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Consumption of Argan Oil Improves Anti-Oxidant
and Lipid Status in Hemodialysis Patients
Rachid Eljaoudi,
1
*
†
Driss Elkabbaj,
2†
Abdelali Bahadi,
2
Azeddine Ibrahimi,
3
Mohammed Benyahia
2
and Mourad Errasfa
4
1
Pharmacology and Toxicology Department, Faculty of Medicine and Pharmacy, University Mohammed V, 10000 Rabat, Morocco
2
Nephrology Department, Military Hospital Mohammed V, 10000 Rabat, Morocco
3
Medical Biotechnologie lab (MedBiotech), Faculty of Medicine and Pharmacy, University Mohammed V, 10000 Rabat, Morocco
4
Pharmacology Department, Faculty of Medicine and Pharmacy, University Sidi Mohamed Ben Abdellah, 30000 Fes, Morocco
Objective: Virgin Argan oil (VAO) is of interest in oxidative stress and lipid prof ile because of its fat composi-
tion and antioxidant compounds. We investigated the effect of VAO consumption on lipid profile and antioxi-
dant status in hemodialysis patients after a 4-week period of consumption. Methods: In a crossover, controlled
trial, 37 patients (18 men, 19 women) with end-stage renal disease on maintenance hemodialysis, were
randomly assigned to a 4-week VAO diet. Fasting plasma lipids, vitamin E and oxidized LDL (ox-LDL) were
analyzed. Malondialdehyde (MDA) was determined before and after hemodialysis session. Results: There
was no significant change in serum total cholesterol and ox-LDL. However, VAO consumption decreased the
levels of triglyceride (p = 0.03), total cholesterol (p = 0.02) and low-density lipoprotein (p =0.03) and increased
the levels of high-density lipoprotein (p =0.01). Plasma vitamin E contents significantly increased from baseline
only in VAO-group (p <0.001). Hemodialysis session increased MDA levels, but the increase in VAO group
was less than in control group. Conclusion: VAO consumption improved lipid profile and oxidative stress status
in hemodialysis patients. Copyright © 2015 John Wiley & Sons, Ltd.
Keywords: Argan oil; chronic renal failure; oxidative stress; lipid profile.
INTRODUCTION
Chronic renal failure (CRF), a serious health problem
all over the world, is characterized by a progressive de-
cline of kidney function. Patients with CRF have three
to five times higher risk of having cardiovascular event
compared to the general population. This risk in-
creases up to 20 times in hemodialysis (HD) patients.
This great increase in cardiovascular risk cannot be
explained entirely by traditional cardiovascular risk
factors. Many studies have demonstrated that CRF is
associated with oxidative stress which is proposed as a
non-traditional cardiovascular risk factor in these pa-
tients (Danielski et al., 2003; Ahmadpoor et al., 2009;
Andreucci et al., 2004).
Oxidative stress (OS) refers to excessive production
of reactive oxygen species (ROS) and inadequate
antioxidant protection. In CRF patients under HD
treatment, the formation of ROS is amplified (Mimic-
Oka et al., 1999; Ceballos-Picot et al., 1996) damaging
intracellular macromolecules, oxidizing lipids, carbohy-
drates, DNA or proteins (Köken et al., 2004). Numerous
biomarkers of OS were studied in hemodialyzed patients
such as antioxidant defense systems (erythrocyte
superoxide dismutase and glutathione peroxidase
activities), free radical scavengers (vitamin E and
β-carotene) and malondialdehyde (MDA) which is
generated in vivo via peroxidation of polyunsaturated
fatty acids. In hemodialyzed patients, most of the stud-
ies reported decreased levels of antioxidant defense
systems and free radical scavengers with a rise in
plasma MDA (Bonnefont-Rousselot et al., 1997). HD
session may also increase the level of MDA in serum
(Elkabbaj et al., 2012).
Virgin Argan oil (VAO) is produced from the fruits
of Argania spinosa, which is an endemic tree of
south-western Morocco. In some regions of Morocco,
this noble oil is intended for everyday therapeutic use
both for internal and external treatment. It has been
shown that VAO has a powerful antioxidant effect
because of its particular phyto-chemical composition
(Drissi et al., 2004; Guillaume and Charrouf, 2011;
Monfalouti et al., 2010). VAO is composed of 99%
acylglycerides but it is rich in unsaturated fatty acids
(80%) principally oleic and linoleic acids. The
oleic/linoleic ratio is generally about 1.25. Interestingly,
the unsaponifiable fraction (1% of the oil constituents)
of VAO is mainly rich in antioxidant compounds such as
tocopherols, which is present in a higher proportion
(Khallouki et al., 2003). Moreover, this non-glyceric
fraction is rich in phenolic compounds, principally
ferulic and syringic acids and some sterols such as
schottenol (Cherki et al., 2005).
We hypothesize that the consumption of VAO could
improve OS biomarkers and lipid profile in CRF
patients, which in turn may lead to protection against
the development CRF complications.
The aim of this study was to evaluate the impact
of VAO on OS and lipid profile in HD patients after a
period of 4 weeks on VAO diet.
* Correspondence to: Rachid Eljaoudi, Pharmacology and Toxicology
Department, Faculty of Medicine and Pharmacy, University Mohammed
V, 10000 Rabat, Morocco.
E-mail: eljaoudi_rachid@yahoo.fr
†
These authors contributed equally to this work.
PHYTOTHERAPY RESEARCH
Phytother. Res. (2015)
Published online in Wiley Online Library
(wileyonlinelibrary.com) DOI: 10.1002/ptr.5405
Copyright © 2015 John Wiley & Sons, Ltd.
Received 17 October 2014
Revised 18 May 2015
Accepted 01 June 2015
MATERIALS AND METHODS
Argan oil. VAO was purchased from a local women-
cooperative production in the southwest of Morocco.
The composition of the oil as shown on the bottle label
was: oleic acid (47%), linoleic acid (32%) and tocopherols
(44 mg/100 g).
Study design. This prospective unicenter study was con-
ducted according to the principles of the declaration of
Helsinki and was approved by the local Ethical Commit-
tee from the Faculty of Medicine and Pharmacy in Rabat,
Morocco, with assigned number of 479/2012. The protocol
and objectives of the study were explained to the partici-
pants, and a written informed consent was signed by all
of them. All patients were with end-stage renal disease
on maintenance HD. Inclusion criteria were patients on
HD for at least 12 months. None of the patients received
lipid-lowering agents, allopurinol, vitamin E, vitamin C
or any antioxidant drugs. The patients were instructed to
maintain their usual patterns of dietary intake during the
study. HD process was performed with online-produced
ultrapure dialysis fluid (Diasafe and heat disinfection with
hot feed Fresenius Medical Care, with reverse osmosis,
deionization and carbon filtration). All patients received
single-use biocompatible synthetic low-flux membranes
(Polyamide, Polyflux Renal Products Gambro). Blood
flow rates were chosen between 300 and 350mL/min,
and ultra filtration rates were set according to individual
needs. Dialysate flow rate was fixed at 500 mL/min.
Using a crossover, controlled trial, 37 patients were ran-
domized to either group A or group B using computer-
generated random numbers. In the first period, group A
consumed 30mL/day of VAO for 4 weeks taken in a single
dose with bread at breakfast while group B was the con-
trol group. After 8weeks as a washout period, the groups
were reversed (Fig. 1). No placebo was used during the
study because of particular smell and taste of VAO.
We determined sample size on available results from
previous study (Sour et al., 2012). Using G*Power soft-
ware, a final sample size of 36 was needed to provide
90% power at α= 0.05 to detect a 30% increase of serum
α-tocopherol by the VAO diet.
Study parameters
Blood sample. Venous blood was collected after 12 h
fast. Routine blood chemistry and levels of lipids: total
cholesterol (TC), triglyceride (TG), high-density lipopro-
tein (HDL) and low-density lipoprotein (LDL) were
analyzed using fresh blood samples. LDL levels were cal-
culated using Fridewald’s formula. For MDA, vitamin E
and oxidized LDL analysis, samples were collected in
EDTA-containing tubes. Blood venous samples (10 mL)
were centrifuged at 1500 ×gfor 10min just after being
collected. The resulting plasma samples were frozen at
80 °C until analysis.
MDA. MDA was determined by Thiobarbituric Acid
Reactive Substances (TBARS) method as previously
described with a slight modification (Yagi, 1976). All
chemicals and reagents used (from Merck) were of
analytical grade, and Milli-Q water was used for each
dilution. P lasma (100 μL) was mixed to 300 μLofa
42 mM thiobarbituric acid solution and 700 μLofa
phosphoric acid solution (1%). The whole volume
was incubated in a water bath at 95 °C for 45 min. The
reaction was then stopped at ice-cold temperature,
and an equal volume of n-butanol was added to the
reaction mixture. Samples were then centrifuged, and
an aliquot of the supernatant was read at 532 nm.
During the measurement, each sample was analyzed
in duplicate. MDA was determined before and after
dialysis session for each patient.
Oxidized LDL. Plasma level of oxidized LDL (ox-
LDL) was measured in duplicate by a commercially
available sandwich ELISA (Mercodia, Uppsala, Swe-
den). This assay is based on a murine monoclonal
anti-body (mAb-4E6) directed against a conforma-
tional epitope in the apoB-100 moiety of LDL, which
is generated as a consequence of reaction of lysine res-
idues with aldehydes.
Vitamin E. Serum α-tocopherol was determined on all
patients by high-performance liquid chromatography as
described (Milne and Botnen, 1986) with some modifi-
cations. Tocopherol acetate was used as an internal
standard and methanol as a mobile phase. Calibrators
and controls purchased from Recipe (Munich, Germany)
were used during the analysis. After sample prepara-
tion, 30 μL was injected into an ACQUITY UPLC®
system coupled to an ACQUITY UPLC® Photodiode
Array (Waters). The column was ACQUITY UPLC®
BEH C18 1.7 μm 2.1 × 50 mm. The whole HPLC system
was controlled by MassLynx Software (version 4.1). The
internal standard and vitamin E peaks were detected
at 295 nm.
Statistical analysis. All analyses were performed using
the SPSS 13.0 for Windows (SPSS, Inc., Chicago, IL,
Figure 1. Study design diagram.
R. ELJAOUDI ET AL.
Copyright © 2015 John Wiley & Sons, Ltd. Phytother. Res. (2015)
USA). Depending on their normal or skewed distribu-
tion, data are reported as mean ± standard deviation
(SD) or median (full range). Comparison between vari-
ables was performed using the t-test, Wilcoxon’sorchi
square test. The analyze crossover experiment (analyses
of variance for a 2× 2 crossover study) was used to evalu-
ate the effect of VAO diet and performed by Stata SE v.11
software. Value of p <0.05 was considered statistically
significant.
RESULTS
The characteristics of the patients, including sex, age, dura-
tion in HD and other baseline levels are detailed in Table 1.
Table 2 shows that the group and period had no effect
on studied parameters. However, VAO consumption
decreased the levels of TG (p = 0.03), TC (p = 0.02) and
LDL (p = 0.03) and increased the levels of HDL (p = 0.01).
MDA, Ox-LDL and vitamin E contents, used as OS
markers, were determined for each subject both at base-
line and after 4 weeks either in VAO and control groups.
MDA increased in blood’s patient following HD session
(p <0.05 for all the groups and phases) but the increase
in control group was more than that of VAO group
(p = 0.002). Plasma vitamin E contents significantly in-
creased from baseline only in VAO-group (p <0.001).
However, there was no effect of VAO consumption on
the ox-LDL concentrations.
DISCUSSION
The aim of our study was to evaluate the impact of VAO
consumption on OS and lipid profile in HD patients. We
hypothesized that this diet may be beneficial to the
status of OS and lipid parameters in a HD population.
After VAO diet, we noticed an increase of plasma
α-tocopherol concentration accompanied by a down-
ward trend in the levels of MDA. This result suggests
an antioxidant effect of this oil and supported by previ-
ous studies (Cherki et al., 2005; Drissi et al., 2004). It
should be noted that the main tocopherol that we can
find in VAO is the γ-tocopherol. The increase of α-
tocopherol in plasma could be a consequence of the
eventual conversion from γto α-tocopherol because of
the close similarity between the chemical structures of
both molecules (Elmadfa et al., 1989). Tocopherols are
molecules with strong antioxidant and free radical scav-
enging properties. They also act synergistically with
other molecules found in VAO such as polyphenols
and sterols. Polyphenol compounds might exert their
antioxidant effect by acting as a ROS scavenger. This
antioxidant activity is principally defined by the pres-
ence of orthodihydroxy substituent’s, which stabilize
radicals and chelate metals. The antioxidant effect of
phenolic acids and their esters depends on the number
of hydroxyl groups in the molecule. VAO contains im-
portant phenolic compound such as ferulic acid and
syringic acid, which can be more effective than ascorbic
acid and tocopherols (Berrougui et al., 2006).
Table 1. Baseline characteristics of the hemodialysis patients
expressed as the mean ± standard deviation or median (full range)
Value
pVariable Group A Group B
Sex M/W 8/11 10/8 0.35
Age (years) 50.7 ± 16.5 47.9 ± 21.5 0.21
Duration in hemodialysis
(months)
36 (6–132) 39 (13–115) 0.29
BMI (kg/m
2
) 23.1 ± 2.9 23.3 ± 3.4 0.81
TG (g/L) 1.27 ± 0.46 1.35 ± 0.55 0.80
TC (g/L) 1.60 ± 0.43 1.63 ± 0.34 0.81
LDL (g/L) 1.00 ± 0.36 1.02 ± 0.35 0.63
HDL (g/L) 0.35 ± 0.08 0.34 ± 0.05 0.35
OxLDL (U/L) 33.29
(21.23–89.31)
35.15
(20.16–95.41)
0.38
Vitamin E (mg/l) 7.89 ± 2.37 8.17 ± 2.41 0.72
ΔMDA (μMol/L) 2.50 ± 0.89 2.76 ± 0.53 0.49
M/W: men/women BMI: body mass index. TG: triglyceride. TC: total
cholesterol. LDL: low-density lipoprotein. HDL: high-density lipoprotein.
OxLDL: oxidized Low-density lipoprotein. ΔMDA: difference between
malondialdehyde level before and after hemodialysis session.
Data are reported as mean ± standard deviation or median (full range).
Table 2. Effect of group, period and consumption of VAO on different studied parameters (analyses of variance for a 2× 2 crossover study)
expressed as the mean ± standard deviation or median (full range)
Control
n=37
VAO diet
n=37
Group effect
(p value)
Period effect
(p value)
Traitement effect
(p value)
BMI (kg/m
2
) 23.2 ± 3.1 23.3 ± 3.4 0.81 0.78 0.65
TG (g/L) 1.36 ± 0.51 1.18 ± 0.52 0.44 0.15 0.03*
TC (g/L) 1.64 ± 0.35 1.55 ± 0.33 0.69 0.50 0.02*
LDL (g/L) 1.02 ± 0.33 0.91 ± 0.30 0.80 0.66 0.03*
HDL (g/L) 0.34 ± 0.05 0.40 ± 0.09 0.74 0.56 0.01*
OxLDL (U/L) 33.58(20.67–93.28) 34.29(22.43–93.08) 0.98 0.58 0.25
Vitamin E (mg/L) 8.48 ± 1.97 11.67 ± 3.05 0.37 0.06 <0.001*
ΔMDA (μMol/L) 2.54 ± 1.07 1.76 ± 1.01 0.98 0.12 0.002*
M/W: men/women BMI: body mass index. TG: triglyceride. TC: total cholesterol. LDL: low-density lipoprotein. HDL: high-density lipoprotein. OxLDL:
oxidized low-density lipoprotein. VAO (Virgin Argan Oil). ΔMDA: difference between malondialdehyde level before and after hemodialysis session.
Data are reported as mean ± standard deviation or median (full range).
*Statistically significant.
ARGAN OIL IN HEMODIALYSIS PATIENTS
Copyright © 2015 John Wiley & Sons, Ltd. Phytother. Res. (2015)
As proposed by previous studies (Pryor and Stanley,
1975; Franckel and Neff, 1983), oxidized lipids are able
to produce MDA as a decomposition product from
polyunsaturated fatty acids with two or more double
bonds. MDA has been found elevated in HD patients
compared to normal controls because of the state of
OS that accompanies this disease. Blood MDA concen-
tration is generally increased following the dialysis ses-
sion as we found it in a previous study (Elkabbaj et al.,
2012). This is probably because of blood cell activation
by dialysis membrane during the process of HD. How-
ever, MDA increase was reduced following VAO con-
sumption compared to control group. Several studies
have shown that consumption of VAO reduces lipid per-
oxidation and therefore contribute to the reduction of
the concentration of MDA (Cherki et al., 2005; Drissi
et al., 2004; Berrougui et al., 2006). Incubation of LDL
with tocopherol, sterol and phenolic extracts of Argan
oil significantly prolonged the initial lag-phase of LDL
peroxidation. Also, the phenolic extract slowered the
rate of lipid peroxidation and reduced the disappear-
ance of Vitamin E in a concentration-dependent manner
(Berrougui et al., 2006; Drissi et al., 2004).
VAO consumption was associated, in addition, with a
low levels of TC (p = 0.02), LDL (p = 0.03) and a high
level of HDL (p = 0.01). The same results were found
by previous studies (Cherki et al., 2005; Drissi et al.,
2004; Sour et al., 2012). The decrease of cholesterol level
may be because of not only unsaturated fatty acid
contained in Argan oil, but also to minor compounds
such as sterols. Indeed, sterols have molecular structure
very similar to that of human cholesterol, so they reduce
cholesterol absorption by mixing with the micelles and
blocking cholesterol from doing so (Drissi et al., 2004).
Our results showed that HDL levels are significantly
higher after VAO diet. HDL is antiatherogenic lipopro-
teins that are implicated in the protection of LDL
against oxidation (Mackness et al., 1993). Paroxonase 1
(PON1) has been targeted as the principal enzyme
contained within HDL and responsible for their antiox-
idant effect (Blatter et al., 1993). It has been shown that,
VAO consumption increases the PON1 activity and de-
creases the susceptibility of LDL to lipid peroxidation
(Cherki et al., 2005). However, in our study, although vi-
tamin E levels were found to be increased, we found no
difference between the levels of ox-LDL before and af-
ter VAO consumption. This result could be because of
the fact that VAO consumption may not affect in vivo
LDL oxidation and/or that vitamin E was not
incorporated enough in LDL to influence their level of
oxidation. Interestingly, a clinical trial (Drissi et al.,
2004) has shown that in healthy volunteers, consump-
tion of Argan oil has induced an increase of blood
vitamin E levels and a decrease of LDL levels, though
no difference of LDL oxidation in vitro was found when
compared to LDL from control volunteers. Instead,
another clinical study have shown that vitamin E supple-
mentation in HD patients (Islam et al., 2000) proved to
be effective in protecting in vitro oxidation of LDL.
The possible anti-oxidant effect of VAO in vivo may
not be the same on the different molecular species, as
we have found an effect on lipid peroxidation (MDA
levels), and no effect was found on ox-LDL levels upon
VAO consumption.
One of the limitations of our study was sample size
that could have limited the ability to find additional or
stronger association between VAO diet and studied
parameters. However, this pilot study showed for the first
time the beneficial effect of VAO consumption in HD
patients by improving the status of vitamin E and lipid
profile on one hand. On the other hand, our data show
that dialysis membrane-related MDA production during
HD process is reduced following VAO consumption.
This study should be complemented by large-scale
trials but, based on these preliminary results, we can rec-
ommend the consumption of this oil to this category of
patients as a natural antioxidant.
Acknowledgements
This work was supported by a grant from the University of Sidi
Mohamed Ben Abdellah, Faculty of Medicine and Pharmacy, Fez,
Morocco.
Conflict of Interest
None declared
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ARGAN OIL IN HEMODIALYSIS PATIENTS
Copyright © 2015 John Wiley & Sons, Ltd. Phytother. Res. (2015)
