Annals of Surgical Oncology 10:102-107 (2003)
© 2003 Society of Surgical Oncology
Skin Involvement in Invasive Breast Carcinoma: Safety of Skin-Sparing Mastectomy
Chiu M. Ho, MS,
Colin K. L. Mak, FHKAM (Path),
Yvonne Lau, FHKAM (Surg),
Wing Y. Cheung, FHKAM (Surg),
Miranda C. M. Chan, FHKAM (Surg) and
Wai K. Hung, FHKAM (Surg)
From the Department of Surgery, Division of Plastic Surgery (CMH, WYC) and Breast Center (YL, MCMC, WKH), and the Department of Pathology (CKLM), Kwong Wah Hospital, Hong Kong SAR, China.
Correspondence: Address correspondence and reprint requests to: Chiu M. Ho, MS, Division of Plastic Surgery, Department of Surgery, Kwong Wah Hospital, Hong Kong SAR, China; Fax: 852-2781-5264; E-mail: hocm{at}ha.org.hk
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ABSTRACT
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Background: There is concern about the oncological safety of preserving most of the breast skin in skin-sparing mastectomy (SSM). Most supportive evidence for SSM evaluates the local recurrence rate on clinical follow-up.
Methods: The skin and 10 mm of the subcutaneous tissue of 30 total mastectomy specimens were studied with a step-serial sectioning technique. The incidence and mode of involvement of the skin and subcutaneous tissue were recorded in detail. This was correlated with other clinical and pathologic parameters.
Results: The incidence of skin involvement outside the nipple-areola complex was 20% (6 of 30). This was significantly related to the clinical T stage, site of the tumor, skin tethering, pathologic tumor size, and perineural infiltration. When the effects of both skin and subcutaneous tissue involvement were considered, the incidence of skin-flap involvement outside the nipple-areola complex was 23% (7 of 30). The significant parameters related to skin-flap involvement were skin tethering (75% vs. 15%; P < .05), pathologic tumor size (P < .03), and perineural infiltration (63% vs. 9%; P < .01).
Conclusions: It would be oncologically safe to perform SSM in T1 and T2 tumors, because the chance of skin involvement is small. It is safe to preserve the skin overlying the tumor if there is no skin tethering.
Key Words: Skin involvement • Invasive breast carcinoma • Skin-sparing mastectomy • Safety
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INTRODUCTION
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Skin-sparing mastectomy (SSM) is regarded as a major improvement in breast reconstruction over the past couple of decades. By preserving most of the skin of the native chest wall, the plastic surgeon is able to reconstruct a more symmetrical and natural breast mound, and the need for a matching operation on the normal contralateral breast can be reduced. However, there is still concern over the oncological safety of preserving most of the breast skin. In this study, we studied the mode and incidence of skin involvement in invasive breast carcinoma.
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MATERIALS AND METHODS
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Selection Criteria
Patients younger than 65 years who would most likely choose immediate breast reconstruction were recruited in the study. All of the patients had total mastectomy as part of the surgical treatment. Patients who had breast-conservation surgery were excluded from the study. Patients who had SSM were excluded because the purpose of this study was to look at the pattern of skin involvement in breast carcinoma. Only patients with invasive breast carcinoma were included. Patients who had ductal carcinoma-in-situ (DCIS) without an invasive component were not included. Patients who had radiotherapy before the operation were excluded.
Preparation of Specimens
The total mastectomy specimen was examined immediately after the operation. The size of the tumor and the presence of skin tethering or nipple retraction were reconfirmed. The site of the tumor was noted and categorized as subareolar or peripheral. The skin edges of the specimen were fixed onto a foam board by using pins and stitches to prevent shrinkage (Fig. 1). The whole specimen was immersed in a 10% formalin solution after its photograph was taken. The pathologist marked the outline of the palpable tumor on the skin by using water-resistant ink. Contour lines in intervals of 5 mm were drawn on the surface of the skin ellipse. The skin and the subcutaneous fat up to 1 cm in thickness were separated from the remaining breast tissue. The skin and the subcutaneous tissue were embedded and sectioned at 5-mm intervals from the center of the tumor up to 5 cm from the palpable edge of the tumor. The slides were stained with hematoxylin and eosin and examined under a light microscope.
Tumor involvement of the dermis and subcutaneous fat was documented in detail, with reference to the depth of its involvement from the skin surface and its distance from the edge of the main tumor. Skin involvement was defined as any tumor infiltration of the dermis. Tumor identified in the subcutaneous level but within 5 mm from the skin surface was separately recorded in detail. This is important because there is a possibility that tumor could be left on the skin flap elevated for SSM. This was categorized separately as subcutaneous tissue involvement. Other pathologic parameters recorded were tumor differentiation (modified Bloom and Richardson grading), size of tumor (macroscopic and microscopic), multicentricity of the tumor, presence of an extensive intraductal component, lymphovascular invasion, tumor satellites in the breast tissue, perineural invasion, lymph node involvement, estrogen and progesterone receptor status, and c-erbB-2 status.
Analysis of the data was performed on a personal computer with SPSS/PC+ version 10.0 (SPSSTM Inc., Chicago, IL). Groups were compared by using 
2 tests when appropriate. A statistically significant difference was reached when the P value was 
.05.
Patient Data
From March 1996 to October 1997, 30 consecutive patients who had invasive carcinoma of the breast were included in the study. The age of the patients ranged from 28 to 64 years, with a median of 45 years. The T and N stages are listed in Table 1. Most (73%) of the tumors were T2. The clinical size of the primary tumor ranged from 10 to 70 mm (median size, 30 mm). Three patients had primary systemic chemotherapy before surgery because of large tumors (>5 cm). Nipple retraction was noted in eight patients, but none of the patients had Paget’s disease or evidence of tumor involvement of the nipple. Tethering of the skin overlying the tumor was present in four patients. Most of the patients (73%) did not have clinically palpable lymph nodes. A total of 1078 histological sections were examined, and the average number of sections per patient was 36.
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RESULTS
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Involvement of the skin was identified in eight (27%) patients (Table 2). The nipple-areola skin was involved in seven patients. The skin overlying the tumor was involved in five patients. Skin involvement away from the location of the primary tumor was identified in three patients.
Since the nipple-areola complex (NAC) was not preserved in SSM, those patients with skin involvement of the nipple-areola skin were not considered to have clinically significant skin involvement. The true incidence of skin involvement was thus 20% (6 of 30). Of the five patients who had tumor involvement of the overlying skin, tethering of the overlying skin was evident clinically in three patients and represented direct tumor extension to the dermis (Fig. 2). In the two patients who did not have tethering of the overlying skin, the spread was via the dermal lymphatics (Fig. 3).
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FIG. 2. Direct tumor (t) infiltration of the dermis (arrows) (hematoxylin and eosin stain, whole mount).
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In the three patients who had skin involvement well away from the edge of the palpable tumor, the furthest spread away from the tumor was 5 cm, and lymphatic permeation in the dermal lymphatics was a prominent feature. All of them were T3 tumors, and two had clinical axillary lymph node metastasis. Two patients also received primary systemic chemotherapy.
Skin involvement was significantly related to the site of the tumor, clinical T staging, skin tethering, pathologic tumor size, and perineural infiltration (Table 3). Other factors that were evaluated but not significant included primary systemic chemotherapy, tumor differentiation (modified Bloom and Richardson grading), tumor multicentricity, an extensive intraductal component, lymphovascular invasion, lymph node involvement (clinical and pathologic), tumor satellites in the breast tissue, estrogen and progesterone receptor status, and c-erbB-2 status.
The pattern of subcutaneous tissue involvement within 5 mm from the skin surface by both invasive tumor and DCIS is shown in Table 4. Invasive carcinoma was identified in 11 patients: 10 at the NAC and 4 distant from the tumor edge but away from the NAC. Three patients had tumor involvement at both sites (Table 4). Pagetoid spread along the large ducts was present in five patients. DCIS was identified within 5 mm from the skin surface at the NAC in five patients. Only four patients had involvement beyond the NAC. In three patients, there was extensive lymphatic spread both in the dermis and the subcutaneous tissue. In the other patient, the spread in the subcutaneous tissue extended 1 cm beyond the edge of the tumor.
Again, only the subcutaneous tissue involvement outside the NAC was analyzed. Subcutaneous tissue involvement was significantly related to the clinical T and N staging, primary systemic chemotherapy, pathologic tumor size and N staging, vascular and lymphatic permeation, and the presence of tumor satellites in the breast tissue (Table 5). It was not related to other clinical parameters, such as skin tethering and nipple retraction, or to other pathologic parameters, such as tumor differentiation (modified Bloom and Richardson grading), perineural infiltration, estrogen and progesterone receptor status, and c-erbB-2 status.
When the effects of both skin and subcutaneous tissue involvement were considered, the incidence of skin-flap involvement outside the NAC was 23% (7 of 30). Three patients had skin involvement only (patients 1, 7, and 8), two patients had subcutaneous tissue involvement only (patients 3 and 14), and two patients had both skin and subcutaneous tissue involvement (patients 2 and 4). The significant parameters related to skin-flap involvement were skin tethering (75% vs. 15%; P < .05), pathologic tumor size (P < .03), and perineural infiltration (63% vs. 9%; P < .01).
The incidence of involvement of the NAC was very high (57%): 7 patients had dermal involvement, 10 had tumor in the subcutaneous tissue, and 5 had DCIS. NAC involvement was significantly related to the presence of nipple retraction (88% vs. 32%; P < .01), the presence of axillary lymph node involvement (88% vs. 45%; P < .05), and centrally located tumor (91% vs. 37%; P < .01; Table 6). It was also related to other pathologic parameters such as perineural infiltration and vascular and lymphatic permeation.
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DISCUSSION
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Toth and Lappert1 first coined the term skin-sparing mastectomy in 1991. This operation is used for patients with early breast cancer who are treated with total mastectomy and immediate breast reconstruction. It is believed that by preserving the skin envelope, a more symmetrical and natural breast reconstruction is possible; that the amount of tissue transfer is less; and that the need for surgery on the contralateral breast is reduced.
However, there is always a worry that by preserving the native breast skin, especially that overlying an invasive carcinoma, the chance of local recurrence will be higher. Several recent reports have shown that this is not the case (Table 7).2–5 The local recurrence rate from invasive cancer for patients treated with SSM was similar to those who had non-SSM.3,6,7
In this study, we investigated the pattern and frequency of skin and skin-flap involvement in invasive breast cancer with a detailed serial-section examination of the total mastectomy specimen. Our study supported the practice of routine removal of the NAC in mastectomy for invasive breast cancer. The incidence of nipple-areola involvement was 57%: 23% had tumor infiltration of the dermis, 33% had tumor within 5 mm of the skin surface, and 17% had DCIS in the lactiferous ducts. It is oncologically unsafe if the NAC is preserved. Kissin and Kark8 reviewed and summarized the significant parameters affecting NAC involvement and included clinical appearance, size of the tumor, centrally located tumors, poorly differentiated tumors, and axillary nodal metastasis. In our study, NAC involvement was significantly related to the presence of nipple retraction, the presence of axillary lymph node metastasis, centrally located tumor, and other pathologic parameters, such as perineural infiltration and vascular and lymphatic permeation.
The reported incidence of NAC involvement is 8% to 50%.8 The high incidence of NAC involvement in this study might be related to the fact that the skin flap was studied in detail by using serial sections. Also, this study excluded patients undergoing breast-conservation therapy. Tumors in these patients were usually small and located away from the NAC; both were low-risk factors for NAC involvement.
Laronga et al.9 reported a 6% occult NAC involvement in breast cancer patients undergoing SSM. This was significantly associated with subareolar or multicentric tumors and with the presence of positive lymph nodes. The authors concluded that NAC preservation would be appropriate in axillary node-negative patients with small, solitary tumors located on the periphery of the breast. This was supported in our study—the incidence of NAC skin-flap involvement was only 7% in peripherally located tumors. However, these patients are also candidates for breast-conservation treatment and may not opt for an SSM and immediate reconstruction. The median tumor size of the group was <1.5 cm in the series of Laronga et al., and whether the feasibility of NAC preservation can be extended to larger tumors still needs further study. On the basis of the results of this study (median tumor size, 3 cm), one has to be extra cautious because 23% of the patients had tumor infiltration of the dermis, which could not be removed if the NAC were to be preserved.
In SSM, the primary concern is skin involvement away from the NAC, because the nipple-areola skin is routinely removed. The true incidence of skin involvement if SSM was performed was 6 (20%) of 30 in our series; 5 (17%) had tumor involvement of the skin overlying the tumor, and 3 (10%) had involvement of the skin away from the tumor. This was high when compared with the 4.4% of neoplastic involvement of skin overlying the tumor reported by Fisher et al.10 However, Fisher et al. did not report further on the neoplastic spread in the skin away from the tumor. Wertheim and Ozzello11 analyzed sections of grossly uninvolved skin taken randomly from each quadrant of the breast, in addition to those taken at the site of any gross abnormality. They reported neoplastic involvement of the skin away from the nipple and areola in 113 (11.3%) of 1000 mastectomy specimens.
There are two modes of skin involvement in invasive breast cancer (Table 8): the tumor can infiltrate the overlying dermis directly, or it can spread via the dermal lymphatics. In this study, the skin involvement was clinically detectable because of tethering of the overlying skin in three patients. In the other three patients, it was associated with big (T3) tumors. All of them had extensive tumor spread in the skin and subcutaneous tissue via the lymphatics throughout the whole mastectomy specimen. Incomplete removal of the tumor seemed inevitable in these patients, even though a wider excision of the chest wall skin was performed.
In SSM, the skin flaps are elevated together with a thin layer of subcutaneous tissue to ensure that the vascularity is not destroyed. Tumors located in the superficial subcutaneous tissue may be included in the skin flaps and lead to local recurrence. Normally the thickness of the skin flaps ranges from 3 to 5 mm. In this study, we arbitrarily defined the subcutaneous tissue involvement as involvement within 5 mm from the skin surface. Seven (23%) of 30 patients had involvement of the skin flap, and the significant relevant parameters were the presence of skin tethering, pathologic tumor size, and the presence of perineural infiltration. This is a more realistic and reliable assessment of the likelihood of leaving tumor behind in SSM. Unfortunately, of the three parameters, only skin tethering can be detected before the operation. There were significant risks in performing SSM for T3 tumors, and the incidence of skin-flap involvement was 60%.
The incidence of skin-flap involvement in this study was higher than the reported local recurrence rates for SSM. It must be appreciated that the three patients who had tethering of the skin overlying the tumor would be routinely removed even if SSM were to be performed, and this would not result in a higher rate of local recurrence. There were another three patients who had extensive dermal and subcutaneous tissue lymphatic involvement 4 to 5 cm away from the edge of the tumor. All of these patients had T3 tumors, and the pattern of skin-flap involvement seemed to be an indicator of the aggressive behavior of the tumor. It was uncertain whether a wider skin excision would affect the outcome of this group. Another uncertain factor was the response of these microscopic tumors to radiotherapy and chemotherapy: these microscopic diseases might not have become macroscopic.
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CONCLUSION
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It is safe to preserve the skin overlying the tumor provided that there is no evidence of tethering of the skin. The chance of skin involvement in T1 and T2 tumors is small. Special attention should be given in those patients with T3 tumors, especially those who receive primary systemic chemotherapy.
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Acknowledgments
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The acknowledgments are available online at www.annalssurgicaloncology.org.
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Footnotes
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The incidence and pattern of skin involvement by invasive breast carcinoma was studied with step-serial sectioning of the total mastectomy specimen. Skin involvement was correlated with clinical and pathologic parameters, and its implications for skin-sparing mastectomy were evaluated.
Received for publication May 1, 2002.
Accepted for publication September 17, 2002.
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REFERENCES
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- Toth B, Lappert P. Modified skin incisions for mastectomy: the need for plastic surgical input in preoperative planning. Plast Reconstr Surg 1991; 87: 1048–53.[Medline]
- Kroll SS, Ames F, Singletary SE, Schusterman MA. The oncologic risks of skin preservation at mastectomy when combined with immediate reconstruction of the breast. Surg Gynecol Obstet 1991; 172: 17–20.
- Carlson GW, Bostwick J, Styblo TM, et al. Skin-sparing mastectomy: oncologic and reconstructive considerations. Ann Surg 1997; 4: 193–7.
- Slavin SA, Schnitt SJ, Duda RB, et al. Skin-sparing mastectomy and immediate reconstruction: oncologic risks and aesthetic results in patients with early-stage breast cancer. Plast Reconstr Surg 1998; 102: 49–62.[Medline]
- Newman LA, Kuerer HM, Hunt KK, et al. Presentation, treatment and outcome of local recurrence after skin-sparing mastectomy and immediate breast reconstruction. Ann Surg Oncol 1998; 5: 620–6.[Abstract]
- Kroll SS, Khoo A, Singletary E, et al. Local recurrence risk after skin-sparing and conventional mastectomy: a 6-year follow-up. Plast Reconstr Surg 1999; 104: 421–5.[Medline]
- Simmons RM, Fish SK, Gayke L, et al. Local and distant recurrence rates in skin-sparing mastectomies compared with non-skin-sparing mastectomies. Ann Surg Oncol 1999; 6: 676–81.[Abstract]
- Kissin MW, Kark AE. Nipple preservation during mastectomy. Br J Surg 1987; 74: 58–61.[Medline]
- Laronga C, Kemp B, Johnston D, Robb GL, Singletary SE. The incidence of occult nipple-areola complex involvement in breast cancer patients receiving a skin-sparing mastectomy. Ann Surg Oncol 1999; 6: 609–13.[Abstract]
- Fisher ER, Gregorio RM, Fisher B, Redmond C, Vellios F, Sommers SC. The pathology of invasive breast cancer. Cancer 1975; 36: 1–85.[CrossRef][Medline]
- Wertheim U, Ozzello L. Neoplastic involvement of nipple and skin flap in carcinoma of the breast. Am J Surg Pathol 1980; 4: 543–9.[Medline]
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TOP
ABSTRACT
INTRODUCTION
