Effects of Watercress Consumption on Metabolism of a Tobacco-Specific Lung Carcinogen in Smokers

Stephen S. Hecht, Fung Lung Chung, John P. Richie, Shobha A. Akerkar, Anna Borukhova, Lisa Skowronski, Steven G. Carmella

Research output: Contribution to journalArticle

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Abstract

Epidemiological studies indicate that vegetable consumption protects against lung cancer in humans, but the protective constituents have not been identified. Phenethyl isothiocyanate (PEITC), which is released upon chewing of watercress {nasturtium officinale), is a chemopreventive agent against lung cancer induced by the tobacco-specific lung carcinogen 4- (methylnitrosamino)-l-(3-pyridyl)-l-butanone (NNK) in rats and mice. PEITC inhibits the carcinogenicity of NNK by inhibiting its metabolic activation and thereby increasing the levels of detoxified metabolites excreted in urine. In this study, our goal was to determine whether watercress consumption would modify NNK metabolism in smokers. Eleven smokers maintained constant smoking habits and avoided cruciferous vegetables and other sources of isothiocyanates throughout the study. They donated 24-h urine samples on 3 consecutive days (baseline period). One to 3 days later, they consumed 2 ounces (56.8 g) of watercress at each meal for 3 days and donated 24-h urine samples on each of these days (watercress consumption period). One and 2 weeks later, they again donated 24-h urine samples on 2-3 consecutive days (follow-up periods). The samples were analyzed for two metabolites of NNK; 4-(methylnitrosamino)-l-(3- pyridyl)-l-butanol (NNAL) and [4-(methyInitrosamino)-l- (3-pyridyl)but-l-yl]-/3-ft-D-glucosiduronic acid (NNAL- Gluc). NNAL-Gluc is believed to be a detoxification product of NNK. The urine samples were also analyzed for PEITC-NAC, a metabolite of PEITC. Minimum exposure to PEITC during the watercress consumption period averaged 19-38 mg/day. Seven of the 11 subjects had increased levels of urinary NNAL plus NNAL-Gluc on days 2 and 3 of the watercress consumption period, compared to the baseline period. Overall, the increase in urinary NNAL plus NNAL-Gluc in this period was significant [mean ± SD 0.924 ± 1.12 nmol/24 h (33.5%); P < 0.01]. Urinary levels of NNAL plus NNAL-Gluc returned to near baseline levels in the follow-up periods. The percentage of increase in urinary NNAL plus NNAL- Gluc during days 2 and 3 of the watercress consumption period correlated with intake of PEITC during this period, as measured by total urinary PEITC-NAC (r = 0.62; P = 0.04). The results of this study support our hypothesis that PEITC inhibits the oxidative metabolism of NNK in humans, as seen in rodents, and support further development of PEITC as a chemopreventive agent against lung cancer. This is the first study to report an effect of vegetable consumption on metabolism of a lung carcinogen in humans.

Original languageEnglish (US)
Pages (from-to)877-884
Number of pages8
JournalCancer Epidemiology Biomarkers and Prevention
Volume4
Issue number8
StatePublished - Dec 1 1995

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Carcinogens
Tobacco
Lung
Urine
Vegetables
Lung Neoplasms
Nasturtium
Isothiocyanates
Butanones
phenethyl isothiocyanate
Butanols
Mastication
Habits
Meals
4-((methylnitrosoamino)-1-(3-pyridyl)but-1-yl)beta-omega-glucosiduronic acid
Epidemiologic Studies
Rodentia
Smoking
Acids

All Science Journal Classification (ASJC) codes

  • Epidemiology
  • Oncology

Cite this

Hecht, S. S., Chung, F. L., Richie, J. P., Akerkar, S. A., Borukhova, A., Skowronski, L., & Carmella, S. G. (1995). Effects of Watercress Consumption on Metabolism of a Tobacco-Specific Lung Carcinogen in Smokers. Cancer Epidemiology Biomarkers and Prevention, 4(8), 877-884.
Hecht, Stephen S. ; Chung, Fung Lung ; Richie, John P. ; Akerkar, Shobha A. ; Borukhova, Anna ; Skowronski, Lisa ; Carmella, Steven G. / Effects of Watercress Consumption on Metabolism of a Tobacco-Specific Lung Carcinogen in Smokers. In: Cancer Epidemiology Biomarkers and Prevention. 1995 ; Vol. 4, No. 8. pp. 877-884.
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abstract = "Epidemiological studies indicate that vegetable consumption protects against lung cancer in humans, but the protective constituents have not been identified. Phenethyl isothiocyanate (PEITC), which is released upon chewing of watercress {nasturtium officinale), is a chemopreventive agent against lung cancer induced by the tobacco-specific lung carcinogen 4- (methylnitrosamino)-l-(3-pyridyl)-l-butanone (NNK) in rats and mice. PEITC inhibits the carcinogenicity of NNK by inhibiting its metabolic activation and thereby increasing the levels of detoxified metabolites excreted in urine. In this study, our goal was to determine whether watercress consumption would modify NNK metabolism in smokers. Eleven smokers maintained constant smoking habits and avoided cruciferous vegetables and other sources of isothiocyanates throughout the study. They donated 24-h urine samples on 3 consecutive days (baseline period). One to 3 days later, they consumed 2 ounces (56.8 g) of watercress at each meal for 3 days and donated 24-h urine samples on each of these days (watercress consumption period). One and 2 weeks later, they again donated 24-h urine samples on 2-3 consecutive days (follow-up periods). The samples were analyzed for two metabolites of NNK; 4-(methylnitrosamino)-l-(3- pyridyl)-l-butanol (NNAL) and [4-(methyInitrosamino)-l- (3-pyridyl)but-l-yl]-/3-ft-D-glucosiduronic acid (NNAL- Gluc). NNAL-Gluc is believed to be a detoxification product of NNK. The urine samples were also analyzed for PEITC-NAC, a metabolite of PEITC. Minimum exposure to PEITC during the watercress consumption period averaged 19-38 mg/day. Seven of the 11 subjects had increased levels of urinary NNAL plus NNAL-Gluc on days 2 and 3 of the watercress consumption period, compared to the baseline period. Overall, the increase in urinary NNAL plus NNAL-Gluc in this period was significant [mean ± SD 0.924 ± 1.12 nmol/24 h (33.5{\%}); P < 0.01]. Urinary levels of NNAL plus NNAL-Gluc returned to near baseline levels in the follow-up periods. The percentage of increase in urinary NNAL plus NNAL- Gluc during days 2 and 3 of the watercress consumption period correlated with intake of PEITC during this period, as measured by total urinary PEITC-NAC (r = 0.62; P = 0.04). The results of this study support our hypothesis that PEITC inhibits the oxidative metabolism of NNK in humans, as seen in rodents, and support further development of PEITC as a chemopreventive agent against lung cancer. This is the first study to report an effect of vegetable consumption on metabolism of a lung carcinogen in humans.",
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Hecht, SS, Chung, FL, Richie, JP, Akerkar, SA, Borukhova, A, Skowronski, L & Carmella, SG 1995, 'Effects of Watercress Consumption on Metabolism of a Tobacco-Specific Lung Carcinogen in Smokers', Cancer Epidemiology Biomarkers and Prevention, vol. 4, no. 8, pp. 877-884.

Effects of Watercress Consumption on Metabolism of a Tobacco-Specific Lung Carcinogen in Smokers. / Hecht, Stephen S.; Chung, Fung Lung; Richie, John P.; Akerkar, Shobha A.; Borukhova, Anna; Skowronski, Lisa; Carmella, Steven G.

In: Cancer Epidemiology Biomarkers and Prevention, Vol. 4, No. 8, 01.12.1995, p. 877-884.

Research output: Contribution to journalArticle

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T1 - Effects of Watercress Consumption on Metabolism of a Tobacco-Specific Lung Carcinogen in Smokers

AU - Hecht, Stephen S.

AU - Chung, Fung Lung

AU - Richie, John P.

AU - Akerkar, Shobha A.

AU - Borukhova, Anna

AU - Skowronski, Lisa

AU - Carmella, Steven G.

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N2 - Epidemiological studies indicate that vegetable consumption protects against lung cancer in humans, but the protective constituents have not been identified. Phenethyl isothiocyanate (PEITC), which is released upon chewing of watercress {nasturtium officinale), is a chemopreventive agent against lung cancer induced by the tobacco-specific lung carcinogen 4- (methylnitrosamino)-l-(3-pyridyl)-l-butanone (NNK) in rats and mice. PEITC inhibits the carcinogenicity of NNK by inhibiting its metabolic activation and thereby increasing the levels of detoxified metabolites excreted in urine. In this study, our goal was to determine whether watercress consumption would modify NNK metabolism in smokers. Eleven smokers maintained constant smoking habits and avoided cruciferous vegetables and other sources of isothiocyanates throughout the study. They donated 24-h urine samples on 3 consecutive days (baseline period). One to 3 days later, they consumed 2 ounces (56.8 g) of watercress at each meal for 3 days and donated 24-h urine samples on each of these days (watercress consumption period). One and 2 weeks later, they again donated 24-h urine samples on 2-3 consecutive days (follow-up periods). The samples were analyzed for two metabolites of NNK; 4-(methylnitrosamino)-l-(3- pyridyl)-l-butanol (NNAL) and [4-(methyInitrosamino)-l- (3-pyridyl)but-l-yl]-/3-ft-D-glucosiduronic acid (NNAL- Gluc). NNAL-Gluc is believed to be a detoxification product of NNK. The urine samples were also analyzed for PEITC-NAC, a metabolite of PEITC. Minimum exposure to PEITC during the watercress consumption period averaged 19-38 mg/day. Seven of the 11 subjects had increased levels of urinary NNAL plus NNAL-Gluc on days 2 and 3 of the watercress consumption period, compared to the baseline period. Overall, the increase in urinary NNAL plus NNAL-Gluc in this period was significant [mean ± SD 0.924 ± 1.12 nmol/24 h (33.5%); P < 0.01]. Urinary levels of NNAL plus NNAL-Gluc returned to near baseline levels in the follow-up periods. The percentage of increase in urinary NNAL plus NNAL- Gluc during days 2 and 3 of the watercress consumption period correlated with intake of PEITC during this period, as measured by total urinary PEITC-NAC (r = 0.62; P = 0.04). The results of this study support our hypothesis that PEITC inhibits the oxidative metabolism of NNK in humans, as seen in rodents, and support further development of PEITC as a chemopreventive agent against lung cancer. This is the first study to report an effect of vegetable consumption on metabolism of a lung carcinogen in humans.

AB - Epidemiological studies indicate that vegetable consumption protects against lung cancer in humans, but the protective constituents have not been identified. Phenethyl isothiocyanate (PEITC), which is released upon chewing of watercress {nasturtium officinale), is a chemopreventive agent against lung cancer induced by the tobacco-specific lung carcinogen 4- (methylnitrosamino)-l-(3-pyridyl)-l-butanone (NNK) in rats and mice. PEITC inhibits the carcinogenicity of NNK by inhibiting its metabolic activation and thereby increasing the levels of detoxified metabolites excreted in urine. In this study, our goal was to determine whether watercress consumption would modify NNK metabolism in smokers. Eleven smokers maintained constant smoking habits and avoided cruciferous vegetables and other sources of isothiocyanates throughout the study. They donated 24-h urine samples on 3 consecutive days (baseline period). One to 3 days later, they consumed 2 ounces (56.8 g) of watercress at each meal for 3 days and donated 24-h urine samples on each of these days (watercress consumption period). One and 2 weeks later, they again donated 24-h urine samples on 2-3 consecutive days (follow-up periods). The samples were analyzed for two metabolites of NNK; 4-(methylnitrosamino)-l-(3- pyridyl)-l-butanol (NNAL) and [4-(methyInitrosamino)-l- (3-pyridyl)but-l-yl]-/3-ft-D-glucosiduronic acid (NNAL- Gluc). NNAL-Gluc is believed to be a detoxification product of NNK. The urine samples were also analyzed for PEITC-NAC, a metabolite of PEITC. Minimum exposure to PEITC during the watercress consumption period averaged 19-38 mg/day. Seven of the 11 subjects had increased levels of urinary NNAL plus NNAL-Gluc on days 2 and 3 of the watercress consumption period, compared to the baseline period. Overall, the increase in urinary NNAL plus NNAL-Gluc in this period was significant [mean ± SD 0.924 ± 1.12 nmol/24 h (33.5%); P < 0.01]. Urinary levels of NNAL plus NNAL-Gluc returned to near baseline levels in the follow-up periods. The percentage of increase in urinary NNAL plus NNAL- Gluc during days 2 and 3 of the watercress consumption period correlated with intake of PEITC during this period, as measured by total urinary PEITC-NAC (r = 0.62; P = 0.04). The results of this study support our hypothesis that PEITC inhibits the oxidative metabolism of NNK in humans, as seen in rodents, and support further development of PEITC as a chemopreventive agent against lung cancer. This is the first study to report an effect of vegetable consumption on metabolism of a lung carcinogen in humans.

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