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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:3076-3082, November 2004

Nutrient Metabolism

Ileal Endogenous Nitrogen Recovery Is Increased and Its Amino Acid Pattern Is Altered in Pigs Fed Quebracho Extract1,2

C. A. (Carina) Steendam3, Seerp Tamminga, Huug Boer, Erik-Jan de Jong, G. Henk Visser* and Martin W. A. Verstegen

Animal Nutrition Group, Wageningen Institute of Animal Sciences (WIAS), Wageningen University and Research Centre, 6700 AH Wageningen, The Netherlands and * Centre for Isotope Research, University Groningen, Groningen, The Netherlands

3To whom correspondence should be addressed. E-mail: Carina.Steendam{at}wur.nl.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Ileal endogenous nitrogen recovery (ENR) in pigs (9 ± 0.6 kg body weight) was estimated simultaneously using the 15N-isotope dilution technique (15N-IDT) and the peptide alimentation ultrafiltration (UF) method. Diets were cornstarch, enzyme-hydrolyzed casein with no (control) or high (4%) content of quebracho extract (Schinopsis spp.) rich in condensed tannins. The amino acid (AA) pattern of the ENR was also determined. The ENR of pigs fed the quebracho diet was higher (P = 0.0001) than that of pigs fed the control diet [6.00 vs. 1.95 g/kg dry matter intake (DMI) for the 15N-IDT and 5.18 vs. 1.49 g/kg DMI for the UF method, respectively]. With the 15N-IDT, ENR values were 0.44–0.79 g/kg DMI (24%) higher (control P = 0.0032, quebracho P = 0.0002) than for the UF method. Apparent nitrogen digestibility depended on diet (69.0% quebracho vs. 86.0% control, P = 0.0001). Real nitrogen digestibility (RD-N) determined by the UF method was higher (P = 0.0001) for the control than for the quebracho diet (91.4 vs. 88.2%). Corresponding values for the 15N-IDT did not differ (P = 0.0569) between diets (92.8 vs. 91.4%). The 15N-IDT gave higher values for RD-N of both diets (control P = 0.0030, quebracho P = 0.0002) compared with the UF method. Endogenous AA recoveries (g/kg DMI) were increased 300% (P = 0.0001) and the AA-pattern of ENR was changed (P from 0.0001 to 0.7530 for different AA) by the quebracho diet. A constant AA-pattern of ENR cannot be assumed. Despite limitations of both techniques, the 15N-IDT and the UF method gave similar results with respect to ENR.

KEY WORDS: • quebracho extract • 15N-isotope dilution technique • peptide alimentation ultrafiltration • endogenous amino acids • condensed tannin

Insight into the amount of endogenous nitrogen recovered (ENR)4 at the terminal ileum gives better estimates of amino acid (AA) requirements (1) and real digestibility of food and feed (2). In pig production, it can ultimately lead to reduced N in waste entering the environment without decreasing production levels (3). Various dietary factors such as trypsin inhibitors, lectins, tannins, and cell walls increase ENR (3,4). There are several methods with which to estimate ENR (2). In the present study the 15N-isotope dilution technique (15N-IDT) (5–7) and the peptide alimentation ultrafiltration (UF) method (8–10) were evaluated with respect to their suitability for estimating ENR and real ileal N digestibility (RD-N).

In this context, the 15N-IDT was described and discussed by several authors (11–13) and also in our previous study (14). In the UF method, animals or subjects are fed a highly digestible diet that contains low-molecular-weight (<5000 Da) protein. After collection, the ileal digesta is divided into 2 fractions by centrifugation followed by UF. The division is at 10,000 Da. The protein that is found in the fraction > 10,000 Da is considered to be of endogenous origin (15). However, the major disadvantage of the UF method is that neither the basal diet nor the test substances can contain N in the form of a complex, large-molecular-weight protein. Furthermore, it ignores the contribution of small-molecular-weight endogenous secretions, such as peptides and AAs, to the total ENR (16).

On the other hand, with the UF method, it is possible to determine the AA pattern of the ENR. It was suggested previously that the AA pattern of ENR was not influenced by the diet (17). However, inclusion of condensed tannins from quebracho in the diet was shown to increase salivary proline rich protein recoveries in rats and other rodents (18,19).

Quebracho extract (from heartwood of Schinopsis spp.), which contains relatively high proportions of condensed tannins [profisitinidines and prorobinetinidins, (20)] has been used as a model for tannins in food and feed (20,21). It has been used in the tanning industry because of its ability to bind proteins (22,23). Reduced apparent N digestibility (AD-N), due to both increased ENR and decreased RD-N, was reported by Mole and co-workers (24). This effect was also found for other condensed tannins (25). Other effects include reduced feed intake and growth (19,26), increased bile salt excretion (27), and lower liver vitamin A content (28). The present study was performed to estimate the effect of dietary quebracho extract on ENR and the AA pattern of ENR, using the 15N-IDT and the UF method.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Details of the materials and methods were described in our previous study (14). New information is presented below.

    Experimental design. Within the 15N-IDT, the tracer was administered either orally or by i.v. infusion. We reported previously that the method of tracer administration did not influence estimates of ENR (14). Dietary treatments were allocated according to a crossover design. The effect of method of ENR estimation was tested with a paired t test.

    Sample preparation and analyses. For the UF method, freeze-dried digesta and feed samples (control diet) were rehydrated and subjected to UF according to Butts et al. (9) with centrifugation at 7000 x g instead of 1650 x g. The precipitate (P) and retentate (R) fractions were combined. The P+R and ultrafiltrate (UF) fraction were analyzed for dry matter (DM), Kjeldahl-N, and 15N enrichment. Amino acid analysis samples of the P+R fraction and feed were done according to Kohler et al. (29). Bile acids were extracted from freeze dried digesta by heating for 30 min at 37°C with 1 mL of a mixture of t-butanol and water (1:1, v:v) and subsequently analyzed according to Xu et al. (30).

    Calculations and statistics. Within the 15N-IDT or UF method, the effect of diet (D) was tested as follows:

(1)

where µ is the mean, Si is sequence of dietary treatment (i = 1,2). Si is tested against Pigj within sequence as an error term (j = 1–12), Dk is the effect of diet (l = 1,2), Pl is the effect of period (l = 1,2), and eijklm is the overall error (n = 1–24). Sequence of dietary treatment and period were added as correction factors.

Differences between methods (ENR 15N – ENRUF) were tested with a paired t test (Tukey, model 1). A Diet effect on the difference between methods indicates a Method x Diet interaction.

For the UF method, endogenous DM, N, and AA recoveries (EDMR, ENR, and EAAR in g/d or in g/kg DMI) were calculated from the digesta DM flow (g/d or g/kg DMI), the dry matter recovery in P+R (>10 kDa, P + RDM, g DM/kg digesta DM) and the N or AA content of the P+R fraction (g/kg DM):

(2)

and

(3)


(4)

The real N digestibility (RD-N, %) was calculated by correcting the AD-N for the endogenous N recovery:

(5)

with Ndig in g/g DM and DM flow, ENR, and N intake in g/d.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
On average, 6% of the AA (and 5% of N) in the rehydrated control diet were retrieved in the precipitate + retentate (P+R) fraction (Table 1) and were, therefore, part of the pool of molecules larger than 10 kDa.


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  		TABLE 1 AA content of the EHC control diet fed to pigs and of its precipitate + retentate fraction (P + R)1, 2

 
For both methods, the ENR in pigs fed the quebracho diet was higher (P = 0.0001) than in pigs fed the control diet (Table 2). There was also an effect of method of determination, with the 15N-IDT giving the highest ENR for both the control (P = 0.0032) and quebracho (P = 0.0002) diets. There was a Method x Diet interaction (P = 0.0156); differences in ENR between methods were slightly higher for pigs fed the quebracho diet than for pigs fed the control diet.


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  		TABLE 2 Apparent (AD-N) and real (RD-N) ileal nitrogen digestibility of the EHC control diet and the quebracho extract diet and ileal ENR in pigs1

 
The AD-N decreased (P = 0.0001) after feeding the quebracho diet (Table 2). The RD-N determined by the UF method was higher (P = 0.0001) for the control diet than for the quebracho diet (Table 2). When the 15N-IDT was used, this effect was not significant (P = 0.0569). The latter method gave higher (control P = 0.0030 and quebracho P = 0.0002) values for RD-N of both diets compared with the UF method. There was a Method x Diet interaction (P = 0.0148); differences in RD-N between methods were slightly higher for pigs fed the quebracho diet than for pigs fed the control diet.

With the UF method, the recovery of digesta DM after centrifugation and UF was 103% for both diets (Table 3). The N recovery was 95% (control) and 96% (quebracho). The distribution of DM and N over the P+R and UF fractions differed between diets. For the quebracho diet, a higher (P = 0.0001) proportion of DM and N was recovered in the endogenous (P+R) fraction compared with the control diet. Dilution factors of the P+R fraction were higher for the quebracho diet (P = 0.030) compared with the control diet, whereas the DF of the UF fraction was lower (P = 0.0151, Table 3).


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  		TABLE 3 Recovery of DM and N in precipitate + retentate (P + R) and ultrafiltrate (UF) from ileal digesta of pigs fed the EHC control diet and the quebracho extract diet, and 15N-enrichments of these fractions expressed as DF compared with 15N-enrichment of trichloroacetic acid-soluble plasma1, 2, 3

 
Endogenous AA recoveries (g/kg DMI) were increased ~300% (P = 0.0001) by feeding the quebracho extract (Table 4). The AA pattern (g AA/160 g N) of the endogenous protein recoveries was altered by the quebracho extract (Table 5). The AA composition was shifted toward increases in proline, arginine, glycine (all P = 0.0001) and leucine (P = 0.0003) content and, to a lesser extent, more tyrosine (P = 0.0012), methionine (P = 0.0003), phenylalanine (P = 0.0032), and alanine (P = 0.0028). Threonine (P = 0.0063), glutamic acid, serine (both P = 0.0001), and isoleucine (P = 0.0456) contents were lowered in the ENR of pigs fed the quebracho extract diet.


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  		TABLE 4 Endogenous AA recoveries in ileal digesta of pigs fed the EHC control diet and the quebracho extract diet1, 2, 3

 

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  		TABLE 5 Endogenous AA recoveries in ileal digesta of pigs fed the EHC control (C) diet and the quebracho (Q) extract diet and as found in studies in literature1, 2

 
The bile acid concentration of the digesta was 19.9 (control) and 9.49 (quebracho) g/kg digesta DM (P = 0.0001). Due to increased digesta flow, the total bile acid flow of pigs fed the quebracho diet was 3.63 g/kg DMI, which was higher (P = 0.0039) than the 2.24 g/kg DMI of pigs fed the control diet.


   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
    Endogenous nitrogen recoveries. The ENRs of 1.5–1.9 g/kg DMI determined for pigs fed the control diet [180 g enzyme-hydrolyzed casein (EHC)/kg feed] were lower compared with most reports on pigs in which levels of dietary EHC ranged from 180 to 200 g/kg feed. These reports showed ENRs ranging from 2.5 to 5.9 g/kg DMI (9,31,32). They were comparable, however, to ENRs of 1.5–1.9 g/kg DMI in studies with 50 (33), 100 (34), and 114 (16) g EHC/kg feed. Differences in the level of protein intake, and the diet and weight of pigs reported in other studies would partially explain the variation of results from the present study.

The addition of quebracho extract to the diet increased the ENR 3–3.5 times above values of ENR for control-fed pigs. This difference was due to the combined effect of condensed tannins, tannic acid, and possibly fiber, present in the extract. Similar ENR increases were reported in chicks fed protein-free diets with the addition of 1.4% tannic acid (35). The addition of tannin-rich faba bean hulls to a casein-based diet increased the ENRs in 10- to 26-kg pigs from 2.62 to 5.10 g/kg (25). However the increase with cotton seed hulls, rich in condensed tannins, fed to rats was much less than in our study [from 1.4 to 1.6 g/kg DMI (36)]. In the latter study, effects were ascribed to fiber.

    N digestibility. The AD-N of the control diet (86%) was higher than literature values, which range from 77 to 81% (7,16,31). The RD-N of both diets were in the range of 91–97% as reported in the literature (7,31), with the exception of an 88.1% estimate for the quebracho diet using the UF method. This value is in agreement with the real AA digestibility of 85% for an EHC diet reported by Leterme and co-workers (16).

Jansman et al. (25) estimated that after adding dietary tannin in faba beans, only 50% of the decrease of AD-N is caused by increased ENR. In the present study, a much higher proportion of decrease in AD-N was caused by increased ENR. Depending on the method of ENR estimation, this was 75% (UF) or 94% (15N-IDT). Differences between studies may be caused by different tannin sources.

    Methods of estimation. The 15N-IDT and UF method gave different results for both ENR and RD-N. These differences were higher (P = 0.015) for pigs fed the quebracho diet than for pigs fed the control diet. However, diets were not ranked differently when using either method.

Estimates of ENR determined by the 15N-IDT were 24 and 14% higher for the control and quebracho diets, respectively, than values measured using the UF method. Hodgkinson et al. (34) found greater (46%) overestimation of ENR for the control diet using the 15N-IDT. However, one should keep in mind that the absolute differences are small. The higher values for the 15N-IDT are in line with the general perception that the 15N-IDT overestimates the ENR (11–13,37). This is in contrast, however, with results found by Schulze et al. (31), who reported that there were no differences between the methods. In another study, the homo-arginine method gave 26% higher ENR values than the 15N-IDT (38).

If both the 15N-IDT and the UF method were 100% correct, then, by definition, the P+R fraction contains only endogenous N and all endogenous N is labeled to the same extent as N in trichloroacetic acid–soluble plasma. Ideally, then, the DF of P+R should be exactly 1. However, they were 0.7 and 0.9 for the control and quebracho group, respectively. This could indicate that the choice of precursor pool (14) gave rise to a relative underestimation of ENR in P+R of 30% (control) or 10% (quebracho). The other possibility is that the UF method leads to an overestimation of endogenous N in the P+R fractions of 30 and 10% for the control and quebracho group, respectively.

A similar overestimation for the UF method is found when we look at the recovery of feed N in the >10 kDa (P+R) fraction. With the exception of tyrosine (35%) and cystine (16%), on average, 6% or less of AA from feed was recovered in the P+R fraction (>10 kDa) after centrifugation and UF of feed (control diet). A similar value of 2.5–6% of EHC was found by Hodgkinson et al. (39). In their study, centrifugation was at 1650 x g instead of the 7000 x g as in the present study. Apparently, the higher centrifugation speed did not influence the fraction of small protein molecules being trapped in the P+R fraction. In the present study, the N intake was 200% higher and the ENR was lower, leading to an overestimation of ENR of 18% (control) or 10% (quebracho). This is much higher than the 2% overestimation reported by Hodgkinson et al. (39) but similar to the 20–27% overestimation in pigs fed a protein-free diet (16).

Sterical hindering of enzyme hydrolysis of the peptide bonds in casein in the proximity of tyrosine, may explain the high proportion of feed tyrosine that was recovered in the P+R fraction. Another cause may be hydrophobic interactions between tyrosine-containing peptides (Kerry BioScience, personal communication).

Formation of a tannin-EHC complex larger than 10 kDa could explain in part the overestimation of the ENR for the quebracho diet. However, condensed tannins have a preference for binding to proline in large, loosely structured molecules with MW > 600 Da (40) cited by (22,41). The quebracho tannins have an especially high specificity and affinity for salivary protein (22). This makes EHC-tannin complex formation unlikely as was confirmed by the DF of the large molecule fraction increasing after the addition of quebracho to the diet.

It should also be mentioned that the ultrafiltrate fractions should not be enriched above baseline because ideally these do not contain endogenous N. However, labeling of the ultrafiltrate fractions showed that 0.78 g (control) or 0.88 g (quebracho) ENR/kg DMI is smaller than 10 kDa. This leads to an underestimation of ENR for the UF method of 52% (control) or 17% (quebracho). For this reason Hodgkinson et al. (42) suggested the use of 3000 Da as a cutoff value. This depends, however, on particle size of the EHC because it will increase the fraction of feed N in the ENR.

In summary, it can be argued that neither method provides quantitative values for ENR. The 15N-IDT may overestimate ENR, but does not always give higher values than other methods. The UF method, on the one hand, neglects small-molecular-weight ENR and, on the other hand, incorrectly labels large molecular feed N as ENR. In sum, it underestimates ENR but absolute values of errors within the UF method differ slightly between diets.

    Amino acid pattern of endogenous recoveries. The AA pattern of ENR in pigs fed an EHC-based diet differed between studies [see Table 5, (16,17,31,43,44)]. The ENR for the control diet of the present study was especially high in isoleucine and serine. Studies with rats showed even higher values for these 2 AAs (15,36,45). The ENR was somewhat lower in glycine compared with literature values (31,33). The glycine content was similar to literature values for rats (45).

Data on AA pattern of ENR after feeding tannins to pigs are not available. In chicks fed a protein-free diet (35), tannic acid shifted the AA pattern toward more histidine, arginine, asparagine, leucine, and tyrosine (Table 6). On the other hand, valine decreased. This is not consistent with the results from the present study. The change in AA pattern of ENR observed after feeding quebracho extract agrees only partially with values for rats fed cottonseed hulls (CSH) [Table 6; (36)] in which effects were ascribed to fiber. As such, CSH increased the relative amount of arginine, leucine, and phenylalanine, which is consistent with the effect of quebracho extract. On the other hand, the increase in threonine and glutamic acid content in the aforementioned study was in contrast to the effects determined in the present study. In summary, differences in tannin sources have variable effects on AA pattern.


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  		TABLE 6 Effect of dietary quebracho extract, tannic acid, and cottonseed hulls on the amount of individual AA (relative to lysine) of ENRs compared with their respective control diets1

 
The high proline and glycine and low serine contents of the ENR after feeding quebracho suggest 3 possible sources of endogenous AAs. These are proline-rich proteins (PRPs), glycoproteins from mucus, and glycine from deconjugated bile salts.

PRP in humans and rats are rich in proline (30–34 mol%), glycine (17–21 mol%), glutamine (19–21 mol%), and asparagine (7–12 mol%) (18). PRP from pig saliva has a higher proline content (45%) and lower glutamine + glutamate (10%) and glycine (15%) content compared with humans and rats (19). An increase in PRP would be consistent with the change in AA pattern that was found in the present study.

Glycoproteins from mucins are rich in nonessential AAs (proline, serine, cystine) and threonine (12,46). Gastric mucin is especially rich in serine (12). However, the serine content of ENR was lowered after feeding quebracho. A decrease in the relative amount of glycoproteins from mucus by feeding quebracho would explain the decrease in serine and glutamine content of the endogenous recoveries in the present study. This is similar to the effect of tannic acid infused into the stomach of rats causing a decrease in concentrations of mucin in gastric juice (47). However, the study of Jansman and co-workers (4) reported a detrimental effect of tannic acid on gastrointestinal mucosa. Orally fed tannic acid was also shown to increase sloughing of esophageal mucosa in chicks (48) and led to hypersecretion of gastric mucus with necrotic effects on gastric mucosa in rats (49).

Glycine accounts for almost 95% of the total AA content of bile (50); therefore, bile could be the origin of the increased glycine content of the ENR in the present study. Pigs fed the quebracho diet had a higher total bile excretion per day, which is in agreement with the increased bile salt excretion in the feces of rats (27). However, the concentration of bile acids in ileal digesta (g/kg DM) was decreased. Therefore, bile secretion does not explain the increased glycine content of ENR. In summary, the change in AA pattern indicates that quebracho increased the amount of PRP and possibly decreased mucin content. Bile was not the likely source of extra glycine.

It can be concluded that quebracho extract increased the ENR by 300%. The UF method gave lower ENR estimates than the 15N-IDT. Recovery of feed N in the P+R fraction and 15N enrichment of the UF and P+R fractions indicated that the UF method underestimated ENR, whereas the 15N-IDT overestimated ENR. Despite previously discussed limitations, both techniques gave similar results.

The AA pattern of ENR for the EHC control diet was within the range of values reported in literature. Feeding quebracho extract altered the AA pattern of ENR. Changes in AA pattern were likely caused by an increase in the amount of proline-rich salivary proteins, possibly along with a decrease in gastric mucin. In this context, a constant AA pattern of ENR cannot be assumed, and it should be determined in each study.


   ACKNOWLEDGMENTS
 
The help of Stefano Mattuzzi with digesta ultrafiltration was much appreciated.


   FOOTNOTES
 
1 Presented in part at the Third International Workshop on Antinutritional Factors in Legume Seeds and Rapeseed, July 8–10, 1998, Wageningen, The Netherlands [Steendam, C. A., de Jong, E. J., Mattuzzi, S. & Visser, G. H. (1998) Comparison of three methods for the measurement of the endogenous N-flow at the terminal ileum of pigs, as affected by dietary quebracho extract. Recent advances of research in antinutritional factors in legume seeds and rapeseed EAAP publication no 93: 335–340(abs.)] and at the 91st Annual Meeting of the American Society of Animal Science, July 21–23, 1999, Indianapolis, IN [Steendam, C. A., Tamminga, S. & Verstegen, M.W.A. (1999) Effect of tannin-rich quebracho extract on ileal endogenous amino acid losses in pigs. J. Anim. Sci. 77 (suppl. 1): 198 (abs.)]. Back

2 Supported by the Netherlands Organization for Scientific Research (NWO). Back

4 Abbreviations: AA, amino acid; AD-N, apparent nitrogen digestibility; CSH, cottonseed hulls; DF, dilution factor; DM, dry matter; DMI, dry matter intake; EAAR, endogenous amino acid recovery; EDMR, endogenous dry matter recovery; EHC, enzyme-hydrolyzed casein; ENR, endogenous nitrogen recovery; 15N-IDT, 15N isotope dilution technique; PRP, proline-rich protein; RD-N, real nitrogen digestibility; UF, peptide alimentation ultrafiltration method. Back

Manuscript received 29 April 2004. Initial review completed 28 June 2004. Revision accepted 27 August 2004.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

1. Gaudichon, C., Bos, C., Morens, C., Petzke, K. J., Mariotti, F., Everwand, J., Benamouzig, R., Dare, S., Tome, D. & Metges, C. C. (2002) Ileal losses of nitrogen and amino acids in humans and their importance to the assessment of amino acid requirements. Gastroenterology 123:50-59.[Medline]

2. Nyachoti, C. M., de Lange, C.F.M., McBride, B. W. & Schulze, H. (1997) Significance of endogenous gut nitrogen losses in the nutrition of growing pigs: a review. Can. J. Anim. Sci. 1:149-163.

3. Tamminga, S., Schulze, H., van Bruchem, J. & Huisman, J. (1995) The nutritional significance of endogenous N-losses along the gastro-intestinal tract of farm animals. Arch. Anim. Nutr. 9:22-44.

4. Jansman, A.J.M. (1993) Tannins in faba beans (Vicia faba, L.). Antinutritional properties in monogastric animals. Department of Animal Nutrition 1993:207 Wageningen Agricultural University Wageningen.

5. Souffrant, W. B., Kohler, R., Matkowitz, R., Gebhardt, G. & Schmandke, H. (1981) Nutritional physiology studies in pigs on the evaluation of modified proteins. 2. Estimation of endogenous nitrogen in the contents of the small intestine by the 15N tracer method. Ernahrungsphysiologische Untersuchungen an Schweinen zur Beurteilung von modifizierten Proteinen. Arch. Anim. Nutr. 31:675-683.

6. de Lange, C.F.M., Souffrant, W. B. & Sauer, W. C. (1990) Real ileal protein and amino acid digestibilities in feedstuffs for growing pigs as determined with the 15N-isotope dilution technique. J. Anim. Sci. 68:409-418.[Abstract]

7. Moughan, P. J., Buttery, P. J., Essex, C. P. & Soar, J. B. (1992) Evaluation of the isotope dilution technique for determining ileal endogenous nitrogen excretion in the rat. J. Sci. Food Agric. 58:165-172.

8. Darragh, A. J., Moughan, P. J. & Smith, W. C. (1990) The effect of amino acid and peptide alimentation on the determination of endogenous amino acid flow at the terminal ileum of the rat. J. Sci. Food Agric. 51:47-56.

9. Butts, C. A., Moughan, P. J., Smith, W. C., Reynolds, G. W. & Garrick, D. J. (1993) The effect of food dry matter intake on endogenous ileal amino acid excretion determined under peptide alimentation in 50 kg liveweight pig. J. Sci. Food Agric. 62:235-243.

10. Butts, C. A., Moughan, P. J., Smith, W. C. & Carr, D. H. (1993) Endogenous lysine and other amino acid flows at the terminal ileum of the growing pig (20 kg bodyweight): the effect of protein-free, synthetic amino acid, peptide and protein alimentation. J. Sci. Food Agric. 61:31-40.

11. Leterme, P., Seve, B. & Thewis, A. (1998) The current 15N-leucine infusion technique is not suitable for quantitative measurements of ileal endogenous amino acid flows in pigs. J. Nutr. 128:1961-1968.[Abstract/Free Full Text]

12. Lien, K. A., Sauer, W. C., Mosenthin, R., Souffrant, W. B. & Dugan, M.E.R. (1997) Evaluation of the 15N-isotope dilution technique for determining the recovery of endogenous protein in ileal digestion of pigs: Effect of dilution in the precursor pool for endogenous nitrogen secretion. J. Anim. Sci. 75:148-158.[Abstract/Free Full Text]

13. Lien, K. A., Sauer, W. C. & Dugan, M.E.R. (1997) Evaluation of the 15N-isotope dilution technique for determining the recovery of endogenous protein in ileal digesta of pigs: effect of the pattern of blood sampling, precursor pools, and isotope dilution technique. J. Anim. Sci. 75:159-169.[Abstract/Free Full Text]

14. Steendam, C. A., Verstegen, M.W.A., Tamminga, S., Boer, H., van ’t End, M., Verstappen, B., Caine, W. R. & Visser, G. H. (2003) Route of tracer administration does not affect ileal endogenous nitrogen recovery measured with the 15N-isotope dilution technique in pigs fed rapidly digestible diets. J. Nutr. 134:3068-3075.

15. Butts, C. A., Moughan, P. J. & Smith, C. (1991) Endogenous amino acid flow at the terminal ileum of the rat determined under conditions of peptide alimentation. J. Sci. Food Agric. 55:175-187.

16. Leterme, P., Monmart, T., Thewis, A. & Morandi, P. (1996) Effect of oral and parenteral nutrition vs N-free nutrition on the endogenous amino acid flow at the ileum of the pig. J. Sci. Food Agric. 71:265-271.

17. Boisen, S. & Moughan, P. J. (1996) Dietary influences on endogenous ileal protein and amino acid loss in the pig—a review. Acta Agric. Scand. Sect. A Anim. Sci. 46:154-164.

18. Mehanso, H., Butler, L. G. & Carlson, D. M. (1987) Dietary tannins and salivary proline-rich proteins: interactions, induction, and defense mechanisms. Annu. Rev. Nutr. 7:423-440.[Medline]

19. Mole, S., Butler, L. G. & Iason, G. (1990) Defense against dietary tannin in herbivores: a survey for proline rich salivary proteins in mammals. Biochem. Syst. Ecol. 287:293-1990.

20. Hagerman, A. E. (2003) Tannin Chemistry 2003 http://www.users.muohio.edu/hagermae [accessed 13 June 2003].

21. Butler, L. G. (1992) Antinutritional effects of condensed and hydrolizable tannins. Hemingway, R. W. Laks, P. E. eds. Plant Polyphenols 1992 Plenum Press New York, NY. .

22. Asquith, T. N. & Butler, L. G. (1986) Interactions of condensed tannins with selected proteins. Phytochemistry 25:1591-1593.

23. Islambekov, S. Y., Karimdzhanov, A. K., Mavlyanov, S. M. & Ismailov, A. I. (1990) Vegetable tanning substances. Dependence of the tanning properties of extracts on their composition. Chem. Nat. Compd. 3:293-230.

24. Mole, S., Rogler, J. C., Morell, C. J. & Butler, L. G. (1990) Herbivore growth reduction by tannins: use of the Waldbauer ratio techniques and manipulation of salivary protein production to elucidate mechanisms of action. Biochem. Syst. Ecol. 3:183-197.

25. Jansman, A.J.M., Verstegen, M.W.A., Huisman, J. & van den Berg, J.W.O. (1995) Effects of hulls of faba beans (Vicia faba L.) with a low or high content of condensed tannins on the apparent ileal and fecal digestibility of nutrients and the excretion of endogenous protein in ileal digesta and feces of pigs. J. Anim. Sci. 73:118-127.[Abstract]

26. Kratzer, F. H., Singleton, V. L., Kadirvel, R. & Rayudu, G. V. (1975) Characterization and growth-depressing activity for chickens of several natural phenolic materials. Poult. Sci. 2124:2127-1975.

27. Levrat, M. A., Texier, M.D.O., Regerat, F., Demigné, C. & Rémésy, C. (1993) Comparison of the effects of condensed tannin and pectin on cecal fermentations and lipid metabolism in the rat. Nutr. Res. 13:427-433.

28. Suschetet, M. & de Larturiere, G. (1978) Effets comparés de différents tannins hydrolysables ou condensés sur la reserve hépatique de vitamine A chez le rat. C. R. Soc. Biol. 172:476-480.

29. Kohler, T., den Hartog, L. A., Huisman, J., Mosenthin, R. & Verstegen, M.W.A. (1991) Digestibility measurements in pigs by using post-valve T-caecum cannulation or end-to-side ileorectal anastomosis. J. Anim. Physiol. Anim. Nutr. 66:278-286.

30. Xu, C., Wensing, T. & Beynen, A. C. (1999) Fat digestion an faecal bile acid excretion in veal calves fed milk replacers containing either coconut fat or tallow. Anim. Feed Sci. Technol. 81:161-166.

31. Schulze, H., Butts, C. A., Moughan, P. J. & Verstegen, M.W.A. (1995) The 15N-isotope dilution method for determining ileal endogenous nitrogen excretion in the young (10 kg liveweight) pig. J. Sci. Food Agric. 69:41-50.

32. Donkoh, A. & Moughan, P. J. (1999) Endogenous ileal nitrogen and amino acid flows in the growing pig receiving a protein-free diet and diets containing enzymically hydrolysed casein or graded levels of meat and bone meal. Anim. Sci. 68:511-518.

33. Hodgkinson, S. M., Moughan, P. J., Reynolds, G. W. & James, K.A.C. (2000) The effect of dietary peptide concentration on endogenous ileal amino acid loss in the growing pig. Br. J. Nutr. 83:421-430.[Medline]

34. Hodgkinson, S. M., Souffrant, W. B. & Moughan, P. J. (2003) Comparison of the enzyme-hydrolyzed casein, guanidination, and isotope dilution methods for determining ileal endogenous protein flow in the growing rat and pig. J. Anim. Sci. 81:2525-2534.[Abstract/Free Full Text]

35. Rostagno, H. S., Rogler, J. C. & Featherston, W. R. (1973) Studies on the nutritional value of sorghum grains with varying tannin contents for chicks. 2. amino acid digestibility studies. Poult. Sci. 52:772-778.

36. Yu, F., Moughan, P. J. & Barry, T. N. (1995) Effect of condensed tannin in cottonseed hulls on endogenous ileal amino acid loss in the growing rat. J. Sci. Food Agric. 68:451-455.

37. Gabert, V. M., Canibe, N., Jorgensen, H., Eggum, B. O. & Sauer, W. C. (1997) Use of 15N amino acid isotope dilution techniques to determine endogenous amino acids in ileal digesta in growing pigs. Acta Agric. Scand. Sect. A Anim. Sci. 47:168-177.

38. Roos, N., Pfeuffer, M. & Hagemeister, H. (1994) Labeling with 15N as compared with homoarginine suggests a lower prececal digestibility of casein in pigs. J. Nutr. 124:2404-2409.

39. Hodgkinson, S. M. & Moughan, P. J. (2001) Effectiveness of an ultrafiltration device for use with the enzyme-hydrolysed protein method for determining endogenous ileal nitrogen and amino acid excretion in the pig. J. Sci. Food Agric. 81:1592-1596.

40. Hagerman, A. E. (1980) Condensed tannin of sorghum grain: purification and interaction with proteins. Doctoral thesis 1980 Purdue University West Lafayette, IN.

41. Hagerman, A. E. (1991) Chemistry of tannin-protein complexation. Hemingway, R. W. Karchesy, J. J. eds. Chemistry and Significance of Condensed Tannins 1991:323-333 Plenum Press New York, NY. .

42. Hodgkinson, S. M. & Moughan, P. J. (2003) The enzyme hydrolysed protein method for the determination of endogenous ileal nitrogen and amino acid flows—a modification. Anim. Feed Sci. Technol. 108:207-214.

43. Hodgkinson, S. M., Moughan, P. J. & Reynolds, G. W. (2000) Effect of the duration of feeding of a protein-free diet on endogenous ileal nitrogen and amino acid loss in the growing pig. J. Sci. Food Agric. 80:1407-1412.

44. Leterme, P., Thewis, A., van Leeuwen, P., Montmart, T. & Huisman, J. (1996) Chemical composition of pea fibre isolates and their effect on the endogenous amino acid flow at the ileum of the pig. J. Sci. Food Agric. 1996:127-134.

45. James, K.A.C., Butts, C. A., Koolaard, J. P. & Donaldson, H. E. (2002) The effect of feeding regimen on apparent and true ileal nitrogen digestibility for rats fed diets containing different sources of protein. J. Sci. Food Agric. 82:1050-1060.

46. Fuller, M. F. & Cadenhead, A. (1991) Effect of the amount and composition of the diet on galactosamine flow from the small intestine. Dig. Physiol. Pigs 330:333-1991.

47. Mitjavila, S., de Saint-Blanquat, G. & Derksen, G. B. (1973) Effet de l’acide tannique sur la secretion gastrique chez le rat. Nutr. Metab. 15:163-170.[Medline]

48. Vohra, P., Kratzer, F. H. & Joslyn, M. A. (1966) The growth depressing and toxic effects of tannins to chicks. Poult. Sci. 45:135-142.[Medline]

49. Mitjavila, S., Lacombe, C., Carrera, G. & Derach, R. (1977) Tannic acid and oxidized tannic acid on the functional state of rat intestinal epithelium. J. Nutr. 107:217-233.

50. Souffrant, W. B. (1991) Endogenous nitrogen losses during digestion in pigs. Proc. 4th Int. Symp. Digestive Physiol. in Pigs 1991:147-166 Wageningen The Netherlands.




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A. Deglaire, P. J. Moughan, S. M. Rutherfurd, C. Bos, and D. Tome
Feeding Dietary Peptides to Growing Rats Enhances Gut Endogenous Protein Flows Compared with Feeding Protein-Free or Free Amino Acid-Based Diets
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