Minor Components of Pulses and Their Potential Impact on Human Health

Food Research International 43 (2010) 461–482

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Food Research International

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Review Minor components of pulses and their potential impact on human health

Rocio Campos-Vega a, Guadalupe Loarca-Piña a, B. Dave Oomah b,* a Programa en Alimentos del Centro de la República (PROPAC), Research and Graduate Studies in Food Science, School of Chemistry, Universidad Autónoma de Querétaro, Querétaro, Qro. 76010, Mexico b National Bioproducts and Bioprocesses Program, Paciﬁc Agri-Food Research Centre, Agriculture and Agri-Food Canada, Summerland, BC, Canada V0H 1Z0 article info abstract

Keywords: Pulses contain a number of bioactive substances including enzyme inhibitors, lectins, phytates, oligosac- Pulses charides, and phenolic compounds. Enzyme inhibitors can diminish protein digestibility, and lectins can Legumes reduce nutrient absorption, but both have little effect after cooking. Phytic acid can diminish mineral bio- Phenolic compounds availability. Some phenolic compounds can reduce protein digestibility and mineral bioavailability, and Enzyme inhibitors galactooligosaccharides may cause ﬂatulence. On the other hand, these same compounds may have pro- Lectins tective effects. Phytic acid exhibits antioxidant activity and protects DNA damage, phenolic compounds Minerals Vitamins have antioxidant and other important physiological and biological properties, and galactooligosaccha- Fatty acids rides may elicit prebiotic activity. These compounds can have complementary and overlapping mecha- Phytoesterols nisms of action, including modulation of detoxifying enzymes, stimulation of the immune system, Phytic acid regulation of lipid and hormone metabolism, antioxidant, antimutagen, and antiangiogenic effects, Galactooligosaccharides reduction of tumor initiation, and promotion and induction of apoptosis. Secondary metabolites are Saponins considerated antinutrients, simultaneously conferring health beneﬁts, so these secondary metabolites Oxalate are currently marketed as functional foods and nutraceuticals ingredients. Human health Crown Copyright Ó 2009 Published by Elsevier Ltd. All rights reserved. Cardiovascular diseases Diabetes Cancer Obesity

Contents

1. Introduction ...... 462 2. Phenolic compounds ...... 464 2.1. Levels of phenolic acids in pulses ...... 464 2.2. Phenolic acids and antioxidant activity ...... 465 2.3. Isoflavones content and health ...... 465 3. Enzyme inhibitors and lectins ...... 466 3.1. Chemical composition ...... 466 3.2. Levels of enzyme inhibitors and lectins in pulses ...... 466 3.3. Nutritional and physiological effects ...... 467 4. Minerals and vitamins ...... 468 4.1. Biological functions of minerals...... 468 4.2. Levels of minerals in pulses ...... 468 4.3. Vitamin contents in pulses ...... 469 5. Fatty acids ...... 471 6. Phytosterols...... 471 7. Phytic acid...... 472 7.1. Biological function...... 472 7.2. Phytate levels in pulses ...... 472 7.3. Phytic acid and health ...... 472 8. Saponins and oxalate ...... 473

* Corresponding author. Tel.: +1 250 494 6399; fax: +1 250 494 0755. E-mail address: [email protected] (B.D. Oomah).

0963-9969/$ - see front matter Crown Copyright Ó 2009 Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2009.09.004 462 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

8.1. Saponins structure...... 473 8.2. Saponins in pulses ...... 473 8.3. Saponins and health ...... 474 8.4. Oxalate ...... 474 9. Others compounds of pulses...... 474 10. Pulses and health ...... 475 10.1. Pulses and cardiovascular diseases ...... 475 10.2. Pulses and diabetes ...... 475 10.3. Pulses and cancer ...... 476 10.4. Pulses and obesity...... 476 10.5. Pulses and other diseases ...... 476 11. Concluding remarks ...... 477 References ...... 477

1. Introduction baseline examination in the First National Health and Nutrition Examination Survey (NHANES 1) Epidemiological Follow-up Study The nutritional properties of pulses reported to impart physio- (NHEFS), Bazzano et al. (2001) found that legume consumption logically beneficial effects in humans have been investigated was significantly and inversely associated with risk of CHD and extensively. Pulse grains are high in protein, carbohydrates, and CVD. Over an average of 19 years of follow-up, 1802 incident cases dietary fibre and are a rich source of other nutritional components of CHD and 3680 incident cases of CVD were found. (Tharanathan & Mahadevamma, 2003) and their consumption and Legumes contain a number of bioactive substances including production extends world-wide (Table 1). Pulses used for human enzyme inhibitors, lectins, phytates, oligosaccharides, and phenolic consumption include peas, beans, lentils, chickpeas, and faba beans compounds that play metabolic roles in humans or animals that (Rochfort & Panozzo, 2007). Frequent legume consumption (four or frequently consume these foods (Table 2). These effects may be re- more times compared with less than once a week) has been asso- garded as positive, negative, or both (Champ, 2002). Some of these ciated with 22% and 11% lower risk of coronary heart disease (CHD) substances have been considered as antinutritional factors due to and cardiovascular disease (CVD), respectively (Flight & Clifton, their effect on diet quality. Enzyme inhibitors and lectins can re- 2006). In an earlier study of 9632 participants free of CVD at their duce protein digestibility and nutrient absorption, respectively,

Table 1 Production and region of pulse consumption.

Main edible legume seeds (grain legumes) Latin name World crop production metric tons Main region of 103 consumption Pulses 3819 Dry beans (Phaseolus spp. including several species now in 1162 Vigna) Kidney bean, haricot bean, pinto bean, navy bean Phaseolus vulgaris World-wide Lima bean, butter bean Vigna lunatus Americas, Africa Adzuki bean Vigna angularis Asia, especially Japan Mung bean, golden gram, green gram Vigna radiata Black gram, urd Vigna mungo Asia Scarlet runner bean Phaseolus coccineus Rice bean Vigna umbellata Moth bean Vigna acontifolia Tepary bean Phaseolus acutifolius Dry broad beans (Vicia faba): Horse bean Vicia faba 255 Broad bean Vicia faba Temperate regions Field bean Vicia faba Temperate regions Dry peas (Pisum spp.): 892 Garden pea Pisum sativum var. sativum Protein pea Pisum sativum var. arvense Chickpea Cicer arietinum 478 Asian and Middle East Dry cowpea, blackeye pea, blackeye bean Vigna unguiculata ssp. 350 Africa, Asia, South dekindtiana America Pigeon pea, cajan pea, congo bean Cajanus cajan 103 Asia, Africa Lentil Lens culinaris 199 World-wide Bambara groundnut, earth pea Vigna subterranea Vetch, common vetch Vicia sativa 99 Lupins Lupinus spp. 45 Minor pulses Lablab, hyacinth bean Lablab purpureus Jack bean, sword bean Canavalia ensiformis, gladiata Winged bean Psophocarpus teragonolobus Velvet bean, cowitch Mucuna pruriens var. utilis Yam bean Pachyrrizus erosus

Adapted from Walker and Ochhar (1982) and Duranti (2006). R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 463

Table 2 Bioactive components of major pulse species (% dry matter basis except where indicated otherwise).

Phaseolus vulgaris Lens esculenta Cicer arietinum Pisum ativum Vici faba Lupins albus Trypsin inhibitor activitya TIU units mg1 DM 9.6 8.4 1–15 5.4–7.8 6.7 <1 TIA g1 0.425 0.178 mg g1 4.4–12.5 Ukg1 DM 2.7–11.7 Chymotrypsin inhibitor activity (IU g1)b 740–10240 380–770 Amylase inhibitor activity (U g1)b 2–18a 14–80 Haemagglutinin activityf HA 8200 640 0 80 HU mg1 0.20–7.7a,d 100–400 25–100 Ukg1 2.45–3.56 5.1–15.06 l g1 2.5–5.0 10–20 10000 Phytatesc 0.2–1.9 0.15–2.34a 0.4–1.1 0.2–1.3 0.5–1.1 Oxalatesd 0.10–0.5 0.12–0.54a 0.07 (0.7) Polyphenolse Total 0.0–0.4 1.0 0.1–0.6 0.25 1.1 Phenolic acid 0.001–0.003 Tannins 0.0–0.7 0.1 0.0–0.1 0.0–1.3 0.0–2.1 Isoﬂavones (mg g1) 100–700 Daidzein (mg g1) 1–4 0–1 1–19 0–5 Genistein (mg g1) 1–52 1–2 7–21 0–5 130–8700 (fwt)f Lignans (mg g1) 30 180 Secoisolariciresinol (mg g1) 6–15 0–1 1 0–1 Saponinsb 0.4–0.5 0.4 0.1–0.3 0.4 (mg100 g1) 40–127

DM, dry matter; TIU, trypsin inhibitor units; TIA, trypsin inhibitor activity; U, Units, IU, International Units; HA, haemagglutinin activity; HU, haemagglutinatin units. Adapted from Champ (2002). a Liener (1976), Melcion and Valdebouze (1977), Viroben (1979), Gueguen, Quemener, and Valdebouze (1980), Valdebouze, Bergeron, Gaborit, and Delort-Laval (1980), Ekpenyoung and Borchers (1981), Bertrand, Delort-Laval, Melcion, and Valdebouze (1982), Lacassagne, Francesch, Carré, and Melcion (1988), Huisman (1990), Jondreville, Grosjean, Buron, Peyronnet, and Beneytout (1992), Zdunczyk, Godycka, and Amarowicz (1997), Chrenkova, Ceresnakova, Sommer, and Slamena (2001), Page, Aubert, Duc, Welham, and Domoney (2001), Smulikowska et al. (2001). b Savage and Deo (1989). c Melcion and Valdebouze (1977), Liener (1979), Viroben (1979), Gueguen et al. (1980), Valdebouze et al. (1980), Ekpenyoung and Borchers (1981), Bertrand et al. (1982), Savage and Deo (1989). d Savage and Deo (1989), Quinteros et al. (1990). e Savage and Deo (1989), Longstaff and McNab (1991), Saini (1993), Zdunczky et al. (1997), Mazur (1998), Binghma et al. (1998), Bravo (1988), Hom-Ross et al. (2000), Liggins et al. (2000), Carbonaro et al. (2001), Smulikowska et al. (2001). f Ranilla et al. (2009).

but both have little effect after cooking (Lajolo & Genovese, 2002). ﬂatulence (Muzquiz, Burbano, Ayet, Pedrosa, & Cuadrado, 1999). Phytic acid can diminish mineral bioavailability (Sandberg, 2002). On the other hand, these same compounds may have protective ef- Some phenolic compounds can also reduce protein digestibility fects against cancer (Lajolo & Genovese, 2002; Mathers, 2002). (Chung, Wong, Wei, Huang, & Lin, 1998) and mineral bioavailabil- Phytic acid has antioxidant and DNA protective effects (Midorika- ity (Sandberg, 2002), while galactooligosaccharides may induce wa, Murata, Oikawa, Hiraku, & Kawanishi, 2001; Phillippy, 2003),

Table 3 Potential beneﬁcial effects of bioactive components in pulses.

Beneﬁcial effects Adverse effects Amount in untreated Primary source(s) pulses*

Protease inhibitors Anticarcinogenic (?) " Carcinogenesis (?) and growth +++ Soya, GL, cereals inhibition (in animals) Amylase inhibitors Potentially therapeutic in diabetes (?) ; Starch digestion +++ Cereals, GL Lectins May help in obesity treatment (??), ; Growth inhibition (in animals), ; ++(+) Beans tumor growth (??) nutrient absorption Phytates Hypocholesterolaemic effect (?), ; Bioavailability of minerals ++ Wheat bran, soya, GL anticarcinogenic (?) Oxalates ; Bioavailability of minerals + Spinach, rhubarb, beans Phenolic compounds ; Risk factors for menopause (CHD..) (?) + Soya, clover Flavonoids, isoﬂavones ; Risk of hormonedependent cancer (?) Infertility syndrome (in animals) (phyto-oestrogens) Condensed tannins Astringent taste, ; food intake (in ++ Tea, sorghum, rapeseed, animals) Vicia faba Lignans (phyto-oestrogens) ; Risk factors for menopause (?) Linseed Lignins ; Fermentability of dietary ﬁbres + Straw Saponins Hypocholesterolaemic effect (?), Bitter taste, ; foodintake (in animals) ++(+) Lucerne (alfalfa), ginseng anticarcinogenic (?) Alkaloids Lupins

CHD, coronary heart disease; GL, grain legumes. From Champ (2002). * Compared to main sources. 464 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 phenolic compounds such as flavonoids and phenolic acids exhibit Table 5 antioxidant and other specific properties (Murphy & Hendrich, Phenolic acid content of commonly consumed dry bean in United States. 2002; Pieta, 2000; Yeh & Yen, 2003), and galactooligosaccharides Bean Cultivars Mean phenolic acid Total phenolic may exert prebiotic activity (De Boever, Deplancke, & Verstraete, class concentration (mg 100 g1) acid content (mg g1) 2000; Rycroft, Jones, Gibson, & Rastall, 2001)(Table 3). Secondary p- Ferulic Sinapic metabolites are considerated antinutrients, simultaneously confer- Coumaric ring health benefits, so these secondary metabolites are currently Pinto Maverik 4.5 22.9 8.5 36.0 marketed as functional foods and nutraceuticals ingredients. Buster 4.5 16.0 9.0 29.5 For example, common bean lines devoid of major lectin proteins Othello 5.6 15.2 5.9 26.7 and with low phenolic content have been developed (Campion, Great Northern Norstar 17.0 9.4 30.4 Perrone, Galasso, & Bollini, 2009) to improve nutritional character- 4.0 istics of bean seeds used for human consumption, and potentially Matterhorn 6.3 17.2 9.0 32.5 for animal feeding. On the other hand, products such as Phase2TM, Navy Vista 12.4 26.6 9.2 48.3 a bean extract, have been on the market since 2001, gained GRAS Black T-39 11.6 25.5 9.0 47.1 Jaguar 7.0 11.7 5.7 24.4 (generally recognized as safe) status in the US in 2006 and have Eclipse 9.8 24.7 6.8 42.5 been shown to influence body composition of overweight subjects Dark red Red Hawk 1.8 15.3 3.8 20.9 (Celleno, Tolaini, D’Amore, Perricone, & Preuss, 2007). kidney Light red Cal Early 7.0 14.8 5.7 27.4 kidney 2. Phenolic compounds Red Mex UI 239 5.8 17.4 5.4 28.6 Cranberry Taylor 1.7 14.0 3.5 19.1 Cranberry 2.1. Levels of phenolic acids in pulses Pink UI 537 6.8 19.4 8.2 34.4 Alubia Beluga 5.3 10.6 4.0 19.8

The major polyphenolic compounds of pulses consist mainly of Adapted from Luthria and Pastor-Corrales (2006). tannins, phenolic acids and flavonoids. The legumes with the highest polyphenolic content are the dark, highly pigmented varieties, such as red kidney beans (Phaseolus vulgaris) and black gram (Vigna mungo). Condensed tannins (proanthocyanidins) have been quanti- fied in hulls of several varieties of field beans (Vicia faba) and are (2005) reported a 5-fold variation (3.3–16.6 mg catechin equiva- also present in pea seeds of colored-flower cultivars. Tannin-free lents g1) in total phenolic content of six Canadian bean varieties, and sweet seeds have been selected among broad beans, lentils while variations in flavonoids, anthocyanins, flavonols, and tartaric and lupins (Smulikowska et al., 2001). esters were minimal. Twenty-four common bean samples analyzed Pulses vary based on their total phenolic contents and antioxi- recently by Long-Ze, Harnly, Pastor-Corrales, and Luthria (2008) dant activities (Table 4). Lentils have the highest phenolic, flavo- contained the same hydroxycinnaminic acids, but the flavonoid noid and condensed tannin content (6.56 mg gallic acid components showed distinct differences. Black beans contained equivalents g1, 1.30 and 5.97 mg catechin equivalents g1, respec- primarily the 3-O-glucosides of delphinidin, petunidin, and malvi- tively), followed by red kidney and black beans (Xu & Chang, 2007). din, while kaempferol and its 3-O-glycosides were present in pinto According to literature, total phenolic content is directly associated beans. Light red kidney bean had traces of quercetin 3-O-glucoside with antioxidant activity (Amarowicz, Troszynska, Barylko-Pikielna, & and its malonates, but pink and dark red kidney beans contained Shahidi, 2004; Awika, Rooney, Wu, Prior, & Zevallos, 2003). Pulses the diglycosides of quercetin and kaempferol. Small red beans con- with the highest total phenolic content (lentil, red kidney, and tained kaempferol 3-O-glucoside and pelargonidin 3-O-glucoside, black beans) exert the highest antioxidant capacity assessed by while flavonoids were undetected in alubia, cranberry, great north- 2,2-diphenyl-1-picryhydrazyl (DPPH) free radical scavenging, ern, and navy beans. ferric reducing antioxidant power (FRAP), and the oxygen radical The content of total anthocyanin in whole grain and seed coat of absorbance capacity (ORAC) (Xu & Chang, 2007). 15 cultivars of black beans grown in Mexico ranged from 37.7 and The potential health benefits of common bean is attributed to 71.6 mg g1grain and between 10.1 and 18.1 mg g1 seed coat, the presence of secondary metabolites such as phenolic com- respectively. The anthocyanins in seed coats of beans were identi- pounds that possess antioxidant properties (Azevedo et al., 2003; fied as delphinidin 3-glucoside 65.7%, petunidin 3-glucoside 24.3%, Cardador-Martinez, Loarca-Pina, & Oomah, 2002; Lazze, Pizzala, and maldivin 3-glucoside 8.7% (Salinas-Moreno, Rojas-Herrera, Savio, Stivala, & Bianchi, 2003). Ferulic acid is the most abundant Sosa-Montes, & Pérez-Herrera, 2005). phenolic acid in common beans and intermediate levels of p-cou- Chickpea also contain a wide range of polyphenolic compounds, maric and sinapic acids are also present (Table 5)(Luthria & including flavonols, flavone glycosides, flavonols, and oligomeric Pastor-Corrales, 2006). Oomah, Cardador-Martínez, and Loarca-Piña and polymeric proanthocyanidins (Sarma, Singh, Mehta, Singh, &

Table 4 Phenolic contents and antioxidant activities of pulses.

Legume Total phenolic Total ﬂavonoid Condensed tannin DPPH scavenging FRAP value (mmol ORAC value (lmol content (mg gallic content (mg catechin content (mg catechin capacity (lmol Trolox Fe2+ equivalents Trolox equivalents g1) acid equivalents g1) equivalents g1) equivalents g1) equivalents g1) 100 g1) Green pea 1.53 0.08 0.26 0.91 1.06 3.86 Yellow pea 1.67 0.18 0.42 2.13 1.28 23.17 Chickpea 1.81 0.18 1.05 1.05 0.73 5.13 Lentil 6.56 1.30 5.97 16.79 7.78 50.06 Red kidney 4.98 2.02 3.85 16.92 3.90 24.43 Black bean 5.04 2.49 3.40 14.61 9.31 46.22

Adapted from Xu and Chang (2007). R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 465

Singh, 2002; Singh, Sarma, & Singh, 2003). Total phenolic content Table 7 in chickpea ranges from 0.92 to 1.68 mg gallic acid equivalents Antioxidant activity of Phaseolus vulgaris L. 1 g (Xu & Chang, 2007; Zia-Ul-Haq et al., 2008). Sample EC50 GAE CE GAE/CE Lignans, diphenolic compounds with a 2,3-dibenzylbutane skel- Landraces eton have both estrogenic and antiestrogenic properties (Orcheson, PVMP00 2810 1.17 0.3 3.9 Rickard, Seidl, & Thompson, 1998). The plant lignans, secoisolaric- PVPM01 2365 1.29 0.22 5.8 iresinol (SEC), and matairesinol (MAT) are converted to the metab- VDVA01 39 3.9 0.64 6.09 olites enterodiol (ED) and enterolactone (EL), known as the VDVA02 82 4 0.58 6.89 mammalian lignans, in the gastrointestinal tract. A review of phy- VDSE01 50 3.71 0.6 6.18 toestrogens (isoﬂavonoids and lignans) in human health in relation OMPM01 96 4.4 1.31 3.36 to estrogen type II binding sites, sex hormone binding globulin, tu- OMVA01 112 4.08 1.43 2.85 OMVA02 135 4.27 1.03 4.14 mor invasion, angiogenesis, and the immune system is given by OMSE01 153 4.2 1.28 3.28 Adlercreutz (1998). Most studies have only looked at the isoﬂavo- ZOPM00 448 3.32 0.33 10.15 noid content of legumes, only one study (Mazur, Duke, Wahala, ZOVA01 244 3.09 0.24 12.87 Rasku, & Adlercreutz, 1998) has analyzed the SEC and MAT content ZOVA02 346 3.13 0.24 13.04 (Table 6). The concentrations of lignans in legumes was found to EC expressed as mg sample mg1 DPPH; GAE expressed as mg gallic acid g1 range for SEC from 0 to 240 g/100 g with higher values for the oil- 50 sample; CE expressed as mg (+)-catechin g1 sample. seeds, peanuts 333 g/100 g SEC and soybean range from 13 to From Heimler et al. (2005). 273 g/100 g SEC (Table 6) with trace or no MAT detected (Mazur et al., 1998).

processing steps result in significant decreases in total phenolic 2.2. Phenolic acids and antioxidant activity content (TPC) and DPPH free radical scavenging activity (DPPH) in all tested CSFL’s. All soaking and atmospheric boiling treatments In the past few years, the antioxidant properties of food have decreased, while pressure boiling and steaming increased the oxy- been studied since reactive oxygen species are widely believed to gen radical absorbing capacity (ORAC). Steaming treatments re- be involved in many diseases such as cancer, diabetes, autoim- sulted in a greater retention of TPC, DPPH, and ORAC values in all mune conditions, various respiratory diseases, eye diseases, and tested CSFL’s as compared to boiling treatments. However, TPC schizophrenia (Cai, Luo, Sun, & Corke, 2004). Heimler, Vignolini, and DPPH in cooked lentils differed significantly between atmo- Dini, and Romani (2005) assessed the antioxidant activity of Phase- spheric and pressure boiling. Pressure processes significantly in- olus vulgaris L. dry beans. Table 7 lists the EC50 values, total phen- creased ORAC values in both boiled and steamed CSFL’s olics according to the Folin–Ciocalteu method expressed as GAE, compared to atmospheric processes. Greater TPC, DPPH, and ORAC and total flavonoids expressed as CE. EC50 indicates the amount values were detected in boiling water than in soaking and steam- of beans, expressed in mg, necessary to reduce the activity of ing water. Boiling also caused more solid loss than steaming. Steam 1 mg of DPPH by one-half; the lower the EC50 value, the higher processing exhibited several advantages in retaining the integrity the antioxidant activity of the sample. With this method, the of the legume appearance and texture of the cooked product, EC50 values (mg of pure standard/mg DPPH) for kaempferol, quer- shortening process time, and greater retention of antioxidant com- cetin, and quercitrin were 0.44, 0.20, and 0.49, respectively; for ponents and activities. The changes in the overall antioxidant prop- ascorbic acid, the EC50 value was 0.21. EC50 data range from 39 erties of processed CSFL’s could be attributed to the synergistic to 2810. The phenolic content of the dry beans under study was combinations or counteracting of several factors, including oxida- of the same order of magnitude as that previously found in one tive reaction, leaching of water-soluble antioxidant compositions, bean cultivar used in central Mexico (Cardador-Martinez et al., formation or breakdown of antioxidant compositions, and solid 2002). losses during processing. Antioxidant activity from foods can be influenced by the methods applied for its consumption, reason why the effects of soaking, boiling and steaming processes on the total phenolic components 2.3. Isoflavones content and health (Table 8) and antioxidant activity in commonly consumed cool season food legumes (CSFL’s) including green pea, yellow pea, chick- Flavones and isoflavones have been isolated from a wide variety pea, and lentil have been investigated (Xu & Chang, 2008). All of plants, though the isoflavones are largely reported from the Fab- aceae/Leguminosae family. According to the USDA survey on isoflavone content, lentils do not contain significant amounts of these isoflavones (USDA, 2002). Chickpeas contain daidzein, geni- Table 6 stein, and formononetin (0.04, 0.06, and 0.14 mg 100 g1, respec- Lignan content (lg 100 g1 dry wt.) of legumes as SEC and MAT or as ED and EL. tively), and approximately 1.7 mg 100 g1 biochanin A. Soybeans a Legumes Direct analysis In vitro fermentation have significantly higher levels of daidzein and genistein (47 and SECb EDc ELc Totald 74 mg 100 g1, respectively) but contain less formononetin and 1 Lentil nr 1092 864 1956 biochanin A compared to chickpeas, 0.03 and 0.07 mg 100 g , Kidney bean 69.9 266 377 643 respectively. There are many biological activities associated with Navy bean 85.8 144 399 543 the isoflavones, including a reduction in osteoporosis, cardiovascu- Pinto bean 79.1 53 173 226 lar disease, prevention of cancer and for the treatment of Yellow pea 8.2 48 185 233 menopause symptoms (Cassidy et al., 2006; Messina, McCaskill- ED, enterodiol; EL, enterolactone. Stevens, & Lampe, 2006; Polkowski & Mazurek, 2000; Ricketts, Adapted from Meagher and Beecher (2000). Moore, Banz, Mezei, & Shay, 2005; Trock, Hilakivi-Clarke, & Clarke, a Mazur et al. (1998); nr, not reported. b SEC, secoisalariciresinol. 2006). c Thompson et al. (1991). Total isoflavones in L. mutabilis range from 9.8 to 87, 16.1 to d Total = sum of ED + EL. 30.8 and 1.3 to 6.1 mg 100 g1 fresh weight of sample (expressed 466 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Table 8 Effect of processing on total phenolic content (TPC-mg gallic acid equivalents g1) and DPPH free radical scavenging capacity (lmol trolox equivalents g1) of selected cool season food legumes.

Legumes Processing conditions Green pea Yellow pea Chickpea Lentil TPC Loss%a TPC Loss% TPC Loss% TPC Loss% Raw 122 (2.77) 138 (3.68) 144 (2.94) 7.34 (19.72) Soaked 100% hydratation 1.16 (2.28) 4.9 (17.6) 1.35 (3.18) 2.2 (13.6) 1.40 (2.63) 2.77 (10.5) 4.56 (17.86) 37.8 (9.4) Boiledb RB, 120 min 0.60 (0.91) 50.8 (67.1) 0.76 (1.72) 44.9 (53.3) 0.92 (0.28) 36.1 (90.5) – Steamedc RS, 70 min 1.05 (0.92) 13.9 (66.7) 1.25 (1.20) 9.4 (67.4) 1.40 (1.66) 2.8 (43.5) –

Adapted from Xu and Chang (2008). a Loss% was calculated using original unprocessed beans as starting materials. DPPH values are in brackets. b Peas were pre-soaked based on 100% hydratation rate, lentil was pre-soaked based on 50% hydratation rate prior to boiling treatments. c All samples were pre-soaked based on 70% hydratation rate prior ro stearning treatments. RB, regular boiling; RS, regular steaming. as genistein) in seed coat, cotyledon, and hypocotyl fractions, moiety on the cell surface (González de Mejía, Rocha, Winter, & respectively (Ranilla, Genovese, & Lajolo, 2009). Barceló and Muñoz Goldstein, 2002). Lectins or haemagglutinins are found in most (1989) identified isoflavones such as genistein, 20 hydroxigenistein, plant foods (Nachbar & Oppenheim, 1980), however, grain legumes luteone, and wighteone in sprouted hypocotyls of L. albus CV are the main sources of lectins in ordinary human food. Beans multolupa, suggesting that these compounds are related with the (most species, including Phaseolus vulgaris) seem to be important lignification of the cell wall. This may explain luteone (a tetrahydr- sources of lectins, but some varieties can have a much higher lectin oxyisoflavone) which was detected in immature seeds of L. luteus content than others (Bond & Duc, 1993). As a result, residual quan- (Fukui, Egawa, & Koshimizu, 1973). Dini, Schettino, and Dini tities of the initial levels may resist even normal cooking at alti- (1998) detected two genistein derivatives, mutabilin (glycosylated tudes well above sea level (De Muelenaere, 1965). Kidney bean form) and mutabilein (aglycon form), in seeds of L. mutabilis. Fur- phytohemagglutinin (PHA) is a tetrameric glycoprotein consisting ther, formononetin, genistein and the phytoestrogen secoisolaric- of two different subunits with a molecular mass of 120 kDa iresinol were found in seeds of L. mutabilis (23, 2420, and 3.1 lg (Sgarbieri & Whitaker, 1982). 100 g1, respectively) (Mazur et al., 1998). Studies have suggested that lectins affect the immune response The cotyledon of Andean lupins have the highest content of to- against ovalbumin and may promote the development of food al- tal isoflavones (16–31 mg 100 g1 cotyledon FW) compared to the lergy to plants containing lectins. Lectins extracts from red kidney hypocotyls (1.3–6.1 mg 100 g1 hypocotyls FW) and seed coats bean inhibits oral tolerance when administered to mice fed ovo- (9.8–10 mg 100 g1 seed coat FW). Interestingly, the genistein mucoid, while lectin extracts from pea have less pronounced and derivative (GD) was the major isoflavone found in seed coats and no effects (Kjaer & Frokiaer, 2002). Lectin is one of the major pro- cotyledons from L. mutabilis cultivars. Furthermore, the H-6 culti- teins found in lentil (Lens culinaris). All lectins bind one transition var was remarkable because of its high total isoflavone content ion, usually manganese, and one calcium ion. Intact and decorticat- in seed coats (87 mg 100 g1 FW), cotyledon (30.8 mg 100 g1 ed lentils exhibit both manganese ion and radical signals, but the FW) and hypocotyls (6.1 mg 100 g1 FW). testa shows only the radical signal (Polat & Korkmaz, 2001). On the other hand, cooking effectively removes trypsin inhibitor and lectins levels of vegetable peas and significantly reduces protein 3. Enzyme inhibitors and lectins and amino acid solubility (Habiba, 2002). Lectin can be completely removed from lentil flour after 72 h fermentation at 42 °C with a 3.1. Chemical composition flour concentration of 79 g L1 (Cuadrado et al., 2002). Lectin is being used for the discovery of protein markers of cancer using a Protein inhibitors of hydrolases present in pulses are active natural glycoprotein microarray approach. Multiple lectins can against proteases, amylases, lipases, glycosidases, and phospha- screen serum samples from patients with pancreatic cancer or pan- tases, those inhibiting proteases being the most well-known. From creatitis by selective detection of glycan structures (Harland, 2002) the nutritional aspect, the inhibitors of the serine proteases trypsin (see Table 9). and chymotrypsin found in plant foodstuffs are the most important (Belitz & Weder, 1990). Beans are the second largest group of seeds after cereals reported as natural sources of a-amylase inhibitors 3.2. Levels of enzyme inhibitors and lectins in pulses (Lajolo, Mancini Filho, & Menezes, 1984). Protease inhibitors isolated from legumes are generally classified into two families, re- Several plant lectins including those present in pulses are ferred to as Kunitz and Bowman-Birk on the basis of their important tools in cell biology and immunology, with potential molecular weights and cystine contents. Kunitz type inhibitors for clinical applications. Grant, Dorward, Buchan, Armour, and have a molecular mass of 20 kDa, with two disulfide bridges, Pusztai (1995a) determined trypsin inhibitor and lectin contents and act specifically against trypsin. Bowman-Birk type inhibitors of kidney beans, soybeans, cowpeas, and lupin seeds. They re- with a molecular mass of 8–10 kDa, have seven disulfide bridges, ported high levels of lectins in kidney beans [840 105 hemag- and inhibit trypsin and chymotrypsin simultaneously at indepen- glutinating activity units (HU) kg1] and very low amounts in dent binding sites. In common beans, lima beans, cowpeas, and cowpea and lupin seeds [3 105 HU kg1]. Protease inhibitor lentils protease inhibitors have been characterized as members of content was moderate in kidney beans and cowpeas (8 and the Bowman-Birk family (Belitz & Weder, 1990; Lajolo, Finardi-Filho, 10.6 g of trypsin and 9.2 g of chymotrypsin inhibited kg1, respec- & Menezes, 1991; Liener, 1994). Trypsin/chymotrypsin inhibi- tively), and low in lupin seeds (1.1 g of trypsin and 1.4 g of chymo- tors from red kidney bean, Brazilian pink bean, lima bean and trypsin inhibited kg1). Brazilian bean varieties with different seed soybean are closely related with high homology (Wu & Whitaker, coat colors had trypsin inhibitory activity of 18–29 (TIA) mg1 1991). (Table 10)(Lajolo & Genovese, 2002). Lectins are proteins or glycoproteins that agglutinate erythro- Amounts of lectin in legumes vary significantly (Zhang, Shi, Ilic, cytes of some or all blood groups in vitro and depend on their spec- Jun, & Kakuda, 2009). Lectin accounts for about 2.4–5% of the total ificity and high binding affinity for a particular carbohydrate protein (17–23%) in kidney bean seeds, 0.8% in soybean and lima R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 467

Table 9 Table 10 Biological effects of dietary phenols. Trypsin inhibitory activity (TIUb mg1 of bean) of raw and autoclaved (121 °C/15 min) Brazilian varieties of common beans. Active compound Biologic effect Reference Bean cultivar Raw bean Autoclaved Quercetin Inhibition fo mitogen activated Bird, Delaney, Sims, protein (MAP) kinase in Thoma, and Dower Aporé 18.78 ± 0.22 0.62 ± 0.01 human epidermal carcinoma (1992) Carioca MG 28.96 ± 0.21 0.71 ± 0.01 cells Emgopa 201 19.68 ± 0.84 1.00 ± 0.02 Induction of cell cycle arrest Choi et al. (2001) Jalo Precoce 26.14 ± 0.93 0.56 ± 0.02 and apoptosis in human breast Roxo 90 20.45 ± 0.62 0.69 ± 0.02 cancer cells in vitro Rio Tibagi 21.47 ± 0.76 0.48 ± 0.03 Inhibits the expression and Xing, Chen, Mitchell, Saﬁra 25.55 ± 1.13 0.92 ± 0.03 function of the androgen and Young (2001) Xamego 26.44 ± 0.36 0.89 ± 0.08 receptor in LNCaP prostate cancer cells prevents and Adapted from Lajolo and Genovese (2002). b protects streptozotocin- TIU, trypsin inhibitory units. induced oxidative stress and b- cell damage in rat pancreas Inhibition of DMBA-induced Coskun, Kanter, hamster buccal pouch Kormaz, and Oter Table 11 carcinogenesis (2005) Trypsin inhibitor activity and lectin content in common (P. vulgaris L.) and tepary a Inhibition of colon cancer in Avila, Velasco, (P. acutifolius) beans. rats and mice induced by Cansado, and Bean type Trypsin inhibitors (TIU mg1) Lectin (HAU g1 protein) azoxymethanol Notario (1994) Expression inhibition of the Ferriola, Cody, and Common bean mutated p53 (tumor Middleton (1989) Flor de Mayo 26.8 a 8.57 b suppressor gene) protein Tepary bean in vitro White Fisetin, quercetin, and Inhibition of protein kinase C L-246-12 18.0 b 3.29 a luteolin (PKC) G-400-16 13.5 b 1.40 a Quercetagetin, Inhibition of human Pruzanski and Vadas PI-246-22 16.8 b 3.69 a kaempferol-3-O- recombinant synovial (1991) L-246 18.0 b 3.29 a galactoside, and Phospholipase A2 L-173 14.9 b 18.16 c scutellarein PI-319-443 11.5 c 1.30 a

Quercetin, apigenin, Inhibition generation of H2O2 Ogasawara, Fujitani, Black and taxifolin in vitro Drzewiecki, and L-242-45 17.5 b 1.68 a Middleton (1986) L-246-19 12.8 c 4.67 ab Quercetin and Inhibition of anti-IgE-induced Ogasawara et al. Brown apigenin histamine release (1986) L-179 12.7 c 1.75 a Catechin Reduced cholesterol Ikeda et al. (1992) absorption from rat intestine Note. Means with different letters are significantly different (Tukey a = 0.05). Inhibition oxidation of LDL Mangiapane et al. Adapted from Gonzalez De Mejia et al. (2005). a induced by the mouse (1992) Mean of two independent experiments with triplicates. TIU, trypsin inhibitory transformed macrophage cell units/mg; HAU, hemagglutinin activity units/mg protein. line, 1774, human monocyte- derived macrophages, and vascular endothelial cells cells isolated from rat small intestine. Common beans had higher isolated from umbilical cords content of trypsin inhibitors and lectins than tepary beans. The Ellagic acid, robinetin, Inhibition of the Chang et al. (1985) quercetin, and tumorigenicity of BP-7,8-diol- percent cellularity on rat epithelial cells was significantly different myricetin 9,10-epoxide-2 on mouse skin among protein extracts from different bean cultivars and ranged and in the newborn mouse between 54% and 87%, suggesting that the incorporation of tepary Caffeic acid Inhibits oxidation of LDL Nardini et al. (1995) beans in the diet would not alter the current nutritional contribu- in vitro Suppressed the growth of Chung et al. (2004) tion of common beans or introduce adverse toxic effects. HepG2 tumor xenografts in The content of a-amylase inhibitors differs greatly among le- nude mice in vivo gumes, with the highest amounts found in dry beans. a-Amylase Ferulic acid Elevate the activities of Kawabata et al. inhibitor was found in common beans and runner beans (Phaseolus detoxifying enzymes, namely (2000) coccineus) at levels of 2–4 g kg1 of seed meal. Field beans, black- glutathione S-transferase and 1 lower incidences of colonic eyed peas, and chickpeas contain low levels of 0.1–0.2 g kg of carcinomas induced by seed meal. In lentils, soybeans, peas, winged beans, lima beans azoximethane in vivo (Phaseolus lunatus), and adzuki beans a-amylase inhibitor activity Luteolin Inhibition of alpha-glucosidase Kim et al. (2000) was undetected (Genovese & Lajolo, 1998; Grant, Edwards, & Pusztai, and amylase 1995b; Grant et al., 1995a; Mancini & Lajolo, 1981; Sgarbieri & Whitaker, 1982). Screening of 150 Brazilian bean varieties classified by color revealed average values between 0.19 and 0.29 bean protein (34% and 21%, respectively), and around 0.6% of the a-amylase inhibitor unit mg1 of protein (Table 12) with no corre- total protein (24–25%) in garden peas. Lectin from kidney bean lation between inhibitory activity and seed coat color (Lajolo et al., seeds directly inhibits HIV-1 reverse transcriptase, an enzyme cru- 1991). cial for HIV replication, as well as b-glucosidase, which has a role in HIV-1 envelope protein gp120 processing, therefore a very potent 3.3. Nutritional and physiological effects element of the antiretroviral chemotherapy. González De Mejía and Prisecaru (2005) compared the levels of Legumes are very rarely consumed by humans without heat antinutritional components and cytotoxic effect of extracts from treatment, and the effects of the consumption of individual compo- tepary and common beans (Table 11). Antinutritional factors were nents cannot always be related to those of a mixture, as normally evaluated by determining their effect on the viability of epithelial present in a diet (Lajolo & Genovese, 2002). 468 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Table 12 raw kidney bean (Phaseolus vulgaris), greatly reduced the growth a-Amylase inhibitory activity of P. vulgaris classified by bean color. of a murine non-Hodgkin lymphoma tumor in the mouse, either Bean color Specific inhibitory activity (AIUa mg1 of protein) as an intraperitoneal ascites tumor or as a solid subcutaneous tu- Range Average mor. The reduced growth rate occurred in a dose-dependent man- ner (Pryme & Bardocz, 2001). The number of Krebs II tumor cells in Pale brown 0.16–0.40 0.29 Brown 0.14–0.35 0.29 the ascitic fluid of mice fed a control diet for 8 d was three times Beige 0.14–0.40 0.26 higher than in mice fed a PHA diet. Feeding PHA for less than 8 d Light brown 0.09–0.32 0.20 after the injection of tumor cells also led to a reduction in tu- Dark brown 0.19–0.33 0.25 mor-cell growth (Bardocz et al., 1997). Black 0.11–0.30 0.19 Inclusion of raw kidney bean in the diet of obese rats reduced Red 0.16–0.37 0.25 Pink 0.16–0.28 0.21 lipid accumulation that was related to a decrease of insulin levels White 0.14–0.33 0.23 caused by lectins. However, no body or muscle protein losses oc- Purple 0.17–0.22 0.19 curred, even at high doses, as with normal rats, suggesting a possi- a An a-amylase inhibitory unit (AIU) value of 10 is defined as a 50% decrease in ble use of lectins as therapeutic agents to treat obesity (Pusztai enzyme activity at 37 °C/5 min after addition of 1% starch as substrate. From Lajolo et al., 1998). The most recent EUREKA study showed that red kid- and Genovese (2002). ney bean lectin given as an additive to piglets at 11–12 days old greatly enhanced successful weaning at 28 days. This result was achieved by stimulating the digestive tract thereby accelerating Administration of a black bean inhibitor in a starch meal by stom- the production of mature intestinal cells faster (Thomsson, Rantzer, ach tubing slowed starch digestion with reduction of serum glucose Weström, Pierzynowski, & Svendsen, 2007). Wean age is a critical and insulin concentrations and increased metabolism of nonesteri- factor in pig health, litter size and economy of hog operations. fied fatty acids from the adipose tissue in rats (Lajolo et al., 1991). These effects were also observed for diabetic rats (Menezes & Lajolo, 1987). A reduction of calorie utilization from the diet was also ob- 4. Minerals and vitamins served in mid-term experiments with rats with restricted calorie ingestion (Lajolo et al., 1984). Similarly, Pusztai et al. (1995) re- 4.1. Biological functions of minerals ported reduced utilization of dietary starch and protein for rats in a 10-day experiment with purified a-amylase inhibitor. The determination of minerals and trace elements in foodstuffs Some legume and cereal lectins can inhibit the growth of exper- is an important part of nutritional and toxicological analyses. Cop- imental animals and reduce the digestibility and biological value of per, chromium, iron, and zinc are essential micronutrients for hu- dietary proteins (Balint, 2000; Grant, Alonso, Edwards, & Murray, man health. In addition, these elements play an important role in 2000). These antinutritional effects are most likely caused by some human metabolism, and interest in these elements is increasing to- lectins that can impair the integrity of the intestinal epithelium gether with reports of relationships between trace element status (Reynoso-Camacho, Gonzalez de Mejia, & Loarca-Pina, 2003) and and oxidative diseases (Fennema, 2000). Copper can be found in thus alter the absorption and utilization of nutrients (Radberg many enzymes, some of which are essential for Fe metabolism. et al., 2001). The administration of lectins to experimental animals Deficiencies of Cu are infrequent. However, various studies have can also alter the bacterial flora (Pusztai, 1996). Thus, dietary lectins reported a direct correlation between the dietary Zn and Cu ratio have generally been considered to be toxic and antinutritional fac- and the incidence of cardiovascular disease. Chromium is involved tors. However, many lectins are non-toxic, such as those from toma- in carbohydrate and lipid metabolism; the most frequent sign of Cr toes, lentils, peas, chickpeas, faba beans, and other common foods. deficiency is altered glucose tolerance. This nutrient has also been Several studies have suggested a strong correlation between associated with diabetes and cardiovascular disease (Neilson, certain lectin-binding patterns and their biological behavior in var- 1994). Provisionally, a daily intake of 50–200 mg Cr has been rec- ious tumors (Table 13). Vicia faba agglutinin (VFA), a lectin present ommended for adults (National Research Council, 1989). Iron is an in broad beans, aggregated, stimulated the morphological differen- essential element, although Fe metabolism occurs in a ‘close cir- tiation, and reduced the malignant phenotype of colon cancer cells cuit’, there exist physiological losses which must be compensated. (Jordinson, El-Hariry, Calnan, Calam, & Pignatelli, 1999). The inclu- When the Fe amount supplied does not satisfy the requirement, Fe sion in the diet of phytohemagglutinin (PHA), a lectin present in deficiency ensues. The recommended daily intake in adults is 10–15 mg Fe (National Research Council, 1989). Zinc enzymes partic- ipate in a wide variety of metabolic processes including carbohy- Table 13 drate, lipid and protein synthesis or degradation. The metal is Inhibitory effects of some pulse lectins on malignant cells in vitro.* required for deoxyribonucleic and ribonucleic acid synthesis; it

Lectin Tumor cells Type of effect References may also play a role in stabilizing plasma membranes (Shils, Olson, & Shike, 1994). Zinc has been recognized as a co-factor of the Con A Merkel cell skin Direct contact/adhesion/ Sames et al. carcinomas binding to cell membrane (2001) superoxide dismutase enzyme, which is involved in protection or receptors against oxidative processes (Shils et al., 1994). The net delivery LCA H3B human hepatoma Cytotoxicity/tumor Wang, Ng, Ooi, of Zn to an organism is a function of the total amount of this ele- Merkel cell skin inhibition Direct contact/ and Liu (2000) ment in foods and its bioavailability. The recommended daily in- carcinomas adhesion/binding to Sames et al. take for adults is 12–15 mg (National Research Council, 1989); cellmembrane or (2001) receptors certain groups of people can be at risk with regard to Zn nutrition. PHA SK-MEL-28, HT-144 and (Cytotoxicity/ Lorea et al. C32 human melanoma tumorinhibition) (1997) Hs729 (HTB-153) human Cytotoxicity/tumor Remmelink 4.2. Levels of minerals in pulses rhabdomyosarcoma and inhibition, (direct contact/ et al. (1999) SK-UT-1 and SK-LMS-1 adhesion/binding to cell Legumes supply adequate protein while being a good source of human leiomyosarcoma membrane or receptors) vitamins and minerals (Fennema, 2000). Mineral contents of le- Adapted from Gonzalez De Mejia and Prisecaru (2005). gumes (Table 14) indicate that beans and lentils have the highest * Note. Parentheses ( ) indicate weak effects. iron (110 and 122 lgg1, respectively), and zinc contents (44 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 469 and 48 lgg1, respectively). The levels of minerals in legumes Legumes also contain compounds that lower the nutritional va- generally range between 1.5–5.0 lgCug1, 0.05–0.60 lgCrg1, lue of a food by lowering the digestibility or bioavailability of 18.8–82.4 lgFeg1, 32.6–70.2 lgZng1, 2.7–45.8 lgAlg1, nutrients. Phytate, and some of the degradation products of phy- 0.02–0.35 lgNig1, 0.32–0.70 lgPbg1 and not detectable– tate, are well-known inhibitors of absorption of essential dietary 0.018 lgCdg1 (Table 15)(Cabrera, Lloris, Giménez, Olalla, & minerals; in particular non-haem iron and Zn. Certain Fe-binding López, 2003). The content of Fe and other minerals is generally polyphenols are potent inhibitors of non-haem iron absorption. high in legumes with beans having the highest mineral content On the other hand, certain polyphenols are able to complex-with (Table 16). Fe, rendering the complex-bound Fe unavailable for absorption Selenium (Se) is an essential micronutrient in human nutrition (Hurrell, Reddy, & Cook, 1999). However, the absorption of miner- and is involved in important regulatory and protective mecha- als depends on the total composition of the meal. In a balanced diet nisms (Schwarz & Foltz, 1957). There is a great necessity for food containing animal protein, a high intake of legumes does not imply systems to provide at least 55 lg per day for maximal expression a risk of inadequate mineral supply. In the modern food industry, of Se enzymes, and large populations in some parts of the world the phytate content of soya-based infant formulas is of concern; are Se deﬁcient. Se deﬁciency compromises the health of develop- major efforts are therefore being made to remove phytate. Once ing children and reduces the ability to combat the effects of heavy phytate is degraded, legumes would become good sources of Fe metals in the human diet (Spallholz, Mallory Boylan, & Rhaman, and Zn as the content of these minerals is high (Sandberg, 2002). 2004). Thavarajah, Ruszkowski, and Vandenberg (2008) showed that Saskatchewan-grown lentils contain 425–673 lg/kg1 of Se 4.3. Vitamin contents in pulses depending on location, soil characteristics, and growing conditions (Table 17). This potentially provides 80–120% of the minimum rec- Legumes constitute an important part of the human diet in ommended daily Se intake in only 100 g of dry lentils. many parts of the world and are sources of vitamins. (Shils, Olson,

Table 14 Copper, iron, and zinc content (lgg1) in legumes and food composition tables.

Sample Origin Copper Iron Zinc Reference Beans Spain – 62.0 35.0 Mataix and Mañas (1998) Spain – – 35.4 ± 2.8 Terrés et al. (2001) Spain – 62.0 35.0 Ministerio de Sanidad y Consumo (1999) Germany 0.14b 0.83b 0.18b Souci, Fachmann, and Kraut (2000) India 9–22 108–150 50–109 Vadivel and Janardhanan (2000) UK 3.2 ± 0.7 68 ± 1.6 44 ± 1.2 Elhardallon and Walker (1992) UK 10.9 42.0 50.5 Holland, Unwin, and Buss (1992) Italy – 57.9 ± 2.0 32.9 ± 4.0 Lombardi-Boccia, Carbonaro, Di Lullo, and Carnovale (1994) – 2.1–2.4 22.5–33.7 10.1–11.6 Fennema (2000) Broad beans Spain – 55.0 31.0 Mataix and Mañas (1998) UK 9.1 ± 0.7 110 ± 3.2 58 ± 2.7 Mataix and Mañas (1998) Chickpeas Spain – – 33.5 ± 3.6 Terrés et al. (2001) Spain – 68.0 10.0 Ministerio de Sanidad y Consumo (1999) Spain 3.51 72.0 8.0 Souci, Fachmann, and Kraut (1994), Jimenez, Cervera, and Bacardí (1998) Lentils Spain – – 45.1 ± 14.2 Terrés et al. (2001) Spain – 82.0 37.0 Mataix and Mañas (1998) Spain 2.5 70.0 55.0 Jimenez et al. (1998) Spain – 82.0 37.0 Ministerio de Sanidad y Consumo (1999)

France – 80.0 – Feinberg, Favier, and Ireland-Ripert (1995) UK 9.1 ± 0.7 122 ± 4.1 48 ± 1.0 Elhardallon and Walker (1992) UK 10.2 111.0 39.0 Holland et al. (1992) Green peas Spain 19.0a 7.0a Mataix and Mañas (1998) Spain 1.75a 19.0a 7.0a Jimenez et al. (1998)

Modiﬁed from Cabrera et al. (2003). a Fresh wt. b Results are expressed as mg M J1.

Table 15 Mineral content (lgg1 of the edible portion) of legumes.

Legume Copper Chromiun Iron Zinc Aluminium Nickel Lead Cadmium Lentil 2.5 0.31 71 56.5 30.2 0.24 0.51 0.009 Bean Haricot bean 2.8 0.15 62.5 39.7 13.4 0.15 0.62 0.0005 Kidney bean 3 0.17 64.4 46.9 19 0.17 0.69 0.007 Broad bean 4.3 0.28 80 41.2 6.7 0.17 0.4 0.012 Chickpea 3.5 0.12 68.8 39.2 10.2 0.26 0.48 0.01 Green peas Fresh 1.7 0.08 20.2 38.9 6.5 0.05 0.37 NDa Canned 1.8 0.09 24.6 58.8 15.5 0.07 0.45 0.015

Adapted from Cabrera et al. (2003). a Not detectable. 470 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Table 16 Mineral content (mg kg1) of dry bean cultivars.

Cultivar MK Ca Mg K P B Cu Zn Fe Mn AC Cruiser Navy 1381de 2002b 17286f 6207b 13.7b 8.8a 25.0c 55.0b 13.3d AC Earlired Small red 1344ef 1677f 17305f 5727d 11.3c 0.4h 18.9e 34.1e 13.2d AC Mast Navy 1649b 1952c 17944d 6564a 11.1c 3.1e 18.3e 44.1de 15.8c AC Ole Pinto 1328f 1758e 18638b 6194b 10.2e 3.6d 21.5d 43.6d 13.3d CDC Jet Black 1229g 1843d 16166h 5044f 10.5de 2.4f 26.6b 46.1cd 13.8d Envoy Navy 2025a 1841d 16945g 5695d 9.4f 6.1c 27.1ab 53.3bc 17.2b Galley Navy 2035a 2078a 19464a 6447a 10.9cd 1.0g 21.2d 42.2d 19.4a Onyx Black 1408d 1746e 18428c 5483e 14.7a 0.1i 18.8e 49.4bcd 13.3d Resolute Great Northern 1516c 1693f 17585e 6034c 10.2e 0.9g 18.5e 28.0e 13.5d ROG 802 Dark Red Kidney 823h 1525g 17090g 5660d 11.1c 7.1b 28.3a 66.6a 10.8e Means Black 1300x 1804x 17070y 5220y 12.2x 1.5y 23.5x 47.4x 13.6x Navy 1749x 1958x 17768x 6209x 11.3x 5.1x 23.1x 49.2x 16.2x Overall mean 1456 1804 17595 5901 11.2 3.6 22.6 46.3 14.2

Means in a column with different letters are signiﬁcantly different (p < 0.05). From Oomah et al. (2008).

Table 17 Table 18 1 Comparison of total Se concentration in 19 lentil genotypes grown in Saskatchewan, Vitamin composition (mg 100 g dry weight) in nine commercial Phaseolus vulgaris. Canada, in 2005 and 2006. Raw Cooked a Genotype Selenium concentration %RDA (100 g of lentil) Thiamin 0.81–1.32 0.64–1.06 1 lgkg Riboﬂavin 0.112–0.411 0.086–0.246 Saskatoon Kyle Meanb North America Europe Niacin 0.85–3.21 0.59–1.96 2005 2006 55 lg day1 65 lg day1 Vitamin B6 0.299–0.659 0.200–0.515 Folic acid 0.148–0.676 0.088–0.521 CDC Robin 2104 2012 672 122 103 Adapted from Augustin et al. (1981). Sedley 1446 2127 612 111 94 Grandora 1694 2351 612 111 94 Greenland 1064 2609 544 99 84 Imperial 1246 1884 538 98 83 Table 19 1 Redberry 1947 1583 533 97 82 Folate content (lg100 g dry weight) of chickpeas and peas, and the water used for a Sovereign 2503 2364 533 97 82 processing. Plato 1178 2035 532 97 82 Samples Undeconjugate folatesc Total folatesc Meteor 1483 1470 510 93 78 Blaze 1413 2119 509 93 78 Chickpea Rosetown 1005 1942 505 92 78 Raw 121.5 c 149.7 c b Richlea 900 2008 498 91 77 Boiled 63.3 a (52.1) 78.8 a (52.6) Impact 1136 1844 491 89 76 Pressure-cooked 73.8 b (60.7) 93.0 b (62.1) Viceroy 1009 1685 471 86 72 In medium Milestone 1186 1236 457 83 70 Soaking water 21.8 a (17.9) 25.9 a (17.3) Rouleau 1271 1585 431 78 66 Boiling water 32.4 b (26.7) 42.2 c (28.2) Eston 901 1555 425 77 65 Pressure cooking water 24.6 a (20.2) 29.7 b (19.8) Laird 1232 1970 593 108 91 Red chief 1429 1421 472 86 73 Peas Raw 87.5 b 101.5 b Mean 1324 1884 Boiled 38.9 a (44.5)b 45.7 a (45.0) Pressure-cooked 43.4 a (49.6) 51.5 a (50.3) From Thavarajah et al. (2008). a %RDA is calculated based on the mean total Se concentrations across eight In medium locations (n = 912) in Saskatchewan. Soaking water 18.3 a (20.9) 21.0 a (20.7) b Values represents mean of 8 locations for 2 years. Boiling water 27.8 c (31.8) 32.3 c (31.8) Pressure cooking water 22.7 cb (25.9) 27.5 b (27.1)

Shike, & Ross, 1999).The variation of vitamins content in nine com- Adapted from Dang et al. (2000). mercial Phaseolus vulgaris classes were evaluated by Augustin, a Values are the mean of six replicate determinations. b Beck, Kalbfleish, Kagel, and Matthews (1981). The raw bean sam- Figures in parentheses represent precent retention of folates (in chickpeas or peas) or loss of folates (in medium). ples contained 0.99 mg of thiamin, 0.20 mg riboflavin, 1.99 mg nia- c Significance of LSD between means at p < 0.05. With columns, means followed cin, 0.49 mg vitamin B12, 0.30 mg folic acid, but only 70–75% of by different letters are significantly different. water-soluble vitamins were retained in cooked seeds (Table 18). Legumes are very good sources of folates which are not readily available due to complex binding with bio-molecules (Kadam & peas and peas respectively, indicating that some folates may have Salunkhe, 1989). Beans are excellent source of folate at 400– leached in the water used for processing. FDA (1996) authorized 600 mcg representing 95% of daily requirements. Higher folate in- voluntary folic acid fortification of enriched grain products to pre- take has been inversely associated with the risk of colon cancer vent neural tube defects (NTD). Folic acid fortification (1995–2002) (Giovannucci et al., 1998). Folate is a methyl donor, and in rodent led to 34–36% drop in NTD among Hispanic and white non-His- models, methyl deficient diet may result in hypomethylation and panic babies. Current folic acid requirement is set at 140 lg therefore loss of regulation of proto-oncogenes (Giovannucci & 100 g1 grains, while clinicians recommend 400 lg day1 for wo- Willett, 1994). Chickpeas have higher content of folates compared men of childbearing age. with peas according to Dang, Arcot, and Shrestha (2000) (Table 19). Pulses are good source of thiamine, riboflavin, niacin, pyridox- Folate contents in raw chickpeas and peas were 149.7 and 101.5 lg amine, pyridoxal and pyridoxine. Lentils var., variabilis have 100 g1, respectively, and 78.8 and 45.7 lg 100 g1 in boiled chick- 0.647, 0.062, and 0.93 mg 100 g1 d.m. of thiamine, riboflavin, R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 471 and niacin, respectively; while Vicia faba var., major have 0.253, Yoshida, Saiki, & Mizushina, 2008). Food legumes generally contain 0.123, and 2.233 mg 100 g1 d.m. of thiamine, riboflavin, and nia- only 1–2% lipids with the unsaponifiable fraction of the oil ranging cin, respectively (Table 20)(Prodanov, Sierra, & Vidal-Valverde, from 0.5% to 4% (Harborne, Boulter, & Turner, 1971). The lipid con- 1997; Vidal-Valverde, Sierra, Diaz-Pollan, & Blazquez, 2001). Most tents of seeds of eight Vicia species collected in Turkey varied be- plant-derived foods contain low to moderate levels of vitamin E tween 2.5% and 3.9% with palmitic (7–23%) and stearic (15–35%) activity. However, owing to the abundance of plant-derived foods acids as the major fatty acids (Akpinar, Akpinar, & Türkog˘lu, 2001). in our diets, they provide a significant and consistent source of vitamin E (Eitenmiller & Lee, 2004). Tocopherol content is higher 6. Phytosterols in seeds and legumes than cereals. Peas contain greater amounts 1 of a than b + c-tocopherols (10.4 and 5.7 mg 100 g , respectively) In pulses, phytosterols are present in small quantities, and the and chickpeas contain similar levels of a- and b + c-tocopherols most common phytosterols are b-sitosterol, campesterol, and stig- 1 (6.9 and 5.5 mg 100 g , respectively) (Table 22)(Ryan, Galvin, masterol (Benveniste, 1986). These compounds are also abundant O’Connor, Maguire, & O’Brien, 2007). as sterol glucosides and esterified sterol glucosides, with b-sitosterol representing 83% of the glycolipids in defatted chickpea flour 5. Fatty acids (Sanchez-Vioque, Clemente, Vioque, Bautista, & Millan, 1998). Ryan, Galvin, O’Connor, Maguire, and O’Brien (2007) recently re- Legume seeds contain 2–21% fat with beneficial composition of ported the phytosterols content in legumes. Total phytosterol con- exogenic unsaturated fatty acids: linoleic (21–53%) and linolenic tent detected in the legumes ranged from 134 mg 100 g1 (kidney (4–22%) acids. These seeds also contain high levels of vitamin E: beans) to 242 mg 100 g1 (peas). Total b-sitosterol content ranged 12–187 i.u. kg1 feed and 470–2560 i.u. kg1 oil. Common beans from 160 mg 100 g1 (chickpeas) to 85 mg 100 g1 (butter bean). are an important source of free unsaturated fatty acids accounting Chickpeas and peas contained high levels of campesterol (21.4 for 61.1% of total fatty acids (FA). The major fatty acids are palmitic and 25.0 mg 100 g1, respectively). Stigmasterol content is higher (16:0), oleic (18:1), and linoleic (18:2). The major acid among the in butter beans (86 mg 100 g1) and squalene content in peas unsaturated FA is linolenic (18:3) acid, there is 43.1% in FA of the (1.0 mg 100 g1)(Table 22). Weihrauch and Gardner (1978) re- common bean (Grela & Gunter, 1995). The main fatty acid present ported similar phytosterol levels for kidney beans at 127 mg in legumes is linoleic (18:2), followed by linolenic (18:3). Chick- 100 g1, with much lower concentration of phytosterols for chickpeas have the highest MUFA content (34.2 g 100 g1); while butter peas, 35 mg 100 g1 as opposed to 205 mg 100 g1 in the present bean has the highest SFA content (28.7 g 100 g1) and kidney beans study. Butter beans and kidney beans contained high levels of stig- have the highest content of PUFA (71.1 g 100 g1)(Table 21)(Ryan, masterol (86.2 and 41.4 mg 100 g1, respectively). Galvin, O’Connor, Maguire, & O’Brien, 2007). Adzuki beans grown The consumption of pulse grains has been reported to lower in Japan contained 2.2% fat consisting mainly of phospholipids serum cholesterol and increase the saturation levels of cholesterol (63.5%), triglycerides (21.2%), steryl esters (7.5%), hydrocarbons in the bile. A dietary study conducted by Duane (1997) on humans (5.1%), diacylglycerols (1.3%), free fatty acids (0.9%), and other min- over a seven week period showed that serum LDL cholesterol was or components. The principal fatty acid composition of adzuki bean significantly lower during the consumption of a diet consisting of lipids were linoleic, palmitic and linolenic acids representing 45%, beans, lentils, and field peas. The study showed that consumption 25%, and 21%, respectively, of the total lipids (Yoshida, Tomiyama, of pulses lowers LDL cholesterol by partially interrupting the

Table 20 Thiamine, riboﬂavin and niacin (mg 100 g1 d.m.), pyridoxamine, pyridoxal and pyridoxine (lg 100 g1 d.m.) contents in pulses.

Legume Thiamine Riboﬂavin Niacin Pyridoxamine Pyridoxal Pyridoxina Lentis culinaris var. vulgaris 0.433 ± 0.005 0.061 ± 0.004 2.01 ± 0.05 Lentis culinaris, var. variabilis 0.647 ± 0.006 0.062 ± 0.001 0.93 ± 0.05 Vicia Faba, var. major 0.253 ± 0.003 0.123 ± 0.008 2.23 ± 0.008 Faba beans 2.79 ± 0.01 Peas 3.15 ± 0.08 Lupins 2.05 ± 0.09 Lentils 63.3 ± 2.6 94.2 ± 2.8 44.2 ± 2.5 Chickpeas 26.9 ± 0.8 74.8 ± 2.3 23.5 ± 1.3 Haricot beans 64.5 ± 1.2 128.8 ± 1.6 24.0 ± 0.2 *Beans (raw) 0.81–1.32 0.112–0.411 0.85–3.21 *Beans (cooked) 0.64–1.06 0.086–0.246 0.59–1.96

Adapted from Prodanová and Vidal-Valverde (1997), Vidal-Valverde et al. (2001). * From Augustin et al. (1981).

Table 21 Total oil (g 100 g1) and fatty acid composition (% of total) of pulses.

Sample Total oil Fatty acid 16:0 16:1 17:0 18:0 18:1 18:2 18:3 20:0 20:1 22:0 22:1 SFA MUFA PUFA Butter bean 0.9 23.68 0.20 0.37 3.62 10.35 42.43 18.64 ND ND 0.30 ND 28.7 10.5 60.8 Chickpeas 5.0 10.87 0.23 0.06 1.85 33.51 49.74 2.41 0.60 0.39 0.21 Tr 13.7 34.2 52.1 Kidney beans 1.2 14.20 0.16 0.22 1.30 11.97 26.04 45.69 0.24 ND 0.51 ND 16.5 12.1 71.7 Lentils 1.4 14.57 0.09 0.13 1.24 22.95 47.17 11.67 0.44 0.70 0.28 ND 16.7 23.7 58.8 Peas 1.5 10.65 0.07 0.19 3.11 28.15 47.59 9.29 0.22 0.21 ND ND 14.7 28.4 56.9

SFA, saturated fatty acids; MUFA, monosaturated fatty acids; PUFA, polysaturated fatty acids; ND, not detected; Tr, trace amounts. Adapted from Ryan, Galvin, O’Connor, Maguire, and O’Brien (2007). 472 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Table 22 Tocopherol, phytosterols, and squalene (mg 100 g1) in legumes.

Legumes a-Tocopherol b + c-Tocopherol b-Sitosterol Campesterol Stigmasterol Squalene Butter beans 0.7 ± 0.18 4.7 ± 0.40 85.1 ± 7.3 15.2 ± 2.9 86.2 ± 5.7 0.4 ± 0.02 Chickpeas 6.9 ± 0.04 5.5 ± 0.72 159.8 ± 7.1 21.4 ± 0.7 23.4 ± 0.7 0.5 ± 0.03 Kidney beans 1.2 ± 0.16 2.6 ± 0.13 86.5 ± 2.6 6.5 ± 0.8 41.4 ± 1.6 0.7 ± 0.05 Lentils 1.6 ± 0.43 4.5 ± 0.11 123.4 ± 4.1 15.0 ± 0.4 20.1 ± 0.6 0.7 ± 0.15 Peas 10.4 ± 0.09 5.7 ± 0.64 191.4 ± 0.4 25.0 ± 6.9 26.0 ± 0.6 1.0 ± 0.07

Adapted from Ryan et al. (2007). entrohepatic circulation of the bile acids and increasing the choles- The phytate content of some legumes is shown in Table 23 terol saturation by increasing the hepatic secretion of cholesterol. (Morris & Hill, 1996; Rochfort & Panozzo, 2007). Inositol phosphate

The study concluded that other pulse components in the diet (InsP) in raw dry legumes was: InsP3 28%, InsP4 10%, InsP5 4%, and may also have contributed to the observed effect; in particular, InsP6 2%; and in cooked dry legumes: 8, 4, 2, and 2%, respectively. 1 saponins, which are hydrolyzed by intestinal bacteria to diosgenin, Raw lentils contained 0.3 mmol kg of InsP3. The highest InsP4 may have exerted a positive effect (Fenwick & Oakenfull, 1983; concentration in raw legumes was 0.26 mmol kg1 in blackeye Thewles, Parslow, & Coleman, 1993). Several studies have demon- peas and accounted, on the average, for only slightly more than strated the efﬁcacy of plant sterols and stanols in the reduction of 1% of the total inositol phosphates in raw, dry legumes. The mean 1 blood cholesterol levels, and plant sterols are increasingly incorpo- InsP5 concentration in raw, dry legumes is 1.9 mmol kg , ranging rated into foods for this purpose (Gylling & Miettinen, 2005; from 1.36 to 2.52 mmol kg1 in green split peas and blackeye peas, Thompson & Grundy, 2005). respectively, accounting for an average of 16% of total inositol phosphates. The most abundant inositol phosphate in raw, dry le-

gumes is InsP6, accounting for an average of 83% of the total inosi- 7. Phytic acid tol phosphates, ranging from 77% in chickpeas to 88% in black

beans. The InsP6 concentration tends to be higher in raw dry beans, 7.1. Biological function blackeye peas, and pigeon peas than in lentils, green and yellow split peas, and chickpeas and ranged between 14.2 and Phytic acid (myo-inositol hexaphosphate or InsP6), a major 6 mmol kg1 in black beans and chickpeas, respectively (Morris & phosphorus storage form in plants, and its salts known as phytates Hill, 1996). Oomah, Blanchard, and Balasubramanian (2008) re- regulate various cellular functions such as DNA repair, chromatin ported that phytic acid expressed as InsP6 represents 75% of the to- remodeling, endocytosis, nuclear messenger RNA export and tal phosphorous in several Canadian bean varieties. Varietal and potentially hormone signaling important for plant and seed devel- agronomic factors, alone and in combination, often result in a wide opment (Zhou & Erdman, 1995), as well as animal and human variation in phytate content of mature legume seeds and cereal nutrition (Vucenik & Shamsuddin, 2006). It is often regarded as grains (Dintzis, Lehrfeld, Nelsen, & Finney, 1992; Mason, Weaver, an anti nutrient because of strong mineral, protein and starch bind- Kimmel, & Brown, 1993). ing properties thereby decreasing their bioavailability (Weaver & Chen (2004) reported InsPn contents in beans. Among InsPn, Kannan, 2002). Enzymatic degradation of phytic acid by exogenous only InsP6 and InsP5 were detected in all beans. There was a wide phytase is already used in feed, particularly to improve mineral variation in the InsP6 or InsP5 content among different types of raw and protein utilization (Graf & Eaton, 1990), simultaneously reduc- dry black beans or red kidney beans. InsP6 content (per kg, ad- ing excessive phosphorus accumulation in the environment (Grases justed by moisture) in raw dry beans ranged from 5.87 to et al., 2006). Phytate play important role in plant metabolism, 14.86 mmol in mung beans and black beans, respectively, and from stress and pathogen resistance in addition to their beneﬁcial effects 5.21 to 9.75 mmol in cooked mung beans and black beans, respec- in human diets by acting as anticarcinogens or by promoting tively. InsP6 was the predominant inositol phosphate of the total health in other ways such as in decreasing the risk of heart disease InsPn determined in raw dry beans, ranging from 63.9% in red kid- or diabetes (Welch & Graham, 2004 and references therein). ney beans to 97.5% in pinto beans, and in the selected cooked InsP6 – the most abundant inositol phosphate in dry legumes is beans, ranging from 81.2% in mung beans to 88.2% in black beans. considered the anticancer agent. However, procedures that can dif- Of the four possible InsP5 isomers (excluding enantiomers), DL- ferentiate among the 6 forms of InsP have been developed only re- Ins(1,2,4,5,6)P5 was dominant in raw dry beans, followed by cently. InsP6 accounts for an average of 88% of the total inositol Ins(1,3,4,5,6)P5, DL-Ins(1,2,3,4,5)P5, and Ins(1,2,3,4,6)P5, if present, phosphates in black beans (Morris & Hill, 1996). Inositol hexaphos- which indicated that there probably were some common proﬁles phate is important in the cell-signaling process and may be in- at least for raw dry beans. The determination results of InsP6 in volved in induction of cell differentiation, apoptosis, chromatin raw dry and cooked beans are very comparable to the literature remodeling, anticarcinogenic action, and other biological effects values, which were summarized by Phillippy (2003). (Shamsuddin & Vucenik, 2005). 7.3. Phytic acid and health 7.2. Phytate levels in pulses In vivo and in vitro studies have demonstrated that inositol

Phytate constitutes 1–3% of cereal grains, legume seeds and hexaphosphate (InsP6, phytic acid) exhibits signiﬁcant anticancer nuts, and also occurs in low concentrations in roots, tubers and (preventive as well as therapeutic) properties. It reduces cell prolif- vegetables. In particular, wholegrain cereals and legumes have a eration and increases differentiation of malignant cells with possi- high content of phytate but also of the minerals Zn, Fe, and Mg ble reversion to the normal phenotype and is involved in host (Sandberg, 2002). In legume seeds, phytate is located in the protein defence mechanism, and tumor abrogation (Shamsuddin, 2002). bodies in the endosperm. Phytate occurs as a mineral complex, InsP6 has been suggested to be responsible for the epidemiological which is insoluble at the physiological pH of the intestine (Fredlund, link between high-ﬁbre diets (rich in InsP6) and low incidence of Isaksson, Rossander-Hulthén, Almgren, & Sandberg, 2006). some cancers. Phytic acids delay postprandial glucose absorption, R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 473

Table 23 synthesized more rapidly than phosphatidyl-myo-inositol in barley 1 Phytate content (lmol g ) in pulses. seeds (Carstensen, Pliska Matyshak, Bhuvarahamurthy, Robbins,

Food legume IP3 IP4 IP5 IP6 & Murthy, 1999), but little is known about the metabolism or func- Baby lima beans Raw ND 0.23 2.13 9.96 tion of D-Chiro-inositol in animals. D-Chiro-inositol, which may be of Cooked 0.25 1.08 3.07 7.08 benefit to diabetics (Steadman et al., 2000), and myo-inositol levels Black beans Raw ND 0.13 1.87 14.2 in urine of older men and women, appear to be related to insulin Cooked 0.18 0.98 3.62 9.96 secretion (Campbell, Ostlund, Joseph, Farrell, & Evans, 2001). Black peas Raw 0.01 0.26 2.52 12.6 Myo-inositol and InsP6 have synergistic or additive effects in inhib- (Cowpeas) Cooked 0.22 0.89 3.38 9.67 iting the development of cancer (Shamsuddin, 1999). In mice, die- Chickpeas Raw ND 0.04 1.76 6.00 tary myoinositol has been shown to be effective in preventing (Garbanzo beans) Cooked 0.10 0.56 2.04 5.18 cancer of the lung (Wattenberg et al., 2000), forestomach (Estensen Great northern beans Raw ND 0.19 2.19 12.7 & Wattenberg, 1993), liver (Nishino et al., 1999) colon, mammary Cooked 0.23 1.05 3.60 9.24 gland, prostate, and skin (Jenab & Thompson, 1998; Jenab & Green split peas Raw ND 0.17 1.36 6.48 Thompson, 2002; Shamsuddin, 1999). Cooked 0.07 0.45 1.73 4.93 Lentils Raw 0.32 0.21 1.39 8.37 Cooked 0.44 0.97 3.62 7.09 8. Saponins and oxalate Navy beans Raw ND 0.14 1.80 12.4 Cooked 0.13 0.68 3.07 8.80 8.1. Saponins structure Pigeon peas Raw ND 0.04 2.41 7.96 Cooked 0.22 0.96 2.77 5.97 Saponins have long been considered undesirable due to toxicity Pinto beans Raw ND 0.17 2.05 11.7 and their haemolytic activity. However, there is enormous struc- Cooked 0.20 0.91 3.33 8.14 tural diversity within this chemical class, and only a few are toxic Red chilli beans Raw ND 0.02 2.18 11.9 (Shi et al., 2004). They consist of a triterpene or steroid nucleus Cooked 0.07 0.81 3.37 10.1 (the aglycone) with mono- or oligosaccharides attached to this Red kidney beans Raw ND 0.16 1.84 13.5 core. Most of the saponins occur as insoluble complexes with 3- Cooked 0.19 1.02 2.81 9.12 b-hydroxysteroids; these complexes again interact with bile acid Roman beans Raw ND 0.02 1.95 10.6 and cholesterol, forming large mixed micelles (Oakenfull & Sidhu, Cooked 0.08 0.73 3.25 9.17 1989). In addition, they form insoluble saponin–mineral com- Yellow Peas Raw ND 0.12 1.49 8.82 plexes with iron, zinc, and calcium (Milgate & Roberts, 1995). Cooked 0.05 0.52 1.53 7.35 The most common saponins in legumes include the soya saponins, Field peas Raw 0.00 0.01 0.08 0.43 which are classified into group A, B, and E saponins on the basis of Cooked 0.01 0.02 0.10 0.33 the chemical structure of the aglycone (Rochfort & Panozzo, 2007). Pink beans Raw ND ND 0.60 13.07 Field peas were initially thought to contain soyasaponin I (S-I) (and Cooked ND ND 1.57 9.40 then soyasaponin VI (S-VI) as the only soyasaponin, but recently Mung beans Raw ND ND 1.18 5.87 field pea extracts were shown to contain dehydrosoyasaponin I Cooked ND ND 1.21 5.21 (D-I) as a minor component (Taylor & Richards, 2008). D-I from pea has insecticidal and antifeedant properties against stored ND – not detectable. Adapted from Morris and Hill (1996), Chen (2004), Phillippy (2003), Rochfort and product insect pests. This triterpenoid saponin dehydrosoyasapo- Panozzo (2007). nin I is a natural product present in chickpeas and other legumes and is known to be a potent calcium-activated potassium channel opener and as such can be used for treating cardiovascular, urolog- ical, respiratory, neurological, and other disorders (Taylor & reduce the bioavailability of toxic heavy metal such as cadmium Richards, 2008 and references therein). and lead, and exhibit antioxidant activity by chelating iron and copper (although phytic acid intake on improving antioxidant status in vivo remains unclear) (Minihane & Rimbach, 2002). Dietary 8.2. Saponins in pulses and endogenous phytic acid have protective effects against cancer and heart disease and may be responsible for the cancer-protective Saponins have been reported in many edible legumes, although effects of high-fibre foods (Fredlund et al., 2006; Grases et al., the detailed structures were not always established. They have 2001; Grases et al., 2006; Jenab & Thompson, 2002). The anticarci- been found in lupins (Woldemichael, Montenegro, & Timmermann, nogenic properties of phytic acid may result from numerous fac- 2003), lentils (Morcos, Gabriel, & El-Hafez, 1976; Ruiz et al., 1996), tors, including its ability to chelate metal ions; this depends on and chickpeas (El-Adawy, 2002), as well various beans, and peas the phytate retaining its integrity in the colon, a profuse microbial (Shi et al., 2004). ecosystem (Steer & Gibson, 2002). Saponin content may vary even among the same species of edi- The backbone of most inositol phosphates in cells is myo-inosi- ble beans, because of variations in cultivars, varieties (Khokhar & tol. An extensive review of the metabolism of myo-inositol in plants Chauhan, 1986), locations (Fenwick & Oakenfull, 1983; Price, Johnson, was published by Loewus and Murthy (2000). Inositol phosphates & Fenwick, 1987), irrigation condition, type of soil, climatic from seeds are a significant food source of myo-inositol, as are the conditions, and year during which they are grown. The saponin phospholipids and free inositol from many plant- and animal- content in various legumes is listed in Table 24. Chickpeas, black based foods (Berdanier, 1992). Myo-inositol has been evaluated grams, month bean, broad beans and peas can contain 3.6, 2.3, for its ability to improve the mental health of patients with various 3.4, 3.7, and 2.5 g kg1 dry matter of saponins, respectively (Khokhar psychiatric disorders (Einat & Belmaker, 2001; Kofman, Einat, & Chauhan, 1986). Saponin content in dehulled light and dark Cohen, Tenne, & Shoshana, 2000; Nemets, Fux, Levine, & Belmaker, colored peas ranges from 1.2 to 2.3 g kg1 dry matter (Daveby, 2001). In addition to myo-inositol, smaller amounts of epi- and scyl- Betz, & Musser, 1998). Some saponin is lost during processing as lo-inositol are present in human brains (McLaurin, Golomb, Jurewicz, has been reported in moth beans (Khokhar & Chauhan, 1986), black Antel, & Fraser, 2000). Phosphatidyl-scyllo-inositol appears to be grams (Kataria, Chauhan, & Punia, 1989), faba beans (Sharma & 474 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Table 24 Table 25 Saponin content of legume seeds. Oxalate content of legumes.

Common name Saponin content (g kg1 dry matter) Legumes Oxalate content (mg 100 g1 wet weight) Beans Beans Broad 0.1–3.7 Anasazi 80 Butter 1.0 Azuki 25 Field 0.03–3.5 Black 72 Green moth 3.3 Garbanzo 9 Haricot 2.3 Great northern 75 Kidney 2.16 Large lima 8 Moth 3.4 Mung 8 Mung 3.5 Navy 57 Navy 2–16 October 28 Red 0.02 Pink 75 Runner 3.5 Pinto 27 Red kidney 16 Peas Small red 35 Black-eyed 0.03 Small white 78 Green 1.8–11 Peas 2.5 Peas Snow 0.01 Blackeye 4 Yellow split 1.1–11 Green split 6 Black grams 2.3 Yellow split 5 Soy bean 5.6–56 Chickpeas 2.3–60 Adapted from Chai and Liebman (2005).

Adapted from Khokhar and Chauhan (1986), Price et al. (1987), Oakenfull and Sidhu (1990). wet weight), respectively (Hönow & Hesse, 2002; Massey, Palmer, & Horner, 2001). Sehgal, 1992) and pigeon peas (Duhan, Khetarpaul, & Bishnoi, 2001). 9. Others compounds of pulses

8.3. Saponins and health Within the last decade, melatonin (N-acetyl-5-methoxytrypta- mine) has been found to have various beneficial effects within cells Recent evidence suggests that legume saponins may possess and organisms. This has translated into protective actions against a anti-cancer activity (Chang, Yu, Lin, Wang, & Tsai, 2006; Ellington, number of experimental and clinical diseases (Blask, Sauer, & Dauchy, Berhow, & Singletary, 2006; Shi et al., 2004) and be beneficial for 2002; Gitto et al., 2001; Herrera, Romero, & Rodríguez-Iturbe, hyperlipidemia (Shi et al., 2004). In addition, they reduce the risk 2001; Lissoni, 2002; Pappolla et al., 2000). Melatonin is normally of heart diseases in humans consuming a diet rich in food legumes produced in vertebrates, most notably by the pineal gland and containing saponins (Geil & Anderson, 1994). Epidemiological thereafter discharged into the blood (Lewy, 1999; Reiter, 1980) studies suggest that saponins may play a role in protection from and the cerebrospinal fluid (CSF) as well (Skinner & Malpaux, cancer (Shi et al., 2004). Metastatic events are critical in cancer 1999). Given that pineal melatonin is produced most abundantly proliferation, and there is evidence that glycosylation is an impor- during the night in darkness (Reiter, 1991), likewise, blood and tant event in this process (Aubert et al., 2000). Chang et al. (2006) CSF melatonin levels are also higher at night than during the day. have recently demonstrated that soyasaponin I decreases the Recently, the presence of melatonin in some legumes (Zielínski, expression of R-2, 3-linked sialic acid on the cell surface, which Lewczuk, Przybylska-Gornowicz, & Kozowska, 2001) has been re- in turn suppresses the metastatic potential of melanoma cells. ported. The immunoreactive melatonin found in raw lentil seeds The observed anticancer activity may therefore in part be due to (122.7 pg g1) was lower than that reported in others plants. In this observed sialyltransferase inhibition activity. germinated seeds the amount of melatonin increased attaining Additional mechanistic studies indicate that there is evidence the highest values between the fifth and the seventh day during for saponin regulation of the apoptosis pathway enzymes (AKT, the germination process. The increase was 747% in lentil seeds Bcl, and ERK1/2), leading to programmed cell death of cancer cells and 620% in vetch seeds after 7 and 6 days of germination, respec- (Ellington et al., 2006; Godlewski, Slazak, Zabielski, Piastowska, & tively (Table 26)(Zielínski et al., 2001). Gralak, 2006; Xiao, Huang, Zhu, Ren, & Zhang, 2007; Zhu, Xiong, Extensive research has focused on melatonin as a sleep-promot- Yu, & Wu, 2005). Research on colon cancer cells suggests that it ing molecule (Oldani et al., 1994; Skene, Lockley, & Arendt, 1999). is the lipophilic saponin cores that may be responsible for the biological activity. The in vitro fermentations carried out by these authors also suggest that colonic microflora hydrolyze soya sapo- Table 26 Melatonin content in lentil and vetch seeds during germination. nins to the aglycones, potentially enhancing the activity of the soyasaponins (Gurfinkel & Rao, 2003). Day of germination Melatonin content (pg g1 d.m.) Lentil Vetch 8.4. Oxalate 0 122.7 ± 21.8 446.3 ± 30.3 1 149.5 ± 22.9 637.6 ± 30.3 2 179.1 ± 23.7 1072.4 ± 64.1 Oxalate salts are poorly soluble at intestinal pH and oxalic acid 3 284.9 ± 28.4 1105.1 ± 64.6 is known to decrease calcium absorption in monogastric animals 4 518.1 ± 40.9 1444.8 ± 82.1 (Allen, 1982). Legumes such as lentils, red kidney beans, and white 5 663.9 ± 44.4 1776.6 ± 101.4 beans have been previously analyzed for oxalate (Table 25). The 6 585.7 ± 40.9 1611.9 ± 91.5 highest and lowest oxalate content is present in Anasazi beans 7 917.3 ± 56.5 1885.1 ± 107.4 (80 mg 100 g1 wet weight) and blackeyed peas (4 mg 100 g1 Adapted from Zielínski et al. (2001). R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 475

Because elevated melatonin levels occur at night coincident with Consuming beans may help lower total cholesterol levels, sleep in humans, it has often been surmised that this neurochem- according to new research from the Agricultural Research Service ical influences the ability to sleep. Melatonin supplements are also of the U.S. Department of Agriculture. beneficial in individuals with delayed sleep phase syndrome Eighty volunteers between the ages of 18 and 55 participated in (Skene et al., 1999), sleep inefficiency that accompanies Alzheimer’s the study, with half being healthy and the other having at least two disease (Pandi-Perumal, Zisapel, Srinivasan, & Cardinali, 2005), symptoms that lead to metabolic syndrome, which indicates a risk and in many other cases. Melatonin as an oncostatic agent has for cardiovascular disease. For 12 weeks, half of the group ate one- been found to limit the growth of various tumors, particularly as half cup of cooked pinto beans every day along with their regular a suppressor of experimental mammary gland tumors (Blask, Hill, diet. The other half ate a replacement serving of chicken soup in- Orstead, & Massa, 1986; Molis, Spriggs, Jupiter, & Hill, 1995). stead of pinto beans. The study found all participants who ate pinto The most important functions of melatonin may relate to its multi- beans lowered their cholesterol during the study (Finley, Burrell, & ple and varied actions in preventing mutilation of essential mole- Reeves, 2007). These findings agree with earlier studies that have cules by free radicals and related reactants (Reiter, 1991; Reiter, found beans to have cholesterol lowering effects. Therefore, 2002). healthy adults consuming dried, cooked pinto beans daily (130 g, 12 weeks) can reduce their TC, LDL (important CVD risk factor) and HDL levels. People who eat beans four times per week reduce 10. Pulses and health their heart-disease risk by 20 percent. Recently, the effects of azuki bean juice supplementation pre- 10.1. Pulses and cardiovascular diseases scribed according to a Kanpo medicine regimen, on serum lipid concentrations were studied in young Japanese women. Triglycer- The prevalence of coronary heart disease (CHD) affected 16.8 ide concentrations were decreased in the azuki juice group medi- million Americans in 2006 (American Heart Association, 2009). ated by inhibited pancreatic lipase activity. Azuki juice intake Soluble fibre has been shown to reduce total and low-density lipo- might be benefical for preventing hypertriglyceridemia (Maruyama protein, cholesterol levels, as well as insulin resistance (Glore, Van et al., 2008). In other hand, Jacobs, Andersen, and Blomhoff (2007) Treeck, Knehans, & Guild, 1994). Consumption of legumes has been reported that whole-grain consumption is associated with a associated with reduced risk of coronary heart disease and cardio- reduced risk of noncardiovascular, noncancer death attributed to vascular disease (CVD); legume consumption of four times or more inflammatory diseases in the Iowa women’s health study. Ortega per week compared with less than once a week, was associated (2001) indicated that the nutrition of pregnant women is decisive with 22% lower risk of CHD, and 11% lower risk of CVD (Bazzano in the course of gestation and the health of both mother and child, et al., 2001; Flight & Clifton, 2006)(Table 27). While the replace- and recommended 7–8 portions of cereals and legumes per day. ment of refined rice with whole grain and legume powder as a source of carbohydrate in a meal showed significant beneficial effects on glucose, insulin, and homocysteine concentrations and li- 10.2. Pulses and diabetes pid peroxidation in coronary artery disease (CAD) patients, these effects are likely to substantially reduce the risk factors for CAD The suggestion that whole-grain foods might protect against and diabetes (Jang, Lee, Kim, Park, & Lee, 2001). The phytochemi- the development of diabetes as well as being useful in the manage- cals from legumes may be responsible for the beneficial cardiovas- ment of people who have already developed type II diabetes mel- cular effects since data from the Nurses’ Health Study showed that litus (T2DM) is relatively recent (Venn & Mann, 2004). folate and vitamin B6, from diet and supplements, conferred pro- Epidemiological studies strongly support the suggestion that high tection against coronary heart disease (Rimm et al., 1998). A re- intakes of whole-grain foods protect against the development of cently published meta-analysis concluded that a higher intake of T2DM. People who consume 3 or more servings of whole-grain folate (0.8 mg folic acid) would reduce the risk of ischaemic heart foods per day are less likely to develop T2DM than low consumers disease by 16% and stroke by 24% (Wald, Law, & Morris, 2002). (63 servings per week) with a 20–30% risk reduction. The role of

Table 27 Relative risk of coronary heart disease and cardiovascular disease according to frequency of legume intake in 9632 NHEFS participants.a

Frequency of legume intake per week Variable Less than once (n = 3885) Once (n = 2128) 2–3 Times (n = 2226) P4 Times (n = 1393) P value for trend Person-years 63,046 36,015 37,283 23,255 ... Coronary heart disease No. events 812 355 401 234 ... RR (95% Cl) Age, race, sex, and energy adjusted 1.00 0.90 (0.79–1.02) 0.93 (0.83–1.03) 0.82 (0.72–0.94) .02 Multivariate model 1b 1.00 0.91 (0.79–1.04) 0.91 (0.81–1.01) 0.78 (0.68–0.90) .002 Multivariate model 2c 1.00 0.93 (0.81–1.07) 0.90 (0.81–1.01) 0.79 (0.69–0.91) .003 Cardiovascular disease No. events 1593 758 818 511 ... RR (95% CI) Age, race, sex, and energy adjusted 1.00 0.95 (0.87–1.03) 0.94 (0.86–1.01) 0.91 (0.82–1.01) .07 Multivariate model 1b 1.00 0.96 (0.87–1.06) 0.94 (0.87–1.02) 0.89 (0.80–0.98) .02 Multivariate model 2c 1.00 0.99 (0.90–1.08) 0.95 (0.88–1.03) 0.91 (0.82–1.01) .06

From Bazzano et al. (2001). a NHEFS indicates First National Health and Nutrition Examination Survey Epidemiologic Follow-up Study; RR, relative risk; and CI, confidence interval. b Stratified by birth cohort and adjusted for age, sex, race, history of diabetes, recreational physical activity, level of education, regular alcohol consumption, current cigarette smoking, and total energy intake; n = 9178. c Additionally adjusted for total serum cholesterol level, systolic blood pressure, body mass index, saturated fat intake, frequency of meat and poultry intake, and frequency of fruit and vegetable intake; n = 9078. 476 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 legumes in the prevention of diabetes is less clear, possibly because has been expressed that refined-grain intake may directly contrib- of the relatively low intake of leguminous foods in the studied pop- ute to increases in obesity (Koh-Banerjee & Rimm, 2003). ulations. However, legumes share several qualities with whole In the United Kingdom (UK) women’s cohort study seven clus- grains of potential benefit to glycaemic control including slow re- ters of food consumption were identified, three of which had high lease carbohydrate and a high fibre content. A substantial increase cereal levels: health conscious (high bran, wholemeal, and pulses), in dietary intake of legumes as replacement food for more rapidly low diversity vegetarians (high wholemeal bread and pulses), and digested carbohydrate might therefore be expected to improve gly- high diversity vegetarians (high wholemeal bread, cereals, pasta caemic control and thus reduce incident diabetes (Venn & Mann, and rice, and pulses) (Greenwood et al., 2000). Women with these 2004). food consumption patterns had significantly lower average BMI Mung bean (Vigna radiata) is an excellent source of vitamins, values as well as the lowest proportion of obese subjects (5–9% minerals and protein with its essential amino acid profile compa- vs. 10–12% in the other four clusters). Another prospective study rable to that of soybean and kidney bean (Mubarak, 2005). Recent performed in the UK identified four diet patterns and found the research indicates that mung bean consumption produces small in- one with high intakes of rice, pasta, and pulses was negatively cor- crease in blood glycemic index in humans making it an attractive related with waist-to-hip (WHR) ratio (Williams et al., 2000). In option for diabetic patients. It is reported to modify glucose and li- the United States, factor analysis of dietary data from the Baltimore pid metabolism favourably in rats (Lerer-Metzger, Rizkalla, & Luo, longitudinal study of aging (BLSA) identified six food patterns. Sub- 1996). It is also well documented that certain proteins in mung jects consuming a fibre-rich pattern, high in non-white bread, bean exerts both antifungal and antibacterial activity (Wang, Wu, whole grains, beans, and legumes, had the lowest BMI, smallest Ng, Ye, & Rao, 2004). waist circumference (WC), and the smallest mean annual increase Recently, Villegas et al. (2008) reported that adherence to veg- in BMI. In older adults, the same pattern was also found. Cluster etables and legumes were inversely associated with the risk of type analysis of the diets of subjects aged 70–77 years in the cross sec- 2 diabetes in a large Chinese population. Tang, Li, and Zhang tional SENECA baseline study in Europe and the Framingham Heart (2008), searched the Traditional Chinese Medicine Database Study cohort identified five dietary patterns; the two that were sig- (TCMD), which documents 10,000 components extracted from nificantly associated with the lowest BMI and WC were those high- 4600 traditional medicinal agents. According to the pharmaco- est in grains and legumes, nuts, and seeds (Haveman-Nies, Tucker, logical activity annotations, they found that some components De Groot, Wilson, & van Staveren, 2001). One small trial performed are directly associated with prevention and/or treatment of in Mexico compared a low- and a high-GI diet, providing 63 g vs. T2DM, because of their aldose reductase inhibitory or hypoglycae- 55 g, respectively, of carbohydrate from cereals and legumes. The mic activity. Besides, the functions (e.g., antiatherosclerotic, anti- low-GI diet (high in whole-grain bread and beans and with less hypertensive, antilipemic, antithrombotic, lipase-, lipid white bread and rice) resulted in improved glycemic control and peroxidation-, lipoxygenase-, and platelet aggregation-inhibitory greater weight loss (Jimenez-Cruz, Bacardi-Gascon, Turnbull, activities) of many other vegetable and legume components are Rosales-Garay, & Severino-Lugo, 2003). also associated with ameliorating T2DM (Tang et al., 2008).

10.3. Pulses and cancer 10.5. Pulses and other diseases

A recent case–control study found an inverse association be- Chickpeas are the largest grown legume crop in Pakistan (Khokar, tween vegetables, particularly dark green/dark yellow vegetables, Muzaffar, & Chaudhri, 2001) and various varieties of chickpeas legumes, and allium vegetables, with endometrial cancer risk are popularly consumed as a source of dietary protein. Seeds enrich (Tao et al., 2005). These findings are consistent with other epidemi- the blood and cure skin diseases and inflammation of the ear ological studies linking reduced risk for hormone-related cancers (Agharkar, 1991; Warrier, Nambiar, & Remankutty, 1995). They with dark green/dark yellow vegetables consumption (Cramer, are used as tonic, appetizer, stimulant and aphrodisiac, and they Kuper, Harlow, & Titus-Ernstoff, 2001; Littman, Beresford, & White, also have anthelmintic properties (Sastry & Kavathekar, 1990). Die- 2001; Malin et al., 2003; McCann et al., 2000). In a large prospec- tary supplementation with chickpeas resulted in significant reduc- tive cohort study a reduced breast cancer risk was associated with tions in serum total and low-density lipoprotein cholesterols in higher intake of legumes (Velie et al., 2005). Also, Fung et al. (2003) adult woman and men (Pittaway et al., 2006). suggest that a diet high in whole grains (including legumes), fruits In a nationwide study of lymphoblastic leukemia (ALL) among and vegetables may reduce the risk of colon cancer in women. children ages 5 years and younger with focus on maternal diet in Other studies revealed that consumption of legumes such as dried Greece, Petridou, Ntouvelis, Dessypris, Terzidis, and Trichopoulos beans, split peas, or lentils was negatively associated with risk of (2005) found that increased maternal consumption of fruits and colorectal adenoma (Agurs-Collins, Smoot, Afful, Makambi, & perhaps vegetables (including pulses) reduces the risk of ALL. Re- Adams-Campbell, 2006). Dark green/dark yellow vegetables con- sults indicate that the incidence of ALL among young children tain high levels of carotenoids, folates (with beans as an excellent could be reduced by maternal adherence during pregnancy to the dietary source) vitamin C, and riboflavin. Carotenoids and vitamin generally accepted principles concerning a healthy diet throughout C may inhibit endometrial carcinogensis via antioxidant effects, life (see Table 28). while folate influences DNA stability via its important role in the Azuki beans (Phaseolus angularis WIGHT.) have long been synthesis of nucleotides and DNA methylation. Folate also could af- widely cultivated and consumed in confectionary and other tradi- fect carcinogenesis in numerous specific cancers (Kim, Kwon, & tional dishes, in Asian countries. Shozu-to is a Chinese medicine, Son, 2000; Lucock, 2000). composed mainly of azuki beans, which has been recognized to have antidotal, diuretic, and laxative effects and is thus used to 10.4. Pulses and obesity treat constipation, beriberi, nephritis, and insufficient postpartum lactation (Namba, 1980). Boiled azuki beans juice prescribed by Overweight and obesity are key features of the metabolic syn- herbal doctors and as a folk remedy has been used to prevent dam- drome and prevention of excessive weight gain is a health priority age associated with the stress of aging. Azuki beans extracts have internationally. Increased consumption of whole-grain foods, like an inhibitory effect on malonaldehyde formation, and thereby ex- cereals and legumes, may protect against obesity, but concern ert antioxidant activity (Lee & Lee, 2005; Lee et al., 2003). Azuki R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 477

Table 28 Pulses and their main potential positive and beneﬁcial effects.

Involved metabolism Beneficial effect Reference Legumes (including some Cardiovascular 22% lower risk of coronary heart disease, and an 11% lower risk of cardiovascular Bazzano et al. (2001) pulses) disease Cardiovascular and Modulation of glucose, insulin, and homocysteine concentrations and lipid Jang et al. (2001) diabetes peroxidation in coronary artery disease patients Azuki bean juice Hypertriglyceridemia Decreased triglyceride concentrations by inhibited pancreatic lipase activity Maruyama et al. (2008) Legumes Type II diabetes Risk reduction to develop T2DM in the order of 20–30% Venn and Mann (2004) mellitus Mung bean Glucose and lipid Modify glucose and lipid metabolism favourably in rats Lerer-Metzger et al. metabolism (1996) Legumes Endometrial cancer Low risk of endometrial cancer Tao et al. (2005) Breast cancer Low breast cancer risk Velie et al. (2005) Colon cancer Low risk of colorectal adenoma Agurs-Collins et al. (2006) Legumes and cereals Obesity Low average body mass index (BMI) and low risk of obesity Greenwood et al. (2000) Pulses Obesity Low waist-to-hip (WHR) ratio Williams et al. (2000) Whole grains, beans, and Obesity Low body mass index and waist circumference (WC) Haveman-Nies et al. legumes (2001) Whole-grain bread and Glycaemia and Glycemic control and weight loss Jimenes-Cruz et al. beans obesity (2003) Chickpeas Skin and ear Low risk of skin diseases and inflammation of the ear Agharkar (1991), Warrier inflammation et al. (1995) Tonic, appetizer, stimulant and aphrodisiac, anthelmintic properties Sastry and Kavathekar (1990) Hypertriglyceridemia Reductions in serum total and low-density lipoprotein cholesterols Pittaway et al. (2006) Vegetables (including some Lymphoblastic Low risk of lymphoblastic leukemia Petridou et al. (2005) seeds of pulses) leukemia Common bean Colon cancer Inhibition of aberrant foci crypt development in rat colon Feregrino-Perez et al. (2008)

beans have also been suggested to have lipase inhibitor activity Avila, M. A., Velasco, J. A., Cansado, J., & Notario, V. (1994). Quercetin mediates the in vitro (Hatano et al., 1997; Shimura et al., 1994). down-regulation of mutant p53 in the human breast cancer cell line MDA- MB468. Cancer Research, 54, 2424–2428. Awika, J. M., Rooney, L. W., Wu, X., Prior, R. L., & Zevallos, L. C. (2003). Screening 11. Concluding remarks methods to measure antioxidant activity of sorghum (Sorghum bicolor) and sorghum products. Journal of Agricultural and Food Chemistry, 51, 6657–6662. Azevedo, A., Gomes, J. C., Stringheta, P. C., Gontijo, A. M. C., Padovani, C. R., Riberio, L. Pulses are good source of minor compounds which may have R. Z., et al. (2003). Black bean (Phaseolus vulgaris L.) as a protective agent against important metabolic and/or physiological effects. These com- DNA damage in mice. Food and Chemical Toxicology, 41, 1671–1676. pounds have been considered as antinutritional factors. More re- Balint, G. A. (2000). Ultrastructural study of liver cell damage induced by ricin. Experimental and Toxicologic Pathology, 52, 413–417. cent evidence, however, provides potential information of their Barceló, A. R., & Muñoz, R. (1989). Epigenetic control of a cell wall scopoletin impact on health, so these secondary metabolites are currently peroxidase by lupisoflavone in Lupinus. Phytochemistry, 28, 1331–1333. marketed as functional foods and nutraceutical ingredients. Future Bardocz, S., Grant, G., Duguid, T. J., Brown, D. S., Pusztai, A., & Pryme, I. F. (1997). Intracellular levels of polyamines in Krebs II lymphosarcoma cells in mice fed research may determine if they should be preserved or eliminated phytohaemagglutinin-containing diets are coupled with altered tumour in each main nutritional situation. growth. Cancer Letters, 121, 25–29. Bazzano, L. H. J., Ogden, L. G., Loria, C., Vupputuri, S., Myers, L., & Whelton, P. K. (2001). Legume consumption and risk of coronary heart disease in US men and References women: NHANES I Epidemiologic Follow-up Study. Archives of Internal Medicine, 161, 2573–2578. Adlercreutz, H. (1998). Human health and phytoestrogens. In K. S. Korach (Ed.), Belitz, H. D., & Weder, J. K. P. (1990). Protein inhibitors of hydrolases in plants Reproductive and developmental toxicology (pp. 299–371). New York: Marcel foodstuffs. Food Reviews International, 6, 151–211. Dekker. Benveniste, P. (1986). Sterol biosynthesis. Annual Review of Plant Physiology, 37, Agharkar, S. P. (1991). Medicinal plants of Bombay presidency. Jodhpur, India: India 275–308. Scientific Publishers. Berdanier, C. D. (1992). Is inositol an essential nutrient? Nutrition Today, 27, 22–26. Agurs-Collins, T., Smoot, D., Afful, J., Makambi, K., & Adams-Campbell, L. (2006). Bertrand, D., Delort-Laval, J., Melcion, J. P., & Valdebouze, P. (1982). Influence de Legume intake and reduced colorectal adenoma risk in African-Americans. l’extrusion et de l’infranisation sur les facteurs antinutritionnels et la valeur Journal of National Black Nurses Association, 17, 6–12. alimentaire du pois (Pisum sativum L.). Sciences des Aliments, 2(Suppl), 197–202. Akpinar, N., Akpinar, M. A., & Türkog˘lu, Sß. (2001). Total lipid content and fatty acid Bird, T. A., Schule, H. D., Delaney, P. B., Sims, J. E., Thoma, B., & Dower, S. K. (1992). composition of the seeds of some Vicia L. species. Food Chemistry, 74, 449–453. Evidence that MAP (mitogen-activated protein) kinase activation may be a Allen, L. H. (1982). Calcium bioavailability and absorption: A review. The American necessary but not sufficient signal for a restricted subset of responses in IL-1- Journal of Clinical Nutrition, 35, 783–808. treated epidermoid cells. Cytokine, 4, 429–440. Amarowicz, R., Troszynska, A., Barylko-Pikielna, N., & Shahidi, F. (2004). Extracts of Blask, D. E., Hill, S. M., Orstead, K. M., & Massa, J. S. (1986). Inhibitory effects of the polyphenolics from legume seeds – Correlation between their total antioxidant pineal hormone melatonin and underfeeding during the promotional phase of activity, total phenolics content, tannins content and astringency. Journal of 7,12-dimethylbenzanthracene (DMBA)-induced mammary carcinogenesis. Food Lipids, 11, 278–286. Journal of Neural Transmission, 67, 125–138. American Heart Association. (2009). Heart disease and stroke statistics – 2009 update. Blask, D. E., Sauer, L. A., & Dauchy, R. T. (2002). Melatonin as a chronobiotic/ TX: Dallas. anticancer agent: Cellular biochemical and molecular mechanisms of action and Aubert, M., Panicot, L., Crotte, C., Gibier, P., Lombardo, D., Sadoulet, M. O., et al. their implications for circadian-based cancer therapy. Current Topics in (2000). Restoration of alpha (1,2) fucosyltransferase activity decreases adhesive Medicinal Chemistry, 2, 113–133. and metastatic properties of human pancreatic cancer cells. Cancer Research, 60, Bond, D. A., & Duc, G. (1993). Plant breeding as a means of reducing antinutritional 1449–1456. factors of grain legumes. In A. Van der Poel, J. Huisman, & H. S. Saini (Eds.), Augustin, J., Beck, C. B., Kalbfleish, G., Kagel, L. C., & Matthews, R. H. (1981). Variation Recent advances of research in antinutritional factors in legume seeds, proceedings in the vitamin and mineral content of raw and cooked commercial Phaseolus of the 2nd international workshop on antinutritional factors (ANFs) in legume seeds vulgaris classes. Journal of Food Science, 46, 1701–1706. (pp. 379–396). Wageningen, Netherlands: Wageningen Press. 478 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Cabrera, C., Lloris, F., Giménez, R., Olalla, M., & López, M. C. (2003). Mineral content Duranti, M. (2006). Grain legume proteins and nutraceutical properties. Fitoterapia, in legumes and nuts: Contribution to the Spanish dietary intake. The Science of 77, 67–82. the Total Environment, 308, 1–14. Einat, H., & Belmaker, R. H. (2001). The effects of inositol treatment in animal Cai, Y., Luo, Q., Sun, M., & Corke, H. (2004). Antioxidant activity and phenolic models of psychiatric disorders. Journal of Affective Disorders, 62, 113–121. compounds of 112 traditional Chinese medicinal plants associated with Eitenmiller, R. R., & Lee, J. (2004). Vitamin E: Food chemistry, composition and analysis. anticancer. Life Sciences, 74, 2157–2184. New York: Marcel Decker. Campbell, W. W., Ostlund, R. E., Joseph, L. J., Farrell, E. A., & Evans, W. J. (2001). Ekpenyoung, T. E., & Borchers, R. L. (1981). Some toxic factors in winged bean seeds. Relationships of plasma C-peptide and gender to the urinary excretion of Nutrition Reports International, 23, 865–870. inositols in older people. Hormone and Metabolic Research, 33, 44–51. El-Adawy, T. A. (2002). Nutritional composition and antinutritional factors of Campion, B., Perrone, D., Galasso, I., & Bollini, R. (2009). Common bean (Phaseolus chickpeas (Cicer arietinum L.) undergoing different cooking methods and vulgaris L.) lines devoid of major lectin proteins. Plant Breeding, 128, 199–204. germination. Plant Foods for Human Nutrition, 57, 83–97. Cardador-Martinez, A., Loarca-Pina, G., & Oomah, B. D. (2002). Antioxidant activity Elhardallon, S. B., & Walker, A. F. (1992). Binding of iron by three starchy legumes in in common beans. Journal of Agricultural and Food Chemistry, 50, 6975–6980. the presence of iron alone, with calcium or with calcium, zinc, magnesium and Carstensen, S., Pliska Matyshak, G., Bhuvarahamurthy, N., Robbins, K. M., & Murthy, copper. Journal of Food Sciences and Nutrition, 43, 61–68. E. P. N. (1999). Biosynthesis and localization of phosphatidyl-scyllo-inositol in Ellington, A. A., Berhow, M. A., & Singletary, K. W. (2006). Inhibition of Akt signaling barley aleurone cells. Lipids, 34, 67–73. and enhanced ERK1/2 activity are involved in induction of macroautophagy by Cassidy, A., Albertazzi, P., Lise Nielsen, I., Hall, W., Williamson, G., Tetens, I., et al. triterpenoid B-group soyasaponins in colon cancer cells. Carcinogenesis, 27, (2006). Critical review of health effects of soyabean phyto-oestrogens in post- 289–306. menopausal women. The Proceedings of the Nutrition Society, 65, 76–92. Estensen, R. D., & Wattenberg, L. W. (1993). Studies of chemopreventive effects of Celleno, L., Tolaini, M. V., D’Amore, A., Perricone, N. V., & Preuss, H. G. (2007). A myo-inositol on benzo[a]pyrene-induced neoplasia of the lung and forestomach dietary supplement containing standardized Phaseolus vulgaris extract of female A/J mice. Carcinogenesis, 14, 1975–1977. influences body composition of overweight men and women. International Feinberg, M., Favier, J. C., & Ireland-Ripert, J. (1995). Repértoir e general des aliments: Journal of Medical Sciences, 4, 45–52. Table de composition. Paris: Institut National de la Recherche Agronomique. Champ, M. M. (2002). Non-nutrient bioactive substances of pulses. British Journal of Fennema, O. R. (2000). Food chemistry. New York: Marcel Dekker. Nutrition, 88(Suppl. 3), S307–S319. Fenwick, D. E., & Oakenfull, D. (1983). Saponin content of food plants and some Chang, R. L., Huang, M. T., Wood, A. W., Wong, C. Q., Newmark, H. L., Yagi, H., et al. prepared foods. Journal of the Science of Food and Agriculture, 34, 186–191. (1985). Effect of ellagic acid and hydroxylated flavonoids on the tumorigenicity Feregrino-Perez, A. A., Berumen, L. C., Garcia-Alcocer, G., Guevara-Gonzalez, R. G., of benzo[a]pyrene and (6)-7 beta, 8 alphadihydroxy-9 alpha, 10 alpha epoxy- Ramos-Gomez, M., Reynoso-Camacho, R., et al. (2008). Composition and 7,8,9,10-tetrahydrobenzo[a]pyrene on mouse skin and in the newborn mouse. chemopreventive effect os polysaccharides from common beans (Phaseolus Carcinogenesis, 6, 1127–1133. vulgaris L.) on azoxymethane-induced colon cancer. Journal of Agricultural and Chang, W. W., Yu, C. Y., Lin, T. W., Wang, P. H., & Tsai, Y. C. (2006). Soyasaponin I Food Chemistry, 56, 8737–8744. decreases the expression of alpha2,3-linked sialic acid on the cell surface and Ferriola, P. C., Cody, V., & Middleton, E. (1989). Protein kinase C inhibition by plant suppresses the metastatic potential of B16F10 melanoma cells. Biochemical and flavonoids, kinetic mechanism and structure–activity relationships. Biochemical Biophysical Research Communications, 341, 614–619. Pharmacology, 38, 1617–1624. Chen, Q. C. (2004). Determination of phytic acid and inositol pentakisphosphates in Finley, J. W., Burrell, J. B., & Reeves, P. G. (2007). Pinto bean consumption changes foods by high-performance ion chromatography. Journal of Agricultural and Food SCFA profiles in fecal fermentations, bacterial populations of the lower bowel, Chemistry, 52, 4604–4613. and lipid profiles in blood of humans. Journal of Nutrition, 137, 2391–2398. Choi, J. A., Kim, J. Y., Lee, J. Y., Kang, C. M., Know, H. J., Yoo, Y. D., et al. (2001). Flight, I., & Clifton, P. (2006). Cereal grains and legumes in the prevention of Induction of cell cycle arrest and apoptosis in human breast cancer cells by coronary heart disease and stroke: A review of the literature. European Journal of quercetin. International Journal of Oncology, 9, 837–844. Clinical Nutrition, 60, 1145–1159. Chung, T. W., Moon, S. K., Chang, Y. C., Ko, J. H., Lee, Y. C., Cho, G., et al. (2004). Novel Fredlund, K., Isaksson, M., Rossander-Hulthén, L., Almgren, A., & Sandberg, A.-S. and therapeutic effect of caffeic acid and caffeic acid phenyl ester on (2006). Absorption of zinc and retention of calcium: Dose-dependent inhibition hepatocarcinoma cells: Complete regression of hepatoma growth and by phytate. Journal of Trace Elements in Medical Biology, 20, 49–57. metastasis by dual mechanism. The FASEB Journal: Official Publication of the Fukui, H., Egawa, H., & Koshimizu, K. (1973). A new isoflavone with antifungal Federation of American Societies for Experimental Biology, 18, 1670–1681. activity from immature fruits of Lupinus luteus. Agricultural and Biological Chung, K. T., Wong, T. Y., Wei, C. I., Huang, Y. W., & Lin, Y. (1998). Tannins and Chemistry, 37, 417–421. human health: A review. Critical Reviews in Food Science and Nutrition, 38, Fung, T., Hu, F. B., Fuchs, C., Giovannucci, E., Hunter, D. J., Stampher, M. J., et al. 421–464. (2003). Major dietary patterns and the risk of colorectal cancer in women. Chrenkova, M., Ceresnakova, Z., Sommer, A., & Slamena, Z. (2001). The nutritive Archives of Internal Medicine, 163, 309–314. value of new-bred varieties of pea grown in Slovakia, In Proceedings of the 4th Geil, P. B., & Anderson, J. W. (1994). Nutrition and health implications of dry beans: European Conference on Grain Legumes, Cracow (pp. 114–115). Paris: AEP A review. Journal of the American College of Nutrition, 13, 549–558. Editions. Genovese, M. I., & Lajolo, F. M. (1998). Inibidores de tripsina do feijaõ (Phaseolus Coskun, O., Kanter, M., Korkmaz, A., & Oter, S. (2005). Quercetin, a flavonoid vulgaris): Isoformas e estabilidade térmica. Anais XVI Congresso Brasileiro Ciência antioxidant, prevents and protects streptozotocin-induced oxidative stress and e Tecnologia de Alimentos. Brazil, Sociedade Brasileira de Ciência eTechnologia de b-cell damage in rat pancreas. Pharmacological Research, 51, 117–123. Alimentos (SBCTA), Rio de Janeiro. Cramer, D. W., Kuper, H., Harlow, B. L., & Titus-Ernstoff, L. (2001). Carotenoids, Giovannucci, E., Stampfer, M. J., Colditz, G. A., Hunter, D. J., Fuchs, C., Rosner, B. A., antioxidants and ovarian cancer risk in pre- and postmenopausal women. et al. (1998). Multivitamin use, folate, and colon cancer in women in the Nurses’ International Journal of Cancer, 94, 128–134. Health Study. Annals of Internal Medicine, 129, 517–524. Cuadrado, C., Hajos, G., Burbano, C., Pedrosa, M. M., Ayet, G., Muzquiz, M., et al. Giovannucci, E., & Willett, W. C. (1994). Dietary factors and risk of colon cancer. (2002). Effect of natural fermentation on the lectin of lentils measured by Annals of Medicine, 26, 443–452. immunological methods. Food and Agricultural Immunology, 14, 41–49. Gitto, E., Malgorzata, K., Russel, J. R., Dun, X. T., Cuzzocrea, S., Chiurazzi, P., et al. Dang, J., Arcot, J., & Shrestha, A. (2000). Folate retention in selected processed (2001). Effects of melatonin treatment on septic newborns. Pediatrics Research, legumes. Food Chemistry, 68, 295–298. 50, 756–760. Daveby, Y. D. A. P., Betz, J. M., & Musser, S. M. (1998). Effect of storage and extraction Glore, S. R., Van Treeck, D., Knehans, A. W., & Guild, M. (1994). Soluble fiber and on ratio of soyasaponin I to 2,3-dihydro-2,5-dihydroxy-6-methyl-4-pyrone- serum lipids: A literature review. Journal of the American Dietetic Association, 94, conjugated soyasaponin I in de-hulled peas (Pisum sativum L.). Journal of the 425–436. Science of Food and Agriculture, 32, 141–146. Godlewski, M. M., Slazak, P., Zabielski, R., Piastowska, A., & Gralak, M. A. (2006). De Boever, P., Deplancke, B., & Verstraete, W. (2000). Fermentation by gut Quantitative study of soybean-induced changes in proliferation and microbiota cultured in a simulator of the human intestinal microbial programmed cell death in the intestinal mucosa of young rats. Journal of ecosystem is improved by supplementing a soygerm powder. Journal of Physiology and Pharmacology, 57, 125–133. Nutrition, 130, 2599–2606. González De Mejía, E., & Prisecaru, V. I. (2005). Lectins as bioactive plant proteins: A De Muelenaere, H. J. (1965). Toxicity and haemagglutining activity of legumes. potential in cancer treatment. Critical Reviews in Food Science and Nutrition, 45, Nature, 206, 827–828. 425–445. Dini, I., Schettino, O., & Dini, A. (1998). Studies on the constituents of Lupinus González de Mejía, E., Rocha, N., Winter, H. C., & Goldstein, I. J. (2002). Differential mutabilis (Fabaceae). Isolation and characterization of two new isoflavonoid effect of a lectin from mesquite (Prosopis juliflora) on HeLa and normal human derivatives. Journal of Agricultural and Food Chemistry, 46, 5089–5092. keratinocyte cells. The FASEB Journal, 15, C128. Dintzis, F. R., Lehrfeld, J., Nelsen, T. C., & Finney, P. L. (1992). Phytate content of soft Graf, E., & Eaton, J. W. (1990). Antioxidant functions of phytic acid. Free Radical wheat brans as related to kernel size, cultivar, location, and milling and flour Biology and Medicine, 8, 61–69. quality parameters. Cereal Chemistry, 69, 577–581. Grant, G., Alonso, R., Edwards, J. E., & Murray, S. (2000). Dietary soya beans and Duane, W. C. (1997). Effects of legume consumption on serum cholesterol, biliary kidney beans stimulate secretion of cholecystokinin and pancreatic digestive lipids, and sterol metabolism in humans. Journal of Lipid Research, 38, enzymes in 400-day-old Hooded-Lister rats but only soya beans induce growth 1120–1128. of the pancreas. Pancreas, 20, 305–312. Duhan, A., Khetarpaul, N., & Bishnoi, S. (2001). Saponin content and trypsin inhibitor Grant, G., Dorward, P. M., Buchan, W. C., Armour, J. C., & Pusztai, A. (1995a). activity in processed and cooked pigeon pea cultivars. International Journal of Consumption of diets containing soya beans (Glycine max), kidney beans Food Science and Nutrition, 52, 53–59. (Phaseolus vulgaris), cowpeas (Vigna unguiculata) or lupin seeds (Lupinus R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 479

augustifolius) by rats for up to 700 days: Effects on body composition and organ Kadam, S. S., & Salunkhe, D. K. (1989). Minerals and vitamins. In D. K. Salunkhe (Ed.), weights. British Journal of Nutrition, 73, 17–29. Handbook of world food legumes (pp. 117–121). Boca Raton: CRC Press. Grant, G., Edwards, J. E., & Pusztai, A. (1995b). a-Amylase inhibitor levels in seeds Kataria, A., Chauhan, B. M., & Punia, D. (1989). Antinutrients in amphidiploids (black generally available in Europe. Journal of the Science of Food and Agriculture, 67, gram Mung bean): Varietal differences and effect of domestic processing and 235–238. cooking. Plant Foods for Human Nutrition, 39, 257–266. Grases, F., Costa-Bauza, A., Perelló, J., Isern, B., Vucenik, I., Valiente, M., et al. (2006). Kawabata, K., Yamamoto, T., Hara, A., Shimizu, M., Yamada, Y., Matsunaga, K., et al. Influence of concomitant food intake on the excretion of orally administered (2000). Modifying effects of ferulic acid on azoxymethane-induced colon myo-inositol hexaphosphate in humans. Journal of Medicinal Food, 9, 72–76. carcinogenesis in F344 rats. Cancer Letters, 157, 15–21. Grases, F., Simonet, B. M., Vucenik, I., Prieto, R. M., Costa-Bauza, A., March, J. G., et al. Khokar, S. N., Muzaffar, A. K., & Chaudhri, M. F. (2001). Some characters of chickpea- (2001). Absorption and excretion of orally administered inositol hexaphosphate modulating Rhizobia native to thai soil. Journal of Biological Sciences, 4, (IP6 or phytate) in humans. BioFactors, 15, 53–61. 1016–1019. Greenwood, D., Cade, J., Draper, A., Barrett, J. H., Calvert, C., & Greenhalgh, A. (2000). Khokhar, S., & Chauhan, B. M. (1986). Antinutritional factors in moth bean: Varietal Seven unique food consumption patterns identified among women in the UK differences and effects of methods of domestic processing and cooking. Journal women’s cohort study. European Journal of Clinical Nutrition, 54, 314–320. of Food Science, 51, 591–594. Grela, E. R., & Gunter, K. D. (1995). Fatty acid composition and tocopherol content of Kim, J. S., Kwon, C. S., & Son, K. H. (2000). Inhibition of alpha-glucosidase and some legume seeds. Animal Feed Science and Technology, 52, 325–331. amylase by luteolin, a flavonoid. Bioscience, Biotechnology, and Biochemistry, 64, Gueguen, J., Quemener, B., & Valdebouze, P. (1980). Elimination of antinutritional 2458–2461. factors of faba bean (Vicia faba L.) and peas (Pisum sativum L.) during the Kjaer, T. M., & Frokiaer, H. (2002). Modulation of ovomucoid-specific tolerance in preparation of protein isolates. Lebensmittel Wissenschaft und-Technologie, 13, mice fed plant extracts containing lectins. British Journal of Nutrition, 88, 443–455. 671–680. Gurfinkel, D. M., & Rao, A. V. (2003). Soyasaponins: The relationship between Kofman, O., Einat, H., Cohen, H., Tenne, H., & Shoshana, C. (2000). The anxiolytic chemical structure and colon anticarcinogenic activity. Nutrition and Cancer, 47, effect of chronic inositol depends on the baseline level of anxiety. Journal of 24–33. Neural Transmission, 107, 241–253. Gylling, H., & Miettinen, T. A. (2005). The effect of plant stanol- and sterol-enriched Koh-Banerjee, P., & Rimm, E. B. (2003). Whole grain consumption and weight gain: foods on lipid metabolism, serum lipids and coronary heart disease. Annals of A review of the epidemiological evidence, possible mechanisms and Clinical Biochemistry, 42, 254–263. opportunities for further research. The Proceedings of the Nutrition Society, 62, Habiba, R. A. (2002). Changes in anti-nutrients, protein solubility, digestibility and 25–29. HCl-extractability of ash and phosphorus in vegetable peas as affected by Lacassagne, L., Francesch, M., Carré, B., & Melcion, J. P. (1988). Utilization of tannin- cooking methods. Food Chemistry, 77, 187–192. containing and tannin-free faba beans (Vicia faba) by young chicks: Effects of Harborne, J., Boulter, D., & Turner, B. E. (1971). Chemotaxonomy of the leguminosae. pelleting feeds on energy, protein and starch digestibility. Animal Feed Science London: Academic Press. and Technology, 20, 59–68. Harland, J. (2002). Prevention is better than cure (soya isoflavones). Liquid Food and Lajolo, F. M., Finardi-Filho, F., & Menezes, E. W. (1991). Amylase inhibitors in Drink Technology, 1. Phaseolus vulgaris beans. Food Technology, 45, 119–121. Hatano, T., Yamashita, A., Hashimoto, T., Oto, H., Kubo, N., Yoshiyama, M., et al. Lajolo, F. M., & Genovese, M. I. (2002). Nutritional significance of lectin and enzyme (1997). Flavan dimers with lipase inhibitory activity from Cassia Nomane. inhibitors from legumes. Journal of Agricultural and Food Chemistry, 50, Phytochemistry, 46, 893–900. 6592–6598. Haveman-Nies, A., Tucker, K., De Groot, L., Wilson, P. W. F., & van Staveren, W. A. Lajolo, F. M., Mancini Filho, J., & Menezes, E. W. (1984). Effect of a bean (Phaseolus (2001). Evaluation of dietary quality in relationship to nutritional and lifestyle vulgaris) a-amylase inhibitor on starch utilization. Nutrition Reports factors in elderly people in the US Framingham Heart Study and the European International, 30, 45–54. SENECA study. European Journal of Clinical Nutrition, 55, 870–880. Lazze, M. C., Pizzala, R., Savio, L. A., Stivala, E. P., & Bianchi, L. (2003). Anthocyanins Heimler, D., Vignolini, P., Dini, M. G., & Romani, A. (2005). Rapid tests to assess the protects against DNA damage induced by tert-butyl hydroperoxide in rat antioxidant activity of Phaseolus vulgaris L. dry beans. Journal of Agricultural and smooth muscle and hepatoma cells. Mutation Research, 535, 103–115. Food Chemistry, 53, 3053–3056. Lee, S., & Lee, K. G. (2005). Inhibitory effects of volatile anti-oxidants found in Herrera, J. N. M., Romero, F., & Rodríguez-Iturbe, B. (2001). Melatonin prevents various beans on malonaldehyde formation in horse blood plasma. Food and oxidative stress resulting from iron and erythropoietin administration. Chemical Toxicology, 43, 515–520. American Journal of Kidney Diseases, 37, 750–757. Lee, K., Shibamoto, T., Takeoka, G. R., Lee, S. E., Kim, J. H., & Park, B. S. (2003). Holland, B., Unwin, I. D., & Buss, D. H. (1992). First supplement to McCance and Inhibitory effects of plant-derived flavonoids and phenolic acids on Widdowson’s. The composition of foods (5th ed.). Cambridge: Royal Society of malonaldehyde formation from ethyl arachidonate. Journal of Agricultural Chemistry. Chemistry, 51, 7203–7207. Hönow, R., & Hesse, A. (2002). Comparison of extraction methods for the Lerer-Metzger, M., Rizkalla, S., & Luo, J. (1996). Effects of long-term low-glycemic determination of soluble and total oxalate in foods by HPLC-enzyme-reactor. index starchy food on plasma glucose and lipid concentrations and adipose Food Chemistry, 78, 511–521. tissue cellularity in normal and diabetic rats. British Journal of Nutrition, 75, Huisman, J. (1990). Antinutritional effects of legume seeds in piglets, rats and chickens. 723–732. PhD thesis, Wageningen, The Netherlands. Lewy, A. J. (1999). Melatonin as a marker and phase-resetter of circadian rhythms in Hurrell, R. F., Reddy, M., & Cook, J. D. (1999). Inhibition of non-haem iron absorption humans. Advances in Experimental Medicine and Biology, 460, 425–434. in man by polyphenolic-containing beverages. British Journal of Nutrition, 81, Liener, I. E. (1976). Legume toxins in relation to protein digestibility – a review. 289–295. Journal of Food Science, 41, 1076–1081. Ikeda, I., Imasato, Y., Sasaki, E., Nakayama, M., Nagao, H., Takeo, T., et al. (1992). Tea Liener, I. E. (1979). Significance of humans of biologically active factors in soybeans catechins decrease micellar solubility and intestinal absorption of cholesterol in and other food legumes. Journal of the American Oil Chemists’ Society, 56, rats. Biochimica et Biophysica Acta, 1127, 141–146. 121–129. Jacobs, D. R. J., Andersen, F. L., & Blomhoff, R. (2007). Whole-grain consumption is Liener, I. E. (1994). Implications of antinutritional components in soybean foods. associated with a reduced risk of noncardiovascular, noncancer death Critical Review in Food Science and Nutrition, 34, 31–67. attributed to inflammatory diseases in the Iowa Women’s Health Study. Lissoni, P. (2002). Is there a role for melatonin in supportive care? Support Care American Journal of Clinical Nutrition, 85, 1606–1614. Cancer, 10, 110–116. Jang, Y., Lee, J. H., Kim, O. Y., Park, H. Y., & Lee, S. Y. (2001). Consumption of whole Littman, A. J., Beresford, S. A., & White, E. (2001). The association of dietary fat and grain and legume powder reduces insulin demand, lipid peroxidation, and plant foods with endometrial cancer (United States). Cancer Causes and Control, plasma homocysteine concentrations in patients with coronary artery disease: 12, 691–702. Randomized controlled clinical trial. Arteriosclerosis, Thrombosis, and Vascular Loewus, F. A., & Murthy, P. P. N. (2000). Myo-inositol metabolism in plants. Plant Biology, 21, 2065–2071. Science, 150, 1–19. Jenab, M., & Thompson, L. U. (1998). The influence of phytic acid in wheat bran on Lombardi-Boccia, G., Carbonaro, M., Di Lullo, G., & Carnovale, E. (1994). Influence of early biomarkers of colon carcinogenesis. Carcinogenesis, 19, 1087–1092. protein components (G1, G2 and albumin) on Fe and Zn dialysability from bean Jenab, M., & Thompson, L. U. (2002). Role of phytic acid in cancer and other diseases in (Phaseolus vulgaris L.). Journal of Food Sciences and Nutrition, 45, 183–190. food phytates. CRC Press: Boca Raton. pp. 225–248. Long-Ze, L., Harnly, J. M., Pastor-Corrales, M. S., & Luthria, D. L. (2008). The Jimenez, A., Cervera, P., & Bacardí, M. (1998). Tabla de composición de alimentos. polyphenolic profiles of common bean (Phaseolus vulgaris L.). Food Chemistry, Bacelona: Novartis Nutrition. 107, 399–410. Jimenez-Cruz, A., Bacardi-Gascon, M., Turnbull, W. H., Rosales-Garay, P., & Severino- Lorea, P., Goldschmidt, D., Darro, F., Salmon, I., Bovin, N., Gabius, H. J., et al. (1997). Lugo, I. (2003). A flexible, low-glycemic index, Mexican-style diet in overweight In vitro characterization of lectin-induced alterations on the proliferative and obese subjects with type 2 diabetes improves metabolic parameters during activity of three human melanoma cell lines. Melanoma Research, 7, 353–363. a 6-week treatment period. Diabetes Care, 26, 1967–1970. Lucock, M. (2000). Folic acid: Nutritional biochemistry, molecular biology, and role Jondreville, C., Grosjean, F., Buron, G., Peyronnet, C., & Beneytout, J. L. (1992). in disease processes. Molecular Genetics and Metabolism, 71, 121–138. Comparison of four pea varieties in pig feeding through digestibility and growth Luthria, D. L., & Pastor-Corrales, M. A. (2006). Phenolic acids content of fifteen dry performance results. Journal of Animal Physiology and Animal Nutrition, 68, edible bean (Phaseolus vulgaris L.) varieties. Journal of Food Composition and 113–122. Analysis, 19, 205–211. Jordinson, M., El-Hariry, I., Calnan, D., Calam, J., & Pignatelli, M. (1999). Vicia faba Malin, A. S., Qi, D., Shu, X. O., Gao, Y. T., Friedmann, J. M., Jin, F., et al. (2003). Intake of agglutinin, the lectin present in broad beans, stimulates differentiation of fruits, vegetables and selected micronutrients in relation to the risk of breast undifferentiated colon cancer cells. Gut, 44, 709–714. cancer. International Journal of Cancer, 105, 413–418. 480 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Mancini, F. J., & Lajolo, F. M. (1981). Fatores antinutricionais em diferentes Nemets, B., Fux, M., Levine, J., & Belmaker, R. H. (2001). Combination of variedades de feijões (Phaseolus vulgaris L.). Ciencia e Cultura, 33, 94–97. antidepressant drugs: The case of inositol. Human Psychopharmacology, 16, Mangiapane, H., Thomson, J., Salter, A., Brown, S., Bell, G. D., & White, D. A. 37–43. (1992). The inhibition of the oxidation of low density lipoprotein by (1)- Nishino, H., Murakoshi, M., Masuda, M., Tokuda, H., Satomi, Y., Onozuka, M., et al. catechin, a naturally occurring flavonoid. Biochemical Pharmacology, 43, (1999). Suppression of lung and liver carcinogenesis in mice by oral 445–450. administration of myo-inositol. Anticancer Research, 19, 3663–3664. Maruyama, C., Araki, R., Kawamura, M., Kondo, N., Kigawa, M., Kawai, Y., et al. Oakenfull, D., & Sidhu, G. S. (1989). Saponins. In P. Cheeke (Ed.), Toxicants of Plant (2008). Azuki bean juice lowers serum triglyceride concentrations in healthy Origin. Boca Raton, FL: CRC. young women. Journal of Clinical Biochemistry and Nutrition, 43, 19–25. Ogasawara, H., Fujitani, T., Drzewiecki, G., & Middleton, E. (1986). The role of Mason, A. C., Weaver, C. M., Kimmel, S., & Brown, R. K. (1993). Effect of soybean hydrogen peroxide in basophil histamine release and the effect of selected phytate content on calcium bioavailability in mature and immature rats. Journal flavonoids. Journal of Allergy and Clinical Immunology, 78, 321–328. of Agricultural Food Chemistry, 41, 246–249. Oldani, A., Ferini-Strambi, L., Zucconi, M., Stankov, B., Fraschini, F., & Smirne, S. Massey, L. K., Palmer, R. G., & Horner, H. T. (2001). Oxalate content of soybean seeds (1994). Melatonin and delayed sleep phase syndrome: Ambulatory polygraphic (glycine max: leguminosae), soyfoods, and other edible legumes. Journal of evaluation. Neuroreport, 30, 132–134. Agricultural and Food Chemistry, 49, 4262–4266. Oomah, B. D., Blanchard, C., & Balasubramanian, P. (2008). Phytic acid, phytase, Mataix, F. J., & Mañas, M. T. (1998). Tabla de composición de alimentos españoles. minerals, and antioxidant activity in Canadian dry bean (Phaseolus vulgaris L.) Instituto de Nutrición y Tecnología de los Alimentos-Universidad de Granada, cultivars. Journal of Agricultural and Food Chemistry, 56, 11312–11319. Granada. Oomah, B. D., Cardador-Martínez, A., & Loarca-Piña, G. (2005). Phenolics and Mathers, J. C. (2002). Pulses and carcinogenesis: Potential for prevention of colon, antioxidative activities in common beans (Phaseolus vulgaris L.). Journal of the breast and other cancers. British Journal of Nutrition, 88, 272–279. Science of Food and Agriculture, 85, 935–942. Mazur, W. M., Duke, J. A., Wahala, K., Rasku, S., & Adlercreutz, H. (1998). Orcheson, L. J., Rickard, S. E., Seidl, M. M., & Thompson, L. U. (1998). Flaxseed and its Isoflavonoids and lignans in legumes: Nutritional and health aspects in mammalian lignan precursor cause a lengthening or cessation of estrous cycling humans. Journal of Nutritional Biochemistry, 9, 193–200. in rats. Cancer Letters, 125, 69–76. McCann, S. E., Freudenheim, J. L., Marshall, J. R., Brasure, J. R., Swanson, M. K., & Ortega, R. M. (2001). Dietary guidelines for pregnant women. Public Health Nutrition, Graham, S. (2000). Diet in the epidemiology of endometrial cancer in Western 4, 1343–1346. New York (United States). Cancer Causes and Control, 11, 965–974. Page, D., Aubert, G., Duc, G., Welham, T., & Domoney, C. (2001). Identification and McLaurin, J., Golomb, R., Jurewicz, A., Antel, J. P., & Fraser, P. E. (2000). Inositol exploitation of seed trypsin inhibitor gene polymorphism for molecular stereoisomers stabilize an oligomeric aggregate of Alzheimer amyloid 13 marker-assisted breeding and selection. In Proceedings of the 4th European peptide and inhibit A 13-induced toxicity. Journal of Biological Chemistry, 275, Conference on Grain Legumes, Cracow (pp. 20–21). Paris: AEP Editions. 18495–18502. Pandi-Perumal, S. R., Zisapel, N., Srinivasan, V., & Cardinali, D. P. (2005). Melatonin Meagher, L. P., & Beecher, G. R. (2000). Assessment of data on the lignan content of and sleep in an aging population. Experimental Gerontology, 40, 911–925. foods. Journal of Food Composition and Analysis, 13, 935–947. Pappolla, M. A., Chyan, Y. J., Poeggeler, B., Frangione, B., Wilson, G., & Ghiso, J. (2000). Melcion, J. P., & Valdebouze, P. (1977). Effect of various industrial treatments on the An assessment of the antioxidant and antiamyloidogenic properties of antinutritional factors of field bean (Vicia faba L.). In Protein Quality from melatonin: Implications for Alzheimer’s disease. Journal of Neural Leguminous Crops. Seminar in EEC Program (pp. 116–124). Kirchberg, Transmission, 107, 203–231. Luxembourg: Commission of the European Communities. Petridou, E., Ntouvelis, E., Dessypris, N., Terzidis, A., & Trichopoulos, D. (2005). Menezes, E. W., & Lajolo, F. M. (1987). Inhibition of starch digestion by a black bean Maternal diet and acute lymphoblastic leukemia in young children. a-amylase inhibitor, in normal and diabetic rats. Nutrition Reports International, Epidemiology Biomarkers and Prevention, 14, 1935–1939. 36, 1185–1189. Phillippy, B. Q. (2003). Inositol phosphates in food. Advances in Food and Nutrition Messina, M., McCaskill-Stevens, W., & Lampe, J. W. (2006). Addressing the soy and Research, 45, 1–60. breast cancer relationship: Review, commentary, and workshop proceedings. Pieta, P. (2000). Flavonoids as antioxidants. Journal of Natural Products, 63, Journal of the National Cancer Institute, 98, 1275–1284. 1037–1042. Midorikawa, K., Murata, M., Oikawa, S., Hiraku, Y., & Kawanishi, S. (2001). Protective Pittaway, J. K., Ahuja, K. D. K., Cehun, M., Chronopoulos, A., Robertson, I. K., Nestel, P. effect of phytic acid on oxidative DNA damage with reference to cancer J., et al. (2006). Dietary supplementation with chickpeas for at least 5 weeks chemoprevention. Biochemical Biophysical Research Communications, 288, results in small but significant significant reductions in serum total and low- 552–557. density lipoprotein cholesterols in adult woman and men. Annals of Nutrition Milgate, J., & Roberts, D. C. K. (1995). The nutritional & biological significance of and Metabolism, 50, 512–518. saponins. Nutrition Research, 15, 1223–1249. Polat, M., & Korkmaz, M. (2001). An EPR study into the effect of annealing on both Minihane, A. N., & Rimbach (2002). Gerald Iron absorption and the iron binding and the Mn(II) and free radical signal in lentil. International Journal of Food Science anti-oxidant properties of phytic acid. International Journal of Food Science and and Technology, 36, 313–320. Technology, 37, 741–748. Polkowski, K., & Mazurek, A. P. (2000). Biological properties of genistein. A review of Ministerio de Sanidad y Consumo (1999). Tablas de composición de alimentos in vitro and in vivo data. Acta Poloniae Pharmaceutica, 57, 135–155. españoles. Ministerio de Sanidad y Consumo. Boletín Oficial del Estado, Madrid. Price, K. R., Johnson, I. T., & Fenwick, G. R. (1987). The chemistry and biological Molis, T. M., Spriggs, L. L., Jupiter, Y., & Hill, S. M. (1995). Melatonin modulation of significance of saponins in food and feeding stuffs. Critical Review in Food Science estrogen-regulated proteins, growth factors, and proto-oncogenes in human and Nutrition, 26, 27–135. breast cancer. Journal of Pineal Research, 18, 93–103. Prodanov, M., Sierra, I., & Vidal-Valverde, C. (1997). Effect of germination on the Morcos, S. R., Gabriel, G. N., & El-Hafez, M. A. (1976). Nutritive studies on some raw thiamine, riboflavin and niacin contents in legumes. Zeitschrift für and prepared leguminous seeds commonly used in the Arab Republic of Syria. Lebensmitteluntersuchung und -Forschung A, 205, 48–52. Zeitschrift fuer Ernaehrungswissenschaft, 15, 378–386. Pruzanski, W., & Vadas, P. (1991). Phospholipase A2 – A mediator between proximal Morris, E. R., & Hill, A. D. (1996). Inositol phosphate content of selected dry beans, and distal effectors of inflammation. Immunology Today, 12, 143–144. peas, and lentils, raw and cooked. Journal of Food Composition and Analysis, 9, Pryme, I. F., & Bardocz, S. (2001). Anti-cancer therapy: Diversion of polyamines in 2–12. the gut. European Journal of Gastroenterology and Hepatology, 13, 1041–1046. Mubarak, A. E. (2005). Nutritional composition and antinutritional factors of mung Pusztai, A. (1996). Characteristics and consequences of interactions of lectins with bean seeds (Phaseolus aureus) as affected by some home traditional processes. the intestinal mucosa. Archivos Latinoamericanos de Nutricion, 44, 10S–15S. Food Chemistry, 89, 489–495. Pusztai, A., Grant, G., Buchan, W. C., Bardocz, S., De Carvalho, A. F., & Ewen, S. W. Murphy, P. A., & Hendrich, S. (2002). Phytoestrogens in foods. Advances in Food and (1998). Lipid accumulation in obese Zucker rats is reduced by inclusion of raw Nutrition Research, 44, 195–246. kidney bean (Phaseolus vulgaris) in the diet. British Journal of Nutrition, 79, Muzquiz, M., Burbano, C., Ayet, G., Pedrosa, M. M., & Cuadrado, C. (1999). The 213–221. investigation of antinutritional factors in Phaseolus vulgaris. Environmental and Pusztai, A., Grant, G., Duguid, T., Brown, D. S., Peumans, W. J., Van Damme, E. J., et al. varietal differences. Biotechnolgie, Agronomie Societe et Environnement, 3, (1995). Inhibition of starch digestion by a-amylase inhibitor reduces the 210–216. efficiency of utilization of dietary proteins and lipids and retards the growth of Nachbar, M. S., & Oppenheim, J. D. (1980). Lectins in the United States diet. A survey rats. Journal of Nutrition, 125, 1554–1562. of lectins in commonly consumed foods and a review of the literature. American Radberg, K., Biernat, M., Linderoth, A., Zabielski, R., Pierzynowski, S. G., & Westrom, Journal of Clinical Nutrition, 33, 2338–2345. B. R. (2001). Enteral exposure to crude red kidney bean lectin induces Namba, T. (1980). Phaseolin semen. A full-color illustrated book of Japanese flora. maturation of the gut in suckling pigs. Journal of Animal Science, 79, 2669–2678. Tokyo: Hoikusha. Ranilla, L. G., Genovese, M. I., & Lajolo, F. M. (2009). Isoflavones and antioxidant Nardini, M., D’Aquino, M., Tomassi, G., Gentili, V., Di-Felice, M., & Scaccini, C. (1995). capacity of Peruvian and Brazilian lupin cultivars. Journal of Food Composition Inhibition of human low-density lipoprotein oxidation by caffeic acid and other and Analysis, in press. doi:10.1016/j.jfca.2008.06.011. hydroxycinnamic acid derivatives. Free Radical Biology and Medicine, 19, Reiter, R. J. (1980). The pineal and its hormones in the control of reproduction in 541–552. mammals. Endocrinology Review, 1, 109–131. National Research Council (1989). Recommended dietary allowances. Washington, Reiter, R. J. (1991). Melatonin: The chemical expression of darkness. Molecular Cell DC: National Academy of Sciences. Endocrinology, 79, C153–C158. Neilson, F. H. (1994). Chromium. In M. E. Shils, J. A. Olson, & M. Shike (Eds.), Modern Reiter, R. J. (2002). Potential biological consequences of excessive light exposure: nutrition in health and disease (8th ed., pp. 264–268). Lea and Febiger: Melatonin suppression, DNA damage, cancer and neurodegenerative diseases. Philadelphia. Neuro Endocrinology Letters, 23, 9–13. R. Campos-Vega et al. / Food Research International 43 (2010) 461–482 481

Remmelink, M., Darro, F., Decaestecker, C., De Decker, R., Bovin, N. V., Gebhart, M., arsenicosis and cancer in Bangladesh and West Bengal, India? Science of the et al. (1999). In vitro influence of lectins and neoglycoconjugates on the growth Total Environment, 323, 21–32. of three human sarcoma cell lines. Journal of Cancer Research and Clinical Steadman, K. J., Burgoon, M. S., Schuster, R. L., Lewis, B. A., Edwardson, S. E., & Oncology, 125, 275–285. Obendoff, R. L. (2000). Fagopyritols, o-chiro-inositol, and other soluble Reynoso-Camacho, R., Gonzalez de Mejia, E., & Loarca-Pina, G. (2003). Purification carbohydrates in buckwheat seed milling fractions. Journal of Agricultural and and acute toxicity of a lectin extracted from tepary bean (Phaseolus acutifolius). Food Chemistry, 48, 2843–2847. Food and Chemical Toxicology, 41, 21–27. Steer, T. E., & Gibson, G. R. (2002). The microbiology of phytic acid metabolism by Ricketts, M. L., Moore, D. D., Banz, W. J., Mezei, O., & Shay, N. F. (2005). Molecular gut bacteria and relevance for bowel cancer. International Journal of Food Science mechanisms of action of the soy isoflavones includes activation of promiscuous and Technology, 37, 783–790. nuclear receptors. A review. Journal of Nutritional Biochemistry, 16, 321–330. Tang, G. Y., Li, X. J., & Zhang, H. Y. (2008). Antidiabetic components contained in Rimm, E. B., Willett, W. C., Hu, F. B., Sampson, L., Colditz, G. A., Manson, J. E., et al. vegetables and legumes. Molecules, 13, 1189–1194. (1998). Folate and Vitamin B6 from diet and supplements in relation to risk of Tao, M. H., Xu, W. H., Zheng, W., Gao, Y. T., Ruan, Z. X., Cheng, J. R., et al. (2005). A coronary heart disease among women. Journal of the American Medical case–control study in Shanghai of fruit and vegetable intake and endometrial Association, 279, 359–364. cancer. British Journal of Cancer, 92, 2059–2064. Rochfort, S., & Panozzo, J. (2007). Phytochemicals for health, the role of pulses. Taylor, W. G., & Richards, K. W. (2008). Plant compositions enriched in Journal of Agricultural and Food Chemistry, 55, 7981–7994. dehydrosoyasaponin I (D-I) and methods of producing such compositions. Ruiz, R. G., Price, K. R., Arthur, A. E., Rose, M. E., Rhodes, M. J. C., & Fenwick, R. G. World Patent WO 2008083461. (1996). Effect of soaking and cooking on the saponin content and composition Terrés, C., Navarro, M., Martín-Lagos, F., Giménez, R., López, H., & López, M. C. of chickpeas (Cicer arietinum) and lentils (Lens culinaris). Journal of Agricultural (2001). Zinc levels in foods from southeastern Spain: Relationship to daily and Food Chemistry, 44, 1526–1530. dietary intake. Food Additives and Contaminants, 18, 687–695. Ryan, E., Galvin, K., O’Connor, T. P., Maguire, A. R., & O’Brien, N. M. (2007). Tharanathan, R. N., & Mahadevamma, S. (2003). Legumes – A boon to human Phytosterol, squalene, tocopherol content and fatty acid profile of selected nutrition. Trends in Food Science and Technology, 14, 507–518. seeds, grains, and legumes. Plant Foods for Human Nutrition, 62, 85–91. Thavarajah, D., Ruszkowski, J., & Vandenberg, A. (2008). High potential for selenium Rycroft, C. E., Jones, M. R., Gibson, G. R., & Rastall, R. A. (2001). A comparative in vitro biofortification of lentils (Lens culinaris L.). Journal of Agricultural and Food evaluation of the fermentation properties of prebiotic oligosaccharides. Journal Chemistry, 56, 10747–10753. of Applied Microbiology, 91, 878–887. Thewles, A., Parslow, R. A., & Coleman, R. (1993). Effect of diosgenin on biliary Salinas-Moreno, Y., Rojas-Herrera, L., Sosa-Montes, E., & Pérez-Herrera, P. (2005). cholesterol transport in the rat. Biochemical Journal, 291, 793–798. Anthocyanin composition in black bean (Phaseolus vulgaris L.) varieties grown in Thompson, G. R., & Grundy, S. M. (2005). History and development of plant sterol México. Agrociencia, 39, 385–394. and stanol esters for cholesterol-lowering purposes. American Journal of Sames, K., Schumacher, U., Halata, Z., Van Damme, E. J., Peumans, W. J., Asmus, B., Cardiology, 96, 3D–9D. et al. (2001). Lectin and proteoglycan histochemistry of Merkel cell carcinomas. Thomsson, A., Rantzer, D., Weström, B. R., Pierzynowski, S. G., & Svendsen, J. (2007). Experimental Dermatology, 10, 100–109. Effects of crude red kidney bean lectin (phytohemagglutinin) exposure on Sanchez-Vioque, R., Clemente, A., Vioque, J., Bautista, J., & Millan, F. (1998). Polar performance, health, feeding behaviour, and gut maturation of pigs at weaning. lipids of defatted chickpea (Cicer arietinum L.) flour and protein isolates. Food Journal of Animal Science, 85, 477–485. Chemistry, 63, 357–361. Trock, B. J., Hilakivi-Clarke, L., & Clarke, R. (2006). Meta-analysis of soy intake and Sandberg, A. S. (2002). Bioavailability of minerals in legumes. British Journal of breast cancer risk. Journal of the National Cancer Institute, 98, 459–471. Nutrition, 88, 281–285. USDA (2002). USDA-Iowa state university database on the isoflavone content of foods. Sarma, B. K., Singh, D. P., Mehta, S., Singh, H. B., & Singh, U. P. (2002). Plant growth- Washington, DC: Agricultural Research Service, U.S. Department of Agriculture. promoting rhizobacteria-elicited alterations in phenolic profile of chickpea Vadivel, V., & Janardhanan, K. (2000). Nutritional and anti-nutritional composition (Cicer arietinum) infected by Selerotium rolfsii. Journal of Phytopathology, 150, of velvet bean: An under-utilized food legume in South India. International 277–282. Journal of Food Sciences and Nutrition, 51, 279–287. Sastry, C. S. T., & Kavathekar, K. Y. (1990). Plants for reclamation of wastelands (p. Valdebouze, P., Bergeron, E., Gaborit, T., & Delort-Laval, J. (1980). Content and 684). New Delhi, India: Council of Scientific and Industrial Research. distribution of trypsin inhibitors and hemagglutinins in some legume seeds. Savage, G. P., & Deo, S. (1989). The nutritional value of peas (Pisum sativum). A Canadian Journal of Plant Science, 60, 695–701. literature review. Nutrition Abstracts and Reviews (Series A), 59, 66–83. Velie, E. M., Schairer, C., Flood, A., He, J.-P., Khattree, R., & Schatzkin, A. (2005). Schwarz, K., & Foltz, C. M. (1957). Selenium as an integral part of factor 3 against Empirically derived dietary patterns and risk of postmenopausal breast cancer dietary necrotic liver degeneration. Journal of the American Chemical Society, 79, in a large prospective cohort study. American Journal of Clinical Nutrition, 82, 3292–3293. 1308–1319. Sgarbieri, V. C., & Whitaker, J. R. (1982). Physical, chemical, and nutritional Venn, B. J., & Mann, J. I. (2004). Cereal grains, legumes and diabetes. European properties of common bean (Phaseolus) proteins. Advances in Food Research, 28, Journal of Clinical Nutrition, 58, 1443–1461. 93–166. Vidal-Valverde, C., Sierra, I., Diaz-Pollan, C., & Blazquez, I. (2001). Determination by Shamsuddin, A. M. (1999). Metabolism and cellular functions of IP6: A review. capillary electrophoresis of total and available niacin in different development Anticancer Research, 19, 3733–3736. stage of raw and processed legumes: Comparison with high-performance liquid Shamsuddin, A. M. (2002). Anti-cancer function of phytic acid. International Journal chromatography. Electrophoresis, 22, 1479–1484. of Food Science and Technology, 37(7), 769–782. Villegas, R., Gao, Y. T., Yang, G., Li, H. L., Elasy, T. A., Zheng, W., et al. (2008). Legume Shamsuddin, A. K. M., & Vucenik, I. (2005). IP6 and inositol in cancer prevention and and soy food intake and the incidence of type 2 diabetes in the Shanghai therapy. Current Cancer Therapy Reviews, 1, 259–269. Women’s Health Study. American Journal of Clinical Nutrition, 87, 162–167. Sharma, A., & Sehgal, S. (1992). Effect of processing and cooking on the Viroben, G. (1979). Substances indesirables pour le monogastrique [substances antinutritional factors of faba bean (Vicia faba). Food Chemistry, 43, 383–385. toxiques et nocives]. Le Sélectionneur-Français, 27, 21–25. Shi, J., Arunasalam, K., Yeung, D., Kakuda, Y., Mittal, G., & Jiang, Y. (2004). Saponins Vucenik, I., & Shamsuddin, A. M. (2006). Protection against cancer by dietary IP6 from edible legumes: Chemistry, processing, and health benefits. Journal of and inositol. Nutrition and Cancer, 55, 109–125. Medicinal Food, 7, 67–78. Wald, D. S., Law, M., & Morris, J. K. (2002). Homocysteine and cardiovascular Shils, M. E., Olson, J. A., Shike, M., & Ross, A. C. (1999). Modern nutrition in health and disease: Evidence on causality from a meta-analysis. British Medical Journal, 325, disease. Baltimore, MD: Williams & Wilkins. 1202–1208. Shils, M. E., Olson, J. A., & Shike, M. (1994). Modern nutrition in health and disease. Walker, A. F., & Ochhar, N. (1982). Effect of processing including domestic cooking Philadelphia, PA: Lea and Febiger. on nutritional quality of legumes. Proceedings of the Nutrition Society, 41, Shimura, S., Itoh, Y., Yamashita, A., Gitano, A., Hatano, T., Yoshida, T., et al. (1994). 41–51. Inhibitory effects of flavonoids on lipase. Nippon Shokuhin kogyo Gakkaishi, 41, Wang, H., Ng, T. B., Ooi, V. E., & Liu, W. K. (2000). Effects of lectins with different 847–850. carbohydrate-binding specificities on hepatoma, choriocarcinoma, melanoma Singh, U. P., Sarma, B. K., & Singh, D. P. (2003). Effect of plant growth promoting and osteosarcoma cell lines. International Journal of Biochemistry and Cell Biology, rhizobacteria and culture filtrate of Selerotium rolfsii on phenolic and salicylic 32, 365–372. acid contents in chickpea (Cicer arietinum). Current Microbiology, 46, 131–140. Wang, S. Y., Wu, J. H., Ng, T. B., Ye, X. Y., & Rao, P. F. (2004). A non-specific lipid Skene, D. J., Lockley, S. W., & Arendt, J. (1999). Use of melatonin in treatment of transfer protein with antifungal and antibacterial activities from the mung phase shift and sleep disorders. Advances in Experimental Medicine and Biology, bean. Peptides, 25, 1235–1242. 467, 79–84. Warrier, P. K. W., Nambiar, V. P. K., & Remankutty, C. (1995). Indian medicinal plants. Skinner, D. C., & Malpaux, B. (1999). High melatonin concentrations in third Chennai, India: Orient Longman. ventricular cerebrospinal fluid are not due to Golen vein blood recirculating Wattenberg, L. W., Wiedmann, T. S., Estensen, R. D., Zimmerman, C. L., Galbraith, A. through the choroid plexus. Endocrinology, 140, 4399–4405. R., Steele, V. E., et al. (2000). Chemoprevention of pulmonary carcinogenesis by Smulikowska, S., Pastuszewska, B., Swiech, E., Ochtabinska, A., Mieczkowska, A., brief exposures to aerosolized budesonide or beclomethasone dipropionate and Nguyen, V. C., et al. (2001). Tannin content affects negatively nutritive value of by the combination of aerosolized budesonide and dietary myo-inositol. pea for monogastrics. Journal of Animal and Feed Sciences (Poland), 10, 511–523. Carcinogenesis, 21, 179–182. Souci, S. W., Fachmann, W., & Kraut, H. (1994). Food composition and nutrition tables Weaver, C. M., & Kannan, S. (2002). Phytate and mineral bioavailability. In Sathe & S. (5th ed.). CRC Press, Stuttgart: Medpharm Scientific Publications. K. Reddy (Eds.), Food phytates (pp. 211–224). Boca Raton: CRC. Spallholz, J. E., Mallory Boylan, L., & Rhaman, M. M. (2004). Environmental Weihrauch, J. L., & Gardner, J. M. (1978). Sterol content of foods of plant origin. hypothesis: Is poor dietary selenium intake an underlying factor for Journal of the American Dietetic Association, 73, 39–44. 482 R. Campos-Vega et al. / Food Research International 43 (2010) 461–482

Welch, R. M., & Graham, R. D. (2004). Breeding for micronutrients in staple food Yeh, C. T., & Yen, G. C. (2003). Effects of phenolic acids on human crops from a human nutrition perspective. Journal of Experimental Botany, 55, phenolsulfotransferases in relation to their antioxidant activity. Journal of 353–364. Agricultural and Food Chemistry, 51, 1474–1479. Williams, D. E., Prevost, A. T., Whichelow, M. J., Cox, B. D., Day, N. E., & Wareham, N. Yoshida, H., Tomiyama, Y., Yoshida, N., Saiki, M., & Mizushina, Y. (2008). Lipid J. (2000). A cross-sectional study of dietary patterns with glucose intolerance classes, fatty acid compositions and triacylglycerol molecular species from and other features of the metabolic syndrome. British Journal of Nutrition, 83, adzuki beans (Vigna angularis). Journal of Food Lipids, 15, 343–355. 257–266. Zdunczyk, Z., Godycka, I., & Amarowicz, R. (1997). Chemical composition and Woldemichael, G. M., Montenegro, G., & Timmermann, B. N. (2003). Triterpenoidal content of antinutritional factors in Polish cultivars of peas. Plant Foods for lupin saponins from the Chilean legume Lupinus oreophilus Phil.. Phytochemistry, Human Nutrition, 50, 37–45. 63, 853–857. Zhang, J., Shi, J., Ilic, S., Jun, X. S., & Kakuda, Y. (2009). Biological properties and Wu, C., & Whitaker, J. R. (1991). Homology among trypsin/chymotrypsin inhibitors characterization of lectin from red kidney bean (Phaseolus vulgaris). Food from red kidney bean, Brazilian pink bean, lima bean, and soybean. Journal of Reviews International, 25, 12–27. Agricultural and Food Chemistry, 39, 1583–1589. Zhou, J. R., & Erdman, J. W. Jr., (1995). Phytic acid in health and disease. Critical Xiao, J. X., Huang, G. Q., Zhu, C. P., Ren, D. D., & Zhang, S. H. (2007). Morphological Reviews in Food Science and Nutrition, 35, 495–508. study on apoptosis HeLa cells induced by soyasaponins. Toxicology in Vitro, 21, Zhu, J., Xiong, L., Yu, B., & Wu, J. (2005). Apoptosis induced by a new member of 820–826. saponin family is mediated through caspase-8-dependent cleavage of Bcl-2. Xing, N., Chen, Y., Mitchell, S. H., & Young, Y. F. C. (2001). Quercetin inhibits the Molecular Pharmacology, 68, 1831–1838. expression and function of the androgen receptor in LNCaP prostate cancer Zia-Ul-Haq, M., Iqbal, S., Ahmad, S., Bhanger, M. I., Wiczkowsi, W., & Amarowicz, R. cells. Carcinogenesis, 22, 409–414. (2008). Antioxidant potential of desi chickpea varieties commonly consumed in Xu, B. J., & Chang, S. K. C. (2007). A comparative study on phenolic proﬁles and Pakistan. Journal of Food Lipids, 15, 326–342. antioxidant activities of legumes as affected by extraction solvents. Journal of Zielínski, H., Lewczuk, B., Przybylska-Gornowicz, B., & Kozowska, H. (2001). Food Science, 72, S159–S166. Melatonin in germinated legume seeds as a potentially signiﬁcant agent for Xu, B. S., & Chang, K. C. (2008). Effect of soaking, boiling, and steaming on total health. In W. Pfanhauser, G. R. Fenwick, & S. Khokhar (Eds.), Biologically-active phenolic content and antioxidant activities of cool season food legumes. Food phytochemicals in food: Analysis, metabolism, bioavailability and function (pp. 26– Chemistry, 110, 1–13. 28). Proceedings of the EUROFOODCHEM XI, Norwich, UK.