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Published in: Cancer Causes & Control 9/2015

01-09-2015 | Original paper

Plasma carotenoids and breast cancer risk in the Cancer Prevention Study II Nutrition Cohort

Authors: Ying Wang, Susan M. Gapstur, Mia M. Gaudet, Jeremy D. Furtado, Hannia Campos, Marjorie L. McCullough

Published in: Cancer Causes & Control | Issue 9/2015

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Abstract

Purpose

Several circulating carotenoids have been inversely associated with postmenopausal breast cancer risk in large cohort studies and a pooled analysis. Whether associations differ by tumor or participant characteristics remains unclear. We investigated the associations of plasma carotenoids with postmenopausal breast cancer risk overall and by estrogen receptor (ER) status, tumor stage, smoking status, and body mass index, in a case–control study nested in the Cancer Prevention Study II Nutrition Cohort.

Methods

A total of 496 invasive breast cancer cases diagnosed between blood draw in 1998–2001 and June 30, 2007 and matched 1:1 with controls on race, birth date, and blood draw date were included. Multivariable-adjusted conditional and unconditional logistic regression models were used to calculate odds ratios (ORs) and 95 % confidence intervals (CIs).

Results

Plasma α-carotene above the lowest quartile was associated with significant 40–43 % lower risk of invasive breast cancer risk (fourth vs. first quartile OR 0.60, 95 % CI 0.41–0.87, P-trend = 0.037) after adjustment for multiple covariates. This inverse association was strengthened after further adjustment for other plasma carotenoids and total fruit and vegetable intake (fourth vs. first quartile OR 0.50, 95 % CI 0.29–0.85, P-trend = 0.041). Other plasma carotenoids or total carotenoids were not associated with breast cancer risk. The inverse association of α-carotene with breast cancer remained for ER+, but not for ER− tumors, although test for heterogeneity was not statistically significant (P-heterogeneity = 0.49).

Conclusions

These results suggest that higher plasma α-carotene is associated with lower risk of invasive breast cancer.
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Literature
1.
go back to reference Maiani G, Caston MJ, Catasta G et al (2009) Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Mol Nutr Food Res 53(Suppl 2):S194–S218CrossRefPubMed Maiani G, Caston MJ, Catasta G et al (2009) Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Mol Nutr Food Res 53(Suppl 2):S194–S218CrossRefPubMed
2.
go back to reference Hozawa A, Jacobs DR Jr, Steffes MW, Gross MD, Steffen LM, Lee DH (2007) Relationships of circulating carotenoid concentrations with several markers of inflammation, oxidative stress, and endothelial dysfunction: the Coronary Artery Risk Development in Young Adults (CARDIA)/Young Adult Longitudinal Trends in Antioxidants (YALTA) study. Clin Chem 53:447–455PubMedCentralCrossRefPubMed Hozawa A, Jacobs DR Jr, Steffes MW, Gross MD, Steffen LM, Lee DH (2007) Relationships of circulating carotenoid concentrations with several markers of inflammation, oxidative stress, and endothelial dysfunction: the Coronary Artery Risk Development in Young Adults (CARDIA)/Young Adult Longitudinal Trends in Antioxidants (YALTA) study. Clin Chem 53:447–455PubMedCentralCrossRefPubMed
3.
go back to reference Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49:1603–1616PubMedCentralCrossRefPubMed Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49:1603–1616PubMedCentralCrossRefPubMed
4.
go back to reference Tang XH, Gudas LJ (2011) Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol 6:345–364CrossRefPubMed Tang XH, Gudas LJ (2011) Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol 6:345–364CrossRefPubMed
5.
go back to reference Hu F, Wang Yi B, Zhang W et al (2012) Carotenoids and breast cancer risk: a meta-analysis and meta-regression. Breast Cancer Res Treat 131:239–253CrossRefPubMed Hu F, Wang Yi B, Zhang W et al (2012) Carotenoids and breast cancer risk: a meta-analysis and meta-regression. Breast Cancer Res Treat 131:239–253CrossRefPubMed
6.
go back to reference Zhang X, Spiegelman D, Baglietto L 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 95:713–725PubMedCentralCrossRefPubMed Zhang X, Spiegelman D, Baglietto L 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 95:713–725PubMedCentralCrossRefPubMed
7.
go back to reference Aune D, Chan DS, Vieira AR 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, Chan DS, Vieira AR 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
8.
go back to reference Jung S, Spiegelman D, Baglietto L et al (2013) Fruit and vegetable intake and risk of breast cancer by hormone receptor status. J Natl Cancer Inst 105:219–236PubMedCentralCrossRefPubMed Jung S, Spiegelman D, Baglietto L et al (2013) Fruit and vegetable intake and risk of breast cancer by hormone receptor status. J Natl Cancer Inst 105:219–236PubMedCentralCrossRefPubMed
9.
go back to reference Aune D, Chan DS, Vieira AR 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, Chan DS, Vieira AR 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
10.
go back to reference Eliassen AH, Hendrickson SJ, Brinton LA et al (2012) Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104:1905–1916PubMedCentralCrossRefPubMed Eliassen AH, Hendrickson SJ, Brinton LA et al (2012) Circulating carotenoids and risk of breast cancer: pooled analysis of eight prospective studies. J Natl Cancer Inst 104:1905–1916PubMedCentralCrossRefPubMed
11.
go back to reference Wallstrom P, Wirfalt E, Lahmann PH, Gullberg B, Janzon L, Berglund G (2001) Serum concentrations of beta-carotene and alpha-tocopherol are associated with diet, smoking, and general and central adiposity. Am J Clin Nutr 73:777–785PubMed Wallstrom P, Wirfalt E, Lahmann PH, Gullberg B, Janzon L, Berglund G (2001) Serum concentrations of beta-carotene and alpha-tocopherol are associated with diet, smoking, and general and central adiposity. Am J Clin Nutr 73:777–785PubMed
12.
go back to reference Stryker WS, Kaplan LA, Stein EA, Stampfer MJ, Sober A, Willett WC (1988) The relation of diet, cigarette smoking, and alcohol consumption to plasma beta-carotene and alpha-tocopherol levels. Am J Epidemiol 127:283–296PubMed Stryker WS, Kaplan LA, Stein EA, Stampfer MJ, Sober A, Willett WC (1988) The relation of diet, cigarette smoking, and alcohol consumption to plasma beta-carotene and alpha-tocopherol levels. Am J Epidemiol 127:283–296PubMed
13.
go back to reference Calle EE, Rodriguez C, Jacobs EJ et al (2002) The American Cancer Society Cancer Prevention Study II Nutrition Cohort: rationale, study design, and baseline characteristics. Cancer 94:2490–2501CrossRefPubMed Calle EE, Rodriguez C, Jacobs EJ et al (2002) The American Cancer Society Cancer Prevention Study II Nutrition Cohort: rationale, study design, and baseline characteristics. Cancer 94:2490–2501CrossRefPubMed
14.
go back to reference El-Sohemy A, Baylin A, Kabagambe E, Ascherio A, Spiegelman D, Campos H (2002) Individual carotenoid concentrations in adipose tissue and plasma as biomarkers of dietary intake. Am J Clin Nutr 76:172–179PubMed El-Sohemy A, Baylin A, Kabagambe E, Ascherio A, Spiegelman D, Campos H (2002) Individual carotenoid concentrations in adipose tissue and plasma as biomarkers of dietary intake. Am J Clin Nutr 76:172–179PubMed
15.
go back to reference Holden JM, Eldridge AL, Beecher GR et al (1999) Carotenoid content of US foods: an update of the database. J Food Compos Anal 12:169–196 Holden JM, Eldridge AL, Beecher GR et al (1999) Carotenoid content of US foods: an update of the database. J Food Compos Anal 12:169–196
16.
go back to reference Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27PubMed Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124:17–27PubMed
17.
go back to reference Wang M, Kuchiba A, Ogino S (2015) A meta-regression method for studying etiologic heterogeneity across disease subtypes classified by multiple biomarkers. Am J Epidemiol (in press) Wang M, Kuchiba A, Ogino S (2015) A meta-regression method for studying etiologic heterogeneity across disease subtypes classified by multiple biomarkers. Am J Epidemiol (in press)
18.
go back to reference Kleinbaum DG, Kupper LL, Muller KE (2007) Applied regression analysis and other multivariable methods. Cengage Learning, Belmont Kleinbaum DG, Kupper LL, Muller KE (2007) Applied regression analysis and other multivariable methods. Cengage Learning, Belmont
19.
go back to reference Dorgan JF, Sowell A, Swanson CA et al (1998) Relationships of serum carotenoids, retinol, alpha-tocopherol, and selenium with breast cancer risk: results from a prospective study in Columbia, Missouri (United States). Cancer Causes Control 9:89–97CrossRefPubMed Dorgan JF, Sowell A, Swanson CA et al (1998) Relationships of serum carotenoids, retinol, alpha-tocopherol, and selenium with breast cancer risk: results from a prospective study in Columbia, Missouri (United States). Cancer Causes Control 9:89–97CrossRefPubMed
20.
go back to reference Hulten K, Van Kappel AL, Winkvist A et al (2001) Carotenoids, alpha-tocopherols, and retinol in plasma and breast cancer risk in northern Sweden. Cancer Causes Control 12:529–537CrossRefPubMed Hulten K, Van Kappel AL, Winkvist A et al (2001) Carotenoids, alpha-tocopherols, and retinol in plasma and breast cancer risk in northern Sweden. Cancer Causes Control 12:529–537CrossRefPubMed
21.
go back to reference Toniolo P, Van Kappel AL, Akhmedkhanov A et al (2001) Serum carotenoids and breast cancer. Am J Epidemiol 153:1142–1147CrossRefPubMed Toniolo P, Van Kappel AL, Akhmedkhanov A et al (2001) Serum carotenoids and breast cancer. Am J Epidemiol 153:1142–1147CrossRefPubMed
22.
go back to reference Sato R, Helzlsouer KJ, Alberg AJ, Hoffman SC, Norkus EP, Comstock GW (2002) Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 11:451–457PubMed Sato R, Helzlsouer KJ, Alberg AJ, Hoffman SC, Norkus EP, Comstock GW (2002) Prospective study of carotenoids, tocopherols, and retinoid concentrations and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 11:451–457PubMed
23.
go back to reference Tamimi RM, Hankinson SE, Campos H et al (2005) Plasma carotenoids, retinol, and tocopherols and risk of breast cancer. Am J Epidemiol 161:153–160CrossRefPubMed Tamimi RM, Hankinson SE, Campos H et al (2005) Plasma carotenoids, retinol, and tocopherols and risk of breast cancer. Am J Epidemiol 161:153–160CrossRefPubMed
24.
go back to reference Sesso HD, Buring JE, Zhang SM, Norkus EP, Gaziano JM (2005) Dietary and plasma lycopene and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 14:1074–1081CrossRefPubMed Sesso HD, Buring JE, Zhang SM, Norkus EP, Gaziano JM (2005) Dietary and plasma lycopene and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 14:1074–1081CrossRefPubMed
25.
go back to reference Dorjgochoo T, Gao YT, Chow WH et al (2009) Plasma carotenoids, tocopherols, retinol and breast cancer risk: results from the Shanghai Women Health Study (SWHS). Breast Cancer Res Treat 117:381–389PubMedCentralCrossRefPubMed Dorjgochoo T, Gao YT, Chow WH et al (2009) Plasma carotenoids, tocopherols, retinol and breast cancer risk: results from the Shanghai Women Health Study (SWHS). Breast Cancer Res Treat 117:381–389PubMedCentralCrossRefPubMed
26.
go back to reference Epplein M, Shvetsov YB, Wilkens LR 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 11:R49PubMedCentralCrossRefPubMed Epplein M, Shvetsov YB, Wilkens LR 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 11:R49PubMedCentralCrossRefPubMed
27.
go back to reference Kabat GC, Kim M, Adams-Campbell LL 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 90:162–169PubMedCentralCrossRefPubMed Kabat GC, Kim M, Adams-Campbell LL 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 90:162–169PubMedCentralCrossRefPubMed
28.
go back to reference Maillard V, Kuriki K, Lefebvre B et al (2010) Serum carotenoid, tocopherol and retinol concentrations and breast cancer risk in the E3N-EPIC study. Int J Cancer 127:1188–1196CrossRefPubMed Maillard V, Kuriki K, Lefebvre B et al (2010) Serum carotenoid, tocopherol and retinol concentrations and breast cancer risk in the E3N-EPIC study. Int J Cancer 127:1188–1196CrossRefPubMed
29.
go back to reference Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 109:1721–1728CrossRefPubMed Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 109:1721–1728CrossRefPubMed
30.
go back to reference Gaudet MM, Gapstur SM, Sun J, Diver WR, Hannan LM, Thun MJ (2013) Active smoking and breast cancer risk: original cohort data and meta-analysis. J Natl Cancer Inst 105:515–525CrossRefPubMed Gaudet MM, Gapstur SM, Sun J, Diver WR, Hannan LM, Thun MJ (2013) Active smoking and breast cancer risk: original cohort data and meta-analysis. J Natl Cancer Inst 105:515–525CrossRefPubMed
31.
go back to reference Marangon K, Herbeth B, Lecomte E et al (1998) Diet, antioxidant status, and smoking habits in French men. Am J Clin Nutr 67:231–239PubMed Marangon K, Herbeth B, Lecomte E et al (1998) Diet, antioxidant status, and smoking habits in French men. Am J Clin Nutr 67:231–239PubMed
32.
go back to reference Ross MA, Crosley LK, Brown KM et al (1995) Plasma concentrations of carotenoids and antioxidant vitamins in Scottish males: influences of smoking. Eur J Clin Nutr 49:861–865PubMed Ross MA, Crosley LK, Brown KM et al (1995) Plasma concentrations of carotenoids and antioxidant vitamins in Scottish males: influences of smoking. Eur J Clin Nutr 49:861–865PubMed
33.
go back to reference Albanes D, Virtamo J, Taylor PR, Rautalahti M, Pietinen P, Heinonen OP (1997) Effects of supplemental beta-carotene, cigarette smoking, and alcohol consumption on serum carotenoids in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Am J Clin Nutr 66:366–372PubMed Albanes D, Virtamo J, Taylor PR, Rautalahti M, Pietinen P, Heinonen OP (1997) Effects of supplemental beta-carotene, cigarette smoking, and alcohol consumption on serum carotenoids in the Alpha-Tocopherol, Beta-Carotene Cancer Prevention Study. Am J Clin Nutr 66:366–372PubMed
34.
go back to reference Heinonen OP, Albanes D (1994) The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. The alpha-tocopherol, beta carotene cancer prevention study group. N Engl J Med 330:1029–1035 Heinonen OP, Albanes D (1994) The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. The alpha-tocopherol, beta carotene cancer prevention study group. N Engl J Med 330:1029–1035
35.
go back to reference Omenn GS, Goodman GE, Thornquist MD et al (1996) Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med 334:1150–1155CrossRefPubMed Omenn GS, Goodman GE, Thornquist MD et al (1996) Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med 334:1150–1155CrossRefPubMed
36.
go back to reference Pradhan AD, Manson JE, Rossouw JE et al (2002) Inflammatory biomarkers, hormone replacement therapy, and incident coronary heart disease: prospective analysis from the Women’s Health Initiative observational study. JAMA 288:980–987CrossRefPubMed Pradhan AD, Manson JE, Rossouw JE et al (2002) Inflammatory biomarkers, hormone replacement therapy, and incident coronary heart disease: prospective analysis from the Women’s Health Initiative observational study. JAMA 288:980–987CrossRefPubMed
Metadata
Title
Plasma carotenoids and breast cancer risk in the Cancer Prevention Study II Nutrition Cohort
Authors
Ying Wang
Susan M. Gapstur
Mia M. Gaudet
Jeremy D. Furtado
Hannia Campos
Marjorie L. McCullough
Publication date
01-09-2015
Publisher
Springer International Publishing
Published in
Cancer Causes & Control / Issue 9/2015
Print ISSN: 0957-5243
Electronic ISSN: 1573-7225
DOI
https://doi.org/10.1007/s10552-015-0614-4

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