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Opuntia ficus-indica (L.) Mill. (prickly pear) is a plant that grows wild in the arid and semi-arid regions of the world, being a food source for ones and a potential for others, but not properly valued.
1. Introduction
Nowadays, health professionals, as well as consumers, are increasingly aware of food and its potential health benefits. There is a growing interest in the nutritional composition and bioactive compounds of foodstuffs as well as the benefits for disease prevention. On the other hand, the reduction of wastes discarded by the food industry has also become one of the main objectives of the European Commission. Thus, the European Commission has supported several actions against food waste [1]. One of the appointed solutions involves the use of byproducts in the formulation of new products, and their study in terms of nutritional composition and bioactive compounds becomes extremely important.
Green chemistry is a quite novel concept that aims to reduce hazards across all the life-cycle stages, to reduce environmental impact. Moreover, it should be an economically profitable approach. According to green chemistry’s twelve principles, it is better to prevent waste generation than to treat or clean it up. However, in the food industry, it is quite inevitable to prevent byproducts generation, which most of the time is treated as waste. Therefore, it is particularly important to valorize this waste by means of green technologies (more innocuous solvents and auxiliaries), which allow to the extraction of bioactive compounds that can be further used, for example, to develop functional foods and/or to obtain added value extracts [2].
Opuntia ficus-indica (L.) Mill., also known as prickly pear, is a plant originating from Mexico and belonging to the Cactaceae family. This plant can also be found in all American hemispheres and grows worldwide, such as Africa, Australia and the Mediterranean basin [3][4]. O. ficus-indica is gaining interest across the world because it can grow where no other crops are able to do that. This the case of some countries, such as Ethiopia, where it is the only crop that can be relied on [5]. In addition to its use in the diet, prickly pear is also used for healthcare due to its high content of polyphenols and antioxidant, anti-inflammatory and anxiolytic properties [6][7][8][9]. O. ficus-indica is a multipurpose crop, not only to provide food and feed but as a source of bioactive compounds with promoting health properties.
2. Bioactive Compounds
Cactus plants are also important sources of bioactive substances and excellent candidates for nutraceutical and functional food preparation. Several authors confirm that prickly pear has a high bioactive potential, being an important source of bioactive compounds and an excellent source of dietary antioxidants, which may have beneficial effects on consumers’ health [10].
2.1. Fatty Acids
The fatty acids composition of prickly pear pulp, seed oil and peel are shown in Table 1. The major fatty acids present in prickly pear peels are palmitic acid (C16:0) and linoleic acid (C18:2), according to data reported by Ramadan and Mörsel [11], El-Said et al. [12] and Andreu-Coll et al. [13]. In relation to cladodes, palmitic acid (C16:0), oleic acid (C18:1), linoleic (C18:2) acid and linolenic acid (C18:3) are the major fatty acids [13][14]. The prickly pear seeds oil owns the potential of high-quality edible oil with potential health benefits. The major fatty acids of the seed oil were linoleic (C18:2), oleic (C18:1), palmitic (C16:0), and stearic (C18:0) acids [15][16][11][17][18][19][20]. This shows the interest in the prickly pear as a natural source of edible oil containing essential fatty acids [15][21][22].
Table 1. Fatty acids content of the different parts of Opuntia ficus-indica (L.) Mill.
| Fatty Acids | Parts of O. ficus-indica | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Pulp Oil | Pulp | Seed Oil | Peel | Cladode | |||||||||
| Lauric | 1.55 b | 0.71 ± 0.15 d | 0.08 b | 1.33 e | 0.91 b | ||||||||
| Myristic | 1.13 ± 0.09 a | 1.52 b | 0.13 ± 0.02 c | 1.95 ± 0.25 d | 0.30 b | 1.96 e | 1.88 b | ||||||
| Palmitic | 34.4 ± 3.12 a | 22.9 b | 20.1 ± 2.26 a | 9.32 ± 0.19 b | 11.66 ± 0.48 c | 12.2 ± 1.70 c | 13.2 ± 0.33 c | 23.1 ± 1.98 d | 23.7 c | 27.0 b | 13.9 e | 39.0 b | 19.1 b |
| Stearic | 2.37 ± 0.10 a | 5.20 b | 2.72 ± 0.13 a | 3.11 ± 0.04 b | 3.93 ± 0.49 c | 0.15 ± 0.03 c | 3.65 ± 0.39 c | 2.67 ± 0.21 d | 3.93 c | 2.23 b | 3.33 e | 5.57 b | 4.82 b |
| Arachidonic | 0.95 ± 0.07 c | 5.52 c | |||||||||||
| Palmitoleic | 1.62 ± 0.06 a | 1.80 ± 0.11 a | 1.42 ± 0.01 b | 2.48 ± 0.22 d | 2.46 c | 0.36 b | 0.24 e | 2.00 b | 0.06 b | ||||
| Oleic | 10.8 ± 0.98 a | 26.8 b | 18.3 ± 1.58 a | 16.8 ± 0.47 b | 16.56 ± 2.35 c | 25.5 ± 1.10 c | 19.2 ± 4.22 c | 21.1 ± 2.15 d | 19.7 c | 14.4 b | 11.1 e | 18.0 b | 19.3 b |
| Linoleic | 37.0 ± 3.87 a | 29.2 b | 53.5 ± 4.89 a | 70.3 ± 0.60 b | 59.12 ± 2.74 c | 61.0 ± 1.30 c | 32.3 ± 2.14 d | 29.0 c | 41.2 b | 34.9 e | 20.4 b | 35.6 b | |
| Linolenic | 12.0 ± 1.05 a | 12.2 b | 2.58 ± 0.16 a | 0.69 ± 0.06 d | 15.7 c | 13.9 b | 32.8 e | 10.9 b | 13.9 b | ||||
| γ-Linolenic | 61.4 ± 1.90 c | 8.60 ± 1.04 d | 0.40 e | ||||||||||
| Behenic | 0.50 ± 0.05 d | ||||||||||||
| Lignoceric | 0.41 ± 0.04 d | ||||||||||||
| cis-13,16-Docosadienoic | 0.93 ± 0.08 d | ||||||||||||
| Cerotic | 0.35 ± 0.04 d | ||||||||||||
| Nervonic | 1.21 ± 0.26 d | ||||||||||||
| Reference | [23] | [13] | [23] | [19] | [20] | [15] | [17] | [11] | [12] | [13] | [14] | [13] | [13] |
Values are expressed as means ± standard deviation or as a mean. a expressed as g/100 g of oil. b expressed as g/100 g of total fatty acid. c expressed as g/100 g. d expressed as g/100 g of total fat. e expressed as g/100 g of fatty acid methyl esters.
In Table 2, the profile of saturated, monounsaturated, and polyunsaturated fatty acids determined in oils extracted from other fruit seeds are presented. If we compare the fatty acid profile of the oil of the prickly pear seeds with the one from oils of other fruit seeds, it is possible to verify that the oil of prickly pear seeds has a fatty acid profile similar to watermelon seeds and grape seeds, with the exception of the saturated fatty acids content, which is superior in the prickly pear. The oil of the seeds of the prickly pear also has a linoleic acid content similar to the content present in blackcurrant and pumpkin seeds oil [24]. The high content of polyunsaturated fatty acids in the oil of prickly pear seeds makes this oil potentially beneficial for health because these fatty acids play a preventive role in cardiovascular diseases. This type of fatty acids is described as having activities to reduce total cholesterol and low-density lipoproteins cholesterol [17].
Table 2. Fatty acid profile (g/100 g) of seeds oils [24].
| Oil | Mango Seed | Apricot Kernel | Paprika Seed | Blackcurrant Seed | Watermelon Seed | Pumpkin Seed | Cranberry Seed | Grape Seed | Prickly Pear |
|---|---|---|---|---|---|---|---|---|---|
| Total SFA | 52.8 | 4.8 | 17.6 | 8.3 | 21.7 | 22 | 9.7 | 6.7 | 30.4 |
| Total MUFA | 41.3 | 66.4 | 14.7 | 16.3 | 18.4 | 26.1 | 22.7 | 18.4 | 16.3 |
| Total PUFA | 7.4 | 28.8 | 67.8 | 75.3 | 60 | 51.5 | 67.6 | 65.4 | 52.9 |
| Linoleic acid | 6.9 | 28.6 | 67.8 | 61.5 | 59.6 | 51.3 | 45.3 | 64.9 | 45.6 |
| Linolenic acid | 0.5 | 0.1 | 13.8 | 0.4 | 0.2 | 22.3 | 0.6 | 7.3 |
SFA, saturated fatty acids; MUFA, monounsaturated fatty acids; PUFA, polyunsaturated fatty acids.
2.2. Amino Acids
The main amino acids (Table 3) present in the prickly pear pulp are serine and proline, and gamma-aminobutyric acid [25][26]. Regarding the amino acids found in prickly pear seeds, the main are arginine (14.62 g/100 g protein) and glutamic acid (20.27 g/100 g protein) [27]. Stintzing et al. [26] evaluated the amino acid content present in pulps of three different cultivars of prickly pear and reported that proline, taurine, and glutamine were present in major quantities. From the results reported, it was also possible to verify that the cultivar Apastillada presented the highest level of proline (1768.7 mg/L) and taurine (572.1 mg/L), while the cultivar Gymno Carpo had the highest glutamine content (574.6 mg/L) [26]. Taurine, semi-essential amino acid, has been considered a cellular protective amino acid. It has been involved in the modulation of the inflammatory response and has demonstrated antioxidant effects [28][29][30].
Table 3. Amino acid content of the different parts of Opuntia ficus-indica (L.) Mill.
| Amino Acids | Parts of O. ficus-indica | ||||
|---|---|---|---|---|---|
| Pulp | Seed Meal | Cladode | |||
| Taurine | ND | 9.36 ± 2.04 | 323.60 ± 572.10 | ||
| Aspartate | 844.24 ± 256.48 | 8.60 | 0.61 ± 0.06 | ||
| Threonine | 120.71 ± 48.48 | 13.10 ± 1.80 | 3.96 | 1.38 ± 0.15 | |
| Serine | 967.94 ± 453.75 | 175.50 ± 43.46 | 4.14 | 0.48 ± 0.11 | |
| Asparagine | 253.21 ± 102.22 | 41.60 ± 5.67 | |||
| Glutamate | 154.25 ± 114.51 | 66.10 ± 21.06 | 20.27 | 1.78 ± 0.32 | |
| Glutamine | 1583.19 ± 922.78 | 346.17 ± 205.84 | |||
| Proline | 6461.79 ± 2476.41 | 1265.20 ± 455.02 | 5.66 | 0.45 ± 0.12 | |
| Glycine | 174.78 ± 98.60 | 11.33 ± 4.23 | 7.67 | 0.36 ± 0.07 | |
| Alanine | 353.86 ± 156.29 | 87.23 ± 8.16 | 4.58 | 0.46 ± 0.05 | |
| Citrulline | 79.14 ± 71.47 | 16.27 ± 11.54 | |||
| Valine | 254.38 ± 107.03 | 39.37 ± 9.28 | 5.69 | 0.58 ± 0.09 | |
| Cysteine | 10.63 ± 8.17 | 3.10 | |||
| Methionine | 189.69 ± 83.08 | 55.23 ± 22.22 | 2.61 | 0.15 ± 0.03 | |
| Isoleucine | 241.39 ± 128.77 | 31.17 ± 8.63 | 3.66 | 0.67 ± 0.05 | |
| Leucine | 218.72 ± 97.02 | 20.60 ± 0.99 | 6.90 | 0.76 ± 0.12 | |
| Tyrosine | 208.35 ± 124.69 | 12.30 ± 2.43 | 3.56 | 0.21 ± 0.09 | |
| Phenylalanine | 337.75 ± 145.43 | 23.33 ± 1.16 | 4.46 | 1.37 ± 0.28 | |
| β-Alanine | 42.25 ± 21.12 | ||||
| γ-Aminobutyric acid | 2272.69 ± 1181.82 | ||||
| Histidine | 505.48 ± 203.07 | 45.20 ± 11.29 | 2.46 | 0.15 ± 0.03 | |
| Tryptophan | 117.36 ± 46.55 | 12.63 ± 4.33 | 0.90 | 0.16 ± 0.02 | |
| Ornithine | 8.37 ± 4.66 | ||||
| Lysine | 205.46 ± 103.14 | 17.40 ± 1.27 | 3.39 | 0.53 ± 0.08 | |
| 2-Aminoethanolamine | 117.31 ± 42.09 | ||||
| Arginine | 375.87 ± 272.37 | 30.50 ± 8.29 | 14.62 | 0.16 ± 0.02 | |
| Carnosine | 5.90 ± 1.71 | ||||
| Reference | [25] | [31] | [26] | [27] | [32] |
| Units | µmol/L | mg/100 g | mg/L | g amino acid/100 g protein | g/100 g protein |
ND—not detected. Values are expressed as means ± standard deviation or as a mean.
2.3. Sterols
Sterols are essential constituents of cell membranes in animals and plants. Some plant sterols are currently incorporated into foods intended to lower blood cholesterol levels [33]. According to the results reported by Ramadan and Mörsel [23][34], who studied the composition of prickly pear pulp and seeds oils, it was shown that for both oils, the main sterol present was β-sitosterol with 1.12 ± 0.121 and 0.675 ± 0.089 g/100 g, respectively. Campesterol is the second sterol present in larger amounts in both oils (0.874 ± 0.075 g/100 g for pulp oil and 0.166 ± 0.021 g/100 g for seeds oil). β-sitosterol and campesterol are also the sterols present in greater amounts in the prickly pear peel oil with 2.11 ± 0.255 and 0.876 ± 0.231 g/100 g, respectively [11]. Δ7-Avenasterol was only detected in small amounts in seed oil [23], whereas ergosterol was only found in the prickly pear peel [11].
2.4. Carotenoids
Carotenoids are important compounds with great benefits for human health, are related to the prevention and reduction of the development of some diseases, such as cardiovascular diseases, cancer and macular degeneration [35].
In cladodes, three carotenoids were quantified: lutein (102 ± 0.07 to 187 ± 0.22 μg/100 g dry weight basis), β-carotene (82 ± 0.22 to 119 ± 0.53 μg/100 g dry weight basis) and β-cryptoxanthin (45 ± 0.60 to 72 ± 0.28 μg/100 g dry weight basis), according to data reported by Jaramillo-Flores et al. [36]. According to Cano et al. [37], the peel had a higher content of total carotenoids than pulp. Moreover, the same authors identified that the main carotenoids in the prickly pear peel of Verdal (orange) variety and Sanguinos (red) variety, respectively, are lutein (767.98 ± 2.20 and 1132.51 ± 1.97 μg/100 g), β-carotene (172.50 ± 2.30 and 200.4 ± 2.83 μg/100 g) and violaxanthin (87.67 ± 2.01 and 92.64 ± 1.87 μg/100 g). Lycopene was found in the peel with a concentration of 45.61 ± 2.68 μg/100 g, whereas in the pulp, only traces were reported. In prickly pear pulp of the varieties described above, the main carotenoids found were lutein (202.90 ± 1.39 and 201.45 ± 2.31 μg/100 g), β-carotene (79.10 ± 2.65 and 37.47 ± 1.67 μg/100 g), violaxanthin (31.95 ± 2.76 and 5.76 ± 0.91 μg/100 g) and zeaxanthin (12.27 ± 1.09 and 14.32 ± 0.83 μg/100 g) [37].
2.5. Phenolics
The phenolic group is constituted by many compounds, in particular phenolic acids (hydroxycinnamic acids and hydroxybenzoic acids), flavonoids, lignins and stilbenes. Their antioxidant potential is involved in many health benefits such as prevention of inflammation, cardiovascular dysregulation, and neurodegenerative diseases [8][38]. For example, Abdel-Hameed et al. [39] analyzed the presence of phenolic compounds and identified gallic acid, catechin, quercetin-3-glucose-(1-6)-gallic acid in two cultivars (red and yellow) of prickly pear pulp and peel. The same authors reported that the juices of peels and pulp of the red cultivar had a higher content of total phenolics (1065.15 ± 10.21 and 1152.97 ± 8.49 mg of gallic acid equivalents/100 mL of juice, respectively) than the yellow cultivar. Cano et al. [37] compared the prickly pear pulp with the peel and found a higher content of phenolic compounds present in the peel (630.30 ± 45.14 and 698.37 ± 29.26 mg of gallic acid equivalents/100 g) of Verdal (orange) and Sanguinos (red) varieties, respectively. Guevara-Figueroa et al. [40] detected the presence of gallic acid (6.4 to 22.7 μg/g dry weight basis), coumaric acid (140.8 to 161.8 μg/g dry weight basis), 3,4-dihydroxy-benzoic acid (0.6 to 25.1 μg/g dry weight basis), 4-hydroxybenzoic acid (5.0 to 47.2 μg/g dry weight basis), ferulic acid (5.6 to 347.7 μg/g dry weight basis) and salicylic acid (5.8 to 35.4 μg/g dry weight basis) in the prickly pear cladodes. Chougui et al. [17] analyzed prickly pear seeds of different cultivars and obtained content of total phenolics of 48 ± 1 to 89 ± 5 mg gallic acid equivalents/100 g [17].
Flavonoids are a group of bioactive compounds that exhibit many effects in the protection of the body, and their regular consumption is associated with reduced risk of several chronic diseases. In addition, they have antioxidant, antiviral and antibacterial properties [41]. Kuti [34] identified kaempferol (2.2 ± 0.3 μg/g), quercetin (42.2 ± 2.5 μg/g) and isorhamnetin (24.1 ± 1.0 μg/g) in prickly pear pulp. Guevara-Figueroa et al. [40] identified iso-quercitrin (22.9 to 396.7 μg/g dry weight basis), isorhamnetin-3-O-glucoside (45.9 to 322.1 μg/g dry weight basis), nicotiflorin (28.9 to 1465.0 μg/g dry weight basis), rutin (22.6 to 261.7 μg/g dry weight basis) and narcissin (146.9 to 1371.0 μg/g dry weight basis) in cladodes of different Opuntia spp. varieties. The prickly pear seeds have contents between 1.5 ± 0.1 and 2.6 ± 0.2 mg quercetin equivalents/100 g, according to the data reported by Abdel-Hameed et al. [39].
2.6. Betalains
Betalains are vacuolar pigments composed of a nitrogenous core structure, betalamic acid. Betalains include two classes of compounds: betacyanins (red–violet) and betaxanthins (yellow), and their concentrations vary according to the color of the fruit. They are powerful radical eliminators in chemical systems and act as efficient antioxidants in biological models [37][42][43]. In addition to the phenolic compounds, betalains are particularly important components of the prickly pear [44]. According to the results obtained by Cano et al. [37], prickly pear peel presents higher values of betaxanthins (1.73 ± 0.04 and 2.00 ± 0.15 mg indicaxanthin/100 g) and betacyanins (1.17 ± 0.04 and 2.52 ± 0.10 mg betanin/100 g) for Verdal (orange) and Sanguinos (red) varieties, respectively, than prickly pear pulp.
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