Abstract
Background
The SSO-ASTRO guidelines defined a negative margin for breast-conserving surgery (BCS) as no ink on tumor, and implementation has reduced rates of additional surgery in patients with invasive ductal cancer (IDC). Outcomes in invasive lobular cancer (ILC) are uncertain.
Methods
We identified patients with stage I-II ILC treated with BCS from 1/2010-2/2018. Guidelines were adopted on 1/1/2014. Clinicopathologic characteristics, margin status, and re-excisions were compared before and after adoption, and to IDC patients treated from 5/2013-2/2015.
Results
Among 745 early-stage ILC patients undergoing BCT, 312 (42%) were treated pre-guideline and 433 (58%) post-guideline. Most clinicopathologic characteristics were similar between groups, with differences in lobular carcinoma in situ, lymphovascular invasion, and node-positivity rates. Overall rates of additional surgery declined significantly (31.4% to 23.1%, p=0.01) post-guideline, but did not reach significance for re-excisions (19.9% to 15.2%, p=0.12) or conversions to mastectomy (11.5% to 7.9%, p=0.099) individually. Between eras, there was no difference in incidence or number of tumor-on-ink or ≤2mm margins (all p=0.2). Larger tumor, younger age, and pre-guideline era were independently associated with additional surgery. Only younger age was predictive of mastectomy. Among 431 pre-guideline and 601 post-guideline IDC patients, re-excisions declined from 21.3% to 14.8% (p=0.008), and conversion to mastectomy was rare (0.6%). The magnitude of reduction in any additional surgery (interaction p=0.92) and re-excisions (interaction p=0.56) was similar between ILC and IDC.
Conclusions
Despite differences in growth pattern and conspicuity, guideline adoption significantly reduced additional surgery in ILC patients, with a magnitude of benefit similar to IDC.
Keywords: invasive lobular cancer, breast-conserving surgery, margins, SSO-ASTRO consensus guidelines, re-excision, mastectomy
INTRODUCTION
Invasive lobular carcinoma (ILC) comprises 10% to 15% of all breast cancers1, and is biologically distinct from the more-common invasive ductal carcinoma (IDC). Classic ILC displays a characteristic single-file formation of discohesive cells infiltrating the breast stroma, with loss of membranous E-cadherin.1 This inherently infiltrative growth pattern poses diagnostic challenges, as ILC may have a poorer clinical and radiographic definition.2,3 As a result, historically, the feasibility of breast-conserving surgery (BCS) for ILC was questioned.2,4 Histology was not examined in early randomized trials demonstrating similar locoregional control and survival with breast-conserving therapy (BCT) compared to mastectomy for early-stage invasive cancer.5,6 However, similar long-term results have since been reported in populations of pure ILC patients, dependent upon achieving negative margins.3,7 Contemporary rates of locoregional recurrence after BCT for ILC are less than 6% when negative margins are obtained.8
The 2014 Society of Surgical Oncology (SSO)-American Society for Radiation Oncology (ASTRO) consensus guidelines defined a “negative” margin as no ink on tumor, based upon a meta-analysis of 33 studies with 28,162 patients that demonstrated no improvement in ipsilateral breast tumor recurrence with a wider margin, including a subset analysis supporting applicability to ILC.9 Single-center studies and population-based samples have demonstrated a decrease in additional surgery after initial lumpectomy with the dissemination of the consensus guideline.10-13 However, ILC patients comprised less than 20% of study populations10,12,13, and outcomes in ILC remain unclear. We sought to examine the impact of the margin consensus guidelines on rates of re-excision and conversion to mastectomy after initial BCS for ILC, and identify factors predictive of additional surgery.
METHODS
Following Institutional Review Board approval, we identified consecutive women with clinical stage I or II pure ILC treated with BCS from January 1, 2010 to February 1, 2018, with planned subsequent whole-breast radiotherapy (WBRT). Patients who received neoadjuvant chemotherapy, those with bilateral cancers, and those with a personal history of prior breast cancer were excluded. During the study period, all surgeons at our institution routinely utilized seed localization for non-palpable lesions and employed a cavity-shave margin technique with separate submission of individual margins. This approach involves resection of the index lesion, followed by retrieval of separately shaved margins from the surgical cavity, with a metal clip or suture designating the final margin surface. The primary specimen was not assessed for margin status. Margins were defined as positive when ILC was present at an inked surface of the cavity shave specimen. Lobular carcinoma in situ (LCIS) on ink was not considered a positive margin. When tumor was present in the separately submitted margin(s), a measurement was provided in millimeters to the inked surface. Our breast disease management team uniformly adopted the SSO-ASTRO consensus recommendations on January 1, 2014. Patients were grouped into 2 study periods: “pre-guideline”, defined as those treated before January 1, 2014; and “post-guideline”, defined as those treated after January 1, 2014.
Clinicopathologic characteristics, margin status, and rates of re-excision and conversion to mastectomy among ILC patients were examined before and after guideline adoption. Rates of additional surgery were then compared to those seen among patients with clinical stage I or II pure IDC similarly treated with BCS and WBRT from May 2013 to February 2015. This subset of pure IDC patients was derived from a previously published cohort of patients with early-stage invasive breast cancer examining the early uptake of the consensus guidelines.10
Comparisons between pre-guideline and post-guideline eras were made using the Wilcoxon rank-sum test for continuous variables and Fisher’s exact test for categorical variables. Univariable and multivariable analysis for factors associated with additional surgery were conducted using binary logistic regression. Factors included in the univariable analyses were determined a priori, and adjustment factors included in multivariable Cox regression analysis were based upon univariable results. Tests for interaction were performed to assess whether changes in additional surgery were due to guideline era differences between IDC and ILC patients. A p-value < 0.05 was considered statistically significant. All statistical analyses were conducted using R software version 3.5.0 (R Core Development Team, Vienna, Austria).
RESULTS
From January 1, 2010 to February 1, 2018, 745 women with early-stage ILC were treated with BCT, of whom 312 (42%) were treated pre-guideline and 433 (58%) were treated post-guideline. Characteristics of the population are summarized in Table 1. Median age was 62 years, and the majority of cancers were pT1 (74.2%), were estrogen receptor (ER) positive (97.9%), had classical morphology (80.0%), and were node negative (79.6%). While higher rates of associated LCIS (95.5% versus 89.6%, p = 0.004), lymphovascular invasion (16.0% versus 6.9%, p < 0.001), and node positivity (19.9% versus 10.9%, p = 0.002) were observed in the pre-guideline versus post-guideline eras, all other clinicopathologic features were similar between treatment periods.
TABLE 1.
Clinicopathologic Characteristics of All ILC Patients, and Stratified by Pre- or Post-Guideline Era of Treatment
MMG, mammogram; US, ultrasound; LCIS, lobular carcinoma in situ; DCIS, ductal carcinoma in situ; ER, estrogen receptor; LVI, lymphovascular invasion
| Characteristic | All n = 745 |
Pre-guideline n = 312 |
Post-guideline n = 433 |
P |
|---|---|---|---|---|
| Age, years | 62 (53, 70) | 61 (52, 69) | 63 (53, 70) | 0.35 |
| Breast density | 0.10 | |||
| Fatty | 43 (5.8%) | 19 (6.1%) | 24 (5.5%) | |
| Scattered fibroglandular | 233 (31.3%) | 83 (26.6%) | 150 (34.6%) | |
| Heterogenous | 392 (52.6%) | 172 (55.1%) | 220 (50.8%) | |
| Extremely dense | 77 (10.3%) | 77 (10.3%) | 39 (9.0%) | |
| MMG/US size, cm* | 1.1 (0.8, 1.7) | 1.2 (0.8, 1.6) | 1.1 (0.8, 1.7) | 0.46 |
| MRI performed | 382 (51.3%) | 151 (48.4%) | 231 (53.3%) | 0.20 |
| MRI size, cm | 1.6 (1.1, 2.4) | 1.5 (1.1, 2.3) | 1.7 (1.1, 2.5) | 0.25 |
| Pathologic tumor size, cm | 1.4 (0.9, 2.1) | 1.4 (0.9, 2.0) | 1.3 (0.9, 2.1) | 0.99 |
| Associated LCIS | 686 (92.1%) | 298 (95.5%) | 388 (89.6%) | 0.004 |
| Associated DCIS | 117 (15.7%) | 54 (17.3%) | 63 (14.5%) | 0.31 |
| Receptor subtype | 0.64 | |||
| ER+/HER2− | 713 (95.7%) | 296 (94.9%) | 417 (96.3%) | |
| ER+/HER2+ | 17 (2.3%) | 7 (2.2%) | 10 (2.3%) | |
| ER−/HER2+ | 4 (0.5%) | 3 (1.0%) | 1 (0.2%) | |
| ER−/HER2− | 7 (0.9%) | 3 (1.0%) | 4 (0.9%) | |
| Unknown | 4 (0.5%) | 3 (1.0%) | 1 (0.2%) | |
| Type | 0.42 | |||
| Classic | 596 (80.0%) | 248 (79.5%) | 348 (80.4%) | |
| Pleomorphic | 133 (17.9%) | 60 (19.2%) | 73 (16.9%) | |
| Alveolar | 14 (1.9%) | 4 (1.3%) | 10 (2.3%) | |
| Unknown | 2 (0.3%) | 0 (0%) | 2 (0.3%) | |
| LVI** | 80 (10.7%) | 50 (16.0%) | 30 (6.9%) | < 0.001 |
| Pathologic T classification | 0.45 | |||
| T1 | 553 (74.2%) | 236 (75.6%) | 317 (73.2%) | |
| T2 | 183 (24.6%) | 74 (23.7%) | 109 (25.2%) | |
| T3 | 9 (1.2%) | 2 (0.6%) | 7 (1.6%) | |
| Pathologic N classification | 0.002 | |||
| N0 or N0(i+) | 593 (79.6%) | 236 (75.6%) | 357 (82.4%) | |
| N1 | 109 (14.6%) | 62 (19.9%) | 47 (10.9%) | |
| NX€ | 43 (5.8%) | 14 (4.5%) | 29 (6.7%) | |
| Pathologic stage | 0.43 | |||
| I | 485 (65.1%) | 195 (62.5%) | 290 (67.0%) | |
| IIA | 210 (28.2%) | 94 (30.1%) | 116 (26.8%) | |
| IIB | 50 (6.7%) | 23 (7.4%) | 27 (6.2%) |
Values presented as median (interquartile range) or n (%)
Size not stated or occult in n = 91
Unknown in n = 14
No axillary surgery performed in n = 43 patients due to age
Between the pre-guideline and post-guideline eras, there was no difference in the closest margin (p = 0.21) or number of margins ≤ 2 mm (p = 0.22)(Table 2). The overall rate of reoperation after initial BCS was 26.6%. There was an 8% absolute decrease in rates of additional surgery after guideline adoption, from 31.4% pre-guideline to 23.1% post-guideline (p = 0.01). This trend was observed both for re-excision lumpectomies (19.9% to 15.2%), and conversion to mastectomy (11.5% to 7.9%), though the difference between guideline eras did not reach statistical significance for these individual procedure types (Fig. 1). Margin status and rates of additional surgery are summarized in Table 2. Among patients who underwent conversion to mastectomy (n = 70), 17 (24.3%) had no residual carcinoma, 7 (10.0%) had ductal carcinoma in situ (DCIS) alone, and 46 (65.7%) had residual invasive carcinoma. The median size of residual carcinoma was 0.6 cm (interquartile range 0.3, 1.1).
TABLE 2.
Margin Status and Additional Surgery After Initial Lumpectomy
| All n = 745 |
Pre-guideline n = 312 |
Post-guideline n = 433 |
P | |
|---|---|---|---|---|
| Closest margin | 0.21 | |||
| Tumor on ink | 121 (16.2%) | 50 (16.0%) | 71 (16.4%) | |
| ≤ 1 mm | 137 (18.4%) | 67 (21.5%) | 70 (16.2%) | |
| 1.1-2 mm | 47 (6.3%) | 22 (7.1%) | 25 (5.8%) | |
| > 2 mm | 440 (59.1%) | 173 (55.4%) | 267 (61.7%) | |
| If ≤ 2 mm margin(s), # of margins involved: | 0.22 | |||
| 1 | 176 (57.7%) | 74 (53.2%) | 102 (61.4%) | |
| 2 | 80 (26.2%) | 43 (30.9%) | 37 (22.3%) | |
| ≥3 | 49 (16.1%) | 22 (15.8%) | 27 (16.3%) | |
| Any additional surgery | 198 (26.6%) | 98 (31.4%) | 100 (23.1%) | 0.01 |
| Re-excision lumpectomy | 128 (17.2%) | 62 (19.9%) | 66 (15.2%) | 0.12 |
| Conversion to mastectomy | 70 (9.4%) | 36 (11.5%) | 34 (7.9%) | 0.10 |
Fig 1.
Annual rates of any additional surgery, re-excision lumpectomy, and conversion to mastectomy.
On univariable analysis, larger tumor size (odds ratio [OR] 1.46, 95% confidence interval [CI] 1.25-1.69, p < 0.001), and pre-guideline era (OR 1.52, 95% CI 1.1-2.12, p = 0.01) were associated with increased odds of additional surgery, whereas older age (OR 0.96, 95% CI 0.95-0.98, p < 0.001) was associated with decreased odds of additional surgery. No statistically significant associations were observed for breast density or tumor morphology. On multivariable analysis, larger tumor size (OR 1.55, 95% CI 1.33-1.81, p < 0.001), and pre-guideline era (OR 1.61, 95% CI 1.15-2.27, p = 0.006) remained significantly associated with increased odds of additional surgery, whereas older age (OR 0.96, 95% CI 0.94-0.97, p < 0.001) remained significantly associated with reduced odds of additional surgery. Only older age (OR 0.96, 95% CI 0.93-0.99, p = 0.005) was significantly associated with a reduced odds of conversion to mastectomy on univariable analysis.
One thousand thirty-two patients with pure IDC were identified for comparison from the previously studied cohort10; 431 (42%) were treated pre-guideline and 601 (58%) were treated post-guideline. The overall rate of additional surgery after initial BCS was 17.5%. There was a 7% absolute decline after guideline adoption, with additional surgery decreasing from 21.3% to 14.8% (p = 0.008). In a model designed to assess interactions between histology and guideline era, the magnitude of reduction in any additional surgery (interaction p = 0.92) and re-excision lumpectomy (interaction p = 0.56) was similar between ILC and IDC. Conversion to mastectomy among IDC patients was rare, performed for only 6 (0.6%) patients overall, limiting further analyses in this respect.
DISCUSSION
In this contemporary population of early-stage ILC patients treated with upfront BCS we have demonstrated a significant decline in rates of additional surgery from 31.4% to 23.1% after adoption of the SSO-ASTRO consensus guidelines endorsing a margin of “no ink on tumor”. There was no difference in the extent of margin involvement between eras, and the magnitude of reduction in re-operation was similar to that seen in IDC patients.
Reported rates of additional surgery after initial BCS for invasive cancer in the pre-guideline era ranged from 20% to 75%.14-16 In a large population-based sample of patients with stage 0-II cancer treated between 2000 and 2010, lobular histology was shown to independently predict additional surgery.17 After the dissemination of the consensus guidelines in 2014, more recent studies show a subsequent decline in re-operations, but include few patients with ILC.10,12,13 The overall rate of additional surgery in our study was 26.6%, which decreased from 31.4% in the pre-guideline era to 23.1% in the post-guideline era. Rosenberger et al. reported a similar reduction in re-excisions from 21.4% to 15.1% after guideline adoption among 1205 patients with stage I-II invasive breast cancer treated from January 2013 to October 2014, of whom 127 (11%) had ILC.10 Chung et al. also saw re-excisions decrease from 19% to 13% (p = 0.03) among 846 patients undergoing BCS, including 169 (20%) cases of lobular or mixed ductal/lobular histology.12 Bhutiani et al. similarly demonstrated a decline in re-excision lumpectomy from 37% to 9% (p < 0.001) after guideline adoption among 237 patients undergoing BCS, of whom 26 (11%) had ILC.13 To our knowledge, this is the largest study showing a decline in additional surgery after primary BCS in a contemporary population of patients with pure ILC, and demonstrates a reduction of similar magnitude as observed for IDC.
With the success of BCT being contingent upon achieving negative margins, it is noteworthy that higher rates of margin positivity have been observed in ILC as compared to IDC, ranging from 12.3% to as high as 63% in early studies.4,18,19 In this study, the rate of margin positivity among ILC patients was 16.2%, and did not differ in the pre- and post-guideline eras. Cavity-shave margin technique, which is uniformly employed at our institution, has been suggested to decrease rates of margin positivity in ILC. In a randomized trial of 235 patients with stage 0-III cancer undergoing BCS, use of cavity-shave margin technique resulted in significantly lower rates of positive margins (19% versus 34%, p = 0.01) and re-excisions (10% versus 21%, p = 0.02), but only 9% of patients in this study had lobular histology.20 In a subsequent study of 365 patients with stage I-III pure ILC, Mukhtar et al. found lower rates of positive margins with the use of cavity-shaved margins (OR 0.39, 95% CI 0.2-0.7, p = 0.002), after adjusting for size and multifocality.21 In our study, cavity-shaved margins were routinely employed, and both rate and number of positive and < 2 mm margins were similar before and after guideline adoption. Given our consistent technique and the lack of a difference in disease burden in the pre- and post-guideline eras, the use of this method likely does not account for the observed decline in re-excisions, but may contribute to our comparatively lower rates of margin positivity as compared to other series. Despite reporting higher rates of margin positivity in ILC, multiple studies have shown no difference in local control and survival outcomes as compared to IDC when negative margins are ultimately obtained.4,18,19 Importantly, many of these studies also predate modern improvements in preoperative imaging, superior localization, and surgical techniques as well as routine utilization of systemic endocrine therapy, which is of particular benefit in overwhelmingly ER positive ILC.1
In addition to pre-guideline era of treatment, younger age and larger tumor size were predictive of additional surgery among ILC patients in this study, consistent with previously reported results in populations comprised mainly of patients with IDC. In a National Cancer Database study of 316,114 patients with early-stage cancers treated with BCS from 2010 to 2014, the rate of additional surgery was 38.5% among the youngest patients age 18 to 29 years, compared to 16.5% among those age > 80 years (p < 0.001).17 There was also a linear association between increasing tumor size and repeat surgery (p < 0.001).17 Similarly, in a population-based sample of 89,448 women treated with primary BCS from 2003 to 2013 in New York State, re-operation was higher among women < 50 years of age as compared to those ≥ 65 years of age (37.7% versus 26.3%, p < 0.001).22 While most patients in these studies had ductal histology, our findings suggest similar trends among early-stage ILC patients which are not altered by application of the margin guideline.
Conversion to mastectomy among ILC patients in our study declined from 11.5% to 7.9% after guideline adoption, which did not reach significance, and remains markedly higher than rates of conversion to mastectomy among IDC patients, which was performed in less than 1% of cases. This is consistent with previous studies with rates of mastectomy after initial BCS ranging from 4.9% to 37% in ILC versus < 1% to 22% in IDC, respectively.2,3,10,23-25 Unreliable clinical and imaging assessment, and the discohesive and multifocal nature of ILC have been suggested as the rationale for higher rates of conversion to mastectomy. However, among patients who did undergo completion mastectomy in this study, 24% had a benign mastectomy specimen, and the median size of remaining tumor was only 0.6 cm among those with residual disease. This raises the possibility that those with minimal residual disease burden may have achieved negative margins with re-excision lumpectomy, and may have potentially avoided mastectomy. Younger age was the only factor predictive of both additional surgery and conversion to mastectomy, consistent with previous reports22, and this may be reflective of the interplay of clinical factors and patient choice.
Limitations of this study include its retrospective nature and inability to examine physician and patient-level decision making. However, its strengths include a large consecutive population of women with early-stage pure ILC treated with consistent and contemporary surgical and pathological techniques. The uniform guideline adoption among a large group of surgeons enables demonstration of a substantial impact of the consensus guidelines on patients with the less-common lobular histology.
CONCLUSIONS
In this large population of early-stage ILC patients treated with primary BCS, we have demonstrated a significant decline in additional surgery with uniform adoption of the 2014 SSO-ASTRO consensus margin guidelines. The extent of this reduction is similar to that seen among patients with IDC, with younger age and larger tumor size being predictive of re-operation. While rates of conversion to mastectomy have also decreased, this reduction was not statistically significant, and rates remain higher among patients with lobular histology. In the contemporary era of superior radiologic, pathologic, and surgical techniques, we anticipate continued progress in tailoring therapies and avoiding overtreatment for this innately unique subset of breast cancer.
Synopsis : Among early-stage ILC patients undergoing primary breast-conserving surgery, rates of additional surgery declined from 31.4% to 23.1% after adoption of SSO-ASTRO consensus guidelines. The magnitude of benefit was similar to that seen among IDC patients.
ACKNOWLEDGEMENTS
The preparation of this study was funded in part by NIH/NCI Cancer Center Support Grant No. P30 CA008748 to Memorial Sloan Kettering Cancer Center. Dr. Monica Morrow has received honoraria from Genomic Health and Roche. All other authors have no conflicts of interest to declare. This study was presented in poster format at the 72nd Society of Surgical Oncology Annual Cancer Symposium, San Diego, CA, USA, March 27-30, 2019.
Footnotes
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