Головна Journal of Functional Foods Inclusion of Hass avocado-oil improves postprandial metabolic responses to a hypercaloric-hyperlipidic..

Inclusion of Hass avocado-oil improves postprandial metabolic responses to a hypercaloric-hyperlipidic meal in overweight subjects

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Journal of Functional Foods
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10.1016/j.jff.2017.09.019
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Journal of Functional Foods 38 (2017) 349–354

Contents lists available at ScienceDirect

Journal of Functional Foods
journal homepage: www.elsevier.com/locate/jff

Inclusion of Hass avocado-oil improves postprandial metabolic
responses to a hypercaloric-hyperlipidic meal in overweight subjects
Cibele Priscila Busch Furlan a, Sandra Costa Valle b, Elin Östman c, Mário Roberto Maróstica Jr. a,
Juscelino Tovar c,⇑
a
b
c

Department of Food and Nutrition, Faculty of Food Engineering, University of Campinas, 13083-862 Campinas, SP, Brazil
Faculty of Nutrition, Federal University of Pelotas, 96001-970 Pelotas, RS, Brazil
Food for Health Science Centre and Department of Food Technology, Engineering & Nutrition, Lund University, Medicon Village, SE-223 81 Lund, Sweden

a r t i c l e

i n f o

Article history:
Received 17 June 2017
Received in revised form 4 September 2017
Accepted 13 September 2017

Keywords:
Butter
Avocado-oil
Inflammation
Endotoxemia
Postprandial lipidemia
Postprandial glycemia

a b s t r a c t
In recent years, the increase of the global incidence of obesity and obesity-related disorders has been
associated with metabolic imbalance and low grade inflammation. Fat-rich meals and diets contribute
importantly to those alterations. The aim of this work was to evaluate the impact of exchanging butter
by Hass avocado-oil on postprandial metabolic parameters in healthy overweight volunteers consuming
a hypercaloric-hyperlipidic breakfast. Thirteen healthy volunteers consumed a control meal (CM) consisting of: butter, eggs, bacon, wheat bread, potatoes and iced sugar, or a test meal (TM), where butter was
totally replaced by Hass avocado-oil. Blood biomarkers were measured postprandially during 240 min.
Participants were 65.1 ± 5.3 years old, body mass index 28.1 ± 1.8 kg/m2 and fasting glycemia
6.1 mmol/L. The consumption of CM or TM resulted in similar high-density lipoprotein and
glucagon-like peptide-1 (GLP-1) responses, but TM improved postprandial profiles of insulin, glycemia,
total choleste; rol, low-density lipoprotein, triacylglycerols, C-reactive protein and interleukin-6
(P < 0.05). The study shows potential of Hass avocado-oil for counteracting the negative impact of a high
fat and hypercaloric breakfast meal on important biomarkers related to cardiometabolic health.
Ó 2017 Elsevier Ltd. All rights reserved.

1. Introduction
In recent years, the increase of the global incidence of obesity
and obesity-related disorders, including insulin resistance, type 2
diabetes and cardiovascular diseases, has been associated with
metabolic imbalance and low grade and chronic inflammation
(Dandona, Aljada, & Bandyopadhyay, 2004; Poirier & Eckel,
2002). Clinical atherosclerosis, one of the many obesity consequences, is related to altered circulating levels of adhesion molecules, blood lipids and inflammatory cytokines, as well as

Abbreviations: CM, control meal; TM, test meal; BMI, body mass index; LDL-c,
low-density lipoprotein cholesterol; HDL-c, high-density lipoprotein cholesterol;
TC, total cholesterol; TG, triacylglycerol; GLP-1, glucagon-like peptide-1; CRP, Creactive protein; IL-6, interleukin 6; LBP, LPS-binding protein; sCD14, soluble
cluster of differentiation 14; TLR, toll like receptors; LPS, lipopolysaccharide; SFA,
saturated fatty acids; TNF-a, tumor necrosis factor alpha.
⇑ Corresponding author.
E-mail addresses: cibelefurlan07@gmail.com (C.P.B. Furlan), sandracostavalle@gmail.com (S.C. Valle), mario@fea.unicamp.br (M.R. Maróstica Jr.), juscelino.
tovar@food-health-science.lu.se (J. Tovar).

http://dx.doi.org/10.1016/j.jff.2017.09.019
1756-4646/Ó 2017 Elsevier Ltd. All rights reserved.

endotoxemia via lipopolysaccharide (LPS), which is related to activation of Toll Like Receptors (TLRs), triggering inflammation signaling pathways (Stoll, Denning, & Weintraub, 2004).
The complex and intrinsic metabolic condition in obesityrelated disorders is also related to the quality of the diet, where
fat composition plays a very important role. Recent findings point
out the devastating effect that the regular intake of inflammatory
fatty acids, such as palmitc, myristic, lauric and stearic acids,
may have on health (Lumeng & Saltiel, 2011).
Studies looking at the metabolic impact of saturated fatty acid
consumption have shown increased insulin resistance and inflammation related to LPS, due to increased gut permeability. These
effects, however, are not seen with diets rich in olive oil, flaxseed
oil and fish oil, which are sources of unsaturated fatty acids
(Inoue et al., 2017; Lee, Sohn, Rhee, & Hwang, 2001; Oliveira
et al., 2015; Zhao, Joshi-Barve, Barve, & Chen, 2004). These observations suggest a link between the intake of saturated fatty acids,
TLRs activation, and inflammation, as part of the atherogenesis
process (Stoll et al., 2004).
In line with those beneficial effects of unsaturated fatty acids,
avocado-oil has emerged as a new product with high contents of

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C.P.B. Furlan et al. / Journal of Functional Foods 38 (2017) 349–354

oleic acid and phytosterols (Berasategi, Barriuso, Ansorena, &
Astiasarán, 2012) that may contribute to improve health-related
parameters, specially to diminish the negative consequences of
atherosclerosis (Dreher & Davenport, 2013). However, there are
few studies about its health promoting benefits (Woolf et al.,
2009).
Nevertheless, despite the enthusiasm opened by those reports,
the beneficial effects of Hass avocado-oil on human health are still
scarcely documented in the literature. Therefore, the present study
investigated the impact of replacing butter by Haas avocado-oil on
postprandial circulating levels of cardiometabolic risk-related
biomarkers in a group of mature healthy overweight subjects, eating a high calorie hyperlipidic meal.

collection tubes for the assessment of biomarkers such as fasting
insulin, lipid profile: total cholesterol (TC), low-density lipoprotein
cholesterol (LDL-c), high-density lipoprotein cholesterol (HDL-c)
and triacylglycerol (TG); levels of inflammatory markers: Creactive protein (CRP), interleukin-6 (IL-6), lipopolysaccharide
binding protein (LBP), cluster of differentiation 14 (sCD14) and
the gut hormone glucagon-like peptide-1 (GLP-1). After each meal,
blood samples were taken at different times over a 240 min period
to assess the postprandial levels of the various biomarkers (see
below).
The study protocol was approved by the Regional Ethical
Review Board (Lund; Dnr 2015/413). The trial was registered at
ClinicalTrials.gov (NCT02623608).

2. Material and methods

2.3. Meals

2.1. Participants
Healthy volunteers, non-smoking and without any known medical condition, were recruited through advertisement in local
newspapers. The characteristics of the experimental cohort correspond to those of a healthy population that, by virtue of age
(mature subjects) and overweight, is at increased risk for cardiometabolic disease (Tovar, Johansson, & Björck, 2016). Subjects
were orally informed and received documents about the practical
details of the experiment. Inclusion criteria were as follows: normal fasting plasma glucose value (6.1 mmol/L), age between 50
and 73 years old and body mass index in the 24.9–29.9 kg/m2
range, not allergic or intolerant to gluten and eggs, and with disposition to visit the clinical unit twice (5.5 h per visit). Only medications accepted were prescription-free painkillers without antiinflammatory action.
2.2. Study protocol
On the screening day, BMI and fasting blood glucose were measured. The participants who met the inclusion criteria were scheduled for visiting the clinical unit (Lund University, Food for Health
Laboratory) in a randomized crossover scheme: two experimental
sessions, separated by at least 6 days (Fig. 1).
Participants were instructed to consume the same dinner on the
night prior to the experimental days (spaghetti, tomato sauce,
chicken, cheese and soybean oil), in order to homogenize the influence of the previous meal on next day fasting glucose levels
(Wolever, Jenkins, Ocana, Rao, & Collier, 1988) (supplementary
material-Table S1). Subjects should not alter their regular physical
activity on the day before the trials.
On each clinical visit, BMI and fasting blood glucose were measured. A finger-tip capillary blood sample was collected for glucose
measurement, and venous blood was then drawn with the aid of

Hass avocado-oil was donated by JaguacyÒ Brasil industry, but
the oil can be also found in Brazilian retail markets. The oil was
extracted from avocado fruit pulp, which was heated to 35 °C,
pressed and centrifuged; the oil was collected and bottled without
additives, for commercialization.
Detailed Hass avocado-oil fatty acid composition (58% monounsaturated fatty acid, 16% polyunsaturated fatty acid and 26% saturated fatty acid) and sterol levels (522.13 ± 0.15 mg 100 g 1 oil)
will be separately reported (manuscript in preparation). The composition of the studied meals was calculated using the nutritional
contents listed in the 2009 food database from the Swedish
National Food Administration (Nacional Food Agency, 2015). The
nutritional profiles of the Control meal (CM) and Hass avocadooil test meal (TM) are shown in Table 1.
The meals consisted of eggs (white and yolk), bacon, potatoes,
iced sugar and butter (80% fat; in control meal) or Hass avocadooil (test meal). CM provided 27 g saturated fatty acids, while TM
had 25 g monounsaturated fatty acids (mainly oleic acid, provided
by Hass avocado-oil). Both meals were designed to provide
900 kcal and 50 g total fat, representing an E% value of 50
(450 kcal) (supplementary material Table S2).
2.4. Biomarker assessment
2.4.1. Lipid profile
Twelve hour fasting values and postprandial levels of TC, LDL-c,
HDL-c and TG were measured in plasma samples by the Clinical
Chemistry Laboratory/Skåne University Hospital (Malmö), using
standard methods (Tovar et al., 2016).
2.4.2. 2Inflammatory markers and GLP-1 levels
Twelve hour fasting values and postprandial levels of CRP, IL-6
and GLP-1 were measured in plasma samples by CRP ELISA kit (Cat.
No. IDG-K9710s, Industrial Distribution Group, Belmont, United

Table 1
Nutritional profile of CM and TM.

Carbohydrate (g)
Fiber (g)
Protein (g)
Fat (g)
SFA (g)
PUFA (g)
MUFA (g)
Cholesterol (mg)
Calories (kcal)
Weight (g)

Fig. 1. Crossover study design.

CM

TM

80.37
5.53
32.10
50.06
26.91
3.62
14.91
321.84
911.48
409.00

80.24
5.53
32.04
50.22
12.84
8.09
26.46
312.48
912.19
392.00

SFA: Saturated fatty acids; PUFA:Polyunsaturated fatty acids; MUFA: Monounsaturated fatty acids.

C.P.B. Furlan et al. / Journal of Functional Foods 38 (2017) 349–354

States), IL-6 ELISA kit (Cat. No. HS600BR&D Systems, Minneapolis,
MN), GLP-1 Total ELISA kit (Cat. No. ALP-43-GP1HU-E01ALPCO,
Salem, United States). Samples were for GLP-1 analyses were collected in the presence of DPP-IV (DPP4-010 Merck Millipore, Darmstadt, Germany) and Pefabloc (PefablocÒ SC (AEBSF), Mannheim,
Germany) inhibitors.

2.4.3. Endotoxemia
LBP and sCD14circulating levels were measured in plasma using
ELISA kits supplied by MSD (Rockville, Maryland, USA) and BioAspect (Toronto, Canada), respectively.

2.4.4. Glucose and insulin
Basal concentrations of blood glucose and serum insulin were
measured in the volunteers after 12 h fasting. Insulin concentration was also measured at 0, 30, 60, 120, 180, 210 and 240 min
post-meal. The analyses were performed by the Clinical Chemistry
Laboratory/Skåne University Hospital (Malmö). Samples of capillary blood were also drawn to determine the glucose concentration
(HemoCue201RT-glucose, HemoCue AB) at 0, 30, 60, 90, 120, 180,
210 and 240 min postprandially as described earlier (Ekstrom,
Bjorck, & Ostman, 2013; Rosén et al., 2011).

2.5. Statistical analysis and power calculation
The results are presented as mean ± standard error of the mean
(SEM). The normality of the data was verified using the ShapiroWilk test and the homogeneity through the Levene test. The CRP
data, with asymmetric distributions, were Ln transformed before
analysis. Statistical analyses were performed using the Student’s
t-test for repeated measures. Paired t-test was used to compare
the means of the curves. The power from these analyses was estimated, and r value 0.5 was considered as a significant strong
power and r value 0.3 was considered as a moderated power.
In order to test the effect of TM and its time interactions, the
ANOVA-RM test was performed, followed by the post hoc Bonferroni test. The p-value lower than 0.05 was considered statistically
significant. All statistical analyses were performed using GraphPad
Prism 5 (GraphPad Software, Inc., La Jolla, CA).

3. Results
3.1. Participants profile
The clinical visits took place between September and October
2015. Nineteen volunteers showed interest in the study, seventeen
showed up for screening and 15 met the inclusion criteria. Two
participants did not complete the study, leaving 13 data-yielding
subjects. Participants were 65.15 ± 5.32 years old, with BMI
28.04 ± 1.75 kg/m2 and fasting glycemia 5.35±0.55 mmol/L, as
recorded on the screening day. No statistically significant change
was observed in BMI or fasting glycemia values over the study
length (Supplementary material-Table S3).

3.2. Postprandial blood lipid responses
Comparison of the average postprandial curves (Table 2; Fig. 2)
indicated that replacement of butter by Hass avocado-oil in TM
reduced significantly (P < 0.05; r > 0.9) TG, TC and LDL-c compared
to CM. Moreover, late levels (240 min) of TC and TG were significantly lower after TM (P < 0.05). HDL-c curves, however, did not
show differences between the two meals.

351

3.3. Acute inflammatory response
The inclusion of Hass avocado-oil improved postprandial
inflammatory responses, as circulating CRP showed a significant
overall reduction (P = 0.019; r = 0.623) after TM (Table 2). Late
levels (240 min) of IL-6 were also significantly lower after TM
(P = 0.003) (Fig. 3a). An early (30 min) decreased LBP/sCD14 ratio
was recorded after TM, although the difference did not reach statistical significance (P = 0.08) (Fig. 3b).
3.4. Glucose and hormonal responses
Hass avocado-oil in TM improved postprandial glucose
(P = 0.03; r = 0.865) and insulin (P = 0.006; r = 0.779) levels
(Table 2). However, GLP-1 post-meal concentrations did not differ
between CM and TM (Table 2).
4. Discussion
Present results show, for the first time in postprandial conditions, potential cardio-protective benefits of Hass avocado-oil compared to butter in a high-fat meal. The bioactive compounds and
MUFA-rich lipid profile in the Hass avocado-oil meal, appear thus
capable of attenuating inflammation even in a high-fat and hypercaloric meal background.
Elevated circulating levels of CRP, cholesterol fraction LDL-c, TC
and TG are some of the strongest prognostic factors for atherosclerosis disease (Singh & Singh, 2016; Verma et al., 2003). Here, the
replacement of butter by Hass avocado-oil resulted in significant
postprandial attenuation of these risk markers. It is known that
semi-long term consumption of avocado fruit contributes to blood
lipid profile improvements and thus may provide protection
against cardiovascular diseases (Wang, Bordi, Fleming, Hill, &
Kris-Etherton, 2015). The reduction of blood lipids can be
explained by the presence of fat-soluble phytosterols in the avocado fruit, mainly in its oil fraction (Berasategi et al., 2012;
Dreher & Davenport, 2013). Phytosterols decrease cholesterol
absorption from the small intestinal lumen as a result of their similar chemical structures. When simultaneously present in the
lumen, plant sterols being more hydrophobic are retained in the
micellar structures competing with cholesterol and, consequently
decreasing its absorption (Sanclemente, Marques-Lopes, Puzo, &
García-Otín, 2009). Although most evidences of circulating cholesterol reduction associated to dietary modifications come from
medium and long-term interventions (Tovar et al., 2016), the postprandial effect of certain foods and ingredients on cholesterol fractions has also been explored in a number of studies (Cara et al.,
1992; De Smet, Mensink, Lütjohann, & Plat, 2015; Liu et al.,
2017). Present data stress the importance of meal composition
for the modulation of acute cholesterolemic responses.
Previous studies (Carranza et al., 1994; López et al., 1995)
showed that medium-term intake of the avocado fruit not only
decreases TC, LDL-c and TG, but it can also increase HDL-c levels,
an effect that was not observed in this investigation. Thus, the
HDL-c fraction enhancement might be related to other bioactive
compounds present in the fruit pulp, but not in the extracted oil.
It could also be that HDL-c changes require a more chronic intake.
Saturated fatty acids (SFA), especially palmitic and stearic acids,
are related to increased gut permeability that leads to bacterial
lipopolysaccharide (LPS) translocation to the circulatory system
(de Lima-Salgado, Alba-Loureiro, do Nascimento, Nunes, & Curi,
2011). The binder molecule LBP and the transfer sCD14 are the
major serum factors responsible for the initiation of innate
immune responses due to activation of Toll-like receptors 2 or 4
(TLR), initiating a signal transduction pathway that leads to the

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C.P.B. Furlan et al. / Journal of Functional Foods 38 (2017) 349–354

Table 2
Effect of butter (CM) replacement by Hass avocado-oil (TM) on postprandial biomarker levels.
Blood markers

TC (mmol/L)
TG (mmol/L)
LDL-c (mmol/L)
HDL-c (mmol/L)
Insulin (mIE/L)
Glucose (mmol/L)
CRP (mg/L)
IL-6 (pg/mL)
LBP/sCD14
GLP-1 (pmol/L)
*
**

CM

TM

Mean

SEM

Mean

SEM

5.76
144.1
3.73
1.63
38.47
6.75
1.79
234.8
0.26
2.86

0.04
17.01
0.04
0.03
7.25
0.33
0.03
79.22
0.01
0.18

5.65
140.9
3.66
1.64
36.89
6.34
1.74
195.0
0.24
2.84

0.03
18.88
0.03
0.02
7.04
0.28
0.02
48.50
0.00
0.25

p value*

r value**

0.001
0.0001
0.0001
0.218
0.006
0.003
0.019
0.306
0.335
0.456

0.910
0.963
0.949
0.490
0.779
0.865
0.623
0.334
0.230
0.381

Paired t-test.
Statistic power: r  0.5 was considered as strong statistic power to improve the blood biomarkers and r  0.3 was considered as a moderated power.

Fig. 2. Postprandial lipids profiles following CM or TM meal. (a) Triacylglycerides (*P = 0.0001); (b) Total cholesterol (*P = 0.001). *Indicates significant differences between the
two meals (ANOVA-RM test). **Significant difference at 240 min (P < 0.05, Bonferroni test).

Fig. 3. Postprandial circulating pro-inflammatory cytokine IL-6 (a) and LBP/sCD14 ratio (b) levels after CM or TM. **Significant difference at 240 min (P = 0.003, Bonferroni
test).

release of pro-inflammatory cytokines, such as Tumor Necrosis
Factor Alpha (TNF-a) via NF-kB nucleo translocation (Schröder
et al., 2004). Increased LBP/sCD14 ratios have been thus associated
with endotoxemia, as an enhanced acute phase inflammatory
response (Laugerette et al., 2014). A tendency to reduced ratios
was observed shortly after the intake of TM, a response that would
be interesting to explore further as part of the potential
cardiometabolic-protective effects of avocado oil.
As we demonstrate here for Hass avocado-oil, the intake of avocado fruit pulp resulted in a late postprandial reduction in circulating pro-inflammatory IL-6 (Li et al., 2013). The role of unsaturated
fatty acids, mainly oleic acid, as anti-inflammatory agents has been
highlighted in studies in vitro (Oh et al., 2009) and in animal mod-

els (Oliveira et al., 2015). Besides, TM showed ability to attenuate
postprandial CRP levels, a systemic inflammatory marker and a risk
factor for atherosclerotic disease (Verma et al., 2003). Data on CRP
postprandial responses in hyperlipidic meal studies are still inconsistent, owing to the many different protocols applied (PerezMartinez et al., 2014; Schmid et al., 2015). However, previous
investigations showed decreased inflammatory markers, such as
TNF-a, IL-6 and CRP, in rats fed with avocado oil, which suggests
protective potential against cardiovascular damage and insulin
resistance (Carvajal-Zarrabal et al., 2014).
The presence of Hass avocado-oil in TM resulted in improved
postprandial glycemia and insulinemia compared with CM. Olive
oil, for instance, may protect against insulin resistance by promot-

C.P.B. Furlan et al. / Journal of Functional Foods 38 (2017) 349–354

ing phosphorylation of the insulin receptor in tyrosine residues
and thus improve peripheral glucose uptake and reduce inflammation (Oliveira et al., 2015). Hence, a similar explanation for the
potentially protective action of Hass avocado-oil on insulin resistance and hampered glucose uptake associated with high fat meals
and diets may be proposed.
Wien, Haddad, Oda, and Sabaté (2013) and Sabaté, Wien, and
Haddad (2015) reported improved insulin and glucose values, as
well as increased satiety via GLP-1, in healthy overweight adults
consuming Hass avocado fruit. The authors attributed the outcomes to the fat and dietary fiber quality of the product. In our
study, GLP-1 responses did not differ between TM and CM, an
observation that may favor the idea of a fiber-dependent GLP-1
secretion enhancing effect for the avocado fruit, as reported for certain soluble fibers (Sabaté et al., 2015). However, it may also be
that the GLP-1 enhancing action requires longer exposures than
the acute condition prevailing here.
Although contribution of other components of the fruit cannot
be ruled out, these observations may be taken as an indication of
the oil fraction as main responsible for the lipid profile amelioration, inflammatory markers improvements and glycemia and insulinemia reductions associated to avocado intake.
As a whole, this study shows that Hass avocado-oil consumed
by healthy subjects can favorably modulate the negative physiological impact associated to high calorie and hyperlipidic meals.
The results showed the attenuation of atherosclerosis risk factors,
protection against inflammation and a tendency to improve endotoxemia. They also stress the importance of correct fat quality
choice as fundamental for the modulation of cardiometabolic risk.
The endotoxemia reducing potential of Hass avocado-oil expands
horizons for further investigations.
Acknowledgments
The authors thank JaguacyÒBrasil for the donation of Hass
avocado-oil. Funding from by The Brazilian National Council for
Scientific and Technological Development (CNPq grant number
301108/2016-1) and by Fundação de Amparo à Pesquisa do Estado
de São Paulo (FAPESP grant number 2015/13320-9) are also
acknowledged. CF is grateful to Science Without Borders for international scholarship (205356/2014-1). We thank Lisbeth Persson
and post doctoral fellow Anestis Dougkas from Lund University
for technical assistance and protocol monitoring, respectively. This
work was fostered by the Antidiabetic Food Centre (AFC), a Vinnova Excellence Centre at Lund University.
Conflict of interest and author participation
The authors declare no conflict of interest. All authors participated
in the conception and design of the study. CF and JT carried out the
experiment. CF, JT and SV processed and evaluated the data. CF and
JT drafted the paper. All authors contributed to the interpretation
and discussion of results and approved the final version of the
manuscript.
Appendix A. Supplementary material
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.jff.2017.09.019.
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