343
Views
20
CrossRef citations to date
0
Altmetric
Original Articles

Lycopene Consumption and Risk of Colorectal Cancer: A Meta-Analysis of Observational Studies

, , , &
Pages 1083-1096 | Received 09 May 2015, Accepted 03 Jun 2016, Published online: 29 Jul 2016

References

  • Smolinska K and Paluszkiewicz P: Risk of colorectal cancer in relation to frequency and total amount of red meat consumption. Systematic review and meta-analysis. Arch Med Sci 6(4), 605–610, 2010.
  • Geelen A, Schouten JM, Kamphuis C, Stam BE, Burema J, et al.: Fish consumption, n-3 fatty acids, and colorectal cancer: a meta-analysis of prospective cohort studies. Am J Epidemiol 166(10), 1116–1125, 2007.
  • Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, et al.: Cancer statistics, 2005. CA Cancer J Clin 55(1), 10–30, 2005.
  • Tuzcu M, Aslan A, Tuzcu Z, Yabas M, Bahcecioglu IH, et al.: Tomato powder impedes the development of azoxymethane-induced colorectal cancer in rats through suppression of COX-2 expression via NF-kappaB and regulating Nrf2/HO-1 pathway. Mol Nutr Food Res 56(9), 1477–1481, 2012.
  • Cho E, Smith-Warner SA, Spiegelman D, Beeson WL, van den Brandt PA, et al.: Dairy foods, calcium, and colorectal cancer: a pooled analysis of 10 cohort studies. J Natl Cancer Inst 96(13), 1015–1022, 2004.
  • Norat T and Riboli E: Dairy products and colorectal cancer. A review of possible mechanisms and epidemiological evidence. Eur J Clin Nutr 57(1), 1–17, 2003.
  • Kinzler KW and Vogelstein B: Lessons from hereditary colorectal cancer. Cell 87(2), 159–170, 1996.
  • Slattery ML, Benson J, Curtin K, Ma KN, Schaeffer D, and Potter JD: Carotenoids and colon cancer. Am J Clin Nutr 71(2), 575–582, 2000.
  • Giovannucci E, Stampfer MJ, Colditz G, Rimm EB, and Willett WC: Relationship of diet to risk of colorectal adenoma in men. J Natl Cancer Inst 84(2), 91–98, 1992.
  • de Kok TM, de Waard P, Wilms LC, and van Breda SG: Antioxidative and antigenotoxic properties of vegetables and dietary phytochemicals: the value of genomics biomarkers in molecular epidemiology. Mol Nutr Food Res 54(2), 208–217, 2010.
  • Bao B, Azmi AS, Ali S, Ahmad A, Li Y, et al.: The biological kinship of hypoxia with CSC and EMT and their relationship with deregulated expression of miRNAs and tumor aggressiveness. Biochim Biophys Acta 1826(2), 272–296, 2012.
  • Sarkar FH, Li Y, Wang Z, and Kong D: The role of nutraceuticals in the regulation of Wnt and Hedgehog signaling in cancer. Cancer Metastasis Rev 29(3), 383–394, 2010.
  • Tan HL, Thomas-Ahner JM, Grainger EM, Wan L, Francis DM, et al.: Tomato-based food products for prostate cancer prevention: what have we learned? Cancer Metastasis Rev 29(3), 553–568, 2010.
  • Agarwal S and Rao AV: Tomato lycopene and its role in human health and chronic diseases. CMAJ Canadian Med Assoc J 163(6), 739–744, 2000.
  • Dias MC, Vieiralves NF, Gomes MI, Salvadori DM, Rodrigues MA, and Barbisan LF: Effects of lycopene, synbiotic and their association on early biomarkers of rat colon carcinogenesis. Food Chem Toxicol 48(3), 772–780, 2010.
  • International symposium on the role of tomato products and carotenoids in disease prevention. April 10, 2001: Proceedings and abstracts. Exp Biol Med (Maywood) 227(10), 843–937, 2002.
  • Palozza P, Colangelo M, Simone R, Catalano A, Boninsegna A, et al.: Lycopene induces cell growth inhibition by altering mevalonate pathway and Ras signaling in cancer cell lines. Carcinogenesis 31(10), 1813–1821, 2010.
  • Giovannucci E, Rimm EB, Liu Y, Stampfer MJ, and Willett WC: A prospective study of tomato products, lycopene, and prostate cancer risk. J Natl Cancer Inst 94(5), 391–398, 2002.
  • Rao AV, Ray MR, and Rao LG: Lycopene. Adv Food Nutr Res 51, 99–164, 2006.
  • Sarkar FH, Li Y, Wang Z, and Kong D: Cellular signaling perturbation by natural products. Cell Signal 21(11), 1541–1547, 2009.
  • Giovannucci E: Tomatoes, tomato-based products, lycopene, and cancer: Review of the epidemiologic literature. J Natl Cancer Inst 91(4), 317–331, 1999.
  • Liu C and Russell RM: Nutrition and gastric cancer risk: an update. Nutr Rev 66(5), 237–249, 2008.
  • Kavanaugh CJ, Trumbo PR, and Ellwood KC: The U.S. Food and Drug Administration's evidence-based review for qualified health claims: tomatoes, lycopene, and cancer. J Natl Cancer Inst 99(14), 1074–1085, 2007.
  • Mannisto S, Yaun SS, Hunter DJ, Spiegelman D, Adami HO, et al.: Dietary carotenoids and risk of colorectal cancer in a pooled analysis of 11 cohort studies. Am J Epidemiol 165(3), 246–255, 2007.
  • La Vecchia C: Tomatoes, lycopene intake, and digestive tract and female hormone-related neoplasms. Exp Biol Med (Maywood, NJ) 227(10), 860–863, 2002.
  • Kune G and Watson L: Colorectal cancer protective effects and the dietary micronutrients folate, methionine, vitamins B6, B12, C, E, selenium, and lycopene. Nutr Cancer 56(1), 11–21, 2006.
  • Terry P, Jain M, Miller AB, Howe GR, and Rohan TE: Dietary carotenoid intake and colorectal cancer risk. Nutr Cancer 42(2), 167–172, 2002.
  • Malila N, Virtamo J, Virtanen M, Pietinen P, Albanes D, and Teppo L: Dietary and serum (alpha)-tocopherol, (beta)-carotene and retinol, and risk for colorectal cancer in male smokers. Eur J Clin Nutr 56(7), 615–621, 2002.
  • Lu MS, Fang YJ, Chen YM, Luo WP, Pan ZZ, et al.: Higher intake of carotenoid is associated with a lower risk of colorectal cancer in Chinese adults: a case-control study. Eur J Nutr 54(4), 619–628, 2014.
  • Kune G and Watson L: Lowering the risk of rectal cancer among habitual beer drinkers by dietary means. Adv Preventive Med 874048, 2011.
  • Slattery ML, Wolff RK, Herrick J, Caan BJ, and Samowitz W: Tumor markers and rectal cancer: Support for an inflammation-related pathway. Int J Cancer 125(7), 1698–1704, 2009.
  • Chaiter Y, Gruber SB, Ben-Amotz A, Almog R, Rennert HS, et al.: Smoking attenuates the negative association between carotenoids consumption and colorectal cancer risk. Cancer Causes Control CCC 20(8), 1327–1338, 2009.
  • Musa-Veloso K, Card JW, Wong AW, and Cooper DA: Influence of observational study design on the interpretation of cancer risk reduction by carotenoids. Nutr Rev 67(9), 527–545, 2009.
  • Stroup DF, Berlin JA, Morton SC, et al.: Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15), 2008–2012, 2000.
  • Stang A: Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9), 603–605, 2010.
  • Atkins D, Best D, Briss PA, Eccles M, Falck-Ytter Y, et al.: Grading quality of evidence and strength of recommendations. BMJ 328(7454), 1490, 2004.
  • Greenland S: Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9, 1–30, 1987.
  • Greenland S and Longnecker MP: Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135(11), 1301–1309, 1992.
  • Orsini N, Bellocco R, and Greenland S: Generalized least squares for trend estimation of summarized dose-response data. Stata J 6(1), 40, 2006.
  • DerSimonian R and Laird N: Meta-analysis in clinical trials. Control Clin Trials 7(3), 177188, 1986.
  • Higgins JP, Thompson SG, Deeks JJ, and Altman DG: Measuring inconsistency in meta-analyses. BMJ 327(7414), 557–560, 2003.
  • Hardy RJ and Thompson SG: Detecting and describing heterogeneity in meta-analysis. Stat Med 17(8), 841–856, 1998.
  • Peters JL, Sutton AJ, Jones DR, Abrams KR, and Rushton L: Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol 61(10), 991–996, 2008.
  • Begg CB and Mazumdar M: Operating characteristics of a rank correlation test for publication bias. Biometrics 50(4), 1088–1101, 1994.
  • Egger M, Davey Smith G, Schneider M, and Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109), 629–634, 1997.
  • Zhou JG, Tian X, Wang X, Tian JH, Wang Y, et al.: Treatment on advanced NSCLC: platinum-based chemotherapy plus erlotinib or platinum-based chemotherapy alone? A systematic review and meta-analysis of randomised controlled trials. Med Oncol 32(2), 471, 2015.
  • Enger SM, Longnecker MP, Chen MJ, Harper JM, Lee ER, et al.: Dietary intake of specific carotenoids and vitamins A, C, and E, and prevalence of colorectal adenomas. Cancer Epidemiol Biomarkers Prev 5(3), 147–153, 1996.
  • Murtaugh MA, Ma KN, Benson J, Curtin K, Caan B, and Slattery ML: Antioxidants, carotenoids, and risk of rectal cancer. Am J Epidemiol 159(1), 32–41, 2004.
  • Nkondjock A and Ghadirian P: Dietary carotenoids and risk of colon cancer: Case-control study. Int J Cancer 110(1), 110–116, 2004.
  • Ramadas A and Kandiah M: Nutritional status and the risk for colorectal adenomas: A case-control study in Hospital Kuala Lumpur, Malaysia. Pakistan J Nutr 9(3), 269–278, 2010.
  • Park SY, Nomura AM, Murphy SP, Wilkens LR, Henderson BE, and Kolonel LN: Carotenoid intake and colorectal cancer risk: The Multiethnic Cohort study. J Epidemiol 19(2), 63–71, 2009.
  • Jung S, Wu K, Giovannucci E, Spiegelman D, Willett WC, and Smith-Warner SA: Carotenoid intake and risk of colorectal adenomas in a cohort of male health professionals. Cancer Causes Control 24(4), 705–717, 2013.
  • Leslie A, Carey FA, Pratt NR, and Steele RJ: The colorectal adenoma-carcinoma sequence. Br J Surg 89(7), 845–860, 2002.
  • Lu MS, Fang YJ, Chen YM, Luo WP, Pan ZZ, et al.: Higher intake of carotenoid is associated with a lower risk of colorectal cancer in Chinese adults: a case-control study. Eur J Nutr 54(4), 619–628, 2014.
  • Chaiter Y, Gruber SB, Ben-Amotz A, Almog R, Rennert HS, et al.: Smoking attenuates the negative association between carotenoids consumption and colorectal cancer risk. Cancer Causes Control 20(8), 1327–1338, 2009.
  • Moran NE, Erdman JW, and Clinton SK: Complex interactions between dietary and genetic factors impact lycopene metabolism and distribution. Arch Biochem Biophys 539(2), 171–180, 2013.
  • Cho E, Smith-Warner SA, Ritz J, van den Brandt PA, Colditz GA, et al.: Alcohol intake and colorectal cancer: a pooled analysis of 8 cohort studies. Ann Intern Med 140(8), 603–613, 2004.
  • Olson JA and Krinsky NI: Introduction: the colorful, fascinating world of the carotenoids: important physiologic modulators. FASEB J 9(15), 1547–1550, 1995.
  • van Breemen RB and Pajkovic N: Multitargeted therapy of cancer by lycopene. Cancer Lett 269(2), 339–351, 2008.
  • Sies H and Stahl W: Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. Am J Clin Nutr 62(6 Suppl), 1315S–1321S, 1995.
  • Karas M, Amir H, Fishman D, Danilenko M, Segal S, et al.: Lycopene interferes with cell cycle progression and insulin-like growth factor I signaling in mammary cancer cells. Nutr Cancer 36(1), 101–111, 2000.
  • Kanagaraj P, Vijayababu MR, Ravisankar B, Anbalagan J, Aruldhas MM, and Arunakaran J: Effect of lycopene on insulin-like growth factor-I, IGF binding protein-3 and IGF type-I receptor in prostate cancer cells. J Cancer Res Clin Oncol 133(6), 351–359, 2007.
  • Ma J, Giovannucci E, Pollak M, and Stampfer M: RESPONSE: Re: Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (IGF)-I and IGF-binding protein-3. J Natl Cancer Inst 91(23), 2052, 1999.
  • Walfisch S, Walfisch Y, Kirilov E, Linde N, Mnitentag H, et al.: Tomato lycopene extract supplementation decreases insulin-like growth factor-I levels in colon cancer patients. Eur J Cancer Prev 16(4), 298–303, 2007.
  • Vrieling A, Voskuil DW, Bonfrer JM, et al.: Lycopene supplementation elevates circulating insulin-like growth factor binding protein-1 and -2 concentrations in persons at greater risk of colorectal cancer. Am J Clin Nutr 86(5), 1456–1462, 2007.
  • Walther A, Johnstone E, Swanton C, Midgley R, Tomlinson I, and Kerr D: Genetic prognostic and predictive markers in colorectal cancer. Nat Rev Cancer 9(7), 489–499.
  • Winder T and Lenz HJ: Molecular predictive and prognostic markers in colon cancer. Cancer Treat Rev 36(7), 550–556, 2010.
  • Bommareddy A, Eggleston W, Prelewicz S, Antal A, Witczak Z, et al.: Chemoprevention of prostate cancer by major dietary phytochemicals. Anticancer Res 33(10), 4163–4174, 2013.
  • Tang FY, Cho HJ, Pai MH, and Chen YH: Concomitant supplementation of lycopene and eicosapentaenoic acid inhibits the proliferation of human colon cancer cells. J Nutr Biochem 20(6), 426–434, 2009.
  • Gouranton E, Thabuis C, Riollet C, Malezet-Desmoulins C, El Yazidi C, et al.: Lycopene inhibits proinflammatory cytokine and chemokine expression in adipose tissue. J Nutr Biochem 22(7), 642–648, 2011.
  • Feng D, Ling WH, and Duan RD: Lycopene suppresses LPS-induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-kappaB in macrophages. Inflam Res 59(2), 115–121, 2010.
  • Tominaga K, Higuchi K, Sasaki E, Suto R, Watanabe T, et al.: Correlation of MAP kinases with COX-2 induction differs between MKN45 and HT29 cells. Aliment Pharmacol Therap 20(Suppl 1), 143–150, 2004.
  • Soslow RA, Dannenberg AJ, Rush D, Woerner BM, Khan KN, et al.: COX-2 is expressed in human pulmonary, colonic, and mammary tumors. Cancer 89(12), 2637–2645, 2000.
  • Conacci-Sorrell M, Simcha I, Ben-Yedidia T, Blechman J, Savagner P, and Ben-Ze'ev A: Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, Slug, and MAPK. J Cell Biol 163(4), 847–857, 2003.
  • Tang FY, Pai MH, and Wang XD: Consumption of lycopene inhibits the growth and progression of colon cancer in a mouse xenograft model. J Agric Food Chem 59(16), 9011–9021, 2011.
  • Ogata Y, Miura K, Ohkita A, Nagase H, and Shirouzu K: Imbalance between matrix metalloproteinase 9 and tissue inhibitor of metalloproteinases 1 expression by tumor cells implicated in liver metastasis from colorectal carcinoma. The Kurume Med J 48(3), 211–218, 2001.
  • Hwang ES and Lee HJ: Inhibitory effects of lycopene on the adhesion, invasion, and migration of SK-Hep1 human hepatoma cells. Exp Biol Med (Maywood, NJ) 231(3), 322–327, 2006.
  • Lin MC, Wang FY, Kuo YH, and Tang FY: Cancer chemopreventive effects of lycopene: suppression of MMP-7 expression and cell invasion in human colon cancer cells. J Agric Food Chem 59(20), 11304–11318, 2011.
  • Park YO, Hwang ES, and Moon TW: The effect of lycopene on cell growth and oxidative DNA damage of Hep3B human hepatoma cells. BioFactors (Oxford, England) 23(3), 129–139, 2005.
  • Nahum A, Zeller L, Danilenko M, Prall OW, Watts CK, et al.: Lycopene inhibition of IGF-induced cancer cell growth depends on the level of cyclin D1. Eur J Nutr 45(5), 275–282, 2006.
  • Ivanov NI, Cowell SP, Brown P, Rennie PS, Guns ES, and Cox ME: Lycopene differentially induces quiescence and apoptosis in androgen-responsive and -independent prostate cancer cell lines. Clin Nutr (Edinburgh, Scotland) 26(2), 252–263, 2007.
  • Palozza P, Serini S, Boninsegna A, Bellovino D, Lucarini M, et al.: The growth-inhibitory effects of tomatoes digested in vitro in colon adenocarcinoma cells occur through down regulation of cyclin D1, Bcl-2 and Bcl-xL. Br J Nutr 98(4), 789–795, 2007.
  • Ferreira AL, Yeum KJ, Liu C, Smith D, Krinsky NI, et al.: Tissue distribution of lycopene in ferrets and rats after lycopene supplementation. J Nutr 130(5), 1256–1260, 2000.
  • Parker RS: Carotenoids in human blood and tissues. J Nutr 119(1), 101–104, 1989.
  • Muhlhofer A, Buhler-Ritter B, Frank J, Zoller WG, Merkle P, et al.: Carotenoids are decreased in biopsies from colorectal adenomas. Clin Nutr 22(1), 65–70, 2003.
  • Gartner C, Stahl W, and Sies H: Lycopene is more bioavailable from tomato paste than from fresh tomatoes. Am J Clin Nutr 66(1), 116–122, 1997.
  • Stahl W and Sies H: Uptake of lycopene and its geometrical isomers is greater from heat-processed than from unprocessed tomato juice in humans. J Nutr 122(11), 2161–2166, 1992.
  • Boileau TW, Boileau AC, and Erdman JW Jr.: Bioavailability of all-trans and cis-isomers of lycopene. Exp Biol Med 227(10), 914–949, 2002.
  • Boileau AC, Merchen NR, Wasson K, Atkinson CA, and Erdman JW Jr.: Cis-lycopene is more bioavailable than trans-lycopene in vitro and in vivo in lymph-cannulated ferrets. J Nutr 129(6), 1176–1181, 1999.
  • Agarwal A, Shen H, Agarwal S, and Rao AV: Lycopene content of tomato products: its stability, bioavailability and in vivo antioxidant properties. J Med Food 4(1), 9–15, 2001.
  • Davis CD, Swanson CA, Ziegler RG, Clevidence B, Dwyer JT, et al.: Promises and perils of lycopene/tomato supplementation and cancer prevention: Executive summary report. J Nutr 135(8), 2014S–2029S, 2005.
  • Agarwal S and Rao AV: Tomato lycopene and its role in human health and chronic diseases. Can Med Assoc J 163(6), 739–744, 2000.
  • Mangels AR, Holden JM, Beecher GR, Forman MR, and Lanza E: Carotenoid content of fruits and vegetables: an evaluation of analytic data. J Am Diet Assoc 93(3), 284–296, 1993.
  • Bohm V, Frohlich K, and Bitsch R: Rosehip—a “new” source of lycopene? Mol Aspects Med 24(6), 385–389, 2003.
  • Palozza P, Bellovino D, Simone R, Boninsegna A, Cellini F, et al.: Effect of (beta)-carotene-rich tomato lycopene (beta)-cyclase (tlcy-b) on cell growth inhibition in HT-29 colon adenocarcinoma cells. Br J Nutr 102(2), 207–214, 2009.
  • Canene-Adams K, Campbell JK, Zaripheh S, Jeffery EH, and Erdman JW Jr.: The tomato as a functional food. J Nutr 135(5), 1226–1230, 2005.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.