Abstract
The axillary treatment of patients with ductal carcinoma in situ (DCIS) remains controversial. The aim of the present study was to evaluate the roles of sentinel lymph node biopsy (SLNB) in patients with breast DCIS. A database containing the data from 262 patients diagnosed with breast DCIS and 100 patients diagnosed with DCIS with microinvasion (DCISM) who received SLNB between January 2002 and July 2014 was retrospectively analyzed. Of the 262 patients with DCIS, 9 presented with SLN metastases (3 macrometastases and 6 micrometastases). Patients with large tumors diagnosed by ultrasound or with tumors of high histological grade had a higher positive rate of SLNs than those without (P=0.037 and P<0.0001, respectively). Of the 100 patients with DCISM, 11 presented with metastases. Younger patients had a higher positive rate of SLNs (P=0.028). According to the results of this study and the systematic review of recent studies, the indications of SLNB for patients with DCIS are as follows: SLNB should be performed in all DCISM patients and in those DCIS patients who received mastectomy, and could be avoided in those who received breast-conserving surgery. However, SLNB should be recommended to patients who have high risks of harboring invasive components. The risk factors include a large, palpable tumor, a mammographic mass or a high histological grade.
Keywords: sentinel lymph node biopsy, breast neoplasms, ductal carcinoma in situ
Introduction
With improvements to the breast cancer screening program, more and more women with early breast cancer are being diagnosed and treated. In early invasive breast cancer patients, sentinel lymph node biopsy (SLNB) has become a routine procedure, as it provides accurate axillary staging, while sparing node-negative patients the morbidity associated with axillary lymph node dissection (ALND) (1). At present, SLNB is the standard treatment for patients with clinical node-negative invasive carcinoma, with the exception of those patients with T4d stage disease (2). However, the axillary treatment of patients with ductal carcinoma in situ (DCIS) remains controversial (3). These patients, who exhibit pre-invasive tumors with no invasive component, are theoretically believed to have no chance of lymph node metastases. However, certain patients with DCIS may harbor an unrecognized focus of invasion in the tumor and therefore have lymph node metastases.
China Breast Cancer Clinical Study Group-001 is a prospective multi-center clinical trial conducted to study the feasibility of using SLNB as a substitute for ALND in 3466 Chinese breast cancer patients recruited from 13 institutes between January 2002 and July 2014. The primary objectives were determining the disease-free survival and complications of SLNB and ALND. The secondary objectives included overall survival, SLN intraoperative diagnosis, micrometastasis detection and prognosis, and radiological safety of the two techniques. All patients enrolled in the study were ≥18 years of age with a diagnosis of early breast cancer and scheduled for a SLNB. Patients who had undergone previous ipsilateral axillary surgery were excluded from the study (4).
The present study selected 362 patients with DCIS or DCIS with microinvasion (DCISM; with the largest diameter of the invasive component of <1 mm) from the CBCSG001 database and analyzed the frequency and the risk of SLN metastases in these patients.
Materials and methods
Patients
Of 362 patients selected from the database, 262 patients presented with the final pathology of DCIS and 100 with DCISM. All patients were ≥18 years of age (range, 22–80 years; median, 47 years) and scheduled for a SLNB. The study was approved by the Ethics Committee of the Shandong Cancer Hospital and informed consent was obtained from each patient. Patients who had undergone previous ipsilateral axillary surgery were excluded from this study.
Identification of SLNs
Sulfur colloid (SC) was labeled with Technetium-99m (99mTc) subsequent to filtration through a millipore filter with a 220-nm pore size. 99mTc-SC ranging from 7.2–37.0 MBq, in 0.5–2.0 ml, was injected subcutaneously above the primary tumor on the day prior to surgery or at least 4 h prior to surgery on the actual day. SLNs were identified by combining the use of an intraoperative γ-detector (Neo2000 Gamma Detection System; Johnson and Johnson, New Brunswick, NJ, USA) and blue dye. Methylthionium (1%; 4ml) was injected subcutaneously above the primary tumor or around the biopsy cavity 10 min prior to surgery. Lymph nodes with blue lymphatic vessels directly leading to them (SLNs by blue dye) and those with a radioactivity count higher than 10% of the highest radioactivity count of the lymph node (SLNs by isotope) were regarded as SLNs.
Evaluation of primary tumors
The excised breast lesions were sampled with serial sections, with at least one block per centimeter. In selected cases, secondary breast tissue sections were obtained. The search for microinvasive foci was performed with HE serial sections and immunostaining for smooth muscle actin and cluster of differentiation 10 for the detection of myoepithelial cells. The largest diameter of the invasive component of the DCISM was <1 mm.
Evaluation of SLNs
The SLNs were identified and dissected, and then they were sectioned along the long axis into two blocks. Intraoperatively, all blocks were assessed by frozen section and touch imprint cytology. ALND was only performed if any of the intraoperative tests were positive.
Post-operatively, all node blocks were fixed in 10% buffered formalin and paraffin embedded, and one 4–6-µm thick slide was taken from each block. Metastases were classified according to the 6th criterion of the American Joint Cancer Committee (5). Macrometastases (≥2 mm), micrometastases (0.2–2 mm) and isolated tumor cells (≤0.2 mm) were all considered node-positive.
Statistical analysis
The primary analysis was performed to determine the frequency of SLN metastases in patients with post-operative diagnoses of DCIS and DCISM. χ2 tests or Fisher's exact tests were performed to compare the rate between different groups. Statistical analyses were performed using SPSS software (version 17.0; SPSS, Inc., Chicago, IL, USA) and P<0.05 was considered to indicate a statistically significant difference.
Results
A total of 1,145 SLNs were removed (mean, 3.16) from 362 patients. Of the 362 patients, 20 (5.52%) exhibited metastases.
Of the 262 patients with DCIS, 9 (3.4%) presented with SLN metastases (3 macrometastases and 6 micrometastases). All 9 patients received ALND and only 1 patient with SLN macrometastases exhibited non-sentinel axillary lymph node (nSLN) metastases. As shown in Table I, the positive rate of SLNs was not associated with patient age, primary tumor location, whether the mass was palpable, breast surgery type, or estrogen receptor (ER) and human epidermal growth factor receptor 2 (HER-2) status. However, patients with large tumors diagnosed by ultrasound or with tumors of high histological grade had a higher positive rate of SLNs than those without (P=0.037 and P<0.0001, respectively).
Table I.
Positive rate of SLNs in patients with ductal carcinoma in situ
| Characteristic | SLN-positive | SLN-negative | P-value |
|---|---|---|---|
| Mean age, yearsa | 46±7 | 48±11 | 0.648 |
| Tumor size on ultrasound, cm | 2.93±0.87 | 1.95±1.40 | 0.037 |
| Clinical palpable mass, n | 0.407 | ||
| Yes | 9 | 235 | |
| No | 0 | 18 | |
| Location, n | 0.420 | ||
| Upper outer quadrant | 8 | 154 | |
| Upper inner quadrant | 0 | 32 | |
| Lower outer quadrant | 1 | 22 | |
| Lower inner quadrant | 0 | 21 | |
| Central area | 0 | 24 | |
| Breast surgery, n | 0.535 | ||
| Breast-conserving treatment | 7 | 172 | |
| Mastectomy | 2 | 81 | |
| ER status, n | 0.246 | ||
| Positive | 5 | 185 | |
| Negative | 4 | 68 | |
| HER-2 status, n | 0.402 | ||
| Positive | 4 | 79 | |
| Negative | 5 | 174 | |
| Histopathological grade, n | <0.0001 | ||
| High | 8 | 119 | |
| Medium | 1 | 94 | |
| Low | 0 | 40 |
SLN, sentinel lymph node; ER, estrogen receptor; HER-2, human epidermal growth factor receptor 2.
Of the 100 patients with DCISM, 11 presented with metastases. Of these, 4 patients exhibited SLN macrometastases, six exhibited micrometastases and 1 possessed isolated tumor cells. Following ALND, 3 patients with SLN macrometastases and 2 patients with SLN micrometastases were diagnosed with nSLN metastases. The positive rate of SLNs was not associated with tumor size, primary tumor location, breast surgery type, or ER and HER-2 status. However, younger patients had a higher positive rate of SLNs (P=0.028) (Table II).
Table II.
Positive rate of SLNs in patients with ductal carcinoma in situ with microinvasion.
| Characteristic | SLN positive | SLN negative | P-value |
|---|---|---|---|
| Mean age, years | 41±8 | 48±10 | 0.028 |
| Tumor size by ultrasound, cm | 2.18±1.03 | 2.00±1.17 | 0.799 |
| Location | 0.773 | ||
| Upper outer quadrant | 6 | 50 | |
| Upper inner quadrant | 2 | 18 | |
| Lower outer quadrant | 1 | 6 | |
| Lower inner quadrant | 0 | 7 | |
| Central area | 2 | 8 | |
| Breast surgery | 0.687 | ||
| Breast-conserving treatment | 9 | 68 | |
| Mastectomy | 2 | 21 | |
| ER status | 0.479 | ||
| Positive | 8 | 55 | |
| Negative | 3 | 34 | |
| HER-2 status | 0.459 | ||
| Positive | 1 | 16 | |
| Negative | 10 | 73 |
SLN, sentinel lymph node; ER, estrogen receptor; HER-2, human epidermal growth factor receptor 2.
Discussion
Theoretically, DCIS without any invasive component cannot invade the lymphatic system and the cancer cells cannot spread to the lymph nodes. Thus, axillary staging appears to be an overtreatment in these patients. However, the fact is that a fraction of patients with the final pathology of DCIS has lymph node metastases. Doubt arises with regard to whether the condition is really pure DCIS. Due to sampling error in the final pathology, DCIS may be upstaged to DCISM or invasive cancer after a more thorough evaluation of the tumor. The interval of pathological serial sections determines the inevitability of this error (6).
To date there has been no prospective randomized trial to address the value of SLNB in patients with DCIS. In the present study, the PubMed database was searched between January 2000 and the current date (July 2014), and the positive rates of SLNs in patients with a final pathology of DCIS in other international studies are listed in Table III (6–22). There are large differences among these studies. We believe that the reason for this lies in the different number of patients enrolled and the different criteria of sampling method. The present study shows that the positive rate of SLNs in patients with the final pathological diagnosis of DCIS was 3.4%, and the positive rate of SLNs in patients with DCISM was significantly higher than that of DCIS (P=0.005). The study also indicated that patients with large tumors diagnosed by ultrasound or with tumors of high histological grade have a relatively higher positive rate of SLNs than those without.
Table III.
Positive rate of sentinel lymph nodes in patients with the final pathology of ductal carcinoma in situ.
| First author (ref.) | Year | Sample size, n | Positive rate, n (%) |
|---|---|---|---|
| Cserni (6) | 2002 | 10 | 1 (10.0) |
| Kelly et al (7) | 2003 | 131 | 3 (2.3) |
| Intra et al (8) | 2003 | 223 | 7 (3.1) |
| Farkas et al (9) | 2004 | 44 | 0 (0.0) |
| Veronesi et al (10) | 2005 | 508 | 9 (1.8) |
| Zavagno et al (11) | 2005 | 102 | 2 (2.0) |
| Katz et al (12) | 2006 | 110 | 8 (7.3) |
| Mabry et al (13) | 2006 | 171 | 10 (5.8) |
| Leidenius et al (14) | 2006 | 74 | 5 (6.8) |
| Sakr et al (15) | 2006 | 39 | 4 (10.3) |
| Di Saverio et al (16) | 2007 | 32 | 4 (12.5) |
| Yi et al (17) | 2008 | 475 | 9 (1.9) |
| Dominguez et al (18) | 2008 | 158 | 16 (10.1) |
| Tada et al (19) | 2010 | 255 | 1 (0.4) |
| Miyake et al (20) | 2011 | 66 | 0 (0.0) |
| Ozkan-Gurdal et al (21) | 2014 | 33 | 1 (3.0) |
| Zetterlund et al (22) | 2014 | 753 | 11 (1.5) |
The pre-operative minimally invasive biopsy also has its limitations, such as the sampling error. A substantial fraction of women identified with DCIS on a core needle biopsy prove to have an invasive component following the final pathological evaluation. The positive rates of SLNs in patients with the pre-operative pathology of DCIS in the other studies are listed in Table IV (17,18,20,23–42). The predictors for patients with invasive cancer in this setting are listed in Table V (17,20,25,26,28,31,32,34,36,38–54). Although there is currently no validated evidence-based medicine model to predict which patients with the pre-operative diagnosis of DCIS should accept SLNB, patients that are highly suspected to have an invasive component should be advised to undergo SLNB. The common predictors in these studies include large, palpable tumors, mammographic masses and high histological grade.
Table IV.
Positive rate of sentinel lymph nodes in patients with the pre-operative pathology of ductal carcinoma in situ.
| First author (ref.) | Year | Sampling size, n | Positive rate, n (%) |
|---|---|---|---|
| Klauber-DeMore et al (23) | 2000 | 76 | 9 (11.8) |
| Pendas et al (24) | 2000 | 87 | 5 (5.7) |
| Wilkie et al (25) | 2005 | 559 | 27 (4.8) |
| Mittendorf et al (26) | 2005 | 41 | 2 (4.9) |
| Camp et al (27) | 2005 | 43 | 5 (11.6) |
| Yen et al (28) | 2005 | 141 | 12 (8.5) |
| Takács et al (29) | 2006 | 44 | 0 (0.0) |
| Fraile et al (30) | 2006 | 142 | 10 (7.0) |
| Moran et al (31) | 2007 | 35 | 3 (8.6) |
| Meijnen et al (32) | 2007 | 30 | 5 (16.7) |
| Moore et al (33) | 2007 | 470 | 43 (9.1) |
| Dominguez et al (18) | 2008 | 177 | 20 (11.3) |
| Sakr et al (34) | 2008 | 110 | 6 (5.5) |
| van la Parra et al (35) | 2008 | 51 | 5 (9.8) |
| Yi et al (17) | 2008 | 624 | 40 (6.4) |
| Doyle et al (36) | 2009 | 145 | 7 (4.8) |
| Schneider et al (37) | 2010 | 110 | 15 (13.6) |
| Kurniawan et al (38) | 2010 | 349 | 65 (18.6) |
| Miyake et al (20) | 2011 | 103 | 2 (1.9) |
| Son et al (39) | 2011 | 66 | 1 (1.5) |
| Chin-Lenn et al (40) | 2014 | 306 | 3 (1.0) |
| Guillot et al (41) | 2014 | 221 | 20 (9.0) |
| Osako et al (42) | 2014 | 336 | 13 (3.9) |
Table V.
Predictors of invasive disease in patients with a pre-operative biopsy diagnosis of DCIS.
| First author (ref.) | Total patients, n | Patients upstaged to invasive cancer, n (%) | Significant predictors |
|---|---|---|---|
| Yi et al (17) | 624 | 149 (23.9) | Core biopsy; DCIS size, >5 cm |
| Miyake et al (20) | 103 | 2 (1.9) | Palpable tumor; tumor size, ≥2.0 cm on MRI |
| Wilkie et al (25) | 675 | 66 (9.8) | High-grade DCIS; mammographic mass; microinvasion |
| Mittendorf et al (26) | 30 | 6 (20.0) | Diagnosis by core-needle biopsy |
| Yen et al (28) | 398 | 80 (20.1) | Age, ≤55 years; mammographic size, ≥4 cm; grade 3 DCIS; diagnosis by core-needle biopsy |
| Moran et al (31) | 62 | 20 (32.3) | DCIS size, >2.5 cm or if mastectomy was required |
| Meijnen et al (32) | 171 | 45 (26.3) | Palpable lesion; mammographic mass; intermediate/poor grade |
| Sakr et al (34) | 110 | 31 (28.2) | DCISM; large DCIS |
| Doyle et al (36) | 145 | 55 (37.9) | Radiological mass; areas of invasion, <1 mm |
| Kurniawan et al (38) | 375 | 65 (17.3) | Palpable lesions; non-calcified mammographic features (mass, architectural distortion, non-specific density); mammographic size, ≥20 mm; prolonged screening interval, ≥3 years; DCIS grade (univariate analysis) |
| Son et al (39) | 78 | 14 (17.9) | Large tumor size; HER2 overexpression |
| Chin-Lenn et al (40) | 394 | 9 (2.3) | Larger pre-operative tumor size |
| Guillot et al (41) | 241 | 85 (35.3) | Palpable tumor; high-grade DCIS; detection of an opacity by mammography |
| Osako et al (42) | 336 | 113 (33.6) | Palpability; mammographic mass; and calcifications (spread, >20 mm) |
| Rutstein et al (43) | 254 | 21 (8.3) | <12 core samples (size, 11–14 gauge); comedo necrosis |
| Goyal et al (44) | 587 | 220 (37.5) | Clinically palpable mass; mammographic mass |
| Huo et al (45) | 200 | 41 (20.5) | Mass lesion on imaging; lesion, >1.5 cm; high nuclear grade; presence of lobular cancerization |
| Hoorntje et al (46) | 255 | 41 (16.1) | Grade 3 DCIS; periductal inflammation in core biopsies; large area of calcification |
| Renshaw (47) | 91 | 17 (18.7) | Comedo DCIS with cribriform/papillary pattern; DCIS size, >4 mm with lobular extension |
| Jackman et al (48) | 1326 | 183 (13.8) | Diagnosis by core-needle biopsy; mammographic mass; ≥10 cores per lesion |
| King et al (49) | 140 | 36 (25.7) | Mass on breast imaging |
| Lee et al (50) | 59 | 17 (28.8) | Inflammatory infiltrate |
| Trentin et al (51) | 733 | 148 (20.2) | Mammographic size, >20 mm; residual lesion on post-VABB mammogram; age, <40 years |
| Lee et al (52) | 493 | 123 (24.9) | Larger DCIS lesion (at least 15 mm); lack of hormone receptor expression; intermediate or high nuclear grade; diagnosis on core biopsy compared with vacuum-assisted biopsy; non-cribriform subtype of DCIS |
| Park et al (53) | 340 | 145 (42.6) | Palpability; mass or calcification by ultrasonography; grade; suspicious microinvasion; biopsy method (univariate analysis) Palpability; ultrasonographic calcification or mass; suspicious microinvasion; core needle biopsy (multivariate analysis) |
| Sculz et al (54) | 205 | 37 (18.0) | Lesion palpability; mass lesion on ultrasound; presence of a mammographically detectable mass; architectural distortion or density; BI-RADS score of 5, lesion diameter, ≥50 mm; ≥50% of histologically affected ducts (univariate analysis); palpable mass (multivariate analysis) |
DCIS, ductal carcinoma in situ; DCISM, DCIS with microinvasion; MRI, magnetic resonance imaging; BI-RADS, breast imaging-reporting and data system.
The American Society of Clinical Oncology panels have updated the guidelines of SLNB for patients with early-stage breast cancer recently, and the guidelines of SLNB for patients with DCIS has been revised accordingly (3). For women with a core needle biopsy showing DCIS who are being treated with breast-conserving surgery, the guidelines state that there is no evidence to support performing SLNB, and that SLNB may be performed as a separate second procedure in those identified with invasive cancer. The exceptions to this may include cases in which breast imaging or a physical examination identify a clear mass that is characteristic of invasive cancer or a large area of calcification without a mass, where there is a high probability of locating invasive cancer in the resection specimen. Upon performing a mastectomy, the guidelines suggest that SLNB may be warranted due to the possibility of finding an invasive component in the final pathology, and the disruption of the lymphatics by the mastectomy may preclude a subsequent SLNB.
According to the results of the present study and the systematic review of recent studies, the indications of SLNB for patients with DCIS are as follows: SLNB should be performed in all DCISM patients and in those DCIS patients who received mastectomy, and could be avoided in those who received breast-conserving surgery. However, SLNB should be recommended to patients who have high risks of harboring invasive components. The risk factors include large, palpable tumors, mammographic massed and a high histological grade.
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