Mediterranean Diet Ingredients: Their Antioxidant and Anti-Inflammatory Potential

    

    

    Figure 2: Nutrients found in the food choices of MD with emphasis on polyphenols and their classification.
    

The allium family of vegetables (garlic, onions, leeks, shallots, scallions, and chives), often considered as key savory ingredients of the MD, add the characteristic culinary flavor to the traditional Mediterranean dishes. They are rich in organosulfur compounds, e.g. allicin, diallyl disulfide and others, and many powerful antioxidants (quercetin, kaempferol), which reduce the oxidative stress known to cause cellular damage, thus, having the anti-cancerogenic and antiinflammatory activities, among others [24-33].

Spices and herbs, such as basil, rosemary, oregano, black cumin, thyme, ginger, cinnamon, clove, dill, parsley, licorice, mint, as well as garlic and onions are often added in the Mediterranean cuisine to introduce variety of flavors and tastes to traditional recipes replacing partially a portion of the salt. This is very beneficial, as the salt intake is becoming an alarming issue in modern diets and has been linked to hypertension and other heart-related diseases. Moreover, herbs and spices are rich sources of micronutrients, antioxidant and antiinflammatory compounds. They have been also used for preservation of foods and beverages due to the high phytochemicals’ content [34- 39].

In the traditional MD, seasonal vegetables and fruits are mostly consumed in the seasons when available, while for the remaining seasons, usually for the winter, they are usually preserved mainly via fermentation and sun-drying processes. Fermentation as one of the oldest techniques for food preservation is often used in the Mediterranean basin for fermenting foods and drinks, e.g. wine. During the fermentation process, natural bacteria are using the sugar and starch in the food and are creating environment that preserves the food and promotes beneficial enzymes, B vitamins, and omega-3 fatty acids, as well as various species of good bacteria. Fermented vegetables, such as cabbage, cauliflower, peppers, green tomatoes, cucumbers, carrots, olives and others are rich with probiotics and are often used during off-seasons. Diets involving high content of fermented foods, i.e. foods rich in probiotics have been found to results in gut microbiome diversity, which is beneficial for the overall health, improved immunity and reduced inflammation [40,41].

Sun-dried fruits, such as dried figs, dates, apricots, prunes, raisins and others, rich with selenium, copper, potassium, magnesium, B-complex vitamin, vitamin C, carotenoids, and dietary fibers are used as snacks and for preparation of traditional desserts replacing a large portion of sugar [42,43].

Fruits, vegetables, and legumes are also known as sources of prebiotics. Prebiotics are actually plant fibers that contain complex carbohydrates. These carbohydrates aren’t digestible by the body, so they pass through the digestive system and serve as food for the gut bacteria and other microbes. The prebiotics stimulate the growth of healthy bacteria, while the probiotics increase the number of microbes in the gut. Probiotics are different from the prebiotics, because they do contain live organisms, usually specific strains of bacteria that directly add to the population of healthy microbes in the gut [44-53].

Seeds, namely, black cumin, hemp, flax, pumpkin, sunflower quinoa, and sesame seeds are usually used in the form of intact raw or dry seeds, oils, or as powder to enrich variety of foods as flavorings, ingredients, or for health purposes. Majority of seeds are low-calorie rich sources of proteins, fibers, vitamins E and B, minerals (calcium, magnesium, manganese, phosphor, iron, zinc) and unsaturated fatty acids which account for more than 85% of their fatty acid composition. Many seeds also contain polyphenols, which provide health benefits and have strong antioxidant activities [54,55].

Whole grains, such as rice, oatmeal and products made of whole grains, viz. variety of breads, pastries, cereals, pasta, crackers and variety of traditional pies filled with cheese, vegetables or fruits, are consumed often. Whole grains are a good source of nutrients, such as dietary fibers, iron, zinc, manganese, folate, magnesium, copper, thiamine, niacin, vitamin B6, phosphorus, selenium, and riboflavin [56].

Protein- and fiber-rich legumes, such as different types of beans, peas, lentils, chickpeas and others, are often used in many Mediterranean dishes combined together with various herbs, spices and vegetables. Phytonutrients often found in the legumes are vitamin B6, folate, flavones, phytosterols and various minerals (Figure 2) [54,55].

Nuts, such as walnuts, almonds, hazelnuts, pistachios, peanuts, pine nuts, cashews, and so on, are frequent snacks, or are often used as ingredients in the Mediterranean dishes and especially in Mediterranean desserts. They are good sources of healthy fats (omega-3 fatty acids), proteins, vitamins (tocopherols-vitamin E, vitamin B2, folate), minerals (potassium, copper, phosphorus, selenium, magnesium), phytosterols, fibers and significant loads of antioxidants. In particular, nuts are also excellent sources of antioxidant phenolics, with some nuts having particularly high levels of proanthocyanidins and hydrolysable tannins (gallotannins and ellagitannins), as shown in Figure 2. Besides their satiating effect, the nuts’ intake usually does not promote obesity and has beneficial effects on many diseases and disorders, such as metabolic syndrome, diabetes, cardiovascular (CVD) and other diseases. Nuts are cholesterol-free and have been shown that their phytosterols actually interfere with the cholesterol absorption, and thus, help to lower the blood cholesterol level. Among the nuts, the walnuts have the highest polyphenol content and are one of the most used nut in the traditional Mediterranean desserts [9,57-62].

The whole grains, legumes, nuts, seeds, vegetables and fruits provide a plethora of dietary fibers, which are essential nutrients for the gut microbiota and the gut lining, and thus, promote good overall health and protection from external “invaders” [44-49].

Extra virgin olive oil is a cornerstone of the MD. Numerous epidemiological studies have linked the consumption of EVOO and better overall health and well-being. Namely, in vitro and in vivo studies have indicated that the regular intake of EVOO is associated with enhanced neuroprotective, antioxidant, anti-inflammatory, anti-atherosclerotic and anti-cancer activity. EVOO is a main source of healthy fats in the traditional MD, beside the fats provided by the consumed nuts and seeds. Its unique composition, the fatty acid composition and the richness with bioavailable polyphenols, is responsible for the health protective benefits of EVOO and its resistance to elevated temperatures, which makes it good for both, cooking and salad dressings. EVOO as one of the most studied oils todate has been associated with extended life expectancy and reduction of the risks of many age-related degenerative diseases in people who consume it regularly. Moreover, EVOO has been reported to be inversely associated with the risks for several cancers and CVDs, as well as positively affects the blood lipids, i.e. cholesterol and triglyceride levels. All these benefits are due to the richness of the EVOO with valuable bioavailable phytochemicals, such as the optimal fatty acid profile, especially Monounsaturated Fatty Acids (MUFA) viz. oleic, palmitic, linoleic, and a-linoleic acid, tocopherols (vitamin E), betacarotene and a variety of polyphenols. Furthermore, EVOO has been implicated in modulation of the aging processes due to its effectiveness in reducing the inflammatory and oxidative processes. Diversity of the polyphenols, such as phenolic acids (caffeic, p-cumaric, ferulic acid), phenolic alcohols (hydroxytyrosol, tyrosol), secoiridoids (oleuropein), flavonoids (quercetin, luteolin, apigenin), lignans and others (Figure 2), result in a strong antioxidative activity of EVOO, capable to scavenge oxidative species, increase cellular endogenous antioxidant defenses, and thus, reduce the oxidative stress in the body. Hydrotyrosol and tyrosol, which comprise over 90% of the total phenolic content of EVOO, have been proven for their very high rates of absorption in humans upon ingestion (40-95% depending on the EVOO quality), while oleuropein in EVOO has been shown to have superior anti-oxidation effects on blood lipids when compared with other cooking oils with similar fatty acid content. Moreover, the EVOO’s phytochemicals decrease the inflammation via modulation of pro-inflammatory cytokines and enhance the immune function in the body, as well as act toward enhanced fat metabolism and enhanced energy expenditure [12,62-73].

A moderate consumption of dairy products, fish (salmon, tuna and sardines), seafood, and other animal-based foods, such as poultry and eggs, is another characteristic of the traditional MD. Low-fat dairy products and especially fermented milk products, such as feta cheese and other types of cheeses, yogurt, kefir, curds, and sour milk products, are consumed moderately during the day or week. These products are rich in vitamin D and calcium, and the fermented dairy products are rich in probiotics and other nutrients important for the optimal gut, bone and heart health [14,19,74,75]. Fish and seafood, are rich in omega-3 long-chain Polyunsaturated Fatty Acids (PUFAs), viz. Eicosapentaenoic Acid (EPA) and Docosahexaenoic Acid (DHA), and are consumed moderate-to-often i.e. several times per week. EPA and DHA promote the production of anti-inflammatory compounds important for suppression of chronic inflammation which has been implicated in the etiology of numerous diseases, such as type 2 diabetes, CVD, cancer, obesity, rheumatoid arthritis, neurodegenerative diseases, etc. Poultry (e.g. chicken, turkey) and eggs are consumed in moderation and represent good sources of proteins, vitamins (vitamin D), minerals (zinc, selenium) and healthy fats [2,14].

Lean read meat (lamb, pork, goat, veal, beef) is consumed rarely in the traditional MD depending on preference, availability and religious beliefs, usually few times per week or even few times per month, or in some countries, only for special occasions, festivities and holidays [19,76]. The meat is usually cooked in small quantities with plenty of vegetables, thus is used more for giving the flavor, and rather as a main ingredient in the Mediterranean dishes.

Hydration is an important factor for an optimal health. Daily intake of plenty of water, non-sugary drinks (juices, herbal teas), fermented drinks (yogurt), coffee, broths and different soups, are frequently consumed in the traditional MD during the day. Often consumption of wine with the meals, but in moderation, is a common practice used in parts of the Mediterranean area and proven to have positive effects on health and longevity due to its polyphenol (resveratrol) content [2,19,77-80].

Processed food products, e.g. sweets, cakes, processed meat products, fast food, frozen food, pizzas, carbonated sugary beverages, and others, are consumed very rarely within the traditional Mediterranean dietary pattern, or during special occasions and holidays. The processed foods usually contain high amounts of refined sugars, salt, emulsifiers and other food additives, unhealthy saturated and trans fats (e.g. butter, margarine) – all of them proven to promote inflammatory processes in the body. Moreover, as these foods are usually energy-dense foods, they do give “immediate” energy boost, but not lasting satiety, and in long term, do contribute to weight gain and development of obesity [17].

MD is characterized with food choices using raw or minimumcooked ingredients (vegetables, grains, and seeds). These ingredients can act as carriers enabling phytochemicals to reach the colon where they may be released by the actions of gut bacteria. For example, grain fibers from raw vegetables and fruits carry the polyphenols to the colon and release the polyphenols there, rather than earlier release in the gastrointestinal tract. The cooking methods can have beneficial effects not only on the palatability of the prepared food, but also on improving the digestibility and bioavailability of phytonutrients. It can enhance the attractiveness of the food by way of appealing texture, flavor and taste, while preventing the loss of nutrients and the formation of toxic compounds. However, the influence of the food processing techniques, e.g. the food preparation and cooking, on the nutrient composition and nutritional value of the foods is not usually taken into consideration when different diets are compared. The food processing methods greatly affect the phytochemicals and the final nutritional profiles of the prepared dishes, and thus, influence the protective effects of the particular diets against chronic diseases. It is known that loss of antioxidant phytochemicals can occur during cooking due to thermal degradation and/or from release of toxic polar compounds from the cooking oil. MD cooking methods usually involve EVOO, which has been found to be one of the best cooking oils due to its higher stability at higher temperatures resulting in less release of polar compounds, while still preserving the majority of its polyphenolic antioxidants. Moreover, EVOO has been found to act as an efficient extracting medium for many phytochemicals from the vegetables cooked in EVOO and making them more bioavailable. An example is the sofrito dip, when tomatoes and other vegetables are cooked along in EVOO, which has been proven for its antiinflammatory and anti-oxidants efficacies [2,19,81-87].

Besides the food choices of the MD, the socializing aspect of the MD, i.e. the conviviality is a very important component of this diet. It adds meaningful social and cultural values to the traditional meals, beyond their nutritional values. The social support and interactions, enjoying life events together with family and friends, preparing and cooking the food together, sharing the food, having lengthy meals with others and mealtime conversations are common practices in the traditional Mediterranean lifestyle. In the past, the mealtimes have been even considered as opportunities for social interactions and have been used to keep families and communities together. The pleasure associated with the conviviality of meals seems to positively affect the well-being and the health status of the people involved, who have been associated with lower risk of CVDs, lower cancer incidence, improved overall mortality and increased longevity [2,19,22,88-93].

Antioxidant and Anti-Inflammatory Potential of Mediterranean Diet Ingredients

The oxidative stress is a result of the generation of oxidative species (free radicals, reactive oxygen and reactive nitrogen species) in the body, which is usually triggered by unhealthy diet and external factors, such as smoke, pollution, chemicals, drugs, UV rays, unhealthy lifestyle, etc. The oxidative stress further causes structural and functional damages of the main biomolecules in the body, such as DNA, lipids, and proteins and has been implicated in the pathogenesis of many chronic degenerative diseases, inflammation, neuro-degenerative disorders and aging processes. In particular, the imbalance between the production of oxidative species in the body and the antioxidant defense could lead to many pathological situations (i.e. diseases). To counteract this oxidative stress caused by the reactive species, the body needs various types of antioxidants. The body tries to fight with its own antioxidative defense mechanism, but de novo antioxidants’ production in the human cells is limited. Therefore, the body needs a continuous supply of external antioxidants, which to ensure better health is preferred to come from the diet in form of dietary antioxidants [10,11,20,94,95].

The inflammation processes usually occur as the immune system’s response to the external invaders, like viruses, bacteria, and subsequent cells’ injuries, but sometimes the immune system can trigger the inflammation even when no external invaders are present, like in the case of autoimmune diseases. In both cases, inflammatory processes have been implicated as undelaying cause of many serious diseases; actually many chronic metabolic diseases, viz. obesity, metabolic syndrome, type 2 diabetes, CVDs, depression, Alzheimer’s disease, certain types of cancers and so on, start in the gut, where 70% of the body immunity is located, and further progress as a result of a long-term inflammation. MD is considered as a highly antioxidant and anti-inflammatory diet due to the richness of phytochemicals originated from different MD ingredients, all acting in synergy and having antioxidant and anti-inflammatory effects. The frequently-found nutrients in MD are given in Figure 2. Emphasis on polyphenolic compounds and their classification along with the chemical structures of some of the representatives of each class are also given in Figure 2 [14-17,94-106].

The phytochemicals, viz. polyphenols, carotenoids, tocopherols, vitamins and minerals are found in MD food ingredients, such as EVOO, vegetables, fruits, nuts, seeds, grains, spices, herbs, tea, wine and others. The polyphenols as products of the secondary metabolism in the plants usually accumulate in the plant organs, like leaves, fruits, roots, and stems. They are essential for the plant life; they provide defense against harmful microorganisms and make the plants unpalatable to predators. On the other hand, the wide spectrum of dietary phenolic compounds provides the health benefits and reduced risks for many Non-Communicable Diseases (NCDs) associated with this diet. More specifically, the polyphenols coming from dietary sources in conjunction with the traditional Mediterranean cooking methods making them more bioavailable are characterized with high antioxidant, anti-cancer, anti-inflammatory, and anti-aging activities [18,96,101,107-111]. These phenolic compounds are also responsible for the organoleptic properties of the foods; the intensity of these properties mostly depends on the phenolic concentration and their structure. For instance, the phenolics are responsible for the bitterness, astringency, color, flavor, odor and oxidative stability of the food products where they are present [82,107,112-117].

The antioxidant properties of the phenolic compounds are expressed via different mechanisms, which can be summarized as follows: a) ability to remove free radicals and inhibit the formation of reactive species, b) ability to prevent the damage of lipids, proteins, nucleic acids, and c) ability to prevent consequent cell damage and death as a result of the previous two mechanisms. All of them are commonly associated with preventing the development of many human diseases, such as cardiovascular diseases, neurodegenerative diseases, autoimmune diseases, diabetes, cancer, but also very important is that they could modulate human gut microbiota [107].

Polyphenols cover wide range of compounds and are classified in different ways; mainly they are divided into flavonoids and nonflavonoids (phenolic acids, stilbenes, lignans, and other phenolics), but there are also other classifications in literature. In general, polyphenols contain at least one aromatic ring with one or more hydroxyl groups (Figure 2). Briefly, some of the polyphenolic compounds are described below along with their beneficial properties.

Phenolic acids, such as gallic, vanillic, cinnamic, ascorbic caffeic, ferulic, and p-coumaric acids are non-flavonoids can be found in fruits, legumes, herbs and vegetables mainly as free phenolic acids, whereas grains contain bound phenolic acids. They have high efficacy in food preservation, as well as antimicrobial, anticancer, antiinflammatory, anti-mutagenic protective effects [118-120].

Resveratrol is a stilbene (non-flavonoid polyphenol), which is found in red grapes and its products (red wine), and berries. The moderate wine consumption with meals in the Mediterranean dietary pattern has been linked to lower incidence of coronary heart diseases exactly due to the presence of resveratrol and other polyphenols found in the red wine. Moreover, resveratrol has chemoprotective, anti-inflammatory and neuroprotective activities, because it can effectively scavenge free radicals and chelate metals [121-127].

Quercetin is a flavonol found in many vegetables (onions, broccoli, peppers, cauliflower and cabbage) and fruits (berries, apples), nuts, seeds and grains. It has been used for used for the treatment of allergic, metabolic, and inflammatory disorders, eye and cardiovascular diseases, and arthritis due to its pronounced antioxidant, antiviral, antibacterial, anti-cancer and anti-inflammatory properties [128,129].

Catechins are simple flavonols, such as Epicatechin (EC), Epigallocatechin (EGC), Epicatechin Gallate (ECG), and Epigallocatechin Gallate (EGCG). They are usually present in apples, teas, grapes, berries, cacao, red wine, beer, etc. and have been found to reduce the incidence of CVDs, inhibit angiogenesis and, therefore, the cancer progression [130-132].

Anthocyanins are flavonoids known for their effects as pigments, which determine the color of the fruits and vegetables (blue, red, and purple). They are found naturally in a number of foods, such as berries, currants, grapes, leafy vegetables, roots, and grains and offer antioxidant, antiviral, anti-inflammatory, anti-obesity, antidiabetic and anti-cancer benefits. The beneficial properties attributed to the consumption of anthocyanin-rich foods have been linked to improved eye health, reduced cardiovascular diseases, and beneficial neuroprotective effects [112-114,133].

Luteolin is a flavone that is found in broccoli, leaves, parsley, thyme, rosemary, green pepper, carrots, olive oil and chamomile tea and has anti-oxidant, anti-inflammatory, anti-bacterial, anti-diabetic and anti-proliferative activities [134-137].

Lignans are present in a wide variety of plant foods, including seeds (flax, pumpkin, sunflower, poppy and sesame), whole grains, beans, fruits and vegetables and they reduce the risk of certain cancers and cardiovascular diseases [138-140].

Final Remarks

Worldwide, NCDs, such as obesity, diabetes, metabolic syndrome, and cardiovascular events account for 70 % of deaths. The modifiable risk factors that contribute to this high percentage NDCs include unhealthy dietary and lifestyle habits, such as consumption of nutrient-poor food rich in refined sugars, ultra-processed fastfood choices, smoking, sleep deprivation, polluted environments, etc. Mediterranean diet, as a healthy dietary pattern and a lifestyle with a proven track that can be easily implemented outside the Mediterranean basin, could significantly reduce the incidence of NCDs worldwide [110,141].

MD is a plant-based dietary pattern, which emphasizes abundant consumption of fruits, vegetables, whole grains, nuts, legumes and seeds, herbs, spices and EVOO as a main source of healthy fats, followed by a moderate consumption of fish, poultry, low-fat dairy and fermented dairy products [2,142]. The plant origin of the food choices in the MD, and especially the high polyphenolic content, variety of vitamins and minerals, heathy fats, probiotics and dietary fibers, have been linked to be responsible for the reduction of inflammatory and the oxidative processes in the body. Beside the MD ingredients, the cooking methods characteristic for the Mediterranean cuisine are believed to help in preserving the phytochemicals and make them more bioavailable. Overall, all consumed phytochemicals in synergy contribute to the good health and the overall well-being of the people adhering to MD; in particular, reduced risks for many chronic diseases, CVDs and several types of cancers have been documented for those adhering to MD.

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