Chemoprevention of Colorectal Cancer by Dietary Compounds
Abstract
:1. Introduction
2. General Aspects of CRC
3. General Aspects Regarding the Dietary Compounds
3.1. Phenolic Compounds
3.2. Carotenoids
3.3. Iridoids
3.4. Nitrogen Compounds
3.5. Organosulfur Compounds
3.6. Phytosterols
3.7. Essential Oil Compounds
3.8. Polyunsaturated Fatty Acids (PUFA)
3.9. Dietary Fiber
4. In Vitro Studies
4.1. Polyphenols
4.1.1. Flavones
4.1.2. Isoflavones
4.1.3. Phenocarboxilic Acids
4.1.4. Stilbens
4.1.5. Other Compounds
4.2. Non-polyphenolic Compounds—In Vitro Mechanism of Action
4.2.1. Carotenoids
4.2.2. Nitrogen Compounds
5. In Vivo Studies in CRC Animal Models
5.1. The Effect of Phenolic Compounds
5.1.1. Isoflavones
5.1.2. Anthocyanidins
5.1.3. Phenocarboxilic Acids
5.1.4. Lignans
5.2. The Effect of Non-Phenolic Compounds
5.2.1. Carotenoids
5.2.2. Iridoids
5.2.3. Nitrogen Compounds
5.2.4. Phytosterols
5.2.5. Organosulfur Compounds
5.2.6. Essential Oils
5.2.7. Polyunsaturated Fatty Acids
5.2.8. Dietary Fiber
6. Chemoprevention of CRC by Dietary Compounds in Humans
6.1. Phenolic Compounds
6.1.1. Isoflavones
6.1.2. Lignans
6.1.3. Anthocyanidins
6.2. Non-phenolic Compounds
6.2.1. Organosulfur Compounds
6.2.2. Carotenoids
6.2.3. Polyunsaturated Fatty Acids
6.2.4. Dietary Fiber
7. Bioavailability of the Natural Dietary Compounds
7.1. Bioavailability of Phenolic Compounds
7.2. Bioavailability of Non-Phenolic Compounds
7.3. Encapsulation Strategies for Increased Bioavailability
8. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
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Dietary Compounds | Chemical Structure | Representative Compounds | Sources |
---|---|---|---|
Flavonoids | |||
Flavones | Apigenin, luteolin | Celery (Apium graveolens L.), onions (Allium cepa L.), broccoli (Brassica oleracea italic Plenck.), red orange (Citrus x sinensis L. Osbeck), green pepper (Capsicum sp.) | |
Flavonols | Quercetin, kaempferol, myricetin | Broccoli (Brassica oleracea italic Plenck.), lettuce (Lactiva sativa L.), onions (Allium cepa L.), kale (Brassica oleracea L.), leek (Allium ampeloprasum L.), apricot (Prunus armeniaca L.), apple (Malus domestica Borkh.), blueberry (Vaccinium corymbosum Rydb.), black currant (Ribes nigrum L.) | |
Flavonones | Naringenin, hesperitin, diosmetin | Orange (Citrus x aurantium sp. L.), grepfruit (Citrus paradise Macfad.), lemon (Citrus limon L.) | |
Isoflavones | Genistein, daidzein, glycitein | Soybeans (Glycine max L.) boiled, miso, tofu, soy milk, soy flour | |
Flavan-3-Ol Monomeric catechins | Catechin, epicatechin, epigallocatechin, epigallocatechin-3-O-gallate | Apple (Malus domestica Borkh.), peach (Prunus persica L.), green tea, black tea (Camelia sinensis L.), red wine, grapes (Vitis vinifera L.), beans (Phaseolus vulgaris L.) | |
Protoanthocyanidins or condensed tannins | Protoanthocyanidin B | Proanthocyanidin A, B | American cranberry (Vaccinium macrocarpon Aiton.), cranberry (Vaccinium oxycoccus L.), chokeberries (Aronia melanocarpa Elliott.), plum (Prunus domestica L.), blueberry (Vaccinium myrtillus L.), red currant (Ribes rubrum L.), lingonberries (Vaccinium vitis-idaea L.), pear (Pyrus communis L.), apple (Malus domestica Borkh.), almonds (Prunus dulcis Mill.), hazelnuts (Corylus spp.), pecans (Carya illinoinensis Wangenh.), pistachio nuts (Pistacia vera L.), walnuts (Juglans regia L.), grape seeds (Vitis vinifera L.), beans (Phaseolus vulgaris L.), cowpea (Vigna unguiculata Walp.), lentils (Lens culinaris Medik.), barley (Hordeum vulgare L.), rice (Oryza sativa L.), sorghum (Sorghum bicolor L. Moench.) |
Anthocyanidins/Anthocianins | Delphinidin (R1, OH; R2, OH; R3, OH); cyanidin (R1, OH; R2, OH; R3, H) malvidin (R1, OH; R2, OCH3; R3, OCH3); pelargonidin (R1, OH; R2, H; R3, H) | Blackberry (Rubus fruticosus L.), raspberry (Rubus idaeus L.), bilberry (Vaccinium myrtillus L.), plum (Prunus sp), sour cherry (Prunus cerasus L.), black grapes (Vitis vinifera L.), elderberry (Sambucus nigra L.), red cabbage (Brassica oleracea L.) | |
Non-Flavonoids | |||
Tannins A. Gallotannins derivatives | Ellagic acid | Raspberry (Rubus idaeus L.), strawberry (Fragaria x ananassa Duchesne.), pomegranate (Punica granatum L.), black currants (Ribes nigrum L.), blackberry (Rubus fruticosus L.), guava (Psidium guajava L.) | |
B. Elagotannins derivatives | Gallic acid | ||
Phenol-Carboxilic Acids A. Hydroxybenzoic acids | Gallic acid (R1, OH; R2, OH; R3, OH), syringic acid (R1, OCH3, R2, OCH3, R3, OH) | Broccoli (Brassica oleracea italica Plenck.), cowpea (Vigna unguiculata Walp.), spinach (Spinacia oleracea L.), black currant (Ribes nigrum L.), acai palm (Euterpe oleracea Mart.), sugar apple (Ananona squamosa L.) | |
B. Hydroxy-cinnamic acids | Cinnamic acid (R1, H; R2, H; R3, H; R4, OH), Caffeic acid (R1, OH; R2, OH; R3, H; R4, OH), chlorogenic acid, ferulic acid acid (R1, H; R2, OH; R3, OCH3; R4, OH), sinapic acid (R1, OCH3; R2, OH; R3, OCH3; R4, OH), p-coumaric acid (R1, H; R2, OH; R3, H; R4, OH), rosmarinic acid | Pear (Pyrus communis L.), kiwi (Actinidia deliciosa C.F.Liang and A.R.Ferguson), plum (Prunus domestica L.), apple (Malus domestica Borkh.), artichoke (Cynara scolymus L.), potato (Solanum tuberosum L.), coffee (Coffea arabica L.), rosemary (Rosmarinus officinalis L.), basil (Ocimum basilicum L.), oregano (Origanum vulgare L.), sage (Salvia officinalis L.) | |
Lignans | Secoisolariciresinol, sesaminol, sesamol, sesamin | Flaxseed/ linseed (Linum usitassimum L.), sesameseed (Sesamum indicum L.) | |
Stilbens | Resveratrol (R1, OH; R2, OH; R3, OH) | Red wine, red grapes (Vitis vinifera L.), plum (Prunus domestica L.) | |
Other Compounds | Curcumin | Turmeric (Curcuma longa L.) | |
Gingerol | Ginger (Zingiberis officinale Roscoe.) |
Dietary Compounds | Chemical Structure | Representative Compounds | Sources |
---|---|---|---|
Carotenoids | Lycopene | Tomatoes (Solanum lycopersicum L.), guava (Psidium guajava L.), pumpkin (Cucurbita pepo L.), carrot (Daucus carota subsp. sativus), rose hip (Rosa rugosa Thunb.), watermelon (Citrullus lanatus Thunb.), saffron (Crocus sativa L.) | |
α-carotene | |||
β-Carotene | |||
Crocetin | |||
Iridoids | Oleuropein | Unripe olive fruits, table olives, virgin olive oil (Olea europaea L.) | |
Nitrogen Compounds A. Alkaloids | Piperine | Black pepper (Piper nigrum L.); long pepper (Piper longum L.) | |
B. Non-alkaloidic compounds | Capsaicin | Chilli pepper (Capsicum sp.) | |
Organosulfur Compounds | Allicin | Garlic (Allium sativum L.), onion (Allium cepa L.), broccoli (Brassica oleracea italica Plenck.) | |
Allin | |||
Sulforaphane | |||
Phytosterols | β-sitosterol | Zucchini (Cucurbita pepo L.), lettuce (Lactuca sativa L.), mangold (Betta vulgaris L.), white cabbage (Brassica oleracea L.), pumpkin seed (Cucurbita pepo L.), oat (Avena sativa L.), peanut (Arachys hypogaea L.), mushrooms (Agaricus bisporus, Lentinula edodes, Grifolia frondosa, Boletus edulis, Pleurotus osteatrus, Armillaria mellea) | |
Stigmasterol | |||
Ergosterol | |||
Campesterol | |||
Essential Oil Compounds | Thymol | Essential oils of thyme (Thymus vulgaris L.), wild thyme (Thymus serphyllum L.), oregano (Origanum vulgare L.), lemon balm (Melissa officinalis L.), cinnamon (Cinnamomum sp.), aniseed (Pimpinella anisum L.), star anise (Illicium verum Hook.), fennel (Foeniculum vulgare Mill.), black cumin (Nigella sativa L.) | |
Carvacrol | |||
Citronellal | |||
Cinnamaldehyde | |||
Anethole | |||
Thymoquinone | |||
Polyunsaturated Fatty Acids A. Omega-3 fatty acids | α-linolenic acid (ALA) | Catfish (Silurus glanis), anchovy (Engraulis encrasicolus), bluefish (Pomatomus saltatrix), sardine (Sardina pilchardus), tuna (Thunnus thynnus), spiny lobster (Panulirus argus), mussels (Mytilus edulis), oyster (Ostrea lurida), herring (Clupea harengus membras, C. h. harengus), mullet (Mugil cephalus), shrimps (Palaemon serratus), seaweeds (Rhodophyta phylum, Phaeophyceae class, Chlorophyta phylum); seed oil from: Hemp (Cannabis sativa L.), chia (Salvia hispanica L.), echium (Echium plantagineum L.), flax (Linum usitassinum L.); walnut oil (Juglans regia L.) | |
Docosahexaenoic acid (DHA) | |||
Eicosapentaenoic acid (EPA) | |||
B. Omega-6 fatty acids | Linoleic acid (LA) | Black currant (Ribes nigrum L.) seed oil, gooseberries (Ribes grossularia L.) seed oil, hemp (Cannabis sativa L.) seed oil; meet from beef (Bos taurus), lamb (Ovis aries), pork (Sus scrofa domesticus) | |
γ–linolenic acid (GLA) | |||
Dietary Fiber | Inulin | Sweet potato (Ipomoea batatas L.), leek (Allium ampeloprasum L.), garlic (Allium sativum L.), onion (Allium cepa L.) | |
Galactooligosaccharides | Apple (Malus domestica Borkh.), pear (Pyrus communis L.), potato (Solanum tuberosum L.), beans (Phaseolus vulgaris L.), brusselsprouts (Brassica oleracea var. gemmifera L.), whole wheat (Triticum L.), whole corn (Zea mays L.), chickpea (Cicer arientinum L.), apricot (Prunus armeaniaca L.) | ||
Fructooligosaccharides | |||
β-glucans | Mushrooms (Agaricus bisporus, Lentinula edodes, Grifolia frondosa, Boletus edulis, Pleurotus osteatrus, Armillaria mellea) | ||
Glucomannans | Konjac (Amorphophallus konjac Koch.) |
Author, Year | Animal Models | Doses and Duration of Administration | Results |
---|---|---|---|
Genistein | |||
Song S. et al., 2018 [157] | Mice with AOM/DSS CRC | 225 mg/kg diet; 450 mg/kg diet and 900 mg/kg diet—six month | Significant improvement of colon architectural repair, anti-inflammatory activity ↓ COX-2, TNF-α; ↓ expression of PI3K/AKT pathway; ↑expression of FOXO3, Bax proteins |
Zhang Y. et al., 2013 [101] | Sprague–Dawley rats with AOM induced CRC | Pre-treatment diet supplementation with 140 mg/kg—six weeks, before induction of cancer | Inhibition of aberrant crypt foci, prevention of nuclear β-catenin accumulation, suppression of cyclin D1, c-myc expression and Wnt signaling genes (Wnt1, Wnt5a, Sfrp1, Sfrp5) |
Son T.G. et al., 2013 [158] | BALB/mice subcutaneously injected with CT26 mouse colon cancer cells | Tumor bearing mice are treated with genistein 200 mg/kg 1 day before radiation (5, 10 Gy); evaluation of tumors after 12 h, 3.5 days | genistein increased progenitor cell survival and cell death after radiation, recovery of intestinal damage after radiation (↑ Ki-67), significant tumor regression for combined treatment |
Cyanidin/Pelargonidin/Malvidin | |||
Kang S.Y. et al., 2003 [159] | Apcmin mice-mutant mouse lineage predisposed to multiple intestinal neoplasia due to mutations in adeno-matous polyposis coli (APC) gene | 800 mg/L anthocyanidins/200 mg/L (rich in cyanidin glucosides) in the drinking water and modified diet with 200 g/kg freeze dried cherries | Fewer and smaller adenomas in the cecum compared to control Colon tumor volume was not significantly reduced |
Shi N. et al., 2015 [160] | Male CRJ:CD-1 (ICR) mice with CRC induced with AOM/DSS | 2.5%; 5%; 10% freeze-dried strawberries—cyanidine glucoside (1.67%) and pelargonidin glucoside (41.1%)—20 weeks | Inhibition of tumor development from 100% (control) to 74–44%, ↓ of nitrotyrosine production, ↓ Nf-kb, PI3K/AKT phosphorylation, ↓ COX-2, iNOS expression |
Silva R.M. et al., 2015 [161] | Wistar rats with AOM induced CRC | Administration of 1% (222 mg/zi) or 2% red grape juice (444 mg/zi), two weeks before AOM or 4 weeks after the last administration of AOM | ↓ COX-2 mRNA with 1% grape juice before AOM and with 2% juice after the last AOM administration |
Fernandez J. et al., 2018 [162] | Male Fischer 344 rats with AOM/DSS induced CRC | 20 g/day/rat of functional sausage with 0.11 anthocyanins (mixture of 1:1 dehydrated strawberries and blackberries powder with 59% cyanidin-3-glucosides and 41% pelargonidin-3-glucosides) | Significant reduction of Peyer patches, caecum weight, number of polyps; Significant reduction of Bilophila wadsworthia—a bacteria that generated high level of H2S and has pro-inflammatory effects |
Chlorogenic Acid | |||
Matsunaga K. et al., 2002 [163] | Male F344 rats with CRC induced with AOM | 250 ppm chlorogenic acid was administered one week before and a one week after tumor induction with AOM; study duration 36 weeks | Significant decrease of colon tumors for pre- treatment with chlorogenic acid |
Banerjee N. et al., 2016 [164] | Sprague Dawly rats with AOM induced CRC | Plum (Prunus salicina L.) beverage rich in chlorogenic and neochlorogenic acids, 10 weeks | Significant decrease of dysplastic polyps, ↓ expression of COX-2, Nf-kB, AKT/mTOR signaling pathway, ↑ miR-143 |
Cinnamic Acid | |||
Zhu B. et al., 2016 [165] | Female BALB/c nude mice inoculated with HT29 colon carcinoma cells | 1 and 1.5 mmol/kg x3/week for two weeks | Significant inhibition of tumor growth, ↑ expression of Bax and caspase 3 |
p-Coumaric Acid | |||
Sharma S.H. et al., 2017 [166] | Male albino rats with DMH induced CRC | 50 mg/kg, 100 mg/kg, 200 mg/kg; 15 weeks | Significant dose-dependent reduction of polyps incidence and formation of pre-neoplasic lesions, reduction of oxidative stress; significant decrease in gut microbial enzymes (mucinases and β-dehydrogenases) |
Rosmarinic Acid (RA) | |||
Venkatachalam K. et al., 2013 [167] | Male wistar rats with DMH induced CRC | 5 mg/kg received during administration of DMH (15 weeks) or one week after the last DMH dose (until 30 weeks) or through the whole period (30 weeks) | Supplementation with RA for the whole period showed the highest tumor reduction, ↓ stress oxidative markers, ↓mucosal bacterial enzymes activity, regulation of xenobiotic metabolizing enzymes, up-regulation of apoptotic factors |
Gallic Acid | |||
Giftson J.S. et al., 2011 [168] | Male albino Wistar rats with DMH induced CRC | 50 mg/kg received one week before DMH and continued 30 weeks (group 1), after cessation of DMH until 30 weeks (group 2), along the whole period (group 3) | Supplementation with gallic acid for the whole period showed the highest tumor reduction, regulation xenobiotic metabolizing enzymes, decreased tumor incidence |
Secoisoscilaresinol | |||
Shah N.R. and Patel B.M., 2016 [169] | Diabetic male Sprague Dawley rats with DMH induced CRC | 500 mg/kg p.o secoisolariciresinol rich extract of L. ussitatissimum—18 weeks | ↓ pro-inflammatory markers, ↓ PCNA, ↓ CEA, ↓ mRNA level of CDK4, reduction in hyperplastic cells |
Gomides A.F. et al., 2016 [170] | C57 BL6 mice with DMH induced CRC | 10% defatted flaxseed meal—15 weeks | Reduction of precancerous lesions in the distal colon |
Sesamol | |||
Shimizu S. et al., 2014 [171] | C57/BL6-Apc Min/+ mice | 500 pp/8 weeks | ↓ pro-inflammatory factors, suppression of intestinal polyps formation |
Author, Year | Animal Models | Doses and Duration of Administration | Results |
---|---|---|---|
Lycopene | |||
Tang F.Y. et al., 2011 [173] | BALB/cAnN-Foxn1 nude mice with CRC induced by inoculation of HT-29 cells | 3/6 mg/kg—5 weeks | Significant inhibition of tumor growth |
Dias M.C. et al., 2010 [174] | Male Wistar rats with DMH induced CRC | 300 mg/kg lycopen + symbiotic (60 mg oligofructose + 50 mg inulin + 109 CFU Bifidobacteria lactis)—eight weeks (before/during or after initiation with DMH) | ↓ PCNA, ↓ p-53 colonic cells, ↓ AFC, ↓colonic Paneth cells |
Crocin | |||
Kawabata K. et al., 2012 [175] | CD1 (ICR) mice with AOM/DSS induced CRC | 50, 100, 200 ppm for 15 weeks after initiation of colon cancer | Significant reduction of inflammation and mucosal ulcers, multiplicity of adenocarcinoma |
Oleuropein | |||
Giner E. et al., 2016 [176] | C57BL6 mice with AOM/DSS colorectal induced cancer | 50 mg/kg or 100 mg/kg—63 weeks | Inhibition of tumor formation, decreased cell proliferation, anti-inflammatory activity |
Capsaicin | |||
Caetano B.F.R. et al., 2018 [177] | Male WISTAR rats with DMH induced colorectal cancer | 5 mg/kg or 50 mg/kg—four weeks | ↓Ki-67, significant ↓ of tumor volume and number of AFC |
Sulforaphane/Organosulfur Compounds | |||
Rajendran P. et al., 2015 [178] | Male WT or Nrf2−/+ mice with DMH induced CRC | Mice received alternating or daily 400 ppm sulforaphane included in the diet for 25 weeks | Significant reduction in tumor multiplicity only after continuous treatment |
β-Sitosterol | |||
Baskar A.A. et al., 2012 [179] | Male albino Wistar rats with DMH induced CRC | 5 mg/kg; 10 mg/kg; 20 mg/kg —16 weeks | Significant increase of antioxidant defense system, ↑ GSH, ↓ hyperplasic lesions |
Thymoquinone (TQ) | |||
Asfour W. et al., 2013 [180] | Male albino rats with DMH induced CRC | Administration of 10 mg/kg for 10 weeks (in the initiation phase + DMH) and 11 weeks (in the post initiation phase, after induction of cancer) | Chemopreventive effect, significant inhibition of tumor growth (for simultaneously administration in the initiation phase), ↓ PCNA, inhibition of VEGF production |
Kortum B. et al., 2015 [181] | Male and female Msh2 loxP/loxP Villin-Cre mice—transgenic mice that simulate intestinal carcinogenesis | Mice were divided in 5 groups: Group 1—regular chow; group 2—500 mg mesalazine/kg chow, group 3—2500 mg mesalazine/kg chow; group 4—37.5 mg TQ /kg chow; group 5—375 mg TQ/kg chow; treatment for 43 weeks | ↓ incidence of tumors dose dependent for TQ; no significant differences between TQ and mesalazine |
Cinnamaldehyde | |||
Long M. et al., 2015 [182] | Experimental Nrf2+/+ and Nrf2−/− C57BL/6 mice with AOM/DSS induced CRC | Supplementation of diet with 0.5% cinnamaldehyde—11 weeks | Supplementation significantly attenuated colon carcinogenesis only for Nrf2+/+ mice; anti-inflammatory and antioxidant effects |
Carvacrol | |||
Sivaranjani A. et al., 2016 [183] | Male Albino WISTAR rats with DMH induced CRC | Administration of 20, 40, 80 mg/kg for 16 weeks | Reduced tumor incidence, inhibition of aberrant crypts formation, ↑ in antioxidant defense system, ↓ activity of colonic bacterial enzymes |
Omega-3/Omega-6 Fatty Acids | |||
Wang W. et al., 2017 [184] | C57 BL6 mice with CRC induced by inoculation of MC38 CRC cells | Pre-treatment (3 weeks) with DHA diet (omega-6/omega-3 ratio = 1.26:1) and DHA high diet (omega-6/omega-3 ratio = 0.56:1) before tumor initiation (3 weeks) DHA diet—22 g/kg LA, 0.31 g/kg ALA, 17.2 g/kg DHA; DHA high diet—12.5 g/kg—LA, 0.17 g/kg—ALA, 21.9 g/kg DHA | Inhibition of colon growth, modulation of fatty acids profile in colon tumors (↓ARA, ↑EPA, DHA), ↓ EETS |
Hao G.W. et al., 2015 [185] | BALB/c nude mice with CRC induced by inoculation of HCT116 colon cancer cells | Ketogenic diet with or without omega-3 fatty acids; supplementation received until tumor volume was 600–700 mm3 (45 days) | Delayed tumor growth ↓ tumor vascularity for ketogenic diet supplemented with omega-3 fatty acids |
Piazzi G. et al., 2014 [186] | C57BLJ/6J mice with AOM/DSS induced CRC | Effect of 1% eicosapentaenoic free fatty acid on both initiation and progression of carcinogenesis, 105 days | Suppression of tumor development, increase of apoptosis, anti-inflammatory effects, modulation of gut microbiota |
Barone M. et al., 2014 [187] | C57BLJ/6J mice with mutation for the Apc gene (Apc Min/+) | Supplementation of diet with olive oil and omega-3 fatty acids, 10 weeks | Decrease in polyps number, pro-apoptotic effects |
Dietary Fibers | |||
Wang J. et al., 2017 [188] | Athymic male nude mice BALB/c-nu with CRCobtained by inoculation of HT-29 cancer cells | Administration of a polysaccharide from Lentinus edodes (0.2 mg/kg; 1 mg/kg; 5 mg/kg) or 20 mg/kg 5-fluorouracil for 21 days after cancer induction | ↓ tumor growth, pro-apoptotic effects |
Masuda Y. et al., 2013 [189] | Female BALB/c, BALB/c-nude, C3H/HeJ mice inoculated with colon-26 cancer cells | Administration of D fraction (β-glucan) from the maitake mushroom (Grifola frondolosa) for 19 days after cancer induction | Significant decrease of tumor growth through systemic immune responses |
Pattananandecha T. et al., 2016 [190] | Male Sprague-Dawley rats with AOM induced CRC | Supplementation of diet with 10% inulin for 17 weeks | Reduction of colonic AFC, reduction in bacterial colon enzymes, increase in Lactobacillus sp, Bifidobacteria |
Qamar T.R. et al., 2016 [191] | Male Wistar rats with DMH induced CRC | Administration of galacto-oligosaccharides (76–151 mg), inulin (114 mg) separately or co-administration for 16 weeks | For co-administration significant ↓ in AFC formation and fecal enzyme activities |
Hijova E. et al., 2013 [192] | Male and female Sprague-Dawly rats with DMH induced CRC | Supplementation of diet with 80 g inulin/kg food for 28 weeks | Significant ↓ coliform counts and ↑ lactobacilli counts, ↓ fecal enzyme activities, anti-inflammatory effects |
Verma A. and Shukla G., 2013 [193] | Male Sprague Dawly rats with DMH induced colorectal cancer | Administration of inulin 10 mg/0.1 mL for a week before initiation of CRC and 6 weeks after initiation | ↓ of AFC and nitroreductase/β-glucosidase activity |
Stofilova J. et al., 2015 [194] | Male and female Sprague Dawly rats with DMH induced colorectal cancer | Co-administration of oligofructose-enriched inulin preparation (95% fructan chains and 5% monosaccharide and disaccharide) with 109 CFU/mL for 28 weeks | ↓ inflammatory process in the jejuna and colon mucosa |
Wu W.T. et al., 2014 [195] | Male C57/BL/6J with AOM induced colorectal cancer | Administration of high-fat low fibre diet (1% cellulose) or high 5% fibre diet with konjac glucomannan, inulin, cellulose for 3 weeks before cancer initiation | Konjac glucomannan and inulin have anti-genotoxic effects, increase cecal short chain fatty-acids, up-regulate antioxidant enzymes genes |
Author, Year | Date/Type of Study | Cases | Control Cases | Dose | OR/HR/RR/IRR/SRR (95%CI)/Observation | Conclusions |
---|---|---|---|---|---|---|
Isoflavones (IF) | ||||||
Akhter M. et al. 2009 [202] | 2004–2005/control-study | 721; men and women 40–79 years old | 697 | 24.77–62.41 mg IF/day | OR 0.49 (0.27–0.90) to 0.53 (0.28–0.98) p < 0.05 | Significant inverse association between high intake of isoflavone consumption and CRC in women |
Shin A. et al. 2015 [210] | Case control study/2010–2013 | 901 men and women | 2669 | Daidzein 3.20–9.89 mg/day Genistein 3.3–9.7 mg/day Glycitein 0.85–2.44 mg/day | OR Daidzein 1.25 (0.96–1.61) to 0.71 (0.54–0.95) Genistein 1.18 (0.91–1.53) to 0.75 (0.57–1) Glycitein 1.32 (1.03–1.70) to 0.39 (0.25–0.61) | A high intake of isoflavones is significantly associated with decreased risk of CRC in both men and women |
Yang G. et al. 2009 [211] | Prospective cohort study /1996–2005 | 68,412 women 40–70 years old | NA | 12.8–21 g soy food intake/day equivalent to 15.1–48.9 mg IF/day | RR Soy food 0.88 (0.67–1.15) to 0.71 (0.53–0.95) Soy isoflavones 0.91 (0.69–1.19) to 0.80 (0.60–1.07) | High intake of soy food products and isoflavones is correlated with reduced incidence in CRC, especially for menopausal women |
Ko K. et al. 2018 [205] | Case control study in Korean (1993–2004) and Vietnamese population (2003–2007) | 101 (Korean study) 222 cases (Vietnamese study) | 391 (Korean study) 226 (Vietnamese study) | Evaluation of plasma IF levels for patients with CRC | OR for genistein 0.67 (0.34–1.31) to 0.50 (0.25–0.98)—Korean patients OR for genistein 0.97 (0.54–1.74) to 0.43 (0.25–0.73)—Vietnamese patients OR for daidzein (Vietnamese patients) 0.84 (0.47–1.49) to 0.48 (0.28–0.82) | Significant inverse correlation between high isoflavones plasma concentrations and reduced colorectal incidence |
Lignans | ||||||
Principi M, et al. 2013 [208] | Randomized double blind placebo-controlled study | 30 patients | 30 placebo | Supplementation of diet with 750 mg insoluble oat fiber, 50 mg flaxseed dry extract with 20% secoisolariciresinol diglycoside +175 mg milk thistle extract (70% silymarin and 30% silibinin)—60 days prior to colonoscopy | Significant increase in ERβ/ERα ratio and activation of caspases | Modulation of ERβ receptor is important for a chemo-preventive effect |
Calabrese C. et al. 2013 [209] | Open study /2012–2013 | 11 patients with familial adenomatous polyposis with ileal pouch anal anastomosis | NA | 5 mg Eviendep® (30% silibinin + 40% secoisolariciresinol diglucoside + indigestible fibers 5% lignin) × 2/day for 3 month | Significant reduction of number and size of polyps with 32% and 51% respectively | Chemo-preventive effect |
Zamora-Ros R. et al. 2013 [204] | Case control study /1996–1998 | 426 | 401 | 0.27–0.50 mg lignans/1000 kcal day | RR for Lignans 0.72 (0.47–1.10) to 0.59 (0.34–0.99) | Significant inverse correlation between high intake of lignans and colorectal incidence |
Anthocyanidins | ||||||
Thomasset S. et al. 2009 [212] | Pilot study 2006–2008 | 15 patients with histological confirmed; 10 patients with colorectal liver metastasis | NA | 1.4/2.8/5.6 g of Mirtocyan (a standardized extract rich in anthocyanidins) for 7 days before surgery | Mild decrease of tumor tissue only for 1.4 g | Possible chemo-preventive effects in humans |
Wang L. S. et al. 2014 [213] | Randomized double blind placebo control study | 14 patients with familial adenomatous polyposis | NA | Group I—7 patients placebo powder (60 g/day) + 2 rectal suppositories (each 720 mg freeze-dried black raspberry extract) Group 2—60 g/day black raspberry freeze dried extract + 2 rectal suppositories—9 month treatment | Reduction of polyps mainly for suppositories Significantly de-methylated regions in adenomas | Regressing of rectal polyps in patients with familial adenomatous polyposis |
Organosulfur Compounds | ||||||
Tanaka S. et al. 2006 [214] | Preliminary double blind randomized clinical trial | 37 patients with colorectal adenomas which are removed if the size was > 5 mm | NA | Group I—6 capsules of aged garlic extract (AGE) equivalent to 2.4 mL AGE/day Group II—control (low dose) 6 capsules of AGE equivalent to 0.16 mL AGE/day. Patients are evaluated after 6, 12 months | AGE suppressed colorectal adenomas after 6, 12 months | Chemo-preventive effect in humans |
McCullough M. et al. 2012 [215] | CPSII Nutrition cohort 1999–2007 | 42,824 men 56,876 women | NA | Supplementation of diet with garlic cloves < 1 clove/month; 1–3 cloves/month; 1 clove/week; 2–4 cloves/week; 5–6 cloves/week, 1 clove daily | Protective effect - women HR for 1–3 cloves/week 1.08 (0.86–1.35); 0.95 (0.72–1.26) for 1 clove/week; 0.77(0.58–1.02) for 2–4 cloves/week; 0.74 (0.48–1.13) to 5–6 cloves/week and 0.87 (0.58–1.32) for 1 clove/day | Weak chemo-preventive effect of garlic consumption for women; but not for men |
Meng S. et al. 2013 [216] | Cohort study 1984–2008 | 76,208 women 45,592 men | NA | Administration of garlic cloves < 1 clove/month; 1–3 cloves/month; 1 clove/week; 2–4 cloves/week; 5–6 cloves/week, 1 clove daily | Women HR 1–3 cloves/month 1.11 (0.94–1.31) compared to HR 1.21 (0.94–1.57) for 1 clove/day (p = 0.14) Men HR 1–3 cloves/month 0.99 (0.84–1.16) compared to HR 1.03 (0.73–1.45) for 1 clove/day (p = 0.99) | No association was found between garlic intake and CRC risk |
Satia J. A. et al. 2009 [217] | Cohort study 2000–2002 | 428 | 76,084 | Administration of garlic pills at least once a week for > 1 year during previous 10 years | HR 1.35 (0.59–1.17) compared to 1.00 (Reference) p = 0.04 | Significant increase of CRC incidence with garlic administration |
Carotenoids | ||||||
Lu M. S. et al. 2015 [218] | On-going case control study 2010–2013 | 845 | 845 | Food frequency questionnaire regarding intake of fruits and vegetables rich in carotenoids | α-carotene OR 0.54 (0.42–0.70) to 0.41 (0.31–0.54) β-carotene OR 0.79 (0.61–1.03) to 0.62 (0.48–0.82) lycopene OR 0.66 (0.51–0.85) to 0.45 (0.35–0.60) p < 0.001 | Significant inverse correlation between carotenoids intake and CRC incidence |
Leenders M. et al. 2014 [219] | Cohort study 1992–2000 | Colon cancer 898 Rectum cancer 501 | 898/501 | Food frequency questionnaire regarding intake of fruits and vegetables rich in carotenoids and vitamins | For colon cancer β-carotene OR 0.89 (0.67–1.18) to 0.69 (0.52–0.94) Vitamin C OR 0.98 (0.74–1.29) to 0.76 (0.57–1.01) Vitamin E OR 0.88 (0.67–1.16) to 0.99 (0.74–1.33) | Significant inverse correlation between CRC incidence and mainly dietary β-carotene, vitamin C intake |
Kabat G. C. et al. 2012 [220] | Large, prospective, multicenter study | 88 CRC in post-menopausal women | 5389 | Analysis of antioxidants from fasting blood samples at baseline, 1/3/6 years follow-up | For CRC β-carotene HR 0.65 (0.39–1.09) to 0.54 (0.31–0.96) For colon cancer β-carotene HR 0.57 (0.32–1.00) to 0.47 (0.25–0.88) | Significant inverse correlation between β-carotene plasma levels and CRC incidence |
Polyunsaturated Fatty Acids | ||||||
Cockbain A. J. et al., 2014 [221] | Phase II double blind randomized placebo control trial 2010–2011 | 203 patients with CRC liver metastasis | NA | 1.Placebo—43 patients 2. Patients receiving 2 g/day of EPA for 30 days prior to surgery, follow-up 18 months after surgery | Significant higher content of EPA in tumor tissues 1.82% compared to 1.30% (for placebo) p = 0.0008, decreased PGE2 in tumor tissues, anti-angiogenic activity (p = 0.075) | Pre-operative treatment has shown provide post-operative benefit |
Song M. et al. 2014 [222] | Study cohort 1984–2008 | 76,386 women 47,143 men | NA | Administration of fish 15–40 g/day (women) and 16–46 g/day (men), marine fish (0.15–0.30 g/day) | Significant risk of distal colon cancer for both fish intake HR 1.12 (0.85–1.48) to 1.36 (1–1.85) and marine fish HR 1.19 (0.89–1.58) to 1.36 (1.03–1.80) p ≤ 0.05 | Associated risk between marine fish intake and CRC risk |
Sasazuki S. at al. 2011 [223] | Prospective study 1995–2006 | 827,833 subjects | NA | Food frequency questioners regarding fish intake; marine fish 0.49–2.18 g/day for men and women | Significant Decrease associated with marine fish intake only for men RR 0.97 (0.51–1.83) to 0.35 (0.14–0.88) p = 0.05 | Chemo-preventive effect of marine fish rich in omega-3 fatty acids |
Mocellin M. C. et al. 2013 [224] | Prospective randomized controlled trial 2011–2012 | 57 patients with CRC undergoing, chemotherapy, only 11 are randomized | NA | 1. Control group (n = 5). 2. Supplemented group (n = 6) with 2g fish oil/day—9 weeks 2 g fish oil = 360 mg/day EPA, 240 mg/day DHA | Significant decrease of C-reactive protein from 18.14 mg/L to 1.14 mg/L (p = 0.04) Significant increase of EPA, DHA compared to control group (p = 0.014, p = 0.019), significant decrease of AA between baseline and 9 weeks follow-up for the supplemented group (p = 0.028) | Significant anti-inflammatory effects for patients undergoing chemotheraphy and increase for plasma fatty acid profile |
Mocellin M. C. et al. 2016 [225] | Meta-analysis of Nine trials | 475 patients with CRC | NA | Supplementation of diet with omega-3 fatty acids or administration of 0.2 g/kg fish oil parenterally at post-operative period Patients undergoing chemotherapy supplementation with 0.6 g/day EPA+DHA -9 weeks | Significant decrease of IL-6 (p = 0.024) and increase of albumin (p = 0.014) Supplementation of EPA+ DHA during chemotherapy significantly reduced CRP concentration (p = 0.017) and CRP/albumin ratio (p = 0.016) | Use of omega-3 fatty acids have benefits, especially for inflammatory markers in CRC patients |
Sorensen L. S. et al. 2014 [226] | Randomized double blind placebo controlled trial | 148 patients awaiting for CRC surgery | NA | 1. Control group 2. Supplemen-tation group with 2 g EPA + 2 g DHA for 7 days before and 7 days after surgery | Pre-operative treatment with omega-3 fatty acids determined a significant increase of EPA, DHA levels in granulocytes and a significant decrease of AA (p < 0.001) compared to control group | Potential immune-stimulatory effects and prevention of post-operative infections |
Ma C. J. et al. 2015 [227] | Prospective randomized double-blind study 2009–2010 | 99 patients with gastric and CRC | NA | 1. Control group 2. Supplementation group with a lipid emulsion containing soybean oil (80–100 g/L), medium chain triglycerides (100 g/L) and PUFA (linoleic acid—38–58 g/L, α-linolenic acid—4–11 g/L) for 7 days after surgery | There are no significant differences regarding inflammatory markers between the control and the supplementation group. Significant positive effect on lipid markers (p < 0.05) | Improvements only in lipid metabolism |
Dietary Fiber | ||||||
Holscher H. D. et al. 2015 [228] | Prospective Randomized double-blind placebo 3-period controlled study | 30 heathy patients | NA | 1. Placebo group 2. Administration of 5 g or 7.5 g inulin for 21 days with 7 days wash-out between periods | Significant increase of Bifidobacterium sp. (p < 0.001), significant decrease of Ruminococcus sp. and Desulfovibrio sp. (p < 0.01); dietary intake was positively associated with fecal butyrate (p = 0.005) | Beneficial changes in gastro-intestinal microbiota are correlated with decreased CRC incidence |
Limburg P et al, 2011 [229] | Randomized phase II clinical trial 2006–2008 | 85 patients with aberrant crypt foci ≥ 5 at baseline | NA | 1. Control group 2. Atorvastatin 20 mg/day 3. Sulindac 150 mg x 2/day 4. Oligo-fructose enriched inulin 6 g powder x 2/day for 6 months | All treatment didn’t provide a significant decrease in AFC number and size | No association was found between inulin intake and CRC |
Mehta RS et al, 2018 [230] | Prospective cohort study 1980–2012 | 121,700 females 51,529 males | NA | Food frequency questionnaires regarding dietary fiber intake | High intake of fiber was associated with a low risk of Fusobacterium nucleatum positive CRCs HR 0.54 (0.33–0.89) to 0.40 (0.24–0.67) | Intestinal microbiota plays an important role in mediating the association between consumption of high amount of dietary fiber/whole grains and CRC incidence |
Ben Q et al, 2014 [231] | Meta-analysis of 20 studies (case-control, cohort) | 10,984 patients with colorectal adenoma | NA | Administration of 10 g/day fibers | SRR for dietary fiber are 0.72 (0.63–0.83) in a high vs low intake, inverse association between total fiber intake and CRC risk SSR 0.66 (0.56–0.77) | Chemopreventive effect of dietary fiber |
Hansen L et al, 2012 [232] | Cohort study, 1997–2008 | 108,081 patients | NA | Administration of fiber 16–28 g/day for men and 15–24 g for women | Significant inverse correlation between CRC incidence and dietary fiber intake for men IRR 0.93 (0.68–1.26) to 0.55 (0.38–0.79) | Chemopreventive effect of dietary fiber |
Kunzman A et al, 2015 [233] | Cohort study 1993–2009 | 2036 patients | 15,976 | Administration of fiber 9.9–12.8 g/1000 kcal/day from fruits/vegetables | Significant inverse correlation between dietary fiber intake and distal colon or rectal adenoma in men OR 0.88 (0.75–1.04) to 0.76 (0.63–0.91) p = 0.003 | Chemopreventive effect of dietary fiber against CRC |
Murphy N et al, 2012 [234] | On-going multicentre prospective cohort study 1992–2000 | 477,312 patients | NA | Administration of dietary fiber 16.4–28.5 g/day | Significant inverse correlation between dietary intake and colon-distal cancer HR 0.90(0.75–1.07) to 0.70 (0.53–0.92) p = 0.021 colon proximal cancer HR 0.93 (0.78–1.1) to 0.86 (0.69–1.07) p = 0.16 rectum cancer HR 1 (0.87–1.17) to 0.79 (0.65–0.96) p = 0.012 | Chemopreventive effect of dietary fiber against CRC |
Mathers JC et al, 2012 [235] | Randomized control trial | 937 eligible patients with Lynch syndrome | NA | 1. 463 patients received 30 g resistant starch/day 2. 455 patients—resistant starch placebo 3. 19 patients 600 mg aspirin/day—29 months | No significant effect of resistant-starch administration on cancer development IRR resistant starch vs resistant starch placebo 1.15 (0.66–2.00) p = 0.61 | No detectable effect on cancer development |
Compound of Interest | Source | Bioavailability | In Vivo Studies | Ref. |
---|---|---|---|---|
Curcumin | Turmeric | - poor absorption, rapid metabolism, rapid elimination - enhanced by piperine with 2000% - better results on animal experiments | - 2g/kg of curcumin in rats → Cmax = 1.35 ± 0.23 μg/mL in 0.83 h - 2 g/kg of curcumin in human subjects → Cmax = 0.006 ± 0.005 μg/mL | [120,248] |
EGCG | Green tea | - poor absorption - alkaloids, vitamins, proteins and fish oil improve absorption - air contact oxidation, metal ions like Ca2+ and Mg2+ and milk reduce absorption | - one oral dose of EGCG half-time = 3.4 ± 0.3 h | [249] |
Resveratrol | Grapes | - poor absorption - bioavailability increased by a liquid micellar formulation | - 500 mg of Vineatrol → Cmax of trans-resveratrol = 10.6 fold higher - no detection of trans-ε-viniferin in plasma or urine | [250] |
Quercetin | Onion Apples Beans Broccoli | - better bioavailability of quercetin glucoside | - 100 mg quercetin → absorption of quercetin glucoside = 3–17% | [251] |
Genistein | Soy | - lower bioavailability in vivo - total genistein—a better bioavailability than genistein aglycone | - 20 mg/kg of genistein in FVB mice → genistein aglycone bioavailability = 23.4% - soy protein feeding Balb/c mice females → bioavailability of total genistein = 90% → bioavailability of genistein aglycone = < 15% | [252] |
Anthocyanins | Bilberries | - poor bioavailability - 30% of amthocyanins are stable in the upper intestine for 8 h. | - bioavailability of anthocyanins from bilberries → ↑ amount of anthocyanins and degradants in the heathy compared to ileostomists group | [253] |
Proantho-cyanidin | Apples Grapes Green tea | - oligomeric flavonoids with limited bioavailability | - ad libitum diet of grape seed extract in lab rats → the presence of PAC in the colonic contents - 11% of PAC—present in the feces | [254] |
Capsaicin | Chilli | - low bioavailability - capsaicin was absorbed into intestinal tissues, jejunum and serosal fluid | - 1 mM of capsaicin in rats → absorption = 50% in the stomach, 80% in the jejunum and 70% in the ileum. | [255] |
Piperine | Black pepper | - insoluble in water with a low bioavailability - used in clinical assays single or as an enhancer for other dietary agents - improved the bioavailability of resveratrol, curcumin and lycopene | - resveratrol + piperine in mice → piperine enhanced the bioavailability of resveratrol with 229% - curcumin + piperine in rats and human subjects → piperine enhanced bioavailability of curcumin with 2000% | [256,257] |
Aliicin | Garlic | - poor bioavailability | - administration of garlic/ pure allicin → no detection in urine or blood | [258] |
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Costea, T.; Hudiță, A.; Ciolac, O.-A.; Gălățeanu, B.; Ginghină, O.; Costache, M.; Ganea, C.; Mocanu, M.-M. Chemoprevention of Colorectal Cancer by Dietary Compounds. Int. J. Mol. Sci. 2018, 19, 3787. https://doi.org/10.3390/ijms19123787
Costea T, Hudiță A, Ciolac O-A, Gălățeanu B, Ginghină O, Costache M, Ganea C, Mocanu M-M. Chemoprevention of Colorectal Cancer by Dietary Compounds. International Journal of Molecular Sciences. 2018; 19(12):3787. https://doi.org/10.3390/ijms19123787
Chicago/Turabian StyleCostea, Teodora, Ariana Hudiță, Oana-Alina Ciolac, Bianca Gălățeanu, Octav Ginghină, Marieta Costache, Constanța Ganea, and Maria-Magdalena Mocanu. 2018. "Chemoprevention of Colorectal Cancer by Dietary Compounds" International Journal of Molecular Sciences 19, no. 12: 3787. https://doi.org/10.3390/ijms19123787