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Article

Organ and Plasma Amino Acid Concentrations Are Profoundly Different in Piglets Fed Identical Diets via Gastric, Central Venous or Portal Venous Routes^{1 ,2}

Robert F. P. Bertolo^*,**, Paul B. Pencharz^,**,,, and Ronald O. Ball^*,,**,,3

Departments of ^* Human Biology & Nutritional Sciences Animal & Poultry Science, University of Guelph, Guelph, ON, Canada N1G 2W1; ^** Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB, Canada T6G 2P5; The Research Institute, The Hospital for Sick Children, Toronto, ON, Canada Departments of Paediatrics and Nutritional Sciences, University of Toronto, Toronto, ON, Canada M5G 1X8

³To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS Amino acid analyses DISCUSSION REFERENCES

 
In a previous study in piglets fed identical diets intravenously, intraportally or intragastrically, we determined that small intestinal atrophy affects nitrogen metabolism to a greater extent than liver by-pass. Because whole-body amino acid homeostasis is dependent on interorgan metabolism, we also measured the free amino acid concentrations in liver, small intestinal mucosa and kidney in order to study alterations in amino acid metabolism within these organs. Piglets (n = 15; 2–4 d old) were fed identical diets continuously for 8 d via gastric (IG), portal (IP) or central venous (IV) catheters. Concentrations of all measured amino acids were affected by route of feeding in one or more organs. In particular, urea cycle amino acid concentrations were altered in plasma and mucosa of IV and IP pigs, suggesting that arginine synthesis by an atrophied gut may have been limited. Furthermore, most indispensable amino acid concentrations were lower in IP pigs for all organs vs. IG pigs; however, except for phenylalanine, plasma concentrations of these amino acids were not different, demonstrating the liver’s "smoothing" capability. Gut atrophy in both IV and IP pigs resulted in significantly lower concentrations of all indispensable amino acids compared with IG pigs. Alterations of all amino acids in various organs due to route of feeding suggest that more detailed analyses of regulatory mechanisms and amino acid interactions on interorgan amino acid metabolism are necessary for all amino acids.

KEY WORDS: • amino acids • small intestine • liver • route of feeding • neonatal piglets

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS Amino acid analyses DISCUSSION REFERENCES

 
The interorgan metabolism of urea cycle amino acids has been described previously for adult species (Jones 1985 ) and involves interrelated metabolic pathways within the small intestine, liver and kidney. However, developmental changes in urea cycle metabolism and enzymes within these organs have been observed in rats and pigs (Morris 1992 , Wu 1998 ). Our long-term objective is to elucidate and quantify the roles of these organs in the metabolism of urea cycle amino acids in the neonatal piglet. As a step in achieving this objective, this study focused on the concentrations of the urea cycle amino acids in these organs as well as the primary precursors of arginine, i.e., proline, glutamate and glutamine. These collective amino acids are referred to as pyrroline-5-carboxylate (P5C)⁴ amino acids because P5C is the central metabolite connecting the carbon pathways between glutamate and proline and the urea cycle. Because the central organs involved in P5C amino acid metabolism are the small intestine, liver and kidney, we chose to measure the free amino acid concentrations in these organs to elucidate their metabolism in the piglet.

To isolate the effects of intestinal metabolism from liver metabolism, we developed three piglet models in which identical complete diets were fed continuously via gastric, central vein or portal vein catheters (Bertolo et al. 1999 ). Intragastrically-fed (IG) pigs represented the "control" group in which first-pass metabolism of nutrients by the small intestine and liver occurred. Feeding via the portal vein (IP) represented a model in which nutrients are metabolized by the liver on first pass, but small intestinal first-pass metabolism is excluded. Nutrients infused into a central vein (IV) by-pass exclusive first-pass metabolism by the intestine and liver; these nutrients are therefore provided to nonsplanchnic organs in concentrations that are not modified by first-pass splanchnic metabolism. We have shown that both IV and IP groups experience gut atrophy, and hence lowered intestinal metabolic capacity (Bertolo et al. 1999 ). Using these in vivo models fed via different routes, we can describe metabolic effects due to different first-pass metabolism and/or lack of small intestinal metabolic capacity. In particular, we are interested in the free amino acid concentrations in the organs that are involved in P5C amino acid metabolism.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS Amino acid analyses DISCUSSION REFERENCES

 
Animals and surgical procedures.

The animal handling protocols have been described previously in detail (Bertolo et al. 1999 ). Briefly, intact male Yorkshire piglets (n = 15) were obtained from the University of Guelph’s minimal disease herd at 2–4 d of age and transported to the laboratory where the piglets immediately underwent surgery to implant catheters. All procedures used in this study had been approved by the Animal Care Committee of the University of Guelph.

Piglets were between 1.4 and 1.8 kg at arrival and were blocked by body weight among the three treatments. Using a modified method of Wykes et al. (1993) and Rombeau et al. (1984) , custom-made Silastic catheters (Ed-Art, Don Mills, Canada) were installed using aseptic technique. Feeding catheters were installed in the stomach for IG piglets, in the jugular vein for IV piglets and in the umbilical vein for IP piglets; all pigs were fitted with a femoral vein catheter for blood sampling. In IG pigs, a Stamm gastrostomy was performed (Rombeau et al. 1984 ). The jugular catheter was inserted into the left jugular vein and advanced to the superior vena cava just cranial to the heart. The umbilical catheter was introduced transperitoneally into the umbilical vein and advanced to the portal-hepatic junction. The femoral catheter was introduced into the left femoral vein and advanced into the inferior vena cava just caudal to the heart. IV pigs also underwent a sham operation in which the abdomen and peritoneum were incised and sutured.

An elemental and complete diet [described in Wykes et al. (1993) ] was fed via one of the feeding routes (IG, IV or IP) continuously for 8 d after surgery. For the IV and IP diets, vitamins (MVI Pediatric, Rhone-Poulenc Rorer Canada, Montreal, Canada) and minerals (Micro⁺6 concentrate, Sabex, Boucherville, Canada) were added to the sterile diet solutions immediately before use. Lipid (Intralipid 20%, Pharmacia-Upjohn, Stockholm, Sweden) was infused separately into the infusion extension sets. The IG diet was made as above, except solutions were not filter sterilized. Distilled water (1.5-fold dilution to lower osmolarity) and lipid were added to the final solutions. Infusion rates of the IG diets were increased so that energy and nitrogen intake rates were identical among groups. After surgery, all piglets were adapted to diet infusions as previously described (Bertolo et al. 1999 ). Piglets were weighed each morning and infusion rates adjusted accordingly.

Diet was administered IV or IP through a tether-swivel system (Alice King Chatham Medical Arts, Los Angeles, CA) using pressure-sensitive infusion pumps; lipid (Intralipid 20%, Pharmacia-Upjohn) was infused simultaneously using syringe pumps. IG diets were premixed and infused continuously using peristaltic enteral pumps. The infusion regimen was designed to supply all nutrients required by piglets (Wykes et al. 1993 ) and targeted intakes were as follows: 15 g amino acids/(kg · d) and 1.1 MJ metabolizable energy/(kg · d) with glucose and lipid each supplying 50% of nonprotein energy. The amino acid pattern (Table 1 ) was similar to that of a commercial parenteral nutrition solution, which is based on human milk protein (Vaminolact: Pharmacia-Upjohn), except that phenylalanine was supplemented to ensure adequate total aromatic amino acid intake (Wykes et al. 1994 ).

Blood samples were collected into heparinized syringes on d 8 via the femoral catheter. Whole-blood samples were centrifuged at 4000 x g for 10 min and plasma was frozen at -20°C until further analyses. Just after blood collection, piglets were killed by lethal injection of 750 mg of sodium pentobarbital. Liver and kidneys were removed and samples were excised and frozen at -70°C until further analyses. The small intestine was removed from the mesenteric sheath. Excluding the duodenum and first 10 cm of proximal jejunum, the next 60 cm of jejunum was excised for mucosa collection. The jejunal segments were flushed with saline and then slit lengthwise; mucosa was scraped, frozen in liquid nitrogen and stored at -70°C until further analyses.

Amino acid analyses.

Amino acid concentrations were determined by reverse-phase HPLC. For plasma free amino acids, 200 µL plasma was mixed with 40 µL of an internal standard (norleucine) and 1 mL of a protein precipitant (0.5 mL trifluoroacetic acid/100 mL methanol), vortexed and centrifuged at 3000 x g for 5 min to remove proteins. For tissue (proximal jejunum, liver, kidney) free amino acids, norleucine was added to 100 mg of tissue, homogenized in a mixture of 10 mL trifluoroacetic acid and 100 mL methanol, and centrifuged. The pellet was homogenized and centrifuged and the supernatants were pooled. For all samples, phenylisothiocyanate derivatives for reverse-phase HPLC were prepared (Bidlingmeyer et al. 1984 ).

Statistical analyses.

Data were analyzed by one-way ANOVA using Fisher’s (protected Least Significant Difference) multiple comparisons between groups (Version 7.1, Minitab, State College, PA) and were considered significant when P < 0.05.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS Amino acid analyses DISCUSSION REFERENCES

 
Body weight gain.

The d 3 (adapted) and d 8 (necropsy) body weights were not different among groups. Furthermore, the rates of body weight gain were not different among groups (IG, 153 g/d; IV, 137; IP, 134; pooled SD, 31). Further information on various growth parameters of these piglets were described previously (Bertolo et al. 1999 ).

	Amino acid analyses

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS Amino acid analyses DISCUSSION REFERENCES

 
The complete free amino acid data for plasma (Table 2 ), liver (Table 3 ), kidney (Table 4 ) and small intestinal mucosa (Table 5 ) of piglets receiving identical diets via IG, IV or IP routes are presented in tabular form. Selected results are presented below for different groups of amino acids.

In plasma, only phenylalanine concentrations were altered by route of feeding; concentrations in IP pigs were higher than those in IG or IV pigs (Table 2) . In both the liver and kidneys, IP feeding led to lower concentrations of the same seven indispensable amino acids compared with IG feeding (including trends for liver valine and isoleucine, P < 0.10); only phenylalanine and tryptophan concentrations were unaffected by route of feeding in both organs. However, IV feeding did not affect any indispensable amino acid concentrations in the liver compared with IG feeding; furthermore, only leucine, lysine and threonine concentrations in the kidneys were lowered by IV feeding. In the small intestinal mucosa, either IV or IP feeding led to lower concentrations of all nine indispensable amino acids compared with IG feeding. Also, in contrast to the liver and kidney, IP feeding led to lower mucosal concentrations of five amino acids (histidine, isoleucine, lysine, methionine and valine) compared with IV feeding (Table 5) .

P5C amino acids.

Our primary interests were in the P5C amino acids (ornithine, citrulline, arginine, proline, glutamate and glutamine). IP feeding led to lower concentrations of ornithine and arginine in all tissues measured compared with IG feeding; furthermore, in three of the four tissues, IP feeding led to lower concentrations of glutamine (except liver). Interestingly, concentrations of citrulline were highest, and aspartate lowest, in all three organs during IP feeding; in contrast, IV feeding led to lower concentrations of citrulline in all organs compared with IP feeding. Similar to IP feeding, IV feeding also led to lower ornithine concentrations (vs. IG) in plasma, kidneys and mucosa. Except for citrulline, concentrations of all P5C amino acids were lower in mucosa from IP pigs and IV pigs (except for glutamine and aspartate) compared with IG pigs. Indeed, concentrations of glutamate and proline were affected in intestinal mucosa only by IP and IV feeding.

Other amino acids.

Of the remaining amino acids measured, only hydroxyproline and serine concentrations were unaffected by route of feeding. IP feeding led to lower concentrations of alanine, asparagine, cystine and serine in all three organs compared with IG feeding. Furthermore, IV feeding led to higher concentrations of alanine (liver, mucosa), asparagine (liver, kidney), cystine (kidney, mucosa) and serine (liver, kidney, mucosa) compared with IP feeding. Interestingly, IP feeding led to lower taurine concentrations in the plasma and liver, but higher concentrations in kidney and mucosa, compared with IG feeding; in contrast, IV feeding led to taurine concentrations that were similar to IG feeding in plasma and liver, but similar to IP in kidney and mucosa.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS Amino acid analyses DISCUSSION REFERENCES

 
Free amino acid concentrations within a tissue are affected by dietary input, protein turnover, biosynthesis of amino acids, transamination reactions, transport rates across tissue membranes and oxidation rates. In general, the size of an amino acid pool within a particular component or tissue is approximated by its free concentration (Waterlow et al. 1978 ). On the basis of this concept, we discuss the free amino acid concentrations in plasma, small intestinal mucosa, liver and kidneys as reflective of amino acid pools. Caution must be applied when relating free amino acid concentrations to other aspects of amino acid metabolism; however, concentration differences under controlled circumstances provide a measure of the "net effect" of various changes, thus identifying those amino acids that warrant further study.

In a previous study (Bertolo et al. 1999 ), we proposed that the lower nitrogen retentions observed for intraportally and intravenously fed pigs compared with orally fed pigs were due to the catabolism of excess amino acids as a result of either lower whole-body protein synthesis or inadequate synthesis of arginine. Arginine has been shown to be indispensable in piglets (Ball et al. 1986 ), and its synthesis occurs primarily in the small intestine (Stoll et al. 1998 ). Given the extensive gut atrophy observed in both IV and IP pigs (Bertolo et al. 1999 ), arginine synthesis may therefore have been inadequate to meet whole-body requirements. The primary precursors for arginine synthesis (via ornithine) in the gut are proline (Brunton et al. 1999 , Murphy et al. 1996 ), glutamate (Reeds et al. 1997 ) and glutamine (Wu et al. 1994 ). In this study, mucosal concentrations of arginine and its precursors were all lower in the parenterally fed groups. In addition, ornithine concentrations were lower in parenterally fed pigs in all tissues measured. Ornithine is a central intermediate in these pathways, and the significance of ornithine as a precursor for arginine synthesis in the piglet has not been quantified. Thus, these data support our hypothesis that reduced arginine synthesis by an atrophied gut may have limited protein deposition in the parenterally fed pigs.

We observed several consistent patterns of P5C amino acid changes due to route of feeding. In the liver of IP pigs, ornithine concentrations were lower, but citrulline concentrations were higher. Because citrulline is synthesized from ornithine and carbamoyl phosphate (which is formed from ammonia and bicarbonate), the large citrulline concentration may have resulted from excess hepatic ammonia being quenched by its incorporation into citrulline, thereby lowering ornithine concentrations. Furthermore, the conversion of citrulline to arginine requires aspartate, which deaminates to provide the second amine group for urea. Interestingly, hepatic aspartate concentrations were dramatically lower in IP pigs compared with IG and IV pigs. A similar pattern of urea cycle amino acids was observed in the kidney and to a lesser extent, in the mucosa. These results indicate that the interorgan metabolism of these amino acids must be explored further using isotope kinetics to determine flux and conversion rates.

Consistent patterns of change due to route of feeding were observed for the indispensable amino acids that are most closely regulated via oxidation and protein synthesis and breakdown. Eight of the nine indispensable amino acids in plasma were not altered due to route of feeding. This result is impressive because in all other tissues, IP pigs had lower concentrations (compared with IG) for most free indispensable amino acids (liver, 5 of 9; kidney, 7 of 9; mucosa 9 of 9). Stoll et al. (1998) demonstrated in piglets that at least one third of dietary essential amino acids are removed by the small intestine on first pass. As a result, the hepatic influx from the portal circulation was at least one third less in IG pigs compared with IP pigs. Thus the liver has a significant "smoothing" capability when large amounts of amino acids are infused into it directly (Bloxam 1971 ). Portal vein amino acids after a protein meal are known to cause hepatocyte swelling, which can be considered an anabolic stimulus [reviewed by Meijer et al. (1999) ]. The consequences of this swelling include increased protein synthesis and increased amino acid oxidation and urea cycle activity. Thus it is reasonable to speculate that chronic infusion of at least one-third higher concentrations of indispensable amino acids directly into the liver could induce hepatocyte swelling and lead to reduced free amino acid concentrations via higher protein synthesis and amino acid oxidation. Considering that the primary mechanism for regulation of amino acid pools may be oxidation (Waterlow 1984 ), this would lower the amount of indispensable amino acids available for protein synthesis in the periphery, leading to the observed lower protein deposition in IP pigs (Bertolo et al. 1999 ). Unlike in IP pigs, all of the indispensable amino acid concentrations in the livers of IV pigs were similar to those of IG pigs. Amino acids infused via a central vein are delivered to the body via the arterial circulation and distributed in a nonphysiologic pattern; metabolism by extrasplanchnic tissues occurs before the influx of dietary amino acids to the liver. As a result, hepatic amino acid concentrations in IV- and IP-fed pigs would be affected differently due to the influx of a different amino acid profile in either situation.

Compared with IG pigs, renal free amino acid concentrations were also lower for seven of the essential amino acids in IP pigs and for three of them in IV pigs. Adeola et al. (1995) demonstrated that kidney protein synthesis rates were higher in parenterally fed piglets compared with orally or sow-fed controls. Also, the total kidney protein content (measured by total nitrogen analysis) was higher in both IV and IP pigs compared with IG-fed controls (Bertolo et al. 1999 ). These results support the supposition that higher protein synthesis rates result in lower free amino acid concentrations for several essential amino acids.

Not surprisingly, IV and IP pigs had lower mucosal concentrations of all nine essential amino acids compared with IG pigs (Table 5) , likely as a result of significant gut atrophy and reduced metabolic capacity (Bertolo et al. 1999 ). Parenterally fed piglets were probably unable to maintain mucosal protein synthesis because both enteral stimulation of anabolic hormones and an enteral amino acid supply were lacking. However, mucosal concentrations of five of the nine indispensable amino acids were even lower in IP pigs than in IV pigs. The total protein content (measured by total nitrogen) per gram of mucosa was the same between IV and IP pigs (Bertolo et al. 1999 ), which implies that protein synthesis/breakdown or balance was not different between parenterally fed groups. However, if amino acid catabolism (via deamination and/or oxidation) was higher in IP vs. IV pigs, then free amino acid concentrations would be correspondingly lower, as was observed for most essential amino acids.

Interesting results were observed for taurine, which increased in concentration in the kidney and small intestine for parenterally fed groups. Taurine excretion is either via biliary excretion (conjugation with bile acids) or via renal excretion (Hayes and Sturman 1981 ). The high renal concentrations in IP and IV pigs could be the result of increased renal excretion because bile acid secretion would be reduced without enteral feeding.

Many of the dispensable amino acids are products of catabolism of indispensable amino acids and thus may reflect these pathways. Dispensable amino acids that were altered include nitrogen carriers such as alanine, glutamate, glutamine, aspartate and asparagine. Harper (1983) suggested that the large pools of these dispensable amino acids (alanine, glutamate, glutamine and aspartate), relative to indispensable amino acids, may function to conserve the indispensable ones through reamination of corresponding -keto acids. Interestingly, the lower tissue concentrations of indispensable amino acids observed in IP pigs seemed to correspond to lower concentrations of the dispensable amino acids that are responsible for reamination reactions.

Our purpose in conducting this experiment is best stated by Waterlow et al. (1978) : "Static measurements of pool sizes give little information about dynamic changes in the components of inflow or outflow, but they may alert one to the fact that some change has occurred, which therefore ought to be investigated." The present data indicate clearly that the P5C amino acids are affected more by interorgan metabolism than any other group of amino acids. Additional research into the P5C amino acid pathways within and between the liver, small intestine and kidney must be pursued using direct and quantitative methods such as amino acid isotope kinetic analysis. Furthermore, such research should focus on the interorgan metabolism of ornithine, which is central to these pathways and may help explain the altered urea cycle metabolism apparent during the various routes of feeding.

	FOOTNOTES

 
¹ Presented in part at the 16th International Congress of Nutrition, July 1997, Montreal, QC [Bertolo, R.F.P., Chen, C., Pencharz, P. B. & Ball, R. O. (1997) Hepatic and small intestinal metabolism of amino acids when identical diets are fed intragastrically, intravenously, or intraportally to piglets.], the 37th Annual Meeting of the American Society for Clinical Nutrition, July 1997, Montreal, QC [Bertolo, R.F.P., Chen, C.Z.L., Pencharz, P. B. & Ball, R. O. (1997) The role of the small intestine (SI) and liver in splanchnic amino acid (AA) metabolism during intragastric (IG), intravenous (IV), or intraportal (IP) feeding of identical diets in piglets.] and Experimental Biology 97, April 1997, New Orleans, LA [Bertolo, R.F.P., Pencharz, P. B. & Ball, R. O. (1997) Urea cycle amino acid changes in organs of piglets fed identical diets via gastric, portal, or central vein routes. FASEB J. 11: A364 (abs.).].

² Supported by grants from the Natural Sciences and Engineering Research Council of Canada, the Alberta Agricultural Research Institute and Alberta Pork. The amino acids were generously donated by Pharmacia-Upjohn, Stockholm, Sweden.

⁴ Abbreviations used: IG, intragastrically-fed; IP, intraportally-fed; IV, intravenously-fed; P5C, pyrroline-5-carboxylate.

Manuscript received July 26, 1999. Initial review completed September 7, 1999. Revision accepted January 31, 2000.

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6. Brunton J. A., Bertolo R.F.P., Pencharz P. B., Ball R. O. Proline ameliorates arginine deficiency during enteral feeding but not during parenteral feeding in neonatal piglets. Am. J. Physiol. 1999;277:E223-E231[Abstract/Free Full Text]

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