The Mediterranean diet (MedDi) is considered today to be among the healthiest of diets, with evidence of increased longevity and protection against CVD and cancer. The geographic and evolutionary origins of the diet are of interest as they encompass the history of Western civilisation. The rise of agriculture (domestication of crops) and animal husbandry took place from 10 000 to 4000 BCE, while the wheel, metallurgy, writing and city states arose from 4000 to 1000 BCE. These essential developments in the evolution of civilisation originated in the fertile crescent – from Mesopotamia, the ancient near East, Canaan and Egypt. The biblical period from the time of the Patriarchs until King David in Jerusalem was from 1750 to 1100 BCE with the fall of Troy and the Greek colonisation of Ionia occurring in the twelfth century BCE.
Evidence of dietary patterns has been obtained from archaeo-botany and written records. Although there are many similarities between the traditional Greek (Cretan) MedDi and that described in the Pentateuch, the differences are of interest as they have special nutritional benefits – in particular pomegranates and figs. The Bible (Deuteronomy 8:8) speaks of the seven species – wheat, barley, grapes, figs, pomegranates, olives and date honey, as well as a land ‘flowing with milk and (date) honey’, and these are also the basic staples of the MedDi. There are also hieroglyphic records of wine and olive exports from Canaan to Egypt. Further, in Roman times, historians recorded that the produce of the land of Israel was of particularly high quality and was served at the best tables. Such cross-cultural influences may be seen during the Passover meal, which was the basis of Jesus’ Last Supper, and was itself adapted from the Greek symposium brought to the region after the conquests of Alexander the Great in the fourth century BCE. The purpose of the present review is to propose that the MedDi that originated in the Middle East may be beneficially modified by the inclusion of certain food items from biblical times.
Origins of the Mediterranean diet and the biblical diet
The MedDi based on the diet of Crete (before 1960) has been significantly correlated with extended life expectancy(Reference Trichopoulou, Costacou and Bamia1) and the lowest global incidence of CHD, as well as certain cancers and other chronic diseases(Reference Sofi, Cesari and Abbate2). The MedDi is not a new diet, which is exactly the reason for its strength. In its traditional form, the food in the region was eaten according to the season and the reason. Climate dictated what was produced agriculturally, and the reason for consumption was determined by daily meal gatherings and festivals. The origins of the MedDi in fact encompass the history of Western civilisation and it has its origins in the diet and lifestyle of the Near Middle East, including those of biblical times.
The dietary laws of the Bible forbade mixing milk with meat (Exodus 23:19, 34:26 and Deuteronomy 14:21) and proscribed eating pig and sea food, allowing only animals with a cloven hoof and which ‘chewed the cud’ (Leviticus 11:3 and following), whereas fish had to have both fins and scales (Leviticus 11:9 and following). The reasons are not clear(Reference Simoons3), but might relate to eating only those animals that were preyed upon and not predators. In addition, the seven species (wheat, barley, vines, figs, pomegranates, olives and honey; Deuteronomy 8:8) in the biblical land ‘flowing with milk and (date) honey’ (Exodus 3:8) were given high priority(Reference Vamosh4). Trade between Palestine and Egypt of olive oil and wine has been documented on hieroglyphs some 2000 years before Christ(Reference Vamosh4). Archeological excavations have uncovered the products eaten during the Minoan period dating back to the Bronze Age civilization that arose on the island of Crete (2700–1450 BCE). In the Copper Age, plants and sea food were almost the sole source of nutrients. The wall paintings Frescos at Knossos show the prime role of bread in the Cretan diet. Despite the evidence of the early origins of the MedDi, recommendations have been made to revert to the traditional MedDi as consumed in Crete ‘before 1960’. But perhaps we should consider going back much further in time and take into consideration the evolution of the diet from biblical times and even before.
Mediterranean lifestyle
Human genetic profiles have not changed significantly over the past 10 000 years, whereas lifestyle has been revolutionised. Modern industrialised populations are characterised by reduced energy expenditure and increased energy intake. Fat intake in the form of trans and saturated fat has increased and there is a decrease in intakes of fibre, complex carbohydrates, fruit and vegetable antioxidants, protein and calcium(Reference Simopoulos5). In the USA, there were three times more deaths due to cancer and CHD than in Crete(Reference Allbaugh6) and this differential has only increased recently. Current trends of eating while watching television promote unhealthy, quick meals and exclude social/family communication. In biblical times, meal times (generally twice a day) nurtured relationships and was an opportunity for communication. The social setting for eating promotes fixed meal times and may overcome the reluctance to change in lifestyle experienced today. The Last Supper was the traditional Passover Seder meal and was styled on the Greek symposium in which people reclined and philosophised while eating.
The Lyon Heart Study adapted the Crete diet for the French population and showed cardioprotective and anticancer effects, thereby demonstrating that the MedDi can be modified to suit other populations(Reference de Lorgeril, Renaud and Mamelle7). Other factors that may contribute to the Mediterranean lifestyle include: relaxing psychosocial environment, mild climate, preservation of the extended-family structure and even a siesta(Reference Trichopoulou and Lagiou8), as well as regular activity, mainly through walking.
The following sections describe the health benefits of different components of the biblical diet in addition to the conventional MedDi recommended today (Table 1). Thus, discussion of the well-known nutritional qualities of grains, legumes, beans, fruit and vegetables and fish is beyond the scope of the present article.
The biblical seven species
The biblical seven species – wheat, barley, grapes, figs, pomegranates, olives and date honey, together with some indigenous foods from the Middle East – are now scientifically recognised as healthy food, and could further improve the beneficial MedDi (Fig. 1).
Grains
The origins and spread of domesticated grains have been traced to the Fertile Crescent spreading from Mesopotamia (the cradle of civilisation)(Reference Braun9–Reference Redman12). It would appear that such food use reached the Middle East before the Greek Islands. The pivotal role of bread is further emphasised in its important status and use during festivals. In the tenth century BC, carvings on limestone describe the harvest seasons in the land of Israel according to the Gezer calendar, which is a rhythmic enumeration of the agricultural seasons. In the dry summer months, vines were pruned and figs, dates, pomegranates and grapes ripened and the wheat was harvested, whereas in the spring season barley was harvested. Wheat flour and grain have provided the staple (breads, pitas, etc.) for different types of meals throughout the Mediterranean basin. It is the basic food par excellence and is at the centre of food culture. The health benefits of fibre and complex carbohydrates are beyond the scope of the present review.
Olives
In ancient times, olives were consumed by farmers and accompanied travellers and nomads, and in addition were a popular appetizer. Romans served olives as starters and desserts in their rich symposiums. Olive oil is a hallmark of the MedDi, and has a moderate fat content, in the range of 30–40 % of energy derived from fat. The majority of fat in olive oil is MUFA. Fat from edible olives and olive oil consists of oleic acid (18 : 1, n-9; 75 %), saturated fat (15 %) and PUFA (10 %). Olive oil is extracted from deeply pigmented olives that are rich in phytonutrients, including the phenolics hydroxytyrosol and oleorupein. When replacing saturated fat, olive oil reduces absolute levels of serum LDL, inhibits its oxidation(Reference Aviram and Eias13, Reference Berry, Eisenberg and Friedlander14) and attenuates atherogenesis, with a most impressive effect shown for extra virgin oil that was enriched with green tea polyphenols(Reference Rosenblat, Volkova and Coleman15).
In biblical times, olive oil was cold pressed and stored in dark, opaque glass containers. This was to avoid the powerful oxidative action of sunlight. Unprocessed olive oil has the greatest antioxidant effect. Comparison of extracted phenolic compounds from extra virgin olive oil and processed olive oil showed that extra virgin olive oil had significantly greater antioxidant effects than processed olive oil(Reference Fitó, Covas and Lamuela-Raventós16). It therefore seems that during the modern process of olive oil refinement, some of the phenolic content is reduced. The extra virgin unprocessed olive oil of the biblical diet has a higher concentration of antioxidants, which in turn may prevent LDL oxidation. In addition to its advantageous effects on blood cholesterol quantity, as well as quality, olive oil also has anti-carcinogenic action. A major component of phenols is lignans, which are found in olive oil. Owen et al.(Reference Owen, Giacosa and Hull17) found that they have a protective function against cancer of the breast, colorectum, oesophagus and prostate. Animal models show that the sterol squalene that is found in olive oil represses tumour growth(Reference Newmark18). Although the high fat content of olives could be of concern due to potential weight gain(Reference Ferro Luzzi, James and Kafatos19), obesity is not just the result of high-fat diets(Reference Willett and Leibel20). Rather, MUFA have been shown to increase postprandial fat oxidation, diet-induced thermogenesis and energy expenditure(Reference Soares, Cummings and Mamo21); hence, moderate consumption of olive oil is less likely to cause weight gain. It is of interest that in all populations studied, irrespective of geography and diet, oleic acid is the major storage adipose tissue fatty acid derived from the diet, as well as from de novo fatty acid synthesis. The reason for this is not clear, but may relate to oleic acid physico-chemical (fluidity) and biochemical (antioxidant) properties(Reference Berry22). Oleic acid is the dominant storage adipose tissue fatty acid, irrespective of where people live and what they eat(Reference Berry23).
Dates
Fruit of the date palm (Phoenix Dactylifera L. Arecaceae) are an important component of the diet in the Middle East and North Africa. Dates are an ideal high-energy food as they contain high sugar content. They are also a good source of fibre and minerals, such as Ca, Fe, Mg, K and Zn(Reference Al-Shahib and Marshall24, Reference Ali, Al-Kindi and Al-Said25). Date fruit are used in folk medicine for the treatment of various infectious diseases and cancer(Reference Puri, Sahai and Singh26), probably as a result of their immunomodulatory activity(Reference Puri, Sahai and Singh26), antibacterial capacity(Reference Sallal and Ashkenani27) and antifungal properties(Reference Shraideh, Abu-El-Teen and Sallal28). Furthermore, aqueous extracts of dates were shown to have potent antioxidant activity(Reference Vayalil29), as they inhibit in vitro lipid and protein oxidation, and possess substantial free radical scavenging capacity. The above antioxidant activity is attributed to the wide range of phenolic compounds present in dates, including p-coumaric, ferulic and sinapic acids, as well as flavonoids and procyanidins(Reference Hung, Tomas-Barberan and Kader30, Reference Al-Farsi, Alasalvar and Morris31). Aviram et al.(Reference Rock, Rosenblat and Borochov-Neori32) showed for the first time the in vivo beneficial effect of Medjool or Hallawi date varieties, despite very high content of sugars, consumed by healthy subjects on serum glucose, lipids and oxidative stress. Both date varieties possessed antioxidative properties in vitro, but their antioxidant properties in vivo were unknown. In the present study, ten healthy subjects consumed for a period of 4 weeks, 100 g/d of either Medjool or Hallawi dates. The dates did not significantly affect serum total cholesterol, or the cholesterol levels in VLDL, LDL or HDL fractions. Fasting serum glucose and TAG levels were not increased, and in fact serum TAG levels even decreased moderately but significantly by 8 % and 15 % after consumption of Medjool or Hallawi dates, respectively. After consumption of Hallawi dates alone, basal serum oxidative status was significantly decreased, as was the susceptibility of serum to 2,2′-azobis(2-amidino-propane) dihydrochloride-induced lipid peroxidation. In agreement with the above results, serum activity of the HDL-associated antioxidant enzyme paraoxonase 1 (PON1) increased significantly after Hallawi date consumption. Thus, date consumption (mainly of the Hallawi variety) by healthy subjects, in spite of their high sugar content, had beneficial effects on serum TAG and oxidative stress, and did not aggravate serum glucose and lipid profiles(Reference Rock, Rosenblat and Borochov-Neori32).
Pomegranates
The pomegranate has been cultivated in the Mediterranean region since ancient times and was introduced into Egypt from Syria and from Israel around 1600 BC. In the Bible, the coat of the high priest was adorned with pomegranates (Exodus 39: 24–26). Many are the quotations concerning this luscious fruit especially in the Song of Songs: ‘As a piece of pomegranate are thy temples (cheeks)’ (6:7); ‘I would cause thee to drink of spiced wine and the juice of my pomegranate’ (8:2).
In Greek mythology, pomegranates were a symbol of life and rejuvenation. They are a potent antioxidant containing ellagitannin polyphenolic compounds such as punicalagins and punicalins, as well as ellagic acid and gallic acid. The antioxidant health benefits of pomegranate were shown to reduce LDL oxidation and it is helpful in reducing the risk of heart disease(Reference Aviram, Rosenblat and Fuhrman33). It was also shown to decrease the progression of prostate cancer(Reference Pantuck, Leppert and Zomorodian34). Furthermore, drinking just 50 ml of pomegranate juice (PJ) daily can significantly lower blood pressure after 3 months by 5 %. Leaf extracts from pomegranate may also be effective in weight loss as, without affecting plasma TAG levels, pomegranate consumption reduces fat absorption from the intestine and can be cardioprotective(Reference Aviram, Volkova and Coleman35).
Pomegranate is a major source of most potent antioxidants (tannins, anthocyanins), which are considered to also be anti-atherogenic. Studies have analysed the effect of PJ on lipoprotein oxidation, aggregation and retention and on macrophage atherogenicity in healthy subjects and atherosclerotic patients, as well as in atherosclerotic apolipoprotein E-deficient (E°) mice. In vitro studies demonstrated a significant dose-dependent antioxidant capability of PJ against lipid peroxidation in plasma (by up to 33 %), in LDL (by up to 43 %) and in HDL (by up to 22 %). The water-soluble fractions of pomegranate's inner and outer peels, but not the seeds, were even stronger antioxidants against LDL oxidation than the juice itself. The antioxidative effects of PJ against lipid peroxidation in whole plasma and in isolated lipoproteins were also shown ex vivo in humans and mice. Furthermore, PJ consumption in humans increased the activity of serum paraoxonase, an HDL-associated esterase (lipo-lactonase) that acts as a potent protector against lipid peroxidation. PJ not only inhibited LDL oxidation, but also reduced two other related modifications of the lipoprotein, that is, its retention to extracellular matrix proteoglycans and its susceptibility to aggregation. The inhibitory effects of PJ consumption on macrophage ability to oxidise LDL on the one hand, and on the uptake of oxidised LDL on the other, contributed substantially to the attenuation of cellular cholesterol accumulation and foam cell formation, as observed in atherosclerotic mice and in atherosclerotic patients(Reference Aviram, Rosenbalt and Gaitini36). PJ supplementation to E° mice significantly reduced the number of macrophage foam cells and the size of the atherosclerotic lesion, in comparison to controls. PJ consumption by patients with carotid artery stenosis for 1 year reduced systolic blood pressure (by 18 %), oxidative stress (by 65 %) and, most importantly, the lesion size as measured by intima-media thickness (IMT; by ∼30 %)(Reference Aviram, Rosenbalt and Gaitini36).
Altogether, the results of the above studies clearly demonstrate that PJ may be considered as a potent nutraceutical agent against CVD(Reference Aviram, Rosenbalt and Gaitini36, Reference Aviram, Dornfeld and Rosenblat37).
Figs
The fig is the fruit of lust and is believed to be a symbol of fertility. The high levels of fibre in figs stimulate bowel movement. Excavations at Gezer have uncovered remains of dried figs from the Neolithic Age and an old seed was recently germinated from the Dead Sea(Reference Sallon, Solowey and Cohen38). Figs are native to the Mediterranean and grow on the ficus tree (Ficus carica), and were one of the first fruits to be cultivated. The fruit is rich in natural and simple sugars, minerals and fibre and is a good source of K, Ca, Mg, Fe, Cu and Mn. Dried figs are popular as they last for a long time and have high calcium content (250 mg of Ca/100 g fruit weight). Potassium is also essential in regulation of blood pressure. Recently, Aviram's group observed high total polyphenol content in fig juice (with some phenolics that are unique to figs), which was associated with significant antioxidant activity against LDL oxidation (M Aviram, unpublished results).
Grapes
Vine cultivation and wine production originated in Mesopotamia. However, the culture of wine consumption belongs to the Mediterranean. An Egyptian inscription from 2375 BC records how a military governor, Uni under the reign of Pharaoh Pepi I, sent troops to put down a revolt in Israel and how they ‘destroyed the fortresses … and felled the fig trees and vines’. A mural from the reign of Amenopsis II (fifteenth century BCE) shows the preparation of wine in Egypt by the Apirou, thought to be the Hebrews(Reference Goor and Nurock39). From early Egyptian civilisation through the classical period and the Roman Empire, wine has been of importance and value and exclusive to the civilised elite. Consumption of wine in the MedDi is subject to different cultural norms, especially in Muslim countries.
Red wine is rich in antioxidants from the flavonoid phenolics family, and includes cathechin, querchitin, anthocyanins and resveratrol. Resveratrol is a trihydroxystilbene phenolic compound found in the grape's seeds and skin and it has been shown to increase blood HDL cholesterol, to protect against LDL oxidation and to attenuate blood clotting. It is found in several vegetal sources and has also been shown to possess lifespan-promoting properties that mimic energy restriction in yeast and metazoans, including small mammals. While in yeast and lower metazoans resveratrol acts mainly by activating the histone deacetylase Sir2, in mammals it appears to target – in addition to the Sir2 homologue SIRT1 – several crucial pathways for the control of metabolism, including the AMPK and the insulin-IGF1 receptor axis(Reference Fröjdö, Durand and Pirola40).
In the Mediterranean culture, wine is consumed in conjunction with a meal, whereas Western cultures may consume wine independent of meals and it is a more alcoholic, less acidic and a less phenolic-rich wine. Alcohol consumption on an empty stomach leads to rapid alcohol absorption and increases the risk of intoxication. It is of interest that the Rambam (Maimonides) recognised the health benefits of wine already more than 800 years ago(Reference Maimonides41).
Red wine, but not white wine, consumption (400 ml/d, for a period of 2 weeks) by healthy volunteers, resulted in a reduced propensity of their LDL to lipid peroxidation as determined by a 46 %, 72 % and 54 % decrement in the content of aldehydes, lipid peroxides and conjugated dienes, respectively. It appeared that some phenolic substances present in red wine are absorbed, bind to serum LDL and may be responsible for the antioxidant properties of red wine against LDL oxidation.
The lower antioxidant activity in white wines, in comparison to red wines, lies in the reduced content of polyphenols extracted from the grape skin, as red wine, but not white wine, is prepared following long contact time (∼1 month) of the grape skin with the produced wine. Nevertheless, it is possible to enrich white wine with the grape skin polyphenols. White wine derived from whole squeezed grapes stored for a short period of time (up to 18 h) contained increased concentrations of polyphenols (from 0·35 after 3 h, up to 0·55 mmol/l after 18 h of storage), and in parallel, exhibited increased capacity to scavenge free radicals and to inhibit copper ion-induced LDL oxidation. Addition of increasing concentrations of alcohol (up to 18 %) to the whole squeezed grapes remarkably augmented the extraction of grape skin polyphenols into the wine (up to 1·25 mmol/l), and thus resulted in increased capacity of the wine to scavenge free radicals and to inhibit LDL oxidation to an extent similar to that of red wine. LDL oxidation inhibition was directly related to the wine's polyphenolic content (r = 0·986). Thus, processing white wine with a short period of grape skins' contact in the presence of increased alcohol concentration led to extraction of their polyphenols and produced polyphenol-rich white wine with antioxidant characteristics similar to those of red wine(Reference Fuhrman, Volkova and Soraski42).
The potent antioxidant activity first shown for the Israeli red wine consumption was also demonstrated later on in a UK study, although the antioxidant capability of this wine was lower than that of the Israeli wine. Analyses of both red wines revealed five-fold increased levels of the polyphenolic subfraction flavonols in the studied Israeli red wine. Flavonols are potent polyphenolic antioxidants, and this may explain the above results. There is wide variation in the flavonol content of different red wines throughout the world and a major determinant for the production of grape flavonols is the amount of sunlight to which the grapes are exposed during cultivation, when flavonols are synthesised. Thus, the climatic conditions under which grapes are grown could explain the five-fold increased content of flavonols in the specific studied Israeli red wine compared to the studied UK wine, and hence the high antioxidant potency observed in the Israeli red wine(Reference Howard, Chopra and Thurnham43).
The effect of consuming red wine, or its major flavonoid constituents, the flavonol catechin or the flavonol quercetin, on the development of atherosclerotic lesions was studied, in relation to LDL oxidation and aggregation, using the atherosclerotic, apolipoprotein E-deficient (E°) mice model(Reference Hayek, Fuhrman and Vaya44). The atherosclerotic lesion area was significantly decreased in the treated mice. These results were associated with reduced susceptibility to oxidation (induced by copper ions, free radical generators or by macrophages) of LDL, isolated after consumption of red wine, quercetin and, to a lesser extent, catechin, in comparison with LDL isolated from control mice. Furthermore, PON1 activity was preserved in red wine-treated mice in comparison to PON1 inactivation in the placebo-treated mice.
LDL oxidation was previously shown to lead to its aggregation. The susceptibility of LDL to aggregation was decreased, in comparison with control mice, by 63 %, 48 % or 50 % on consuming catechin, quercetin or whole red wine, respectively. In vitro studies revealed that the inhibition of LDL aggregation by the above polyphenols could be related, at least in part, to a direct effect of the polyphenols on the LDL particle(Reference Fuhrman, Lavy and Aviram45, Reference Fuhrman and Aviram46).
Additional biblical foods
The MedDi, particularly that from Crete, has a balanced intake of polyunsaturated essential fatty acids (EFA) in a ratio of 2:1 (n-6:n-3) in contrast to the much higher ratios observed in the Western and Northern European diets, and in the USA(Reference Simopoulos5, Reference Dubnov and Berry47). In the traditional MedDi, a sweet tooth was satisfied by intake of carob, and figs stuffed with walnuts as a snack.
Carob
During the Roman persecutions, Rabbi Shimon Bar Yochai and his son survived for 13 years in a cave and survived on carob, dates and water. (Kohelet Raba 10:8)(Reference Goor and Nurock39) Carob is a legume native to the Mediterranean. The word ‘carob’ is derived from the Arab kharrub and means ‘pod’, and it also gave the name carat to the measure of gold. Carob beans can be dried, ground and roasted to produce carob flour or powder. Carob is caffeine-free and naturally sweet and a rich source of calcium and potassium and smaller amounts of iron and some B vitamins. Carob binds to the intestinal tract and acts as a remedy for diarrhoea.
Aviram's research group recently measured the total polyphenol concentration in carob pod honey and found that it was comparable to concentrated PJ. The carob pod honey contained 25·8 (sd 2·4) mg, whereas concentrated PJ contained only 28·3 (sd 2·4) mg of gallic acid equivalents/ml. The carob pod honey also exhibited significant dose-dependent free radical scavenging capacity. These studies demonstrated that carob pod honey contains high concentrations of total polyphenols, even in comparison to polyphenol-rich PJ.
Nuts
Nut consumption has an inverse relationship with risk for CVD. Nuts are rich in protein, fibre, phytonutrients and polyphenolic antioxidants, as well as MUFA and PUFA.
The US Food and Drug Administration have promoted the intakes of almonds, hazelnuts, peanuts, pecans, pistachios and walnuts as they contain <8 g of saturated fat per 100 g. Walnuts have a particularly high content of n-3 fatty acids, in addition to being high in fibre, vitamin B, magnesium and several types of antioxidants. Walnuts are active in improvement of blood vessel elasticity and in reducing atherosclerotic plaque accumulation, blood LDL cholesterol concentration and the inflammatory C-reactive protein biomarker.
Nuts are also rich sources of fibre, vitamin E and phytochemicals such as ellagic acid, flavonoids, phenolics, luteolin, isoflavones and tocotrienols. Nuts are also an excellent source of Mg, Zn, Se, Cu, riboflavin, niacin, Fe and folic acid. Of interest is that peanuts were shown to contain the flavonoid resveratrol (∼70 μg/ounce of peanuts), whereas almonds contain the flavonoids quercetin and kaempferol.
Nut consumption reduces the risk of CHD, as shown in the Iowa Women's Health Study and that on California Seventh-Day Adventists(Reference Sabate48–Reference Fraser, Sabate and Beeson50).
Additional antiatherogenic properties of nuts may be related to the type of the nut's proteins that are rich in the amino acid arginine and low in lysine. Arginine is a precursor of the vasodilator, antiatherogenic agent nitric oxide. Reduced arginine/lysine ratio is directly related to accelerated atherogenesis(Reference Kritchevsky, Tepper and Czarnecki51).
An additional important mechanism for the protective effect of nut consumption against atherogenesis is the attenuation of oxidative stress by nut antioxidants such as vitamin E, polyphenols, flavonoids and other phytochemicals(Reference Bolling, McKay and Blumberg52).
Acknowledgements
The authors have no conflict of interests to declare. E.M.B. conceptualized the review and wrote and edited the manuscript. M.A. provided data from his research and critically reviewed the many draft versions. Y.A. performed the literature review and background to the table and figure.