Glucosinolates in Brassica foods: bioavailability in food and significance for human health

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1 Phytochem Rev (2008) 7: DOI /s Glucosinolates in Brassica foods: bioavailability in food and significance for human health María Elena Cartea Æ Pablo Velasco Received: 11 June 2007 / Accepted: 21 September 2007 / Published online: 20 October 2007 Ó Springer Science+Business Media B.V Abstract Glucosinolates are sulphur compounds that are prevalent in Brassica genus. This includes crops cultivated as vegetables, spices and sources of oil. Since 1970s glucosinolates and their breakdown products, have been widely studied by their beneficial and prejudicial biological effects on human and animal nutrition. They have also been found to be partly responsible for the characteristic flavor of Brassica vegetables. In recent years, considerable attention has been paid to cancer prevention by means of natural products. The cancer-protective properties of Brassica intake are mediated through glucosinolates. Isothyocianate and indole products formed from glucosinolates may regulate cancer cell development by regulating target enzymes, controlling apoptosis and blocking the cell cycle. Nevertheless, variation in content of both glucosinolates and their bioactive hydrolysis products depends on both genetics and the environment, including crop management practices, harvest and storage, processing and meal preparation. Here, we review the significance of glucosinolates as source of bioactive isothiocyanates for human nutrition and M. E. Cartea (&) P. Velasco Department of Plant Genetics, Misión Biológica de Galicia, Spanish Council for Scientific Research (CSIC), Apartado 28, Pontevedra, Spain ecartea@mbg.cesga.es P. Velasco pvelasco@mbg.cesga.es health and the influence of environmental conditions and processing mechanisms on the content of glucosinolate concentration in Brassica vegetables. Currently, this area is only partially understood. Further research is needed to understand the mechanisms by which the environment and processing affect glucosinolates content of Brassica vegetables. This will allow us to know the genetic control of these variables, what will result in the development of high quality Brassica products with a healthpromoting activity. Keywords Brassica Bioactive compounds Chemoprevention Isothiocyanates Sulforaphane Indole-3-carbinol Seasonal variation Thermal degradation Introduction Brassicaceae family includes vegetables as broccoli, Brussels sprouts, cabbage, collards, kale, turnip greens or leaf rape. They are commonly grown and consumed worldwide. Among these, broccoli intake and cancer prevention research have been widely studied, having multiple references related to different types of cancers in scientific literature. This fact is due to the presence of a type of bioactive components: glucosinolates. Glucosinolates are the major class of secondary metabolites found in Brassica crops. The molecule comprises a b-thioglucoside

2 214 Phytochem Rev (2008) 7: N-hydroxysulphate, containing a side chain and a b-d-glucopyranose moiety. Glucosinolates can be grouped into three chemical classes: aliphatic, indole and aromatic, according to whether their amino acid precursor is methionine, tryptophan or an aromatic amino acid (tyrosine or phenylalanine), respectively (Giamoustaris and Mithen 1996). The most important glucosinolates found in Brassica vegetables are methionine-derived glucosinolates (Mithen et al. 2003). However, several glucosinolates belonging to the three chemical classes have been identified in the edible parts of Brassica crops. The first observations on the unique properties of glucosinolates and isothiocyanates were recorded at the beginning of the 17th century as a result of the study on the chemical origin of the sharp taste of mustard seeds (Fahey et al. 2001). Glucosinolates known as sinigrin (2-propenyl) and sinalbin (4-hydroxybenzyl) were isolated early in the 1830s from black (Brassica nigra) and white (Sinapis alba) mustard seeds, respectively. In 1956, Ettlinger and Lundeen (1956) proposed the correct structure of glucosinolates and they described the first chemical glucosinolate synthesis (Fahey et al. 2001). Although approximately 120 classes of glucosinolates have been identified in plants, each plant species contains up to four different glucosinolates in significant amounts (Fahey et al. 2001). Glucosinolates are not bioactive until they have been enzymatically hydrolysed to various bioactive breakdown products by the endogenous plant enzyme myrosinase (thioglucoside glucohydrolase, E.C ). These breakdown products include isothiocyanates, nitriles, thiocyanates, epithionitriles, oxazolidine-2-thiones, and epithioalkanes (Grubb and Abel 2006) depending on the substrate, ph conditions, availability of ferrous ions and the level and activity of specific protein factors such as the epithiospecifier protein (ESP). At physiological ph, isothiocyanates are the major products, whereas nitriles are formed at more acid ph (Halkier and Du 1997). Comparative studies of glucosinolate profiles indicate significant differences among cruciferous crops (VanEtten et al. 1976; Carlson et al. 1987; Kushad et al. 1999; Ciska et al. 2000). Apart from glucosinolate profile, large differences in the levels of both aliphatic and indole glucosinolates have been observed in Brassica plants, presumably due to the use of different varieties, analytical methods and growing conditions. Moreover, the chemical structure and glucosinolate concentrations in cruciferous plants vary considerably, depending on the stage of development, tissue type and environmental conditions (Velasco et al. 2007). Several published studies have described the glucosinolate composition of different vegetable Brassica species and these have been reviewed extensively (see Table 1). Fenwick et al (1983a) provide a comprehensive review on the glucosinolate content of crop plants, and more recently, Rosa et al. (1997) and Rosa (1999) reported the glucosinolate content of different Brassica vegetables. Each type of cruciferous vegetables shows a characteristic glucosinolates profile, differing substantially, even though they are all part of the same species (Fenwick et al. 1983a; Kushad et al. 1999). In B. oleracea, there is a considerable variation in glucosinolate structure and in the total amount of glucosinolates. All the different B. oleracea types contain glucobrassicin (3-indolylmethyl) and glucoiberin (3-methylsulfinilpropyl) and most contain substantial amounts of sinigrin. For example, sinigrin, glucobrassicin and glucoiberin have been identified as the major glucosinolates in kales and cabbages. Sinigrin makes the major contribution of glucosinolates to kales, while glucobrassicin or glucoiberin do so to cabbage leaves (Cartea et al. 2007b). In broccoli, common glucosinolates are glucoraphanin (4-methylsulfinylbutyl), sinigrin, progoitrin (2-hydroxy-3-butenyl), gluconapin (3-butenyl) and the indole glucosinolates glucobrassicin and neoglucobrassicin (1-methoxy- 3-indolylmethyl) (Kushad et al. 1999). The predominant glucosinolate is glucoraphanin (making up more than 50% of the total glucosinolates), being sinigrin levels comparatively low. In Brussels sprouts, collard and cauliflower, the predominant glucosinolates are sinigrin, progoitrin and glucobrassicin (VanEtten et al. 1976; Carlson et al. 1987; Kushad et al. 1999). Each of these vegetables also contains smaller amounts of other glucosinolates (Table 1). In contrast to this glucosinolate variation within B. oleracea species, there is a relatively little variation in glucosinolate structure of B. rapa crops. Chinese cabbage accumulates gluconapin and glucobrassicanapin (4-pentenyl) and their hydroxylated forms, progoitrin and gluconapoleiferin (2-hydroxy- 4-pentenyl), respectively. In turnip roots, the

3 Phytochem Rev (2008) 7: Table 1 Principal glucosinolates identified in leaves of Brassica vegetable crops Crop Aliphatic glucosinolates Indole glucosinolates Aromatic GIB PRO SIN GAL GRA GNA GBN GIV GER GNL GBS NGBS 4HGBS 4MGBS GST Brassica oleracea White cabbage a,b,c,d Savoy cabbage a,b,c,d Red cabbage a,c,d Kale a,c,d,e Collard e Tronchuda cabbage c,f Broccoli e,g Brussels sprouts d,e,g Cauliflower d,g Kohlrabi d Brassica rapa Turnip b Turnip greens h Turnip tops i Chinese cabbage b Brassica napus Swede b Leaf rape j Major glucosinolates found in each crop are shown in bold GIB: glucoiberin (3-methylsulfinylpropyl); PRO: progoitrin (2-hydroxy-3-butenyl); SIN: sinigrin (2-propenyl); GAL: glucoalysiin (5-methylsulphinylpentyl); GRA: glucoraphanin (4-methylsulphinylbutyl); GNA: gluconapin (3-butenyl); GBN: glucobrassicanapin (4-pentenyl); GIV: Glucoiberverin (3-methylthiopropyl); GER: glucoerucin (4-methylthiobutyl); GNL: gluconapoleiferin (2-hydroxy-4-pentenyl); GBS: glucobrassicin (3-indolylmethyl); NGBS: neoglucobrassicin (1-methoxy-3-indolylmethyl); 4HGBS: 4-hydroxyglucobrassicin (4-hydroxy-3-indolylmethyl); 4MGBS: 4-methoxyglucobrassicin (4-methoxy-3-indolylmethyl), GST: Gluconasturtiin (2-phenylethyl) Sources VanEtten et al. (1980) b Sones et al. (1984) c Cartea et al. (2007b) d Ciska et al. (2000) e Carlson et al. (1987) f Rosa et al. (1996) g Kushad et al. (1999) h Padilla et al. (2007) i j Rosa (1997) Cartea et al. (2007a) predominant glucosinolates found by Sones et al (1984) were progoitrin and gluconasturtiin (2-phenylethyl), while gluconapin and glucobrassicanapin have been identified as the most abundant glucosinolates in the edible parts of turnip greens (Kim et al. 2003; Padilla et al. 2007) and turnip tops (Rosa 1997). Vegetable crops of B. napus include leaf rape and swedes. Cartea et al. (2007a) found that glucobrassicanapin followed by progoitrin and gluconapin proved to be the most abundant glucosinolates in a variety of leaf rape called nabicol. In swedes, glucobrassicin, progoitrin and gluconasturtiin have

4 216 Phytochem Rev (2008) 7: been found as the major glucosinolates (Carlson et al. 1987). As components of feed and food, some abovementioned glucosinolates as source of bioactive compounds (i.e., isothiocyanates, thiocyanates, nitriles and epithionitriles) have been recognized for long for their distinctive benefits to human nutrition and plant defence. This feature has lead to consider Brassica foods as possible functional foods. The term functional foods describes foods that, if they are normal dietary constituents, can provide sufficient amounts of bioactive components that are valuable for health improvement. In order to acquire the full benefit of functional foods, it is necessary to know the natural variation in content of bioactive food components (Dekker and Verkerk 2003). Such variation might be regulated genetically or it might result from changes in the growing environment or from differences in post-harvest handling, processing, storage or food preparation. Here, we review the significance of glucosinolates as bioactive compounds for human nutrition and health and the influence of environmental conditions, processing, and storage on glucosinolate concentration in Brassica vegetables. Human nutrition and anticarcinogenic activity Different epidemiological studies have indicated that diet and cancers are closely interlinked. Over the past 30 years, various studies showed that fruits and vegetables contain natural phytochemicals such as glucosinolates that have anticarcinogenic properties (Block et al. 1992; Talalay and Zhang 1996; Hecht 2000; Talalay and Fahey 2001; Anilakumar et al. 2006). Consequently, cruciferous vegetables have been very interesting in the last years for their potential use in cancer chemoprevention (Rosa et al. 1997; Farnham et al. 2004; Smith et al. 2005). Results have consistently shown that the chemoprotective agents derived from this class of vegetables of the Cruciferae family have an influence on carcinogenesis during the initiation and promotion phases of cancer development. Similarly, reports from epidemiological studies and clinical trials support this notion. Isothiocyanates and indoles are two major groups of autolytic breakdown products of glucosinolates. Both of them exhibit protective activities against many types of cancer. In vitro and in vivo studies have reported that these compounds affect many stages of cancer development, including the induction of detoxification enzymes (Phase II enzymes) and the inhibition of activation enzymes (Phase I enzymes) (Zhang and Talalay 1994; Hecht 2000; Fahey et al. 2002; Anilakumar et al. 2006). Phase II enzymes such as quinone reductase, glutathione-s-tranferase, UDP-glucuronyl transferase and NADPH reductase are able to conjugate with activated carcinogens and turn them into inactive water soluble compounds. They can be excreted through the urine, what results in the neutralisation of potential carcinogens from mammalian cells. Inductions of Phase II cellular enzymes are largely mediated by the antioxidant responsive element (ARE), which is regulated by the transcriptional factor, Nrf2. The most powerful inducers of the Phase II enzymes are the isothiocyanates sulforaphane, iberin and erucin, which are the hydrolysis products of glucoraphanin, glucoiberin, and glucoerucin (4-metylthiobutyl), respectively (Nilsson et al. 2006). Another mechanism for glucosinolate breakdown products requires the inhibition of the enzymes involved in cancer induction. Phase I enzymes are responsible for in vivo and in vitro metabolic activation of most carcinogens in human and animal cells. Under certain conditions, products of Phase I enzymes (cytochrome P450 enzymes) serve as substrates for Phase II enzymes, which turn them into electrophilic carcinogens that can be eliminated by the kidney (Talalay and Zhang 1996). Cytochrome P450 enzymes are a battery of Phase I enzymes. It has been shown that they activate metabolically chemical carcinogens such as nitrosamines and aflatoxins. In addition to the modulation of Phase I and Phase II enzymes, apoptosis and cell cycle perturbations appear to be yet other potential chemopreventive mechanisms due to isothiocyanates, especially with respect to the effects on initiated tumor cells (Mithen et al. 2000). Glucosinolates and their breakdown products may regulate cancer cell development by blocking the cell cycle and promoting apoptosis (Mithen et al. 2003; Lund 2003). Apoptosis or programmed cell death is the genetically encoded destruction of an active cell, what reduces tumor invasion and metastasis. Moreover, it has been shown that glucosinolate breakdown products prevent and/or suppress estrogen-dependent cancers, such as cervical and breast, in both animal and

5 Phytochem Rev (2008) 7: human cells by blocking the estrogen receptor function (Keum et al. 2004). Aliphatic glucosinolates A great deal of research on functional foods like anticarcinogens has focused on broccoli and on a single bioactive component within broccoli, which is called sulforaphane (Zhang et al. 1992; Fahey et al. 1994; Talalay and Zhang 1996; Fahey et al. 2002), the isothiocyanates derived from its cognate glucosinolates glucoraphanin (Fig. 1). Initial interest in sulforaphane was due to its powerful ability to induce Phase II enzymes coupled with the inhibition of cytochrome P450 (Phase I enzyme) (Zhang and Talalay 1994; Talalay and Zhang 1996; Fahey et al. 1997). Moreover, sulforaphane serves as an indirect antioxidant and it induces cell cycle arrest and apoptosis. Rose et al (2005) studied an actively proliferating HT29 cell line established from human colon cancer and they identified sulforaphane as an inductor of cell cycle arrest followed by apoptosis. In a similar way, several studies have also stated the ability of sulforaphane to induce apoptosis in a range of cell lines including prostate, lymphocyte and mammary. Moreover, sulforaphane shows potential for treating Helicobacter pylori, which caused stomach cancer (Fahey et al. 2002). These results are motivating efforts to increase sulforaphane content of broccoli and to promote the health benefits of this vegetable. Currently, the evidence of health benefits from sulforaphane is strong enough to demand the development of broccoli sprouts with a uniform and high sulforaphane concentration. Although the most characterized isothiocyanate compound is sulforaphane, other isothiocyanates may also contribute to the anti-carcinogenic properties of crucifers. Glucosinolate hydrolysis products from glucoiberin, sinigrin and progoitrin have also been identified as suppressing agents, protecting human and animal cells against carcinogenesis. These glucosinolates may well exert comparable levels of biological activity to sulforaphane by either inducing Phase II detoxification enzymes or inhibiting Phase I enzymes (Fahey et al. 1997; Nilsson et al. 2006). Indole and aromatic glucosinolates Indole-3-carbinol, the degradation product of the indole glucosinolate glucobrassicin, and benzyl and Fig. 1 The most studied glucosinolates and their hydrolysis products implicated in human nutrition in each chemical class: (A) aliphatic, (B) aromatic, (C) indole

6 218 Phytochem Rev (2008) 7: phenethyl isothiocyanates, the degradation products of two aromatic glucosinolates, glucotropaeolin and gluconasturtiin, respectively, have been investigated for their potential as cancer chemoprotective agents (Fig.1). These compounds may be responsible for the selective induction of cancer cells to apoptosis, supporting the potential preventive and/or therapeutic benefit of the glucosinolate hydrolysis products against different type of cancers (Zhang and Talalay 1994; Fahey et al. 1997). Isothiocyanates formed from indole glucosinolates are unstable and they separate spontaneously into indole-3-carbinol. This compound may condense under the acid conditions of the stomach to form toxic compounds. Despite this toxicity, it has proved to be successful against breast cancer (Telang et al. 1997) and respiratory papilloma (Rosen et al. 1998). It has been shown that indole-3-carbinol elevates quinone reductase, glutathione transferase (Phase II detoxication enzymes) and CYP1A (a Phase I enzyme) contents and, in some cases, does so synergistically. However, the association between broccoli consumption, cancer risk and glutathione S-transferase genotype suggests that isothiocyanates may be more important than indole compounds in modulating risks. For more detailed action of this dual nature, see reviews by Fenwick et al. (1983a) and Rosa et al. (1997). Phenethyl isothiocyanate is the hydrolysis product of the glucosinolate gluconasturtiin. It is found at high levels in some minor crops such as watercress and radishes. This compound may inhibit Phase I enzymes which are related to the activation of carcinogens and it has been shown that this compound inhibits induction of lung and esophageal cancer in both rat and mouse tumor models. The effect of phenethyl isothiocyanate metabolites on human leukemia cells in vitro has been proved as well as its role to inhibit tobacco smoke-induced lung tumors in mice. Kuang and Chen (2004) have shown the effects of indole-3-carbinol, phenethyl isothiocyanate and benzyl isothiocyanate on the induction of apoptosis in human cell lung cancer. The results indicated that all compounds tested are able to inhibit the growth of A549 cells by inducing apoptosis at low concentrations and necrosis at high concentrations. Indole-3-carbinol showed an antiproliferative effect in A549 cells, but not through induction of apoptosis. A recent study by Rose et al. (2005) showed that extracts of broccoli and watercress inhibit the invasive potential of the human breast cancer cell line in vitro. This study also suggested that their phytochemical constituents, isothiocyanates, are a new kind of invasion inhibitors. Anti-nutritional effects The degradation products of some glucosinolates have been traditionally considered as damaging or prejudicial because of their goitrogenic and growth retardation activities. Their presence in the seeds of oilseed cruciferous crops reduces in a significant way the quality of the seed meal left after oil extraction. For these reasons, in the past 40-years glucosinolates have assumed major agricultural significance because of the increasing importance of rapeseed cultivars of B. napus, B. rapa, and B. juncea as oil crops in temperate and subtropical areas of the world. The most remarkable of the prejudicial degradation products is oxazolidine-2-thione, derived from progoitrin (Rosa et al. 1997). This glucosinolate is accumulated in the seeds of oilseed rape and it causes goiter and other harmful effects on animal nutrition, such as depressed growth, poor egg production and liver damage. However, there is no evidence of any goitrogenic effect on humans because of Brassica consumption (Mithen 2001) and an international study indicated no relationship between glucosinolate intake and the incidence of thyroid cancer. Goitrin is an inhibitor of thyroid peroxidase and it prevents iodide from oxidation into iodine for subsequent iodination of tyrosine residues in the biosynthesis of the thyroxines T3 and T4. Thiocyanate anions act as a competitive inhibitor of iodide, and thereby they prevent iodide uptake by the thyroid. In addition to the alterations in size, structure and function of the thyroid, it has been shown that goitrin can undergo nitrosation reactions which might have implications for human health where nitrate levels in water are high (Luthy et al. 1984). The precise cause of this is not fully understood, but it may be related either to the presence of intact glucosinolates or the production of nitriles in the digestive tract. Plant breeders have drastically reduced glucosinolate levels of the seed to allow the protein-rich seed

7 Phytochem Rev (2008) 7: cake (the residue left after crushing to obtain oil) to be sold as an animal feed supplement. Efforts to avoid the goitrogenicity of mustard/rapeseed oil cake led to the successful development of the oilseed crop Canola, which was developed in the 1970s by a plant-breeding program designed to develop cultivars of oilseed rape with low levels of glucosinolates and erucic acid. Canola seed contains about 40% of oil and this oil must contain less than 2% of erucic acid. The seed meal, which is used for feed animals after the oil extraction, must have less than 30 lmol of glucosinolates per gram of meal. In conclusion, the potential negative effects of glucosinolates require a further examination, as this topic has been scarcely researched in recent years. For more detailed treatment of the antinutritional nature of these compounds, see reviews by Fenwick et al. (1983a), Rosa et al. (1997), Griffiths et al. (1998) and Anilakumar et al. (2006). Sensorial and organoleptic effects Apart from the medicinal value of these sulfur compounds, glucosinolates are responsible for the characteristic flavour and odour of Brassica vegetables. Glucosinolate-derived isothiocyanates produce a pungent and bitter flavour and sulfurous aroma when the plant tissue is injured, playing a significant organoleptic role in Brassica products (Chong et al. 1982; Fenwick et al. 1983a; Rosa et al. 1997). However, the direct relation between glucosinolate content and sensory properties is complex. Literature describes a bitter effect mainly because of isothiocyanates formed from sinigrin, gluconapin and progoitrin, but also from glucobrassicin and neoglucobrassicin, but in different intensities. In contrast, alkyl glucosinolates as glucoerucin, glucoiberverin (3-methylthiopropyl), glucoiberin and glucoraphanin do not contribute to the attribute bitter. In Brussels sprouts, isothiocyanates derived from sinigrin and progoitrin have been related to bitterness (Fenwick et al. 1983b; Van Doorn et al. 1998) while in cooked cauliflower, neoglucobrassicin and sinigrin glucosinolates were found responsible for the bitter taste and, thereby, they were considered responsible for consumers acceptance (Engel et al. 2002; Schonhof et al. 2004). In cabbage, isothiocyanates derived from progoitrin and gluconasturtiin are pungent and very bitter compounds (Fenwick et al. 1983b; Rosa et al. 1997). In turnip greens, gluconapin and glucobrassicanapin have been described as flavour compounds (Rosa 1997; Padilla et al. 2007). A sensory profile of turnip greens, affected by variety and maturity, has been reported by Jones and Sanders (2002), who concluded that both sources had a significant effect on their sensory characteristics and preferences. Sensorial analysis comparing bitterness with variation in glucosinolate concentration suggests that these compounds and their breakdown products are not the only determinants of the characteristic flavour of Brassica vegetables (Hansen et al. 1997; Baik et al. 2003; Padilla et al. 2007). Bitter taste is probably a synergistic property of various phytochemicals, not just of hydrolysis products derived from some glucosinolates. Indole hydrolysis products, phenolic content or flavonoids could have some influence on organoleptic properties and on the bitter flavour, as it has already been reported (Drewnowski et al. 2001). Influence of environmental conditions on glucosinolate content Variation on the amount and pattern of glucosinolates has been attributed to genetic and environmental factors, including: Genetics Glucosinolate diversity varies widely in families and species, suggesting that diversification has accompanied speciation (Rosa et al. 1997). For this reason, glucosinolates have been used as chemical markers in chemotaxonomy. Glucosinolate levels of vegetative tissues and seeds vary regardless of each other. Therefore, they are probably controlled by different genetic and physiological mechanisms. Biosynthesis and genetics of glucosinolates have been the target of several comprehensive reviews (Giamoustaris and Mithen 1996; Rosa et al. 1997; Fahey et al. 2001; Halkier and Gershenzon 2006; Grubb and Abel, 2006). These features are not the focus of this review. Thereby, they will not be discussed in the next sections.

8 220 Phytochem Rev (2008) 7: Plant development There is a great variation in the profile and the amount of glucosinolates of Brassica species (Cartea et al. 2007a, b; Padilla et al. 2007). Besides, there is a great variation inside the plant depending on the plant development. In a variety of kale (B. oleracea acephala group), Velasco et al. (2007) detected an increasing concentration of aliphatic glucosinolates in leaves, from the early stage until the prebolting stage. Indole glucosinolates were increasing from the early stage to five months after sowing, and then they started to decrease (Fig. 2). This result agrees with Fieldsend and Milford (1994) who found that total glucosinolate and most of individual glucosinolate content in oilseed rape increased from vegetative to reproductive stages and maturity. Aliphatic and indole glucosinolates showed unlike variation throughout the plant development. The highest contents of all aliphatic glucosinolates, including sinigrin and glucoiberin, were noticed in flower buds, whilst the highest levels of indole glucosinolates, as glucobrassicin, and the aromatic glucosinolate levels were observed in leaves harvested at the optimum Concentration Aliphatic Indolic Aromatic 2 3 Plant stages Flower buds Leaves Flower buds Leaves Fig. 2 Mean concentration (lmol g 1 dw) for the three classes of glucosinolates through plant growth (form Velasco et al. 2007). Plant stages: (1): the initial plant stage before transplanting at the five or six leaves stage, 30 days after sowing (DAS); (2) the vegetative phase at the first optimum consumption stage, 90 DAS; (3) the vegetative phase at the second optimum consumption stage, 180 DAS; (4) the vegetative-reproductive phase transition, at the last consumption stage 300 DAS; (5) the reproductive phase before bolting, 390 DAS 4 5 consumption stage, 180 days after sowing (Booth et al. 1991; Velasco et al. 2007). Glucosinolate differences between plants and large changes in the types of glucosinolates that occur in vegetative and floral tissues during ontogeny, makes a comprehensive characterization of plant material necessary when sampling for analysis and consumption. Plant part Glucosinolate content depends on the plant part, and its levels in stems and petioles proved to be lower than those of roots and heads (Rosa et al. 1997). In general, seeds had the highest glucosinolate concentration, followed by leaves, roots and stems in B. napus (Velasco et al. submitted). In Arabidopsis, Brown et al. (2003) found that dormant and germinating seeds had the highest glucosinolate concentration ( % by dry weight) followed by inflorescences, siliques, leaves and roots. Environmental factors The synthesis and degradation of glucosinolates can happen in a wide range of climate conditions. Bible and Chong (1975) showed that climate can influence amounts of glucosinolates. They concluded that cold unit accumulation is the most reliable index of root radish glucosinolate content, regardless of soil and climate. Thiocyanate content was negatively correlated with mean daily air temperature on organic soil and positively correlated with rainfall. Velasco et al. (2007) found that temperature could have a positive effect on the glucosinolate concentration throughout the vegetative cycle of plants, as low temperatures caused a reduction on glucosinolate content. This was also established by Ciska et al. (2000), who found that a high average temperature increased in a significant way the glucosinolate content of different Brassica crops. Temperature was not the only environmental factor to take into account, since a lower average rainfall also increased glucosinolate content. In watercress plants, Engelen-Eigles et al. (2006) stated that the major environmental influence on gluconasturtiin content is daylength. In this sense, plants grown under long days contained a 30 40% higher gluconasturtiin concentration than plants

9 Phytochem Rev (2008) 7: grown under short days. But with the same daylength, plants grown under temperatures between 10 and 15 C had a 50% higher gluconasturtiin content, but a lower fresh weight than plants grown at C. These data suggested that gluconasturtiin content can be increased by growing plants under lowtemperature and long-day regimes. Besides, crop season has an effect on glucosinolate concentration. Winter or autumn seasons seem to lead to lower glucosinolate levels, due to short days, wetter conditions, cool temperatures and less radiation (Rosa and Heaney 1996; Rosa et al. 1997). Charron et al. (2005) found that total and indole glucosinolate concentrations in different groups of B. oleracea were significantly affected by the season, and they were generally higher in spring than in fall season. The effect of season was mainly explained by the average temperature, daylength and photosynthetic photon flux. Cartea et al. (2007b) confirmed this result since they found that local varieties of cabbage planted during the fall season had a 40% less of total glucosinolate than the same varieties planted during the spring season. This difference was mainly due to indole glucosinolates with a 55% less in fall season. Cultural practices: soil type and nutrients It has been said that different cultural practices affect glucosinolate content, specially plant irrigation and density. Closer spacing affects the morphology of the plant, i.e., by reduction of head size, increasing concentrations of glucosinolates (Rosa et al. 1997). In other plants like rapeseed, a higher density does not lead to an increase in glucosinolates concentration in leaves or seeds. Following Ju et al. (1980), the soil composition has an influence on glucosinolate content, with plants in organic soils having the highest total glucosinolate concentration. The addition of different nutrients to the soil has a different effect on glucosinolate content. For example, Brassica crops require more sulphur than most other crops due to its role in the synthesis of glucosinolates, as well as sulphur aminoacids and proteins (Rosa et al. 1997). Sulphur application increases the glucosinolate content in oilseed rape leaves and flowers (Booth et al. 1991). Nitrogen is also a constituent of the glucosinolate molecule, but different studies have shown that a high dose of nitrogen application tended to give lower glucosinolate levels. Kim et al. (2002) found that glucosinolate content from the edible parts of B. rapa is strongly affected by nitrogen and sulphur applications. This was also stated by Rosen et al. (2005) who showed that total glucosinolates and glucobrassicin content were maximized in cabbage cultivars grown at low nitrogen and high sulphur application rates. The environmental effect in the hydroxylation step that links gluconapin and progoitrin in the aliphatic pathway was reported by Zhao et al. (1994). They showed that sulphur deficiency reduces the aliphatic glucosinolate concentration and increasing nitrogen results in higher proportions of progoitrin, what suggests that the hydroxylation step is favoured. Influence of storage and processing on glucosinolate content The use of Brassica vegetables to improve human health and the interpretation of epidemiological data require an understanding of glucosinolate chemistry and metabolism across the whole food chain, from production and processing to the consumer. Glucosinolate and related isothiocyanate contents of Brassica vegetables are affected by methods of storage and food processing, e.g., cutting, chewing, cooking, fermenting or freezing (Song and Thornalley 2007). Nevertheless, given the importance of glucosinolates in terms of their anticarcinogenic activity, few thermal degradation studies have been carried out with regard to food processing. Most of the research has been done in crude extracts and information about the plant myrosinase stability throughout processing is limited. When vegetables are sliced and washed as part of processing, conditions for myrosinase activity are probably optimal. This enzyme is temperature-sensitive and consequently, throughout conventional thermal processing, it will be inactivated and it cannot transform glucosinolates into beneficial products. Thereby, it is important to maintain the levels of beneficial glucosinolates after harvest and to provide the correct way of cooking to ensure optimal health benefits. The effect of storage, processing and cooking methods on glucosinolate content has been studied in

10 222 Phytochem Rev (2008) 7: several Brassica vegetables as broccoli, Brussels sprouts, cauliflower and cabbage. However, results are often confusing (Verkerk et al. 2001; Vallejo et al. 2002; Verkerk and Dekker 2004). Recently, the influence of the environmental factors, post-harvest and processing on the content of glucosinolates and other bioactive components of broccoli have been reviewed by Jeffery et al. (2003), Jones et al. (2006) and Song and Thornalley (2007). Storage The effect of storage on glucosinolate preservation is unclear and it depends on glucosinolates, being indole glucosinolates more sensitive to storage conditions than the aliphatic or aromatic glucosinolates (Verkerk et al. 2001; Jeffery et al. 2003). Indole glucosinolate levels were evaluated in stored chopped broccoli, showing a significant 2 4-fold increase after 48 h (Verkerk et al. 2001). This suggests that not only conditions in the field, but also conditions during harvest and handling may alter indole glucosinolate synthesis. When stored at ambient temperature (12 22 C), there was not a significant decrease in glucosinolate content of Brassica vegetables such as broccoli, Brussels sprouts, cauliflower and cabbages (Song and Thornalley 2007). When these vegetables were stored in a domestic refrigerator (4 8 C), the total glucosinolate contents decreased 11 27% for 7 days and minor changes were observed during the first 3 days of storage. Regarding individual glucosinolates, losses of glucoiberin, glucoraphanin and glucoalyssin (5-methylsulphinylpentyl) were higher than those of sinigrin, gluconapin and progoitrin. The loss of glucoiberin in broccoli was 40 50%, whereas with regard to gluconapin the loss was 5 10% in all vegetables studied. A great deal of attention has been paid to glucoraphanin and its decomposition product, the isothiocyanate sulforaphane, because of its anticarcinogenic properties. Although investigations on the effects of storage and cooking on the glucosinolate content of broccoli have been performed (Goodrich et al. 1989; Vallejo et al. 2003), most recent studies (Jones et al. 2006; Winkler et al. 2007) have examined the effects of storage or cooking on sulforaphane formation in dietary broccoli. Rodrigues and Rosa (1999) reported a decrease in the glucoraphanin content of broccoli stored at 4 C for 5 days. Rangkadilok et al. (2002) found no significant losses in the glucosinolate content of broccoli stored at the same temperature for 7 days, while the decline of glucoraphanin content happened at 20 C in 7 days. In contrast, Hansen et al. (1997) stated that glucoraphanin and glucoiberin contents increased when broccoli was stored at 10 C for 7 days. Winkler et al. (2007) concluded that there were no significant differences between storage temperatures, storage times and marketing temperatures as for glucoraphanin content. Relative humidity only appears to be a critical factor for glucosinolate retention when postharvest temperatures rise above approximately 4 C. A high relative humidity of % is recommended to maintain postharvest quality in broccoli. Rangkadilok et al. (2002) found that broccoli heads stored in plastic bags with a high relative humidity ([90%) showed no significant loss at 20 C, whereas heads stored at low relative humidity and at the same temperature showed a 50% decrease of glucoraphanin content during the first 3 days of storage. Similarly, Rodrigues and Rosa (1999) found that glucoraphanin content decreased by [80% in broccoli heads left at low relative humidity and at 20 C for 5 days. However, when broccoli was stored at 4 C, there was no difference in glucoraphanin content after 7 days either in open boxes at ambient humidity (approximately 60% RH) or in plastic bags (approximately 100% RH) (Rangkadilok et al. 2002). The effect of controlled atmosphere storage and the modified atmosphere packaging on glucosinolate content is confusing. Jones et al (2006) summarized several studies about both features. Authors concluded that both controlled atmosphere storage and modified atmosphere packaging appear to be useful tools in maintaining glucosinolate content after harvest. Either the atmospheres reached or relative humidity achieved may have prevented membrane degradation and subsequent mixing of glucosinolates with myrosinase. However, more work is necessary to clearly elucidate the atmospheres that may best maintain glucosinolate content. On the other hand, little is either known about the effect of other postharvest factors, such as ethylene or cytokinin application on glucosinolate content. To sum up, the most important postharvest conditions necessary for maintaining broccoli quality are

11 Phytochem Rev (2008) 7: low temperature (less than 4 C) and a high relative humidity (Rodrigues and Rosa 1999; Jones et al. 2006). These conditions maintain cellular integrity and the process seems to maintain glucosinolate content by preventing the mixing of glucosinolates with myrosinase. Domestic treatments: cooking, steaming and microwaving All the factors and operations through the postharvest chain will activate complex reaction mechanisms, and physical and physiological processes change glucosinolates levels and, subsequently, their breakdown products (Jeffery et al. 2003). Prior to consumption, Brassica vegetables are subject to different ways of processing. Although some Brassica vegetables as broccoli, cauliflower or cabbage can be eaten raw in salads or pickled form, most of them are cooked before consumption. It has been generally shown that conventional cooking methods such as boiling, steaming, pressure cooking and microwaving reduce the intake of glucosinolates by approximately 30 to 60%, depending on the method, intensity and type of compound (Rodrigues and Rosa 1999; Verkerk et al. 2001; Rangkadilok et al. 2002; Verkerk and Dekker 2004). Therefore, increased bioavailability of dietary isothiocyanates may be achieved by avoiding boiling of vegetables. Cooking at high temperatures denatures myrosinase into vegetable material, resulting in a lower conversion of glucosinolates to isothiocyanates. Glucosinolate levels can be reduced because of enzymatic breakdown, thermal breakdown and leaching into the cooking water. Leaching of glucosinolates may not represent a dietary loss when culinary practices use this cooking water for soups (Rosa and Heaney 1993). Rosa and Heaney (1993) found a reduction of total glucosinolate content when boiling Portuguese cabbage and they reported 40 to 80% leaching of glucosinolates from broccoli heads, cabbage leaves and Brussels sprouts into the cooking water. Ciska and Kozlowska (2001) also observed a decrease of glucosinolate content after 5 min of cooking (35%), which gradually decreased to 87% of loss after 30 min in white cabbage. The individual and total glucosinolates content was measured in Portuguese cabbage and white cabbage before and after cooking, and about 50% of total glucosinolates was lost during the cooking process (Pereira et al. 2002). Gliszczynska-Swiglo et al. (2006) proved that water-cooking resulted in a decrease of the total glucosinolate content, as well as in the main glucosinolates of broccoli if compared with fresh broccoli, whereas steam-cooking had the opposite effect. Thermal degradation of indole glucosinolates has been examined in details (Slominski and Campbell 1989; Bones and Rositer 2006). It was observed that heat treatment resulted in a substantial decomposition of indole glucosinolates with thiocyanate and indoleacetonitriles as products, while autolysis (macerated tissue) gave little indoleacetonitriles, but high levels of thiocyanate and carbinols. Steaming, microwaving and stir-fry cooking are popular cooking methods that had little effect on the total glucosinolate contents of Brassica vegetables. Jones et al. (2006) reported that steaming for 2 min is the most effective way to maintain glucosinolate content. Vallejo et al. (2002) investigated the effect of steaming on the quality of broccoli. Results indicated that steaming induces the isothiocyanate content, which was approximately 3-fold lower in steamed than in fresh broccoli. This was presumably due to the effects of myrosinase activity in broccoli, which increased the conversion of glucosinolates into corresponding isothiocyanates rather than to the loss of glucosinolate content during steaming. Similar observations were found by Goodrich et al. (1989) who indicated that large glucosinolate losses occur in blanched broccoli but not in blanched Brussels sprouts. Microwave cooking is an efficient alternative for cooking vegetables due to the low amount of cooking water required, and it has been used as a good method to inactivate myrosinase with a negligible loss of glucosinolates. The effect of microwave treatment on myrosinase activity has been studied. Nevertheless, most studies about microwave cooking and its relation to glucosinolates are confusing. The effects of microwave treatment on the glucosinolate content measured in red cabbage showed higher levels of these compounds than in untreated vegetables (Verkerk and Dekker 2004). This feature is probably due to the increased extractability of glucosinolates by using microwave treatment. However, Rouzaud et al. (2004) reported that microwaving of cabbage

12 224 Phytochem Rev (2008) 7: resulted in a loss of sinigrin (8%), and according to Vallejo et al. (2002), microwaving of broccoli florets resulted in a 74% loss of total glucosinolates and it produced significant decreases of glucoiberin, progoitrin and gluconapin. Moreover, these losses were not associated with the leaching of glucosinolates into the cooking water. Stir-fry cooking is gradually becoming one of the major cooking methods used worldwide for Brassica vegetables. Song and Thornalley (2007) cooked Brassica vegetables by means of the stir-fry method for 3 5 min. Glucosinolate content of several vegetables as broccoli, cabbage, cauliflower or Brussels sprouts did not change significantly through this cooking procedure, presumably because the temperature in the stir-fry process was lower than expected. These authors stated that the stir-fry procedure inhibited myrosinase activity rapidly without any effect on glucosinolate content. This may explain why glucosinolate contents were preserved. Glucosinolate levels do not necessarily decline rapidly after the chopping and cooking process and even induction can occur. Mithen et al. (2000) discuss two opposing mechanisms that take place through vegetable processing: hydrolysis of glucosinolates by myrosinase and the induction of indole glucosinolates by an unknown mechanism. In fact, Verkerk et al. (2001) observed increased levels of indole glucosinolates and some aliphatic after chopping. Matusheski et al (2004) also found that heating fresh broccoli simultaneously increased sulforaphane formation and decreased sulforaphane nitrile formation, which is the primary hydrolysis product when the plant tissue is crushed at room temperature. Recent evidence suggests that sulforaphane:sulforaphane nitrile ratio appeared to be genetically determined (Mithen et al. 2003; Matusheski et al. 2004) and it is influenced itself by hydrolysis conditions and the action of the epithiospecifier protein. As sulforaphane had a far more potent effect on Phase I and II enzymes than sulforaphane nitrile, the health effects of predominant sulforaphane production could be significant. Industrial processes The effects of industrial processes as freezing, fermenting and canning on glucosinolate variation have been little studied (Dekker and Verkerk 2003). Freezing broccoli is commonly used in food industry. Commercial production of frozen vegetables involves, however, steam treatments during blanching (Rodrigues and Rosa 1999) that inactivated myrosinase and decreased glucosinolate breakdown to isothiocyanates. If there was not a blanching step before freezing, glucosinolates would be completely broken down by myrosinase soon after thawing (Rosa et al. 1997; Mithen et al. 2000). Fermenting is another type of industrial process used in some Brassica vegetables. The most common among fermented Brassica (e.g., cabbage) products is sauerkraut, which is manufactured either by natural or controlled fermentation. Apart from myrosinase enzymes found in plants and in the human intestinal flora, it has been reported that some lactic acid bacteria strains degrade glucosinolates and possess myrosinase-like activity. Ciska and Pathak (2004) investigated the relationship between the contents of degradation products in fermented cabbage and the glucosinolates in raw cabbage. Ascorbigen formed from one of the degradation products of glucobrassicin was found to be the major compound in fermented cabbage. Storage of fermented cabbage caused a reduction in the contents of isothiocyanates. The lowest relative contents (expressed as a percentage of the initial glucosinolate content) of degradation products were found for the products of sinigrin degradation, whereas the highest were found for the products of glucoraphanin degradation. Canning is another way for the consumers to find Brassica vegetables. Dekker and Verkerk (2003) showed a significant reduction of glucosinolates content in canned cabbage as compared to fresh and frozen cabbage. Most likely, the reason for this reduction, although it is unclear, was either thermal and/or enzymatic degradation. Canned vegetables undergo an important heat treatment and, therefore, the thermal degradation of glucosinolates is thought to be the most important mechanism. The thermal degradation of glucosinolates in red cabbage has been studied in some details by first inactivating myrosinase (Oerlemans et al. 2006). It was found that aliphatic glucosinolates were less sensitive to heat treatment compared to indole glucosinolates (8% and 38%, respectively). These authors identified two indole glucosinolates

13 Phytochem Rev (2008) 7: hydroxyglucobrassicin (4-hydroxy-3-indolylmethyl) and 4-methoxyglucobrassicin (4-methoxy-3-indolylmethyl) to be the most thermolabile glucosinolates throughout cooking. Several studies agree with this remark: Rosa and Heaney (1993) identified that neoglucobrassicin and 4-methoxyglucobrassicin along with an aliphatic glucosinolate (glucoiberin) were more thermolabile than other glucosinolates. In broccoli, glucobrassicin was identified to be more thermolabile than glucoiberin and glucoraphanin (Vallejo et al. 2002; Oerlemans et al. 2006). Brassica vegetables, such as broccoli, Brussels sprouts, cauliflower and cabbages were evaluated by Song and Thornalley (2007). Authors found that regarding individual glucosinolates, losses of glucoiberin, glucoraphanin and glucoalyssin by thermal degradation were higher than those of sinigrin, gluconapin and progoitrin. The loss of glucoiberin in broccoli was 40 50%, whereas the loss of gluconapin was 5 10% in all vegetables studied. Influence of the human digestive tract on glucosinolate content Raw cruciferous vegetables yield isothiocyanates and nitriles, while residual glucosinolates in cooked vegetables with thermally inactivated myrosinase are degraded into isothiocyanates by myrosinases also present in the microflora of the human digestive tract (Shapiro et al. 2001). Glucosinolates are broken down by plant myrosinase in the small intestine or by bacterial myrosinase in the colon, and metabolites are detectable in human urine 2 3 h after the intake of Brassica vegetables. The effect of cooking on isothiocyanate production from glucosinolates during and after cabbage ingestion was examined in human individuals. Isothiocyanate content was larger after consumption of raw vegetables. However, isothiocyanates still arise, even though to a lesser extent, when cooked vegetables are consumed. This suggests that the colon microflora catalyses glucosinolates. The formation of allyl isothiocyanates from sinigrin has been shown in the digestive tract of rats associated with Bacteroides sp., a human colonic strain. In that study, sinigrin content and the nature of the inoculum used were shown to significantly affect the allyl isothiocyanate production. Very little work has been carried out on the degradative enzymes of the gut microflora. However, more recently, several groups have identified bacterial strains associated with glucosinolate degradation (see review by Bones and Rossiter 2006). Recent evidence (Cheng et al. 2004) suggests that strains of Bifidobacterium sp., B. longum, B. pseudocatenulatum and B. adolescentis were able to digest in vitro both sinigrin and glucotropaeolin (benzylglucosinolate), causing a reduction in the medium ph. All these findings allow us to conclude that these bifidobacteria species could be involved in the digestive degradation of glucosinolates in the human intestinal tract, affecting the final bioavailability of glucosinolates present in Brassica foods. Conclusions With an increased interest in diet and health, it is necessary to have information about glucosinolates profiles and levels in plants. Glucosinolates from most economic important Brassica vegetables as broccoli, cauliflower or cabbage have been widely studied. Conversely, few reports concerning the glucosinolate concentration on other minor Brassica vegetables as kale, turnip greens or leaf rape are found in scientific literature. Our group has recently published the glucosinolate profile and content of these crops. These studies provide valuable information for developing new cultivars with an appropriate glucosinolate profile, from which high quality added value products can be produced. Investigations on degradation products of glucosinolates (mainly isotiocyanates) and other nutritional phytochemicals caused by different processing mechanisms are currently in progress in our group. Genes necessary to alter glucosinolate profiles have been found within Brassica genus and Arabidopis thaliana. Aliphatic glucosinolate content is highly heritable and they vary among Brassica crops and varieties of the same crop (Kushad et al. 1999). On the other hand, indole glucosinolates are common in Brassica vegetables, although their levels are not only subject to environmental fluctuations but to conditions during harvest and processing. In fact, qualitative differences observed among aliphatic composition may be due to allelic variation in a few genes encoding key regulatory enzymes at key points in the glucosinolate pathway. For example, biosynthesis of gluconapin requires a functional allele at the Gsl-alk locus that turns glucoraphanin into its alkenyl homolog,

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