Advances in Nutrition and Cancer 2 pp 159-168

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 472)

Brassica Vegetables and Cancer Prevention

Epidemiology and Mechanisms
  • Geert van Poppel
  • Dorette T. H. Verhoeven
  • Hans Verhagen
  • R. Alexandra Goldbohm

Abstract

This paper first gives an overview of the epidemiological data concerning the cancer-preventive effect of brassica vegetables, including cabbages, kale, broccoli, Brussels sprouts, and cauliflower. A protective effect of brassicas against cancer may be plausible due to their relatively high content of glucosinolates. Certain hydrolysis products of glucosinolates have shown anticarcinogenic properties. The results of six cohort studies and 74 case-control studies on the association between brassica consumption and cancer risk are summarized. The cohort studies showed inverse associations between the consumption of brassica’s and risk of lung cancer, stomach cancer, all cancers taken together. Of the case-control studies 64% showed an inverse association between consumption of one or more brassica vegetables and risk of cancer at various sites. Although the measured effects might have been distorted by various types of bias, it is concluded that a high consumption of brassica vegetables is associated with a decreased risk of cancer. This association appears to be most consistent for lung, stomach, colon and rectal cancer, and least consistent for prostatic, endometrial and ovarian cancer. It is not yet possible to resolve whether associations are to be attributed to brassica vegetables per se or to vegetables in general. Further epidemiological research should separate the anticarcinogenic effect of brassica vegetables from the effect of vegetables in general.

The mechanisms by which brassica vegetables might decrease the risk of cancer are reviewed in the second part of this paper. Brassicas, including all types of cabbages, broccoli, cauliflower, and Brussels sprouts, may be protective against cancer due to their glucosinolate content. Glucosinolates are usually broken down through hydrolysis catalysed by myrosinase, an enzyme that is released from damaged plant cells. Some of the hydrolysis products, viz. indoles, and isothiocyanates, are able to influence phase 1 and phase 2 biotransformation enzyme activities, thereby possibly influencing several processes related to chemical carcinogenesis, e.g. the metabolism, DNA-binding, and mutagenic activity of promutagens. Most evidence concerning anticarcinogenic effects of glucosinolate hydrolysis products and brassica vegetables has come from studies in animals. In addition, studies carried out in humans using high but still realistic human consumption levels of indoles and brassica vegetables have shown putative positive effects on health. The combination of epidemiological and experimental data provide suggestive evidence for a cancer preventive effect of a high intake of brassica vegetables.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    G. Block, B. Patterson, and A. Subar. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer, 18 (1992) 1–29.PubMedCrossRefGoogle Scholar
  2. 2.
    K.A. Steinmetz and J.D. Potter. Vegetables, fruit, and cancer. I. Epidemiology. Cancer Causes Contr., 2 (1991) 325–357.CrossRefGoogle Scholar
  3. 3.
    G.R. Fenwick, R.K. Heany, and W.J. Mullin. Glucosinolates and their breakdown products in food and food plants. CRC Crit. Rev. Food Sci. Nutr., 18 (1983) 123–201.Google Scholar
  4. 4.
    Y. Zhang and P. Talalay. Anticarcinogenic activities of organic isothiocyanates: chemistry and mechanisms. Cancer Res., 54 (1994) 1976s - 1981s.PubMedGoogle Scholar
  5. 5.
    C.W. Boone, G.J. Kelloff, and W.E. Malone. Identification of candidate cancer chemopreventive agents and their evaluation in animal models and human clinical trials: a review. Cancer Res., 50 (1990) 2–9.PubMedGoogle Scholar
  6. 6.
    R. McDanell and A.E.M. McLean. Chemical and biological properties of indole glucosinolates (glucobrassicins): a review. Food Chem. Toxicol., 26 (1988) 59–70.CrossRefGoogle Scholar
  7. 7.
    M.A. Morse, K.I. Eklind, S.S. Hecht, and F.-L. Chung. Inhibition of tobacco-specific nitrosamine 4-(Nnitrosomethylamino)-1-(3-pyridyl)-1-butanone (NNK) tumorigenesis with aromatic isothiocyanates. IARC Sci. Pub1., 105 (1991) 529–534.Google Scholar
  8. 8.
    S. Sugie, A. Okumura, T. Tanaka, and H. Mori. Inhibitory effects of benzyl isothiocyanate and benzyl thiocyanate on diethylnitrosamine-induced hepatocarcinogenesis in rats. Jpn. J. Cancer Res., 84 (1993) 865–870.PubMedCrossRefGoogle Scholar
  9. 9.
    R.H. Dashwood, D.N. Arbogast, A.T. Fong, C. Pereira, J.D. Hendricks, and G.S. Bailey. Quantitative inter-relationships between aflatoxin B1 carcinogen dose, indole-3-carbinol anti-carcinogen dose, target organ DNA adduction and final tumor response. Carcinogenesis, 10 (1989) 175–181.PubMedCrossRefGoogle Scholar
  10. 10.
    T. Tanaka, Y. Mori, Y. Morishita, A. Hara, T. Ohno, T. Kojima, and H. Mori. Inhibitory effect of sinigrin and indole-3-carbinol on diethylnitrosamine-induced hepatocarcinogenesis in male ACl/N rats. Carcinogenesis, 11 (1990) 1403–1406.PubMedCrossRefGoogle Scholar
  11. 11.
    D.T.H. Verhoeven, R.A. Goldbohm, G. van Poppel, H. Verhagen, and P.A. van den Brandt. Review: Epidemiological studies on brassica vegetables and cancer risk. Cancer Epidemiology, Biomarkers and Prevention 5 (1996) 733–748.Google Scholar
  12. 12.
    K.A. Steinmetz and J.D. Potter. Vegetables, fruit, and cancer. II. Mechanisms. Cancer Causes Contr., 2 (1991) 427–442.CrossRefGoogle Scholar
  13. 13.
    C.C. Harris. Chemical and physical carcinogenesis: advances and perspectives for the 1990s, Cancer Res., 51 (1991) 5023s - 5044s.PubMedGoogle Scholar
  14. 14.
    S. de Flora, A. Izzotti, and C. Bennicelli. Mechanisms of antimutagenesis and anticarcinogenesis: role in primary prevention. In: G. Bronzetti, H. Hayatsu, S. de Flora, M.D. Waters, and D.M. Shankel (Eds.), Antimutagenesis and anticarcinogenesis mechanisms III, Plenum Press, New York, 1993, pp. 1–16.CrossRefGoogle Scholar
  15. 15.
    W.B. Jakoby. Enzymatic basis of detoxification, Vol I and II, Academic press, London, 1980.Google Scholar
  16. 16.
    Nordic Council of Ministers, Naturally occurring antitumourigens. II Organic isothiocyanates, Temallord, Copenhagen, 1994.Google Scholar
  17. 17.
    D.T.H. Verhoeven, H. Verhagen, R.A. Goldbohm, P.A. van den Brandt, and G. van Poppel. A review of mechanisms underlying anticarcinogenicity by brassica vegetables. Chem-Biol. Interactions 103 (1997) 79–129.CrossRefGoogle Scholar
  18. 18.
    W.M.F. Jongen, R.J. Topp, P.J. van Bladeren, J. Lapre, K.J.H. Wienk, and R. Leenen. Modulating effects of indoles on benzo[a]pyrene-induced sister chromatid exchanges and the balance between drug-metabolizing enzymes, Toxic. in Vitro, 3 (1989) 207–213.CrossRefGoogle Scholar
  19. 19.
    J.J. Michnovicz and H.L. Bradlow. Induction of estradiol metabolism by dietary indole-3-carbinol in humans, J. Natl Cancer Inst., 82 (1990) 947–949.PubMedCrossRefGoogle Scholar
  20. 20.
    J.J. Michnovicz and H.L. Bradlow. Altered estrogen metabolism and excretion in humans following consumption of indole-3-carbinol, Nutr. Cancer, 16 (1991) 59–66.Google Scholar
  21. 21.
    H.L. Bradlow, J.J. Michnovicz, M. Halper, D.G. Miller, G.Y.C. Wong, and M.P. Osborne. Long-term responses of women to indole-3-carbinol or a high fiber diet, Cancer Epidemiol., Biomarkers & Prev., 3 (1994) 591–595.Google Scholar
  22. 22.
    H. Verhagen, H.E. Poulsen, S. Loft, G. van Poppel, M.I. Willems, and P.J. van Bladeren. Reduction of oxidative DNA-damage in humans by Brussels sprouts, Carcinogenesis, 16 (1995) 969–970.PubMedCrossRefGoogle Scholar
  23. 23.
    J.J. Bogaards, H. Verhagen, M.I. Willems, G. van Poppel, and P.J. van Bladeren. Consumption of Brussels sprouts results in elevated a-class glutathione S-transferase levels in human blood plasma, Carcinogenesis, 15 (1994) 1073–1075.PubMedCrossRefGoogle Scholar
  24. 24.
    E.J. Pantuck, C.B. Pantuck, W.A. Garland, B.H. Min, L.W. Wattenberg, K.E. Anderson, A. Kappas, and A.H. Conney. Stimulatory effect of Brussels sprouts and cabbage on human drug metabolism, Clin. Pharmacol. Ther., 25 (1979) 88–95.Google Scholar
  25. 25.
    W.A. Nijhoff, T.P.J. Mulder, H. Verhagen, G. van Poppel, and W.H.M. Peters. Effects of consumption of Brussels sprouts on plasma and urinary glutathione S-transferase class a-and -n in humans, Carcinogenesis, 16 (1995) 955–958.PubMedCrossRefGoogle Scholar
  26. 26.
    W.A. Nijhoff, F.M. Nagengast, M.J.A.L. Grubben, J.B.M.J. Jansen, H. Verhagen, G. van Poppel, and W.H.M. Peters. Effects of consumption of Brussels sprouts on intestinal and lymphocytic glutathione and glutathione S-transferases in humans, Carcinogenesis, 16 (1995) 2125–2128.PubMedCrossRefGoogle Scholar
  27. 27.
    S. Yannai, H.L. Bradlow, J. Westin, and E.D. Richter. Consumption of cruciferous vegetables-probable protection against breast cancer, In: H. Kozlowska, J. Fornal, and Z. Zdu czyk (Eds.), Proceedings of the International Conference Euro Food Tox IV “Bioactive substances in food of plant origin”, Vol.2 “Dietary Cancer Prevention”, Centre for Agrotechnology and Veterinary Sciences, Olszytn, Poland, 1994, pp. 480–483.Google Scholar
  28. 28.
    M.A. Kall, O. Vang, and J. Clausen. Effects of dietary broccoli on human in vivo drug metabolizing enzymes: evaluation of caffeine, oestrone, and chlorzoxazone metabolism, Carcinogenesis, 17 (1996) 793–799.PubMedCrossRefGoogle Scholar
  29. 29.
    R. Mawson, R.K. Heany, Z. Zdunczyk, and H. Kozlowska. Rapeseed meal-glucosinolates and their antinutritional effects. Part 3. Animal growth and performance, Nahrung, 38 (1994) 167–177.PubMedCrossRefGoogle Scholar
  30. 30.
    R. Mawson, R.K. Heany, Z. Zdunczyk, and H. Kozlowska. Rapeseed meal-glucosinolates and their antinutritional effects. Part 4. Goitrogenicity and internal organs abnormalities in animals, Nahrung, 38 (1994) 178–191.PubMedCrossRefGoogle Scholar
  31. 31.
    L. Nugon-Baudon, S. Rabot, O. Szylit, and P. Raibaud. Glucosinolates toxicity in growing rats: interactions with the hepatic detoxification system, Xenobiotica, 20 (1990) 223–230.PubMedCrossRefGoogle Scholar
  32. 32.
    G. van Poppel, W.I. Willems, and H. Verhagen. Thyroid function after consumption of Brussels sprouts: a controlled experiment in humans, TNO Nutrition and Food Research Institute, Zeist, Netherlands, 1993.Google Scholar
  33. 33.
    M. McMillan, E.A. Spinks, and G.R. Fenwick. Preliminary observations on the effect of dietary Brussels sprouts on thyroid function, Hum. Toxicol., 5 (1986) 15–19.PubMedCrossRefGoogle Scholar
  34. 34.
    R.H. Vos and W.G.H. Blijleven. The effect of processing conditions on glucosinolates in cruceferous vegetables, Zeitschrift für Lebensmitteluntersuchung und -Forschung 187,6 (1988) 525–529.Google Scholar

Copyright information

© Springer Science+Business Media New York 1999

Authors and Affiliations

  • Geert van Poppel
    • 1
  • Dorette T. H. Verhoeven
    • 1
  • Hans Verhagen
    • 1
  • R. Alexandra Goldbohm
    • 1
  1. 1.TNO Nutrition and Food Research InstituteZeistThe Netherlands

Personalised recommendations