Oat Polar Lipids Improve Cardiometabolic-Related Markers after Breakfast and a Subsequent Standardized Lunch: A Randomized Crossover Study in Healthy Young Adults

Abstract

It has been suggested that intake of polar lipids may beneficially modulate various metabolic variables. The purpose of this study was to evaluate the effect of oat polar lipids on postprandial and second meal glycemic regulation, blood lipids, gastrointestinal hormones, and subjective appetite-related variables in healthy humans. In a randomized design, twenty healthy subjects ingested four liquid cereal-based test beverages (42 g of available carbohydrates) containing: i. 30 g of oat oil with a low concentration (4%) of polar lipids (PLL), ii. 30 g of oat oil containing a high concentration (40%) of polar lipids (PLH), iii. 30 g of rapeseed oil (RSO), and iv. no added lipids (NL). The products were served as breakfast meals followed by a standardized lunch. Test variables were measured at fasting and during 3 h after breakfast and two additional hours following a standardized lunch. PLH reduced glucose and insulin responses after breakfast (0–120 min) compared to RSO, and after lunch (210–330 min) compared to RSO and PLL (p < 0.05). Compared to RSO, PLH resulted in increased concentrations of the gut hormones GLP-1 and PYY after the standardized lunch (p < 0.05). The results suggest that oat polar lipids have potential nutraceutical properties by modulating acute and second meal postprandial metabolic responses.

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nutrients
Article
Oat Polar Lipids Improve Cardiometabolic-Related Markers
after Breakfast and a Subsequent Standardized Lunch: A
Randomized Crossover Study in Healthy Young Adults
Mohammad Mukul Hossain 1, * , Juscelino Tovar 1, Lieselotte Cloetens 2, Maria T. Soria Florido 2,
Karin Petersson 3, Frederic Prothon 3and Anne Nilsson 1


Citation: Hossain, M.M.; Tovar, J.;
Cloetens, L.; Florido, M.T.S.;
Petersson, K.; Prothon, F.; Nilsson, A.
Oat Polar Lipids Improve
Cardiometabolic-Related Markers
after Breakfast and a Subsequent
Standardized Lunch: A Randomized
Crossover Study in Healthy Young
Adults. Nutrients 2021,13, 988.
https://doi.org/10.3390/
nu13030988
Academic Editor: Osama Hamdy
Received: 29 January 2021
Accepted: 16 March 2021
Published: 18 March 2021
Publisher’s Note: MDPI stays neutral
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iations.
Copyright: © 2021 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
1Department of Food Technology, Engineering and Nutrition, Lund University, P.O. Box 124,
221 00 Lund, Sweden; juscelino.tovar@food.lth.se (J.T.); anne.nilsson@food.lth.se (A.N.)
2Division of Pure and Applied Biochemistry, Lund University, P.O. Box 124, 221 00 Lund, Sweden;
lieselotte.cloetens@tbiokem.lth.se (L.C.); maria.soria_florido@tbiokem.lth.se (M.T.S.F.)
3Oatly AB, 261 51 Landskrona, Sweden; karin.petersson@oatly.com (K.P.); frederic.prothon@oatly.com (F.P.)
*Correspondence: mohammad_mukul.hossain@food.lth.se; Tel.: +46-46-222-95-34
Abstract:
It has been suggested that intake of polar lipids may beneficially modulate various
metabolic variables. The purpose of this study was to evaluate the effect of oat polar lipids on
postprandial and second meal glycemic regulation, blood lipids, gastrointestinal hormones, and
subjective appetite-related variables in healthy humans. In a randomized design, twenty healthy
subjects ingested four liquid cereal-based test beverages (42 g of available carbohydrates) containing:
i. 30 g of oat oil with a low concentration (4%) of polar lipids (PLL), ii. 30 g of oat oil containing a high
concentration (40%) of polar lipids (PLH), iii. 30 g of rapeseed oil (RSO), and iv. no added lipids (NL).
The products were served as breakfast meals followed by a standardized lunch. Test variables were
measured at fasting and during 3 h after breakfast and two additional hours following a standardized
lunch. PLH reduced glucose and insulin responses after breakfast (0–120 min) compared to RSO, and
after lunch (210–330 min) compared to RSO and PLL (p< 0.05). Compared to RSO, PLH resulted in
increased concentrations of the gut hormones GLP-1 and PYY after the standardized lunch (p< 0.05).
The results suggest that oat polar lipids have potential nutraceutical properties by modulating acute
and second meal postprandial metabolic responses.
Keywords:
appetite regulation; blood lipids; glycemic regulation; GLP-1; metabolic regulation; oat;
polar lipids; postprandial glucose response; PYY; RCT
1. Introduction
The pandemic of lifestyle-related diseases, such as obesity and type 2 diabetes (T2D),
constitutes a major public health and economic challenge, since these illnesses have serious
consequences, e.g., cardiovascular disease (CVD) and premature death [
1
]. About half
a billion (9.3%) people worldwide have diabetes (2019), and the number is predicted to
rise to 10.2% by 2030, whereof T2D is 90% of all cases [
1
]. Thus, preventive strategies are
urgently needed.
It has been shown that bioactive components of whole grains may be associated with
lower body mass index (BMI) and reduced risk of CVD and T2D [
2
,
3
]. In this regard, oats
are rich in health-promoting components, such as soluble dietary fiber (beta-glucan), lipids,
and bioactive phenolic compounds (avenanthramides, tocopherols) [
4
–
7
]. Many studies
have demonstrated that regular consumption of oat products rich in beta-glucans is linked
to reduction of low-density lipoprotein (LDL) cholesterol levels in blood and postprandial
glycemia, which has led to health claims on beta-glucans containing products [
4
,
8
–
11
].
Moreover, oats are particularly rich in polar lipids, which constitute approximately 15 wt%
of total lipids. The oat polar lipids include phospholipids, glycolipids, and sphingolipids.
Nutrients 2021,13, 988. https://doi.org/10.3390/nu13030988 https://www.mdpi.com/journal/nutrients

Nutrients 2021,13, 988 2 of 16
The most abundant polar lipids in oat are the galactolipids, mainly digalactosyldiacylglyc-
erol (DGDG) and its derivatives with different polarity (TriGDG, TetraGDG, and various
types of estolides) [
12
–
15
]. These galactolipids in plants constitute the bulk of thylakoid
membrane lipids, and provide a lipid bilayer matrix for photosynthetic complexes as the
main constituents [12].
The gut hormones glucagon-like peptide 1 (GLP-1) and peptide YY (PYY) are released
in response to food intake, and are important in metabolic and appetite regulation [16]. It
has been reported that dietary lipids decrease the gastric emptying rate, and are a potent
stimulus for the release of gut hormones, thus having the potential to lower postprandial
glucose response and induce satiety [
17
]. There is a lack of studies investigating the effects
of extracted oat polar lipids on metabolic variables. It has been suggested that polar lipid
fractions may be involved in the cholesterol-lowering effects of oats [
18
]. Ohlsson et al.
(2014) studied the effects on plasma lipids and gut hormones after intake of liposomes
made from fractionated oat oils [
19
]. It was observed that a breakfast meal containing
oat oil liposomes significantly increased plasma concentrations of certain gut hormones,
prolonged elevation of triglycerides, decreased free fatty acids (FFA), and reduced volun-
tary energy intake during the rest of the day. However, there is only scarce information
regarding the effects of oat polar lipids on cardio-metabolic risk-related markers in the
acute and second meal postprandial period perspective.
The aim of this study was to investigate the metabolic effects of oat polar lipids con-
sumed at breakfast on glycemic responses, appetite sensations, circulating gut hormones,
and the lipid profile in the postprandial phases following two consecutive meals (test
breakfast and standardized lunch). For this purpose, a randomized crossover meal study
was performed in healthy young adults.
2. Materials and Methods
2.1. Study Subjects
Recruitments of test subjects took place between January and March 2019, and the
clinical phase took place between March and May 2019. The inclusion criteria were
age between 20–40 years, BMI between 19–25 kg/m
2
, being a non-smoker, and having
no diagnosed metabolic disorders or food allergies. Each subject got a full explanation
(written and oral) of the purpose and protocol of the study, and written informed consent
was obtained. Volunteers were aware of the possibility of withdrawing from the study
at any time. Twenty healthy volunteers, five men and 15 women, aged (mean
±
SEM)
24.8 ±0.9 years
, and with BMI (mean
±
SEM) 22.2
±
0.4 kg/m
2
were enrolled to participate
in the study.
2.2. Study Design and Procedure
The study was performed using a single-blind crossover design. Each participant
consumed all of the meals, and in a random order. The different products were tested
approximately one week apart. The day before each experiment, the participants had to
avoid strenuous exercise, alcohol intake, and the consumption of oat products and food
with high fiber content (beans, whole grain bread, fiber enriched pasta, whole cereal kernels,
etc.). No antibiotics or probiotics were allowed within two weeks before and during the
study period. To keep track of standardization of meal patterns prior to each experiment
day, the participants were requested to provide a meal record from the day before each
experiment day. Furthermore, the participants were instructed to consume individualized
dinner meals at 18:00 on the day before each experiment. They consumed the same dinner
on all occasions. In addition, the participants consumed a standardized evening meal at
21:00, consisting of a commercial white wheat bread with topping of their choice (same
topping before each experimental day). After this meal, they fasted until a test breakfast
meal was served at the research unit. Small quantities (half a glass) of water were, however,
allowed prior to bedtime and when they woke up. The participants had to keep to the
same routine before each experimental day.

Nutrients 2021,13, 988 3 of 16
The subject arrived at the research unit at 07:30 after overnight fasting. Finger-prick
blood samples and subjective appetite scores were obtained prior to the breakfast, which
was served at 08:00 (time = 0 min, baseline). After that, the participants were instructed
to consume the test meal within 12 min. For glucose measurements, additional capillary
blood samples were drawn at 15, 30, 45, 60, 90, 120, 150, 180, and 210 min after the start of
the breakfast meal. After the blood test, at 210 min, the standardized lunch was served, and
blood samples were drawn at 225, 240, 255, 270, 300, and 330 min after baseline. Insulin
was measured at the same time points as glucose, excluding 15 and 225 min. Considering
the limited amount of capillary blood that can be drawn, triglycerides and gastrointestinal
hormones were measured only at 0, 60, 210, and 330 min. During the experimental days,
participants remained at the clinical facility, quietly seated, and were not allowed to eat or
drink anything, except for the breakfast and lunch meals provided.
2.3. Test Meals
The test meals were provided as liquid breakfasts, and consisted of an oat-based
preparation specially designed for this study, added with different types and amounts
of lipids (developed and manufactured by Oatly AB, Sweden). A glucose solution was
included as the reference product. The oat base preparation was added with: i. oat oil con-
taining low concentrations of polar lipids (PLL), ii. oat oil containing high concentrations
of polar lipids (PLH), or iii. rapeseed oil (RSO) as a reference oil. Their metabolic effects
were compared to those of the oat base preparation with no added lipids (NL). The oat oils
were provided by Swedish Oat Fiber AB (Bua, Sweden), and rapeseed oil was purchased
from AAK AB (Karlshamn, Sweden). All of the breakfast meals containing added lipids
supplied an equivalent amount of total fat (33 g). All breakfast beverages contained 42 g of
available carbohydrates. The nutritional composition of the breakfast meals is displayed in
Table 1.
Table 1. Nutritional composition of the breakfast meals per serving (500 mL) 1.
PLL PLH RSO NL Glucose
Available Carbohydrates (g)
42 42 42 42 42
Free glucose (g) 1.75 1.75 1.75 1.75 42
Fat (g) 33 33 33 3 0
Polar lipids (g) 21 12 1 <0.5 0
Protein (g) 6.5 6.5 6.5 6.5 0
Dietary fiber (g) 5 5 5 5 0
beta-glucans (g) 2.5 2.5 2.5 2.5 0
Energy (Kcal) 491 491 491 221 168
1
PLL, oat preparation with a low concentration of oat polar lipids; PLH, oat preparation with a high concentration
of oat polar lipids; RSO, oat preparation with added rapeseed oil; NL, oat preparation without added lipids.
2
Polar lipid contents in PLL and PLH according to the supplier, and in NL and RSO estimated according to
reference [20].
2.4. Standardized Lunch
The standardized lunch consisted of 122 g of white wheat bread (Pågen AB, Malmö,
Sweden), corresponding to 42 g of available starch, 100 g of meatballs (Scan AB, Stockholm,
Sweden), and 250 mL of water. Based on the nutritional facts declared by the producers,
the total energy content of the lunch meal was 537 kcal. Table 2shows the macronutrient
composition of the lunch meal.
Table 2. Nutritional composition of lunch meal per 100 g 1.
Meatballs Bread
Carbohydrate (g) 8 47.0
Fat (g) 15 3.5
Protein (g) 13 8.5
1Based on the nutritional facts declared by the producers.

Nutrients 2021,13, 988 4 of 16
2.5. Physiological Test Parameters
Plasma glucose concentrations were determined in whole blood using a HemoCue
Glucose 201
+
analyzer (HemoCue AB, Ängelholm, Sweden). Samples for serum insulin,
serum free fatty acids (FFAs), and serum triglycerides (TGs) analyses were collected in BD
Microtainer SST tubes. The tubes were left at room temperature for approximately 30 min
and centrifuged for 5 min (5000 rpm, 25
◦
C, Eppendorf mini spin, F-45-12-11). The serum
was then frozen at
−
40
◦
C until analysis. Additional blood plasma samples for GLP-1,
GIP, PYY, and ghrelin analyses were collected in BD Microtainer K2E tubes. An inhibition
cocktail consisting of DPP-4 inhibitor (10
µ
L/mL blood) (Millipore, St. Charles, MO, USA)
and aprotinin (50
µ
L/mL blood) (Sigma-Aldrich, St. Louis, MO, USA) was added to the
tube. The tubes were kept on ice before and after sampling, and then centrifuged for
10 min
(4200 rpm, 4
◦
C) immediately after collecting the blood. Plasma samples were then frozen
at −40 ◦C until analysis.
The determination of serum insulin concentrations was performed using a solid phase
two-site enzyme immunoassay kit (Insulin ELISA 10-1113-01, Mercordia AB, Uppsala,
Sweden). FFA concentrations were analyzed with an enzymatic colorimetric method with
a 96 microplate (NEFA-HR (2) ACS-ACOD method, FUJIFILM Wako Chemicals Europe
GmbH, Neuss, Germany). Serum triglyceride concentrations were determined by using a
multi-sample enzymatic assay (LabAssay
™
Triglyceride 290-63701, GPO.DAOS method,
FUJIFILM Wako Chemicals Europe GmbH, Germany). The quantitative determination
of total plasma GLP-1, PYY, GIP, and Ghrelin concentrations was performed by using a
10 spot U-plex assay kit (Meso Scale Diagnostics LLC, Rockville, MD, USA).
A 100 mm visual analogue scale (VAS) was used to rank the subjective appetite
variables satiety, hunger, and desire to eat. The left end of the VAS scale represented not at
all (e.g., hungry), and right end of the scale represented extremely. The participants were
told to rank the scale at every blood sampling point.
2.6. Statistical Analysis
Data are expressed as means
±
SEM. A trapezoid model was used to calculate the
incremental areas and areas under the curves (iAUCs and AUCs, respectively) for each
subject and test meal. The iAUCs were used for statistical evaluations of blood glucose
and insulin concentrations. Results presenting iAUCs of postprandial glucose and insulin
responses after the standardized lunch (210–330 min) were calculated by considering the
glucose concentrations prior to lunch (time = 210 min) as baseline. AUCs were used to
present the results of appetite sensations, triglycerides, free fatty acids, ghrelin, GLP-1,
PYY, and GIP. The plotting of graphs and calculations of areas was performed in GraphPad
Prism (version 8.0, GraphPad Software, San Diego, CA, USA).
Randomization of the consumption order of the test meals was performed by using
random tools of Microsoft Excel (Washington, DC, USA). Differences in the test variables
between the products (‘Meal’: NL, RSO, PLL, and PLH) at different time points during the
experimental day (‘Time’) were evaluated using a mixed model (PROC MIXED in SAS re-
lease 9.4; SAS Institute Inc., Cary, NC, USA) with repeated measures and an autoregressive
covariance structure for the test variables. Subjects were modelled as a random variable,
and the corresponding baseline (fasting values) was modelled as the covariate. The effects
of the test meals on physiological responses were evaluated using ANOVA (general linear
model), followed by Tukey’s pairwise multiple comparison in MINITAB Statistical Software
(version 18, Minitab, Minitab Inc., State College, PA, USA). Box Cox transformation was
performed on the data prior to ANOVA analysis if the residuals were distributed unevenly
(tested with Anderson–Darling, where p< 0.05 was considered unevenly distributed).
If the value from a test subject was missing for one of the products, the test subject was
excluded from the statistical evaluation of that specific test variable. Two subjects failed to
follow the instructions at ranking appetite sensations, and these subjects were therefore
excluded from the statistical analysis (n= 18). Due to missing samples, two subjects were
excluded from GIP calculations (n= 18). The significance level was set at a p-value < 0.05.

Nutrients 2021,13, 988 5 of 16
3. Results
3.1. Postprandial Glucose and Insulin Responses after Consuming the Test Meals at Breakfast and
Following the Standardized Lunch
3.1.1. Evaluation of Acute Postprandial Glycemic Properties of the NL
To gain knowledge about the glycemic properties of the NL preparation, the post-
prandial (iAUC = 0–120 min) and second meal (iAUC = 210–330 min) glucose and insulin
responses after the NL consumed at breakfast were compared with the responses after a glu-
cose solution, containing similar amounts of available carbohydrates (42 g). No main effects
of products on glucose (Figure 1) and insulin responses during the experimental session
were detected between intake of the glucose solution and NL at breakfast. There were no
differences at fasting prior to consumption of the glucose solution and the NL with respect
to glucose concentrations (5.06
±
0.07 and 4.91
±
0.11 mmol/L, respectively,
p> 0.05
) or
insulin concentrations (0.040
±
0.004 and 0.0410
±
0.004 nmol/L, respectively,
p> 0.05
). No
significant differences between the glucose solution and the NL were observed regarding
glucose responses (162
±
13 and 149
±
16 mmol*min/L, respectively,
p> 0.05
) and insulin
responses (17.43
±
1.84 and 18.10
±
1.85 nmol/L, respectively,
p> 0.05
) in the postpran-
dial period after intake at breakfast (iAUC = 0–120 min). Neither were there significant
differences after the standardized lunch (iAUC = 210–330 min) between glucose and NL
breakfasts with respect to glucose responses (210.3
±
24.0 and
231.8 ±19.1 mmol*min/L
,
p> 0.05
) and insulin responses (21.24
±
2.25 and 19.74
±
2.32 nmol/L, respectively,
p> 0.05
)
(Figure 1).
Figure 1.
Incremental changes in serum blood glucose concentrations after test breakfasts and
standardized lunch meals. Values are means
±
SEM, n= 20 healthy subjects. Repeated measures;
mixed model in SAS. NL, oat preparation without added oat polar lipids; glucose, glucose solution.
Since no differences were observed between the glucose solution and NL with respect
to postprandial glucose and insulin responses, only NL was included in further evaluations.
3.1.2. Evaluation of the Lipid-Supplemented Oat Preparations with Respect to
Postprandial (Breakfast) and Second Meal (Lunch) Glucose and Insulin Responses
The results revealed significant main effects of meals on blood glucose responses
and meal*time interactions (Figure 2). Lower postprandial blood glucose was observed
after the test meal PLL and PLH compared to NL (p< 0.05) (iAUC = 0–120 min). In
addition, the glucose iAUC (0–120 min) after the breakfast meal with PLH was lower

Nutrients 2021,13, 988 6 of 16
compared to RSO (p< 0.01). Regarding the glycemic response to the standardized lunch
(
iAUC = 210–330 min
), PLH breakfast resulted in significantly lower glycemic response
compared with the breakfasts containing NL (p< 0.001), PLL (p< 0.01), and RSO (p< 0.001,
Table 3).
Figure 2.
Incremental changes in serum blood glucose concentrations after test breakfasts and
standardized lunch meals. Values are means
±
SEM, n= 20 healthy subjects. Repeated measures;
mixed model in SAS. NL, oat preparation without added lipids; RSO, oat preparation added with
rapeseed oil; PLL, oat preparation with a low concentration of polar lipids; PLH, oat preparation
with a high concentration of polar lipids.
Table 3.
Blood glucose and insulin concentrations at fasting and after consumption of test meals at breakfast, followed by a
standardized lunch meal 1.
Test Variables NL RSO PLL PLH
%∆2%∆2%∆2
Glucose
Fasting blood glucose (mmol/L) 4.91 ±0.11 a4.85 ±0.10 a−1.22 4.96 ±0.09 a1.01 4.99 ±0.09 a1.62
Blood glucose prior to std. lunch
(at 210 min) (mmol/L) 4.4 ±0.11 a4.8 ±0.12 a8.07 4.9 ±0.08 a11.65 5.0 ±0.12 a12.78
Blood glucose iAUC = 0–120 min
(mmol*min/L) 149 ±16.3 a136 ±16.4 ab −8.45 106 ±11 bc −28.30 85 ±12.9 c−42.58
Blood glucose iAUC =
210–330 min (mmol*min/L) 231.8 ±19.1 a232.1 ±23.3 a0.12 223.3 ±21.1 a−3.66 166.4 ±19.6 b−28.21
Blood glucose iAUC = 0–330 min
(mmol*min/L) 335.5 ±34.6 ab 413.5 ±39.5 a23.24 371.3 ±36.9 ab 10.67 293.9 ±42.9 b−12.39
Insulin
Fasting blood insulin (nmol/L) 0.041 ±0.004 a0.039 ±0.004 a−4.87 0.04 ±0.003 a−2.43 0.04 ±0.003 a−2.43
Blood insulin prior to std. lunch
(at 210 min) (nmol/L) 0.023 ±0.002 a0.030 ±0.002 a30.43 0.03 ±0.002 a30.43 0.041 ±0.007 a78.26
Insulin iAUC = 0–120
(nmol*min/L) 18.1 ±1.85 a16.3 ±1.8 ab −9.94 15.16 ±1.73 bc −16.24 12.51 ±1.24 c−30.88
Insulin iAUC = 210–330
(nmol*min/L) 19.74 ±2.32 a22.16 ±2.97 a12.66 24.83 ±3.51 a25.78 19.86 ±2.22 a0.60
Insulin iAUC = 0–330
(nmol*min/L) 38.44 ±4.04 ab 41.59 ±4.72 ab 8.19 42.39 ±5.14 a10.27 34.95 ±3.56 b−9.07
1
Data are presented as means
±
SEM, n= 20 healthy subjects. Values in the same row with different superscript letters are significantly
different, p< 0.05 (ANOVA, followed by Tukey’s test).
2
The percentage change is calculated as the difference from the NL. NL, oat
preparation without added lipids; RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low concentration of polar
lipids; PLH, oat preparation with a high concentration of polar lipids; iAUC, incremental area under the curve.

Nutrients 2021,13, 988 7 of 16
The main effects of meal and meal*time were also observed on insulin responses
during the experimental period (iAUC = 0–330 min; Figure 3). The breakfast postprandial
insulin responses (iAUC = 0–120 min) were significantly lower after PLH compared to NL
(p< 0.001) and RSO (p< 0.01). The insulin responses to the standardized lunch (iAUC
= 210–330 min) were similar regardless of the test meal consumed at breakfast (p> 0.05,
Table 3). No significant differences were observed concerning fasting glucose or fasting
insulin concentrations before the start of the breakfast meals (p> 0.05, Table 3).
Figure 3.
Postprandial incremental changes in blood serum insulin concentrations after test breakfasts
and standardized lunch meals. Values are means
±
SEM, n= 20 healthy subjects. Repeated measures;
mixed model in SAS. NL, oat preparation without added lipids; RSO, oat preparation added with
rapeseed oil; PLL, oat preparation with a low concentration of polar lipids; PLH, oat preparation
with a high concentration of polar lipids.
3.2. Triglycerides
Significant main effects of meals on TG and meal*time effects were found in the post-
prandial period after breakfast (0–210 min) (Figure 4). Intake of PLH resulted in lower TG
concentrations compared to RSO and PLL. The AUCs (0–210 min) were significantly higher
after RSO (p< 0.05) and PLL (p< 0.01) compared to after NL. At the end of the experimental
session (330 min), the concentration of TG was significantly lower after the RSO breakfast
compared with after the NL breakfast (p< 0.05, Table 4). No significant differences were
observed between fasting TG concentrations before the start of the breakfast meals (
p> 0.05
,
Table 4).

Nutrients 2021,13, 988 8 of 16
Figure 4.
Concentration of serum triglycerides (TGs) after the breakfast meal. Values are
means ±SEM,
n= 20 healthy subjects. Repeated measures; mixed model in SAS. NL, oat preparation
without added lipids; RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low
concentration of polar lipids; PLH, oat preparation with a high concentration of polar lipids.
Table 4. TG and FFA responses after breakfast (0–210 min) and a subsequent standardized lunch (210–330 min) 1.
Test variables NL RSO PLL PLH
%∆2%∆2%∆2
Triglycerides (TG)
Fasting TG (mmol/L) 0.70 ±0.04 a0.66 ±0.05 a−5.71 0.71 ±0.05 a1.428 0.66 ±0.04 a−5.714
TG = AUC 0–210 min
(mmol*min/L) 157.2 ±10.5 a203.2 ±20.6 b29.26 221.8 ±19.5 b41.09 187.4 ±13.9 ab 19.21
TG at 330 min (mmol/L) 0.89 ±0.05 a0.70 ±0.05 b−20.64 0.77 ±0.07 ab −12.93 0.75 ±0.05 ab −15.38
Free Fatty Acid
Fasting FFA (mmol/L) 0.45 ±0.03 a0.51 ±0.03 a13.33 0.43 ±0.03 a−4.44 0.52 ±0.04 a15.55
FFA = AUC 0–210 min
(mmol*min/L) 70.7 ±2.83 a91.94 ±3.34 b30.04 92.51 ±3.93 b30.84 80.92 ±2.9 c14.45
FFA = AUC 210–330 min
(mmol*min/L) 39.05 ±1.86 ab 44.65 ±2.19 a14.34 46.15 ±2.72 a18.18 36.04 ±1.85 b−7.70
1
Data are presented as means
±
SEM, n= 20 healthy subjects. Values in the same row with different superscript letters are significantly
different, p< 0.05 (ANOVA, followed by Tukey’s test).
2
The percentage change is calculated as the difference from the NL. NL, oat
preparation without added lipids; RSO, oat preparation added with rapeseed oil; PLL, oat preparation added with oat oil containing a low
concentration of polar lipids; PLH, oat preparation added with oat oil containing a high concentration of polar lipids; AUC, area under the
curve.
3.3. Free Fatty Acids
The results showed a significant main effect of meals as well as a meal*time effect
during the experimental period (Figure 5). The FFA AUCs (0–210 min) were significantly
lower after the PLH breakfast meal compared to RSO (p< 0.05) and PLL (p< 0.01). After
the standardized lunch, reduced FFA AUCs (210–330 min) were observed after the PLH
breakfast compared to PLL (p< 0.01) and RSO (p< 0.01). No significant differences in FFA
concentrations were observed at fasting prior to the start of the breakfast meals (p> 0.05,
Table 4).

Nutrients 2021,13, 988 9 of 16
Figure 5.
Concentrations of serum free fatty acid (FFAs) after breakfast and a standardized lunch
meal. Values are means
±
SEM, n= 20 healthy subjects. Repeated measures; mixed model in SAS.
NL, oat preparation without added lipids; RSO, oat preparation added with rapeseed oil; PLL, oat
preparation with a low concentration of polar lipids; PLH, oat preparation with a high concentration
of polar lipids.
3.4. Ghrelin
Figure 6shows main effects of meals and meal*time effects after the test breakfast
(0–210 min). The results revealed that the ghrelin concentrations were significantly lower
after breakfasts (0–210 min) composed of PLH compared to NL (p< 0.001). After the stan-
dardized lunch (330 min), no significant differences (p> 0.05) were observed between the
test meals. No significant differences were observed between fasting ghrelin concentrations
before the start of the breakfast meals (p> 0.05, Table 5).
Figure 6.
Mean concentrations of ghrelin after the breakfast meals. Values are means
±
SEM,
n= 20
healthy subjects. Repeated measures; mixed model in SAS. NL, oat preparation without added lipids;
RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low concentration of polar
lipids; PLH, oat preparation with a high concentration of polar lipids.

Nutrients 2021,13, 988 10 of 16
Table 5. Plasma GLP-1, PYY, Ghrelin, and GIP response after breakfast and lunch 1.
Test Variables NL RSO PLL PLH
%∆2%∆2%∆2
Fasting plasma Ghrelin (pg/mL) 3444.8 ±63.1 a518.4 ±89 a16.54 458.4 ±67.2 a3.05 441.6 ±65.8 a−0.719
Ghrelin AUC = 0–210 (pg*min/mL) 3
78,698
±
10,536
a
64,764
±
9599
b−17.70 66,503 ±9950
ab −15.49
58,184
±
7246
b−26.06
Plasma Ghrelin at 330 min (pg/mL) 3255.8 ±41 a251.7 ±38 a−1.60 226.5 ±36 a−11.45 232.4 ±22 a−9.14
Fasting plasma GLP-1 (pg/mL) 338.95 ±2.37 a47.86 ±5.63 a22.87 39.99 ±2.12 a2.67 45.18 ±4.06 a15.99
GLP-1 AUC = 0–210 (pg*min/mL) 310,345 ±726 a12,973 ±668 ab 25.40 14,731 ±825 bc 42.397
17,357
±
1050
c67.78
Plasma GLP-1 at 330 min (pg/mL) 352.9 ±4.14 a56.71 ±4.75 a7.20 59.93 ±6a13.28 79.83 ±6.55 b50.90
Fasting plasma PYY (pg/mL) 347.1 ±3.57 a43.65 ±3.04 a−7.32 43.3 ±3.21 a−8.06 42.55 ±3.72 a−9.66
PYY AUC = 0–210 (pg*min/mL) 310,066 ±802 a11,068 ±597 ab 9.95 12,594 ±1187
bc 25.11 13,972 ±893 c38.80
Plasma PYY at 330 min (pg/mL) 343.6 ±2.08 a44.48 ±3.52 a2.01 45.06 ±3.12 a3.34 58.33 ±4.09 b33.78
Fasting plasma GIP (pg/mL) 4134.1 ±18 a154 ±17.4 a14.83 160.8 ±25.3 a19.91 119.4 ±11.5 a−10.96
GIP AUC = 0–210 (pg*min/mL) 4
51,723
±
4651
a
98,274
±
13,425
bc 90.00 133,403 ±
13,243 c157.91 77,645 ±8641
ab 50.11
Plasma GIP at 330 min (pg/mL) 4354.2 ±125 a338.8 ±139 a−4.34 349.7 ±178 a−1.27 363.8 ±175 a2.71
1
Data are presented as means
±
SEM,
3
n= 20,
4
n= 18 healthy subjects. Values in the same row with different superscript letters are
significantly different, p< 0.05 (ANOVA, followed by Tukey’s test).
2
The percentage change is calculated as the difference from the NL. NL,
oat preparation without added lipids; RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low concentration of
polar lipids; PLH, oat preparation with a high concentration of polar lipids; AUC, area under the curve.
3.5. GLP-1
The results regarding GLP-1 are presented in Figure 7and Table 5. Significant meals
and meal*time effects were detected in the postprandial period after breakfast (
0–210 min
).
The GLP-1 concentrations (AUC = 0–210 min) were significantly increased after the break-
fast composed of PLH compared to NL (p< 0.001) and RSO (p< 0.001). In addition, PLH
breakfast resulted in increased GLP-1 concentrations in the end of the experimental period,
time = 330 min, compared to NL (p< 0.01), PLL (p< 0.05), and RSO (p< 0.01) breakfasts.
No significant differences were observed between fasting GLP-1 concentrations before the
start of the breakfast meals (p> 0.05).
Figure 7.
Mean concentrations of GLP-1 after the breakfast meal. Values are means
±
SEM, n= 20
healthy subjects. Repeated measures; mixed model in SAS. NL, oat preparation without added lipids;
RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low concentration of polar
lipids; PLH, oat preparation with a high concentration of polar lipids.

Nutrients 2021,13, 988 11 of 16
3.6. PYY
Results regarding PYY concentrations are presented in Figure 8and Table 5. The
results showed significant main effects of meal and significant meal*time in the postpran-
dial period after breakfast (0–210 min). The PYY concentrations after the PLH breakfast
(
AUC = 0–210 min
) were significantly higher compared to after the NL (p< 0.001) and RSO
breakfasts (p< 0.01). Additionally, at the end of the test period (330 min), the PLH breakfast
resulted in significantly higher concentrations of PYY compared to NL (p< 0.001), PLL
(p< 0.01), and RSO breakfasts (p< 0.001). No significant differences in the fasting PYY
concentrations were observed before the breakfast meals were served.
Figure 8.
Mean concentration of PYY after the breakfast meal. Values are means
±
SEM, n= 20
healthy subjects. Repeated measures; mixed model in SAS. NL, oat preparation without added lipids;
RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low concentration of polar
lipids; PLH, oat preparation with a high concentration of polar lipids.
3.7. GIP
Postprandial GIP responses after the breakfast and standardized lunch meals are
presented in the Figure 9and Table 5. Significant main effects of meal and meal*time
were observed in the postprandial period after breakfast (0–210 min), revealing higher GIP
concentrations after PLL compared to after PLH (p< 0.01) and NL (p< 0.001) breakfasts.
There were no significant differences in the fasting GIP concentrations before the breakfast
meals were served.
Figure 9.
Mean concentrations of GIP after intake of test meals at breakfast. Values are means
±
SEM,
n= 18 healthy subjects. Repeated measures; mixed model in SAS. NL, oat preparation without added
lipids; RSO, oat preparation added with rapeseed oil; PLL, oat preparation with a low concentration
of polar lipids; PLH, oat preparation with a high concentration of polar lipids.

Nutrients 2021,13, 988 12 of 16
3.8. Subjective Appetite Ratings
Appetite ratings after the meals and standardized lunches are presented in
Figure 10
and Supplementary Table S1. No significant differences in appetite ratings (desire to eat,
hunger, and satiety) were observed at fasting prior to the start of the breakfast meals
(
p> 0.05
), nor were significant differences detected in appetite variables depending on
meals after breakfast or after the standardized lunch (p> 0.05).
Figure 10.
Subjective appetite ratings after test breakfasts and standardized lunch meals. Values are means
±
SEM of
subjective appetite ratings (VAS) of (
a
) desire to eat, (
b
) hunger, and (
c
) satiety; n= 20 healthy subjects. Repeated measures;
mixed model in SAS. NL, oat preparation without added lipids; RSO, oat preparation added with rapeseed oil; PLL, oat
preparation with a low concentration of polar lipids; PLH, oat preparation with a high concentration of polar lipids.
4. Discussion
This study investigated the metabolic effects of oat polar lipids in an acute breakfast
and a second-meal standardized lunch meal setting. The dietary intake of polar lipids
varies widely depending on the choice of diet. It has been estimated that 1–10% of total
dietary lipids are polar lipids including all types of plant and animal sources, e.g., whole
grains, nuts, vegetable oil, dairy products, fish, and meat [
21
]. The effects of oat polar lipids
rich in glycolipids were compared with those of a widely used edible oil, i.e., rapeseed
oil [
22
], which contains low amounts of glycolipids (<1%) [
20
]. The results indicate that
supplementation of breakfast with oat polar lipids, particularly rich in galactosylacylglyc-
erols, has the potential to improve cardio-metabolic risk-associated variables and increase
the release of gut hormones in a 5.5 h time perspective after ingestion.
Ingestion of polar lipids of both animal and plant origins has previously been shown
to exert beneficial effects, e.g., with respect to inflammation and gut health. Most of these
studies have been conducted to investigate the effects of milk polar lipids, and only a few

Nutrients 2021,13, 988 13 of 16
studies have investigated the health effects of plant polar lipids [
19
,
23
–
29
]. These studies
were carried out using low doses of polar lipids (i.e., <3 g) [
23
–
26
,
28
], or not focusing
directly on their effects on postprandial glucose or insulin responses [
19
]. Therefore, to
our knowledge, the present work is the first to observe improved postprandial glycemic
regulation following the ingestion of a meal rich in oat polar lipids. Our results revealed
that the breakfast meal containing 12 g of polar lipids from oats (PLH) reduced both glucose
and insulin responses compared to rapeseed oil (RSO) or to an essentially fat-free breakfast
(NL). In addition, PLH decreased after-lunch postprandial TG and FFA compared to NL
and to RSO, respectively, as well as increased gut hormones involved in metabolic and
appetite regulation (GLP-1 and PYY) compared to RSO. The beneficial effects of PLH also
included an improved postprandial glycemic regulation and reduced FFA concentration
following a lunch meal consumed 3.5 h after breakfast. Increased secretion of GLP-1 and
PYY was also observed until the end of the experimental session (5.5 h). This constitutes
an important finding, since a diet rich in high glycemic impact foods is an established risk
factor for the development of T2D [30]. Furthermore, high levels of TG are an established
risk factor for CVD [
31
,
32
]. Thus, the results indicate that oat polar lipids have the potential
to improve multiple risk markers encompassed by the metabolic syndrome, and therefore
can be suggested to be protective against T2D and CVD.
In this study, oat polar lipids triggered the release of PYY and the incretin hormone
GLP-1 in the gut, both of which have important implications in glycemic and appetite
regulation. These hormones may be involved in a variety of mechanisms, including
reduction of the gastrointestinal motility and gastric emptying rate, and as signal molecules
in the gut–brain axis, resulting in satiety sensations. The results regarding the effects of
oat polar lipids on gut hormones are thus in line with the improved postprandial glucose
increments also observed here, both after breakfast and following lunch. Although fat
in general reduces the acute gastric emptying rate, this study shows that the PLH meal
has a more potent reducing effect on postprandial glucose than the other lipid-rich meals.
These results suggest that oat polar lipids effectively reduce the postprandial glycemia
after breakfast and a second meal.
The concentration of ghrelin was significantly lower after the PLH breakfast compared
to NL, but no significant differences were recorded between the lipid-containing products.
A possible reason for this apparent inconsistency could be the small number of participants
in the study, which might have been insufficient to detect significant differences. Neverthe-
less, only the PLH breakfast significantly reduced ghrelin concentrations compared to NL,
indicating a higher potential for polar lipids to reduce hunger sensations compared to the
other high-lipid products included in this study.
One possible underlying mechanism behind the increased concentrations of gut hor-
mones relates to slower hydrolysis or limited digestion of oat polar lipids compared to e.g.,
rapeseed triglycerides, resulting in a delayed absorption, and thus potentially increased
stimulation of gut hormones release (GLP-1 and PYY) throughout the gastrointestinal
tract. Such a hypothetical mechanism was already suggested by Ohlsson et al. [
19
], and
is supported by observations showing delayed enzymatic hydrolysis of polar lipids from
oat and other sources in
in vitro
models [
33
,
34
]. GIP was another gut hormone investi-
gated. Besides its initially described incretin action, a number of additional effects have
been reported for this hormone, the physiological importance of which is not yet clear.
Consequently, while GLP-1 is known to suppress the postprandial glucagon response, GIP
has been suggested to exert the opposite effect, i.e., to promote an enhanced response [
35
].
In addition GIP has also been shown to facilitate fat accumulation in adipocytes [
35
].
Interestingly, PLH promoted a lower GIP response than the RSO meal.
This study demonstrated that a breakfast meal containing 12 g of oat polar lipids
resulted in a significantly lowered concentration of FFAs at the time of the standardized
lunch meal. Similar observations were reported by Ohlsson et al. [
19
], and are in agreement
with a putative delayed hydrolysis of lipids and prolonged absorption time of the digestion
products. It could be suggested that the reduced late postprandial concentrations of serum

Nutrients 2021,13, 988 14 of 16
FFAs promoted by the polar lipids, as compared with the other test meals, contributed to the
improved glycemic response seen after lunch. Accordingly, it has been demonstrated that
elevated circulating concentrations of FFAs correlate with impaired insulin signaling [
36
]
and reduced glucose tolerance [
37
]. It is also in accordance with studies showing that
a meal supplemented with plant-derived diacylglycerol has the potential to improve
postprandial lipid profiles (by reducing VLDL cholesterol) and insulin sensitivity [
38
].
Reduced circulating concentrations of FFAs and TGs are important effects of dietary polar
lipids, since elevated concentrations are considered a cardiovascular risk factor [
32
,
39
,
40
].
However, the lower blood lipid concentration observed here after the intake of PLH
might also relate to differences in the actual TG concentration in the different oils tested.
All test meals (with the exception of the NL) contained 33 g of added lipids. However,
supplementation with PLH provides a significant proportion, 40%, of polar lipids and
approximately 60% TG, while the PLL contained only 4% polar lipids, and the remainder
were mainly TGs; RSO is essentially made of TGs. Therefore, the total amount of fatty acids
ingested, and thus potentially absorbable as substrates for endogenous TG formation, was
lower in the PLH breakfast.
A limitation in this study was the relatively low number of subjects, which may
have compromised the statistical power for some of the test variables. Another potential
limitation was the unbalanced gender ratio, since 15 out of 20 participants were women.
The combination of the breakfast products was formulated to evaluate the metabolic effects
of oat polar lipids included in a drink. It would be interesting to investigate the effects of
oat polar lipids added to more complex food matrices, e.g., a solid meal. The breakfast
meals containing added lipids should be considered as high-fat meals, since 60% of their
calorie content comes from dietary lipids. The reason for the high total fat content in
the investigated meals was the limited availability of more concentrated oat polar lipid
preparations. However, for future studies, we aim at including highly purified oat polar
lipids to reach the amounts needed to achieve metabolic effects, without significantly
increasing the total fat intake.
In summary, this study shows the beneficial effects of polar lipids from oats on post-
prandial glycemic regulation, blood lipids, and gut hormones in healthy volunteers, which
suggests antidiabetic and anti-obesogenic properties, with the potential to prevent cardio-
metabolic diseases. Further studies are needed to elucidate the underlying mechanisms
behind these promising health effects of oat lipids.
Supplementary Materials:
The following is available online at https://www.mdpi.com/2072-6643/
13/3/988/s1, Table S1: Subjective appetite ratings after breakfast and lunch.
Author Contributions:
Conceptualization: M.M.H., J.T., L.C., K.P., F.P., and A.N.; experiments and
formal analysis: M.M.H.; visualization: M.M.H.; draft preparation: M.M.H., J.T., and A.N.; review
and editing: M.M.H., J.T., L.C., M.T.S.F., K.P., F.P., and A.N. All authors have read and agreed to the
published version of the manuscript.
Funding:
This research was conducted within ScanOats, an industrial research center with an oat
focus. Financial support was received from the Swedish Foundation for Strategic Research (grant
number IRC15-0068).
Institutional Review Board Statement:
The ethical approval of the study was given by the Regional
Ethical Review Board in Lund, Sweden (Dnr. 2018/658) and the study was conducted according to
the guidelines laid down in the Declaration of Helsinki. The study was registered at ClinicalTrials.gov
(NCT03830736).
Informed Consent Statement:
Informed consent was obtained from all subjects involved in the
study.
Data Availability Statement:
The datasets analyzed during this study are available from the corre-
sponding author on reasonable request.

Nutrients 2021,13, 988 15 of 16
Acknowledgments:
We thank Oatly AB for preparing the test meals and Swedish Oat Fiber AB for
providing oat polar lipid preparations. We acknowledge all study participants for their cooperation.
We gratefully thank research engineer Olexandr Fedkiv, Hanaa Hussein, and Aishwarya Venkateshan
for practical assistance in the clinical trial.
Conflicts of Interest:
The authors declare no conflict of interest. Karin Petersson and Frederic
Prothon work for Oatly AB.
References
1.
Saeedi, P.; Petersohn, I.; Salpea, P.; Malanda, B.; Karuranga, S.; Unwin, N.; Colagiuri, S.; Guariguata, L.; Motala, A.A.; Ogurtsova,
K.; et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the
International Diabetes Federation Diabetes Atlas, 9th edition. Diabetes Res. Clin. Pract. 2019,157, 107843. [CrossRef]
2.
Jane, M.; McKay, J.; Pal, S. Effects of daily consumption of psyllium, oat bran and polyGlycopleX on obesity-related disease risk
factors: A critical review. Nutrition 2019,57, 84–91. [CrossRef]
3.
Maki, K.C.; Beiseigel, J.M.; Jonnalagadda, S.S.; Gugger, C.K.; Reeves, M.S.; Farmer, M.V.; Kaden, V.N.; Rains, T.M. Whole-grain
ready-to-eat oat cereal, as part of a dietary program for weight loss, reduces low-density lipoprotein cholesterol in adults with
overweight and obesity more than a dietary program including low-fiber control foods. J. Am. Diet. Assoc.
2010
,110, 205–214.
[CrossRef] [PubMed]
4.
Lina, G.; Li-Tao, T.; Liya, L.; Kui, Z.; Ju, Q.; Sumei, Z. The cholesterol-lowering effects of oat varieties based on their difference in
the composition of proteins and lipids. Lipids Health Dis. 2014,13, 13–30. [CrossRef]
5.
Menon, R.; Gonzalez, T.; Ferruzzi, M.; Jackson, E.; Winderl, D.; Watson, J. Oats-From Farm to Fork. Adv. Food Nutr. Res.
2016
,77.
[CrossRef]
6. Meydani, M. Potential health benefits of avenanthramides of oats. Nutr. Rev. 2009,67, 731–735. [CrossRef]
7.
Sang, S.; Chu, Y. Whole grain oats, more than just a fiber: Role of unique phytochemicals. Mol. Nutr. Food Res.
2017
,61. [CrossRef]
[PubMed]
8.
Joyce, S.A.; Kamil, A.; Fleige, L.; Gahan, C.G.M. The Cholesterol-Lowering Effect of Oats and Oat Beta Glucan: Modes of Action
and Potential Role of Bile Acids and the Microbiome. Front. Nutr. 2019,6, 171. [CrossRef]
9.
Wu, J.R.; Leu, H.B.; Yin, W.H.; Tseng, W.K.; Wu, Y.W.; Lin, T.H.; Yeh, H.I.; Chang, K.C.; Wang, J.H.; Wu, C.C.; et al. The benefit of
secondary prevention with oat fiber in reducing future cardiovascular event among CAD patients after coronary intervention.
Sci. Rep. 2019,9, 3091. [CrossRef]
10.
EFSA Panel on Dietetic Products Nutrition and Allergies. Scientific Opinion on the substantiation of a health claim related to oat
beta glucan and lowering blood cholesterol and reduced risk of (coronary) heart disease pursuant to Article 14 of Regulation (EC)
No 1924/2006. EFSA J. 2010,8, 1885. [CrossRef]
11.
EFSA Panel on Dietetic Products Nutrition and Allergies. Scientific Opinion on the substantiation of health claims related to
beta-glucans from oats and barley and maintenance of normal blood LDL-cholesterol concentrations (ID 1236, 1299), increase in
satiety leading to a reduction in energy intake (ID 851, 852), reduction of post-prandial glycaemic responses (ID 821, 824), and
“digestive function” (ID 850) pursuant to Article 13(1) of Regulation (EC) No 1924/2006. EFSA J. 2011,9, 2207. [CrossRef]
12.
Doehlert, D.C.; Moreau, R.A.; Welti, R.; Roth, M.R.; McMullen, M.S. Polar Lipids from Oat Kernels. Cereal Chem.
2010
,87, 467–474.
[CrossRef]
13.
Hamberg, M.; Liepinsh, E.; Otting, G.; Griffiths, W. Isolation and structure of a new galactolipid from oat seeds. Lipids
1998
,33,
355–363. [CrossRef] [PubMed]
14.
Leonova, S. Department of Plant Breeding, Swedish University of Agricultural Sciences: Alnarp, Sweden, 2013.Lantbruksuniver-
sitet stitutionen för, v. In Lipids in Seeds of Oat (Avena spp.), a Potential Oil Crop: Content, Quality, Metabolism, and Possibilities for
Improvement; Department of Plant Breeding, Swedish University of Agricultural Sciences: Alnarp, Sweden, 2013.
15.
Moreau, R.A.; Doehlert, D.C.; Welti, R.; Isaac, G.; Roth, M.; Tamura, P.; Nuñez, A. The identification of mono-, di-, tri-, and
tetragalactosyl-diacylglycerols and their natural estolides in oat kernels. Lipids 2008,43, 533–548. [CrossRef]
16. Wren, A.M.; Bloom, S.R. Gut hormones and appetite control. Gastroenterology 2007,132, 2116–2130. [CrossRef] [PubMed]
17.
Blaychfeld-Magnazi, M.; Reshef, N.; Zornitzki, T.; Madar, Z.; Knobler, H. The effect of a low-carbohydrate high-fat diet and
ethnicity on daily glucose profile in type 2 diabetes determined by continuous glucose monitoring. Eur. J. Nutr.
2020
,59,
1929–1936. [CrossRef]
18.
Yuan, Q.; Ramprasath, V.R.; Harding, S.V.; Rideout, T.C.; Chan, Y.M.; Jones, P.J. Diacylglycerol oil reduces body fat but does not
alter energy or lipid metabolism in overweight, hypertriglyceridemic women. J. Nutr. 2010,140, 1122–1126. [CrossRef]
19. Ohlsson, L.; Rosenquist, A.; Rehfeld, J.F.; Härröd, M. Postprandial effects on plasma lipids and satiety hormones from intake of
liposomes made from fractionated oat oil: Two randomized crossover studies. Food Nutr. Res. 2014,58. [CrossRef]
20.
Sosulski, F.; Zadernowski, R.; Babuchowski, K. Composition of polar lipids in rapeseed. J. Am. Oil Chem. Soc.
1981
,58, 561–564.
[CrossRef]
21.
Lordan, R.; Nasopoulou, C.; Tsoupras, A.; Zabetakis, I. The Anti-inflammatory Properties of Food Polar Lipids. In Bioactive
Molecules in Food; Mérillon, J.-M., Ramawat, K.G., Eds.; Springer International Publishing: Cham, The Netherlands, 2018;
pp. 1–34.
[CrossRef]
22. Carré, P.; Pouzet, A. Rapeseed market, worldwide and in Europe. OCL 2014,21, D102. [CrossRef]

Nutrients 2021,13, 988 16 of 16
23.
Christensen, L.P. Galactolipids as potential health promoting compounds in vegetable foods. Recent Pat. Food Nutr. Agric.
2009
,1,
50–58. [CrossRef] [PubMed]
24.
Cohn, J.S.; Kamili, A.; Wat, E.; Chung, R.W.S.; Tandy, S. Dietary Phospholipids and Intestinal Cholesterol Absorption. Nutrients
2010,2, 116–127. [CrossRef] [PubMed]
25.
Hou, C.-C.; Chen, Y.-P.; Wu, J.-H.; Huang, C.-C.; Wang, S.-Y.; Yang, N.-S.; Shyur, L.-F. A galactolipid possesses novel cancer
chemopreventive effects by suppressing inflammatory mediators and mouse B16 melanoma. Cancer Res.
2007
,67, 6907–6915.
[CrossRef]
26.
Sugawara, T.; Miyazawa, T. Beneficial effect of dietary wheat glycolipids on cecum short-chain fatty acid and secondary bile acid
profiles in mice. J. Nutr. Sci. Vitaminol. 2001,47, 299–305. [CrossRef] [PubMed]
27.
Ulivi, V.; Lenti, M.; Gentili, C.; Marcolongo, G.; Cancedda, R.; Cancedda, F.D. Anti-inflammatory activity of monogalactosyldia-
cylglycerol in human articular cartilage
in vitro
: Activation of an anti-inflammatory cyclooxygenase-2 (COX-2) pathway. Arthritis
Res. Ther. 2011,13, R92. [CrossRef]
28.
Weiland, A.; Bub, A.; Barth, S.W.; Schrezenmeir, J.; Pfeuffer, M. Effects of dietary milk- and soya-phospholipids on lipid-
parameters and other risk indicators for cardiovascular diseases in overweight or obese men—Two double-blind, randomised,
controlled, clinical trials. J. Nutr. Sci. 2016,5, e21. [CrossRef] [PubMed]
29.
Zheng, L.; Fleith, M.; Giuffrida, F.; O’Neill, B.V.; Schneider, N. Dietary Polar Lipids and Cognitive Development: A Narrative
Review. Adv. Nutr. 2019,10, 1163–1176. [CrossRef] [PubMed]
30.
Livesey, G.; Taylor, R.; Livesey, H.F.; Buyken, A.E.; Jenkins, D.J.A.; Augustin, L.S.A.; Sievenpiper, J.L.; Barclay, A.W.; Liu, S.;
Wolever, T.M.S.; et al. Dietary Glycemic Index and Load and the Risk of Type 2 Diabetes: A Systematic Review and Updated
Meta-Analyses of Prospective Cohort Studies. Nutrients 2019,11, 1280. [CrossRef] [PubMed]
31.
Hedayatnia, M.; Asadi, Z.; Zare-Feyzabadi, R.; Yaghooti-Khorasani, M.; Ghazizadeh, H.; Ghaffarian-Zirak, R.; Nosrati-Tirkani, A.;
Mohammadi-Bajgiran, M.; Rohban, M.; Sadabadi, F.; et al. Dyslipidemia and cardiovascular disease risk among the MASHAD
study population. Lipids Health Dis. 2020,19, 42. [CrossRef]
32.
Miller, M.; Stone Neil, J.; Ballantyne, C.; Bittner, V.; Michael, H.C.; Henry, N.G.; Anne, C.G.; William, J.H.; Marc, S.J.; Penny,
M.K.-E.; et al. Triglycerides and Cardiovascular Disease. Circulation 2011,123, 2292–2333. [CrossRef]
33.
Wattanakul, J.; Sahaka, M.; Amara, S.; Mansor, S.; Gontero, B.; Carrière, F.; Gray, D.
In vitro
digestion of galactolipids from
chloroplast-rich fraction (CRF) of postharvest, pea vine field residue (haulm) and spinach leaves. Food Funct.
2019
,10, 7806–7817.
[CrossRef] [PubMed]
34.
Yilmaz, J.L.; Adlercreutz, P.; Tullberg, C. Polar Lipids Reduce
in vitro
Duodenal Lipolysis Rate of Oat Oil and Liquid Oat Base
Products. Eur. J. Lipid Sci. Technol. 2021,123, 2000317. [CrossRef]
35.
Seino, Y.; Fukushima, M.; Yabe, D. GIP and GLP-1, the two incretin hormones: Similarities and differences. J. Diabetes Investig.
2010,1, 8–23. [CrossRef]
36.
Belfort, R.; Mandarino, L.; Kashyap, S.; Wirfel, K.; Pratipanawatr, T.; Berria, R.; Defronzo, R.A.; Cusi, K. Dose-response effect of
elevated plasma free fatty acid on insulin signaling. Diabetes 2005,54, 1640–1648. [CrossRef]
37.
Nilsson, A.C.; Ostman, E.M.; Holst, J.J.; Björck, I.M.E. Including Indigestible Carbohydrates in the Evening Meal of Healthy
Subjects Improves Glucose Tolerance, Lowers Inflammatory Markers, and Increases Satiety after a Subsequent Standardized
Breakfast. J. Nutr. 2008,138, 732–739. [CrossRef] [PubMed]
38.
Yanai, H.; Yoshida, H.; Tomono, Y.; Hirowatari, Y.; Kurosawa, H.; Matsumoto, A.; Tada, N. Effects of diacylglycerol on glucose,
lipid metabolism, and plasma serotonin levels in lean Japanese. Obesity 2008,16, 47–51. [CrossRef]
39.
Megson, I.L.; Whitfield, P.D.; Zabetakis, I. Lipids and cardiovascular disease: Where does dietary intervention sit alongside statin
therapy? Food Funct. 2016,7, 2603–2614. [CrossRef] [PubMed]
40.
Roche, H.M.; Gibney, M.J. Postprandial triacylglycerolaemia—Nutritional implications. Prog. Lipid Res.
1995
,34, 249–266.
[CrossRef]