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The Effect of Nopal (Opuntia Ficus Indica) on Postprandial Blood Glucose, Incretins, and Antioxidant Activity in Mexican Patients with Type 2 Diabetes after Consumption of Two Different Composition Breakfasts

Authors:
  • Hospital Regional de Alta Especialidad Península de Yucatán
  • National Institute of Medical Sciencies and Nutrition

Abstract and Figures

Nopal is a plant used in traditional Mexican medicine to treat diabetes. However, there is insufficient scientific evidence to demonstrate whether nopal can regulate postprandial glucose. The purpose for conducting this study was to evaluate the glycemic index, insulinemic index, glucose-dependent insulinotropic peptide (GIP) index, and the glucagon-like peptide 1 (GLP-1) index, and the effect of nopal on patients with type 2 diabetes after consumption of a high-carbohydrate breakfast (HCB) or high-soy-protein breakfast (HSPB) on the postprandial response of glucose, insulin, GIP, GLP-1, and antioxidant activity. In study 1, the glycemic index, insulinemic index, GIP index, and GLP-1 index were calculated for seven healthy participants who consumed 50 g of available carbohydrates from glucose or dehydrated nopal. In study 2, 14 patients with type 2 diabetes consumed nopal in HCB or HSPB with or without 300 g steamed nopal. The glycemic index of nopal was 32.5±4, insulinemic index was 36.1±6, GIP index was 6.5±3.0, and GLP-1 index was 25.9±18. For those patients with type 2 diabetes who consumed the HCB+nopal, there was significantly lower area under the curve for glucose (287±30) than for those who consumed the HCB only (443±49), and lower incremental area under the curve for insulin (5,952±833 vs 7,313±1,090), and those patients with type 2 diabetes who consumed the HSPB avoided postprandial blood glucose peaks. Consumption of the HSPB+nopal significantly reduced the postprandial peaks of GIP concentration at 30 and 45 minutes and increased the antioxidant activity after 2 hours measured by the 2,2-diphenyl-1-picrilhidracyl method. These findings suggest that nopal could reduce postprandial blood glucose, serum insulin, and plasma GIP peaks, as well as increase antioxidant activity in healthy people and patients with type 2 diabetes.
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RESEARCH
Research and Practice Innovations
The Effect of Nopal (Opuntia Ficus Indica)on
Postprandial Blood Glucose, Incretins, and
Antioxidant Activity in Mexican Patients with
Type 2 Diabetes after Consumption of Two
Different Composition Breakfasts
Patricia López-Romero; Edgar Pichardo-Ontiveros; Azalia Avila-Nava, MSc; Natalia Vázquez-Manjarrez; Armando R. Tovar, PhD;
José Pedraza-Chaverri, PhD; Nimbe Torres, PhD
ARTICLE INFORMATION
Article history:
Accepted 19 February 2014
Keywords:
Nopal
Antioxidant activity
Diabetes
Glucose-dependent insulinotropic peptide (GIP)
Glycemic control
2212-2672/Copyright ª2014 by the Academy of
Nutrition and Dietetics.
http://dx.doi.org/10.1016/j.jand.2014.06.352
ABSTRACT
Nopal is a plant used in traditional Mexican medicine to treat diabetes. However, there
is insufcient scientic evidence to demonstrate whether nopal can regulate post-
prandial glucose. The purpose for conducting this study was to evaluate the glycemic
index, insulinemic index, glucose-dependent insulinotropic peptide (GIP) index, and the
glucagon-like peptide 1 (GLP-1) index, and the effect of nopal on patients with type 2
diabetes after consumption of a high-carbohydrate breakfast (HCB) or high-soy-protein
breakfast (HSPB) on the postprandial response of glucose, insulin, GIP, GLP-1, and
antioxidant activity. In study 1, the glycemic index, insulinemic index, GIP index, and
GLP-1 index were calculated for seven healthy participants who consumed 50 g of
available carbohydrates from glucose or dehydrated nopal. In study 2, 14 patients with
type 2 diabetes consumed nopal in HCB or HSPB with or without 300 g steamed nopal.
The glycemic index of nopal was 32.54, insulinemic index was 36.16, GIP index was
6.53.0, and GLP-1 index was 25.918. For those patients with type 2 diabetes who
consumed the HCBþnopal, there was signicantly lower area under the curve for
glucose (28730) than for those who consumed the HCB only (44349), and lower
incremental area under the curve for insulin (5,952833 vs 7,3131,090), and those
patients with type 2 diabetes who consumed the HSPB avoided postprandial blood
glucose peaks. Consumption of the HSPBþnopal signicantly reduced the postprandial
peaks of GIP concentration at 30 and 45 minutes and increased the antioxidant activity
after 2 hours measured by the 2,2-diphenyl-1-picrilhidracyl method. These ndings
suggest that nopal could reduce postprandial blood glucose, serum insulin, and plasma
GIP peaks, as well as increase antioxidant activity in healthy people and patients with
type 2 diabetes.
J Acad Nutr Diet. 2014;-:---.
THE CACTUS OPUNTIA, WHICH IS ALSO KNOWN AS
nopal, is native to central Mexico
1
and the pads are
eaten as a vegetable. Cactus plants have long served
as a source of food for people, and they have long
been used in traditional Mexican medicine for treating dia-
betes. Nopal is considered a functional food because it is a
proven source of dietary ber
2
and bioactive compounds
with antioxidant activity, such as avonoids, avonols, car-
otenes, and ascorbic acid,
3
in addition to being low in calo-
ries (27 kcal/100 g). The current epidemic of obesity and
diabetes has led to a search for functional foods that could
aid in ameliorating these pathologies. In the case of dia-
betes, consuming high-calorie meals can lead to exagger-
ated postprandial peaks in blood glucose and in lipids that
generate reactive oxygen species,
4,5
which results in inam-
mation
5
and endothelial dysfunction.
6
In addition, post-
prandial glucose homeostasis is controlled not only by
direct stimulation of insulin release by absorbed nutrients,
but also through secretion of incretin hormones, that is,
glucagon-like peptide-1 (GLP-1) and glucose-dependent in-
sulinotropic peptide (GIP).
7
These incretins are released
from enteroendocrine cells and are responsible for at least
50% of the total insulin
8
secreted after the ingestion of
food.
9
Therefore, the purpose of conducting this study was
rst to evaluate the glycemic index, insulinemic index, GIP
index, and GLP-1 index, and second, to evaluate the meta-
bolic effect of steamed nopal on postprandial peaks of
glucose, insulin, GIP, and antioxidant activity after the
ª2014 by the Academy of Nutrition and Dietetics. JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 1
consumption of a high-carbohydrate breakfast (HCB) or
high-soy-protein breakfast (HSPB).
MATERIALS AND METHODS
Ethics Statement
All of the procedures were conducted with an adequate un-
derstanding by, and the written consent of, the participants.
The study was approved by the Ethics Committee of Humans
by the Instituto Nacional de Ciencias Médicas y Nutrición and
was in compliance with the Declaration of Helsinki. The study
was registered in the Institutional Committee for Human
Biomedical Research (no. 118).
Participants
Two separate studies were performed using two separate
groups of participants. Study 1 was performed to determine
the glycemic index of nopal. This study included seven
healthy, nonsmoking, nonmedicated, normal-weight volun-
teers (three men and four women, meanstandard error of
mean [SEM]¼26.31.2 years of age), with a meanSEM body
mass index (calculated as kg/m
2
) of 23.50.8, according to
the recommendations of the Joint Food and Agricultural Or-
ganization of the United Nations/World Health Organization
Expert Consultation.
10
Study 2 was performed to evaluate the effect of nopal on
postprandial blood glucose after the consumption of two
different types of breakfasts. This study included 14 out-
patients (four men and 10 women) who were diagnosed with
type 2 diabetes with durations of <8 years. Patients with type
2 diabetes were treated with metformin only and were be-
tween 40 and 60 years old (meanSEM¼482.1 years of
age), with a body mass index <30 (meanSEM¼28.91).
They did not have dyslipidemia, hypertension, or severe
hypoglycemic episodes during the past year. Their glycosy-
lated hemoglobin levels were <8% (meanSEM¼6.5%0.2%),
and their fasting serum glucose concentration was 100 to
120 mg/dL (6.7 mmol/L). Patients with type 2 diabetes
were studied on four separate occasions. The day of the study,
patients with type 2 diabetes were instructed not to take
their morning doses of metformin. In this study, we included
seven adults without diabetes who were recruited through
iers as a control group, including four men and three
women within the age range of 25 to 54 years old (mean-
SEM¼24.11.2 years) with a BMI 25 (meanSEM¼
22.20.6) for the past 6 months. No participant received any
compensation for participation in the study. Exclusion
criteria included current cigarette smoker, presence of known
medical problem, or currently being on any medication.
Test Meals: Study 1
The test meal was composed of a portion of nopal containing
50 g of available carbohydrates, which is dened as total
carbohydrates minus dietary ber, according to the recom-
mendation of the Joint Food and Agricultural Organization of
the United Nations/World Health Organization Expert
Consultation.
10
Because raw nopal contains a signicant
amount of water, dehydrated nopal was utilized to determine
the glycemic index. Fresh nopal was obtained from Milpa
Alta, México City, and dried for 48 hours at 55C.
The chemical composition in the dry basis was as follows:
carbohydrates, 24.8%; insoluble ber, 32.2%; soluble ber,
4.8%; fat, <1.9%; and protein, 15.4%.
Test Meals: Study 2
The HCB contained 300 kcal and comprised 89% carbohy-
drates, 6% protein, and 5% fat, in the form of apple juice
(240 mL), white bread (55.6 g), and strawberry jam (21 g).
The HSPB contained 344 kcal and comprised 42.4% carbo-
hydrates, 40.7% protein, and 16.9% fat, in the form of soy
hamburger (61.5 g) and soymilk beverage (230 mL). The HSPB
was designed based on previous studies that have demon-
strated that soy protein reduces the postprandial peaks of
insulin and increases insulin sensitivity.
11,12
The HCBþnopal or the HSPBþnopal contained the foods
described here, with the addition of 300 g steamed nopal cut
into small pieces (2.0- to 2.5-cm cubes), the traditional form
consumed in Mexican cuisine. Raw nopal was cooked in a
steamer for 11 minutes over a medium heat, and nal cooked
weight was approximately 250 g. It was then served as side
dish. The chemical composition in fresh weight basis was
determined according to Association of Analytic Commu-
nities methods: carbohydrates, 1.4%; insoluble ber, 1.7%;
soluble ber, 0.17%; fat, negligible; and protein, 1.1%. Nopal
was always obtained from the same location during the same
season and harvested at the same time of day to minimize
chemical variability.
Protocol
Each participant arrived in the morning after a 12-hour
overnight fast and consumed the test meal as described
here for either study 1 or study 2. All participants consumed
the meal in the same order, and the washout period between
test meals was 1 week. All participants completed the study.
The test meals were consumed within 10 minutes and only
within each selected study. Capillary blood samples for
glucose determination in healthy participants were obtained
intermittently using a nger-stick before and at 15, 30, 45, 60,
90, and 120 minutes after commencing the test meals. Whole
blood glucose was measured using an automatic analyzer
(Model 2700, YSI Inc.). An additional sample in patients with
type 2 diabetes was collected at 150 minutes. Venous blood
samples were also obtained at the same time as capillary
blood to measure serum insulin, plasma GIP, GLP-1, and
antioxidant activity. The insulin concentration was measured
using a human radioimmunoassay kit (Linco Research Inc.).
GIP and GLP-1 were determined in blood samples that were
collected in tubes containing ethylenediamine tetraacetic
acid. Immediately after the blood collection, 30
m
L of the
dipeptidyl peptidase 4 inhibitor for the GLP-1 measurement
(Lincos DPP IV inhibitor) was added. Plasma was removed
after centrifugation and stored at 20C. The incretins were
analyzed using the Human Gut Hormone Panel (LINCOplex
Kit, Linco Research, Inc). The antioxidant capacity was
determined by the method of 2,2-diphenyl-1-picrilhidracyl,
which has been described previously.
13
Statistical Analysis
Calculation of the glycemic index and incremental area under
the curve (IAUC), excluding the area below fasting, were
calculated using the trapezoid rule.
14
Data are expressed as meanSEM. Analysis of repeated
measures was used to determine the diet and timing effects
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2JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS -- 2014 Volume -Number -
on the glucose, insulin, GIP, and GLP-1 concentrations. Stu-
dentsttest was used to compare the IAUC among the groups.
For all of the statistical tests, a Pvalue <0.05 was considered
to be signicant. Statistical analysis was performed with
Prism 6.0b for Mac OSXb (GraphPad Software Inc). Power
analysis indicated that with seven individuals, the study had
sufcient power to detect medium to small effects (0.80).
RESULTS
Study 1
The ingestion of 50 g of available carbohydrates from nopal
resulted in a signicant reduction (P<0.001) in the IAUC of
blood glucose (71.43.5) with respect to the 50 g of glucose
(231.717.4), as demonstrated in Figure 1A, which resulted in
a glycemic index of nopal of 32.54.0, a value that is
considered to be low.
15
With respect to insulin, the IAUC for
nopal was 7.81.0 and was signicantly different (P<0.05)
with respect to the glucose (25.55.8). The insulinemic index
was 36.16.1, which is also considered low, as demonstrated
in Figure 1B.
As shown in Figure 1C, low levels of GIP (8.61.4 pg/mL
[1.80.3 pmol/L]) were observed after a 12-hour fast. After
50 g oral glucose, the GIP concentration rapidly increased
within 45 minutes and reached a maximum value of
76.313.4 pg/mL (15.92.8 pmol/L). The consumption of
nopal did not increase the GIP concentration in the 2-hour
period, which had a value of 12.517.3 pg/mL (2.6 to 3.6
pmol/L). There was a signicant reduction in the IAUC for
plasma GIP after the consumption of 50 g of available car-
bohydrate from nopal in comparison with 50 g glucose
(1,370235 vs 88.519.3; P<0.01), as demonstrated in
AB
CD
Figure 1. (A) Blood glucose, (B) serum insulin, (C) plasma glucose-dependent insulinotropic peptide (GIP), and (D) glucagon-like protein
1 (GLP-1) concentrations at fasting state and 15, 30, 45, 60, 90, and 120 minutes after the consumption of 50 g oral glucose or 50 g
available carbohydrates (CHO) from nopal. Values were obtained in seven healthy adults without diabetes.
RESEARCH
-- 2014 Volume -Number -JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 3
Figure 1C. As shown in Figure 1D, the GLP-1 concentration
was low (43.915.8 pg/mL [13.34.8 pmol/L]) after 12 hours
of fasting. The consumption of 50 g glucose triggered a rapid
increase in GLP-1 to 79.117.1 pg/mL (245.2 pmol/L) within
45 minutes. In contrast, the 50 g of available carbohydrates
from nopal did not produce a peak in the GLP-1, instead, the
values remained constant (approximately 56 to 59 pg/mL [17
to 18 pmol/L]) during the 2-hour period.
Study 2
Effect of Steamed Nopal on Blood Glucose after
Ingesting an HCB or HSPB. Patients with type 2 diabetes
had a higher fasting blood glucose concentration (104.53.6
mg/dL [5.80.2 mmol/L]) compared with healthy partici-
pants (721.1 mg/dL [40.06 mmol/L]), as demonstrated in
Figure 2A. The consumption of an HCB in patients with type 2
diabetes gradually increased blood glucose concentration,
reaching a maximum value of 183.89 mg/dL (10.20.5
mmol/L) at 60 minutes, and the consumption of an
HCBþnopal signicantly decreased the postprandial peaks of
glucose at 45 and 60 minutes (P<0.01), as demonstrated in
Figure 2A. The IAUC for glucose in the group with an
HCBþnopal was signicantly lower (28730) than the group
with an HCB (44349; P<0.001 (inset, Figure 2A).
The consumption of an HCB by healthy participants grad-
ually increased blood glucose concentration, reaching a
maximum value of 120.71.8 mg/dL (6.70.1 mmol/L) at 30
minutes, and the consumption of an HCBþnopal reached a
maximum value of 106.35.4 mg/dL (5.90.3 mmol/L).
Therefore, the inclusion of nopal signicantly decreased the
postprandial peaks of glucose at 30, 45, and 60 minutes
(P<0.05), as demonstrated in Figure 2A. There was no dif-
ference in the IAUC for glucose in healthy participants after
the consumption of both breakfasts.
With respect to the HSPB, patients with type 2 diabetes
had a higher fasting blood glucose (99.15.4 mg/dL [5.50.3
mmol/L]) than healthy participants (73.91.8 mg/dL [4.10.1
mmol/L]), as demonstrated in Figure 2B. Interestingly, the
HSPB with and without nopal produced a smaller postprandial
blood glucose peak (126.15.4 mg/dL [7.00.3 mmol/L]) than
the HCB at 30, 45, 60, 90 (P<0.001), and 120 minutes (P<0.01);
therefore, it was more effective in reducing the postprandial
glucose peaks. No signicant differences were observed be-
tween the HSPB and HSPBþnopal. The IAUC for blood glucose
in patients with type 2 diabetes was similar in the HSPB
(12421) and HSPBþnopal (91.921).
Effect of Steamed Nopal on Serum Insulin after
Ingesting an HCB
The fasting serum insulin concentration in patients with
type 2 diabetes was higher (233
m
IU/mL [13818 pmol/L])
than in healthy participants (92
m
IU/mL [5412 pmol/L]), as
demonstrated in Figure 2C.
There was no difference in insulin concentration in both
over time; however, the IAUC for insulin concentration
was lower in the HCBþnopal group (5,953834) compared
with the HCB breakfast group (7,3131091) ( P<0.05) (inset,
Figure 2C).
There was no signicant difference in insulin concentration
over time in the HCB or HCBþnopal groups in healthy
participants.
Effect of Steamed Nopal on Serum Insulin after
Ingesting an HSPB
The fasting serum insulin concentration in patients with type
2 diabetes was higher (22.42
m
IU/mL [134.412 pmol/L])
than in healthy participants (13.21.8
m
IU/mL [79.210.8
pmol/L]), as demonstrated in Figure 2D. After the consump-
tion of an HSPB, the insulin concentration in patients with
type 2 diabetes increased during the postprandial period,
reaching a maximum value at 90 minutes. There was no
signicant difference in insulin concentration over time or in
the IAUC between the HSPB and the HSPBþnopal groups in
patients with type 2 diabetes (inset Figure 2D), and
HSPBþnopal signicantly reduced the IAUC for insulin in
healthy participants (inset, Figure 2D).
Effect of Steamed Nopal on Plasma GIP after
Ingesting an HCB
Patients with type 2 diabetes had higher fasting plasma GIP
concentration (70.114.9 pg/mL [14.63.1 pmol/L]) compared
with healthy participants (22.14.8 pg/mL [4.61 pmol/L]).
Fifteen minutes after consuming an HCB, patients with type 2
diabetes had a rapid increase in GIP concentration, which
reached a maximum value (170.422.1 pg/mL [35.54.6 pmol/
L]) at 60 minutes. Consuming the HCBþnopal reduced the
postprandial peaks of GIP between 30 and 60 minutes, as
demonstrated in Figure 3A. The consumption of an HCBþnopal
by healthy participants signicantly reduced the GIP peak at 60
minutes compared with the HCB group (P<0.05), as demon-
strated in Figure 3A. There was no signicant difference in the
IAUC in patients with type 2 diabetes after the consumption of
an HCBþnopal, but in healthy participants, there was a sig-
nicant difference (P<0.01) compared with the HCB group
(2,842802 pg/mL [592167 pmol/L] vs 8,2521,171 pg/mL
[1,719244 pmol/L]).
Effect of Steamed Nopal on Plasma GIP after
Ingesting an HSPB
Fastingplasma GIP concentrations were similar in patients with
type 2 diabetes and in healthy participants (35.15.3 pg/mL
[7.321.1 pm o l / L] a nd ( 26 .1 5.3 pg/mL [5.431.1 pmol/L],
respectively). Fifteen minutes after theconsumption of an HSPB,
patients with type 2 diabetes had a rapid increase in GIP con-
centration, which reached a maximum value (137.312 pg/mL
[28.62.5 pmol/L]) after 30 minutes, as demonstrated in
Figure 3B. In patients with type 2 diabetes, consumption of an
HSPBþnopal signicantly reduced the GIP concentration at 30
and 40 minutes (P<0.00 at 30 minutes and P<0.05 at 45 mi-
nutes). There was a signicant reduction (P<0.01) in the IAUC
after the consumption of the HSPBþnopal compared with the
HSPB (1,744258 vs 2,448229) in patients with type 2 dia-
betes. In healthy participants, there was an increase in the GIP
plasma concentrations starting after 15 minutes of HSPB
ingestion, with a maximum peak (14416.3 pg/mL [30.03.4
pmol/L]) after90 minutes. There was no signicant difference in
the IAUCbetween the HSPBand HSPBþnopal (inset, Figure 3B).
Effect of Steamed Nopal on Plasma GLP-1 after
Ingesting an HCB or HSPB
The GLP-1 concentration in patients with type 2 diabetes
was 15.53 pg/mL (4.70.9 pmol/L) after 12 hours of fasting,
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4JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS -- 2014 Volume -Number -
AB
CD
Figure 2. Fasting and postprandial blood glucose and increase in the incremental area under the curve (IAUC) for blood glucose
after the consumption of a high-carbohydrate breakfast (HCB) (A) or a high-soy-protein breakfast (HSPB) (B) with or without 300 g of
steamed nopal (N); *P<0.05, **P<0.01. We also show fasting and postprandial serum insulin and IAUC after the consumption of an
HCB (C) or HSPB (D) with or without 300 g steamed nopal. Values were obtained in seven healthy adults without diabetes and in 14
patients with type 2 diabetes (PT2D). Values are meanstandard error of mean. HCB-D¼HCB-patients with type 2 diabetes; HCB-
H¼HCB-healthy subjects; HCBþN-D¼HCBþnopal-patients with type 2 diabetes; HCBþN-H¼HCBþnopal-healthy subjects; HSPB-
D¼HSPB-patients with type 2 diabetes; HSPB-H¼HSPB-healthy subjects; HSPBþN-D¼HSPBþnopal-patients with type 2 diabetes;
HSPBþN-H¼HSPBþnopal-healthy subjects.
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-- 2014 Volume -Number -JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 5
AB
C
Figure 3. Fasting and postprandial glucose-dependent insulinotropic peptide (GIP) and incremental area under the curve (IAUC)
after the consumption of a high-carbohydrate breakfast (HCB) (A) or a high soy-protein breakfast (HSPB) (B) with or without 300 g
steamed nopal (N) in 7 healthy adults without diabetes and in 14 patients with type 2 diabetes (PT2D); *P<0.05, **P<0.01,
***P<0.001. (C) Plasma antioxidant activity after 2 hours of consuming the HCB or the HSPB in PT2D and healthy adults without
diabetes. HCB-D¼HCB-patients with type 2 diabetes; HCB-H¼HCB-healthy subjects; HCBþN-D¼HCBþnopal-patients with type 2
diabetes; HCBþN-H¼HCBþnopal-healthy subjects; HSPB-D¼HSPB-patients with type 2 diabetes; HSPB-H¼HSPB-healthy subjects;
HSPBþN-D¼HSPBþnopal-patients with type 2 diabetes; HSPBþN-H¼HSPBþnopal-healthy subjects. a >b>c>d.
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6JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS -- 2014 Volume -Number -
and GLP-1 concentration in healthy subjects was 310.4 pg/
mL (9.41.2 pmol/L). After the consumption of the
HCBþnopal or HSPBþnopal, there was no effect on GLP-1 in
patients with type 2 diabetes or healthy participants (data
not shown).
Serum Antioxidant Activity after Ingesting Nopal in
an HCB or HSPB
Healthy participants showed similar antioxidant activity
(9.2%6.4%) compared with patients with type 2 diabetes
(7.7%1.6%) at 120 minutes regardless of the breakfast
consumed. The inclusion of nopal increased the antioxidant
activity in healthy participants and in patients with type 2
diabetes and was more evident after the consumption of the
HSPB (Figure 3C).
DISCUSSION
Excessive and prolonged postprandial blood glucose peaks
are a serious health problem for individuals with diabetes. As
a result, changes in lifestyle have been suggested as the main
strategy for controlling the biochemical abnormalities that
are associated with type 2 diabetes.
16
We developed a dietary
strategy including the use of the inexpensive regional food
nopal to minimize postprandial glucose peaks. Our results
show that nopal has low glycemic and insulinemic indexes
that could be recommended for patients with type 2 diabetes.
Interestingly, the low glycemic index and insulinemic index
of nopal were associated with a dramatic reduction of
the IAUC for the total plasma GIP concentration. These
results suggest that nopal could regulate blood glucose and
serum insulin concentrations by modulating GIP levels.
Interestingly, the inclusion of steamed nopal in the HCB
signicantly reduced postprandial blood glucose peaks.
Remarkably, the HSPB and HSPBþnopal helped prevent
postprandial blood glucose peaks. These results are impor-
tant because recommendations from the American Diabetes
Association are for patients with type 2 diabetes to maintain,
blood glucose levels in the normal range or as close to
normal as is safely possible.
17
The European Diabetes Policy
Group has set the maximum postprandial glucose peak to not
exceed 135 mg/dL (7.5 mmol/L) to reduce arterial risk and
160 mg/dL (9.0 mmol/L) to reduce microvascular risk.
18
The
inclusion of nopal in the HCB in patients with type 2 diabetes
reduced blood glucose by 36 mg/dL (2 mmol/L), reaching a
value near that recommended by the European Diabetes
Policy Group. The presence of nopal in the HSPB helped
signicantly to avoid blood glucose peaks reaching a value of
127 mg/dL (7.07 mmol/L) at 60 minutes, a value below that
recommended by the European Diabetes Policy Group. Nopal
consumption signicantly reduced the IAUC for serum insulin
in patients with type 2 diabetes after ingesting the HCB and
prevented an increase in insulin levels after consuming an
HSPB.
In this study, GIP levels seemed to be signicantly
increased in patients with type 2 diabetes in the postprandial
state compared with those in healthy participants, and the
insulinotropic effect of GIP was maintained and associated
with insulin concentration in patients with type 2 diabetes
because the insulin levels increased as the GIP increased.
However, the postprandial blood glucose concentra-
tion remained high, which indicates insulin resistance.
Interestingly, the inclusion of nopal in the HCB or HSPB
signicantly reduced the postprandial peaks of the total GIP
in patients with type 2 diabetes and in healthy participants.
One limitation of the study was the difference in age and sex;
patients with type 2 diabetes were older than healthy
subjects.
It is recommended to include two or three medium nopales
(approximately 250 g after cooking) in a salad, soup, grilled,
nopal juice, or as side dish for patients with type 2 diabetes
and 1
1
/
2
to 2 medium nopales for healthy people. Nopal can
be found in ethnic grocery stores in the United States, mainly
in Southern California and Texas. Another option is to
consume dehydrated nopal (13.7 g) dried at low temperature
(no higher than 55C to maintain antioxidant activity), which
is equivalent to 300 g raw nopal.
There is considerable evidence from in vitro and in vivo
studies that hyperglycemia results in the generation of
reactive oxygen species and consequently increased oxidative
stress. The presence of polyphenols (such as quercetin, iso-
rhamnetin, and kaempferol; vitamin C) and beta carotenes in
nopal contributes to nopal antioxidant activity. We demon-
strated that consumption of nopal provides antioxidant ac-
tivity in the serum of both healthy people and patients with
type 2 diabetes 2 hours after consumption. The consumption
of nopal could have a compensatory effect on the decreased
endogenous antioxidants during type 2 diabetes.
CONCLUSIONS
The current epidemic of diabetes has led to a search for
functional foods that could aid in ameliorating this pathol-
ogy. Nopal has long been used in traditional Mexican med-
icine to control diabetes, however, there was insufcient
scientic evidence regarding the ability of this plant to help
control postprandial blood glucose peaks. Our results show
that nopal has low glycemic, insulinemic, and GIP indexes
and could be recommended for patients with type 2
diabetes. The inclusion of nopal in an HCB had anti-
hyperglycemic and antihyperinsulinemic effects, and in the
HSPB, it prevented postprandial blood glucose peaks. The
consumption of nopal increased the antioxidant activity in
both healthy people and patients with type 2 diabetes.
Nopal is not a complete replacement for prescription blood
glucose drugs, but the ndings in this study support the
traditional use of nopal for the safe management of glucose
without any side effects.
References
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AUTHOR INFORMATION
P. López-Romero is an assistant researcher, E. Pichardo-Ontiveros is an assistant researcher, A. Avila-Nava is an assistant researcher, N. Vázquez-
Manjarrez is an assistant researcher, A. R. Tovar is a professor, and N. Torres is a professor, Departamento de Fisiología de la Nutrición, Instituto
Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Vasco de Quiroga, México. J. Pedraza-Chaverri is a professor, Departamento de
Biología, Facultad de Química, Edicio F, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, Coyoacan, México.
Address correspondence to: Nimbe Torres, PhD, Departamento de Fisiología de la Nutrición, Instituto Nacional de Ciencias Médicas y Nutrición
Salvador Zubirán, Vasco de Quiroga, No. 15, Sección XVI, 14000, México. E-mail: nimbester@gmail.com
STATEMENT OF POTENTIAL CONFLICT OF INTEREST
No potential conict of interest was reported by the authors.
FUNDING/SUPPORT
This study was supported by the Instituto de Ciencia y Tecnología del Distrito Federal, Fundación Produce 2010 and Nutriva de México S.A. de
C.V. Aguascalientes, Ags. México. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
RESEARCH
8JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS -- 2014 Volume -Number -
... Por su valor económico, cultural, ecológico y nutricional, el nopal (Opuntia spp.) es una cactácea de suma importancia en México, donde presenta una enorme variedad de especies y cuyo crecimiento es característico de zonas áridas y semiáridas. Posee una extraordinaria capacidad de adaptación a condiciones climáticas y edáficas, razón por la cual organismos como la FAO han considerado al nopal como una alternativa viable para la restauración de suelos, la reducción de la erosión y la producción sustentable de alimentos (Stintzing y Carle, 2005;López-Romero et al., 2014;Torres-Ponce et al., 2015;Ibarra-Rodríguez et al., 2017;du Toti et al., 2018;Ciriminna et al., 2019;Saénz et al., 2019). ...
... Por su versatilidad, el nopal no solo ha impactado en el ámbito alimenticio y farmacéutico, sino que su uso ha trascendido a aplicaciones en la industria química, cosmética, textil e incluso como fuente alterna de energía (Stintzing y Carle, 2005;López-Romero et al., 2014;Torres-Ponce et al., 2015;Ibarra-Rodríguez et al., 2017;du Toti et al., 2018;Ciriminna et al., 2019;Saénz et al., 2006). ...
... Se han realizado diversos estudios sobre estos beneficios a la salud, López-Romero et al. (2014) investigaron los efectos del consumo de nopal sobre el nivel de glucosa postprandial en individuos sanos y pacientes con diabetes tipo 2; en ambos casos encontraron que la ingesta de este vegetal disminuyó significativamente los niveles de glucosa postprandial y generó un menor incremento en la curva de insulina, sugiriendo que el nopal puede reducir el nivel postprandial de glucosa en sangre, insulina sérica y picos de péptido insulinotrópico dependiente de glucosa (GIP) en plasma. ...
... Por su valor económico, cultural, ecológico y nutricional, el nopal (Opuntia spp.) es una cactácea de suma importancia en México, donde presenta una enorme variedad de especies y cuyo crecimiento es característico de zonas áridas y semiáridas. Posee una extraordinaria capacidad de adaptación a condiciones climáticas y edáficas, razón por la cual organismos como la FAO han considerado al nopal como una alternativa viable para la restauración de suelos, la reducción de la erosión y la producción sustentable de alimentos (Stintzing y Carle, 2005;López-Romero et al., 2014;Torres-Ponce et al., 2015;Ibarra-Rodríguez et al., 2017;du Toti et al., 2018;Ciriminna et al., 2019;Saénz et al., 2019). ...
... Por su versatilidad, el nopal no solo ha impactado en el ámbito alimenticio y farmacéutico, sino que su uso ha trascendido a aplicaciones en la industria química, cosmética, textil e incluso como fuente alterna de energía (Stintzing y Carle, 2005;López-Romero et al., 2014;Torres-Ponce et al., 2015;Ibarra-Rodríguez et al., 2017;du Toti et al., 2018;Ciriminna et al., 2019;Saénz et al., 2006). ...
... Se han realizado diversos estudios sobre estos beneficios a la salud, López-Romero et al. (2014) investigaron los efectos del consumo de nopal sobre el nivel de glucosa postprandial en individuos sanos y pacientes con diabetes tipo 2; en ambos casos encontraron que la ingesta de este vegetal disminuyó significativamente los niveles de glucosa postprandial y generó un menor incremento en la curva de insulina, sugiriendo que el nopal puede reducir el nivel postprandial de glucosa en sangre, insulina sérica y picos de péptido insulinotrópico dependiente de glucosa (GIP) en plasma. ...
... Por su valor económico, cultural, ecológico y nutricional, el nopal (Opuntia spp.) es una cactácea de suma importancia en México, donde presenta una enorme variedad de especies y cuyo crecimiento es característico de zonas áridas y semiáridas. Posee una extraordinaria capacidad de adaptación a condiciones climáticas y edáficas, razón por la cual organismos como la FAO han considerado al nopal como una alternativa viable para la restauración de suelos, la reducción de la erosión y la producción sustentable de alimentos (Stintzing y Carle, 2005;López-Romero et al., 2014;Torres-Ponce et al., 2015;Ibarra-Rodríguez et al., 2017;du Toti et al., 2018;Ciriminna et al., 2019;Saénz et al., 2019). ...
... Por su versatilidad, el nopal no solo ha impactado en el ámbito alimenticio y farmacéutico, sino que su uso ha trascendido a aplicaciones en la industria química, cosmética, textil e incluso como fuente alterna de energía (Stintzing y Carle, 2005;López-Romero et al., 2014;Torres-Ponce et al., 2015;Ibarra-Rodríguez et al., 2017;du Toti et al., 2018;Ciriminna et al., 2019;Saénz et al., 2006). ...
... Se han realizado diversos estudios sobre estos beneficios a la salud, López-Romero et al. (2014) investigaron los efectos del consumo de nopal sobre el nivel de glucosa postprandial en individuos sanos y pacientes con diabetes tipo 2; en ambos casos encontraron que la ingesta de este vegetal disminuyó significativamente los niveles de glucosa postprandial y generó un menor incremento en la curva de insulina, sugiriendo que el nopal puede reducir el nivel postprandial de glucosa en sangre, insulina sérica y picos de péptido insulinotrópico dependiente de glucosa (GIP) en plasma. ...
... When compared to maize, Opuntia ficus-indica has 80% of its energy value, but it has the potential to produce 20-30 times more forage in the same land unit [25]. Opuntia fruit is considered relatively low-caloric, as is common with fruit, having 27 kcal/100 g of fresh fruit [26]. ...
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Adapting our food production chain and increasing the flora and fauna’s livelihood in climate change-affected areas using Opuntia is not only theoretical but already exists in practice in many places. This cactus grows in unsuitable soil for most species as it is adapted to arid and semi-arid soils and hot weather. In these regions, Opuntia protects from erosion and contributes to soil health. The usage of this plant as fodder is also discussed, with immense potential in substituting a part of livestock’s diet and even increasing the quality of the animal’s by-products and decreasing water consumption. This would result in a feed that is low-cost and has a lower environmental impact. It is to be noted that Opuntia has a high potential as an invasive species, with caution always being recommended when dealing with this specie. The high content of specific compounds, such as proline, indicaxanthin, and betanin, found in Opuntia ficus-indica, influence the plant’s adaptation to unfavourable conditions. This collective evidence depicts Opuntia as a crop that can battle climate change and ensure food security.
... The inclusion of this medicinal plant in a high-carbohydrate breakfast or in high soy protein (HSBP) has anthohergic and antihyperinsulin effects and even prevented postprandial blood glucose peaks in HSPB. Its consumption also increased the antioxidant activity (López-Romero et al., 2014). This agrees with the results of a study performed on diabetic rats induced by low doses of STZ. ...
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The present study aimed to document the traditional use of medicinal plants used to treat Diabetes mellitus Type II in Bolivia. Based on the scientific literature were identified 35 medicinal plant species distributed in 21 botanical families, of which 52 % are native to Bolivia and 48 % are introduced. The botanical families with the highest representation of species were Asteraceae (7 species, 19%) and Fabaceae (17%). The most frequented growth forms were herbs (34%) and trees (29%). Leaves (30%) were the most frequently used plant parts, followed by roots (14%), and bark (9%), mostly prepared as an infusion (40%) and decoction (33%). From the available scientific studies, 25 medicinal species were verified for their antidiabetic properties with positive results, but it is necessary provide more biochemical and clinical analysis of medicinal plants to make better use of their potential.
... Nopal (Opuntia ficus indica) seems to suppress the inflammatory effect of lipopolysaccharides, which are responsible for inducing insulin resistance and glucose intolerance. For instance, in patients with T2DM, a significantly lower area under a curve (AUC) for glucose (287 ± 30) was achieved in the high-soy-protein breakfast + nopal group compared to the high-soy-protein breakfast only group (443 ± 49) [50]. ...
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Background and Objectives: Type 2 diabetes mellitus (T2DM) is a chronic metabolic disease affecting an estimated 537 million individuals worldwide. 'Superfoods' can be integrated into the diet of T2DM patients due to their health benefits. Study Objectives: (i) To carry out a narrative review of 'superfoods' with the potential to reduce glycaemic levels in T2DM patients (2019 to 2022), (ii) to identify 'superfoods' with the potential to reduce HbA1c and (iii) to propose new guidance on the use of 'superfoods'. Materials and Methods: A narrative review was carried out using the databases PubMed, SciELO, DOAJ and Google Scholar. The keywords were ["type 2 diabetes" and ("food" or "diet" or "nutrition") and ("glycaemia" or "glycemia")]. Only review studies were included. Results: Thirty reviews were selected. The 'superfoods' identified as having a potential impact on glycaemic control were foods with polyphenols (e.g., berries), fermented dairy products, whole cereals/grains, nuts and proteins, among others. The possibility of an extensive reduction in Hb1Ac was reported for fermented dairy products, especially yoghurts enriched with vitamin D or probiotics (HbA1c reduction of around 1%) or by increasing the fibre intake by 15 g (or up to 35 g) (HbA1c reduction of around 2%). Conclusion: It is recommended that the identified 'superfoods' are included in the diet of T2DM patients, although this should not substitute an appropriate diet and exercise plan. In particular, yoghurts and an increased fibre intake (by 15 g or up to 35 g) can be used as nutraceuticals. New recommendations on the introduction of 'superfoods' in the diet of T2DM patients have been proposed.
... The beneficial health effects of cladode consumption have been documented, with blood sugar control exhibiting the most promising results (Frati et al., 1990). López-Romero et al. (2014) reported that the incorporation of steamed cladodes in a carbohydrate rich meal can improve the glycemic response in patients with type 2 diabetes mellitus, which is considered beneficial for the management of the disease. ...
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The effect of very highly purified gastric inhibitory polypeptide (GIP) on insulin secretion in man was tested in normal volunteers. Administration of physiological doses of GIP together with glucose by IV infusion resulted in potentiation of the rise in IRI in the blood and improvement in glucose tolerance. It is concluded that GIP is a potent insulinotropic hormone and probably takes part in physiological potentiation of insulin secretion in response to hyperglycemia during absorption of nutrients from the intestine.
Article
The acute effects of different macronutrients on the secretion of glucagon-like peptide-1(7–36)amide (GLP-1(7–36)amide) and glucose-dependent insulinotropic polypeptide (GIP) were compared in healthy human subjects. Circulating levels of the two hormones were measured over a 24-h period during which subjects consumed a mixed diet. In the first study, eight subjects consumed three equicaloric (375 kcal) test meals of carbohydrate, fat and protein. Small increases in plasma GLP-1(7–36) amide were found after all meals. Levels reached a maximum 30 min after the carbohydrate and 150 min after the fat load. Ingestion of both carbohydrate and fat induced substantial rises in GIP secretion, but the protein meal had no effect. In a second study, eight subjects consumed 75 g glucose or the equivalent portion of complex carbohydrate as boiled brown rice or barley. Plasma GIP, insulin and glucose levels increased after all three meals, the largest increase being observed following glucose and the smallest following the barley meal. Plasma GLP-1(7–36)amide levels rose only following the glucose meal. In the 24-h study, plasma GLP-1(7–36)amide and GIP concentrations were increased following every meal and remained elevated throughout the day, only falling to fasting levels at night. The increases in circulating GLP-1(7–36)amide and GIP levels following carbohydrate or a mixed meal are consistent with their role as incretins. The more sustained rises observed in the daytime during the 24-h study are consistent with an anabolic role in lipid metabolism. Journal of Endocrinology (1993) 138, 159–166
A key issue in diabetes care is selecting glucose parameters to monitor and control. The recommendations of the American Diabetes Association for glycaemic control do not address postprandial glucose (PPG), but patients with type 2 diabetes experience wide variations in glucose levels after meals. We have observed a remarkable increase in plasma glucose two hours after breakfast and/or lunch in most non-insulin-treated patients; for up to 40% of them the increase is >40 mg/dl (2.2 mmol/l). As many as 70% of patients with an HbA1c <7% have PPG values >160 mg/dl (8.9 mmol/l) after meals. Fasting plasma glucose (FPG) is a poor indicator of plasma glucose at other times. The coefficient of correlation of FPG with plasma glucose at other times ranges from 0.50-0.70. Nor is the correlation of FPG with HbA1c very strong: in hundreds of determinations of HbA1c and FPG in our patients, the coefficient of correlation was not greater than 0.73. For the same FPG value, HbA1c varied markedly, and vice versa; further, the correlation between PPG and HbA1c was no higher than that between FPG and HbA1c (r = 0.65). Thus, monitoring in type 2 diabetes should include PPG along with FPG and HbA1c. Recent data provide direct and indirect evidence suggesting that PPG is independently related to cardiovascular disease (CVD), and supporting the idea that PPG should be assessed and glucose excursions with meals should be controlled: 1. Studies conducted by other investigators and ourselves in patients with type 2 diabetes have shown that the incidence of CVD is independently related to postprandial or post-OGTT (oral glucose tolerance test) blood glucose at baseline. In addition, data collected in the general population show an association between 2-hour OGTT plasma glucose (a surrogate of PPG) and cardiovascular morbidity and mortality that is independent of FPG. Also, subjects with impaired glucose tolerance (IGT) and isolated post-challenge hyperglycaemia have an increased cardiovascular risk over subjects with normal glucose tolerance (NGT). We found that IGT subjects had a risk of carotid stenosis 3-fold higher than subjects with NGT, even after adjustment for several confounders. Thus, a modest increase in post-OGTT plasma glucose and, by extrapolation, PPG seems to have a major detrimental effect on the arteries. 2. When FPG and/or HbA1c were the targets of glucose control in studies of patients with type 2 diabetes (the UGDP, VACSDM, and UKPDS) the effects on CVD were minimal. However, when the targets of glucose control included PPG (the Kumamoto Study and DIGAMI Study) favorable effects on CVD were observed. 3. There is experimental data suggesting that acute hyperglycaemia can exert deleterious effects on the arterial wall through mechanisms including oxidative stress, endothelial dysfunction, and activation of the coagulation cascade. This evidence prompted the European Diabetes Policy Group to set postprandial targets for blood glucose control: postprandial peaks should not exceed 135 mg/dl (7.5 mmol/ml) to reduce arterial risk and should not exceed 160 mg/dl (8.9 mmol/l) to reduce microvascular risk. Thus, glucose care in diabetes is not only "fasting glucose care" or "HbA1c care" but is also "postprandial glucose care."