Piglet Studies

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We used a multiply catheterized piglet model, with catheters placed in the carotic artery, jugular vein, portal vein, stomach, and duodenum, and a flow probe placed around the portal vein. The catheters were placed during surgery

Fig. 2. Rate of postnatal weight gain of the small intestine.

in formula-fed piglets on the 21st day of life. After full recovery from surgery, as indicated by a similar weight gain rate as prior to surgery, metabolic studies were performed in the fully conscious, enterally fed piglets [7]. This model allowed us to measure the utilization rates of enteral and systemic substrates by the portal-drained viscera (stomach, spleen, pancreas, intestine).

Intestinal Energy Expenditure

We measured the energy expenditure of the portal-drained viscera of neonatal piglets by means of sodium bicarbonate labeled with 13C [8]. It appeared to be almost three times as high as could be expected on the basis of its weight. While some 12% of total body energy expenditure occurred within the portal-drained viscera, the weight of the portal-drained viscera accounted for only 4% of total body weight. This high energy expenditure reflects the rapid growth rate and high metabolic rate of these organs (especially the intestine).

Intestinal Sources of Energy

As early as 25 years ago, Windmueller and Spaeth [9] already examined amino acid utilization rates in isolated perfused intestinal loops in rats. From these in vivo experiments, they concluded that several substrates may serve as energy sources. Glutamate and glutamine, and aspartate and glucose were the major fuel sources found. We repeated these experiments in fully conscious piglets, using the model described above [10]. We found amino acids to be the major source of energy, with glutamate being the single most used amino acid. Almost all (90%) enterally administered glutamate was utilized in the first pass, of which 47% was used for oxidative purposes. Not only non-essential

Table 1. Contributions (expressed as %) of different substrates to CO2 production by the portal-drained viscera in piglets [10] (mean ± SD)

Normal protein intake

Low protein intake

Leucine

11 ± 3

Lysine

2 ± 0

-

Threonine

2 ± 1

2 ± 1

Methionine

1 ± 0

n.d.

Glutamate

32 ± 15

10 ± 3

Glucose

39 ± 10

52 ± 30

Miscellaneous

13

36

amino acids were used, but also leucine (an essential branched chain amino acid) was oxidized by the portal-drained viscera, slightly more than 10% of the intake. This is a crucial finding in that essential amino acids cannot be synthesized de novo, indicating that oxidation of such essential amino acids means an irreversible loss. Also a substantial part (31%) of whole-body lysine (another essential amino acid) oxidation occurred in the intestine, although lysine oxidation contributed little as an energy source [8]. But again, it meant an irreversible loss of lysine which is one of the most limiting amino acids in the diet. Table 1 shows the contributions of different substrates to total energy expenditure. At least half of the energy generated within the intestines is derived from amino acid oxidation under normal feeding conditions. Interestingly, when we reduced protein intake to a maintenance level, visceral amino acid oxidation was substantially suppressed. This was only partially compensated for by an increase in glucose oxidation, indicating that other substrates such as fatty acids might become more important.

Intestinal Amino Acid Utilization and Systemic Availability

The higher the intestinal utilization rate, the lower the systemic availability of dietary amino acids. This indicates that the intestinal utilization rate of amino acids determines whole body growth. We found that in piglets the utilization rate of essential amino acids was approximately 65% of the dietary intake during the first few hours following feeding [8]. Thus the systemic availability of essential amino acids was only 35%. For some amino acids like threonine, the systemic availability was only 16% of the intake (table 2) [11]. In a subsequent study, therefore, we examined whether the amino acids that were utilized within the intestine would perhaps become systemically available the next day [12]. It appeared that 26% of the amino acids that were utilized within the intestine were released in the portal vein during the hours following the feeding period and thus became systemically available. So a substantial part of dietary intake was again released into the systemic circulation

Table 2. The net systemic availability of essential dietary amino acids as a percentage of enteral intake during the first 6h following continuous feeding (mean ± SEM; n = 9 piglets)

Amino acid

Intake

Systemic availability

Systemic availability

^mol/(kg/h)

^mol/(kg/h)

(% of intake)

Threonine

934

152 ± 36

16 ± 4

Valine

765

315 ± 31

41 ± 4

Isoleucine

780

218 ± 18

28 ± 2

Leucine

748

350 ± 33

47 ± 4

Phenylalanine

254

94 ± 9

37 ± 4

Lysine

518

277 ± 23

54 ± 4

Total essential

3,999

1,406 ± 101

35 ± 3

amino acids amino acids on the day after feeding. This can be attributed to either amino acid release by proteolysis of constitutive proteins in the intestinal wall or amino acids derived from secreted glycoproteins that are degraded and reabsorbed from the intestinal lumen. Such secreted (glyco-)proteins can be mucins because, for instance, Muc-2 is rich in threonine, one of the most abundantly utilized amino acids by the intestine [13].

Apart from oxidation, the metabolic fate of utilized amino acids in the intestine can be protein synthesis. For instance, enteral glutamate is preferentially used for glutathione synthesis [14]. We have recently measured the metabolic fate of methionine in the intestine of piglets. Interestingly, hardly any dietary methionine was utilized in the first pass, but the gastrointestinal tissues consumed 20% of the arterially derived methionine which represented a significant site of transmethylation and transsulfuration [Riedijk et al., unpubl. data]. Threonine is also utilized from the arterial site, but in equimolar amounts as from the luminal site [11].

The combined findings are consistent with the intestine being a major consumer of amino acids, inasmuch as it uses the equivalent of approximately half of the dietary amino acid intake. These amino acids can be derived from the luminal site of the intestine or from the systemic site. The utilization grades of the various amino acids differ markedly. Some might be utilized almost completely (glutamate, threonine) whereas, for instance, less than half of the intake of lysine is utilized. Oxidation is an important metabolic fate, but a substantial part of the utilized amino acids is used for protein synthesis.

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