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Annals of Surgical Oncology 9:161-164 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Pure Mucinous Carcinoma of the Breast: Is Axillary Staging Necessary?

Juan C. Paramo, MD, Christopher Wilson, MD, Diego Velarde, MD, Jaime Giraldo, MD, Robert J. Poppiti, MD and Thomas W. Mesko, MD, FACS

From the Departments of Surgery (JCP, DV, JG, TWM) and Pathology (CW, RJP), Mount Sinai Medical Center, Miami Beach, Florida.

Correspondence: Address correspondence and reprint requests to Juan C. Paramo, MD, Mount Sinai Medical Center, Section of Surgical Oncology, 4300 Alton Rd., Miami Beach, FL 33140; Fax: 305-674-2863; E-mail: jcparamo{at}med411.com


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Mucinous carcinoma of the breast (MCB) may be associated with a low risk of axillary metastases.

Methods: To evaluate the incidence of axillary nodal metastasis in MCB, a review of all cases from January 1990 to July 2000 was performed. Pure MCB was defined as all tumor cells being completely surrounded by mucin. Patient demographics, tumor size, estrogen receptor status, total number of dissected lymph nodes, and incidence of nodal metastasis were studied. Deeper sections on the lymph nodes from the pure tumors were performed and stained with low-molecular cytokeratin.

Results: Nineteen cases of pure MCB and 41 cases of mixed MCB were identified. Patients with pure MCB were older than those with mixed MCB. Tumor size and estrogen receptor status showed no statistically significant differences between the two groups. None of the patients with pure MCB demonstrated lymph node metastases, whereas 12 of 41 cases with mixed MCB demonstrated metastatic lymph node involvement.

Conclusions: Because pure MCB seems unlikely to metastasize, axillary lymph node staging in these patients may not be necessary. The presence of lymph node metastases strongly indicates the presence of a mixed MCB.

Key Words: Mucinous breast cancer • Axillary node staging • Axillary node dissection • Breast carcinoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Mucinous carcinoma of the breast (MCB) is a tumor containing large amounts of extracellular epithelial mucin surrounding and within tumor cells.1 On the basis of microscopic appearance, MCB is divided into two groups: pure MCB, in which the entire tumor consists of tumor cells with excessive extracellular mucin surrounding them, and mixed MCB, in which the tumor also contains areas with infiltrating carcinoma devoid of extracellular mucin.2,3

It has been recognized that pure MCB carries a better prognosis than other more frequent types of breast cancer.4–10 However, although pure MCB may have a lower incidence of lymph node metastases,1,4,5,10 the presence of axillary metastatic nodal disease still remains the most important negative prognostic factor in patients with breast cancer.1,2,11,12

This study is a review of our experience with MCB to determine whether axillary staging is necessary in patients with either pure or mixed MCB tumors.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All patients with tumors coded as pure or mixed MCB from the tumor registry and from the files of the Department of Pathology at our institution from January 1990 to July 2000 were reviewed. Pure MCB was defined histologically as that in which all the tumor cells were completely surrounded by mucin (Fig. 1). The diagnosis of mixed MCB was assigned to those tumors that also showed any component of invasive ductal carcinoma (Fig. 2). The entirety of all tumors was processed in all cases.



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  		FIG. 1. Pure mucinous carcinoma of the breast. Tumor cells are completely surrounded by mucin.

 


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  		FIG. 2. Mixed mucinous carcinoma of the breast. The tumor contains areas of infiltrating ductal carcinoma (arrow) devoid of extracellular mucin.

 
Patients’ demographics, tumor size defined by gross pathologic measurements, estrogen receptor status, and type of surgical therapy were evaluated in all cases. The total number of dissected lymph nodes was documented, as was the incidence of metastatic nodal involvement when stained with hematoxylin and eosin (H&E). In those tumors defined as pure MCB, deeper sections on the lymph nodes were performed and stained with low-molecular cytokeratin (CAM 5.2; Becton-Dickinson, San Jose, CA). This was performed to improve the detection of nodal micrometastases that might have been missed with standard H&E evaluation. Histological grading and ploidy were documented for all cases of pure MCB.

Statistical analysis for continuous data was performed with Student’s t-test. Ordinal data and ratios were compared by using a z-test with Yates correction. A P value of <.05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
A total of 60 cases of MCB were identified during the study period. All patients were women.

The pure MCB group consisted of 19 patients. The average age was 75 years (range, 59 to 90 years), with a median of 76 years. Average tumor size was 1.7 cm (range, .8 to 4 cm). All cases were low grade, diploid, and estrogen receptor positive. Eighteen (95%) cases were treated with lumpectomy and axillary node dissection, and one (5%) was treated with modified radical mastectomy.

The total number of lymph nodes studied per patient averaged 13 (range, 4 to 21). All nodes were determined negative for metastases on H&E examination. Deeper sections and staining with CAM 5.2 confirmed no evidence (0% incidence) of metastases in all examined lymph nodes.

The mixed MCB group consisted of 41 patients with an average age of 65 years (range, 35 to 89 years) and a median age of 68 years. The average tumor size was 2.0 cm (range, .7 to 7 cm), and an average of 18 (range, 4 to 41) nodes were examined per patient. A total of 39 patients (95%) were estrogen receptor positive. Thirty-eight (92%) patients were treated with lumpectomy and axillary node dissection, and three (8%) were treated with modified radical mastectomy.

Twelve patients (29%) of the mixed MCB group had lymph node metastases, with an average of 3 positive nodes per patient (range, 1 to 31 nodes per patient). We found no relationship between the tumor size and the incidence of lymph node metastases.

A comparison of the two groups is listed in Tables 1 and 2. Patients with pure MCB were older that their mixed counterparts (P = .02). However, tumor size (P = .5) and estrogen receptor status (P > .05) showed no statistically significant differences between the two groups.


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  		TABLE 1. Comparison between the pure and mixed mucinous carcinoma groups
 

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  		TABLE 2. Comparison of nodal disease between pure and mixed mucinous carcinoma groups
 
The patients with mixed MCB had a higher average of dissected nodes per patient when compared with the cases of pure MCB (P = .02). Likewise, the mixed MCB group had a significantly higher incidence (29%) of metastatic lymph node involvement than the 0% incidence in the pure MCB group (P = .05).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
MCB, also known as colloid carcinoma, constitutes 1% to 6% of primary breast cancers.3,6,11,13–15 MCB usually presents in postmenopausal women7,16 and is characterized by mucus production by the tumor.

MCB has been classified histologically into pure and mixed types. Pure MCB has a higher degree of mucus production than mixed MCB. In addition, mixed MCB contains areas of infiltrating ductal carcinoma. Because of these characteristics, mixed MCB has a more aggressive behavior, a higher rate of metastatic nodal involvement, and a decreased survival rate.1,2,4 The 10-year survival rate for pure MCB is 90% to 100%,1,17 whereas it is 60% in mixed MCB.1

Mammography and breast ultrasonography (US) provide clinically valuable information for the treatment of MCB.14,18 Pure MCB usually presents as a circumscribed lesion on a mammogram. Margins on US are usually well defined, and the tumor is isoechogenic relative to the fat surrounding the breast tissue. Mixed MCB, however, often shows an indistinct mammographic pattern and has a hypoechogenic signal on US.14,18 Because of these clearly different patterns, mammographic and US evaluations should be performed in all cases of MCB.

The incidence of axillary metastases is 2% to 14% in pure MCB2,4,10,14,16,17 and 45% to 64% in mixed MCB.1,2,17 This trend was corroborated in our study, although we found a lower incidence of nodal metastases (0% in pure MCB and 29% in mixed MCB). Because the status of the axillary lymph nodes is the most important determinant of prognosis in breast cancer, we can infer that pure MCB has a better prognosis than mixed MCB. This has been corroborated in previous studies.1,2,4,16,17

In patients with pure MCB, Avisar et al.16 demonstrated that there are certain factors associated with a higher incidence of axillary nodal disease. These include younger age, aneuploidy, high nuclear grade, and a negative estrogen receptor status. Our study corroborates these findings, because all our pure MCB cases were diploid, had low nuclear grade, were estrogen receptor positive, and had a 0% incidence of nodal metastases.

Patients in the pure MCB group were older than the mixed MCB group. We found no relationship between tumor size and the incidence of axillary metastatic involvement in the mixed MCB group. Although we did not measure the size or percentage of the nonmucinous component in the mixed MCB cases, other studies have shown no relationship between the size or degree of the mucin component and the incidence of axillary nodal metastases and prognosis.1,2 For pure MCB, size does not correlate with the incidence of metastatic involvement, although smaller tumors carry an excellent prognosis.10,16

In our study we used immunohistochemistry to verify the negative status of all axillary lymph nodes in cases of pure MCB. This was performed to improve the detection of micrometastases and therefore the overall sensitivity.19 Immunohistochemical staining is not a cost-effective technique when performed on all excised nodes. The sentinel node technique for axillary staging in breast cancer may enable the detection of axillary nodes that are most likely to contain metastatic deposits from the primary tumor.20 Although controversial, immunohistochemical evaluation of these nodes is therefore reasonable and should be cost-effective in experimental protocols.

It is important to emphasize that a complete sampling of the entire tumor needs to be performed to classify it as a pure MCB. Because of the very low incidence of axillary nodal metastases in pure MCB (0% in our study), axillary nodal dissection may be unnecessary. The sentinel node technique may be an option because it might identify the rare patient who may have a positive axilla with pure MCB and provide staging for the patient who in reality has a mixed tumor falsely interpreted as a pure MCB. The sentinel node technique, however, should be validated by individual surgeons and institutions, as is currently being done in national experimental protocols.

Because the incidence of axillary nodal metastases was 0% in pure MCB and 29% in mixed MCB in our study, the presence of axillary metastatic involvement in an MCB patient should strongly indicate the presence of a mixed MCB, with its concomitant worse prognosis.

Received for publication March 17, 2001. Accepted for publication September 26, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  5. Rosen PP, Wang T. Colloid carcinoma of the breast: analysis of 64 patients with long term follow-up (abstract). Am J Clin Pathol 1980; 73: 304.
  6. Silverberg SG, Kay S, Chitale AR, Lewitt SH. Colloid carcinoma of the breast. Am J Clin Pathol 1971; 55: 355–63.[Medline]
  7. Simpson JF, Page DL. Prognostic value of histopathology in the breast. Semin Oncol 1992; 19: 254–62.[Medline]
  8. Gallager HS. Pathological types of breast cancer: their prognosis. Cancer 1984; 53: 623–9.[Medline]
  9. Melamed MR, Robbins GF, Foote FW Jr. Prognostic significance of gelatinous mammary carcinoma. Cancer 1961; 14: 699–704.[Medline]
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  12. Garne JP, Aspegren K, Linell F, Rank F, Ranstam J. Primary prognostic factors in invasive breast cancer with special reference to ductal carcinoma and histologic malignancy grade. Cancer 1994; 73: 1438–48.[CrossRef][Medline]
  13. Ackerman LV, Rosai J. Breast invasive carcinoma.In: Ackerman LV, Rosai J, eds. Ackerman’s Surgical Pathology. 8th ed. St. Louis: Mosby, 1996: 1607–9.
  14. Memis A, Ozdemir N, Parildar M, Ustun EE, Erhan Y. Mucinous (colloid) breast cancer: mammographic and US features with histologic correlation. Eur J Radiol 2000; 35: 39–43.[CrossRef][Medline]
  15. O’Connell JT, Shao ZM, Drori E, Basbaum CB, Barsky SH. Altered mucin expression is a field change that accompanies mucinous (colloid) breast carcinoma histogenesis. Hum Pathol 1998; 29: 1517–23.[CrossRef][Medline]
  16. Avisar E, Khan MA, Axelrod D, Oza K. Pure mucinous carcinoma of the breast: a clinicopathologic correlation study. Ann Surg Oncol 1998; 5: 447–51.[Abstract]
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  19. International (Ludwig) Breast Cancer Study Group. Prognostic importance of occult axillary lymph node micrometastases from breast cancers. Lancet 1990; 335: 1565–8.[CrossRef][Medline]
  20. Veronesi U, Paganelli G, Galimberti V, et al. Sentinel node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 1997; 349: 1864–7.[CrossRef][Medline]



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