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Maternal olive oil intake enhances lipid metabolism and lipase activities in offspring of cafeteria diet-induced obese rats

Abstract

It has long been established that maternal nutritional condition and fatty acid intake during pregnancy and/or lactation may influence the modifications in the individual risk for developing metabolic diseases throughout life, but little is known about the possible role of maternal nutrition before conception. The aim of this study was to investigate the effect of maternal supplementation with olive oil on offspring lipid metabolism under obesogenic conditions. Female Wistar rats were fed control or cafeteria diet which were either supplemented or not supplemented with olive oil (5%) for 2 months before and during gestation. Pregnant rats and their offspring were also fed on similar diet. After overnight fasting, offspring were sacrificed at 1 and 3 month of life. Cafeteria diet led to higher body weight, hyperglycemia and hyperlipidemia, LDL cholesterol, serum Lecithin–cholesterol acyltransferase activity and tissues lipoprotein lipase and hormone-sensitive lipase in offspring. In contrast, adult obese offspring had a lower HDL cholesterol. Olive oil rich-CAF diet decreased plasma lipids, increased HDL cholesterol and up-regulated lipolytic enzyme activities at weaning until adulthood. These data suggest that maternal olive oil may an effective strategy to improving metabolic alterations related to cafeteria diet in offspring.
Vol.:(0123456789)
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Oriental Pharmacy and Experimental Medicine
https://doi.org/10.1007/s13596-018-0329-7
RESEARCH ARTICLE
Maternal olive oil intake enhances lipid metabolism andlipase
activities inospring ofcafeteria diet‑induced obese rats
SalimaDerouiche1· FatimaZohraBabaAhmed1· HadaMerzouk1· SamiraBouanane1· SidAhmedMerzouk2
Received: 20 July 2017 / Accepted: 17 July 2018
© Institute of Korean Medicine, Kyung Hee University and Springer Science+Business Media B.V., part of Springer Nature 2018
Abstract
It has long been established that maternal nutritional condition and fatty acid intake during pregnancy and/or lactation may
influence the modifications in the individual risk for developing metabolic diseases throughout life, but little is known about
the possible role of maternal nutrition before conception. The aim of this study was to investigate the effect of maternal sup-
plementation with olive oil on offspring lipid metabolism under obesogenic conditions. Female Wistar rats were fed control
or cafeteria diet which were either supplemented or not supplemented with olive oil (5%) for 2months before and during
gestation. Pregnant rats and their offspring were also fed on similar diet. After overnight fasting, offspring were sacrificed
at 1 and 3month of life. Cafeteria diet led to higher body weight, hyperglycemia and hyperlipidemia, LDL cholesterol,
serum Lecithin–cholesterol acyltransferase activity and tissues lipoprotein lipase and hormone-sensitive lipase in offspring.
In contrast, adult obese offspring had a lower HDL cholesterol. Olive oil rich-CAF diet decreased plasma lipids, increased
HDL cholesterol and up-regulated lipolytic enzyme activities at weaning until adulthood. These data suggest that maternal
olive oil may an effective strategy to improving metabolic alterations related to cafeteria diet in offspring.
Keywords Maternal olive oil· Cafeteria diet· Lipid metabolism· Lipoprotein lipase· Offspring
Abbreviations
C Standard chow
CAF Cafeteria diet
HDL-C High density lipoprotein cholesterol
HSL Hormone sensitive lipase
LCAT Lecithin cholesterol acyl transferase
LDL-C Low density lipoprotein cholesterol
LPL Lipoprotein lipase
MUFA Monounsaturated fatty acids
PPARα Peroxisome proliferator-activated receptor
alpha
PUFA Polyunsaturated fatty acids
SREBP-1 Sterol regulatory element-binding protein-1
TC Total cholesterol
TG Triglycerides
VLDL-C Very low-density lipoprotein cholesterol
Introduction
Maternal nutrition has historically been a key determinant
for offspring health, and gestation is the critical time window
that can affect the growth and development of offspring.
Inadequate nutritional and environmental factors may
modify the fetal metabolic programming which could be
reflected as deleterious consequences in adulthood, such as
predisposition to development of several diseases including
cardiovascular and metabolic diseases (Godfrey and Barker
2001; Gillman 2002).
Several studies have reported that obesity is associated
with is associated with many deleterious changes of lipid
metabolism: increased low-density lipoprotein cholesterol
(LDL-C), very low-density lipoprotein cholesterol (VLDL-
C), triglycerides (TG) and reduced high density lipoprotein
cholesterol (HDL-C) concentrations (Manjunath etal. 2013).
However, serum lipids are not sufficient indicators of lipo-
protein metabolism. As previously stated, lipoprotein lipid
partitioning is largely dependent on the enzymatic action of
* Fatima Zohra Baba Ahmed
fatimazohra_7@yahoo.fr
1 Laboratory ofPhysiology, Physiopathology
andBiochemistry ofNutrition, Department ofBiology,
Faculty ofSNVSTU, University Abou-Bekr Belkaïd
Tlemcen, 13000Tlemcen, Algeria
2 Department ofTechnical Sciences, Faculty ofEngineering,
University Abou-Bekr Belkaïd Tlemcen, 13000Tlemcen,
Algeria
S.Derouiche et al.
1 3
lipoprotein lipase (LPL) [EC 3.1.1.34], and free fatty acids
mobilization is largely dependent on the enzymatic action of
hormone-sensitive lipase (HSL) [EC 3.1.1.79]. LCAT (EC
2.3.1.43) is also critical for the maintenance of plasma lipo-
proteins and involved in the transesterification of cholesterol,
the maturation of HDL and the efflux of cholesterol from
cells membranes into HDL (Rousset etal. 2009).
Human epidemiological studies as well as a variety of
animal ones revealed that prenatal and early postnatal nutri-
tional statuses may influence adult susceptibility to impaired
glucose tolerance, cardiovascular disease, and obesity (Leon
1998; Vogt etal. 2014). Several findings indicate that the
quantity and quality of fatty acids consumed by mothers dur-
ing pregnancy and lactation can induce permanent changes
in lipid metabolism in their offspring (Mennitti etal. 2015).
There is, therefore, significant interest in understanding the
type of maternal dietary and lifestyle interventions, which
may lead to optimal outcomes for mother and child.
Olive oil is considered a healthy product because of its
constituents, which include oleic acid and other unsaturated
fatty acids; in addition to traces of squalence and sterols.
There is a considerable data demonstrating that the con-
sumption of olive oil is beneficial to cardiovascular health;
specifically on cholesterol regulation in male Wistar rats
(Mangas-Cruz etal. 2001) and on lipid metabolism in the
offspring of mild diabetic rats (Capobianco etal. 2015).
The current study was designed to explore the effect of
maternal supplementation with olive oil at 5% on serum
glucose, cholesterol, triglycerides and serum LCAT activ-
ity, lipoprotein cholesterol levels and tissues lipase activities
in offspring rat exposed to a cafeteria diet during and post
intrauterine life.
Materials andmethods
Olive oil sample
Olive oil used in this experiment was the table olive oil
was obtained from INRA (INRA, Algeria). The fatty acids
composition of olive oil was determined by GPC and the
vitamin E by HPLC laboratory UPRES lipids, University
of Burgundy, France. Its chemical composition is provided
in Table1.
Animals andexperimental protocol
Healthy Albino Wistar rats (1months aged and 90–100g
weighed), were obtained from Animal Resource Cen-
tre (Algeria) and housed under controlled light and tem-
perature conditions (12h light/dark cycle; 20 ± 2°C).
Forty female rats were randomly assigned into four feed-
ing groups for 60days prior mating. The group 1 (control,
C; n = 10 females) received the standard laboratory chow
(ONAB, Algeria). Group 2 (CO, n = 10) was fed a control
diet enriched with olive oil at 5%. Group 3 (CAF, n = 10)
was fed with a cafeteria diet composed of dough, cheese,
bacon, potato chips, biscuits and chocolate (in a proportion
of 2:2:2:1:1:1, by weight) mixed with standard chow (w/w).
Group 4 (CAFO, n = 10) was fed a cafeteria diet enriched
with olive oil at 5%. The composition of four diets is given
in Table2.
At the end of this period, females were mated, and each
pregnant female was housed in an individual cage with free
access to water and continued with similar diet before mat-
ing. A total of 320 pups from all groups of dams were deliv-
ered spontaneously and weighed within 12h. The postnatal
Table 1 Composition in fatty acids and vitamins of the olive oil used
Constituent in % Olive oil
Palmitic acid c16:0 11.8
Stearic acid c18:0 2.2
Oleic acid c1:1n-9 72.6
Linoleic acid c18:2n-6 7.9
Eicosapentaenoic acid c20:5n-3 /
Docosahexaenoic acid c22:6n-3 /
Vitamin E 0.5
Table 2 Composition of experimental diets
The control and cafeteria diets for CO and CAFO were given in pow-
der form, and were supplemented with purified olive oil at 5%. α: sat-
urated fatty acids. β: monounsaturated fatty acid. Fatty acid composi-
tion was analyzed by gas liquid chromatography, INSERM UMR 866,
“Lipids Nutrition Cancer”, University of Burgundy, France
SFA, saturated fatty acids
Control (C) Control
olive
(CO)
Caf-
eteria
(CAF)
Caf-
eteria olive
(CAFO)
Energy sources (% energy)
Protein 20 20 20 20
Carbohydrate 60 60 24 24
Fat 10 10 50 50
Sunflower oil 10 5 10 5
Olive oil / 5 / 5
Vitamin (mg/100g) 5 5 1 1
Energy
(Kcal/100g)
386 386 523 523
(% fatty acids)
SFAα29 23 42 39.5
C18:1n-9β21 22 30 33
C18:2n-6 46 38 27 26.5
C18:3n-3 3 16 1 1
C20:4n-6 1 1 0 0
Maternal olive oil intake enhances lipid metabolism andlipase activities inoffspring of…
1 3
litter size was adjusted at 8pups/dam to maintain a simi-
lar postnatal nutritional intake during the suckling period.
Weaning occurred on day 30 of lactation.
After weaning, the offspring continue to follow the same
diet as their mothers. Male and females rats were housed
separately and were followed into adulthood (12weeks).
Four groups were then formed (C; n = 8, CO; n = 8, CAF,
n = 8, CAFO; n = 8). Fresh food was given daily and body
weights were recorded.
Blood andtissue samples
After overnight fasting, at weaning (day 30) andat adult-
hood (day 90), rats from each group were sacrificed under
anesthesia by intraperitoneal injection of sodium pentobar-
bital (60mg/kg of body weight). The blood was drawn from
the abdominal aorta, and plasma and serum were used for
glucose and lipid determinations. The liver, abdominal adi-
pose tissue and muscle were removed, washed with ice-cold
saline, quickly blotted and weighed. An aliquot of tissues
was homogenized in 0.9% (w/v) NaCl containing heparin
(Sigma, St. Louis, MO, USA) and used for lipoprotein lipase
(LPL) activity.
Another aliquot of adipose tissue portion was homog-
enized in ice-cold buffer containing 0.25M sucrose, 1mM
dithiothreitol and 1mM EDTA, pH 7.4, supplemented with
20mg/mL leupeptin, 2mg/mL antipain and 1mg/mL pep-
statin and was used for the adipose hormone-sensitive lipase
(HSL) assay.
Chemical analysis
Plasma glucose and serum cholesterol were measured using
colorimetric enzymatic kits (Sigma, St. Louis, MO).
Serum lipoprotein (LDL, d: 1.063; HDL, d: 1.21gmL)
were separated by sequential ultracentrifugation in a Beck-
man ultracentrifuge (Model L5-65, 65 Tirotor), using
sodium bromide for density adjustment. HDL-cholesterol,
LDL-cholesterol and VLDL-cholesterol concentrations were
also measured by enzymatic kits (Sigma).
LCAT (EC 2.3.1.43) activity was assayed by conversion
of unesterified [3 H] cholesterol to esterified [3 H] cho-
lesterol, according to the method of Glomset and Wright
(1964), as previously described (Merzouk etal. 1997).
Serum LCAT activity was expressed as nmol of esterified
cholesterol/h/mL of serum.
Lipase activity (LPL, EC 3.1.1.34; LHS, EC 3.1.1.79)
was measured by pH–stat by titrimetric measurement of fatty
acids released after hydrolysis of triglycerides of synthetic
substrate with NaOH 0.05M at pH 8 and at 25°C. Enzyme
activity was expressed in international units (IU). One unit
corresponds to the release of a micro-equivalent of fatty acid
per minute.
Statistical analysis
Results are expressed as mean ± standard deviation (SD).
Significant differences among the groups were analyzed by
ANOVA. Significant differences between control and control
olive oil rats and between cafeteria and cafeteria olive oil,
at each age, were assessed using a Student’s t test. The sig-
nificance level was set at P < 0.05. These calculations were
performed using STATISTICA version 4.1 (STATSOFT,
Tulsa, OK).
Results
Ospring body andtissue weights
Cafeteria diet consumption led to significantly higher body
weight among offspring at weaning and at adulthood as
compared with normal diets. However, supplementation
with olive oil (5%) to mother reduced body weight in obese
offspring at weaning and at adulthood. On the other hand,
liver and abdominal adipose tissue weights show a signifi-
cant increase in obese versus control offspring, which are
positively correlated to final body weight. Olive oil sup-
plementation induced a significant decrease in both liver
and adipose tissue weights in obese offspring at weaning
compared with obese group (Table3). At day 90, statistically
significant reduction of adipose tissue weight was observed
in CAFO group as was compared with CAF group, however,
the cafeteria diet, and olive oil had no effect on liver weight
at day 90.
No significant difference in muscle weight was observed
among offspring of the four groups at weaning and at
adulthood.
Ospring glycaemia andserum lipids
At day 30 and 90day, serum glucose and cholesterol,
concentrations were significantly increased in obese pups
compared with controls. However, olive oil supplementa-
tion reduced plasma glucose in offspring of CAFO group
at weaning and adulthood with no changes in CO group
compared with controls. Indeed, feeding olive oil reduced
serum cholesterol significantly in CAFO and CO offspring
at day 30 and day 90 compared with obese and control rats
respectively (Table4).
Ospring lipoproteins lipids concentrations
Both at weaning and at adulthood, a significant increase
was noted in VLDL-C and LDL-C in obese rats compared
with controls. Olive oil administration decrease significantly
VLDL-C and LDL-C levels in both obese and control rats.
S.Derouiche et al.
1 3
At weaning, no differences were observed in offspring
HDL-C concentrations among the four groups. At day 90,
the HDL-C concentrations increased significantly in off-
spring of CAFO and C group. As expected, the lowest
values of HDL-C were obtained in CAF group (Table4).
Ospring LCAT activity
A significant increase in serum LCAT activity was observed
in the offspring fed with cafeteria diet compared with con-
trols at day 30 and day 90. Maternal supplementation with
Table 3 Body and tissues
weight in the offspring
Values are presented as means ± standard deviations (SD)
Values with different superscript letters (a, b, c, d) are significantly different (ANOVA)
AT, adipose tissue; C, control diet; CO, control diet enriched with olive oil at 5%; CAF, cafeteria diet;
CAFO, cafeteria diet enriched with olive oil at 5%
$ P < 0.05, $$P < 0.01 and $$$P < 0.001 compared with cafeteria rats at each age
Control rats Cafeteria obese rats P (ANOVA)
CCO CAF CAFO
Day 30
Body weight (g) 57.04 ± 4.00c68.16 ± 4.62b78.5 ± 1.87a70.83 ± 3.60b$$ 0.0001
Liver weight (g) 4.79 ± 0.33c4.47 ± 0.36c7.28 ± 0.62a5.57 ± 0.65b$$ 0.0001
AT weight (g) 0.93 ± 0.21c0.73 ± 0.09c1.41 ± 0.05a1.28 ± 0.06b$$ 0.0001
Muscle weight (g) 0.42 ± 0.02 0.40 ± 0.04 0.41 ± 0.05 0.40 ± 0.04 0.801
Day 90
Body weight (g) 190.48 ± 2.36c196.5 ± 13.08c266.83 ± 6.49a261 ± 3.34b0.0001
Liver weight (g) 8.66 ± 0.87c8.75 ± 1.19c11.43 ± 0.61a10.65 ± 1.44b0.0001
AT weight (g) 1.56 ± 0.30d2.40 ± 0.45c4.60 ± 0.59a3.03 ± 0.36b$$$ 0.0001
Muscle weight (g) 0.68 ± 0.12 0.74 ± 0.04 0.77 ± 0.05 0.78 ± 0.09 0.024
Table 4 Effect of the different
diets on lipid parameters of the
offspring
Values are presented as means ± standard deviations (SD)
Values with different superscript letters (a, b, c, d) are significantly different (ANOVA)
VLDL-C, VLDL cholesterol; LDL-C, LDL cholesterol; HDL-C, HDL cholesterol; TC, total cholesterol;
C, control diet; CO, control diet enriched with olive oil at 5%; CAF, cafeteria diet; CAFO, cafeteria diet
enriched with olive oil at 5%
*P < 0.05, **P < 0.01 and ***P < 0.001 compared with control rats at each age
$ P < 0.05, $$P < 0.01 and $$$P < 0.001 compared with cafeteria rats at each age
Control rats Cafeteria obese rats P (ANOVA)
CCO CAF CAFO
Day 30
Glucose (mg/dL) 79.83 ± 7.13c90.45 ± 13.98b100.29 ± 4.61a81.36 ± 4.47c$$$ 0.0001
CT (mg/dL) 103.82 ± 7.20b95.6 ± 4.36c*150.23 ± 2.44a120.39 ± 14.1b$$$ 0.0001
VLDL-C (mg/dL) 19.34 ± 1.65c16.88 ± 1.47d*37.77 ± 1.70a20.54 ± 0.83b$$$ 0.0001
LDL-C (mg/dL) 30.47 ± 1.73c16.27 ± 2.09d*** 56.73 ± 2.77a44.83 ± 4.86b$$$ 0.0001
HDL-C (mg/dL) 57.55 ± 1.91 60.74 ± 4.82 58.09 ± 1.36 56.55 ± 1.85 0.0803
LCAT (nmol/mL/h) 14.01 ± 1.55d23.87 ± 1.81c43.35 ± 3.40a38.17 ± 1.96b$$ 0.0001
Day 90
Glucose (mg/dL) 87.2 ± 8.53c86.33 ± 8.18c140 ± 11.33a121 ± 17.43b$ 0.0001
CT (mg/dL) 121.42 ± 5.92c104.91 ± 10.7d** 160.53 ± 2.62a137.63 ± 18.3b$$$ 0.0001
VLDL-C (mg/dL) 23.01 ± 1.69c19.49 ± 1.56d** 50.50 ± 1.98a24.61 ± 1.92b$$$ 0.0001
LDL-C (mg/dL) 35.31 ± 2.34b20.10 ± 1.37c*** 53.79 ± 1.80a33.85 ± 2.87b$$$ 0.0001
HDL-C (mg/dL) 62.12 ± 1.99a53.35 ± 2.11c41.16 ± 2.23d58.42 ± 1.33a$$$ 0.0001
LCAT (nmol/mL/h) 18.55 ± 2.04d26.92 ± 4.33c47.77 ± 3.01a41.68 ± 1.97b$$ 0.0001
Maternal olive oil intake enhances lipid metabolism andlipase activities inoffspring of…
1 3
olive oil decrease significantly serum LCAT in obese rats but
not in control rats at day 30 and day 90 (Table4).
Ospring lipases activities
LPL activity was measured in liver, abdominal adipose tis-
sue and muscle. As shown in Fig.1, the LPL activity of
liver, abdominal adipose tissue and muscle was higher in
the offspring of CAF group than in those of C group; once
again, this variable decreased in the obese offspring sup-
plemented with olive oil at 5% (CAFO), both at weaning
and at adulthood (Fig.1). In contrast, olive oil had no effect
on LPL activity of liver, adipose tissue and muscle in con-
trol suckling offspring (CO) but it decreased significantly at
adulthood (90day).
At day 30 and day 90, adipose HSL activity was signifi-
cantly increased in obese offspring compared with controls.
This activity was enhanced significantly after olive oil sup-
plementation in obese offspring (CAFO) but it was not
affected in the CO group.
Discussion
Diet composition during pregnancy or lactation is known
to alter the risk of obesity in adulthood (Howie etal. 2009).
Therefore, diet quality may be improved through a change
in the amount and type of fat ingested without causing side
effects and offering lower costs in comparison the use of
drugs (Moreno and Mitjavila 2003). Olive oil is regarded as
especially enriched in monounsaturated fatty acids (MUFA)
and appears to have important functions in the modulation of
cardiovascular disease (Guasch-Ferré etal. 2014). The pre-
sent study was undertaken to ascertain the beneficial effects
of olive oil at 5% on obesity development in offspring at
weaning and at adulthood.
A cafeteria diet was used as an experimental model of
metabolic syndrome. Cafeteria diet selected in our study was
given to female rats 8weeks prior mating, during pregnancy,
lactation and to offspring. The offspring of these dams pre-
sented significant increases in body and organs (liver, adi-
pose tissue and muscle) weights, and they remained through-
out adulthood. Our findings are in general agreement with
a previous report (Benkalfat etal. 2011; Jacobs etal. 2014;
Masuyama and Hiramatsu 2014). Increases in body and
abdominal adipose tissue weights in the offspring of rats
fed cafeteria diet are the chief indicators for the gradual pro-
gress of obesity.
However, supplementation with olive oil had a signifi-
cant decrease in body weight (only at day 30) and adipose
and liver weight at 1 and 3weeks of age of obese offspring
(CAFO), which proved its antiobese action. In contrast,
Olive oil had no effect on muscle weight throughout life of
offspring. Increased body weight observed in offspring of
0
50
100
150
200
250
300
350
d 30 d 90
Liver LPL (nmol/min/g)
cc
a
$$
b
c***
d
a$$
b
0
50
100
150
200
250
300
350
400
d 30 d 90
Adipose LPL (nmol/min/g)
C
CO
CAF
CAFO
cc
a
$$
b
c***
d
a$$
b
0
20
40
60
80
100
d 30 d 90
Muscle LPL (nmol/min/g)
cc
a$
b
c*
d
a
$$$
b
0
10
20
30
40
50
60
70
d 30 d 90
Adipose HSL (nmol/min/g
)
cc
a$$
bcc
a$$$
b
Fig. 1 Liver, muscle and adipose tissue lipase activities in the off-
spring. Values are presented as means ± standard deviations (SD). C,
control diet; CO, control diet enriched with olive oil at 5%; CAF, caf-
eteria diet; CAFO, cafeteria diet enriched with olive oil at 5%. Values
with different superscript letters (a, b, c, d) are significantly different
(ANOVA). *P < 0.05, **P < 0.01 and ***P < 0.001 compared with
control rats at each age. $P < 0.05, $$P < 0.01 and $$$P < 0.001 com-
pared with cafeteria rats at each age
S.Derouiche et al.
1 3
CAFO group at adulthood possibly due to a long consump-
tion of cafeteria diet. Priego etal. showed that maternal olive
oil supplementation decreased body weight gain through an
increase in uncoupling protein-1 protein level in brown adi-
pose tissue of offspring at weaning. They proposed that oleic
acid prevents the development of obesity and steatosis by
stimulating thermogenic capacity (Priego etal. 2013).
In agreement with several previous studies (Dos Santos
Perez etal. 2015; Bouanane etal. 2010), results in our study
revealed that obese offspring of cafeteria-fed dams showed
a significant increase in plasma glucose, TC, LDL-C, and
VLDL-C at weaning and at adulthood. Hypercholester-
olemia is described as one of the main independent risk fac-
tors for atherosclerotic disease, and saturated fat, which was
abundant in the diet used in the present study, is the main
predictor of an increase in lipid and lipoprotein levels. These
findings were associated with a significant increase in serum
LCAT activity in offspring at day 30 and day 90. In diabetes
and the metabolic syndrome, increased LCAT activity was
noted, which was reflective of LCAT production (Benaicheta
etal. 2016; Merzouk etal. 2001). It has been demonstrated
that this elevation did not predict low incidence of cardiovas-
cular disease (Dullaart etal. 2010), because it might modify
the antioxidant and anti-inflammatory effects of HDL.
In this study, after 1month of life (day 30), which corre-
sponded to the suckling period, increased LCAT activity was
associated with higher LPL activity in obese than in control
rats. HDL-C concentrations in obese offspring became simi-
lar to those of their respective controls. These findings sug-
gest that an increased rate of lipoprotein synthesis combined
with an enhanced lipoprotein catabolism in obese offspring
might contribute to maintaining a normal lipoprotein profile
at day 30. A higher demand for lipid during the phase of
rapid growth could explain high lipoprotein turnover, know-
ing that most of the obese rat’s tissues were hypertrophic in
agreement with previous study (Merzouk etal. 2002).
At adulthood (day 90), the obese offspring again showed
an increase in LCAT activity associated with a low HDL-C
levels compared to control rats. The LCAT-mediated esteri-
fication of cholesterol is increased in obese subjects with
insulin resistance (Mooradian etal. 2008). The latter change
depletes HDL of its cholesterol and contributes to lowering
of HDL levels.
Increased LPL in liver, adipose tissue and muscle could
be due to high insulin levels in these obese rats at weaning
and at adulthood. The contribution of hyperinsulinaemia to
the maintenance of high adipose LPL activity in the obese
Zucker fa/fa rat is well known (Boivin and Deshaies 2000).
Regarding adipose hormone-sensitive lipase, its activity has
also been found increased in CAF group at day 30 and 90, as
previously shown in younger rats (Benkalfat etal. 2011). It
can be suggested that high adipose tissue HSL activity and
lipolysis may prevent worsening of the TAG accumulation
related to high LPL activity in adult obese rats. Several stud-
ies have shown that the lipolytic effect of catecholamines
is attenuated in obese subjects (Connacher etal. 1991;
Kaartinen etal. 1995; Reynisdottir etal. 1994), which may
be due to a defect in the lipolytic cascade that normally leads
to the activation of HSL.
On the other hand, Olive oil supplementation modulated
several lipid parameters in both control and obese offspring,
with beneficial effects including reduction in glycaemia and
in lipidemia, lower lipid accumulation, and modulation of
enzyme activities. According to recently studies (Mousavi
etal. 2017), olive oil supplemented to control diet, showed
a significant decrease (P < 0.05) in all the lipid parameters
while there was a significant (P < 0.05) increase in HDL
level. It was also seen that olive oil supplemented to caf-
eteria fed pups, showed a significant decrease in all the
lipid parameters (P < 0.05) with a significant rise in HDL
(P < 0.05) level as compared to cafeteria pups (CAF), and
remained throughout adulthood suggesting a lipid-lowering
effect of olive oil.
Epidemiological studies demonstrate that high levels of
HDL potentially contribute more toward the antiatherogenic
properties of this lipoprotein, including its capacity to inhibit
the oxidation of LDL and protect endothelial cells from
the cytotoxic effect of oxidized LDL (Assmann and Nofer
2003). Thus, the increase in HDL in the offspring of mothers
fed a diet rich in omega-9 suggests a protective effect from
atherosclerosis (De Oliveira Cipriano Torres etal. 2012).
Improvements in lipid profile in the offspring fed with
their mothers on the diet containing olive oil may be explains
on the basis that olive oil is a rich source of monounsatu-
rated fatty acids (MUSFA) that improves blood lipid profile.
Olive oil is excellent source of oleic acid. Previous studies
demonstrated that olive oils containing a large fraction of
MUSFAs and a substantial amount of polyunsaturated fatty
acids (PUSFAs) promote a better triacylglycerol clearance
from the blood. In additionally, a diet with olive oil is a good
source of monounsaturated fatty reduced serum TG, LDL-c
concentrations with respect to diets rich in SFAs.
However, the effects observed in the offspring supple-
mented with olive oil could be due not only to the MUFA
but also the fraction minor olive oil has compounds with
beneficial effects on the reduction of weight gain as is the
case of aromatic compounds (Hexanal and 2-Hexanal) that
by exercising their satiating action through stimulating the
production of serotonin (Schieberle etal. 2009–2012), could
decrease faster food intake in pups compared to controls.
Moreover olive oil also inhibits lipid and lipoprotein accu-
mulation by significantly modulating the enzymes of the lipid
metabolism. Our results have showed that olive oil decrease
LCAT activity in the serum in cafeteria and control olive oil-
fed rats and LPL activity in cafeteria olive oil-fed rats at day
30 and 90. These results are in accordance with other authors
Maternal olive oil intake enhances lipid metabolism andlipase activities inoffspring of…
1 3
(Arunima and Rajamohan 2012), who found that decreased
activity of both LCAT and LPL in olive oil fed rats may be one
possible mechanism for accumulation of lipids in olive oil fed
rats compared to rats fed virgin coconut oil.
In the present study, the Low LPL activity in olive oil fed
rats could be related to the suppression of hepatic expression
of sterol regulatory element-binding protein 1 (SREBP-1) and
lipogenic enzymes. Previous study demonstrates that substitu-
tion of dietary fat, particularly n-3 long-chain PUFAs, for car-
bohydrate can effectively mitigate up-regulation of SREBP-1c
and lipogenic enzymes in the hyperinsulinemic corpulent JCR:
LA-cp rat (Deng etal. 2004). It is possible that the reduced
expression of SREBP-1 and lipogenic enzymes observed in
corpulent rats fed the olive oil diet was attributable at least in
part to the PUFA content of that diet. This in turn could up-
regulate the expressions of fatty acid catabolic genes through
the activation of peroxisome proliferator-activated receptor
alpha (PPARα) in the liver and down-regulate the expressions
of lipid storage and lipogenic gene through the suppression
of SREBP-1c in the abdominal white adipose tissue (Hsu and
Huang 2006).
Olive oil supplementation Lower also HSL activity in
response to feeding olive oil consistent with previous works
(Liao etal. 2010), which could explain the lipid depletion in
this tissues in obese rats.
In conclusion, our results clearly demonstrate that olive oil
rich diets seemed to beneficially deplete white adipose tis-
sue accumulation by decreasing plasma lipid concentrations,
improve hepatic, adipose and muscle lipolytic enzyme activi-
ties involved in β-oxidation and displays remarkable health
benefits for the prevention of obesity and associated metabolic
disorders affected by early dietary olive oil in adult offspring.
Acknowledgements This work was supported by the French Foreign
Office (International Research Extension Grant TASSILI 08MDU723)
and by the Algerian Research Project (PNR, 2011).
Compliance with ethical standards
Ethical statement The study was conducted in accordance with the
national guidelines for the care and use of laboratory animals. All the
experimental protocols were approved by the Regional Ethical Com-
mittee.
Conflict of interest This manuscript described has not been published
before; not under consideration for publication anywhere else; and has
been approved by all co-authors.
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