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Published in: Breast Cancer Research and Treatment 2/2015

01-06-2015 | Epidemiology

Premenopausal plasma carotenoids, fluorescent oxidation products, and subsequent breast cancer risk in the nurses’ health studies

Authors: Julia S. Sisti, Sara Lindström, Peter Kraft, Rulla M. Tamimi, Bernard A. Rosner, Tianying Wu, Walter C. Willett, A. Heather Eliassen

Published in: Breast Cancer Research and Treatment | Issue 2/2015

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Abstract

High levels of circulating carotenoids are hypothesized to reduce breast cancer risk, potentially due to their antioxidant properties. However, little is known about the relationship between carotenoid exposure earlier in life and risk. We examined associations of premenopausal plasma carotenoids and markers of oxidative stress and risk of breast cancer among 1179 case–control pairs in the Nurses’ Health Study (NHS) and NHSII. Levels of α- and β-carotene, β-cryptoxanthin, lycopene, and lutein/zeaxanthin were quantified by high-performance liquid chromatography. Three fluorescent oxidation products (FlOP_360, FlOP_320, FlOP_400) were measured in a subset of participants by spectrofluoroscopy. Multivariate conditional logistic regression was used to estimate odds ratios and 95 % confidence intervals for breast cancer by quartile, as well as P values for tests of linear trend. We additionally examined whether 45 single-nucleotide polymorphisms (SNPs) in five genes involved in oxidative and antioxidative processes or carotenoid availability were associated with risk. Carotenoid measures were not inversely associated with breast cancer risk. No differences by estrogen receptor status were observed, though some inverse associations were observed among women postmenopausal at diagnosis. Plasma FlOP levels were not positively associated with risk, and suggestive inverse associations with FlOP_320 and FlOP_360 were observed. Several SNPs were associated with carotenoid levels, and a small number were suggestively associated with breast cancer risk. We observed evidence of interactions between some SNPs and carotenoid levels on risk. We did not observe consistent associations between circulating levels of premenopausal carotenoids or FlOP levels and breast cancer risk.
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Literature
1.
go back to reference Van Gils CH et al (2005) Consumption of vegetables and fruits and risk of breast cancer. JAMA, J Am Med Assoc 293:183–193CrossRef Van Gils CH et al (2005) Consumption of vegetables and fruits and risk of breast cancer. JAMA, J Am Med Assoc 293:183–193CrossRef
2.
go back to reference Lissowska J et al (2008) Intake of fruits, and vegetables in relation to breast cancer risk by hormone receptor status. Breast Cancer Res Treat 107:113–117CrossRefPubMed Lissowska J et al (2008) Intake of fruits, and vegetables in relation to breast cancer risk by hormone receptor status. Breast Cancer Res Treat 107:113–117CrossRefPubMed
4.
go back to reference Smith-Warner SA et al (2001) Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 285:769–776CrossRefPubMed Smith-Warner SA et al (2001) Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 285:769–776CrossRefPubMed
5.
go back to reference Aune D et al (2012) Fruits, vegetables and breast cancer risk: a systematic review and meta-analysis of prospective studies. Breast Cancer Res Treat 134:479–493CrossRefPubMed Aune D et al (2012) Fruits, vegetables and breast cancer risk: a systematic review and meta-analysis of prospective studies. Breast Cancer Res Treat 134:479–493CrossRefPubMed
6.
7.
go back to reference Dorjgochoo T et al (2009) Plasma carotenoids, tocopherols, retinol and breast cancer risk: results from the Shanghai Women Health Study (SWHS). Breast Cancer Res Treat 117:381–389CrossRefPubMedCentralPubMed Dorjgochoo T et al (2009) Plasma carotenoids, tocopherols, retinol and breast cancer risk: results from the Shanghai Women Health Study (SWHS). Breast Cancer Res Treat 117:381–389CrossRefPubMedCentralPubMed
8.
go back to reference Kabat GC et al (2009) Longitudinal study of serum carotenoid, retinol, and tocopherol concentrations in relation to breast cancer risk among postmenopausal women. Am J Clin Nutr 90:162–169CrossRefPubMedCentralPubMed Kabat GC et al (2009) Longitudinal study of serum carotenoid, retinol, and tocopherol concentrations in relation to breast cancer risk among postmenopausal women. Am J Clin Nutr 90:162–169CrossRefPubMedCentralPubMed
9.
go back to reference Epplein M et al (2009) Plasma carotenoids, retinol, and tocopherols and postmenopausal breast cancer risk in the Multiethnic Cohort Study: a nested case-control study. Breast Cancer Res. BCR 11:R49CrossRef Epplein M et al (2009) Plasma carotenoids, retinol, and tocopherols and postmenopausal breast cancer risk in the Multiethnic Cohort Study: a nested case-control study. Breast Cancer Res. BCR 11:R49CrossRef
10.
go back to reference Tamimi RM et al (2005) Plasma carotenoids, retinol, and tocopherols and risk of breast cancer. Am J Epidemiol 161:153–160CrossRefPubMed Tamimi RM et al (2005) Plasma carotenoids, retinol, and tocopherols and risk of breast cancer. Am J Epidemiol 161:153–160CrossRefPubMed
11.
go back to reference Sato R et al (2002) Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomark Prev 11:451–457 Sato R et al (2002) Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomark Prev 11:451–457
12.
go back to reference Maillard V et al (2010) Serum carotenoid, tocopherol and retinol concentrations and breast cancer risk in the E3 N-EPIC study. J Int Cancer 127:1188–1196CrossRef Maillard V et al (2010) Serum carotenoid, tocopherol and retinol concentrations and breast cancer risk in the E3 N-EPIC study. J Int Cancer 127:1188–1196CrossRef
13.
go back to reference Aune D et al (2012) Dietary compared with blood concentrations of carotenoids and breast cancer risk: a systematic review and meta-analysis of prospective studies. Am J Clin Nutr 96:356–373CrossRefPubMed Aune D et al (2012) Dietary compared with blood concentrations of carotenoids and breast cancer risk: a systematic review and meta-analysis of prospective studies. Am J Clin Nutr 96:356–373CrossRefPubMed
15.
go back to reference Nagel G et al (2010) Dietary beta-carotene, vitamin C and E intake and breast cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Breast Cancer Res Treat 119:753–765CrossRefPubMed Nagel G et al (2010) Dietary beta-carotene, vitamin C and E intake and breast cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Breast Cancer Res Treat 119:753–765CrossRefPubMed
16.
go back to reference Zhang X et al (2012) Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 95:713–725CrossRefPubMedCentralPubMed Zhang X et al (2012) Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 95:713–725CrossRefPubMedCentralPubMed
17.
go back to reference Eliassen AH et al (2012) Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104:1905–1916CrossRefPubMedCentralPubMed Eliassen AH et al (2012) Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104:1905–1916CrossRefPubMedCentralPubMed
18.
go back to reference Klaunig JE, Kamendulis LM (2004) The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 44:239–267CrossRefPubMed Klaunig JE, Kamendulis LM (2004) The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 44:239–267CrossRefPubMed
19.
20.
go back to reference Lee K-H et al (2010) Breast cancer and urinary biomarkers of polycyclic aromatic hydrocarbon and oxidative stress in the Shanghai Women’s Health Study. Cancer Epidemiol Biomark Prev 19:877–883CrossRef Lee K-H et al (2010) Breast cancer and urinary biomarkers of polycyclic aromatic hydrocarbon and oxidative stress in the Shanghai Women’s Health Study. Cancer Epidemiol Biomark Prev 19:877–883CrossRef
21.
go back to reference Fortner RT, Tworoger SS, Wu T, Eliassen AH (2013) Plasma florescent oxidation products and breast cancer risk: repeated measures in the Nurses’ Health Study. Breast Cancer Res Treat 141:307–316CrossRefPubMedCentralPubMed Fortner RT, Tworoger SS, Wu T, Eliassen AH (2013) Plasma florescent oxidation products and breast cancer risk: repeated measures in the Nurses’ Health Study. Breast Cancer Res Treat 141:307–316CrossRefPubMedCentralPubMed
22.
go back to reference Hankinson SE et al (1995) Alcohol, height, and adiposity in relation to estrogen and prolactin levels in postmenopausal women. J Natl Cancer Inst 87:1297–1302CrossRefPubMed Hankinson SE et al (1995) Alcohol, height, and adiposity in relation to estrogen and prolactin levels in postmenopausal women. J Natl Cancer Inst 87:1297–1302CrossRefPubMed
23.
go back to reference Tworoger SS, Sluss P, Hankinson SE (2006) Association between plasma prolactin concentrations and risk of breast cancer among predominately premenopausal women. Cancer Res 66:2476–2482CrossRefPubMed Tworoger SS, Sluss P, Hankinson SE (2006) Association between plasma prolactin concentrations and risk of breast cancer among predominately premenopausal women. Cancer Res 66:2476–2482CrossRefPubMed
24.
go back to reference Eliassen AH et al (2014) Plasma carotenoids and risk of breast cancer over 20 years of follow-up. Am J Clin Nutr 74:2919 Eliassen AH et al (2014) Plasma carotenoids and risk of breast cancer over 20 years of follow-up. Am J Clin Nutr 74:2919
25.
go back to reference El-Sohemy A et al (2002) Individual carotenoid concentrations in adipose tissue and plasma as biomarkers of dietary intake. Am J Clin Nutr 76:172–179PubMed El-Sohemy A et al (2002) Individual carotenoid concentrations in adipose tissue and plasma as biomarkers of dietary intake. Am J Clin Nutr 76:172–179PubMed
26.
go back to reference Wu T, Rifai N, Roberts LJ 2nd, Willett WC, Rimm EB (2004) Stability of measurements of biomarkers of oxidative stress in blood over 36 h. Cancer Epidemiol Biomark Prev 13:1399–1402 Wu T, Rifai N, Roberts LJ 2nd, Willett WC, Rimm EB (2004) Stability of measurements of biomarkers of oxidative stress in blood over 36 h. Cancer Epidemiol Biomark Prev 13:1399–1402
27.
go back to reference Rosner B, Cook N, Portman R, Daniels S, Falkner B (2008) Determination of blood pressure percentiles in normal-weight children: some methodological issues. Am J Epidemiol 167:653–666CrossRefPubMed Rosner B, Cook N, Portman R, Daniels S, Falkner B (2008) Determination of blood pressure percentiles in normal-weight children: some methodological issues. Am J Epidemiol 167:653–666CrossRefPubMed
28.
go back to reference De Bakker PIW et al (2005) Efficiency and power in genetic association studies. Nat Genet 37:1217–1223CrossRefPubMed De Bakker PIW et al (2005) Efficiency and power in genetic association studies. Nat Genet 37:1217–1223CrossRefPubMed
29.
go back to reference Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265CrossRefPubMed Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21:263–265CrossRefPubMed
30.
31.
go back to reference Lietz G, Lange J, Rimbach G (2010) Molecular and dietary regulation of beta, beta-carotene 15,15′-monooxygenase 1 (BCMO1). Arch Biochem Biophys 502:8–16CrossRefPubMed Lietz G, Lange J, Rimbach G (2010) Molecular and dietary regulation of beta, beta-carotene 15,15′-monooxygenase 1 (BCMO1). Arch Biochem Biophys 502:8–16CrossRefPubMed
32.
go back to reference Hendrickson SJ et al (2013) Plasma carotenoid- and retinol-weighted multi-SNP scores and risk of breast cancer in the National Cancer Institute Breast and Prostate Cancer Cohort Consortium. Cancer Epidemiol Biomark Prev 22:927–936CrossRef Hendrickson SJ et al (2013) Plasma carotenoid- and retinol-weighted multi-SNP scores and risk of breast cancer in the National Cancer Institute Breast and Prostate Cancer Cohort Consortium. Cancer Epidemiol Biomark Prev 22:927–936CrossRef
33.
go back to reference Rosner B (1983) Percentage points for a generalized ESD many-outlier procedure. Technometrics 25:165–172CrossRef Rosner B (1983) Percentage points for a generalized ESD many-outlier procedure. Technometrics 25:165–172CrossRef
34.
go back to reference Marshall RJ, Chisholm EM (1985) Hypothesis testing in the polychotomous logistic model with an application to detecting gastrointestinal cancer. Stat Med 4:337–344CrossRefPubMed Marshall RJ, Chisholm EM (1985) Hypothesis testing in the polychotomous logistic model with an application to detecting gastrointestinal cancer. Stat Med 4:337–344CrossRefPubMed
35.
go back to reference Hendrickson SJ et al (2012) β-Carotene 15,15′-monooxygenase 1 single nucleotide polymorphisms in relation to plasma carotenoid and retinol concentrations in women of European descent. Am J Clin Nutr 96:1379–1389CrossRefPubMedCentralPubMed Hendrickson SJ et al (2012) β-Carotene 15,15′-monooxygenase 1 single nucleotide polymorphisms in relation to plasma carotenoid and retinol concentrations in women of European descent. Am J Clin Nutr 96:1379–1389CrossRefPubMedCentralPubMed
36.
go back to reference Frei B (1994) Reactive oxygen species and antioxidant vitamins: mechanisms of action. Am J Med 97, 5S–13S; discussion 22S–28S Frei B (1994) Reactive oxygen species and antioxidant vitamins: mechanisms of action. Am J Med 97, 5S–13S; discussion 22S–28S
37.
go back to reference Wu T, Willett WC, Rifai N, Rimm EB (2007) Plasma fluorescent oxidation products as potential markers of oxidative stress for epidemiologic studies. Am J Epidemiol 166:552–560CrossRefPubMed Wu T, Willett WC, Rifai N, Rimm EB (2007) Plasma fluorescent oxidation products as potential markers of oxidative stress for epidemiologic studies. Am J Epidemiol 166:552–560CrossRefPubMed
38.
39.
go back to reference Wu T, Rifai N, Willett WC, Rimm EB (2007) Plasma fluorescent oxidation products: independent predictors of coronary heart disease in men. Am J Epidemiol 166:544–551CrossRefPubMed Wu T, Rifai N, Willett WC, Rimm EB (2007) Plasma fluorescent oxidation products: independent predictors of coronary heart disease in men. Am J Epidemiol 166:544–551CrossRefPubMed
40.
go back to reference Wang S et al (2009) Association between manganese superoxide dismutase (MnSOD) Val-9Ala polymorphism and cancer risk—A meta-analysis. Eur J Cancer 1990(45):2874–2881CrossRef Wang S et al (2009) Association between manganese superoxide dismutase (MnSOD) Val-9Ala polymorphism and cancer risk—A meta-analysis. Eur J Cancer 1990(45):2874–2881CrossRef
41.
go back to reference Tong S-Y et al (2009) Functional polymorphism in manganese superoxide dismutase and antioxidant status: their interactions on the risk of cervical intraepithelial neoplasia and cervical cancer. Gynecol Oncol 115:272–276CrossRefPubMed Tong S-Y et al (2009) Functional polymorphism in manganese superoxide dismutase and antioxidant status: their interactions on the risk of cervical intraepithelial neoplasia and cervical cancer. Gynecol Oncol 115:272–276CrossRefPubMed
42.
go back to reference Mikhak B et al (2008) Manganese superoxide dismutase (MnSOD) gene polymorphism, interactions with carotenoid levels and prostate cancer risk. Carcinogenesis 29:2335–2340CrossRefPubMedCentralPubMed Mikhak B et al (2008) Manganese superoxide dismutase (MnSOD) gene polymorphism, interactions with carotenoid levels and prostate cancer risk. Carcinogenesis 29:2335–2340CrossRefPubMedCentralPubMed
43.
go back to reference Ahn J et al (2006) Associations between catalase phenotype and genotype: modification by epidemiologic factors. Cancer Epidemiol Biomark Prev 15:1217–1222CrossRef Ahn J et al (2006) Associations between catalase phenotype and genotype: modification by epidemiologic factors. Cancer Epidemiol Biomark Prev 15:1217–1222CrossRef
44.
go back to reference Nadif R et al (2005) Association of CAT polymorphisms with catalase activity and exposure to environmental oxidative stimuli. Free Radic Res 39:1345–1350CrossRefPubMedCentralPubMed Nadif R et al (2005) Association of CAT polymorphisms with catalase activity and exposure to environmental oxidative stimuli. Free Radic Res 39:1345–1350CrossRefPubMedCentralPubMed
45.
go back to reference Bastaki M et al (2006) Genotype-activity relationship for Mn-superoxide dismutase, glutathione peroxidase 1 and catalase in humans. Pharmacogenet Genomics 16:279–286CrossRefPubMed Bastaki M et al (2006) Genotype-activity relationship for Mn-superoxide dismutase, glutathione peroxidase 1 and catalase in humans. Pharmacogenet Genomics 16:279–286CrossRefPubMed
46.
go back to reference Ahn J et al (2005) Associations between breast cancer risk and the catalase genotype, fruit and vegetable consumption, and supplement use. Am J Epidemiol 162:943–952CrossRefPubMed Ahn J et al (2005) Associations between breast cancer risk and the catalase genotype, fruit and vegetable consumption, and supplement use. Am J Epidemiol 162:943–952CrossRefPubMed
47.
go back to reference Quick SK et al (2008) Effect modification by catalase genotype suggests a role for oxidative stress in the association of hormone replacement therapy with postmenopausal breast cancer risk. Cancer Epidemiol Biomark Prev 17:1082–1087CrossRef Quick SK et al (2008) Effect modification by catalase genotype suggests a role for oxidative stress in the association of hormone replacement therapy with postmenopausal breast cancer risk. Cancer Epidemiol Biomark Prev 17:1082–1087CrossRef
48.
go back to reference Lietz G, Oxley A, Leung W, Hesketh J (2012) Single nucleotide polymorphisms upstream from the β-carotene 15,15′-monoxygenase gene influence provitamin A conversion efficiency in female volunteers. J Nutr 142:161S–165SCrossRefPubMed Lietz G, Oxley A, Leung W, Hesketh J (2012) Single nucleotide polymorphisms upstream from the β-carotene 15,15′-monoxygenase gene influence provitamin A conversion efficiency in female volunteers. J Nutr 142:161S–165SCrossRefPubMed
49.
go back to reference Leung WC et al (2009) Two common single nucleotide polymorphisms in the gene encoding beta-carotene 15,15′-monoxygenase alter beta-carotene metabolism in female volunteers. FASEB J 23:1041–1053CrossRefPubMed Leung WC et al (2009) Two common single nucleotide polymorphisms in the gene encoding beta-carotene 15,15′-monoxygenase alter beta-carotene metabolism in female volunteers. FASEB J 23:1041–1053CrossRefPubMed
50.
go back to reference Ferrucci L et al (2009) Common variation in the beta-carotene 15,15′-monooxygenase 1 gene affects circulating levels of carotenoids: a genome-wide association study. Am J Hum Genet 84:123–133CrossRefPubMedCentralPubMed Ferrucci L et al (2009) Common variation in the beta-carotene 15,15′-monooxygenase 1 gene affects circulating levels of carotenoids: a genome-wide association study. Am J Hum Genet 84:123–133CrossRefPubMedCentralPubMed
51.
go back to reference Kotsopoulos J et al (2010) Reproducibility of plasma and urine biomarkers among premenopausal and postmenopausal women from the Nurses’ Health Studies. Cancer Epidemiol Biomark Pre 19:938–946CrossRef Kotsopoulos J et al (2010) Reproducibility of plasma and urine biomarkers among premenopausal and postmenopausal women from the Nurses’ Health Studies. Cancer Epidemiol Biomark Pre 19:938–946CrossRef
Metadata
Title
Premenopausal plasma carotenoids, fluorescent oxidation products, and subsequent breast cancer risk in the nurses’ health studies
Authors
Julia S. Sisti
Sara Lindström
Peter Kraft
Rulla M. Tamimi
Bernard A. Rosner
Tianying Wu
Walter C. Willett
A. Heather Eliassen
Publication date
01-06-2015
Publisher
Springer US
Published in
Breast Cancer Research and Treatment / Issue 2/2015
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI
https://doi.org/10.1007/s10549-015-3391-6

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