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Cancer Epidemiology Biomarkers & Prevention Vol. 12, 1536-1539, December 2003
© 2003 American Association for Cancer Research

Short Communication

Urinary Isothiocyanate Excretion, Brassica Consumption, and Gene Polymorphisms among Women Living in Shanghai, China

Jay H. Fowke1, Xiao-Ou Shu1, Qi Dai1, Ayumi Shintani1, C. Clifford Conaway2, Fung-Lung Chung2, Qiuyin Cai1, Yu-Tang Gao3 and Wei Zheng1

1 Vanderbilt University Medical Center, Nashville, Tennessee, 2 American Health Foundation Cancer Center, Institute for Cancer Prevention, Valhalla, New York; and 3 Shanghai Cancer Center, Shanghai, Peoples Republic of China


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Alternative measures of Brassica vegetable consumption (e.g., cabbage) may clarify the association between Brassica and cancer risk. Brassica isothiocyanates (ITCs) are excreted in urine and may provide a sensitive and food-specific dietary biomarker. However, the persistence of ITCs in the body may be brief and dependent on the activity of several Phase II enzymes, raising questions about the relationship between a single ITC measure and habitual dietary patterns. This study investigates the association between urinary ITC excretion and habitual Brassica consumption, estimated by a food frequency questionnaire, among healthy Chinese women enrolled in the Shanghai Breast Cancer Study. Participants (n = 347) completed a validated food frequency questionnaire querying habitual dietary intake during the prior 5 years and provided a fasting first-morning urine specimen. Genetic deletion of glutathione S-transferases (GSTM1/GSTT1), and single nucleotide substitutions in GSTP1 (A313G) and NAD(P)H:quinone oxidoreductase 1 (NQO1: C609T), were identified from blood DNA. Urinary ITC excretion levels were marginally higher with the GSTT1-null or GSTP1-G/G genotypes (P = 0.07, P = 0.05, respectively). Mean habitual Brassica intake was 98.3 g/day, primarily as bok choy, and Brassica intake significantly increased across quartile categories of ITC levels. The association between habitual Brassica intake and urinary ITC levels was stronger among women with GSTT1-null or GSTP1-A/A genotypes, or NQO1 T-allele, and the interaction was statistically significant across GSTP1 genotype. In conclusion, a single urinary ITC measure, in conjunction with markers of Phase II enzyme activity, provides a complementary measure of habitual Brassica intake among Shanghai women.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Enzymatic degradation of the glucosinolates from Brassica vegetables (e.g., cabbage) generates isothiocyanates (ITCs) and other agents with potential to induce Phase II enzymes and apoptosis and stabilize cellular proliferation, possibly reducing cancer risk (1 , 2) . However, it is difficult to evaluate the association between habitual Brassica vegetable consumption and cancer in epidemiological analyses. Most food frequency questionnaires (FFQs) do not query the less common, but potentially potent, Brassica vegetables. Furthermore, FFQs do not capture variability in glucosinolate exposure because of cooking practices, cultivar, storage conditions, and myrosinase and gut microflora activities (3, 4, 5) .

Conjugated urinary ITCs have been measured after consumption of glucosinolate rich foods (6) , and urinary ITC levels correlate favorably with recent glucosinolate exposure (7) and decrease with vegetable cooking (3) . Two epidemiological studies have found greater urinary ITC levels protectively associated with breast and lung cancer (8 , 9) . However, excretion of urinary ITCs after a single Brassica meal peaks within 24 h, and ITCs are removed within 3 days (7) . Therefore, inference from a single urinary ITC biomarker to a habitual pattern of Brassica intake may be limited to analyses of study populations with high-level and steady-state Brassica vegetable consumption. In Singapore, Seow et al. (10) found that urinary ITC levels were favorably associated with habitual Brassica intake as measured by FFQ. Furthermore, homozygous deletion of the Phase II enzyme GSTT1 modified the ITC and Brassica association. This study extends the evaluation of urinary ITC as a biomarker of habitual Brassica intake to women living in Shanghai, China, and potential modification by GSTP1, GSTM1, GSTT1, and NQO1 genetic polymorphisms.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Participants.
The present study is limited to a subset of controls recruited as a part of the Shanghai Breast Cancer Study (SBCS), and SBCS details have been reported (11) . The controls of the SBCS were recruited from women randomly selected from the female general Shanghai population using the Shanghai Resident Registry, a registry of all adult residents in urban Shanghai. Eligible women had to live at the registered address between 1996 and 1998 and were between 25 and 64 years of age. A total of 1724 eligible population controls were recruited (90.3% recruitment; refusals: n = 166, 9.6%; death or prior cancer diagnosis: n = 2, 0.1%). Demographics and other data were measured by a structured questionnaire. Habitual dietary intake was measured using a validated food frequency questionnaire (12) , which included the five most commonly consumed Brassica vegetables (green cabbage, nappa, Chinese cabbage and bok choy, cauliflower, and white turnip). Nutrient scores were computed using the Chinese Food Composition TableCitation (13) .


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  		Table 1 Urinary isothiocynates (ITC) levels (µmol/ml/mg creatinine) among Chinese women in Shanghai

 
A fasting first-morning urine sample was collected from 99.8% of subjects. After collection, 125 mg of ascorbic acid were added to ~100 ml of urine to prevent oxidation of labile compounds, and samples were placed on ice during transport to the central laboratory for processing and storage at -70°C. Urinary ITC levels were measured in urine specimens collected from a sample of 348 women. These participants were selected as controls in a case-control subgroup study and were matched to breast cancer cases by age group (5 years) and menopausal status. A comparison of SBCS controls with our sub-study population found that our substudy was generally comparable with the SBCS control population (8) .

Laboratory Analysis.
The method of urinary ITC analysis has been reported previously (6) . Briefly, triplicate aliquots of 100 µl of clarified urine were mixed with 10 mM 1,2-benzenedithiol (Lancaster Synthesis, Inc., Windham NH) and degassed 0.1 mM potassium phosphate (pH 8.5). The reaction mixtures incubated (2 h at 65°C) in capped high-performance liquid chromatography vials, were cooled and then were centrifuged (2800 rpm, 20 min) before detection of the cyclocondensation product 1,3-benzendithiol-2-thione by reverse-phase high-performance liquid chromatography [Waters µBondapak C18 (150 x 3.9 mm); Waters C18 guard column], wavelength, 365 nm; isocratic mobile phase methanol/water, 7:3). The interbatch coefficient of variation [(CV = SD/mean) * 100] was 3.40%. The intrabatch coefficient of variation was 9.64, 6.64, 5.57, 5.11, and 3.84% at ITC concentrations of 2, 5, 10, 15, and 100 µM, respectively. Urinary creatinine levels were measured using a Vitros 500 Clinical Chemistry Analyzer (Johnson & Johnson Clinical Diagnostics, Rochester, NY). Urines were analyzed in two batches, separated by ~18 months.

Genotyping Methods.
Genomic DNA was extracted from buffy coat fractions (Puregene DNA isolation kit; Gentra Systems, Minneapolis, MN). A multiplex PCR protocol conclusively identified the null genotype for the GSTM1 and GSTT1 genes (14) . The Albumin gene was used as an internal control. The GSTP1 A313G polymorphism, leading to an Ile104Val substitution, was determined by PCR-RFLP method, as reported previously (15) . The NQO1 C609T polymorphism was evaluated by the PCR-RFLP method as described previously (8) .

Statistical Analysis.
Total habitual Brassica intake was calculated as the sum of the five Brassica vegetables reported by the FFQ. The ITC exposure index was calculated using estimated Brassica vegetable ITC levels reported by Jiao et al. (16) , where watercress ITC values were used for turnip intake. Urinary ITC concentrations were standardized to urinary creatinine, to control for variability in urine volume, and the distribution of natural log-transformed ITC values approached normality (Shapiro-Wilk P = 0.14). One subject with a highly influential urinary ITC value was excluded. Normality of the residuals of the general linear models was assessed and confirmed using Shapiro-Wilk tests. Natural log-transformed ITC levels were compared across genotypes, age categories, or menopausal status in a general linear model adjusted for laboratory batch. Geometric mean ITC levels are reported.

Epidemiological studies categorize continuous dietary intake measures before investigating diet-disease relationships. Urinary ITC exposure categories were determined at the quartiles of the ITC distribution, and average habitual Brassica intake was calculated for each ITC category. Trend tests were performed by regressing an ordinal variable representing the ITC category on normalized (natural log-transformed) Brassica intake. Normality of the residuals was confirmed.

Modification of the Brassica and urinary ITC associations by Phase II enzyme genotypes was assessed by further including cross-product term of a genotype by ITC continuous value (nontransformed) with main effects of genotype and ITC variables, in the general linear model predicting Brassica intake. Partial Spearman rank correlations, adjusted for laboratory batch, described the monotonic association between individual-level urinary ITC levels and Brassica intake. All of the analyses were performed using SAS 8.02 (SAS Institute, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Participants included healthy female Shanghai residents (n = 347), with an average age and body mass index of 47.6 years (range, 30–64 years) and 23.0 (range, 15.7–42.2), respectively. The majority of participants were premenopausal [n = 221 (64%)], married [n = 326 (94%)], and nonsmokers [n = 340 (98%)], and had less than a high school education [less than high school, n = 202 (58%); high school, n = 114 (33%); more than high school, n = 31 (9%)].

There was no evidence that urinary ITC excretion was modified by GSTM1 deletion (Tables 1Citation and 2Citation ). ITC levels were marginally higher with homozygous GSTT1 deletion (P = 0.07), and subjects with the G/G genotype of GSTP1 had marginally higher urinary ITC levels compared with subjects with the A/A or G/A genotypes (P = 0.05 and P = 0.08, respectively). Mean urinary ITC levels did not substantively differ across the NQO1 C/C, C/T, or T/T genotypes, or when we combined subjects with the NQO1 T-allele to increase sample size within strata.


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  		Table 2 Urinary isothiocynates (ITC) levels (µmol/ml/mg creatinine) by Phase II enzyme genotypes among Chinese women in Shanghai

 
Participants reported consuming 98 g/day of Brassica vegetables, primarily as bok choy (75 g/day). Urinary ITC levels were categorized, and average Brassica consumption generally increased across categories (Table 3)Citation . Trends were statistically significant with total Brassica, bok choy and green cabbage intakes, and a marginal pattern was evident with turnip intake. The associations between urinary ITC and nappa or cauliflower intakes were inconsistent. These patterns were not affected by simultaneous control for Phase II enzyme genotypes described in Table 2Citation .


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  		Table 3 Mean Brassica intake across quartiles of urinary isothiocynate (ITC) excretion among Chinese women in Shanghai

 
The trends between ITC and Brassica were more consistent among women with GSTT1/M1-null, NQO1-C/T or -T/T, or GSTP1-A/A genotypes, although variability due to GSTM1 genotype was trivial (Table 4)Citation . The interaction between reported Brassica intake, urinary ITC levels, and GSTP1 genotype was statistically significant, with a trend between ITC and Brassica observed only among subjects with the GSTP1 A/A genotype. This interaction persisted after further adjustment for the remaining Phase II enzyme genotypes (P = 0.03). With only 11 subjects homozygous for the G-allele, it was not possible to consider the G/G genotype separately.


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  		Table 4 Reported Brassica (g/day) intake across quartile (Q) of urinary isothiocynate (ITC) excretion, stratified by Phase II enzyme genotype among Chinese women in Shanghai

 
At an individual level, urinary ITC levels were weakly correlated with Brassica intake (rs = 0.16, P < 0.01; adjusted for batch) and the ITC Index, a calculated estimate of dietary ITC exposure (rs = 0.16, P < 0.01). The Brassica intake and urinary ITC correlation was somewhat stronger among subjects with the GSTP1 A/A (A/A: rs = 0.19, P < 0.01; G/A or G/G: rs = 0.04, P = 0.72), NQO1 T-allele (T/T or C/T: rs = 0.20, P < 0.01, C/C: rs = 0.01, P = 0.88), or GSTT1-null (Null: rs = 0.19, P < 0.01; positive: rs = 0.09, P = 0.21) genotypes, but was stable with participant age, menopausal status, and GSTM1 deletion.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Several investigations suggest that Brassica vegetable consumption reduces the risk of lung, colon, bladder, prostate, and breast cancers (17, 18, 19) . The urinary ITC biomarker provides a measure of internalized glucosinolate exposure, the class of phytochemicals with purported biological action, while avoiding dietary assessment errors associated with participant recall and report of past dietary patterns. Urinary ITC levels have been inversely associated with breast or lung cancer risk (8 , 9) . However, in either a case-control or a cohort study, it must be assumed that a biomarker measured at a single point in time reflects a long-term pattern. In our investigation, habitual Brassica consumption significantly increased with urinary ITC excretion, suggesting that this biomarker provides an additional measure of overall habitual Brassica consumption within Shanghai women.

Our FFQ included five commonly consumed Brassica vegetables in the typical Shanghai diet, as was validated against repeated 24-h dietary recall surveys (10) . Bok choy was the predominant Brassica, and the associations between urinary ITC levels and either total Brassica, bok choy, or the ITC index were similar. Green cabbage and turnip intakes also were associated with urinary ITC levels. Although reported intakes of green cabbage and turnip were low, Jiao et al. (16) suggest that the relatively higher ITC content of these vegetables may contribute more ITCs. Furthermore, there was no evidence of an association between cauliflower or nappa intakes and urinary ITC levels, consistent with a lower ITC content (16) . FFQs are not a "gold-standard" dietary measure, and weak correlations may be explained by the validity of the FFQ, as well.

Brassica ITCs induce Phase II enzymes, and, in turn, Phase II enzymes conjugate ITCs leading to excretion (20) . Seow et al. (10) interviewed participants for dietary intake during the prior 12 months and measured urinary ITC levels in spot samples collected ~16 months after the interview. They found greater urinary ITC levels with greater Brassica intake and the GSTT1-positive genotype, primarily among subjects with high Brassica intake, and ITC levels were not associated with GSTM1 or GSTP1 (A313G) genotypes (10) . We collected fasting first-morning urine specimens and also found ITC levels unaffected by GSTM1 genotype. However, urinary ITC excretion was marginally higher with the GSTT1-null and GSTP1-A/A or -A/G genotypes, and trends between ITC levels and habitual Brassica intake was more consistent within subjects with the GSTT1-null, GSTP1-A/A, and NQO1-C/T or -T/T genotypes. Urinary ITC levels may better reflect a time-weighted index of Brassica consumed during the prior several days among subjects with low-activity GSTT1-null and NQO1 T-allele (21) genotypes. The interaction with GSTP1 was statistically significant, and the GSTP1 A/A and G/G genotypes are known to have differential activities in polycyclic aromatic hydrocarbon catalysis (22, 23, 24) . A recent in vitro analysis suggests the G/G genotype has less activity toward an ITC called sulforaphane (25) , and perhaps the rate of intracellular ITC conjugation and excretion is more stable with the GSTP1-A/A genotype. Reasons for inconsistencies with Seow et al. (10) are unclear but may include differences in urine collection protocols, dietary assessment methods, types or amounts of Brassica consumed, or genetic profiles between the Shanghai and Singapore study procedures and populations.

In summary, Brassica consumption may contribute to the observed variability in cancer incidence and mortality across countries. However, analyses based solely on FFQ data may be limited by reporting errors, constrained food lists, and natural variability in glucosinolate profiles. We found the urinary ITC levels measured from a first-morning urine sample, with Phase II enzyme genotyping, provides a complementary measure of habitual Brassica consumption among Shanghai residents.


   Footnotes
 
Grant support: NIH Grants RO3CA89845, R01CA64277, and P30CA68485 to the Vanderbilt-Ingram Cancer Center.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Requests for reprints: Jay H. Fowke; 6110 Medical Center East, Vanderbilt University Medical Center, Nashville, TN 37232-8300. Phone: (615) 936-2903; E-mail: jay.fowke{at}vanderbilt.edu.

Received 5/ 5/03; revised 7/22/03; accepted 8/21/03.


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