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Dairy food and nutrient intake in different life periods in relation to risk of ovarian cancer

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Abstract

Purpose

High lactose intake has been suggested to increase epithelial ovarian cancer (EOC) risk. We evaluated the association between lactose consumed during specific life periods (high school, premenopause, and postmenopause) and later risk of EOC.

Methods

We assessed the association of dairy food and nutrient intake with risk of EOC during 28 years of follow-up including 764 cases in the Nurses’ Health Study (NHS) and NHSII. Cox proportional hazards regression was used to model the hazard ratios (HRs) and 95 % confidence intervals (CIs) for EOC across categories of dairy food or nutrient intake. We examined dietary intake in adulthood overall, as well as during premenopausal/postmenopausal years and high school.

Results

In analyses of the highest versus lowest cumulative average intake in adulthood, we observed a non-significant inverse association with skim milk intake (HR 0.76, 95 % CI 0.54–1.06, p trend = 0.05), a non-significant inverse association with lactose intake (HR 0.87, 95 % CI 0.69–1.11, p trend = 0.22) and no association with consumption of whole milk, dairy calcium, or dairy fat. Similar risk estimates were observed for dairy food/nutrient intake during high school, premenopause or postmenopause. Lactose intake in adulthood was inversely associated with risk of endometrioid EOC (HR 0.32, 95 % CI 0.16–0.65, p trend < 0.001).

Conclusions

These findings do not support the hypothesis that higher lactose intake increases EOC risk. The inverse association with endometrioid tumors deserves further study.

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References

  1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–2917

    Article  CAS  PubMed  Google Scholar 

  2. Cramer DW, Harlow BL, Willett WC, Welch WR, Bell DA, Scully RE, Ng WG, Knapp RC (1989) Galactose consumption and metabolism in relation to the risk of ovarian cancer. Lancet 2(8654):66–71

    Article  CAS  PubMed  Google Scholar 

  3. Chen YT, Mattison DR, Feigenbaum L, Fukui H, Schulman JD (1981) Reduction in oocyte number following prenatal exposure to a diet high in galactose. Science 214(4525):1145–1147

    Article  CAS  PubMed  Google Scholar 

  4. Swartz WJ, Mattison DR (1988) Galactose inhibition of ovulation in mice. Fertil Steril 49(3):522–526

    CAS  PubMed  Google Scholar 

  5. Genkinger JM, Hunter DJ, Spiegelman D, Anderson KE, Arslan A, Beeson WL, Buring JE, Fraser GE, Freudenheim JL, Goldbohm RA, Hankinson SE, Jacobs DR Jr, Koushik A, Lacey JV Jr, Larsson SC, Leitzmann M, McCullough ML, Miller AB, Rodriguez C, Rohan TE, Schouten LJ, Shore R, Smit E, Wolk A, Zhang SM, Smith-Warner SA (2006) Dairy products and ovarian cancer: a pooled analysis of 12 cohort studies. Cancer Epidemiol Biomark Prev 15(2):364–372

    Article  Google Scholar 

  6. Larsson SC, Orsini N, Wolk A (2006) Milk, milk products and lactose intake and ovarian cancer risk: a meta-analysis of epidemiological studies. Int J Cancer 118(2):431–441

    Article  CAS  PubMed  Google Scholar 

  7. Fairfield KM, Hunter DJ, Colditz GA, Fuchs CS, Cramer DW, Speizer FE, Willett WC, Hankinson SE (2004) A prospective study of dietary lactose and ovarian cancer. Int J Cancer 110(2):271–277

    Article  CAS  PubMed  Google Scholar 

  8. Gates MA, Rosner BA, Hecht JL, Tworoger SS (2010) Risk factors for epithelial ovarian cancer by histologic subtype. Am J Epidemiol 171(1):45–53

    Article  PubMed Central  PubMed  Google Scholar 

  9. Kurian AW, Balise RR, McGuire V, Whittemore AS (2005) Histologic types of epithelial ovarian cancer: have they different risk factors? Gynecol Oncol 96(2):520–530

    Article  PubMed  Google Scholar 

  10. Yang HP, Trabert B, Murphy MA, Sherman ME, Sampson JN, Brinton LA, Hartge P, Hollenbeck A, Park Y, Wentzensen N (2012) Ovarian cancer risk factors by histologic subtypes in the NIH-AARP diet and health study. Int J Cancer 131(4):938–948

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Merritt MA, Cramer DW, Vitonis AF, Titus LJ, Terry KL (2013) Dairy foods and nutrients in relation to risk of ovarian cancer and major histological subtypes. Int J Cancer 132(5):1114–1124

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Lee JE, Willett WC, Fuchs CS, Smith-Warner SA, Wu K, Ma J, Giovannucci E (2011) Folate intake and risk of colorectal cancer and adenoma: modification by time. Am J Clin Nutr 93(4):817–825

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Cho E, Chen WY, Hunter DJ, Stampfer MJ, Colditz GA, Hankinson SE, Willett WC (2006) Red meat intake and risk of breast cancer among premenopausal women. Arch Intern Med 166(20):2253–2259

    Article  PubMed  Google Scholar 

  14. Linos E, Willett WC (2007) Diet and breast cancer risk reduction. J Natl Compr Canc Netw 5(8):711–718

    PubMed  Google Scholar 

  15. Linos E, Willett WC, Cho E, Colditz G, Frazier LA (2008) Red meat consumption during adolescence among premenopausal women and risk of breast cancer. Cancer Epidemiol Biomark Prev 17(8):2146–2151

    Article  Google Scholar 

  16. Missmer SA, Smith-Warner SA, Spiegelman D, Yaun SS, Adami HO, Beeson WL, van den Brandt PA, Fraser GE, Freudenheim JL, Goldbohm RA, Graham S, Kushi LH, Miller AB, Potter JD, Rohan TE, Speizer FE, Toniolo P, Willett WC, Wolk A, Zeleniuch-Jacquotte A, Hunter DJ (2002) Meat and dairy food consumption and breast cancer: a pooled analysis of cohort studies. Int J Epidemiol 31(1):78–85

    Article  PubMed  Google Scholar 

  17. Colditz GA, Hankinson SE (2005) The Nurses’ Health Study: lifestyle and health among women. Nat Rev Cancer 5(5):388–396

    Article  CAS  PubMed  Google Scholar 

  18. Rockhill B, Willett WC, Hunter DJ, Manson JE, Hankinson SE, Spiegelman D, Colditz GA (1998) Physical activity and breast cancer risk in a cohort of young women. J Natl Cancer Inst 90(15):1155–1160

    Article  CAS  PubMed  Google Scholar 

  19. Rimm EB, Giovannucci EL, Stampfer MJ, Colditz GA, Litin LB, Willett WC (1992) Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals. Am J Epidemiol 135(10):1114–1126 discussion 1127–1136

    CAS  PubMed  Google Scholar 

  20. Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C, Witschi J, Hennekens CH, Speizer FE (1985) Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 122(1):51–65

    CAS  PubMed  Google Scholar 

  21. Salvini S, Hunter DJ, Sampson L, Stampfer MJ, Colditz GA, Rosner B, Willett WC (1989) Food-based validation of a dietary questionnaire: the effects of week-to-week variation in food consumption. Int J Epidemiol 18(4):858–867

    Article  CAS  PubMed  Google Scholar 

  22. U.S. Department of Agriculture Agricultural Research Service (2011) USDA National Nutrient Database for Standard Reference

  23. Maruti SS, Feskanich D, Colditz GA, Frazier AL, Sampson LA, Michels KB, Hunter DJ, Spiegelman D, Willett WC (2005) Adult recall of adolescent diet: reproducibility and comparison with maternal reporting. Am J Epidemiol 161(1):89–97

    Article  PubMed Central  PubMed  Google Scholar 

  24. Frazier AL, Willett WC, Colditz GA (1995) Reproducibility of recall of adolescent diet: Nurses’ Health Study (United States). Cancer Causes Control 6(6):499–506

    Article  CAS  PubMed  Google Scholar 

  25. Tworoger SS, Hecht JL, Giovannucci E, Hankinson SE (2006) Intake of folate and related nutrients in relation to risk of epithelial ovarian cancer. Am J Epidemiol 163(12):1101–1111

    Article  PubMed  Google Scholar 

  26. Zhang X, Lee JE, Ma J, Je Y, Wu K, Willett WC, Fuchs CS, Giovannucci EL (2012) Prospective cohort studies of vitamin B-6 intake and colorectal cancer incidence: modification by time? Am J Clin Nutr 96(4):874–881

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124(1):17–27

    CAS  PubMed  Google Scholar 

  28. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188

    Article  CAS  PubMed  Google Scholar 

  29. Glynn RJ, Rosner B (2004) Methods to evaluate risks for composite end points and their individual components. J Clin Epidemiol 57(2):113–122

    Article  PubMed  Google Scholar 

  30. Poole EM, Merritt MA, Jordan SJ, Yang HP, Hankinson SE, Park Y, Rosner B, Webb PM, Cramer DW, Wentzensen N, Terry KL, Tworoger SS (2013) Hormonal and reproductive risk factors for epithelial ovarian cancer by tumor aggressiveness. Cancer Epidemiol Biomark Prev 22(3):429–437

    Article  CAS  Google Scholar 

  31. Cramer D, Welch WR (1983) Determinants of ovarian cancer risk. II. Inferences regarding pathogenesis. J Natl Cancer Inst 71(4):717–721

    CAS  PubMed  Google Scholar 

  32. Koralek DO, Bertone-Johnson ER, Leitzmann MF, Sturgeon SR, Lacey JV Jr, Schairer C, Schatzkin A (2006) Relationship between calcium, lactose, vitamin D, and dairy products and ovarian cancer. Nutr Cancer 56(1):22–30

    Article  CAS  PubMed  Google Scholar 

  33. Mommers M, Schouten LJ, Goldbohm RA, van den Brandt PA (2006) Dairy consumption and ovarian cancer risk in the Netherlands Cohort Study on diet and cancer. Br J Cancer 94(1):165–170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Kushi LH, Mink PJ, Folsom AR, Anderson KE, Zheng W, Lazovich D, Sellers TA (1999) Prospective study of diet and ovarian cancer. Am J Epidemiol 149(1):21–31

    Article  CAS  PubMed  Google Scholar 

  35. Larsson SC, Bergkvist L, Wolk A (2004) Milk and lactose intakes and ovarian cancer risk in the Swedish Mammography Cohort. Am J Clin Nutr 80(5):1353–1357

    CAS  PubMed  Google Scholar 

  36. Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM, Nagle CM, Doherty JA, Cushing-Haugen KL, Wicklund KG, Chang-Claude J, Hein R, Lurie G, Wilkens LR, Carney ME, Goodman MT, Moysich K, Kjaer SK, Hogdall E, Jensen A, Goode EL, Fridley BL, Larson MC, Schildkraut JM, Palmieri RT, Cramer DW, Terry KL, Vitonis AF, Titus LJ, Ziogas A, Brewster W, Anton-Culver H, Gentry-Maharaj A, Ramus SJ, Anderson AR, Brueggmann D, Fasching PA, Gayther SA, Huntsman DG, Menon U, Ness RB, Pike MC, Risch H, Wu AH, Berchuck A (2012) Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol 13(4):385–394

    Article  PubMed Central  PubMed  Google Scholar 

  37. Merritt MA, De Pari M, Vitonis AF, Titus LJ, Cramer DW, Terry KL (2013) Reproductive characteristics in relation to ovarian cancer risk by histologic pathways. Hum Reprod 28(5):1406–1417

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Somigliana E, Vigano P, Parazzini F, Stoppelli S, Giambattista E, Vercellini P (2006) Association between endometriosis and cancer: a comprehensive review and a critical analysis of clinical and epidemiological evidence. Gynecol Oncol 101(2):331–341

    Article  PubMed  Google Scholar 

  39. Wiegand KC, Shah SP, Al-Agha OM, Zhao Y, Tse K, Zeng T, Senz J, McConechy MK, Anglesio MS, Kalloger SE, Yang W, Heravi-Moussavi A, Giuliany R, Chow C, Fee J, Zayed A, Prentice L, Melnyk N, Turashvili G, Delaney AD, Madore J, Yip S, McPherson AW, Ha G, Bell L, Fereday S, Tam A, Galletta L, Tonin PN, Provencher D, Miller D, Jones SJ, Moore RA, Morin GB, Oloumi A, Boyd N, Aparicio SA, Shih IM, Mes-Masson AM, Bowtell DD, Hirst M, Gilks B, Marra MA, Huntsman DG (2010) ARID1A mutations in endometriosis-associated ovarian carcinomas. N Engl J Med 363(16):1532–1543

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  40. Harris HR, Chavarro JE, Malspeis S, Willett WC, Missmer SA (2013) Dairy-food, calcium, magnesium, and vitamin d intake and endometriosis: a prospective cohort study. Am J Epidemiol 177(5):420–430

    Article  PubMed Central  PubMed  Google Scholar 

  41. Trabert B, Peters U, De Roos AJ, Scholes D, Holt VL (2011) Diet and risk of endometriosis in a population-based case–control study. Br J Nutr 105(3):459–467

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Parazzini F, Chiaffarino F, Surace M, Chatenoud L, Cipriani S, Chiantera V, Benzi G, Fedele L (2004) Selected food intake and risk of endometriosis. Hum Reprod 19(8):1755–1759

    Article  CAS  PubMed  Google Scholar 

  43. Zemel MB, Sun X (2008) Dietary calcium and dairy products modulate oxidative and inflammatory stress in mice and humans. J Nutr 138(6):1047–1052

    CAS  PubMed  Google Scholar 

  44. Hartmann S, Lacorn M, Steinhart H (1998) Natural occurrence of steroid hormones in food. Food Chem 62(1):7–20

    Article  CAS  Google Scholar 

  45. Crosignani P, Olive D, Bergqvist A, Luciano A (2006) Advances in the management of endometriosis: an update for clinicians. Hum Reprod Update 12(2):179–189

    Article  CAS  PubMed  Google Scholar 

  46. Nagle CM, Bain CJ, Green AC, Webb PM (2008) The influence of reproductive and hormonal factors on ovarian cancer survival. Int J Gynecol Cancer 18(3):407–413

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank the participants and staff of the NHS and NHSII cohorts for their dedication to these studies and their contribution to this research. The authors thank the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA and WY. This research was supported by the National Cancer Institute, National Institutes of Health Grants P01 CA87969 and R01 CA50385 and training Grants to M.A.M. (R25 CA098566) and E.M.P. (T32 CA009001).

Conflict of interest

The authors declare that they have no conflict of interest.

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Author notes

  1. Melissa A. Merritt

    Present address: Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, Norfolk Place, London, W2 1PG, UK

Authors and Affiliations

  1. Department of Epidemiology, Harvard School of Public Health, 677 Huntington Ave., Boston, MA, 02115, USA

    Melissa A. Merritt, Elizabeth M. Poole, Susan E. Hankinson, Walter C. Willett & Shelley S. Tworoger

  2. OB/GYN Epidemiology Center, Brigham and Women’s Hospital, Harvard Medical School, 221 Longwood Ave., Boston, MA, 02115, USA

    Melissa A. Merritt

  3. Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, 450 Brookline Ave, Boston, MA, 02215, USA

    Melissa A. Merritt

  4. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA, 02115, USA

    Elizabeth M. Poole, Susan E. Hankinson, Walter C. Willett & Shelley S. Tworoger

  5. Division of Biostatistics and Epidemiology, University of Massachusetts, 715 North Pleasant St., Amherst, MA, 01003, USA

    Susan E. Hankinson

  6. Department of Nutrition, Harvard School of Public Health, 677 Huntington Ave., Boston, MA, 02115, USA

    Walter C. Willett

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Correspondence to Melissa A. Merritt.

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Merritt, M.A., Poole, E.M., Hankinson, S.E. et al. Dairy food and nutrient intake in different life periods in relation to risk of ovarian cancer. Cancer Causes Control 25, 795–808 (2014). https://doi.org/10.1007/s10552-014-0381-7

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