Chemoprevention of colorectal cancer (original) (raw)
Abstract
Department of Medicine, Queen Elizabeth Hospital, Birmingham B15 2TH, UK
P BOYLE
Colorectal cancer is the fourth commonest form of cancer in men with 678 000 estimated new cases per year worldwide, representing 8.9% of all new cancers. The disease is most frequent in Occidental countries and particularly so in North America, Australia, New Zealand, and parts of Europe. Prospects for colorectal cancer control are bright and a number of possible approaches could prove fruitful. Among these, pharmaceutical measures seem to be valid and logical approaches to the prevention of colorectal cancer and diminishing its impact. Such approaches could concentrate in primary prevention in at-risk subjects or be applied in altering the course of precursor or established disease. Treatments used must fulfil basic requirements of biological plausibility and safety in continued use in large numbers of subjects. Those available include vitamins and minerals, and other drugs with potential as antioxidants, immune modulators or promoters of cell differentiation or apoptosis. Of the various regimens suggested, vitamin A supplementation may even predispose to adverse outcomes, and antioxidant vitamins in general have no coherent body of evidence to support their use. N-acetylcysteine and ursodeoxycholic acid have promising characteristics but there are as yet no clinical data to support the use of the former in gut epithelial cancer, and formal dose ranging studies must be carried out before the latter is submitted to large scale trial. Folate shows promising characteristics but non-steroidal anti-inflammatory drugs and vitamin D seem the most promising agents. Both seem to reduce the incidence of disease, and to reduce growth rates and/or induce differentiation or apoptosis in gut epithelial cancer cells. Both are also well understood pharmacologically. They may be preferred to newer selective compounds in the same class until these newer compounds are confirmed as safe for widespread long term use.
Full Text
The Full Text of this article is available as a PDF (131.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adams W. J., Morris D. L. Short-course cimetidine and survival with colorectal cancer. Lancet. 1994 Dec 24;344(8939-8940):1768–1769. [PubMed] [Google Scholar]
- Baron J. A., Sandler R. S., Haile R. W., Mandel J. S., Mott L. A., Greenberg E. R. Folate intake, alcohol consumption, cigarette smoking, and risk of colorectal adenomas. J Natl Cancer Inst. 1998 Jan 7;90(1):57–62. doi: 10.1093/jnci/90.1.57. [DOI] [PubMed] [Google Scholar]
- Belleli A., Shany S., Levy J., Guberman R., Lamprecht S. A. A protective role of 1,25-dihydroxyvitamin D3 in chemically induced rat colon carcinogenesis. Carcinogenesis. 1992 Dec;13(12):2293–2298. doi: 10.1093/carcin/13.12.2293. [DOI] [PubMed] [Google Scholar]
- Bestor T. H. Gene silencing. Methylation meets acetylation. Nature. 1998 May 28;393(6683):311–312. doi: 10.1038/30613. [DOI] [PubMed] [Google Scholar]
- Binderup L., Bramm E. Effects of a novel vitamin D analogue MC903 on cell proliferation and differentiation in vitro and on calcium metabolism in vivo. Biochem Pharmacol. 1988 Mar 1;37(5):889–895. doi: 10.1016/0006-2952(88)90177-3. [DOI] [PubMed] [Google Scholar]
- Binderup L., Latini S., Binderup E., Bretting C., Calverley M., Hansen K. 20-epi-vitamin D3 analogues: a novel class of potent regulators of cell growth and immune responses. Biochem Pharmacol. 1991 Sep 27;42(8):1569–1575. doi: 10.1016/0006-2952(91)90426-6. [DOI] [PubMed] [Google Scholar]
- Bird C. L., Swendseid M. E., Witte J. S., Shikany J. M., Hunt I. F., Frankl H. D., Lee E. R., Longnecker M. P., Haile R. W. Red cell and plasma folate, folate consumption, and the risk of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev. 1995 Oct-Nov;4(7):709–714. [PubMed] [Google Scholar]
- Bostick R. M., Potter J. D., Fosdick L., Grambsch P., Lampe J. W., Wood J. R., Louis T. A., Ganz R., Grandits G. Calcium and colorectal epithelial cell proliferation: a preliminary randomized, double-blinded, placebo-controlled clinical trial. J Natl Cancer Inst. 1993 Jan 20;85(2):132–141. doi: 10.1093/jnci/85.2.132. [DOI] [PubMed] [Google Scholar]
- Bostick R. M., Potter J. D., McKenzie D. R., Sellers T. A., Kushi L. H., Steinmetz K. A., Folsom A. R. Reduced risk of colon cancer with high intake of vitamin E: the Iowa Women's Health Study. Cancer Res. 1993 Sep 15;53(18):4230–4237. [PubMed] [Google Scholar]
- Bostick R. M., Potter J. D., Sellers T. A., McKenzie D. R., Kushi L. H., Folsom A. R. Relation of calcium, vitamin D, and dairy food intake to incidence of colon cancer among older women. The Iowa Women's Health Study. Am J Epidemiol. 1993 Jun 15;137(12):1302–1317. doi: 10.1093/oxfordjournals.aje.a116640. [DOI] [PubMed] [Google Scholar]
- Boyle P., Zaridze D. G., Smans M. Descriptive epidemiology of colorectal cancer. Int J Cancer. 1985 Jul 15;36(1):9–18. doi: 10.1002/ijc.2910360103. [DOI] [PubMed] [Google Scholar]
- Bunce C. M., Mountford J. C., French P. J., Mole D. J., Durham J., Michell R. H., Brown G. Potentiation of myeloid differentiation by anti-inflammatory agents, by steroids and by retinoic acid involves a single intracellular target, probably an enzyme of the aldoketoreductase family. Biochim Biophys Acta. 1996 May 28;1311(3):189–198. doi: 10.1016/0167-4889(96)00005-5. [DOI] [PubMed] [Google Scholar]
- Bussey H. J., DeCosse J. J., Deschner E. E., Eyers A. A., Lesser M. L., Morson B. C., Ritchie S. M., Thomson J. P., Wadsworth J. A randomized trial of ascorbic acid in polyposis coli. Cancer. 1982 Oct 1;50(7):1434–1439. doi: 10.1002/1097-0142(19821001)50:7<1434::aid-cncr2820500733>3.0.co;2-f. [DOI] [PubMed] [Google Scholar]
- Byrne P. M., Freaney R., McKenna M. J. Vitamin D supplementation in the elderly: review of safety and effectiveness of different regimes. Calcif Tissue Int. 1995 Jun;56(6):518–520. doi: 10.1007/BF00298580. [DOI] [PubMed] [Google Scholar]
- Cahill R. J., O'Sullivan K. R., Mathias P. M., Beattie S., Hamilton H., O'Morain C. Effects of vitamin antioxidant supplementation on cell kinetics of patients with adenomatous polyps. Gut. 1993 Jul;34(7):963–967. doi: 10.1136/gut.34.7.963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cali R. L., Pitsch R. M., Thorson A. G., Watson P., Tapia P., Blatchford G. J., Christensen M. A. Cumulative incidence of metachronous colorectal cancer. Dis Colon Rectum. 1993 Apr;36(4):388–393. doi: 10.1007/BF02053945. [DOI] [PubMed] [Google Scholar]
- Calle E. E., Miracle-McMahill H. L., Thun M. J., Heath C. W., Jr Estrogen replacement therapy and risk of fatal colon cancer in a prospective cohort of postmenopausal women. J Natl Cancer Inst. 1995 Apr 5;87(7):517–523. doi: 10.1093/jnci/87.7.517. [DOI] [PubMed] [Google Scholar]
- Castaigne S., Chomienne C., Daniel M. T., Ballerini P., Berger R., Fenaux P., Degos L. All-trans retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results. Blood. 1990 Nov 1;76(9):1704–1709. [PubMed] [Google Scholar]
- Clark L. C., Hixson L. J., Combs G. F., Jr, Reid M. E., Turnbull B. W., Sampliner R. E. Plasma selenium concentration predicts the prevalence of colorectal adenomatous polyps. Cancer Epidemiol Biomarkers Prev. 1993 Jan-Feb;2(1):41–46. [PubMed] [Google Scholar]
- Colin-Jones D. G., Langman M. J., Lawson D. H., Logan R. F., Paterson K. R., Vessey M. P. Postmarketing surveillance of the safety of cimetidine: 10 year mortality report. Gut. 1992 Sep;33(9):1280–1284. doi: 10.1136/gut.33.9.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cravo M. L., Mason J. B., Dayal Y., Hutchinson M., Smith D., Selhub J., Rosenberg I. H. Folate deficiency enhances the development of colonic neoplasia in dimethylhydrazine-treated rats. Cancer Res. 1992 Sep 15;52(18):5002–5006. [PubMed] [Google Scholar]
- De Flora S., Astengo M., Serra D., Bennicelli C. Inhibition of urethan-induced lung tumors in mice by dietary N-acetylcysteine. Cancer Lett. 1986 Sep;32(3):235–241. doi: 10.1016/0304-3835(86)90175-8. [DOI] [PubMed] [Google Scholar]
- DeCosse J. J., Miller H. H., Lesser M. L. Effect of wheat fiber and vitamins C and E on rectal polyps in patients with familial adenomatous polyposis. J Natl Cancer Inst. 1989 Sep 6;81(17):1290–1297. doi: 10.1093/jnci/81.17.1290. [DOI] [PubMed] [Google Scholar]
- Earnest D. L., Holubec H., Wali R. K., Jolley C. S., Bissonette M., Bhattacharyya A. K., Roy H., Khare S., Brasitus T. A. Chemoprevention of azoxymethane-induced colonic carcinogenesis by supplemental dietary ursodeoxycholic acid. Cancer Res. 1994 Oct 1;54(19):5071–5074. [PubMed] [Google Scholar]
- Eberhart C. E., Coffey R. J., Radhika A., Giardiello F. M., Ferrenbach S., DuBois R. N. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology. 1994 Oct;107(4):1183–1188. doi: 10.1016/0016-5085(94)90246-1. [DOI] [PubMed] [Google Scholar]
- Ehsanullah R. S., Page M. C., Tildesley G., Wood J. R. Prevention of gastroduodenal damage induced by non-steroidal anti-inflammatory drugs: controlled trial of ranitidine. BMJ. 1988 Oct 22;297(6655):1017–1021. doi: 10.1136/bmj.297.6655.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eisman J. A., Barkla D. H., Tutton P. J. Suppression of in vivo growth of human cancer solid tumor xenografts by 1,25-dihydroxyvitamin D3. Cancer Res. 1987 Jan 1;47(1):21–25. [PubMed] [Google Scholar]
- Elder D. J., Hague A., Hicks D. J., Paraskeva C. Differential growth inhibition by the aspirin metabolite salicylate in human colorectal tumor cell lines: enhanced apoptosis in carcinoma and in vitro-transformed adenoma relative to adenoma relative to adenoma cell lines. Cancer Res. 1996 May 15;56(10):2273–2276. [PubMed] [Google Scholar]
- Emerson J. C., Weiss N. S. Colorectal cancer and solar radiation. Cancer Causes Control. 1992 Jan;3(1):95–99. doi: 10.1007/BF00051919. [DOI] [PubMed] [Google Scholar]
- Ferraroni M., La Vecchia C., D'Avanzo B., Negri E., Franceschi S., Decarli A. Selected micronutrient intake and the risk of colorectal cancer. Br J Cancer. 1994 Dec;70(6):1150–1155. doi: 10.1038/bjc.1994.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Freston J. W., Borch K., Brand S. J., Carlsson E., Creutzfeldt W., Håkanson R., Olbe L., Solcia E., Walsh J. H., Wolfe M. M. Effects of hypochlorhydria and hypergastrinemia on structure and function of gastrointestinal cells. A review and analysis. Dig Dis Sci. 1995 Feb;40(2 Suppl):50S–62S. doi: 10.1007/BF02214871. [DOI] [PubMed] [Google Scholar]
- Freudenheim J. L., Graham S., Marshall J. R., Haughey B. P., Cholewinski S., Wilkinson G. Folate intake and carcinogenesis of the colon and rectum. Int J Epidemiol. 1991 Jun;20(2):368–374. doi: 10.1093/ije/20.2.368. [DOI] [PubMed] [Google Scholar]
- Gann P. H., Manson J. E., Glynn R. J., Buring J. E., Hennekens C. H. Low-dose aspirin and incidence of colorectal tumors in a randomized trial. J Natl Cancer Inst. 1993 Aug 4;85(15):1220–1224. doi: 10.1093/jnci/85.15.1220. [DOI] [PubMed] [Google Scholar]
- Garland C. F., Comstock G. W., Garland F. C., Helsing K. J., Shaw E. K., Gorham E. D. Serum 25-hydroxyvitamin D and colon cancer: eight-year prospective study. Lancet. 1989 Nov 18;2(8673):1176–1178. doi: 10.1016/s0140-6736(89)91789-3. [DOI] [PubMed] [Google Scholar]
- Garland C., Shekelle R. B., Barrett-Connor E., Criqui M. H., Rossof A. H., Paul O. Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men. Lancet. 1985 Feb 9;1(8424):307–309. doi: 10.1016/s0140-6736(85)91082-7. [DOI] [PubMed] [Google Scholar]
- Garland M., Morris J. S., Stampfer M. J., Colditz G. A., Spate V. L., Baskett C. K., Rosner B., Speizer F. E., Willett W. C., Hunter D. J. Prospective study of toenail selenium levels and cancer among women. J Natl Cancer Inst. 1995 Apr 5;87(7):497–505. doi: 10.1093/jnci/87.7.497. [DOI] [PubMed] [Google Scholar]
- Giardiello F. M., Hamilton S. R., Krush A. J., Piantadosi S., Hylind L. M., Celano P., Booker S. V., Robinson C. R., Offerhaus G. J. Treatment of colonic and rectal adenomas with sulindac in familial adenomatous polyposis. N Engl J Med. 1993 May 6;328(18):1313–1316. doi: 10.1056/NEJM199305063281805. [DOI] [PubMed] [Google Scholar]
- Giovannucci E., Egan K. M., Hunter D. J., Stampfer M. J., Colditz G. A., Willett W. C., Speizer F. E. Aspirin and the risk of colorectal cancer in women. N Engl J Med. 1995 Sep 7;333(10):609–614. doi: 10.1056/NEJM199509073331001. [DOI] [PubMed] [Google Scholar]
- Giovannucci E., Rimm E. B., Stampfer M. J., Colditz G. A., Ascherio A., Willett W. C. Aspirin use and the risk for colorectal cancer and adenoma in male health professionals. Ann Intern Med. 1994 Aug 15;121(4):241–246. doi: 10.7326/0003-4819-121-4-199408150-00001. [DOI] [PubMed] [Google Scholar]
- Giovannucci E., Stampfer M. J., Colditz G. A., Rimm E. B., Trichopoulos D., Rosner B. A., Speizer F. E., Willett W. C. Folate, methionine, and alcohol intake and risk of colorectal adenoma. J Natl Cancer Inst. 1993 Jun 2;85(11):875–884. doi: 10.1093/jnci/85.11.875. [DOI] [PubMed] [Google Scholar]
- Greenberg E. R., Baron J. A., Tosteson T. D., Freeman D. H., Jr, Beck G. J., Bond J. H., Colacchio T. A., Coller J. A., Frankl H. D., Haile R. W. A clinical trial of antioxidant vitamins to prevent colorectal adenoma. Polyp Prevention Study Group. N Engl J Med. 1994 Jul 21;331(3):141–147. doi: 10.1056/NEJM199407213310301. [DOI] [PubMed] [Google Scholar]
- Gustafson-Svärd C., Lilja I., Hallbök O., Sjödahl R. Cyclooxygenase-1 and cyclooxygenase-2 gene expression in human colorectal adenocarcinomas and in azoxymethane induced colonic tumours in rats. Gut. 1996 Jan;38(1):79–84. doi: 10.1136/gut.38.1.79. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hennekens C. H., Buring J. E., Manson J. E., Stampfer M., Rosner B., Cook N. R., Belanger C., LaMotte F., Gaziano J. M., Ridker P. M. Lack of effect of long-term supplementation with beta carotene on the incidence of malignant neoplasms and cardiovascular disease. N Engl J Med. 1996 May 2;334(18):1145–1149. doi: 10.1056/NEJM199605023341801. [DOI] [PubMed] [Google Scholar]
- Huang M. E., Ye Y. C., Chen S. R., Chai J. R., Lu J. X., Zhoa L., Gu L. J., Wang Z. Y. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood. 1988 Aug;72(2):567–572. [PubMed] [Google Scholar]
- Jacoby R. F., Marshall D. J., Newton M. A., Novakovic K., Tutsch K., Cole C. E., Lubet R. A., Kelloff G. J., Verma A., Moser A. R. Chemoprevention of spontaneous intestinal adenomas in the Apc Min mouse model by the nonsteroidal anti-inflammatory drug piroxicam. Cancer Res. 1996 Feb 15;56(4):710–714. [PubMed] [Google Scholar]
- Jang M., Cai L., Udeani G. O., Slowing K. V., Thomas C. F., Beecher C. W., Fong H. H., Farnsworth N. R., Kinghorn A. D., Mehta R. G. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 1997 Jan 10;275(5297):218–220. doi: 10.1126/science.275.5297.218. [DOI] [PubMed] [Google Scholar]
- Jansen J. B., Klinkenberg-Knol E. C., Meuwissen S. G., De Bruijne J. W., Festen H. P., Snel P., Lückers A. E., Biemond I., Lamers C. B. Effect of long-term treatment with omeprazole on serum gastrin and serum group A and C pepsinogens in patients with reflux esophagitis. Gastroenterology. 1990 Sep;99(3):621–628. doi: 10.1016/0016-5085(90)90946-x. [DOI] [PubMed] [Google Scholar]
- Kampman E., Giovannucci E., van 't Veer P., Rimm E., Stampfer M. J., Colditz G. A., Kok F. J., Willett W. C. Calcium, vitamin D, dairy foods, and the occurrence of colorectal adenomas among men and women in two prospective studies. Am J Epidemiol. 1994 Jan 1;139(1):16–29. doi: 10.1093/oxfordjournals.aje.a116931. [DOI] [PubMed] [Google Scholar]
- Kane K. F., Langman M. J., Williams G. R. 1,25-Dihydroxyvitamin D3 and retinoid X receptor expression in human colorectal neoplasms. Gut. 1995 Feb;36(2):255–258. doi: 10.1136/gut.36.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kane K. F., Langman M. J., Williams G. R. Antiproliferative responses to two human colon cancer cell lines to vitamin D3 are differently modified by 9-cis-retinoic acid. Cancer Res. 1996 Feb 1;56(3):623–632. [PubMed] [Google Scholar]
- Kargman S. L., O'Neill G. P., Vickers P. J., Evans J. F., Mancini J. A., Jothy S. Expression of prostaglandin G/H synthase-1 and -2 protein in human colon cancer. Cancer Res. 1995 Jun 15;55(12):2556–2559. [PubMed] [Google Scholar]
- Kelly J. P., Kaufman D. W., Jurgelon J. M., Sheehan J., Koff R. S., Shapiro S. Risk of aspirin-associated major upper-gastrointestinal bleeding with enteric-coated or buffered product. Lancet. 1996 Nov 23;348(9039):1413–1416. doi: 10.1016/S0140-6736(96)01254-8. [DOI] [PubMed] [Google Scholar]
- Kim Y. I., Salomon R. N., Graeme-Cook F., Choi S. W., Smith D. E., Dallal G. E., Mason J. B. Dietary folate protects against the development of macroscopic colonic neoplasia in a dose responsive manner in rats. Gut. 1996 Nov;39(5):732–740. doi: 10.1136/gut.39.5.732. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kumar A. Cimetidine: an immunomodulator. DICP. 1990 Mar;24(3):289–295. doi: 10.1177/106002809002400316. [DOI] [PubMed] [Google Scholar]
- Kune G. A., Kune S., Watson L. F. Colorectal cancer risk, chronic illnesses, operations, and medications: case control results from the Melbourne Colorectal Cancer Study. Cancer Res. 1988 Aug 1;48(15):4399–4404. [PubMed] [Google Scholar]
- Kuo S. M. Antiproliferative potency of structurally distinct dietary flavonoids on human colon cancer cells. Cancer Lett. 1996 Dec 20;110(1-2):41–48. doi: 10.1016/s0304-3835(96)04458-8. [DOI] [PubMed] [Google Scholar]
- Labayle D., Fischer D., Vielh P., Drouhin F., Pariente A., Bories C., Duhamel O., Trousset M., Attali P. Sulindac causes regression of rectal polyps in familial adenomatous polyposis. Gastroenterology. 1991 Sep;101(3):635–639. doi: 10.1016/0016-5085(91)90519-q. [DOI] [PubMed] [Google Scholar]
- Ladenheim J., Garcia G., Titzer D., Herzenberg H., Lavori P., Edson R., Omary M. B. Effect of sulindac on sporadic colonic polyps. Gastroenterology. 1995 Apr;108(4):1083–1087. doi: 10.1016/0016-5085(95)90206-6. [DOI] [PubMed] [Google Scholar]
- Lala P. K., Parhar R. S., Singh P. Indomethacin therapy abrogates the prostaglandin-mediated suppression of natural killer activity in tumor-bearing mice and prevents tumor metastasis. Cell Immunol. 1986 Apr 15;99(1):108–118. doi: 10.1016/0008-8749(86)90220-0. [DOI] [PubMed] [Google Scholar]
- Langman M. J., Weil J., Wainwright P., Lawson D. H., Rawlins M. D., Logan R. F., Murphy M., Vessey M. P., Colin-Jones D. G. Risks of bleeding peptic ulcer associated with individual non-steroidal anti-inflammatory drugs. Lancet. 1994 Apr 30;343(8905):1075–1078. doi: 10.1016/s0140-6736(94)90185-6. [DOI] [PubMed] [Google Scholar]
- Lashner B. A. Red blood cell folate is associated with the development of dysplasia and cancer in ulcerative colitis. J Cancer Res Clin Oncol. 1993;119(9):549–554. doi: 10.1007/BF01686465. [DOI] [PubMed] [Google Scholar]
- Lehmann J. M., Jong L., Fanjul A., Cameron J. F., Lu X. P., Haefner P., Dawson M. I., Pfahl M. Retinoids selective for retinoid X receptor response pathways. Science. 1992 Dec 18;258(5090):1944–1946. doi: 10.1126/science.1335166. [DOI] [PubMed] [Google Scholar]
- Liu T., Mokuolu A. O., Rao C. V., Reddy B. S., Holt P. R. Regional chemoprevention of carcinogen-induced tumors in rat colon. Gastroenterology. 1995 Oct;109(4):1167–1172. doi: 10.1016/0016-5085(95)90575-8. [DOI] [PubMed] [Google Scholar]
- Logan R. F., Little J., Hawtin P. G., Hardcastle J. D. Effect of aspirin and non-steroidal anti-inflammatory drugs on colorectal adenomas: case-control study of subjects participating in the Nottingham faecal occult blood screening programme. BMJ. 1993 Jul 31;307(6899):285–289. doi: 10.1136/bmj.307.6899.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Longnecker M. P., Martin-Moreno J. M., Knekt P., Nomura A. M., Schober S. E., Stähelin H. B., Wald N. J., Gey K. F., Willett W. C. Serum alpha-tocopherol concentration in relation to subsequent colorectal cancer: pooled data from five cohorts. J Natl Cancer Inst. 1992 Mar 18;84(6):430–435. doi: 10.1093/jnci/84.6.430. [DOI] [PubMed] [Google Scholar]
- Love R. R., Carbone P. P., Verma A. K., Gilmore D., Carey P., Tutsch K. D., Pomplun M., Wilding G. Randomized phase I chemoprevention dose-seeking study of alpha-difluoromethylornithine. J Natl Cancer Inst. 1993 May 5;85(9):732–737. doi: 10.1093/jnci/85.9.732. [DOI] [PubMed] [Google Scholar]
- Lu X. P., Fanjul A., Picard N., Pfahl M., Rungta D., Nared-Hood K., Carter B., Piedrafita J., Tang S., Fabbrizio E. Novel retinoid-related molecules as apoptosis inducers and effective inhibitors of human lung cancer cells in vivo. Nat Med. 1997 Jun;3(6):686–690. doi: 10.1038/nm0697-686. [DOI] [PubMed] [Google Scholar]
- Matsumoto S. Cimetidine and survival with colorectal cancer. Lancet. 1995 Jul 8;346(8967):115–115. doi: 10.1016/s0140-6736(95)92136-2. [DOI] [PubMed] [Google Scholar]
- McKeown-Eyssen G., Holloway C., Jazmaji V., Bright-See E., Dion P., Bruce W. R. A randomized trial of vitamins C and E in the prevention of recurrence of colorectal polyps. Cancer Res. 1988 Aug 15;48(16):4701–4705. [PubMed] [Google Scholar]
- Meyskens F. L., Jr, Gerner E. W. Development of difluoromethylornithine as a chemoprevention agent for the management of colon cancer. J Cell Biochem Suppl. 1995;22:126–131. doi: 10.1002/jcb.240590816. [DOI] [PubMed] [Google Scholar]
- Narisawa T., Sato M., Sano M., Takahashi T. Inhibition of development of methylnitrosourea-induced rat colonic tumors by peroral administration of indomethacin. Gan. 1982 Jun;73(3):377–381. [PubMed] [Google Scholar]
- Narisawa T., Takahashi M., Masuda T., Nagasawa O., Koyama H. [Prevention of peritoneal carcinomatosis recurrence with a prostaglandin synthesis inhibitor, indomethacin]. Gan To Kagaku Ryoho. 1987 Aug;14(8):2496–2501. [PubMed] [Google Scholar]
- Nelson R. L., Davis F. G., Sutter E., Kikendall J. W., Sobin L. H., Milner J. A., Bowen P. E. Serum selenium and colonic neoplastic risk. Dis Colon Rectum. 1995 Dec;38(12):1306–1310. doi: 10.1007/BF02049157. [DOI] [PubMed] [Google Scholar]
- Newcomb P. A., Storer B. E. Postmenopausal hormone use and risk of large-bowel cancer. J Natl Cancer Inst. 1995 Jul 19;87(14):1067–1071. doi: 10.1093/jnci/87.14.1067. [DOI] [PubMed] [Google Scholar]
- O'Dwyer P. J., Szarka C. E., Yao K. S., Halbherr T. C., Pfeiffer G. R., Green F., Gallo J. M., Brennan J., Frucht H., Goosenberg E. B. Modulation of gene expression in subjects at risk for colorectal cancer by the chemopreventive dithiolethione oltipraz. J Clin Invest. 1996 Sep 1;98(5):1210–1217. doi: 10.1172/JCI118904. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Omenn G. S., Goodman G. E., Thornquist M. D., Balmes J., Cullen M. R., Glass A., Keogh J. P., Meyskens F. L., Valanis B., Williams J. H. Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med. 1996 May 2;334(18):1150–1155. doi: 10.1056/NEJM199605023341802. [DOI] [PubMed] [Google Scholar]
- Oshima M., Dinchuk J. E., Kargman S. L., Oshima H., Hancock B., Kwong E., Trzaskos J. M., Evans J. F., Taketo M. M. Suppression of intestinal polyposis in Apc delta716 knockout mice by inhibition of cyclooxygenase 2 (COX-2). Cell. 1996 Nov 29;87(5):803–809. doi: 10.1016/s0092-8674(00)81988-1. [DOI] [PubMed] [Google Scholar]
- Paganelli G. M., Biasco G., Brandi G., Santucci R., Gizzi G., Villani V., Cianci M., Miglioli M., Barbara L. Effect of vitamin A, C, and E supplementation on rectal cell proliferation in patients with colorectal adenomas. J Natl Cancer Inst. 1992 Jan 1;84(1):47–51. doi: 10.1093/jnci/84.1.47. [DOI] [PubMed] [Google Scholar]
- Parkin D. M., Pisani P., Ferlay J. Estimates of the worldwide incidence of eighteen major cancers in 1985. Int J Cancer. 1993 Jun 19;54(4):594–606. doi: 10.1002/ijc.2910540413. [DOI] [PubMed] [Google Scholar]
- Pasricha P. J., Bedi A., O'Connor K., Rashid A., Akhtar A. J., Zahurak M. L., Piantadosi S., Hamilton S. R., Giardiello F. M. The effects of sulindac on colorectal proliferation and apoptosis in familial adenomatous polyposis. Gastroenterology. 1995 Sep;109(3):994–998. doi: 10.1016/0016-5085(95)90411-5. [DOI] [PubMed] [Google Scholar]
- Peleg I. I., Maibach H. T., Brown S. H., Wilcox C. M. Aspirin and nonsteroidal anti-inflammatory drug use and the risk of subsequent colorectal cancer. Arch Intern Med. 1994 Feb 28;154(4):394–399. [PubMed] [Google Scholar]
- Piazza G. A., Rahm A. L., Krutzsch M., Sperl G., Paranka N. S., Gross P. H., Brendel K., Burt R. W., Alberts D. S., Pamukcu R. Antineoplastic drugs sulindac sulfide and sulfone inhibit cell growth by inducing apoptosis. Cancer Res. 1995 Jul 15;55(14):3110–3116. [PubMed] [Google Scholar]
- Pisani P., Parkin D. M., Ferlay J. Estimates of the worldwide mortality from eighteen major cancers in 1985. Implications for prevention and projections of future burden. Int J Cancer. 1993 Dec 2;55(6):891–903. doi: 10.1002/ijc.2910550604. [DOI] [PubMed] [Google Scholar]
- Powell S. M., Zilz N., Beazer-Barclay Y., Bryan T. M., Hamilton S. R., Thibodeau S. N., Vogelstein B., Kinzler K. W. APC mutations occur early during colorectal tumorigenesis. Nature. 1992 Sep 17;359(6392):235–237. doi: 10.1038/359235a0. [DOI] [PubMed] [Google Scholar]
- Rao C. V., Rivenson A., Katiwalla M., Kelloff G. J., Reddy B. S. Chemopreventive effect of oltipraz during different stages of experimental colon carcinogenesis induced by azoxymethane in male F344 rats. Cancer Res. 1993 Jun 1;53(11):2502–2506. [PubMed] [Google Scholar]
- Reddy B. S., Rao C. V., Rivenson A., Kelloff G. Inhibitory effect of aspirin on azoxymethane-induced colon carcinogenesis in F344 rats. Carcinogenesis. 1993 Aug;14(8):1493–1497. doi: 10.1093/carcin/14.8.1493. [DOI] [PubMed] [Google Scholar]
- Reddy B. S., Rivenson A., El-Bayoumy K., Upadhyaya P., Pittman B., Rao C. V. Chemoprevention of colon cancer by organoselenium compounds and impact of high- or low-fat diets. J Natl Cancer Inst. 1997 Apr 2;89(7):506–512. doi: 10.1093/jnci/89.7.506. [DOI] [PubMed] [Google Scholar]
- Reshef R., Rozen P., Fireman Z., Fine N., Barzilai M., Shasha S. M., Shkolnik T. Effect of a calcium-enriched diet on the colonic epithelial hyperproliferation induced by N-methyl-N'-nitro-N-nitrosoguanidine in rats on a low calcium and fat diet. Cancer Res. 1990 Mar 15;50(6):1764–1767. [PubMed] [Google Scholar]
- Rodrigues C. M., Kren B. T., Steer C. J., Setchell K. D. The site-specific delivery of ursodeoxycholic acid to the rat colon by sulfate conjugation. Gastroenterology. 1995 Dec;109(6):1835–1844. doi: 10.1016/0016-5085(95)90750-5. [DOI] [PubMed] [Google Scholar]
- Roncucci L., Di Donato P., Carati L., Ferrari A., Perini M., Bertoni G., Bedogni G., Paris B., Svanoni F., Girola M. Antioxidant vitamins or lactulose for the prevention of the recurrence of colorectal adenomas. Colorectal Cancer Study Group of the University of Modena and the Health Care District 16. Dis Colon Rectum. 1993 Mar;36(3):227–234. doi: 10.1007/BF02053502. [DOI] [PubMed] [Google Scholar]
- Rosenberg L., Palmer J. R., Zauber A. G., Warshauer M. E., Stolley P. D., Shapiro S. A hypothesis: nonsteroidal anti-inflammatory drugs reduce the incidence of large-bowel cancer. J Natl Cancer Inst. 1991 Mar 6;83(5):355–358. doi: 10.1093/jnci/83.5.355. [DOI] [PubMed] [Google Scholar]
- Schultz R. M., Altom M. G. Potentiation of nonspecific immunotherapy of experimental lung metastases by indomethacin. J Immunopharmacol. 1983;5(4):277–290. doi: 10.3109/08923978309026449. [DOI] [PubMed] [Google Scholar]
- Shiff S. J., Qiao L., Tsai L. L., Rigas B. Sulindac sulfide, an aspirin-like compound, inhibits proliferation, causes cell cycle quiescence, and induces apoptosis in HT-29 colon adenocarcinoma cells. J Clin Invest. 1995 Jul;96(1):491–503. doi: 10.1172/JCI118060. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silverstein F. E., Graham D. Y., Senior J. R., Davies H. W., Struthers B. J., Bittman R. M., Geis G. S. Misoprostol reduces serious gastrointestinal complications in patients with rheumatoid arthritis receiving nonsteroidal anti-inflammatory drugs. A randomized, double-blind, placebo-controlled trial. Ann Intern Med. 1995 Aug 15;123(4):241–249. doi: 10.7326/0003-4819-123-4-199508150-00001. [DOI] [PubMed] [Google Scholar]
- Singh J., Kulkarni N., Kelloff G., Reddy B. S. Modulation of azoxymethane-induced mutational activation of ras protooncogenes by chemopreventive agents in colon carcinogenesis. Carcinogenesis. 1994 Jul;15(7):1317–1323. doi: 10.1093/carcin/15.7.1317. [DOI] [PubMed] [Google Scholar]
- Singh S., Sheppard M. C., Langman M. J. Sex differences in the incidence of colorectal cancer: an exploration of oestrogen and progesterone receptors. Gut. 1993 May;34(5):611–615. doi: 10.1136/gut.34.5.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sitrin M. D., Halline A. G., Abrahams C., Brasitus T. A. Dietary calcium and vitamin D modulate 1,2-dimethylhydrazine-induced colonic carcinogenesis in the rat. Cancer Res. 1991 Oct 15;51(20):5608–5613. [PubMed] [Google Scholar]
- Slater S. J., Kelly M. B., Taddeo F. J., Larkin J. D., Yeager M. D., McLane J. A., Ho C., Stubbs C. D. Direct activation of protein kinase C by 1 alpha,25-dihydroxyvitamin D3. J Biol Chem. 1995 Mar 24;270(12):6639–6643. doi: 10.1074/jbc.270.12.6639. [DOI] [PubMed] [Google Scholar]
- Taha A. S., Hudson N., Hawkey C. J., Swannell A. J., Trye P. N., Cottrell J., Mann S. G., Simon T. J., Sturrock R. D., Russell R. I. Famotidine for the prevention of gastric and duodenal ulcers caused by nonsteroidal antiinflammatory drugs. N Engl J Med. 1996 May 30;334(22):1435–1439. doi: 10.1056/NEJM199605303342204. [DOI] [PubMed] [Google Scholar]
- Tsujii M., DuBois R. N. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell. 1995 Nov 3;83(3):493–501. doi: 10.1016/0092-8674(95)90127-2. [DOI] [PubMed] [Google Scholar]
- Tutton P. J., Barkla D. H. Comparison of the tumor inhibiting effects of three histamine H2-receptor antagonists. Anticancer Res. 1983 Jan-Feb;3(1):7–10. [PubMed] [Google Scholar]
- Tønnesen H., Knigge U., Bülow S., Damm P., Fischerman K., Hesselfeldt P., Hjortrup A., Pedersen I. K., Pedersen V. M., Siemssen O. J. Effect of cimetidine on survival after gastric cancer. Lancet. 1988 Oct 29;2(8618):990–992. doi: 10.1016/s0140-6736(88)90743-x. [DOI] [PubMed] [Google Scholar]
- Wali R. K., Bissonnette M., Khare S., Hart J., Sitrin M. D., Brasitus T. A. 1 alpha,25-Dihydroxy-16-ene-23-yne-26,27-hexafluorocholecalciferol, a noncalcemic analogue of 1 alpha,25-dihydroxyvitamin D3, inhibits azoxymethane-induced colonic tumorigenesis. Cancer Res. 1995 Jul 15;55(14):3050–3054. [PubMed] [Google Scholar]
- Wali R. K., Frawley B. P., Jr, Hartmann S., Roy H. K., Khare S., Scaglione-Sewell B. A., Earnest D. L., Sitrin M. D., Brasitus T. A., Bissonnette M. Mechanism of action of chemoprotective ursodeoxycholate in the azoxymethane model of rat colonic carcinogenesis: potential roles of protein kinase C-alpha, -beta II, and -zeta. Cancer Res. 1995 Nov 15;55(22):5257–5264. [PubMed] [Google Scholar]
- Watson S. A., Wilkinson L. J., Robertson J. F., Hardcastle J. D. Effect of histamine on the growth of human gastrointestinal tumours: reversal by cimetidine. Gut. 1993 Aug;34(8):1091–1096. doi: 10.1136/gut.34.8.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weil J., Colin-Jones D., Langman M., Lawson D., Logan R., Murphy M., Rawlins M., Vessey M., Wainwright P. Prophylactic aspirin and risk of peptic ulcer bleeding. BMJ. 1995 Apr 1;310(6983):827–830. doi: 10.1136/bmj.310.6983.827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Welch G. N., Loscalzo J. Homocysteine and atherothrombosis. N Engl J Med. 1998 Apr 9;338(15):1042–1050. doi: 10.1056/NEJM199804093381507. [DOI] [PubMed] [Google Scholar]
- Weppelmann B., Mönkemeier D. The influence of prostaglandin antagonists on radiation therapy of carcinoma of the cervix. Gynecol Oncol. 1984 Feb;17(2):196–199. doi: 10.1016/0090-8258(84)90077-5. [DOI] [PubMed] [Google Scholar]
- Willett W. C., Hunter D. J. Vitamin A and cancers of the breast, large bowel, and prostate: epidemiologic evidence. Nutr Rev. 1994 Feb;52(2 Pt 2):S53–S59. doi: 10.1111/j.1753-4887.1994.tb01387.x. [DOI] [PubMed] [Google Scholar]
- Winawer S. J., Zauber A. G., O'Brien M. J., Ho M. N., Gottlieb L., Sternberg S. S., Waye J. D., Bond J., Schapiro M., Stewart E. T. Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps. The National Polyp Study Workgroup. N Engl J Med. 1993 Apr 1;328(13):901–906. doi: 10.1056/NEJM199304013281301. [DOI] [PubMed] [Google Scholar]
- Zelen M. Are primary cancer prevention trials feasible? J Natl Cancer Inst. 1988 Nov 16;80(18):1442–1444. doi: 10.1093/jnci/80.18.1442. [DOI] [PubMed] [Google Scholar]
- de Vries N., van Zandwijk N., Pastorino U. The EUROSCAN Study. EUROSCAN Steering Committee. Br J Cancer. 1991 Dec;64(6):985–989. doi: 10.1038/bjc.1991.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- van den Brandt P. A., Goldbohm R. A., van 't Veer P., Bode P., Dorant E., Hermus R. J., Sturmans F. A prospective cohort study on toenail selenium levels and risk of gastrointestinal cancer. J Natl Cancer Inst. 1993 Feb 3;85(3):224–229. doi: 10.1093/jnci/85.3.224. [DOI] [PubMed] [Google Scholar]