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Clinical subtypes and prognosis in breast cancer according to parity: a nationwide study in Korean Breast Cancer Society

  • Epidemiology
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Abstract

Purpose

We explored the association between parity and the risk of developing a specific subtype of breast cancer. We also assessed the association between parity and prognosis according to subtypes.

Methods

A total of 158,189 patients were enrolled in the Korean Breast Cancer Society Registry database between 1996 and 2015 in Korea. The database provided information on sex, age, number of parity, surgical method, stage, histological findings, presence of biologic markers, adjuvant therapy, and date and cause of death.

Results

The patients with higher parity showed a higher ratio of triple-negative breast cancer (TNBC) and human epidermal growth factor receptor 2 (HER2) subtypes. In univariate analysis, women with TNBC who had more than three children had a worse prognosis compared to other groups (HR 1.83; 95% CI 1.34–2.49; P < 0.001). This association was also observed in women younger than 50 years (HR 1.63; 95% CI 1.07–2.48; P = 0.021). In multivariate analysis stratified by subtypes, women who had more than three children were associated with a worse prognosis in TNBC in the total population (HR 1.53; 95% CI 1.11–2.12; P = 0.011). This association was also observed in patients younger than 50 years of age (HR 1.53; 95% CI 1.09–2.61; P = 0.017).

Conclusion

Women who had more than three children were more likely to develop hormone receptor-negative (HR−) subtypes. Women who had more than three children were associated with worse prognosis in patients younger than 50 years of age and in patients with TNBC.

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References

  1. Azim HA Jr, Partridge AH (2014) Biology of breast cancer in young women. Breast Cancer Res 16(4):427. https://doi.org/10.1186/s13058-014-0427-5

    Article  PubMed  PubMed Central  Google Scholar 

  2. Beral V (2002) Breast cancer and breastfeeding: collaborative reanalysis of individual data from 47 epidemiological studies in 30 countries, including 50302 women with breast cancer and 96973 women without the disease. Lancet 360(9328):187–195. https://doi.org/10.1016/s0140-6736(02)09454-0

    Article  Google Scholar 

  3. MacMahon B, Cole P, Lin TM, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S (1970) Age at first birth and breast cancer risk. Bull World Health Organ 43(2):209–221

    PubMed  PubMed Central  CAS  Google Scholar 

  4. Lambe M, Hsieh C, Trichopoulos D, Ekbom A, Pavia M, Adami HO (1994) Transient increase in the risk of breast cancer after giving birth. N Engl J Med 331(1):5–9. https://doi.org/10.1056/nejm199407073310102

    Article  PubMed  CAS  Google Scholar 

  5. Morch LS, Skovlund CW, Hannaford PC, Iversen L, Fielding S, Lidegaard O (2017) Contemporary hormonal contraception and the risk of breast cancer. N Engl J Med 377(23):2228–2239. https://doi.org/10.1056/NEJMoa1700732

    Article  PubMed  Google Scholar 

  6. Gierisch JM, Coeytaux RR, Urrutia RP, Havrilesky LJ, Moorman PG, Lowery WJ, Dinan M, McBroom AJ, Hasselblad V, Sanders GD, Myers ER (2013) Oral contraceptive use and risk of breast, cervical, colorectal, and endometrial cancers: a systematic review. Cancer Epidemiol Biomarkers Prev 22(11):1931–1943. https://doi.org/10.1158/1055-9965.epi-13-0298

    Article  PubMed  Google Scholar 

  7. Ambrosone CB, Zirpoli G, Ruszczyk M, Shankar J, Hong CC, McIlwain D, Roberts M, Yao S, McCann SE, Ciupak G, Hwang H, Khoury T, Jandorf L, Bovbjerg DH, Pawlish K, Bandera EV (2014) Parity and breastfeeding among African-American women: differential effects on breast cancer risk by estrogen receptor status in the Women’s Circle of Health Study. Cancer Causes Control 25(2):259–265. https://doi.org/10.1007/s10552-013-0323-9

    Article  PubMed  Google Scholar 

  8. de la Rochefordiere A, Asselain B, Campana F, Scholl SM, Fenton J, Vilcoq JR, Durand JC, Pouillart P, Magdelenat H, Fourquet A (1993) Age as prognostic factor in premenopausal breast carcinoma. Lancet 341(8852):1039–1043

    Article  PubMed  Google Scholar 

  9. Yang XR, Chang-Claude J, Goode EL, Couch FJ, Nevanlinna H, Milne RL, Gaudet M, Schmidt MK, Broeks A, Cox A, Fasching PA, Hein R, Spurdle AB, Blows F, Driver K, Flesch-Janys D, Heinz J, Sinn P, Vrieling A, Heikkinen T, Aittomaki K, Heikkila P, Blomqvist C, Lissowska J, Peplonska B, Chanock S, Figueroa J, Brinton L, Hall P, Czene K, Humphreys K, Darabi H, Liu J, Van ‘t Veer LJ, van Leeuwen FE, Andrulis IL, Glendon G, Knight JA, Mulligan AM, O’Malley FP, Weerasooriya N, John EM, Beckmann MW, Hartmann A, Weihbrecht SB, Wachter DL, Jud SM, Loehberg CR, Baglietto L, English DR, Giles GG, McLean CA, Severi G, Lambrechts D, Vandorpe T, Weltens C, Paridaens R, Smeets A, Neven P, Wildiers H, Wang X, Olson JE, Cafourek V, Fredericksen Z, Kosel M, Vachon C, Cramp HE, Connley D, Cross SS, Balasubramanian SP, Reed MW, Dork T, Bremer M, Meyer A, Karstens JH, Ay A, Park-Simon TW, Hillemanns P, Arias Perez JI, Menendez Rodriguez P, Zamora P, Benitez J, Ko YD, Fischer HP, Hamann U, Pesch B, Bruning T, Justenhoven C, Brauch H, Eccles DM, Tapper WJ, Gerty SM, Sawyer EJ, Tomlinson IP, Jones A, Kerin M, Miller N, McInerney N, Anton-Culver H, Ziogas A, Shen CY, Hsiung CN, Wu PE, Yang SL, Yu JC, Chen ST, Hsu GC, Haiman CA, Henderson BE, Le Marchand L, Kolonel LN, Lindblom A, Margolin S, Jakubowska A, Lubinski J, Huzarski T, Byrski T, Gorski B, Gronwald J, Hooning MJ, Hollestelle A, van den Ouweland AM, Jager A, Kriege M, Tilanus-Linthorst MM, Collee M, Wang-Gohrke S, Pylkas K, Jukkola-Vuorinen A, Mononen K, Grip M, Hirvikoski P, Winqvist R, Mannermaa A, Kosma VM, Kauppinen J, Kataja V, Auvinen P, Soini Y, Sironen R, Bojesen SE, Orsted DD, Kaur-Knudsen D, Flyger H, Nordestgaard BG, Holland H, Chenevix-Trench G, Manoukian S, Barile M, Radice P, Hankinson SE, Hunter DJ, Tamimi R, Sangrajrang S, Brennan P, McKay J, Odefrey F, Gaborieau V, Devilee P, Huijts PE, Tollenaar RA, Seynaeve C, Dite GS, Apicella C, Hopper JL, Hammet F, Tsimiklis H, Smith LD, Southey MC, Humphreys MK, Easton D, Pharoah P, Sherman ME, Garcia-Closas M (2011) Associations of breast cancer risk factors with tumor subtypes: a pooled analysis from the Breast Cancer Association Consortium studies. J Natl Cancer Inst 103(3):250–263. https://doi.org/10.1093/jnci/djq526

    Article  Google Scholar 

  10. Ma H, Bernstein L, Pike MC, Ursin G (2006) Reproductive factors and breast cancer risk according to joint estrogen and progesterone receptor status: a meta-analysis of epidemiological studies. Breast Cancer Res 8(4):R43. https://doi.org/10.1186/bcr1525

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Setiawan VW, Monroe KR, Wilkens LR, Kolonel LN, Pike MC, Henderson BE (2009) Breast cancer risk factors defined by estrogen and progesterone receptor status: the multiethnic cohort study. Am J Epidemiol 169(10):1251–1259. https://doi.org/10.1093/aje/kwp036

    Article  PubMed  PubMed Central  Google Scholar 

  12. Anderson KN, Schwab RB, Martinez ME (2014) Reproductive risk factors and breast cancer subtypes: a review of the literature. Breast Cancer Res Treat 144(1):1–10. https://doi.org/10.1007/s10549-014-2852-7

    Article  PubMed  PubMed Central  Google Scholar 

  13. Park B, Choi KS, Lee YY, Jun JK, Seo HG (2012) Trends in Cancer Screening Rates among Korean Men and Women: Results from the Korean National Cancer Screening Survey (KNCSS), 2004–2011. Cancer Res Treat 44(2):113–120. https://doi.org/10.4143/crt.2012.44.2.113

    Article  PubMed  PubMed Central  Google Scholar 

  14. Hammond ME, Hayes DF, Wolff AC (2011) Clinical notice for American Society of Clinical Oncology-College of American Pathologists guideline recommendations on ER/PgR and HER2 testing in breast cancer. J Clin Oncol 29(15):e458. https://doi.org/10.1200/jco.2011.35.2245

    Article  PubMed  Google Scholar 

  15. Brouckaert O, Rudolph A, Laenen A, Keeman R, Bolla MK, Wang Q, Soubry A, Wildiers H, Andrulis IL, Arndt V, Beckmann MW, Benitez J, Blomqvist C, Bojesen SE, Brauch H, Brennan P, Brenner H, Chenevix-Trench G, Choi JY, Cornelissen S, Couch FJ, Cox A, Cross SS, Czene K, Eriksson M, Fasching PA, Figueroa J, Flyger H, Giles GG, Gonzalez-Neira A, Guenel P, Hall P, Hollestelle A, Hopper JL, Ito H, Jones M, Kang D, kConFab KJA, Kosma VM, Li J, Lindblom A, Lilyquist J, Lophatananon A, Mannermaa A, Manoukian S, Margolin S, Matsuo K, Muir K, Nevanlinna H, Peterlongo P, Pylkas K, Saajrang S, Seynaeve C, Shen CY, Shu XO, Southey MC, Swerdlow A, Teo SH, Tollenaar R, Truong T, Tseng CC, van den Broek AJ, van Deurzen CHM, Winqvist R, Wu AH, Yip CH, Yu JC, Zheng W, Milne RL, Pharoah PDP, Easton DF, Schmidt MK, Garcia-Closas M, Chang-Claude J, Lambrechts D, Neven P (2017) Reproductive profiles and risk of breast cancer subtypes: a multi-center case-only study. Breast Cancer Res 19(1):119. https://doi.org/10.1186/s13058-017-0909-3

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Work ME, John EM, Andrulis IL, Knight JA, Liao Y, Mulligan AM, Southey MC, Giles GG, Dite GS, Apicella C, Hibshoosh H, Hopper JL, Terry MB (2014) Reproductive risk factors and oestrogen/progesterone receptor-negative breast cancer in the Breast Cancer Family Registry. Br J Cancer 110(5):1367–1377. https://doi.org/10.1038/bjc.2013.807

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Phipps AI, Chlebowski RT, Prentice R, McTiernan A, Wactawski-Wende J, Kuller LH, Adams-Campbell LL, Lane D, Stefanick ML, Vitolins M, Kabat GC, Rohan TE, Li CI (2011) Reproductive history and oral contraceptive use in relation to risk of triple-negative breast cancer. J Natl Cancer Inst 103(6):470–477. https://doi.org/10.1093/jnci/djr030

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ellingjord-Dale M, Vos L, Tretli S, Hofvind S, Dos-Santos-Silva I, Ursin G (2017) Parity, hormones and breast cancer subtypes - results from a large nested case-control study in a national screening program. Breast Cancer Res 19(1):10. https://doi.org/10.1186/s13058-016-0798-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Rajkumar L, Guzman RC, Yang J, Thordarson G, Talamantes F, Nandi S (2004) Prevention of mammary carcinogenesis by short-term estrogen and progestin treatments. Breast Cancer Res 6(1):R31–R37. https://doi.org/10.1186/bcr734

    Article  PubMed  CAS  Google Scholar 

  20. Dontu G, El-Ashry D, Wicha MS (2004) Breast cancer, stem/progenitor cells and the estrogen receptor. Trends Endocrinol Metab 15(5):193–197. https://doi.org/10.1016/j.tem.2004.05.011

    Article  PubMed  CAS  Google Scholar 

  21. Faupel-Badger JM, Arcaro KF, Balkam JJ, Eliassen AH, Hassiotou F, Lebrilla CB, Michels KB, Palmer JR, Schedin P, Stuebe AM, Watson CJ, Sherman ME (2013) Postpartum remodeling, lactation, and breast cancer risk: summary of a National Cancer Institute-sponsored workshop. J Natl Cancer Inst 105(3):166–174. https://doi.org/10.1093/jnci/djs505

    Article  PubMed  Google Scholar 

  22. Yang XR, Figueroa JD, Falk RT, Zhang H, Pfeiffer RM, Hewitt SM, Lissowska J, Peplonska B, Brinton L, Garcia-Closas M, Sherman ME (2012) Analysis of terminal duct lobular unit involution in luminal A and basal breast cancers. Breast Cancer Res 14(2):R64. https://doi.org/10.1186/bcr3170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Shinde SS, Forman MR, Kuerer HM, Yan K, Peintinger F, Hunt KK, Hortobagyi GN, Pusztai L, Symmans WF (2010) Higher parity and shorter breastfeeding duration: association with triple-negative phenotype of breast cancer. Cancer 116(21):4933–4943. https://doi.org/10.1002/cncr.25443

    Article  PubMed  Google Scholar 

  24. Islami F, Liu Y, Jemal A, Zhou J, Weiderpass E, Colditz G, Boffetta P, Weiss M (2015) Breastfeeding and breast cancer risk by receptor status—a systematic review and meta-analysis. Ann Oncol 26(12):2398–2407. https://doi.org/10.1093/annonc/mdv379

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Lambertini M, Santoro L, Del Mastro L, Nguyen B, Livraghi L, Ugolini D, Peccatori FA, Azim HA Jr (2016) Reproductive behaviors and risk of developing breast cancer according to tumor subtype: a systematic review and meta-analysis of epidemiological studies. Cancer Treat Rev 49:65–76. https://doi.org/10.1016/j.ctrv.2016.07.006

    Article  PubMed  Google Scholar 

  26. Rosenberg L, Thalib L, Adami HO, Hall P (2004) Childbirth and breast cancer prognosis. Int J Cancer 111(5):772–776. https://doi.org/10.1002/ijc.20323

    Article  PubMed  CAS  Google Scholar 

  27. Barnett GC, Shah M, Redman K, Easton DF, Ponder BA, Pharoah PD (2008) Risk factors for the incidence of breast cancer: do they affect survival from the disease? J Clin Oncol 26(20):3310–3316. https://doi.org/10.1200/jco.2006.10.3168

    Article  PubMed  Google Scholar 

  28. Alsaker MD, Opdahl S, Romundstad PR, Vatten LJ (2013) Association of time since last birth, age at first birth and parity with breast cancer survival among parous women: a register-based study from Norway. Int J Cancer 132(1):174–181. https://doi.org/10.1002/ijc.27593

    Article  PubMed  CAS  Google Scholar 

  29. Halmin M, Bellocco R, Lagerlund M, Karlsson P, Tejler G, Lambe M (2008) Long-term inequalities in breast cancer survival—a ten year follow-up study of patients managed within a National Health Care System (Sweden). Acta Oncologica 47(2):216–224. https://doi.org/10.1080/02841860701769768

    Article  PubMed  Google Scholar 

  30. Lyons TR, O’Brien J, Borges VF, Conklin MW, Keely PJ, Eliceiri KW, Marusyk A, Tan AC, Schedin P (2011) Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med 17(9):1109–1115. https://doi.org/10.1038/nm.2416

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. O’Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, Man YG, Borges V, Schedin P (2010) Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol 176(3):1241–1255. https://doi.org/10.2353/ajpath.2010.090735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Fredholm H, Eaker S, Frisell J, Holmberg L, Fredriksson I, Lindman H (2009) Breast cancer in young women: poor survival despite intensive treatment. PLoS ONE 4(11):e7695. https://doi.org/10.1371/journal.pone.0007695

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Baselga J, Campone M, Piccart M, Burris HA III, Rugo HS, Sahmoud T, Noguchi S, Gnant M, Pritchard KI, Lebrun F, Beck JT, Ito Y, Yardley D, Deleu I, Perez A, Bachelot T, Vittori L, Xu Z, Mukhopadhyay P, Lebwohl D, Hortobagyi GN (2012) Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med 366(6):520–529. https://doi.org/10.1056/NEJMoa1109653

    Article  PubMed  CAS  Google Scholar 

  34. Bianchini G, Balko JM, Mayer IA, Sanders ME, Gianni L (2016) Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat Rev Clin Oncol 13(11):674–690. https://doi.org/10.1038/nrclinonc.2016.66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Butt S, Borgquist S, Garne JP, Landberg G, Tengrup I, Olsson A, Manjer J (2009) Parity in relation to survival following breast cancer. Eur J Surg Oncol 35(7):702–708. https://doi.org/10.1016/j.ejso.2008.03.017

    Article  PubMed  CAS  Google Scholar 

  36. Goss PE, Ingle JN, Martino S, Robert NJ, Muss HB, Livingston RB, Davidson NE, Perez EA, Chavarri-Guerra Y, Cameron DA, Pritchard KI, Whelan T, Shepherd LE, Tu D (2013) Impact of premenopausal status at breast cancer diagnosis in women entered on the placebo-controlled NCIC CTG MA17 trial of extended adjuvant letrozole. Ann Oncol 24(2):355–361. https://doi.org/10.1093/annonc/mds330

    Article  PubMed  CAS  Google Scholar 

  37. Hill K (1996) The demography of menopause. Maturitas 23(2):113–127

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the research grant of the Korean Breast Cancer Society and the Chungbuk National University Hospital in 2018.

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Correspondence to Soo Youn Bae.

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Park, S., Moon, B.I., Oh, S.J. et al. Clinical subtypes and prognosis in breast cancer according to parity: a nationwide study in Korean Breast Cancer Society. Breast Cancer Res Treat 173, 679–691 (2019). https://doi.org/10.1007/s10549-018-5032-3

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