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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 METHODSRESULTSDISCUSSIONREFERENCES |
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-linolenic rapeseed oil was significantly higher than that
of the other fats (P < 0.05), except corn oil. The
lymphatic transport of the other fats followed a slower course, with
cocoa butter and menhaden oil having the lowest amounts transported.
The amount of triacylglycerols found in lymph in response to the
administered fats at 8 h ranged from 27.5% of the administered
dose for cocoa butter to 72.1% for olive oil. The value for cocoa
butter was significantly lower than that for most other fats. At
24 h, the values ranged from 66.5% for cocoa butter to 121.2%
for olive oil. The high value for olive oil suggested transport of
endogenous as well as exogenous fatty acids. The low value observed
after cocoa butter resulted from decreased lipolysis and possibly also
low absorption of triacylglycerols with high levels of long-chain
saturated fatty acids in the sn-1/3 position.
Furthermore, a low value was observed after menhaden oil
administration, suggesting decreased absorption of fats containing
(n-3) long-chain polyunsaturated fatty acids. Overall, these
results demonstrate the influence of the fatty acid composition and
triacylglycerol structure on the lymphatic absorption of dietary
fat.
KEY WORDS: • dietary fats • fatty acid profile • lymphatic absorption • rats • triacylglycerol structure
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Hamosh and Scow 1973
,
Paltauf et al. 1974
). The highest activity was found
toward short- and medium-chain fatty acids (Cohen et al. 1971
, Hamosh 1979
). This rapid hydrolysis is
especially important for the digestion of milk fat triacylglycerols
before reaching the duodenum in newborns (Hamosh 1979
)
and also in certain disease states with pancreatic insufficiency such
as cystic fibrosis (Bronstein et al. 1992
).
The enzyme primarily responsible for hydrolysis of dietary
triacylglycerols is pancreatic lipase, which degrades
triacylglycerols into sn-2 monoacylglycerols and fatty
acids after emulsification of the triacylglycerols with bile acids
(Hofmann and Borgström 1964
, Mattson and Beck 1956
). The lipase hydrolyzes ester bonds with
long-chain saturated fatty acids, e.g., palmitic acid, 16:0 and
stearic acid, 18:0 (Bergstedt et al. 1990
, Ockner et al. 1972
) and long-chain polyunsaturated fatty acids
(PUFA)3
of the (n-3) family, e.g., eicosapentaenoic acid (EPA), 20:5(n-3), and
docosahexaenoic acid, 22:6(n-3) (Bottino et al. 1967
,
Chen et al. 1994
, Christensen et al. 1995a
) less efficiently than other fatty acids, leading to slow
absorption of dietary fats containing high amounts of these fatty acids
located in the sn-1/3 positions of the triacylglycerols.
After absorption into the enterocytes, long-chain fatty acids are
activated and 2-monoacylglycerols are reacylated into a new population
of triacylglycerols (Åkesson et al. 1978
,
Christensen et al. 1995a
), but with conservation of the
fatty acids in the 2-position as in the dietary fats and secreted to
the lymph packaged as chylomicrons. After entering the circulation,
lipoprotein lipase in the endothelial lining hydrolyzes the chylomicron
triacylglycerols with positional specificity toward the primary ester
bonds (Nilsson-Ehle et al. 1973
). Fatty acids from
chylomicron triacylglycerols derived from different dietary sources are
not removed from the circulation at the same rate (Botham et al. 1997
, Levy et al. 1991
), indicating that the
initial fatty acid profile and triacylglycerol structure may influence
the degradation by lipoprotein lipase of chylomicron triacylglycerols
and thereby the postprandial clearance of triacylglycerols.
In this experiment, we compared the intestinal absorption in rats of
nine different dietary fats representing a wide spectrum of fatty acid
compositions and intramolecular structures. The administered fats were
two rapeseed oils, differing primarily in the content of linoleic and
-linolenic acid, olive, corn, palm and menhaden oil, as well as
butter, cocoa butter and lard. We wanted to determine the effect of
differences in fatty acid composition and triacylglycerol structure on
the absorption under similar experimental conditions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The following experiment was approved by the Danish Committee for
Animal Experiments. Male albino Wistar rats were obtained from
Møllegaard Breeding and Research Center, Ll. Skensved, Denmark. They
were fed a standard nonpurified diet (Altromin No. 1324, Chr. Petersen
A/S, Ringsted, Denmark) as used previously (Christensen et al. 1998
) and weighed 250–300 g at the time of surgery. Rats were
anesthetized intraperitoneally with pentobarbital (~0.05 mg/g body
weight) and were subjected to cannulation of the main mesenteric lymph
duct (Bollman et al. 1948
) with a clear vinyl tube
(o.d., 0.8 mm; i.d., 0.5 mm; Critchley Electrical Products, New South
Wales, Australia). A feeding silicone tube (o.d., 3.0 mm; i.d., 1.0 mm;
Polystan, Værløse, Denmark) was inserted into the fundus region of
the stomach and fixed with a purse-string suture. After surgery,
the rats were placed in individual restraining cages (Bollman 1948
) with tap water freely available, no food, but a steady
infusion of physiological saline (9 g/L NaCl) at 3 mL/h through the
feeding tube.
Administration of fat and collection of lymph.
The postoperative day, the experiment was initiated by collection of a baseline fraction of lymph from -1 to 0 h. At time "zero," a sonicated emulsion of 0.3 mL dietary fat and either 10 mg phosphatidylcholine (Sigma Chemical, St. Louis, MO) mixed with 0.3 mL saline (rapeseed, olive, corn and menhaden oil) or 0.3 mL of a solution containing 20 mmol/L taurocholate (Sigma) and 10 g/L choline (Sigma) in distilled water (palm oil, butter, cocoa butter and lard) was injected through the feeding tube followed by 0.6 mL saline. Preliminary experiments showed that the absorption and lymphatic transport of fat were not affected by the nature of the emulsifying agent. The infusion of saline was continued at 3 mL/h for the rest of the experiment. Solid fats (butter, cocoa butter and lard) were gently melted before emulsification. For the next 8 h, lymph was collected in 1-h fractions in tubes containing 100 µL of a 100 g/L Na2-EDTA-solution (E. Merck, Darmstadt, Germany). A combined fraction was obtained from 8 to 24 h. The tubes were frozen immediately after collection and kept at -20°C until further processing.
Fats and lipid analysis.
Low -linolenic rapeseeds were selected by DLF-Trifolium, St.
Heddinge, Denmark, and the oil was refined at the Department of
Biotechnology, DTU, Lyngby, Denmark. High -linolenic rapeseed oil
was purchased from Scanola, Aarhus, Denmark, cocoa butter and palm oil
from Aarhus Olie, Aarhus, Denmark, menhaden oil from Zapata Haynie (now
Omega Protein), Hammond, LA; corn and olive oil, butter and lard were
purchased in local supermarkets. The fatty acid composition was
determined by gas-liquid chromatography (GLC) after methylation
with KOH in methanol (Christopherson and Glass 1969
).
The structure of dietary fats was determined by Grignard degradation
with allyl magnesium bromide followed by isolation and analysis of the
sn-2 monoacylglycerol fraction (Becker et al. 1993
) and methylation with KOH in methanol. The resulting fatty
acid methyl esters were analyzed using a Hewlett-Packard 5880A
chromatograph (Waldbronn, Germany) with a SP2380 capillary
column (30 m, i.d. 0.32 mm; Supelco, Bellefonte, PA),
flame-ionization detection and helium as a carrier gas. Initial
oven temperature was 120°C followed by temperature programming as
follows: 4°C/min to 160°C, maintained for 2 min, followed by
8°C/min to 200°C, which was maintained for 10 min, and finally the
temperature was raised to 225°C and maintained for 5 min. Peak areas
were calculated using a Hewlett-Packard computing integrator and
used to calculate the mol/100 mol of fatty acids following correction
for response factors based on actual standards (Nu-Chek-Prep, Elysian,
MN).
Analysis of lymph lipids.
Total lipid was extracted from lymph fractions according to the method
of Folch et al. (1956)
after addition of internal
standards (13:0 and 17:0 methyl esters). After methylation with KOH in
methanol, the fatty acids were analyzed by GLC as described above. The
internal standards were used to calculate the amounts of fatty acids
transported in lymph.
Statistical methods.
Results are expressed as means ± SEM
(n = 7 in groups receiving butter and high
-linolenic rapeseed oil, n = 6 in other groups).
Differences among the accumulated lymphatic transport of fatty acids in
rats fed different fats were tested using ANOVA (Jandel SigmaStat
statistical package, Version 2.0, Jandel Corporation, Erkrath,
Germany). The Student-Newman-Keuls method was used to determine
specific differences. The level of statistical significance was taken
as P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The dietary fats represented a wide range of different fatty acid
compositions (Table 1
). Between one third and two thirds of the fatty acids in palm and
menhaden oil, butter, cocoa butter and lard were saturated, with the
highest levels in butter and cocoa butter. Olive oil and the two
rapeseed oils were composed primarily of the monounsaturated fatty
acid, oleic acid [18:1(n-9)], but most other fats, except menhaden
oil, contained reasonably high amounts of this fatty acid. Linoleic
acid [18:2(n-6)] was especially abundant in corn oil and represented
one fourth of the fatty acids in the two rapeseed oils. Linolenic acid,
[18:3(n-3)], was present in appreciable amounts only in the two
rapeseed oils, whereas menhaden oil contained 20:5(n-3) and 22:6(n-3).
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The intramolecular structure of the dietary fats represented by the
fatty acid composition in sn-2 monoacylglycerols is shown in
Table 2
. From the total fatty acid composition and the fatty acids in the
sn-2 position, the distribution of fatty acids between
sn-1/3 and sn-2 positions can be calculated. The
two rapeseed oils together with olive oil, palm oil and cocoa butter
had 18:1(n-9) as the major fatty acid in the sn-2 position.
Corn oil contained 18:2(n-6) as the major fatty acid, whereas the fatty
acid present at the highest proportion in the sn-2 position
of menhaden oil, butter and lard was 16:0.
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Administration of dietary fats differing in fatty acid composition and
intramolecular structure resulted in major differences in the
accumulated lymphatic transport of total fatty acids (Fig. 1
). The rats were given the same amount of fat (0.3 mL), corresponding to
~270 mg fat, except for rats fed butter. Butter contains 18% water;
correcting for this, the rats administered butter received 221 mg fat.
Administration of either olive or low -linolenic rapeseed oil
resulted in the highest lymphatic transport of fatty acids, with corn
oil slightly lower than these two oils. The transport of the other
administered fats was slower, with cocoa butter giving rise to the
lowest lymphatic transport in 8 h. The accumulated transport at
8 h after olive and low -linolenic rapeseed oil administration
was significantly higher than that after all other fats (P
< 0.05), except corn oil. The transport of corn oil was
significantly higher than the transport of cocoa butter, menhaden and
palm oil (P < 0.05), whereas administration of lard
resulted in lymphatic transport higher than cocoa butter and menhaden
oil (P < 0.03). The total transport after 24 h
was significantly higher after olive oil administration compared with
all other fats (P < 0.02), except low -linolenic
rapeseed and corn oil (not shown).
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The fatty acid profiles of the administered fats were reflected in the
fatty acid profiles of total lymph lipids 8 h after
administration, although the endogenous contribution of fatty acids was
evident (Table 3
). Lymph lipids from rats fed rapeseed and olive oil contained around
one third 18:1(n-9). The highest level of 18:2(n-6) (38 mol/100 mol)
was found in lymph lipids from rats fed corn oil, although this fatty
acid constituted a major part of lymph lipids derived from all fats.
The high level of 16:0 in palm and menhaden oil, butter, cocoa butter
and lard was reflected in lymph lipids (constituting ~25 mol/100 mol
of total fatty acids). The difference in 18:3(n-3) content between the
two rapeseed oils resulted in a significantly higher level of this
fatty acid in lymph lipids from rats fed the high -linolenic
rapeseed oil (P = 0.001). Furthermore, the presence of
20:5(n-3) and 22:6(n-3) in menhaden oil and their absence in the other
fats led to significantly higher levels of these fatty acids in lymph
lipids from rats fed menhaden oil compared with those fed the other
fats (P < 0.01).
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The estimated amounts of triacylglycerols found in lymph in response to
the administered fats 8 and 24 h after administration showed wide
variations (Table 4
). The values at 8 h ranged from 27.5% of the administered dose
for cocoa butter to 72.1% for olive oil. The value at 8 h for
olive oil was significantly higher than most others (P
< 0.03), except butter, corn and low -linolenic rapeseed oil.
These four fats were the only fats with a value at 8 h of 
50%.
The values at 24 h varied from 66.5% of the administered dose for
cocoa butter to 121.2% for olive oil. Transport of butter, low
-linolenic rapeseed and corn oil led to values of >90%.
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|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Important determinants of the digestion and absorption of fats are the
fatty acid composition and the intramolecular structure of the
triacylglycerols. The preduodenal lipases acting in the stomach are
most active toward short- and medium-chain fatty acids
(DeNigris et al. 1985
, Hamosh 1979
,
Paltauf et al. 1974
); in this study, the main example of
this process was a more rapid hydrolysis of butter because this is the
only fat used that contained these fatty acids (~14 mol/100 mol of
total fatty acids). In this context, it is important to note that
short- and medium-chain fatty acids are absorbed primarily directly
into the blood through the portal vein (Bernard and Carlier 1991
, Vallot et al. 1985
) and therefore are not
incorporated into lymph triacylglycerols. Degrace et al. (1996)
compared the intestinal absorption of butter with corn
and menhaden oil after intragastric administration of pure fats to rats
and observed a lower triacylglycerol output in lymph during the first
6 h after butter administration compared with after the other
fats. This was explained by an increased portal absorption of butter
fatty acids. In our experiment, we did not observe this decreased
lymphatic transport after butter, and we found approximately the same
amount 8 h after administration of butter and corn oil (49.8 and
52.5%, respectively), whereas menhaden oil led to a significantly
lower amount (33.0%) compared with the administered fat.
The absorption of fish oils has been investigated by many groups
because of the suggested antiatherogenic effect of (n-3) long-chain
PUFA (Green et al. 1990
, Harris 1989
,
von Schacky et al. 1985
). Chen et al. (1987)
observed less digestion and absorption of menhaden oil
compared with corn oil by rats, suggesting reduced hydrolysis of fish
oil triacylglycerols by the pancreatic lipase. Chernenko et al. (1989)
compared the absorption of MaxEPA and olive oil in rats
and found similar triacylglycerol amounts in lymph in response to the
administered fats 6 and 24 h after intraduodenal infusion. The
value after administration of MaxEPA at 6 and 24 h was 35.0 and
73.1%, respectively. The different fatty acid compositions of various
fish oils as well as differences in treatment protocols, fat load and
coinfused emulsions may account for the divergence between the studies
by Chen et al. (1987)
and Chernenko et al. (1989)
.
The pancreatic lipase released during fat absorption is primarily
responsible for hydrolysis of the ingested triacylglycerols.
Bottino et al. (1967)
and Chen et al. (1994)
showed that esters of long-chain PUFA of marine
origin [20:5(n-3) and 22:6(n-3)] are highly resistant to the action
of pancreatic lipase possibly as a result of the structure of the (n-3)
PUFA with a double bond close to the ester bond. The menhaden oil used
in our study had a relatively high content of 20:5(n-3) and 22:6(n-3)
(Table 1)
compared with the menhaden oil used by others. Chen et al. (1987)
used menhaden oil with 14.9% 20:5(n-3) and 6.9%
22:6(n-3) for absorption experiments in rats, whereas Myher et al. (1990)
performed stereospecific analysis of menhaden oil
with 12.5% 20:5(n-3) and 7.6% 22:6(n-3). Furthermore, Myher et al. (1990)
found 12.1% 20:5(n-3) and 12.5% 22:6(n-3) in the
sn-2 position. These values correspond to those found in the
menhaden oil used in our experiment (Table 2)
. The high content of
these fatty acids in our menhaden oil might account for the slow
hydrolysis of the triacylglycerols and for the observed relatively low
amount of triacylglycerols found in lymph in response to the oil
(33.0% at 8 h, 72.3% at 24 h).
Long-chain saturated fatty acids are generally believed to be absorbed
less efficiently by the enterocytes and possibly also reesterified less
efficiently into triacylglycerols than corresponding unsaturated fatty
acids (Bergstedt et al. 1990
, Mattson et al. 1979
, Ockner et al. 1972
). Palm oil and cocoa
butter have high levels of 18:1(n-9) in the sn-2 position
(Table 2)
and thus a high concentration of the saturated fatty acids
(16:0 and 18:0) in the sn-1/3 positions. This intramolecular
structure seems to lead to poor lipolysis by pancreatic lipase and
could explain the relatively low amount of lymph fatty acids after palm
oil and cocoa butter administration observed in this experiment (36.5
and 27.5% at 8 h, 66.8 and 66.5% at 24 h, respectively).
Chen et al. (1989)
compared the absorption of cocoa
butter, palm kernel and corn oil in rats. The absorption of cocoa
butter was significantly lower than the absorption of corn oil, whereas
no differences were observed between palm kernel and corn oil. The
value 8 h after cocoa butter administration in our experiment was
significantly lower than after most other fats (P = 0.01), except high -linolenic rapeseed, palm and menhaden oils.
Apgar et al. (1987)
compared the bioavailability of
cocoa butter and corn oil in rats by analysis of total fecal lipids
after feeding the fats in diets for 2 wk. The fecal lipid loss was
significantly greater in the cocoa butter group, suggesting that
decreased bioavailability of this fat was due to its high content of
long-chain saturated fatty acids.
The overall fatty acid compositions of cocoa butter and lard are
similar (Table 1)
; this is also reflected in the fatty acid profile of
total lymph lipids (Table 3)
, but the intramolecular structures differ
substantially (Table 2)
. Cocoa butter has 18:1(n-9) as the major fatty
acid in sn-2 monoacylglycerols, whereas lard has 16:0. This
difference may explain the significantly higher amount of lymphatic
fatty acids recovered 8 h after lard administration compared with
after cocoa butter (P < 0.01), leading to an unimpeded
lipolysis of lard triacylglycerols. The same effect of triacylglycerol
structure could explain the high value observed after butter
administration.
Olive oil administration led to an amount of triacylglycerols found in
lymph in response to the oil of 121.2% at 24 h. This high value,
which we have observed consistently, suggests extensive transport of
endogenous fatty acids as well as those administered exogenously.
Shiau et al. (1985)
showed that a substantial fraction
of total triacylglycerols is derived from endogenous sources during
absorption. In another study (Porsgaard et al. 1999
), we
observed that the fatty acids transported from 15 to 24 h after
administration of fat were derived mainly from endogenous stores. None
of the other monounsaturated- and polyunsaturated-rich vegetable
oils used in this study resulted in values >100%. This may indicate
that olive oil is absorbed more quickly than the other fats, possibly
due to its high 18:1(n-9) content, thereby mobilizing the endogenous
stores of fatty acids after postprandial release of gastrointestinal
hormones such as glucose-dependent insulinotropic polypeptide.
Administration of low -linolenic rapeseed oil led to higher values
(63.6 and 93.7% at 8 and 24 h, respectively) than high
-linolenic rapeseed oil (40.7 and 78.4%), although differences were
not significant (P = 0.06 at 8 h, P = 0.10
at 24 h).
This study has demonstrated that the fatty acid composition and
triacylglycerol structure of the ingested fats influence the absorption
process. We do not know at which step the differences in transported
amounts of fatty acids arise. In addition, further investigations are
required to determine what happens to the fatty acids not transported
by the mesenteric lymph duct. The subsequent fate of the synthesized
chylomicrons is also highly dependent on the absorbed fats.
Botham et al. (1997)
examined the in vitro hydrolysis by
lipoprotein lipase of chylomicrons derived from palm, olive, corn and
fish oils. Chylomicrons derived from corn oil were hydrolyzed most
rapidly and those from palm oil most slowly. The clearance of
chylomicrons was investigated by Levy et al. (1991)
in
rats fed diets rich in safflower oil, coconut oil or medium-chain
triacylglycerols. Chylomicrons derived from safflower oil–fed rats
were cleared more rapidly than the others; furthermore, safflower oil
feeding led to increased adipose tissue lipoprotein lipase activity. In
a study by Christensen et al. (1995b)
, it was shown that
the metabolism of chylomicrons was affected by the intramolecular
structure of the triacylglycerols after feeding different oils rich in
(n-3) long-chain PUFA. This indicates that the absorption as well
as the systemic clearance are dependent on the fatty acid profile and
intramolecular distribution of fatty acids in the dietary fats.
|
ACKNOWLEDGMENTS |
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-linolenic rapeseed oil. |
FOOTNOTES |
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3 Abbreviations used: EPA, eicosapentaenoic acid; GLC, gas-liquid chromatography; PUFA, polyunsaturated fatty acids.
Manuscript received September 10, 1998. Initial review completed October 23, 1998. Revision accepted March 1, 2000.
|
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