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T
HE CACTUS OPUNTIA, WHICH IS ALSO KNOWN AS
nopal, is native to central Mexico1 and the pads are mation 5 and endothelial dysfunction.6 In addition, post-
eaten as a vegetable. Cactus plants have long served prandial glucose homeostasis is controlled not only by
as a source of food for people, and they have long direct stimulation of insulin release by absorbed nutrients,
been used in traditional Mexican medicine for treating dia- but also through secretion of incretin hormones, that is,
betes. Nopal is considered a functional food because it is a glucagon-like peptide-1 (GLP-1) and glucose-dependent in-
proven source of dietary fiber2 and bioactive compounds sulinotropic peptide (GIP).7 These incretins are released
with antioxidant activity, such as flavonoids, flavonols, car- from enteroendocrine cells and are responsible for at least
otenes, and ascorbic acid,3 in addition to being low in calo- 50% of the total insulin 8 secreted after the ingestion of
ries (27 kcal/100 g). The current epidemic of obesity and food.9 Therefore, the purpose of conducting this study was
diabetes has led to a search for functional foods that could first to evaluate the glycemic index, insulinemic index, GIP
aid in ameliorating these pathologies. In the case of dia- index, and GLP-1 index, and second, to evaluate the meta-
betes, consuming high-calorie meals can lead to exagger- bolic effect of steamed nopal on postprandial peaks of
ated postprandial peaks in blood glucose and in lipids that glucose, insulin, GIP, and antioxidant activity after the
ª 2014 by the Academy of Nutrition and Dietetics. JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 1
RESEARCH
consumption of a high-carbohydrate breakfast (HCB) or carbohydrates, 24.8%; insoluble fiber, 32.2%; soluble fiber,
high-soy-protein breakfast (HSPB). 4.8%; fat, <1.9%; and protein, 15.4%.
on the glucose, insulin, GIP, and GLP-1 concentrations. Stu- considered to be low.15 With respect to insulin, the IAUC for
dent’s t test was used to compare the IAUC among the groups. nopal was 7.81.0 and was significantly different (P<0.05)
For all of the statistical tests, a P value <0.05 was considered with respect to the glucose (25.55.8). The insulinemic index
to be significant. Statistical analysis was performed with was 36.16.1, which is also considered low, as demonstrated
Prism 6.0b for Mac OSXb (GraphPad Software Inc). Power in Figure 1B.
analysis indicated that with seven individuals, the study had As shown in Figure 1C, low levels of GIP (8.61.4 pg/mL
sufficient power to detect medium to small effects (0.80). [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
RESULTS 76.313.4 pg/mL (15.92.8 pmol/L). The consumption of
Study 1 nopal did not increase the GIP concentration in the 2-hour
The ingestion of 50 g of available carbohydrates from nopal period, which had a value of 12.517.3 pg/mL (2.6 to 3.6
resulted in a significant reduction (P<0.001) in the IAUC of pmol/L). There was a significant reduction in the IAUC for
blood glucose (71.43.5) with respect to the 50 g of glucose plasma GIP after the consumption of 50 g of available car-
(231.717.4), as demonstrated in Figure 1A, which resulted in bohydrate from nopal in comparison with 50 g glucose
a glycemic index of nopal of 32.54.0, a value that is (1,370235 vs 88.519.3; P<0.01), as demonstrated in
A B
C D
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.
Figure 1C. As shown in Figure 1D, the GLP-1 concentration Effect of Steamed Nopal on Serum Insulin after
was low (43.915.8 pg/mL [13.34.8 pmol/L]) after 12 hours Ingesting an HSPB
of fasting. The consumption of 50 g glucose triggered a rapid The fasting serum insulin concentration in patients with type
increase in GLP-1 to 79.117.1 pg/mL (245.2 pmol/L) within 2 diabetes was higher (22.42 mIU/mL [134.412 pmol/L])
45 minutes. In contrast, the 50 g of available carbohydrates than in healthy participants (13.21.8 mIU/mL [79.210.8
from nopal did not produce a peak in the GLP-1, instead, the pmol/L]), as demonstrated in Figure 2D. After the consump-
values remained constant (approximately 56 to 59 pg/mL [17 tion of an HSPB, the insulin concentration in patients with
to 18 pmol/L]) during the 2-hour period. type 2 diabetes increased during the postprandial period,
reaching a maximum value at 90 minutes. There was no
Study 2 significant difference in insulin concentration over time or in
Effect of Steamed Nopal on Blood Glucose after the IAUC between the HSPB and the HSPBþnopal groups in
Ingesting an HCB or HSPB. Patients with type 2 diabetes patients with type 2 diabetes (inset Figure 2D), and
had a higher fasting blood glucose concentration (104.53.6 HSPBþnopal significantly reduced the IAUC for insulin in
mg/dL [5.80.2 mmol/L]) compared with healthy partici- healthy participants (inset, Figure 2D).
pants (721.1 mg/dL [40.06 mmol/L]), as demonstrated in
Figure 2A. The consumption of an HCB in patients with type 2 Effect of Steamed Nopal on Plasma GIP after
diabetes gradually increased blood glucose concentration, Ingesting an HCB
reaching a maximum value of 183.89 mg/dL (10.20.5 Patients with type 2 diabetes had higher fasting plasma GIP
mmol/L) at 60 minutes, and the consumption of an concentration (70.114.9 pg/mL [14.63.1 pmol/L]) compared
HCBþnopal significantly decreased the postprandial peaks of with healthy participants (22.14.8 pg/mL [4.61 pmol/L]).
glucose at 45 and 60 minutes (P<0.01), as demonstrated in Fifteen minutes after consuming an HCB, patients with type 2
Figure 2A. The IAUC for glucose in the group with an diabetes had a rapid increase in GIP concentration, which
HCBþnopal was significantly lower (28730) than the group reached a maximum value (170.422.1 pg/mL [35.54.6 pmol/
with an HCB (44349; P<0.001 (inset, Figure 2A). L]) at 60 minutes. Consuming the HCBþnopal reduced the
The consumption of an HCB by healthy participants grad- postprandial peaks of GIP between 30 and 60 minutes, as
ually increased blood glucose concentration, reaching a demonstrated in Figure 3A. The consumption of an HCBþnopal
maximum value of 120.71.8 mg/dL (6.70.1 mmol/L) at 30 by healthy participants significantly reduced the GIP peak at 60
minutes, and the consumption of an HCBþnopal reached a minutes compared with the HCB group (P<0.05), as demon-
maximum value of 106.35.4 mg/dL (5.90.3 mmol/L). strated in Figure 3A. There was no significant difference in the
Therefore, the inclusion of nopal significantly decreased the IAUC in patients with type 2 diabetes after the consumption of
postprandial peaks of glucose at 30, 45, and 60 minutes an HCBþnopal, but in healthy participants, there was a sig-
(P<0.05), as demonstrated in Figure 2A. There was no dif- nificant difference (P<0.01) compared with the HCB group
ference in the IAUC for glucose in healthy participants after (2,842802 pg/mL [592167 pmol/L] vs 8,2521,171 pg/mL
the consumption of both breakfasts. [1,719244 pmol/L]).
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
Effect of Steamed Nopal on Plasma GIP after
mmol/L]), as demonstrated in Figure 2B. Interestingly, the Ingesting an HSPB
HSPB with and without nopal produced a smaller postprandial Fasting plasma GIP concentrations were similar in patients with
blood glucose peak (126.15.4 mg/dL [7.00.3 mmol/L]) than type 2 diabetes and in healthy participants (35.15.3 pg/mL
the HCB at 30, 45, 60, 90 (P<0.001), and 120 minutes (P<0.01); [7.321.1 pmol/L] and (26.15.3 pg/mL [5.431.1 pmol/L],
therefore, it was more effective in reducing the postprandial respectively). Fifteen minutes after the consumption of an HSPB,
glucose peaks. No significant differences were observed be- patients with type 2 diabetes had a rapid increase in GIP con-
tween the HSPB and HSPBþnopal. The IAUC for blood glucose centration, which reached a maximum value (137.312 pg/mL
in patients with type 2 diabetes was similar in the HSPB [28.62.5 pmol/L]) after 30 minutes, as demonstrated in
(12421) and HSPBþnopal (91.921). Figure 3B. In patients with type 2 diabetes, consumption of an
HSPBþnopal significantly reduced the GIP concentration at 30
and 40 minutes (P<0.00 at 30 minutes and P<0.05 at 45 mi-
Effect of Steamed Nopal on Serum Insulin after nutes). There was a significant reduction (P<0.01) in the IAUC
Ingesting an HCB after the consumption of the HSPBþnopal compared with the
The fasting serum insulin concentration in patients with HSPB (1,744258 vs 2,448229) in patients with type 2 dia-
type 2 diabetes was higher (233 mIU/mL [13818 pmol/L]) betes. In healthy participants, there was an increase in the GIP
than in healthy participants (92 mIU/mL [5412 pmol/L]), as plasma concentrations starting after 15 minutes of HSPB
demonstrated in Figure 2C. ingestion, with a maximum peak (14416.3 pg/mL [30.03.4
There was no difference in insulin concentration in both pmol/L]) after 90 minutes. There was no significant difference in
over time; however, the IAUC for insulin concentration the IAUC between the HSPB and HSPBþnopal (inset, Figure 3B).
was lower in the HCBþnopal group (5,953834) compared
with the HCB breakfast group (7,3131091) (P<0.05) (inset,
Figure 2C). Effect of Steamed Nopal on Plasma GLP-1 after
There was no significant difference in insulin concentration Ingesting an HCB or HSPB
over time in the HCB or HCBþnopal groups in healthy The GLP-1 concentration in patients with type 2 diabetes
participants. was 15.53 pg/mL (4.70.9 pmol/L) after 12 hours of fasting,
A B
C D
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.
A B
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.
and GLP-1 concentration in healthy subjects was 310.4 pg/ Interestingly, the inclusion of nopal in the HCB or HSPB
mL (9.41.2 pmol/L). After the consumption of the significantly reduced the postprandial peaks of the total GIP
HCBþnopal or HSPBþnopal, there was no effect on GLP-1 in in patients with type 2 diabetes and in healthy participants.
patients with type 2 diabetes or healthy participants (data One limitation of the study was the difference in age and sex;
not shown). patients with type 2 diabetes were older than healthy
subjects.
Serum Antioxidant Activity after Ingesting Nopal in It is recommended to include two or three medium nopales
an HCB or HSPB (approximately 250 g after cooking) in a salad, soup, grilled,
nopal juice, or as side dish for patients with type 2 diabetes
Healthy participants showed similar antioxidant activity
and 11/2 to 2 medium nopales for healthy people. Nopal can
(9.2%6.4%) compared with patients with type 2 diabetes
be found in ethnic grocery stores in the United States, mainly
(7.7%1.6%) at 120 minutes regardless of the breakfast
in Southern California and Texas. Another option is to
consumed. The inclusion of nopal increased the antioxidant
consume dehydrated nopal (13.7 g) dried at low temperature
activity in healthy participants and in patients with type 2
(no higher than 55 C to maintain antioxidant activity), which
diabetes and was more evident after the consumption of the
is equivalent to 300 g raw nopal.
HSPB (Figure 3C).
There is considerable evidence from in vitro and in vivo
studies that hyperglycemia results in the generation of
DISCUSSION reactive oxygen species and consequently increased oxidative
Excessive and prolonged postprandial blood glucose peaks stress. The presence of polyphenols (such as quercetin, iso-
are a serious health problem for individuals with diabetes. As rhamnetin, and kaempferol; vitamin C) and beta carotenes in
a result, changes in lifestyle have been suggested as the main nopal contributes to nopal antioxidant activity. We demon-
strategy for controlling the biochemical abnormalities that strated that consumption of nopal provides antioxidant ac-
are associated with type 2 diabetes.16 We developed a dietary tivity in the serum of both healthy people and patients with
strategy including the use of the inexpensive regional food type 2 diabetes 2 hours after consumption. The consumption
nopal to minimize postprandial glucose peaks. Our results of nopal could have a compensatory effect on the decreased
show that nopal has low glycemic and insulinemic indexes endogenous antioxidants during type 2 diabetes.
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 CONCLUSIONS
the IAUC for the total plasma GIP concentration. These The current epidemic of diabetes has led to a search for
results suggest that nopal could regulate blood glucose and functional foods that could aid in ameliorating this pathol-
serum insulin concentrations by modulating GIP levels. ogy. Nopal has long been used in traditional Mexican med-
Interestingly, the inclusion of steamed nopal in the HCB icine to control diabetes, however, there was insufficient
significantly reduced postprandial blood glucose peaks. scientific evidence regarding the ability of this plant to help
Remarkably, the HSPB and HSPBþnopal helped prevent control postprandial blood glucose peaks. Our results show
postprandial blood glucose peaks. These results are impor- that nopal has low glycemic, insulinemic, and GIP indexes
tant because recommendations from the American Diabetes and could be recommended for patients with type 2
Association are for patients with type 2 diabetes to maintain, diabetes. The inclusion of nopal in an HCB had anti-
“blood glucose levels in the normal range or as close to hyperglycemic and antihyperinsulinemic effects, and in the
normal as is safely possible.”17 The European Diabetes Policy HSPB, it prevented postprandial blood glucose peaks. The
Group has set the maximum postprandial glucose peak to not consumption of nopal increased the antioxidant activity in
exceed 135 mg/dL (7.5 mmol/L) to reduce arterial risk and both healthy people and patients with type 2 diabetes.
160 mg/dL (9.0 mmol/L) to reduce microvascular risk.18 The Nopal is not a complete replacement for prescription blood
inclusion of nopal in the HCB in patients with type 2 diabetes glucose drugs, but the findings in this study support the
reduced blood glucose by 36 mg/dL (2 mmol/L), reaching a traditional use of nopal for the safe management of glucose
value near that recommended by the European Diabetes without any side effects.
Policy Group. The presence of nopal in the HSPB helped
significantly to avoid blood glucose peaks reaching a value of
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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, Edificio 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 conflict 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.