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Review

Culinary Herbs and Spices: Their Bioactive Properties, the Contribution of Polyphenols and the Challenges in Deducing Their True Health Benefits

by
Elizabeth I. Opara
1,* and
Magali Chohan
2
1
School of Life Sciences, Kingston University, Penrhyn Road, Kingston upon Thames KT1 2EE, UK
2
School of Sport, Health and Applied Science, St. Mary's University, Waldegrave Road, Strawberry Hill, Twickenham TW1 4SX, UK
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2014, 15(10), 19183-19202; https://doi.org/10.3390/ijms151019183
Received: 14 July 2014 / Revised: 18 September 2014 / Accepted: 26 September 2014 / Published: 22 October 2014
(This article belongs to the Special Issue Bioactive Phenolics and Polyphenols)
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Abstract

Herbs and spices have been used for both culinary and medicinal purposes for centuries. Over the last decade, research into their role as contributors of dietary polyphenols, known to possess a number of properties associated with reducing the risk of developing chronic non-communicable diseases, has increased. However, bearing in mind how these foods are consumed, normally in small quantities and in combination with other foods, it is unclear what their true benefit is from a health perspective. The aim of this review is to use the literature to discuss how preparative and digestive processes, bioavailability and interactions between foods may influence the bioactive properties of these foods, and whether or not polyphenols are responsible for these properties. Furthermore, this review aims to highlight the challenges that need to be addressed so as to determine the true benefits of these foods and the mechanisms of action that underpin their purported efficacy.
Keywords: herbs; spices; polyphenols; bioactive properties; health herbs; spices; polyphenols; bioactive properties; health

1. Introduction

The leaf, root, bark, berry, bud, seed, stigma of a plant or flower used for the purpose of cooking are commonly referred to as herbs and spices, which were and are primarily used for, and associated with, adding to or enhancing the flavor of foods including meats, sauces, vegetables and desserts [1]. Beyond acting as a replacement for salt [2], the nutritional contribution of these dietary plants has in the past been deemed negligible probably because of the relatively small, although increasing amounts consumed [3,4]. However, the literature indicates that within the last decade, this view is beginning to change [1].
The long historical use of herbs and spices for their medicinal benefits is fully acknowledged, and there is a growing amount of literature concerning the potential/purported benefits of these foods from a health perspective. These benefits include their possible role in conferring protection against cardiovascular and neurodegenerative diseases, cardiovascular disease, cancer and type 2 diabetes [1,5,6,7,8,9]. However, what is unclear is the true significance of these “benefits”. In their comprehensive review on the health benefits of herbs and spices Tapsell et al., [1] argue that the real challenge in establishing the role of these foods in maintaining health is not proving that they “have health benefits but in defining what these benefits are and developing methods to expose them by scientific means”.
One approach that is being used to begin to address this challenge is to investigate the bioactive properties of these foods within a nutritional context (that is investigating whether or not such properties are evident at levels at which herbs and spices are consumed). This approach has led to questions about the contribution of a group of phytochemical constituents which predominate in herbs and spices—the polyphenols [10,11,12,13]—and ultimately whether or not herbs and spices have a meaningful “health” role to play via their contribution to dietary polyphenol intake.

2. Dietary Polyphenols in Culinary Herbs and Spices

Polyphenols are a large family of structurally diverse compounds that can be classified based on the number of phenol rings (hydroxyl groups attached to aromatic rings) and the groups that bind these rings [14,15,16]. The main classes/groups of dietary polyphenols are the phenolic acids (hydroxybenzoic and hydroxycinnamic acids), the flavonoids (flavonols, flavones, isoflavones, flavonones, flavanols and the anthocyanidins), the stilbenes and the lignans. Other classes of dietary polyphenols are the coumarins and the tannins: the coumarins are cinnamic derived phenolic compounds and the term tannin is applied to large polyphenolic compounds including proanthocyanidins and gallic acid esters–moleular weight > 500) [15,17,18,19]. A large number of polyphenols occur in nature however environmental factors, both biotic and abiotic, affect the polyphenolic content of foods. Furthermore, the type of diet may limit the level and composition of intake [11,12,13,15,16,20].
Polyphenols are found in numerous plant derived foods including herbs and spices, which, especially in their dried forms, generally contain relatively high levels of polyphenols compared to other polyphenol rich foods including broccoli, dark chocolate, red, blue and purple berries, grape and onion [11,12,13,21] (Table 1 and Table 2).
Table
Table 1. Total phenolic content of common culinary herbs and spices.
Table 1. Total phenolic content of common culinary herbs and spices.
FoodTotal Phenolic Content (mg/100 g FW a) b
HerbsCoriander (Coriandrum sativum L.)dried2260
fresh158.90
Dill (Anethum graveolens L.)dried1250
fresh208.18
Oregano (Wild Majoram) (Origanum vulgare L.)dried6367
fresh935.34
Parsley (Petroselinum crispum (P. Mill.))dried1584
fresh89.27
Rosemary (Rosmarinus officinalis L.)dried2518
fresh1082.43
Sage (Common) (Salvia officinalis L.)dried2919
fresh185.20
Thyme (Common) (Thymus vulgaris L.)dried1815
fresh1173.28
SpicesCinnamon (Ceylan) (Cinnamomum verum J. Presl) 9700
Cloves (Syzygium aromaticum) 16,047.25
Coriander seed (Coriandrum sativum L.) 357.36
Ginger (Zingiber officinale Roscoe)dried473.50
fresh204.66
Nutmeg (Myristica fragans Houtt.) 1905
Turmeric (Curcuma longa L.) 2117
a FW: Fresh weight; and b values obtained from Phenol-Explorer Database Neveu et al. [11], Pérez-Jiménez et al. [12], Pérez-Jiménez et al. [13].
Table
Table 2. Total phenolic content of other polyphenol rich foods.
Table 2. Total phenolic content of other polyphenol rich foods.
Total Phenolic Content (mg/100 g FW a) b
FoodDark Chocolate1859.80
Broccoli (Brassica oleracea var. italica Plenck)198.55
Blackcurrant (raw) (Ribes nigrum L.)820.64
Red raspberry (raw) (Rubus idaeus L.)148.10
Strawberry (raw) (Fragaria L.)289.20
BlueberriesHalf Highbush (Vaccinium augustifolium Ait. × Vaccinium corymbosum L.)151.33
Highbush (raw) (Vaccinium corymbosum L. and Vaccinium corymbosum L.)223.4
Lowbush (raw) (Vaccinium augustifolium Aiton)471.55
Rabbiteye (Vaccinium corymbosum L.)549.98
CranberryAmerican (Vaccinium macrocarpon Ait.)315.00
European (Vaccinium oxycoccos L.)139.50
Grape (Vitis vinifera L.)Black184.97
Green121.80
Onion (raw)Red (Allium cepa var. cepa L.)102.83
a FW: Fresh weight; and b values obtained from Phenol-Explorer Database Neveu et al. [11], Pérez-Jiménez et al. [12], Pérez-Jiménez et al. [13].
The predominant class/group of polyphenols in herbs and spices are the phenolic acids and flavonoids (mainly the flavone and flavonol sub groups). However, some, (parsley (Petroselinum crispum), Chinese cinnamon (Cinnamomum aromaticum Nees) ginger (Zingiber officinale), turmeric (Curcuma longa L.)) also contain other sub-groups of polyphenols (furanocoumarins (parsley), hydroxycoumarins (Chinese cinnamon), hydoxyphenylpropenes (ginger), curcuminoids (turmeric)) [11,12,13,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39].

Properties of Polyphenols

Polyphenols and polyphenol rich foods especially fruits, vegetables and green tea, are widely known for their antioxidant properties however they exert other biological effects (anti-inflammatory, anti-cancer and neuro-protective), which may also contribute to their purported benefits, possibly or not, via their antioxidant properties, and they are therefore linked to the maintenance of health via protection against the development of non-communicable diseases [16,19,40,41,42,43,44,45,46,47,48]. Other properties include anti-microbial, anti-diabetic (Type II), and anti-asthma activities [16,49,50] and there is now a growing amount of literature on how polyphenols confer health benefits via their action on gut microbiota [51,52,53,54].
Culinary herbs and spices have also been shown to possess these properties [1,5,7,8,10,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70]. Furthermore, evidence suggests that it is the polyphenols that have a significant role to play in conferring these properties [1,10,57,58,70,71] and as these foods have high polyphenol contents they may be important dietary sources of the purported protective properties that their polyphenols confer [57,58,64,70]. In order to begin to determine if culinary herbs and spices are indeed significant dietary contributors of polyphenols, and their properties, the following need to be considered: Habitual levels of intake; the significance of their bioactive properties at habitual levels of intake; how the preparative and digestive processes they undergo prior to, and after consumption, respectively, and absorption affect these properties (especially as much of the research on the bioactive properties of these foods has been done on their uncooked state); and the influence of other foods on the bioactive properties of herbs and spices (as they are rarely consumed on their own).

3. Habitual Levels of Intake of Culinary Herbs and Spices

In light of the bioactive properties that culinary herbs and spices possess, the need to determine their intake is being acknowledged. Intake data are available for particular groups/populations [3,4,72] (Table 3). The levels of intake are clearly and predictably much lower than for foods more widely known for their protective properties, and the values provided vary considerably possibly due to a number of factors that are very difficult to control including, under-reporting, the inclusion of non-herb and spice seasonings, the large varieties of recipes for a given dish, how such recipes are interpreted, appetite and portion size [3,4,70,72]. However, the relatively low intake levels of culinary herbs and spices do not necessarily mean that they are of little value as their high polyphenol content, and thus ultimately the potential biological impact of this content, cannot be ignored.
Table
Table 3. Culinary herb and spice intake studies.
Table 3. Culinary herb and spice intake studies.
StudyIntake Data
Pellegrini et al. [72]: Determined daily intake of spices using 3 day weighed food record (3D-WR) and food frequency questionnaire (FFQ). For the 3D-WR median data were obtained. For the FFQ, interquartile range data were obtained. n = 285; Subjects: men (n = 159) and women (n = 126); Country of study: Italy0.4 (1.3) g (3D-WR); 3.2 (2.7) g (FFQ)
Carlsen et al. [3]: Determined herb and spice intake using a FFQ and 2–4 weeks later 28 days recording of herb and spice consumption (HSR). n = 146; Subjects: men (n = 63) and women (n = 83); Country of study: NorwayMedian estimates of total herb and spice consumption: 2.7 g/person/day (range 0.19–45.0; Interquartile range 4.4) from the FFQ; 1.6 g/person/day (range 0–10; interquartile range 1.8) from the HSR; Main herb/spice contributors: Basil (dried and fresh), oregano (dried), cinnamon, pepper, and spice blends
Pérez-Jiménez et al. [4]: Measured the contribution of seasonings (included non-herb and spice seasonings) to daily polyphenol intake using 24 h dietary records every 2 months from 1995–1996 and the Phenol-Explorer database. Mean intake data obtained. n = 4942; Subjects: men (n = 2596) and women (n = 2346); Country of study: France0.4 (0.3) mg/day/person; Main herb/spice contributors: Ginger and parsley

4. The Impact of Processes Prior to, and Post Consumption on the Bioactive Properties of Culinary Herbs and Spices

4.1. Antioxidant Capacity and Total Phenolic Content

Culinary herbs and spices are, in many instances, cooked prior to consumption, and then undergo digestion. Thus, to further elucidate their biological and nutritional significance, the impact of these processes needs to be understood especially at levels of habitual intake. Chohan et al., [20] carried out a study on the impact of cooking on a number of common culinary herbs and spices, namely cinnamon, cloves, fennel, ginger, parsley, rosemary, sage and thyme at amounts used in the preparation of food (0.2–1 g). Microwaving, simmering and stewing all increased the antioxidant capacity probably as a result of heat liberating the antioxidant compounds [73,74]. In contrast, cooking techniques that involved dry heating, grilling and frying, resulted in a decrease in antioxidant capacity which was associated with browning and thus may be indicative of the Maillard reaction, or more specifically its products, influencing antioxidant capacity [74,75,76].
Subsequent studies using culinary herbs from the Lamiaceae family: parsley, rosemary, sage and thyme showed that changes in antioxidant capacity due to cooking processes were strongly and significantly associated with changes in total phenolic content [72,77]. This finding is not surprising as the assays used to determine antioxidant capacity (Trolox equivalent antioxidant capacity/2,2'-Azinobis-(3-ethyl benzothiazoline-6-sulfonic acid) assay-TEAC/ABTS assay) and total phenolic content (the Folin-Ciocalteau/gallic acid equivalents–GAE-assay) are based on similar redox reactions [78] however the role of polyphenols as major contributors of antioxidant capacity in culinary herbs and spices is well established [10,32,57,79,80]. Chohan et al., [71] also showed that the effect of cooking on antioxidant capacity is not always consistent, which is an observation that may be associated with the nature of the food matrix and the type of cooking method used [81,82,83]. Related work by Chohan [77] also showed that cooking time can also affects the antioxidant capacity (TEAC), total phenolic content (GAE) and polyphenol, specifically phenolic acid, profile of culinary herbs.
Chohan et al., [71] also investigated the impact of digestion post cooking on the antioxidant capacity and total phenolic content of these culinary herbs and found that both were significantly increased compared to uncooked and also cooked culinary herbs. Other studies on the impact of digestion, in vitro, on antioxidant capacity/activity and/or total phenolic content reported a decrease in fruit beverages [84], either no change or a decrease for herbal teas, prepared from infusions of powdered herbs [85] or either decreases, increases or no statistically significant change for dietary antioxidant supplements [86]. The type of in vitro model (i.e., the chemical and enzymatic environment within the models) used could account for some of these differences [87]. However the nature of the food/delivery matrix may have also influenced the outcomes of these studies and thus suggests that the form of the food may contribute to its impact as a dietary contributor of the bioactive properties of its constituents.
Preliminary HPLC analysis of rosemary, sage and thyme (uncooked, cooked and cooked and digested) strongly suggest that significant increases in rosmarinic acid, which is a predominant phenolic acid in these herbs, is most likely responsible for the observed increases in antioxidant capacity following cooking and also cooking and digestion. These results also suggest that to some extent other phenolic acids including caffeic acid, ferulic acid and vanillic acid may also contribute to the increase reported for some but not all of the herbs investigated [77]. These results certainly strengthen the role of polyphenols in the conferment of antioxidant properties on to these foods. They also highlight the variations that occur in the chemical composition of different batches of foods as there was only partial agreement with data obtained from the Phenol-Explorer database [11,12,13] specifically for the uncooked herbs. These variations could be due to biotic and abiotic factors as stated above [57,88] and/or the sensitivity of the analytical technique used.
For culinary spices, Baker et al., [70] found that cooking and digestion affected the antioxidant capacity and total phenolic content of cinnamon, cloves and nutmeg-again at levels associated with the preparation of food. However, these changes were not consistent. One possible reason given for this is the behavior of the phytochemical constituents (both polyphenol and non-polyphenolic) within the food matrix during these processes giving rise to additive, antagonistic and/or synergistic effects on the bioactivity of these foods.

4.2. Anti-Inflammatory Activity and Total Phenolic Content

There is a paucity of data concerning the effect of preparative and digestive processes on the anti-inflammatory activity of culinary herbs and spices. Investigations of the impact of cooking and digestion on the anti-inflammatory properties of culinary herbs and spices demonstrate that this property is not diminished by these processes. Chohan et al., [71] reported that at amounts used in food preparation, uncooked, cooked, and cooked and digested rosemary, sage and thyme elicited an anti-inflammatory effect via the inhibition of, and also protection against, the action of pro-inflammatory agents hydrogen peroxide (H2O2) and tumor necrosis factor α (TNFα) which resulted in the inhibition of IL-8 release from peripheral blood lymphocytes (PBLs). These decreases were only significant for PBLs exposed to H2O2 for the most part which may be indicative of an activity that involves more than the inhibition of a single pro-inflammatory mediator. There was a strong and significant correlation between inhibition of IL-8 release and antioxidant capacity and total phenolic content irrespective of whether the herbs were uncooked, cooked or cooked and digested which indicates that the polyphenols within these foods contribute to this anti-inflammatory activity, and that this activity may be due to their antioxidant properties. However, the findings of Baker et al., [70] which were focused on culinary spices at levels associated with habitual intake suggest that the contributory role of polyphenols is not so straight forward (as indicated by Chohan et al. [71]): Baker et al., [70] reported that the spices cinnamon, clove and nutmeg (uncooked, cooked and digested) significantly inhibited the pro-inflammatory enzyme cyclo-oxygenase-2 (COX-2). The study also reported via correlation analysis that the anti-COX-2 activity was only partially associated with the antioxidant capacities and polyphenolic content of these spices. The partial correlation to phenolic content suggests the involvement of non-polyphenolic compounds, which is supported by the literature. For example, cinnamaldehyde, a major constituent of cinnamon, and the essential oil responsible for its aroma and flavor [89], has been shown to inhibit COX-2 activity [90]. The partial correlation with antioxidant capacity suggests that other actions may contribute to the anti-inflammatory properties.
The inflammatory response is a complex one and involves numerous mediators, a number of which may be affected by individual polyphenols and thus by culinary herbs and spices: Yoon and Baek [91] discuss the inhibitory effect of polyphenolic compounds including phenolic acids and flavonoids on one or possibly several cellular pathways that are involved in the inflammatory process. These pathways include the arachidonic dependent pathways, which involve the action of the cyclo-oxygenase (COX) enzymes, and the arachidonic independent, pathways, which include peroxisome proliferator activated receptors (PPARs), nitric oxide synthase (NOS), nuclear transcription factor κB (NF-κB), which regulates the expression of pro-inflammatory cytokines including IL-8, as well as the non-steroidal anti-inflammatory drug (NSAID) activated gene. Some of these polyphenols include those that are found in culinary herbs and spices. For example, rosmarinic acid has been shown to inhibit the pro-inflammatory PKC/NF-κB pathway [92]. Curcumin, a predominant polyphenol in turmeric, also inhibits NF-κB [93] COX-2 has also been shown to be down-regulated and/or inhibited by eugenol (clove) and apigenin (parsley) [94,95].
Culinary herbs, including lemon grass, rosemary and thyme are also reported to enhance the activity of the enzyme superoxide dismutase (SOD), which in addition to being an important antioxidant enzyme has the potential to act as an anti-inflammatory agent as it catalyses the dismutation of the free radical superoxide, which is associated with chronic inflammation [96,97]. A recent study by Chohan et al. [98] identified rosemary, sage and thyme as possessing superoxide dismutase mimetic (SODm) activity which was significantly associated with the antioxidant capacity, total phenolic content and inhibition of IL-8 release. The association with the former (antioxidant capacity) is not surprising but this analysis does indicate that polyphenols in these herbs may be responsible for the SODm activity as suggested by Huaefi and Smetanska [99] and that it (SODm) may also contribute to the herbs’ anti-inflammatory activity. Thus, this mimetic activity possessed by these herbs may account for some of the antioxidant and anti-inflammatory properties that these foods possess.
In summary, studies on the antioxidant and anti-inflammatory activities of culinary herbs and spices at levels associated with habitual intake show that these properties are not diminished post cooking and digestion. In addition, this work also indicates, via correlation analysis, that polyphenols are significant in conferring both these activities. However, for some spices non-polyphenolic compounds may also have a role to play.

5. Bioavailability of Polyphenols from Culinary Herbs and Spices

For a clearer understanding of the significance of the potential health benefits of culinary herbs and spices, it is essential to establish the bioavailability of their bioactive constituents. The literature on the bioavailability of polyphenols reports that the intestinal absorption of dietary polyphenols into systemic circulation is poor as they are metabolized by gut flora and/or the liver (post-absorption), and/or eliminated from the body rapidly [15,17,100]. Ultimately these factors will influence their activity and thus their health effects significantly. A preliminary study by Chohan et al. [101], carried out using a Caco-2 in vitro model, which has a high level of agreement with bioavailability studies in humans [102,103], on the bioavailability of polyphenols from culinary herbs (1 g starting amounts, post cooking and digestion) found that 8.3%–10.6% of the total phenolic content of cooked and digested rosemary, sage and thyme was detected post-passage through the Caco-2 monolayer. In addition, low levels of antioxidant capacity were also detected (8.5%–15% of pre-passage through the monolayer). Furthermore, despite the detection of polyphenolic content and antioxidant capacity following passage through the monolayer, no constituent polyphenols, specifically phenolic acids, were detected using HPLC. This finding at face value appears to contrast with that of Lee et al. [104] who reported detecting hydroxycinniamic acids post passage across a Caco-2 monolayer, although permeability across the monolayer was low. However, the lack of detection in the study by Chohan et al. [101] may be due to the small starting amounts of herb being diluted first during the cooking and in vitro digestion stage and then during the bioavailability experiments. The small starting amount was used to help establish the significance of the health promoting properties of the herbs in vivo, at levels that are used in the preparation of food, and are thus consumed. The samples used by Lee et al. [104] to investigate bioavailability were not foods but pure polyphenols, which did not undergo cooking and/or digestion prior to passage across the Caco-2 monolayer.
The observation regarding low bioavailability suggests that the action of dietary polyphenols may be localized to the gut, although how polyphenols interact with the gut is unclear [17,100]. In addition, there is a growing amount of literature on the positive role of polyphenols and polyphenol rich foods on gut health specifically with regards to the prevention and treatment of colorectal cancer [84,105,106,107,108,109,110,111,112,113,114,115] However, there are a number of additional factors that need to be considered when attempting to elucidate the action of the gut on these foods and their polyphenols. First, in the study by Chohan et al. [101] the time periods for the Caco-2 study were 60 and 120 min but it needs to be borne in mind that some polyphenols may remain in the small intestine for longer periods. In addition, the role of intestinal microflora also needs to be taken into consideration as they may be of potential significance with regards to making polyphenols more available for intestinal absorption [84]. The role of the colon needs to be factored in as the non-starch polysaccharide constituents, mainly cellulose, of the herbs investigated, although not affected in the gastric and small intestinal stages of digestion, could be metabolized by intestinal colonic microflora [17,100]. Thus, following cellulose breakdown, the polyphenols in these herbs could be metabolized in the colon. This theory is supported by a study which found large amounts of metabolites of phenolic compounds in human fecal water [116]. Furthermore, a study by Dall’Asta et al. [117] showed evidence of metabolism of dietary polyphenols following colonic fermentation, in vitro.
Research to establish the bioavailability of polyphenols in culinary herbs and spices highlights a plethora of factors that paradoxically contribute to and also limit our knowledge and understanding of the bioavailability of these compounds from these foods, the impact on their bioactive properties and ultimately their health benefits. To obtain further insight regarding the significance of bioavailability, studies on the impact of the food matrix and interactions between its constituents, the chemical, enzymatic and bacterial environment within the gut, and habitual, as opposed to single dose, intake are required [100,118,119].

6. Bioactive Properties of Combinations of Culinary Herbs and Spices: The Role of Synergy

It is fully acknowledged and recognized that identifying the constituents within foods that confer bioactive properties is important especially from a mechanistic perspective [18,120,121,122]. However, it is the whole food that is consumed, and it is normally consumed in combination with other foods, so a key question is: How do the food matrix and its constituents influence the whole foods’ bioactive properties? Answering such a question will facilitate the unravelling of the true health benefits of plant derived foods like culinary herbs and spices in vivo as they are commonly consumed in combination with each other and with other types of foods. There is a growing amount of literature regarding the efficacy of combinations of individual polyphenols, culinary and medicinal herbs, foods rich in polyphenols, and polyphenols and other protective phytochemicals based on their anti-proliferative and antioxidant properties in vitro (predominantly) and in vivo. De Kok et al., [123] provided a comprehensive review of the literature in this area in 2008 and recent studies subsequent to this work further highlight the importance of investigating the efficacy of these combinations [124,125,126,127,128,129,130,131,132] (Table 4). The findings of these studies indicate that the outcome of combining dietary polyphenols and their foods is influenced by the constituents themselves, the number of constituents (food or polyphenol) that make up the combination, the amount/concentration of a constituent, any processing that the combinations may undergo, for example cooking, and also the assay used [129,130,131,132]. Furthermore, the analysis used to determine if antagonism or synergy has occurred is another factor that needs to be considered [133]. Some studies use analysis based on the summation of effects method, which compares the effect of constituents combined with that of the expected effect, which is the sum of the effects of the individual constituents. However, it is argued that this method is limited when it comes to complex mixtures (such as food) as it depends on the mechanism of action of each constituent and assumes that the response of each constituent is linear in nature. Thus, another method, the isobole method, is more appropriate as it is independent of the mechanism of action and is said to apply under most conditions [133]. This method is more complicated as the different combinations used for the isobolographic analysis must have generated an iso-effect however it has been used to investigate interactions between herbs based on antioxidant and antiproliferative activities [125,129,131]. In summary, and as with bioavailability, studies on food synergy highlight the challenges of determining the benefit in vivo of culinary herbs and spices as well as fully elucidating the mechanisms that underpin their true efficacy.
Table
Table 4. Recent studies on the antagonistic and synergistic effects of combinations of individual polyphenols or combinations containing polyphenol rich foods.
Table 4. Recent studies on the antagonistic and synergistic effects of combinations of individual polyphenols or combinations containing polyphenol rich foods.
CombinationsEffectStudy
Epigallocatechin gallate (EGCG) and curcuminSynergistically cytotoxic to MDA-MB-231 estrogen receptor α (ERα) human breast cancer cells in vitro when compared to effects of the individual polyphenols.EGCG + curcumin also synergistically inhibited tumor growth within female athymic nude mice implanted with MDA-MB-231 estrogen receptor (ERα) human breast cancer cells compared to individual polyphenols. Proposed mechanism of action: Cell cycle arrest and decrease in the expression of vascular endothelial growth factor receptor in tumor may play a role.Somers-Edgar et al. [124]
Curcumin and resveratrolSynergistic inhibition of growth of p53 positive and p53 negative human colorectal cancer HCT116 cells in vitro when compared to effects of the individual polyphenols.Curcumin and resveratrol combination also synergistically inhibited tumor growth within severe combined immunodeficient female mice implanted with HCT-116 cells. Proposed mechanism of action: Decrease in proliferation and induction of apoptosis, decreased NF-κB activity, inhibition of activation of epidermal growth factor receptor.Majumdar et al. [125]
Carnosic acid and curcuminCombinations (at levels shown to be non-cytotoxic to normal human fibroblasts or human peripheral blood mononuclear cells) inhibited the growth of, and induced apoptosis in, HL-60 and KG-1a human acute myeloid leukemia cells. Proposed mechanism of action: Apoptosis associated with activation of caspases 8, 9 and 3 and Bid (a proapoptotic protein) which is a member of the Bcl family. No other Bcl proteins shown to be affected. No evidence that oxidative stress was involved.Pesakhov et al. [126]
Chicken +/−herb and spice based marinating saucesMarinating and cooking significantly decreased the antioxidant capacities of herb and spice marinating sauces.Thomas et al. [127]
Antioxidant rich spice (black pepper, cloves, cinnamon, garlic powder, ginger, oregano, paprika and rosemary) added to hamburger meatSignificant reduction in malondialdehyde concentration (a biomarker of oxidative stress) in the spiced burger compared to that in the unspiced (control) burger. There was also a significant increase in plasma malondialdehyde concentration following consumption of the control burger. Following consumption of the spiced burger there was a “trend to decrease” in plasma malondialdehyde concentration. Urinary malondialdehyde concentration decreased by almost 50% in subjects that consumed the spiced burgers compared to those who consumed the control burgers.Li et al. [128]
Combinations of Aspalathus linearis and Malus domestica, Aspalathus linearis and Vaccinium, Myrtillus, Punica granatum and Malus domesticaCombinations demonstrated additive or synergistic effects (based on antioxidant capacity) but these outcomes depended on the type of assay used.Blasa et al. [129]
Polyphenol rich herbs oregano, ajowan (Trachyspermum ammi) and Indian borage (Plectranthus amboinicus)Addition of oregano extract increased the radical scavenging activity of ajowan and Indian borage extracts.Khanum et al. [130]
Peppermint, rosemary, sage, spearmint, thyme.All herb extracts inhibited the growth of SW-480 human colorectal cancer cells. Combinations of these extracts herbs had additive, antagonistic and synergistic effects, which were based on the combinations and/or the concentrations of the herb extracts used in the combinations.Yi and Wetzstein [131]
Blueberries, grapes, chocolate covered strawberries, and polyphenol rich fruit smoothies.Significant synergy, based on antioxidant capacity, found in combinations of chocolate covered strawberries; reported either antagonism or synergy within the combinations of constituent polyphenols; the effect depended on the constituents, and their number, and also the antioxidant assay used.Epps et al. [132]

7. Conclusions

Current research on the impact of preparative and digestive processes on the bioactive properties of culinary herbs and spices has shed some light on their potential benefits. However, further work is needed to fully understand if the low bioavailability of polyphenols from these foods really limits their health benefits. Furthermore, there is very little understanding of the impact of combining these foods on their bioactivity. Ultimately, it is the use of a combination of in vivo and in vitro methods that will determine the true health benefits of culinary herbs and spices and the contributory role of their constituent polyphenols.

Acknowledgments

Magali Chohan was the recipient of a Biomedical and Pharmaceutical Sciences Research Group, Kingston University, funded Ph.D.

Author Contributions

Elizabeth I. Opara prepared the manuscript; Magali Chohan assisted in the preparation of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Tapsell, L.C.; Hemphill, I.; Cobiac, L.; Sullivan, D.R.; Fenech, M.; Patch, C.S.; Roodenrys, S.; Keogh, J.B.; Clifton, P.M.; Williams, P.G.; et al. Health benefits of herbs and spices: The past, the present, the future. Med. J. Aust. 2006, 185, S1–S24. [Google Scholar]
  2. Ghawi, S.K.; Rowland, I.; Methven, L. Enhancing consumer liking of low salt tomato soup over repeated exposure by herb and spice seasonings. Appetite 2014, 81, 20–29. [Google Scholar]
  3. Carlsen, M.H.; Blomhoff, R.; Andersen, L.F. Intakes of culinary herbs and spices from a food frequency questionnaire evaluated against 28-days estimated records. Nutr. J. 2011, 10, 50. [Google Scholar]
  4. Pérez-Jiménez, J.; Fezeu, L.; Touvier, M.; Arnault, N.; Manach, C.; Hercberg, S.; Galan, P.; Scalbert, A. Dietary intake of 337 polyphenols in French adults. Am. J. Clin. Nutr. 2011, 93, 1220–1228. [Google Scholar]
  5. Kaefer, C.M.; Milner, J.A. The role of herbs and spices in cancer prevention. J. Nutr. Biochem. 2008, 19, 347–361. [Google Scholar]
  6. Raghavendra, R.H.; Naidu, A.K. Spice active principles as the inhibitors of human platelet aggregation and thromboxane biosynthesis. Prostaglandins, Leukot. Essent. Fat. Acids 2009, 81, 73–78. [Google Scholar]
  7. Iriti, M.; Vitalini, S.; Fico, G.; Faoro, F. Neuroprotective herbs and foods from different traditional medicines and diets. Molecules 2010, 15, 3517–3555. [Google Scholar]
  8. Jungbauer, A.; Medjakovic, S. Anti-inflammatory properties of culinary herbs and spices that ameliorate the effects of metabolic syndrome. Maturitas 2012, 71, 227–239. [Google Scholar]
  9. Fleenor, B.S.; Sindler, A.L.; Marvi, N.K.; Howell, K.L.; Zigler, M.L.; Yoshizawa, M.; Seals, D.R. Curcumin ameliorates arterial dysfunction and oxidative stress with aging. Exp. Gerontol. 2013, 48, 269–276. [Google Scholar]
  10. Zheng, W.; Wang, S.Y. Antioxidant activity and phenolic compounds in selected herbs. J. Agric. Food Chem. 2001, 49, 5165–5170. [Google Scholar]
  11. Neveu, V.; Perez-Jiménez, J.; Vos, F.; Crespy, V.; du Chaffaut, L.; Mennen, L.; Knox, C.; Eisner, R.; Cruz, J.; Wishart, D.; Scalbert, A. Phenol-Explorer: An online comprehensive database on polyphenol contents in foods. Database 2010. [Google Scholar] [CrossRef]
  12. Pérez-Jiménez, J.; Neveu, V.; Vos, F.; Scalbert, A. A systematic analysis of the content of 502 polyphenols in 452 foods and beverages—An application of the Phenol-Explorer database. J. Agric. Food Chem. 2010, 58, 4959–4969. [Google Scholar]
  13. Pérez-Jiménez, J.; Neveu, V.; Vos, F.; Scalbert, A. Identification of the 100 richest dietary sources of polyphenols—An application of the Phenol-Explorer database. Eur. J. Clin. Nutr. 2010, 64, s112–s120. [Google Scholar]
  14. Kondratyuk, T.P.; Pezzuto, J.M. Natural product polyphenols of relevance to human health. Pharm. Biol. 2004, 42, 46–63. [Google Scholar]
  15. Scalbert, A.; Williamson, G. Dietary intake and bioavailability of polyphenols. J. Nutr. 2000, 130, 2073S–2085S. [Google Scholar]
  16. Pandey, K.B.; Risvi, S.I. Plant polyphenols as dietary antioxidants in human health and disease. Oxid. Med. Cell. Longev. 2009, 2, 270–278. [Google Scholar]
  17. Manach, C.; Scalbert, A.; Morand, C.; Remesy, C.; Jimenez, L. Polyphenols: Food sources and bioavalability. Am. J. Clin. Nutr. 2004, 79, 727–747. [Google Scholar]
  18. Liu, R.H. Potential synergy of phytochemicals in cancer prevention: Mechanism of action. J. Nutr. 2004, 134, 3479S–3485S. [Google Scholar]
  19. Singh, M.; Arseneault, M.; Sanderson, T.; Murthy, V.; Ramassamy, C. Challenges for research on polyphenols from foods in Alzheimer’s disease: Bioavailability, metabolism, and cellular and molecular mechanisms. J. Agric. Food Chem. 2008, 56, 4855–4873. [Google Scholar]
  20. Chohan, M.; Forster-Wilkins, G.; Opara, E.I. Determination of the antioxidant capacity of culinary herbs subjected to various cooking and storage processes using the ABTS*+ radical cation assay. Plant Foods Hum. Nutr. 2008, 63, 47–52. [Google Scholar]
  21. Ninfali, P.; Mea, G.; Giorgini, S.; Rocchi, M.; Bacchiocca, M. Antioxidant capacity of vegetables, spices and dressings relevant to nutrition. Br. J. Nutr. 2005, 93, 257–266. [Google Scholar]
  22. Beier, R.C.; Ivie, G.W.; Oertli, E.H. Linear furanocoumarins and graveolone from the common herb parsley. Phytochemistry 1994, 36, 869–872. [Google Scholar]
  23. Justesen, U.; Knuthsen, P.; Leth, T. Quantitative analysis of flavonols, flavones, and flavanones in fruits, vegetables and beverages by high-performance liquid chromatography with photo-diode array and mass spectrometric detection. J. Chromatogr. A 1998, 799, 101–110. [Google Scholar]
  24. Variyar, P.S.; Bandyopadhyay, C.; Thomas, P. Effect of gamma-irradiation on the phenolic acids of some Indian spices. Int. J. Food Sci. Technol. 1998, 33, 533–537. [Google Scholar]
  25. Kahkonen, M.P.; Hopia, A.I.; Vuorela, H.J.; Rauha, J.P.; Pihlaja, K.; Kujala, T.S.; Heinonen, M. Antioxidant activity of plant extracts containing phenolic compounds. J. Agric. Food Chem. 1999, 47, 3954–3962. [Google Scholar]
  26. Bandoniene, D.; Pukalskas, A.; Venskutonis, P.R.; Gruzdiene, D. Preliminary screening of antioxidant activity of some plant extracts in rapeseed oil. Food Res. Int. 2000, 33, 785–791. [Google Scholar]
  27. Mattila, P.; Astola, J.; Kumpulainen, J. Determination of flavonoids in plant material by HPLC with diode-array and electro-array detections. J. Agric. Food Chem. 2000, 48, 5834–5841. [Google Scholar]
  28. Jayaprakasha, G.K.; Rao, L.J.M.; Sakariah, K.K. Improved HPLC method for the determination of curcumin, demethoxycurcumin, and bisdemethoxycurcumin. J. Agric. Food Chem. 2002, 50, 3668–3672. [Google Scholar]
  29. Wang, H.; Provan, G.J.; Helliwell, K. Determination of rosmarinic acid and caffeic acid in aromatic herbs by HPLC. Food Chem. 2004, 87, 307–311. [Google Scholar]
  30. Proestos, C.; Chorianopoulos, N.; Nychas, G.J.E.; Komaitis, M. RP-HPLC analysis of the phenolic compounds of plant extracts. Investigation of their antioxidant capacity and antimicrobial activity. J. Agric. Food Chem. 2005, 53, 1190–1195. [Google Scholar]
  31. Proestos, C.; Komaitis, M. Ultrasonically assisted extraction of phenolic compounds from aromatic plants: Comparison with conventional extraction technics. J. Food Qual. 2006, 29, 567–582. [Google Scholar]
  32. Shan, B.; Cai, Y.Z.; Corke, H. Antioxidant capacity of 26 spice extracts and characterisation of their phenolic constituents. J. Agric. Food Chem. 2005, 53, 7749–7759. [Google Scholar]
  33. Luthria, D.L.; Pastor-Corrales, M.A. Phenolic acids content of fifteen dry edible bean (Phaseolus vulgaris L.) varieties. J. Food Compos. Anal. 2006, 19, 205–211. [Google Scholar]
  34. Tayyem, R.F.; Heath, D.D.; Al-Delaimy, W.K.; Rock, C.L. Curcumin content of turmeric and curry powders. Nutr. Cancer 2006, 55, 126–131. [Google Scholar]
  35. Anilakumar, K.R.; Saritha, V.; Khanum, F.; Bawa, A.S. Effect of cooking on total phenols, flavonoids and antioxidant activity in spices of Indian culinary. J. Food Sci. Technol. 2007, 44, 357–359. [Google Scholar]
  36. Baskan, S.; Oztekin, N.; Erim, F.B. Determination of carnosic acid and rosmarinic acid in sage by capillary electrophoresis. Food Chem. 2007, 101, 1748–1752. [Google Scholar]
  37. Kivilompolo, M.; Hyotylainen, T.A. Comprehensive two-dimensional liquid chromatography in analysis of Lamiaceae herbs: Characterisation and quantification of antioxidant phenolic acids. J. Chromatogr. A 2007, 1145, 155–164. [Google Scholar]
  38. Kivilompolo, M.; Oburka, V.; Hyotylainen, T. Comparison of GC-MS and LC-MS methods for the analysis of antioxidant phenolic acids in herbs. Anal. Bioanal. Chem. 2007, 388, 881–887. [Google Scholar]
  39. Suresh, D.; Manjunatha, H.; Srinivasan, K. Effect of heat processing of spices on the concentrations of their bioactive principles: Turmeric (Curcuma longa), red pepper (Capsicum annuum) and black pepper (Piper nigrum). J. Food Compos. Anal. 2007, 20, 346–351. [Google Scholar]
  40. Scalbert, A.; Johnson, I.T.; Salmarch, M. Polyphenols: Antioxidants and beyond. Am. J. Clin. Nutr. 2005, 81, 215s–217s. [Google Scholar]
  41. Tsai, P.-J.; Tsai, T.-H.; Yu, C.-H.; Ho, S.-C. Evaluation of NO-suppressing activity of several Mediterranean culinary spices. Food Chem. Toxicol. 2007, 45, 440–447. [Google Scholar]
  42. Romier, B.; van de Walle, J.; During, A.; Larondelle, Y.; Schneider, Y. Modulation of signaling nuclear factor-κB activation pathway by polyphenols in human intestinal Caco-2 cells. Br. J. Nutr. 2008, 100, 542–551. [Google Scholar]
  43. Romier-Crouzet, B.; van de Walle, J.; During, A.; Joly, A.; Rousseau, C.; Henry, O.; Larondelle, Y.; Schneider, Y. Inhibition of inflammatory mediators by polyphenolic plants extracts in human intestinal Caco-2 cells. Food Chem. Toxicol. 2009, 47, 1221–1230. [Google Scholar]
  44. Hollman, P.C.; Cassidy, A.; Comte, B.; Heinonen, M.; Richelle, M.; Richling, E.; Serafini, M.; Scalbert, A.; Sies, H.; Vidry, S. The biological relevance of direct antioxidant effects of polyphenols for cardiovascular health in humans is not established. J. Nutr. 2010, 141, 989S–1009S. [Google Scholar]
  45. Link, A.; Balaguer, F.; Goel, A. Cancer chemoprevention by dietary polyphenols: Promising role for epigenetics. Biochem. Pharmacol. 2010, 80, 1771–1792. [Google Scholar]
  46. Vauzour, D.; Rodriguez-Mateos, A.; Corona, G.; Oruna-Concha, M.J.; Spencer, J.P. Polyphenols and human health: Prevention of disease and mechanisms of action. Nutrients 2010, 2, 1106–1131. [Google Scholar]
  47. Ebrahimi, A.; Schluesener, H. Natural polyphenols against neurodegenerative disorders: Potentials and pitfalls. Ageing Res. Rev. 2012, 11, 329–345. [Google Scholar]
  48. Thomas, R.; Williams, M.H.; Sharma, H.; Chaudry, A.; Bellamy, P. A double-blind, placebo-controlled randomised trial evaluating the effect of a polyphenol-rich whole food supplement on PSA progression in men with prostate cancer—The UK NCRN Pomi-T study. Prostate Cancer Prostatic Dis. 2014, 17, 180–186. [Google Scholar]
  49. Anhê, F.F.; Desjardinsb, Y.; Pilona, G.; Dudonnéb, S.; Genovesec, M.I.; Lajoloc, F.M.; Marettea, A. Polyphenols and type 2 diabetes: A prospective review. Pharma Nutr. 2013, 1, 105–114. [Google Scholar]
  50. Daglia, M. Polyphenolsas antimicrobial agents. Curr. Opin. Biotechnol. 2013, 23, 174–181. [Google Scholar]
  51. Queipo-Ortuño, M.I.; Boto-Ordóñez, M.; Murri, M.; Gomez-Zumaquero, J.M.; Clemente-Postigo, M.; Estruch, R.; Cardona-Diaz, F.; Andrés-Lacueva, C.; Tinahones, F.J. Influence of red wine polyphenols and ethanol on the gut microbiota ecology and biochemical biomarkers. Am. J. Clin. Nutr. 2012, 95, 1323–1334. [Google Scholar]
  52. Tuohy, K.M.; Conterno, L.; Gasperotti, M.; Viola, R. Up-regulating the human intestinal microbiome using whole plant foods, polyphenols, and/or fiber. J. Agric. Food Chem. 2012, 61, 8776–8782. [Google Scholar]
  53. Etxeberria, U.; Fernández-Quintela, A.; Milagro, F.I.; Aguirre, L.; Martínez, J.A.; Portillo, M. Impact of polyphenols and polyphenol-rich dietary sources on gut microbiota composition. J. Agric. Food Chem. 2013, 61, 9517–9533. [Google Scholar]
  54. He, X.; Marco, M.L.; Slupsky, C.M. Emerging aspects of food and nutrition on gut microbiota. J. Agric. Food Chem. 2013, 61, 9559–9574. [Google Scholar]
  55. Liu, Z.; Nakano, H. Antibacterial activity of spice extracts against food related bacteria. J. Fac. Appl. Biol. Sci. 1996, 35, 181–190. [Google Scholar]
  56. Akhondzadeh, S.; Noroozian, M.; Mohammadi, M.; Ohadinia, S.; Jamshidi, A.H.; Khani, M. Salvia officinalis extract in the treatment of patients with mild to moderate Alzheimer’s disease: A double blind randomized and placebo controlled trial. J. Clin. Pharm. Ther. 2003, 28, 53–59. [Google Scholar]
  57. Dragland, S.; Senoo, H.; Wake, K.; Holte, K.; Blomhoff, R. Several culinary and medicinal herbs are important sources of dietary antioxidants. J. Nutr. 2003, 133, 1286–1290. [Google Scholar]
  58. Halvorsen, B.L.; Carlsen, M.H.; Phillipis, K.M.; Bøhn, S.K.; Jacobs, D.R.; Blomhoff, J.R. Content of redox-active compounds (i.e., antioxidants) in foods consumed in the United States. J. Clin. Nutr. 2006, 84, 95–135. [Google Scholar]
  59. Ozsoy-Sacan, O.; Yanardag, R.; Orak, H.; Ozgey, Y.; Yarat, A.; Tunali, T. Effects of parsley (Petroselinum crispum) extract versus glibornuride on the liver of streptozotocin-induced diabetic rats. J. Ethnopharmacol. 2006, 104, 175–181. [Google Scholar]
  60. Cheung, S.; Tai, J. Anti-proliferative and antioxidant properties of rosemary Rosmarinus officinalis. Oncol. Rep. 2007, 17, 1525–1531. [Google Scholar]
  61. Moreno, S.; Scheyer, T.; Romano, C.; Vojnov, A. Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radic. Res. 2006, 40, 223–231. [Google Scholar]
  62. Shan, B.; Cai, Y.; Brooks, J.; Corke, H. The in vitro antibacterial activity of dietary spice and medicinal herb extracts. Int. J. Food. Microbiol. 2007, 117, 112–119. [Google Scholar]
  63. Shukla, Y.; Singh, M. Cancer preventive properties of ginger: A brief review. Food Chem. Toxicol. 2007, 45, 683–690. [Google Scholar]
  64. Carlsen, M.H.; Halvorsen, B.L.; Holte, K.; Bohn, S.K.; Dragland, S.; Sampson, L.; Willey, C.; Senoo, H.; Umezono, Y.; Sanada, C.; et al. The total antioxidant content of more than 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr. J. 2010, 9, 3. [Google Scholar]
  65. Kwon, H.K.; Hwang, J.S.; Therefore, J.S.; Lee, C.G.; Sahoo, A.; Ryu, J.H.; Jeon, W.K.; Ko, B.S.; Im, C.R.; Lee, S.H.; et al. Cinnamon extract induces tumor cell death through inhibition of NF-κB and AP1. BMC Cancer 2010, 10, 392–402. [Google Scholar]
  66. Mueller, M.; Hobiger, S.; Jungbauer, A. Anti-inflammatory activity of extracts from fruits, herbs and spices. Food Chem. 2010, 122, 987–996. [Google Scholar]
  67. Van Breemen, R.B.; Tao, Y.; Li, W. Cyclooxygenase-2 inhibitors in ginger (Zingiber officinale). Fitoterapia 2011, 82, 38–43. [Google Scholar]
  68. Keshavarz, M.; Bidmeshkipour, A.; Mostafaie, A.; Monsouri, K.; Mohammadi-Motlagh, H.-R. Anti-tumor activity of Salvia officinalis is due to its anti-proliferative effects. Cell J. 2011, 12, 477–482. [Google Scholar]
  69. Karna, P.; Chagani, S.; Gundala, S.R.; Rida, P.C.G.; Asif, G.; Sharma, V.; Gupta, M.V.; Aneja, R. Benefits of whole ginger extract in prostate cancer. Br. J. Nutr. 2012, 107, 473–484. [Google Scholar]
  70. Baker, I.; Chohan, M.; Opara, E.I. Impact of cooking and digestion, in vitro, on the antioxidant capacity and anti-inflammatory activity of cinnamon, clove and nutmeg. Plant Foods Hum. Nutr. 2013, 68, 364–369. [Google Scholar]
  71. Chohan, M.; Naughton, D.P.; Jones, L.; Opara, E.I. An investigation of the relationship between the anti-inflammatory activity, polyphenolic content, and antioxidant activities of cooked and in vitro digested culinary herbs. Oxid. Med. Cell. Longev. 2012, 2012, 627843. [Google Scholar]
  72. Pellegrini, N.; Salvatore, S.; Valtueña, S.; Bedogni, G.; Porrini, M.; Pala, V.; del Rio, D.; Sieri, S.; Miglio, C.; Krogh, V.; et al. Development and validation of a food frequency questionnaire for the assessment of dietary total antioxidant capacity. J. Nutr. 2007, 137, 93–98. [Google Scholar]
  73. Choi, Y.; Lee, S.M.; Chun, J.; Lee, H.B.; Lee, J. Influence of heat treatment on the antioxidant activities and polyphenolic compounds of Shiitake (Lentinus edodes) mushroom. Food Chem. 2006, 99, 381–387. [Google Scholar]
  74. Kim, S.; Jeong, S.; Park, W.; Nam, K.C.; Ahn, D.U.; Lee, S. Effect of heating conditions of grape seeds on the antioxidant activity of grape seed extracts. Food Chem. 2006, 97, 472–479. [Google Scholar]
  75. Nicoli, M.C.; Anese, M.; Parpinel, M.T.; Franceschi, S.; Lericia, C.R. Loss and/or formation of antioxidants during food processing and storage. Cancer Lett. 1997, 114, 71–74. [Google Scholar]
  76. Morales, F.J.; Jiménez-Pérez, S. Free radical scavenging capacity of Maillard reaction products as related to color and fluorescence. Food Chem. 2001, 72, 119–125. [Google Scholar]
  77. Chohan, M. The Impact of Digestion and Gut Bioavailability, in Vitro, on the Polyphenolic Associated Activity of Cooked Culinary Herbs. Ph.D. Thesis, Thesis, Kingston University, Kingston upon Thames, UK, 2011. [Google Scholar]
  78. Phipps, S.M.; Sharaf, M.H.M.; Butterweck, V. Assessing antioxidant activity in botanicals and other dietary supplements. Pharmacop. Forum 2007, 33, 810–814. [Google Scholar]
  79. Khatun, M.; Eguchi, S.; Yamahuchi, T.; Takamura, H.; Matoba, T. Effect of thermal treatment on radical-scavenging activity of some spices. Food Sci. Technol. Res. 2006, 12, 178–185. [Google Scholar]
  80. Patil, S.B.; Ghadyale, V.A.; Taklikar, S.S.; Kulkarni, C.R.; Arvinder, A.U. Insulin secretagogue, α-glucosidase and antioxidant activity of some selected spices in streptozotocin-induced diabetic rats. Plant Foods Hum. Nutr. 2011, 66, 85–90. [Google Scholar]
  81. Miglio, C.; Chiavaro, E.; Visconti, A.; Fogliano, V.; Pellegrini, N. Effects of different cooking methods on nutritional and physicochemical characteristics of selected vegetables. J. Agric. Food Chem. 2008, 56, 139–147. [Google Scholar]
  82. Mulinacci, N.; Ieri, F.; Giaccherini, C.; Innocenti, M.; Andrenelli, L.; Canova, G.; Saracchi, M.; Casiraghi, M.C. Effects of cooking on the anthocyanins, phenolic acids, glycoalkaloids, and resistant starch content in two pigmented cultivars of Solanum tuberrosum L. J. Agric. Food Chem. 2009, 56, 11830–11837. [Google Scholar]
  83. Pellegrini, N.; Chiavaro, E.; Gardana, C.; Mazzeo, T.; Contino, D.; Gallo, M.; Riso, P.; Fogliano, V.; Porrini, M. Effect of different cooking methods on color, phytochemical concentration, and antioxidant capacity of raw and frozen brassica vegetables. J. Agric. Food Chem. 2010, 58, 4310–4321. [Google Scholar]
  84. Cilla, A.; González-Sarrías, A.; Tomás-Barberán, F.A.; Espín, J.C.; Barberá, R. Availability of polyphenols in fruit beverages subjected to in vitro gastrointestinal digestion and their effects on proliferation, cell-cycle and apoptosis in human colon cancer Caco-2 cells. Food Chem. 2009, 114, 813–820. [Google Scholar]
  85. Gião, M.S.; Gomes, S.; Madureira, A.R.; Faria, A.; Pestana, D.; Calhau, C.; Pintado, M.E.; Azevedo, I.; Malcata, X. Effect of in vitro digestion upon the antioxidant capacity of aqueous extracts of Agrimonia eupatoria, Rubus idaeus, Salvia sp. and Satureja Montana. Food Chem. 2012, 131, 761–767. [Google Scholar]
  86. Henning, S.M.; Zhang, Y.; Rontoyanni, V.G.; Huang, J.; Lee, R.-P.; Trang, A.; Nuernberger, G.; Heber, D. Variability in the antioxidant activity of dietary supplements from pomegranate, milk thistle, green tea, grape seed, goji, and acai: Effects of in vitro digestion. J. Agric. Food Chem. 2014, 62, 4313–4321. [Google Scholar]
  87. Minekus, M.; Alminger, M.; Alvito, P.; Balance, S.; Bohn, T.; Bourlieu, C.; Carrière, F.; Boutrou, R.; Corredig, M.; Dupont, D.; et al. A standardized static in vitro digestion method suitable for food—An international consensus. Food Funct. 2014, 5, 1113–1124. [Google Scholar]
  88. Luis, J.C.; Johnson, C.B. Seasonal variations of rosmarinic acid and carnosic acid in rosemary extracts. Analysis of their in vitro antiradical activity. Span J. Agric. Res. 2005, 3, 106–112. [Google Scholar]
  89. Cocchiara, J.; Letizia, C.S.; Lalko, J.; Lapczynski, A.; Api, A.M. Fragrance material review on cinnamaldehyde. Food Chem. Toxicol. 2005, 43, 867–923. [Google Scholar]
  90. Guo, J.; Huo, H.; Zhao, B.; Liu, H.; Li, L.; Ma, Y.; Guo, S.; Jiang, T. Cinnamaldehyde reduces IL-1β-induced cyclooxygenase-2 activity in rat cerebral microvascular endothelial cells. Eur. J. Pharmacol. 2005, 537, 174–180. [Google Scholar]
  91. Yoon, J.H.; Baek, S.J. Molecular targets of dietary polyphenols with anti-inflammatory properties. Yonsei Med. J. 2005, 46, 585–596. [Google Scholar]
  92. Osakabe, N.; Yasuda, A.; Natsume, M.; Yoshikama, T. Rosmarinic acid inhibits epidermal inflammatory responses: Anticarcenogenic effect of Perilla frutescens extracts in the murine two-stage skin model. Carcinogenesis 2004, 25, 549–557. [Google Scholar]
  93. Dhandapani, K.M.; Mahesh, V.B.; Brann, D.W. Curcumin suppresses AP-1 and NF-κB transcription factors. J. Neurochem. 2007, 102, 522–538. [Google Scholar]
  94. Kim, S.S.; Oh, O.; Min, H.; Park, E.; Kim, Y.; Park, H.; Han, Y.N.; Lee, S.K. Eugenol suppresses cyclooxygenase-2 expression in liposaccharide-stimulated mouse macrophage RAW264.7 cells. Life Sci. 2003, 73, 337–348. [Google Scholar]
  95. Pan, M.H.; Lai, C.S.; Ho, C.T. Anti-inflammatory activity of natural dietary flavonoids. Food Funct. 2010, 1, 15–31. [Google Scholar]
  96. Yoo, K.M.; Lee, C.H.; Lee, H.; Moon, B.; Lee, C.Y. Relative antioxidant and cryoprotective activities of common herbs. Food Chem. 2008, 106, 929–936. [Google Scholar]
  97. Yasui, K.; Baba, A. Therapeutic potential of superoxide dismutase for resolution of inflammation. Inflamm. Res. 2006, 55, 359–363. [Google Scholar]
  98. Chohan, M.; Naughton, D.P.; Opara, E.I. Determination of superoxide dismutase mimetic activity in common culinary herbs. SpringerPlus 2014, 3, 578. [Google Scholar]
  99. Hunaefi, D.; Smetanska, I. The effect of tea fermentation on rosmarinic acid and antioxidant properties using selected in vitro sprout culture of Orthosiphon aristatus as a model study. SpringerPlus 2013, 2, 167. [Google Scholar]
  100. D’Archivio, M.; Filesi, C.; Varì, R.; Scazzocchio, B.; Masella, R. Bioavailability of the polyphenols: Status and controversies. Int. J. Mol. Sci. 2010, 11, 1321–1342. [Google Scholar]
  101. Chohan, M.; Naughton, D.P.; Jones, L.; Opara, E.I. The impact of digestion and absorption on the antioxidant capacities and polyphenol concentrations of a selection of cooked culinary herbs. Polyphenols communications. Salamanca, Spain, July 2008; 695–695. [Google Scholar]
  102. Pinto, M.; Robineloeon, S.; Appay, M.D.; Kedinger, M.; Triadou, N.; Dussaulx, E.; Lacroix, B.; Simonassmann, P.; Haffen, K.; Fogh, J.; et al. Enterocyte-like differentiation and polarization of the human colon carcinoma cell-line (Caco-2) in culture. Biol. Cell 1983, 47, 323–330. [Google Scholar]
  103. Mc Clement, J.; Decker, E.A. Designing Functional Foods; Woodhead Publishing Ltd.: Cambridge, UK, 2009; p. 347. [Google Scholar]
  104. Lee, H.J.; Cha, K.H.; Kim, C.Y.; Nho, C.W.; Pan, C.H. Bioavailability of hydroxycinnamic acids from Crepidiastrum denticulatum using simulated digestion and Caco-2 intestinal cells. J. Agric. Food Chem. 2014, 62, 5290–5295. [Google Scholar]
  105. Wang, W.; Heideman, L.; Chung, C.S.; Pelling, J.C.; Koehler, K.J.; Birt, D.F. Cell-cycle arrest at G2/M and growth inhibition byapigeninin human colon carcinoma cell lines. Mol. Carcinog. 2000, 28, 102–110. [Google Scholar]
  106. Aggarwal, B.B.; Shishodia, S.; Sandur, S.K.; Pandey, M.K.; Sethi, G. Inflammation and cancer: How hot is the link? Biochem. Pharmacol. 2006, 72, 1605–1621. [Google Scholar]
  107. Ramos, S. Cancer chemoprevention and chemotherapy: Dietary polyphenols and signaling pathways. Mol. Nutr. Food Res. 2008, 52, 507–526. [Google Scholar]
  108. Xavier, C.P.; Lima, C.F.; Fernandes-Ferreira, M.; Pereira-Wilson, C. Salvia fruticosa, Salvia officinalis, and rosmarinic acid induce apoptosis and inhibit proliferation of human colorectal cell lines: The role in MAPK/ERK pathway. Nutr. Cancer 2009, 61, 564–571. [Google Scholar]
  109. Araújo, J.R.; Gonçalves, P.; Martel, F. Chemopreventive effect of dietary polyphenols in colorectal cancer cell lines. Nutr. Res. 2011, 31, 77–87. [Google Scholar]
  110. Carroll, R.E.; Benya, R.V.; Turgeon, D.K.; Vareed, S.; Neuman, M.; Rodriguez, L.; Kakarala, M.; Carpenter, P.M.; McLaren, C.; Meyskens, F.L., Jr.; et al. Phase IIa clinical trial of curcumin for the prevention of colorectal neoplasia. Cancer Prev. Res. 2011, 4, 354–364. [Google Scholar]
  111. Aggarwal, B.B.; Prasad, S.; Yadav, V.R.; Park, B.; Kim, J.I.; Gupta, S.C.; Yoon, S.W.; Lavasanifar, A.; Sung, B. Targeting inflammatory pathways by dietary agents for prevention and therapy of cancer. J. Food Drug Anal. 2012, 20, 213–236. [Google Scholar]
  112. Macdonald, R.S.; Wagner, K. Influence of dietary phytochemicals and microbiota on colon cancer risk. J. Agric. Food Chem. 2012, 60, 6728–6735. [Google Scholar]
  113. García-Pérez, E.; Noratto, G.D.; García-Lara, S.; Gutiérrez-Uribe, J.A.; Mertens-Talcott, S.U. Micropropagation effect on the anti-carcinogenic activitiy of polyphenolics from Mexican oregano (Poliomintha glabrescens Gray) in human colon cancer cells HT-29. Plant Foods Hum. Nutr. 2013, 68, 155–162. [Google Scholar]
  114. Haraguchi, T.; Kayashima, T.; Okazaki, Y.; Inoue, J.; Mineo, S.; Matsubara, K.; Sakaguchi, E.; Yanaka, N.; Kato, N. Cecal succinate elevated by some dietary polyphenols may inhibit colon cancer cell proliferation and angiogenesis. J. Agric. Food Chem. 2014, 62, 5589–5594. [Google Scholar]
  115. Dempe, J.S.; Scheerle, R.K.; Pfeiffer, E.; Metzler, M. Metabolism and permeability of curcumin in cultured Caco-2 cells. Mol. Nutr. Food Res. 2013, 57, 1543–1549. [Google Scholar]
  116. Jenner, A.M.; Rafter, J.; Halliwell, B. Human fecal water content of phenolics: The extent of colonic exposure to aromatic compounds. Free Radic. Biol. Med. 2004, 38, 763–772. [Google Scholar]
  117. Dall’Asta, M.; Calani, L.; Tedeschi, M.; Jechiu, L.; Brighenti, F.; del Rio, D. Identification of microbial metabolites derived from in vitro fecal fermentation of different polyphenolic food sources. Nutrition 2012, 28, 197–203. [Google Scholar]
  118. Bermúdez-Soto, M.J.; Larrosa, M.; García-Cantalejo, J.; Espín, J.C.; Tomás-Barberan, F.A.; García-Conesa, M.T. Transcriptional changes in human Caco-2 colon cancer cells following exposure to a recurrent non-toxic dose of polyphenol-rich chokeberry juice. Genes Nutr. 2007, 2, 111–113. [Google Scholar]
  119. Bermúdez-Soto, M.J.; Larrosa, M.; Garcia-Cantalejo, J.M.; Espín, J.C.; Tomás-Barberan, F.A.; García-Conesa, M.T. Up-regulation of tumor suppressor carcinoembryonic antigen-related cell adhesion molecule 1 in human colon cancer Caco-2 cells following repetitive exposure to dietary levels of a polyphenol-rich chokeberry juice. J. Nutr. Biochem. 2007, 18, 259–271. [Google Scholar]
  120. Jacobs, D.R.; Gross, M.D.; Tapsell, L.C. Food synergy: An operational concept for understanding nutrition. Am. J. Clin. Nutr. 2009, 89, 1543S–1548S. [Google Scholar]
  121. Jacobs, D.R.; Tapsell, L.C.; Temple, N.J. Food synergy: The key to balancing the nutrition research effort. Public Health Rev. 2012, 33, 507–529. [Google Scholar]
  122. Jacobs, D.R.; Tapsell, L.C. Food synergy: The key to a healthy diet. Proc. Nutr. Soc. 2013, 72, 200–206. [Google Scholar]
  123. De Kok, T.M.; van Breda, S.G.; Manson, M.M. Mechanisms of combined action of different chemopreventive dietary compounds: A review. Eur. J. Nutr. 2008, 47, 51–59. [Google Scholar]
  124. Somers-Edgar, T.J.; Scandlyn, M.J.; Stuart, E.C.; le Nedelec, M.J.; Valentine, S.P.; Rosengren, R.J. The combination of epigallocatechin gallate and curcumin suppresses ERα-breast cancer cell growth in vitro and in vivo. Int. J. Cancer 2008, 122, 1966–1971. [Google Scholar]
  125. Majumdar, A.P.N.; Banerjee, S.; Nautiyal, J.; Patel, B.B.; Patel, V.; Du, J.; Yu, Y.; Elliot, A.A.; Levi, E.; Sarkar, F. Curcumin synergizes with resveratrol to inhibit colon cancer. Nutr. Cancer 2009, 61, 544–553. [Google Scholar]
  126. Pesakhov, S.; Khanin, M.; Studzinski, G.P.; Danilenko, D. Distinct combinatorial effects of the plant polyphenols curcumin, carnosic acid and silibinin on proliferation and apoptosis in acute myeloid leukemia cells. Nutr. Cancer 2010, 62, 811–824. [Google Scholar]
  127. Thomas, R.H.; Bernards, M.A.; Drake, E.E.; Guglielmo, C.G. Changes in the antioxidant activities of seven herb and spice-based marinating sauces after cooking. J. Food Compos. Anal. 2010, 23, 244–252. [Google Scholar]
  128. Li, Z.; Henning, S.M.; Zhang, Y.; Zerlin, A.; Li, L.; Gao, K.; Lee, R.-P.; Karp, H.; Thames, G.; Bowerman, S.; et al. Antioxidant-rich spice added to hamburger meat during cooking results in reduced meat, plasma, and urine malondialdehyde concentrations. Am. J. Clin. Nutr. 2010, 91, 1180–1184. [Google Scholar]
  129. Blasa, M.; Angelino, D.; Gennari, L.; Ninfali, P. The cellular antioxidant activity in red blood cells (CAA-RBC): A new approach to bioavailability and synergy of phytochemicals and botanical extracts. Food Chem. 2011, 125, 685–691. [Google Scholar]
  130. Khanum, H.; Ramalakshmi, K.; Srinivas, P.; Borse, B.B. Synergistic antioxidant action of oregano, ajowan and borage extracts. Food Nutr. Sci. 2011, 2, 387–392. [Google Scholar]
  131. Yi, W.; Wetzstein, H.Y. Anti-tumorigenic activity of five culinary and medicinal herbs grown under greenhouse conditions and their combination effects. J. Sci. Food Agric. 2011, 91, 1849–1854. [Google Scholar]
  132. Epps, C.T.; Stequist, B.P.; Lowder, K.T.; Blacker, B.C.; Low, R.M.; Egget, D.L.; Parker, T.L. Synergistic endo- and exo-interactions between blueberry phenolic compounds, grape variety fractions, chocolate covered strawberries, and fruit smoothies. J. Food Res. 2013, 2, 33–47. [Google Scholar]
  133. Williamson, E.M. Synergy and other interactions in phytomedicines. Phytomedicine 2001, 8, 401–409. [Google Scholar]
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