![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
|
|
|
|
|
||
Facultad de Ciencias Experimentales y Técnicas, Universidad San Pablo-CEU, E-28668 Boadilla del Monte, Madrid, Spain
2To whom correspondence and reprint requests should be addressed.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
KEY WORDS: • sucrose-rich diet • pregnancy • hypertriglyceridemia • VLDL • rats
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
,
Swanson et al. 1992
) or hyperlipidemic subjects
(Antar et al. 1970
), and the inclusion of sucrose in a
lipid-rich meal amplifies the postprandial triglyceridemia
(Grant et al. 1994
); the effect is likely a consequence
of the fructose moiety of the sucrose (Cohen and Schall 1988
, Nikkila and Pelkonen 1966
, Swanson et al. 1992
). In normal rats, a sucrose- or a fructose-rich
diet also induces hypertriglyceridemia and insulin resistance
(Bernal et al. 1989
, Gutman et al. 1987
,
Lombardo et al. 1996
, Zavaroni et al. 1982
). The factors responsible for the hypertriglyceridemia are
increased hepatic VLDL synthesis and secretion (Sleder et al. 1980
, Zavaroni et al. 1982
) and impaired
peripheral clearance due to both increased insulin resistance
(Zavaroni et al. 1980
) and decreased adipose tissue
lipoprotein lipase activity (Bernal et al. 1989
,
Soria et al. 1996
).
Although the mechanism is not yet completely understood, in male rats,
the increase in plasma triglyceride levels due to high sucrose intake
is multiphasic, depending on the period of treatment. These levels
increase progressively until d 22–25 of treatment, then decline up to
normal values at 45–50 d and rise again to attain the highest values
at 75–90 d (Gutman et al. 1987
).
Both hypertriglyceridemia and insulin resistance occur during pregnancy
in humans (Alvarez et al. 1996
, Freinkel 1980
, Montelongo et al. 1992
) and rats
(Knopp et al. 1970
, Martin-Hidalgo et al. 1994
, Ramirez et al. 1983
). Gestational
hypertriglyceridemia seems to be the result of enhanced production of
triglycerides by the liver (Wasfi et al. 1980
) and
decreased clearance of circulating triglycerides, which is a
consequence of reduced lipoprotein lipase activity in adipose tissue
(Herrera et al. 1988
, Martin-Hidalgo et al. 1994
). Although one would expect that these changes would be
greatly enhanced when a sucrose-rich diet
(SRD)3
is fed during pregnancy, we found previously that the
hypertriglyceridemic responsiveness to this diet is similar in virgin
and pregnant rats when fed for 20 d (Soria et al. 1996
). However, a SRD during pregnancy in rats has been
reported to have teratogenic effects (Ornoy and Cohen 1980
) or to reduce fetal or newborn weights (Jen et al. 1991
, Soria et al. 1996
), although other authors
report no effect on this variable (Oliveros et al. 1995
).
Although the response to a SRD may differ depending on the time of treatment, this time effect has not been studied previously in female rats, nor has the nature of the variation in gestational hypertriglyceridemia and pregnancy outcome been examined when established at different times after SRD intake. Thus, the goal of the present work was to compare the long-term effects of SRD on plasma triglycerides in pregnant and virgin female rats.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Female Sprague-Dawley rats from our animal quarters were initially
fed a nonpurified diet (B&K Universal, Barcelona, Spain) and housed
under controlled light and temperature conditions (12-h light:dark
cycle; 22–23°C). The experimental protocol was approved by the
Animal Research Committee of the University San Pablo-CEU in
Madrid, Spain. Rats weighing either 160–170 g or 140–150 g (9 and 7
wk old, respectively) were divided into two groups as follows:
1) experimental, in which rats were fed a purified
sucrose-rich diet (63 g sucrose/100g; SRD); and 2)
control, in which rats were fed the same diet except that the sucrose
was replaced with cornstarch (63 g/100g; CD). The diets were based on
the AIN-76A diet; its composition has been reported previously
(Soria et al. 1996
). Both diets were isocaloric (15.28
kJ/g) and rats had free access to food and tap water.
Half of the rats (initial weight 160–170 g) from each group were mated with males of the same strain after 5 d of consuming the diets; rats initially weighing 140–150 g were mated after 45 or 90 d of consuming the diets. The day spermatozoids appeared in vaginal smears was considered d 0 of gestation. Rats were housed in collective cages (n = 4/cage). Daily food intake was not measured directly and was estimated only roughly because a considerable loss of food was detected. However, there were no apparent differences in food intake between rats fed SRD and CD (data not shown).
Pregnant and virgin rats were always studied in parallel. On different days of the experiment, blood was collected from the tip of the tail into heparinized receptacles. On d 25, 65 or 110 of feeding, the SRD or the CD, which always corresponded to d 20 of pregnancy in the case of pregnant rats, rats were decapitated and trunk blood was collected into ice-chilled tubes containing 1g/L Na2-EDTA. The two uterine horns were dissected immediately to obtain the whole conceptus and fetal weights. Livers were quickly removed and placed into liquid nitrogen before freezing at -80°C until analysis.
Analytical methods.
Plasma was separated by centrifugation at 1500 x g for 15 min at 4°C. Plasma samples from tail blood were kept frozen until processed, but plasma from trunk blood was subjected immediately to sequential ultracentrifugation in a Beckman TL-100 ultracentrifuge (Beckman Instruments España, Madrid, Spain) with a Beckman TLA 100.2 rotor. VLDL were separated at 224,000 x g for 3 h at d = 1.006 kg/L. Supernatants were recovered by tube slicing; after appropriate dilution, triglycerides were determined by a whole enzymatic method with colorimetric determination, using a commercial kit (#B-7648, Meranini Diagnostic, Florence, Italy). Triglyceride concentration was also determined in plasma using the same commercial kit.
Portions of frozen liver were extracted with chloroform/methanol (2:1)
(Folch et al. 1957
). Triglycerides were quantified after
image analysis and separation by one-dimensional TLC (Ruiz and Ochoa 1997
) using the G5–700 BIOIMAGE TLC scanner of
Bio-Rad (Hercules, CA). Spots were quantified as integrated optical
densities (IOD) against an internal standard of cholesteryl formate,
which had been included in every application. Calibration curves were
constructed by plotting the IOD of triglyceride standards, corrected by
the IOD of cholesteryl formiate, vs. the amount of lipid loaded, and
were drawn from second-order least-square regression equations.
Statistics.
Data are expressed as means ± SEM. Data were log transformed because it was necessary to achieve equal variance among means. Statistical analysis of data was performed by one-way ANOVA followed by Tukey’s test to establish differences among the four groups in rats treated for 25, 65 or 110 d. Two-way ANOVA was performed to test the main and interactive effects of diet and pregnancy on plasma triglycerides. Three-way ANOVA was also performed to test the main and interactive effects of diet, pregnancy and time of treatment, at the end of each experiment. Differences between two groups were analyzed by the Student’s t test. All statistical analyses were performed using a computer software package (Systat Version 5.03, Wilkinson, Evanston, Il).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
). However, at 110 d of SRD intake, virgin rats had the same body
weight as those fed the CD, whereas pregnant rats had a higher body
weight than those fed the CD. This difference corresponded mainly with
the net maternal weight because fetal body weight did not differ
between pregnant rats fed either the CD or SRD (Table 1)
; however,
maternal body weight, free of conceptus, in rats fed the SRD for
110 d was significantly higher (447 ± 6 g) than in
those fed the CD (381 ± 19 g, P < 0.01).
Feeding the SRD greatly affected liver weight, which was significantly
higher in virgin rats fed this diet for 65 or 110 d than in those
fed the CD, whereas pregnant rats fed CD always had a heavier liver
than virgin rats fed the CD. Feeding the SRD for 25 or 65 d did
not further modify this variable. Liver was heavier, however, in
pregnant rats fed the SRD for 110 d than in those fed the CD for
the same time period (Table 1)
. A three-way ANOVA was performed to
investigate whether the effects of diet, time or pregnancy on final
body and liver weight were interactive; the analysis showed that their
respective main effects on either variable were significant, except for
that of diet on final body weight (Table 1)
.
|
). Between d 15 and 25 of the experiment, rats fed the SRD showed a
further increase in plasma triglycerides, which was similar in virgin
and pregnant rats. In rats fed the CD, however, this increase was seen
only in pregnant rats (Fig. 1)
. Thus, at d 25 of feeding the diets,
which corresponded to d 20 of pregnancy, plasma triglycerides did not
differ in virgin rats fed the SRD and pregnant rats fed either the SRD
or CD; concentrations were always higher than those found in virgin
rats fed the CD, because the interaction of diet and pregnancy was
significant (see Fig. 1
legend).
|
), as shown by a progressive rise that lasted up to d 35, followed by a
decline to d 45; at that point, concentrations did not differ from
those of virgin rats fed CD. This was followed by a new rise up to the
d 65. When rats were mated at d 45 of treatment, pregnant rats fed the
CD developed hypertriglyceridemia compared with virgin rats fed the
same diet, and this change was similar to that seen in pregnant or
virgin rats consuming the SRD during the same period (Fig. 2)
. In fact,
at d 65 of consumption of the SRD, plasma triglyceride levels did not
differ significantly between virgin rats fed the SRD and pregnant rats
fed either the SRD or CD, and values in these three groups were higher
than those in virgin rats fed the CD (Fig. 2)
. Although the effect of
diet or pregnancy appeared significant, this was not the case when the
interactions of the two factors were considered (see Fig. 2
legend).
|
). Pregnancy in rats fed the CD led to the expected increase in plasma
triglycerides, whereas rats mated at d 90 of consuming the SRD showed a
decline in plasma triglycerides at d 10 of pregnancy (d 100 of
consuming the SRD). This was followed by a later rise, similar to the
differences seen at the same time points in virgin rats fed the SRD
(Fig. 3)
. Plasma triglyceride levels at 110 experimental days were not
different in virgin and 20 d pregnant rats fed the SRD, although
values in the latter group were higher than those in pregnant rats fed
the CD; values in both groups were higher than those in virgin rats fed
the CD (Fig. 3)
. In this experiment, the effect of diet was
significant, whereas this was not the case for the effect of pregnancy
nor for the diet x pregnancy interaction (see Fig. 3
legend).
|
). The ANOVA showed that the main effects of diet and pregnancy on
plasma triglycerides were significant, whereas time interaction became
significant only when dietary treatment was taken into account (Table 2)
.
|
). Pregnant rats fed the CD had plasma VLDL-triglycerides that were
always higher than those of virgin rats fed the same diet,
independently of the time of treatment (Fig. 4)
. However, unlike what
occurred in virgin rats, and with the exception of pregnant rats fed
the SRD for 110 d in which VLDL-triglycerides were higher than
in those fed the CD for the same time, no significant difference was
found in this variable between pregnant rats fed the SRD and CD for 25
or 65 d, and these concentrations were similar to those in virgin
rats fed the SRD for the same times (Fig. 4)
. Although both diet and
pregnancy and these two factors together significantly enhanced plasma
VLDL-triglycerides, the time factor was not reach significant, nor
was the interaction of time, diet and pregnancy (see Fig. 4
legend).
|
). In pregnant rats fed the CD, liver triglyceride concentration was not
different from that of virgin rats fed the same diet. Pregnant rats fed
SRD for 25 or 65 d had liver triglycerides that did not differ
from those fed CD; levels were even lower than those in virgin rats fed
the SRD for the same period of time (Fig. 5)
. However, this was not the
case when rats were studied after 110 d of consuming the SRD; in
that case, liver triglyceride concentration in pregnant rats was higher
than that in other pregnant rats and not significantly different from
virgin rats fed the SRD for 110 d (Fig. 5)
. The three-way
ANOVA of total liver triglycerides showed that there was a significant
interaction between diet and time, although this was not the case when
pregnancy was considered (legend for Fig. 5
).
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
) showed that the proportional hypertriglyceridemic
effect of feeding a SRD for 25 d is similar in virgin and pregnant
rats, and Oliveros et al. (1995)
showed that 19 d
of gestation and feeding a SRD in rats does not modify plasma
triglyceride levels compared with those seen in pregnant rats fed an
isocaloric dextrin diet for the same period of time. Our rats were
killed at a time of treatment, which coincided with the highest
hypertriglyceridemia response to SRD, i.e., 25, 65 and 110 d,
showing that such change corresponded mainly to an enhancement in
plasma VLDL-triglycerides.
The development of hypertriglyceridemia during the induction period of
feeding a SRD (2–5 wk) in male rats appeared to be the combined effect
of increased liver VLDL secretion and decreased clearance in the
presence of insulin resistance (Bernal et al. 1989
,
Gutman et al. 1987
). These changes coincided with those
taking place during pregnancy under normal conditions
(Martín et al. 1986
, Soria et al. 1996
). Because present findings showed that
hypertriglyceridemia has already developed after 5 d of feeding
SRD in nonpregnant rats, it is possible that liver VLDL secretion
capability was stimulated, whereas extrahepatic clearance was already
decreased in nonpregnant rats after this short time of feeding the SRD,
leaving no possibility of additional changes when pregnancy was
initiated. Liver triglyceride secretion rate would also depend on
triglyceride availability, and it seems that due to the enhanced
ability to secrete newly formed triglycerides in pregnant rats fed the
SRD for 25 d (Soria et al. 1996
), the liver does
not accumulate triglycerides as in virgin rats. This would limit the
possibility for an additional increment in liver triglyceride secretion
when rats fed the SRD are studied during pregnancy, thus avoiding an
additional increase in plasma triglyceride levels in pregnant rats fed
the SRD over those in rats fed the CD.
Consistent with previous studies conducted in male rats (Gutman et al. 1987
, Schonfeld and Pfleger 1971
), we
found a spontaneous normalization of plasma triglyceride levels in the
medium-term treatment with the SRD in female rats (40–50 d), which
was followed by a recurrent period that was not modified when rats were
subjected to pregnancy and studied at d 65 of consuming the same diet.
This recurrent period also appears with a glucose intolerance and
insulin resistance condition in nonpregnant rats (Gutman et al. 1987
); here again, the metabolic conditions seem to mimic those
normally found in pregnancy. Thus, it is not surprising that the
hypertriglyceridemic responsiveness of pregnancy in control rats is
similar to that seen in nonpregnant rats fed the SRD for this period of
time; nevertheless, one would expect that these changes would be
synergistically enhanced when the two conditions coincide. However, it
was found here that not only does pregnancy not enhance the
hypertriglyceridemic effect of the SRD but that pregnant rats fed the
SRD for either 25 or 65 d had a lower liver triglyceride
concentration than virgin rats. This difference is likely a consequence
of the greater capability of the liver of pregnant rats to secrete
triglycerides, as discussed above. In fact, this hypothesis agrees with
the findings of previous reports showing unchanged or even decreased
liver triglyceride concentrations in control rats during late pregnancy
despite hypertriglyceridemia (Herrera et al. 1969 and 1988
, Montes et al. 1978
).
The difference in liver triglyceride concentration between pregnant and
nonpregnant rats disappeared, however, when rats were studied at d 110
of consuming the SRD; at that time point, liver triglycerides had
accumulated in pregnant as in virgin rats, and plasma VLDL
triglycerides in SRD-fed rats in late pregnancy reached a higher
level than in pregnant rats fed the CD. At this time, the net body
weight increase of pregnant rats (free of conceptus) fed the SRD is
greater than that in any other condition studied. Because we know that
the increase in net maternal body weight during pregnancy corresponds
mainly to fat (Herrera et al. 1988
,
López-Luna et al. 1986
), such a change indicates
that those rats had highly enhanced fat depots. Significant increases
in body weight gain and food intake were seen previously in male rats
fed the SRD for 30 wk, although not for shorter time periods
(Lombardo et al. 1996
). Because pregnancy itself causes
hyperphagia, the increase in body weight found in our pregnant rats fed
the SRD for 110 d may have been the result of an enhanced intake
of sucrose; thus, they reached the threshold for fat accumulation
earlier than nonpregnant rats fed the same diet.
The increase in plasma triglycerides in pregnant rats fed the SRD for
110 d to the level found in nonpregnant rats would indicate that
liver triglyceride export capability can become saturated. A saturation
of triglyceride output capability was reported previously in perfused
livers or cultured hepatocytes of nonpregnant rats after consumption of
the SRD for short (3 d to 3 wk) or long (15 wk) periods (Bernal et al. 1995
, Boogaerts et al. 1984
,
Yamamoto et al. 1987
), and any further uptake or
synthesis of triglycerides would result in increased cellular storage.
Thus, because we found that liver triglyceride accumulation occurred
only in pregnant rats fed the SRD for 110 d but not for shorter
period of times, whereas it was already present in nonpregnant rats at
25 d, it appears that the high capability of maternal liver to
secrete triglycerides during pregnancy protects her from developing a
fatty liver when fed a SRD for short periods of time.
In agreement with previous reports carried out for only 19 d
(Oliveros et al. 1995
), feeding a SRD for up to 110 d did not affect pregnancy outcome in the present study. This finding
contrasts, however, with the decreased fetal weight reported previously
in pregnant rats fed SRD for 25 d (Soria et al. 1996
). The reason for this different response is unknown, but
it could reside in the strain because Wistar rats were used in that
study, whereas Sprague-Dawley rats were used here. More experiments
are required, however, to determine the precise reason(s) for this
different response, which may well be secondary to differences in the
sensitivity of the response to sucrose in other metabolic sites,
including maternal insulin resistance. In any case, these findings show
that the conditions of exaggerated maternal hypertriglyceridemia and
liver triglyceride accumulation that are seen in pregnant rats fed the
SRD for 110 d do not necessarily impair fetal growth; such
protection could well be the result of the impermeability of the
placenta for maternal circulating triglycerides (Herrera et al. 1998
).
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
3 Abbreviations used: CD, control diet; IOD, integrated optical density; SRD, sucrose-rich diet.
Manuscript received May 30, 2000. Initial review completed July 14, 2000. Revision accepted August 22, 2000.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
1. Alvarez J. J., Montelongo A., Iglesias A., Lasunción M. A., Herrera E. Longitudinal study on lipoprotein profile, high density lipoprotein subclass, and postheparin lipases during gestation in women. J. Lipid Res. 1996;37:299-308[Abstract]
2. Antar M. A., Litle J. A., Lucas C., Buckley G. C., Csima A. Interrelationship between the kinds of dietary carbohydrates and fat in hyperlipoproteinemic patients. Part 3. Synergistic effect of sucrose and animal fat on serum lipids. Atherosclerosis 1970;11:191-201[Medline]
3. Bernal C., Basilico M. Z., Gutman R., Lombardo Y. B. Secretion and removal rates of very low density lipoprotein triglycerides at the three metabolic periods of hypertriglyceridemia induced by a sucrose rich diet. Nutr. Rep. Int. 1989;40:71-83
4. Bernal C., Gutman R., Lombardo Y. B. The duration of feeding on a sucrose rich diet determines variable in vitro effects of insulin and fructose in rat liver triglyceride metabolism. J. Nutr. Biochem. 1995;:
5.
Boogaerts J., Malone-McNeal M., Archambault-Schexnayder J., Davis R. A. Dietary carbohydrate induces lipogenesis and very low density lipoprotein synthesis. Am. J. Physiol. 1984;246:E77-E83
6.
Cohen J. C., Schall R. Reassessing the effects of simple carbohydrates on the serum triglyceride responses to fat meals. Am. J. Clin. Nutr. 1988;48:1031-1034
7. Folch J., Lees M., Sloane-Stanley G. H. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 1957;22:24-36
8. Freinkel N. Banting Lecture 1980. Of pregnancy and progeny. Diabetes 1980;29:1023-1035[Abstract]
9.
Grant K. I., Marais M. P., Dhansay M. A. Sucrose in a lipid-rich meal amplifies the postprandial excursion of serum and lipoprotein triglyceride and cholesterol concentrations by decreasing triglyceride clearance. Am. J. Clin. Nutr. 1994;59:853-860
10. Gutman R. A., Basilico M. Z., Bernal C. A., Chicco A., Lombardo Y. B. Long-term hypertriglyceridemia and glucose intolerance in rats fed chronically an isocaloric sucrose-rich diet. Metabolism 1987;36:1013-1020[Medline]
11. Herrera E., Bonet B., Lasunción M. A. Maternal-fetal transfer of lipid metabolites. Polin R.A. Fox W. W. eds. Fetal and Neonatal Physiology 2nd ed. 1998:447-458 W. B. Saunders Philadelphia, PA.
12. Herrera E., Knopp R. H., Freinkel N. Carbohydrate metabolism in pregnancy VI. Plasma fuels, insulin, liver composition, gluconeogenesis and nitrogen metabolism during gestation in the fed and fasted rat. J. Clin. Investig. 1969;48:2260-2272
13. Herrera E., Lasunción M. A., Gomez Coronado D., Aranda P., Lopez Luna P., Maier I. Role of lipoprotein lipase activity on lipoprotein metabolism and the fate of circulating triglycerides in pregnancy. Am. J. Obstet. Gynecol. 1988;158:1575-1583[Medline]
14. Jen K.-L.C., Rochon C., Zhong S., Whitcomb L. Fructose and sucrose feeding during pregnancy and lactation in rats changes maternal and pup fuel metabolism. J. Nutr. 1991;121:1999-2005
15. Knopp R. H., Ruder H. J., Herrera E., Freinkel N. Carbohydrate metabolism in pregnancy VII. Insulin tolerance during late pregnancy in the fed and fasted rat. Acta Endocrinol. (Copenhagen) 1970;65:352-360
16. Lombardo Y. B., Drago S., Chicco A., Fainstein-Day P., Gutman R., Gagliardino J. J., Gomez Dumm C. L. Long-term administration of a sucrose-rich diet to normal rats: relationship between metabolic and hormonal profiles and morphological changes in the endocrine pancreas. Metabolism 1996;45:1527-1532[Medline]
17. López-Luna P., Muñoz T., Herrera E. Body fat in pregnant rats at mid- and late-gestation. Life Sci 1986;39:1389-1393[Medline]
18. MacDonald I. Influence of fructose and glucose on serum lipid levels in men and pre- and postmenopausal women. Am. J. Clin. Nutr. 1966;18:369-372[Abstract]
19. Martín A., Zorzano A., Caruncho I., Herrera E. Glucose tolerance tests and "in vivo" response to intravenous insulin in the unanaesthesized late pregnant rat and their consequences to the fetus. Diabetes Metab. 1986;12:302-307
20.
Martin-Hidalgo A., Holm C., Belfrage P., Schotz M. C., Herrera E. Lipoprotein lipase and hormone-sensitive lipase activity and mRNA in rat adipose tissue during pregnancy. Am. J. Physiol. 1994;266:E930-E935
21. Montelongo A., Lasunción M. A., Pallardo L. F., Herrera E. Longitudinal study of plasma lipoproteins and hormones during pregnancy in normal and diabetic women. Diabetes 1992;41:1651-1659[Abstract]
22. Montes A., Humphrey J., Knopp R. H., Childs M. T. Lipid metabolism in pregnancy. VI. Lipoprotein composition and hepatic lipids in the fed pregnant rat. Endocrinology 1978;103:1031-1038[Medline]
23. Nikkila E. A., Pelkonen R. Enhancement of alimentary hypertriglyceridemia by fructose and glycerol in man. Proc. Soc. Exp. Biol. Med. 1966;123:91-94[Medline]
24. Oliveros L., Giménez I., Giménez M. S. Effect of sucrose feeding during pregnancy on rat maternal and fetal liver lipid and glycogen metabolism. Biosci. Biotechnol. Biochem. 1995;59:412-416[Medline]
25. Ornoy A., Cohen A. M. Teratogenic effects of sucrose diet in diabetic and nondiabetic rats. Isr. J. Med. Sci. 1980;16:789-791[Medline]
26. Ramirez I., Llobera M., Herrera E. Circulating triacylglycerols, lipoproteins, and tissue lipoprotein lipase activities in rat mothers and offspring during the perinatal period: effect of postmaturity. Metabolism 1983;32:333-341[Medline]
27. Ruiz J. I., Ochoa B. Quantification in the subnanomolar range of phospholipids and neutral lipids by monodimension thin-layer chromatography and image analysis. J. Lipid Res. 1997;38:1482-1489[Abstract]
28. Schonfeld G., Pfleger B. Utilization of exogenous free fatty acids for the production of very low density lipoprotein triglyceride by livers of carbohydrate-fed rats. J. Lipid Res. 1971;12:614-621[Abstract]
29. Sleder J., Chen Y.-D.I., Cully M. D., Reaven G. M. Hyperinsulinemia in fructose-induced hypertriglyceridemia in the rat. Metabolism 1980;29:970-973[Medline]
30. Soria A., Chicco A., Mocchiutti N., Gutman R. A., Lombardo Y. B., Martin-Hidalgo A., Herrera E. A sucrose-rich diet affects triglyceride metabolism differently in pregnant and nonpregnant rats and has negative effects on fetal growth. J. Nutr. 1996;126:2481-2486
31.
Swanson J. E., Laine D. C., Thomas W., Bantle J. P. Metabolic effects of dietary fructose in healthy subjects. Am. J. Clin. Nutr. 1992;55:851-856
32. Wasfi I., Weinstein I., Heimberg M. Increased formation of triglyceride from oleate in perfused livers from pregnant rats. Endocrinology 1980;107:584-596[Medline]
33. Yamamoto M., Yamamoto I., Tanaka Y., Ontko J. A. Fatty acid metabolism and lipid secretion by perfused livers from rats fed laboratory stock and sucrose-rich diets. J. Lipid Res. 1987;28:1156-1165[Abstract]
34. Zavaroni I., Chen Y.D.I., Reaven G. M. Studies of the mechanisms of fructose-induce hypertriglyceridemia in the rat. Metabolism 1982;31:1077-1083[Medline]
35. Zavaroni I., Sander S., Scott S., Reaven G. M. Effect of fructose feeding on insulin secretion and insulin action in the rat. Metabolism 1980;29:970-973
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
