t h e s u r g e o n x x x ( 2 0 1 4 ) 1 e7
Available online at www.sciencedirect.com
ScienceDirect The Surgeon, Journal of the Royal Colleges of Surgeons of Edinburgh and Ireland www.thesurgeon.net
Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment Francesco Petrella a,*, Davide Radice b, Alessandro Borri a, Domenico Galetta a, Roberto Gasparri a, Monica Casiraghi a, Adele Tessitore a, Alessandro Pardolesi a, Piergiorgio Solli a, Giulia Veronesi a, Stefania Rizzo c, Stefano Martella d, Mario Rietjens d, Lorenzo Spaggiari a,e a
Department of Thoracic Surgery, European Institute of Oncology, Italy Department of Epidemiology and Biostatistics, European Institute of Oncology, Italy c Department of Radiology, European Institute of Oncology, Italy d Department of Plastic and Reconstructive Surgery, European Institute of Oncology, Italy e University of Milan School of Medicine, Italy b
article info
abstract
Article history:
Introduction: Breast cancer is the leading cause of cancer death among women in the
Received 14 October 2013
industrialized countries. The incidence of local recurrences after mastectomy and breast-
Received in revised form
conserving therapy varies between 5% and 40% depending on risk factors and primary
22 February 2014
therapy.
Accepted 3 March 2014
Methods: From April 1999 to April 2011, 40 patients underwent chest wall resection and
Available online xxx
reconstruction for locally recurrent breast carcinoma with chest wall invasion. The main goal of surgery was local disease control to palliate clinical symptoms.
Keywords:
Results: Local radical resection was achieved in 26 patients (65%). One, 2 and 5 year overall
Breast cancer
survival rates were 94.4%, 82.0% and 68.5%; 1, 2 and 5 year disease-free survival rates were
Chest wall resection
94.4%, 73.6% and 45.5% respectively.
Chest wall reconstruction
Univariate analysis indicated age (p ¼ 0.002) and synchronous distant metastases (p ¼ 0.020) as factors having a negative impact on overall survival; multivariate analysis disclosed age (p ¼ 0.052) and synchronous metastases (p ¼ 0.059) as factors with a slight negative impact on overall survival. Older age was associated with improved overall survival. Univariate analysis indicated synchronous distant metastases (p ¼ 0.029) and the need of post resectional additional treatments (p ¼ 0.022) as factors adversely conditioning disease-free survival or time to progression; multivariate analysis disclosed the need of post resectional additional treatments (p ¼ 0.036) as the only factor adversely conditioning disease-free survival or time to progression.
* Corresponding author. Department of Thoracic Surgery, European Institute of Oncology, Via Ripamonti, 435, 20141 Milan, Italy. Tel.: þ39 0257489362; fax: þ39 0294379218. E-mail addresses: [email protected], [email protected] (F. Petrella). http://dx.doi.org/10.1016/j.surge.2014.03.001 1479-666X/ª 2014 Royal College of Surgeons of Edinburgh (Scottish charity number SC005317) and Royal College of Surgeons in Ireland. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
2
t h e s u r g e o n x x x ( 2 0 1 4 ) 1 e7
Conclusions: Chest wall resection and reconstruction for locally recurrent breast cancer is a feasible and safe procedure providing adequate local disease control and an excellent palliation of very disabling symptoms in a selected group of patients. ª 2014 Royal College of Surgeons of Edinburgh (Scottish charity number SC005317) and Royal College of Surgeons in Ireland. Published by Elsevier Ltd. All rights reserved.
Introduction Breast cancer is the leading cause of cancer death among women in the industrialized countries.1 The incidence of local recurrences after mastectomy and breast-conserving therapy varies between 5% and 40% depending on risk factors and primary therapy.2 The first-line treatments in recurrent breast cancer are endocrine therapy for patients with estrogen or progesterone receptor positive cancer, and chemotherapy for patients with receptor-negative cancers.3e5 However, local therapies such as radiotherapy or surgery may be required in selected cases for local disease control and palliation of disabling symptoms like pain, bleeding, ulceration, malodorous secretion, infection and fungating lesions.6,7 On the one hand, locoregional recurrence of breast cancer following breast surgery may be a systemic disease and in many patients it tends to occur at the same time as distant metastases, making the indication for surgical resection questionable.8,9 On the other, although the primary goal of chest wall resection is to achieve local tumor control, it may lead to long-term palliation and even cure for a small subset of patients with isolated chest wall recurrence of breast cancer after multimodal treatment failure.10 Early detection of locoregional recurrence and small tumor size predicted a better prognosis.11e13 Options for local treatment of locoregional recurrence include wide local excision and/or radiotherapy whether or not in combination with hyperthermia14; however, for small lesions, the type of local treatment did not affect the final outcome.15 Whether complete resection of local recurrence offers a merely palliative or possibly curative approach or a major prolongation of survival remains unsettled.16 The aim of this study was to define the role of chest wall resection for locally recurrent breast cancer as a salvage treatment for a selected group of symptomatic patients.
Methods The present study was conducted in accordance with the Declaration of Helsinki.17 Written informed consent was obtained from all subjects before any procedure was done. The investigators explained all the planned procedures verbally to all subjects who received and signed a subject information sheet to acquaint themselves with details of the planned therapeutic schedule. All patients authorized the investigators to use their data anonymously only for scientific purposes according to Italian legislation (law no. 675/1996).
Data were collected prospectively and entered into our institutional general thoracic database at the point of care. The database was reviewed retrospectively. From April 1999 to April 2011, 40 patients underwent chest wall resection and reconstruction for locally recurrent breast carcinoma with chest wall invasion proven by routine preoperative chest computed tomography (CT) or by chest wall magnetic resonance imaging (MRI) in selected cases. The main goal of surgical therapy was local disease control to palliate clinical symptoms like pain, cutaneous ulceration and discomfort related to chest wall deformity. For this reason a distant metastasis was not a contraindication. Selection criteria for surgery were multimodal treatment failure and life expectancy of more than 6 months. The surgical approach involved soft tissue resection with broad margins and chest wall resection with total or partial sternectomy and resection of one or more ribs. In case of major tissue defect following resective surgery reconstruction was performed using different types of prostheses covered by a vascularized pedicle muscle flap. Technical aspects of demolition and reconstructive procedures were reviewed (sternectomy, ribs resection, soft tissue resection, endothoracic organ resection, type of prosthesis, type of flap and technical complications) together with oncologic history including previous type and date of breast operation, histology and biology of breast and thoracic surgical specimens (Ki67%, Her2 neu expression, estrogen and progesterone receptor expression), and the interval between breast and thoracic surgery. Patients were defined as triple negative if estrogen, progesterone and Her2 neu expression were negative; otherwise, they were defined as non-triple negative.10 Recurrence was defined as the return of cancer after treatment and after a period of time during which the cancer could not be detected. Local recurrence was defined as the reappearance of disease in locoregional lymph nodes or in the chest wall adjacent to the site of thoracic excision. Distant recurrence was defined as distant sites of visceral disease, including malignant pleural effusions or implants. Progression was defined as cancer growth without a period of time during which the cancer could not be detected. Distant progression was defined as cancer spreading to distant sites; locoregional progression was defined as cancer worsening close to the surgical field. A complete resection (R0) was defined as pathologic demonstration of negative tissue margins and an assessment by the operating surgeon that all detectable disease had been removed. Microscopically incomplete resection (R1) was defined as complete macroscopic resection with positive margins found on final pathologic review. Macroscopically
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
3
t h e s u r g e o n x x x ( 2 0 1 4 ) 1 e7
incomplete resection (R2) was defined as gross residual disease after attempted resection.18
Statistical analysis Patient characteristics were summarized and tabulated using either counts and percentage or counts, mean, standard deviation (SD), median, min and max for the categorical or continuous variables, respectively. Overall survival (OS) and disease-free survival (DFS) were defined as the time from surgery to the last follow-up date or death and to the last follow-up date or recurrence date respectively, then estimated and plotted using the KaplaneMeier method. Univariate and multivariate hazard ratios (HR) for the OS and DFS were estimated using the Cox proportional hazards model and tabulated alongside their 95% confidence Intervals. The statistical analyses were conducted using SAS Software 9.2 (NC, USA).
rib resection and among them a median of 2.5 ribs were removed (range 1e5). Three out of 40 patients (7.5%) received extended soft tissue resection involving periostium removal but without complete chest wall resection. Four out of 40 patients (10%) received endothoracic organ resection as follows: left lung in 2 cases, pericardium in 1 case, pericardium plus left innominate vein in 1 case. Local radical resection was achieved in 26/40 patients (65%). Microscopic residual disease was left in 13/40 patients (32.5%). Macroscopic residual disease was left in 1 patient (2.5%). A prosthesis was used in 34/40 patients (85%): 26/34 (76.4%) received monofilament polypropylene mesh plus resinous
Table 1b e Clinico-pathological features of the study population. %
Results With regard to initial non-surgical treatment, at the time of breast cancer diagnosis 11 patients (27.5%) received chemotherapy þ hormone therapy; 7 patients (17.5%) received chemotherapy alone; 6 patients (15%) received hormone therapy þ radiotherapy; 5 patients (12.5%) received chemotherapy þ radiotherapy; 4 patients (10%) received hormone therapy alone; 2 patients (5%) received radiotherapy alone; 1 patient (2.5%) did not receive any treatment; 4 patients (10%) received other combined treatments (e.g., chemotherapy þ hormone therapy þ target therapy or chemotherapy þ hormone therapy þ radiotherapy).
Surgical aspects The study population consisted of 40 patients with a median age of 59 years (range 30e83 years) at chest wall resection. The median interval between breast and chest wall operations was 59 months (range 0e402). Chest wall resection included total or partial sternectomy in 21/40 cases (52.5%). 34/40 patients (85%) received at least 1
Table 1a e Technical aspects of the procedures. Variable
Subgroup
%
Prosthesis
Polypropylene mesh þ resinous material Polyglactin knitted mesh Polypropylene mesh alone Titanium bars Latissimus dorsi Pectorialis major TRAM Fascio e cutaneous Cyclopization Flap ischemia Prosthesis infection Bleeding Operative mortality
76.4
Flap
Surgical complication
8.9 8.9 5.8 40 20 30 3.4 6.6 5 7.5 2.5 0
Median age Sternectomy required Median ribs resected Endothoracic organ resection Mean tumor size Synchronous metastases at CWRRa Synchronous metastases (lymph nodes) Synchronous metastases (distant sites) Treatments before CWRRa (combined) Chemotherapy Radiotherapy Hormone therapy Target therapy None Treatments after CWRRa (combined) Chemotherapy Radiotherapy Hormone therapy Target therapy None Outcome after salvage therapy Disease control Toxicity Previous breast surgery
Previous breast histology
a b
59 (30e83) 21/40 2.5 (1e5) 4/40
10
5.4 cm (1.3e18) 15/40
37.5%
5/15
33.3%
10/15
66.6%
31/40 23/40 23/40 4/40 4/40
77.5 57.5 57.5 10 10
22/40 6/40 25/40 5/40 1/40
55 15 62.5 12.5 2.5
30/40 8/40 Mastectomy Quadrantectomy Ductal resection Bilateral mastectomy Ductal carcinoma Papillary carcinoma Medullary carcinoma Mucinous carcinoma Lobular carcinoma Combined lobular and ductal carcinoma Phyllodes tumor NOSb histology
75 20 62.5 32.5 2.5 2.5 52.5 5 2.5 2.5 2.5 2.5
52.5
2.5 30
CWRR: Chest wall resection and reconstruction. NOS: Not otherwise specified.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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Table 2 e Clinical characteristics of deceased patients. N.
Age at diagnosis
Age at recurrence
Cause of death
Her2neu/Er/Pr/
Adjuvant therapy
DFI (months)
R status at resection
Distant disease at time of treatment
37 57 49 58 53 51 30 52 34
39 59 52 61 55 53 31 54 34
Rec Rec Rec Rec Rec Rec Prog Prog Prog
// // /þ/þ // // // // // //
No C C/H/R H C C C/T C C
NA 21 13 19 10 1 5 16 NA
Not radical Not radical Radical Radical Radical Radical Radical Not radical Radical
No Yes Yes No Yes Yes Yes Yes Yes
1 2 3 4 5 6 7 8 9
Table legend: DFI ¼ disease-free interval; Rec ¼ recurrence; Prog ¼ progression; C ¼ chemotherapy; H ¼ hormone therapy; R ¼ radiotherapy; T ¼ target therapy; NA ¼ not applicable.
material (Bard* Mesh, Bard Davol Inc., Cranston, RI, USA; Cranioplastic, Codman & Shurtleff, Inc. Raynham, MS, USA); 3/34 (8.8%) received adsorbable polyglactin knitted mesh (Vicryl knitted mesh, Ethicon Inc., New Brunswick, NJ, USA); 3/ 34 (8.8%) received monofilament polypropylene mesh alone (Bard * Mesh, Bard Davol Inc., Cranston, RI, USA) and 2/34 patients (5.8%) received titanium bars. Thirty out of 40 (75%) patients received a flap to complete chest wall reconstruction: latissimus dorsi muscle flap was used in 12/30 cases (40%); pectorialis major muscle flap was used in 6/30 cases (20%); transposition of rectus abdominis muscle (TRAM) was used in 9/30 cases (30%); a fasciocutaneous sliding flap was used in 1/30 case (3.3%); cyclopization was used in 2/30 cases (6.6%). Six out of 40 patients (15%) had postoperative surgical complications requiring a re-do operation: The operative mortality rate was 0% (Table 1).
Specimen biological assessment Biological assessment on chest wall specimens disclosed a Ki67 mean value of 49.9%; Her2 neu mean expression of 17.2%, evaluated as percentage of neoplastic cells showing membrane immunoreactivity to the Dako polyclonal antiserum (Dako Denmark A/S, Glsotrup, Denmark); estrogen and progesterone receptors expression of 49.2% and 12.1% respectively. With regard to the hormonal status of chest wall specimens we observed estrogen and progesterone receptors both positive in 12 patients (30%); both negative in 15 patients (37.5%). We observed 7 triple-negative patients (17.5%).
Follow-up After a median follow-up of 30.6 months 15/40 patients (37.5%) were alive and disease-free; 15/40 patients (37.5%) were alive with disease; 9/40 patients (22.5%) had died from disease; 1/40 (2.5%) patient was lost to follow-up. Age at diagnosis, age at recurrence, cause of death, hormonal patterns, adjuvant therapies and disease-free interval of deceased patients are summarized in Table 2.
Multimodality treatments Following chest wall resection 22/40 patients (55%) received chemotherapy, 25/40 patients (62.5%) received hormone therapy, 6/40 patients (15%) received radiotherapy, 5/40 patients (12.5%) received target therapy. Only 1/40 patient (2.5%) did not receive any additional treatment following chest wall resection; in all cases additional treatments were proposed on clinical, histological and biological bases, without any fixed algorithm.
Overall and disease-free survival One, 2 and 5 year overall survival rates were 94.4%, 82.0% and 68.5%; 1, 2 and 5 year disease-free survival rates were 94.4%, 73.6% and 45.5% respectively. After a median follow-up of 30.6 months the median overall survival (OS) was not reached. The median disease-free survival was 49.1 months (Fig. 1a and b). Univariate analysis indicated age (p ¼ 0.002) and synchronous distant metastases (p ¼ 0.020) as factors adversely impacting on overall survival; multivariate analysis disclosed age (p ¼ 0.052) and synchronous metastases (p ¼ 0.059) as factors with a slight negative impact on overall survival. Univariate analysis indicated synchronous distant metastases (p ¼ 0.029) and the need for post-resectional additional treatments (p ¼ 0.022) as factors adversely impacting on disease-free survival or time to progression. Multivariate analysis disclosed the use of post-resectional additional treatments (p ¼ 0.036) as the only factor with an adverse impact on disease-free survival or time to progression.
Discussion Despite major therapeutic advances, recurrent breast cancer is still a lethal disease in most patients.5,19 Isolated local recurrences are thought to represent about 20% of all recurrences, while local disease, in combination with either regional or distant recurrences, represents a further 3%.20 The majority of locoregional recurrences occur as isolated chest wall disease, and only a small proportion present with concurrent systemic disease or following distant metastases.21,22 In our series 15 patients (37.5%) presented with concurrent systemic disease: 10 patients (66.6%) presented with
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
t h e s u r g e o n x x x ( 2 0 1 4 ) 1 e7
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Fig. 1 e a) Overall survival b) disease-free survival.
distant metastases (pleura or distant bone), while 5 patients (33.4%) presented with regional nodal involvement (internal mammary chain or axillary lymph nodes). We never observed true distant soft tissue metastases, probably because of the local invasive biology of the original breast disease. Although palliation rather than prolongation of survival is usually the main aim of chest wall resection, some studies found that a small subset of patients would have a long disease-free interval and possibly cure after chest wall resection and reconstruction.23,24 Our results confirm existing evidence that surgery is indicated in patients who have isolated breast cancer recurrence, even when surgery means chest wall resection. Moreover, adjuvant radiotherapy and e for estrogen receptor positive tumors e adjuvant hormone therapy is indicated.11 On the contrary, although it is well-known that the longer the disease-free interval, the better the survival outcome, our uni and multivariate analysis disclosed that the interval between breast and thoracic surgery had no impact on overall survival, probably due to the small number of patients. As peripheral osteomuscular structures are the major target sites of recurrence, macroscopic radical resection was
very often possible Fig. 2. Microscopic infiltration of the resection margins was observed in some isolated cases, whereas macroscopic residual disease was anecdotal. The vast majority of our patients required prosthetic reconstruction of the chest wall because of the large tissue defect following resective surgery Figs. 3. Our preferred reconstruction technique comprises a prosthesis (monofilament polypropylene mesh plus resinous material) followed by latissimus dorsi muscle flap. This combination offers a stable assessment of the chest wall, allowing adequate ventilation. In addition, the procedure is relatively faster than other reconstruction techniques (e.g. TRAM) and gives rise to fewer postoperative complications. We assume that our good overall and disease-free survival rates are only partially due to surgical resection itself. We believe these patients benefit from an ideal pre and postoperative multimodality treatment and from strict candidate selection that led us to operate on less than one-third of the patients referred to us with this indication; the need of post resection treatments is probably a surrogate for presence of systemic disease; in fact all patients but one required additional treatment following chest wall resection. However, due to the small number of enrolled patients and the non-randomized retrospective design of our study, further studies are required to confirm our results.
Conclusions Chest wall resection and reconstruction for locally recurrent breast cancer is a feasible and safe procedure providing adequate local disease control and an excellent palliation of very disabling symptoms. This approach may be advocated as an effective palliative procedure in selected patients.
Competing interest and disclosure Fig. 2 e CT scan disclosing chest wall recurrence following left mastectomy, involving the left hemimanubrium of the sternum and the 2nd chondro-costal joint.
The authors declare that they have no competing interests and anything to disclose.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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Fig. 3 e Intra operative view: a) Chest wall recurrence b) Post resectional view c) Latissimus dorsi pedicled muscle flap d) Final view.
Acknowledgment The authors thank Anne Collins for editing the English text.
references
1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74e108. 2. Bedwinek J. Natural history and management of isolated local-regional recurrence following mastectomy. Semin Radiat Oncol 1994;4:260e9. 3. Buzdar AU. Phase III study of letrozole versus tamoxifen as first-line therapy of advanced breast cancer in postmenopausal women: analysis of survival and update of efficacy from the international letrozole breast cancer group. J Clin Oncol 2004;22:3199e200. 4. Robertson JF, Come SE, Jones SE, Beex L, Kaufmann M, Makris A, et al. Endocrine treatment options for advanced breast cancer - the role of fulvestrant. Eur J Cancer 2005;41:346e56. 5. Sledge GW, Neuberg D, Bernardo P, Ingle JN, Martino S, Rowinsky EK, et al. Phase III trial of doxorubicin, paclitaxel and the combination of doxorubicin and paclitaxel as frontline chemotherapy for metastatic breast cancer: an intergroup trial. J Clin Oncol 2003;21:588e92. 6. Veronesi G, Scanagatta P, Goldhirsch Rietjens M, Colleoni M, Pelosi G, et al. Results of chest wall resection for recurrent or locally advanced breast malignancies. Breast 2007;16:297e302. 7. Hanagiri T, Nozoe T, Yoshimatsu T, Mizukami M, Ichiki Y, Sugaya M, et al. Surgical treatment for chest wall invasion due to the local recurrence of breast cancer. Breast Cancer 2008;15:298e302.
8. Buchanan CL, Dorn PL, Fey J, Giron G, Naik A, Mendez J, et al. Locoregional recurrence after mastectomy: incidence and outcomes. J Am Coll Surg 2006;203:469e74. 9. Jagsi R, Raad RA, Goldberg S, Sullivan T, Michaelson J, Powell SN, et al. Locoregional recurrence rates and prognsotic factors for failure in node-negative patients treated with mastectomy: implications for postmastectomy radiation. Int J radiat Oncol Biol Phys 2005;62:1035e9. 10. Santillan AA, Kiluk JV, Cox JM, et al. Outcomes of locoregional recurrence after surgical chest wall resection and reconstruction for breast cancer. Ann Surg Oncol 2008;15(5):1322e9. 11. van der Pol CC, van Geel AN, Menke-Pluymers MB, Schmitz PI, Lans TE. Prognostic factors in 77 curative chest wall resections for isolated breast cancer recurrence. Ann Surg Oncol 2009;16:3414e21. 12. Halverson KJ, Perez CA, Kuske RR, Garcia DM, Simpson JR, Fineberg B. Survival following loco regional recurrence of breast cancer: univariate and multivariate analysis. Int J Radiat Oncol Biol Phys 1992;23:285e91. 13. Kurtz JM, Amalric R, Brandone H, Ayme Y, Jacquemier J, Pietra JC, et al. Local recurrence after breast-conserving surgery and radiotherapy. Frequency, time course, and prognosis Cancer 1989;63:1912e7. 14. Monyak DLS. Breast: locally advanced (T3 and T4) and recurrent tumors. In: Perez CA, Brady LW, editors. Principles and practice of radiation oncology. Philadelphia: Lippincott; 1992. pp. 948e69. 15. Le MG, Arriagada R, Spielmann M, Guinebretie`re JM, Rochard F, et al. Prognostic factors for death after an isolated local recurrence in aptients with early-stage breast carcinoma. Cancer 2002;94:2813e20. 16. Friedel G, Kuipers T, Dippon V, Al-Kammash F, Walles T, Kyriss T, et al. Full-thickness resection with myocutaneous flap reconstruction for locally recurrent breast cancer. Ann Thorac Surg 2008;85:1894e900.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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17. World Medical Association Declaration of Helsinki Ethical principles for medical research involving human subjects Helsinki 1964, amended in Tokyo 1975, Venice 1983, Hong Kong 1989, South Africa 1996, Edinburgh 2000. 18. Downey RJ, Rusch V, Ida Hsu F, Leon L, Venkatraman E, Linehan D, et al. Chest wall resection for locally recurrent breast cancer: is it worthwhile? J Thorac Cardiovasc Surg 2000;119:420e8. 19. Imkampe A, Bendall S, Bates T. The significance of the site of recurrence to subsequent breast cancer survival. Eur J Surg Oncol 2007;33:420e3. 20. Crowe Jr JP, Gordon NH, Antunez AR, Shenk RR, Hubay CA, Shuck JM. Local-regional breast cancer recurrence following mastectomy. Arch Surg 1991;126:429e32. 21. Clemos M, Danson S, Hamilton T, Goss P. Locoregionally recurrent breast cancer: incidence, risk factors and survival. Cancer Treat Rev 2001;27:67e82.
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22. Taghian A, Jeong JH, Mamounas E, Anderson S, Bryant J, Deutsch M, et al. Patterns of loco-regional failure in patients with operable breast cancer treated by mastectomy and adjuvant chemotherapy with or without tamoxifen and without radiotherapy: results form five National Surgical Adjuvant Breast and Bowel Project randomized clinical trials. J Clin Oncol 2004;22:4247e54. 23. Faneyte IF, Rutgers EJ, Zoetmuller FA. Chest wall resection in the treatment of locally recurrent breast carcinoma: indications and outcome for 44 patients. Cancer 1997;80:886e91. 24. Pameijer CR, Smith D, McCahill LE, Bimston DN, Wagman LD, Ellenhorn JD. Full-thickness chest wall resection for recurrent breast carcinoma: an institutional review and meta-analysis. Am Surg 2005;71:711e5.
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Available online at www.sciencedirect.com
ScienceDirect The Surgeon, Journal of the Royal Colleges of Surgeons of Edinburgh and Ireland www.thesurgeon.net
Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment Francesco Petrella a,*, Davide Radice b, Alessandro Borri a, Domenico Galetta a, Roberto Gasparri a, Monica Casiraghi a, Adele Tessitore a, Alessandro Pardolesi a, Piergiorgio Solli a, Giulia Veronesi a, Stefania Rizzo c, Stefano Martella d, Mario Rietjens d, Lorenzo Spaggiari a,e a
Department of Thoracic Surgery, European Institute of Oncology, Italy Department of Epidemiology and Biostatistics, European Institute of Oncology, Italy c Department of Radiology, European Institute of Oncology, Italy d Department of Plastic and Reconstructive Surgery, European Institute of Oncology, Italy e University of Milan School of Medicine, Italy b
article info
abstract
Article history:
Introduction: Breast cancer is the leading cause of cancer death among women in the
Received 14 October 2013
industrialized countries. The incidence of local recurrences after mastectomy and breast-
Received in revised form
conserving therapy varies between 5% and 40% depending on risk factors and primary
22 February 2014
therapy.
Accepted 3 March 2014
Methods: From April 1999 to April 2011, 40 patients underwent chest wall resection and
Available online xxx
reconstruction for locally recurrent breast carcinoma with chest wall invasion. The main goal of surgery was local disease control to palliate clinical symptoms.
Keywords:
Results: Local radical resection was achieved in 26 patients (65%). One, 2 and 5 year overall
Breast cancer
survival rates were 94.4%, 82.0% and 68.5%; 1, 2 and 5 year disease-free survival rates were
Chest wall resection
94.4%, 73.6% and 45.5% respectively.
Chest wall reconstruction
Univariate analysis indicated age (p ¼ 0.002) and synchronous distant metastases (p ¼ 0.020) as factors having a negative impact on overall survival; multivariate analysis disclosed age (p ¼ 0.052) and synchronous metastases (p ¼ 0.059) as factors with a slight negative impact on overall survival. Older age was associated with improved overall survival. Univariate analysis indicated synchronous distant metastases (p ¼ 0.029) and the need of post resectional additional treatments (p ¼ 0.022) as factors adversely conditioning disease-free survival or time to progression; multivariate analysis disclosed the need of post resectional additional treatments (p ¼ 0.036) as the only factor adversely conditioning disease-free survival or time to progression.
* Corresponding author. Department of Thoracic Surgery, European Institute of Oncology, Via Ripamonti, 435, 20141 Milan, Italy. Tel.: þ39 0257489362; fax: þ39 0294379218. E-mail addresses: [email protected], [email protected] (F. Petrella). http://dx.doi.org/10.1016/j.surge.2014.03.001 1479-666X/ª 2014 Royal College of Surgeons of Edinburgh (Scottish charity number SC005317) and Royal College of Surgeons in Ireland. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
2
t h e s u r g e o n x x x ( 2 0 1 4 ) 1 e7
Conclusions: Chest wall resection and reconstruction for locally recurrent breast cancer is a feasible and safe procedure providing adequate local disease control and an excellent palliation of very disabling symptoms in a selected group of patients. ª 2014 Royal College of Surgeons of Edinburgh (Scottish charity number SC005317) and Royal College of Surgeons in Ireland. Published by Elsevier Ltd. All rights reserved.
Introduction Breast cancer is the leading cause of cancer death among women in the industrialized countries.1 The incidence of local recurrences after mastectomy and breast-conserving therapy varies between 5% and 40% depending on risk factors and primary therapy.2 The first-line treatments in recurrent breast cancer are endocrine therapy for patients with estrogen or progesterone receptor positive cancer, and chemotherapy for patients with receptor-negative cancers.3e5 However, local therapies such as radiotherapy or surgery may be required in selected cases for local disease control and palliation of disabling symptoms like pain, bleeding, ulceration, malodorous secretion, infection and fungating lesions.6,7 On the one hand, locoregional recurrence of breast cancer following breast surgery may be a systemic disease and in many patients it tends to occur at the same time as distant metastases, making the indication for surgical resection questionable.8,9 On the other, although the primary goal of chest wall resection is to achieve local tumor control, it may lead to long-term palliation and even cure for a small subset of patients with isolated chest wall recurrence of breast cancer after multimodal treatment failure.10 Early detection of locoregional recurrence and small tumor size predicted a better prognosis.11e13 Options for local treatment of locoregional recurrence include wide local excision and/or radiotherapy whether or not in combination with hyperthermia14; however, for small lesions, the type of local treatment did not affect the final outcome.15 Whether complete resection of local recurrence offers a merely palliative or possibly curative approach or a major prolongation of survival remains unsettled.16 The aim of this study was to define the role of chest wall resection for locally recurrent breast cancer as a salvage treatment for a selected group of symptomatic patients.
Methods The present study was conducted in accordance with the Declaration of Helsinki.17 Written informed consent was obtained from all subjects before any procedure was done. The investigators explained all the planned procedures verbally to all subjects who received and signed a subject information sheet to acquaint themselves with details of the planned therapeutic schedule. All patients authorized the investigators to use their data anonymously only for scientific purposes according to Italian legislation (law no. 675/1996).
Data were collected prospectively and entered into our institutional general thoracic database at the point of care. The database was reviewed retrospectively. From April 1999 to April 2011, 40 patients underwent chest wall resection and reconstruction for locally recurrent breast carcinoma with chest wall invasion proven by routine preoperative chest computed tomography (CT) or by chest wall magnetic resonance imaging (MRI) in selected cases. The main goal of surgical therapy was local disease control to palliate clinical symptoms like pain, cutaneous ulceration and discomfort related to chest wall deformity. For this reason a distant metastasis was not a contraindication. Selection criteria for surgery were multimodal treatment failure and life expectancy of more than 6 months. The surgical approach involved soft tissue resection with broad margins and chest wall resection with total or partial sternectomy and resection of one or more ribs. In case of major tissue defect following resective surgery reconstruction was performed using different types of prostheses covered by a vascularized pedicle muscle flap. Technical aspects of demolition and reconstructive procedures were reviewed (sternectomy, ribs resection, soft tissue resection, endothoracic organ resection, type of prosthesis, type of flap and technical complications) together with oncologic history including previous type and date of breast operation, histology and biology of breast and thoracic surgical specimens (Ki67%, Her2 neu expression, estrogen and progesterone receptor expression), and the interval between breast and thoracic surgery. Patients were defined as triple negative if estrogen, progesterone and Her2 neu expression were negative; otherwise, they were defined as non-triple negative.10 Recurrence was defined as the return of cancer after treatment and after a period of time during which the cancer could not be detected. Local recurrence was defined as the reappearance of disease in locoregional lymph nodes or in the chest wall adjacent to the site of thoracic excision. Distant recurrence was defined as distant sites of visceral disease, including malignant pleural effusions or implants. Progression was defined as cancer growth without a period of time during which the cancer could not be detected. Distant progression was defined as cancer spreading to distant sites; locoregional progression was defined as cancer worsening close to the surgical field. A complete resection (R0) was defined as pathologic demonstration of negative tissue margins and an assessment by the operating surgeon that all detectable disease had been removed. Microscopically incomplete resection (R1) was defined as complete macroscopic resection with positive margins found on final pathologic review. Macroscopically
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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incomplete resection (R2) was defined as gross residual disease after attempted resection.18
Statistical analysis Patient characteristics were summarized and tabulated using either counts and percentage or counts, mean, standard deviation (SD), median, min and max for the categorical or continuous variables, respectively. Overall survival (OS) and disease-free survival (DFS) were defined as the time from surgery to the last follow-up date or death and to the last follow-up date or recurrence date respectively, then estimated and plotted using the KaplaneMeier method. Univariate and multivariate hazard ratios (HR) for the OS and DFS were estimated using the Cox proportional hazards model and tabulated alongside their 95% confidence Intervals. The statistical analyses were conducted using SAS Software 9.2 (NC, USA).
rib resection and among them a median of 2.5 ribs were removed (range 1e5). Three out of 40 patients (7.5%) received extended soft tissue resection involving periostium removal but without complete chest wall resection. Four out of 40 patients (10%) received endothoracic organ resection as follows: left lung in 2 cases, pericardium in 1 case, pericardium plus left innominate vein in 1 case. Local radical resection was achieved in 26/40 patients (65%). Microscopic residual disease was left in 13/40 patients (32.5%). Macroscopic residual disease was left in 1 patient (2.5%). A prosthesis was used in 34/40 patients (85%): 26/34 (76.4%) received monofilament polypropylene mesh plus resinous
Table 1b e Clinico-pathological features of the study population. %
Results With regard to initial non-surgical treatment, at the time of breast cancer diagnosis 11 patients (27.5%) received chemotherapy þ hormone therapy; 7 patients (17.5%) received chemotherapy alone; 6 patients (15%) received hormone therapy þ radiotherapy; 5 patients (12.5%) received chemotherapy þ radiotherapy; 4 patients (10%) received hormone therapy alone; 2 patients (5%) received radiotherapy alone; 1 patient (2.5%) did not receive any treatment; 4 patients (10%) received other combined treatments (e.g., chemotherapy þ hormone therapy þ target therapy or chemotherapy þ hormone therapy þ radiotherapy).
Surgical aspects The study population consisted of 40 patients with a median age of 59 years (range 30e83 years) at chest wall resection. The median interval between breast and chest wall operations was 59 months (range 0e402). Chest wall resection included total or partial sternectomy in 21/40 cases (52.5%). 34/40 patients (85%) received at least 1
Table 1a e Technical aspects of the procedures. Variable
Subgroup
%
Prosthesis
Polypropylene mesh þ resinous material Polyglactin knitted mesh Polypropylene mesh alone Titanium bars Latissimus dorsi Pectorialis major TRAM Fascio e cutaneous Cyclopization Flap ischemia Prosthesis infection Bleeding Operative mortality
76.4
Flap
Surgical complication
8.9 8.9 5.8 40 20 30 3.4 6.6 5 7.5 2.5 0
Median age Sternectomy required Median ribs resected Endothoracic organ resection Mean tumor size Synchronous metastases at CWRRa Synchronous metastases (lymph nodes) Synchronous metastases (distant sites) Treatments before CWRRa (combined) Chemotherapy Radiotherapy Hormone therapy Target therapy None Treatments after CWRRa (combined) Chemotherapy Radiotherapy Hormone therapy Target therapy None Outcome after salvage therapy Disease control Toxicity Previous breast surgery
Previous breast histology
a b
59 (30e83) 21/40 2.5 (1e5) 4/40
10
5.4 cm (1.3e18) 15/40
37.5%
5/15
33.3%
10/15
66.6%
31/40 23/40 23/40 4/40 4/40
77.5 57.5 57.5 10 10
22/40 6/40 25/40 5/40 1/40
55 15 62.5 12.5 2.5
30/40 8/40 Mastectomy Quadrantectomy Ductal resection Bilateral mastectomy Ductal carcinoma Papillary carcinoma Medullary carcinoma Mucinous carcinoma Lobular carcinoma Combined lobular and ductal carcinoma Phyllodes tumor NOSb histology
75 20 62.5 32.5 2.5 2.5 52.5 5 2.5 2.5 2.5 2.5
52.5
2.5 30
CWRR: Chest wall resection and reconstruction. NOS: Not otherwise specified.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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Table 2 e Clinical characteristics of deceased patients. N.
Age at diagnosis
Age at recurrence
Cause of death
Her2neu/Er/Pr/
Adjuvant therapy
DFI (months)
R status at resection
Distant disease at time of treatment
37 57 49 58 53 51 30 52 34
39 59 52 61 55 53 31 54 34
Rec Rec Rec Rec Rec Rec Prog Prog Prog
// // /þ/þ // // // // // //
No C C/H/R H C C C/T C C
NA 21 13 19 10 1 5 16 NA
Not radical Not radical Radical Radical Radical Radical Radical Not radical Radical
No Yes Yes No Yes Yes Yes Yes Yes
1 2 3 4 5 6 7 8 9
Table legend: DFI ¼ disease-free interval; Rec ¼ recurrence; Prog ¼ progression; C ¼ chemotherapy; H ¼ hormone therapy; R ¼ radiotherapy; T ¼ target therapy; NA ¼ not applicable.
material (Bard* Mesh, Bard Davol Inc., Cranston, RI, USA; Cranioplastic, Codman & Shurtleff, Inc. Raynham, MS, USA); 3/34 (8.8%) received adsorbable polyglactin knitted mesh (Vicryl knitted mesh, Ethicon Inc., New Brunswick, NJ, USA); 3/ 34 (8.8%) received monofilament polypropylene mesh alone (Bard * Mesh, Bard Davol Inc., Cranston, RI, USA) and 2/34 patients (5.8%) received titanium bars. Thirty out of 40 (75%) patients received a flap to complete chest wall reconstruction: latissimus dorsi muscle flap was used in 12/30 cases (40%); pectorialis major muscle flap was used in 6/30 cases (20%); transposition of rectus abdominis muscle (TRAM) was used in 9/30 cases (30%); a fasciocutaneous sliding flap was used in 1/30 case (3.3%); cyclopization was used in 2/30 cases (6.6%). Six out of 40 patients (15%) had postoperative surgical complications requiring a re-do operation: The operative mortality rate was 0% (Table 1).
Specimen biological assessment Biological assessment on chest wall specimens disclosed a Ki67 mean value of 49.9%; Her2 neu mean expression of 17.2%, evaluated as percentage of neoplastic cells showing membrane immunoreactivity to the Dako polyclonal antiserum (Dako Denmark A/S, Glsotrup, Denmark); estrogen and progesterone receptors expression of 49.2% and 12.1% respectively. With regard to the hormonal status of chest wall specimens we observed estrogen and progesterone receptors both positive in 12 patients (30%); both negative in 15 patients (37.5%). We observed 7 triple-negative patients (17.5%).
Follow-up After a median follow-up of 30.6 months 15/40 patients (37.5%) were alive and disease-free; 15/40 patients (37.5%) were alive with disease; 9/40 patients (22.5%) had died from disease; 1/40 (2.5%) patient was lost to follow-up. Age at diagnosis, age at recurrence, cause of death, hormonal patterns, adjuvant therapies and disease-free interval of deceased patients are summarized in Table 2.
Multimodality treatments Following chest wall resection 22/40 patients (55%) received chemotherapy, 25/40 patients (62.5%) received hormone therapy, 6/40 patients (15%) received radiotherapy, 5/40 patients (12.5%) received target therapy. Only 1/40 patient (2.5%) did not receive any additional treatment following chest wall resection; in all cases additional treatments were proposed on clinical, histological and biological bases, without any fixed algorithm.
Overall and disease-free survival One, 2 and 5 year overall survival rates were 94.4%, 82.0% and 68.5%; 1, 2 and 5 year disease-free survival rates were 94.4%, 73.6% and 45.5% respectively. After a median follow-up of 30.6 months the median overall survival (OS) was not reached. The median disease-free survival was 49.1 months (Fig. 1a and b). Univariate analysis indicated age (p ¼ 0.002) and synchronous distant metastases (p ¼ 0.020) as factors adversely impacting on overall survival; multivariate analysis disclosed age (p ¼ 0.052) and synchronous metastases (p ¼ 0.059) as factors with a slight negative impact on overall survival. Univariate analysis indicated synchronous distant metastases (p ¼ 0.029) and the need for post-resectional additional treatments (p ¼ 0.022) as factors adversely impacting on disease-free survival or time to progression. Multivariate analysis disclosed the use of post-resectional additional treatments (p ¼ 0.036) as the only factor with an adverse impact on disease-free survival or time to progression.
Discussion Despite major therapeutic advances, recurrent breast cancer is still a lethal disease in most patients.5,19 Isolated local recurrences are thought to represent about 20% of all recurrences, while local disease, in combination with either regional or distant recurrences, represents a further 3%.20 The majority of locoregional recurrences occur as isolated chest wall disease, and only a small proportion present with concurrent systemic disease or following distant metastases.21,22 In our series 15 patients (37.5%) presented with concurrent systemic disease: 10 patients (66.6%) presented with
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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Fig. 1 e a) Overall survival b) disease-free survival.
distant metastases (pleura or distant bone), while 5 patients (33.4%) presented with regional nodal involvement (internal mammary chain or axillary lymph nodes). We never observed true distant soft tissue metastases, probably because of the local invasive biology of the original breast disease. Although palliation rather than prolongation of survival is usually the main aim of chest wall resection, some studies found that a small subset of patients would have a long disease-free interval and possibly cure after chest wall resection and reconstruction.23,24 Our results confirm existing evidence that surgery is indicated in patients who have isolated breast cancer recurrence, even when surgery means chest wall resection. Moreover, adjuvant radiotherapy and e for estrogen receptor positive tumors e adjuvant hormone therapy is indicated.11 On the contrary, although it is well-known that the longer the disease-free interval, the better the survival outcome, our uni and multivariate analysis disclosed that the interval between breast and thoracic surgery had no impact on overall survival, probably due to the small number of patients. As peripheral osteomuscular structures are the major target sites of recurrence, macroscopic radical resection was
very often possible Fig. 2. Microscopic infiltration of the resection margins was observed in some isolated cases, whereas macroscopic residual disease was anecdotal. The vast majority of our patients required prosthetic reconstruction of the chest wall because of the large tissue defect following resective surgery Figs. 3. Our preferred reconstruction technique comprises a prosthesis (monofilament polypropylene mesh plus resinous material) followed by latissimus dorsi muscle flap. This combination offers a stable assessment of the chest wall, allowing adequate ventilation. In addition, the procedure is relatively faster than other reconstruction techniques (e.g. TRAM) and gives rise to fewer postoperative complications. We assume that our good overall and disease-free survival rates are only partially due to surgical resection itself. We believe these patients benefit from an ideal pre and postoperative multimodality treatment and from strict candidate selection that led us to operate on less than one-third of the patients referred to us with this indication; the need of post resection treatments is probably a surrogate for presence of systemic disease; in fact all patients but one required additional treatment following chest wall resection. However, due to the small number of enrolled patients and the non-randomized retrospective design of our study, further studies are required to confirm our results.
Conclusions Chest wall resection and reconstruction for locally recurrent breast cancer is a feasible and safe procedure providing adequate local disease control and an excellent palliation of very disabling symptoms. This approach may be advocated as an effective palliative procedure in selected patients.
Competing interest and disclosure Fig. 2 e CT scan disclosing chest wall recurrence following left mastectomy, involving the left hemimanubrium of the sternum and the 2nd chondro-costal joint.
The authors declare that they have no competing interests and anything to disclose.
Please cite this article in press as: Petrella F, et al., Chest wall resection and reconstruction for locally recurrent breast cancer: From technical aspects to biological assessment, The Surgeon (2014), http://dx.doi.org/10.1016/j.surge.2014.03.001
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Fig. 3 e Intra operative view: a) Chest wall recurrence b) Post resectional view c) Latissimus dorsi pedicled muscle flap d) Final view.
Acknowledgment The authors thank Anne Collins for editing the English text.
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