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Annals of Surgical Oncology 9:924-928 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Stage Migration After Biopsy of Internal Mammary Chain Lymph Nodes in Breast Cancer Patients

Viviana Galimberti, MD, Paolo Veronesi, MD, Paolo Arnone, MD, Concetta De Cicco, MD, Giuseppe Renne, MD, Mattia Intra, MD, Stefano Zurrida, MD, Virgilio Sacchini, MD, Roberto Gennari, MD, Annarita Vento, MD, Alberto Luini, MD and Umberto Veronesi, MD

From the Divisions of Senology (VG, PV, PA, MI, SZ, AV, AL, UV), Nuclear Medicine (CDC), and Pathology (GR), European Institute of Oncology, Milan, Italy; Breast Service (VS), Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York; and Divisione di Chirurgia Generale (RG), Fondazione Salvatore Maugeri, Pavia, Italy.

Correspondence: Address correspondence and reprint requests to: Viviana Galimberti, MD, European Institute of Oncology, Via Ripamonti 435, 20141 Milano, Italy; Fax: 39-02-57489780; E-mail: viviana.galimberti{at}ieo.it


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Involvement of the internal mammary chain lymph nodes (IMNs) is associated with worsened prognosis in breast cancer. Use of lymphoscintigraphy to visualize sentinel nodes reveals that IMNs often receive lymph from the area containing the tumor.

Methods: We biopsied IMNs in 182 patients because there was radiouptake to the IMNs or because the tumor was located in the medial portion of the breast. After tumor removal, pectoralis major fibers were divided to expose intercostal muscle. A portion of intercostal muscle adjacent to the sternum was removed. Lymph nodes and surrounding fatty tissue in the intercostal space were freed, removed, and analyzed histologically. The pleural cavity was breached in four cases (2.2%), with spontaneous resolution.

Results: IMNs were found in 160 (88%) of 182 patients; 146 (94.4%) were negative and 14 (8.8%) were positive. The latter received internal mammary chain radiotherapy. The axilla was negative in 4 of 14 cases and positive in 10.

Conclusions: IMNs can be quickly and easily removed via the breast incision with insignificant risk and no increase in postoperative hospitalization. The patients with a positive IMN migrated from N0 (4 cases) or N1 (10 cases) to N3, prompting modification of both local (radiotherapy to internal mammary chain) and systemic treatment; without IMN sampling, they would have been understaged.

Key Words: Breast cancer • Stage migration • Internal mammary chain • Sentinel node biopsy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The last two decades have seen major advances in the treatment of breast cancer, thanks to greater understanding of breast cancer biology, advances in technology, earlier detection, and improved staging. It is now often possible to conserve the breast and spare the axillary nodes. The development of regional lymph node mapping has been fundamental in improving the staging of breast cancer. After initial reports in the mid 1990s,1,2 numerous series have demonstrated that sentinel node biopsy can reliably predict axillary node status, permitting avoidance of complete axillary dissection when the biopsied node is negative.3–10 However, use of this technique requires a more complete and careful pathologic examination of the sentinel node than is traditionally performed on lymph nodes, and this has led to the more frequent discovery of micrometastases, with improved staging accuracy as a consequence.2,11–15

When radioactive tracer plus lymphoscintigraphy is used to localize the sentinel nodes before surgery, lymph nodes in the internal mammary chain are sometimes picked out.16–19 This lymphatic drainage pathway from the breast has been ignored in recent decades after randomized trials that showed that internal mammary chain dissection did not improve survival.20–23 Nevertheless, the long-term results of these trials did show that the metastatic status of the internal mammary chain is as important prognostically as the status of the axillary nodes and, in particular, that the prognosis is very unfavorable if both axillary and internal mammary chain lymph nodes (IMNs) are involved.20,24,25 We decided to perform a pilot study to assess the feasibility of biopsying IMNs, to determine how often they are metastatic, and to assess the effect of their status on disease stage and consequent adjuvant therapy decisions.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between September 1998 and September 2001, we explored IMNs in 182 consecutive patients with breast cancer conforming to one of the following criteria: (1) radioactive uptake to the IMN region, as revealed by lymphoscintigraphy after peritumoral (131 cases) or superficial (16 cases) injection of radiotracer, or (2) tumor location in the medial portion of the breast, as defined in Fig. 1. The characteristics of these patients are listed in Table 1.



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  		FIG. 1. Diagram illustrating the policy for internal mammary chain lymph node (IMN) biopsy in the absence of radio-uptake to the IMN region. II/III i.s., 2nd/3rd intercostal space.

 

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  		TABLE 1. Patient characteristics
 
In 30 patients, surgical exploration of the opened intercostal space did not reveal macroscopically identifiable lymph nodes: these are in any event small and difficult to distinguish from adipose lobules. In these cases, we removed the adipose tissue and sent it to the pathologist; in 22 cases (12.0% of total), no lymph nodes were found. These 22 patients are not considered further.

Of the remaining 160 patients, 154 received conservative breast surgery, and 71 of these underwent axillary dissection; the remaining 83 received axillary sentinel node biopsy as the only axillary treatment. Six patients received ablative surgery, one of whom was not given axillary dissection.

Radiotracer was injected before surgery in 147 patients, and radioactive take-up was observed in the IMN area in 95 of these. In the 52 patients in whom no take-up was observed in this area and in the 13 patients in whom no tracer was injected (65 cases in all), we sampled IMNs without the aid of a gamma-detecting probe. In these 65 patients, the tumor was always located medial to a vertical line drawn to touch the lateral margin of the areola (Fig. 1). Taking into account the anatomy of the lymphatic network of the breast, we decided to explore the second intercostal space if the tumor was located in the inner-upper quadrant and to explore the third intercostal space if it was in the lower quadrant. Post hoc analysis of scintigraphic data in 147 patients revealed that for tumors in the upper quadrant (101 cases), the radioactive node was in the first space in 6 cases, in the second space in 68 cases, and in the third space in 27 cases. For tumors in the lower quadrant (41 cases), the hot node was in the second space in 2 cases, in the third space in 31 cases, and in the fourth space in 1 case. For central tumors (five cases), two nodes were in the second space and three in the third space. These data confirmed our anatomical intuition.

In patients with an IMN identified by lymphoscintigraphy, the node was removed with the aid of a handheld gamma-detecting probe. After surgery to remove the breast tumor, breast tissue was detached from the fascia of the pectoralis major to provide access. The longitudinal fibers of the pectoralis major were divided to expose the sternum and the two ribs and their intercostal muscle immediately above the hot spot (Fig. 2a) or space of interest. A short strip of intercostal muscle adjacent to the sternum was removed, providing access to the subcostal space and exposing the internal mammary vein and artery surrounded by fat containing small lymph nodes, under which lies the pleural membrane. The fatty tissue was carefully freed from the blood vessels, taking care not to damage these or the underlying pleura (Fig. 2b). If a hot spot had been revealed by lymphoscintigraphy, the probe was used to assist the location and excision of this material. In patients with no radioactive take-up in the IMN region or who were not injected with radiotracer, the second intercostal space was opened if the tumor was in the upper-inner quadrant, and the third intercostal space was opened if the tumor was in the lower-inner quadrant. In both these cases, fatty tissue considered to contain lymph nodes was removed. After careful hemostasis, the fibers of the pectoralis major were joined with sutures, and the breast was reconstructed as usual.



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  		FIG. 2. Drawings showing (a) ribs, sternum, and intercostal muscle and (b) the position of fatty tissue and blood vessels in the subcostal space (the authors thank Dr. Vittorio Fornasari, of La Sapienza University, Rome, for this drawing).

 
All material removed from the subcostal space was sent for permanent section histological analysis, without frozen section examination because the intraoperative result would not influence the surgical treatment. By contrast, in patients undergoing axillary sentinel node biopsy, the sentinel node was examined during surgery to determine whether axillary dissection should be performed immediately.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In the 147 patients given lymphoscintigraphy, we found uptake to the IMC only in 12 cases, to both the IMC and axilla in 82 cases, and to the axilla alone in 53 cases. An average of 1.4 IMNs per patient were recovered from the 160 patients. Among these, 146 (91.2%) had negative IMNs (45 with positive and 101 with negative axillary nodes), and 14 patients (8.8%) had a metastatic IMN (Table 2). In 4 of the 14 cases with a metastatic IMN, the axilla or axillary sentinel node was negative; in the remaining 10, the axilla was positive (6 cases with 1 positive lymph node, 1 case with 2, 1 with 3, 1 with 5, and 1 with 26 positive axillary lymph nodes). Four patients had micrometastatic IMNs. The involved node was removed from the second intercostal space in 9 of 14 patients, from the first space in 1, and from the third space in 4. Among the 10 patients with a positive IMN and positive axillary sentinel node, the sentinel node was the only positive axillary node in 6. All 14 patients with metastatic IMNs received mammary chain radiotherapy.


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  		TABLE 2. Axillary (Ax) status and internal mammary node (IMN) status
 
The pleural cavity was accidentally breached when sampling internal mammary material in four cases (2.2%). The tear was immediately sutured. These cases resolved spontaneously, and drainage was not necessary. Another patient developed a serous accumulation above the breached costal space which resolved after aspiration.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Complete dissection of the IMNs is an aggressive treatment that does not improve prognosis.20,24,25 However, Veronesi et al.21 found that survival was significantly poorer in patients with both the axillary and IMNs involved. It remains unclear whether radiotherapy to the internal mammary chain can improve survival in patients with positive IMNs.26–28

After the interest shown by surgeons in the internal mammary chain in the 1960s and 1970s, the problem of IMN involvement was ignored until recently. With the development of lymphoscintigraphic methods to visualize sentinel nodes in breast cancer, it has become evident that the IMNs often receive lymph from the breast area containing the tumor. This has again raised the problem of IMNs in breast cancer and has at the same time provided a method by which they can be investigated. This pilot study has shown that these nodes can be easily removed through the incision used for breast resection or quadrantectomy in breast-conservative surgery. Furthermore, the sampling method we developed is simple and quick to perform and is often performed while waiting for the result of the intraoperative histological examination of the axillary sentinel node. The risks of the procedure also proved to be insignificant and did not increase the postoperative hospitalization period, showing that the procedure is not aggressive and is well tolerated.

Our unpublished data indicate that when radiotracer is injected superficially, uptake by IMNs is rare. We therefore decided to biopsy IMNs in some cases even when there was no uptake; furthermore, in other cases no radiotracer was injected, for example, when axillary nodes were palpable. Our series therefore consists of two separate subgroups: (1) 195 patients with radiouptake to the intramammary chain in whom we sampled the internal mammary chain sentinel node and (2) 65 patients with no uptake to the intramammary chain in whom the sampling was decided according to the location of the primary carcinoma.

What have we learned from this experience? We found an involved IMN in 14 (7.7%) of the 182 cases explored, or 8.8% of the 160 patients in whom IMNs were found. According to the International Union Against Cancer staging classification, these cases migrated from N0 (4 cases) or N1 (10 cases) to N3. If internal mammary sampling had not been performed, they would have been understaged. The change of stage led to a modification of the postoperative treatment plan, with radiotherapy given to the internal mammary chain and systemic therapy also given in some cases.

Obtaining information on IMN involvement has two implications. First, if it is reasonable to remove the axillary nodes when the sentinel node is positive, then it is consistent to irradiate the internal mammary chain when an IMN is positive, in the hope of destroying other IMN metastases. Second, because IMN involvement carries a worse prognosis,20 more aggressive (anthracycline-based) chemotherapy should be applied. In fact, we gave systemic therapy to the four patients who would have been N0 without the IMN result.29

To conclude, we have developed a conservative technique that provides more accurate staging of breast cancer patients. It remains to be seen whether this additional information can lead to better survival.


   Acknowledgments
 
We thank D. C. Ward for help with the English.


   Footnotes
 
It is feasible and safe to surgically biopsy internal mammary chain lymph nodes during breast tumor removal, providing more accurate disease staging. It is logical to give more aggressive therapy to cases in which the biopsied node is metastatic.

Received for publication February 22, 2002. Accepted for publication June 17, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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