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A study on nutritional and functional study properties of Mayan plant foods as

a new proposal for type 2 diabetes prevention

Article  in  Food Chemistry · October 2020

DOI: 10.1016/j.foodchem.2020.128247

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 Food Chemistry 341 (2021) 128247

Contents lists available at ScienceDirect

Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem

A study on nutritional and functional study properties of Mayan plant foods T

as a new proposal for type 2 diabetes prevention
Jonatan Jafet Uuh-Narváez, María Alejandra González-Tamayo, Maira Rubí Segura-Campos
⁎

Facultad de Ingeniería Química, Universidad Autónoma de Yucatán, Periférico Norte Km. 33.5, Tablaje Catastral 13615, Colonia Chuburná de Hidalgo Inn., Mérida,
Yucatán, Mexico

ARTICLE INFO ABSTRACT

Keywords: Mayan communities cultivate a great variety of plant foods that could be of interest due to their nutritional and
Digestive enzymes functional potential. The aim of this study was to evaluate the nutritional value, glycemic index (GI), total
Antioxidants phenol content (TPC), and total flavonoid content (TFC), and in vitro antioxidant and antidiabetic activity of 24
Glycemic index plant foods of a Mayan community from the Yucatan Peninsula. Multivariate statistical analysis indicated that
Bioactive compounds
Psidium guajava L. (fruit), Cucurbita moschata (vegetable), Raphanus sativus L. (tuber), Brassica oleracea var. ca-
Antidiabetic activity
pitata L. (leaf), and Bixa orellana L. (seed) had the highest nutritional and functional value for each plant food
group. Principal component analysis suggested that TFC is a key feature to select plant foods with antidiabetic
potential. Mayan plant foods have nutritional and functional properties that can be used in the development of a
new proposal aimed at preventing type 2 diabetes.

1. Introduction maltose, maltotriose, and oligoglycans by α-amylase; subsequently, α-

The diabetes mellitus prevalence is increasing worldwide; this dis-
ease is a one major public health care problem. Type 2 diabetes mellitus
(T2DM) is characterized by insulin resistance and β cell dysfunction
resulting in the decline of insulin production and secretion. It is the
main form of DM, accounting for ~90% of diabetes cases.
Consequently, the exploration of foods with high nutritional and
functional value as an affordable and safe alternative for T2DM pre-
vention has become a topic of interest to the scientific community
(Wongsa, Chaiwarit, & Zamaludien, 2012).
Plant foods are a rich source of nutrients and bioactive compounds
with biological activity. An increase in their consumption is associated
with risk reduction of metabolic diseases such as T2DM. In this sense,
dietary components of food have a significant role in glucose home-
ostasis. Several studies have determined that replacing a percentage of
animal-derived lipids and proteins with vegetable-derived ones has
positive effects on the health of patients with T2DM (Russell et al.,
2016). In addition, the inclusion of plant foods with a high fiber content
and low glycemic index (GI) in the diet of patients with T2DM provides
desirable benefits in their treatment (Weickert & Pfeiffer, 2018).
Bioactive compounds such as phenols and flavonoids have been
shown to decrease blood glucose levels through the inhibition of key
enzymes in carbohydrate metabolism (α-amylase and α-glucosidase).
Starch, glycogen, and several oligosaccharides are hydrolyzed into
glucosidase hydrolyzes the disaccharides into free glucose, increasing
blood glucose levels (Proença et al., 2017). Therefore, α-amylase and α-
glucosidase inhibition is a key therapeutic target in T2DM management.
In addition, oxidative stress contributes to the formation of free radicals
that result in the development of insulin resistance, a complication of
T2DM (Van Der Schaft et al., 2019). For that reason, the control of
excess free radicals is a strategy for T2DM prevention and management.
In recent decades, there has been considerable interest in the study
of indigenous plant foods as potential promoters of health in developing
countries and to integrate their use in the modern medical system. In
this context, studies have reported a low prevalence of metabolic dis-
orders in rural areas of the Mediterranean basin due to the consumption
of plant foods rich in bioactive compounds that are cultivated in that
region. Many characteristics of plant foods in the Mediterranean diet
are functional components with positive effects on health and well-
being (Aguilera, Martin-Cabrejas, & González de Mejia, 2016). How-
ever, many of these plant resources are not cultivated in other regions.
For that reason, the study of plant resources in a specific region could
provide interesting information for the health of the consumer and
revalue their nutritional and functional properties.
The Yucatan Peninsula has unique geology, geomorphology, land-
scape, and biota; this region has been an historically important part of
the Mayan culture. In this region, traditional farming systems (milpa
and home gardens) are the main source of plant foods, which are part of

⁎
Corresponding author.

https://doi.org/10.1016/j.foodchem.2020.128247
Received 24 April 2020; Received in revised form 17 September 2020; Accepted 26 September 2020
Available online 01 October 2020
0308-8146/ © 2020 Published by Elsevier Ltd.
J.J. Uuh-Narváez, et al. Food Chemistry 341 (2021) 128247

Table 1 huchin, Estrada-Mota, Estrada-Leon, Cuevas-Glory, and Ortiz-Vazquez

Plant foods of Mayan community from Tixmehuac, Yucatan, Mexico as study (2013). The vegetal materials were cleaned with distilled water; edible
material. parts were extracted manually with a knife and cut into pieces, crushed
Scientific name Family Common Use edible part for 2 min in a blender to obtain a pulp, and stored at −20 °C until
name further analysis. Seeds and leaves were dried in an oven (Thermo-Fisher
Scientific® Precision, Waltham, Massachusetts, USA) at 50 °C for 24 h
Fruits
and then a flour was obtained, passing the samples through a Cyclotec
Averrhoa carambola L. Oxalidaceae Star fruit Peel + pulp
Psidium guajava L. Myrtaceae Guava Pulp 1093 mill (Tecator, Höganas, Sweden) (Wongsa et al., 2012). Finally,
Pouteria sapota (Jacq.) Sapotaceae Mamey Pulp dried and ground samples were stored at room temperature in a de-
Carica papaya L. Caricaceae Papaw Pulp siccator until further analysis. The pulps and flours were used to eval-
Hylocereus undatus (Haw.) Cactaceae Pitahaya Pulp + seed
uate nutritional value and the GI.
Vegetables To obtain the extracts, 5 g of pulps or flours was mixed with 100 mL
Cucurbita moschata Cucurbitaceae Pumpkin Peel + pulp distilled water and stirred for 3 h. The mixture was centrifuged
Sechium edule (Jacq.) Cucurbitaceae Chayote Peel + pulp
Capsicum chinense (Jacq.) Solanaceae Habanero Peel + pulp
(Thermo-Fisher Scientific SL8) at 704 g for 15 min and filtered using a
pepper Whatman® grade 50 filter paper (Thermo-Fisher Scientific). The su-
Solanum lycopersicum L. Solanaceae Tomato Peel + pulp pernatant was stored at −20 °C until analysis (Sulaiman & Ooi, 2014).
Cucumis sativus L. Cucurbitaceae Withe pulp The extracts were used to measure total phenol content (TPC) and total
cucumber
flavonoid content (TFC), and to evaluate antioxidant and antidiabetic
Tubers activities.
Ipomoea batatas Convolvulaceae Sweet potato Root
Raphanus sativus L. Brassicaceae Radish Root
Beta vulgaris L. Amaranthaceae Beetroot Root 2.3. Nutritional value
Manihot esculenta Euphorbiaceae Cassava Root

Leaves The nutritional value of Mayan plant food pulps and flours was
Coriandrum sativum L. Apiaceae Coriander Leaves determined using official procedures from A.O.A.C. (1997): humidity
Dysphania ambrosioides Amaranthaceae Epazote Leaves (method 925.09), nitrogen (method 954.01), fat (method 920.39), fiber
Mentha spicata L. Lamiaceae Mint Leaves (method 962.09), and ash (method 923.03). Protein content was cal-
Opuntia ficus-indica Cactaceae Nopal Leaves
Brassica oleracea var Brassicaceae Cabbage Leaves
culated as nitrogen × 6.25, and carbohydrate (NFE) content was esti-
capitata L. mated as the remainder after subtracting the rest of the components.
Seeds
Bixa orellana L. Bixaceae Achiote Seeds 2.4. In vitro GI determination
Phaseolus lunatus L. Leguminosae Ibes Seeds
Lens culinaris Leguminosae Lentilis Seeds The GI was determined by in vitro starch hydrolysis according to the
Zea mays L. Poaceae Corn Seeds
Vigna unguiculata L. Leguminosae X’pelon bean Seeds
method of Goñi, Garcia-Alonso, and Saura-Calixto (1997). Pulps and
flours (50 mg) were incubated with 0.2 mL pepsin (100 mg/mL) in
10 mL HCl-KCl buffer (pH 1.5) at 40 °C for 60 min in a shaking water
the populations’ diet and of the productive activity in Mayan commu- bath (New Brunswick Scientific Model R76, Edison, NJ, USA). Subse-
nities. A distinctive feature of milpas and home gardens is the presence quently, the mixture was diluted with 25 mL phosphate buffer (pH 6.9),
of a great diversity of introduced and native species from several groups followed by the addition of 5 mL (0.5 mg/mL) α-amylase; the mixture
of vegetables, fruit trees, spices, and condiments (Uuh-Narvaez & was incubated at 37 °C in a shaking water bath. One milliliter aliquots
Segura-Campos, 2020). However, nutrimental and functional properties were taken every 30 min from 0 to 3 h and boiled for 15 min to in-
of plant foods commonly consumed in Mayan communities on diseases activate the enzyme. To convert the residual starch into glucose, 3 mL
such as T2DM have been poorly studied. In addition, because abiotic of sodium acetate buffer (0.4 M and pH 4.75) and 60 µL amylogluco-
conditions of the region can modify bioactive compound concentra- sidase was added to the sample and incubated at 60 °C for 45 min. The
tions, research on this matter is necessary. The objective of the study volume was adjusted to 10 mL with distilled water, and 0.5 mL aliquots
was to evaluate the nutritional and functional potential of plant foods of were taken and incubated with 1 mL glucose oxidase/peroxidase for
a Mayan community from the Yucatan Peninsula as an alternative for 30 min at 37 °C. The absorbance of the mixture was measured at
T2DM prevention and treatment. 500 nm. Glucose (50 mg) was used as a control. The starch converted
into glucose was multiplied by 0.9. The rate of starch digestion is ex-
pressed as the percentage of hydrolyzed starch at different times (30,
2. Material and methods
60, 90, 120, and 180 min). The following first order equation was used
to determine the hydrolysis curve:
2.1. Raw materials and reagents
C t = CE (1 e kt )
(1)
Twenty-four plant foods, which are commonly cultivated in Mayan t
communities, were collected from milpas and home gardens in where C is the concentration at time t, CE is the remaining con-
Tixmehuac, Yucatan, Mexico [20°14′07″N 89°06′30″E] from June to centration, k is a kinetic constant, and t is time. The area under the
August 2018 (Table 1). About 2 kg of each plant food was collected hydrolysis curve (AUC, 0–180 min) was calculated by following equa-
without blemish and injury and classified into five groups for the study. tion:
The samples were processed within a 24 h interval between collection CE kt (tf t 0) )]
AUC = CE (tf t 0) [ (1 e
and extraction. Analytical grade reagents and enzymes were purchased k (2)
from J.T. Baker (Phillipsburg, NJ, USA) and Sigma Chemical Co. (St.
Louis, MO, USA). where t0 is the initial time (0 min) and tf is the final time (180 min).
The hydrolysis index (HI) was calculated as the relation between the
AUC for a sample and the AUC for a standard multiplied by 100. Thus,
2.2. Sample preparation and water extraction
the estimated glycemic index (GIe) was calculated by:

Fruits, vegetables, and tubers were processed according to Moo- GIe = 39.71 + (0.549HI ) (3)

2
J.J. Uuh-Narváez, et al.
2.5. TPC determination
TPC was determined according to Lee, Kim, Lee, and Lee (2003),
using the Folin–Ciocalteu reagent and gallic acid as a standard. One-
hundred microliters from the extract was placed with 500 µL Fo-
lin–Ciocalteu reagent (diluted 1:10 in distilled water) in a cell, homo-
genized for 30 s with a vortex, and incubated at room temperature for
2 min. Then, 400 µL Na2CO3 (75 mg/mL) was added, the sample was
incubated for 15 min at 50 °C in the dark, and, finally, allowed to rest
for 10 min. The absorbances of the samples and calibration curve
standards were determined at 760 nm. Data were calculated by a
comparison between a standard curve (0–0.06 mg/mL of gallic acid)
and the absorbance of each sample. The results are expressed in mg
equivalent of gallic acid per g of 100 g of sample (pulp or flour) (mg
GAE/100 g).
2.6. TFC determination
TFC was determined according to Georgé, Brat, Alter, and Amiot
(2005), using catechin as a standard. Two-hundred-fifty microliters
extract was added to 250 µL NaNO2 solution (5% w/v) in a cell and
homogenized. After 5 min, 125 µL aqueous AlCl3·6H2O (10% w/v) was
added. After 6 min, 124 µL 1.0 M NaOH was added. The absorbance at
490 nm was determined. Data were calculated by a comparison be-
tween a standard curve (0–0.06 mg/mL of catechin) and the absorbance
of each sample. The results are expressed in mg equivalent of catechin
per g of 100 g sample (pulp or flour) (mg CAT/100 g).
2.7. Antioxidant activity
2.7.1. α-Diphenyl-β-picrylhydrazyl radical scavenging activity
The α-diphenyl-β-picrylhydrazyl (DPPH) radical scavenging activity
was determined using the methodology proposed by Deladino,
Anbinder, Navarro, and Martino (2008), with some modifications. A
mixture of 175 µL DPPH radical (100 µM in methanol) and 25 µL ex-
tract (50 mg/mL) was shaken and stored in the dark for 30 min. The
absorbance was measured at 517 nm. The results were calculated using
the following equation: DPPH radical scavenging activity
(%) = [(Ab − Ae)/Ab] × 100, where Ab is the absorbance of the DPPH
radical without extract and Ae is the absorbance of the DPPH radical in
the presence of extract.
2.7.2. 2,2′-Azino-bis-(3-ethylbenzothiazoline)-6-sulfonic acid radical
scavenging activity
The 2,2′-azino-bis-(3-ethylbenzothiazoline)-6-sulfonic acid (ABTS)
radical scavenging activity was determined according to the method
proposed by Zhou et al. (2018), with some modifications. The ABTS
cation was released through the interaction of ABTS (7 mM) with po-
tassium persulfate (2.45 mM) for 16 h in the dark. The solution with the
released ABTS cation was adjusted with ethanol to an absorbance of 0.7
( ± 0.02) at 734 nm. Subsequently, 10 µL extract (50 mg/mL) was re-
acted with 195 µL ABTS radical solution and the absorbance was
measured after 6 min at 734 nm. The results were calculated using the
following equation: ABTS radical scavenging activity
(%) = [(Ab − Ae)/Ab] × 100, where Ab is the absorbance of the ABTS
radical without extract and Ae is the absorbance of the ABTS radical in
the presence of the extract.
2.8. Antidiabetic activity
2.8.1. α-Amylase inhibition assay
α-Amylase inhibition was determined with the method of
Dineshkumar, Mitra, and Mahadevappa (2011). Starch (2 mg) was
added in a tube with 200 µL 0.5 M Tris-HCl buffer (pH 6.9) with 0.01 M
CaCl2. The tube was boiled for 5 min and cooled at room temperature
for 5 min. It was then incubated at 37 °C for 5 min. Two-hundred
3
Food Chemistry 341 (2021) 128247
microliters 50% dimethyl sulfoxide (DMSO) was added to the control
group and to the extract (50 mg/mL) to be evaluated. Then, 2.11 U/mL
α-amylase in 200 µL buffer was added and incubated at 37 °C for
10 min. Subsequently, 500 µL 0.1% 3,5-dinitro salicylic acid (DNS) was
added and incubated at 100 °C for 10 min. It was then cooled at room
temperature for 10 min. Finally, the absorbance was determined at
540 nm. The assay was performed in triplicate and α-amylase inhibition
was calculated as follows:
(Ac+) (Ac ) (As Ab)
%inhibition = × 100
(Ac+) (Ac ) (4)
where Ac+ is the absorbance when the enzyme acts without inter-
ference (solvent with enzyme), Ac– is the absorbance when the enzyme
does not act (solvent without enzyme), As is the absorbance when the
enzyme acts in the presence of sample (sample with enzyme), and Ab is
the absorbance of the blank (sample without enzyme).
2.8.2. α-Glucosidase inhibition assay
α-Glucosidase inhibition was determined according to Dineshkumar
et al. (2011). A mixture of 2 U/mL α-glucosidase and 20 µL extract
(50 mg/mL) was incubated for 5 min at 37 °C. Twenty microliters 1 mM
para-nitrophenyl glucopyranoside (pNPG) dissolved in phosphate
buffer (50 mM, pH 6.8) was added. The mixture was incubated at 37 °C
for 20 min, and the reaction was stopped by adding 50 µL 1 M sodium
carbonate. α-Glucosidase activity was determined at 405 nm to quan-
tify the amount of para-nitrophenolate released by pNPG. The assay was
performed in triplicate and the α-glucosidase inhibitory activity was
calculated according to Eq. (4).
2.9. Statistical analysis
The results were analyzed in triplicate using descriptive and in-
ferential statistics. One-way analysis of variance (ANOVA) followed by
Tukey’s test was performed to determine the differences between
treatments. Pearson correlation tests were performed to determine the
correlations between variables (biological activities, GI, TPC, and TFC).
A multifactor ANOVA (followed by Tukey’s test) was applied to de-
termine which plant foods (per group) had greater nutritional (fiber,
protein, and lipid content) and functional (biological activities, TPC,
and TFC) properties. Principal component analysis (PCA) was per-
formed to reduce the dimensionality of the correlated variables; an
eigenvalue > 1 was considered significant. All analyses were per-
formed using Statgraphics Centurion XV (Manugistics Inc., Rockville,
MD, USA) and GraphPad Prism® version 7.00 (GraphPad Software Inc.,
San Diego, CA, USA). For all analyses, p ≤ 0.05 was considered sig-
nificant.
3. Results and discussion
3.1. Nutritional value
Table 2 presents nutritional values of 24 Mayan plant foods. In
general, the range of moisture, ash, fiber, lipids, protein, and NFE of the
evaluated foods ranged from 2.67% to 96.92%, 2.86% to 36.52%,
2.66% to 35.11%, 0.02% to 7.25%, 0.44% to 25.77%, and 47.12% to
92.13%, respectively. The highest nutritional value for each plant food
group (fruits, vegetables, tubers, leaves, and seeds) were: Averrhoa
carambola (90.81%), Crocus sativus (96.92%), Coriandrum sativum
(94.49%), Brassica oleracea (92.75%), and Vigna unguiculata (9.29%) in
moisture; Pouteria sapota (36.52%), Capsicum chinense (7.47%),
Morchella esculenta (19.68%), Mentha spicata (8.78%), and Bixa orellana
(9.27%) in ash; Psidium guajava (35.01%), Saccharum edule (21.29%),
Raphanus sativus (12.19%), C. sativum (12.68%), and Zea mays (16.84%)
in fiber; Hylocereus undatus (1.01%), Cucurbita moschata (0.92%), M.
esculenta (0.83%), Dysphania ambrosioides (3.79%), and B. orellana
(7.25%) in lipids; P. sapota (0.44%), C. moschata (1.47%), R. sativus
J.J. Uuh-Narváez, et al. Food Chemistry 341 (2021) 128247

Table 2
Proximal composition (% dry basis) and glycemic index of plant foods.
Plant food Moisture Ash Fiber Lipid Protein NFE GI

Fruits
Averrhoa carambola L. (90.81 ± 0.05a) 8.86 ± 0.05c 10.04 ± 0.33b 0.10 ± 0.00c 0.78 ± 0.01c 80.22 ± 0.39a 45.30 ± 2.29b
Psidium guajava L. (82.90 ± 0.75b) 16.66 ± 0.73b 35.01 ± 1.18a 0.57 ± 0.08b 0.64 ± 0.03d 47.12 ± 0.51e 40.14 ± 2.73c
Pouteria sapota (Jacq.) (62.59 ± 0.17c) 36.52 ± 0.29a 6.07 ± 4.03d 0.97 ± 0.08a 1.41 ± 0.080a 55.03 ± 1.28d 54.04 ± 1.25a
Carica papaya L. (90.36 ± 0.54a) 9.30 ± 0.51c 12.13 ± 2.11b 0.38 ± 0.01b 0.44 ± 0.03e 77.75 ± 0.67b 56.34 ± 2.47a
Hylocereus undatus (Haw.) (84.01 ± 0.73b) 15.58 ± 0.56b 9.21 ± 1.61c 1.01 ± 0.01a 0.92 ± 0.05b 73.28 ± 0.56c 44.01 ± 0.76bc

Vegetables
Cucurbita moschata (94.50 ± 0.10b) 5.21 ± 0.06b 10.85 ± 1.75b 0.92 ± 0.01a 1.47 ± 0.07a 81.55 ± 2.47b 71.32 ± 1.76a
Sechium edule (Jacq.) (94.81 ± 0.33b) 5.05 ± 0.28b 21.29 ± 5.75a 0.40 ± 0.01b 1.09 ± 0.12b 72.17 ± 3.08c 57.72 ± 5.01b
Capsicum chinense (Jacq.) (91.99 ± 0.09c) 7.47 ± 0.10a 20.37 ± 0.50a 0.54 ± 0.13b 1.42 ± 0.01a 70.20 ± 0.19c 29.75 ± 2.02d
Solanum lycopersicum L. (94.53 ± 0.94b) 5.09 ± 0.91b 1.04 ± 0.00c 0.87 ± 0.25a 0.93 ± .07b 92.13 ± 1.23a 37.38 ± 3.82c
Cucumis sativus L. (96.92 ± 0.06a) 2.86 ± 0.08c 9.41 ± 1.47b 0.17 ± 0.01c 0.76 ± 0.04c 86.80 ± 1.60b 26.67 ± 2.25d

Tubers
Ipomoea batatas (83.78 ± 1.09c) 15.43 ± 1.09b 3.31 ± 0.14c 0.43 ± 0.07b 0.62 ± 0.02b 80.21 ± 0.33a 66.41 ± 1.53a
Raphanus sativus L. (94.49 ± 0.23a) 4.77 ± 0.19d 12.19 ± 0.04a 0.43 ± 0.00b 1.81 ± 0.42a 80.80 ± 0.67a 30.12 ± 1.26c
Beta vulgaris L. (92.17 ± 0.03b) 7.20 ± 0.04c 9.61 ± 2.97b 0.02 ± 0.01c 1.53 ± 0.27a 81.64 ± 3.29a 59.28 ± 2.18b
Manihot esculenta (79.64 ± 0.58d) 19.68 ± 0.56a 3.92 ± 0.09c 0.83 ± 0.16a 1.68 ± 0.05a 70.60 ± 0.86b 57.58 ± 1.74b

Leaves
Coriandrum sativum L. (86.44 ± 0.69c) 7.44 ± 1.73ab 12.78 ± 0.27a 3.03 ± 0.24a 12.76 ± 0.16b 63.99 ± 0.81b 33.12 ± 3.24a
Dysphania ambrosioides (82.31 ± 0.09d) 8.54 ± 0.54a 9.18 ± 0.11b 3.79 ± 0.05a 19.10 ± 2.42a 59.39 ± 1.47c 30.35 ± 1.62a
Mentha spicata L. (82.70 ± 1.47d) 8.78 ± 1.25ab 2.66 ± 0.19c 3.64 ± 1.34a 16.60 ± 0.51a 68.26 ± 0.98a 31.54 ± 1.86a
Opuntia ficus-indica (89.86 ± 0.41b) 6.62 ± 0.85b 12.41 ± 0.21a 1.50 ± 0.05b 8.91 ± 0.38c 70.56 ± 2.49a 33.26 ± 2.07a
Brassica oleracea var capitata L. (92.75 ± 0.16a) 6.89 ± 0.22b 11.11 ± 1.75ab 1.28 ± 0.04b 12.90 ± 0.10b 67.82 ± 1.35a 29.78 ± 2.43a

Seeds
Bixa orellana L. (2.67 ± 0.06d) 9.27 ± 0.06a 13.48 ± 1.52ab 7.25 ± 2.61a 17.19 ± 0.13c 47.19 ± 1.05c 41.44 ± 1.00c
Phaseolus lunatus L. (7.61 ± 0.22c) 8.90 ± 0.30ab 5.49 ± 0.19c 0.56 ± .001d 22.67 ± 0.48b 62.38 ± 0.24b 50.97 ± 4.29b
Lens culinaris (9.86 ± 0.03a) 8.64 ± 0.10b 16.84 ± 2.01a 0.49 ± 0.00e 22.62 ± 0.06b 74.78 ± 2.17a 44.93 ± 0.98c
Zea mays L. (8.47 ± 0.43b) 3.56 ± 0.50c 13.19 ± 0.77b 1.21 ± 0.01b 10.12 ± 0.88c 71.92 ± 2.16a 67.92 ± 4.65a
Vigna unguiculata L. (9.29 ± 1.20ab) 3.89 ± 1.24c 11.74 ± 2.24b 1.08 ± 0.00c 25.77 ± 1.20a 57.52 ± 4.68b 47.99 ± 3.04bc

Different letter superscripts in the same column of plant foods group indicate significant difference (p ≤ 0.05). Data correspond to the average ± standard deviation
of three replicates. NFE: nitrogen free extract; GI: glycemic index.

(1.81%), D. ambrosioides (19.10%), and V. unguiculata (25.77%) in
protein; and A. carambola (80.22%), Solanum lycopersicum (92.13%),
Beta vulgaris L. (81.64%), Opuntia ficus-indica (70.56%), and Lens culi-
naris (74.78%) in NFE.
Increased plant food consumption has been associated with a de-
crease in the rate and risk of developing chronic non-communicable
diseases, including T2DM. Thus, dietary patterns and macronutrient
sources have been shown to play an important role in T2DM manage-
ment and prevention. In this study, the leaf and seed groups showed the
highest protein values (8.91% to 27.77%) compared with fruits, vege-
tables and tubers (< 1.81%). Replacement of 5% of the total intake of
animal proteins by plant proteins have been associated with a 23%
reduction in the T2DM risk, with beans, nuts, and peanuts being the
main sources of protein substitution (Russell et al., 2016). The me-
chanism of action is possibly related to the variation of the amino acid
composition, mainly of branched chain and aromatic amino acids,
which are very prominent in red meat and are related to a higher in-
cidence of T2DM.
Mayan plant foods registered lipid values less than 3.79%, except
for B. orellana (7.25%). Lipids do not have a direct effect on blood
glucose levels. However, they are directly related to other T2DM risk
factors such as insulin resistance. For this reason, plant sources are
more advantageous compared with animal sources due to their low
saturated fatty acid content.
The evaluated plant foods showed > 6% fiber content, except S.
lycopersicum, Ipomoea batatas, M. esculenta, M. spicata, and Phaseolus
lunatus (< 5%). Fiber is the most relevant macronutrient for T2DM
treatment; regular consumption of 25 g per day can reduce the T2DM
risk by up to 30% (Weickert & Pfeiffer, 2018). Plant foods are the main
fiber source, and both soluble and insoluble forms exert a beneficial
effect on glucose homeostasis. Soluble fiber effects include an increase
in satiety and a decrease in postprandial glucose and total and low-
density cholesterol levels. Insoluble fiber effects are an increase in the
time of intestinal transit and a decrease in insulin resistance. Other
effects such as decreased energy density, weight, and inflammation are
shared by both fiber types (Weickert & Pfeiffer, 2018).
3.2. Gi
The concept of GI was developed as tool for diabetic patients to
select foods. A food’s GI is defined according to how it affects blood
glucose levels after consumption; it is classified as low (≤55), medium
(56–69), and high (≥70) (Oboh et al., 2015). The slower the absorption
of carbohydrates, the lower the blood glucose levels and, therefore, the
lower the GI. The composition and microstructure of the food, the
starch profile, the range of amylose and amylopectin, as well as the
presence of secondary metabolites are contributing factors in a food’s GI
(Oboh et al., 2015). The GI range of plant foods evaluated in this study
ranged from 26.67 to 71.32; most foods showed a GI ≤ 55 (low). By
group, the lowest GI values were: the fruit P. guajava (40.14), the ve-
getable C. sativus (26.67), the tuber R. sativus (30.12), the leaf B. oler-
acea (29.78), and the seed B. orellana (41.44) (Table 2).
Studies have shown that foods with a low GI can improve the health
and glycemic response of patients with T2DM. Likewise, organizations
have specifically recommended diets with low GI foods. However,
dietary recommendations based only on GI may be insufficient, because
a low GI does not always mean a food has high nutritional value.
Indeed, foods such as Z. mays, with a GI of 67.92 (average) reported in
this work, is an irreplaceable food of the Mayan population due to its
high energy content. In addition, C. moschata (71.32) has been shown to
have functional properties such as anti-inflammatory (Mohanraj &
Sivasankar, 2013). Hence, in addition to the GI, it is important to
consider other nutritional and functional aspects of food for patients
with T2DM.

4
J.J. Uuh-Narváez, et al. Food Chemistry 341 (2021) 128247

Table 3
Bioactive compounds (Total phenolic and flavonoids content), antioxidant and antidiabetic activities of plant foods.
Plant food TPC (mg GAE/100 g) TFC (mg CAT/ DPPH free radical ABTS free radical α-amylase inhibition α-glucosidase
100 g) scavenging activity (%) scavenging activity (%) activity (%) inhibition activity
(%)

Fruits
Averrhoa carambola L. 46.50 ± 3.04c 14.61 ± 2.30c 16.29 ± 0.91c 39.05 ± 0.89d 92.99 ± 2.48b 16.85 ± 1.20b
Psidium guajava L. 101.75 ± 2.53a 161.83 ± 2.48a 79.92 ± 3.76a 45.18 ± 0.22c 93.46 ± 0.12b 76.62 ± 3.95a
Pouteria sapota (Jacq.) 80.13 ± 2.20b 26.25 ± 1.94b 37.32 ± 0.87b 49.98 ± 0.54b 98.92 ± 0.21a 5.52 ± 0.44c
Carica papaya L. 36.88 ± 4.64d 13.72 ± 3.27c 8.88 ± 0.85e 48.64 ± 0.61b 97.92 ± 0.99a 10.5 ± 3.66c
Hylocereus undatus 21.20 ± 4.55e 30.18 ± 6.47b 12.60 ± 1.03d 53.60 ± 0.03a 97.750.54a 10.2 ± 0.95c
(Haw.)

Vegetables
Cucurbita moschata 78.70 ± 3.86a 68.15 ± 2.17a 9.90 ± 0.71bc 24.87 ± 0.26e 88.32 ± 0.08b 6.44 ± 0.28a
Sechium edule (Jacq.) 16.29 ± 5.40bc 34.48 ± 1.46c 7.71 ± 1.66c 26.80 ± 0.33d 92.83 ± 0.29a 3.95 ± 2.33b
Capsicum chinense 74.19 ± 2.54a 50.31 ± 1.94b 33.40 ± 2.07a 48.09 ± 0.41c 64.76 ± 0.35c 6.98 ± 1.61a
(Jacq.)
Solanum lycopersicum 13.47 ± 1.69c 23.09 ± 0.33d 11.98 ± 1.80b 58.22 ± 0.08a 46.65 ± 2.12d 0.00
L.
b d b b d
Cucumis sativus L. 21.91 ± 2.53 13.85 ± 1.59 10.60 ± 2.03 54.55 ± 0.09 54.28 ± 2.04 0.00

Tubers
Ipomoea batatas 75.73 ± 2.36a 72.46 ± 2.17a 12.64 ± 1.01c 50.26 ± 0.45c 94.09 ± 2.85a 8.16 ± 0.83b
Raphanus sativus L. 74.03 ± 4.46a 33.72 ± 0.74b 17.67 ± 1.14b 56.69 ± 0.04b 98.78 ± 3.44a 18.13 ± 0.32a
Beta vulgaris L. 43.06 ± 2.44b 39.04 ± 2.58b 45.57 ± 2.72a 95.68 ± 0.96a 0.60 ± 1.44c 18.26 ± 1.19a
Manihot esculenta 12.88 ± 3.54c 18.28 ± 1.76c 16.83 ± 4.65bc 38.81 ± 0.73d 82.74 ± 0.75b 10.52 ± 0.57b

Leaves
Coriandrum sativum L. 106.15 ± 5.39b 181.91 ± 1.75b 70.18 ± 3.11c 100.00 ± 0.06a 90.39 ± 1.73b 98.77 ± 0.25a
Dysphania ambrosioides 104.25 ± 5.39b 176.38 ± 2.30c 12.99 ± 1.85 98.22 ± 0.28a 82.29 ± 1.44b 97.28 ± 0.62a
Mentha spicata L. 99.14 ± 5.20b 181.24 ± 0.96b 83.81 ± 2.24a 93.52 ± 0.78c 86.77 ± 0.08b 98.68 ± 0.76a
Opuntia ficus-indica 51.85 ± 3.52c 180.69 ± 0.92b 0.00 88.33 ± 1.04b 96.21 ± 7.69a 97.35 ± 0.25a
Brassica oleracea var 140.25 ± 5.04a 208.83 ± 0.15a 77.62 ± 1.39b 97.46 ± 0.48a 99.64 ± 0.14a 97.84 ± 0.54a
capitata L.

Seeds
Bixa orellana L. 108.05 ± 5.39a 123.60 ± 0.33a 81.97 ± 5.84b 100.00 ± 0.50a 81.38 ± 0.43b 61.11 ± 1.36a
Phaseolus lunatus L. 106.15 ± 5.05a 77.77 ± 4.32d 50.50 ± 4.60e 68.45 ± 0.60c 96.17 ± 0.29a 31.23 ± 0.49b
Lens culinaris 102.78 ± 4.54ab 117.78 ± 1.41b 72.95 ± 2.16c 92.96 ± 0.06b 79.08 ± 1.15b 50.6 ± .071b
Zea mays L. 97.00 ± 5.07b 101.45 ± 4.50c 66.97 ± 2.33d 100.00 ± 0.23a 93.63 ± 3.31a 34.73 ± 4.04c
Vigna unguiculata L. 103.77 ± 4.38ab 100.56 ± 2.12c 100.00 ± 0.62a 0.00 76.12 ± 0.57c 38.44 ± 1.05c

Different letter superscripts in the same column of plant foods group indicate significant difference (p ≤ 0.05). Data correspond to the average ± standard deviation
of three replicates. TPC: total phenolic compounds; TFC: total flavonoids compounds.

3.3. TPC and TFC determination 3.4. Antioxidant activity

Plant foods are rich in phenols and flavonoids, and their regular
consumption as part of the diet has an important role in the manage-
ment and prevention of T2DM. Table 3 shows the TPC and TFC of
Mayan plant foods. The TPC range of the evaluated foods was
12.88–140.25 mg GAE/100 g. The plant foods with the highest TPC
(p ≤ 0.05) per group were: P. guajava (101.75 mg/100 g) in fruits; C.
moschata (78.70 mg/100 g) and C. chinense (74.19 mg/100 g) in ve-
getables; B. vulgaris (18.26 mg/100 g) and R. sativus (18.13 mg/100 g)
in tubers; B. oleracea (140.25 mg/100 g) in leaves; and B. orellana
(108.5 mg/100 g), P. lunatus (106.15 mg/100 g), L. culinaris
(102.78 mg/100 g), and V. unguiculata (103.77 mg/100 g) in seeds.
The TFC range was 13.72–208.83 mg CAT/100 g. The plant foods
per group with the highest TFC (p ≤ 0.05) were P. guajava (150.43 mg/
100 g) in fruits; C. moschata (68.15 mg/100 g) in vegetables; I. batatas
(72.46 mg/100 g) in tubers; B. oleracea (208.83 mg/100 g) in leaves;
and B. orellana (123.6 mg/100 g) in seeds. Of the plant foods evaluated,
B. oleracea showed the highest values of TPC and TFC.
Šamec, Pavlović, and Salopek-Sondi (2017) reported a TPC in B.
oleracea between 0.98 and 153.30 mg GAE/100 g, higher than that
reported in this study. On the other hand, Batista, Barros, Carvalho, and
Ferreira (2011) reported a B. oleracea TFC of 222.57 mg CAT/100 g,
similar to this study. This variation could be due to genetic diversity
and environmental factors, such as light, temperature, humidity, ferti-
lity, and soil salinity, which influence biosynthesis and the accumula-
tion of secondary metabolites, including phenols and flavonoids.
A diet rich in bioactive compounds with antioxidant capacity has
been linked to a decreased risk of T2DM (Van Der Schaft et al., 2019);
however, the role of “antioxidants” in human health is not entirely clear
and has generated debate in the scientific community. Bioactive com-
pounds could act to reduce oxidative stress by inhibiting the formation
of reactive oxygen species and free radicals. By inhibiting the formation
of these reactive species, the activation of pathways (such as nuclear
factor kappa B) that affect insulin receptor signaling is avoided and
cannot contribute to the development of insulin resistance. A reduction
in oxidative stress also has an indirect effect on blood glucose levels by
promoting sensitivity to the insulin receptor (Straub, Efthymiou,
Grandl, Balaz, Challa, Truscello, Horvath, & Moser, 2019; Van Der
Schaft et al., 2019). Therefore, screening the antioxidant potential of
bioactive compounds present in plant food should be considered a first
step in the development of functional foods and nutraceuticals aimed at
the prevention of metabolic disorders associated with oxidative stress
such as T2DM (deCamargo et al., 2019).
Table 3 presents the antioxidant activity of Mayan plant foods
evaluated at 50 mg/mL. The DPPH radical scavenging activity ranged
from 0% to 100%. The foods with the highest DPPH radical scavenging
activity (p ≤ 0.05) per group were the fruit P. guajava (79.92%), the
vegetable C. chinense (33.40%), the tuber B. vulgaris (56.42%), the leaf
M. spicata (83.81%), and the seed V. unguiculata (100%). The ABTS
radical scavenging activity range was 0% to 100%. By group, the plant
foods that showed the highest ABTS radical scavenging activity
(p < 0.05) were the fruits H. undatus (53.60%) and S. lycopersicum

5
J.J. Uuh-Narváez, et al.
(58.22%); the tuber B. vulgaris (95.68%); and the leaves C. sativum
(100.00%), D. ambrosioides (98.22%), and B. oleracea (97.46%),
without a statistical difference (p ≤ 0.05); the seed B. orellana and the
vegetable Z. mays both had 100% scavenging activity.
Musa, Abdullah, Jusoh, and Subramaniam (2011) reported that a P.
guajava aqueous extract showed a DPPH radical scavenging activity of
60.71%; its effect was associated with the presence of luteolin. Segura-
Campos, Ramírez-Gómez, Moguel-Ordoñez, and Betancur-Ancona
(2013) evaluated seven genotypes of C. chinense grown in Yucatán and
reported a range of free radical scavenging from 44.46% to 94.98%,
observing a greater activity in the yellow, orange, and red genotypes.
The variation in C. chinense antioxidant activity could have been at-
tributed to the growing conditions. The synergistic effect between be-
talains, 4-hydroxybenzoic acid, caffeine acid, catechin, and epicatechin
present in B. vulgaris var. Detroid Dark Red is associated with 90.7%
DPPH and 92.3% ABTS radical scavenging activity (Wootton-Beard,
Moran, & Ryan, 2011). A M. spicata methanolic extract inhibited 71% of
the DPPH radical, and the presence of eugenol, rosmarinic acid, caffeic
acid, and α-tocopherol was related to antioxidant activity (Ahmad,
Fazal, Ahmad, & Abbasi, 2012). An acetonic extract of V. unguiculata (a
bean from Asia) registered 86.3% DPPH radical scavenging activity; its
effect was possibly related to the hydroxyl groups of the phenolic
compounds of the extract, mainly due to the presence of protocatechuic
acid that acts as a hydrogen donor (Siddhuraju & Becker, 2007).
A water:methanol:acetic acid (70:29.5:0.5) H. undatus extract at
500 mg/mL had a low antioxidant capacity with an ABTS radical
scavenging activity of 359.59 µmol Trolox/100 g (Moo-huchin et al.,
2013). Oboh et al. (2015) evaluated a lyophilized S. lycopersicum juice
and reported ABTS radical scavenging activity of 9.23 mM Trolox/µg. A
methanolic extract of C. sativus leaves showed a low antioxidant ca-
pacity of the ABTS radical (< 14.01 µmol Trolox/g) (Przygodzka,
Zielińska, Ciesarová, Kukurová, & Zieliński, 2014). Ajaib, Hussain,
Farooq, and Ashiq (2016) reported an ABTS radical antioxidant capa-
city of 10.52 µmol Trolox/mL in an aqueous D. ambrosioides extract
compared with other lower polarity solvents. Cuong and Chin (2016)
reported a 100% ABTS radical inhibitory effect with10 mg/mL of a B.
orellana aqueous extract, similar to what was reported in this study.
Lopez-Martinez et al. (2009) evaluated the absorption of the ABTS ra-
dical from 18 Z. mays phenotypes in Mexico and reported that the
phenotypes with an 89%–100% inhibitory effect contained more an-
thocyanins and phenolic compounds, mainly ferulic acid.
The antioxidant potential of Mayan plant foods was different from
studies carried out in other regions and countries. These differences
suggest the importance of adapting studies to specific cultural regions.
Furthermore, knowledge of the antioxidant activity of the various
Mayan foods could be useful for the elaboration of dietary therapeutic
strategies for the prevention of diseases related to oxidative stress such
as T2DM.
3.5. Antidiabetic activity
Table 3 presents the inhibitory effect of Mayan plant foods eval-
uated at 50 mg/mL on the activity of α-amylase and α-glucosidase. The
α-amylase inhibition ranged from 0.60% to 99.64%. Plant foods with
the higher inhibitory effect (p ≤ 0.05) by group were P. sapota
(98.92%) and Carica papaya in fruits (97.92%); S. edule (92.83%) in
vegetables; R. sativus (98.78%) and I. batatas (94.09%) in tubers; B.
oleracea (99.64%) and O. ficus-indica (96.21%) in leaves; and P. lunatus
(96.17%) and Z. mays in seeds (93.63%). The range of α-glucosidase
inhibitory activity was 0% to 98.84%. Plant foods with the greatest
effect (p ≤ 0.05) by group were: P. guajava (76.62%) in fruits; C. mo-
schata (6.44%) and C. chinense (6.98%) in vegetables; R. sativus
(18.13%) and B. vulgaris (18.26%) in tubers; no plant from the leaf
group showed a significant difference (the inhibitory effect varied be-
tween 97.28% and 98.68%); and B. orellana (61.11%) in the seeds.
An ethanolic extract of Pouteria torta (Mart.) Radlk, a species of the
6
Food Chemistry 341 (2021) 128247
Sapotaceae family, inhibited 92% of α-amylase extract when used at
500 µg/mL; the compounds catechin, epicatechin, and gallocatechin
could be responsible for the inhibition (De Sales et al., 2017). This in-
hibition percentage was similar to P. sapota evaluated in this study. A
lyophilized C. papaya juice showed a half-maximal inhibitory con-
centration (IC50) of 37.95 µg/mL for α-amylase; the presence of pro-
cyanidin, catechin, epicatechin, quercetin, ρ-coumaric, and gallic acid
possibly exert the effect on inhibition (Oboh et al., 2015). A S. edule
methanolic extract inhibited 50% of α-amylase activity at 0.2 mg/mL;
the presence of phenols and flavonoids showed a correlation with the
inhibitory activity (Loizzo et al., 2016).
Kim, Kim, Kwak, and Jeong (2014) determined an ethanolic R. sa-
tivus extract (10 mg/ mL) exerted < 10% α-amylase inhibition, a
lower effect compared to the reported in this study. The presence of
sulfaropene groups present in R. sativus probably explains their in-
hibitory effect. An aqueous O. ficus-indica extract at 300 mg/mL in-
hibited 37.6% α-amylase activity; the effect was correlated with the
phenolic content (De Souza, Santana, de Macedo, de Brito, & Correia,
2015). Kim et al. (2014) reported that B. oleracea extract (10 mg/mL)
inhibited 43.2% of α-glucosidase activity but had no effect on α-amy-
lase activity; these findings differ from this study. Ferulic acid has been
shown to strongly inhibit α-amylase and α-glucosidase activity, with an
IC50 of 9.5 and 4.9 mM, respectively. Hence, the presence of this
compound in B. oleracea can explain the effect observed in this study
(Dunja, Bogovi, Vincek, Martin, & Salopek-sondi, 2014). Kwon,
Apostolidis, Kim, and Shetty (2007) reported an 89% inhibition α-
amylase activity of an aqueous Z. may extract (200 mg/mL), a lower
effect than reported in this study. Flavonoids and phenolic compounds
such as the derivatives of quercetin, kaempferol, apigenin, luteolin, and
myricetin present in Z. mays could have an essential role in the in-
hibition of α-amylase.
A P. guajava juice (200 mg/mL) did not inhibit α-glucosidase ac-
tivity (Sulaiman & Ooi, 2014), a finding that is different from this study.
Quercetin is a flavone present in P. guajava and in previous studies it
has proven to be a competitive α-glucosidase inhibitor. The presence of
hydroxyl groups (–OH) in carbons 3, 3′, and 4′ in quercetin interacts
with Asp214 and Glu276 of the α-glucosidase active site (Proença et al.,
2017). An aqueous C. moschata extract (5 mg/mL) inhibited α-amylase
and α-glucosidase activity by 20% (Wongsa et al., 2012), a lower effect
on α-amylase activity but a greater effect on α-glucosidase activity,
compared with C. moschata extract at 50 mg/mL in this study. The
presence of caffeic acid in C. moschata is possibly related to the in-
hibitory effect observed in this study (Wongsa et al., 2012).
An aqueous C. sativum extract showed competitive-type inhibition
of α-glucosidase with an IC50 of 1.63 mg/mL; the effect was the result of
the synergy of different compounds, mainly rutin (Brindis, González-
Andrade, González-Trujano, Estrada-Soto, & Villalobos-Molina, 2014).
Alu’datt et al. (2016) reported a 92.97% inhibition of a methanol:ace-
tone:water (1:1:1) M. spicata extract; the inhibitor compound was
possibly rutin, which is found in greater proportions in this leaf. A study
on the inhibitory effect of methanolic B. orellana leaf extracts on α-
amylase activity reported IC50 values of 49 µg/mL; the authors attrib-
uted the inhibitory activity to the presence of β-tocopherol
(Ponnusamy, Ravindran, Zinjarde, Bhargava, & Kumar, 2011). No
previous studies of B. orellana seed extract on α-glucosidase activity
have been reported.
The antidiabetic potential through the inhibitory effect on the α-
amylase and α-glucosidase enzymes of Mayan plant foods can be useful
for the dietary management of hyperglycemia. The observed differences
between the antidiabetic effect of Mayan foods from other studies un-
derscores the importance of the functional characterization of food
from a specific region for its therapeutic use or as a source of bioactive
compounds in the Maya region.
Pearson correlation coefficients between α-amylase and α-glucosi-
dase inhibitory activities, DPPH and ABTS radical scavenging, and GI,
TPC, and TFC are shown in Table 4. α-Glucosidase, DPPH, and ABTS
J.J. Uuh-Narváez, et al. Food Chemistry 341 (2021) 128247

Table 4 The results suggest that B. oleracea has the highest antidiabetic
Pearson correlation matrix for 24 plant foods of a Mayan community from potential of all evaluated plant foods, due to its nutritional and func-
Yucatan Peninsula. tional properties. The results of this study contrast with those of Kim
α-AMY α-GLU DPPH ABTS TPC TFC GI et al. (2014), who did not consider B. oleracea as a food with anti-
diabetic potential in a screening of 26 vegetables from Korea because it
α-AMY – 0.24 −0.05 −0.12 0.32 0.26 0.03 did not inhibit α-amylase, had weak antioxidant activity, and had low
α-GLU – – 0.50* 0.63* 0.66* 0.96* −0.49
TPC and TFC. Bioactive compounds in B. oleracea are affected by en-
DPPH – – – 0.31 0.73* 0.54* −0.11
ABTS – – – – 0.41 0.59* −0.32 vironmental conditions (Šamec et al., 2017). For that reason, the results
TPC – – – – – 0.75* −0.18 of this study suggest that environmental factors in Mayan communities
promote a richer content of bioactive compounds in B. oleracea than in
* Statistically significant correlation (p ≤ 0.05). Remark: α-AMY: α-amylase Korea (Kim et al., 2014). Hence, it should be noted that bioactive
inhibition activity; α-GLU: α-glucosidase inhibition activity; DPPH: inhibition compounds, nutrients and biological activity may be different from
of radical DPPH; ABTS: inhibition of radical ABTS; TPC: total phenolic com-
those obtained in other countries (Oboh et al., 2015). B. oleracea is one
pounds; TFC: total flavonoids compounds; GI: glycemic index. Number of
of the most cultivated plant foods in the world and due to its affordable
samples n = 72.
price, year-round availability, and versatility of consumption (Šamec
et al., 2017), B. oleracea could be a good candidate for essential food in
inhibition had significant direct correlations (p ≤ 0.05) with TPC
the diet of people with T2DM in Mayan communities.
(R = 0.96, 0.54, and 0.59, respectively) and TFC (R = 0.63, 0.73, and
0.41, respectively). Thus, the results of this study suggest that phenols
3.7. PCa
and flavonoids are active metabolites that contribute to α-glucosidase
inhibitory activity and antioxidant activity. These findings are similar
When analyzing large multivariate datasets, it is desirable to reduce
to another study (Wongsa et al., 2012). In addition, α-glucosidase in-
their dimensionality. Thus, it is necessary to use multivariate statistical
hibition had a positive correlation (p ≤ 0.05) with DPPH (R = 0.50)
techniques such as PCA. This technique describes datasets in terms of
and ABTS (R = 0.63) inhibition. Thus, possible metabolites with an
new variables (components) not by correlation but by ordering them by
inhibitory effect on α-glucosidase can also neutralize free radicals.
their amount of original variance. Principal component 1 (PC1) and
α-Amylase inhibitory activity and GI did not correlate with TPC,
principal component 2 (PC2) have an eigenvalue > 1 and represent
TFC, DPPH, ABTS, and α-glucosidase. These results suggest that other
51.82% and 21.85% of the variation, respectively. Together, they ex-
compounds, such as soluble fiber, act as α-amylase inhibitors.
plain 73.67% of the total variability.
According to the correlation data, digestive enzyme inhibitors do not
The factor loading value refers to the correlation between each
affect the GI of a food. Therefore, other properties such as a food’s
variable and the main analyzed component. A correlation is high when
composition, microstructure, and starch profile are factors to consider
the values of the weights are close to 1 or −1, which indicates a direct
in future studies.
and or inverse correlation to the factor, respectively. The main factor
related to PC1 is TFC, with a factor loading of 0.51. This component
3.6. ANOVA factorial analysis also shows a positive correlation with all other variables, the ones that
contribute the most are TPC (0.47), α- glucosidase (0.46), and DPPH
The factorial ANOVA indicates the effect between many factors (0.45). The main factor positively related to PC2 is ABTS, with a factor
(nutrimental and functional results) and different responses (plant loading of 0.63, followed by α-glucosidase (0.19). The rest of the
foods). The results showed that P. guajava (fruits), C. moschata (vege- variables in PC2 have inversely proportional correlations.
tables), R. sativus (tubers), B. oleracea (leaves), and B. orellana (seeds) The biplot of two dimensions shows PC1 on the “x” axis and PC2 on
had the highest interaction response (p ≤ 0.05) on the nutritional and the vertical “y” axis (Fig. 2). In PC1, the variables with a positive di-
functional properties of their respective vegetable food groups. Overall, rection of the horizontal axis (x) present a high potential TFC, while a
B. oleracea had the highest interaction response (Fig. 1). negative direction exhibits a low potential TFC. B. oleracea, located at
(3.15, −1.15) of the biplot, shows the highest potential for TFC. In PC2,
the variables that show a positive direction of the vertical axis (y) show
greater potential for ABTS radical inhibition, while a negative direction
indicates a lower response. B. vulgaris, located at (−0.90, 3.38) of the
biplot, shows the highest potential of ABTS radical inhibition.
The PCA findings suggest that TFC is a key point to select plant
foods with antidiabetic potential due to the significant (p < 0.05)
correlation with other compounds such as TPC and α-glucosidase and
DPPH radical inhibition. The presence of flavonoids in plant foods are
relevant for the treatment of T2DM: They inhibit digestive enzymes
from starch and as hydrogen donors. B. oleracea shows the highest
potential for TFC in PC1; this result coincides with the ANOVA factor
analysis. An increased intake of crucifers, such as B. oleracea, is asso-
ciated with a lower risk of type 2 T2DM because they contain poly-
phenols (mainly flavonoids), vitamin C, carotenoids (α-carotene, β-
carotene), and glucosinolates. Thus, B. oleracea could be a good can-
didate as an antidiabetic functional food.

Fig. 1. Graph of confidence intervals of means of the nutritional and functional
properties of plant foods of a Mayan community from Yucatan Peninsula with
the highest antidiabetic potential by group. Data correspond to the average ±
standard deviation of three replicates. Different letter superscripts of plant
foods indicate significant difference (p ≤ 0.05).
4. Conclusion
This study shows the potential of Mayan foods as ingredients or
functional foods that can contribute to the approach of new diet-ther-
apeutic alternatives to prevent non-communicable diseases such as
T2DM. Thus, knowing the nutritional and functional properties of plant

7
J.J. Uuh-Narváez, et al.
foods from the Mayan diet could inspire novel disease prevention
strategies, as an alternative to the Mediterranean diet, that promote
health and wellness. Multivariate analysis indicates that biological ac-
tivities are associated with the synergistic effect of the phenols and
flavonoids present in the plant foods and content of flavonoids is a key
point to select foods with antidiabetic potential. Based on these find-
ings, B. oleracea shows the highest antidiabetic potential; however,
other evaluated plant foods, such as P. guajava, C. moschata, R. sativus,
and B. orellana, could also be considered for future research.
CRediT authorship contribution statement
Jonatan Uuh-Narváez: Formal analysis, Investigation,
Methodology, Writing - original draft. María Alejandra González-
Tamayo: Formal analysis. Maira Rubí Segura-Campos:
Conceptualization, Funding acquisition, Investigation, Methodology,
Project administration, Resources, Supervision, Writing - review &
editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgments
Thanks to CONACYT for providing scholarship 700507 to Uuh-
Narvaez. Also, to Kellogg’s foundation for project P3037075.
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Food Chemistry 341 (2021) 128247
Fig. 2. Factor score of 24 plant foods from
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