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Center for Advanced Food Studies and Department of Biochemistry and Nutrition, The Technical University of Denmark, DK-2800 Lyngby, Denmark
2To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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90% less than that of normal rats. The
present study demonstrates improved hydrolysis and absorption of the
specific oil compared with the other oils examined both in rats with
normal absorption and in rats with malabsorption.
KEY WORDS: • interesterified fats • intestinal absorption • rapeseed oil • decanoic acid • rats
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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,
Morley et al. 1973
). The sn-2 MAG and
long-chain free fatty acids are absorbed by the enterocytes. In the
intestinal mucosa cells, the sn-2 MAG are reesterified with
fatty acids of exogenous or endogenous origin to form a new population
of triacylglycerols (Mattson and Volpenhein 1964
). These
are packed into chylomicrons and excreted into the lymph.
The hydrolysis of the triacylglycerol by the pancreatic lipase is
affected by chain length and unsaturation of the fatty acids in the
sn-1/3 positions (Jandacek et al. 1987
,
Mattson and Volpenhein 1964
, Morley et al. 1973
), with medium-chain triacylglycerols (MCT) being
degraded faster than long-chain triacylglycerols (LCT)
(Greenberger et al. 1966
). After intestinal absorption,
medium-chain fatty acids (MCFA) are preferentially transported via
the portal vein (Bernard and Carlier 1991
, Kiyasu et al. 1952
) to the liver, where they are oxidized
(Mascioli et al. 1991
).
In the treatment of malabsorption (Hubbard and McKenna 1987
) and postsurgical patients (Kenler et al. 1996
, Sandström et al. 1995
), it is
advantageous to have a combination of long-chain fatty acids (LCFA)
and MCFA to provide both energy and essential fatty acids (EFA) as in
randomized lipids. Randomized lipids thus increased body weight and
improved nitrogen balance in thermally injured rats compared with rats
fed LCT (Gollaher et al. 1993
, Mok et al. 1984
, Teo et al. 1989
).
Lipids produced via interesterification of vegetable oils with
MCFA, with a regiospecific lipase, contain MCFA in the
sn-1/3 positions and LCFA in the sn-2 position
(specific triacylglycerol). The intake of these fats may result in
higher fat acid absorption than randomized fat and thus be useful in
the dietary treatment of malabsorption. One reason for the higher
absorption is the rapid hydrolysis of the specific lipid, which is
comparable to that of MCT (Jandacek et al. 1987
).
Another reason is that lingual and gastric lipases (Gargouri et al. 1986
, Paltauf et al. 1974
, Rogalska et al. 1990
, Staggers et al. 1981
)
preferentially hydrolyze fatty acids in the sn-3 position
with high activity toward MCFA. Although a number of studies have been
published on the absorption of interesterified fatty acids, a direct
comparison between rats with normal absorption versus malabsorption
using similar fats has not yet been published. In the present study, we
examined the lymphatic transport of fatty acids in two different rat
models: normal absorption and malabsorption. We compared the lymphatic
transport of a specific fat, a randomized fat and a physical mixture,
all made from rapeseed oil and decanoic acid (or tridecanoin) and with
similar fatty acid profiles, and as the control, rapeseed oil.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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Rapeseed oil (Aarhus Oliefabrik A/S, Aarhus, Denmark) and decanoic acid (Sigma Chemical, St. Louis, MO) were used as substrates for lipase catalyzed interesterification (Lipozyme IM; Novo Nordisk A/S, Bagsværd, Denmark), whereas rapeseed oil and tridecanoin (Grünau GmbH, Illertissen, Germany) was used for chemical interesterification with sodium methoxide as catalyst. The interesterifications were performed as batch processes by S. Balchen at the Department of Biotechnology, The Technical University of Denmark.
The lipase-catalyzed interesterification resulted in regiospecific
triacylglycerols with 10:0 mainly located in the sn-1/3
positions, whereas the chemical interesterification resulted in a
random location of fatty acids in the triacylglycerol molecules. A
physical mixture was made from rapeseed oil and tridecanoin by simple
mixing, and rapeseed oil was used as the LCT control (Table 1
).
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Fatty acid methyl esters (FAME) were prepared from triacylglycerols
through transesterification catalyzed by KOH in methanol
(Christopherson and Glass 1969
). The FAME dissolved in
heptane were analyzed by gas-liquid chromatography using a
Hewlett-Packard 5890 series II Chromatograph with
flame-ionization detection (Hewlett-Packard GmbH, Waldbronn,
Germany) and a fused silica capillary column (SP-2380, 60 m, I.D.
0.25 mm; Supelco, Bellefonte, PA). Carrier gas was helium. A split
ratio of 1:14.6 was applied. The initial column flow rate was 1.2
mL/min. The initial oven temperature was 70°C for 0.5 min, and
temperature programming was as follows: 15°C/min to 160°C,
1.5°C/min to 200°C, which was maintained for 15 min, and then
30°C/min to 225°C, which was maintained for 5 min.
Regiospecific analysis of the test oils was performed by degradation
with allyl magnesium bromide as Grignard reagent (Becker et al. 1993
). The sn-2 MAG fraction was isolated by
thin layer chromatography on boric acid–impregnated thin layer
chromatography plates developed twice (2 x 60 min) in
chloroform/acetone (90:10 v/v), methylated and analyzed by
gas-liquid chromatography as described here.
Housing of animals.
Male Wistar rats weighing 220–240 g were purchased from Møllegård
Breeding Center (Ll. Skensved, Denmark). They were housed in groups of
four and, until surgery was performed, fed a commercial standard
nonpurified pelleted rat diet (Altromin no. 1324; Chr. Petersen A/S,
Ringsted, Denmark) as described previously (Christensen et al. 1998
). The diet contained 4% fat. The rats were randomly
divided into eight groups.
Tubing.
A clear vinyl tubing (I.D. 0.5 mm, O.D. 0.8 mm) was used for cannulation of the main mesenteric lymph duct (Dural Plastics and Engineering, Crictley Electrical Products Pty., New South Wales, Australia). Silicone tubing (I.D. 1.0 mm, O.D. 3.0 mm) was used as a feeding tube, and polyethylene tubing (I.D. 0.28 mm, O.D. 0.6 mm) was used for cannulation of the common bile and pancreatic ducts (both from Polystan, Værløse, Denmark).
Surgery, administration of fat and collection of lymph.
The Danish National Committee for Animal Experiments approved the
experiments. Rats weighing 245–300 g were anesthetized with
pentobarbital (100 g/L) injected intraperitoneally (0.1 mL/100 g
body wt) and subjected to cannulation of the main mesenteric lymph duct
with clear vinyl tubing (Bollman et al. 1948
). A
gastrostomy tube was inserted 2 cm into the fundus region of the
stomach and fixed with a purse-string suture. Rats used in the
malabsorption examination were further subjected to cannulation of the
common bile duct. After surgery, the rats were placed in individual
restraining cages (Bollman 1948
) and kept hydrated via
infusion of 3 mL of saline/h (normal rats 0.15 mol/L NaCl, malabsorbing
rats 0.15 mol/L NaCl, 0.004 mol/L KCl, 0.28 mol/L glucose) administered
through the gastrostomy tube and had free access to drinking water.
The rats recovered from surgery overnight. On the next day, 270 mg of oil was administered as a bolus through the gastrostomy feeding tube followed by 0.5 mL of saline. The fats to the malabsorbing rats were emulsified with a solution of taurocholate, whereas the normal rats (with only lymph cannulation) received pure oil. Fat emulsions were prepared by sonicating 270 mg of oil with 0.3 mL of a 20 mmol of taurocholate and 10 g of choline per L solution (M.S.E. 150-W Ultrasonic Disintegrator; M.S.E., Inc., Crawley, England). The settings were medium power and amplitude of 3.
One-hour lymph samples were collected from -1 h (i.e., 1 h before fat administration) through 8 h and one sample from 8 to 24 h for the normal rats. For the malabsorbing rats, a sample from 8 to 23 h and a 23- to 24-h sample were collected. The lymph was collected at room temperature in tubes (containing 100 µL of a 100 g Na2-EDTA-H2O per L solution; E. Merck, Darmstadt, Germany) that protected it from direct light. The samples were stored at -20°C until analysis. Immediately after the experiments, the rats were administered an overdose of pentobarbital and killed by decapitation.
Analysis of lymph lipids.
After the addition of internal standard (heptadecanoic acid as methyl
ester), lipids were extracted from the lymph according to the method of
Folch et al. (1957)
. The fatty acid composition in lymph
was determined after transesterification catalyzed by KOH in methanol
(Christopherson and Glass 1969
), and the FAME were
analyzed by gas-liquid chromatography as described earlier.
Calculation of recoveries.
Lymph was collected from the main mesenteric duct, which is the major channel for fat transport from the duodenum after absorption.
Recoveries of total fatty acids and individual fatty acids were calculated using the internal standard and thus included a contribution of endogenous fatty acids transported by the lymph.
Statistical analysis.
Results are expressed as mean ± SEM. The values for accumulated transport and recoveries at 24 h were tested using one-way ANOVA. The Student-Newman-Keuls test was used to determine specific differences.
Differences in lymphatic transport between the two rat models of the
individual oils were tested by Mann-Whitney rank sum test after
calculation of area under the curve (AUC) using the trapezoidal rule
(Matthews et al. 1990
) from 0 to 8 h or by
comparing the accumulated transport at 24 h.
The SigmaStat statistical package (Version 1; Jandel, Erkrath, Germany) was used to carry out all procedures. The level of statistical significance was P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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The lymphatic transport of fatty acids during 24 h of four different oils was examined in the mesenteric lymph.
The absorption of the fatty acids decanoic acid [10:0], oleic acid
[18:1(n-9)] and linoleic acid [18:2(n-6)] was faster in normal rats
than in malabsorbing rats (Figs. 1
, 2
). The initial baseline level of 18:2(n-6) was higher than those of 10:0
and 18:1(n-9) due to the endogenous contribution of 18:2(n-6).
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, the AUC from 0 to 8 did
not differ between the randomized oil and the physical mixture, but the
appearance of the curves differed due to the steep increase and
decrease for the physical mixture, whereas the randomized oil curve was
flatter. This may explain the similar accumulated transport and
recoveries over 24 h. The malabsorbing rats had slower absorption of 10:0 than the normal rats. Maximum transport was reached between 5 and 7 h but returned to baseline within 24 h. Maximum absorptions of 18:1(n-9) and 18:2(n-6) were probably between 8 and 23 h. The exact time of maximum absorption could not be identified because we collected one sample from 8 to 23 h. Furthermore, it was not possible to determine whether maximum absorption of the different oils occurred at the same time.
The lymphatic transport profiles of total fatty acids 10:0, 18:1(n-9)
and 18:2(n-6) were significantly lower in malabsorbing rats than in
normal rats both during the first 8 h (AUC P < 0.003, Figs. 1
, 2
) and for accumulated transport after 24 h
(P < 0.006, Tables 2
,
3
). The transport profile of total fatty acids was similar to that of
18:1(n-9) (data not shown).
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Normal rats |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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The accumulated lymphatic transport (in mg) of total fatty acids after
24 h did not differ among the four groups (Table 2)
.
Recoveries of fatty acids.
The recoveries of fatty acids calculated from the amount of each fatty
acid administered and the amount of fatty acids transported in the
mesenteric lymph express the lymphatic transport for the four oils in
another way (Table 4
). The recoveries of 18:1(n-9) and linolenic acid [18:3(n-3)] in rats
fed the specific oil were higher than those of the rats fed the
randomized oil, physical mixture or rapeseed oil (P < 0.05). The recovery of 18:2(n-6) was different in rats fed specific oil
and rapeseed oil, with the highest recovery in the former (P
< 0.05, Table 4
). No significant differences were observed
between the physical mixture group and the randomized oil group (Fig.1
,
Tables 2
and 4
).
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Malabsorbing rats |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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Differences between the specific oil and rapeseed oil groups in
accumulated lymphatic transport were observed only for total fatty
acids and 18:1(n-9) (P < 0.05, Table 3
).
Recoveries of fatty acids.
Higher recoveries of all of the examined fatty acids as well as total
fatty acids were found in rats fed the specific oil compared with those
fed the rapeseed oil (P < 0.05, Table 5
).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSNormal ratsMalabsorbing ratsDISCUSSIONREFERENCES |
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, Selleck et al. 1994
), randomized lipids containing MCFA and LCFA
improved nitrogen balance, increased the gain in body weight and
normalized serum albumin (DeMichele et al. 1988
and 1989
, Teo et al. 1989
). LCFA did not influence
the effects of randomized oils on nitrogen balance regardless of
whether the LCFA were from vegetable oils (DeMichele et al. 1988
and 1989
, Mok et al. 1984
) or fish oil
(Selleck et al. 1994
, Teo et al. 1989
).
Interesterification using an sn-1/3 specific lipase produces
fat with regiospecific locations of fatty acids within the
triacylglycerol molecules. Interesterification of LCT with MCFA results
in a specifically structured lipid with LCFA in the sn-2
position and MCFA located mainly in the sn-1/3 positions.
This kind of specifically structured triacylglycerol was hydrolyzed as
rapidly as MCT in vitro, and the absorption into an isolated, irrigated
loop of the small intestine was >2.5 times higher than that of an LCT
analogue (Jandacek et al. 1987
).
In malabsorbing rats, the lymphatic transport of 18:2(n-6) from a
specific oil was higher during an 8-h experiment than the transport of
18:2(n-6) from a randomized oil, a physical mixture or the native
soybean oil (Christensen et al. 1995
). This study
demonstrated a faster uptake and transport of the specific fat than of
the randomized fat. On the other hand, in normal rats, Jensen et al. (1994)
observed that the level of 18:2(n-6) in the
sn-2 position of the lymph lipids after a bolus of
randomized oil was two thirds of the level found after a bolus of
specific lipid, even though only one third of the 18:2(n-6) was in the
sn-2 position of the randomized oil and all of the 18:2(n-6)
of the specific oil was in the sn-2 position. They suggested
that better hydrolysis of the randomized oil could account for this
observation. Tso et al. (1995)
observed a reduced uptake
of sn-2 linoleate from a specific oil (8:0/18:2/8:0)
compared with the randomized analogue in normal rats. This was not the
result of limited hydrolysis but rather reflected the inability of the
small intestine to resynthesize triacylglycerol after absorption of
sn-2-MAG and free fatty acids because of a low supply of
LCFA for triacylglycerol resynthesis.
The conflicting results for specific fat compared with randomized fat may result from differences in the oils and the experimental conditions. Here, we extend the examinations of lymphatic transport of four test oils to include both rats with normal absorption and malabsorbing rats.
In normal rats, the maximum absorptions of 18:1(n-9) and 18:2(n-6) were obtained after 3 h for the specific oil and physical mixture and after 5–6 h for rapeseed and randomized oils. This difference in the time of maximum transport may result from a faster hydrolysis of the specific oil than of the randomized and rapeseed oils. The MCFA and the sn-2 MAG released via the rapid hydrolysis of MCT in the physical mixture by pancreatic lipase may improve the emulsification of the LCT. This, again, may result in an earlier maximum absorption than for the randomized and rapeseed oils. The maximum absorption occurred earlier for 10:0 than for 18:1(n-9) and 18:2(n-6), probably due to rapid hydrolysis and/or rapid absorption of MCFA compared with LCFA.
Although rapeseed oil had a considerably higher level of 18:3(n-3) both overall and in the sn-2 position compared with the other oils, the recoveries of C18:3(n-3) were similar for the physical mixture and the randomized oil and significantly lower than that for the specific oil. This indicates that the triacylglycerol structure of the oil and the presence of 10:0, and not the level of the individual fatty acid in the oil, were the major determinants of the amount of fatty acids absorbed and transported.
The improved recoveries of 18:1(n-9), 18:2(n-6) and 18:3(n-3) in normal
rats of the specific oil group may reflect a better hydrolysis of the
specific oil due to the location of 10:0 in the sn-1/3
positions (Jandacek et al. 1987
). However, the
endogenous contribution of fatty acids also influenced the lymphatic
transport, especially of 18:2(n-6) (Mansbach and Dowell
1992
, Savary and Constantin 1967
), which is
evident from the recovery of total fatty acids (121%) and 18:2(n-6)
(175%) from the specific oil. Low recoveries of the exogenous
18:3(n-3), were observed, but the recovery was high from the specific
oil, which indicates a better hydrolysis and absorption of the specific
oil over 24 h than of the other oils tested. Experiments conducted
in our laboratory (Maj-Britt Fruekilde, unpublished data) showed a
contribution of endogenous fatty acids from the bile to the lymph,
which in addition to the exogenous fatty acids from the dietary oil may
account for the 121% recovery of total fatty acids from the specific
oil. However, the endogenous fatty acids from the bile and the
exogenous fatty acids account for only 129% (Maj-Britt Fruekilde,
personal communication) of the 175% 18:2(n-6) recovered from the
specific oil. Endogenous fatty acids from other sources (e.g., adipose
tissue) thus may contribute to the lymphatic transport of fatty acids.
The differences in lymphatic transport of fatty acids after the intake
of the various oils may therefore result from both differences in rates
of absorption and different mobilizations of endogenous fatty acids
(Porsgaard et al. 2000).
The three manufactured oils had similar contents of 10:0, but the
specific oil had only 19.6 mol/100 mol 10:0 in the sn-2
position, whereas the randomized oil and the physical mixture had 45.3
and 46.6 mol/100 mol, respectively. If dietary 10:0 from the
sn-1/3 positions was absorbed directly to the portal vein
(Bernard and Carlier 1991
, Kiyasu et al. 1952
), we would expect the specific oil to result in less 10:0
appearing in the lymph compared with the randomized oil and physical
mixture (Ikeda et al. 1991
). Actually we observed
similar amounts of 10:0 in the mesenteric lymph from the three oils,
which may reflect better hydrolysis and higher absorption of the
specific oil, as well as acyl migration in the triacylglycerol
molecules during hydrolysis.
In the malabsorbing rats, there was no endogenous fatty acid
contribution from the bile due to the surgical technique
(Mansbach and Dowell 1992
). A higher lymphatic transport
of 18:2(n-6) in the rats fed the specific oil compared with the other
groups was observed, suggesting a better hydrolysis of the specific oil
or greater mobilization of endogenous fatty acids.
Christensen et al. (1995)
observed a significantly
improved lymphatic transport of 18:2(n-6) in malabsorbing rats fed a
specific oil compared with a randomized oil, a mix of soybean oil and
MCT (all with similar overall fatty acid profiles) and a soybean oil.
We observed only significant differences between the specific oil and
the rapeseed oil groups in lymphatic transport of malabsorbing rats.
The differences between our results and those of Christensen et
al. (1995)
may arise from several factors: 1) their
specific oil had no detectable MCFA in the sn-2 position,
2) most of the MCFA in their oils were 8:0 with a higher
chyloportal partition than 10:0 (Christensen et al.
1995
), 3) they used rats anesthetized during the
experiment 4) that had a thoracic lymph duct cannulation and
5) the duration of the experiment was only 8 h. We used
1) a specific oil with 19.6 mol/100 mol MCFA in the
sn-2 position, 2) with 10:0 as MCFA,
3) unanesthetized rats 4) with a main mesenteric
lymph duct cannulation, and 5) the structured fats were
manufactured from rapeseed oil and therefore had only 21.9 mol/100 mol
18:2(n-6), which increased the relative importance of endogenous fatty
acids during the 24 h of the experiment.
Our specific oil was a pilot scale batch product that was less specific
than the laboratory scale products used by Jensen et al. (1994)
and the pure 8:0/18:2/8:0 used by Tso et al. (1995).
They observed no improvement in the lymphatic transport
of fatty acids from a specific oil compared with a randomized oil. The
higher level of LCFA in the sn-1/3 positions in our specific
oil may explain the similar transport and recoveries of fatty acids
from the randomized oil and the specific oil in normal rats. However,
differences in contents of 18:2(n-6) and 18:1(n-9) may also have
influenced absorption and lymphatic transport. Linoleic acid is a major
endogenous fatty acids in the baseline lymph (Porsgaard et al. 1999
). Oils with either 18:2(n-6) or 18:1(n-9) as major LCFA
may differently mobilize endogenous fatty acids transported by the
lymph.
The recoveries of 18:1(n-9) and 18:3(n-3) in normal rats did not reach
100% after 24 h. Absorption of these fatty acids into the portal
vein (Bernard et al. 1991
, Mathieu et al. 1996
, McDonald et al. 1980
) and to the thin
accessory lymph duct next to the main mesenteric lymph duct and
oxidation by the intestine (Bernard et al. 1991
,
Vallot et al. 1985
) may explain the lower recoveries.
The intragastric administration of fat in both rat models probably
excluded the activation of lingual lipase (Hamosh et al. 1989
), and only a trace amount of gastric lipase is present in
rats (DeNigris et al. 1988
). The hydrolysis of the test
oils therefore results from pancreatic lipase activity. The preduodenal
lipases preferentially hydrolyze short- and medium-chain fatty
acids (Gargouri et al. 1986
, Staggers et al. 1981
) from the sn-3 position (Paltauf et al. 1974
, Rogalska et al. 1990
). We would therefore
expect an even more improved recovery of fatty acids from the specific
oil in cases of malabsorption (Hamosh 1994
), where not
only the pancreatic lipase but also the preduodenal lipases contribute
to the hydrolysis of dietary lipid. In the clinical treatment of
short-bowel patients, this may be important, because it has
recently been demonstrated that they frequently have compromised EFA
status (Jeppesen et al. 1997
and 1998
).
The present study indicates improved hydrolysis and absorption of fatty acids from the specific oil compared with the other oils examined but also indicates that optimal absorption of a structured fat indeed depends on the regiospecific structure of the product.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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3 Abbreviations used: AUC, area under the curve;
FAME, fatty acid methyl esters; LCFA, long-chain fatty acid; LCT,
long-chain triacylglycerol; 2-MAG, 2-monoacylglycerol; MCFA,
medium-chain fatty acid; MCT, medium-chain triacylglycerol.
Manuscript received March 10, 2000. Initial review completed April 14, 2000. Revision accepted August 7, 2000.
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|---|
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