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Eur J Cardiothorac Surg 2002;22:335-344
© 2002 Elsevier Science NL

Results of lung metastasectomy from breast cancer: prognostic criteria on the basis of 467 cases of the international registry of lung metastases

^a Department of Thoracic Surgery, Klink Schillerhoehe, Solitudestrasse 18, D-70839 Gerlingen, Germany
^b Department of Thoracic Surgery, European Institute of Oncology, Milan, Italy
^c Department of Thoracic Surgery, Toronto General Hospital, Toronto, Canada
^d Department of Thoracic Surgery, The Royal Brompton Hospital, England, UK
^e Department of Surgery and Oncology, Wayne State University, Harper Hospital, Detroit, USA
^f Department of Thoracic and Cardiovascular Surgery, The University of Texas MD Anderson Cancer Center, Houston, TX, USA

Received 15 October 2001; received in revised form 3 April 2002; accepted 18 April 2002.

* Corresponding author. Tel.: +49-7156-203-2241; fax: +49-7156-203-2003
e-mail: friedel{at}klinik-schillerhoehe.de

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 
Objective: Metastatic breast cancer is still defined as an incurable disease. Although the prognosis after resection of isolated metastases to the lung is much better than after chemotherapy most oncologists and gynecologists disapprove of lung metastasectomy. Methods: In order to summarize the experience of pulmonary metastatic surgery and to achieve more relevant data by an increased number of cases, we evaluate the data of the International Registry of Lung Metastases of 467 patients having lung metastases from breast cancer with regard to long-term survival and prognostic factors. Results: In 84% a complete metastatic resection was possible. The survival rates are 38% after 5 years, 22% after 10 years, and 20% after 15 years. Prognostic factors are a disease-free interval of 36 months with 5-year survival of 45%, a 10-year survival of 26% and a 15-year survival of 21% (P=0.0001), solitary lung metastasis is associated with a survival rate of 44% after 5 years and of 23% after 10 and 15 years, but this is not statistically significant compared to multiple metastases. When establishing prognostic groups as suggested by Pastorino and the International Registry of Lung Metastases based on the risk factors disease-free interval, number of metastases and complete resection the group with the best prognosis showed 5-year survival of 50%, 10- and 15-year survival of 26% with a median survival of 59 months. Conclusion: Considering the low morbidity and mortality rate, we think that lung metastasectomy today is the best treatment option in selected cases of lung metastases from breast cancer.

Key Words: Breast cancer • Lung metastases • Lung metastasectomy • Prognostic factors

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 
With an incidence of 20–25% in Europe, breast cancer still is the most frequent malignant disease in women. In about 30%, the tumor disease recurs within 5 years, 36% of these patients have local recurrences and 56% metastases [1]. In the metastatic stage, about 15–25% of women have an isolated metastatic development in the lung and the pleural space [2,3]. Therapy of metastatic breast cancer is still controversial ranging from best supportive care to high-dose chemotherapeutic regimes [4]. The present therapeutic concept offers three different procedures alone and in combination, i.e. chemotherapy, radiotherapy and hormone therapy. Since it is assumed that metastatic breast cancer is a systemic, incurable disease, local surgical measures are generally rejected. However, on the basis of admittedly small numbers of cases, it has been suggested that the resection of pulmonary metastases from solid tumors in nearly all cases provided better long-term results than systemic therapy alone. In order to summarize the experience of pulmonary metastatic surgery and to achieve more relevant data by an increased number of cases, the International Registry of Lung Metastases was established in 1991. In cooperation with specialized centers from Europe, the United States, and Canada, the data of altogether 5206 resections of pulmonary metastases from different primary tumors were collected [5]. In the following, we evaluate the data of the registry of those patients having lung metastases from breast cancer with regard to long-term survival and prognostic factors.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 
The Istitutio Nazionale Tumori of Milan developed a stringent database for the registration of lung metastasectomies. The database includes a record form for each patient and is divided into four sections: identification of the patient; therapy of primary neoplasm; description of each lung metastasectomy performed (date of surgery, size and number of resected metastases, kind of surgery, histology, and adjuvant forms of therapy) and a complete follow-up (recurrence in the lung or/and in other organs, therapy and survival data). Combined metastatic surgery in several organs was also registered. Planned bilateral thoracotomies were considered as one intervention, even if they were performed separately.

Patients who underwent surgery for lung metastases with a potentially curative intention were included in the Registry, this means that there were no signs of carcinosis or local inoperability. If a complete resection turned out to be impossible intraoperatively, this was documented and the patient was nevertheless included in the database. Interventions with a primary palliative approach were not included. Simultaneous resections of the primary tumor and metastases in other organs were included as well.

The number of patients included with regard to the different centers is listed in Appendix A.

Data analysis was performed by an independent agency, the Institute of Drug Development (ID2) in Brussels. Evaluation was performed using the StatView Analysis System under the license of the SAS Institute (Cary, NC).

The following variables were tested: number of resected as well as pathologically proved metastases, disease-free interval (DFI), uni- or bilateral metastases, surgical approach, method of resection, time of adjuvant chemotherapy, redo surgery and prognostic groups as suggested by the International Registry [5].

Using the Kaplan–Meier method, survival was calculated from the time of the first metastatic resection to the last follow-up or the time of death. Significances were calculated using the log–rank test.

Altogether, 481 patients with lung metastasectomies from breast cancer were included in the database. The documented metastatic resections were performed between 1960 and 1994. Four patients were excluded from the analysis for missing follow-up data, three patients for negative definite histology. In addition, seven male patients were excluded from the analysis. The following evaluation was thus performed on the basis of 467 female patients.

The patients data were detailed in Table 1 relating to the treatment of the primary tumor as well as to the metastasectomy. A radical resection of the primary tumor was documented in 376 (81%) of cases, no data were available in 62 (13%) patients and 23 (5%) patients were without surgical therapy.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

Mean age of the patients at the time of the first metastatic resection was 53 years (21–87 years). The median interval between primary and metastatic surgery was 43 months. Sixty percent had a free interval of more than 35 months. Surgical approach was thoracotomy in 75% and sternotomy in 20%. Thoracoscopic resections were performed in 4%, in 1% the approach was not specified. Unilateral thoracotomy was applied in 72%, bilateral in 3%. The usual surgical procedure was wedge or segmental resection in 73%. In 24% a lobectomy and in only 1% a pneumonectomy were performed, also in 2% the procedure was not specified. A solitary metastasis was found in 66% i.e. in 58% of complete resections and in 8% of incomplete resections. Major causes of incomplete resections were tumor occupation of lymph nodes or chest wall or diaphragm infiltration with short or tumerous resection margins. In 21% of patients, two to three pathologically proved metastases were resected and in 10% more than three metastases. Involved mediastinal lymph nodes were found in 7%; 4% in complete resections and 3% in incomplete resections. Thirty-three percent received an additional chemotherapy, 8% prior to metastatic resection, 19% thereafter, and 6% before and after resection. In 20 (4%) patients recurrent metastases were treated surgically.

On 1 March 1995, 186 (48%) of 390 patients with completely resected metastases were still alive, one patient more than 15 years, 12 (3%) more than 10 years and 58 (15%) more than 5 years. Of 77 patients having incomplete resections, 26 (35%) were survivors, 4 (5%) of them more than 5 years. Six patients (1%) died within 30 days after metastatic surgery.

The total group of 467 patients has a cumulative 5-year survival rate of 35%, a 10-year survival rate of 20%, and a 15-year survival rate of 18%. Median survival is 35 months.

Fig. 1 presents survival data with regard to complete and incomplete resection of metastases. The survival rates associated with complete resection are 38% after 5 years, 22% after 10 years, and 20% after 15 years. Median survival is 37 months. Incomplete resections are associated with a 5-year survival of 18% with median survival being 25 months. The difference in the log–rank test is significant with P=0.0009.

View larger version (24K): [in this window] [in a new window]   Fig. 1. Complete vs. incomplete resections.

View larger version (23K): [in this window] [in a new window]   Fig. 2. Complete resections according to DFI.

View larger version (28K): [in this window] [in a new window]   Fig. 3. Complete resections according to number of metastases.

Among complete resections, bilateral metastases have worse results compared to unilateral ones with a 5-year survival of 21 vs. 40%. However, the difference is not statistically significant. The median survival was 39 months in unilateral metastases and 34 months in bilateral ones (Fig. 4 ).

View larger version (20K): [in this window] [in a new window]   Fig. 4. Complete resections according to mono- or bilateral metastases.

View larger version (23K): [in this window] [in a new window]   Fig. 5. Complete resections according to number of metastasectomies.

Group I: Complete resection, DFI36 months, solitary metastasis 5-year survival 50%, 10 and 15-year survival 26% with a median survival of 59 months.

Group II: Complete resection, DFI<36 months or multiple metastases 5-year survival 35%, 10-year survival of 21% and 15-year survival of 18% with a median survival of 36 months.

Group III: complete resection, DFI<36 months and multiple metastases survival after 5 and 10 years 13% with a median survival of 25 months.

Group IV: Incomplete resection. Five-year survival of 18% with a median survival of 25 months.

The differences between the groups I and II compared to groups III and IV are statistically significant (log–rank P<0.001, ²=30.014) (Fig. 6 ).

View larger version (32K): [in this window] [in a new window]   Fig. 6. Complete resections according to risk groups.

Mean follow-up period of all patients is 34 months (max 240, min 0), that of patients with complete resections 36 months (max 240, min 0).

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 
Medical and gynecological oncologists still regard metastatic breast carcinoma as an incurable disease. Based on the assumption that it is a systemic disease, local surgical measures are rejected or only considered as palliative procedures in symptomatic metastases. This is mainly true for bone metastases implying a risk of fracture and symptomatic cerebral metastases. However, systemic therapies applied in the last years have achieved little progress in terms of prolongation of life. Median survival after chemotherapy is 10–20 months. In the last years, high-dose chemotherapy with stem-cell transplantation has been increasingly applied in trials. In this connection, the possibility of a curative therapy is mentioned for the first time [6]. Median survival after high-dose chemotherapy is only 20–30 months partly due to the very high therapy-associated mortality of up to 5% [4,7]. There are only very few reports on the outcome of isolated lung metastases after chemotherapy or hormone therapy. Schlappack reports on the course of 41 patients with a median survival of 13 months and a 5-year survival of 10% after chemotherapy and/or hormone therapy. Three of the patients additionally underwent resection of pulmonary metastases. In patients with a DFI>18 months, prognosis was statistically not significantly better with a 5-year survival of 25%. There was no difference in survival between solitary and multiple lung metastases [8]. In a randomized chemotherapeutic study, Heidemann et al. among others report on 20 patients with isolated lung metastases whose 5-years survival was 21% with a median survival of 25 months. Prognostic factors were DFI>18 months and a positive receptor status [9]. The new molecular target therapy like inhibition of Her2-neu receptor or VEGF-receptor-2 antibody or p53 gene replacement are still under observation in preclinical or phase I/II studies.

Surgery of lung metastases of almost all solid tumors is reported to provide good long-term results [10]. In its first publication, the International Registry of Lung Metastases reports on a 5-year survival of 36% in 4572 patients having complete resection of lung metastases. Since after 15 years 22% of the patients are still alive, metastatic surgery represents a curative approach in almost one quarter of patients [5]. In contrast to these results, surgical therapy of lung metastases is of minor importance in the oncological field. Only in case of germ cell tumors and increasingly in osteosarcomas, metastatic surgery plays a role in the multimodal overall concept [11,12]. Equally in renal cell carcinomas, the results of lung metastatic surgery are increasingly recognized because of the obvious failure of systemic therapeutic approaches [13]. Metastatic surgery for breast cancer, however, still is highly controversial. Although in the last years metastasectomy has provided markedly better results than systemic therapy even in lung metastases from breast cancer, this kind of therapy is strongly rejected by most oncologists. In 1992, Staren reports on 27 patients after resection of lung metastases. Five-year survival in this group is 35% with a median survival of 55 months. The number of metastases in this report was not a prognostic factor and the DFI was not documented [14]. Lanza examined 44 patients after resection of lung metastases from breast cancer. In 37 cases, a complete resection could be achieved. The median survival in this group was 47 months with a 5-year survival of 49%. A significant prognostic factor was a DFI>12 months with a 5-year survival of 57% [15]. In a study with 68 completely resected patients Friedel reported a 5-year survival of 31% with a median survival of 36 months. There were no statistically significant prognostic factors, but a tendency of a prolonged survival for patients with solitary metastases and a DFI24 months. In the group with both prognostically favorable factors, there was a 5-year survival of 40% [16]. McDonald et al. investigated 60 patients with the surprising result that incomplete resections provided better results in terms of long-term survival than complete resections. All other authors report on the complete resection as a significant prognostic factor. The 5-year survival of the whole group also exceeded the results of chemotherapy with 37.8% [17].

The opponents of lung metastatic surgery have criticized that the results presented so far are based on too small numbers of cases. For this reason, the International Registry of Lung Metastases was established presenting exactly documented long-term courses of patients after lung metastatic resection in large numbers also with regard to individual tumor entities. To our knowledge, the course of disease of such a large number as 465 patients with lung metastases from breast cancer has not been published so far. The cumulative 5-year survival of 35% in the total group has so far not been achieved by any other therapeutic approach [2,6,8,9]. Significant prognostic criteria include the resectability of the metastases and the disease-free interval. However, the group of metastases, which cannot be resected completely, has to be defined or documented more exactly in future prospective studies. In previous retrospective analyses, this group includes patients with pleural disease, tumor debulking i.e. R2 resections as well as patients with R1 resections or lymph node involvement. It can be assumed that this group differs in its prognosis depending on the amount of residual metastases.

In the group of completely resected patients, the disease-free interval is the only univariate significant prognostic parameter, which is a DFI of36 months in this study. In other studies, it varies between 12 and 48 months [5,15,16]. The number of pathologically proved metastases shows a tendency towards longer survival for patients with solitary metastasis, but it is not statistically significant. This is also confirmed by Bodzin [18]. The prognostic groups suggested by our registry also show their relevance in this investigation [5]. Risk group I comprising patients with solitary metastases and a DFI36 months shows a 5-year survival of 50% according to the Kaplan–Meier method. Fifteen-year survival in this group is 25%, thus we regard lung metastatic surgery for breast cancer as a curative approach. In group II with one risk factor, 5-year survival is still 35% while declining to 13 and 18% in groups III and IV, respectively. The differences are statistically significant with P=0.0001. The choice between unilateral or bilateral approach does not provide any relevant difference in survival. Neither was there any major differences concerning the kind of surgery. Pneumonectomy being performed in only five cases and 60% having died within only 2 years. This underlines the demand that pneumonectomy is only justified in exceptional cases. Additional chemotherapy does not appear to provide a major advantage. The most favorable results were achieved in patients without chemotherapy. As well chemotherapy before, or before and after metastasectomy provides worse results including patients in the prognostically favorable risk group I. There are other important prognostic factors like TNM-status of the primary tumor, hormone receptor status of primary tumor and metastasis as well as the new molecular markers like proliferating markers, angiogenic factors and onco- or suppressor-genes which have to be considered in future trials undoubtedly.

Recurrent metastases from breast cancer are rarely treated surgically. In 19 cases, recurrent metastases were resected. A 5-year survival of 53% shows that these patients benefit from redo surgery and we think that this option should be chosen more frequently.

In conclusion, this study with the largest documented number of resected lung metastases from breast cancer shows that metastasectomy at present provides better long-term results than chemotherapy and hormone therapy. Whether high-dose chemotherapy with stem cell support is able to achieve comparable survival data has to be clarified by future studies. This applies also to the new therapeutic options like immunotherapy with HER2 monoclonal antibodies or the new hormone agents. At least in risk group I as defined by the International Registry of Lung Metastases, metastatic surgery at present has to be regarded as the therapeutic option with the longest survival rates thus to be offered to the patients as the most effective therapeutic procedure. In our opinion, with 15-year survival rates of 26%, the statement that a curative approach is not possible in lung metastases from breast cancer is not tenable. Further prospective studies on multimodal therapeutic concepts including metastatic surgery are urgently needed.

	Footnotes

 
Presented at the joint 15th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 9th Annual Meeting of the European Society of Thoracic Surgeons, Lisbon, Portugal, September 16–19, 2001.

	Appendix A. Participating institutions and responsible researcher

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 

n England Dr Peter Goldstraw 5 Royal Brompton Hospital (RBH), Sydney street SW3 6NP London France Dr Philippe Dartevelle, and Dr Alain Chapelier 35 Centre Chirurgical Marie Lannelongue (CCML), Plessis Robinson, Paris Dr Dominique Grunenwald, and Dr Philippe Girard 86 Hopital Porte de Choisy, Paris Germany Professor Dr Ingolf Vogt-Moykopf, Dr J. Schirren 21 Thoraxklinik, Heidelberg Professor Heikki Toomes, Dr Godehard Friedel 104 Thoraxchirurgie, Klinik Schillerhoehe, Stuttgart-Gerlingen Netherlands Dr A.N. van Geel 9 Dr Daniel den Hoed Cancer Center, Rotterdam Poland Dr A. Pietraszek, Maria Sklodowska, Warsaw 13 Italy Professor Dr Ugo Pastorino, and Dr Luca Tavecchio 51 Istituto Nazionale dei Tumori (INT), Milano Dr Costante Ricci, Dr Tommaso Mineo, and Dr Vincenzo Ambrogi 10 Chirurgia Toracica, Università La Sapienza e Tor Vergata, Roma Dr Giuliano Maggi 14 Chirurgia Toracica, Università di Torino Dr Antonio Briccoli 8 Patologia Chirurgica, Università di Modena Dr Vanni Beltrami 11 Clinica Chirurgica, Università"G. D'Annunzio" Chieti United States Professor Dr Robert Ginsberg, and Dr Patricia McCormack 77 Thoracic Surgery, Memorial Sloan Kettering (MSKCC), New York Professor Dr Jack Roth, and Professor Dr J.B. Putnam 27 Thoracic Surgery, M.D. Anderson Cancer Center (MDACC), Houston Dr Carmack Holmes 1 Thoracic Surgery, University of California (UCLA), Los Angeles Dr Harvey Pass 4 National Cancer Institute, Bethesda Canada Dr Michael Johnston 5 Thoracic Surgery, Mount Sinai Hospital, Toronto

	Appendix B. Conference discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 
Dr H.-B. Ris (Lausanne, Switzerland): You made the comment that you had a 80% five-year survival rate in patients with R2 disease. Does that mean that you left visible disease behind? And could you please comment whether or not there was a statistical significance between incomplete resection and complete resection but multiple metastases?

Dr Friedel: Patients with so called R2 resections are problematic to evaluate. These are patients with pleural carcinosis and left gross disease. So this is a very mixed group. Another group consists of patients with nodal tumor invasion. I showed in my presentation the significant differences of some prognostic factors. There are significant differences between a disease-free interval of more or less than 36 months, but after 10 or 15 years the groups showed equal survival curves. That is why it is problematic to stress the significance.

Dr Ris: I just want to stress out whether or not in your results it is justified, do you think it is justified if you have an 80% five-year survival rate in R2 disease, pleural metastases, comparing with about a 28% five-year survival rate and complete resection with multiple metastases or a short disease-free survival? In other words, should these category II or III patients be considered for metastasectomy for breast cancer with your result in mind?

Dr Friedel: I don't really understand your question. You must have misunderstood my interpretation of the results, we don’t have an 80% five year survival rate in R2-disease, the five year survival in incomplete resection was 18%.

Dr Ris: You said that you had an 18% five-year survival rate in R2 disease, and you had a 25% five-year survival rate after complete metastasectomy but more than one metastasis.

So if these results are not significantly different at five years, is it justified to recommend metastasectomy for more than one metastasis in breast cancer?

Dr Friedel: You can perform metastasectomies for more than one metastasis. This is a collection of about 400 patients and it is the largest series in the world with breast cancer, but the number of patients are not enough to differentiate prognosis between groups with one, two or more metastases.

Dr A. Chapelier (Le Plessis-Robinson, France): I have a comment and a question. Regarding the 44% five-year survival after resection of a single metastasis and considering that most patients won't have another lung metastasectomy for breast cancer, we could consider that this group of patients with a single metastasis would benefit from a lobectomy rather than a wedge resection. Did you observe a difference of survival between wedge resection and lobectomy in these patients? We participated to the collective work you have reported today ; we have now more than 50 patients who underwent a lobectomy for a single metastasis with a five-year survival of 55%.

Dr Friedel: We have not differentiated the wedge resection versus lobectomy for the single metastasis group. Benign lesions and primary tumors of the lung must be excluded. We made an evaluation of the whole group of metastasectomy and there was no difference in outcome between lobectomy and wedge resection. For the metastasectomy, the wedge resection is the standard operation, if it could be performed.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Participating... Appendix B. Conference... References

 

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