International Journal of Gastronomy and Food Science 32 (2023) 100706

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International Journal of Gastronomy and Food Science

journal homepage: www.elsevier.com/locate/ijgfs

Nutritional and functional properties of corn tortillas added with cabbage

as an option for diabetes management
Jonatan Jafet Uuh Narvaez, Ulil Us Medina, David Muñoz Rodríguez,
Maira Rubi Segura Campos *
Faculty of Chemical Engineering, Autonomous University of Yucatán, Periférico Norte Km. 33.5, Tablaje Catastral, 13615, Colonia Chuburná de Hidalgo Inn, Merida,
Yucatan, Mexico

A R T I C L E I N F O A B S T R A C T

Keywords: Corn tortillas (CTs) are an essential part of the Mexican population’s diet, although they are not highly rec­
Corn tortillas ommended for the nutritional therapy of type 2 diabetes (T2D). Therefore, the integration of ingredients with
Functional foods functional properties, such as cabbage (Brassica oleracea var. capitata L.), can serve the development of healthier
Bioactive compounds
foods for T2D patients. This study evaluated nutritional value, mineral content, bioactive compounds, biological
Hyperglycemia
activity, and sensorial analysis of CTs combined with cabbage flour. CTs is developed with cabbage flour (w/w)
Antioxidant
as follows: 0% (T0), 5% (T5), 10% (T10), and 15% (T15). In the CTs added with cabbage flour, moisture, and
fiber increased, while fat content, nitrogen-free extract (NFE), and energy intake decreased. T15 had higher K,
Na, and Mg concentrations (p<0.05) than the other treatments. T10 and T15 had similar Ca, Fe, Zn, and P
contents to T5 and T0 (p<0.05). Total phenolic compounds (TPC) and total flavonoid content (TFC) in T15 were
13 and 380 times higher than in T0. T15 (p<0.05) inhibited DPPH, ABTS+, α-amylase, and α-glucosidase ac­
tivities. Taste, color, and overall impression were similar (p<0.05) between T0 and T15. The addition of 15%
cabbage flour improves CTs nutritional and functional properties; thus, this food could be an option for T2D.

1. Introduction low-income countries. In the indigenous south region of Mexico, be­

tween 2006 and 2018, DM went from 5.4% to 10.7%, an increase of
Since pre-Hispanic times, corn tortillas (CTs) have been an essential ~50%; also, mortality from the disease increased by 128% in the same
food in Mexico, providing a high degree of satiety. Likewise, CTs plays a period. Against this backdrop, health programs have not successfully
vital role in the context of poverty, mainly in indigenous populations, curbed the growing epidemic of T2D in this region (Loria et al., 2018).
making CTs consumption essential in daily dietary practices (Esca­ Lack of adherence to dietary recommendations, such as restricting
lante-Aburto et al., 2020; Juárez-Ramírez et al., 2019). Its main corn-based foods, such as CTs, is misaligned with the food culture and is
component is carbohydrates, which range between 44.08% and 87.56%, one of the significant obstacles facing medical intervention in this
depending on the nixtamalization conditions and the type of corn. Also, population (Juárez-Ramírez et al., 2019). In this context, the production
the pancreatic α-amylase rapidly hydrolyzes up to 70% of CT starch in of healthier CTs may be feasible to manage nutritional constraints
the first 15 min, increasing the glycemic response after intake (Esca­ without affecting the traditional dietary patterns of the population.
lante-Aburto et al., 2020). Hence, foods with the high glycemic Cabbage (Brassica oleracea var. capitata) is a cruciferous plant
response, such as CTs, are not highly recommended for the nutritional distinguished by its capsule-shaped morphology, cultivated and
therapy of patients with type 2 diabetes (T2D). consumed in different cultures worldwide. Regardless of its origin,
T2D is a metabolic disease characterized by hyperglycemia produced cabbage is important in the gastronomy and diet of people due to its
by alterations associated with oxidative stress, which damages accessible price, easy cultivation, and adaptability in many regions,
β-pancreatic cells and underlies the blockage of insulin signaling path­ including the indigenous. Scientific evidence shows that cabbage has
ways, leading to insulin resistance (Galicia-Garcia et al., 2020). T2D has functional properties that could be used in dietary therapeutic strategies
become one of the most common disorders affecting middle- and for T2D control (Uuh-Narvaez and Segura-Campos, 2021).

* Corresponding author.
E-mail address: [email protected] (M.R. Segura Campos).

https://doi.org/10.1016/j.ijgfs.2023.100706
Received 16 January 2023; Received in revised form 20 February 2023; Accepted 8 March 2023
Available online 9 March 2023
1878-450X/© 2023 Elsevier B.V. All rights reserved.
J.J. Uuh Narvaez et al. International Journal of Gastronomy and Food Science 32 (2023) 100706

Cabbage has been shown to regulate glucose by attenuating oxida­ 2.2. Production of cabbage flour
tive stress, insulin resistance, and hyperglycemia leading to T2D com­
plications. Cabbage has been shown to increase the production of The cabbage was washed with distilled water, disinfected for 5 min
endogenous antioxidants activated and inhibit the production of with a hypochlorite (200 ppm), and dried using paper towels. After
proinflammatory cytokines by improving insulin sensitization. It has removing the outermost leaves, the cabbage was sliced and dried for 36
also decreased glucose absorption by inhibiting digestive enzymes that h at 50 ◦ C in a convection oven (Thermo-Fisher Scientific® Precision,
hydrolyze carbohydrates (Uuh-Narváez et al., 2021). The antidiabetic Waltham, Massachusetts, USA). The dried leaves were ground into flour
properties of cabbage have been attributed to its many bioactive com­ using a Cyclotec 1093 mill (Tecator, Höganas, Sweden), which produced
pounds, such as fiber, phenolic compounds, flavonoids, and others some flour. Finally, the flour was kept in a desiccator at ambient tem­
(Uuh-Narváez et al., 2021). For this reason, it becomes a valuable source perature until analysis.
to improve CTs nutritional and functional value. Hence, it has become a
valuable source for improving CTs nutritional and functional value. This
2.3. CTs preparation
study evaluated the nutritional properties, total phenol (TPC) and
flavonoid content (TFC), and in vitro antidiabetic and antioxidant ac­
Commercial nixtamalized yellow corn flour was mixed with cabbage
tivity of CTs with the inclusion of cabbage flour.
flour at different concentrations (T5-5%, T10-10%, and T15-15%, w/w)
(Fig. 1). The corn flour alone was considered the control treatment (T0).
2. Materials and methods
The treatments were mixed with commercial corn flour (Maseca®) and
hydrated with purified water in a 1:1.5 w/v ratio until a dough was
2.1. Raw materials and reagents
obtained. Tortillas were obtained by passing the dough through a
RODOTEC-50 NG 3E ELITE tortilla machine (Tecnomaiz, S.A. de C.V.,
Yellow nixtamalized corn flour (Maseca®) was purchased at the local
Grupo Gruma, Mexico) for 2 min at 320 ◦ C. CTs had a diameter of 14 cm
market in Merida, Yucatan, Mexico. Cabbage was harvested in Tixme­
and a thickness of 1 mm, and each tortilla weighed 24 g. Subsequently,
huac, Yucatan, Mexico [20◦ 14’07 "N 89◦ 06’30 "E] in May 2021. About 2
the CTs were cooled, dried (50 ◦ C, 24 h), and milled. The flour obtained
kg of this vegetable was collected without stains or damage. The sample
from the tortillas was stored at − 20 ◦ C until analysis. A portion of the
was processed within 24 h between collections. The reagents and en­
tortillas from each treatment was used for sensory analysis within 6 h
zymes used in this study were acquired from J.T. Baker (Phillipsburg,
after processing.
NJ, USA) and Sigma Chemical Co., respectively (St. Louis, MO, USA).

2.4. Nutritional value of CTs

The nutritional content of the CTs was determined according to A.O.

Fig. 1. Corn tortillas added with cabbage at different concentrations (w/w): T0 as control (A); T5-5% (B), T10-10% (C), and T15-15% (D).

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J.J. Uuh Narvaez et al. International Journal of Gastronomy and Food Science 32 (2023) 100706

A.C. (1995) approved protocols for moisture (method 925.09), ash for 30 min. At a wavelength of 517 nm, the absorbance was measured.
(method 923.03), fiber (method 962.09), nitrogen (method 954.01), and The following equation was used to compute the percentage of
fat (method 920.39). Nitrogen x 6.25 was used to consider the protein inhibition:
content; the nitrogen-free extract (NFE) was estimated by subtracting [ ]
(Ab − As)
the other components from it. % radical scavening activity (%) = ∗ 100 (Eq. 1)
Ab
2.5. Mineral content determination of CTs
Where Ab is the DPPH radical’s absorbance in the absence of sample
extract and As is the DPPH radical’s absorbance in the presence of
The mineral content of CTs was determined by modifying the method
sample extract. Inhibition percentage (%) and antioxidant activity
described by Herman-Lara et al. (2019). Initially, 1 g of the sample was
equivalents for Trolox, CAT, and GAE were used to express the results.
digested with 3 mL of 65% HNO3 (Merck, Darmstadt, Germany) and
The Trolox (0.5–5 mg/mL), CAT (0.7–4.2 mg/mL), and GAE (0.1–1.5
heated (100 ◦ C) for 48 h. Then, the mixture was diluted (1: 250) with a
mg/mL) concentration vs. % inhibition were plotted to obtain the trend
solution of HNO3 (5%), and its content of major elements such as cal­
line equation and its correlation.
cium (Ca), potassium (K), magnesium (Mg), and sodium (Na), phos­
phorus (P), iron (Fe), and zinc (Zn) were assessed, employing a
2.10. ABTS +
radical scavenging activity
microwave-induced plasma atomic emission spectroscopy equipment
(MP-AES, 4200 MP-AES, Agilent Technologies, New Castle, Delaware,
The radical scavenging activity of ABTS+ was measured using a
USA) integrated to a nitrogen generator (Peak Genius 3055, Agilent
method modified by Pukalskas et al. (2002). First, a stock solution of
Technologies, New Castle, Delaware, USA). For Ca, Fe, K, Mg, and Na,
ABTS+ radical cation was produced by dissolving 54.8 mg of ABTS+ salt
the multi-element solutions were diluted to concentrations ranging from
in 50 mL phosphate-buffered saline (PBS, 0.01 M, and pH 7.4). The
0.5 to 5 μg/mL, and Na and concentrations from 0.2 to 2 μg/mL for P and
radical was produced after a 16-h dark reaction between 10 mL ABTS+
Zn. Mineral content in the samples was calculated by comparing a
solution and 40 μL potassium persulfate (K2S4O8, 70 mM). With ethanol,
standard curve for each element (R2 = 0.99) and the signal intensity of
the solution containing the released ABTS+ was adjusted to an absor­
each sample.
bance of 0.8 ± 0.30 at 734 nm. After 6 min, 3 μL of extract (150 mg/mL)
interacted with 297 μL of ABTS+ to determine the absorbance at 734 nm.
2.6. CTs water extract
The Trolox (0.12–0.87 mg/mL), CAT (0.052–0.62 mg/mL), and GAE
(0.017–0.25 mg/mL) concentration vs. % inhibition were plotted to
CTs flour (1.5 g) and distilled water (10 mL) were combined and
obtain the trend line equation and its correlation. Inhibition percentage
agitated for 3 h. For 15 min, the mixture was centrifuged at 704×g and
(%) and antioxidant activity equivalents for Trolox, CAT, and GAE were
filtered through Whatman® grade 50 filter paper (Thermo-Fisher Sci­
used to express the results.
entific). Total phenol content (TPC) and total flavonoid content (TFC)
were measured in the extracts, as well as antioxidant and antidiabetic
properties. The supernatant was employed in the above tests. The 2.11. α-Amylase inhibition assay
extraction was performed on the same day of each test (Uuh-Narváez
et al., 2021). According to Dineshkumar et al. (2011), α-amylase inhibition was
measured. Tris-HCl buffer (0.5 M, pH 6.9) with CaCl2 (0.01 M) was
2.7. TPC determination of CTs added to a tube containing 2 mg of starch. A 5 min boiling was per­
formed, followed by a 5 min cooling. After 5 min at 37 ◦ C, 100 μL of
TPC was measured using the Folin–Ciocalteu reagent and gallic acid extract and 200 μL of amylase (2.11 U/mL in buffer) were added and
as a standard (Lee et al., 2003). In a cell, 50 μL of Folin–Ciocalteu re­ incubated for 10 min at 37 ◦ C. Subsequently, 500 μL DNS (3,5-dinitro
agent (1:10) was mixed with 10 μL of the extract, homogenized for 30 s, salicylic acid) at 1% acid was added to the mixture and boiled for 10
and kept at room temperature for 2 min. Afterward, 40 μL of Na2CO3 min. Finally, absorbance was determined at 540 nm after cooling the
(75 mg/mL) was added, and the sample was incubated at 50 ◦ C for 15 sample. The α-amylase inhibition activity was calculated as follows:
min in the dark and then allowed to rest for 10 min. The 760 nm (Ac+ ) − (Ac− ) − (As − Ab)
wavelength was used to measure the absorbances of the samples and the Inhibition (%) = ∗ 100 (Eq. 2)
(Ac+ ) − (Ac− )
calibration curve standards. The results were derived by comparing the
absorbance of each sample to a standard curve (0–0.06 mg/mL gallic Ac+ is the absorbance when enzymes are present (solvent with
acid). The results are presented in mg of gallic acid equivalent (mg enzyme), Ac– is the absorbance when enzymes are not present (solvent
GAE/100g). without enzyme), and As is the absorbance when enzymes are present
with the extract (sample with enzyme). Ab is the absorbance of the blank
2.8. TFC determination of CTs (solvent) (sample without enzyme). Inhibition percentage (%) and
antidiabetic activity equivalents for CAT and GAE were used to express
TFC was calculated using catechin as a standard (Georgé et al., the results. The CAT (0.1–2 mg/mL) and GAE (0.05–0.6 mg/mL) con­
2005). In a cell, 20 μL extract was homogenized with 6 μL NaNO2 (5%). centration vs. % inhibition were plotted to obtain the trend line equation
Aqueous AlCl3–6H2O (10%) was added after 5 min 40 μL of NaOH (1.0 and its correlation.
M) was added after 6 min. The 510 nm absorbance was measured. The
data were determined by comparing each sample’s absorbance to a 2.12. α-Glucosidase inhibition assay
standard curve (0–0.06 mg/mL catechin). The results are presented in
mg of catechin equivalent (mg CAT/100 g). α-Glucosidase inhibition was determined according to Dineshkumar
et al. (2011). For 5 min at 37 ◦ C, 2 U/mL α-glucosidase and 20 μL extract
2.9. DPPH radical scavenging activity were incubated. Twenty p-NPG (para-nitrophenyl glucopyranoside)
microliters were added at 1 mM in phosphate buffer (50 mM, pH 6.8).
The radical scavenging activity of DPPH (α-diphenyl-β-picrylhy­ After 20 min at 37 ◦ C, the mixture was stopped by adding 50 μL (1 M) of
drazyl) was measured using the methods provided by Shimada et al. sodium carbonate. At 405 nm, the activity of α-glucosidase was
(1992), with some changes. 135 μL of DPPH radical (100 mM in ethanol) measured to assess the amount of para-nitrophenolate produced by
and 15 μL of extract (150 mg/mL) were mixed and kept in the darkness p-NPG. The inhibitory activity of α-glucosidase was determined

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J.J. Uuh Narvaez et al. International Journal of Gastronomy and Food Science 32 (2023) 100706

employing Eq. (2). Inhibition percentage (%), antidiabetic activity the treatments increase of 38.39–46.81 g/100g for T5 and T15,
equivalents for CAT, and GAE were used to express the results. The CAT respectively. Protein and ash concentration did not vary significantly
(0.75–1.75 mg/mL) and GAE (0.05–0.5 mg/mL) concentration vs. % (p<0.05) between treatments and control. The fat level reduced from
inhibition were plotted to obtain the trend line equation and its 3.21 g/100 g in T0 to 1.21–2.34 g/100 g in T5 and T10 in the tortillas
correlation. with cabbage. Fiber content increased from T0 (1.77 g/100 g of CTs) to
T5 (1.90 g/100 g of CTs) and T15 (2.48 g/100 g of CTs). T0 had the
2.13. Sensorial analysis highest value (62.80 g/100 g) in NFE, whereas the values of tortillas
with cabbage were 52.29–43.36 g/100 g for T5 and T15, respectively.
For the sensory evaluation, 52 subjects aged between 20 and 65 The energy of tortillas decreased (p<0.05), with the control having the
participated in this study. For sensory analysis, the tortilla with the highest (305.09 Kcal/100 g), and T5 and T15 had the lowest
highest addition of cabbage flour in this study (T15) was chosen, and its (242.93–205.64 Kcal/100 g).
attributes were compared with tortillas without cabbage flour (T0). The Cabbage flour significantly (p<0.05) and proportionately improved
evaluation was performed in the sensory evaluation laboratory of the the mineral content of the CTs when it was included in the formulation
Chemistry Engineering Faculty at the Autonomous University of Yuca­ (Table 1). The K, Na, and Mg concentrations in T15 were significantly
tan. A hedonic scale of seven described points that specify the liking higher (p<0.05) compared to the other treatments. However, Ca, Fe, Zn,
characteristic was used for the color, smell, taste, and texture test. The and P contents in T10 and T15 were statistically equal (p<0.05) and
points higher than 4 indicated the levels of liking: like (5), like a lot (6), higher than in T5 and T0.
and like very much (7); the points lower than 4 were about the dislike The addition of cabbage flour decreased the NFE content (− 30.95%)
levels: dislike (3), much dislike (2) and very much dislike (1). Each judge and increased the fiber content (+34.46%) at the highest concentration
was given a tortilla on a codified plastic plate, an answer sheet, and (T15) compared to T0. Therefore, adding cabbage flour possibly
water for washing themselves out among each tortilla. For the purchase replaced a part of the NFE by increasing the fiber content. As a result, the
intention test, panelists chose one of the following: would surely buy, energy content of the treatments was reduced, ranging from 20.37% to
would probably buy, maybe I would buy, or would probably not buy. 32.87%.
A high carbohydrate and low fiber content characterize CTs. Exces­
sive carbohydrate intake is associated with the development of T2D.
2.14. Statistical analysis
While fiber is a non-digestible carbohydrate, regardless of the type
(soluble or insoluble), it can affect glucose homeostasis. The possible
Triplicate analyses of the results using descriptive and inferential
mechanism of action of fiber possibly relates to decreasing postprandial
statistics were performed. One-way analysis of variance (ANOVA) was
hyperglycemia (PHG) due to its viscous properties that delay the ab­
used to determine the differences between treatments, followed by
sorption of hydrolyzable carbohydrates. Also, fiber consumption is
Tukey’s test. For the sensorial analysis, the non-parametric Kruskal-
linked to a lower incidence of T2D; the Mexican Ministry of Health
Wallis test was used (p<0.05). Statgraphics Centurion XVI (StatPoint
advises 25 g per day (Weickert and Pfeiffer, 2018).
Technologist, Warrenton, VA, USA) and GraphPad Prism® version 8.00
Moisture content increased with increasing cabbage flour concen­
were used for all analyses (GraphPad Software Inc., San Diego, CA,
tration, with up to 19.94% higher moisture content observed at T15 than
USA). The significance level for all analyses was set at p<0.05.
at T0. Previously, cabbage flour has been reported to have a high
rehydration rate, hygroscopicity, and swelling potential, as well as a
3. Results and discussion high absorption rate and water solubility. Therefore, these characteris­
tics could explain the increased moisture content in CTs added with
3.1. Nutritional value and mineral content of CTs cabbage flour (Waseem et al., 2022). Also, in the fat content, a decrease
in T5 is observed, but between T10 and T15, the changes were not
The addition of cabbage to CTs improved the nutritional content significant (p<0.05), possibly due to the low lipid intake by cabbage
(Table 1). The moisture of the control registered 26.87 g/100 g, while in flour and the increase of the other components, such as fiber.
Minerals are required for many metabolic events, and they have a
Table 1 dual function: they keep cell structures stable at ideal levels, but their
Nutritional value (g/100 g d.b.) and mineral content (μg/100 g d. b.) of corn deficiency leads to other routes, which can lead to illness (Dubey et al.,
tortillas added with cabbage.
2020). Minerals such as Ca, P, Mg, Fe, Na, K, Cu, and Zn, play an
Parameter T0 T5 T10 T15 essential role in intracellular response and biological processes,
Humidity 26.87 ± 0.97c 38.39 ± 0.50b 40.01 ± 0.27b 46.81 ± 0.85a including cell division and death, and changes in homeostasis, particu­
Protein 5.78 ± 0.05a 5.58 ± 0.79a 4.97 ± 0.6a 4.95 ± 0.59a larly of Zn, have been linked to T2D and insulin resistance (Barman and
Fiber 1.77 ± 0.16c 1.90 ± 0.06bc 2.48 ± 0.00a 2.38 ± 0.22a Srinivasan, 2020; Dubey et al., 2020). Therefore, dietary supplementa­
Fat 3.21 ± 0.38a 1.21 ± 0.05c 2.34 ± 0.12b 1.98 ± 0.28b
tion of these minerals may reduce oxidative stress and insulin resistance
Ash 1.10 ± 0.43a 1.27 ± 0.04a 1.19 ± 0.08a 1.19 ± 0.07a
N.F.E. 62.80 ± 0.87a 52.29 ± 2.01b 50.62 ± 2.72b 43.36 ± 1.06c and improve glycemic indices in T2D patients. Thus, CTs with cabbage is
Energy 305.09 ± 242.93 ± 242.26 ± 35b 205.62 ± a high-nutrient food that may aid in controlling T2D.
(kcal) 1.16a 2.13b 5.62c
Ca 115.32 ± 169.89 ± 186.58 ± 191.71 ±
3.2. Quantification of phenols and flavonoids in CTs
3.17c 9.41b 2.47a 9.61a
K 100.35 ± 201.15 ± 205.44 ± 236.31 ±
1.30c 2.22b 2.20b 4.15a The TPC and TFC in the CT treatments are presented in Table 2. The
Na 13.48 ± 0.40c 21.59 ± 2.87b 25.98 ± 1.59b 31.87 ± 0.93a treated CTs significantly (p<0.05) increased TPC and TFC compared to
Mg 30.44 ± 44.72 ± 1.06c 47.23 ± 0.56b 53.25 ± 1.22a T0. Additionally, TPC and TFC improved as the concentration of cab­
0.87d
Fe 0.61 ± 0.04c 0.86 ± 0.05b 1.07 ± 0.04a 1.20 ± 0.08a
bage flour in the CTs improved. Treatment T15 exhibited the highest
Zn 1.66 ± 0.07c 2.33 ± 0.04b 2.38 ± 0.04ab 2.40 ± 0.00a TPC and TFC with 926.84 and 383.51 mg/100g, respectively, compared
P 106.61 ± 137.19 ± 148.55 ± 153.43 ± to the other treatments (p<0.05). Thus, TPC and TFC in T15 were 13 and
1.58c 3.51b 1.52a 3.05a 380 times higher than in T0.
Average values ± of standard deviation (n = 3). Superscripts of different letters Phenols and flavonoids are secondary metabolites present in many
in the same row indicate a significant difference (p<0.05) determined by Tukey vegetables. These compounds have been related to various biological
test. NFE: extract free nitrogen. activities such as antioxidant and antidiabetic. The consumption of 500

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J.J. Uuh Narvaez et al. International Journal of Gastronomy and Food Science 32 (2023) 100706

Table 2 Antioxidant compounds could decrease oxidative stress by inhibiting

Total phenolic and flavonoids content (mg/100 g d.b.) and antioxidant activity the formation of reactive oxygen species and free radicals. By inhibiting
of corn tortillas added with cabbage. these reactive species, the involvement of important pathways in insulin
Parameter T0 T5 T10 T15 receptor signaling, and thus the development of insulin resistance, is
Bioactive compounds content
prevented. Thus, reducing oxidative stress also indirectly affects blood
TPC (mg/GAE 100 71.55 ± 663.57 ± 757.12 ± 926.84 ± glucose levels by promoting insulin receptor sensitivity (Uuh-Narváez
g d.b.) 8.35 46.24 25.46 33.38 et al., 2021).
TFC (mg/CAT 100 ND 99.19 ± 247.62 ± 383.51 ± Several studies have reported a decrease in the antioxidant activity of
g d.b.) 16.59 22.02 41.76
nixtamalized corn dough tortillas due to primary cooking conditions,
Antioxidant Activity
that is, because phenols and flavonoids are degraded (De La Parra et al.,
DPPH free radical scavenging activity 2007). In this context, some authors suggest increasing the biological
Inhibition (%) 13.92 ± 22.44 ± 30.80 ± 40.34 ±
0.24d 1.21c 0.48b 0.96a
activity of tortillas by adding active biological compounds reported an
mg eq Trolox 1.43 ± 2.22 ± 2.98 ± 0.04b 3.86 ± antioxidant activity of tortillas elaborated with 5% of Moringa oleifera of
0.02d 0.11c 0.09a 113.1 mg Trolox equivalent/100 g of the sample determined with DPPH
mg eq CAT 0.67 ± 1.31 ± 1.93 ± 0.04b 2.65 ± assay (Páramo-Calderón et al., 2019). Tortillas formulated with 10%
0.02d 0.09c 0.07a
sorghum bran flour inhibited DPPH above 8% (Buitimea-Cantúa and
mg eq GAE ND ND 0.43 ± 0.03b 1.01 ±
0.06a Serna-Saldívar, 2020). The authors showed that high polyphenols in the
ABTS free radical scavenging activity formula increased the antioxidant response. In the current study, the
Inhibition (%) 21.52 ± 26.06 ± 27.74 ± 35.37 ± antioxidant activity increased to increase the cabbage in the
0.74d 0.23c 1.96b 0.71a formulation.
mg eq Trolox 192.69 ± 225.86 ± 232.68 ± 295.47 ±
5.41c 1.65b 11.45b 4.96a
mg eq CAT 56.63 ± 76.23 ± 80.25 ± 117.34 ±
3.19c 0.98b 6.76b 2.93a 3.4. Antidiabetic activity of CTs
mg eq GAE 31.64 ± 39.43 ± 43.58 ± 54.93 ±
1.27d 0.39c 2.68b 0.96a The inhibitory effect of CTs with cabbage flour on α-amylase and
Average values ± of standard deviation (n = 3). Superscripts of different letters α-glucosidase activity is shown in Table 3. These results were expressed
in the same row indicate a significant difference (p<0.05) determined by Tukey as polyphenols (GAE and CAT) that showed a high inhibitory activity on
test. ND: non detected, CAT: catechin, GA: gallic acid. α-amylase and α-glucosidase (Oboh et al., 2016; Zhu et al., 2019). CTs
with cabbage flour on α-amylase inhibition was significant (p<0.05)
mg per day of these compounds can prevent the development and compared to T0 and dependent on cabbage flour concentration. T15
attenuate the complications of T2D through different mechanisms of showed the highest percentage inhibition, 44.33%, 0.4053 (mg eq.
action that regulate glucose. Integrating ingredients with high phenols GAE), and 0.9144 (mg eq. CAT). The treated CTs was a significant effect
and flavonoids in foods may increase functionality (Al-Ishaq et al., 2019; (p<0.05) on α-glucosidase inhibition compared to T0. However, the
Rienks et al., 2018). effect between T5, T10, and T15 was equal (p<0.05). The greatest effect
Previously, a significant correlation between TPC and TFC with on α-glucosidase corresponded to T15 with a percentage of 16.43% in­
antioxidant and antidiabetic activity has been reported (Moo-Huchin hibition, 0.7842 (mg eq. GAE), and 0.8531 (mg eq. CAT) (Table 3).
et al., 2013; Uuh-Narváez et al., 2021). Thus, the observed effects could PHG depends on many factors, including the meal’s timing, amount,
relate to bioactive compounds retained in treated CTs. Likewise, a composition, and carbohydrate content. CTs is a food with a high car­
higher TPC and TFC were observed compared to other studies that added bohydrate content (70%) hydrolyzed quickly during the first 15 min of
functional ingredients such as Pleurotus agaves (García-Rojas et al., its consumption. α-Amylase hydrolyzes starch, glycogen, and other oli­
2020), Opuntia ficus-indica/Persea americana mix (Rodiles-López et al., gosaccharides into maltose, maltotriose, and oligoglycans. α-Glucosi­
2019), or Brosimum alicastrum (Subiria-Cueto et al., 2019). dase then hydrolyzes the disaccharides into free glucose, raising blood
The cooking process degrades the content of bioactive compounds by glucose levels (Proença et al., 2017). Thus, a therapeutic target for PHG
up to 31% in red cabbage when boiled in water (4 min, 98 ◦ C). The control is to delay the breakdown of complex carbohydrates into free
cooking conditions of CTs in this work were 320 ◦ C/2 min; however, glucose by inhibiting key enzymes in carbohydrate metabolism.
retention of TPCs and TFCs was observed (Murador et al., 2016). The Cabbage has shown high inhibitory effects on α-amylase and
retention of these compounds was possibly due to the interaction be­
tween starch and phenolic compounds that formed complexes resistant Table 3
to the cooking process (Buitimea-Cantúa and Serna-Saldívar, 2020). In Inhibitory effect of corn tortillas added with cabbage flour on α-amylase and
that sense, a partial substitution of cabbage in tortillas provided a high α-glucosidase.
TPC and TFC. Parameter T0 T5 T10 T15

α-amylase inhibition
3.3. Antioxidant activity Inhibition 6.48 ± 1.95d 24.66 ± 37.76 ± 44.33 ±
(%) 2.80c 3.80b 2.92a
mg eq GAE 0.0144 ± 0.2021 ± 0.3387 ± 0.4053 ±
According to the DPPH and ABTS+ tests, the antioxidant activity of
0.02d 0.02c 0.03b 0.03a
CTs increased significantly (p<0.05) as the amount of cabbage in the mg eq CAT 0.0411 ± 0.4604 ± 0.7626 ± 0.9144 ±
formulation increased (Table 2). The treatment had more antioxidant 0.04d 0.06c 0.06b 0.07a
potential in the DPPH test than in the control. In this sense, T15 pre­ α-glucosidase inhibition
sented the most significant (p<0.05) inhibition of 40.34%, representing Inhibition 4.08 ± 2.39b 12.47 ± 14.20 ± 16.43 ±
(%) 1.28a 2.62a 1.06a
equivalents of Trolox, catechin, and gallic acid of 3.86, 2.65, and 1.01 mg eq GAE 0.0409 ± 0.1502 ± 0.1565 ± 0.1864 ±
mg/g of sample, respectively. In the ABTS+ assay evaluated in CTs with 0.05b 0.02a 0.04a 0.02a
cabbage, a significant increase (p<0.05) was observed in inhibiting free mg eq CAT 0.4851 ± 0.7701 ± 0.7842 ± 0.8531 ±
radicals compared to the control. The highest activity was observed in 0.07b 0.04a 0.08a 0.05a
T15 with inhibition of 35.37%, representing the equivalent of Trolox, Superscripts of different letters in the same row indicate a significant difference
catechin, and gallic acid of 295.47, 117.34, and 54.93 mg/g of sample, (p<0.05). Data corresponds to the average ± standard deviation of three rep­
respectively. licates. CAT; catechin; GAE; gallic acid.

5
J.J. Uuh Narvaez et al. International Journal of Gastronomy and Food Science 32 (2023) 100706

α-glucosidase activity in vitro and in vivo assays. In that sense, the results and 6.3–5.9, respectively. While taste, color, and overall impression
reported in this work indicate that it is possible to include it as a func­ acceptability had no significant changes (p<0.05) between T0 and T15.
tional ingredient and thus counteract PHG through the inhibition of The acceptability scores for T0 and T15 were 6.3 and 5.9 for flavor, 6.5
α-amylase and α-glucosidase. It is possible that some phenolic com­ and 6.4 for color, and 6.5 and 6.1 for overall impression, respectively.
pounds such as ferulic acid, caffeic acid, and chlorogenic acid, among Fig. 2b shows the results of the purchase intention for tortillas made
others, and flavonoids such as quercetin, catechin, kaempferol, and with corn dough and with 15% replacement of the dough by cabbage.
rutin, among others, are acting as inhibitors of α-amylase and α-gluco­ The judges who evaluated the T0 indicated that they would surely buy
sidase (Uuh-Narvaez and Segura-Campos, 2021). (75%), probably would buy (17.31%), maybe they would buy (5.77%),
It is essential to highlight the limited evidence in the study of the and probably would not buy (1.92%). While, for T15, the values regis­
antidiabetic effects of CTs added with any other functional ingredient tered for surely would buy (53.85%), probably would buy (26.92%),
(Subiria-Cueto et al., 2019). Milán-carrillo et al. (2019) demonstrated maybe would buy (11.54%), and probably would buy (7.69%).
that blue corn tortillas added with amaranth flour (30%) have an CTs with 15% cabbage had a greater acceptance than other CTs, such
elevated effect on α-amylase (IC50-28.67 mg/mL) and α-glucosidase as those containing soy (10%) and sardine protein (5%), which
(IC50-20.97 mg/mL) activity. On the other hand, CTs added with nopal increased nutritional value but were not sensory-approved
and avocado (5%–5%) decreased glucose (24.72%) in male Wistar rats (López-Alarcón et al., 2018; Waliszewski et al., 2002). Argüello-García
induced to obesity with a high caloric diet after 21 days of treatment et al. (2016) revealed that CTs with jatropha flour (up to 20%) could be
(Rodiles-López et al., 2019). acceptable and increase nutritional characteristics, like this study.
The information presented in this study suggests that ingredients Sensory evaluation showed that T15 was like T0, except for aroma and
such as cabbage could be an alternative for preparing healthier CTs with texture.
effects that could reduce PHG. Because cabbage has been shown to have Cruciferous plants like cabbage contain sulfur compounds called
several antidiabetic properties that could give it more support as a glucosinolates, which give them their unique odor. They also increase
functional ingredient for managing T2D. Likewise, further studies are glucose tolerance and insulin sensitivity and lower fasting blood glucose
needed to evaluate the effect of cabbage-added CTs on other therapeutic and glycosylated hemoglobin (Axelsson et al., 2017; Nagata et al.,
targets related to glucose regulation, such as increased insulin secretion 2017). The result showed that CTs with cabbage flour was pleasant and
and decreased insulin resistance. highly accepted by consumers, implying that producing CTs with high
nutritional and functional value and strong sensory acceptability might
3.4.1. Sensorial analysis be a commercially viable strategy.
Fig. 2A shows the sensory evaluation of T0 and T15 in various at­ On the other hand, intake of 100 g (wet basis) per day of cruciferous
tributes. Acceptability was considered for a more precise analysis with a vegetables, such as cabbage, was associated with a lower risk of all-cause
seven-level scoring system for each parameter evaluated. According to mortality, cancers, and depression, and their consumption is generally
the Kruskal-Wallis test, the smell and texture acceptability scores for T0 safe (Li et al., 2022). However, excessive consumption of cabbage can
and T15 showed significant differences (p<0.05) with a mean of 6.3–5.9 lead to flatulence and other stomach discomforts, mainly due to its
raffinose content (Moreb et al., 2020). After consumption, it can remain
in the intestine and be degraded by intestinal bacteria, leading to gas
production, which can cause bloating and discomfort in some people
(Moreb et al., 2020). Boiling (1 h) and soaking (12 h) decreased the
raffinose content in soybean flour by ~27% and ~45% (Singh and
Kayastha, 2013). Therefore, future studies could consider the applica­
tion of these treatments on cabbage flour to decrease its raffinose con­
tent. Despite the possible adverse effects of consuming CTs added with
cabbage flour, an intake of 50 g of tortillas (approximately 2 pieces)
would represent only 7.5 g of cabbage flour (dry basis), a safe dose
considering moisture content of ~92% (Uuh-Narváez et al., 2021).
The inclusion of cabbage flour as an ingredient improved the nutri­
tional and functional properties of the CTs compared to the untreated
product. The results are promising due to the increased antioxidant and
antidiabetic activity, and its acceptability demonstrated in the sensory
analysis. Also, CTs with cabbage could be an ideal vehicle with effects on
the general health of consumers, especially for the population with
diabetes or at risk of developing the disease. However, these results may
vary depending on where the raw materials are grown.

4. Conclusion

Cabbage can be used as an ingredient to prepare CTs with high

nutritional properties and functional value for managing T2D. CTs
nutritional and functional properties were significantly improved
(p<0.05) by adding up to 15% cabbage flour. Likewise, the sensory
analysis indicated high acceptance by the judges, with responses similar
to the control, except for the aroma and texture. This work highlights the
need to enhance the nutritional and functional value of essential foods
that are impossible to replace as CTs in the diets of diabetic patients in
Mexico.
Fig. 2. Sensory evaluation of corn tortillas added with cabbage flour. A) He­
donic evaluation; B) Buy intention. T0: corn tortillas without cabbage flour;
T15: corn tortillas with 15% (w/w) of cabbage flour.

6
J.J. Uuh Narvaez et al. International Journal of Gastronomy and Food Science 32 (2023) 100706

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