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© 2007 American Society for Nutrition J. Nutr. 137:2431-2436, November 2007

Nutrient Requirements and Optimal Nutrition

Feeding Dietary Peptides to Growing Rats Enhances Gut Endogenous Protein Flows Compared with Feeding Protein-Free or Free Amino Acid-Based Diets1,2

Amélie Deglaire3,4,*, Paul J. Moughan3, Shane M. Rutherfurd3, Cécile Bos4 and Daniel Tomé4

3 Riddet Centre, Palmerston North, New Zealand 445 and 4 INRA, AgroParisTech, UMR914 Nutrition Physiology and Ingestive Behavior, CRNH-IdF, F-75005 Paris, France

* To whom correspondence should be addressed. E-mail: a.deglaire{at}massey.ac.nz.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
The effect of dietary peptides on gut endogenous nitrogen (N) flow (ENFL) and amino acid (AA) flow (EAAFL) was studied. Semisynthetic diets containing enzyme-hydrolyzed casein (HC; 11%) or a free AA mixture devoid of Asp and Ser (A1) or Gly and Ala (A2) were formulated to have similar AA compositions except for the excluded AA and similar dietary electrolyte balances (Na++K+–Cl–). A protein-free diet (PF) served as a control. Sprague-Dawley rats were given the diets 8 times/d for 10 min each hour for 7 d. Rats were killed and digesta were sampled (6 observations within each group) along the intestinal tract 6 h after the first meal on d 7. EAAFL and ENFL, estimated with reference to the dietary marker TiO2, were determined directly (PF, A1, and A2) or after centrifugation and ultrafiltration of the digesta (HC). Endogenous flows of Asp and Ser or Gly and Ala did not differ (P > 0.05) in any of the intestinal sections between rats fed PF and A1 or PF and A2, respectively, except in the stomach where Ser flow was greater for rats fed A1. Ileal endogenous flows for most of the AA and for N were higher (P < 0.05) for rats fed the HC diet compared with those for rats fed the PF, A1, or A2 diets, except for Phe, Tyr, Lys, which did not differ among the groups. Ileal EAAFL and ENFL were not influenced by body N balance per se but were affected by the presence in the gut of dietary peptides derived from casein.


   Introduction
TOP
 ABSTRACT
 Introduction
Materials and Methods
 Results
 Discussion
 LITERATURE CITED
 
It is important to be able to distinguish between amino acids (AA)5 of body origin (i.e. endogenous) present in digesta and those of dietary origin. Ileal endogenous AA flows (EAAFL), considered as losses to the body, are an important component of the daily dietary AA requirement in humans (1,2). A better understanding of factors influencing these endogenous losses is thus required.

Several methods are available for determining gut EAAFL. The protein-free diet (PF), although used routinely in dietary protein evaluation (3), creates a nonphysiological state (4) by inducing a negative body nitrogen (N) balance, which may lead to a decreased rate of whole body protein synthesis (5) and thus lowered gut EAAFL compared with protein alimentation (2,6,7). However, previous results suggest that body N balance per se does not affect EAAFL (6–8). Peptides arising from protein digestion may have a specific effect on gut protein secretion and reabsorption (6). The enzyme-hydrolyzed protein method was proposed as an alternative method to the PF diet for determining ileal endogenous protein losses routinely (9). This technique consists of measuring ileal endogenous N and AA under conditions in which the gut is supplied with dietary AA and peptides [hydrolyzed casein, molecular weight (MW) <5 kDa], mimicking the breakdown products of natural digestion. After digesta centrifugation and ultrafiltration (10 kDa, MW cutoff), endogenous protein is determined in the high fraction MW. Any undigested dietary AA (MW <10 kDa) are discarded as well as any small endogenous peptides and free AA, leading to some degree of underestimation of EAAFL. Nevertheless, application of the enzyme hydrolyzed protein method appears to lead to higher estimates of endogenous ileal protein losses than PF or synthetic AA diets (6,7,10), but this has not been assessed in a study whereby dietary electrolyte balance (DEB; Na++K+–Cl–) and dietary AA composition have been controlled. Our aim was to assess the effect on ileal endogenous protein flows consequent on feeding animals diets supplying similar AA either in the form of peptides (HC diet) or free L-AA (A1 and A2 diet) when DEB was adjusted to be similar in the various diets. A PF diet served as a control. The HC, A1, and A2 diets had similar AA compositions, except that Asp and Ser were omitted from diet A1 and Gly and Ala were omitted from the A2 diet, to enable direct determination of their endogenous losses (8). The omitted dietary nonessential AA were chosen as representative of different AA absorption mechanisms (11). Endogenous N and AA losses in rats fed the HC diet were determined using the hydrolyzed-protein/ultrafiltration technique (12).


   Materials and Methods
TOP
 ABSTRACT
 Introduction
 Materials and Methods
Results
 Discussion
 LITERATURE CITED
 
    Animals and housing. Forty-eight Sprague-Dawley male rats [242 ± 3 g bodyweight (BW)] were housed individually in raised stainless steel cages with wire mesh floors in a room maintained at 21 ± 2°C with a 12-h-light/-dark cycle. Food was given during the light cycle. Water was continuously available. Ethics approval was received from the Massey University Animal Ethics Committee (protocol 05/04).

    Diets. We prepared 4 semisynthetic test diets (Table 1), including a PF diet and diets containing as the sole source of N enzyme-hydrolyzed casein (HC diet) or a free L-AA mixture simulating the HC except for the omitted AA Ser and Asp (A1 diet) or Gly and Ala (A2 diet). All diets were formulated to meet the nutrient requirements of the growing rat (13). Dietary AA contents (Table 2), although lower in the HC diet than in the A1 and A2 diets, were in a comparable range. Sodium bicarbonate was added to the PF, A1, and A2 diets. The DEB in the final diets ranged from 158 (HC) to 216 ± 2 mEq/kg (PF, A1, and A2). Titanium dioxide was added to the diets as an indigestible marker. A standard casein-based preliminary diet was prepared.


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  		TABLE 1 Ingredient compositions of the preliminary, PF, A1, A2, and HC diets fed to growing rats

 

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  		TABLE 2 Nutrient and selected mineral contents of the PF, A1, A2, and HC diets fed to growing rats

 
Hydrolyzed casein was prepared (INRA) from native micellar casein extracted by microfiltration followed by diafiltration of milk (14). Casein solution (1:10 w:v) was heated up to 50°C, pig pancreatin was added with an enzyme to a substrate ratio of 0.0089 (pH 8.0, 50°C, 1 h 50 min), and was then inactivated (85°C, 20 min). The final product was freeze dried.

The MW profile was determined using an HPLC gel filtration column (TSKGel G2000SWXL, 30 cm, Phenomenex). The eluting solvent contained 36% acetonitrile and 0.1% trifluoroacetic acid, with detection at a wavelength of 205 nm; 21% of the peptides were 1–5 kDa in size and 79% were <1 kDa.

    Experimental design. For the entire study, rats received 8 meals/d given at hourly intervals and each for a 10-min period. The rats were acclimatized from d 0–9 while receiving the preliminary diet. The rats were then randomly allocated to the test diets (n = 12 per treatment), which they received from d 10 to d 17. Food intake was recorded daily. The rats were killed 6 h ± 15 min after the first meal as previously described (15). The stomach, the final 20 cm of ileum, and the cecum/colon were first removed. The remaining section of the small intestine was divided into 2 equal parts labeled proximal and medial intestine. Digesta were gently removed using ice-cold saline solution and immediately frozen at –20°C, then freeze-dried and ground.

    Chemical analysis. Digesta were pooled across randomly selected pairs of rats within each treatment to yield 6 digesta samples per treatment for each intestine section. Ileal digesta from rats fed the HC diet were divided into 2 portions to be analyzed in the original condition or after centrifugation and ultrafiltration (UF digesta). The latter portion was rehydrated overnight and then centrifuged (1400 x g; 30 min, 3 ± 1°C). The supernatant was ultrafiltered (Centriprep-10 devices, 10-kDa MW cutoff; Amicon) as described previously (16). The resulting retentate (MW >10 kDa) was added to the precipitate from the centrifugation step and freeze-dried and finally ground.

Diets and digesta samples were analyzed for TiO2, total N (TN), and AA. TN was determined using an elemental N analyzer (NA series 2, Fisons Instruments) (17). AA were determined after acid hydrolysis using a Waters ion exchange HPLC system (18). Met and Cys were measured as methionine sulfone and cysteic acid after performic acid oxidation (19). Met and Cys were not determined in HC ileal digesta because of limited sample size. TiO2 was determined by a colorimetric assay after ashing the sample and digestion of the minerals (20).

Minerals were determined in hydrolyzed casein. Na and K were analyzed after acid digestion using inductively coupled plasma optical emission spectrometry (21). The chloride ion was analyzed after weak acid extraction by potentiometric determination (21).

    Data analysis. Gut AA flow (AAFL) and N flow (NFL) [µg/g dry matter intake (DMI)] were determined as follows:

Formula 1(Eq. 1)

Total (dietary and endogenous) NFL were calculated using Eq. 1 in digesta from rats fed the HC diet before any processing. Endogenous NFL (ENFL) and EAAFL were calculated using Eq. 1 in digesta from rats fed the PF diet and in UF digesta from rats fed the HC diet. EAAFL of the omitted AA were determined directly in digesta from rats fed diets A1 and A2.

Apparent ileal digestibility (AID) and standardized digestibility (SID; %) of AA (or N) were calculated as follows:

Formula 2(Eq. 2)


Formula 3(Eq. 3)

The N contents of individually determined AA were summed to give an estimate of {alpha}-amino N ({alpha}-AN). The terminology "standardized digestibility" was used as defined by Stein et al. (22) and relates to the previously used term "true digestibility."

Data were tested for homogeneity of variance using Bartlett's test and then subjected to a 1-way ANOVA (SAS, version 8.2). The food intake data were subjected to a 1-way ANOVA for repeated measures. For P < 0.05, the significance of differences between means was determined using Tukey's test. Results are given as means ± SE.


   Results
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
Discussion
 LITERATURE CITED
 
The rats receiving the PF diet lost BW (7.0 ± 1.8 g), whereas rats fed the A1, A2, and HC diets had similar (P > 0.05) BW gains (17.2 ± 2.4, 17.9 ± 2.4, 17.4 ± 1.5 g, respectively). Daily food intakes were lower (P < 0.01) for rats fed the PF diet (10.4 ± 0.4 g/d) than for those fed the A1 (14.7 ± 0.5 g/d), A2 (14.8 ± 0.5 g/d), and HC (15.5 ± 0.5 g/d) diets.

The endogenous flows of Asp and Ser were similar between rats fed the PF and A1 diets but were lower (P < 0.001) than those for rats fed the HC diet (Table 3). The endogenous flow of Ala was similar between rats fed the PF and A2 diets but was lower (P < 0.001) compared with that of rats fed the HC diet. On the contrary, the endogenous flow of Gly was higher (P < 0.05) for rats fed the PF and A2 diets than that for rats fed the HC diet (Table 3). Endogenous flows of Asp and Ser or Ala and Gly were not significantly different (P > 0.05) in any of the intestinal sections between rats fed the PF and A1 diets or the PF and A2 diets, except for the flow of Ser in the stomach, which was greater for rats fed the A1 diet than for those fed the PF diet (Table 3). EAAFL were considerable in the stomach and in the proximal intestine and thereafter declined to lower and relatively constant flows.


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  		TABLE 3 EAAFL along the digestive tract of growing rats fed PF, A1, A2, and HC diets1

 
The AID of AA were not significantly different (P > 0.05) between rats fed diets A1 and A2, except for the AID of His and Arg (data not shown). A similar result was found for the SID of AA. AA digestibilities were thus pooled across diets A1 and A2 (Table 4). Most AA (Table 4) had a SID close to 100%, except for Cys (63.3%), indicating that they were fully absorbed prior to the end of the ileum. Therefore, we assumed that their ileal flows were endogenous (Table 5). For several of the AA, the pattern of their endogenous flows was similar to that found for the omitted AA (Asp, Ser, and Ala) with no significant difference between rats fed PF, A1, and A2 diets but with a higher (P < 0.05) flow in those fed the HC diet. Flows of Phe, Tyr, and Lys did not differ in the rats fed the different diets. For His, the endogenous flow was lower for rats fed the HC diet than for those fed PF or A1 diets, whereas for Arg, the endogenous flows for rats fed the HC, A1, and PF diets were similar. Of note, the endogenous Met flows for rats fed diets A1 and A2 were higher (~2 times; P < 0.05) compared with that for rats given the PF diet.


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  		TABLE 4 Apparent and standardized ileal AA digestibility for growing rats fed the synthetic AA-based diets A1 and A21

 

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  		TABLE 5 Endogenous ileal AAFL measured in rats fed PF, A1, A2, and HC diets1

 
Ileal ENFL were not significantly different (P > 0.05) in rats fed the PF, A1, and A2 diets but were significantly lower compared with rats fed the HC diet (Table 6). We found a corresponding result for the endogenous flows of {alpha}-AN, the values for which were 628 ± 57 for rats fed the PF diet, 637 ± 29 for rats fed the A1 diet, 647 ± 40 for rats fed the A2 diet, and 1071 ± 56 for rats fed the HC diet. The total NFL for rats fed the HC diet was 1428 ± 194 µg/g DMI.


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  		TABLE 6 Ileal ENFL and N digestibility in rats fed PF, A1, A2, and HC diets1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
LITERATURE CITED
 
EAAFL at the terminal ileum have been compared previously in rats fed PF, synthetic AA, or HC-based diets, revealing a possible stimulatory effect of peptides on gut secretions (6,7,12,23,24). EAAFL and NFL have not, however, hitherto been directly compared where diet AA composition and DEB have been controlled.

DEB, in particular, may be an important consideration when determining endogenous AA losses, because it has been reported to influence the AID of N (25). Enzyme-hydrolyzed casein contains a high amount of sodium, so in this study, NaHCO3 was added to the PF, A1, and A2 diets to ensure comparable DEB. The TN content of diets A1 and A2 was lower than that of the HC diet, because AA were purposefully omitted from the diet AA mixtures and no correction was made for the N from the carboxyamide groups of Gln and Asn lost during AA analysis of the HC. The {alpha}-AN content was similar in the A1, A2, and HC diets.

Ileal endogenous flows of Asp, Ser, Gly, and Ala were similar in rats fed diets A1 and A2 (devoid of these particular AA) and in rats fed the PF diet, which is consistent with earlier data (7,8). When endogenous ileal AAFL were determined for the other AA, assuming a virtually complete absorption of the synthetic AA, flows were generally similar to those observed for the PF diet. Methionine was an exception whereby the flow was much lower for the PF diet. The ENFL for rats fed the PF diet were in agreement with earlier data (15,23,26) and were similar to those for rats fed diets A1 and A2. These findings confirm the observation that body N balance per se does not influence gut endogenous protein losses in the growing rat. A similar observation has been made in pigs fed a PF diet with a simultaneous i.v. AA infusion (27,28).

The ileal EAAFL in rats fed the HC diet were in the range of previous estimates (7,12,16,23,24,29). The HC diet generally resulted in higher EAAFL compared with the PF diet, which is consistent with earlier findings in rats (7,12,23,30), pigs (27,31,32), and humans (2). The difference in our study was of a lower magnitude than previously reported (7,12,23,30).

A higher endogenous flow of Gly was observed for the PF feeding, which has also been noted previously (8,29,33). This has been suggested to be directly related to the protein-free condition of the animals, because an i.v. infusion of AA to pigs fed a PF diet numerically decreased Gly flow (27,28), which is consistent with the effect observed here when synthetic AA were ingested. It is important to note, however, that the differences were not significant in either study. An underestimation of Gly flow may occur with the centrifugation and ultrafiltration technique, thus explaining the low Gly flow for the HC diet. Gly is one of the predominant AA in bile acids (34) and whereas most of the bile salt conjugates are reabsorbed after intestinal bacteria hydrolysis, substantial amounts of deconjugated Gly escape reabsorption and are thus discarded after digesta ultrafiltration (30). The overall degree of underestimation of endogenous N is, however, likely to be low in our study, because only 7% of the TN was removed in UF digesta, whereas previous studies reported values of 13–24% (27,33,35).

The present findings suggest that gut endogenous protein losses are increased by peptides derived from casein but not by free AA. This presumably results from lower reabsorption and/or higher secretions of endogenous N and AA. The activity of the L-AA transporters or the di-/tri-peptide transporters, regulated through complex mechanisms, is possibly influenced by dietary AA and N after several days of feeding (36,37). However, a similar brush border AA and peptide uptake was reported in mice fed for 14 d diets based on peptides or free AA, both simulating casein (38). The higher endogenous protein losses induced by dietary peptides are more likely due to enhanced proteic secretions. Endogenous protein losses are composed mainly of mucins, enzymatic secretions, sloughed cells, and bacteria (technically nondietary rather than endogenous) (39). Dietary peptides are known to stimulate pancreatic secretions more effectively than do free AA (40,41) and the degree of AA polymerization has been shown to influence small bowel mucosa growth rate (42–45). A higher distal (but not proximal) gut growth rate has been observed in rats fed for 10 d a diet based on casein-derived peptides compared with rats fed a free AA-based diet (42). This would theoretically result in higher mucosa sloughing and possibly higher ileal endogenous N losses in rats fed dietary peptides. However, a lower rate of mitosis per crypt was observed in the jejunum from rats fed for 4 d diets based on whey-derived peptides compared with free AA (43). Recently, bioactive peptides, such as ß-casomorphins (0.5–1 kDa MW), have been shown to induce mucus secretion in rat jejunum (46). Bioactivity, however, is related to the size and nature of the peptide (47) and is likely affected by protein hydrolysis conditions. There may be specific effects of dietary peptides from a prehydrolyzed protein vs. peptides naturally released during casein digestion (31).

This work demonstrates that feeding dietary peptides induces increased endogenous ileal N and AAFL compared with feeding a PF diet or diets containing only free AA, which yield similar estimates of endogenous ileal NFL and AAFL. This suggests that EAAFL and ENFL are not influenced by body N balance per se but rather by the presence of dietary peptides in the gut lumen. Further investigation is required to determine whether this is a specific effect of dietary peptides compared with peptides released during protein digestion in the gut and if this is a specific effect of casein-derived peptides. The underlying mechanisms need to be understood.


   ACKNOWLEDGMENTS
 
We thank Anne Singh for providing us with the pig pancreatin.


   FOOTNOTES
 
1 Supported by grants from the Riddet Centre (Massey University, Palmerston North, New Zealand) and INRA (Paris, France). Back

2 Author disclosures: A. Deglaire, P. J. Moughan, S. M. Rutherfurd, C. Bos, and D. Tomé, no conflicts of interest. Back

5 Abbreviations used: A1, free amino acid-based diet 1; A2, free amino acid-based diet 2; AA, amino acid; AAFL, amino acid flow; {alpha}-AN, {alpha}-amino nitrogen; AID, apparent ileal digestibility; BW, bodyweight; DEB, dietary electrolyte balance; DMI, dry matter intake; EAAFL, endogenous amino acid flow; ENFL, endogenous nitrogen flow; HC, hydrolyzed casein-based diet; MW, molecular weight; NFL, nitrogen flow; PF, protein-free diet; SID, standardized ileal digestibility; TN, total nitrogen; UF, ultrafiltration. Back

Manuscript received 18 May 2007. Initial review completed 28 June 2007. Revision accepted 23 August 2007.


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 ABSTRACT
 Introduction
 Materials and Methods
 Results
 Discussion
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A. Deglaire, P. J. Moughan, C. Bos, K. Petzke, S. M. Rutherfurd, and D. Tome
A Casein Hydrolysate Does Not Enhance Gut Endogenous Protein Flows Compared with Intact Casein When Fed to Growing Rats
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