Abstract
The purpose of this study was to examine influencing factors and outcomes of accelerated partial breast irradiation through brachytherapy (APBIb) versus whole breast irradiation (WBI) for ductal carcinoma in situ (DCIS). From the Surveillance Epidemiology and End Results program of the US National Cancer Institute, we identified 40,749 women who were diagnosed with first primary DCIS between 2002 and 2011 and treated with breast-conserving surgery and radiotherapy. A multi-level logistic regression analysis was performed to estimate odds ratios of APBIb use. Hazard ratios (HRs) of developing ipsilateral breast tumors (IBTs) and contralateral breast tumors (CBTs) were analyzed in 1962 patients with APBIb and 7203 propensity score-matched patients with WBI, using Cox proportional hazards regression. Overall, 2212 (4.5 %) of 40,749 women (the whole cohort) received APBIb. Factors associated with the increased use of APBIb included older age, non-Hispanic white race/ethnicity, smaller tumor size, hormone receptor positivity, comedo subtypes, and urban residence. During the 46-month follow-up, 74 (0.8 %) and 131 (1.4 %) of 9165 propensity score-matched patients developed IBTs and CBTs, respectively. Compared with WBI, APBIb was associated with a significantly increased risk of IBTs (HR 1.74; 95 % CI 1.06–2.85) but not CBTs (OR 0.91; 95 % CI 0.59–1.41). This population-based study suggests that APBIb use for DCIS was influenced by patient and tumor characteristics as well as urbanization of residence. We observed a moderately increased IBT risk associated with APBIb versus WBI, suggesting that APBIb should be used with caution for DCIS before data from randomized controlled trials with long-term follow-ups are available.
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Clarke M, Collins R, Darby S, Davies C, Elphinstone P, Evans E, Godwin J, Gray R, Hicks C, James S, MacKinnon E, McGale P, McHugh T, Peto R, Taylor C, Wang Y (2005) Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet 366:2087–2106
Correa C, McGale P, Taylor C, Wang Y, Clarke M, Davies C, Peto R, Bijker N, Solin L, Darby S (2010) Overview of the randomized trials of radiotherapy in ductal carcinoma in situ of the breast. J Natl Cancer Inst Monogr 2010:162–177
Fisher B, Anderson S, Bryant J, Margolese RG, Deutsch M, Fisher ER, Jeong JH, Wolmark N (2002) Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med 347:1233–1241
Cox JA, Swanson TA (2013) Current modalities of accelerated partial breast irradiation. Nat Rev Clin Oncol 10:344–356
Smith GL, Xu Y, Buchholz TA, Smith BD, Giordano SH, Haffty BG, Vicini FA, White JR, Arthur DW, Harris JR, Shih YC (2011) Brachytherapy for accelerated partial-breast irradiation: a rapidly emerging technology in breast cancer care. J Clin Oncol 29:157–165
Hattangadi JA, Taback N, Neville BA, Harris JR, Punglia RS (2012) Accelerated partial breast irradiation using brachytherapy for breast cancer: patterns in utilization and guideline concordance. J Natl Cancer Inst 104:29–41
Czechura T, Winchester DJ, Pesce C, Huo D, Winchester DP, Yao K (2013) Accelerated partial-breast irradiation versus whole-breast irradiation for early-stage breast cancer patients undergoing breast conservation, 2003-2010: a report from the national cancer data base. Ann Surg Oncol 20:3223–3232
Roberts KB, Soulos PR, Herrin J, Yu JB, Long JB, Dostaler E, Gross CP (2013) The adoption of new adjuvant radiation therapy modalities among Medicare beneficiaries with breast cancer: clinical correlates and cost implications. Int J Radiat Oncol Biol Phys 85:1186–1192
Smith BD, Arthur DW, Buchholz TA, Haffty BG, Hahn CA, Hardenbergh PH, Julian TB, Marks LB, Todor DA, Vicini FA, Whelan TJ, White J, Wo JY, Harris JR (2009) Accelerated partial breast irradiation consensus statement from the American Society for Radiation Oncology (ASTRO). Int J Radiat Oncol Biol Phys 74:987–1001
Yao K, Czechura T, Liederbach E, Winchester DJ, Pesce C, Shaikh A, Winchester DP, Huo D (2014) Utilization of accelerated partial breast irradiation for ductal carcinoma in situ, 2003–2011: report from the national cancer database. Ann Surg Oncol 21:3457–3465
Vicini F, Shah C, Ben Wilkinson J, Keisch M, Beitsch P, Lyden M (2013) Should ductal carcinoma-in situ (DCIS) be removed from the ASTRO consensus panel cautionary group for off-protocol use of accelerated partial breast irradiation (APBI)? A pooled analysis of outcomes for 300 patients with DCIS treated with APBI. Ann Surg Oncol 20:1275–1281
Surveillance, Epidemiology, and End Results (SEER) Program (2014) Research Data (1973–2011), National Cancer Institute, DCCPS, Surveillance Research Program, Cancer Statistics Branch. Released April 2014, based on the November 2013 submission. http://seer.cancer.gov/. Accessed 31 May 2014
Lian M, Schootman M, Doubeni CA, Park Y, Major JM, Stone RA, Laiyemo AO, Hollenbeck AR, Graubard BI, Schatzkin A (2011) Geographic variation in colorectal cancer survival and the role of small-area socioeconomic deprivation: a multilevel survival analysis of the NIH-AARP diet and health study cohort. Am J Epidemiol 174:828–838
Martinez SR, Shah DR, Tseng WH, Canter RJ, Bold RJ (2012) Rural–urban disparities in use of post-lumpectomy radiation. Med Oncol 29:3250–3257
Johnson CH, Peace S, Adamo P, Fritz A, Percy-Laurry A, Edwards BK (2007) The 2007 multiple primary and histology coding rules. National Cancer Institute, Surveillance, Epidemiology and End Results Program, Bethesda
Austin PC, Grootendorst P, Anderson GM (2007) A comparison of the ability of different propensity score models to balance measured variables between treated and untreated subjects: a Monte Carlo study. Stat Med 26:734–753
Brookhart MA, Schneeweiss S, Rothman KJ, Glynn RJ, Avorn J, Sturmer T (2006) Variable selection for propensity score models. Am J Epidemiol 163:1149–1156
Shamliyan T, Wang SY, Virnig BA, Tuttle TM, Kane RL (2010) Association between patient and tumor characteristics with clinical outcomes in women with ductal carcinoma in situ. J Natl Cancer Inst Monogr 2010:121–129
Newman LA, Griffith KA, Jatoi I, Simon MS, Crowe JP, Colditz GA (2006) Meta-analysis of survival in African American and white American patients with breast cancer: ethnicity compared with socioeconomic status. J Clin Oncol 24:1342–1349
Nguyen-Pham S, Leung J, McLaughlin D (2014) Disparities in breast cancer stage at diagnosis in urban and rural adult women: a systematic review and meta-analysis. Ann Epidemiol 24:228–235
Austin PC (2011) Optimal caliper widths for propensity-score matching when estimating differences in means and differences in proportions in observational studies. Pharm Stat 10:150–161
Austin PC (2009) Balance diagnostics for comparing the distribution of baseline covariates between treatment groups in propensity-score matched samples. Stat Med 28:3083–3107
Austin PC (2014) The use of propensity score methods with survival or time-to-event outcomes: reporting measures of effect similar to those used in randomized experiments. Stat Med 33:1242–1258
Lin DY, Wei LJ (1989) The robust inference for the proportional hazards model. J Am Stat Assoc 84:1074–1078
Schneeweiss S (2006) Sensitivity analysis and external adjustment for unmeasured confounders in epidemiologic database studies of therapeutics. Pharmacoepidemiol Drug Saf 15:291–303
Proxima Therapeutics Announces New Reimbursement Codes for MammoSite Radiation Therapy System (2004) Business Wire. http://www.thefreelibrary.com/Proxima+Therapeutics+Announces+New+Reimbursement+Codes+for+Mammosite.-a0115232206. Accessed 28 May 2014
Wang SY, Shamliyan T, Virnig BA, Kane R (2011) Tumor characteristics as predictors of local recurrence after treatment of ductal carcinoma in situ: a meta-analysis. Breast Cancer Res Treat 127:1–14
Abbott AM, Habermann EB, Tuttle TM (2011) Trends in the use of implantable accelerated partial breast irradiation therapy for early stage breast cancer in the United States. Cancer 117:3305–3310
Yao N, Matthews SA, Hillemeier MM, Anderson RT (2013) Radiation therapy resources and guideline-concordant radiotherapy for early-stage breast cancer patients in an underserved region. Health Serv Res 48:1433–1449
Shah C, Badiyan S, Ben Wilkinson J, Vicini F, Beitsch P, Keisch M, Arthur D, Lyden M (2013) Treatment efficacy with accelerated partial breast irradiation (APBI): final analysis of the American Society of Breast Surgeons MammoSite((R)) breast brachytherapy registry trial. Ann Surg Oncol 20:3279–3285
Benitez PR, Streeter O, Vicini F, Mehta V, Quiet C, Kuske R, Hayes MK, Arthur D, Kuerer H, Freedman G, Keisch M, Dipetrillo T, Khan D, Hudes R (2006) Preliminary results and evaluation of MammoSite balloon brachytherapy for partial breast irradiation for pure ductal carcinoma in situ: a phase II clinical study. Am J Surg 192:427–433
Abbott AM, Portschy PR, Lee C, Le CT, Han LK, Washington T, Kinney M, Bretzke M, Tuttle TM (2013) Prospective multicenter trial evaluating balloon-catheter partial-breast irradiation for ductal carcinoma in situ. Int J Radiat Oncol Biol Phys 87:494–498
Polgar C, Fodor J, Major T, Sulyok Z, Kasler M (2013) Breast-conserving therapy with partial or whole breast irradiation: ten-year results of the Budapest randomized trial. Radiother Oncol 108:197–202
Vaidya JS, Tobias JS, Baum M, Wenz F, Kraus-Tiefenbacher U, D’Souza D, Keshtgar M, Massarut S, Hilaris B, Saunders C, Joseph D (2005) TARGeted Intraoperative radiotherapy (TARGIT): an innovative approach to partial-breast irradiation. Semin Radiat Oncol 15:84–91
Orecchia R, Ciocca M, Lazzari R, Garibaldi C, Leonardi MC, Luini A, Intra M, Gatti G, Veronesi P, Petit JI, Veronesi U (2003) Intraoperative radiation therapy with electrons (ELIOT) in early-stage breast cancer. Breast 12:483–490
Polgar C, Strnad V, Major T (2005) Brachytherapy for partial breast irradiation: the European experience. Semin Radiat Oncol 15:116–122
McCormick B (2005) Partial-breast radiation for early staged breast cancers: hypothesis, existing data, and a planned phase III trial. J Natl Compr Cancer Netw 3:301–307
Ontario Clinical Oncology Group (OCOG) (2010) Canadian Institutes of Health Research (CIHR), Canadian Breast Cancer Research Alliance. RAPID: Randomized Trial of Accelerated Partial Breast Irradiation. http://clinicaltrials.gov/ct2/show/NCT00282035. Accessed 28 May 2014
Coles C, Yarnold J (2006) The IMPORT trials are launched (September 2006). Clin Oncol (R Coll Radiol) 18:587–590
Breast cancer with low risk of local recurrence: partial and accelerated radiation with three-dimensional conformal radiotherapy (3DCRT) vs. standard radiotherapy after conserving surgery (phase III study). http://groups.eortc.be/radio/res/irma/synopsis_trial_irma1.pdf. Accessed 28 May 2014
Radiation therapy (WBI versus PBI) in treating women who have undergone surgery for ductal carcinoma in situ or stage I or stage II breast cancer. http://clinicaltrials.gov/ct2/show/study/NCT00103181. Accessed 28 May 2014
Wang SY, Chu H, Shamliyan T, Jalal H, Kuntz KM, Kane RL, Virnig BA (2012) Network meta-analysis of margin threshold for women with ductal carcinoma in situ. J Natl Cancer Inst 104:507–516
Jawad MS, Wilkinson JB, Shah C, Wobb J, Stone B, Fowler A, Mitchell CK, Wallace M, Chen PY, Grills IS (2012) Impact of lymphovascular space invasion, extensive intraductal component, and multifocality on outcomes following accelerated partial breast irradiation. Int J Radiat Oncol Biol Phys 84:S246
Smith GL, Xu Y, Buchholz TA, Giordano SH, Jiang J, Shih YC, Smith BD (2012) Association between treatment with brachytherapy vs whole-breast irradiation and subsequent mastectomy, complications, and survival among older women with invasive breast cancer. JAMA 307:1827–1837
Benson JR, Wishart GC (2013) Predictors of recurrence for ductal carcinoma in situ after breast-conserving surgery. Lancet Oncol 14:e348–e357
Allegra CJ, Aberle DR, Ganschow P, Hahn SM, Lee CN, Millon-Underwood S, Pike MC, Reed SD, Saftlas AF, Scarvalone SA, Schwartz AM, Slomski C, Yothers G, Zon R (2010) National institutes of health state-of-the-science conference statement: diagnosis and management of ductal carcinoma in situ September 22–24, 2009. J Natl Cancer Inst 102:161–169
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YL and GAC are supported by the Barnes-Jewish Hospital Foundation, St. Louis, Missouri. ML is supported in part by a Career Development Award from the National Cancer Institute (K07 CA178331). DTS is supported by the Washington University School of Medicine Dean’s Fellowship.
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Liu, Y., Schloemann, D.T., Lian, M. et al. Accelerated partial breast irradiation through brachytherapy for ductal carcinoma in situ: factors influencing utilization and risks of second breast tumors. Breast Cancer Res Treat 151, 199–208 (2015). https://doi.org/10.1007/s10549-015-3389-0
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DOI: https://doi.org/10.1007/s10549-015-3389-0