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First published online December 1, 2006
Journal of Experimental Biology 209, 4885-4894 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02597
Postprandial changes in plasma free amino acid levels obtained simultaneously from the hepatic portal vein and the dorsal aorta in rainbow trout (Oncorhynchus mykiss)
1 Aquaculture Protein Centre (APC), Centre of Excellence, Norwegian
University of Life Sciences, PO Box 5003, N-1432 Aas, Norway
2 Department of Animal and Aquacultural Sciences, Norwegian University of
Life Sciences, PO Box 5003, N-1432 Aas, Norway
3 Department of Zoology and Faculty of Land and Food Systems, University of
British Columbia, BC, Vancouver, V6T 1Z4, Canada
* Author for correspondence at address 2 (e-mail: anders.kiessling{at}umb.no)
Accepted 16 October 2006
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Key words: Hepatic portal vein cannulation, plasma free amino acids, urea, ammonium, digestibility, protein metabolism, rainbow trout, Oncorhynchus mykiss
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Introduction |
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). Although these studies are useful from a fish
production point of view, they provide little insight into specific rates of
nutrient absorption via the intestine and metabolism by the liver. A
few studies have therefore made attempts to follow postprandial nutrient
uptake by serially sampling blood from slaughtered fish (reviewed by
Carter et al., 2001). However,
such studies may yield ambiguous results because of several shortcomings.
There is the obvious sampling effect of terminal blood sampling techniques
which stress fish and greatly alter gut blood flow
(Thorarensen et al., 1993). In
addition, a high individual variation of plasma nutrients may mask anything
but major changes. Sunde et al. (Sunde et
al., 2003) tried to circumvent these obstacles by sampling blood
from the dorsal aorta (DA) via a permanent cannula in free-swimming
fish. By measuring postprandial free amino acid (AA) concentrations in the
blood of fish given different diets, they revealed differences in feed quality
not easily discovered with traditional growth rate-based experiments. However,
a limitation of using DA blood samples is that the blood metabolites may have
undergone hepatic modification en route from the intestine to the
DA.
Blood leaving the gut via the hepatic portal vein (HPV) first
passes through the liver, and, given the central role of the liver in the AA
metabolism of higher vertebrates (McDonald
et al., 2002), differences in the pre- and post-liver profiles of
plasma free AAs are to be expected in fish. In fact, it is estimated that
20-50% of the free AAs entering the blood never get past the liver
(Hoerr et al., 1991;
Hoerr et al.,1993;
Biolo et al., 1992;
Matthews et al., 1993). Lyndon
et al. tried to estimate the pre- and post-hepatic free AA plasma levels by
serial slaughter of cod (Gadus morhua) and sampling of blood from HPV
and cardiac puncture immediately after death
(Lyndon et al., 1993). Ash et
al. (Ash et al., 1998) sampled blood using a double DA and HPV cannulation
technique (McLean and Ash,
1989) from lightly sedated fish but made only one measurement 3 h
postprandially. Thus, to date reliable information does not exist on the time
course of the postprandial free AA changes in plasma in fish or on the degree
of hepatic modification of free AA during their first pass through the liver
after uptake by the intestine. By combining the DA and HPV cannulation
techniques, the present study is a first attempt to follow, over time, the
postprandial free AA profiles in plasma simultaneously collected before and
after the liver in anaesthetized and free-swimming fish. Furthermore, by
simultaneously sampling blood from both the DA and the HPV, we can test the
hypothesis that hepatic metabolism of free AAs during their first pass through
the liver is possible in rainbow trout. Two different dietary treatments were
used to assess the effect of varying dietary amino acid composition on the
free AA plasma profile. In addition to free AAs, plasma levels of the
metabolites urea and ammonium were analysed to evaluate the potential for
intestinal AA catabolism. Therefore, the present study provides the first
comprehensive study of postprandial AA uptake and immediate metabolic
processing of AAs in a fish.
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Fish were starved for 24-48 h prior to surgery. Cannulation was performed
on anaesthetized fish (0.1 g l-1 MS-222; tricaine methane
sulphonate). The DA cannulation was performed according to the method of
Soivio et al. (Soivio et al.,
1975) and included adjustments described
(Kiessling et al., 1995;
Kiessling et al., 2003). The
HPV cannulation has been described in detail elsewhere (Eliason et al., 2006).
After at least 24 h of recovery from surgery, the fish were sedated (0.1 g
l-1 MS-222) and force-fed a single meal of 1% of their body mass by
intubation using a stiff PVC tube with rounded tip. The diets were ground
through a 0.5 mm screen, and analysed for dry matter
(EC, 1971b), ash
(EC, 1971a), crude protein
(EC, 1993), crude fat
(EC, 1998), starch
(McCleary et al., 1994),
non-starch polysaccharides (Lee et al.,
1992) and amino acid composition
(EC, 1998). The experimental
design involved two diets (six fish were tested on each diet), with diet 1
containing fish meal as the only protein source and diet 2 containing 20% corn
gluten as a partial replacement for fish meal. Nevertheless, this adjustment
produced only very small differences in the total and individual dietary AAs
between the two diets (Tables 1
and 2). Perhaps as a result, no
significant effect (P>0.05), or any tendencies
(P>0.15) were found between the diets for the resulting plasma
free AA profiles. Therefore, plasma free AA data for the two diets were pooled
for the analysis presented here.
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Blood samples (0.4-0.5 ml) were taken from both cannulae immediately prior
to force-feeding (0 h), and at 3, 6, 12, 24 and 48 h postprandially. Whole
blood was centrifuged at 500 g for 5 min, and plasma was
removed and immediately frozen at -20°C prior to storage within hours at
-80°C until analysis. The status of the fish was monitored visually and
with measurements of haematocrit and leucocrit from the blood samples. Plasma
levels of alanine aminotransferase (ALAT; hepatocyte specific) and aspartate
aminotransferase (ASAT; cardiac, hepatic but also general tissue unspecific)
were analysed with standardized methods for measurement of enzymes according
to the International Federation of Clinical Chemistry
(Bergmeyer et al., 1986a;
Bergmeyer et al., 1986b) on a
Konelab 30 analyser using kit no. 981769 and 981771 for ALAT and ASAT (Thermo
Electron Corp., Vantaa, Finland), respectively, as indicators of liver damage
(Table 3).
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The concentrations of free AA in plasma samples were analysed by ion exchange chromatography on a lithium high performance column (Biochrom Ltd, Cambridge, UK) in an automated amino acid analyser (Biochrom 30, Biochrom Ltd), using lithium-based eluents and post-column derivatization with ninhydrin (Physiological Fluid Chemical Kit, Biochrom Ltd). Data were analysed against external standards (Sigma amino acid standard solutions: acidics, neutrals and basics, supplemented with glutamine, tryptophan and S-2-aminoethyl-1-cysteine; all purchased from Sigma Chemical, St. Louis, MO, USA) using the Chromeleon® Chromatography Management Software (Dionex Ltd, Surrey, UK).
Plasma (80 µl) was deproteinized by mixing with 8 µl of 35% sulfosalicylic acid solution. The mixture was incubated at 4°C for 20 min and centrifuged at 16 000 g for 15 min (Biofuge Fresco, Heraeus Instruments, Kendro Laboratory Products GmbH, Hanau, Germany). Of the supernatants, 60 µl were diluted with 60 µl 0.2 mol l-1 lithium citrate loading buffer, pH 2.2 (Biochrom Ltd) and micro-filtrated (0.2 µm Spartan membrane filter, Schleicher & Schuell, Dassel, Germany) prior to injection (30 µl). Some supernatants were stored at -80°C until analysis. S-2-aminoethyl-1-cysteine was used as an internal standard.
Data were analysed statistically using the Statistical Analysis System for
Windows, Version 8.2 (SAS,
2002). The effects of the main variables, i.e. sample time and
vessel, were tested by a main factorial model (GLM procedure for unbalanced
data). Fish was included as a discrete variable. Groups were compared by the
ad hoc variance test (F-test) using the least-squares means
procedure when significant effects were found in the main model. All data were
tested for normality by a normal probability plot (proc univariate plot).
P<0.05 was considered to be statistically significant.
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Results |
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There was a definitive appearance profile for the free AA in the plasma from both the HPV and DA (Fig. 1). A postprandial peak of the total free AA concentration occurred at 6 h (DA: 7107±369 nmol ml-1 and HPV: 9999±572 nmol ml-1). For most individual free AAs, the plasma concentrations changed over time (P<0.05), more so with the HPV samples than the DA samples (Tables 4, 5 and 6). All free AAs, with the exceptions of threonine (Table 4) and proline (Table 5) returned to, or below, baseline levels within 48 h.
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If there was no hepatic metabolism of the absorbed free AAs during their first pass through the liver, the ratio of HPV to DA free AA concentrations would be constant both over time and among individual free AAs, but this was not the case. The total free AA concentrations were consistently higher (P<0.05) in the HPV than in the DA at 3, 6, 12 and 24 h (Fig. 1). However, a few non-essential free AAs did not differ between the two sample sites (Tables 5 and 6). The highest relative difference (calculated as percentage difference between DA and HPV values, as given in Tables 4, 5 and 6) of an individual AA was that of serine (62%) at 24 h (Table 4), but this occurred well after the peak uptake of serine at 6 h. The lowest significant difference was that of glutamic acid, which had a peak hepatic absorption of only 25% difference in the 3-h sample (Table 4). Despite the fact that the removal of serine and glutamic acid differed greatly, the liver absorption of both of these AAs stayed elevated throughout the entire 48 h postprandial period. The hepatic removal of some of the type I profile AAs (taurine, isoleucine, lysine, arginine and glutamine) stayed elevated for a considerable period of time, thus the 48 h postprandial concentration in the DA was lower than before feeding (Tables 4 and 5).
A postprandial peak in the AA metabolites (ammonia and urea) was anticipated for the DA blood samples (Fig. 3). However, a significant elevation in plasma ammonia and urea in the HPV compared with the DA blood samples was also found (Fig. 3). Whereas plasma levels of urea were identical in the DA and HPV at the start of the experiment, they diverged with time, such that there was a significantly higher plasma concentration in the HPV 12 h compared with the DA, before returning to similar levels (Fig. 3). By contrast, the plasma ammonia levels were always significantly higher in the HPV than in the DA. This difference was about twofold at the start and end of the experiment, but increased to over fourfold for most of the postprandial period (6-24 h; Fig. 3) when the free AA uptake was occurring (Fig. 2).
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). Since
its establishment as a method for long-term nutrition studies in the mid-1990s
(Kiessling et al., 1995), it
has been standardized, well characterized for its physiological components and
acknowledged as yielding representative data of a fish in a normal
physiological state (B. Djordjevic, T. Kristensen, Ø. Øverli, B.
O. Rosseland and A. Kiessling, manuscript submitted for publication). Fish
with a DA cannulation seem to recover their physiological and nutritional
status within 24 h post-surgery (Kiessling
et al., 1995; Kiessling et
al., 2003) (B. Djordjevic, T. Kristensen, Ø. Øverli,
B. O. Rosseland and A. Kiessling, manuscript submitted for publication). In
contrast to the DA cannulation technique, HPV cannulation in fish is more
difficult and intrusive (McLean and Ash,
1989), but the recovery time is similar, with blood cortisol,
glucose, ion, pH, CO2 and haematocrit values being restored during
the first 24 h (Eliason et al.,
2007). We were pleased to observe normal haematocrit, leucocrit,
and stable ALAT and ASAT values for the duration of our 48-h experiments, as
well as clear evidence of digestion, nutrient absorption from the intestine,
and AA metabolism by the liver with the staged, double cannulation technique
used here.
The present study clearly shows that plasma free AA measurements in the HPV
provide a much greater resolution of the uptake profiles than do DA
measurements, presumably because of hepatic metabolism. The free AA
concentrations reported here for DA samples are comparable to earlier studies
where only the DA was cannulated (Ok et
al., 2001; Sunde et al.,
2003). In general, our data also agree with the earlier study of
Ash et al. (Ash et al., 1989),
who measured the postprandial concentrations of free AA in both the DA and HPV
of lightly anaesthetized rainbow trout, but only at 3 h. They found a much
smaller increase from the base line (48 h starved fish) at 3 h and smaller
differences between the DA and HPV samples compared with the present study.
However, beyond general comparison with this earlier study, detailed
comparisons are complicated by the reporting of blood rather than plasma
concentrations and by measuring baseline and postprandial values in different
sets of fish. Also, Ash et al. occluded a major route from intestine to HPV by
cannulating the intestinal vein, whereas we minimized vessel occlusion by
cannulating a smaller side vein off the main dorsal and ventral intestinal
veins (Ash et al., 1989). Since
the concentration of free AAs in the HPV is probably a combination of the
rates of intestinal blood flow and AA uptake, alterations to intestinal blood
flow could alter free AA concentrations. Therefore, comparisons with
anaesthetized fish are compromised because anaesthetic procedures and handling
reduce gut blood flow (Thorarensen et al.,
1993; Eliason et al.,
2007). Sedatives could also affect AA uptake rates even though
Kolanczyk et al. did not find any significant changes in liver enzyme activity
after exposure to MS-222 (Kolanczyk et
al., 2003).
Ok et al. found that postprandial plasma free AA concentrations in the DA
peaked at 4 h, except for glycine (Ok et
al., 2001). Here, the total free AA concentration peaked at 6 h, a
time frame that agrees with the results reported after serial sampling of
slaughtered fish (see Sunde et al.,
2003; Espe et al.,
1993). This slight delay in the peak of free AA compared with
those found by Ok et al. may be related to the warmer temperature
(
17°C) used in the experiments of Ok et al. compared with the two
subsequent studies (10°C), although an effect of dietary differences
cannot be excluded. Ok et al. used a combination of crystalline amino acids
and casein and gelatine (Ok et al.,
2001), and crystalline AAs are known to be absorbed quickly
(Cowey and Walton, 1988). A
more rapid uptake should result in higher and sharper peaks of plasma free
AAs.
The three different uptake patterns of free AAs observed in the present
study are difficult to confirm. Neither Ash et al.
(Ash et al., 1989) nor Sunde et
al. (Sunde et al., 2003) used
repeated sampling, whereas Ok et al. used an artificial diet, possibly
compressing digestion (Ok et al.,
2001). Lyndon et al. found both single and double peaks in uptake
profiles for cod (Lyndon et al.,
1993), but their data show great divergence for the same free AAs
between the two sample sites, suggesting ambiguous results due to serially
slaughtering a group of fish to obtain blood samples from the HPV and by
cardiac puncture. Espe et al. also used serial slaughter with Atlantic salmon
(Salmo salar) and reported three uptake profiles using caudal
puncture to obtain blood (Espe et al.,
1993). A mixed artery-vein sample makes direct comparisons to the
present work difficult. In the present work, it was clear that free AA uptake
was well underway by 3 h, despite the gavage method, and that the maximum
uptake rates, as judged by the HPV concentrations, occurred between 6 and 24
h, depending on the individual AA.
Free amino acid uptake profiles
We observed three different free AA uptake profiles. Different AAs are
digested and absorbed by different mechanisms, grossly classified as active
and passive carriers and channel-mediated diffusion. In addition, di- and
tripeptides are absorbed independently. In fact, as much as 70-85% of all
luminal AAs may be absorbed from the digesta into enterocytes in the form of
small peptides (Krehbiel and Matthews,
2003). However, after absorption into the enterocytes, the
peptides are further hydrolysed intracellularly. As a result, most of the AAs
appearing the hepatic portal vein are free AAs
(Krehbiel and Matthews, 2003).
Such differences in absorption mechanisms could explain the three profiles
observed here. With the exception of cysteine, all the AAs with uptake
profiles 2 and 3 (Fig. 2B,C)
are known to be taken up by the mammalian gut via active transport
mechanisms. Similar active transport mechanisms may exist in fish, although
they are not yet identified (Smith,
1989; Halver and Hardy,
2002). Thus, if the number of transporters is limited, the uptake
profile will have a longer duration. By contrast, AAs absorbed via
passive carriers and diffusion will be concentration dependent, and small
peptides are known to be absorbed more rapidly
(Steinhardt and Adibi, 1986;
Matthews, 2000;
Bogé et al., 2002;
Dabrowski et al., 2005).
An alternative explanation for the plasma free AA profiles
(Fig. 2A-C) is regional
absorption of specific AAs, with the ones displaying a slower peak being
absorbed in more distal parts of the intestine. This is a less plausible
explanation because several studies indicate that the majority of AA and
peptide absorption occurs in the proximal- to mid-intestine
(Webb Jr, 1990;
Matthews, 2000). The AAs for
which there were two peaks (tryptophan and threonine,
Fig. 2C) could be an exception
in that the second peak could partly reflect reabsorption of AAs from
proteolytic enzymes containing significant amounts of tryptophan and threonine
in the distal intestine. Also, Umezawa et al.
(Umezawa et al., 1985) showed
that co-administration of leucine and tryptophan may delay the tryptophan
absorption.
Free AA uptake efficiency and metabolism
Finding similar pre- and post-digestion plasma free AA concentrations was
an encouraging quality control for the experiments and therefore we feel
confident about discussing the ratios of free AA in HPV and DA samples. We
expected the HPV concentration to be elevated over the DA concentration
because blood returning to the sinus venosus from the hepatic circulation is
diluted by other systemic venous return in direct proportion to the relative
proportion of hepatic blood flow. Based on available literature
(McLean and Ash, 1989;
Thorarensen et al., 1993;
Eliason, 2006) and personal
observations, roughly 30% of cardiac output is channelled via the HPV
in resting and unfed fish and has been estimated as 12.8 ml min-1
kg-1 fish (McLean and Ash,
1989). Gut blood flow increases by 60-100% after a meal and
approaches 50% of cardiac output
(Thorarensen et al., 1993;
Eliason, 2006). Had we
measured these relative flows in the present experiment, we could have
directly calculated uptake efficiency as
([AAHPV]-[AADA])xblood flow)/total intake of AA,
and then estimated liver metabolism of individual free AAs from their
respective DA and HPV concentrations. Despite the lack of blood flow data, we
still found evidence of hepatic and systemic metabolism of free AA because the
concentration ratio varied among AAs and over time.
If there was no hepatic metabolism of the absorbed free AAs during their first pass through the liver, the difference between the HPV and DA free AA concentrations would reflect simple dilution by systemic venous return and, based on the above blood flow distributions, a 50% dilution is a reasonable dilution for the postprandial state. Such a dilution can explain the HPV-DA difference for several (e.g. glutamic acid and taurine; Tables 4, 5 and 6), but not all free AAs. These free AAs also have parallel curves throughout the active absorption phase (3-24 h samples). A complicating factor in this estimate is the possibility of an accumulation of AAs in the plasma as neither the hepatic or systemic tissues completely remove all AA before the blood is returned to either the intestine or the systemic vasculature. In cases where the HPV curve shows a sharper inclination before the maximum peak, compared to the DA curve, we assume that hepatic absorption dominates (e.g. valine, cysteine, tryptofan, threonine, serine; Tables 4 and 5). However, with major removal of AAs by the systemic tissues, such as muscle, the dilution effect will become more prominent, resulting in an increased HPV-DA difference. But such a situation should be signified by a reduction in concentration in the DA rather than by an increase in the concentration in the HPV, especially after the absorption peak, as seen for, e.g. histidine, isoleucine, lysine, arginine, glycine and glutamine (Tables 4 and 5).
An additional novel discovery here is the possibility of intestinal
metabolism of AAs before they reach the liver. This conclusion is supported by
the fact that not only was the ammonia level higher in the HPV than the DA,
but that the difference between the two blood sampling sites increased during
free AA absorption such that the plasma ammonia levels were three times higher
in the HPV than the DA. Thus, there is a clear role for the liver in
protecting the rest of the fish from elevated and perhaps even toxic levels of
ammonia in the general circulation. There was a different signature for plasma
urea, with a significant difference only existing at 12 h. These results
suggest that there is a significant deamination of AAs, and to a lesser extent
urea formation, before blood from the intestinal mucosa reaches the liver
via the HPV. Utilising the same calculation as given above, the
amount of deaminated AAs could be estimated, yielding information on the
effect of diet alteration on AA as a substrate for fuelling the digestion
processes, especially if labelled substances were used. At the same time, the
majority of ammonia [main metabolite of AA deamination in fish
(Halver and Hardy, 2002)] is
excreted across the gills just before the DA sample site, thereby yielding a
baseline value for the plasma entering the intestine. To what degree ammonia
and urea might be generated in the lumen of the intestine during digestion,
and pass directly into the hepatic portal blood is unclear. However, Mommsen
et al. discovered a high activity of glutamine synthetase in tilapia
gastrointestinal tract and have suggested its role is in ammonia
detoxification (Mommsen et al.,
2003). Our data concur with the need for such a role, but suggest
that if present in Atlantic salmon, the detoxification role is partial and
hepatic metabolism in combination with gill excretion are additional
components of such a protective detoxification system.
In conclusion, the present work shows that a double cannulation in rainbow trout is a feasible tool for physiological studies of nutrition in fish and can be used to accurately track uptake profiles of individual free AAs and provide a much deeper appreciation of underlying mechanisms compared with information provided by a single DA cannulation. In addition, we provide clear evidence in support of the hypothesis that there is hepatic metabolism of certain amino acids during their first pass through the liver after absorption by the intestine. Furthermore, by combining these types of studies with measurements of blood flow, it should be possible to accurately estimate tissue assimilation and nutrient catabolism of a specific nutrient during digestion.
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Acknowledgments |
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