Abstract
Background
Epidemiological evidence for the impact of fruit and vegetable intake on breast cancer risk among the Japanese populations is scarce.
Objective
The purpose of this study was to evaluate the association between fruit and vegetable intake and breast cancer risk among 47,289 Japanese women.
Design
The study was conducted under a population-based prospective cohort design. Dietary assessment was performed using a validated food frequency questionnaire. A Cox proportional hazards regression model was used to calculate relative risks (RRs) and their corresponding 95 % confidence intervals (CIs).
Results
During an average of 10.2 years of follow-up, 452 cases of breast cancer were newly diagnosed. No association with breast cancer risk was seen for intake of total fruits and vegetables, cruciferous vegetables, green-leaf vegetables, yellow vegetables, or tomato products in overall or postmenopausal women. Cruciferous vegetable intake was associated with a statistically significant decrease in risk of premenopausal breast cancer [multivariable-RRQ4 vs. Q1 = 0.64 (95 % CI = 0.38–1.10; p trend = .046)] and showed a marginally inverse association with ER+ PR+ tumors [RRper 100 g increment = 0.64 (95 % CI = 0.41–1.00)]. In contrast, positive associations were seen between intake of total fruits and citrus fruits and breast cancer risk in overall and premenopausal women. However, these associations for fruit were all attenuated with additional adjustment for vitamin C intake.
Conclusions
Our results suggest an overall null association between total fruit and vegetable intake and breast cancer risk. Intake of cruciferous vegetable showed a statistically significant association with a decreased risk of breast cancer among premenopausal women.
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Abbreviations
- BMI:
-
Body mass index
- CIs:
-
Confidence intervals
- ER:
-
Estrogen receptor
- EFH:
-
Exogenous female hormones
- FFQ:
-
Food frequency questionnaire
- The JPHC Study:
-
The Japan Public Health Center-based Prospective Study
- OC:
-
Oral contraceptive
- PR:
-
Progesterone receptor
- RR:
-
Relative risk
- SD:
-
Standard deviation
- DCN:
-
Death certificate notification
- DCO:
-
Death certificate only
References
Matsuda T, Marugame T, Kamo KI, Katanoda K, Ajiki W, Sobue T (2009) Cancer incidence and incidence rates in Japan in 2003: based on data from 13 population-based cancer registries in the Monitoring of Cancer Incidence in Japan (MCIJ) Project. Jpn J Clin Oncol 39(12):850–858
National Health and Nutrition Examination Survey (2006) Current status of the nations Health and Nutrition in Japan, 2004. Daiich Publisher, Tokyo
IARC (1998) Carotenoids, vol 2. World Health Organization: IARC Working Group on the Evaluation of Cancer-preventive Agents, Lyon
IARC (2003) Fruit and vegetables. IARC Press, Lyon
Smith-Warner SA, Spiegelman D, Yaun SS et al (2001) Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 285:769–776
van Gils CH, Peeters PH, Bueno-de-Mesquita HB et al (2005) Consumption of vegetables and fruits and risk of breast cancer. JAMA 293:183–193
World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington DC
World Health Organization / International Agency For Research on Cancer (2004) Cruciferous vegetables, isothiocyanates and indoles. IARC Press, Lyon
Terry P, Wolk A, Persson I, Magnusson C (2001) Brassica vegetables and breast cancer risk. JAMA 285:2975–2977
Pledgie-Tracy A, Sobolewski MD, Davidson NE (2007) Sulforaphane induces cell type-specific apoptosis in human breast cancer cell lines. Mol Cancer Ther 6:1013–1021
Olsen A, Tjonneland A, Thomsen BL et al (2003) Fruits and vegetables intake differentially affects estrogen receptor negative and positive breast cancer incidence rates. J Nutr 133(7):2342–2347
Gaudet MM, Britton JA, Kabat GC et al (2004) Fruits, vegetables, and micronutrients in relation to breast cancer modified by menopause and hormone receptor status. Cancer Epidemiol Biomarkers Prev 13:1485–1494
Lissowska J, Gaudet MM, Brinton LA et al (2008) Intake of fruits, and vegetables in relation to breast cancer risk by hormone receptor status. Breast Cancer Res Treat 107:113–117
Boggs DA, Palmer JR, Wise LA et al (2010) Fruit and vegetable intake in relation to risk of breast cancer in the Black Women’s Health Study. Am J Epidemiol 172:1268–1279
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 105:219–236
Food and Agriculture Organization of United Nation, Food balance sheets FAOSTAT (2009). http://faostat.fao.org/
Tsugane S, Sobue T (2001) Baseline survey of JPHC study–design and participation rate. Japan Public Health Center-based Prospective Study on Cancer and Cardiovascular Diseases. J Epidemiol 11:S24–S29
Tsubono Y, Takamori S, Kobayashi M et al (1996) A data-based approach for designing a semiquantitative food frequency questionnaire for a population-based prospective study in Japan. J Epidemiol 6:45–53
Tsugane S, Kobayashi M, Sasaki S (2003) Validity of the self-administered food frequency questionnaire used in the 5-year follow-up survey of the JPHC Study Cohort I: comparison with dietary records for main nutrients. J Epidemiol 13:S51–S56
The Ministry of Education, Culture, Sports, Science and Technology (2005) The Ministry of Education, Culture, Sports, Science and Technology (Fifth Revised and Enlarged Edition). www.mext.go.jp
Willett W (1998) Nutritional epidemiology, 2nd edition, 2nd edn. Oxford University Press, New York
Sasaki S, Kobayashi M, Tsugane S (2003) Validity of a self-administered food frequency questionnaire used in the 5-year follow-up survey of the JPHC Study Cohort I: comparison with dietary records for food groups. J Epidemiol 13:S57–S63
Sasaki S, Ishihara J, Tsugane S (2003) Reproducibility of a self-administered food frequency questionnaire used in the 5-year follow-up survey of the JPHC Study Cohort I to assess food and nutrient intake. J Epidemiol 13:S115–S124
World Health Organization (2000) International classification of diseases for oncology, 3rd edn. World Health Organization, Geneva
Korn EL, Graubard BI, Midthune D (1997) Time-to-event analysis of longitudinal follow-up of a survey: choice of the time-scale. Am J Epidemiol 145:72–80
Collett D (1999) Modeling survival data in medical researched. Chapman & Hall/CRC Press, LLC
Ambrosone CB, McCann SE, Freudenheim JL, Marshall JR, Zhang Y, Shields PG (2004) Breast cancer risk in premenopausal women is inversely associated with consumption of broccoli, a source of isothiocyanates, but is not modified by GST genotype. J Nutr 134:1134–1138
Meng Q, Yuan F, Goldberg ID, Rosen EM, Auborn K, Fan S (2000) Indole-3-carbinol is a negative regulator of estrogen receptor-alpha signaling in human tumor cells. J Nutr 130:2927–2931
Ju YH, Carlson KE, Sun J et al (2000) Estrogenic effects of extracts from cabbage, fermented cabbage, and acidified brussels sprouts on growth and gene expression of estrogen-dependent human breast cancer (MCF-7) cells. J Agric Food Chem 48:4628–4634
Wang TT, Milner MJ, Milner JA, Kim YS (2006) Estrogen receptor alpha as a target for indole-3-carbinol. J Nutr Biochem 17:659–664
Song JK, Bae JM (2013) Citrus fruit intake and breast cancer risk: a quantitative systematic review. J Breast Cancer 16:72–76
Bao PP, Shu XO, Zheng Y et al (2012) Fruit, vegetable, and animal food intake and breast cancer risk by hormone receptor status. Nutr Cancer 64:806–819
Kobayashi M, Sasaki S, Tsugane S (2003) Validity of a self-administered food frequency questionnaire used in the 5-year follow-up survey of the JPHC Study Cohort I to assess carotenoids and vitamin C intake: comparison with dietary records and blood level. J Epidemiol 13:S82–S91
Takahashi Y, Sasaki S, Tsugane S (2001) Development and validation of specific carotene food composition tables for use in nutritional epidemiologic studies for Japanese populations. J Epidemiol 11:266–275
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–S218
Acknowledgments
We thank all staff members in each study area and in the central offices for their cooperation and technical assistance. We also wish to thank the Iwate, Akita, Ibaraki, Niigata, Osaka, Kochi, Nagasaki and Okinawa Cancer Registries for their provision of incidence data. RS, MI, and ST designed the research; ST conducted research; RS analyzed data; RS wrote the paper; RS, MI and ST were primarily responsibility for final content. All authors read and approved the final manuscript. Our study was supported by grants-in-aid for Cancer Research from the Ministry of Health, Labour and Welfare of Japan, for Scientific Research on Priority Areas from the Ministry of Education, Culture, Sports, Science, and Technology of Japan, and for the 3rd Term Comprehensive 10-Year- Strategy for Cancer Control from the Ministry of Health, Labour and Welfare of Japan. RS received a Grant-in-Aid from the Japan Society for the Promotion of Science Fellowship (H23).
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The authors declare no conflict of interest related to this manuscript.
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Appendix
Appendix
Members of the Japan Public Health Center-based Prospective Study Group (principal investigator: S. Tsugane): S. Tsugane, M. Inoue, T. Sobue, and T. Hanaoka, National Cancer Center, Tokyo; J. Ogata, S. Baba, T. Mannami, A. Okayama, and Y. Kokubo, National Cardiovascular Center, Osaka; K. Miyakawa, F. Saito, A. Koizumi, Y. Sano, I. Hashimoto, and T. Ikuta, Iwate Prefectural Ninohe Public Health Center, Iwate; Y. Miyajima, N. Suzuki, S. Nagasawa, Y. Furusugi, and N. Nagai, Akita Prefectural Yokote Public Health Center, Akita; H. Sanada, Y. Hatayama, F. Kobayashi, H. Uchino, Y. Shirai, T. Kondo, R. Sasaki, Y. Watanabe, Y. Miyagawa, and Y. Kobayashi, Nagano Prefectural Saku Public Health Center, Nagano; Y. Kishimoto, E. Takara, T. Fukuyama, M. Kinjo, M. Irei, and H. Sakiyama, Okinawa Prefectural Chubu Public Health Center, Okinawa; K. Imoto, H. Yazawa, T. Seo, A. Seiko, F. Ito, and F. Shoji, Katsushika Public Health Center, Tokyo; A. Murata, K. Minato, K. Motegi, and T. Fujieda, Ibaraki Prefectural Mito Public Health Center, Ibaraki; K. Matsui, T. Abe, M. Katagiri, and M. Suzuki, Niigata Prefectural Kashiwazaki and Nagaoka Public Health Center, Niigata; M. Doi, A. Terao, Y. Ishikawa, and T. Tagami, Kochi Prefectural Chuo-higashi Public Health Center, Kochi; H. Sueta, H. Doi, M. Urata, N. Okamoto, and F. Ide, Nagasaki Prefectural Kamigoto Public Health Center, Nagasaki; H. Sakiyama, N. Onga, H. Takaesu, and M. Uehara, Okinawa Prefectural Miyako Public Health Center, Okinawa; F. Horii, I. Asano, H. Yamaguchi, K. Aoki, S. Maruyama, M. Ichii, and M. Takano, Osaka Prefectural Suita Public Health Center, Osaka; S. Matsushima and S. Natsukawa, Saku General Hospital, Nagano; K. Suzuki, Research Institute for Brain and Blood Vessels Akita, Akita; M. Kabuto, National Institute for Environmental Studies, Ibaraki; M. Yamaguchi, Y. Matsumura, S. Sasaki, and S. Watanabe, National Institute of Health and Nutrition, Tokyo; M. Noda, International Medical Center of Japan, Tokyo; S. Tominaga, Aichi Cancer Center Research Institute, Aichi; H. Shimizu, Sakihae Institute, Gifu; M. Iida, W. Ajiki, and A. Ioka, Osaka Medical Center for Cancer and Cardiovascular Disease, Osaka; S. Sato, Osaka Medical Center for Health Science and Promotion, Osaka; Y. Tsubono, Tohoku University, Miyagi; K. Nakamura, Niigata University, Niigata; Y. Honda, K. Yamagishi, and S. Sakurai, Tsukuba University, Ibaraki; M. Akabane, Tokyo University of Agriculture, Tokyo; T. Kadowaki, Tokyo University, Tokyo; Y. Kawaguchi, Tokyo Medical and Dental University, Tokyo; Y. Takashima, Kyorin University, Tokyo; H. Sugimura, Hamamatsu University, Shizuoka; H. Iso, Osaka University, Osaka; E. Maruyama, Kobe University, Hyogo; M. Konishi, K. Okada, and I. Saito, Ehime University, Ehime; N. Yasuda, Kochi University, Kochi; and S. Kono, Kyushu University, Fukuoka.
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Suzuki, R., Iwasaki, M., Hara, A. et al. Fruit and vegetable intake and breast cancer risk defined by estrogen and progesterone receptor status: the Japan Public Health Center-based Prospective Study. Cancer Causes Control 24, 2117–2128 (2013). https://doi.org/10.1007/s10552-013-0289-7
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DOI: https://doi.org/10.1007/s10552-013-0289-7