Journal Article
. 2016 Jan; 34(9):927-35.
doi: 10.1200/JCO.2015.62.3504.

Annual Hazard Rates of Recurrence for Breast Cancer During 24 Years of Follow-Up: Results From the International Breast Cancer Study Group Trials I to V

Marco Colleoni 1 Zhuoxin Sun 2 Karen N Price 2 Per Karlsson 2 John F Forbes 2 Beat Thürlimann 2 Lorenzo Gianni 2 Monica Castiglione 2 Richard D Gelber 2 Alan S Coates 2 Aron Goldhirsch 2 
  • PMID: 26786933
  •     32 References
  •     119 citations


Purpose: Predicting the pattern of recurrence can aid in the development of targeted surveillance and treatment strategies. We identified patient populations that remain at risk for an event at a median follow-up of 24 years from the diagnosis of operable breast cancer.

Patients And Methods: International Breast Cancer Study Group clinical trials I to V randomly assigned 4,105 patients between 1978 and 1985. Annualized hazards were estimated for breast cancer-free interval (primary end point), disease-free survival, and overall survival.

Results: For the entire group, the annualized hazard of recurrence was highest during the first 5 years (10.4%), with a peak between years 1 and 2 (15.2%). During the first 5 years, patients with estrogen receptor (ER)--positive disease had a lower annualized hazard compared with those with ER-negative disease (9.9% v 11.5%; P = .01). However, beyond 5 years, patients with ER-positive disease had higher hazards (5 to 10 years: 5.4% v 3.3%; 10 to 15 years: 2.9% v 1.3%; 15 to 20 years: 2.8% v 1.2%; and 20 to 25 years: 1.3% v 1.4%; P < .001). Among patients with ER-positive disease, annualized hazards of recurrence remained elevated and fairly stable beyond 10 years, even for those with no axillary involvement (2.0%, 2.1%, and 1.1% for years 10 to 15, 15 to 20, and 20 to 25, respectively) and for those with one to three positive nodes (3.0%, 3.5%, and 1.5%, respectively).

Conclusion: Patients with ER-positive breast cancer maintain a significant recurrence rate during extended follow up. Strategies for follow up and treatments to prevent recurrences may be most efficiently applied and studied in patients with ER-positive disease followed for a long period of time.

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Mark D Zarella, Rebecca C Heintzelman, Nikolay K Popnikolov, Fernando U Garcia.
BMC Clin Pathol, 2018 Dec 24; 18. PMID: 30574014    Free PMC article.
Access to high-cost drugs for advanced breast cancer in Latin America, particularly trastuzumab.
Carlos Henrique Barrios, Tomás Reinert, Gustavo Werutsky.
Ecancermedicalscience, 2019 Feb 23; 13. PMID: 30792815    Free PMC article.
Combined Targeting of Estrogen Receptor Alpha and XPO1 Prevent Akt Activation, Remodel Metabolic Pathways and Induce Autophagy to Overcome Tamoxifen Resistance.
Eylem Kulkoyluoglu-Cotul, Brandi Patrice Smith, +12 authors, Zeynep Madak-Erdogan.
Cancers (Basel), 2019 Apr 17; 11(4). PMID: 30987380    Free PMC article.
Diagnosis of Primary Colorectal Carcinoma with Primary Breast Cancer: Associations or Connections?
Simcha Weissman, Jefferey Sebrow, +6 authors, Saad Saleem.
Cureus, 2019 Jun 12; 11(3). PMID: 31183268    Free PMC article.
Dynamic and subtype-specific interactions between tumour burden and prognosis in breast cancer.
S B Lee, H-K Kim, +13 authors, H-G Moon.
Sci Rep, 2020 Sep 24; 10(1). PMID: 32963275    Free PMC article.
Early treatment-related neutropenia predicts response to palbociclib.
Nicholas P McAndrew, Mark A Dickson, +10 authors, Angela DeMichele.
Br J Cancer, 2020 Jul 10; 123(6). PMID: 32641862    Free PMC article.
Inter-tumor genomic heterogeneity of breast cancers: comprehensive genomic profile of primary early breast cancers and relapses.
Caterina Fumagalli, Alberto Ranghiero, +8 authors, Massimo Barberis.
Breast Cancer Res, 2020 Oct 17; 22(1). PMID: 33059724    Free PMC article.
Assessment of IGF-1 expression in the peripheral blood of women with recurrent breast cancer.
Danylo Rafhael Costa-Silva, Maria da Conceição Barros-Oliveira, +18 authors, Benedito Borges da Silva.
Medicine (Baltimore), 2020 Oct 31; 99(43). PMID: 33120836    Free PMC article.
Clinical Implications of Serum 25-Hydroxyvitamin D Status after 5-Year Adjuvant Endocrine Therapy for Late Recurrence of Hormone Receptor-positive Breast Cancer.
Seung Taek Lim, Ye Won Jeon, Hongki Gwak, Young Jin Suh.
J Breast Cancer, 2020 Nov 07; 23(5). PMID: 33154825    Free PMC article.
Adherence to post-surgery follow-up assessment and its association with sociodemographic and disease characteristics in patients with breast cancer in Central China.
Ran Feng, Jingfeng Jing, +2 authors, Jinnan Gao.
BMC Cancer, 2020 Nov 14; 20(1). PMID: 33183247    Free PMC article.
Association of Circulating Tumor DNA With Disease-Free Survival in Breast Cancer: A Systematic Review and Meta-analysis.
Carolyn Cullinane, Christina Fleming, +5 authors, Henry Paul Redmond.
JAMA Netw Open, 2020 Nov 20; 3(11). PMID: 33211112    Free PMC article.
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Protein Corona Gold Nanoparticles Fingerprinting Reveals a Profile of Blood Coagulation Proteins in the Serum of HER2-Overexpressing Breast Cancer Patients.
María Del Pilar Chantada-Vázquez, Antonio Castro López, +3 authors, Cristina Núñez.
Int J Mol Sci, 2020 Nov 14; 21(22). PMID: 33182810    Free PMC article.
Can Complete Axillary Node Dissection Be Safely Omitted in Patients with Early Breast Cancer When the Sentinel Node Biopsy Is Positive for Malignancy? An Update for Clinical Practice.
Ritika Gera, Abdul Kasem, Kefah Mokbel.
In Vivo, 2018 Oct 24; 32(6). PMID: 30348682    Free PMC article.
Examination of a paradox: recurrent metastatic breast cancer incidence decline without improved distant disease survival: 1990-2011.
Judith Malmgren, Marc Hurlbert, Mary Atwood, Henry G Kaplan.
Breast Cancer Res Treat, 2018 Dec 19; 174(2). PMID: 30560462    Free PMC article.
Using natural language processing and machine learning to identify breast cancer local recurrence.
Zexian Zeng, Sasa Espino, +6 authors, Yuan Luo.
BMC Bioinformatics, 2018 Dec 29; 19(Suppl 17). PMID: 30591037    Free PMC article.
Systemic treatment and radiotherapy, breast cancer subtypes, and survival after long-term clinical follow-up.
Sherry X Yang, Eric C Polley.
Breast Cancer Res Treat, 2019 Feb 13; 175(2). PMID: 30746635    Free PMC article.
Risk of loco-regional recurrence and distant metastases of patients with invasive breast cancer up to ten years after diagnosis - results from a registry-based study from Germany.
Bernd Holleczek, Christa Stegmaier, +2 authors, Hermann Brenner.
BMC Cancer, 2019 May 31; 19(1). PMID: 31146706    Free PMC article.
Fourth-generation chimeric antigen receptor T cells targeting folate receptor alpha antigen expressed on breast cancer cells for adoptive T cell therapy.
Piriya Luangwattananun, Mutita Junking, +4 authors, Pa-Thai Yenchitsomanus.
Breast Cancer Res Treat, 2021 Jan 04; 186(1). PMID: 33389403
The lingering mysteries of metastatic recurrence in breast cancer.
Alessandra I Riggio, Katherine E Varley, Alana L Welm.
Br J Cancer, 2020 Nov 27; 124(1). PMID: 33239679    Free PMC article.
Androgen Receptor Expression and Breast Cancer Survival: Results From the Nurses' Health Studies.
Kevin H Kensler, Elizabeth M Poole, +10 authors, Rulla M Tamimi.
J Natl Cancer Inst, 2018 Nov 18; 111(7). PMID: 30445651    Free PMC article.
Long-Term Prognostication for 20 114 Women With Small and Node-Negative Breast Cancer (T1abN0).
David Jaraj, Jonas Höijer, +9 authors, Pettersson Andreas.
JNCI Cancer Spectr, 2021 Jan 15; 5(1). PMID: 33442658    Free PMC article.
The clinical usefulness of the CTS5 in the prediction of late distant recurrence in postmenopausal women with estrogen receptor-positive early breast cancer.
Wakako Tajiri, Hideki Ijichi, +8 authors, Eriko Tokunaga.
Breast Cancer, 2020 Jul 01; 28(1). PMID: 32601800    Free PMC article.
Impact of Hormone Receptor Status on the Behaviour of HER2+ Breast Cancer.
Iveta Kolarova, Ladislav Dusek, +11 authors, Jiri Jarkovsky.
In Vivo, 2020 Nov 05; 34(6). PMID: 33144452    Free PMC article.
Genistein Reduces the Risk of Local Mammary Cancer Recurrence and Ameliorates Alterations in the Gut Microbiota in the Offspring of Obese Dams.
Fabia de Oliveira Andrade, Fang Liu, +7 authors, Leena Hilakivi-Clarke.
Nutrients, 2021 Jan 15; 13(1). PMID: 33440675    Free PMC article.
Cost-effectiveness of MR-mammography as a solitary imaging technique in women with dense breasts: an economic evaluation of the prospective TK-Study.
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Eur Radiol, 2020 Aug 29; 31(2). PMID: 32856166    Free PMC article.
Intensity of metastasis screening and survival outcomes in patients with breast cancer.
Jong-Ho Cheun, Jigwang Jung, +8 authors, Hyeong-Gon Moon.
Sci Rep, 2021 Feb 04; 11(1). PMID: 33531549    Free PMC article.
Validation of the Role of Thrombin Generation Potential by a Fully Automated System in the Identification of Breast Cancer Patients at High Risk of Disease Recurrence.
Patricia Gomez-Rosas, Marina Pesenti, +19 authors, HYPERCAN Investigators.
TH Open, 2021 Feb 16; 5(1). PMID: 33585786    Free PMC article.
Twenty-year risks of breast cancer-specific mortality for stage III breast cancer in the surveillance, epidemiology, and end results registry.
José P Leone, Bernardo A Leone, +7 authors, Nancy U Lin.
Breast Cancer Res Treat, 2021 Feb 17; 187(3). PMID: 33590387
Does Failure to Achieve Pathologic Complete Response with Neoadjuvant Chemotherapy Identify Node-Negative Patients Who Would Benefit from Postmastectomy Radiation or Regional Nodal Irradiation?
Angelena Crown, Mithat Gonen, Tiana Le, Monica Morrow.
Ann Surg Oncol, 2020 Sep 23; 28(3). PMID: 32959140    Free PMC article.
Impact of Pathologic Complete Response following Neoadjuvant Chemotherapy ± Trastuzumab in Locally Advanced Breast Cancer.
Taher Al-Tweigeri, Mahmoud Elshenawy, +9 authors, Adher Al Sayed.
J Oncol, 2021 Feb 26; 2021. PMID: 33628241    Free PMC article.
PD-L1 Protein Expression in Middle Eastern Breast Cancer Predicts Favorable Outcome in Triple-Negative Breast Cancer.
Sandeep Kumar Parvathareddy, Abdul K Siraj, +6 authors, Khawla S Al-Kuraya.
Cells, 2021 Jan 29; 10(2). PMID: 33503961    Free PMC article.
Early Discontinuation of Endocrine Therapy and Recurrence of Breast Cancer among Premenopausal Women.
Lindsay J Collin, Deirdre P Cronin-Fenton, +10 authors, Timothy L Lash.
Clin Cancer Res, 2020 Dec 19; 27(5). PMID: 33334905    Free PMC article.
Molecular Biomarkers for Contemporary Therapies in Hormone Receptor-Positive Breast Cancer.
Allegra Freelander, Lauren J Brown, +4 authors, Elgene Lim.
Genes (Basel), 2021 Mar 07; 12(2). PMID: 33671468    Free PMC article.
Predictors and outcomes in breast cancer patients who did or did not pursue fertility preservation.
Molly B Moravek, Rafael Confino, +6 authors, Mary Ellen Pavone.
Breast Cancer Res Treat, 2021 Jan 05; 186(2). PMID: 33392838
Patient, Oncologist, and Payer Preferences for Adjuvant Endocrine Therapy and CDK4/6 Inhibitor Regimens in Early-Stage Breast Cancer: A Discrete Choice Experiment.
Kathleen Beusterien, Martine C Maculaitis, +3 authors, Ernest H Law.
Patient Prefer Adherence, 2021 Mar 30; 15. PMID: 33776424    Free PMC article.
A Clinical Decision Support System for Predicting Invasive Breast Cancer Recurrence: Preliminary Results.
Raffaella Massafra, Agnese Latorre, +13 authors, Vito Lorusso.
Front Oncol, 2021 Mar 30; 11. PMID: 33777733    Free PMC article.
Opioid Use Disorder and Overdose in Older Adults With Breast, Colorectal, or Prostate Cancer.
Andrew W Roberts, Samantha Eiffert, +2 authors, Devon K Check.
J Natl Cancer Inst, 2020 Aug 18; 113(4). PMID: 32805032    Free PMC article.
Loco-regional recurrence trend and prognosis in young women with breast cancer according to molecular subtypes: analysis of 1099 cases.
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World J Surg Oncol, 2021 Apr 15; 19(1). PMID: 33849563    Free PMC article.
The development and initial validation of the Breast Cancer Recurrence instrument (BreastCaRe)-a patient-reported outcome measure for detecting symptoms of recurrence after breast cancer.
Beverley Lim Høeg, Lena Saltbæk, +5 authors, Pernille Envold Bidstrup.
Qual Life Res, 2021 Apr 18; 30(9). PMID: 33864164
Factors associated with late risks of breast cancer-specific mortality in the SEER registry.
José P Leone, Carlos T Vallejo, +8 authors, Nancy U Lin.
Breast Cancer Res Treat, 2021 Apr 25; 189(1). PMID: 33893907    Free PMC article.
Risk of recurrence among patients with HR-positive, HER2-negative, early breast cancer receiving adjuvant endocrine therapy: A systematic review and meta-analysis.
Elizabeth M Salvo, Abril Oliva Ramirez, +4 authors, Imtiaz A Samjoo.
Breast, 2021 Mar 08; 57. PMID: 33677313    Free PMC article.
Evaluation of circulating tumor cells as a prognostic biomarker for early recurrence in stage II-III breast cancer patients using CytoSorter® system: a retrospective study.
Lidan Jin, Wan-Hung Fan, +2 authors, Wenhe Zhao.
PeerJ, 2021 May 15; 9. PMID: 33987029    Free PMC article.
Innovative Approaches in the Battle Against Cancer Recurrence: Novel Strategies to Combat Dormant Disseminated Tumor Cells.
Scott Sauer, Damon R Reed, +3 authors, Dalit Barkan.
Front Oncol, 2021 May 15; 11. PMID: 33987095    Free PMC article.
Recent advances in the treatment of hormone receptor-positive/human epidermal growth factor 2-positive advanced breast cancer.
Huimin Lv, Min Yan, Zefei Jiang.
Ther Adv Med Oncol, 2021 May 18; 13. PMID: 33995599    Free PMC article.
Effects of Diet and Exercise-Induced Weight Loss on Biomarkers of Inflammation in Breast Cancer Survivors: A Systematic Review and Meta-analysis.
Tyler J Bruinsma, Anne-Marie Dyer, +2 authors, Kathleen M Sturgeon.
Cancer Epidemiol Biomarkers Prev, 2021 Mar 20; 30(6). PMID: 33737299    Free PMC article.
A rude awakening from tumour cells.
Fatima Cardoso, Giuseppe Curigliano.
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Identification of inhibitory immune checkpoints and relevant regulatory pathways in breast cancer stem cells.
Haojun Shi, Yisi Yang.
Cancer Med, 2021 May 02; 10(11). PMID: 33932112    Free PMC article.
Immunoregulatory Monocyte Subset Promotes Metastasis Associated With Therapeutic Intervention for Primary Tumor.
Takumi Shibuya, Asami Kamiyama, +13 authors, Satoshi Yotsumoto.
Front Immunol, 2021 Jun 25; 12. PMID: 34163472    Free PMC article.
Validation of a liquid biopsy assay with molecular and clinical profiling of circulating tumor DNA.
Justin D Finkle, Hala Boulos, +12 authors, Nike Beaubier.
NPJ Precis Oncol, 2021 Jul 04; 5(1). PMID: 34215841    Free PMC article.
Assessment of 25-Year Survival of Women With Estrogen Receptor-Positive/ERBB2-Negative Breast Cancer Treated With and Without Tamoxifen Therapy: A Secondary Analysis of Data From the Stockholm Tamoxifen Randomized Clinical Trial.
Huma Dar, Annelie Johansson, +9 authors, Linda S Lindström.
JAMA Netw Open, 2021 Jul 01; 4(6). PMID: 34190995    Free PMC article.
Inorganic Nanomaterial-Mediated Gene Therapy in Combination with Other Antitumor Treatment Modalities.
Guanyou Lin, Richard A Revia, Miqin Zhang.
Adv Funct Mater, 2021 Aug 10; 31(5). PMID: 34366761    Free PMC article.