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Food Reviews International
ISSN: 8755-9129 (Print) 1525-6103 (Online) Journal homepage: https://www.tandfonline.com/loi/lfri20
Opuntia Ficus Indica Edible Parts: A Food and

Nutritional Security Perspective
Francisco J. Barba, Cyrielle Garcia, Amandine Fessard, Paulo E.S. Munekata,

Jose M. Lorenzo, Aouatif Aboudia, Adbelouahab Ouadia & Fabienne Remize
To cite this article: Francisco J. Barba, Cyrielle Garcia, Amandine Fessard, Paulo E.S. Munekata,
Jose M. Lorenzo, Aouatif Aboudia, Adbelouahab Ouadia & Fabienne Remize (2020): Opuntia�Ficus
Indica Edible Parts: A Food and Nutritional Security Perspective, Food Reviews International, DOI:
10.1080/87559129.2020.1756844
To link to this article: https://doi.org/10.1080/87559129.2020.1756844
Published online: 15 May 2020.
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FOOD REVIEWS INTERNATIONAL
https://doi.org/10.1080/87559129.2020.1756844
Opuntia Ficus Indica Edible Parts: A Food and Nutritional

Security Perspective
Francisco J. Barba a, Cyrielle Garcia b, Amandine Fessardb, Paulo E.S. Munekatac,
Jose M. Lorenzo c, Aouatif Aboudiad, Adbelouahab Ouadiad, and Fabienne Remize b
a
Nutrition and Food Science Area, Preventive Medicine and Public Health, Food Science, Toxicology and
Forensic Medicine Department, Universitat de València, València, Spain; bUMR QualiSud, Université de La
Réunion, CIRAD, Université Montpellier, Montpellier SupAgro, Université d’Avignon et des Pays de Vaucluse,
Sainte Clotilde, France; cCentro Tecnológico de la Carne de Galicia, San Cibrao Das Viñas, Ourense, Spain;
d
Laboratoire Aliments-Environnement-Santé, Faculté des Sciences et Techniques, Université Cadi Ayyad,
Marrakech, Morocco
ABSTRACT KEYWORDS
Cactus Opuntia ficus indica is widely distributed in (semi-) arid regions. Prickly pear; phenolic
Fruit and cladodes are processed into many food products. Cladodes are compounds; carotenoids;
used as vegetables, but their main use is flour, which can partly substitute health; food safety; lactic
acid bacteria;
wheat or corn flour in bread, cookies or cakes. Fruit are mainly trans-
minimally-processed
formed into snacks, juices or minimally-processed foods. Mucilage, color-
ing extracts and antimicrobial extracts are valuable by-products of cactus
processing. Fruit and cladodes are characterized by a high antioxidant
activity. They contain ferulic acid as the predominant phenolic acid, rutin
and isorhamnetin derivatives as the main flavonoids, and betalain pig-
ments, but also lutein and beta-carotene, as the most abundant colored
compounds present in skin and pulp. Bakery products containing cladode
flour are enriched in fiber, minerals and polyphenols. Processing, through
drying, heat treatment or innovative technologies, aims to preserve fruit
nutritional and sensory characteristics. In recent years, lactic acid fermen-
tation of plant-based foods demonstrated many benefits. Fermentation
modifies vitamin C level, carotenoid, phenolic compound content and
antioxidant activity. Moreover, fermentation of cladode pulp showed
promising functional feature on inflammatory response through modula-
tion of cytokine secretion. This opens new perspectives for the develop-
ment of products with health benefits.
Introduction
The importance of fruit and vegetables for human diet is recognized as they provide
nutrients and phytochemicals (e.g. phenolic compounds, alkaloids, nitrogen compounds,
organosulfur compounds, dietary fibers, phytosterols and carotenoids) which can mod-
ulate metabolic processes and thus, provide desirable health effects[1–3]
Opuntia ficus indica is a member of the Cactaceae family, with 300 other species. It originally
comes from America but has been spread into Europe and Africa.[4–6] O. ficus indica is the most
widely found species, being the only cultivated species in the Mediterranean areas. Nowadays, it
is mainly cultivated in arid or semi-arid regions, like in Central and South America, southern
Spain, around the Mediterranean Sea, Angola, Australia, India and South Africa.[7,8]
CONTACT Fabienne Remize [email protected] QualiSud, ESIROI Université De La Réunion, 2 Rue

Wetzell, Sainte Clotilde F-97490, France
© 2020 Taylor & Francis
2 F. J. BARBA ET AL.
Its edible fruit, called prickly pear or cactus pear, is a good source of minerals, provides
essential amino acids and vitamins, and presents a high antioxidant activity, thanks to its
high content in carotenoids and phenolic compounds.[9,10] Cladodes, which are the
flattened stems of the plant, are consumed as vegetables when they are young and tender,
or used to feed cattle when they become older. These edible parts of the plant are currently
used to produce a large variety of products.[7]
Among food processes which can increase shelf-life, fermentation has a prominent
place regarding its sustainability and ability to maintain nutritional and sensory quality of
food products.[11–15] Lactic acid fermentation can increase the content of bioactive pep-
tides, short chain fatty acids or polysaccharides, whereas the contents of sugar or anti-
nutritional compound can decrease. During lactic acid fermentation, phenolic compounds
are converted into substances with increased biological value. Lastly, lactic fermented
foods may provide pre- and pro-biotics, which are recognized for their positive effect on
gastrointestinal health.[16–18]
This review aims to underline the current and future importance of O. ficus indica from
a food and nutritional security perspective. The effect of processing applied to obtain fruit-
or cladode-based food or beverages on safety, sensory features and nutritional composi-
tion was reviewed. The advantages of lactic acid fermentation or probiotic addition
towards the development of products from O. ficus indica were also discussed.
Characteristics of the plant

More than all, Opuntia plants are a natural resource in countries with low water avail-
ability. The plant can grow in conditions where other plants do not survive. The root
system can exploit scarce water rainfall. Water can be stored in large parenchyma of the
cladode tissues where the water loss is limited because of a thick cuticle, presence of spines
and a low number of stomas, which are closing during the day.[8] Moreover, photosynth-
esis occurs in the cladodes.[19,20]
Opuntia, like Agave and pineapple, exhibits a crassulacean acid metabolism (CAM),
which is a specialized mode of photosynthesis enhancing plant water-use efficiency.
Climate change models simulate a potential increase in the frequency and intensity of
drought, resulting into an increased competition for land and water resources. The context
of sustainable practices in agriculture and the growing interest for local crops appear now
as key-drivers to investigate the development of Opuntia crop and food products.[4,21]
Yang et al.[20] proposed to develop a system-level analysis of agricultural production in
order to implement productivity models for CAM plants. It should be noted that Opuntia
productivity is extremely variable (4–30 tons/ha), depending on the production area and
agricultural practices.[4] Yields up to 263 t/ha have been recorded.[6]
In Mexico, Opuntia is cultivated in two areas, both above 1800 meters above sea level,
with a wet period in summer when rainfall represents 400 to 700 mm, and average
temperatures of 14–18°C. In South Africa, it is cultivated in several provinces, from 314
to 1348 meters above sea level, and with annual rainfall in the range 239–556 mm,
essentially in summer.[22] Fruit yield varied in South Africa from 4.97 to 30.67 t/ha
depending on the cultivar for both the same area of production and year.[22] In this
country, the exploration of cactus pear as a commercial crop has become of great concern
as a consequence of climate changes on food security. The influence of crop location,
FOOD REVIEWS INTERNATIONAL 3
cultivar and season on fruit nutritional and sensory quality has been explored.[23,24] On
the other hand, in Sardinia, Opuntia spp. was rarely found above 800 mm and did not
survive where temperatures were below 2°C, but rainfall did not affect occurrence nor fruit
size, whereas it affected plant size and vigor.[25] The plant also grows in Canada where
temperatures are often negative.[21]
Cactus pear fruit production plays a strategic role in semiarid areas of the world, like
Mexico, Spain, Italy, South Africa, Egypt, Morocco and Algeria. For instance, in Sicily, the
survival of SMEs (Small and Medium-sized enterprises) was reported to depend on the
production and transformation of cactus fruit.[26]
Fruit and cladode characteristics

The plant can grow up to 3–5 meters in shrubs (Fig. 1). The cladodes have a racket-shape, and
harbor buds which can lead to flowers or new cladodes, or even roots. The fruit is a false berry
and non-climacteric. It exhibits a mass in the range 75 to 200 g and its color varies from green
to red, possible yellow, orange, or purple. The pulp has the same color as the peel and contains
many seeds. Up to now, seedless or parthenocarpic fruit were difficult to obtain because of the
requirement of ovule fertilization stimulus for pulp differentiation from epidermal cells. But
treatments with gibberellic acid resulted in the artificial induction of seed abortion. However,
seedless fruit were smaller with a thicker skin.[4,27,28]
It was hypothesized that vegetative vigor and fruit size were correlated to ploidy
level.[27] Fruit mass, percent of pulp, total soluble solid content, pH, titratable acidity
and glucose and fructose content significantly differ among cultivars and sampling
seasons. For instance, pulp pH varied from 5.4 to 7.5 depending on the cultivar and the
season.[29] Cultivar, season and their interaction influence those attributes.[29,30] Season
impact was confirmed by Boutakiout et al.[31] who observed a ca. 2-fold higher antioxidant
Figure 1. Examples of products. (a): Opuntia ficus indica crop, (b): fruits at retail, (c): fruit on cladode,
(d): peeled fruits, (e): hand-crafted products: dried flowers, jam, juice, and cattle-cake, (f): fruit nectar,
(g): cladode in brine. All pictures are from A. Aboudia, and A. Ouadia, Université Cadi Ayyad, Marrakech,
Morocco.
activity, together with a lower water content, of cladodes sampled in summer compared to
spring. They hypothesized that drought stress influenced the accumulation of secondary
bioactive metabolites, like polyphenols.
Willingness to buy a cactus fruit is influenced by many factors, like local origin of fruit,
related to a presumption of safety, expected nutritional benefits, environmental sustain-
ability and ethical considerations, appearance, and a low quantity of seeds. For cactus fruit
in Italy, it was shown that besides environmental, local origin and healthfulness consid-
erations, red color, few seeds and availability of peeled fruit, due to the presence of fine
barbed spines on the fruit skin, prevail on the consumption intentions.[32]
Traditionally, the fruit is eaten fresh, after peeling. Fresh fruit is sensitive to chilling
injury at temperatures below 8–10°C.[33,34] Over storage, fruit mass loss reaches 8% over
77 days. However, storage at room temperature is possible over 5 weeks, without altering
nutritional and bioactive properties.[35]
Bioactive compounds
Fruit
Prickly pear fruit has an aqueous pulp and contains 87.5% of water. It has a low energy
density of 170 kJ/100 g. Its carbohydrate content, mainly glucose and fructose, provides
94% of the energy density. It exhibits a low titratable acidity of 1.83 g citric acid/kg, which
is below what found in orange, pineapple and banana.[36,37]
Prickly pear fruit contains 11.14 ± 0.40 g/100 g of dry weight (dw) of dietary fiber, meaning
carbohydrate polymers with ten or more monomeric units not hydrolyzed by endogenous
enzymes, quantified using AOAC official methodologies. The dietary fiber soluble fraction
represents 2.41 ± 0.03 g/100 dw in the pulp and 6.97 ± 0.28 g/100 dw in the peel. It is mainly
constituted by mucilage, a pectin-like compound with high content of galacturonic acids, that
has the ability to promote water retention. Fructo-oligosaccharides are observed in the pulp
too.[37] The composition of insoluble dietary fiber mainly consists of hemicellulose and cellulose
while lignin content is scarce.[36] Peel dietary fibers are structural polysaccharides associated with
minerals in plant cells, thereby prickly pear peels show a notable mineral content, higher than in
pulps, which is mainly composed of potassium, phosphorus, magnesium and calcium.[36]
The antioxidant activity of prickly pear is reported to be comparable to that of red oranges
and grapes.[38] It exerts biological effects, may be due to synergistic action of betalains,
flavonoids and other biologically active components.[39] All parts of the cactus plant are rich
in polyphenols, being various flavonoids and phenolic acids. The total phenolic content
measured of prickly pear fruit pulp can reach 218.8 mg gallic acid equivalents/100 g fresh
fruit in red-skinned fruit. Prickly pear fruit is considered as a rich source of flavonols (Fig. 2)
and the quantification of five types of flavonoids showed that quercetin was the predominant
one (58.7 ± 54.3%), followed by isorhamnetin (31.7 ± 18.8%), luteolin (11.5 ± 5.4%), and
kaempferol (11.0 ± 4.8%).[40] The analysis of the peels showed that isorhamnetin glycosides,
especially isorhamnetin-3-O-rutinoside, are the main flavonol glycosides present in prickly
pear peels.[41] More than 20 polyphenolic compounds, including flavonoids and tannins, were
also detected in the seeds and their content was significantly correlated with the antioxidant
activity of defatted seeds.[7,42,43]
Figure 2. Structure of the main prickly pear flavonols and carotenoids.
Prickly pear is rich in carotenoids, and their concentration is significantly higher in the
peel than in the pulp. Carotenoid content ranges from 2.58 to 6.68 µg/100 g fresh weight
in Spanish orange and red fleshed whole fruit.[38,40,44] HPLC analysis showed nine
xanthophylls, contributing to around 84–86% of the total carotenoids, and four carotenes,
all in the unesterified form. The predominant compounds were (all-E-)-lutein, (all-E-)-β-
carotene and (all-E-)-violaxanthin, representing respectively ≈69–72%, 12–14% and 5% of
the total carotenoid content in the whole fruit, followed by (all-E-)-zeaxanthin, (all-E-)-
anteraxanthin and (all-E-)-neoxanthin[38] (Fig. 2).
Besides carotenoids, other antioxidant compounds, like betacyanins, phenols and
vitamin C levels are proportionally higher in peel tissues than in pulp, while betaxanthins
are distributed uniformly among the fruit, peel and pulp.[38] Betalains are water soluble
hydroxylated and glycosylated pigments that contribute to prickly pear fruit color, varying
from yellow to purple (Fig. 3). The fruit pulp shows a majority of betacyanins, including
betanin, isobetanin, betanidin, isobetanidin and phyllocactin; representing 26.2–89.2 μg/g
dw in yellow fruit, 343–525 μg/g dw in red fruit, 1083.6–2066.9 μg/g dw in purple fruit
among Mexican and Spanish varieties[45] which corresponds to 11–19%, 46-68% and
84–91% of total betalains in yellow, red and purple fruit pulp, respectively. Antioxidant
compound content is the highest in purple or orange fruit.[24,46] The same studies showed
that antioxidant activity of orange or pink fruit is mostly due to ascorbic acid.
The prickly pear fruit contains ≈23 mg betanin equivalents/100 g fresh weight, mostly
in the endocarp, thus conferring strong antioxidant properties linked to their structural
features.[47] A study on prickly pear juices from cultivars of different colors, also showed
higher betacyanins/betaxanthins ratios in red/purple cultivars than in orange and yellow
ones, and this was confirmed by a precise RP-LC-DAD-MS/MS analysis comparing pulp
and peel fruits.[39,48] Moreover, prickly pear fruit has a considerably higher ascorbic acid
content than other fruit, such as peaches, grapes and apples. Although this concentration
Figure 3. General structure of betalains. (a) betaxanthins and (b) betacyanins.
is higher in red than in yellow fruit (815 μg/g fresh weight versus 23.7 μg/g fresh weight),
ascorbic acid content is not correlated with prickly fruit skin color.[44]
Prickly pear peel makes up about 40% of the whole fruit weight and its lipid content is
36.8 g/kg dw.[49] Neutral lipids are the predominant, with linoleic acid being the main
component of triglycerides (49.3–62.1% of total fatty acids), followed by oleic acid (13–-
23.5%) and palmitic acid (10.6–20.1%).[49–51]
Cactus pear pulp can be divided into 15% seeds and 85% strained pulp. The seeds are rich in
lipophilic compounds with a large amount of oil (98.8 g/kg dw), while total lipids recovered
from lyophilized strained pulp, accounted for 8.70 g/kg.[51] Vitamin E level seems to be higher in
the pulp than in the seed. A study on 10 cultivars of O. ficus indica quantified low amounts of
total tocopherols in fruit by HPLC, being the highest ≈92 μg/100 g fw, with an α-tocopherol/δ-
tocopherol ratio about 2:1 in all the cultivar lines, while β- and γ-tocopherol were not found.[52]
In prickly pear, prolin is the predominant amino acid, representing around 46% of
amino acid content. A considerable taurine content was also reported after RP-HPLC
quantification, representing ≈16% of the total amino acids content,[40] but this high level
has been recently questioned after using Ion Exchange Chromatography as the authors did
not observe any taurine. Some antioxidant activity of taurine has been reported, likewise
involved in blood pressure regulation.[42] By contrast, the major amino acid found in seeds
is glutamic acid (15.73–20.27%), followed by arginine (4.81–14.62%).[8]
Cladodes
Phenolic compounds (2.48 g gallic acid equivalent/100 g dw) and flavonoids (1.06 g quercetin
equivalent/100 g dw) are the main antioxidant compounds of O. ficus indica cladodes.[53,54] As
previously reported,[55] the stage of maturity of cladodes influences their phytochemical
profile as young cladodes (12 days, 40 ± 10 g) are the richest in condensed and hydrolysable
tannins whereas medium-age cladodes (20 days, 74 ± 20 g) contain the highest concentration
of p-hydroxybenzoic acid, p-coumaric acid, rutin, narcissin, nicotiflorin, β-sitosterol, and
sitosteryl-3-β-glucopyranoside. Lutein, β-carotene and β-criptoxanthin are the most abun-
dant carotenoids in fresh cladodes.[56] Cladodes contain more carotene and phenolic com-
pounds than the fruit, regardless of the cultivar.[24]
Health effects
The richness in antioxidant molecules, particularly polyphenols, makes prickly pear a good
candidate to be used in functional food. A review by El-Mostafa et al.[8] reported interesting
results regarding the antioxidant and/or anti-inflammatory properties of prickly pear pre-
parations in different experimental models, in vitro and in vivo studies. Concerning prickly
pear betalain compounds specifically, a positive correlation was found between betaxanthins
content of prickly pear pulp and peel and the antiangiogenic activity (r > 0.5176), a phenom-
enon related to inflammatory processes.[48] By comparison with red flesh fruits, yellow and
orange water prickly pear extracts exhibited significant ability to protect DNA from the
damage caused by hydrogen peroxide. However, this effect may be irrespective of color
pigments, since the vitamin C was most likely responsible for prevention of oxidative DNA
damage. Yellow flesh pulp water-extract also displayed some potential to induce glutathione
S-transferases, phase II detoxification enzymes, following 6 h incubation with HT-29 intestinal
cells.[57] Prickly pear indicaxanthin, a betalain pigment with demonstrated bioavailability,[58]
was reported to inhibit oxidized low-density lipoproteins-induced cytotoxicity in vitro by
modulating the transcriptional activity of NF-κB.[59] Opuntia fruit in combination with
cladodes also showed some anti-microbial effects and anti-diabetic effects, improving meta-
bolic parameters and lipid profile.[8] It was observed that cladodes on their side, undergoing
in vitro colonic fermentation and following gastro-intestinal digestion, could reduce the H2O2
-induced DNA damage in a colonic cell model. This effect may be attributed to polyphenolic
compounds that remained stable in the gut.[60]
Beyond studies on prickly pear extract supplementation using an animal model, a five
human trial meta-analysis also disclosed that prickly pear supplementation can cause
significant reductions in body fat percentage, blood pressure, and total cholesterol without
significant difference in body weight.[61]
Processing and uses of cladodes

Exploitation as food products
Cactus cladodes are usually consumed fresh after peeling, or cooked (boiled, griddled, fried) or
also as juices or sauces.[6,62,63] Cooking induces changes in the nutritional composition of
cactus cladodes. For instance, microwaving and griddling treatments are the most favorable
culinary methodologies to increase the content of flavonoids and phenolic acids, as well as
antioxidant capacity of Opuntia cladodes.[62] These two cooking methods also increased the
content of soluble and insoluble fiber. Cladode juice, dried cladodes, cladodes in brine (Fig. 1),
pickles of cladodes and cladode chutney can be processed from different cultivars, and the
impact of processing on antioxidant activity is higher than that of the cultivar.[64] Several
blended juices containing cladode juice were assayed: blends with guava juice and with kiwi
fruit and pear were the better sensory acceptable.[23]
Processing into flours and food fortification

Cladode flour is produced from mature cladodes and can be incorporated in dough,
biscuits, soups or desserts, thereby increasing fiber content.[23,63] Mixed with nixtamalized
corn flour, cladode flour incorporated at a 4% level, resulted in an increased fiber content
and improved rheological properties and workability of an instant corn meal dough.[65]
Similarly, the addition of cladode flour to bake tortillas positively affected the nutritional
and rheological properties.[66]
The substitution of 5% wheat flour in bread by cladode flour increased fiber, calcium,
potassium and polyphenol contents. It increased dough extensibility and water holding
capacity.[53,67] This replacement, thus led to a reduction of bread mass loss after baking
and the sensory characteristics of the obtained bread were acceptable, in spite of a specific
odor and a light green color. Similar results were obtained with cladode flour mixed with
seeds and whole wheat flour.[23] The conditions for cladode flour processing were shown
to have a great impact on rheological properties and composition.[68]
Oat cookies and carrot cakes with replacement of respectively 10% and 25% of flour by
cladode flour resulted in acceptable products for taste and texture.[23]
Eventually, African fermented beer from maize or sorghum was produced with repla-
cement of 25% of flour with cladode flour.[23]
Natural polymers
Mucilage of O. ficus indica is a polysaccharide composed of arabinose, galactose, rham-
nose, xylose, and galacturonic acid which is mainly found in cladodes and skin of the
fruits.[69] Its hydrocolloid properties have been investigated for use as an encapsulation
material for phenolic acid[70] or pigments,[71,72] as an emulsifying agent,[69,73,74] and as an
edible coating to preserve fresh fruit[75,76] or fresh-cut fruit.[77] It was also used to replace
25–50% gelatine in Turkish delight.[23]
The use of mucilage showed a good degree of encapsulation of the bioactive com-
pounds over spray-drying process and a further release of the compounds under simulated
intestinal tract conditions.[70] For example, encapsulation of betalains in maltodextrin/
mucilage was achieved with a high recovery rate and the bioactive compounds were
retained over 25 days at 18°C when relative humidity was below 57%.[72]
The firmness, color and sensory characteristics of strawberries stored up to 9 days
under refrigeration were improved when coated with a mucilage film from Opuntia.[76]
Similar results were obtained with coated figs, and Enterobacteriaceae growth on fruit was
significantly slowed down.[75] The application of mucilage coating onto kiwi fruit slices
also resulted in an improved preservation of physical and sensory properties during
refrigerated storage. However, the effect of coating on microbiological quality was positive
only for 5 days of storage.[77]
Microwave assisted gum extraction of the fruit allowed to obtain a heterogenic polysacchar-
ide composed of glucose, arabinose, xylose, galactose and mannose. The associated phenol
content conferred a strong radical scavenging activity, comparable to that of BHT. This
polysaccharide also exhibited excellent stabilizing property due to its high molecular weight,
viscofying and gelation ability, allowed to consider it use in food or pharmaceutical systems.[78]
Extracts used for antimicrobial or coloring properties

Consumer demand for healthier foods induces a growing trend towards the development
of natural ingredients such as colorants and antimicrobials. Extraction of these com-
pounds add value to by-products. Natural pigments present in prickly pear are of high
interest to replace artificial colorants in food.[79] For instance, both the extraction and
encapsulation of betalains has been widely investigated by different authors.[80–82]
A successful encapsulation of red/violet betacyanins and yellow/orange betaxanthins
was obtained with a polymer based on modified corn starch, added to purple pulp or an
ultra-filtered extract. However, a loss of 50% of betanin was observed after 20 to 35 days of
storage at 60°C.[82] In another study, betalains extracted from prickly pear pulp, were
encapsulated and used to prepare gummy candies.[80]
Cladode methanolic extracts exerted a high anti-Vibrio cholerae activity, caused by
membrane damages and decrease of ATP cellular level.[83] Moreover, stem extracts were
compared to other plant extracts for their antibacterial activity against Enterobacter
aerogenes, Escherichia coli, Salmonella typhi and Staphylococcus aureus, observing that
O. ficus indica extracts were efficient but in a lesser extent than other plants.[84] More
recently, it was found that Opuntia cladodes (crude and aqueous extracts) were capable of
inhibiting the growth of S. aureus, E. coli, Klebsiella pneumoniae and Pseudomonas
aeruginosa at a concentration of 0.1 mg/mL.[85] The authors attributed the inhibition to
the polar components present in the extract.
Prickly pear pulp also showed an antimicrobial activity against S. aureus, Bacillus cereus,
Micrococcus flavus, Listeria monocytogenes, E. coli, P. aeruginosa, Salmonella enterica serotype
Typhimurium, Enterobacter cloacae, Aspergillus fumigatus, Aspergillus ochraceus, Aspergillus
versicolor, Aspergillus niger, Penicillium funiculosum, Penicillium ochrochloron, Penicillium
verrucosum var. cyclopium, and Trichoderma viride.[79] An aqueous extract of pulp was
efficiently used to prolong shelf-life from 4 to 8 days of sliced beef.[86] Not only the red
color of beef was maintained, but texture changes were limited by the extract.
Processing of prickly pear

Fresh-cut fruit
The valorization of prickly pear for the food sector largely depends on its transformation.
Whatever its purpose, any transformation operation involves the destruction of tissues
and cells through peeling, slicing, shredding, chopping, etc., which brings into contact the
fruit components with air and microorganisms. As a result, enzymatic degradation,
oxidation, loss of flavor and color, and growth of spoilage microorganisms and foodborne
pathogens start.
Prickly pear processing has to meet not only consumer requirements, but also safety
requirements. Due to the pH of the pulp in the range 5.3 to 7.1, the fruit is prone to
microbial spoilage and possibly promotes the development of foodborne pathogens.[87]
The quality of peeled cactus pear can be maintained over 8 days at 4°C, but a temperature
≈15°C limits the shelf-life to 4 days.[88,89]
Minimal processing consists of removing fruit peel and spines (Fig. 1). It is used to
increase fruit acceptability.[87] Different packaging strategies of minimally processed
prickly pear were tested to prolong the shelf-life.[7] Shelf-life determination of fresh-cut
prickly pear fruit was assessed at 4, 8, 12 and 20°C in control (air) and modified (65% N2,
30% CO2, 5% O2) atmosphere.[87] The counts of all microbial groups studied increased
over storage. Moreover, no significant differences between the control conditions (air) and
modified atmosphere packaging were observed. Recently, a shelf-life of 8 days was
obtained by packaging prickly pear fruit in a polystyrene tray under vacuum-applied

polymeric film.[90] In addition, coating prickly pear fruit with alginate seemed to prolong
the shelf-life up to 13 days, reducing the extend of O2 level decrease and CO2 level
increase, although no differences were found in microbial counts.[91] In another study,
chitosan coating containing 1% acetic acid was successfully used to limit microbial growth
over 16 days of storage of fresh prickly pear, but this coating was not efficient to reduce
weight loss neither firmness decrease.[92]
Jam, dehydrated and extruded products

The elimination of peel (48% of fruit mass) and seeds (7%) of prickly pear results in pulp
(45%) which can be used to prepare jam[93] (Fig. 1). Pilot scale manufacturing of jams
resulted in well-accepted products either without or with aromatization with clove extract,
orange or grapefruit flavor.
Air-dried 1 g-fruit pieces were obtained using a solar-dryer at drying temperatures of
50–60°C.[94] In Sicily, pulp purée in 100 g blocks is traditionally processed by natural or
forced drying at ambient temperature for 20–25 days.[95]
Extrusion of prickly pear pulp mixed with rice flour resulted in new snack products.[96] The
extruded rice flour enriched with fruit pulp showed an increased apparent density and breaking
strength whereas porosity and expansion ratios showed the reverse trend. The addition of
freeze-dried pulp to rice or maize flour resulted in extruded snacks enriched in flavanols.[97] The
thermostability of flavanols during extrusion processing allowed increasing isorhamnetin glyco-
side content, especially isorhamnetin-3-O-rutinoside. The obtained prickly pear enriched snacks
exhibited then better nutritional properties than rice- or corn-based ones. Another technology,
instant controlled pressure drop, was applied to obtain textured snacks from prickly pear
peel.[98] This new way of using the peel is an alternative to reduce wastes and by-products
obtained during prickly pear fruit processing. The obtained crispy snacks were very well
accepted by consumers and provided an important amount of β-carotene (229.4–1103.8 mg/
100 g dw), enhancing at the same time phenolics content and antioxidant activity.[98]
A greater impact of processing method (juice pasteurization, fruit drying, canning and
chutney processing) than the initial color of fruit was showed on antioxidant properties
and the content of antioxidant compounds.[46] Dried fruit exhibited the highest content of
antioxidant compounds.
Juices and derived products

Cactus-pear juice is a convenient way to consume the fruit (Fig. 1). But, because of its high
pH value, juice requires a stabilization treatment to preserve its microbiological quality.[7]
Preservation of micronutrients, taste, flavor and color should also be achieved. For
instance, a pasteurization of 20 min at 100°C was reported to improve stability of
O. ficus indica fruit juice, but with dramatical effects on color and flavor.[63]
The preparation of concentrated juices using a two-step non-thermal membrane treat-
ment: i) ultra-filtration to clarify the juice, then followed by ii) osmotic distillation to
concentrate the permeate, was investigated.[99] Ascorbic acid and betaxanthin content in
the concentrated juice represented ca. 37% of the initial content. On the other hand,
betacyanin was better preserved, as the recovery was 56.4%. Osmotic membrane
distillation was used to remove water from the juice, the process being performed at 35°C
for 18 h.[100] Total soluble sugar content increased from 15 °Brix to 23.4 °Brix. The
increase was more pronounced for total phenolics and total flavonoids.
Other non-conventional technologies such as high-pressure processing, pulsed electric
fields and ultrasound have also been used for juice preservation (for a review see[7]). For
instance, several authors have used ultrasound (US) as an alternative to heat-treatments to
preserve prickly pear juice.[101–103] A treatment of 15 min or above significantly reduced total
mesophilic bacteria and enterobacteria counts, without any decrease in antioxidant activity
nor phenolic compound content, and less than 20% ascorbic acid degradation.[102,103]
Antimicrobial effect was confirmed with E. coli-controlled inoculation: US application inacti-
vated E. coli and its population in juice remained lower than in the control condition over
5 days of storage.[104]
The application of US combined with mild thermal treatment (50ºC) (Thermo-US), was
also evaluated.[101] The authors observed a synergistic effect when US and mild treatment were
combined, efficiently reducing total bacteria and enterobacteria counts, maintaining popula-
tions below the control up to 21 days of storage. This processing of prickly pear juice decreased
viscosity and maintained physical stability. However, this treatment could not prevent
browning of juice and a reduction of betaxantin level was also noticed.
Among non-thermal innovative technologies, pulsed electric field (PEF) presents two
positive effects: high voltage application modifies membrane permeability, leading to
microorganism inactivation and to a release of compounds from plant cells.[105] PEF
was applied to another species, Opuntia dillenii, characterized by a different production
season than O. ficus indica, a lower pH and different sensory features.[106] PEF pre-
treatment increased juice yield and the flavonol content, especially isorhamnetin
3-O-rutinoside in the juice, while decreasing viscosity.
Lactic acid fermentation of prickly pear

O. ficus-indica fruit is sweet, delicious and attractive for consumers. Moreover, its inter-
esting composition in functional and bioactive components encourages the development
of beverages with health-promoting and functional properties. However, extending its
short shelf-life requires inactivation of foodborne pathogens and spoilage microorganisms.
Lactic acid fermentation is an alternative to physical treatments to extend the shelf-life of
fruit juice with a preservation of nutritional and functional properties during the
storage.[11,107] Lactic acid bacteria synthesize lactic acid and antimicrobial compounds
(acids, exopolysaccharides, bacteriocins, enzymes, bioactive molecules) which prevent the
growth of undesirable microorganisms.[12,14,108]
Traditionally, cactus pear juice is fermented to provide low-alcoholic beverages, occasionally
further processed into spirits, but also vinegar by a subsequent acetic fermentation.[6] However,
lactic acid fermentation is not reported as a traditional process applied to cactus pear.
Prickly pear fruit subjected to lactic acid fermentation is highly interesting to extend
its shelf-life and improve its functional properties (Table 1). Lactic acid fermentation of
prickly pear was firstly investigated by Son & Lee.[109] The authors used prickly pear
extract (PPE), obtained by mixing 200 grams of fruit with 800 mL of water, as a sub-
strate. The PPE had a pH of 3.99 and 0.35% (w/v) acidity as lactic acid. After a heat
treatment at 80°C for 10 min, the extract was fermented with Lactobacillus rhamnosus
LS isolated from soymilk curd residue, Lactobacillus bulgaricus KCTC3188 and

Lactobacillus brevis KCTC3498 at 30°C for 2 days followed by a storage for 4 weeks at
4°C. Fermentation of the PPE extract was optimized by adding 5% of fructose syrup and
0.2% of yeast extract. The fermented beverage was characterized by an attractive red
color. Viability of LAB was well maintained during the storage, with a population of
1.5–3 × 108 CFU/mL, suggesting that prickly pear beverage is suitable for the growth of
lactic acid bacteria.
More recently, the effect of lactic acid fermentation of cactus fruit puree was
investigated.[111] Lactic acid bacteria population of fresh prickly fruit was 3.25 ± 0.16 log
CFU/g, which was in the same range to that found in other fruits.[107] Due to its high
initial pH, 6.01 ± 0.02, the fruit puree was heat treated (75°C for 5 min) before fermenta-
tion to inactivate vegetative microorganisms. Autochthonous strains of Leuconostoc
mesenteroides fermented the fruit puree at 25°C for 12 h, which was then stored for
21 days at 4°C.[111] The pH of the puree dropped to 3.92 after fermentation. Moreover,
lactic acid fermentation preserved the safety of the prickly pear puree as neither yeast nor
enterobacteria were found after 21 days of storage at 4°C, contrarily to the un-started
puree. A decrease in glucose, fructose and citric acid content was observed during fruit
fermentation, while lactic acid and acetic acid were the main metabolites produced. Total
free amino acid content increased during fermentation with some strains. In addition,
vitamin C and betacyanin contents were significantly higher in the fermented puree. No
significant changes in the polyphenols content was observed over fermentation but the
radical scavenging activity was increased. The fermented purees were preferred compared
to the control regarding smoothness, odor and aroma. Moreover, the accumulation of
galactose and a decrease in viscosity during fermentation proved that selected starters
were able to degrade mucilage. On the other hand, the authors evaluated the impact of
lactic acid fermentation on the anti-inflammatory response by evaluating the release of
nitric oxide after stimulation of Caco-2/TC7 cells by TNFα, IL-1β and IFN-ϒ. Under
optimal culture conditions, Caco-2/TC7 cells developed intercellular tight junctions and
the integrity of the tight junctions can be measured by Trans-Epithelial Electric Resistance
(TEER). Stimulation of the Caco-2/TC7 cells with IL-1β significantly reduced the value of
TEER. All fermented fruit puree attenuated the negative effect and reduced the inflam-
matory status of the Caco-2/TC7 cells.
Prickly pear was also used for the preparation of kefir-like beverage.[112] In this study,
other kinds of fruit were also subjected to fermentation: apple, quince, grape, kiwifruit,
prickly pear and pomegranate by a kefir microbial preparation composed of Lactobacillus
fermentum, Lactobacillus kefiri, Lactoccocus lactis, Lc. mesenteroides and Saccharomyces
cerevisiae. The kefir beverages were produced by back-slopping: first the freeze-dried
microorganisms were activated in fruit juices at 25°C for 72 h to produce an inoculant.
Each inoculant was added (4% v/v) to 1 L of the corresponding juice and the fermentation
was carried out at 25°C for 48 h. Prickly pear kefir exhibited the highest level in
microorganisms, also the highest level of lactic acid (1.00 g/L) but its overall sensory
quality was less appreciated than apple or grape kefir.
In addition to their safety and functional properties, some lactic acid bacteria are
desirable for their probiotic properties. Lactic acid fermentation of prickly pear juice
was carried out using the probiotic strain Lb. fermentum ATCC 9338 for 48 h at 28°
C.[113] The initial pH of the juice was 6.3 ± 0.2 and decreased down to 4.1 ± 0.2 after
Table 1. Main effects of lactic acid fermentation on Opuntia ficus indica beverages.
pH evolution
over
Substrate Processing Fermentative microorganisms fermentation Safety Functional and health effects Sensory properties Reference
[109]
Fruit/water Pasteurization 80°C 10 min; Lb. rhamnosus LS; Lb. bulgaricus From 3.99 to Maintain of ND Attractive pink/red
extract Fermentation 2 days at 30° KCTC3188; Lb. brevis KCTC3498 2.90–3.48 viability of LAB (8 color
C (5% v/v fructose syrup + log CFU/mL)
0.2% w/v yeast extract)
followed by 4 weeks at 4°C
[110]
Young cladode Fermentation 24 h at 30°C Allochthonous strains of Lb. From 4.3 to Presence of yeasts Increase of radical scavenging ND
pulp plantarum; Lb. brevis; Lb. fermentum; 3.98–4.05 (1.0 log CFU/mL) activity
Lb. rossiae; Lb. curvatus; after fermentation Preserve vitamin C and
P. pentosaceus; Lc. mesenteroides; carotenoids
W. cibaria/confusa Increase of kaemferol and
isorhamnetin contents
Reduce inflammatory status of
Caco-2/TC7 cells
[111]
Fruit puree Pasteurization: 75°C for Autochthonous strains of Lc. From 6.01 to pH 3.72–3.78 Antimicrobial activity against Higher sensory
5 min mesenteroides 3.92–4.10 No alteration B. megaterium F6 and E. coli properties (odor,
Fermentation: 12 h at 25°C DSM30083 aroma,
followed by 21 days at 4°C Increase of radical scavenging smoothness)
activity
Maintain of vitamin C and
increase of betacyanins
Reduce inflammatory and
oxidative status of Caco-2/TC7
and PBMC cells
[112]
Fruit juice Pasteurization: 75°C for Kefir microbial preparation From 6.26 to Presence of ND Decrease of
5 min composed of: Lb. fermentum; Lb. 4.11 Enterobacteriaceae redness (a*)
Fermentation: kefiri; L. lactis; Lc. mesenteroides; and Pseudomonas Increase of
- backslopping 72 h at 25°C S. cerevisiae after fermentation isoamylalcohol
inoculation 0.25% (w/v) and
- Fermentation 48 h at 25° phenylethylalcohol
C inoculation 4% (v/v)
[113]
Fruit juice Heat treatment: boiling for Lb. fermentum ATCC 9338 From 6.30 to ND* Decrease of vitamin C and Formation of
15–20 min 4.1 DPPH activity alkenes, organic
Fermentation: 48 h at Maintain of total phenolic acids, hydroxyl
28 ± 2°C content groups and nitro
Metabolization or groups
disintegration of risky organic Sensory properties
compounds overall
FOOD REVIEWS INTERNATIONAL
appreciated
[114]
Green Fruit juice Pasteurization 64°C for Autochthonous strains of Lb. From 5.4 to ND Antimicrobial activity against ND
30 min plantarum and F. fructosus 2.5–5.2 Bacillus sp.
Fermentation: 48 h at 37°C No effect on phenolic content
13
followed by 30 days at 4°C Maintain or increase of

antioxidant activity
*ND: not described
fermentation. The lactic acid content increased from 0.01 ± 0.1 mg/100 mL to
0.32 ± 0.01 mg/100 mL, whereas the reducing sugar content decrease from 1.35 ± 0.6 g/
100 mL to 0.20 ± 0.03 g/100 mL. The juice was thus an adequate medium for the growth
of the Lactobacillus strain. However, a significant decrease in the vitamin C content was
also observed during lacto-fermentation. No significant change in the phenolic content
was observed but the radical scavenging activity was reduced during fermentation. Fourier
transform infrared (FT-IR) analysis showed that new compounds containing organic,
aromatic carboxylic, hydroxyl, alkyle and nitro groups were produced during the fermen-
tation, but no furfuryl alcohol, furan or catechol present in the fresh juice were found in
the fermented juice. Sensory evaluation revealed that the juice obtained after lactic acid
fermentation was highly appreciated by a panel of 30 members.
Another recent study investigated the probiotic effect of lactic acid fermentation on
green cactus fruit.[114] Following isolation of 17 lactic acid bacteria, autochthonous starters
were used to ferment the juice at 37°C for 48 h followed by 30 days of storage at 4°C. All
isolates were able to grow in the cactus juice and almost all isolates were able to reduce the
pH from 5.4 to below 4.5. After 30 days of storage, eight isolates survived at pH lower than
4.4, suggesting their natural adaptation to the fruit matrix. Only five fermented juices
showed antibacterial activity against the contaminant Bacillus spp. As the experiment was
conducted with a green-color cultivar, betalain content was relatively low and did not
change during fermentation. The phenolic content did not significantly vary during the
fermentation and the storage. Moreover, for some isolates, an increase in the antioxidant
activity was observed during the fermentation and the storage, compared to the control
juice. Examination of probiotic properties assessed from resistance to gastric juice and bile
salts, cell surface hydrophobicity and auto-aggregation resulted in the selection of four
autochthonous Lactobacillus plantarum and Fructobacillus fructosus.
More recently, Lb. plantarum S-811 has been used to ferment cactus pear fruit juice in
a functional beverage with health-promoting properties.[115] The initial pH of the fruit
juice was 5.5 and dropped to 3.7 after lactic acid fermentation. Results showed a protective
effect of the fermented juice towards an H2O2-induced oxidative stress. Moreover,
a decrease in the body weight and an amelioration of obesity disorders (insulin resistance,
hyperglycemia) were observed on obese rats fed with the lactic fermented pear fruit juice.
So, lactic acid fermentation of cactus pear fruit juice is an interesting way to produce
functional beverage for the prevention of oxidative-induced diseases, such as diabetes,
obesity or cardiovascular diseases.
Lactic acid fermentation of cladodes

Pickled cladodes, called nopalitos, are commonly found in Mexico.[6] To obtain them, the
tender stems are first blanched to inactivate heat-sensitive microorganisms and degrada-
tive enzymes, then immersed in cold water, chopped, acidified with vinegar and flavored
with spices. In most cases, a pasteurization step achieves the stabilization processing.
Alternatively, young cladodes can be preserved in a brine containing up to 2% sodium
chloride. No fermentation of these products is described in spite of frequent lactic acid
fermentation occurring in pickled vegetables.[116–118]
Cladode pulp, which exhibited initial pH values of 4.3 ± 0.18, was fermented with
allochthonous starters of Lb. plantarum, Lb. brevis, Lb. fermentum, Lactobacillus rossiae,
Lactobacillus curvatus, Pediococcus pentosaceus, Lc. mesenteroides and Weissella cibaria/

confusa.[110] During fermentation at 30°C for 24 h, the cladode pulp pH dropped to 3.98
with Lb. plantarum strains. High growth during fermentation was observed for Lb.
plantarum, Lb. rossiae, Lb. brevis and P. pentosaceus, up to 8 to 9.24 log CFU/mL.
Moreover, total free amino acid content increased during cladode fermentation with
some strains and lactic acid fermentation had a preserving effect on vitamin C and
carotenoid contents of the cactus cladode. In addition, lactic acid fermentation signifi-
cantly increased the radical scavenging activity of the cladode pulp. Interestingly, flavo-
noids derivatives, such as kaempferol and isorhamnetin, appeared during cladode pulp
fermentation, obtaining the highest concentrations for cladode pulp fermented with Lb.
plantarum and Lb. brevis. The release of flavonoid derivatives was responsible for the
antioxidant and anti-inflammatory activity increase. Metabolization of food phenolics is of
great interest, as it might result in a better bioavailability and bioaccessibility of these
compounds. Metabolization of phenolic compounds during lactic acid fermentation of
cherry juice and broccoli puree has previously been reported with Lactobacillus
strains.[119] However, the effect of fermentation of prickly pear or cladode pulp on
bioavailability, bioaccessibility or gut microbiota remains unexplored.
Fermented cladode pulp reduced the inflammatory status of the Caco-2/TC7 cells
induced by TNFα, IL-1β and IFN-ϒ cytokines.[110] The highest anti-inflammatory activity
was observed with cladode pulp fermented with Lb. plantarum and Lb. brevis strains. All
fermented cladode pulp attenuated the negative effect on the integrity of Caco-2/TC7 cells
junctions (TEER method) induced by IL-1β. Fermented cladode pulp also inhibited the
synthesis of IL-8 and TNFα after treatment with IFN-ϒ.
Conclusion
Cactus fruit and cladodes exhibit a high potential for food and nutritional security in arid
and semi-arid regions. Many different processes can be applied for food diversification
from cactus fruit or cladodes. Among those, lactic acid fermentation clearly enhances
safety, shelf-life and functional properties of fruit and vegetables. Both cactus fruit and
cladode pulp appeared to be suitable for the growth of lactic acid bacteria, and fermenta-
tive and probiotic strains are described. Lactic acid fermentation with autochthonous and
allochthonous starters have shown a better preservation of bioactive compounds com-
pared to fermentations with commercial starters.
Declaration of interest statement

The authors declare no conflict of interest.
Funding
Part of this work was funded by European Union project RE0017203. This work has been developed
in the framework of and supported by COST Action CA15136 EUROCAROTEN. Francisco J. Barba
and Fabienne Remize are WG members of this action. Moreover, Fabienne Remize would like to
thank COST Action CA15136 for her STSM fellowship.
ORCID
Francisco J. Barba http://orcid.org/0000-0002-5630-3989
Cyrielle Garcia http://orcid.org/0000-0001-6705-6859
Jose M. Lorenzo http://orcid.org/0000-0002-7725-9294
Fabienne Remize http://orcid.org/0000-0002-6860-2089
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Food Reviews International

ISSN: 8755-9129 (Print) 1525-6103 (Online) Journal homepage: https://www.tandfonline.com/loi/lfri20

Opuntia Ficus Indica Edible Parts: A Food and

Francisco J. Barba, Cyrielle Garcia, Amandine Fessard, Paulo E.S. Munekata,

To link to this article: https://doi.org/10.1080/87559129.2020.1756844

Published online: 15 May 2020.

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Opuntia Ficus Indica Edible Parts: A Food and Nutritional

CONTACT Fabienne Remize [email protected] QualiSud, ESIROI Université De La Réunion, 2 Rue

Characteristics of the plant

Fruit and cladode characteristics

Figure 2. Structure of the main prickly pear ﬂavonols and carotenoids.

Figure 3. General structure of betalains. (a) betaxanthins and (b) betacyanins.

Processing and uses of cladodes

Processing into ﬂours and food fortiﬁcation

Extracts used for antimicrobial or coloring properties

Processing of prickly pear

obtained by packaging prickly pear fruit in a polystyrene tray under vacuum-applied

Jam, dehydrated and extruded products

Juices and derived products

Lactic acid fermentation of prickly pear

LS isolated from soymilk curd residue, Lactobacillus bulgaricus KCTC3188 and

followed by 30 days at 4°C Maintain or increase of

Lactic acid fermentation of cladodes

Lactobacillus curvatus, Pediococcus pentosaceus, Lc. mesenteroides and Weissella cibaria/

Declaration of interest statement

[47] Osorio-Esquivel, O.; Alicia-Ortiz-Moreno,; Álvarez, V. B.; Dorantes-Álvarez, L.; Giusti, M. M.

Generates Flavonoid Derivatives with Antioxidant and Anti-Inﬂammatory Properties. PLoS

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