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Using isothiocyanate excretion as a biological marker of Brassica vegetable consumption in epidemiological studies: evaluating the sources of variability

Published online by Cambridge University Press:  02 January 2007

Jay H Fowke ,
Jed W Fahey ,
Katherine K Stephenson  and
James R Hebert
Jay H Fowke*
Affiliation:
Department of Epidemiology and Biostatistics and the Nutrition Center, School of Public Health, University of South Carolina and the South Carolina Cancer Center, Columbia, SC, USA
Jed W Fahey
Affiliation:
Department of Pharmacology and Molecular Sciences, Brassica Chemoprotection Laboratory, Johns Hopkins University School of Medicine, Baltimore, MD, USA
Katherine K Stephenson
Affiliation:
Department of Pharmacology and Molecular Sciences, Brassica Chemoprotection Laboratory, Johns Hopkins University School of Medicine, Baltimore, MD, USA
James R Hebert
Affiliation:
Department of Epidemiology and Biostatistics and the Nutrition Center, School of Public Health, University of South Carolina and the South Carolina Cancer Center, Columbia, SC, USA
*
*Corresponding author: Email [email protected]
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Abstract

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Objective:

Brassica vegetable consumption (e.g. broccoli) leads to excretion of isothiocyanates (ITC) in urine. We evaluated the consistency of ITC as a biomarker for dietary Brassica vegetable consumption across the types of vegetables and methods of preparation used in Western societies, and across consumption levels.

Design:

A single-armed behavioural intervention with duplicate baseline assessment and post-intervention assessment. Urinary ITC excretion and estrogen metabolites were measured from 24-hour urine samples. Dietary intake was measured by a 24-hour recall.

Setting:

The behavioural intervention facilitated daily Brassica intake among participants by providing peer support, food preparation instruction, guided practice in a teaching kitchen, and other information.

Subjects:

Thirty-four healthy free-living postmenopausal women who recently had a negative screening mammogram at the University of Massachusetts Medical Center.

Results:

Urinary ITC excretion and total Brassica intake followed the same pattern over the intervention. The ITC biomarker significantly predicted Brassica intake when Brassica consumption averaged about 100 g day−1, but not when Brassica consumption averaged about 200 g day−1. Urinary ITC levels were somewhat higher when more raw vegetables were consumed as compared to lightly cooked vegetables, while the types of Brassica consumed appeared to have only a small, non-significant effect on urinary ITC levels.

Conclusion:

Urinary ITC excretion would be a good exposure biomarker among populations regularly consuming a vegetable serving/day, but may be less accurate among populations with greater intake levels or a wide range of cooking practices.

Keywords

IsothiocyanateBiomarkerDietEstrogen metabolismDietary assessmentBrassica
Type
Research Article
Information
Public Health Nutrition , Volume 4 , Issue 3 , June 2001 , pp. 837 - 846
Copyright
Copyright © CABI Publishing 2001

References

1Beecher, CW. Cancer preventive properties of varieties of Brassica oleracea: a review. Am. J. Clin. Nutr. 1994; 59: 1166S–70S.Google Scholar
2Block, G, Patterson, B, Subar, A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr. Cancer 1992; 18: 18–1.Google Scholar
3Steinmetz, KA, Potter, JD. Vegetables, fruit, and cancer prevention: a review. J. Am. Diet. Assoc. 1996; 96: 1027–39.CrossRefGoogle ScholarPubMed
4Michaud, DS, Spiegelman, D, Clinton, SK, Rimm, EB, Willett, WC, Giovannucci, EL. Fruit and vegetable intake and incidence of bladder cancer in a male prospective cohort. J. Natl. Cancer Inst. 1999; 91(7): 605–13.CrossRefGoogle Scholar
5Verhoeven, DT, Goldbohm, RA, van Poppel, G, Verhagen, H, van denBrandt, PA. Epidemiological studies of Brassica vegetables and cancer risk. Cancer Epidemiol. Biomark. Prev. 1996; 5: 733–48.Google Scholar
6Kohlmeier, L, Su, L. Cruciferous vegetable consumption and colorectal cancer risk: meta-analysis of the epidemiological evidence. FASEB J. 1997; 11(3), 2141.Google Scholar
7Graham, S, Dayai, H, Swanson, M, Mittleman, A, Wilkinson, G. Diet in the epidemiology of cancer of the colon and rectum. J. Natl. Cancer Inst. 1978; 61(3): 709–14.Google ScholarPubMed
8Zhang, S, Hunter, D, Forman, MR, Rosner, BA, Speizer, FE, Colditz, GA, et al. Dietary carotenoids and vitamin A, C, and E and risk of breast cancer. J. Natl. Cancer Inst. 1999; 91(6): 547–56.CrossRefGoogle Scholar
9Rosa, EAS, Heany, RK, Fenwick, GR, Portas, CAM. Glucosinolates in crop plants. Horticult. Rev. 1997; 19: 19–99.Google Scholar
10Fahey, JW, Zalcmann, AT, Talalay, P. The chemical diversity and distribution of glucosinolates among plants. Phytochemistry 2001; 56: 56–5.CrossRefGoogle ScholarPubMed
11Shapiro, TA, Fahey, JW, Wade, KL, Stephenson, KK, Talalay, P. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of Cruciferous vegetables. Cancer Epidemiol. Biomark. Prev. 1998; 7: 1091–1100.Google Scholar
12Cover, CM, Hseih, SJ, Tran, SH, Hallden, G, Kim, GS, Bjeldanes, LF, et al. Indole-3-carbinol inhibits the expression of cyclin-dependent kinase-6 and induces a G1 cell cycle arrest of human breast cancer cells independent of estrogen receptor signaling. J. Biol. Chem. 1998; 273(7): 3838–47.Google Scholar
13Vang, O, Frandsen, H, Hansen, KT, Nielsen, JB, Andersen, O. Modulation of drug-metabolising enzyme expression by condensation products of indole-3-ylcarbinol, and inducer in cruciferous vegetables. Pharmacol. Toxicol. 1999; 84: 84–59.CrossRefGoogle ScholarPubMed
14Fares, FA, Ge, X, Yanni, S, Rennert, G. Dietary indole derivatives induce apoptosis in human breast cancer cells. Adv. Exp. Med. Biol. 1998; 451: 451–153.Google ScholarPubMed
15Fahey, JW, Stephenson, KK. Cancer chemoprotective effects of cruciferous vegetables. Horticult. Sci. 1999; 34(7): 1159–63.Google Scholar
16Prestera, T, Talalay, P. Electrophile and antioxidant regulation of enzymes that detoxify carcinogens. Proc. Natl. Acad. Sci. USA 1995; 92: 92–8965.CrossRefGoogle ScholarPubMed
17Talalay, P. The war against cancer: new hope. Proc. Am. Phil. Soc. 1999; 143(1): 52–72.Google Scholar
18Kensler, TW. Chemoprevention by inducers of carcinogen detoxication enzymes. Environ. Health Persp. 1997; 105(Suppl.): 964–70.Google ScholarPubMed
19Fahey, JW, Talalay, P. Antioxidant functions of sulforaphane: a potent inducer of phase 2 detoxication enzymes. Food Chem. Tox. 1999; 37(9): 973–9.CrossRefGoogle Scholar
20Willett, W. Nutritional Epidemiology. New York: Oxford University Press, 1990.Google Scholar
21Hebert, JR, Clemow, L, Pbert, L, Ockene, IS, Ockene, JK. Social desirability bias in dietary self-report may compromise the validity of dietary intake measures. Int. J. Epidemiol. 1995; 24(2): 389–98.CrossRefGoogle ScholarPubMed
22Zhang, Y, Wade, KL, Prestera, T, Talalay, P. Quantitative determination of isothiocyanates, dithiocarbamates, carbon disulfide, and related thiocarbonyl compounds by cyclocondensation of 1,2-benzenedithiol. Anal. Biochem. 1996; 239: 239–160.CrossRefGoogle ScholarPubMed
23Seow, A, Shi, C-Y, Chung, F-L, Jiao, D, Hankin, JH, Lee, H-P, et al. Urinary total isothiocyanate (ITC) in a population-based sample of middle-aged and older Chinese in Singapore: relationship with dietary total ITC and glutathione S-transferase M1/T1/P1 genotypes. Cancer Epidemiol. Biomark. Prev. 1998; 7: 775–81.Google Scholar
24Kaaks, R, Riboli, E, Sinha, R. Biochemical markers of dietary intake. In: Toniolo, P, Boffetta, P, Shuker, D, Rothman, N, Hulka, B, Pearce, N, eds. Application of Biomarkers in Cancer Epidemiology. Lyon: IARC, 1997; 103–26.Google Scholar
25Getahun, SM, Chung, F-L. Conversion of glucosinolates to isothiocyanates in humans after ingestion of cooked watercress. Cancer Epidemiol. Biomark. Prev. 1999; 8: 8–447.Google ScholarPubMed
26Chung, F-L, Jiao, D, Getahun, SM, Yu, MC. A urinary biomarker for uptake of dietary isothiocyanates in humans. Cancer Epidemiol. Biomark. Prev. 1998; 7: 7–103.Google ScholarPubMed
27Chung, F-L, Morse, MA, Eklind, KI, Lewis, J. Quantitation of human uptake of the anticarcinogen phenethyl isothiocyanate after a watercress meal. Cancer Epidemiol. Biomark. Prev. 1992; 1: 1–383.Google Scholar
28Goodrich, RM, Anderson, JL, Stoewsand, GS. Glucosinolate changes in blanched broccoli and Brussels sprouts. J. Food Process. 1989; 13: 13–275.Google Scholar
29Kushad, MM, Brown, AF, Kurlich, AC, Juvik, JA, Klein, BP, Wallig, MA, et al. Variation of glucosinolates in vegetable crops of the Brassica oleracea. J. Agric. Food Chem. 1999; 47(4): 1541–8.CrossRefGoogle ScholarPubMed
30Nugon-Baudon, L, Rabot, S. Glucosionolates and glucosinolate derivatives: implications for protection against chemical carcinogenesis. Nutr. Res. Rev. 1994; 7: 7–205.CrossRefGoogle ScholarPubMed
31London, SJ, Yuan, J-M, Chung, FL, Gao, Y-T, Coetzee, BA, Ross, RK, et al. Isothiocyanates, glutathione S-transferase M1 and T1 polymorphisms, and lung cancer risk: a prospective study of men in Shanghai, China. Lancet 2000; 356: 724–9.CrossRefGoogle Scholar
32Fowke, JH, Longcope, C, Hebert, JR. Brassica vegetable consumption shifts estrogen metabolism in healthy postmenopausal women. Cancer Epidemiol Biomark. Prev. 2000; 9: 773–9.Google ScholarPubMed
33Feskanich, D, Sielaff, B, Chong, K, Buzzard, I. Computerized collection and analysis of dietary intake information. Comput. Meth. Prog. Biol. 1989; 30: 30–47.CrossRefGoogle ScholarPubMed
34Martin, HJ. A revised measure of approval motivation and its relationship to social desirability. J. Pers. Assess. 1984; 48: 48–508.CrossRefGoogle ScholarPubMed
35Marlowe, D, Crowne, D. Social desirability and responses to perceived situational demands. J. Consult. Clin. Psychol. 1961; 25: 25–109.Google ScholarPubMed
36Bradlow, HL, Sepkovic, DW, Klug, T, Osborne, MP. Application of an improved ELISA assay to the analysis of urinary estrogen metabolites. Steroids 1998;63(7–8): 406–13.CrossRefGoogle Scholar
37Hebert, JR, Hurley, T, Chiraboga, DE, Barone, JA. A comparison of selected nutrient intakes derived from three diet assessment methods used in a low-fat maintenance trial. Public Health Nutr. 1998; 1: 1–207.Google Scholar
38Buzzard, IM, Faucett, CL, Jeffrey, RW, McBane, L, McGovern, P, Baxter, JS, et al. Monitoring dietary change in a low-fat diet intervention study: advantages of using 24-hour dietary recalls vs food records. J. Am. Diet. Assoc. 1996; 96: 96–574.Google Scholar
39Fenwick, GR, Heaney, RK, Mullin, WJ. Glucosinolates and their breakdown products in food and food plants. In: CRC Critical Reviews in Food Science and Nutrition, 1983; 123–200.CrossRefGoogle ScholarPubMed
40Steinmetz, KA, Kushi, LH, Bostick, RM, Folsom, AR, Potter, JD. Vegetables, fruit, and colon cancer in the Iowa Women's Health Study. Am. J. Epidemiol. 1994; 139(1): 1–15.Google Scholar
41McDanell, R, McLean, AEM, Hanley, AB, Heaney, RK, Fenwick, GR. Differential induction of mixed-function oxidase activity in rat liver and intestine by diets containing processed cabbage: correlation with cabbage levels of glucosinolates and glucosinolate hydrolysis products. Food Chem. Tox. 1987; 25(5): 363–8.CrossRefGoogle ScholarPubMed
42Howard, LA, Jeffrey, EH, Wallig, MA, Klein, BP. Retention of phytochemicals in fresh and processed broccoli. J. Food Sci. 1997; 62(6): 1098–100.CrossRefGoogle Scholar
43Slominski, BA, Campbell, LD. Formation of indole glucosinolate breakdown products in autolyzed, streamed, and cooked Brassica vegetables. J. Agric. Food Chem. 1989; 37: 1297–302.CrossRefGoogle Scholar
44Bjeldanes, LF, Kim, J-Y, Grose, KR, Bartholomew, JC, Bradfield, CA. Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc. Natl. Acad. Sci. USA 1991; 88: 9543–7.Google Scholar
45Kabat, GC, Chang, CJ, Sparano, JA, Sepkovic, DW, Hu, X-P, Khalil, A, et al. Urinary estrogen metabolites and breast cancer: a case–control study. Cancer Epidemiol. Biomark. Prev. 1997; 6: 6–505.Google Scholar
46Zheng, W, Dunning, L, Jin, F, Holtzman, J. Correspondence re: GC Kabat et al., Urinary estrogen metabolites and breast cancer: a case–control study. Cancer Epidemiol. Biomark. Prev. 1998: 7: 85–6.Google ScholarPubMed
47Bradlow, HL, Telang, NT, Sepkov, DW, Osborne, MP. 2-Hydroxyestrone: the 'good' estrogen. J. Endocrinol. 1996; 150: S256–65.Google Scholar
48Ursin, G, London, S, Stanczyk, FZ, Gentzchein, E, Paganini-Hill, A, Ross, RK, et al. Urinary 2-hydroxyestrone/16α-hydroxyestrone ratio and risk of breast cancer in postmenopausal women. J. Natl. Cancer Inst. 1999; 91(12), 1067–72.CrossRefGoogle ScholarPubMed
49Ho, GH, Luo, XW, Ji, CY, Foo, SC, Ng, EH. Urinary 2/16-hydroxyestrone ratio: correlation with serum insulin-like growth factor binding protein-3 and a potential biomarker of breast cancer. Ann. Acad. Med. Singapore 1998; 27: 294–9.Google Scholar
50Meilahn, E, DeStavola, B, Allen, D, Fentim, I, Bradlow, H, Sepkovic, D, et al. Do urinary oestrogen metabolites predict breast cancer? Guernsey III cohort follow-up. Br. J. Cancer 1998; 78(9): 1250–5.Google Scholar
51Walter-Sack, I, Klotz, U. Influence of diet and nutritional status on drug metabolism. Clin. Pharmacokinetics 1996; 31(1): 47–64.CrossRefGoogle ScholarPubMed