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Japanese Journal of Cancer Research : Gann logoLink to Japanese Journal of Cancer Research : Gann
. 2001 Oct;92(10):1026–1033. doi: 10.1111/j.1349-7006.2001.tb01056.x

Beef Tallow, but Not Perilla or Corn Oil, Promotion of Rat Prostate and Intestinal Carcinogenesis by 3,2‐Dimethyl‐4‐aminobiphenyl

Toshio Mori 1, Katsumi Imaida 1, Seiko Tamano 1, Masashi Sano 1, Satoru Takahashi 1, Makoto Asamoto 1, Masazumi Takeshita 2, Hiroshi Ueda 3, Tomoyuki Shirai 1,
PMCID: PMC5926612  PMID: 11676852

Abstract

The modifying effects of three kinds of fat (corn oil, beef tallow or perilla oil, each at 20% in the diet) on F344 rat prostate carcinogenesis induced by 3,2‐dimethyl‐4‐aminobiphenyl (DMAB) were investigated. Non‐invasive carcinomas of the ventral prostate were induced by DMAB alone and invasive carcinomas of the other prostate lobes and seminal vesicles by DMAB and testosterone propionate (TP). Eight groups of F344 rats were initiated with 50 mg/kg body weight of DMAB at 2‐week intervals for the first 20 weeks, four also receiving TP, extended until week 60. The animals received basal chow powder diet or one of three high fat diets throughout the experiment (60 weeks). One further group served as a non‐carcinogen‐treated control maintained on basal chow powder diet. Beef tallow significantly increased the development of ventral prostate carcinomas with DMAB alone (from 15 to 45%, P<0.05), while perilla oil reduced the incidence of prostatic intraepithelial neoplasia (PIN) in the ventral lobe of rats given DMAB + TP (from 70 to 10%, P<0.01), but not in those given DMAB alone. No other effects of high fats were observed regarding PIN or invasive cancers of the dorsolateral and anterior prostate or seminal vesicles. A satellite experiment demonstrated that all high fat diets for 4 weeks increased the 5‐bromo‐2‐deoxyuridine (BrdU) labeling index of prostate epithelial cells, suggesting that a high fat intake, irrespective of the fatty acid composition, may accelerate cell kinetics in the prostate. Of the three high fat diets, beef tallow was also found to increase intestinal carcinogenesis. Thus, the present data revealed carcinogenesis in the prostate and intestine to be promoted by beef tallow.

Keywords: High fat diets, Prostate cancer, Rat

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REFERENCES

  • 1. ) Doll , R.Nature and nurture: possibilities for cancer control . Carcinogenesis , 17 , 177 – 184 ( 1996. ). [DOI] [PubMed] [Google Scholar]
  • 2. ) Willett , W. C.Diet and health: what should we eat ? Science , 264 , 532 – 537 ( 1994. ). [DOI] [PubMed] [Google Scholar]
  • 3. ) Minamoto , T. , Mai , M. and Ronai , Z.Environmental factors as regulators and effectors of multistep carcinogenesis . Carcinogenesis , 20 , 519 – 527 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 4. ) Hill , M. J.Nutrition and human cancer . Ann. NY Acad. Sci. , 833 , 68 – 78 ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 5. ) Steinmetz , K. A. and Potter , J. D.Vegetables, fruit, and cancer prevention: a review . J. Am. Diet Assoc. , 96 , 1027 – 1039 ( 1996. ). [DOI] [PubMed] [Google Scholar]
  • 6. ) Kroes , R. , Beems , R. B. , Bosland , M. C. , Bunnik , G. S. and Sinkeldam , E. J.Nutritional factors in lung, colon, and prostate Carcinogenesis in animal models . Fed. Proc. , 45 , 136 – 141 ( 1986. ). [PubMed] [Google Scholar]
  • 7. ) Eichholzer , M.The significance of nutrition in primary prevention of cancer . Ther. Umsch. , 54 , 457 – 462 ( 1997. ). [PubMed] [Google Scholar]
  • 8. ) Kolonel , L. N.Nutrition and prostate cancer . Cancer Causes Control , 7 , 83 – 94 ( 1996. ). [DOI] [PubMed] [Google Scholar]
  • 9. ) Brawley , O. W. , Knopf , K. and Thompson , I.The epidemiology of prostate cancer part II: the risk factors . Semin. Urol. Oncol. , 16 , 193 – 201 ( 1998. ). [PubMed] [Google Scholar]
  • 10. ) De Stefani , E. , Fierro , L. , Barrios , E. and Ronco , A.Tobacco, alcohol, diet and risk of prostate cancer . Tumori , 81 , 315 – 320 ( 1995. ). [DOI] [PubMed] [Google Scholar]
  • 11. ) Vlajinac , H. D. , Marinkovic , J. M. , Ilic , M. D. and Kocev , N. I.Diet and prostate cancer: a case‐control study . Eur. J. Cancer , 33 , 101 – 107 ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 12. ) Woutersen , R. A. , Appel , M. J. , van Garderen‐Hoetmer , A. and Wijnands , M. V.Dietary fat and Carcinogenesis . Mutat. Res. , 443 , 111 – 127 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 13. ) Kolonel , L. N. , Nomura , A. M. and Cooney , R. V.Dietary fat and prostate cancer: current status . J. Natl. Cancer Inst. , 91 , 414 – 428 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 14. ) Giovannucci , E. , Rimm , E. B. , Colditz , G. A. , Stampher , M. J. , Ascherio , A. , Chute , C. C. and Willett , W. C.A prospective study of dietary fat and risk of prostate cancer . J. Natl. Cancer Inst , 85 , 1571 – 1579 ( 1993. ). [DOI] [PubMed] [Google Scholar]
  • 15. ) Pollard , M. and Luckert , P. H.Promotional effects of testosterone and high fat diet on the development of autochthonous prostate cancer in rats . Cancer Lett. , 32 , 223 – 227 ( 1986. ). [DOI] [PubMed] [Google Scholar]
  • 16. ) Pour , P. M. , Groot , K. , Kazakoff , K. , Anderson , K. and Schally , A. V.Effects of high‐fat diet on the patterns of prostatic cancer induced in rats by N‐nitrosobis(2‐oxopropyl)amine and testosterone . Cancer Res. , 51 , 4757 – 4761 ( 1991. ). [PubMed] [Google Scholar]
  • 17. ) Shirai , T. , Yamamoto , A. , Iwasaki , S. , Tamano , S. and Masui , T.Induction of invasive carcinomas of the seminal vesicles and coagulating glands of F344 rats by administration of N‐methylnitrosourea or N‐nitrosobis(2‐oxopropyl)amine and followed by testosterone propionate with or without high‐fat diet . Carcinogenesis , 12 , 2169 – 2173 ( 1991. ). [DOI] [PubMed] [Google Scholar]
  • 18. ) Kondo , Y. , Homma , Y. , Aso , Y. and Kakizoe , T.Promotional effect of two‐generation exposure to a high‐fat diet on prostate Carcinogenesis in ACI/Seg rats . Cancer Res. , 54 , 6129 – 6132 ( 1994. ). [PubMed] [Google Scholar]
  • 19. ) Harvei , S. , Bjerve , K. S. , Tretli , S. , Jellum , E. , Robsahm , T. E. and Vatten , L.Prediagnostic level of fatty acids in serum phospholipids: omega‐3 and omega‐6 fatty acids and the risk of prostate cancer . Int. J. Cancer , 71 , 545 – 551 ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 20. ) Gann , P. H. , Hennekens , C. H. , Sacks , F. M. , Grodstein , R , Giovannucci , E. L. and Stampfer , M. J.Prospective study of plasma fatty acids and risk of prostate cancer . J. Natl. Cancer Inst. , 86 , 281 – 286 ( 1994. ). [DOI] [PubMed] [Google Scholar]
  • 21. ) Bagga , D. , Capone , S. , Wang , H.‐J. , Heber , D. , Lill , M. , Chap , L. and Glaspy , J. A.Dietary modulation of omega‐3/omega‐6 polyunsaturated fatty acid ratios in patients with breast cancer . J. Natl. Cancer Inst , 89 , 1123 – 1131 ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 22. ) Stoll , B. A.Breast cancer and the western diet: role of fatty acids and antioxidant vitamins . Eur. J. Cancer , 34 , 1852 – 1856 ( 1998. ). [DOI] [PubMed] [Google Scholar]
  • 23. ) Rose , D. P.Effects of dietary fatty acids on breast and prostate cancers: evidence from in vitro experiments and animal studies . Am. J. Clin. Nutr. , 66 , 1513S – 1522S ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 24. ) Narisawa , T. , Takahashi , M. , Koyanagi , H. , Kusaka , H. , Yamazaki , Y. , Koyama , H. , Fukaura , Y. , Nishizawa , Y. , Kotsugai , M. , Isoda , Y. , Hirano , J. and Tanida , N.Inhibitory effect of dietary perilla oil rich in the n‐3 polyunsaturated fatty acid α‐linolenic acid on colon Carcinogenesis in rats . Jpn. J. Cancer Res. , 82 , 1089 – 1096 ( 1991. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25. ) Noguchi , M. , Minami , M. , Yagasaki , R. , Kinoshita , K. , Earashi , M. , Kitagawa , H. , Taniya , T. and Miyazaki , I.Chemoprevention of DMBA‐induced mammary carcinogenesis in rats by low‐dose EPA and DHA . Br. J. Cancer , 75 , 348 – 353 ( 1997. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26. ) Rose , D. P. and Cohen , L. A.Effects of dietary menhaden oil and retinyl acetate on the growth of DU 145 human prostatic adenocarcinoma cells transplanted into athymic nude mice . Carcinogenesis , 9 , 603 – 605 ( 1988. ). [DOI] [PubMed] [Google Scholar]
  • 27. ) Pandalai , P. K. , Pilat , M. J. , Yamazaki , K. , Naik , H. and Pienta , K. J.The effects of omega‐3 and omega‐6 fatty acids on in vitro prostate cancer growth . Anticancer Res. , 16 , 815 – 820 ( 1996. ). [PubMed] [Google Scholar]
  • 28. ) Kobayashi , M. , Sasaki , S. , Hamada , G. S. and Tsugane , S.Serum n‐3 fatty acids, fish consumption and cancer mortality in six Japanese populations in Japan and Brazil . Jpn. J. Cancer Res. , 90 , 914 – 921 ( 1999. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29. ) Norrish , A. E. , Skeaff , C. M. , Arribas , G. L. , Sharpe , S. J. and Jackson , R. T.Prostate cancer risk and consumption of fish oils: a dietary biomarker‐based case‐control study . Br. J. Cancer , 81 , 1238 – 1242 ( 1999. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30. ) Shirai , T. , Tamano , S. , Kato , T. , Iwasaki , S. , Takahashi , S. and Ito , N.Induction of invasive carcinomas in the accessory sex organs other than the ventral prostate of rats given 3,2′‐dimethyl‐4‐aminobiphenyl and testosterone propionate . Cancer Res. , 51 , 1264 – 1269 ( 1991. ). [PubMed] [Google Scholar]
  • 31. ) Shirai , T. , Imaida , K. , Iwasaki , S. , Mori , T. , Tada , M. and Ito , N.Sequential observation of rat prostate lesion development induced by 3,2′‐dimethyl‐4‐aminobiphenyl and testosterone . Jpn. J. Cancer Res. , 84 , 20 – 25 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 32. ) Shirai , T. , Imaida , K. , Masui , T. , Iwasaki , S. , Mori , T. , Kato , T. and Ito , N.Effects of testosterone, dihydrotestosterone and estrogen on 3,2′‐dimethyl‐4‐aminobiphenyl‐induced rat prostate carcinogenesis . Int. J. Cancer , 57 , 224 – 228 ( 1994. ). [DOI] [PubMed] [Google Scholar]
  • 33. ) Shirai , T. , Tamano , S. , Sano , M. , Imaida , K. , Hagiwara , A. , Futakuchi , M. , Takahashi , M. and Hirose , M.Site‐specific effects of testosterone propionate on the prostate of rat pre‐treated with 3,2′‐dimethyl‐4‐aminobiphenyl: dose‐dependent induction of invasive carcinomas . Jpn. J. Cancer Res. , 86 , 645 – 648 ( 1995. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34. ) Bligh , E. G. and Dyer , W. J.A rapid method of total lipid extraction and purification . Can. J. Biochem. Physiol. , 37 , 911 – 917 ( 1959. ). [DOI] [PubMed] [Google Scholar]
  • 35. ) Yamamoto , N. , Hashimoto , A. , Takemoto , Y. , Okuyama , H. , Nomura , M. , Kitajima , R. , Togashi , T. and Tamai , Y.Effect of the dietary α‐linolenate/linoleate balance on lipid compositions and learning ability of rats. II. Discrimination process, extinction process, and glycolipid compositions . J. Lipid Res. , 29 , 1013 – 1021 ( 1988. ). [PubMed] [Google Scholar]
  • 36. ) Takeshita , M. , Ueda , H. , Shirabe , K. , Higuchi , Y. and Yoshida , S.Lack of promotion of colon carcinogenesis by high‐oleic safflower oil . Cancer , 79 , 1487 – 1493 ( 1997. ). [DOI] [PubMed] [Google Scholar]
  • 37. ) Shirai , T. , Nakamura , A. , Fukushima , S. , Takahashi , S. , Ogawa , K. and Ito , N.Effects of age on multiple organ carcinogenesis induced by 3,2′‐dimethyl‐4‐aminobiphenyl in rats, with particular reference to the prostate . Jpn. J. Cancer Res. , 80 , 312 – 316 ( 1989. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38. ) Shirai , T. , Nakamura , A. , Fukushima , S. , Yamamoto , A. , Tada , M. and Ito , N.Different carcinogenic responses in a variety of organs, including the prostate, of five different rat strains given 3,2′‐dimethyl‐4‐aminobiphenyl . Carcinogenesis , 11 , 793 – 797 ( 1990. ). [DOI] [PubMed] [Google Scholar]
  • 39. ) De Vries , C. E. and van Noorden , C. J.Effects of dietary fatty acid composition on tumor growth and metastasis . Anticancer Res. , 12 , 1513 – 1522 ( 1992. ). [PubMed] [Google Scholar]
  • 40. ) Cuendet , M. and Pezzuto , J. M.The role of cyclooxygenase and lipoxygenase in cancer chemoprevention . Drug Metabol. Drug Interact. , 17 , 109 – 157 ( 2000. ). [DOI] [PubMed] [Google Scholar]
  • 41. ) Latham , P. , Lund , E. K. and Johnson , I. T.Dietary n‐3 PUFA increases the apoptotic response to 1,2‐dimethylhy‐drazine, reduces mitosis and suppresses the induction of carcinogenesis in the rat colon . Carcinogenesis , 20 , 645 – 650 ( 1999. ). [DOI] [PubMed] [Google Scholar]
  • 42. ) Dorgan , J. F. , Judd , J. T. , Longcope , C. , Brown , C. , Schatzkin , A. , Clevidence , B. A. , Campbell , W. S. , Nair , P. P. , Franz , C. , Kahle , L. and Taylor , P. R.Effects of dietary fat and fiber on plasma and urine androgens and estrogens in men: a controlled feeding study . Am. J. Clin. Nutr. , 64 , 850 – 855 ( 1996. ). [DOI] [PubMed] [Google Scholar]
  • 43. ) Hirose , M. , Masuda , A. , Ito , N. , Kamano , K. and Okuyama , H.Effects of dietary perilla oil, soybean oil and safflower oil on 7,12‐dimethylbenz[a]anthracene (DMBA) and 1,2‐dimethylhydrazine (DMH)‐induced mammary gland and colon carcinogenesis in female SD rats . Carcinogenesis , 11 , 731 – 735 ( 1990. ). [DOI] [PubMed] [Google Scholar]
  • 44. ) Tagawa , Y. , Shirai , T. , Fukushima , S. , Nakamura , A. , Hirose , M. and Ito , N.Lack of modification by dietary unsaturated fat of 3,2′‐dimethyl‐4‐aminobiphenyl‐induced rat prostate and colon carcinogenesis . J. Toxicol. Pathol. , 2 , 49 – 53 ( 1989. ). [Google Scholar]

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