Abstract
Purpose
To estimate the incidence rate of second primary cancers (SPCs) and the cumulative incidence of metachronous [diagnosed > 2 months after a first primary cancer (FPC)] SPCs in patients with a breast FPC, and to compare the incidence of SPC [overall, synchronous (≤ 2 months of the FPC) and metachronous] with that expected in the general female population.
Methods
A cohort of patients with a breast FPC from the North Region Cancer Registry of Portugal, diagnosed in 2000–2010 (n = 15,981), was followed to 31 December 2015 for synchronous and metachronous SPCs. Cumulative incidence of metachronous SPCs considering death as a competing event, and incidence rates and standardized incidence ratios of SPCs were estimated.
Results
The diagnosis of an SPC occurred in 1229 (7.7%) of patients with a breast FPC. SPCs occurred mainly in the breast, followed by digestive organs, lung, thyroid, and female genital organs. Globally, patients with a breast FPC had a higher incidence for all types of cancer compared to the general female population, and in particular for cancers of the breast, stomach, colon, lung, lymphoma, uterus, and ovary. The 10-year cumulative incidence of metachronous SPCs following a breast FPC was 6.6% and the corresponding 10-year cumulative mortality was 26.2%.
Conclusion
In Portugal, patients with a breast FPC have a higher incidence of cancer compared to the general female population, highlighting important aspects of care, surveillance, and counselling among this growing number of patients.
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Data availability
The data that support the findings of this study are available from RORENO, but restrictions apply to the availability of these data, which were used under license for the current study and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of RORENO.
Abbreviations
- 95%CI:
-
95% confidence interval
- BCa:
-
Breast cancer
- FPC:
-
First primary cancer
- IACR:
-
International Association of Cancer Registries
- IARC:
-
International Agency for Research on Cancer
- NHL:
-
Non-Hodgkin lymphoma
- P25-P75:
-
Percentile 25 – percentile 75
- PYAR:
-
Person-years at risk
- RORENO:
-
North Region Cancer Registry of Portugal
- SIR:
-
Standardized incidence ratios
- SPC:
-
Second primary cancer
- US:
-
United States
References
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global Cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249. https://doi.org/10.3322/caac.21660
Liu Y, Dong C, Chen L (2017) The clinicopathological features of second primary cancer in patients with prior Breast cancer. Med (Baltim) 96:e6675. https://doi.org/10.1097/md.0000000000006675
Sánchez L, Lana A, Hidalgo A, Rodríguez JM, Del Valle Mdel O, Cueto A, Folgueras MV, Belyakova E, Comendador MA, López ML (2008) Risk factors for second primary tumours in Breast cancer survivors. Eur J Cancer Prev 17:406–413. https://doi.org/10.1097/CEJ.0b013e3282f75ee5
Li D, Weng S, Zhong C, Tang X, Zhu N, Cheng Y, Xu D, Yuan Y (2019) Risk of second primary cancers among long-term survivors of Breast cancer. Front Oncol 9:1426. https://doi.org/10.3389/fonc.2019.01426
Allen I, Hassan H, Sofianopoulou E, Eccles D, Turnbull C, Tischkowitz M, Pharoah P, Antoniou AC (2023) Risks of second non-breast primaries following Breast cancer in women: a systematic review and meta-analysis. Breast Cancer Res 25:18. https://doi.org/10.1186/s13058-023-01610-x
Parhizgar P, Bahadori Monfared A, Mohseny M, Keramatinia A, Hashemi Nazari SS, Rahman SA, Al Marzouqi A, Al-Yateem N, Mosavi Jarrahi A (2022) Risk of second primary cancer among Breast cancer patients: a systematic review and meta-analysis. Front Oncol 12:1094136. https://doi.org/10.3389/fonc.2022.1094136
Molina-Montes E, Pollán M, Payer T, Molina E, Dávila-Arias C, Sánchez MJ (2013) Risk of second primary cancer among women with Breast cancer: a population-based study in Granada (Spain). Gynecol Oncol 130:340–345. https://doi.org/10.1016/j.ygyno.2013.04.057
Corso G, Veronesi P, Santomauro GI, Maisonneuve P, Morigi C, Peruzzotti G, Intra M, Sacchini V, Galimberti V (2018) Multiple primary non-breast tumors in Breast cancer survivors. J Cancer Res Clin Oncol 144:979–986. https://doi.org/10.1007/s00432-018-2621-9
Trentham-Dietz A, Newcomb PA, Nichols HB, Hampton JM (2007) Breast cancer risk factors and second primary malignancies among women with Breast cancer. Breast Cancer Res Treat 105:195–207. https://doi.org/10.1007/s10549-006-9446-y
Mellemkjaer L, Friis S, Olsen JH, Scélo G, Hemminki K, Tracey E, Andersen A, Brewster DH, Pukkala E, McBride ML, Kliewer EV, Tonita JM, Kee-Seng C, Pompe-Kirn V, Martos C, Jonasson JG, Boffetta P, Brennan P (2006) Risk of second cancer among women with Breast cancer. Int J Cancer 118:2285–2292. https://doi.org/10.1002/ijc.21651
Ricceri F, Fasanelli F, Giraudo MT, Sieri S, Tumino R, Mattiello A, Vagliano L, Masala G, Quirós JR, Travier N, Sánchez MJ, Larranaga N, Chirlaque MD, Ardanaz E, Tjonneland A, Olsen A, Overvad K, Chang-Claude J, Kaaks R, Boeing H, Clavel-Chapelon F, Kvaskoff M, Dossus L, Trichopoulou A, Benetou V, Adarakis G, Bueno-de-Mesquita HB, Peeters PH, Sund M, Andersson A, Borgquist S, Butt S, Weiderpass E, Skeie G, Khaw KT, Travis RC, Rinaldi S, Romieu I, Gunter M, Kadi M, Riboli E, Vineis P, Sacerdote C (2015) Risk of second primary malignancies in women with Breast cancer: results from the European prospective investigation into Cancer and Nutrition (EPIC). Int J Cancer 137:940–948. https://doi.org/10.1002/ijc.29462
Lee KD, Chen SC, Chan CH, Lu CH, Chen CC, Lin JT, Chen MF, Huang SH, Yeh CM, Chen MC (2008) Increased risk for second primary malignancies in women with Breast cancer diagnosed at young age: a population-based study in Taiwan. Cancer Epidemiol Biomarkers Prev 17:2647–2655. https://doi.org/10.1158/1055-9965.Epi-08-0109
Raymond JS, Hogue CJ (2006) Multiple primary tumours in women following Breast cancer, 1973–2000. Br J Cancer 94:1745–1750. https://doi.org/10.1038/sj.bjc.6603172
Andersson M, Jensen MB, Engholm G, Henrik Storm H (2008) Risk of second primary cancer among patients with early operable Breast cancer registered or randomised in Danish Breast Cancer cooperative group (DBCG) protocols of the 77, 82 and 89 programmes during 1977–2001. Acta Oncol 47:755–764. https://doi.org/10.1080/02841860801978921
Hung MH, Liu CJ, Teng CJ, Hu YW, Yeh CM, Chen SC, Chien SH, Hung YP, Shen CC, Chen TJ, Tzeng CH, Liu CY (2016) Risk of second non-breast primary cancer in male and female Breast cancer patients: a population-based cohort study. PLoS ONE 11:e0148597. https://doi.org/10.1371/journal.pone.0148597
Curtis RE, Freedman DM, Ron E, Ries LAG, Hacker DG, Edwards BK, Tucker MA, Fraumeni JF (2006) New malignancies among cancer survivors: SEER Cancer Registries, 1973–2000. National Cancer Institute, NIH Publ. No. 05-5302. Bethesda
Registo Oncológico do Norte (2016) Registo Oncológico Regional do Norte 2015. Instituto Português de Oncologia do Porto Francisco Gentil - EPE
Ferlay J, Burkhard C, Whelan S, Parkin D (2005) Check and conversion programs for cancer registries. International Agency for Research on Cancer, Lyon
Fritz A, Percy C, Jack A, Shanmugaratnam K, Sobin L, Parkin DM, Whelan S (2000) International classification of diseases for oncology (ICD-O) third edition. World Health Organization, Geneva
World Health Organisation (1992) International Statistical Classification of Diseases and related health problems – 10th revision. World Health Organization, Geneva
Working Group Report (2005) International rules for multiple primary cancers (ICD-0 third edition). Eur J Cancer Prev 14:307–308. https://doi.org/10.1097/00008469-200508000-00002
Howe HL, Weinstein R, Hotes J, Kohler B, Roffers SD, Goodman MT (2003) Multiple primary cancers of the ovary in the United States, 1992–1997. Cancer 97:2660–2675. https://doi.org/10.1002/cncr.11348
Youlden DR, Baade PD (2011) The relative risk of second primary cancers in Queensland, Australia: a retrospective cohort study. BMC Cancer 11:83. https://doi.org/10.1186/1471-2407-11-83
Kalbfleisch J, Prentice R (2002) The statistical analysis of failure time data. New York; John Wiley & Songs
Morais S, Gonçalves E, Fontes F, Rodrigues J, Calisto R, Bento MJ, Lunet N (2022) Risk and survival of third primary cancers in a population-based cohort of Breast cancer patients. Breast Care (Basel) 17:349–355. https://doi.org/10.1159/000522057
Silverman BG, Lipshitz I, Keinan-Boker L (2017) Second primary cancers after primary Breast cancer diagnosis in Israeli women, 1992 to 2006. J Glob Oncol 3:135–142. https://doi.org/10.1200/jgo.2016.003699
Grantzau T, Overgaard J (2015) Risk of second non-breast cancer after radiotherapy for Breast cancer: a systematic review and meta-analysis of 762,468 patients. Radiother Oncol 114:56–65. https://doi.org/10.1016/j.radonc.2014.10.004
Gomes IA, Nunes C (2020) Analysis of the Breast cancer mortality rate in Portugal over a decade: spatiotemporal clustering analysis. Acta Med Port 33:305–310. https://doi.org/10.20344/amp.11749
Registo Oncológico Nacional (2022) Registo Oncológico Nacional de Todos os Tumores na População Residente em Portugm 2019. In: Instituto Português de Oncologio do Porto Francisco Gentil - EPE (ed), Porto
Funding
This study was funded by national funds from the Foundation for Science and Technology – FCT (Portuguese Ministry of Science, Technology and Higher Education), under the Unidade de Investigação em Epidemiologia – Instituto de Saúde Pública da Universidade do Porto (EPIUnit; UIDB/04750/2020) and the Laboratório para a Investigação Integrativa e Translacional em Saúde Populacional (ITR; LA/P/0064/2020). SM was funded by FEDER through the Operational Program Competitiveness and Internationalization, and national funding from FCT under the scope of the project “NEON-PC - Neuro-oncological complications of prostate cancer: longitudinal study of cognitive decline” (POCI-01-0145-FEDER-032358; ref. PTDC/SAU-EPI/32358/2017) and the EPIUnit – Junior Research – Prog Financing (UIDP/04750/2020). The funding sources had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
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All authors contributed to the study conception and design. Data preparation and collection were performed by Elisabete Gonçalves, Jéssica Rocha Rodrigues, Rita Calisto, Maria José Bento, and Samantha Morais. Analyses were performed by Elisabete Gonçalves and Samantha Morais. The first draft of the manuscript was written by Elisabete Gonçalves, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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The study was approved by the Ethics Committee of the Portuguese Institute of Oncology of Porto (Ref. CES IPO: 332/020) and the analyses were performed according to RORENO guidelines ensuring the anonymity of information used.
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Gonçalves, E., Fontes, F., Rodrigues, J.R. et al. Second primary cancers among females with a first primary breast cancer: a population-based study in Northern Portugal. Breast Cancer Res Treat 204, 367–376 (2024). https://doi.org/10.1007/s10549-023-07224-3
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DOI: https://doi.org/10.1007/s10549-023-07224-3