Abstract
Existing evidence suggests that preoperative breast magnetic resonance imaging (MRI) might not improve surgical outcomes in the general breast cancer population. To determine if patients differentially benefit from breast MRI, we examined surgical outcomes—initial mastectomy, reoperation, and final mastectomy rates—among patients grouped by histologic type. We identified women diagnosed with early-stage breast cancer from 2004 to 2007 in the SEER-Medicare dataset. We classified patients as having invasive ductal carcinoma (IDC), invasive lobular carcinoma (ILC), mixed ductal/lobular carcinoma (IDLC) or other histologic type. Medicare claims were used to identify breast MRI and definitive surgeries during the initial surgical treatment episode. We used propensity score methods to account for the differential likelihood of exposure to MRI. Of the 20,332 patients who met our inclusion criteria for this study, 12.2 % had a preoperative breast MRI. Patients with ILC as compared to other histologic groups were most likely to receive MRI [OR 2.32; 95 % CI (2.02–2.67)]. In the propensity score-adjusted analyses, breast MRI was associated with an increased likelihood of an initial mastectomy for all patients and among all histologic subgroups. Among patients with ILC, having a breast MRI was associated with lower odds of a reoperation [OR 0.59; 95 % CI (0.40–0.86)], and an equal likelihood of a final mastectomy compared to similar patients without a breast MRI. Overall and among patients with IDC and IDLC, breast MRI was not significantly associated with a likelihood of a reoperation but was associated with greater odds of a final mastectomy. Our study provides evidence in support of the targeted use of preoperative breast MRI among patients with ILC to improve surgical planning; it does not provide evidence for the routine use of breast MRI among all newly diagnosed breast cancer patients or among patients with IDC.
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Introduction
Preoperative breast magnetic resonance imaging (MRI) is increasingly used to assess the extent of breast tumor involvement and to inform surgical decision-making for older patients with early-stage invasive breast cancer [1–4]. Despite its rapid adoption, there is a growing body of evidence—including two randomized controlled trials (RCT) and several population based studies—that suggests routine use of preoperative breast MRI results in more extensive surgeries without clear evidence of clinical benefit such as improved surgical outcomes [4–8]. Due to the lack of evidence demonstrating improved outcomes for patients with preoperative breast MRI in the general breast cancer population, it is important to examine and identify subpopulations of breast cancer patients in which the imaging technique may be the most beneficial.
Because of the diffuse growth pattern of invasive lobular carcinoma (ILC), the second most common histologic type of invasive breast cancer, it has been suggested that patients with ILC may be likely more to benefit from preoperative breast MRI than women with invasive ductal carcinoma (IDC) or other histologic types [9, 10]. As compared to women with IDC, women with ILC are more prone to tumors not detected with mammography and ultrasound examination [11, 12], to multifocal and multicentric breast involvement [13], and to have higher reoperation rates [14–16]. Preoperative breast MRI has been found to be highly sensitive in detecting lesions not seen using mammography or ultrasound among patients with ILC [17]. However, only a few studies have examined the association between breast MRI and surgical outcomes in women with ILC [5, 18–20]. These studies were limited in that they were single institution studies [18–20] and an RCT from the United Kingdom [5] with a small number of ILC patients from settings with distinct surgical treatment patterns, health service resources, and insurance structures that may not be generalizable to the US elderly population. A meta-analysis among ILC patients found that breast MRI was associated with an increased likelihood of mastectomy but found only weak evidence that breast MRI was associated with a lower likelihood of a reoperation [8]. Thus, additional evidence is needed to determine the association between preoperative breast MRI and surgical outcomes among patients with ILC in a sample comparable to the US elderly population.
In this retrospective, population-based study, we used the Surveillance, Epidemiology, and End Results (SEER)-Medicare linked dataset to assess the utilization and potential benefits of preoperative breast MRI among newly diagnosed, elderly breast cancer patients by histologic subgroup—IDC, ILC, and IDLC. To evaluate the benefit of breast MRI among different histologic subgroups, we examined the association between preoperative breast MRI and surgical outcomes—initial mastectomy, reoperation, and final mastectomy—for all patients and within each histologic subgroup using propensity score methods.
Methods
Data
We conducted a retrospective study using the SEER-Medicare linked dataset, which is derived from a consortium of population-based cancer registries across the United States linked to Medicare administrative data and healthcare claims [21]. The SEER dataset comprises 17 registries nationwide covers approximately 25 % of the incident US cancer population, and is nearly nationally representative [21]. The SEER data contain demographic and incident cancer characteristics, including histology, grade, and stage. Medicare covers payment for hospital services, physician services, some drug therapy, and other medical services for more than 97 % of Americans aged 65 and older [22]. The Medicare claims provide information about the use and cost of health care services and co-morbid health conditions. The National Cancer Institute (NCI) hospital file contains hospital-level information, including staffing, structure, research network affiliation, and information on accreditation [22].
Study population
This study’s cohort was composed of women aged 66 or older diagnosed with their first, unilateral, pathologically confirmed, stage I-IIB breast cancer [American Joint Committee on Cancer (AJCC) sixth edition] between January 1, 2004 and December 31, 2007. To capture each patient’s complete claims experience, we excluded women who were not continuously enrolled in Medicare Part A and Part B or who were enrolled in a health maintenance organization during the study period. Since this study focuses on the utilization of preoperative breast MRI for surgical planning, we excluded women who received neoadjuvant chemotherapy prior to surgery because breast MRI also is used to measure tumor response to neoadjuvant chemotherapy [23–27]. In order to limit the cohort to women in whom either breast conserving surgery or a mastectomy was likely to be considered, we excluded patients with tumors larger than 5 cm [28]. Women who were diagnosed with a second primary cancer identified in SEER within 12 months of diagnosis were excluded in order to avoid including claims for surgeries for second primaries in the initial surgical treatment episode.
To capture health services received by the patients, we examined all claims in Medicare outpatient, inpatient, and physician claims files to identify breast cancer treatments and surgical procedures during the initial surgical treatment episode. Treatments were identified using the American Medical Association Current Procedural Terminology (CPT) and the Healthcare Common Procedure Classification System (HCPCS) codes (for all codes used see Table S1). We defined the initial surgical treatment episode as the time period beginning with the first claim with a diagnosis code for a suspected breast disorder (e.g., lump or mass in breast, or abnormal mammogram) 12 or fewer months prior to the SEER diagnosis. The initial surgical treatment episode ended with the claim for a definitive surgery before a gap in surgery of more than 90 days [29, 30]. We defined definitive surgery as either a partial mastectomy or mastectomy and did not consider open biopsies or breast excisions to be definitive surgeries [7, 31, 32]. Patients who had conflicting claims for a mastectomy and a partial mastectomy on the same day or who did not have their first definitive surgery within 4 months of their SEER-diagnosis were excluded.
Each patient’s tumor histology was classified using International Classification of Diseases for Oncology (ICD-O-3) histologic codes for IDC (M-8500 or M-8521), ILC (M-8520), mixed ductal/lobular carcinoma (IDLC) (M-8522-4), and other histology. Patients with histologic codes that indicated pre-malignant or non-malignant lesions were excluded. Detailed study population and inclusion/exclusion criteria can be found in Table S2.
Variables and measures
Preoperative breast MRI receipt (our primary independent variable) and the three surgical outcomes of interest—initial surgery, reoperation after partial mastectomy, and final surgery (our dependent variables)—were identified by examining claims in the initial surgical treatment episode. Patients were classified as having a preoperative breast MRI if they had a claim for a breast MRI (CPT: 76093-94, 77058-59, HCPCS: C8903-C8908) before the date of their initial surgery. The initial surgery was defined as the first claim for partial mastectomy or mastectomy during the initial surgical treatment episode. For women with a partial mastectomy as their initial surgery, a reoperation was defined as a claim for another partial mastectomy or mastectomy after the date of the initial surgery but within the initial surgical treatment episode. A sensitivity analysis defining a reoperation as a claim after the initial surgery for an open breast excision, partial mastectomy, or mastectomy within the initial surgical treatment episode produced equivalent results to our main analysis. The final surgery was defined as the last definitive surgery in the initial surgical treatment episode.
We controlled for several other variables that have been previously shown to affect breast cancer surgical decision-making in our analyses [33, 34]. We obtained tumor characteristics from SEER including grade, tumor size, any node positivity, and hormone receptor status. We used the NCI Comorbidity Index method to account for competing health demands and risks of complications that may affect treatment selection [35]. Demographic characteristics examined included age group at diagnosis, marital status, race, Hispanic ethnicity, and SEER region. We included quartiles of the percentage of high school graduates in a given zip code of residence and included a person-level indicator for Medicare state buy-in coverage, which identified women who had their Medicare premiums and deductibles subsidized by the state during the study period owing to their financial status. We identified the facility where the initial surgery took place and linked it to the NCI Hospital file to identify whether or not the facility was a teaching hospital or a designated NCI Cancer Center, and constructed a variable for whether or not the facility was affiliated with NCI Cooperative Groups having breast cancer research portfolios [36]. We also included a variable measuring breast cancer surgical volume. To construct this variable, we used the number of breast cancer surgeries for each surgical facility from 2004 to 2009.
Statistical analysis
We compared unadjusted baseline characteristics between patients grouped by histologic type and breast MRI receipt using Pearson χ2 tests for categorical variables and Student’s t tests for continuous variables. Because previous studies using the SEER-Medicare dataset have shown that patients who receive a preoperative breast MRI differ from women who do not on observed baseline characteristics such as age, race, and health service area resources [1–4], we used propensity score methods to balance the groups of women with and without breast MRI on measured covariates and to control for potential confounders [37]. To estimate the treatment effect of breast MRI in the treated population (i.e., those patients with breast MRI), we used standardized mortality ratio (SMR) propensity score-based weighting [38]. Propensity scores for all patients and for each histologic group were generated using multivariate logistic regression including the patient and surgical facility characteristics described in the previous section [37]. Using SMR weighting, women with breast MRI received a weight of 1 and women without breast MRI were weighted with their propensity odds [38]. We assessed balance and the performance of the model by examining the distribution of propensity scores and covariates between the two groups (MRI vs no MRI) and the change in standardized difference for each variable before and after weighting [39, 40], and we determined the covariates were well balanced (Fig. S1). No patients from the Hawaii SEER region with ILC (N = 14) or IDLC (N = 18) had an MRI, thus these patients had a zero propensity for breast MRI and were excluded in those subgroup analyses. To generate our propensity score-weighted estimates, we used logistic regression with robust standard errors. Z test statistics and 95 % confidence intervals were used to examine the difference in the likelihood of our surgical outcomes between those women with and without a breast MRI. Traditional multivariate models are presented in the Supplementary Appendix (Tables S3–6) and were similar to our findings using propensity scores.
Analyses were performed using Stata version 12.0 (Stata Corporation, College Station, TX). All tests were conducted using a minimum significance level of 0.05.
Results
Characteristics of the study population
Of the 20,332 patients who met inclusion criteria, 14,357 (70.6 %) had IDC, 1,928 (9.5 %) had ILC, and 2,398 (11.8 %) had IDLC (Table 1). Demographic, tumor, and surgical facility characteristics significantly differed by histologic type for all variables. Notably, compared to other histologic types, women with ILC were more likely to have tumors that were larger and hormone receptor positive.
Overall, 2,471 (12.2 %) patients received a preoperative breast MRI. Breast MRI receipt differed by histologic type with 10.8 % of patients with IDC receiving a breast MRI compared to 20.5 % of patients with ILC (P value < 0.001). The number of patients receiving preoperative breast MRI increased over time for all patients and among all histologic types (Fig. 1). The subgroups of women with ILC and IDLC saw the greatest increase in use of preoperative breast MRI. From 2004 to 2007, the proportion of patients with preoperative breast MRI increased from 9.6 to 30.6 % of those with ILC, from 8.9 to 27.3 % of those with IDLC, and from 4.6 to 18.5 % of those with IDC.
In the multivariate logistic regression model predicting MRI receipt among all patients in our sample, women with ILC or IDLC were more likely to have received a breast MRI than women with IDC (Table S3). Women with a preoperative breast MRI were on average younger, diagnosed more recently, and with fewer comorbidities overall and among all histologic type subgroups. Women living in lower education areas had greater odds of having an MRI, but having a state buy-in insurance supplement was associated with lower odds of getting MRI. Women having their surgeries at facilities that were affiliated with cooperative groups and a high surgical volume had significantly greater odds of receiving a breast MRI.
Surgical outcomes
Initial mastectomy
Among the patients in our sample, 30.1 % of patients (N = 6,122) had a mastectomy as their initial surgery (Table 2). Patients with ILC had the highest rate of initial mastectomy (35.0 %, N = 675), and patients with IDLC had the lowest rate (28.7 %, N = 688). After propensity score adjustment (Fig. 2), having a preoperative breast MRI was significantly associated with greater odds of an initial mastectomy for all patients [odds ratio (OR) 1.33; 95 % confidence interval (CI) (1.19–1.48)] and among all histologic type subgroups [IDC OR 1.21; 95 % CI (1.07–1.38); ILC OR 1.48; 95 % CI (1.10–2.00); IDLC OR 1.98; 95 % CI (1.50–2.62)].
Reoperations
Overall, 20.6 % (N = 2,929) of women in our sample had an additional reoperation after having an initial breast conserving surgery. Reoperations were most common in women with ILC, (28.3 %, N = 355) and least common in women with IDC (19.1 %, N = 1,920). After propensity score adjustment, having a breast MRI was associated with lower odds of having a reoperation among women with ILC [OR 0.59; 95 % CI (0.40–0.86)], but was not significantly associated with reoperations among other histologic subgroups.
Final mastectomy
Of all patients in our sample, 35.5 % (N = 7,224) had a mastectomy as their only or final surgery. Among histologic type subgroups, patients with ILC had the highest percentage of final mastectomies (43.5 %, N = 839) and patients with IDC had the lowest (34.7 %, N = 4,984). After propensity score adjustment, breast MRI receipt was associated with increased odds of a final mastectomy among all patients [OR 1.20; 95 % CI (1.08–1.33)] and among patients with IDC [OR 1.21; 95 % CI (1.07–1.37)] and IDLC [1.43; 95 % CI (1.10–1.85)]. Having a breast MRI was not significantly associated with a final mastectomy in the subgroup of patients with ILC.
Discussion
In this large, population-based study, we found that the association between breast MRI and surgical outcomes differed by histologic subgroup. In particular, among women with ILC, breast MRI was associated with a reduced likelihood of a reoperation and an equal likelihood of a final mastectomy compared to similar patients without a breast MRI. We did not find breast MRI to be associated with improved surgical outcomes overall and among IDC patients and IDLC patients; In fact, in these groups of patients, preoperative breast MRI was significantly associated with an increased likelihood of more extensive surgeries—including both initial and final mastectomy—but not with reoperations.
This is the largest study of breast MRI among ILC patients (N = 1,928) to date. Previous research examining the association between breast MRI and surgical outcomes for ILC patients found conflicting results regarding the benefit of breast MRI [5, 8, 18–20]. Our findings are similar to a meta-analysis among ILC patients which found that breast MRI was significantly associated with an increased likelihood of an initial mastectomy and weakly associated with a lower likelihood of a reoperation [8]. Our results differed from the meta-analysis in that the meta-analysis reported that preoperative breast MRI was associated with an increased likelihood of a final mastectomy whereas we found that ILC patients with breast MRI were no more likely to have a final mastectomy than those ILC women who did not receive a preoperative breast MRI. Our results may differ because the included studies were single institution studies [18–20] and one RCT [5] which included only a small number of patients with ILC. Furthermore, these studies reflect surgical practices from single institutions or in the United Kingdom, where breast cancer treatment patterns, decision-making factors, health service/insurance structures, and fiscal considerations may be different than and not generalizable to the US elderly population.
Breast MRI may be most useful in women with ILC because the biologic and clinical features of ILC make it difficult to detect by screening and to determine the extent of disease. Women with ILC are more likely to be inadequately imaged with conventional assessment that includes mammography and sonography [11, 12], which in turn can complicate surgical planning and lead to suboptimal surgical outcomes for patients with ILC. We found that patients with ILC received more intensive surgical treatment than patients with other subtypes and were more likely to have an initial mastectomy (35 vs 30 %), a reoperation (28 vs 21 %), and a final mastectomy (44 vs 36 %) compared to all breast cancer patients. Thus, particularly as the incidence of ILC is increasing in older women [9], it is promising that breast MRI may be beneficial to optimize surgical planning and reduce reoperations in this group of women without compromising the likelihood of breast conservation.
Our results contribute to the growing body of literature documenting that routine breast MRI is associated with an increased likelihood of a mastectomy [4–6, 8, 41, 42] and not associated with a reduction in reoperations [5–8, 41–47] among all breast cancer patients. The results from our analyses among patients with IDC and IDLC provide novel evidence about the association between breast MRI and surgical outcomes in these histologic type subgroups.
Since preoperative breast MRI was not associated with improved surgical outcomes among older women with IDC and IDLC, it is important to assess the potential consequences of the increasing use of preoperative breast MRI in the general population. Concern exists that breast MRI may overestimate tumor size, resulting in a more extensive surgery than may be required to obtain negative margins. In our study, preoperative breast MRI was associated with an increased likelihood of an initial mastectomy and an increased likelihood of a final mastectomy overall and in patients with IDC or IDLC without a reduction in the likelihood of a reoperation. The association between breast MRI and mastectomies could be concerning if women are electing or surgeons are recommending more extensive surgery based on MRI findings that over-estimate the true extent of disease or could be adequately managed by radiation and systemic therapy [48]. Additionally, preoperative breast MRI may contribute to greater use of additional diagnostic procedures which carry their own potential morbidities. Studies have found that breast MRI may be associated with more downstream imaging such as follow-up ultrasounds, more biopsies, and treatment delay [44, 49, 50]. The increased morbidity that may arise from the downstream consequences of breast MRI in absence of clear clinical benefit is troubling as more breast cancer patients are having comparatively favorable prognoses, and many clinicians are focusing on reducing treatment burden and morbidity [51].
This study provides evidence to support the targeted use of preoperative breast MRI among patients with ILC. Given that women with ILC were more likely to have a preoperative breast MRI [OR 2.32; 95 % CI (2.02–2.67)] than women with other histologic types, some providers or surgical facilities may already be using ILC as section criteria to optimize the benefit of preoperative breast MRI. We did not find evidence to support routine use of preoperative breast MRI among all patients, however, the rapid increase in use of the imaging technique from 2004 to 2007 and the observed variation in preoperative breast MRI by provider and SEER region suggests that it is unlikely that breast MRI is being utilized solely among select subpopulations, such as women with ILC or women inadequately imaged using conventional assessment.
Our study is limited in several aspects. Like all observational studies, we were unable to control for unmeasured confounding. Using propensity score methods, we successfully balanced women with and without breast MRI on observed clinical, sociodemographic, and surgical facility variables, however, we were unable to balance the women on unobserved characteristics that may be associated with breast MRI and our outcomes, and thus we are concerned that our models are underspecified due to variables not available in our dataset. For example, the clinical rationale for why the MRI was ordered is unknown, and we are unable differentiate women who received an MRI as a part of routine preoperative work-up from those women who received an MRI because their tumors were inadequately imaged using conventional assessment. The specific MRI results for each patient are also unknown, and we are unable to verify the extent to which the MRI results changed surgical decision-making using claims data. These unknown factors may be associated with breast MRI receipt and also may influence surgical outcomes. Also, we were unable to control for women who chose to have an initial mastectomy instead of breast conserving surgery based on their preferences. Other mastectomy and reoperation risk factors not available in the SEER-Medicare data included information about multifocal disease, mammographic density and micro-calcifications, and surgeon experience and practice style [7, 34, 52–54]. We were, nevertheless, able to control for tumor size, grade and histology, age, advanced stage, hormone receptor negative status, which have also been reported as mastectomy and or reoperation risk factors [52].
As new and advanced imaging modalities such as breast MRI are introduced into clinical practice, it is important to generate evidence about their appropriate use and to inform their dissemination into practice. Our study provides evidence in support of the targeted use of preoperative breast MRI among patients with ILC to improve surgical planning. Our study also adds to the growing body of literature documenting that routine breast MRI among all breast cancer patients is associated with an increased likelihood of a mastectomy and not associated with a reduction in reoperations among the majority of breast cancer patients in whom it is used. Future research should examine the association between preoperative breast MRI and long-term outcomes such as breast cancer recurrence and survival, particularly among patients with ILC.
References
Sommer CA, Stitzenberg KB, Tolleson-Rinehart S, Carpenter WR, Carey TS (2011) Breast MRI utilization in older patients with newly diagnosed breast cancer. J Surg Res 170(1):77–83
Wang SY, Virnig BA, Tuttle TM, Jacobs DR, Kuntz KM, Kane RL (2013) Variability of preoperative breast MRI utilization among older women with newly diagnosed early-stage breast cancer. Breast J 19(6):627–636
Killelea BK, Lannin DR, Horvath LJ, Horowitz NR, Chagpar AB (2013) Factors associated with breast MRI use: a population-based analysis. Ann Surg Oncol 20(6):1798–1805
Killelea BK, Long JB, Chagpar AB, Ma X, Soulos PR, Ross JS, Gross CP (2013) Trends and clinical implications of preoperative breast MRI in medicare beneficiaries with breast cancer. Breast Cancer Res Treat 141(1):155–163
Turnbull L, Brown S, Harvey I, Olivier C, Drew P, Napp V, Hanby A, Brown J (2010) Comparative effectiveness of MRI in breast cancer (COMICE) trial: a randomised controlled trial. Lancet 375(9714):563–571
Peters NH, van Esser S, van den Bosch MA, Storm RK, Plaisier PW, van Dalen T, Diepstraten SC, Weits T, Westenend PJ, Stapper G et al (2011) Preoperative MRI and surgical management in patients with nonpalpable breast cancer: the MONET: randomised controlled trial. Eur J Cancer 47(6):879–886
Wang S-Y, Kuntz KM, Tuttle TM, Jacobs Jr DR, Kane RL, Virnig BA: The association of preoperative breast magnetic resonance imaging and multiple breast surgeries among older women with early stage breast cancer. Breast Cancer Res Treat 2013
Houssami N, Turner R, Morrow M (2013) Preoperative magnetic resonance imaging in breast cancer: meta-analysis of surgical outcomes. Ann Surg 257(2):249–255
Li CI, Anderson BO, Daling JR, Moe RE (2003) Trends in incidence rates of invasive lobular and ductal breast carcinoma. JAMA 289(11):1421–1424
Sardanelli F (2010) Overview of the role of pre-operative breast MRI in the absence of evidence on patient outcomes. Breast 19(1):3–6
Krecke KN, Gisvold J (1993) Invasive lobular carcinoma of the breast: mammographic findings and extent of disease at diagnosis in 184 patients. Am J Roentgenol 161(5):957–960
Yeatman TJ, Cantor AB, Smith TJ, Smith SK, Reintgen DS, Miller MS, Ku NN, Baekey PA, Cox CE (1995) Tumor biology of infiltrating lobular carcinoma. Implications for management. Ann Surg 222(4):549–559 discussion 559–561
Silverstein MJ, Lewinsky BS, Waisman JR, Gierson ED, Colburn WJ, Senofsky GM, Gamagami P (2006) Infiltrating lobular carcinoma. Is it different from infiltrating duct carcinoma? Cancer 73(6):1673–1677
Waljee JF, Hu ES, Newman LA, Alderman AK (2008) Predictors of re-excision among women undergoing breast-conserving surgery for cancer. Ann Surg Oncol 15(5):1297–1303
Keskek M, Kothari M, Ardehali B, Betambeau N, Nasiri N, Gui G (2004) Factors predisposing to cavity margin positivity following conservation surgery for breast cancer. Eur J Surg Oncol 30(10):1058–1064
Van den Broek N, van der Sangen MJC, Van de Poll-Franse L, van Beek MWPM, Nieuwenhuijzen GAP, Voogd A (2007) Margin status and the risk of local recurrence after breast-conserving treatment of lobular breast cancer. Breast Cancer Res Treat 105(1):63–68
Mann RM, Hoogeveen YL, Blickman JG, Boetes C (2008) MRI compared to conventional diagnostic work-up in the detection and evaluation of invasive lobular carcinoma of the breast: a review of existing literature. Breast Cancer Res Treat 107(1):1–14
Heil J, Bühler A, Golatta M, Rom J, Harcos A, Schipp A, Rauch G, Junkermann H, Sohn C (2011) Does a supplementary preoperative breast MRI in patients with invasive lobular breast cancer change primary and secondary surgical interventions? Ann Surg Oncol 18(8):2143–2149
Mann RM, Loo CE, Wobbes T, Bult P, Barentsz JO, Gilhuijs KGA, Boetes C (2010) The impact of preoperative breast MRI on the re-excision rate in invasive lobular carcinoma of the breast. Breast Cancer Res Treat 119(2):415–422
McGhan LJ, Wasif N, Gray RJ, Giurescu ME, Pizzitola VJ, Lorans R, Ocal IT, Stucky CCH, Pockaj BA (2010) Use of preoperative magnetic resonance imaging for invasive lobular cancer: good, better, but maybe not the best? Ann Surg Oncol 17:255–262
Warren JL, Harlan LC, Fahey A, Virnig BA, Freeman JL, Klabunde CN, Cooper GS, Knopf KB (2002) Utility of the SEER-medicare data to identify chemotherapy use. Med Care 40(8):IV–55–61
Warren JL, Klabunde CN, Schrag D, Bach PB, Riley GF (2002) Overview of the SEER-Medicare data: content, research applications, and generalizability to the United States elderly population. Med Care 40(8 Suppl):3–18
Croshaw R, Shapiro-Wright H, Svensson E, Erb K, Julian T (2011) Accuracy of clinical examination, digital mammogram, ultrasound, and MRI in determining postneoadjuvant pathologic tumor response in operable breast cancer patients. Ann Surg Oncol 18(11):3160–3163
McGuire KP, Toro-Burguete J, Dang H, Young J, Soran A, Zuley M, Bhargava R, Bonaventura M, Johnson R, Ahrendt G (2011) MRI staging after neoadjuvant chemotherapy for breast cancer: does tumor biology affect accuracy? Ann Surg Oncol 18(11):3149–3154
Chen JH, Feig B, Agrawal G, Yu H, Carpenter PM, Mehta RS, Nalcioglu O, Su MY (2008) MRI evaluation of pathologically complete response and residual tumors in breast cancer after neoadjuvant chemotherapy. Cancer 112(1):17–26
Marinovich ML, Sardanelli F, Ciatto S, Mamounas E, Brennan M, Macaskill P, Irwig L, von Minckwitz G, Houssami N (2012) Early prediction of pathologic response to neoadjuvant therapy in breast cancer: systematic review of the accuracy of MRI. Breast 21(5):669–677
Lobbes MB (2012) Treatment response evaluation by MRI in breast cancer patients receiving neoadjuvant chemotherapy: there is more than just pathologic complete response prediction. Breast Cancer Res Treat 136(1):313–314
NCCN Clinical Practice Guidelines in Oncology: Breast cancer screening and diagnosis (nccn.org)
Earle CC, Nattinger AB, Potosky AL, Lang K, Mallick R, Berger M, Warren JL (2002) Identifying cancer relapse using SEER-medicare data. Med Care 40(8):IV–75–81
Cheng L, Swartz MD, Zhao H, Kapadia AS, Lai D, Rowan PJ, Buchholz TA, Giordano SH (2012) Hazard of recurrence among women after primary breast cancer treatment: a 10-year follow-up using data from SEER-medicare. Cancer Epidemiol Biomarkers Prev 21(5):800–809
Friese CR, Neville BA, Edge SB, Hassett MJ, Earle CC (2009) Breast biopsy patterns and outcomes in surveillance, epidemiology, and end results: medicare data. Cancer 115(4):716–724
Gutwein LG, Ang DN, Liu H, Marshall JK, Hochwald SN, Copeland EM, Grobmyer SR (2011) Utilization of minimally invasive breast biopsy for the evaluation of suspicious breast lesions. Am J Surg 202(2):127–132
Mandelblatt JS, Hadley J, Kerner JF, Schulman KA, Gold K, Dunmore-Griffith J, Edge S, Guadagnoli E, Lynch JJ, Meropol NJ et al (2000) Patterns of breast carcinoma treatment in older women: patient preference and clinical and physical influences. Cancer 89(3):561–573
McCahill LE, Single RM, Aiello Bowles EJ, Feigelson HS, James TA, Barney T, Engel JM, Onitilo AA (2012) Variability in reexcision following breast conservation surgery. JAMA 307(5):467–475
Klabunde CN, Legler JM, Warren JL, Baldwin LM, Schrag D (2007) A refined comorbidity measurement algorithm for claims-based studies of breast, prostate, colorectal, and lung cancer patients. Ann Epidemiol 17(8):584–590
Carpenter WR, Reeder-Hayes K, Bainbridge J, Meyer A-M, Amos KD, Weiner BJ, Godley PA (2011) The role of organizational affiliations and research networks in the diffusion of breast cancer treatment innovation. Med Care 49(2):172–179
Rosenbaum P (1983) The central role of the propensity score in observational studies for causal effects. Biometrika 70:41–55
Sato T, Matsuyama Y (2003) Marginal structural models as a tool for standardization. Epidemiology 14(6):680–686
Stuart EA (2010) Matching methods for causal inference: a review and a look forward. Stat Sci 25(1):1–21
Austin PC (2008) A critical appraisal of propensity-score matching in the medical literature between 1996 and 2003. Stat Med 27(12):2037–2049
Houssami N, Ciatto S, Macaskill P, Lord SJ, Warren RM, Dixon JM, Irwig L (2008) Accuracy and surgical impact of magnetic resonance imaging in breast cancer staging: systematic review and meta-analysis in detection of multifocal and multicentric cancer. J Clin Oncol 26(19):3248–3258
Plana MN, Carreira C, Muriel A, Chiva M, Abraira V, Emparanza JI, Bonfill X, Zamora J (2012) Magnetic resonance imaging in the preoperative assessment of patients with primary breast cancer: systematic review of diagnostic accuracy and meta-analysis. Eur Radiol 22(1):26–38
Pengel KE, Loo CE, Teertstra HJ, Muller SH, Wesseling J, Peterse JL, Bartelink H, Rutgers EJ, Gilhuijs KGA (2009) The impact of preoperative MRI on breast-conserving surgery of invasive cancer: a comparative cohort study. Breast Cancer Res Treat 116(1):161–169
Bleicher RJ, Ciocca RM, Egleston BL, Sesa L, Evers K, Sigurdson ER, Morrow M (2009) Association of routine pretreatment magnetic resonance imaging with time to surgery, mastectomy rate, and margin status. J Am Coll Surg 209(2):180–187
Miller BT, Abbott AM, Tuttle TM (2012) The influence of preoperative MRI on breast cancer treatment. Ann Surg Oncol 19(2):536–540
Hwang N, Schiller DE, Crystal P, Maki E, McCready DR (2009) Magnetic resonance imaging in the planning of initial lumpectomy for invasive breast carcinoma: its effect on ipsilateral breast tumor recurrence after breast-conservation therapy. Ann Surg Oncol 16(11):3000–3009
Shin HC, Han W, Moon HG, Yom CK, Ahn SK, You JM, Kim JS, Chang JM, Cho N, Moon WK et al (2012) Limited value and utility of breast MRI in patients undergoing breast-conserving cancer surgery. Ann Surg Oncol 19(8):2572–2579
Morrow M (2010) Magnetic resonance imaging for screening, diagnosis, and eligibility for breast-conserving surgery: promises and pitfalls. Surg Oncol Clin N Am 19:475–492
Krishnan M, Thorsteinsson D, Horowitz N, Weinreb J, Lanin D, Lee C (2008) The influence of preoperative MRI in the timing and type of therapy in women newly diagnosed with breast cancer. Am J Roentgenol 190:A31–A34
Hulvat M, Sandalow N, Rademaker A, Helenowski I, Hansen NM (2010) Time from diagnosis to definitive operative treatment of operable breast cancer in the era of multimodal imaging. Surgery 148(4):746–751
Morrow M, Katz SJ (2012) The challenge of developing quality measures for breast cancer surgery. JAMA 307(5):509–510
O’Flynn EA, Currie RJ, Mohammed K, Allen SD, Michell MJ (2013) Pre-operative factors indicating risk of multiple operations versus a single operation in women undergoing surgery for screen detected breast cancer. Breast 22(1):78–82
Shin HC, Han W, Moon HG, Cho N, Moon WK, Park IA, Park SJ, Noh DY (2012) Nomogram for predicting positive resection margins after breast-conserving surgery. Breast Cancer Res Treat 134(3):1115–1123
Wilkinson L, Given-Wilson R, Hall T, Potts H, Sharma A, Smith E (2005) Increasing the diagnosis of multifocal primary breast cancer by the use of bilateral whole-breast ultrasound. Clin Radiol 60(5):573–578
Acknowledgments
This work was supported by funding from the National Cancer Institute (5R25CA116339). This study used the linked SEER-Medicare database. The interpretation and reporting of these data are the sole responsibility of the authors. The authors would like to thank Seth Tyree and Huan Liu for assistance in creating the initial dataset, and Keith Amos for insight into initial surgical treatment episode and for helping to define the types of breast cancer surgeries.
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The authors state that they have no conflicts of interest.
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Fortune-Greeley, A.K., Wheeler, S.B., Meyer, AM. et al. Preoperative breast MRI and surgical outcomes in elderly women with invasive ductal and lobular carcinoma: a population-based study. Breast Cancer Res Treat 143, 203–212 (2014). https://doi.org/10.1007/s10549-013-2787-4
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DOI: https://doi.org/10.1007/s10549-013-2787-4