The fiber and/or polyphenols present in lingonberries null the

glycemic effect of the sugars present in the berries when

consumed together with added glucose in healthy
human volunteers
Kaisa M. Linderborg
a,

, Riikka Jrvinen
a
, Henna-Maria Lehtonen
a
,
Matti Viitanen
b, c
, Heikki P.T. Kallio
a
a
Department of Biochemistry and Food Chemistry, University of Turku, Turku, Finland
b
Department of Geriatrics, University of Turku, Turku City Hospital, Turku, Finland
c
Karolinska Institutet, Karolinska University Hospital Huddinge, Stockholm, Sweden
A R T I C L E I N F O A B S T R A C T
Article history:
Received 18 October 2011
Revised 7 June 2012
Accepted 8 June 2012
This study was undertakenon the broad hypothesis that lingonberry (Vacciniumvitis-idaea L.)
has potential to reduce postprandial glycemic and lipemic response. More specifically, 2
postprandial crossover studies with healthy normal-weight male subjects were conducted
to study the influence of commercial lingonberry powder on postprandial glycemia and
lipemia. The test meals contained fat-free yoghurt with either glucose (50 g) or
triacylglycerols (35 g) with or without (control) the lingonberry powder. The lingonberry
powder provided the meals with a known amount of fiber and a known amount and
composition of sugars, and it was a rich source of polyphenols. Postprandial glucose, insulin,
and triacylglycerol responses were analyzed. There were no significant differences in the
postprandial glucose concentration between the meals in the glycemia trial despite the fact
that the lingonberry meal contained more glucose and fructose. When the meal did not
contain added sugar but, instead, added triacylglycerol, no glycemia or lipemia-lowering
effect was detected. On the contrary, there were indications of higher glycemic and
insulinemic effect after the lingonberry meal. The results of this study indicate that the
fibers and/or polyphenols present in lingonberries null the glycemic effect of the sugars
present in the berries when consumed together with added glucose. By contrast, the
lingonberry powder did not affect the postprandial lipemic response.
2012 Elsevier Inc. All rights reserved.
Keywords:
Lingonberry
Glycemia
Lipemia
Polyphenols
Men
1. Introduction
Lingonberry (Vaccinium vitis-idaea L.) is a wild, semiwoody
chamaephyte that keeps its leaves through the winter and
commonly grows at the northern latitudes. Edible fruits of
lingonberries are the most abundantly picked wild berries in
many Eurasian countries, and they are commercially used in a
wide range of products. Among other northern berries,
lingonberry is associated with a number of bioactive com-
pounds such as phenolics, lignans, vitamins C, inositols,
N U T R I T I O N R E S E A R C H 3 2 ( 2 0 1 2 ) 4 7 1 4 7 8
Corresponding author. Department of Biochemistry and Food Chemistry, University of Turku, FI-20014 Turku, Finland. Tel.: +358 2 333 6874.
E-mail address: kaisa.linderborg@utu.fi (K.M. Linderborg).
0271-5317/$ see front matter 2012 Elsevier Inc. All rights reserved.
doi:10.1016/j.nutres.2012.06.004
Avai l abl e onl i ne at www. sci encedi r ect . com
www. nr j our nal . com
triacylglycerols, glycerophospholipids, fatty acids, tocoph-
erols, phytosterols [1], and fibers including pectin, cellulose,
lignin, and cuticular polymers [2].
On the whole, berries contain a wide range of phenolic
compounds in different conjugated forms. From lingon-
berries, a total of 28 different phenolic compounds have
been identified [3]. Based on the weight of the aglycone,
anthocyanidins, mainly cyaniding-containing compounds, as
well as proanthocyanidins represent most phenolic com-
pounds in lingonberries, followed by mainly quercetin-
containing flavonols [1]. Although cyanidin-3-galactoside,
cyaniding-3-glucoside, and cyaniding-3-arabinoside are the
most abundant anthocyanins in lingonberries, the most
abundant flavonols are quercetin glycosides followed by
kaemferol glycosides [3].
It is likely that polyphenols affect the glucose metabolism
via a multifaceted mechanism. Many polyphenols have
inhibited intestinal -glucosidase activity or glucose transport
in vitro and suppressed the elevation of blood glucose
concentration after oral administration of glucose in animal
models, as reviewed by Hanhineva et al [4]. Phytochemicals
found in grapes or grape plantderived products have shown
inhibitory effects in the chemically induced diabetic models,
possibly via reducing oxidative stress in the pancreas and
aiding in the preservation of the -cell mass [5]. Recently, the
administration of polyphenols was associated with the
prevention of fatty lipid disease in mice possibly at least via
the activation of 5-adenosine monophosphateactivated
protein kinase [6].
The mechanisms through which berries could attenuate
lipemia remain speculative. In the case of grape seed
procyanidins, the suggested mechanism has been the regula-
tion of bile acid pathway [7], whereas black tea polyphenols
have been indicated to suppress the lymphatic transport of
dietary fat [8]. In an in vitro trial, apple, but not wine,
polyphenol extract decreased the enterocyte secretion of
lipoproteins [9]. The cardioprotective potential of cranberries
has been reviewed, and one of the suggested mechanisms is
the decrease of the amount of oxidized low-density lipopro-
tein in human plasma [10]. In addition to polyphenols,
different dietary fibers influence the postprandial glucose
and lipid response at least via the gastric-emptying rates [11].
In humans, mixed berries have been found to suppress
postprandial hyperglycemia [12,13], and we have reported the
beneficial effects of seabuckthornonpostprandial glucose and
insulin response [14]. The inclusion of cinnamon in a rice
pudding meal has lowered the postprandial glucose response
[15]. Regarding postprandial lipemia, we are aware of only 3
studies investigating the effects of berries or polyphenols on
human subjects; first, strawberry polyphenols were reported
to lower postprandial lipemia in overweight hyperlipidemic
men and women [16]; second, red wine polyphenols attenu-
ated postprandial chylomicron and chylomicron remnant
levels in postmenopausal women [17]; and third, our recent
study showed that sea buckthorn extraction residues delayed
postprandial lipemia [18]. Inanimals, black [8], oolong [19], and
green tea have found to decrease postprandial lipemia [20].
To our knowledge, the present study pioneers an investi-
gationinto the effects of the fibers and/or polyphenols present
in lingonberries in human subjects. More specifically, the aim
of the study was to assess how a commercial lingonberry
powder affects postprandial hyperglycemia, insulinemia, and
lipemia after either a high-glucose or a high-fat meal. We
hypothesized that the addition of fiber and polyphenol-
containing lingonberry powder could attenuate the glycemic
and lipemic responses to the meals. Fat-free yoghurt, glucose,
and canola oil were chosen as components of the study meal
to mimic a common use of lingonberries in Scandinavia.
Healthy young men were recruited as volunteers to establisha
starting point in postprandial lingonberry research.
2. Methods and materials
2.1. Subjects
Healthy normal-weight nonsmoking men aged between 18
and 40 years were recruited for the study. The subjects had
normal liver, kidney, and thyroid functions indicated by
plasma alanine aminotransferase level lower than 60 U/L,
creatinine level lower than 115 mol/L, and a thyroid-
stimulating hormone level of 0.3 to 4.2 mU/L.
Ten subjects were recruited for the glycemia trial and 13 for
the lipemia trial. All subjects finished the study. The baseline
characteristics of the subjects are explained in Table 1.
2.2. Study design
The study subjects acted as their own controls and consumed
the meals at a random order on 2 distinct study days, which
were at least 6 days apart from each other. Regarding the
evening preceding the study visits, the subjects were
instructed to eat a standardized evening snack with a low
flavonoid content, which consisted of wheat bread, cucumber,
water, and a banana. Before the study, the subjects were given
information about the investigation, and they had an oppor-
tunity to ask questions. They were also informed of their right
to discontinue the study at any time without explanation. All
subjects provided a written consent. The study was performed
in accordance with the ethical standards laid down in the
Declaration of Helsinki. The protocol was evaluated and
approved by the ethics committee of the Hospital District of
Southwestern Finland.
2.3. Study meal composition
The meals contained yoghurt (lactose-free and fat-free
nonflavored natural yoghurt, 200 g; Valio Ltd, Helsinki,
Table 1 Baseline characteristics of the male subjects
Glycemia Lipemia
Age (y) 24.7 4.6 25.6 5.0
BMI (kg/m
2
) 23.7 3.1 23.7 2.2
Fasting glucose (mmol/L) 5.25 0.28 5.08 0.36
Fasting triacylglycerols (mmol/L) 1.14 0.26 0.83 0.29
Values are means SD (n = 10 in the glycemia trial and n = 13 in the
lipemia trial). BMI, body mass index.
472 N U T R I T I O N R E S E A R C H 3 2 ( 2 0 1 2 ) 4 7 1 4 7 8
Finland), 2.5 dL of water, and commercial dried lingonberry
powder (Mahevi Ltd, Polvijrvi, Finland). The amount of the
lingonberry powder was 40 g in the glycemia trial and 60 g in
the lipemia trial. When converted to fresh lingonberries,
according to the typical water content of the berries, the dose
roughly corresponds to about 270 and 400 g of fresh
lingonberries. The powder was easily incorporated into the
yoghurt. In addition to the lingonberry powder, the meal in
the glycemia trial contained 50 g glucose, and the meal in the
lipemia trial contained 35 g canola oil (Raisio plc, Raisio,
Finland). The control meals contained the above ingredients
excluding the lingonberry powder. The composition of the
meals is presented in Table 2. The subjects were offered an
additional 0.5 L of water to be consumed during the 6-hour
postprandial period. The subjects were advised and moni-
tored to consume the water in a similar manner during both
study visits.
2.4. Lingonberry powder
Commercial lingonberry powder made of Finnish lingon-
berries was obtained from Mahevi Ltd. Whole lingonberries
were used in the drying and milling, but the slight juice loss
during the process was not compensated for. Therefore, the
lingonberry powder was richer in seeds and skin of the berries
compared with whole lingonberries.
The total amount of flavonol glycosides, the main flavo-
nols, sugars, and acids, as well as the amount of dietary fiber
in the dried lingonberry powder, was analyzed as explained in
the following sections.
2.5. Analysis and composition of flavonol glycosides
Flavonol glycosides were analyzed with a method previously
reported by the authors [14]. In short, the homogenized berry
product was extracted once with 0.1% trifluoroacetic acid
water (Fluka, Deisenhofen, Germany) and twice with 0.1%
trifluoroacetic acidmethanol. The flavonol glycosides were
eluted from solid phase extraction tubes (C18 500mg, Supelco,
Bellefonte, PA, USA) with solid-phase extraction tubes with
trifluoroacetic acidmethanolwater (40% of 0.1% trifluoroa-
cetic acidwater, 60% methanol). The samples were analyzed
with ultra-high-performance liquid chromatographytandem
mass spectrometry in the positive-ion mode. Syringetin-3-
glucoside (Extrasynthese, Genay, France) was used as an
internal standard and isorhamnetin-3-O-glucoside and iso-
rhamnetin-3-O-rutinoside (Extrasynthese) as external stan-
dards. The phenolic compounds of lingonberry have also
been characterized in detail elsewhere [3], and their avail-
ability in humans has been assessed [21]. The lingonberry
powder contained 0.22 g of flavonol glycosides per 100 g of
powder. The main flavonol glycosides were kemferol-3-
glucoside, quersetin-3-rhamnoside, quersetin-3-galactoside,
and quersetin-3-glucoside.
2.6. Analysis of sugars and acids
The sugars and acids were analyzed as trifluoroacetic acid
derivatives of dried juice samples by gas chromatography
equipped with a Supelco Simplicity-1fused silica column and
a flame ionization detector [22]. Reference compounds
D-fructose, D-quinic acid, and L-ascorbic acid were purchased
from Sigma Chemical Co (St Louis, MO, USA). D-Glucose and
D-sorbitol (internal standard for sugars) were purchased from
Fluka (Buchs, Switzerland). Malic acid and D-tartaric acid
(internal standard for acids) were purchased from Merck
(Darmstedt, Germany), and sucrose and citric acid were from
JT Baker (Deventer, the Netherlands).
2.7. Analysis of dietary fiber
The amount of dietary fiber was determined by an enzymatic-
gravimetric method [2325] that measures both soluble and
insoluble dietary fibers. In short, the food samples were
defatted, heated to gelatinize the starch, and then subjected to
enzymatic digestion by protease, amylase, and glucoamylase
to remove the digestible components of the food. The amount
of protein and ash was determined, and the sum was
subtracted from the total residue. The remaining matter was
taken as dietary fiber.
2.8. Clinical analysis
Blood was drawn from the forearm at the fasting state and at
30, 60, 90, 120, 180, 270, and 360 minutes postprandially.
Glucose (VF-053SFX; Oriola, Helsinki, Finland) and serum
tubes with coagulant activator (VF-054SPW) were used in the
glycemia trial and lithium heparin tubes (VF-054SPV; Oriola)
in the lipemia trial. All samples were stored at 80C before
analysis. Plasma triacylglycerol and glucose as well as serum
insulin were analyzed with standard biochemical analyses.
Serum glucose and triacylglycerol were determined by a
photometric method and insulin by an electrochemilumines-
cence immunoassay. All analytes were measured from a
single tube with Roche Modular PPEE analyzer, with commer-
cial reagents provided by Roche Diagnostics GmbH (Mann-
heim, Germany).
Table 2 Composition of meals given to men for the
glycemic and lipemia trials
Ingredient Glycemia meal Lipemia meal
Lactose-free, fat-free yoghurt 200 g 200 g
Glucose 5 g 5 g
Galactose 5 g 5 g
Fat 0.8 g 0.8 g
Glucose 50 g
Canola oil 35 g
Water 2.5 g 2.5 g
Lingonberry powder 40 g 60 g
Citric acid 2.0 g 3.0 g
Quinic acid 2.0 g 3.0 g
Malic acid 0.1 g 0.2 g
Fructose 7.3 g 11.0 g
Glucose 7.3 g 11.0 g
Dietary fiber 14.7 g 23.9 g
Flavonol glycosides 89 mg 133 mg
Details on the analysis of components and the lingonberry powder
are described in the Methods and materials. The control meal
included all ingredients excluding the lingonberry powder.
473 N U T R I T I O N R E S E A R C H 3 2 ( 2 0 1 2 ) 4 7 1 4 7 8
Fig The postprandial response of plasma glucose, insulin, and triacylglycerols to the study meal that contained glucose (A)
and to the study meal that contained triacylglycerols (B) with () and without () lingonberry powder (40 g in the glycemia trial
and 60 g in the lipemia trial). All meals included 200 g of lactose-free and fat-free yoghurt. Values are the mean (SD) of 10 male
subjects in the glycemia trial and the mean (SD) of 13 subjects in the lipemia trial. An asterisk (*) represents a significant
between meal differences (P < .05).
474 N U T R I T I O N R E S E A R C H 3 2 ( 2 0 1 2 ) 4 7 1 4 7 8
Fig (continued).
475 N U T R I T I O N R E S E A R C H 3 2 ( 2 0 1 2 ) 4 7 1 4 7 8
2.9. Statistical analyses
Normal distribution of the data was tested using the Shapiro-
Wilk test. Paired-samples t test or Wilcoxon matched-pairs
signed rank test, depending on the normality of the data, was
used to compare the measured responses to control. Areas
under the response curves were calculated for insulin values
of the glycemia trial from baseline to 180 and 360 minutes, as
well as triacylglycerol values in the lipemia trial from baseline
to 120, 180, and 360 minutes. Values were expressed as means
SD. Statistical significance was indicated by P < .05.
Statistical analyses were performed with SPSS 18.0 software
(SPSS Inc, Chicago, IL, USA).
3. Results
3.1. Glycemia
The primary result of this study indicates that there were no
significant differences to the responses of the 2 meals in the
glycemia trial, although the sugar content of the lingonberry
meal (64.7 g) was considerably higher than that of the control
meal (50 g). No significant differences were detected in the
plasma glucose concentrations, and the glucose curves were
almost identical. Lingonberry powder somewhat shifted the
shape of the insulin curve, but the effect was not significant
(P = .205 at peak concentration). There were no significant
differences in the incremental areas under the insulin curves.
No significant differences were detected in the plasma
triacylglycerol concentrations, whereas triacylglycerols were
insignificantly higher at every postprandial time point after
the lingonberry meal compared with the control meal.
3.2. Lipemia
The plasma glucose response was significantly higher after
the lingonberry meal compared with the control meal at 30
minutes (P = .003), 60 minutes (P = .022), and 90 minutes (P =
.011) postprandially (Fig).
The insulin values were elevated at every postprandial
time point after the lingonberry meal compared with the
control meal, and the time points of 90 minutes (P = .006), 120
minutes (P = .046), 180 minutes (0.002) and 270 minutes (P <
.001) were significant. The incremental area (0-360 minutes)
under the insulin curve was significantly larger after the
lingonberry meal (P = .008).
The areas under the triacylglycerol response curves did not
differ between the meals, but lingonberry caused a signifi-
cantly higher lipemia level at the 270-minute (P = .033) time
point compared with the control.
4. Discussion
In this study, the addition of 40 g of lingonberry powder
provided the meal of the glycemia trial, 16 g of fiber, and
14.7 g of sugars. However, an interesting finding was that
the glucose response was almost identical after both
glycemia meals despite the difference in the sugar content
(50 g in the control meal and 64.7 g in the lingonberry meal).
This seems to indicate that the sugars of the lingonberry
powder were compensated by a glycemia-lowering effect of
fibers and/or polyphenols. Furthermore, the insulin re-
sponse, although insignificant, supports the effect seen in
the glycemic response because it points to an attenuating
effect of the lingonberry.
By comparison to berries other than lingonberry, we
recently found that dried and crushed whole sea buckthorn
berries suppressed postprandial peak insulin response and
stabilized postprandial hyperglycemia compared with non
berry-containing control. Moreover, we found that the
removal of the supercritical carbon dioxidesoluble compo-
nents, mainly, triacylglycerols, sterol esters, wax esters, and
fat-soluble vitamins, from the berries did not cause a
significant change in the postprandial effects studied,
while the ethanol-soluble components showed advanta-
geous properties in both insulin and glucose responses
[14]. A complementary effect of polyphenols and fibers
was likely also in the current study, and this promotes the
use of berries or whole berry products instead of refined
polyphenol supplements.
When the meal did not contain added glucose but did
contain added lipids, the glycemia was higher at 3 time
points after the lingonberry meal, as might be expected from
the basis of the higher glucose content. Such effect was also
seen in the insulin values. Thus, the lingonberry powder
appears to delay the plasma triacylglycerol response to an
extent, but the only significant time point was at 270
minutes. By comparison, a very similar amount of dietary
fiber in sea buckthorn extraction residues was recently found
to delay postprandial lipemia [18]. The mechanism of the
delay may be mediated via gastric-emptying rates [26]. The
differences in the lipemia-lowering effects between straw-
berry [16] or red wine polyphenols [17], compared with the
lingonberry powder, may result from the polyphenol and
fiber content and source as well as from the age, weight, and
sex of the study subjects.
Recently, Khossousi et al [27] found in a study with
overweight men that the triacylglycerol response was signif-
icantly lowered by dietary psyllium fiber compared with a
low-fiber meal, and they concluded that a single acute dose of
dietary fiber can decrease arterial exposure to triacylglycerol
and modify chylomicron triacylglycerol responses in the
postprandial period. The somewhat deviating findings in the
present study can be explained by the nature of the fiber and
by the fact that our subjects were of normal weight, whereas
the subjects in the trial of Khossousi et al were overweight.
Because lingonberries have a rather low sugar-to-acid
ratio, they are most often consumed in a sweetened form.
The discrepancy of the glycemia-lowering effect in the
glycemia and lipemia trial may result from the sugar
content or composition, or from the difference of high-fat
and high-glucose meals in gastric-emptying rates. It has
previously been investigated if different simple sugars can
affect lipemia in different ways. The addition of glucose to
fatty test meals may or may not increase postprandial
lipemia in healthy subjects [2830], whereas the addition of
sucrose [31] or fructose [32] has been shown to increase
postprandial triacylglycerolemia.
476 N U T R I T I O N R E S E A R C H 3 2 ( 2 0 1 2 ) 4 7 1 4 7 8
We chose to conduct the study with a commercial
lingonberry product instead of whole crushed lingonberries,
or a supplement enriched in berry polyphenols, to better
mimic a real-life situation and to promote the commercial-
ization and advanced use of the northern berries. The dried
powder is a food rather than a supplement, and it is easy to
use, for example, blended in yoghurt or porridge. Moreover,
its manufacturing process is simple compared with supple-
ments enriched in polyphenols, and therefore, it is a more
economical product and a source of not only polyphenols but
also fiber.
Regarding the limitations of this study, we point out that it
involved only 4 meals. Therefore, a study in which a meal with
both glucose and lipid with and without lingonberries, a meal
with the lingonberry powder but without the added glucose, a
meal with sucrose instead of glucose, and a meal with
identical content and composition of sugars but different
content of lingonberry polyphenols and fibers would un-
doubtedly add our knowledge on the effect of lingonberry
polyphenols and fibers on postprandial glycemia and lipemia.
Furthermore, it might be interesting to study the effect of
other matrixes than the yoghurt and to perform a dose-
response study. Finally, the present deviations in insulin and
triacylglycerol values suggest that the effect of fiber and/or
polyphenols on lipemia should be studied in larger popula-
tions, albeit the number of human subjects used here is
typical for a postprandial crossover study.
Although prolonged postprandial lipemia has been asso-
ciated with the risk of future cardiovascular disease [3335],
repeated high postprandial insulin response and postpran-
dial hyperglycemia have been found to increase oxidative
stress [36], inflammation [37], and, possibly, insulin resis-
tance and -cell dysfunction [38]. Studies in the postprandial
state in humans are therefore important because most
Western individuals are in a postprandial state throughout
the day.
In conclusion, this study was launched on the broad
hypothesis that lingonberry has a beneficial effect on
human postprandial metabolism. The hypothesis was sup-
ported when postprandial glycemia was assessed, whereas
no effect was seen on postprandial lipemia. Overall, the
results of this study indicate that the fibers and/or poly-
phenols present in lingonberries null the glycemic effect of
the sugars that originate from the berries when consumed
together with added sugar. It can thus be argued that berries
should not be excluded from healthy diets despite their
sugar content.
Acknowledgment
The authors are grateful to the volunteers of the study for their
participation. Katja Oksa and Hannele Jokioinen are thanked
for their skilful technical assistance. Research grants from the
Finnish Food and Drink Industries' Federation (ETL), The Juho
Vainio Foundation, The Magnus Ehrnrooth Fund of the
Finnish Society of Sciences and Letters, EVO research funds
of Turku City Hospital, and Raisio Ltd ResearchFoundation are
acknowledged for their financial support. The authors declare
no conflicts of interest.
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