A Comprehensive Assessment of Carob, C. siliqua L.: Comparison
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The carob tree (C. siliqua L.) is an evergreen perennial tree from the Fabaceae (Leguminosae) family. Originating in the Mediterranean region, it now populates many parts of the world, including North and South America, Africa, and Australia. The tree grows up to 15 m tall and boasts long, dark green leathery leaves.

  • carob
  • Ceratonia siliqua
  • phytochemistry
  • pharmacology
  • toxicity

1. Introduction

The carob tree (C. siliqua L.) is an evergreen perennial tree from the Fabaceae (Leguminosae) family. Originating in the Mediterranean region, it now populates many parts of the world, including North and South America, Africa, and Australia. The tree grows up to 15 m tall and boasts long, dark green leathery leaves [1,2][1][2]. Until 1980, the Ceratonia genus contained only one species, C. siliqua. However, another species, C. oreothauma, has since been discovered in East Africa and the Arabian Peninsula [3].
This plant has been utilized by humans since the ancient times. It is valued for its economic and culinary importance. Its seeds, also known as carob, are used as a food source for both humans and livestock [4,5][4][5]. High in carbohydrates and protein, they can be ground into a powder and used as a chocolate substitute [6]. The leaves, bark, and seeds have traditionally been used in medicine to treat various diseases, including diarrhea, diabetes, and hypertension [7,8][7][8]. In addition to its culinary uses, carob is believed to have several pharmacological activities, including antioxidant, antidiarrheal, antibacterial, antiulcer, and anti-inflammatory effects [9,10][9][10]. Rtibi et al., 2015, suggest using carob as a natural antioxidant in the form of a food supplement for the prevention of damage caused by oxidative stress [9]. In Morocco, the carob tree is particularly abundant in certain regions (Marrakech, El Ksiba, Khenifra, Beni Mellal, Meknes, Essaouira, Elhaouz, Kasba Tadla…); it provides farmers in these areas with a way to add value to land unsuitable for other crops. These regions could become the centers of carob production in Morocco. Nothing appears to hinder the success of the carob tree in these areas, with some specimens growing with minimal care and yielding interesting outputs [11].

2. Phytochemistry of C. siliqua L.

Phytochemical compounds in carob vary greatly, influenced by factors including environment, maturation stage, and tree parts [80][12]. In a study conducted by Fadel et al., 2011 [81][13], the phenolic compounds present in the aqueous acetone extracts of carob pulps and seeds were analyzed. These carob samples were harvested from two areas, Izouika and Reggada, in southwest Morocco. The High-Performance Liquid Chromatography (HPLC) analysis of the extracts showed their richness in phenolic compounds. In both areas, the pulp extracts were richer in phenolic compounds than the seeds, both qualitatively and quantitatively. The phenolic profile of the pulp was dominated by coumaric acid (20.52% in Izouika vs. 17.05% in Reggada) and gallic acid (17.8% in Izouika vs. 12.57% in Reggada). In seed extracts, coumaric acid and gallic acid were also the predominant phenolic acids, with coumaric acid representing 8.07% in Izouika and 8.18% in Reggada, while gallic acid represented 5.01% in Izouika and 3.95% in Reggada. Syringic acid, 4-hydroxybenzoic acid, and gentisic acid are all benzoic acids present in carob [82][14]. HPLC methods have been used to determine polyphenols in carob pods, revealing the presence of condensed tannins (proanthocyanidins), composed of flavan-3-ol groups and their galloyl esters, gallic acid, catechin, epicatechingallate (ECG), epigallocatechingallate (EGCG), and quercetin glycosides [83,84][15][16]. The presence of hydrolysable tannins (gallotanins and ellagitannins) has also been detected in carob pods [85][17]. Carob fiber was found to contain a rich variety of phenolic compounds, with a total of 24 polyphenol compounds identified, yielding 3.94 g/kg (dry weight). The profile was dominated by gallic acid in various forms: free gallic acid (42% of polyphenols by weight), gallotannins (29%), and methyl gallate (1%). Simple phenols, mainly cinnamic acid, comprised about 2% of the total, and major flavonoids were identified as the glycosides myricetin and quercetin-3-O-α-L-rhamnoside [80][12]. In another study, HPLC analysis showed the main compounds in mature carob pods to be pyrogallol (48.02 ± 3.55%), catechin (19.10 ± 2.11%), and tannic acid (9.01 ± 1.40%) [9]. In immature carob pods, pyrogallol (26.45 ± 3.03%), catechin (16.52 ± 2.34%), gallic acid (15.12 ± 2.31%), chlorogenic acid (15.01 ± 1.72%), and epicatechin (12.26 ± 1.04%) were detected [10]. The HPLC technique also identified several phenolic compounds in leaves such as kaempferol (77 ± 2.43%), tannic acid (13 ± 0.45%), catechin hydrate (4.30 ± 0.34%), and polydatin (0.85 ± 0.22%) [86][18]. Phytochemical screening of the crude ethyl acetate and methanolic extracts of three types of carob tree barks (spontaneous male, spontaneous female, and grafted female) indicated the presence of flavonoids and tannins. Alkaloids and saponins were not detected. The total phenolic contents from the ethyl acetate and methanolic extracts of the three varieties of C. siliqua L. barks varied from 0.46 to 0.76 (g/L gallic acid equivalents). In this study, the methanolic extract had a higher phenolic content than the ethyl acetate extract. These phenolic compounds and other reported bioactive compounds are generally more soluble in polar solvents [87][19]. Carobs are particularly rich in flavonols such as quercetin, myricetin, kaempferol, and their glycosidic derivatives. Quercetin and myricetin rhamnosides are usually the most abundant flavonoids in carob. The presence of flavones (apigenin, luteolin, and chrysoidium), flavanones (naringenin), or isoflavones (genistein) is low [80,83,88][12][15][20]. According to a semi-quantitative ultra-performance liquid chromatography (UPLC) analysis carried out on the leaves of C. siliqua from the southern region of Morocco (Tafraoute), it was found that the major compounds in the aqueous extract of C. siliqua were luteolin-7-glucoside followed by epicatechin, apigenin-7-glucoside, quercetin-3-O-glucoside, caffeic acid, gallic acid, and chlorogenic acid. This indicates that C. siliqua leaves represent a good source of natural bioactive compounds. No aglycons were identified in the sample [89][21] (Figure 21).
Plants 12 03303 g002
Figure 21.
Chemical compounds present in
C. siliqua
L. (drawn with ChemDraw 15.0).
Indeed, carob pulp is a substantial source of dietary fiber and sugars, along with a variety of bioactive compounds including polyphenols, as previously mentioned. Dietary fiber is composed of various substances and is typically categorized as soluble or insoluble. Both types of fibers have important health benefits. In the context of carob:
-
Total dietary fiber in carob pulp ranges from 30 to 40% [90][22].
-
This fiber is primarily made up of lignin (50–65%), cellulose (15–25%), and hemicellulose (15–25%), with smaller amounts of pectin (0.5–2%), tannins (3–7%), and moisture (4–8%) [91][23].
-
Carob fiber is primarily insoluble and is not easily fermented by gut bacteria [92][24].
-
The soluble fiber content, which can be fermented in the colon, is significantly lower in carob and this portion contains simple carbohydrates [82][14].
The total sugar content in carob pulp typically ranges from 30 to 60%. Sucrose forms the largest portion of these sugars, contributing 65–75% of the total sugar content. The remainder of the sugar content is mostly made up of the monosaccharides fructose and glucose, contributing 15% and 25% of the total sugars, respectively [93][25]. Carob pods are especially notable for their high sugar content, which is even higher than that of beets or sugar cane (about 200 g/kg) [94][26]. Carob seeds, on the other hand, primarily contain the sugars sucrose (8.1 ± 0.04%) and glucose (2.2 ± 0.01%). They also contain various monosaccharides following polysaccharide hydrolysis, namely mannose (54.0 ± 0.50%), galactose (15.5 ± 0.14%), glucose (2.2 ± 0.01%), arabinose (1.0 ± 0.00%), and xylose (0.4 ± 0.00%). Fructose was not detected [95][27]. Carob is a good source of protein, and its protein content is particularly rich in both essential and non-essential amino acids. The protein fraction in carob seeds, for instance, has a substantial amount of the non-essential amino acids like arginine (27.8 ± 0.25 g/100 g) and alanine (17.0 ± 0.16 g/100 g) and the essential amino acid lysine (15.0 ± 0.14 g/100 g). Moderate amounts of essential amino acids like isoleucine (8.6 ± 0.08 g/100 g) and valine (7.3 ± 0.06 g/100 g) are also present in carob seeds [95][27]. In terms of the overall amino acid content in carobs, it is composed of a mixture of 17 residues including aspartic acid, glutamic acid, serine, glycine, histidine, arginine, threonine, alanine, tyrosine, valine, proline, methionine, isoleucine, leucine, cysteine, phenylalanine, and lysine [96,97][28][29]. In particular, aspartic acid, asparagine, alanine, glutamic acid, leucine, and valine make up approximately 57% of the total amino acid content of the pods [98][30]. Ground carob flour contains about 4.45% protein, with carob germ flour proteins including albumin and globulin (32%) and glutelin (68%) [96][28]. Importantly, no prolamins are detected in carob germ flour proteins [99][31], which contributes to the gluten-free property of carob [100][32]. Carob seeds are characterized by high protein content (25.7 ± 0.18%). Even in naturally grown carob seeds, like those from the Tazmalt region in northern Algeria, a moderate protein content was reported (18.6 ± 0.3%) [101][33]. Carob leaves also have a balanced nutrient composition. A proximate analysis based on dry weight showed the presence of carbohydrates (16.62%), fat (4.60%), protein (22.25%), ash (4.255%), and dietary fibers (11.77%) [102][34]. According to research by Özcan et al., 2007 [103][35], the protein, oil, crude fiber, ash, and energy values of carob fruit and carob flour were found to be not statistically different. However, carob syrup showed lower values for protein, crude fiber, ash, and energy compared to both carob fruit and carob flour. Interestingly, carob syrup had the highest total sugar content, with 48.3% in the fruit and 41% in the flour. Carob pods from the eastern parts of Sicily in Italy, as reported by Avallone et al., 2002 [85][17], had the following composition (dry weight): moisture (6–10%), ash (1–6%), protein (1–5%), fat (0.4–0.8%), sucrose (27–40%), D-glucose (3–5%), D-fructose (3–8%), and starch (0.1–1.3%). The carob germ which consists of fine fragments of hull and endosperm, and could be obtained industrially, has the following composition: 8.3% moisture, 6.5% ash, 6.6% lipids (neutral and polar) which contain approximately 21% polar lipids, 54.7% crude proteins, and an energy value of 17.5 kJ/g [104][36]. Moreover, the average proximate composition of raw carob pods is as follows: 8.17–9.56% moisture, 89.57–91.12% carbohydrates, 40.69–54.74% total sugars (33.70–45.09% sucrose, 1.79–4.95% glucose, and 1.80–5.19% fructose), 29.88–36.07% dietary fiber, 3.07–4.42% protein, 2.58–3.08% polyphenols, 0.45–0.86% fat, and 2.13–2.69% ash [17][37]. The mineral content of carob varies depending on the part of the tree analyzed (leaves, bark, integument, pulp) and the specific variety of the carob tree (C. siliqua L.), such as spontaneous female, spontaneous male, and grafted female. In a study conducted in Chefchaouen, northern Morocco, it was found that calcium (Ca) generally appears to be the most prevalent mineral in the leaves and bark of the carob tree, regardless of the category studied. Other detected elements in significant amounts include potassium (K), magnesium (Mg), sodium (Na), phosphorus (P), chlorine (Cl), copper (Cu), iron (Fe), zinc (Zn), and selenium (Se). It was also demonstrated that while potassium (K) was the main macronutrient in the bark, leaves had higher concentrations of other minerals such as calcium (Ca), magnesium (Mg), phosphorus (P), and zinc (Zn). Conversely, for copper (Cu), iron (Fe), and selenium (Se), the bark had higher levels [105][38]. A separate study of Anatolian carob pods by Ayaz et al. (2009) discovered the following mineral concentrations: 970 mg/100 g K, 71 mg/100 g P, 300 mg/100 g Ca, 60 mg/100 g Mg, 1.88 mg/100 g Fe, 1.29 mg/100 g manganese (Mn), and 0.85 mg/100 g Cu [98][30]. Furthermore, research on both wild and grafted carob trees in the province of Antalya in Turkey showed that the pods and seeds of the grafted carob trees generally had higher mineral concentrations than their wild counterparts. In all the samples, potassium was the most prevalent mineral, with the highest concentration found in the pods of the wild carob fruit. Of the micro-minerals, iron was the most abundant in the seeds of grafted carob fruits [106][39]. The study by El Bouzdoudi et al., 2017 [107][40] on carobs grown in Morocco identified five macroelements (potassium, calcium, chlorine, magnesium, and sodium) and thirty microelements (iron, aluminium, strontium, rubidium, copper, zinc, manganese, zirconium, barium, thorium, bromine, thulium, chromium, selenium, cerium, lanthanum, caesium, antimony, neodymium, mercury, cobalt, arsenic, scandium, molybdenum, tantalum, gold, hafnium, samarium, silver, and europium) in the whole pod, pulp, and seed and other constituents. The detection of these mineral elements in such a wide variety underscores the role of carob as a valuable source of essential nutrients, contributing to its longstanding use in human and animal diets. Moreover, the study by Khlifa et al., 2013 [93][25] examining carob pods from the Chefchaouen region in northern Morocco indicated a low-fat content in the carob pod. Another study on carob seeds from Malaga, Spain, which involved treating the seeds with acid or hot water to isolate the carob germ meal, revealed the presence of polar lipids accounting for 13–24% of the total lipid content (1.1–1.7% of carob germ meal). This lipid fraction primarily consisted of oleic acid (34.4%) and linoleic acid (44.5%) as the major fatty acids, with palmitic acid (16.2%) and stearic acid (3.4%) being the main saturated fatty acids [104][36]. According to Fidan et al., 2020 [95][27], the lipid fraction content of carob seeds was determined to be around 2.1%, consisting of non-saponifiable lipids (17.2 ± 0.13%), sterols (4.0 ± 0.04%), phospholipids (7.2 ± 0.07%), and tocopherols (2801.0 ± 40.16 mg/kg). They identified 11 fatty acids that constituted the total oil content, with oleic (45.0 ± 0.42%) and linoleic (32.4 ± 0.30%) acids being the most abundant. Palmitic (16.6 ± 0.15%) and stearic (4.7 ± 0.15%) acids were also present in moderate amounts. Research by Dallali et al., 2018 [108][41] on Tunisian carob tree leaves found a fatty acid profile dominated by unsaturated fatty acids. Among the 12 common fatty acids identified, linolenic and linoleic acids were the most prevalent. Table 31 groups the chemical compounds present in the different parts of the carob tree including the leaves, pods, pulp, and seeds.
Table 31.
Chemical composition of carob (
C. siliqua
L.).
Class Compounds Part of the Plant References
Phenols Resorcinol Leaves, pods, pulp, seeds [102][34]
Vanillin, fraxidin, 2,4-

bis(dimethylbenzyl)-6-butylphenol		 Leaves [102,109][34][42]
Alizarin, hydroquinone, lignan

bis(trihydroxyphenyl)methanone		 Pods [110,111][43][44]
Phenolic acids Gallic acid, chlorogenic acid,

syringic acid, ferulic acid,

coumaric acid, cinnamic acid		 Leaves, pods, pulp, seeds [4,5,89,102,110,111,112,113,114,115,[116,117,118,119,120,121,122,123,124,125,126,127,5][128,21][129,130][4]34][43][44][45][46][47][48][49][50][51][52][53][54][55][56][57][58][59][60][61][62][63]
4-Hydroxybenzoic acid, caffeic acid,

vanillic acid, gentisic acid		 Leaves, pods, pulp [5,89,102,112,113,114,119,121,122,125,126,127,128,129][5][21][34][45][46][47][52][54][55][58][59][60][61][62]
Tannic acid Leaves, pods, seeds [4,122][4][55]
Ellagic acid, rosmarinic acid Pods, pulp, seeds [111,119,125,126,127][44][52][58][59][60]
Sinapic acid Pulp, seeds [111,126][44][59]
Pyrogallol, methyl gallate, benzoic acid,

protocatechuic acid		 Pods, pulp [4,5,110,111,119,120,122,128,129][4][5][43][44][52][53][55][61][62]
Quinic acid Leaves, pods [109,120][42][53]
Transferulic acid, O-feruloylrutinose, O-

feruloylrutinose isomer, p-coumaroyl-

galloylhexose, O-p-coumaroylrutinose,

siliquapyranone		 Pods [110,120,125][43][53][58]
4-Hydroxy-coumaric acid Leaves [112,113][45][46]
5-Caffeoylquinic acid, myristic acid,

ascorbic acid		 Pulp [111,126,131][44][59][64]
Flavonoids Epicatechin, quercetin, kaempferol,

luteolin, catechin, apigenin		 Leaves, pods, pulp, seeds [4,5,589,102,]110,111,[21][34][43112,]113,115,[44]116,[45]118,[46]119,[120,121,48122,123,124,125,126,127,128,][49130,][51131,132][4][][52][53][54][55][56][57][58][59][60][61][63][64][65]
Epigallocatechin gallate, rutin,

myricetin, naringenin		 Leaves, pods, pulp [4,5,5110,111,][43112,]113,114,[44]116,[117,118,45][46][47][49][50119,120,121,123,124,125,][51126,][52127,128][4][][53][54][56][57][58][59][60][61]
Iso-rhamnetin Leaves, pods, seeds [102,110,111,119,125][34][43][44][52][58]
Leucoanthocyanins Leaves, pulp, seeds [133][66]
Genistein Leaves, pods [5,119][5][52]
Quercitrin, catechin tannins Leaves, pulp [112,113,115,127,133][45][46][48][60][66]
Anthocyanins Pods, pulp, seeds [5,134,135][5][67][68]
Myricitrin, daidzein, flavonol, morin Leaves [102,112,113,114,116][34][45][46][47][49]
Rhamnosides, chrysoeriol, tricetin

dimethyl ether, (iso)schaftoside-4′-O-

glucoside, gallocatechin, chrysoeriol-O-

deoxyheoxoside, dihydroxyflavanone

hexoside, tetrahydroxy flavanone, trihy-

droxy flavone (apigenin isomer), kamp-

feride, methoxykampferol, dihydroxy

flavanone, tricetin dimethyl ether, cirsi-

liol, flavone glycosides, hydroxytyrosol		 Pods [5,110,119,120,122][5][43][52][53][55]
Crismaritin, catechol, isoquercetrin,

flavonols 3′,4′,5,7-OH, 2-hexadecanol

scutellarin tetramethyl ether, silybin B,

hydroxytyrosol, catechin gallate		 Pulp [4,126,][4][129,59][62]131[64]
Apigenin flavone, chrysin aglycones Seeds [119][52]

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