Abstract
To compare overall survival between women with unilateral breast cancer (UBC) and contralateral breast cancer (CBC). Women with UBC (N = 182,562; 95 %) and CBC (N = 8,912; 5 %) recorded in the Netherlands Cancer Registry between 1989 and 2008 were included and followed until 2010. We incorporated CBC as a time-dependent covariate to compute the overall mortality rate ratio between women with CBC and UBC. Prognostic factors for overall death were examined according to age at first breast cancer. Women with CBC exhibited a 30 % increase in overall mortality (Hazard Ratio (HR), 95 % Confidence Interval: 1.3, 1.3–1.4) compared with UBC, decreasing with rising age at diagnosis of first breast cancer (<50 years: 2.3, 2.2–2.5 vs. ≥70 years: 1.1, 1.0–1.1). Women older than 50 years at CBC diagnosis and diagnosed 2–5 years after their first breast cancer exhibited a 20 % higher death risk (1.2, 1.0–1.3) compared to those diagnosed within the first 2 years. In women younger than 50 years, the HR was significantly lower if the CBC was diagnosed >5 years after the first breast cancer (0.7, 0.5–0.9). The prognosis for women with CBC significantly improved over time (2004–2008: 0.6, 0.5-0.7 vs. 1989–1993). Women with CBC had a lower survival compared to women with UBC, especially those younger than 50 years at first breast cancer diagnosis. A tailored follow-up strategy beyond current recommendations is needed for these patients who, because of their age and absence of known familial risk, are currently not invited for population-based screening.
Similar content being viewed by others
References
Soerjomataram I, Lortet-Tieulent J, Parkin DM, Ferlay J, Mathers C, Forman D, Bray F (2012) Global burden of cancer in 2008: a systematic analysis of disability-adjusted life-years in 12 world regions. Lancet 380:1840–1850. doi:10.1016/S0140-6736(12)60919-2
Netherlands Cancer Registry (NCR) (2012) Most common types of cancer. http://cijfersoverkanker.nl/meest-voorkomende-soorten-52.html. Accessed 21 June 2012
Louwman WJ, Voogd AC, van Dijck J, Nieuwenhuijzen GA, Ribot J, Pruijt JF, Coebergh JW (2008) On the rising trends of incidence and prognosis for breast cancer patients diagnosed 1975–2004: a long-term population-based study in southeastern Netherlands. Cancer Causes Control 19:97–106
Karim-Kos HE, Kiemeney LALM, Louwman MWJ, Coebergh JWW, de Vries E (2012) Progress against cancer in the Netherlands since the late 1980s: an epidemiological evaluation. Int J Cancer 130:2981–2989
Nationwide breast cancer screening programme fully implemented in the Netherlands, Fracheboud J, de Koning HJ, Boer R, Groenewoud JH, Verbeek ALM, Broeders MJM, van Ineveld BM, Hendriks JHCL, de Bruyn AE, Holland R, van der Maas PJ (2001) Nationwide breast cancer screening programme fully implemented in the Netherlands. Breast 10:6–11
Bray F, Jemal A, Grey N, Ferlay J, Forman D (2012) Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. Lancet Oncol 13:790–801. doi:10.1016/S1470-2045(12)70211-5
Soerjomataram I, Louwman WJ, Lemmens VEPP, de Vries E, Klokman WJ, Coebergh JWW (2005) Risks of second primary breast and urogenital cancer following female breast cancer in the south of The Netherlands, 1972–2001. Eur J Cancer 41:2331–2337
Holmberg L, Adami H, Ekbom A, Bergstram R, Sandstram A, Lindgren A (1988) Prognosis in bilateral breast cancer. Effects of time interval between first and second primary tumours. Br J Cancer 58:191–194
Brenner H, Engelsmann B, Stegmaier C, Ziegler H (1993) Clinical epidemiology of bilateral breast cancer. Cancer 72:3629–3635
Gajalakshmi C, Shanta V, Hakama M (1999) Survival from contralateral breast cancer. Breast Cancer Res Treat 58:115–122
Abdalla I, Thisted R, Heimann R (2000) The impact of contralateral breast cancer on the outcome of breast cancer patients treated by mastectomy. Cancer J 6:266–272
Jobsen JJ, Jvd Palen, Ong F, Meerwaldt JH (2003) Synchronous, bilateral breast cancer: prognostic value and incidence. Breast 12:83–88
Hartman M, Czene K, Reilly M, Adolfsson J, Bergh J, Adami HO, Dickman PW, Hall P (2007) Incidence and prognosis of synchronous and metachronous bilateral breast cancer. J Clin Oncol 25:4210–4216
Schaapveld M, Visser O, Louwman W, Willemse PH, de Vries EG, van der Graaf WT, Otter R, Coebergh JW, van Leeuwen FE (2008) The impact of adjuvant therapy on contralateral breast cancer risk and the prognostic significance of contralateral breast cancer: a population based study in the Netherlands. Breast Cancer Res Treat 110:189–197
Kuo WH, Yen AM, Lee PH, Chen KM, Wang J, Chang KJ, Chen TH, Tsau HS (2009) Cumulative survival in early-onset unilateral and bilateral breast cancer: an analysis of 1907 Taiwanese women. Br J Cancer 100:563–570
Vichapat V, Garmo H, Holmberg L, Fentiman IS, Tutt A, Gillett C, Lüchtenborg M (2011) Prognosis of metachronous contralateral breast cancer: importance of stage, age and interval time between the two diagnoses. Breast Cancer Res Treat 130:609–618
Schwentner L, Wolters R, Wischnewsky M, Kreienberg R, Wöckel A (2012) Survival of patients with bilateral versus unilateral breast cancer and impact of guideline adherent adjuvant treatment: a multi-centre cohort study of 5292 patients. Breast 21:171–177
Heron D, Komarnicky L, Hyslop T, Schwartz G, Mansfield C (2000) Bilateral breast carcinoma: risk factors and outcomes for patients with synchronous and metachronous disease. Cancer 88:2739–2750
Takahashi H, Watanabe K, Takahashi M, Taguchi K, Sasaki F, Todo S (2005) The impact of bilateral breast cancer on the prognosis of breast cancer: a comparative study with unilateral breast cancer. Breast Cancer 12:196–202
Verkooijen HM, Chatelain V, Fioretta G, Vlastos G, Rapiti E, Sappino AP, Bouchardy C, Chappuis PO (2007) Survival after bilateral breast cancer: results from a population-based study. Breast Cancer Res Treat 105:347–357
Irvine T, Allen DS, Gillett C, Hamed H, Fentiman IS (2009) Prognosis of synchronous bilateral breast cancer. Br J Surg 96:376–380
Mose S, Adamietz IA, Thilmann C, Saran F, Bernhard M, Pahnke R, Böttcher HD (1997) Bilateral breast carcinoma versus unilateral disease: review of 498 patients. Am J Clin Oncol 20:541–545
Michowitz M, Noy S, Lazebnik N, Aladjem D (1985) Bilateral breast cancer. J Surg Oncol 30:109–112
Gustafsson A, Tartter P, Brower S, Lesnick G (1994) Prognosis of patients with bilateral carcinoma of the breast. J Am Coll Surg 178:111–116
Skowronek J, Piotrowski T (2002) Bilateral breast cancer. Neoplasma 49:49–54
Casparie M, Tiebosch AT, Burger G, Blauwgeers H, van de Pol A, van Krieken JH, Meijer GA (2007) Pathology databanking and biobanking in The Netherlands, a central role for PALGA, the nationwide histopathology and cytopathology data network and archive. Cell Oncol 29:19–24
Schouten LJ, Jager JJ, van den Brandt PA (1993) Quality of cancer registry data: a comparison of data provided by clinicians with those of registration personnel. Br J Cancer 68:974–977
Schouten LJ, Hoppener P, van den Brandt PA, Knottnerus JA, Jager JJ (1993) Completeness of cancer registration in Limburg, The Netherlands. Int J Epidemiol 22:369–376
International Association of Cancer Registries (IACR) (2005) International rules for multiple primary cancers. Asian Pac J Cancer Prev 6:104–106
Rothman KJ, Greenland S (1998) Cohort studies. In: Rothman KJ, Greenland S (eds) Modern epidemiology, 2nd edn. Lippincott-Raven, Philadelphia, pp 79–91
Maaskant AJ, van de Poll-Franse LV, Voogd AC, Coebergh JW, Tutein Nolthenius-Puylaert MC, Nieuwenhuijzen GA (2009) Stage migration due to introduction of the sentinel node procedure: a population-based study. Breast Cancer Res Treat 113:173–179
Janssen-Heijnen ML, van Steenbergen LN, Voogd AC, Nijhuis PH, Poortmans PH, Coebergh JW (2012) Long-term excess mortality for survivors of breast cancer in the Netherlands 2013 (submitted)
Alkner S, Bendahl P, Fernö M, Manjer J, Rydénm L (2011) Prediction of outcome after diagnosis of metachronous contralateral breast cancer. BMC Cancer 11:114. doi:10.1186/1471-2407-11-114
Neta G, Anderson WF, Gilbert E, Berrington A (2012) Variation in the risk of radiation-related contralateral breast cancer by histology and estrogen receptor expression in SEER. Breast Cancer Res Treat 131:1021–1027
Kurian AW, McClure LA, John EM, Horn-Ross PL, Ford JM, Clarke CA (2009) Second primary breast cancer occurrence according to hormone receptor status. J Natl Cancer Inst 101:1058–1065
Hartman M, Czene K, Reilly M, Bergh J, Lagiou P, Trichopoulos D, Adami HO, Hall P (2005) Genetic implications of bilateral breast cancer: a population based cohort study. Lancet Oncol 6:377–382
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:e7695. doi:10.1371/journal.pone.0007695
Vichapat V, Garmo H, Holmqvist M, Liljegren G, Wärnberg F, Lambe M, Fornander T, Adolfsson J, Lüchtenborg M, Holmberg L (2012) Tumour stage affects risk and prognosis of contralateral breast cancer: results from a large Swedish-population-based study. J Clin Oncol 30:3478–3484
Chaudary MA, Millis RR, Hoskins EO, Halder M, Bulbrook RD, Cuzick J, Hayward JL (1984) Bilateral primary breast cancer: a prospective study of disease incidence. Br J Surg 71:711–714
Janschek E, Kandioler-Eckersberger D, Ludwig C, Kappel S, Wolf B, Taucher S, Rudas M, Gnant M, Jakesz R (2001) Contralateral breast cancer: molecular differentiation between metastasis and second primary cancer. Breast Cancer Res Treat 67:1–8
Brommesson S, Jönsson G, Strand C, Grabau D, Malmström P, Ringnér M, Fernö M, Hedenfalk I (2008) Tiling array-CGH for the assessment of genomic similarities among synchronous unilateral and bilateral invasive breast cancer tumor pairs. BMC Clin Pathol 8:6
Vichapat V, Garmo H, Holmberg L, Fentiman IS, Tutt A, Gillett C, Lüchtenborg M (2012) Patterns of metastasis in women with metachronous contralateral breast cancer. Br J Cancer 107:221–223
Eaker S, Dickman PW, Bergkvist L, Holmberg L (2006) Differences in management of older women influence breast cancer survival: results from a population-based database in Sweden. PLoS Med 3:e25. doi:10.1371/journal.pmed.0030025
Comprehensive Cancer Centre of the Netherlands (IKNL) (2012) Mammacarcinoom: Aanbevelingen nacontrole (Breast cancer: recommendations for surveillance). http://www.oncoline.nl/mammacarcinoom. Accessed 22 July 2012
Houssami N, Abraham LA, Miglioretti DL, Sickles EA, Kerlikowske K, Buist DS, Geller BM, Muss HB, Irwig L (2011) Accuracy and outcomes of screening mammography in women with a personal history of early-stage breast cancer. JAMA 305:790–799
Setz-Pels W, Duijm LE, Groenewoud JH, Voogd AC, Jansen FH, Hooijen MJ, Louwman MW (2011) Detection of bilateral breast cancer at biennial screening mammography in the Netherlands: a population-based study. Radiology 260:357–363
Berg WA, Zhang Z, Lehrer D, Jong RA, Pisano ED, Barr RG, Böhm-Vélez M, Mahoney MC, Evans WP III, Larsen LH, Morton MJ, Mendelson EB, Farria DM, Cormack JB, Marques HS, Adams A, Yeh NM, Gabrielli G (2012) Detection of breast cancer with addition of annual screening utrasound or a single screening MRI to mammography in women with elevated breast cancer risk. JAMA 307:1394–1404
Tan MB, Bleiker EM, Menke-Pluymers MB, Van Gool AR, van Dooren S, Van Geel BN, Tilanus-Linthorst MM, Bartels KC, Klijn JG, Brekelmans CT, Seynaeve C (2009) Standard psychological consultations and follow up for women at increased risk of hereditary breast cancer considering prophylactic mastectomy. Hered Cancer Clin Pract 7:6
van Schoor G, Broeders MJM, Paap E, Otten JDM, den Heeten GJ, Verbeek ALM (2008) A rational for starting breast cancer screening under age 50. Ann Oncol 19:1208–1209
Soerjomataram I, Pukkala E, Brenner H, Coebergh JW (2008) On the avoidability of breast cancer in industrialized societies: older mean age at first birth as an indicator of excess breast cancer risk. Breast Cancer Res Treat 111:297–302
Louwman WJ, Janssen-Heijnen ML, Houterman S, Voogd AC, van der Sangen MJ, Nieuwenhuijzen GA, Coebergh JW (2005) Less extensive treatment and inferior prognosis for breast cancer patient with comorbidity: a population-based study. Eur J Cancer 41:779–785
Acknowledgments
The authors thank the registration clerks and data managers at the Comprehensive Cancer Centres for their collection of data for the Netherlands Cancer Registry as well as the scientific staff of the Netherlands Cancer Registry. This study is part of a project funded by the Dutch Cancer Society (KWF): The increasing burden of second primary cancers in the Netherlands: trend in incidence, survival and causes-of-death since 1970 (EMCR 2008-4132). Anna Font-Gonzalez was funded through an Academy Assistantship from the KNAW (Royal Netherlands Academy of Arts and Sciences).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Font-Gonzalez, A., Liu, L., Voogd, A.C. et al. Inferior survival for young patients with contralateral compared to unilateral breast cancer: a nationwide population-based study in the Netherlands. Breast Cancer Res Treat 139, 811–819 (2013). https://doi.org/10.1007/s10549-013-2588-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10549-013-2588-9