Download Vinegar supplementation lowers glucose and insulin responses and

European Journal of Clinical Nutrition (2005) 59, 983–988
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ORIGINAL COMMUNICATION
Vinegar supplementation lowers glucose and insulin
responses and increases satiety after a bread meal in
healthy subjects
E Östman1*, Y Granfeldt1, L Persson1 and I Björck1
1
Applied Nutrition and Food Chemistry, Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden
Objective: To investigate the potential of acetic acid supplementation as a means of lowering the glycaemic index (GI) of a
bread meal, and to evaluate the possible dose–response effect on postprandial glycaemia, insulinaemia and satiety.
Subjects and setting: In all, 12 healthy volunteers participated and the tests were performed at Applied Nutrition and Food
Chemistry, Lund University, Sweden.
Intervention: Three levels of vinegar (18, 23 and 28 mmol acetic acid) were served with a portion of white wheat bread
containing 50 g available carbohydrates as breakfast in randomized order after an overnight fast. Bread served without vinegar
was used as a reference meal. Blood samples were taken during 120 min for analysis of glucose and insulin. Satiety was measured
with a subjective rating scale.
Results: A significant dose–response relation was seen at 30 min for blood glucose and serum insulin responses; the higher the
acetic acid level, the lower the metabolic responses. Furthermore, the rating of satiety was directly related to the acetic acid
level. Compared with the reference meal, the highest level of vinegar significantly lowered the blood glucose response at 30 and
45 min, the insulin response at 15 and 30 min as well as increased the satiety score at 30, 90 and 120 min postprandially. The
low and intermediate levels of vinegar also lowered the 30 min glucose and the 15 min insulin responses significantly compared
with the reference meal. When GI and II (insulinaemic indices) were calculated using the 90 min incremental area, a significant
lowering was found for the highest amount of acetic acid, although the corresponding values calculated at 120 min did not
differ from the reference meal.
Conclusion: Supplementation of a meal based on white wheat bread with vinegar reduced postprandial responses of blood
glucose and insulin, and increased the subjective rating of satiety. There was an inverse dose–response relation between the level
of acetic acid and glucose and insulin responses and a linear dose–response relation between acetic acid and satiety rating. The
results indicate an interesting potential of fermented and pickled products containing acetic acid.
Sponsorships: Dr P Håkansson’s foundation and Direktör Albert Påhlsson’s foundation for research and charity.
European Journal of Clinical Nutrition (2005) 59, 983–988. doi:10.1038/sj.ejcn.1602197; published online 29 June 2005
Keywords: acetic acid; vinegar; insulin; satiety; appetite; glycaemic index
*Correspondence: E Östman, Applied Nutrition and Food Chemistry,
Department of Food Technology, Engineering and Nutrition, Lund
University, PO Box 124, SE-221 00 Lund, Sweden.
E-mail: [email protected]
Guarantor: E Östman.
Contributors: YG made the design of the experiment with assistance
from EÖ and IB. LP did the blood sampling and analysis. YG was in
charge of the collection and analysis of data. EÖ had the primary
responsibility for writing the manuscript, but YG and IB provided
comments on several drafts. None of the authors had any conflicts of
interest.
Received 22 April 2004; revised 30 December 2004; accepted 13 May
2005; published online 29 June 2005
Introduction
Today, we see a rapid increase in obesity and diseases related
to the insulin resistance syndrome (IRS). The health costs
will rise profoundly, and it is a great challenge for the future
to find means to counteract this development. The quality
of the diet has been shown to play an important role in the
combat of metabolic disorders and one quality parameter
of dietary carbohydrates relates to the glycaemic index
(GI), which is used to classify the glycaemic responses to
carbohydrate rich foods (Jenkins et al, 1981). At this time
point, there is a substantial amount of evidence that a diet
Vinegar improves glucose tolerance and satiety
E Östman et al
984
characterized by a low GI has benefits in both prevention
and treatment of several diseases linked to the IRS, such
as cardiovascular disease (CVD) (Liu et al, 2000) and
type II diabetes (Salmerón et al, 1997a, b). New crosssectional data also indicate that such a diet is associated
with a lower prevalence of insulin resistance and metabolic syndrome (McKeown et al, 2004). Furthermore,
evidences are at hand suggesting a beneficial role of
low-GI foods adjunct to appetite regulation. Consequently,
studies have demonstrated either increased satiety,
delayed return of hunger or decreased ad libitum food
intake after low-GI compared with high-GI foods (Ludwig,
2000). However, the role of dietary GI in relation to the
increasing prevalence of overweight and obesity remains
unclear. A shortcoming regarding the implementation
of the GI concept is the lack of low-GI products on the food
market.
A range of factors is known to affect the GI of carbohydrate-rich foods connected either to the characteristics of the
raw material (ratio of amylose/amylopectin (Granfeldt et al,
1995), soluble fibre content (Braaten et al, 1991), inclusion
of intact cereal kernels (Liljeberg & Björck, 1994), etc.) or the
process (eg manufacturing process of pasta (Granfeldt et al,
1991), pumpernickel baking (Åkerberg et al, 1998) and
fermentation (Liljeberg et al, 1995)). Previous results have
shown that the presence of lactic acid lowers the GI of bread
(Liljeberg et al, 1995) as well as improves the glucose
tolerance at a subsequent high-GI meal (second-meal effect)
(Östman et al, 2002a). The mechanism for the glucoselowering action of lactic acid has been suggested to be due
to a lowered rate of starch hydrolysis in the upper small
intestine (Östman et al, 2002b). Other organic acids that
have been investigated in relation to GI include acetic and
propionic acids. Both these acids have shown to lower the
glucose response to bread meals (Liljeberg & Björck, 1998;
Darwiche et al, 2001), but in contrast to lactic acid, the
mechanism of action appears to be a lowered rate of gastric
emptying (Liljeberg & Björck, 1998; Darwiche et al, 2001).
Propionic acid is present in certain types of cheese and
is also used in low amount as a preservative, for example,
in bread products. Acetic acid is found in a range of food
products such as vinegar, dressings and pickled products.
It is also formed upon fermentation processes, such as
sourdough fermentation, and can be considered a constituent of a normal diet. The public interest for vinegar
has been increasing in the past few years, and new products
are currently being introduced in the market. In the
present study, the possible dose–response relationship
between the amount of acetic acid added to a bread meal
in the form of vinegar, and the glycaemic and insulinaemic responses were evaluated in healthy subjects. In
addition, the satiating effect of the different amounts of
vinegar as supplements to a white bread meal was evaluated.
The lower level of vinegar used in the present study is the
same as the one used in a former study by Liljeberg and
Björck (1998).
European Journal of Clinical Nutrition
Subjects and methods
Subjects and meals
A total of 12 healthy, nonsmoking volunteers, 10 women
and two men, aged 22.9 (s.e.m. ¼ 0.5) y, with normal body
mass indices (21.470.7 kg/m2) and without drug therapy
participated in the study. Besides a reference portion of white
wheat bread, three test meals containing an identical portion
of white wheat bread were served with 18, 23 or 28 g white
vinegar (6% acetic acid, Druvan, Eslöv, Sweden), which is
equivalent to 18, 23 and 28 mmol acetic acid in the
respective portions. The highest amount of acetic acid
corresponds with approximately 30 ml vinegar of this type.
The white wheat bread was baked according to Liljeberg
and Björck (1994) and was identical to the reference bread
normally used in the GI determinations in our laboratory.
The bread was soaked in the portion of vinegar before
ingestion, and the intake of vinegar was thus distributed
over the meal. All meals contained 50 g available starch. The
subjects were served the meals in random order at four
separate occasions. The tests were performed approximately
1 week apart and commenced at the same time in the
morning. All meals were consumed steadily and finished
within 12–14 min. Water (150 ml) and 150 ml tea or coffee
was served with each meal. The test subjects were allowed to
choose between these drinks at the first occasion and then
the same drink was retained through all the test meals.
Sampling and analysis
The subjects arrived at the laboratory in the morning after
an overnight fast. A fasting blood sample was taken and the
subjects feeling of hunger/satiety was rated on a subjective
rating scale before the meal was served. The rating scale was
bipolar and graded from 10, to represent extreme hunger,
to þ 10, to explain extreme satiety (Liljeberg et al, 1995).
After the breakfast, blood samples were taken at 15, 30, 45,
60, 90 and 120 min for analysis of glucose and at 15, 30,
45, 90 and 120 min for analysis of insulin. The feeling of
hunger/satiety was rated at 15, 30, 45, 70, 90 and 120 min
postprandially. Blood glucose concentrations were determined with a glucose oxidase peroxidase reagent and serum
insulin concentrations were determined with an enzyme
immunoassay kit (Mercodia AB, Uppsala, Sweden).
The Ethics Committee of the Faculty of Medicine at Lund
University approved the study.
Statistical analysis
The areas under the curves (AUCs) were determined for the
blood glucose, serum insulin and satiety score (GraphPad
Prism ver. 3.0; GraphPad Software, San Diego, USA). GI and II
(insulinaemic indices) were determined by calculating the
difference between the AUCs for the test meal and the
reference meal in percent, with each subject being their own
reference. All areas below the baseline were excluded from
the calculations. Values are presented as mean7s.e.m.
Vinegar improves glucose tolerance and satiety
E Östman et al
985
Subjects that rated their postprandial hunger lower than
the hunger at fasting, hence indicating no satiety after the
meal, were excluded from the calculations. All statistical
calculations were performed in MINITAB Statistical Software
(release 13 for Windows; Minitab Inc., State College, PA,
USA). Significances were evaluated with the general linear
model (analysis of variance) followed by Tukeýs multiple
comparisons test. Values of Po0.05 were considered significant. The dose–response relation between the level of acetic
acid and glucose, insulin or satiety AUC was evaluated with
linear regression in GraphPad Prism (ver. 3.0).
Table 1 Blood glucose levels and glycaemic indices (GIs) at 90 and
120 min in 12 healthy subjects at a breakfast with carbohydrate
equivalent portions of white wheat bread served with various amounts
of vinegar
Meal
White wheat bread (WWB)
WWB þ 18 g vinegar
WWB þ 23 g vinegar
WWB þ 28 g vinegar
GI 90 min
GI 120 min
100a
89.474.3ab
104.7711.2ab
76.877.9b
100a
96.275.6a
117.0715.8a
84.878.7a
Values within a column not followed by the same letter are significantly
different.
Results
When vinegar was served with the white wheat bread, the
glycaemic responses were significantly lower at 30 min
postprandially (Po0.05), compared with the reference meal
without vinegar (Figure 1). No differences were noted in
between the test meals with acetic acid at this time point.
At 45 min, the highest amount of vinegar still lowered the
glucose level (P ¼ 0.0540), compared with the reference. The
GI of the test meal with the highest amount of vinegar
(GI ¼ 77) was significantly lower than that of the reference
meal, using the 90 min areas for calculation (Table 1). When
GI was calculated using the AUC at 120 min no significant
differences were found between any of the meals. A negative
linear relation was found between 30 min blood glucose
levels and vinegar content of the test meal (r ¼ 0.47,
P ¼ 0.001).
The insulin responses at 15 min were significantly lower
for the high and intermediate levels of vinegar compared
with the reference meal (Figure 2). At 30 min, only the
highest amount of vinegar lowered the insulin level
significantly compared with the reference. The II of the
Figure 1 Mean blood glucose responses in 12 healthy subjects at a
breakfast with carbohydrate equivalent portions of white wheat
bread (’) served with 18 g(m), 23 g (.) and 28 g (E) of vinegar.
Values are presented as means (n ¼ 12) with bars indicating s.e.m.
Significant differences between glucose levels at certain time points
are indicated with letters (Po0.05).
Figure 2 Mean serum insulin responses in 12 healthy subjects at a
breakfast with carbohydrate equivalent portions of white wheat
bread (’) served with 18 g (m), 23 g (.) and 28 g (E) of vinegar.
Values are presented as means (n ¼ 12) with bars indicating s.e.m.
Significant differences between insulin levels at certain time points
are indicated with letters (Po0.05).
meal with highest amount of vinegar (II ¼ 78) was significantly lower than the reference, when using the 90 min
AUCs for calculation (Table 2). Calculating with the AUCs at
120 min, no significant differences in II were found between
any of the meals. When expressing the 30 min insulin
responses as a function of the vinegar content of the test
meal, a negative linear relation was found (r ¼ 0.44,
P ¼ 0.002).
The reference meal resulted in the lowest rating of satiety
(Figure 3). The satiety scores after the highest level of vinegar
were rated significantly higher than the reference at 30, 90
and 120 min after the meal. The score for the low and
intermediate levels of vinegar did not differ significantly
at any of the time points from either the reference or the
meal with a high amount of vinegar. The satiety AUC was
significantly larger for the meal with a high amount of
vinegar compared with that of the reference meal (Table 3). A
significant linear relation was found between the satiety
AUC and the acetic acid content of the test meals (r ¼ 0.41,
P ¼ 0.004). The satiety rating of the reference meal without
European Journal of Clinical Nutrition
Vinegar improves glucose tolerance and satiety
E Östman et al
986
Table 2 Serum insulin levels and insulinaemic indices (Is) at 90 and
120 min in 12 healthy subjects at a breakfast with carbohydrate
equivalent portions of white wheat bread served with various amounts
of vinegar
Meal
White wheat bread (WWB)
WWB þ 18 g vinegar
WWB þ 23 g vinegar
WWB þ 28 g vinegar
II 90 min
II 120 min
100a
102.8712.0ab
87.3711.2ab
77.8710.4b
100a
108.4711.4a
94.2712.7a
84.6711.3a
Values within a column not followed by the same letter are significantly
different.
Figure 3 Mean satiety scores in 11 healthy subjects at a breakfast
with carbohydrate equivalent portions of white wheat bread (’)
served with 18 g (m), 23 g (.) and 28 g (E) of vinegar. Values are
presented as means (n ¼ 10 (reference and 18 g vinegar) or 11 (23
and 28 g vinegar)) with bars indicating s.e.m. Significant differences
between satiety scores at certain time points are indicated with
letters (Po0.05).
Table 3 Area under curve (0–120 min) for satiety scores in healthy
subjects after a breakfast with carbohydrate equivalent portions of white
wheat bread served with various amounts of vinegar
Meal
n
Area under curve for satiety score
White wheat bread (WWB)
WWB þ 18 g vinegar
WWB þ 23 g vinegar
WWB þ 28 g vinegar
10
10
11
11
210745a
363738ab
435775ab
5127105b
Values within a column not followed by the same letter are significantly
different.
acetic acid had returned to the rating at fasting after 90 min,
whereas the meals with acetic acid maintained positive
ratings over the entire experimental period of 120 min
(Figure 3).
Discussion
The most important finding in the present study was that
addition of acetic acid/vinegar improved not only the
European Journal of Clinical Nutrition
postprandial blood glucose and insulin profiles, but also
the satiating effect of a meal based on white wheat bread.
With respect to satiety rating, the intake of acetic acid/
vinegar appeared not only to increase, but also to prolong
satiety. Furthermore, a significant dose–response relation
was found at 30 min postprandially for blood glucose and
serum insulin responses, indicating that the higher the acetic
acid level, the lower the metabolic response.
In previous work by Liljeberg and Björck (1998) with meals
based on white wheat bread, a 35% lowering of GI and II was
seen with 18 mmol acetic acid (20 g vinegar) when served as
a vinaigrette sauce. In the present study, the same amount of
acetic acid (18 mmol) lowered mean GI by 11% but without
reaching statistical significance, and with no effect on II. In
the study by Liljeberg and Björck (1998), the vinegar was
supplied as a vinaigrette sauce including water and olive oil
(8 g). Results from studies investigating the effect of fats with
various degrees of saturation on the blood glucose response
of a meal are conflicting (Gatti et al, 1992; MacIntosh et al,
2003). Consequently, it remains to be elucidated if the
combination of acetic acid and olive oil caused the more
potent lowering of the glycaemic response in the work by
Liljeberg and Björck (1998). However, in a recent study, the
addition of 15 g sunflower oil (62% PUFA, 26% MUFA and
12% SFA) had no effect on the glycaemic excursions
following a potato meal in healthy subjects (Johnsson,
Andersson, Granfeldt and Björck, unpublished data). Also,
in work by MacIntosh et al (2003) no differences in GI or II
were found for a meal with mashed potato and either butter
(SFA), sunola oil (MUFA) or sunflower oil (PUFA). Furthermore, Owen and Wolever (2003) concluded that a variation
of fat intake (nonhydrogenated-fat margarine: 41% PUFA,
41% MUFA and 14% SFA) across the normal range did not
significantly affect the glycaemic response to a white bread
meal.
The glucose-lowering effect of acetic acid/vinegar has also
been observed by other investigators. Johnston et al (2004)
reported that vinegar could significantly improve insulin
sensitivity in insulin resistant subjects. In a recent study by
Sugiyama et al (2003), the GI of a white rice meal was
lowered with 25–35% by adding either vinegar (11 g/portion)
or pickled cucumber (15 g vinegar/portion). Furthermore,
Brighenti et al (1995) found a 30% lowering of AUC for
glucose of 17 mmol acetic acid when served as a vinaigrette
together with sliced lettuce and white bread. In the latter
study, the suggested glucose-lowering effect was an inhibition of digestive amylases caused by the acid. However, in
vitro measurements of the rate of starch hydrolysis using a
simulated gastrointestinal model did not reveal any amylase
inhibition in the case of acetic acid containing bread
(Liljeberg et al, 1996). Moreover, as judged from studies in
healthy volunteers using paracetamol as a marker for the
gastric emptying rate, the presence of acetic acid appeared to
significantly reduce the gastric emptying rate, suggesting an
effect different from obstructed amylolysis (Liljeberg &
Björck, 1998). In a study by Ebihara and Nakajima (1988)
Vinegar improves glucose tolerance and satiety
E Östman et al
987
the administration of acetic acid improved the glycaemia in
rats and lowered the insulin response in humans significantly. No lowering effect on the glucose response was seen
in humans, but a postponed glucose peak and prolonged
time to reach the fasting level postprandially were registered
with the acetic acid containing meal. Also, in the rat study,
the glucose response showed a slower decrease in the late
postprandial phase in the presence of the acid, which is in
line with a mechanism related to a lowered gastric emptying
rate (Ebihara & Nakajima, 1988).
In studies from the 1960s and 1970s, the influence of
organic acids on gastric emptying was evaluated in both
humans (Hunt & Knox, 1969, 1972) and animals (Blum et al,
1976). In one of these early reports, Hunt and Knox (1972)
stated that the higher the molecular weights of weak acids,
the lower the potential of slowing gastric emptying. This
finding suggests that acetic acid (Mw ¼ 60 g/mol) would be
more effective than lactic acid (Mw ¼ 90 g/mol) in lowering
the gastric emptying rate. This is in accordance with results
from Liljeberg and Björck (1996, 1998) showing that the
presence of acetic acid but not lactic acid lowered the
postprandial appearance of paracetamol in the blood,
indicative of a delay in gastric emptying rate in the case of
acetic acid. In addition to organic acids, the rate of gastric
emptying can also be influenced by volume, caloric content,
viscosity, density and particle size of the gastric content
(Horowitz et al, 1994). Some peptides that are released in the
small intestine, such as cholecystokinin (CCK), amylin and
glucagon-like peptide-1 (GLP-1), have also been shown to
be involved in the regulation of the gastric emptying rate
(Hellström & Näslund, 2001; Feinle et al, 2002).
A difference between lactic- and acetic acid supplemented
bread meals, beyond their immediate glucose-lowering
effect, is that improved glucose tolerance at a subsequent
standardized meal (second meal effect) has only been
observed in meals with lactic acid (Östman et al, 2002a).
When acetic acid was served as a supplement to a white
bread breakfast meal, no effect on the glucose tolerance
was observed at the subsequent standardized lunch meal
(Liljeberg et al, 1999). In contrast, the presence of lactic acid
in a barley bread-based breakfast meal reduced glycaemia at a
subsequent standardized lunch meal by 25% (Östman et al,
2002a). The suggested mechanism for a second meal effect of
a low-GI food is that the prolonged digestive phase causes a
suppression of the plasma levels of free fatty acids (Wolever
et al, 1995). This may lead to improved insulin sensitivity at
the time of the next meal. The difference in the second meal
effect between low-GI foods may be related to the fact that
different gastrointestinal mechanisms may be responsible for
the slow release properties. Since a lowered gastric emptying,
and not a lowered starch digestion, causes the glucoselowering effect of acetic acid, it can be hypothesized that the
criteria for a second meal effect in the perspective from
breakfast to lunch depend mainly on a mechanism connected to a prolonged digestive phase. In animal studies,
Fushimi et al (2001) showed that acetic acid could activate
gluconeogensis and induce glycogenesis in the liver after
a fasting state. Furthermore, when Caco-2 cells (human
colonic carcinoma cells) were cultivated with acetic acid for
15 days, Ogawa et al (2000) showed that acetic acid
suppresses the increase in disaccharidase activity (sucrase,
maltase, trehalase and lactase). These two latter studies add
pieces of evidence to the knowledge on how acetic acid
affects glucose absorption and metabolism, but more
research is needed to understand the importance of each
physiological phenomenon.
There is currently an ongoing discussion concerning the
need to standardize the GI methodology. One potentially
interesting issue for ranking of carbohydrate characteristics
relates to the time interval used for the calculation of GI. In
the present study, there are important differences between
glucose and insulin responses to the vinegar containing
meals and the reference meal in the early postprandial phase
(15–30 min). Despite these lowering effects of vinegar, a
difference in GI and II is only significant for the meal with
the highest amount of vinegar at 90 min and not at 120 min.
This suggests that the ranking of products may be slightly
different depending on the time period used. In fact,
products with an extended digestive phase and with low
but sustained increments in blood glucose may produce a
substantial late glycaemic area, thus evening out differences
in incremental areas compared with the rapidly digested
and absorbed starch in the wheat bread reference. This has
previously been shown to be the case with pasta (Granfeldt
et al, 1991).
In the present study, the meal with the highest amount
of vinegar also increased the late postprandial satiety more
than two-fold, compared with the reference meal. None of
the former articles on meal supplementation with vinegar
have evaluated satiety, so the current finding adds new
knowledge both to the specific effect of vinegar on satiety
and to the more general relation between GI and satiety,
suggesting that low-GI foods can produce not only a higher
satiety, with potential effects on food intake, but also
prolong the duration of satiety, which may influence the
voluntary intake at a subsequent meal.
Significant dose–response relations between the amount of
added vinegar and the glucose, insulin or satiety responses
were found based on the 30 min values in the present study.
The highest amount of acetic acid used in the present study
corresponds to approximately 30 ml of vinegar. This is a level
comparable with that of acetic acid in a portion of
pumpernickel bread (GI ¼ 68, II ¼ 63) previously tested in
our laboratory (Liljeberg & Björck, 1994). However, a similar
amount of acetic acid served as a salad dressing, as pickled
vegetables may be difficult to ingest. The selection of pickled
and fermented products or meal additives, and the use of
vinegar-based drinks, which are currently introduced in the
market, may provide means to reach efficient levels of acetic
acid. Addition of vinegar to carbohydrate-rich meals of highGI character, or the use of, for example, homofermentative,
acetic acid producing starter cultures offers a potential to
European Journal of Clinical Nutrition
Vinegar improves glucose tolerance and satiety
E Östman et al
988
lower the GI and increase the postmeal satiety. The possible
long-term health benefits of including pickled products or
fermented products in the diet need to be examined.
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