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3
*
Division of Nutritional Sciences,
Department of Food Science and Human Nutrition, University of Illinois, Urbana, IL 61801 and
University of Cincinnati Medical Center, Cincinnati, OH 45267
3To whom correspondence should be addressed.
 |
ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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1 µg ßC, 0.5
µg 
-carotene (C)/kJ diet] for 2 wk
(n = 12/group). Increasing dietary fat resulted in
higher VA (P = 0.074) and lower ßC
(P = 0.0001) stores in the liver, suggesting that
consumption of high fat diets enhances conversion of ßC to VA. The
effect of soluble fiber on hepatic VA storage was dependent on fiber
type. Consumption of citrus pectin resulted in lower hepatic VA stores
and higher hepatic ßC stores compared with all other groups,
suggesting less conversion of ßC to VA. In contrast, consumption of
oat gum resulted in hepatic VA and ßC stores that were higher
(P = 0.012) and lower (P = 0.022), respectively, than those of citrus pectin–fed gerbils. The
level of dietary fat consumed with soluble fiber had no interactive
effects on hepatic VA, ßC or C stores. Results demonstrate that
ßC BV is independently affected by dietary fat level and type of
soluble fiber, and suggest that these dietary components modulate
postabsorptive conversion of ßC to VA. This study confirms the
negative effects of citrus pectin on ßC BV, and suggests that oat gum
does not adversely affect ßC BV.
KEY WORDS: • ß-carotene • dietary fat • soluble fiber • vitamin A • Mongolian gerbils
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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), and
this percentage will increase if the U.S. population follows dietary
guidelines to increase consumption of fruits and vegetables. Current
guidelines for Americans also recommend a decrease in fat intake along
with an increase in fiber consumption. However, a decrease in the
bioavailability (BV) of carotenoids may be associated with both of
these recommendations. The typical American diet is considered to be a
high fat, low fiber diet. The percentage of energy from fat is
estimated to be as high as 36% and the total fiber content
approximately one half of the recommended level of at least 25 g/d
(Ganji and Betts 1995
). In contrast, a low fat, high
fiber diet may consist of as little as 10% of total energy from fat
and would approach or exceed the recommended level of fiber.
Several studies suggest that carotenoid BV is enhanced by the
consumption of dietary fat. Plasma and serum ßC responses after a
meal are increased dramatically by the presence of dietary fat
(Dimitrov et al. 1988
, Jalal et al. 1998
,
Jayarajan et al. 1980
, Prince and Frisoli 1993
, Roels et al. 1958
, Shiau et al. 1994
). When dietary fat is absent or intake is too low,
absorption of ß-carotene is reduced (Jialal et al. 1991
, Prince and Frisoli 1993
). Nevertheless,
addition of even a small amount of fat to the diet improves the
absorption of carotenoids from vegetables (Roels et al. 1958
), and optimal absorption may require an intake of as
little as 3–5 g of fat per meal (Jalal et al. 1998
,
Jayarajan et al. 1980
, Roodenburg et al. 2000
, van het Hof et al. 2000
).
Dietary fiber is one factor contributing to the low BV of ßC,
especially from fruits and vegetables. Erdman and co-workers (1986)
reported that among various purified dietary fiber
components, high methoxyl citrus pectin had the highest inhibitory
effect on hepatic VA deposition in chicks fed ßC. Rock and Swendseid (1992)
similarly reported a reduction in plasma ßC
levels when citrus pectin was added to a meal fed to humans. However,
Castenmiller and co-workers (1999)
reported no
effect of dietary fiber on serum ßC response in humans when sugar
beet fiber was added back to enzymatically treated spinach.
In recent years, soluble oat fiber has achieved wide popularity in the
American diet after the Food and Drug Administration approved a health
claim associating its consumption with the lowering of serum
cholesterol levels and reduction in risk of coronary heart disease
(Food and Drug Administration 1997
). As a result, it is
likely that consumption of oat products by the American population may
increase. Because dietary fat enhances absorption of carotenoids, the
amount of fat consumed with a diet high in fiber could alter subsequent
ßC BV. The objective of this study was to evaluate the effects of
consuming low and high fat diets (10 or 30% of total energy)
containing soluble fiber, either citrus pectin or oat gum, on ßC BV.
For the purposes of this study, the definition of the term BV includes
both accumulation of ßC and bioconversion of ßC to VA in tissues.
|
MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Male 4- to 5-wk-old Mongolian gerbils (Meriones unguiculatus) with body weights ranging from 28 to 38 g were obtained from Charles River Laboratories (Raleigh, NC). All gerbils had been fed a commercial diet, postweaning, by the breeder. Upon arriving at our animal facility, gerbils were housed individually in plastic shoebox cages and given free access to water and diet. Room temperature was held constant and lighting was provided on a diurnal cycle of 12 h light:12 h dark for the duration of the study. The University of Illinois Laboratory Animal Care Advisory Committee approved all animal handling procedures.
Experimental design.
The study was designed as a 2 x 4 factorial using two levels of
dietary fat (10 or 30% of total energy) and four dietary fiber types
(zero-fiber, or 7 g/100 g silica, citrus pectin or oat gum). The
duration of the study was 3 wk. Upon arrival, gerbils were acclimated
to a semipurified, pelleted diet free of VA, ßC and -carotene
(C) for 1 wk to help equalize VA stores in body tissues. Overall
health was monitored and body weight was recorded three times during
this week. After this time, a group of 24 gerbils was randomly selected
and killed to determine baseline levels of VA, ßC and C in
tissues. The remaining gerbils were assigned to one of eight treatment
groups (n = 12/group), so that mean body weights of
the groups were not different. During the treatment period, food intake
and body weight were recorded daily and every 2 d, respectively.
After 2 wk, gerbils were deprived of food overnight; the next morning,
they were weighed and killed, and tissues collected.
Diets.
During the 1-wk acclimation period, gerbils consumed a semipurified,
pelleted diet free of VA and ßC, containing 30% of total energy from
fat and 7 g/100 g silica. During the treatment period, gerbils consumed
one of eight semipurified, pelleted diets formulated to be isocaloric
and to contain either 10 or 30% of total energy from fat, and either
no fiber, or 7 g/100 g silica, citrus pectin or oat gum (Table 1
). Diets were designed to deliver 16.7 kJ/g diet and were adapted
from a powdered diet, which has been shown in our laboratory to provide
adequate nutrition for growth in gerbils (Lee et al. 1998
, Pollack et al. 1994
, Thatcher et al. 1998
).
|
)
and lower plasma ßC levels in humans fed a meal containing fiber and
ßC (Rock and Swendseid 1992
). Diets containing silica
(pulverized sand donated by Wedron Silica, Wedron, IL), an inert
bulking material, were used as additional control diets to equalize
energy density with the fiber-containing diets. Two soluble fibers
were chosen from food-grade sources as follows: 1) a
high methoxyl citrus pectin (Grindsted Pectin 1100, Danisco
Ingredients, New Century, KS), and 2) an oat gum containing
high-molecular-weight ß-glucans (courtesy of Agriculture and
Agri-Food Canada, Guelph, Canada). The oat gum was a highly
purified source of ß-glucan and did not contain bran or husks.
ß-Carotene and C were added to treatment diets as freeze-dried
carrot powder (prepared and donated by The Procter and Gamble,
Cincinnati, OH) to achieve a concentration of 1 µg ßC
and 0.5 µg C/kJ of diet. The target ßC
concentrations in the diet were estimated on the basis of the
following: 1) the estimated VA utilization rate of 3.1
µg/(100 g body · d) for gerbils (Lee et al. 1998
); 2) the assumption that the conversion
efficiency of ßC to VA of gerbils is within the range of that for
humans (Lee et al. 1998
); 3) a safety margin
for losses during pelleting and storage; and 4) the average
amount of food consumed by gerbils [8–10 g/(100g body · d)].
Diets were formulated and prepared by Research Diets, (East Brunswick,
NJ), shipped within 3 d of pelleting and subsequently stored at
-80°C throughout the study to limit migration of carotene into the
lipid phase of the pellets. Actual consumption of ßC and C was
calculated directly from diet analysis and total food intake (TFI).
Diet analysis.
Treatment diets were analyzed in duplicate for ßC and C, 2–3
times during the 3-wk study period. Immediately before each extraction,
two pellets (4–5 g) were selected randomly and crushed to a fine
powder using a mortar and pestle. A representative sample of the powder
(0.8–1.0 g) was mixed with 4 mL of absolute ethanol containing BHT (1
g/L) to denature protein and saponified with 2 mL of saturated KOH in a
water bath at 70°C for 30 min. After samples were cooled to room
temperature, 2 mL of distilled water was added and this mixture was
extracted five times with 8 mL of hexane. Hexane layers were combined
and evaporated using an Automatic Speed Vacuum System, Model AES1010
(Savant Instruments, Farmington, NY). Dried extracts were flushed with
argon and stored at -20°C. Analysis using HPLC was completed within
24 h of extraction.
Tissue analyses.
Blood samples were collected by cardiac puncture in gerbils under CO2 anesthesia. Gerbils were subsequently killed by cervical dislocation followed by removal of the liver, adrenal glands and kidneys. Tissues were rinsed with distilled water, dried, weighed and frozen at -20°C for subsequent analyses. Liver tissue was extracted in duplicate. Tissue samples (0.1–0.15 g) were minced and mixed with 4 mL of absolute ethanol containing BHT (1g/L) and were saponified with 1 mL saturated KOH in a water bath at 70°C for 30 min. After samples were cooled to ambient temperature, 3 mL of distilled water was added and this mixture was extracted three times with 8 mL of hexane.
Two separate extraction procedures were completed for kidney. One
kidney from each gerbil was used for VA analysis. The remaining kidney
from each gerbil was pooled with that of another gerbil for ßC and
C analyses. Adrenal glands from two gerbils were pooled, minced and
extracted as described for other tissues. Volumes of serum between 150
and 300 µL were mixed with an equal volume of absolute
ethanol containing BHT (1 g/L) and extracted three times with 1 mL of
hexane. Tissue extracts were flushed with argon, stored at -20°C and
analyzed using HPLC within 24 h.
All extraction procedures were performed under yellow lighting.
Echinenone (a generous gift from Hoffmann La Roche, Nutley, NJ) was
added as an internal standard before extraction for quantification of
ßC and C in diets and tissues.
HPLC analysis.
VA was quantified using a Dynamax Model SD200 Solvent Delivery System, a Dynamax Absorbance Detector UV D-II and a Dynamax HPLC Methods Manager integrator (Rainin Instrument, Woburn, MA). Dried extracts were reconstituted in methly-tert butyl ether (MTBE) immediately before HPLC analysis. VA was separated isocratically using a Supelcosil LC-18 HPLC column (25 cm x 4.6 mm, 5-µm particle size, #58298 Supleco, Bellefonte, PA) with a mobile phase of methanol/acetonitrile/chloroform (47:47:6, v/v/v) at a flow rate of 1.5 mL/min monitored at 325 nm. A precolumn (Upchurch Scientific, Oak Harbor, WA) packed with ODS C-18 (Alltech Associates, Deerfield, IL) protected the analytical column. The retention time for VA was 3.9 min.
ß-Carotene and C were quantified using a Dynamax Model SD200
Solvent Delivery System, a BioRad Model 1790 UV/Vis Detector (BioRad,
Richmond, VA) and a Dynamax HPLC Methods Manager integrator. MTBE was
used to reconstitute the dried extracts. Carotenoids were eluted from a
Vydac C-18 analytical column (25 cm x 4.6 cm,
5-µm particle size, #201TP54, The Separations Group,
Hesparia, CA) protected by a precolumn packed with ODS C-18. A mobile
phase of methanol/acetonitrile/water (88:9:3, v/v/v) plus 10 mL
isooctane was used for isocratic elution of C and ßC at a flow
rate of 2 mL/min monitored at 452 nm. The retention times for C and
ßC were 11.5 and 13.1 min, respectively.
Statistical analyses.
The effects of dietary fat level and dietary fiber type on ßC and
C concentrations in treatment diets, TFI, body weight gain (BWG) and
total ßC and C intake were analyzed using two-way ANOVA. The
main effect of dietary fat level was represented as a contrast between
the groups fed 30% energy as fat with those groups fed 10% energy as
dietary fat (orthogonal coding). The main effects of dietary fiber were
represented as the following three comparisons of groups fed either no
fiber or silica, oat gum or citrus pectin (orthogonal coding):
1) silica contrasted with no fiber to evaluate the
effect of adding an inert bulking agent to the diet, 2)
oat gum and citrus pectin contrasted with silica and no fiber to
evaluate the effect of soluble fiber, and 3) oat gum
contrasted with citrus pectin to evaluate the effect of fiber type.
The effects of dietary fat level and dietary fiber type on tissue
levels of VA, ßC and C were analyzed by multiple linear
regression. Each of the main treatment effects was a separate variable
in the regression model and was represented by the same contrasts as
described for the two-way ANOVA. Thus, the effect of dietary fat
level was assigned one variable, and three variables were assigned to
represent the effects of dietary fiber. Three additional variables were
included for the interaction terms. The outcome variables were the
tissue levels of VA, ßC and C for each gerbil. Total ßC intakes
over the duration of the study were included in the regression model as
a covariate and coded as a deviation from the mean ßC intake.
Data analyses were completed using the Statistical Analysis System
(SAS, 6.12, Institute, Cary, NC) with an assigned -level of 0.05.
Interaction terms and main effects were evaluated only if the multiple
R2 for the two-way ANOVA or the
regression model was significant (P < 0.05). If
the interaction terms were not significant, they were removed from the
regression model, and only the main effects were evaluated. Tissue
levels of VA, ßC and C were predicted to be higher with increasing
dietary fat level. Addition of silica to the diet was not expected to
alter tissue levels of VA, ßC and C significantly compared with no
fiber. Soluble fiber was expected to result in lower tissue levels of
VA, ßC and C compared with the no-fiber and silica groups, and
tissue levels of oat gum–fed gerbils were expected to be similar to
those of citrus pectin–fed gerbils. Two-tailed
P-values were used to evaluate all treatment contrasts.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Diets containing 10 and 30% of total energy as fat will be referred to
as low fat and high fat diets, respectively. Concentrations of ßC and
C in diets, and BWG, TFI, total ßC intake and total C intake in
gerbils fed treatment diets are found in Table 2
. There were no effects of dietary fat level or dietary fiber type on
concentrations of ßC and C in treatment diets.
|
BWG was not affected by dietary fat level or dietary fiber type (Table 2)
. Despite the similarities in weight gain, there was a significant
effect of dietary fat level on TFI (P = 0.005). As
expected, mean TFI was higher for groups fed the low fat diets than for
those fed the high fat diets, except for the two groups fed citrus
pectin, which had similar TFI. Consequently, TFI was also significantly
affected when the groups fed soluble fibers were compared with those
fed no fiber and silica (P = 0.005). Although it was
expected that gerbils would eat more fiber-containing diet to
compensate for the lower energy density of the diet, short-chain
fatty acid (SCFA) production from fermentative breakdown of soluble
fibers by gut microflora would provide additional energy, which would
explain in part the lower TFI for the groups fed citrus pectin and oat
gum.
TFI was positively correlated with total ßC intake (r
= 0.58, P = 0.0001) and C intake (r
= 0.59, P = 0.0001). Therefore, the differences in
TFI could have contributed in part to the significant main effects of
dietary fat level and dietary fiber type and significant interactions
(not shown) on total ßC intake and C intake (Table 2)
. The
regression model using TFI as a covariate was similar to that using
total ßC intake as a covariate. Thus, we chose to use total ßC
intake as the only covariate in the regression model to test for main
effects of treatment and interactions on tissue VA, ßC and C.
Total C intake was not included as a covariate because it was highly
correlated with ßC intake (r = 0.99, P
= 0.0001).
Tissue analyses.
After 1 wk of consumption of the acclimation diet, the baseline group
of gerbils had the following stores: 1) mean hepatic VA
stores of 765.8 ± 35.2 nmol; 2) a mean serum VA
concentration of 1.70 ± 0.26 µmol/L; 3)
mean kidney VA stores of 4.8 ± 0.19 nmol; and 4) a mean VA
concentration in adrenal tissue of 21.6 ± 1.66 nmol/g. ß-Carotene
and C in liver, serum, kidney and adrenal tissues could not be
detected at baseline by the methods used in our laboratory (2 pmol
lower limit); thus, baseline levels were assigned a value of zero.
Liver.
Descriptive statistics of hepatic VA, ßC and C stores for each
treatment group are presented in Table 3
. All groups had higher stores of VA, ßC and C than the baseline
group. The changes in hepatic stores of VA, ßC and C of contrasted
groups of gerbils fed low and high fat diets with and without fiber are
summarized in Table 4
and Figure 1
. There were no significant interactions between the main effects of
dietary fat level and dietary fiber type on tissue levels of VA, ßC
and C (data not shown). Increasing dietary fat from 10 to 30% of
total energy resulted in higher hepatic VA stores (Fig. 1)
. Hepatic VA
stores of groups fed high fat diets were 57.65 nmol (P
= 0.074) higher than those for groups fed low fat diets (Table 4)
.
In contrast, unexpected and significant reductions in hepatic ßC
(Fig. 1B
) and C (Fig. 1C
) stores were observed
with increasing dietary fat. Hepatic ßC and C stores for groups
fed high fat diets were 19.65 (P = 0.0001) and 7.51
nmol (P = 0.0001) lower, respectively, than those for
the groups fed low fat diets (Table 4)
.
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.
Soluble fiber (combined effects of citrus pectin and oat gum) did not
dramatically alter hepatic VA stores. Hepatic VA stores of groups fed
soluble fiber tended to be lower than those of the control groups
(P = 0.429; Table 4
). However, as expected, hepatic
ßC and C stores for groups fed soluble fiber were significantly
lower than those for the control groups by 44.2 (P = 0.0001) and 18.7 nmol (P = 0.0001), respectively.
Consumption of oat gum resulted in unexpected effects on hepatic VA and
carotenoid stores. Hepatic VA stores of groups fed oat gum were
dramatically and significantly higher by 210.38 nmol (P
= 0.012) compared with those fed citrus pectin (Table 4
and Fig. 1
). In contrast, hepatic ßC stores of groups fed oat gum were 14.5
nmol lower (P = 0.022) than those fed citrus pectin.
Serum, kidney, and adrenal tissues.
Dietary fat level and dietary fiber had no effect on VA levels in serum, kidney or adrenal tissues (data not shown). Serum VA concentrations ranged from 1.81 to 2.19 µmol/L. Total VA stores in kidney tissue ranged from 4.3 to 5.6 nmol. Concentrations of VA in adrenal tissues ranged from 8.9 to 14.6 nmol/g.
ß-Carotene and C were not detected in serum before or after
treatment. Food was withheld before killing, which could have
contributed to the absence of serum carotenoids. After the treatment
period, C was not detected in kidney. The concentration of ßC in
kidneys ranged from 0.016 to 0.018 nmol/g. Concentrations of ßC in
adrenal tissues (0.045–0.135 nmol/g) were higher than those in kidney.
Surprisingly, mean concentrations of C in adrenal tissues
(0.04–0.09 nmol/g) were higher than those of ßC, and adrenal
concentrations of C in groups fed oat gum were approximately two- to
threefold higher than in any other treatment group.
|
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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C
stores, suggesting that these dietary components altered ßC BV
independently in this animal model. Increasing dietary fat from 10 to
30% of total energy resulted in higher hepatic VA stores and
significantly lower hepatic ßC stores, suggesting that higher amounts
of dietary fat may enhance postabsorptive conversion of ßC to VA. As
expected, consumption of citrus pectin resulted in lower hepatic VA
stores. Moreover, the higher hepatic ßC in pectin-fed gerbils
compared with all other groups also suggests less conversion of ßC to
VA after consumption of pectin. In contrast to citrus pectin,
consumption of oat gum, unexpectedly, did not affect hepatic VA stores.
In fact, the higher VA levels and lower ßC levels in the livers of
oat gum–fed gerbils compared with pectin–fed gerbils suggest that
this purified ß-glucan fraction from oats had no adverse effect on
uptake and/or conversion of ßC to VA.
Several studies have indicated that carotenoid BV is influenced by the
amount as well as the type of dietary fat consumed in a meal or in the
diet. BV, assessed by changes in plasma/serum responses of ßC in
humans, is dramatically increased by the presence of dietary fat
(Dimitrov et al. 1988
, Jalal et al. 1998
,
Jayarajan et al. 1980
, Prince and Frisoli 1993
, Roels et al. 1958
, Shiau et al. 1994
), and is reduced when dietary fat is absent or intake is
too low (Jialal et al. 1991
, Prince and Frisoli 1993
). Although some studies suggest that optimal absorption of
carotenoids in a single meal may require as little as 3–5 g of dietary
fat (Jalal et al. 1998
, Jayarajan et al. 1980
, Roodenburg et al. 2000
, van het Hof et al. 2000
), recent evidence suggests that fatty acid
composition of a meal may also affect ßC absorption. Hu and co-workers (2000)
reported a lower apparent intestinal
absorption of ßC in humans, as measured by appearance in
chylomicrons, when ßC was ingested with a sunflower oil–rich meal,
high in polyunsaturated fatty acids (PUFA), compared with a beef
tallow–rich meal high in saturated fatty acids (SFA). Additional
evidence suggests that high fat diets rich in PUFA may enhance the
total ability of the small intestine to convert ßC to VA.
During and co-workers (1996)
reported that a diet
containing 15 g/100 g soybean oil elevated total cleavage activity of
ßC 15,15'-dioxygenase and total cellular retinol-binding protein
type II in small intestinal mucosa of rats compared with a diet
containing 2.5 g/100 g soybean oil. Interestingly, this enhanced effect
was observed only for soybean oil, a fat high in PUFA, and not for oils
high in SFA or monounsaturated fatty acids. Results from our study also
support enhanced bioconversion of ßC to VA after consumption of diets
containing a high PUFA cottonseed oil.
Hepatic VA stores were higher, whereas hepatic ßC stores were lower,
in gerbils fed high fat diets compared with those fed low fat diets.
This observation suggests that higher amounts of dietary fat enhance
bioconversion of ßC to VA and may have implications for affecting the
accumulation of VA in tissues. However, the variation in hepatic VA
explained by the main effects of dietary fat level, dietary fiber type
and total ßC intake, was 20% (Fig. 1)
, 5% of which was due to
dietary fat level (data not shown). This suggests that other factors
may be influencing tissue VA. First, because gerbils were depleted of
VA and ßC for only 1 wk before treatment, the VA status of the
baseline group of gerbils was high (766 nmol total liver stores or
306 nmol/g liver), which might minimize ßC uptake and
bioconversion to VA. In addition, the better than adequate VA status of
the gerbils may explain in part why the levels of ßC and VA in serum
and peripheral tissues were not affected by dietary fat level and
dietary fiber. Because the liver is the main storage site for VA, the
levels of ßC and VA in this organ may be more metabolically sensitive
to dietary manipulation of fat and fiber. In addition, the duration of
the dietary treatment period (2 wk) used in this study may not reflect
the long-term effects on tissue VA.
The amount of dietary fat may be a second factor influencing tissue VA.
Some studies suggest that the amount of dietary fat required for
optimal absorption of carotenoids is very low (Jalal et al. 1998
, Jayarajan et al. 1980
, Roodenburg et al. 2000
). Although no studies have reported a
dose-response effect of dietary fat on changes in hepatic VA after
consumption of ßC, the low fat diets in the current study likely
contained an adequate amount of fat for optimal
absorption/bioconversion of ßC in the gerbil model.
Dietary fat level has also been reported to stimulate cell
proliferative activity in the small intestine (Jenkins and Thompson 1992
, Pell et al. 1995
), which is
consistent with higher cell exfoliation. Jenkins and Thompson (1992)
observed regional increases in mucosal mass and cell
proliferation in the mid-small intestine of rats fed diets
containing 2, 10, 25 and 50% of total energy as fat for 20–23 d.
Pell and co-workers (1995)
reported a higher crypt
cell production rate in the jejunum and ileum of mice fed an 8 g/100 g
fat diet compared with those fed a 1 g/100 g fat diet for 2 wk. It is
possible that gerbils fed high fat diets for 2 wk in the current study
may have absorbed substantial amounts of ßC into the intestinal
mucosa, some of which could have been subsequently lost in the feces as
a result of increased cell proliferative activity in the small
intestine.
Dietary fiber may alter absorption of nutrients such as lipids by
binding them, by inducing a bulking effect or by changing the
physiology of the small intestine (Farness and Schneeman 1982
). A widely accepted hypothesis for the mechanism
explaining the effect of soluble fiber on ßC absorption is related to
its disruptive effects on lipid absorption (Lairon 1996
). Soluble fiber changes gastric contents by enhancing
viscosity and delaying gastric emptying. Bile salts and other lipid
compounds, such as cholesterol, may also physically bind fiber
molecules and/or become entrapped in the gel phase of gastric contents
instead of participating in micelle formation. Disruption of micelle
formation could result subsequently in decreased absorption and
increased fecal losses of fats and fat-soluble compounds such as
ßC. Increased fat and bile acid excretions in the feces have resulted
from both pectin and oat bran consumption in humans and animals
(Eastwood and Kay 1979
, Jenkins et al. 1975
, Judd and Truswell 1985
, Kay and Truswell 1977
, Kay et al. 1978
, Leveille and Sauberlich 1966
). In addition, both soluble fibers appear
to be equally effective at lowering serum cholesterol levels
(Brown et al. 1999
, Gallaher and Schneeman 1996
, Jenkins et al. 1975
, Kirby et al. 1981
, Pilch 1987
). Delayed gastric emptying has
also been reported in human subjects after consumption of a meal
containing 15 g of pectin (DiLorenzo et al. 1988
).
When citrus pectin was added in comparable proportions (7 g/100 g) in
chick diets (3.85 g citrus pectin/mg ßC) (Erdman et al. 1986
) and in a meal fed to humans (0.48 g citrus pectin/mg
ßC) (Rock and Swendseid 1992
), the reduction in
hepatic VA stores and serum ßC concentrations was also comparable at
45 and 42%, respectively. In this study, the proportions of citrus
pectin and oat gum in gerbil diets (7 g/100 g; 3.02 g citrus
pectin/mg ßC, 3.49 g oat gum/mg ßC)) were comparable to those
used in the chick and human studies. However, citrus pectin reduced
hepatic liver VA by 29%, whereas oat gum enhanced hepatic VA by 10%.
The lower reduction in hepatic VA in gerbils fed citrus pectin compared
with that in the chick and human studies may be due to the use of
carrot powder, rather than the more bioavailable, commercial ßC
beadlets, as a source of ßC. Castenmiller and co-workers (1999)
reported no effect of dietary fiber on serum ßC
response in humans when sugar beet fiber (FIBREX, TEFCO Food
Ingredients, Bodegraven, The Netherlands) was added back to
enzymatically treated spinach (10g/kg wet weight). This group suggested
that the lack of effect of dietary fiber, in this case, may be due to
the concentration of fiber (0.23 g fiber/mg ßC), which was only half
that used in the study by Rock and Swendseid (1992)
.
Notably, this sugar beet fiber product was reported to contain 73 g fiber/100 g product, one third of which was soluble fiber and 22 g was pectin.
Results from this study and the studies with chicks (Erdman et al. 1986
) and humans (Rock and Swendseid 1992
)
suggest that citrus pectin could have an adverse effect on hepatic VA
accumulation. Although this may be true for citrus pectin, this is not
the case for oat gum. Both fibers are gel-forming polysaccharides
that potentially enhance intraluminal viscosity. Actual viscosity is
highly dependent on the chemical structure of the fiber compound. The
viscosity of pectin depends on both molecular weight and methoxyl
content; a reduction in either will reduce its viscosity
(Gallaher and Schneeman 1996
). Judd and Truswell (1985)
found that high-molecular-weight, low methoxyl pectins
were effective hypocholesterolemic agents only when fed to rats at
twice the dietary concentration of high-molecular-weight, high methoxyl
pectins. In addition, Erdman and co-workers (1986)
reported an inverse relationship between methoxyl content of pectin and
gain in hepatic VA stores in chicks fed ßC. In fact, consumption of
the low methoxyl pectin in that study had no adverse effect on gain in
hepatic VA compared with the control. Furthermore, although the
pectin-fed gerbils in the current study had the lowest stores of
hepatic VA, they also had the highest stores of hepatic ßC,
suggesting that consumption of high methoxyl citrus pectin negatively
influenced the cleavage of ßC to VA.
The higher hepatic VA accumulation in oat gum–fed gerbils compared
with those fed citrus pectin may also be explained by the trophic
effects of SCFA, colonic fermentation products of soluble fiber, on the
small intestinal epithelium. Physiologic changes in small intestinal
morphology and rate of cell proliferation have been reported after
infusion of SCFA in the hindgut of rats (Frankel et al. 1994
, Sakata 1987
) and after consumption of
pectin and oat bran (Jacobs 1983
). Jacobs (1983)
observed enhanced crypt cell proliferation and shortened
cell transit time in the small intestinal mucosa of pectin-fed
rats. These observations are consistent with high cell
exfoliation/turnover rates (Brown et al. 1979
,
Chun et al. 1989
, Jacobs 1983
), which
would predict postabsorptive losses of ßC from the intestinal mucosa.
Interestingly, the opposite effects were observed in oat bran–fed
rats, i.e., reduced crypt cell population and cell replication,
suggesting lower rates of cell exfoliation/turnover. As a result,
predicted postabsorptive losses of ßC would be lower in oat bran–fed
animals than in pectin–fed animals, and newly absorbed ßC would be
available for cleavage in the gut mucosa. The oat bran used in this rat
study was 34% carbohydrate, of which 26% was dietary fiber. The oat
gum used in our study was a purified source of oat ß-glucan without
husks or bran, and we are not aware of any studies that have compared
changes in small intestinal morphology after consumption of citrus
pectin and oat gum.
In summary, we hypothesized that the current dietary guidelines for Americans, i.e., reduce dietary fat intake and increase dietary fiber consumption, could negatively affect ßC BV. Results from this study demonstrated that ßC BV, assessed by accumulation of ßC and bioconversion of ßC to VA in tissue, was independently and adversely affected by consumption of low dietary fat and citrus pectin. Increasing dietary fat from 10 to 30% of the total energy in the diet appeared to enhance bioconversion of ßC to VA in the gerbil model, suggesting that lower fat diets could negatively affect tissue VA. Although a very low dietary fat level could be problematic, it is unlikely that many Americans consume a dietary fat level < 10% of total energy. Moreover, hepatic VA levels did increase after consumption of ßC and either level of dietary fat used in this study.
The effect of dietary fiber on bioconversion of ßC to VA was dependent on soluble fiber type, and only citrus pectin appeared to hinder hepatic VA accumulation. The lower levels of hepatic VA after consumption of citrus pectin vs. oat gum in this study emphasize that the physiologic effects of similar dietary fiber types do vary. Because dietary recommendations are to enhance the consumption of whole grains, fruits and vegetables that contain a variety of both soluble and insoluble fibers, reduced utilization of ßC will most likely occur only in diets with specific, single-fiber supplements.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
2 Funded by a grant from The Procter and Gamble Company, Cincinnati, OH.
4 Abbreviations used: BV, bioavailability; BWG, body weight gain; C, -carotene; ßC, ß-carotene; MTBE, methyl tert-butyl ether; PUFA, polyunsaturated fatty acids; SCFA, short chain fatty acids; SFA, saturated fatty acids; TFI, total food intake; VA, vitamin A.
Manuscript received May 22, 2000. Initial review completed June 21, 2000. Revision accepted July 26, 2000.
|
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