measures of both exogenous body urea and exogenous urinary nitrogen allow the estimation of the kinetics of deamination of the incoming exogenous amino acids. In the postprandial period, these amino acids are used intensely toward the repletion of postabsorptive losses (Garlick et al. 1980 ), while a fraction is irreversibly oxidized. A measure of the direct protein utilization for protein synthesis is assumed to be valid if it is assessed in the postprandial phase because it avoids accounting for postabsorptive losses, which are considered in nitrogen balance data (Millward and Pacy 1995 ). Nitrogen from the SPI meal was mainly oxidized during the first 3 h, then the rate of oxidation decreased. This confirms the hypothesis that dietary nitrogen that is not utilized by the body for synthetic purposes is rapidly deaminated. Considering the quickness of the majority of the exogenous deamination, the first pass effect appears as a major determining factor of final dietary amino acid retention within the body. SPI mixed with carbohydrates exhibited a high PBV of 86%. This means that 86% of the absorbed amino acids bypassed the oxidative processes during the 8 h following meal ingestion. This ability of the body to efficiently utilize dietary amino acids is indicative of a good nutritional value. Nevertheless, it should be stressed that this value is related to both the nature of the isolate (processing conditions) and to the composition of the meal (e.g., associated carbohydrates).

The present study focused on the assessment of bioavailability and acute efficiency of the utilization of soy protein nitrogen during the postprandial period. Bioavailability is the first determinant factor of protein quality (Kies 1981 ), and efficiency of nitrogen utilization is dependent on 1) the effect of dietary protein upon protein metabolism that enables repletion to occur and 2) the intrinsic quality of the protein allowing its utilization within protein synthesis. The NPPU method takes into account these factors that are highly relevant for protein quality evaluation. In addition, FAO/WHO (1990 ) has promoted the protein digestibility-corrected amino acid score for routine evaluation of dietary protein quality. The method is considered valid to evaluate properly processed and highly digestible proteins (Sarwar 1997 ). Yet, it is obvious that any method based on chemical evaluation needs to be validated against the direct measurement of the metabolic value in humans (Millward and Pacy 1995 , Sarwar and McDonough 1990 ). In this context, the NPPU method allows for the discrimination of nutritional quality between proteins. In a previous study using the same experimental design as in the present experiment (Gaudichon et al. 1999 ), milk protein concentrate NPPU was 85%, i.e., higher than the 78% of SPI, mainly because of a difference in digestibility (95% for milk protein vs. 91% for SPI) and in PBV (89% for milk protein vs. 86% for SPI). In the same way, an ileal digestibility of 89% and a NPPU of 73% for pea flour were previously determined (Gausserès et al. 1997 ). Under those conditions, the nutritional quality of SPI would represent 92% that of milk protein concentrate in humans. These differences of nutritional quality between protein in humans need to be further examined and compared to the chemical score methods. The consequences of the difference of nutritional quality between proteins that exhibit satisfactory NPPU, particularly in terms of dietary habit and nutritional advantage, remain to be studied.

	ACKNOWLEDGMENTS

 
The skillful assistance of the gastroenterology unit as well as the biochemistry laboratory of Avicenne Hospital (Bobigny, France) is gratefully acknowledged. The authors thank the Unité de formation et de Recherche Génétique et Amélioration des Plantes (INRA, Montpellier and Melgueil, France) for soybean [¹⁵N] labeling and Nestec Research Center (Lausanne, Switzerland) for SPI preparation.

	FOOTNOTES

 
¹ This work was supported in part by a grant from Arilait Recherche.

³ Abbreviations used: IRMS, isotopic ratio mass spectrometry; NPPU, net postprandial protein utilization; PBV, postprandial biological value; PSP, phenol red; SPI, soy protein isolate.

Manuscript received March 1, 1999. Initial review completed April 28, 1999. Revision accepted July 4, 1999.

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