Journal of Surgical Oncology 49:189-195 (1992)
Chest Wall Resection for locally Recurrent Breast Cancer: Indications, Technique, and Results STEVEN T. BROWER,
HUBERT WEINBERG, MD, PAUL I. TARTTER, MD, AND JORGE CAMUNAS, MD From the Departments of Surgery (S.T.B., P.I.T., H.W.) and Cardiothoracic Surgery (J.C.), Mount Sinai Medical Center, New York, New York MD,
A series of 100 patients with locally advanced carcinoma of the breast was analyzed for chest wall recurrence alone after primary treatment. Five patients were found to have had chest wall recurrence alone and were treated with en bloc chest wall resection. This group of patients was analyzed for the pathophysiology of recurrence including characteristics of the primary tumor, location of the chest wall recurrence, and overall local salvage and survival after chest wall recurrence. In this series, local recurrence after radical chest wall resection was 20%. The incidence of systemic recurrence after chest wall resection was 60%. The mean survival for the entire group was 17 months after chest wall recurrence and radical resection. The main surgical objectives, including relief from painful, inflammatory, and bleeding complications, were achieved in all patients after chest wall resection. Although patients with isolated chest wall recurrence included a highly selected group, chest wall resection with myocutaneous reconstruction may provide long-term disease-free survival for these patients. 0 1992 Wiley-Liss, Inc. KEYWORDS:salvage, treatment of breast carcinoma, advanced breast carcinoma
INTRODUCTION The spectrum of recurrence for carcinoma of the breast is variable and distant sites predominate with chest wall recurrence accounting for only 5-30% of patients [ 1,2]. Although late recurrence to the chest wall after mastectomy associated with systemic recurrence has been noted, the usual pattern of recurrence to the chest wall occurs within 2 years and is usually a harbinger of distant metastasis [3,4]. In this circumstance, optimal and rational treatment for the chest wall recurrence includes a multidisciplinary approach in which concern for the systemic disease is prioritized. This includes a combination of surgical biopsy of the chest wall recurrence and in most circumstances local chest wall irradiation and systemic chemotherapy [ 5 ] . The local control rate has varied from 15 to 50% and the overall median survival with simultaneous local and systemic recurrence is 9-12 months [2,3]. Chest wall recurrence after mastectomy occurs without demonstrable clinical evidence of systemic breast cancer 0 1992 Wiley-Liss, Inc.
in 2 5 4 5 % of patients [5]. Although the number of patients with this form of local chest wall breast recurrence is quite small, some authors have documented reasonable disease-free survival after surgery for chest wall recurrence and some series have documented long-term survivors [5,6]. Palliation of isolated chest wall recurrence is also important in this setting. Local chest wall recurrence may rapidly progress with destruction of the overlying skin and underlying ribs and sternum, requiring salvage treatment for advanced and life-threatening infection or bleeding. In an effort to prevent these debilitating, painful, and life-threatening circumstances, we have taken an aggressive approach to the treatment of chest wall recurrence after mastectomy for breast carcinoma in the absence of Accepted for publication December 9, 1991. Address reprint requests to Dr. Steven T. Brower, Division of Surgical Oncology, Department of Surgery, Box 1259, Mount Sinai Medical Center, 1 Gustave L. Levy Place, New York, NY 10029.
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systemic recurrence. We report on our indications, techniques, and results in a group of five breast cancer patients treated with aggressive surgery as part of the approach to isolated chest wall recurrence.
MATERIALS AND METHODS Since I986 patients on the Breast Service at The Mount Sinai Medical Center with locally advanced disease (stages IIB, IIIA, IIIB) have been placed in a prospective tumor registry. This registry includes 100 patients of whom 5 were found to have chest wall recurrence alone. The pathology material and tumor registry data collected on each patient were reviewed. For the purpose of this study, a local chest wall recurrence was defined as a pathological positive mammary carcinoma biopsy that occurred in the skin, subcutaneous tissue, musculoskeletal, or lymph nodal area within the ipsilateral operated site. Analysis included only patients who had undergone simple mastectomy or modified radial or radical mastectomy for their initial treatment of carcinoma of the breast. The age range of the patients was 47 to 65 years. The follow-up period after resection ranged from 9 months to 3 years with a median follow up of 17 months. All patients prior to being considered for salvage by en bloc recurrence were vigorously scrutinized for metastatic disease. This included routine blood chemistries as well as determination of lipid associated sialic acid, carcinoembryonic antigen (CEA), and CA 15-3 serum markers, as well as chest x-ray and bone scan. In addition, all patients had an abdominal and chest CT scan and some patients were subjected to bone marrow aspirates or biopsies. Technique of Chest Wall Resection The strategy for chest wall resection is planned by a multidisciplinary group of surgical oncologists, thoracic surgeons, and plastic and reconstructive surgeons. Bulky disease was found attached to either the underlying bony chest wall or pleura (Fig. 1). Although the recurrence may be localized to any area of the chest wall or scar, we assumed a wide area of microscopic infiltration especially along the skin, subcutaneous tissue, and chest wall musculature (Fig. 2). Accordingly, a wide paddle of skin and subcutaneous tissue was included in the chest wall resection with no attempt to preserve soft tissue for closure. Similarly, the extent of parietal pleura, intercostal muscle, or bony rib involvement was ascertained by the thoracic surgeon, and a margin of normal muscle and ribs was sacrificed well around the lesion within the thoracic cavity. Since no attempt was made to conserve chest wall tissue, we have relied upon myocutaneous flap reconstruction [7-lo]. The location of the chest wall tumor recurrence was carefully noted and a circular or elliptical incision on the chest wall was made with a large radius of normal skin around the lesion. Frequent frozen-section biopsies were
taken of skin and muscle to ensure negative microscopic margins. The dissection was continued through the pectoralis major muscle and essentially encompassed the entire scar. Laterally, the serratus was released from the ribs. With fixation to the underlying ribs or sternum, the deep tumor-free margin was assumed to be the intrathoracic cavity. The chest wall musculature above and below the rib or interspace of the prior scar were divided in the anterior axillary line. The surgeon then palpated the parietal pleura to make sure there were no nodules at this lateral margin of the chest wall. If this was free of tumor, resection of the soft tissue and rib(s) proceeded from lateral to medial. Beneath the area of the chest wall recurrence, we occasionally saw a cicatrix of parietal pleura, with some puckering of the pleura, intercostal muscle, and periosteal reaction. Care was taken not to disrupt this architecture, which surrounded the tumor and contained microscopic disease. The dissection continued medially to the costostemal margin, where once again the ribs were divided and the en bloc specimen was removed leaving the uninvolved visceral pleura and pericardium intact (Fig. 3 ) .
RESULTS We have recently performed resection and reconstruction in five patients following extensive local recurrence after carcinoma of the breast (Table I). Patient 1 had been treated 2 years previously with a modified radical mastectomy for an ulcerated 6 cm primary tumor with positive lymph nodes. The patient had recurrence noted as a subcutaneous nodule. CAT scan evaluation revealed an enlarged internal mammary lymph node that had eroded the overlying costostemal border (Fig. 4). This mass had grown in size while the patient continued on chemotherapy and it was felt that salvage therapy was indicated. The salvage resection included a full-thickness chest wall resection of ribs 2, 3, and 4 as well as the left hemisection of the manubrium and upper third of the sternum. This was followed by reconstruction using a Marlex mesh-methylmethacrylate lattice covered with a transverse rectus abdominus myocutaneous (TRAM) flap. After our salvage en bloc resection of chest wall, sternum, and pericardium, she was symptom free for 6 months. However, at that time, recurrence was noted with bilateral pleural effusions. The patient ultimately succumbed 12 months after our palliative surgery with no evidence of local recurrence. Patient 2 presented with an infiltrative recurrence along the pectoralis fascia fixed to the overlying skin after modified radical mastectomy completed 18 months prior to the current surgery. The prior infiltrating breast cancer was a large, 8 cm cancer (stage IIIA). Although the recurrence at this time was over a wide field area (approximately 6 X 6 cm) it was felt that en bloc resection with a wide paddle of skin could achieve negative margins. Accordingly, full-thickness chest wall resection was com-
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Fig. 1. A: Bulky recurrent chest wall tumor at medial edge of prior mastectomy incision fixed to underlying pectoralis muscle, ribs, and sternum. B: CT scan of patient in A with obvious large anterior chest wall recurrence but associated bulky retrosternal, costosternal, and pleural disease with attachment to underlying pericardium.
pleted with TRAM myocutaneous flap (Fig. 5). The final pathology revealed recurrent breast cancer with all lateral and deep margins clear of microscopic tumor. At 9 months of study, the patient continues without any evidence of local or systemic recurrence. Patient 3 was a 60 year old female who presented initially with stage IIIA carcinoma of the breast. This was treated with modified radical mastectomy. At approximately 9 months, recurrence was noted at the midportion of the scar closure. No evidence of systemic disease was noted at this point. Full-thickness chest wall resection of skin, muscle, ribs, and pleura was completed with TRAM flap (Fig. 6A). The patient remained without any evidence of disease for 20 months. At that time, OSSeOUS metastases were noted with no evidence of local recurrence. The patient is currently symptom free after radia-
Fig. 2. Extensive full thickness chest wall recurrence with involvement of skin, subcutaneous tissue, and underlying pectoralis, intercostal and serratus muscles. Note en bloc resection of all tissue involved with free margin at transected ribs
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vival for the entire group is 17 months, with one patient living 3 years. The incidence of systemic recurrence after chest wall resection was 60%. Local recurrence after chest wall resection was 20%. No patient with a local recurrence after our salvage resection had a delay in the diagnosis of recurrence due to the overlying myocutaneous flap. It was clear that skin had been infiltrated by microscopic disease and nodularity. This is similar to the findings of Wagman et al. demonstrating that the TRAM flap does not delay diagnosis for recurrent breast carcinoma [ 111.
DISCUSSION We have described our favorable experience with en Fig. 3. Chest wall defect following extensive resection of recurrent bloc chest wall resection following recurrence of carcibreast cancer. Visceral pleura, lung parenchyma, sternum, ribs, and noma of the breast after mastectomy. We have attempted soft tissue are free of microscopic tumor. to understand the patterns of dermal, lymphatic, and musculoskeletal recurrence in an effort to achieve a strategy for maximal wide excision. This has required that we tion therapy and chemotherapy with complete healing of view the chest wall recurrence as a full-thickness recurrence. Our main objectives for this approach were to the chest wall resection and reconstruction (Fig. 6B). Patient 4 presented with stage IIIB carcinoma of the render the patient free of painful, inflammatory, infecbreast with satellite nodules throughout the breast and tious, and bleeding complications associated with chest fixation to the pectoralis major muscle and ipsilateral wall recurrence. In this setting, our palliative treatment lymph nodes. Twenty-four months earlier, the patient was uniformly successful. Although survival in this small had undergone radical mastectomy with local radiation group of patients was not altered, a number of the patients therapy and systemic chemotherapy. At the time of recur- lived for an extended period of time. We have carefully selected patients whom we feel are rent presentation the patient had infiltration of the scar, skin, and periosteum. There was no evidence of systemic candidates for this extensive surgery. In this way we have recurrence. She underwent en bloc resection of chest wall ensured the excellent local results. Patients who would including ribs 3 through 5. Because of the prior radical not be eligible for this surgery include patients with metmastectomy, Gortex mesh and combined latissimus dorsi astatic disease. In addition, patients with a local recurand TRAM flap reconstruction was chosen. This patient rence with multiple pleural nodules or skip lesions at a remained symptom free for 6 months. However, at that distance from the recurrence on the parietal pleura are time recurrence within the reconstructed site was noted. excluded from surgery. Neither fixation to the chest wall Extensive edema of latissimus dorsi flap and infiltration nor extensive skin involvement precludes successful en of the flap margins with tumor nodules was noted. This bloc resection. With newer techniques of myocutaneous recurrence might have been predicted by two prior local transfer, areas as great as 20 cm2 have been encompassed attempts with radiation and chemotherapy after chest re- including a portion of the sternum and contralateral breast currence prior to transfer to our medical center for ulti- skin and tissue. Recurrence within the internal mammary mate control of disease. There was no intrapleural recur- nodal group and adherence to the sternum or chest wall is rence noted beneath the prosthesis, Malignant pleural not a contraindication to chest wall resection. However, effusions and regional lymphadenopathy were noted 11 our results indicate that these patients are at extremely months after surgery. high risk for systemic disease, and a vigorous attempt to Patient 5 presented with a subcutaneous nodule supe- eradicate systemic metastases with chemotherapy should rior to the scar of a prior modified radical mastectomy. be developed. This nodule was fixed to the underlying pectoralis major Chest wall recurrence from carcinoma of the breast is a muscle and on the bone scan was thought to involve the result of a variety of biological and anatomic considerfifth rib at the midclaviclar line. Accordingly, a full- ations. The most common situation is that of the growth thickness resection was performed with TRAM flap re- of resistant metastases, both locally at the site of prior construction. This patient remains free of local and sys- definitive surgery and at the same time the growth of temic disease after chemotherapy for her chest wall microscopic metastases at multiple distant sites. In this recurrence at 3 years after surgery. situation the chest wall recurrence is usually a predictor Overall survival was unaffected by chest wall resection of systemic disease that manifests in 1-4 months [12]. for recurrent carcinoma of the breast. The median sur- Alternatively, the local recurrence may be the result of
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TABLE 1. Chest Wall Resection for Recurrent Breast Cancer Lymph node status
Time on studv (months)
Age
Stage
1
12
50
IIIB
+
2 3
9 22
65 60
IIIA IIIB
-
4
11
47
IIIB
+
5
38
52
IIIB
+
Patient
Characteristics of the primary tumor
Initial surgery a
Ulceration, fixation
MRM
Large (8 cm) Large, ulceration
MRM MRM
Satellite nodule pectoralis major involvement Large, ulceration
Radical mastectomy MRM
Location of chest wall recurrence
Recurrence after chest wall resection Local
Systemic
Costosternal junction, internal mammary nodal group Pectoralis fascia Subcutaneous nodule, scar, pectoralis major muscle Scar, skin, rib, periosteum
-
+
Subcutaneous nodule, Dectoralis fascia
-
-
+
+
-
-
+
~~
aMRM, modified radical mastectomy.
Fig. 5 . Reconstruction of the chest wall defect following en bloc resection. Prosthetic mesh has been fixed to cut ends of ribs. Note abdominal TRAM myocutaneous flap being fashioned for transfer to chest wall location. Fig. 4. Retrosternal extension of costosternal breast cancer recurrence. Note probable enlarged internal mammary lymph node.
residual carcinoma cells trapped in the previously operated site in the absence of systemic recurrence. The most common sites of local recurrence are within the scar of the prior surgery, cutaneous nodules, subcutaneous nodules, and infiltrating breast carcinoma along the deep fascia of the pectoralis major or intercostal muscles. In addition, lytic involvement of the sternum or ribs secondary to direct invasion by chest wall tumor or extracapsular internal mammary lymph nodal tumor extension was also noted in our patients. We have also observed a rare recurrence in the form of inflammatory breast carcinoma with microscopic intraderrnal lymphatic tumor after a curative resection for noninflammatory invasive ductal breast carcinoma.
Local recurrence from residual mammary tissue after mastectomy is a rare phenomenon. The majority of the nodules are either cutaneous or subcutaneous and are not thought to represent true parenchymal recurrence. Cutaneous recurrences are most likely intradermal lymphatics or microscopic subdermal implants with invasion of the epidermis. However, we have observed one patient who became pregnant and presented with an enlarging mass at the periphery of a prosthetic mammary implant after prior mastectomy for infiltrating breast cancer. The subsequent biopsy revealed ductal carcinoma. Recurrence in the area of a scar is most likely due to microscopic dissemination of malignant cells that are trapped within the stroma of scar tissue. The most common subcutaneous nodules are the result of lymphatic permeation of the subcutaneous tissue.
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Fig. 6. A: Completion of myocutaneous reconstruction following chest wall resection for recurrent breast cancer. Note large area of defect with adequate coverage. B: Chest wall reconstruction result I year after en bloc resection of extensive tumor (See A). Note excellent stabilization of chest wall with satisfactory cosmesis
The results of surgery and long-term survival for patients with this local recurrence are poor [ 131. Although there are substantial differences in outcome among the various subgroups of patients with locally advanced breast cancer [4], most of these patients have a very poor prognosis after being treated with local therapy alone. Because of these uniformly poor results after surgery or radiotherapy alone, combined local therapies are utilized when breast cancer is locally advanced [14]. Even the best combination of local therapies, however, fails to prevent the appearance of distant metastasis and local control. The survival of patients with stage I11 breast cancer is approximately 2&30% at 5 years and 10-20% after 10 years. Although it does not seem that a local chest wall recurrence after mastectomy affects the overall survival in patients initially presenting with locally advanced disease or early stage disease, the local manifestations can be devastating for the patient [ 151.
Local recurrence following primary treatment of breast cancer ranges from less than 5 % for stage I to greater than 25% for stages I1 and 111. Since chest wall recurrence is associated with disseminated metastasis in 60-1 00% of cases [16], simple excision, radiation therapy, and chemotherapy are utilized to treat the local and systemic disease. McCormick et al. reviewed a series of 36 patients with chest wall recurrence and noted a subset of 18 (50%) patients with chest wall recurrence alone [6]. These authors reported on treatment with surgical resection and reconstruction of the chest wall. Local control was excellent and median survival for these patients was 50 months. This remains as one of the most outstanding results in the literature of local surgery alone for recurrent chest wall cancer. Another recent study examined 106 patients who developed chest wall recurrence after radical mastectomy,
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modified radical mastectomy, or simple mastectomy for carcinoma of the breast. Patients were treated with either limited surgical excision alone, radiation therapy alone, or limited surgical excision followed by radiation therapy [2]. In this study (follow-up period 6 months to 12 years), 42% of patients remain free of disseminated disease with local chest wall recurrence the only sign of recurrence. When these authors compared recurrence locally after surgery, radiation, or combination treatment for recurrence, the results were uniformly poor. Surgical excision alone was associated with a 62% recurrence, radiation therapy was associated with an 83% recurrence, and a combination of the two was associated with 30% chest wall recurrence. It therefore seems likely that some of these patients might benefit from a combination approach that includes our recommendation for en bloc radical chest wall recurrence followed by radiation and chemotherapy. The numbers of patients with this type of recurrence may be too small to preclude a prospective randomized study to evaluate this hypothesis in a context other than that of a multiinstitutional study. An intraarterial chemotherapy regimen for chest wall recurrent disease has been utilized with subsequent surgery, radiation, and consolidation systemic chemotherapy for locally advanced breast cancer [ 17,181. Sixteen patients with noninflammatory carcinoma were treated by radiotherapy and mastectomy after intraarterial Adriamycin, 5-fluorouracil , vincristine, and methotrexate induction chemotherapy. Fifteen of 16 patients achieved local control after 5 years. It is clear that even with the advances in the treatment of locally recurrent and advanced breast cancer 5670% of patients will succumb to their disease [19,20]. Therefore improvements in disease control necessarily include multimodality therapy, and innovative surgery and radiation therapy. Our data and that of others would suggest that aggressive surgery for recurrent disease remains an integral part of the control of major complications associated with chest wall recurrence and also may provide patients with a durable disease-free remission. A chest wall recurrence after mastectomy for carcinoma of the breast remains a major problem. It is clear that new programs for the treatment of both local and systemic recurrence that include aggressive surgery for local control may offer the patient the best chance for success.
Cancer Society Grant 88- 1 2 5 4 a r e e r Development Award to S.T.B.
ACKNOWLEDGMENTS The authors wish to acknowledge the expert assistance of Ms. Joanne Madio for her preparation of this manuscript. This work was supported in part by an American
19.
REFERENCES 1. Leffall L: Surgical management of metastatic and locally ad-
2. 3.
4.
5.
6. 7. 8.
9. 10.
11. 12.
13.
14.
15. 16. 17. 18.
20.
vanced breast cancer. In Feig S , McLelland R (eds): “Breast Carcinoma: Current Diagnosis and Treatment.” New York: Masson Publishing, pp 505-51 1, 1983. Probstfeld M, O’Connell T: Treatment of locally recurrent breast carcinoma. Arch Surg 124:1127-1130, 1989. Hellman S , Harris J, Canellos G , Fisher B: Cancer of the breast. In DeVita V, Hellman S, Rosenberg S (eds): “Cancer-Principals and Practice of Oncology.” Philadelphia: J.B. Lippincott Company, pp 914-962, 1990. Hortobagyi G: Comprehensive management of locally advanced breast cancer. CA 66:1387-1391, 1990. Ghossein N, Vilcoq J, Stacey P, Calle R: Conservation surgery and radiotherapy in the treatment of localized breast cancer. A retrospective analysis. Front Radiat Ther Oncol 17:102-109, 1983. McCormick P, Bains M, Burt ME, Chaglassian T, Hidalgo D: Local recurrent mammary carcinoma failing multimodality therapy. Arch Surg 124:158-161, 1989. Depoorter M: Reconstructive procedures after breast cancer surgery. Acta Chir Belg 79:124-159, 1980. Holt R, Chetham P: Myocutaneous flaps in the management of locally advanced or recurrent breast cancer. Proc Annu Meet Am SOCClin Oncol 1985;277. Shukla H, Gupta B, Sahni K, Samuels S. Role of rectus abdominis myocutaneous flap in surgery for breast cancer. J Surg Oncol 13:321-329, 1987. Nakao K , Miyata M, Ito T, Ogino N, Kawashima Y, Maeda M, Matsumoto K: Omental transportation and skin graft in patients for advanced or recurrent breast cancer. Jpn J Surg 16:112-117, 1986. Wagman L: Does TRAM flap reconstruction obscure recognition of breast cancer recurrence? Proc SOCSurg Oncol, May, 1990, abstract 39. Mueller C: Perspectives on primary treatment, local recurrence, and ultimate outcomes: Statistics on breast carcinoma. In Gant T, Vasconez L (eds): “Postmastectomy Reconstruction.” Baltimore: Williams & Wilkins, pp 5-17, 1988. Stotter A, McNeese M, Ames F, Oswald M, Ellerbroek N: Predicting the rate and extent of locoregional failure after breast conservation therapy for early breast cancer. CA 64:22 17-2225, 1989. Toonkel L, Fix I, Jacobson L, Bamberg N. Wallach C: Locally advanced breast carcinoma: Results with combined regional therapy. J Radiat Oncol Biol Phys 12:1583-1587, 1986. Wilson R: Surgical management of locally advanced and recurrent breast cancer. CA 53:752-757, 1984. Valagussa P, Bonadonna G, Veronesi U: Patterns of relapse and survival following radical mastectomy: Analysis of 71 consecutive patients. CA41:117&1178, 1978. Stephens F, Harker G, Crea P, Roberts B, Hambly C: Intraarterial chemotherapy as treatment in advanced and fungating primary breast cancer. Lancet 2:435438, 1980. Stephens F: Intraarterial induction chemotherapy in locally advanced stage 111 breast cancer. CA 66:645-650, 1990. Donegan WL: Local and regional recurrence. In Donegan WL, Spratt JS (eds): “Cancer of the Breast.” Philadelphia: W.B. Saunders Co., pp 648-662, 1988. McKenna RJ Jr, McMurtry MJ, Larson DL: A perspective on chest wall resection in patients with breast cancer. Am Thorac Surg 38:482, 1984.
Chest Wall Resection for locally Recurrent Breast Cancer: Indications, Technique, and Results STEVEN T. BROWER,
HUBERT WEINBERG, MD, PAUL I. TARTTER, MD, AND JORGE CAMUNAS, MD From the Departments of Surgery (S.T.B., P.I.T., H.W.) and Cardiothoracic Surgery (J.C.), Mount Sinai Medical Center, New York, New York MD,
A series of 100 patients with locally advanced carcinoma of the breast was analyzed for chest wall recurrence alone after primary treatment. Five patients were found to have had chest wall recurrence alone and were treated with en bloc chest wall resection. This group of patients was analyzed for the pathophysiology of recurrence including characteristics of the primary tumor, location of the chest wall recurrence, and overall local salvage and survival after chest wall recurrence. In this series, local recurrence after radical chest wall resection was 20%. The incidence of systemic recurrence after chest wall resection was 60%. The mean survival for the entire group was 17 months after chest wall recurrence and radical resection. The main surgical objectives, including relief from painful, inflammatory, and bleeding complications, were achieved in all patients after chest wall resection. Although patients with isolated chest wall recurrence included a highly selected group, chest wall resection with myocutaneous reconstruction may provide long-term disease-free survival for these patients. 0 1992 Wiley-Liss, Inc. KEYWORDS:salvage, treatment of breast carcinoma, advanced breast carcinoma
INTRODUCTION The spectrum of recurrence for carcinoma of the breast is variable and distant sites predominate with chest wall recurrence accounting for only 5-30% of patients [ 1,2]. Although late recurrence to the chest wall after mastectomy associated with systemic recurrence has been noted, the usual pattern of recurrence to the chest wall occurs within 2 years and is usually a harbinger of distant metastasis [3,4]. In this circumstance, optimal and rational treatment for the chest wall recurrence includes a multidisciplinary approach in which concern for the systemic disease is prioritized. This includes a combination of surgical biopsy of the chest wall recurrence and in most circumstances local chest wall irradiation and systemic chemotherapy [ 5 ] . The local control rate has varied from 15 to 50% and the overall median survival with simultaneous local and systemic recurrence is 9-12 months [2,3]. Chest wall recurrence after mastectomy occurs without demonstrable clinical evidence of systemic breast cancer 0 1992 Wiley-Liss, Inc.
in 2 5 4 5 % of patients [5]. Although the number of patients with this form of local chest wall breast recurrence is quite small, some authors have documented reasonable disease-free survival after surgery for chest wall recurrence and some series have documented long-term survivors [5,6]. Palliation of isolated chest wall recurrence is also important in this setting. Local chest wall recurrence may rapidly progress with destruction of the overlying skin and underlying ribs and sternum, requiring salvage treatment for advanced and life-threatening infection or bleeding. In an effort to prevent these debilitating, painful, and life-threatening circumstances, we have taken an aggressive approach to the treatment of chest wall recurrence after mastectomy for breast carcinoma in the absence of Accepted for publication December 9, 1991. Address reprint requests to Dr. Steven T. Brower, Division of Surgical Oncology, Department of Surgery, Box 1259, Mount Sinai Medical Center, 1 Gustave L. Levy Place, New York, NY 10029.
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systemic recurrence. We report on our indications, techniques, and results in a group of five breast cancer patients treated with aggressive surgery as part of the approach to isolated chest wall recurrence.
MATERIALS AND METHODS Since I986 patients on the Breast Service at The Mount Sinai Medical Center with locally advanced disease (stages IIB, IIIA, IIIB) have been placed in a prospective tumor registry. This registry includes 100 patients of whom 5 were found to have chest wall recurrence alone. The pathology material and tumor registry data collected on each patient were reviewed. For the purpose of this study, a local chest wall recurrence was defined as a pathological positive mammary carcinoma biopsy that occurred in the skin, subcutaneous tissue, musculoskeletal, or lymph nodal area within the ipsilateral operated site. Analysis included only patients who had undergone simple mastectomy or modified radial or radical mastectomy for their initial treatment of carcinoma of the breast. The age range of the patients was 47 to 65 years. The follow-up period after resection ranged from 9 months to 3 years with a median follow up of 17 months. All patients prior to being considered for salvage by en bloc recurrence were vigorously scrutinized for metastatic disease. This included routine blood chemistries as well as determination of lipid associated sialic acid, carcinoembryonic antigen (CEA), and CA 15-3 serum markers, as well as chest x-ray and bone scan. In addition, all patients had an abdominal and chest CT scan and some patients were subjected to bone marrow aspirates or biopsies. Technique of Chest Wall Resection The strategy for chest wall resection is planned by a multidisciplinary group of surgical oncologists, thoracic surgeons, and plastic and reconstructive surgeons. Bulky disease was found attached to either the underlying bony chest wall or pleura (Fig. 1). Although the recurrence may be localized to any area of the chest wall or scar, we assumed a wide area of microscopic infiltration especially along the skin, subcutaneous tissue, and chest wall musculature (Fig. 2). Accordingly, a wide paddle of skin and subcutaneous tissue was included in the chest wall resection with no attempt to preserve soft tissue for closure. Similarly, the extent of parietal pleura, intercostal muscle, or bony rib involvement was ascertained by the thoracic surgeon, and a margin of normal muscle and ribs was sacrificed well around the lesion within the thoracic cavity. Since no attempt was made to conserve chest wall tissue, we have relied upon myocutaneous flap reconstruction [7-lo]. The location of the chest wall tumor recurrence was carefully noted and a circular or elliptical incision on the chest wall was made with a large radius of normal skin around the lesion. Frequent frozen-section biopsies were
taken of skin and muscle to ensure negative microscopic margins. The dissection was continued through the pectoralis major muscle and essentially encompassed the entire scar. Laterally, the serratus was released from the ribs. With fixation to the underlying ribs or sternum, the deep tumor-free margin was assumed to be the intrathoracic cavity. The chest wall musculature above and below the rib or interspace of the prior scar were divided in the anterior axillary line. The surgeon then palpated the parietal pleura to make sure there were no nodules at this lateral margin of the chest wall. If this was free of tumor, resection of the soft tissue and rib(s) proceeded from lateral to medial. Beneath the area of the chest wall recurrence, we occasionally saw a cicatrix of parietal pleura, with some puckering of the pleura, intercostal muscle, and periosteal reaction. Care was taken not to disrupt this architecture, which surrounded the tumor and contained microscopic disease. The dissection continued medially to the costostemal margin, where once again the ribs were divided and the en bloc specimen was removed leaving the uninvolved visceral pleura and pericardium intact (Fig. 3 ) .
RESULTS We have recently performed resection and reconstruction in five patients following extensive local recurrence after carcinoma of the breast (Table I). Patient 1 had been treated 2 years previously with a modified radical mastectomy for an ulcerated 6 cm primary tumor with positive lymph nodes. The patient had recurrence noted as a subcutaneous nodule. CAT scan evaluation revealed an enlarged internal mammary lymph node that had eroded the overlying costostemal border (Fig. 4). This mass had grown in size while the patient continued on chemotherapy and it was felt that salvage therapy was indicated. The salvage resection included a full-thickness chest wall resection of ribs 2, 3, and 4 as well as the left hemisection of the manubrium and upper third of the sternum. This was followed by reconstruction using a Marlex mesh-methylmethacrylate lattice covered with a transverse rectus abdominus myocutaneous (TRAM) flap. After our salvage en bloc resection of chest wall, sternum, and pericardium, she was symptom free for 6 months. However, at that time, recurrence was noted with bilateral pleural effusions. The patient ultimately succumbed 12 months after our palliative surgery with no evidence of local recurrence. Patient 2 presented with an infiltrative recurrence along the pectoralis fascia fixed to the overlying skin after modified radical mastectomy completed 18 months prior to the current surgery. The prior infiltrating breast cancer was a large, 8 cm cancer (stage IIIA). Although the recurrence at this time was over a wide field area (approximately 6 X 6 cm) it was felt that en bloc resection with a wide paddle of skin could achieve negative margins. Accordingly, full-thickness chest wall resection was com-
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Fig. 1. A: Bulky recurrent chest wall tumor at medial edge of prior mastectomy incision fixed to underlying pectoralis muscle, ribs, and sternum. B: CT scan of patient in A with obvious large anterior chest wall recurrence but associated bulky retrosternal, costosternal, and pleural disease with attachment to underlying pericardium.
pleted with TRAM myocutaneous flap (Fig. 5). The final pathology revealed recurrent breast cancer with all lateral and deep margins clear of microscopic tumor. At 9 months of study, the patient continues without any evidence of local or systemic recurrence. Patient 3 was a 60 year old female who presented initially with stage IIIA carcinoma of the breast. This was treated with modified radical mastectomy. At approximately 9 months, recurrence was noted at the midportion of the scar closure. No evidence of systemic disease was noted at this point. Full-thickness chest wall resection of skin, muscle, ribs, and pleura was completed with TRAM flap (Fig. 6A). The patient remained without any evidence of disease for 20 months. At that time, OSSeOUS metastases were noted with no evidence of local recurrence. The patient is currently symptom free after radia-
Fig. 2. Extensive full thickness chest wall recurrence with involvement of skin, subcutaneous tissue, and underlying pectoralis, intercostal and serratus muscles. Note en bloc resection of all tissue involved with free margin at transected ribs
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vival for the entire group is 17 months, with one patient living 3 years. The incidence of systemic recurrence after chest wall resection was 60%. Local recurrence after chest wall resection was 20%. No patient with a local recurrence after our salvage resection had a delay in the diagnosis of recurrence due to the overlying myocutaneous flap. It was clear that skin had been infiltrated by microscopic disease and nodularity. This is similar to the findings of Wagman et al. demonstrating that the TRAM flap does not delay diagnosis for recurrent breast carcinoma [ 111.
DISCUSSION We have described our favorable experience with en Fig. 3. Chest wall defect following extensive resection of recurrent bloc chest wall resection following recurrence of carcibreast cancer. Visceral pleura, lung parenchyma, sternum, ribs, and noma of the breast after mastectomy. We have attempted soft tissue are free of microscopic tumor. to understand the patterns of dermal, lymphatic, and musculoskeletal recurrence in an effort to achieve a strategy for maximal wide excision. This has required that we tion therapy and chemotherapy with complete healing of view the chest wall recurrence as a full-thickness recurrence. Our main objectives for this approach were to the chest wall resection and reconstruction (Fig. 6B). Patient 4 presented with stage IIIB carcinoma of the render the patient free of painful, inflammatory, infecbreast with satellite nodules throughout the breast and tious, and bleeding complications associated with chest fixation to the pectoralis major muscle and ipsilateral wall recurrence. In this setting, our palliative treatment lymph nodes. Twenty-four months earlier, the patient was uniformly successful. Although survival in this small had undergone radical mastectomy with local radiation group of patients was not altered, a number of the patients therapy and systemic chemotherapy. At the time of recur- lived for an extended period of time. We have carefully selected patients whom we feel are rent presentation the patient had infiltration of the scar, skin, and periosteum. There was no evidence of systemic candidates for this extensive surgery. In this way we have recurrence. She underwent en bloc resection of chest wall ensured the excellent local results. Patients who would including ribs 3 through 5. Because of the prior radical not be eligible for this surgery include patients with metmastectomy, Gortex mesh and combined latissimus dorsi astatic disease. In addition, patients with a local recurand TRAM flap reconstruction was chosen. This patient rence with multiple pleural nodules or skip lesions at a remained symptom free for 6 months. However, at that distance from the recurrence on the parietal pleura are time recurrence within the reconstructed site was noted. excluded from surgery. Neither fixation to the chest wall Extensive edema of latissimus dorsi flap and infiltration nor extensive skin involvement precludes successful en of the flap margins with tumor nodules was noted. This bloc resection. With newer techniques of myocutaneous recurrence might have been predicted by two prior local transfer, areas as great as 20 cm2 have been encompassed attempts with radiation and chemotherapy after chest re- including a portion of the sternum and contralateral breast currence prior to transfer to our medical center for ulti- skin and tissue. Recurrence within the internal mammary mate control of disease. There was no intrapleural recur- nodal group and adherence to the sternum or chest wall is rence noted beneath the prosthesis, Malignant pleural not a contraindication to chest wall resection. However, effusions and regional lymphadenopathy were noted 11 our results indicate that these patients are at extremely months after surgery. high risk for systemic disease, and a vigorous attempt to Patient 5 presented with a subcutaneous nodule supe- eradicate systemic metastases with chemotherapy should rior to the scar of a prior modified radical mastectomy. be developed. This nodule was fixed to the underlying pectoralis major Chest wall recurrence from carcinoma of the breast is a muscle and on the bone scan was thought to involve the result of a variety of biological and anatomic considerfifth rib at the midclaviclar line. Accordingly, a full- ations. The most common situation is that of the growth thickness resection was performed with TRAM flap re- of resistant metastases, both locally at the site of prior construction. This patient remains free of local and sys- definitive surgery and at the same time the growth of temic disease after chemotherapy for her chest wall microscopic metastases at multiple distant sites. In this recurrence at 3 years after surgery. situation the chest wall recurrence is usually a predictor Overall survival was unaffected by chest wall resection of systemic disease that manifests in 1-4 months [12]. for recurrent carcinoma of the breast. The median sur- Alternatively, the local recurrence may be the result of
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TABLE 1. Chest Wall Resection for Recurrent Breast Cancer Lymph node status
Time on studv (months)
Age
Stage
1
12
50
IIIB
+
2 3
9 22
65 60
IIIA IIIB
-
4
11
47
IIIB
+
5
38
52
IIIB
+
Patient
Characteristics of the primary tumor
Initial surgery a
Ulceration, fixation
MRM
Large (8 cm) Large, ulceration
MRM MRM
Satellite nodule pectoralis major involvement Large, ulceration
Radical mastectomy MRM
Location of chest wall recurrence
Recurrence after chest wall resection Local
Systemic
Costosternal junction, internal mammary nodal group Pectoralis fascia Subcutaneous nodule, scar, pectoralis major muscle Scar, skin, rib, periosteum
-
+
Subcutaneous nodule, Dectoralis fascia
-
-
+
+
-
-
+
~~
aMRM, modified radical mastectomy.
Fig. 5 . Reconstruction of the chest wall defect following en bloc resection. Prosthetic mesh has been fixed to cut ends of ribs. Note abdominal TRAM myocutaneous flap being fashioned for transfer to chest wall location. Fig. 4. Retrosternal extension of costosternal breast cancer recurrence. Note probable enlarged internal mammary lymph node.
residual carcinoma cells trapped in the previously operated site in the absence of systemic recurrence. The most common sites of local recurrence are within the scar of the prior surgery, cutaneous nodules, subcutaneous nodules, and infiltrating breast carcinoma along the deep fascia of the pectoralis major or intercostal muscles. In addition, lytic involvement of the sternum or ribs secondary to direct invasion by chest wall tumor or extracapsular internal mammary lymph nodal tumor extension was also noted in our patients. We have also observed a rare recurrence in the form of inflammatory breast carcinoma with microscopic intraderrnal lymphatic tumor after a curative resection for noninflammatory invasive ductal breast carcinoma.
Local recurrence from residual mammary tissue after mastectomy is a rare phenomenon. The majority of the nodules are either cutaneous or subcutaneous and are not thought to represent true parenchymal recurrence. Cutaneous recurrences are most likely intradermal lymphatics or microscopic subdermal implants with invasion of the epidermis. However, we have observed one patient who became pregnant and presented with an enlarging mass at the periphery of a prosthetic mammary implant after prior mastectomy for infiltrating breast cancer. The subsequent biopsy revealed ductal carcinoma. Recurrence in the area of a scar is most likely due to microscopic dissemination of malignant cells that are trapped within the stroma of scar tissue. The most common subcutaneous nodules are the result of lymphatic permeation of the subcutaneous tissue.
194
Brower et al.
Fig. 6. A: Completion of myocutaneous reconstruction following chest wall resection for recurrent breast cancer. Note large area of defect with adequate coverage. B: Chest wall reconstruction result I year after en bloc resection of extensive tumor (See A). Note excellent stabilization of chest wall with satisfactory cosmesis
The results of surgery and long-term survival for patients with this local recurrence are poor [ 131. Although there are substantial differences in outcome among the various subgroups of patients with locally advanced breast cancer [4], most of these patients have a very poor prognosis after being treated with local therapy alone. Because of these uniformly poor results after surgery or radiotherapy alone, combined local therapies are utilized when breast cancer is locally advanced [14]. Even the best combination of local therapies, however, fails to prevent the appearance of distant metastasis and local control. The survival of patients with stage I11 breast cancer is approximately 2&30% at 5 years and 10-20% after 10 years. Although it does not seem that a local chest wall recurrence after mastectomy affects the overall survival in patients initially presenting with locally advanced disease or early stage disease, the local manifestations can be devastating for the patient [ 151.
Local recurrence following primary treatment of breast cancer ranges from less than 5 % for stage I to greater than 25% for stages I1 and 111. Since chest wall recurrence is associated with disseminated metastasis in 60-1 00% of cases [16], simple excision, radiation therapy, and chemotherapy are utilized to treat the local and systemic disease. McCormick et al. reviewed a series of 36 patients with chest wall recurrence and noted a subset of 18 (50%) patients with chest wall recurrence alone [6]. These authors reported on treatment with surgical resection and reconstruction of the chest wall. Local control was excellent and median survival for these patients was 50 months. This remains as one of the most outstanding results in the literature of local surgery alone for recurrent chest wall cancer. Another recent study examined 106 patients who developed chest wall recurrence after radical mastectomy,
Breast Cancer RecurrenceLhest Wall Resection
195
modified radical mastectomy, or simple mastectomy for carcinoma of the breast. Patients were treated with either limited surgical excision alone, radiation therapy alone, or limited surgical excision followed by radiation therapy [2]. In this study (follow-up period 6 months to 12 years), 42% of patients remain free of disseminated disease with local chest wall recurrence the only sign of recurrence. When these authors compared recurrence locally after surgery, radiation, or combination treatment for recurrence, the results were uniformly poor. Surgical excision alone was associated with a 62% recurrence, radiation therapy was associated with an 83% recurrence, and a combination of the two was associated with 30% chest wall recurrence. It therefore seems likely that some of these patients might benefit from a combination approach that includes our recommendation for en bloc radical chest wall recurrence followed by radiation and chemotherapy. The numbers of patients with this type of recurrence may be too small to preclude a prospective randomized study to evaluate this hypothesis in a context other than that of a multiinstitutional study. An intraarterial chemotherapy regimen for chest wall recurrent disease has been utilized with subsequent surgery, radiation, and consolidation systemic chemotherapy for locally advanced breast cancer [ 17,181. Sixteen patients with noninflammatory carcinoma were treated by radiotherapy and mastectomy after intraarterial Adriamycin, 5-fluorouracil , vincristine, and methotrexate induction chemotherapy. Fifteen of 16 patients achieved local control after 5 years. It is clear that even with the advances in the treatment of locally recurrent and advanced breast cancer 5670% of patients will succumb to their disease [19,20]. Therefore improvements in disease control necessarily include multimodality therapy, and innovative surgery and radiation therapy. Our data and that of others would suggest that aggressive surgery for recurrent disease remains an integral part of the control of major complications associated with chest wall recurrence and also may provide patients with a durable disease-free remission. A chest wall recurrence after mastectomy for carcinoma of the breast remains a major problem. It is clear that new programs for the treatment of both local and systemic recurrence that include aggressive surgery for local control may offer the patient the best chance for success.
Cancer Society Grant 88- 1 2 5 4 a r e e r Development Award to S.T.B.
ACKNOWLEDGMENTS The authors wish to acknowledge the expert assistance of Ms. Joanne Madio for her preparation of this manuscript. This work was supported in part by an American
19.
REFERENCES 1. Leffall L: Surgical management of metastatic and locally ad-
2. 3.
4.
5.
6. 7. 8.
9. 10.
11. 12.
13.
14.
15. 16. 17. 18.
20.
vanced breast cancer. In Feig S , McLelland R (eds): “Breast Carcinoma: Current Diagnosis and Treatment.” New York: Masson Publishing, pp 505-51 1, 1983. Probstfeld M, O’Connell T: Treatment of locally recurrent breast carcinoma. Arch Surg 124:1127-1130, 1989. Hellman S , Harris J, Canellos G , Fisher B: Cancer of the breast. In DeVita V, Hellman S, Rosenberg S (eds): “Cancer-Principals and Practice of Oncology.” Philadelphia: J.B. Lippincott Company, pp 914-962, 1990. Hortobagyi G: Comprehensive management of locally advanced breast cancer. CA 66:1387-1391, 1990. Ghossein N, Vilcoq J, Stacey P, Calle R: Conservation surgery and radiotherapy in the treatment of localized breast cancer. A retrospective analysis. Front Radiat Ther Oncol 17:102-109, 1983. McCormick P, Bains M, Burt ME, Chaglassian T, Hidalgo D: Local recurrent mammary carcinoma failing multimodality therapy. Arch Surg 124:158-161, 1989. Depoorter M: Reconstructive procedures after breast cancer surgery. Acta Chir Belg 79:124-159, 1980. Holt R, Chetham P: Myocutaneous flaps in the management of locally advanced or recurrent breast cancer. Proc Annu Meet Am SOCClin Oncol 1985;277. Shukla H, Gupta B, Sahni K, Samuels S. Role of rectus abdominis myocutaneous flap in surgery for breast cancer. J Surg Oncol 13:321-329, 1987. Nakao K , Miyata M, Ito T, Ogino N, Kawashima Y, Maeda M, Matsumoto K: Omental transportation and skin graft in patients for advanced or recurrent breast cancer. Jpn J Surg 16:112-117, 1986. Wagman L: Does TRAM flap reconstruction obscure recognition of breast cancer recurrence? Proc SOCSurg Oncol, May, 1990, abstract 39. Mueller C: Perspectives on primary treatment, local recurrence, and ultimate outcomes: Statistics on breast carcinoma. In Gant T, Vasconez L (eds): “Postmastectomy Reconstruction.” Baltimore: Williams & Wilkins, pp 5-17, 1988. Stotter A, McNeese M, Ames F, Oswald M, Ellerbroek N: Predicting the rate and extent of locoregional failure after breast conservation therapy for early breast cancer. CA 64:22 17-2225, 1989. Toonkel L, Fix I, Jacobson L, Bamberg N. Wallach C: Locally advanced breast carcinoma: Results with combined regional therapy. J Radiat Oncol Biol Phys 12:1583-1587, 1986. Wilson R: Surgical management of locally advanced and recurrent breast cancer. CA 53:752-757, 1984. Valagussa P, Bonadonna G, Veronesi U: Patterns of relapse and survival following radical mastectomy: Analysis of 71 consecutive patients. CA41:117&1178, 1978. Stephens F, Harker G, Crea P, Roberts B, Hambly C: Intraarterial chemotherapy as treatment in advanced and fungating primary breast cancer. Lancet 2:435438, 1980. Stephens F: Intraarterial induction chemotherapy in locally advanced stage 111 breast cancer. CA 66:645-650, 1990. Donegan WL: Local and regional recurrence. In Donegan WL, Spratt JS (eds): “Cancer of the Breast.” Philadelphia: W.B. Saunders Co., pp 648-662, 1988. McKenna RJ Jr, McMurtry MJ, Larson DL: A perspective on chest wall resection in patients with breast cancer. Am Thorac Surg 38:482, 1984.
