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Published: 6 June 2024

Bioactive Compounds, Health Benefits and Food Applications of Artichoke (Cynara scolymus L.) and Artichoke By-Products: A Review

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Department of Food Technology, Nutrition and Food Science, Veterinary Faculty, University of Murcia, Regional Campus of International Excellence “Campus Mare Nostrum”, Campus de Espinardo, 30100 Murcia, Spain
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Appl. Sci.2024, 14(11), 4940;https://doi.org/10.3390/app14114940
This article belongs to the Special Issue Antioxidant Compounds in Food Processing
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Abstract

Cynara scolymus L. is an herbaceous plant originally from the western Mediterranean area, with Italy, Spain and France the main being producers. Both the edible flowering head and the by-products generated during processing (outer bracts, leaves and stem) are characterized by a high content of essential vitamins, minerals and bioactive compounds. In particular, the leaves represent a great source of phenolic acids derived from caffeoylquinic acid or flavonoids such as luteonin and apigenin, while the head and stem contain a high content of soluble and insoluble dietary fiber, especially inulin and pectins. Its high content of bioactive compounds provides artichoke a high antioxidant power due to the modulation effect of the transcription factor Nrf2, which may lead to protection against cardiovascular, hepatic and neurological disorders. The potential use of artichoke as a functional ingredient in the food industry may be promising in terms of improving the nutritional value of products, as well as preventing oxidation and extending the shelf-life of processed foods due to its antimicrobial activity. This review aims to provide an overview of the nutritional qualities of Cynara scolymus L. and its by-products, focusing on the possible health effects and potential applications in food products as a higher-value-added alternative ingredient.

1. Introduction

Cynara cardunculus L. var. scolymus (L.) Fiori or Cynara scolymus L. is a perennial herbaceous plant native to the Mediterranean basin []. It belongs to the specie Cynara cardunculus L., which is divided into three subspecies: the wild thistle Cynara cardunculus L. var. sylvestris (Lamk) Fiori; the cultivated thistle Cynara cardunculus var. altilis DC; and the cultivated artichoke Cynara cardunculus var. scolymus L. Fiori. All these varieties belong to the family Asteraceae, the largest existing family with up to 32,913 species and 1911 genera [].
According to Food and Agriculture Organization Corporate Statistical Database (FAOSTAT), the world production of artichoke was 1,584,513 tonnes in 2022. The European Union accounts for 38.5% of the total world production, with Italy, Spain and France being the main producers []. The planting period comprises the months from June to August, and harvesting usually begins in October and ends in May []. The artichoke cultivar has a silvery-green appearance and reaches an average height of 1.0–1.5 m [], although its flower size, appearance and taste differ among the 286 cultivated artichoke genotypes []. The edible parts of artichoke are its immature flowers called the capitulum or head []. Nevertheless, the flowering head represents only 30–40 g/100 g of its fresh weight, so during the industrial processing of artichoke, about 60–85 g/100 g is discarded as bio-waste and by-products, including its leaves, external bracts and stems [] (Figure 1).
Figure 1. (A) Cultivars of the “Blanca de Tudela” variety in the region of Murcia, Spain; (B) cross-section of an immature artichoke head; (C) mature artichoke inflorescence [].
The therapeutic benefits of artichoke have been known since the ancient Egyptians, Greeks and Romans, who used it as a medicine for the treatment of liver and digestive disorders []. The high content of bioactive compounds, such as phenolic acids, flavonoids, anthocyanins, vitamins, inulin and pectins, provide artichoke beneficial effects against a variety of diseases. Numerous studies have found that artichoke present an anti-inflammatory [], antioxidant [], antimicrobial [] and anticarcinogenic [] effect, as well as an hepato- and cardioprotective action []. Moreover, new alternative uses for artichoke bio-wastes have been proposed in order to avoid environmental problems []. Artichoke by-products in combination with novel ultrasound- and enzyme-assisted extraction techniques can be a valuable raw material for the manufacturing of value-added products such as food additives, biofuels and agrochemicals [].
Due to the growing interest in research on the beneficial effects of artichoke, this article aims to review the functional characteristics and health benefits of Cynara scolymus L. for potential applications in the food industry.

2. Nutritional Characteristics

2.1. Aproximate Composition of Artichoke

There is a large variability in nutrients between the different botanical parts of artichoke (head, bracts, leaves and stem) [,]. Genetic [], harvest [,], geographic [] and environmental [] factors also contribute to this variation. According to Petropoulos et al. [], artichoke provides 79.73 kcal per 100 g edible portion, with it being considered a low-calorie food due to its high moisture content (approximately 80%) [,].
Carbohydrates represent up to 56.62 g/100 g (Table 1) of the dry weight (DW) of artichoke. However, a large part of this constitutes dietary fiber [] (Section 2.4). Free sugars of a low molecular weight constitute a very small fraction of the total carbohydrates, with sucrose being the most abundant one followed by glucose and fructose [].
Artichoke head has a protein content of 24.27% DW (Table 1). However, the content of this macronutrient varies in other parts of the artichoke considered as by-products, with it being lower in leaves (8.74%) [] and bracts (10.35%) []. In terms of amino acid composition, essential amino acids represent about 41.04% of the total amino acids, with aromatic amino acids (phenylalanine and proline) being the most abundant followed by the branched amino acids valine and leucine []. On the other hand, artichoke is able to fulfil the requirements of all amino acids, with it being a better source of essential amino acids than other vegetables such as carrots, tomatoes, cauliflower, corn or beans [].
Table 1. Approximate composition of the edible part of artichoke.
Table 1. Approximate composition of the edible part of artichoke.
Nutrient ValueRef.
Energy(kcal/100 g FW)79.73 ± 0.04[]
Moisture(g/100 g FW)74.54 ± 0.21[]
Ash(g/100 g DW)6.88 ± 0.14[]
Proteins(g/100 g DW)24.27 ± 0.12 []
Carbohydrates(g/100 g DW) 56.62 ± 1.41 []
Fats(g/100 g DW)2.06 ± 0.05[]
SFAs(%)53.2 ± 0.5[]
MUFAs(%)2.26 ± 0.05[]
PUFAs(%)44.5 ± 0.6[]
DW: dry weight; FW: fresh weight; MUFAs: monounsaturated fatty acids; SFAs: saturated fatty acids; PUFAs: polyunsaturated fatty acids.
The fat content of artichoke is 2–4% DW, with it being lower in the edible flower and higher in the leaves []. In addition, artichoke is characterized by a fatty acid profile rich in polyunsaturated fatty acids (PUFAs), representing almost half of the total fatty acids (44.5%). The most abundant unsaturated fatty acid is linoleic acid, with 55.20 mg per 100 g edible portion followed by palmitic acid (34.80 mg/100 g) and α-linolenic acid (20.40 mg/100 g) []. Additionally, the edible part of artichoke displays a good PUFAs/SFAs (0.84) and n-6/n-3 (4.64) ratio [], being in accordance with the parameters recommended by the Food and Agriculture Organization (FAO) []. Finally, triterpenes (fardiol and taraxasterol) and sesquiterpenes were found to be the major class of lipophilic components of cultivated cardoon and artichoke leaves []. Sesquiterpenes are responsible for up to 80% of the bitter taste of artichoke [], with cyanoropicrin being the most abundant one []. These bioactive compounds have been reported as having anti-inflammatory and anti-hyperlipidemic activity [].

2.2. Minerals

Artichoke and its by-products represent a good source of minerals necessary for organisms []. Compared to the mineral composition of other vegetables reported in the literature, artichoke represents a good source of K and mainly Fe and Zn (Table 2). Deficiency of these minerals can lead to various disorders, such as anemia [] or neurological [] and immunological alterations []. The concentration of macro- and microelements varies depending on the botanical part of C. scolymus L. [], but, generally, all parts of artichoke are able to cover the mineral requirements. Also, the genotype and environmental factors play an important role in the mineral content []. On the other hand, the Na/K ratio of artichoke (0.1) [] is one of the lowest among other vegetables such as carrot, cabbage or spinach. Increased values of this parameter are associated with increased blood pressure and cardiovascular disease [].
Table 2. Micronutrients and bioactive compounds of diverse botanical parts of artichoke.

2.3. Vitamins

The artichoke head has a high content of vitamins A, B, C, E and K (Table 2). However, the different sections of artichoke are considered vitamin-rich foods, and their content may vary depending on the genotype, storage [] or harvest []. Romo-Hualde et al. [] observed a variation in the levels of vitamin E and lutein in different varieties of artichoke grown in France, Spain and Italy. Moreover, it has been shown that the content of vitamins C, A, B1, B2, B9 and B12 in artichokes is reduced after cooking []. In particular, artichoke has a high vitamin C content, reaching values similar to those of bananas, broccoli or blueberries. This compound contributes to immune defense by supporting various cellular functions of the innate and adaptive immune system. In addition, vitamin C also contributes to epithelial barrier function against pathogens and protects the body from environmental oxidative stress [].

2.4. Dietary Fiber

The fiber content of artichoke ranges from 31.47 to 85.28 g/100 g DW depending on the plant section (Table 2), with it being more abundant in the floral stem. The total dietary fiber (TDF) of artichoke is proportionally higher than other plants of the same family and of the cruciferous family; its content is also higher than that of other vegetables such as carrot, radish, turnip or asparagus []. A large part of its TDF corresponds to insoluble dietary fiber (75%) [], with cellulose, hemicellulose and lignins being the most abundant compounds, which play an important role in plant growth []. Regarding soluble dietary fiber, artichoke has a high content of pectins (20 g/100 g) [], with galacturonic acid being the most abundant. However, inulin represents a large soluble fiber content of artichoke []. Inulin is a fructan-type plant polysaccharide, whose structure is constituted by a variable number of fructose units []. This compound is present in all sections of artichoke but is more abundant in the stems (25 g/100 g DW) [], and its content depends on factors such as storage [] or food processing []. Inulin intake has been shown to improve intestinal flora and stimulate the production of short-chain fatty acids (SCFA), so it is considered a prebiotic [].

2.5. Phenolic Compounds

Artichoke represents a great source of bioactive compounds such as phenolic compounds. These are secondary metabolites present in plants with a common structure: one or more phenol groups attached to an aromatic or aliphatic structure. These compounds are produced under stressful conditions such as UV radiation, injury and infection. Its main function is to protect against pathogen attack and to intervene in the growth and maturity of the plant []. However, the importance of these compounds resides mainly in their function as antioxidants [].
The most abundant phenolic compounds in artichoke are hydroxycinnamic acids derived from caffeic acid. Most of the caffeic acid present is conjugated with quinic acid, forming caffeoylquinic derivatives. The most relevant are cynarin (1,3-O-dicaffeoylquinic acid), chlorogenic acid (3-O-caffeoylquinic acid), neochlorogenic acid (5-O-caffeoylquinic acid) and 1,5-O-dicaffeoylquinic acid []. Although these caffeic acid derivatives are found mainly in artichoke head [], higher levels of 5-O-caffeoylquinic acid and 1,5-O-dicaffeoylquinic acid have been reported in the leaves and stems [].
The second most abundant class of natural polyphenols in artichokes are flavonoids, especially flavones. The most abundant are apigenin, luteolin and their respective glycosides and rutosides []. Flavonoids in artichoke are mainly concentrated in the leaves and head and are absent in the flower stalk []. These compounds have an anti-inflammatory effect [] as well as the ability to protect cells from oxidative damage. Other important flavonoids in artichoke are anthocyanins, including peonidin, delphinidin and cyanidin and its glycosides (cyanidin-3-glucoside and cyanidin-3,5-diglucoside) []. These compounds have been shown to downregulate the production of the inducible nitric oxide synthase (iNOS) isomer, which has a pro-inflammatory effect in the vascular system []. In addition, these pigments are responsible for the color of artichoke capitula, which ranges from green to violet [].
Finally, the amount of these polyphenols varies depending on the harvest [], genotype [] and fertilization []. Pandino et al. [] reported a higher amount of phenolic compounds, especially caffeoylquinic acid derivatives, in artichokes harvested between February and April. The processing of the vegetable also plays an important role, as Lim [] reported a significant increase in the phenolic acids level after boiling artichoke in water. The high water solubility of many phenolic compounds in artichoke can lead to the lixiviation of these compounds, which may be extracted from the plant and become part of the cooking water.

2.6. Enzymes

Several enzymes present in artichoke have been isolated, purified and biochemically characterized. The most important is polyphenol oxidase (EC 1.10.3.1), which, alongside peroxidase (EC 1.11.1.7), is responsible for plant browning []. In the presence of oxygen, this copper enzyme hydroxylates monophenols to o-diphenols and oxidizes o-diphenols to o-quinones []. Browning is the main problem in the processing of artichoke, as it reduces shelf-life and commercial quality, causing significant economic losses. In addition, many of the phenolic compounds described above are lost by the action of these enzymes, reducing their beneficial effects on health. However, this enzyme can be inactivated if the vegetable is subjected to high temperatures by blanching (75–95 ºC for 1–10 min) [,] or immersion in citric or ascorbic acid [,], as the chelating compounds present in these compounds sequester the copper from the active center of the enzyme.
Other enzymes present in artichoke are aspartic proteases such as cyprosins A, B and C and cardosins A, B, E, F, G and H []. The extraction of these enzymes is of increasing interest as they present a proteolytic activity similar to pepsin [] and a milk-coagulating activity [].

3. Health Benefits

3.1. Antioxidant Activity

As described above, C. scolymus L. contains a large number of bioactive compounds, such as vitamin C, caffeic acid derivatives, apigenin, luteolin and various anthocyanins. Apart from performing essential functions in the plant, these compounds, once ingested, can perform protective functions against the generation of reactive oxygen species (ROS) and oxidative damage []. Phenolic compounds provide artichoke with a high antioxidant capacity, showing higher ABTS (2,2-azino-bis-3-(ethylbenzothiazoline-6-sulfonic acid)) and FRAP (ferric-ion-reducing antioxidant power) values than other vegetables such as asparagus, cabbage, cucumber, radish, turnip or red beet []. This high antioxidant capacity is mainly found in the head and leaves [], although the rest of the artichoke by-products represent a better source of phenolic compounds than many other foods.
Several studies have observed the inhibition of low-density lipoprotein cholesterol (LDL) oxidation and protection against oxidative stress at an in vitro level in different types of cell lines. Zapolska-Downar et al. [] (Table 3) observed the protective effects of artichoke leaf extract on endothelial cells and monocytes obtained from umbilical cords, resulting in a reduction in oxidized LDL levels and ROS generation. Carpentieri et al. [] reported similar results in the application of artichoke stem extracts (1 and 2 mg/mL) in human THP-1 macrophages stimulated with lipopolysaccharide (LPS), obtaining a reduction in ROS and a decrease in proinflammatory cytokines.
Table 3. Health benefits of different artichoke parts.
The antioxidant effect of artichoke has also been confirmed in in vivo experiments through several meta-analyses [,]. Ben Salem et al. [] investigated the effects of alloxan-induced diabetic rats treated with artichoke leaf extracts daily for 4 weeks, reporting marked changes associated with a protective effect against ROS. Specifically, an increase in catalase (CAT), superoxide dismutase (SOD) and glutathione (GSH) activities was observed in liver and kidney. El-Boshy et al. [] explored the protective effect of artichoke leaf extract against organic oxidative damage induced by cadmium (Cd) toxicity in rats. After treatment, the artichoke extract significantly improved the immune response and antioxidant system and hepatorenal function, with a significant decrease in malondialdehyde (MDA). Another study in mice with alcohol-induced acute liver injury showed that artichoke leaf ethanol extract could increase SOD and glutathione peroxidase (GPx) levels as well as decrease MDA []. There are several mechanisms that explain the antioxidant action of the bioactive compounds present in artichoke. Polyphenols are known to be able to inhibit lipid peroxidation and scavenge ROS due to their metal-ion-chelating effect []. The antioxidant capacity of caffeoylquinic acids and flavonoids can also be attributed to their H-donating function due to their specific structural characteristics []. However, the modulating effects could be mostly attributed to the interception of free radicals and ROS at the level of critical signaling pathways involving several protein kinases, phosphatases and transcription factors []. In particular, antioxidants are able to modulate the nuclear factor E2-related factor 2 (Nrf2) signaling pathway. It has been shown that polyphenols can genetically and epigenetically regulate Nrf2 at the transcriptional, post-transcriptional and translational levels, increasing the cytoplasmic concentration of this protein []. The main function of Nrf2 is to transcriptionally activate genes that synthesize enzymes such as NADPH quinone oxidoreductase (NQO1), heme oxygenase (HO-1), CAT and GPx. In addition, Nrf2 regulates inflammatory genes such as transforming growth factor-β (TGF-β) and nuclear factor-kappa (NF-kB) []. The sesquiterpene lactone content of artichoke may also regulate antioxidant activity. It has been revealed that cyanoropicrin may inhibit ROS production by upregulating the transcription of genes encoding Nrf2 and NQO1 [].

3.2. Hepatoprotective Action

The association between the use of different parts of artichoke and a hepatoprotective action against non-alcoholic fatty liver disease (NAFLD) has been supported by numerous studies [,,]. NAFLD is the most common cause of liver disease in the Western world, affecting 25% of the world’s adult population, and it is associated with an increased risk of progression to cirrhosis, hepatocellular carcinoma and cardiovascular disease []. NAFLD is characterized by inflammation and liver cell damage that can cause fibrosis. Damaged liver cells secrete enzymes such as aspartate aminotransferase (AST) and alanine aminotransferase (ALT) into the bloodstream, which are considered biomarkers for monitoring disease prognosis [].
It has been suggested that the antioxidant and anti-inflammatory properties of artichoke could prevent liver toxicity and improve cell membrane integrity, which could be characterized by a reduction in ALT and AST enzyme levels []. Phenolic compounds such as caffeic acid and isochlorogenic acid exert hepatoprotective effects by inhibiting oxidative stress through increasing Nrf2 expression, enhancing antioxidant enzyme activities and exerting a protective effect against liver injury []. The study by Panahi et al. [] observed changes in liver size, a reduction in portal vein diameter and a reduction in total bilirubin after consumption of artichoke extract for 8 weeks in adult NAFLD, as well as a reduction in ALT and AST and lipid markers as triglycerides (TG), total cholesterol, high-density lipoprotein cholesterol (HDL-C) and low-density lipoprotein cholesterol (LDL-C). Another study observed a hepatoprotective effect of artichoke in rats after the induction of toxicity with lead (Pb), reporting a reduction in serum levels of ALT, AST, TG, very-low-density lipoprotein cholesterol (VLDL-C) and MDA []. A large number of studies have observed changes in the lipid profile associated with changes at the hepatic level produced by artichoke intake []. The reduction in LDL, TC and TG induced by artichoke possibly affects liver transaminases, as TG accumulation in hepatocytes is one of the main factors in the development of NAFLD. Luteolin, luteolin-7-O-glucoside and chlorogenic acid have been shown to inhibit 3-hydroxy-3-methylglutaryl coenzyme-A (HMG-CoA) reductase, the enzyme that regulates cholesterol biosynthesis []. Therefore, the hepatoprotective effect of artichoke extracts is achieved through various pathways and mechanisms of action.

3.3. Prebiotic and Anti-Inflammatory Effect

The anti-inflammatory and gastrointestinal-disease-modulating effects of artichoke have been extensively studied in recent decades. Numerous studies report the therapeutic properties of artichoke against inflammatory bowel disease (IBF) [,,], a condition characterized by chronic relapses and remissions of inflammation in the gastrointestinal tract. IBD results from immune disorders arising from complex interactions between genetic and environmental factors such as diet, stress, insufficient sleep, alcohol and microbial composition [].
Holgado et al. [] measured the prebiotic effect of artichoke by-products after in vitro fermentation by human fecal microbiota, observing an increase in the production of total acetate, propionate and SCFA by the gut microbiota. Another study reported the benefits of artichoke head after short-term colonic fermentation using an in vitro intestinal model; the results showed an increase in total SCFA production and an increase in the bacterial genus Lactobacillus spp. []. Vacca et al. [] observed the effects of gluten-free bread enriched with artichoke leaf extract on Caco-2 cells exposed to LPS after in vitro digestion and colonic fermentations. The extracts produced a decrease in cellular expression of the inflammatory markers TNF-α and IL-1β as well as an increase in the total antioxidant capacity.
Many of the beneficial properties of artichoke are attributed to the large amount of phenolic compounds present in the leaves; however, the head and stems of artichoke are the parts most commonly used to treat digestive disorders. The anti-inflammatory and prebiotic properties are due to the high fiber content of these sections, particularly the presence of inulin and pectins. Inulin has been reported to positively alter the gut microbiota by being fermented in the large intestine and colon by beneficial bacteria such as Bifidobacteria and Lactobacillus, increasing the levels of these species. The functional attributes of these bacteria are known to contribute directly or indirectly to various health benefits, including protection against oxidative stress, pathogenic microbes, hypertension, inflammation and diabetes []. Costabile et al. [] observed that the application of very-long-chain inulin extracted from artichoke in healthy adults for 3 weeks was able to modify the composition of the intestinal microbiota, increasing the levels of Bifidobacteria, Lactobacillus and Bacteroides-Prevotella. As mentioned previously, inulin is also capable of triggering the production of SCFAs (acetate, propionate and butyrate) through bacterial fermentation in the colon []. These three compounds present remarkable beneficial health functions; acetate is a substrate for cholesterol and fatty acid synthesis, and propionate is a precursor for the synthesis of glucose in the liver []. Butyrate provides an anticancer activity, as it is the main substrate for colonic epithelial cells and plays an important role in cell differentiation and regulation []. Pectins present in artichoke also play an important role in its anti-inflammatory effect. One study showed that artichoke pectins reduced the expression of inflammatory markers such as TNF-α, ICAM-I, IL-1β and IL-6 in C57BL/6 mice with colitis []. In addition, pectin from artichoke increased the expression of the intestinal barrier genes Occludin and MUC-1. Toll-like receptor (TLR) signaling has been shown to be suppressed by MUC-1, so artichoke pectins increase MUC-1 expression, leading to decreased TLR-4 levels and, thus, a low expression of pro-inflammatory cytokines [].

3.4. Hypoglycemic Action

Diabetes mellitus (DM) is a complex metabolic disorder characterized by hyperglycemia, a physiologically abnormal condition represented by continued elevated blood glucose levels. Approximately 95% of patients with DM present type 2 diabetes, which is characterized by insulin resistance and β-cell dysfunction [].
Many studies have evidenced the ability of artichoke to show beneficial effects against this condition due to its hypoglycemic action [,]. Alves et al. [] evaluated the effects of artichoke in alloxan-induced diabetic rats, obtaining positive results with a reduction in plasma glucose levels. Treatment with the extract also significantly prevented serum fructosamine levels and had significantly lower serum TC and TG levels than untreated animals. A study in overweight patients with impaired fasting glucose (IFG) treated with two daily oral doses of artichoke extract for 8 weeks showed similar results, reducing blood glucose and insulin concentrations. Other diabetes markers such as homeostasis model assessment (HOMA) and A1c-derived average glucose (ADAG) were also reduced [].
The possible mechanisms responsible for the hypoglycemic effects of artichoke are diverse, and several remain unknown. However, it has been evidenced that some bioactive compounds present in artichoke, such as chlorogenic acid, cynarin and luteolin, can decrease glucose uptake through the intestine []. In addition, chlorogenic acid is known to be a potent inhibitor of glucose-6-phosphate translocase, and dicaffeoylquinic acid derivatives can modulate alpha-glucosidase activity []. Both enzymes are involved in gluconeogenesis and glycogenolysis and therefore in the homeostatic regulation of blood glucose levels. On the other hand, the presence of fiber is known to stabilize the blood glucose level by allowing glucose to be slowly absorbed into the blood []. Inulin, the main component of artichoke fiber, can regulate glucagon-like peptide-1, promote β-cell proliferation and reduce β-cell apoptosis []. Due to this relationship with the production of SCFA, this compound may also have a role in maintaining the insulin signaling pathway and energy homeostasis [].

3.5. Cardioprotective Effect

Cardiovascular disease (CVD) is the leading cause of morbidity and mortality, affecting over 523 million people globally, and it is responsible for 45 % of deaths in Europe []. The most prevalent CVDs are head failure, hypertension, coronary artery disease, myocardial infarction, cardiomyopathies and peripheral vascular diseases. One of the most important risk factors in the development of CVD is hyperlipidemia. Although definitions vary, it can be defined as concurrent elevations in LDL-C and TG levels [].
Some studies and meta-analyses have demonstrated the ability of artichoke to reduce hyperlipidemia, blood pressure and hypertension after consumption (Figure 2) [,]. Mocelin et al. [] studied the hypolipidemic and antiatherogenic effects of C. scolymus L. in cholesterol-fed rats and obtained similar effects to simvastatin, a therapeutic drug commonly used to lower TC levels. The treatment reduced serum levels of TC, LDL-C and oxidized-LDL as well as significantly reducing other markers of inflammation (IL-1, IL-6, TNF-α, IFN-γ and C-reactive protein). Another study was able to increase HDL-C levels and decrease the TC/HDL-C ratio after artichoke leaf extract supplementation in adults with low HDL-C and mild hypercholesterolemia []. This hypolipidemic activity is mainly due to the presence of various phenolic compounds, such as flavonoids and caffeic acid derivatives, found mainly in artichoke leaves. Chlorogenic acid, a derivative of caffeic acid, is able to induce AMP-activated protein kinase and inhibit sterol regulatory element binding protein, leading to a reduction in cholesterol synthesis. In addition, chlorogenic acid can induce β-oxidation and inhibit malonyl-CoA, which lowers triglyceride levels due to the stimulation of carnitine palmitoyl transferase []. As previously mentioned, flavonoids such as luteolin are also able to inhibit the activity of insulin-dependent HMG-CoA reductase, an enzyme involved in cholesterol biosynthesis [].
Figure 2. Beneficial effects of Cynara scolymus L. ↑ Increase; ↓ decrease.
It has been found that the inulin present in artichoke heads can modulate the lipid profile by promoting the conversion of cholesterol into bile salts, thereby reducing serum levels of very-low-density lipoproteins and LDL-C []. Villanueva-Suarez et al. [] tested this effect in HFD-fed hamsters treated with a 20% fiber by-product from artichoke, obtaining a decrease in total fat, TC and TG in the liver and an increase in fecal excretion of bile acids as the results.
A study conducted in human coronary smooth muscle cells showed that cynarin and cyanidin present artichoke leaf reduced the activation of the inducible nitric oxide synthase (iNOS) promoter and iNOS protein expression []. The main function of this enzyme is the synthesis of nitric oxide (NO), which plays a pro-inflammatory role in the vasculature. On the other hand, artichoke also plays another role in NO regulation, as flavonoids activate the endothelial expression of NO (eNOS), which has a vasoprotective effect, demonstrating a positive synergistic effect in the regulation of this molecule [].

3.6. Neuroprotective Effect

Neurodegenerative disorders are characterized by a progressive loss of selectively vulnerable populations of neurons []. Conditions such as Alzheimer’s disease, Parkinson’s disease, amyotrophic lateral sclerosis and frontotemporal lobar dementia are some of the most challenging problems in developed societies with ageing populations [].
Research in recent years has suggested that the inflammatory response of the central nervous system (CNS) may have an impact in the development of neurodegenerative diseases. In response to neuronal damage, astrocytes and microglial brain cells can release proinflammatory cytokines, such as IL-1, TNF-α and IL-6, into the cerebrospinal fluid []. On the other hand, it has been shown that compounds present in artichoke may play an important role in reducing neuroinflammation. A recent study tested the effects of C. scolymus L. on Parkinson’s disease in rats induced with rotenone [], observing that the compounds present in artichoke leaves can significantly reduce the inflammatory markers IL-1β and IL-6 as well as the apoptotic markers caspase-3 and cytochrome-c. Ibrahim et al. [] evaluated the neuroprotective effects against aflatoxin in male rats, observing a reduction in free radical production and an increase in antioxidant enzyme activity and also reporting a reduction in markers related to inflammation as AChE and NO []. Many polyphenols have been shown to inhibit platelet aggregation, preventing thrombus formation and reducing the risk of cerebral ischemia []. In addition, some of these molecules can also reduce hypertension, an important risk factor for cerebral hemorrhage. Polyphenols may reduce inflammation through other pathways such as the control of gene expression regulatory proteins like histones and the transcriptional factor NF-κB []. It has also been shown that phenolic compounds can improve serotonin levels in the brain and stimulate the production of brain-derived neurotrophic factor (BDNF), reducing inflammation [].
One study evaluated the effect of cynarin on 4-aminopyridine-induced glutamate release in rat synaptosomes []. This study concludes that cynarin, through the suppression of P/Q-type Ca2+ channels, inhibits PKA activation, thereby decreasing the availability of synaptic vesicles and contributing to the inhibition of glutamate release in the cerebral cortex terminals. This compound present in artichoke could therefore be beneficial against neurodegenerative diseases, as a lot of evidence suggests that glutamatergic dysregulation is an important contributor to the pathology of these diseases [].

4. Food Industry Application

4.1. Use of Artichoke as a Functional Ingredient

Due to its remarkable antioxidant, anti-inflammatory and prebiotic properties, the use of artichoke in the development of food products may be a key opportunity for the food industry. Several studies have considered the incorporation of different parts of C. scolymus L. in different food products (Table 4) []. The valorization of artichoke by-products in the form of extracts has become a promising possibility due to the high inulin content of the stems as well as the antioxidant properties of the leaves as a result of their high content of phenolic compounds.
Table 4. Application of artichoke extracts in food products.
Bakery products are the most studied food products for the introduction of artichoke. Its high fiber content, high soluble/insoluble fiber ratio and high water-holding capacity make artichoke fiber a great option to incorporate into bread []. In particular, several studies have used fiber-rich artichoke by-products in the form of flour to replace wheat, resulting in acceptable sensory characteristics and a bread with a lower volume and higher firmness [,,]. Artichoke has also been used to prepare crackers [,], although a negative impact on the overall sensory qualities has been reported. An emerging field of application of artichoke is pasta, where the main objective of its addition is to increase the contribution of the total phenolic content (TPC) and bioactive compounds as well as to improve the shelf-life of the product [,]. Finally, its incorporation into pastry products, such as cookies [] or cakes [,], has also been described. These reformulations have as an objective the replacement of both fat and wheat flour.
Meat composition is low in antioxidant compounds and fiber; for this reason, meat products have become a promising field of application for artichoke. Ergezer et al. [] studied the impact on the antioxidant and shelf-life qualities of beef patties with 500 and 1000 ppm artichoke extract, showing a significant improvement in antioxidant capacity values (TPC and DPPH) as well as a decrease in lipid oxidation (TBARS) at the end of storage. Another study examined the addition of 1% and 3% of artichoke extract in aubergine burgers [], observing a decrease in the color intensity and firmness of the burger but positively affecting the inhibition of microbial growth. A beneficial effect on meat products such as sausages [] or mincemeat [] has also been described, where artichoke application also had a positive impact on the increase in shelf-life.
The addition of artichoke to dairy products has also been documented. The inulin present in artichoke has been used to increase the viability of probiotic bacteria in yogurt [,], with satisfactory results being observed in the level of TPC as well as a faster increase in acidity and a shorter incubation time. On the other hand, artichoke has been used as an alternative to calf rennet in cheese production. Artichoke represents a great source of aspartic proteases, also called cardosins/cyprosins or cynarases (cardosin A and cardosin B). Several studies have verified the potential activity of these enzymes as milk coagulants [,,]. Llorente et al. [] tested the replacement of animal rennet with artichoke head extract in the manufacture of Gouda-type cheeses, obtaining no significant differences in chemical parameters or organoleptic characteristics depending on the coagulant. Therefore, artichoke head extracts may be of interest to replace traditionally used calf rennet.
Finally, artichoke extracts have also been used to prepare healthier beverages [] or as a substitute for hops in beer []. Finally, artichoke extracts have also been used to replace hops in beer or to make healthier beverages. Its use in the form of leaf extract has also been investigated as an effective feed for broilers, increasing the antioxidant capacity of the chicken meat [] and improving its productive performance [].

4.2. Antimicrobial Effect

Numerous studies have reported the potential application of artichoke as a functional ingredient in processed foods, showing its high antimicrobial effect. They have demonstrated the ability of artichoke extracts to inhibit the growth of bacteria [,,,,] and fungi [].
Meat and meat products are exposed to many potential hazards in the post-slaughter production process, such as foodborne pathogenic microorganisms and environmental contamination of equipment [], so the use of artichoke as a meat preservative may be of interest. Both Gram-negative and Gram-positive bacteria can be inhibited by artichoke heads, leaves or stems, especially common pathogens such as Staphylococcus aureus, Pseudomonas aeruginosa, Escherichia coli and Salmonella spp. [,]. In addition, there is a growing disapproval of the use of synthetic additives in the food industry. Therefore, the replacement of these additives by artichoke extracts may be of interest in the search for natural alternatives to the management of microbial contamination of perishable foods.
The reason for this potent antimicrobial activity is probably based on the high content of phenolic compounds in the different parts of the artichoke. Polyphenols can lower the intracellular pH, chelate some metals that are necessary for the survival of microorganisms or change the permeability of the bacterial cell membrane and disrupt the transport of substrates []. Flavonoids present in artichoke leaves can also interfere with microbial enzyme activity [], and different caffeoylquinic acid derivatives can disrupt bacterial cell walls [].

Author Contributions

Conceptualization, P.A. and G.N.; methodology, P.A.; validation, P.A., J.Q., M.d.l.Á.R., R.P. and G.N.; investigation, P.A.; writing—original draft preparation, P.A.; writing—review and editing, P.A., J.Q., M.d.l.Á.R., R.P. and G.N.; visualization, G.N.; supervision, G.N.; project administration, G.N.; funding acquisition, G.N. All authors have read and agreed to the published version of the manuscript.

Funding

This study forms part of the Agroalnext program and was supported by MCIU with funding from European Union Next GenerationEU (PRTR-C17.I1) and by Comunidad Autónoma de la Región de Murcia—Fundación Séneca.

Conflicts of Interest

The authors declare no conflicts of interest.

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