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Journal of Functional Foods 95 (2022) 105183

Contents lists available at ScienceDirect

Journal of Functional Foods


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

Nopal cladodes (Opuntia Ficus Indica): Nutritional properties and


functional potential
Ezequiel Hernández-Becerra a, María de los Angeles Aguilera-Barreiro b,
Margarita Contreras-Padilla c, Esther Pérez-Torrero d, *, Mario E. Rodriguez-Garcia e
a
Ciencias de la Salud, Universidad del Valle de México, Campus Querétaro, Naranjos Punta Juriquilla 1000, Santa Rosa Jáuregui, 76230 Santiago de Querétaro, Qro.,
Mexico
b
Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Querétaro, Qro. C.P. 76230, Mexico
c
Centro Académico de Innovación y Desarrollo de Productos, Facultad de Ingeniería Universidad Autónoma de Querétaro, Centro Universitario, Cerro de las campanas s/
n, Las Campanas, C.P. 76010 Santiago de Querétaro, Qro., Mexico
d
Facultad de Ingenieria, Campus Aeropuerto, Universidad Autónoma de Querétaro, Querétaro, Qro. C.P. 76230, Mexico
e
Departamento de Nanotecnología, Centro de Física Aplicada y Tecnología Avanzada, Universidad Nacional Autónoma de México, Campus Juriquilla, Querétaro,
Querétaro C.P. 76230, Mexico

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

Keywords: Nopal pads at different maturity stages show changes in their chemical composition. They are an excellent
Minerals nutritional source and should be included in human diets worldwide. Moreover, they can be considered a novel
Fiber potential food resource and used for scientific studies when transformed into powders, to reduce product loss
Probiotic
during harvest season. Their physicochemical properties in the maturity stage can be used to treat or prevent
Functional foods
Nopal
nutritional related diseases. The nopal pad powder at high maturity stages could help normalize the fiber intake,
Cladodes and the high amount of Ca and Mg could help maintain bone mineral density. Soluble fiber can be included in
human diets by consuming f fresh young nopals. Authors considered it necessary to increase the studies of the
nutritional properties of different varieties of nopal cladodes as a function of the maturity and select them ac­
cording to the nutritional requirements.

1. Introduction increase in CO2, which caused the planet’s rise in temperature. The
nopal plant also diminishes the deforestation environmental impact that
The nopal plant belongs to the vegetable kingdom, to the Cactaceae affects the significant ecosystems of the world (Piga, D’Aquino, Agabbio,
family, of the genus Opuntia, with more than 150 species classified as & Schirra, 1996; Le Houérou, 1996; Nobel & Bobich, 2002; Betancourt-
originating in Mexico. It is an endemic plant of arid and semi-arid zones. Domínguez et al., 2006).
Nopal cladodes are considered modified stems instead of classical leaves These plants were used in pre-Hispanic civilization as food and
in their photosynthetic function. The outer cladode and the chloren­ medicine. Nowadays, nopal cladodes are a promising vegetable because
chyma are crucial for its photosynthetic action (Saenz, Sepulveda, & of their high ecological adaptivity and, more importantly, their chemical
Matsuhiro, 2004). In contrast, the inner part contains the medullary composition, which gives them a huge potential application as a func­
parenchyma, whose primary purpose is water storage. The nopal ab­ tional food due to their nutritional value (Rodriguez-Garcia et al., 2007).
sorbs water from steam or light rain, which allows the vegetable to take When young, fresh nopal cladodes, also called nopalitos, have been
in water and store it in the parenchyma (Saenz, 1997). consumed in Mexico and United States, with different cooking methods.
The nopal plant plays a vital ecological role in diminishing soil However, nopal cladodes with medium and advanced stages of maturity
erosion, considering that the arid or semi-arid land suitable for culti­ are not used in the human diet and represent a significant loss for the
vating these species require little water. This helps to understand their farmer (Contreras-Padilla et al., 2016). These cannot be included in the
ecological importance in preventing or ameliorating the environmental diet due to the undesirable textural properties of the high insoluble fiber.
impact of soil impoverishment. Also, due to its peculiar acidic meta­ These older nopal cladodes are frequently used as forage for livestock,
bolism, this plant can be a potential alternative to capture part of the especially when another fresh forage is scarce in the dry station.

* Corresponding author.

https://doi.org/10.1016/j.jff.2022.105183
Received 3 May 2022; Received in revised form 5 July 2022; Accepted 10 July 2022
Available online 21 July 2022
1756-4646/© 2022 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).
E. Hernández-Becerra et al. Journal of Functional Foods 95 (2022) 105183

Some studies indicate that nopal cladodes can be functional food and
an excellent source of nutraceutical compounds. These cladodes have
been studied as a functional food because they contribute to human
health maintenance. Cladodes help prevent diabetes (Andrade-Cetto, &
Heinrich, 2005; Nuñez-López, Paredes-López, & Reynoso-Camacho,
2013), hypercholesterolemia (Ennouri, Fetoui, Bourret, Zeghal, Guer­
mazi, & Attia, 2006), obesity (Zhaoet al., 2012), and hypertension
(Halmi et al., 2013).
However, in the above-mentioned previous research, the maturation
stage was not considered. Instead, there were subsequent studies
(Aguilera-Barreiro et al., 2013). They used nopal powder from the late
maturity stage (600 g) to improve bone mineral density in perimeno­
pausal women. However, few studies evaluate functional foods prop­
erties of nopal cladodes in the metabolic syndrome, which shares the
same risk factors as diabetes, hypertension, and obesity. Metabolic
syndrome is a public health problem in Mexico, with a prevalence in
42.3 % of adults over 20 years old, 4 out of 10 Mexicans (Gutiérrez,
et al., 2013). They share the same unhealthy lifestyles, such as a diet
mainly without dietary fiber content, high in fats and refined sugars.
However, nopal cladode can also be a beneficial food source due to their
nutritional value, which justifies using the nopal or its products as food.
There is a remarkable interest in people from different cultures and
traditions in consuming natural food that is nutritious and contribute to
improving human health. In this trend, two different ways to introduce
natural foods have been incorporated into the diets. First, the nutra­
ceutical compounds as pharmaceutical intake; and second and more
natural, through the inclusion of some functional foods that are already
part of the diet with inherent health benefits without adverse effects on
the health (Guevara-Arauza, Pimentel-González, & De Órnelas-Paz,
2012).
Nopal cladodes are nutritious, have potential applications as func­
tional food, have a lower impact on our planet due to their high
ecological adaptivity, and can be affordable, accessible, besides being
tasty. The current review aimed to compile, analyze, and discuss the
main knowledge related to the physicochemical, nutritional, and func­
tional properties of fresh nopal cladodes and their powders as a function
of the maturity stage. On the other hand, the review attempted to open a
new window of opportunities in the topic that involves nopal and its
different products. Their physicochemical properties in the maturity
stage can be used to treat or prevent nutritional related diseases. The
nopal pad powder at high maturity stages could help normalize the fiber
intake, and the high amount of Ca and Mg could help to maintain bone
mineral density. Soluble fiber can be included in human diets by
consuming fresh young nopals. Authors considered it necessary to in­
crease the studies of the nutritional properties of the different varieties
of nopal cladodes as a function of the maturity and select them according
to the nutritional requirements.

2. Physicochemical characteristics of nopal cladodes as a


function of the maturity

2.1. Nopal consumption


Fig. 1. (a) Shows the nopal cladodes for different maturation stages. (b) Shows
the transformation of fresh nopal cladodes to dried nopal and powder. (c)
In Mexico, nopal has been part of human diets for centuries. It is
Shows the changes in weight as a function of the harvest day for the Opuntia
consumed as salad, in fresh and in different traditional sauces where
Ficus Indica redonda variety.
cladodes are used at different maturity stages from 24 to 48 days (60 to
150 g, respectively) (Hernández-Urbiola et al., 2010).
according to each necessity to cure or prevent non-hereditary chronic
Nopal consumption is growing around the world mainly because in
diseases. Soluble fiber from young cladodes, insoluble fiber, and min­
the last years there has been an increasing scientific interest in the
erals from older cladodes can be consumed. Then the application of
changes in its physicochemical properties as a function of the age. There
nopal in different fields could be linked to the physicochemical prop­
has also been an increasing remarkable interest in the consumption of
erties related to the age of cladodes (Hernández-Urbiola, Pérez-Torrero,
natural products (Missaoui et al., 2020; Aragona, Lauriano, Pergolizzi, &
& Rodríguez García, 2010; Contreras-Padilla et al, 2011; Mounir,
Faggi, 2018).
Younes, Asmaa, Abdeljalil, & Abdellah, 2020).
Fig. 1(a) shows the nopal cladodes for different maturation stages.
Fig. 1(b) shows the transformation of fresh nopal cladodes to vacuum
Changes in these stages are related to weight and size, but also to a
dried nopal and powder that serves as a nutraceutical form for different
variation in their chemical compounds content, which can be used

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E. Hernández-Becerra et al. Journal of Functional Foods 95 (2022) 105183

clinical trials. Vacuum drying process does not affect physicochemical meanwhile, the insoluble fiber content increases (Hernández-Urbiola
and nutritional properties (Contreras-Padilla et al., 2011). As seen in et al., 2010). Studies by Saenz-Hernandez, Corrales-Garcia, and Aquino-
Fig. 1 (c), the changes in weight as a function of age behave as a logistic Pérez (2002) reported that a potential source of dietary fiber could be
curve. As it is well known, this curve depends on the variety, season, and found in the nopal due to its high levels of total fiber. The high content of
agronomical conditions (Saenz, 1997). dietary fibers from nopal powder could be a valuable source of these
essential components for human food intake (Contreras-Padilla et al.,
2.2. Nopal nutritional values 2012).

Rodríguez-Garcia et al., 2007 studied the physicochemical and 2.4. Mucilage


nutritional characterization of fresh nopal cladodes and nopal powders
obtained by the vacuum obtained at different stages of development. Gums, mucilage, and pectins form the soluble fiber. The nopal
The results showed that the nutritional and mineral composition of the mucilage has some applications in the food industry. These macromol­
nopal changes as a function of maturity. As mentioned before, young ecules are used as an edible coating in fruits (Del-Valle, Hernandez-
cladodes are eaten as nopalitos, mainly in Mexico and in south of the Muñoz, Guarda, & Galotto, 2005); as a stabilizer of emulsions and foam
USA. Several authors have studied the composition and quality of edible (Garti & Leser, 2001); to control the crystallization; as a suspension
cladodes (Rodriguez-Felix & Cantwell, 1987) and analyzed three Cactus stabilizer; to inhibit the syneresis, and to form gels (Dziezak, 1991).
species (Opuntia arnyclaea, O. ficus-indica, and O. inermis). They found Missaoui et al. (2020) found that the dietary fiber, mucilage, and pectin,
the following average composition per 100 g: 91.7 g of water, 1.1 g of were composed of arabinose, galactose, glucose, mannose, rhamnose,
protein, 0.2 g of lipids, 1.3 g of ash, 1.1 g of crude fiber, 4.6 g of complex and xylose sugars.
carbohydrates, 0.82 g of simple sugars, 12.7 mg of ascorbic acid, and The mucilage is a hetero-polysaccharide of high molecular weight
28.9 µg of carotenes. They concluded that the nutritive value of the produced in specialized cells in plants. According to different studies,
cladodes in which they are commonly harvested and consumed (15 to the main composition of this polysaccharide consists of six neutral
25 cm long, weighing 50 to 80 g per stem), was similar for the three sugars: arabinose, galactose, rhamnose, xylose, uronic acid, and gal­
species. acturonic acid (Trachtenberg & Mayer, 1982). The mucilage is an
The 88–95 % water content makes cladodes a low-calorie food with interesting compound of these kinds of plants. It has remarkable prop­
27 kcal/100 g (Muñoz de Chavez, Chavez, Valles, & Roldan, 1995). erties such as a high capacity for water holding, ion binding, and its gel-
According to Table 1, the ash mineral content increases with age, formation ability that contributes to considering mucilage as a func­
making advantage of the availability of minerals in the vegetable can be tional additive that can be used in several industries (McGarvie, &
beneficial in combating food scarcity-related diseases. It is well known Parolis, 1979; Saenz, Sepulveda & Matsuhiro, 2004).
that the mineral content in diets in developing countries is low in min­ The studies of the physicochemical and rheological properties of the
erals like calcium. Calcium comes from dairy products and cheese, nopal mucilage at three different maturity stages (100, 200, and 400 g).
among others. However, these products are expensive. Instead, we The X-ray diffraction analysis showed calcium carbonate in the mucilage
propose the nopal product intake as a calcium source. Moreover, the in two different crystalline forms: calcite and calcium carbonate (Con­
problem relative to lactose intolerance mainly reduces calcium con­ treras-Padilla, et al., 2016). These compounds are bioavailable for
sumption and can lead to low bone mineral density and osteoporosis humans. Mucilage extracted from cladodes at different maturity shows
(Aguilera-Barreiro et al., 2013). Table 1 indicates that nopal is a crucial changes related to its rheological properties. These findings open the
source of minerals within the diet of people who ingest it. When nopal opportunities for potential uses of this hydrocolloid of the cladodes
can be introduced into the daily diet, it combats the mineral deficiencies depending on the functional application required, considering the
of human populations. properties associated with each of the different maturity stages Table 2
Even though the fat content is low, another work found that fatty
acid analysis of cladodes indicated an important amount of omega fatty 2.5. Aminoacid and protein content
acids. The most abundant was eicosadienoic acid (C 20:2, ω6), followed
by oleic acid, then palmitic acid. Also, γ-Linolenic acid was detected in a A complete study found that nopal cladodes contain 17 different
considerable amount for cladodes. These results showed nopal cladodes amino acids, nine considered essential. The study showed different
as a source of omega and essential fatty acids (Abdel-Razek et al., 2019). levels of content related to the maturity stages (Hernández-Urbiola
et al., 2010) and revealed that threonine and isoleucine are better
2.3. Fiber content sources for these amino acids in younger samples. On the other hand, the
histidine, leucine, and lysine content increase in older cladodes. Besides,
According to Table 1, the total fiber content increases with the age of phenylalanine, threonine, and isoleucine have the highest content of
nopal cladodes. Soluble fiber content decreases with the maturity stage; amino acids for all stages. These results indicate that the nopal powders

Table 1
Shows the proximate chemical analysis of Opuntia ficus indica variedad redonda for nopal powders as a function of the maturation (Hernández-Urbiola, et al., 2010).
Weight Moisture Ash Fat Crude Protein Carbo Insoluble Insoluble
Nopal cladodes (%) (%) (%) Fiber (%) hydrates (%) fiber fiber
(days) (%) (%) (%)

40 5.03 17.65 2.16 11.00 7.07 42.94 40.14 25.50


50 8.81 19.59 2.37 13.26 8.99 53.04 – –
60 5.43 20.64 2.38 16.14 8.39 53.01 58.61 11.38
70 4.85 21.09 1.62 19.03 8.92 55.53 – –
80 4.36 21.64 1.53 18.73 7.25 53.53 61.24 10.81
90 4.81 21.92 1.50 19.12 7.78 55.15 _ _
100 4.08 22.80 1.42 20.11 8.29 56.73 51.68 8.49
115 4.58 22.91 1.72 21.48 8.48 59.20 50.40 8.81

125 4.35 20.91 1.70 19.85 5.85 52.67 56.82 9.80


135 4.18 24.30 1.87 23.33 7.07 60.77 58.20 9.94

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Table 2
Shows the main mineral content of Opuntia Ficus indica variedad redonda for nopal powders as a function of weight (Hernández-Urbiola et al., 2010).
Weight P Ca K Na Mg Mn Fe Zn
Nopal cladodes (mg/g) (mg/g) (mg/g) (mg/g) (mg/g) (mg/g) (mg/g) (mg/g)
(days)

40 0.236 17.520 55.200 0.300 8.800 0.290 0.090 0.070


60 0.411 22.800 68.750 0.300 11.200 0.070 0.010 0.080
80 0.351 27.560 70.900 0.550 10.200 0.080 0.120 0.030
100 0.382 29.010 68.500 0.200 11.000 0.050 0.130 0.070
120 0.252 30.700 68.800 0.200 8.950 0.030 0.160 0.040
135 0.282 34.400 63.350 0.300 9.550 0.080 0.135 0.080

might be a good food complement due to their essential amino acid variable. No changes were observed in insoluble fiber content, chroma,
content. and lightness for any of the three different drying processes.
In an experimental study, which includes nopal pads of 6 and 12
2.6. Minerals source months Opuntia ficus indica cladodes, results showed an increased sugar
release for 12-month cladodes and notorious increases in the presence of
The mineral composition of nopal cladodes depends on diverse fac­ cellulose. Results suggest a benefit of the increasing hydrolysis activity
tors such as the variety of plants, the cultivation region, water quality, for the association with sugar release increment and cellulose fiber
soil, and cultivation practices, among others. The main elements are (Mounir et al., 2020).
calcium, potassium, phosphorus, magnesium, and sodium. Meanwhile,
iron, zinc, and manganese are present in small quantities. Some studies 3. Food, nutritional aspects, and functional properties
indicate that these minerals are in different compounds: carbonates,
chlorides, sulfates, and phosphates (Rodriguez-Garcia et al., 2007; Nopal is also used in traditional medicine to treat several diseases
Hernández-Urbiola et al., 2010). Other studies show similar results due to its hypoglycemic properties in diabetes, to reduce weight on
about this vegetable. Missaoui et al. (2020) indicate that it is a source of obesity, and to reduce cholesterol levels (Piga et al., 1996; Le Houérou,
minerals, such as cations (calcium, sodium, potassium, and magnesium) 1996; Betancourt-Domínguez et al., 2006). Nopal also contains nutri­
and anions (sulfate and chloride), with high magnesium bioaccessibility tional substances of the daily diet, such as vitamins and several minerals.
(93 %). For nutritional deficiencies associated with a degenerative disease,
According to previous reports, the maturation stage is an important currently widespread in developing countries, attention should be
factor in the variation of the mineral content of nopal cladodes (Rodri­ focused on affordable options of regional food resources. The focus
guez-Garcia et al., 2007; Hernández-Urbiola et al., 2010; Contreras- should also be on returning to customs of the precedent cultures, com­
Padilla et al., 2011). The calcium content in this plant was studied in bined with the global tendency on feeding habits and thus improving
different ways. The concentration of calcium increases at later maturity food. Always respecting their habits and cultural trends, nopal powders
stages. Contreras-Padilla et al. (2011) demonstrated that the molar ratio can be an alternative because of their low-slung cost and can be used as a
between oxalate and calcium in all states of maturity was lower than 1. dietary supplement in all seasons, taking advantage of the best harvest
Therefore, these results suggest that the bioavailability of this mineral season and storage when scarcity comes. The dried nopal has significant
has not been modified for the antinutritional effect of oxalates. benefits due to its management, transport, and storage for long periods
They analyzed crystalline structures present in nopal cladodes. They and ensuring supreme nutritional values.
identified calcium carbonate or calcite (CaCO3, calcium-magnesium
bicarbonate (CaMg(CO3)2), magnesium oxide (MgO), calcium oxalate 3.1. Secondary metabolites
monohydrate (Ca(C2O4)•(H2O), potassium peroxydiphosphate (K4P2O),
and potassium chloride (KCl) (Contreras-Padilla, Rivera-Muñoz, In Mexican culture, the consumption of nopal includes different
Gutiérrez-Cortez, del Real-López, & Rodríguez-García 2015). The CaCO3 preparations such as roasted, cooked, and fried. Nopal is poor in mac­
compound is key due to its bioavailability for humans. Calcium and ronutrients such as carbohydrates (digested by human enzymes), pro­
magnesium have essential functions in the biochemical processes of teins, and lipids. The main component is water, 90–93 %. It is rich in
plants, animals, and humans. fiber (soluble and insoluble), some vitamins, and minerals. It also con­
tains secondary metabolites in the fresh plant. These compounds are
2.7. Postharvest technology and nutritional quality distributed in several parts of the plant (El-Mostafa, et al.. (2014), but
many of them are lost by culinary treatments. Therefore, the secondary
The nopal cladodes harvested early in the morning had moderate metabolites may be overestimated in scientific reports concerning
CO2 and low ethylene production rates, which initially declined and popular food. Secondary metabolites are synthesized by living organ­
then remained almost constant with time in storage (Cantwell, isms for physiological activities and defense mechanisms. A study of
Rodriguez-Felix, & Robles-Contreras, 1992). Storage at 5 ◦ C permitted a cladodes of the genus Opuntia showed the presence of several metabo­
shelf-life of 3 weeks without the development of any visual signs of low- lites. These are Gallic, vallinic, p-hydroxybenzoic, chlorogenic, and p-
temperature damages. Postharvest technology is crucial to maintain the coumaric acids; flavonoids quercetin, isorhamnetin, rutin, and apigenin.
quality of nopal cladodes to maximize storage life for human con­ The presence of secondary metabolites is modified, but fluctuation is not
sumption. One of the most important conservative technology is drying. identifiable (López-Palacios and Peña-Valdivia (2020). The secondary
Contreras-Padilla et al. (2012) found that it is vital to consider the metabolites type is determined by several factors, including age, variety,
appropriate equipment for the drying process. Their study focuses on and soil nutrition. In recent years, several authors have identified many
changes of nutritional characteristics of nopal powders from three secondary metabolites. Many of them are precursors to other metabo­
different maturity stages: 50, 100, and 150 days, and obtained by three lites. Some are chemical isomers with similar biological activity in vitro
different drying processes: freeze-dried, forced air oven, and tunnel. and in vivo. These activities include antioxidants, anti-carcinogenic,
Results indicated that nopal powder obtained by freeze-drying retains hypocholesterolemia, anti-inflammatory, hypoglycemic, antimicrobial,
higher contents of protein, soluble fiber, and fat than the other two among others studies (Bensadón, Hervert-Hernández, Sáyago-Ayerdi, &
processes. Also, the freeze-drying process had less effect on the color Goñi, 2010; Figueroa-Pérez, Pérez-Ramírez, Paredes-López, Mondragón-

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E. Hernández-Becerra et al. Journal of Functional Foods 95 (2022) 105183

Jacobo, & Reynoso-Camacho, 2018; Mena et al., 2018; Ressaissi et al. compromised. Also, results suggest that nopal cladodes in advanced
2016; Osuna-Martínez, Reyes-Esparza, & Rodríguez-Fragoso, 2014). maturity stages can be a natural source of calcium that might be
included in human diets.
3.2. Polyphenols, flavonoids, and phytosterols Welegerima, Zemene, and Tilahun (2018) determined the antimi­
crobial activity of Opuntia ficus indica cladodes extracts against some
Many chronic and degenerative diseases such as cancer, hyperten­ selected bacterial isolates. The extracts showed the presence of phenolic
sion, obesity, and cardiovascular diseases can be controlled and pre­ substances, tannins, glycosides, alkaloids, flavonoids, saponins, steroids,
vented through diets, including specific chemical compounds present in alkaloids, and amino acids. The results indicated antibacterial activity
nopal powders obtained at different maturity stages (Halmi et al., 2013; against Gram-positive (B. subtilis and S. pneumoniae) and Gram-
Morán-Ramos et al., 2012; Nuñez-López et al., 2013). negative bacteria (E. coli and S. typhimurium).
The nopal effect on chronic degenerative diseases has been reported
in both clinical and preclinical studies. Most of them refer to a contri­ 3.4. Nopal intake in non-transmissible chronic diseases
bution of some constitute of nopal. Such secondary metabolite high­
lights phenolic compounds and flavonoids. (Medina-Torres, et al., 2011) Among the most studied nopal species in preclinical experiments are
studied the effect of convection drying on flavonoids, carotenoid, and the Opuntia Ficus Indica and Streptacantha Lemaire. Its effects have
ascorbic acid, reporting that the drying at 65 ◦ C decreases the secondary focused on controlling glucose metabolism associated with metabolic
metabolite content. (Guevara-Figueroa, et al., 2010) studied the syndrome. The potential of the nopal as an adjuvant in glucose control
phytochemical and flavonoid content in wild and commercial samples of and glycosylated hemoglobin levels was reported in rats administered
nopal. They found that the phytochemical and flavonoid content intraperitoneally with nopal extract plus insulin. The hypoglycemic ef­
decreased in tablets of commercial nopal due to the drying method. fect was maintained after removing the insulin from the treatment
Later, the effect of cooking bioactive component contents versus raw (Trejo-González et al., 1996). Similar results were found years later in
nopal was evaluated (Ramírez-Moreno, et al., 2013). In general, they healthy rats and diabetic mice (Son, Yoon, Lee, & Kim, 2011; Butterweck
reported a negative impact of temperature on bioactive components of et al., 2011), respectively. The first approaches aimed at knowing the
the nopal. In consequence, the effects of raw nopal can be over­ mechanisms of action of the nopal on the glucose metabolism include
estimated. The analysis found that bioactive compounds are distributed the study conducted by (Cárdenas-Medellín, Serna Saldívar, & Velazco
in different parts of the nopal, highlighting the presence of flavonoids, de la Garza,1998)) through fasting tests to evaluate the hypoglycemic
sterols, minerals, fatty acids, and anthocyanins. (El-Mostafa et al., 2014; effect and glucose tolerance tests to know the antihyperglycemic activity
Astello-García, et al., 2015) confirm the presence of such structures in in rats. In a bifactorial experimental design with two levels, they
different parts of the plant. In addition, they reported the presence of compared the effect of the administration of different doses of raw and
fatty acids, mainly: medium-chain fatty acids and eight essential amino cooked nopal (6 and 12 %) on lipid metabolism and glucose control.
acids. Only raw nopal at a concentration of 12 % was found to show a statis­
Figueroa-Pérez et al. (2018) shows the inhibitory activity of these tically significant reduction in LDL cholesterol levels of 34 % compared
compounds on alfa amylase, aminoglycosides, and lipase enzymes. to the control group, but glucose levels did not decrease. The lack of
However, many mechanisms are not established at present. A complete standardization of the nopal used can explain these controversies. Most
analysis of the main secondary metabolites and their biological activity studies using nopal do not consider the state of maturity to determine its
found in nopal Opuntia ficus indica as a function of the maturity until now biological effects. Several reports point out that important nutrients and
were shown and classified as phenolic compounds, flavonoids, saponins chemical composition change as a function of age (Rodriguez-Garcia
and phytosterols in their work. Missaoui et al. (2020) studied the et al., 2007; Hernández-Urbiola et al., 2010; Contreras-Padilla et al.,
chemical and antioxidant components of nopal. They found eleven 2011).
compounds between phenolic acids and flavonoids, with piscidic acid In hyperlipidemic rat models, (Zhao et al., 2012; Halmi et al., 2013)
and isorhamnetin derivatives being the most abundant. The polyphenol found the same in rabbits. Until then, the coincidences in the beneficial
bioaccessibility was very high. Nopal cladodes showed a good capacity effects of nopal consumption on important parameters of metabolic
for radical scavenging measured by DPPH and ABTS methods. In the syndrome. However, the mechanisms of action were not clearly defined.
same way, the results obtained by Blando, Russo, Negro, De Bellis, & An interesting study discarded the hypoglycemic effect of nopal by
Frassinetti (2019) studied two stages of nopal pads maturity. They polysaccharides extracted from two species of Opuntia Ficus Indica and
observed a remarkable antioxidant activity in immature nopal cladodes. Opuntia Streptacantha Lemaire, when it is subcutaneous administrated
(Alarcon-Aguilar et al., 2003). However, when administered intra­
3.3. Antinutritional compounds in nopal gastrically, the antihyperglycemic effect was observed with a possible
reduction in intestinal glucose absorption. Andrade-Cetto and Wie­
The tannins content of nopal was modified depending on their denfeld (2011), Nuñez-López et al. (2013) found hypoglycemic and
maturation stage. The content of the antinutritional factors in the nopal antihyperglycemic effects in the Opuntia Strptacantha Lemaire adminis­
remained undefined, and did maintain a relationship with the matura­ tered. In another research, (Laurenz, Collier, & Kuti, 2003) observed the
tion state, as noted in the case of minerals. In general terms, a higher hypoglycemic effect in the diabetic pig model induced with streptozo­
content of tannins in the nopal was detected at 500–550 g of weight. In tocin but not in the healthy-one. The use of lyophilized raw nopal
this regard, it was established that a high concentration of this anti­ Opuntia Ficus Indica confirmed these findings and suggested that the
nutritional component in food could give them an astringent taste, clot presence of some compounds could mediate a decrease in the parame­
alkaloids, and albumins, in addition to being a chelating agent and se­ ters related to lipid metabolism, such as LDL (low-density lipoproteins)
questrating heavy metals (Otero & Hidalgo, 2004). Regarding tannins cholesterol, and triglycerides. In contrast, an increase of HDL (High-
content, an increase is observed as the nopal age increases, suggesting density lipoproteins) cholesterol was observed (Galati, Tripodo, Tro­
that old cladodes samples have antinutrient action. In contrast, old vato, Aquino, & Monforte, 2003). Other species, such as Opuntia Dillenni,
nopal has the advantage of implementing an antioxidant action. The have also shown hypocholesterolemic effects in healthy rats (Ennouri
oxalates in the nopal, form indigestible complexes at the intestinal level et al., 2006).
with components like calcium (McConn & Nakata, 2004). However, An interesting revision analyzes nopal products as an alternative to
Contreras-Padilla et al. (2011) demonstrated that the molar ratio be­ synthetic sources to maintain health or prevent chronic diseases. Ac­
tween oxalate and calcium in all states of maturity was lower than 1. cording to a wide medical substance derived from the nopal Opuntia
This result indicates that the bioavailability of this mineral has not been ficus-indica (L.), these demonstrated that physical and chemical

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E. Hernández-Becerra et al. Journal of Functional Foods 95 (2022) 105183

properties are beneficial for their use as functional and nutraceutical ovariectomized Sprague Dowly rats. Other interesting results from
food. Additionally, studies propose the application of Opuntia to premenopausal women showed that an intake of cladodes powder is an
ameliorate water pollution by using nopal as a biological method. Also, efficient calcium source, improves bone mineral density (BMD) in the
plants could be a bio-absorbent for removing heavy metals from polluted hip and lumbar spine regions, and maintains basal calciuria levels
water and other water contaminants (Mounir et al., 2020). (Aguilera-Barreiro et al., 2013).

3.5. Nopal nutraceutical studies 3.7. Nopal on bone health (Clinical studies)

They isolated several extracts in different phases and found that The intake of dehydrated nopal at a high stage of maturity (600 g)
aqueous extracts showed no significant effect in decreasing blood and with high calcium content could improve bone mineral density
glucose, but the ether extract showed a normoglycemic effect. Luo et al. (BMD) and calciuria and thus prevent osteoporosis (Aguilera-Barreiro
(2010); Manzano et al. (2017), Becerra-Jiménez and Andrade-Cetto et al., 2013).
(2012) report that some extracts of Opuntia streptacantha inhibit the The increase of the calcium content in the diet during growth is an
activity of the alpha-glucosidase enzyme at the intestinal level, which is excellent alternative to increase the peak bone mineral density and
responsible for the antihyperglycemic effect. Those results were also reduce the risk of losses in the bone mineral density after 60 years
found in the same species, in addition to demonstrating the hypogly­ (Arjmandi et al., 2010; Hooshmand et al., 2008; Ishimi, 2009; Nomura
cemic and hypolipidemic effects mainly due to the soluble fiber content et al., 2005; Watkins et al., 2007). Similar results are shown in a study of
in young cladodes (Becerra-Jiménez & Andrade-Cetto, 2012; Leem, Kim, 181 women aged 35 to 55 with low bone mass from a total population of
Hahm, & Kim, 2016; Bouzghaya et al., 2016). They also found a pro­ 817 women, all of whom are from the central part of Mexico (Aguilera-
tective effect in the pancreatic islets compared to the control group in a Barreiro et al., 2013). Four groups were formed: A regular group that
diabetic rat model and suggested an effect of nopal extracts at the level included women with normal BMD (bone mineral density) as a reference
of the islets of Langerhans in the pancreas, promoting the production of population by Dual-energy X-ray absorptiometry (DXA) (n = 50), a
insulin by β-cells (Butterweck et al., 2011). Control group (CG), including women with normocalciuria (n = 66),
Opuntia ficus-indica could have a greater effect on cholesterol and finally the two experimental groups with hypercalciuria (n = 65),
reduction since some polyphenolic compounds inhibit the functions of called Experimental group 1 (EG1), with 2.5 g of dehydrated nopal (n =
enzymes involved in the hydrolysis of carbohydrates and fats. Pancreatic 29) and Experimental group 2 (EG2), with 15 g of dehydrated nopal (n
lipase is a key enzyme in the digestion and absorption of triacylglycerol = 36). The study had two years of follow-up and was divided into pre
in the diet. It hydrolyzes triacylglycerol to monoacrylic glycerol and and post-menopausal women. Its important remark was that after the
fatty acids. It is known that dietary fat is not absorbed directly in the first semester of treatment, calciuria levels in women from both exper­
intestine unless it has undergone the action of pancreatic lipase. Ac­ imental groups returned to normal, remaining constant for the rest of the
cording to the study in which the hypocholesterolemic effect of an treatment. The percentage difference in BMD significantly increased in
Opuntia ficus-indica extract was tested, it could be because the extract the total hip region in the CG (pre 4.5 % and post 2.1 %) and EG2 (pre
prevents hydrolysis of dietary fat fiber possibly in the small intestine and 1.8 % and post 2.5 %) groups compared to NG and EG1, which exhibited
reduces the subsequent intestinal absorption of dietary fat. However, a significant decrease in their BMD.BMD increased by 2.5 % for the
until now, the main mechanisms were not clear. Therefore, the next group EG2 (premenopausal) only for the lumbar region. This work
investigations with nopal should focus on controlling the maturity of the concludes that the maximum dehydrated nopal dose (15 g) used im­
used nopal and clarifying the mechanisms of action (Padilla-Camberos proves BMD in premenopausal women with low bone mass in the total
et al., 2015). hip and lumbar spine, maintaining the calciuria at normal levels. This
study is very important to prevent osteoporosis since it is known that
3.6. Nopal on bone health (Preclinical studies) after 40 years of age in women, there is a negative balance in the BMD,
which is responsible for the physiological loss of bone mass (0.5 per
Experiments with the Opuntia genus related to bone health include year). Besides, in postmenopause, it is lost from 3 to 5 % per year,
the work done by administering the nopal himifusa species to Sprague especially the trabecular bone (lumbar spine), during the first 7 years,
Dowly male rats to evaluate bone mineral density and bone health then, the loss is from 0.75 % per year (Riggs, Sundeep, & Melton, 2002).
biomarkers, such as osteocalcin and parathyroid hormone, as well as
alkaline phosphatase, among others. They suggest that Opuntia himufusa 4. Conclusions
can be used as a functional food to improve bone mineral density and
strengthen bone through hormonal regulation (Kang, Park, Choi, Igawa, The nopal cladodes are becoming an invaluable plant for human and
& Song, 2012). Subsequently, they showed the potential of nopal as a animal food worldwide due to their physicochemical composition
functional food in rats fed during the growth stage with nopal Opuntia changes as a function of the maturity and physiological condition that
ficus indica using nopal with 1000 g of weight as a sole source of calcium. tolerates a low quantity of water, their nutritional values, and human
The results showed thicker trabeculae in the metaphyseal region of the health benefits. This is an advantage in the process of climate change
femur of male Wistar rats compared to the control group. Besides, the that provokes a major extension of arid and semi-arid zones on the
bone mineral density was higher in the rats fed with nopal in the late whole planet.
maturity stage than in the rat group fed with nopal in the early maturity According to this review, the potential applications of nopal depend
stage (Hernández-Becerra et al, 2017). In the same way, changes in on the in-depth knowledge of all physicochemical properties consid­
biomarkers (osteocalcin and procollagen amino-terminal propeptide) of ering the maturity stage that reveals strong differences in their proper­
bone health were previously reported (Hernandez-Becerra et al., 2019), ties, which opens a new window for potential applications of nopal
indicating that the maturity stage determines their attributes for bone cladodes as a functional food, which can select the cladode maturity
health. In addition to being a vitak calcium source, the nopal contains according to food and nutrition requirements. In the same way, based on
high magnesium and potassium concentrations that contribute to bone our experience, we consider that future research using nopal for treat­
formation. Posterior research found that nopal avoids the potassium and ment of different diseases such as osteopenia, osteoporosis, hiper-
magnesium bone loss in ovariectomized Wistar rats and improves the calciurea, diabetes should consider the maturity state and the vari­
bone mineral density and trabecular and cortical bone tissue micro­ eties. We suggest that the nopal as functional food can be selected for
structure. (Quintero-García et al., 2020; Ko et al., 2014) reported a different diseases according to maturity. Future studies should clarify
synergetic effect of nopal extract on menopausal symptoms in macromolecules and secondary metabolites’ main action mechanisms in

6
E. Hernández-Becerra et al. Journal of Functional Foods 95 (2022) 105183

chronic degenerative diseases. of cladodes from Opuntia spp. cultivars with different domestication gradient.
Journal of Food Composition and Analysis, 43, 119–130. https://doi.org/10.1016/j.
jfca.2015.04.016
5. Perspectives and suggestions Becerra-Jiménez, J., & Andrade-Cetto, A. (2012). Effect of Opuntia streptacantha Lem. on
alpha-glucosidase activity. Journal of Ethnopharmacology, 139(2), 493–496. https://
doi:10.1016/j.jep.2011.11.039.
Considering the nutritional values for each maturity stage of clad­
Bensadón, S., Hervert-Hernández, D., Sáyago-Ayerdi, S. G., & Goñi, I. (2010). By-
odes products, they can be included in the diet as food, thus treating or products of Opuntia ficus-indica as a source of antioxidant dietary fiber. Plant Foods
preventing nutritional non-hereditary chronic diseases associated with for Human Nutrition, 65(3), 210–216. https://doi.org/10.1007/s11130-010-0176-2
nutritional scarcity. Nopal pad powder at high maturity stages could be Betancourt-Domínguez, M. A., Hernández-Pérez, T., García-Saucedo, P., Cruz-
Hernández, A., Paredes-López, O. (2006). Physico-chemical changes in cladodes
an alternative fiber and mineral source to receive the daily calcium (nopalitos) from cultivated and wild cacti (Opuntia spp.). Plant Foods for Human
required for bone health in developing countries. Young nopals in Nutrition, 61, 115-119. https://doi:10.1007/s11130-006-0008-6.
human diets are recommendable because of their mucilage content and Blando, F., Russo, R., Negro, C., De Bellis, L., & Frassinetti, S. (2019). Antimicrobial and
antibiofilm activity against Staphylococcus aureus of Opuntia ficus-indica (L.) Mill.
normalizing glycemic homeostasis. To include nopal cladodes in the cladode polyphenolic extracts. Antioxidants, 8(5), 117. https://doi.org/10.3390/
diet, selecting them according to the maturity stage is a better strategy, antiox8050117
using adequate food products for the nutritional requirements of the Bouzghaya, S., Bendhifi-Zarroug, M., Borgi, M. A., & Sami, S. (2016). Hypoglycemic and
antioxidant effects of Opuntia streptacantha cladodes juice in alloxan-induced
human individual. diabetic rats in alloxan-induced diabetic rats. Elixer Food Science, 96, 41790–41795.
Considering the mineral content in this vegetable, it can ameliorate Butterweck, V., Semlin, L., Feistel, B., Pischel, I., Bauer, K., & Verspohl, E. J. (2011).
the damage of food deficiencies or prevent the development of non- Comparative evaluation of two different Opuntia ficus-indica extracts for blood sugar
lowering effects in rats. Phytotherapy Research, 25(3), 370–375. https://doi:10.1002/
heritage chronic diseases. To treat the low mineral content in diets,
ptr.3271.
we recommend using nopal products alternative to dairy products. We Cantwell, M., Rodriguez-Felix, A., & Robles-Contreras, F. (1992). Postharvest physiology
also recommend its use when there is a lactose intolerance problem, thus of prickly pear cactus. Scientia Horticulturae, 50(2), 1–9. https://doi.org/10.1016/
S0304-4238(05)80003-2
solving the calcium requirement.
Cárdenas-Medellín, M. L., Serna Saldívar, S. O., & Velazco de la Garza, J. (1998). Effect of
raw and cooked nopal (Opuntia ficus indica) ingestion on growth and profile of total
Ethical statement cholesterol, lipoproteins, and blood glucose in rats. Archivos Latinoamericanos de
Nutricion, 48, 316–323.
Contreras-Padilla, M., Pérez-Torrero, E., Hernández-Urbiola, M., Hernández-
The review paper not involved any human and animal experimental Quevedo, G., del Real, A., … Rodriguez-Garcia, M. E. (2011). Evaluation of oxalates
subjects. and calcium in nopal pads (Opuntia Ficus Indica var. redonda) at different maturity
stages. Journal of Food Composition and Analysis, 24, 38–43. https://doi.org/
10.1016/j.jfca.2010.03.028
Declaration of Competing Interest Contreras-Padilla, M., Gutiérrez-Cortez, E., M.C. Valderrama-Bravo, M., Rojas-Molina, I.,
Espinosa-Arbeláez, D. G., … Rodriguez-Garcia, M. E. (2012). Effects of drying
process on the physicochemical properties of nopal cladodes at different maturity
The authors declare that they have no known competing financial
stages. Plant foods for Human Nutrition, 67(1), 44-49. https://doi.10.1007/s11130-
interests or personal relationships that could have appeared to influence 011-0265-x.
the work reported in this paper. Contreras-Padilla, M., Rivera-Muñoz, E. M., Gutiérrez-Cortez, E., del López, A. R., &
Rodríguez-García, M. E. (2015). Characterization of crystalline structures in Opuntia
ficus-indica. Journal of Biological Physics, 41(1), 99–112. https://doi.org/10.1007/
Acknowledgment s10867-014-9368-6
Contreras-Padilla, M., Rodríguez-García, M. E., Gutiérrez-Cortez, E., M.C. Valderrama-
Ezequiel Hernández thanks CONACYT-México for the financial Bravo, M., Rojas-Molina, J. I., & Rivera-Muñoz, E. M. (2016). Physicochemical and
rheological characterization of Opuntia ficus mucilage at three different maturity
support of his postdoctoral fellowship pat CFATA, UNAM Campus stages of cladode. European Polymer Journal, 78, 226-234. https://doi.org/10.1016/
Juriquilla. Authors thank Beatriz Millan-Malo for the technical support. j.eurpolymj.2016.03.024.
E. Perez-Torrero thanks Universidad Autónoma de Querétaro for the Del-Valle, V., Hernandez-Muñoz, P., Guarda, A., & Galotto, M. J. (2005). Development of
a cactus-mucilage edible coating (Opuntia ficus indica) and its application to extend
project FIN-2021-23, Fondo para el Desarrollo del Conocimiento. strawberry (Fragaria ananassa) shelf-life. Food Chemistry, 91, 751–756. https://doi.
org/10.1016/j.foodchem.2004.07.002
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