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Originally published as Ann Surg Oncol Early Release 10.1245/ASO.2003.04.009 on November 10, 2003

Annals of Surgical Oncology 10:1160-1165 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Sentinel Lymph Node Metastasis in Microinvasive Breast Cancer

Mattia Intra, MD, Stefano Zurrida, MD, Fausto Maffini, MD, Angelica Sonzogni, MD, Giuseppe Trifirò, MD, Roberto Gennari, MD, Paolo Arnone, MD, Guillermo Bassani, MD, Antonio Opazo, MD, Giovanni Paganelli, MD, Giuseppe Viale, MD, FRCPath and Umberto Veronesi, MD, PhD

From the Department of Surgery, Breast Unit (MI, SZ, RG, PA, GB, AO), and the Department of Pathology and Laboratory Medicine (FM, AS, GV), University of Milan School of Medicine; and the Department of Nuclear Medicine (GT, GP) and Division of Chemoprevention (UV), European Institute of Oncology, Milan, Italy.

Correspondence: Address correspondence and reprint requests to: Mattia Intra, MD, Via Ripamonti, 435, 20141 Milano, Italy; Fax: 39-02-57489780; E-mail: mattia.intra{at}ieo.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Ductal carcinoma in situ with microinvasion (DCISM) is a separate pathological entity, distinct from pure ductal carcinoma in situ (DCIS). DCISM is a true invasive breast carcinoma with a well-known metastatic potential. Currently, there is controversy regarding the indication for complete axillary dissection (CAD) to stage the axilla in patients with DCISM. The role of CAD is questioned given its morbidity and reported low incidence of axillary involvement. Sentinel lymph node biopsy (SLNB) may obviate the need for CAD in these patients without compromising the staging of the axilla and the important prognostic information.

Methods: From March 1996 to December 2002, 4602 consecutive patients with invasive breast carcinoma underwent SLN biopsy. Of these, 41 patients with DCISM were selected.

Results: Metastasis in the SLN were detected in 4 of 41 (9.7%) patients. Two of the 4 patients had only micrometastasis in the SLN. In three patients, the SLN was the only positive node after CAD.

Conclusions: SLN biopsy should be considered as a standard procedure in DCISM patients. SLNB can detect nodal micrometastasis and accurately stage the axilla avoiding the morbidity of a CAD. Complete AD may not be mandatory if only the SLN contains micrometastatic disease. Informed consent is very important in the decision not to undergo CAD.

Key Words: Breast cancer • Ductal carcinoma in situ • Microinvasion • Sentinel lymph node • Metastasis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Ductal carcinoma in situ with microinvasion (DCISM) is an uncommon pathological entity representing < 1% of all breast cancers.1 Although microinvasion is a property of infiltrating disease, the potential for lymphatic metastatic spread is not obvious and the subsequent optimal surgical approach to the axilla is controversial. In the past, traditional treatment involved appropriate local therapy to the breast with wide resection or total mastectomy in cases of extensive intramammary spread, as well as complete axillary dissection (CAD) to guide decisions about adjuvant therapy and to improve locoregional control. On the other hand, some authors have advocated omitting CAD in selected patients with tumors less than 1 cm,2 indolent histological subtypes,3 elderly,4 and also in patients with DCISM,5,6 based on their very low risk of lymph node spread. Currently there is disagreement regarding the indications for CAD to stage the axilla in patients with DCISM, given its morbidity and the reported low incidence of axillary involvement. Sentinel lymph node biopsy (SLNB) may obviate CAD in these patients without loosing the important prognostic information of the histological status of the axilla.

The aim of this study is to determine the prevalence of SLN metastasis in a series of patients with DCISM of the breast, to determine the clinical usefulness of the SLNB in these patients, to identify if patients at higher risk of dissemination to the axillary lymph node exist, and finally, to identify biological risk factors if they are present.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Patients
Between March 1996 and December 2002, 4602 patients with clinically node-negative breast carcinoma underwent SLNB at the European Institute of Oncology in Milan, Italy, and were prospectively included into a database. To be offered SLNB, the patients had to have cytologically or histologically verified breast carcinoma 3 cm or less in size (measured clinically and/or by imaging techniques) and clinically uninvolved axillary lymph nodes. The Ethical Committee approved the study protocol, and all patients signed an informed consent form.

Among these patients, 41 patients (aged between 29 and 67 years, average 35.6) affected by DCISM, were included in the current investigation.

Lymphoscintigraphy
Lymphatic mapping was performed using a radiocolloid technique as previously described.7 Briefly, 5–10 MBq of 99mTc-labeled colloidal particles of human albumin size range 20–80 nm, (Nanocol; Nycomed Amersham-Sorin, Saluggia-VC, Italy) in 0.2 mL of isotonic sodium chloride solution were injected close to the tumor subdermally or peritumorally, the day before surgery or the same day. Lymphoscintigraphy was then performed 5–30 minutes after injection and repeated after 3 hours if no SLNs were evident in early images. Anterior and anterior-oblique projections of the breast and axilla were obtained to determine the exact position of the SLN. The skin projection of the lymph node was then marked and used as a landmark when beginning the operation.

If the primary tumor was nonpalpable, we performed a new technique that we called ROLL (Radioguided Occult Lesion Localization) to localize the tumor using Tc-99m macroaggregates. For SLN identification, the same procedure described above was performed on the skin projection of the occult lesions.8

In case of diffuse microcalcifications in which total mastectomy was indicated, the lymphoscintigraphy was performed using a single subdermal periareolar injection of the radiotracer (Nanocol, Nycomed Amersham-Sorin, Saluggia-VC, Italy).9

Surgery
SLN biopsy took place 4–20 hours after injection of radiolabeled albumin. A gamma ray–detecting probe (Neoprobe 2000, Ethicon, Inc, Somerville, NY) was used to locate the radioactive lymph node and facilitate its removal. Radioactivity detected by the probe was transduced into digital readout and acoustic signals whose intensity was directly proportional to the level of radioactivity. In the case of breast-conserving surgery, the SLN biopsy was performed through the same incision of the tumor resection in the upper outer quadrants or through a 2–3 cm separated axillary incision if the tumor was in another breast quadrant. The SLN was identified and isolated using the probe as a guide. After the SLN was removed, the surgical bed was reexamined for any residual radioactivity. If there was activity again, additional SLNs were identified and removed. If the primary tumor was nonpalpable, we also performed the radioguided resection of the lesion (ROLL).8 This technique allowed the correct removal of the nonpalpable breast lesions (cluster of microcalcifications or small opacities), without interfering with the SLN biopsy due to the capability of the gamma ray–detecting probe of modifying the radio sensitivity. Whenever indicated, we also performed intraoperative X-ray examination of the resected tissue to ensure complete removal of the lesion. If surgical margins were involved by the tumor at the primary surgery, re-resection or mastectomy was performed. All the nodes uptaking the radiotracer were classified as sentinel nodes and were removed for histopathological examination.

Histopathological Examination
The surgically removed breast lesions were thoroughly sampled for histopathological examination. In case of microcalcifications, the specimens were sliced and subjected to x-ray examination to ensure complete sampling of all the microcalcification-containing tissue. Specimens without calcifications were extensively sampled taking at least one block/cm of the lesion. Samples from the surrounding tissue were also examined and in case of mastectomy, the areola- nipple complex was also evaluated histologically. Tissue sections from all previous needle biopsies (at least 3 sections/core, cut at 110–200 µm intervals) and from all surgical resections performed elsewhere were reviewed. Tumors were classified histologically according to the World Health Organization Histological Classification of Breast Tumors, as modified by Rosen and Obermann.10 Tumor grading was assessed according to Elston and Ellis.11 We looked for peritumoral vascular invasion as recommended by Rosen and Obermann.10 DCISM was diagnosed according to the TNM classification and following the criteria of Rosen and Obermann.10 Immunoreactions for the evaluation of sex steroid hormone receptor status and the proliferative tumor fraction were performed as previously reported.12 Results were recorded as the percentage of cells showing definite nuclear immunoreactivity over at least 2000 neoplastic cells in 10 randomly selected HPF (x400) at the periphery of the tumor. Her2/neu overexpression was investigated immunohistochemically, using a specific polyclonal antiserum (Dako, Copenhagen, Denmark) and the Envision detection reagent (Dako, Copenhagen, Denmark), according to the manufacturer’s instructions. The staining results were recorded in a 4-tier scale, from 0 to 3+, according to the percentage of immunoreactive cells, and to the intensity and completeness of membrane staining.

The SLN examination was performed as previously described.13 Briefly, the SLNs were bisected fresh along the major axis if larger than 5 mm and fixed in 10% formalin for 6–8 hours, before being embedded in paraffin. Lymph nodes < 5 mm were embedded uncut. Fifteen pairs of paraffin-embedded sections, 4-µm thick, were cut at 50-µm intervals. If residual tissue was left, additional pairs of sections were cut at 100-µm intervals until the lymph node was entirely sectioned. One section of each pair was stained with hematoxylin and eosin (H&E). Whenever needed, to ascertain the nature of atypical cells seen on the H&E sections, the mirror sections were immunostained for cytokeratins using a rapid staining method (EPOS Anti-cytokeratins/HRP; Dako, Copenhagen, Denmark). Non–sentinel axillary lymph nodes were tagged by Berg level. They were bisected if larger than 5 mm, and processed routinely for paraffin embedding. Three to six H&E stained sections per lymph node cut at 100–500 µm intervals were examined.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
In 20 patients, the clinical presentation was a palpable breast mass, three patients had diffuse microcalcifications, 14 patients had a single cluster of microcalcifications, and three patients had nonpalpable mammographic or ultrasonographic abnormalities. One patient’s presentation was unknown. Out of 41 patients, 31 (75.6%) were treated with wide resection and 10 (24.4%) with mastectomy. Fifty-one SLNs were identified and examined: 25 patients had one SLN, 10 had two SLNs and 2 had three SLNs.

Pathological Findings
SLN metastasis were detected in 4 of the 41 patients (9.7%). Two of the 4 patients with a positive SLN had only micrometastasis (<2 mm). The SLNs were the only affected nodes in 3 patients who underwent subsequent CAD. In the other macrometastatic SLN patient, 4 metastatic I Berg level lymph nodes were found. No immunohistology was needed for the detection of metastasis. The biological characteristics of the patients are shown in Table 1.


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  		TABLE 1. Main characteristics of 41 DCISM patients evaluated
 
Postsurgical Treatments
All patients submitted to breast-conserving surgery received standard external radiotherapy (50 Gy to the whole breast and 10 Gy as a boost to the tumor bed). All the 41 patients were evaluated for adjuvant therapy according to the main predictive and prognostic factors.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
DCIS with microinvasion (DCISM) is a separate clinicopathological entity, distinct from pure DCIS without microinvasion. It is a true invasive breast carcinoma with well-known metastatic potential.14 The reported lymphatic metastatic spread is very variable in the different series, ranging between 0% and 14%. Perhaps this wide range may be explained by the diversity in the histopathological definition of the primary tumor in the past,15 but also depends on the different techniques utilized to stain axillary nodes (HE or immunohistochemical) and the subsequent kind of nodal metastasis detected (macro or micrometastasis).

In 1997, the American Joint Committee on Cancer defined microinvasive breast carcinoma as the extension of cancer cells beyond the basement membrane into the adjacent tissues, with no single focus larger than 1 mm in greatest dimension.16 This system refers only to the largest invasive component and ignores the size of the DCIS and the number of invasive foci. Successively, Silver and Tavassoli6 in 1997 defined microinvasion as a single focus of invasive carcinoma less or same to 2 mm or up to 3 foci of invasion, each less or same to 1 mm in greater dimension. In our series, using the TNM classification and following the criteria of Rosen and Obermann10 for the definition of the primary tumor, we found 41 DCISM (0.9%) of 4602 consecutive breast cancer submitted to breast surgery and SLNB at the European Institute of Oncology, with a 9.7% incidence of metastatic lymph nodes.

The surgical treatment of the axilla is also controversial. The CAD was routinely indicated in the past because of the prevalence of nodal metastases in DCISM was higher than pure DCIS. In contrast, the current prevailing view is that microinvasive carcinoma carries a very low risk of associated axillary nodal metastatic disease, which is similar to extensive high grade DCIS in several series, and has a comparable favorable prognosis with a low risk of subsequent development of metastatic disease and death.17 For this reason, some authors5,6,15,18–21 have advocated no CAD for DCISM (Table 2). The very low rate of axillary involvement in all reported cases could be due to the fact that all these patients were treated with the standard CAD in which only three to six H&E stained sections per lymph node are cut at 100–500 µm intervals and examined. This standard technique is not able to detect all axillary micrometastasis as SLNB does and could underestimate the axillary involvement rate of DCISM.22 The SLNB reduces the morbidity of axillary staging by minimizing lymphatic disruption,23 while improving the accuracy of staging because it allows a more thorough pathological examination of the SLN. In fact, because SLNB became a routine part of the clinical practice, it increased the detection rate of micro and macro axillary metastasis in invasive carcinoma.24,25,26 In our previous experience of 295 T1N0 breast cancer patients,13 the extensive intraoperative frozen section examination of SLN by H&E-stained serial multi sections correctly predicted a metastasis-free sentinel node in 95.4% of cases (negative predictive value) and was therefore suitable for identifying patients in whom CAD might be avoided. Immunocytochemical staining for cytokeratins or other epithelial markers may be helpful for reducing the risk of missing micrometastatic foci but did not increase the rate of axillary metastasis when they were compared to H&E stained serial multi sections technique. In only 4% of the positive cases the H&E findings were questionable, and cytokeratin immunostaining on the adjacent section was useful for confirming the presence of malignancy.


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  		TABLE 2. Axillary involvement in DCISM patients treated by axillary dissection
 
The techniques of lymphatic mapping and SLN biopsy have also been applied to cases of pure DCIS and DCISM in some series. The kind of metastasis, the frequency and the management of these patients have been only partially established. We previously demonstrated that, due to the low prevalence of metastatic involvement, in pure DCIS completely excised by radical surgery, SLN biopsy can be avoided. It may only be considered in cases of DCIS with a higher risk of harboring an invasive component at definitive histology (large solid tumors or diffuse or pluricentric microcalcifications), especially undergoing mastectomy, in which a successive SLN biopsy can no longer be performed.27 Zavostky,28 published 14 cases of DCISM that underwent intraoperative lymphatic mapping and SLN, and found two patients with positive SLNs (14.3%). The CAD revealed no further positive lymph nodes. The study population was too small for meaningful analysis of the incidence of axillary metastasis in DCISM but the authors confirmed the feasibility of SLNB as a staging alternative to conventional axillary dissection for this neoplasm. Of 31 patients with DCISM reported by Klauber-DeMore et al.,29 3 (10%) had positive SLNs and the SLN was the only metastatic node after CAD. Our series confirm previous results: four patients (9.7%) of 41 affected by DCISM had metastatic sentinel nodes. In two cases, there were micrometastasis. In three cases, no further positive lymph nodes were found after CAD. In one patient with macrometastatic SLN, four further positive axillary lymph nodes were found.

Due to the low number of positive SLN patients and the subsequent imbalance of the two groups, it is impossible to perform any kind of comparison between the SLN positive and negative DCISM patients (Table 1). With the only exception of the clinical presentation, we did not observe any difference between the biological characteristics of the two groups. The risk of lymph node metastasis does not seem to be correlated to grade, predominant histological pattern, sex steroid hormone receptor status, proliferative index (Ki67), perivascular invasion (PVI), or the type of surgery. Only the clinical presentation of the neoplasm seems to be important to predict the risk of SLN metastasis. In three of 4 patients with metastatic SLN, a large breast mass was palpable, whereas in nonmetastatic SLNs group, only 47% of patients had palpable mass. However, any kind of conclusion in this direction is impossible.

SLNs micrometastasis represent a controversial issue, with unknown clinical implications and prognostic value. The American Joint Committee on Cancer (AJCC) has stated that a lymph node with a metastatic deposit < 0.2 cm has the same prognostic implications as a negative node.16 In the recent sixth edition of the TNM Classification of Malignant Tumors of the International Union Against Cancer (UICC),30 patients with only isolated tumor cells (ITCs) in regional lymph nodes are classified as pN0. ITC are single tumor cells or small clusters of cells, not more than 0.2 mm in greatest dimension, that are usually detected by immunohistochemistry or molecular methods but which may be verified on H&E stains. ITCs do not typically show evidence of metastatic activity, proliferation, or stromal reaction. Furthermore, the risk to find further metastatic axillary lymph nodes in case of micrometastatic SN is very low. The randomized multicentric study of the International Breast Cancer Study Group (23–01 IBCSG) is actually enrolling patients affected by unicentric infiltrating carcinoma and micrometastatic SLNs in two arms: CAD and no treatment. The results of this study will provide useful indications about the prognostic value of the micrometastasis of SLNs. After this consideration, it appears reasonable to discuss with the patients affected by DCISM and micrometastatic SLNs the possibility of avoiding CAD.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Due to the significant rate of axillary metastasis in DCISM breast cancer, SLN biopsy should be considered a standard procedure in all these patients. SLNB can detect lymph node micrometastasis and accurately stage the axilla avoiding morbidity of a CAD. Complete AD may not be mandatory if only the SLN has micrometastatic disease. Informed consent and a careful discussion with the patients are very important in this decision.


   FOOTNOTES
 
Ductal carcinoma in situ with microinvasion is a true invasive breast carcinoma with metastatic potential. Sentinel lymph node biopsy should be considered as a standard procedure in these patients. It can detect nodal micrometastasis and accurately stage the axilla avoiding the morbidity of a complete axillary dissection.

Received for publication April 8, 2003. Accepted for publication August 25, 2003.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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