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Ann Thorac Surg 1997;63:777-784
© 1997 The Society of Thoracic Surgeons

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Original Article: General Thoracic

Factors Influencing Long-Term Survival After Lung Metastasectomy

Unit of Thoracic Surgery and Centre d'Informatique Médicale, Geneva University Hospital, Geneva, Switzerland; and Department of Thoracic Surgery, Royal Brompton National Heart and Lung Hospital, London, Great Britain

Accepted for publication September 18, 1996.

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Background. Disease-free interval, histology of primary tumor, and number and size of metastases resected (at first metastasectomy) were studied after resection of pulmonary metastases.

Methods. Between 1980 and 1993, 276 consecutive patients underwent lung resections for curative removal of metastatic disease. At subsequent relapse, 63 patients had a second-stage metastasectomy, 12 went on to a third phase, and 2 patients had four stages.

Results. The primary tumor was sarcoma in 126 cases (46%), teratoma in 88 (32%), carcinoma in 53 (19%), melanoma in 5, and miscellaneous in 4. Actuarial survival was 69% at 2 years (95% confidence interval 62% to 74%), 48% at 5 years (40% to 55%), and 35% at 10 years (23% to 44%).

Conclusions. Survival was not related to disease-free interval. Multivariate analysis showed that nearly all predictive information can be obtained through histologic studies (p < 0.0001); inclusion of the number of metastases resected contributed to a lesser degree (p = 0.032). Short disease-free intervals, numerous lung metastases, or even deposits recurring after a first or second metastasectomy should not preclude patients from operation.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
For editorial comment, see page 611.

Expectations after the resection of lung metastases arose from anecdotal reports—Barney and Churchill's patient survived 23 years after the wedge resection of a hypernephroma lung metastasis [1]—but have gained considerable respectability since with survival figures that frequently surpass those achieved by operations for primary lung cancer [2]. Our understanding of how metastasectomies work and to whom they should (and should not) be applied is still incomplete, however, because published series are too small and follow-up intervals are too limited to allow irrefutable conclusions [3]. The present study is another contribution to the field of lung metastasectomy and is concerned with the identification of patients most likely to benefit from this procedure. We report our 14-year experience and use univariate and multivariate analyses to see which of the factors commonly addressed in the field of lung metastasectomy (disease-free interval, size and number of resected metastases) can be relied upon for predictiveness.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
This study covers the 14-year period from January 1980 to December 1993 and includes 276 patients who underwent lung metastasectomies on one or several occasions. The last follow-up was set at January 1, 1994. Excisions were performed by the senior author (P.G.) using a standard protocol throughout the study period.

Prerequisites for metastasectomy included: (1) Complete excision of all intrathoracic disease was considered feasible; and (2) reliable control of primary disease, usually (but not exclusively) by means of operation; if present, extrathoracic disease had to be removed operatively before lung metastasectomy. Occasionally, when metastases were in the upper abdomen or retroperitoneum, this could be done simultaneously, usually by means of a thoracolaparotomy.

The number of lung deposits did not exclude patients from metastasectomy (although referring oncologists were clearly less likely to refer patients with numerous deposits). In addition, tumor doubling time, cell type, and the free interval between treatment of the primary disease and the appearance of secondary tumor (see later) were not contraindications. Twenty-nine patients were excluded from the study: 16 appeared to have mediastinal metastases only; the chest wall was involved in 7 and the parietal pleura in 4. Finally, upon histologic examination of the resected specimens, 1 patient had a primary bronchoalveolar carcinoma and another had sarcoidosis. Screening for metastatic deposits relied on computed tomographic scanning using contiguous or overlapping cuts over the whole of both lung fields.

In the case of bilateral disease, median sternotomy was the preferred approach except in the following instances, in which staged lateral thoracotomies—usually 1 month apart—were used: (1) more than four metastases in each lung; (2) large deposits close to the hilum; (3) deposits in the lower lobe, particularly in posterior segments; and (4) consistency of deposits anticipated to be similar to that of lung tissue (as with synovial sarcomas, for instance).

The type of resection performed refers to the maximum resection needed in each case; for instance, those cases treated by wedge excision include only those in which all resections were accomplished by wedge excision. Wedge excisions encompassing the tumor with a surrounding cuff of 5 mm of normal lung were nearly always done by hand with a 3.0 Prolene (Ethicon, Somerville, NJ) suture running back and forth. Patients designated as having had a lobectomy may have had an additional wedge excision during the same procedure.

Survival curves were calculated according to Kaplan and Meier. When shown, confidence intervals are set at 95%. Comparison of survival curves was performed using the Mantel-Cox log rank test, or a trend test when three ordered categories were considered [4]. Categories were chosen to obtain subgroups of comparable sizes. Cox proportional hazards model was used to investigate simultaneously the effects of multiple factors on survival [5], without resorting to categorization for continuous variables (ie, free interval and number of metastases excised).

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Two hundred seventy-six patients underwent pulmonary resections for removal of metastatic disease with an intent for cure. There were 193 male and 83 female patients, with ages ranging from 5 to 78 years (mean, 38 years). The free interval ranged from 1 month to 27 years (median, 21 months; mean, 36 months). At subsequent relapse, 63 of these patients (23%) went on to have second-stage metastasectomy, 12 (4%) went on to a third phase, and 2 patients (1%) had four stages. The median interval was 13.7 months between the first and second metastasectomy (range, 2 months to 6.8 years) and 13.5 months between the second and third procedure (range, 8 months to 4.2 years). The 2 patients with four operations had the fourth 12 and 15 months, respectively, after the third.

The following data refer to the first metastasectomy. Pulmonary deposits were solitary in 118 instances (44%) and multiple in 148 (56%), and one-sided in 191 (69%) and bilateral in 85 (31%). In the cases of unilateral disease, the incision was a lateral thoracotomy (in 177) or a thoracolaparotomy in the presence of associated abdominal deposits (in 14). As for bilateral disease, the incision used was a median sternotomy (in 48) or staged lateral thoracotomies, usually 1 month apart (in 24); 13 patients had only the first stage of a planned bilateral thoracotomy, usually because of rapidly progressive disease.

Pulmonary resection was achieved by wedge excision in 184 (66%), segmentectomy in 13 (5%), lobectomy in 66 (24%), and pneumonectomy in 13 (5%).

The primary tumor was a sarcoma in 126 instances (46%), a teratoma in 88 (32%), a carcinoma in 53 (19%), a melanoma in 5, and miscellaneous in 4 (carcinoid in 2, lymphoma in 1, and neuroectodermal tumor in 1). The sarcomas included: osteosarcoma in 34, leiomyosarcoma in 18, synovial sarcoma in 13, malignant fibrous histiocytoma in 10, Ewing sarcoma in 9, liposarcoma in 6, rhabdomyosarcoma in 6, alveolar soft part sarcoma in 6, fibrosarcoma in 5, chondrosarcoma in 5, myxoid sarcoma in 2, malignant schwannoma in 2, clear cell sarcoma in 1, small cell sarcoma in 1, endometrial stroma sarcoma in 1, and no further description in 7. The carcinomas included: colon-rectum in 18, kidney-bladder in 17, gynecologic in 4, ear/nose/throat in 4, breast in 3, thymus in 2, thyroid in 2, adrenal in 1, liver in 1, and stomach in 1. Pulmonary deposits ranged from one to 23 per patient at the first procedure (median, two; mean, 3.6).

There were five early deaths after the first metastasectomy (1.8% mortality per patient), but none after the second, third, or fourth operations. Two patients died on the third postoperative day, one of cardiac arrest and the other of a tumor embolus in a cerebral artery; 1 on postoperative day 4 of pneumonia; 1 on postoperative day 10 of sepsis due to methicillin-resistant Staphylococcus aureus; and 1 on postoperative day 17 of sepsis and hemorrhage.

Twenty-nine patients (11%) were lost to follow-up before January 1, 1993. Median follow-up for all 166 surviving patients was 38 months (range, 3 weeks to 161 months), and 23 months for the 81 patients with sarcomas and carcinomas (range, 4 weeks to 141 months). Survival of the entire group (including early postoperative deaths) was 69% at 2 years (95% confidence interval, 62% to 74%), 48% at 5 years (40% to 55%), and 35% at 10 years (23% to 44%), as shown in Figure 1.

View larger version (13K): [in this window] [in a new window]   Fig 1. . Survival for the entire group. Vertical bars represent 95% confidence intervals; open circles are deceased patients; the numbers of patients at risk at 2-year intervals are given below.

View larger version (18K): [in this window] [in a new window]   Fig 2. . Survival in relation to histology.

View larger version (14K): [in this window] [in a new window]   Fig 3. . Survival in relation to sex.

View larger version (18K): [in this window] [in a new window]   Fig 4. . Survival in relation to disease-free interval from primary treatment to (first) metastasectomy.

View larger version (18K): [in this window] [in a new window]   Fig 5. . Survival according to the number of metastases excised at first metastasectomy.

View larger version (19K): [in this window] [in a new window]   Fig 6. . Survival according to the size of the largest metastasis excised at the first metastasectomy.

View larger version (17K): [in this window] [in a new window]   Fig 7. . Survival according to the type of excision performed at first metastasectomy. Wedge resections and segmentectomies were plotted against lobectomies and pneumonectomies to obtain samples of more comparable sizes.

View larger version (18K): [in this window] [in a new window]   Fig 8. . Survival after the first, second, and third metastasectomy.

Male patients fared better than female patients (p = 0.014), and this significant difference is undoubtedly due to the optimizing effect of teratomas, found exclusively in men (see Fig 3).

The free interval had no influence on outcome (trend test, p = 0.8; see Fig 4). The three periods considered (13, 14 to 32, and 33 months) were chosen to obtain subgroups of comparable sizes (the same applies to the number and size of resected metastases).

The number of metastases excised (one, two or three, four or more) did not appear to affect survival either (trend test, p = 0.51; see Fig 5). Similarly, the outcome of bilateral disease did not differ significantly from that of one-sided disease (p = 0.15). To determine whether a one-sided lateral thoracotomy (dictated by computed tomography) could result in missing contralateral disease, we analyzed the data of the 63 patients who underwent at least two metastasectomy procedures (excluding staged lateral thoracotomies). The initial approach was bilateral in 19 and one-sided in 44. The 19 patients whose first explorations were two-sided (sternotomies in 14 and staged lateral thoracotomies in 5) had a recurrence within a median interval of 14 months (range, 5 to 53 months), whereas in the group who had had unilateral thoracotomies, 25 had recurrence on the same side within a median interval of 14 months (range, 3 to 42 months) and 19 on the opposite side (median, 12 months; range, 3 to 89 months). Comparison of these figures showed that these three subgroups behaved similarly in terms of time to recurrence.

In contrast, there was a highly significant tendency for large metastases (plus those of undetermined size) to behave less favorably (p = 0.0004; see Fig 6), probably because most teratomas had small metastases. Finally, there was a significant trend for larger excisions to be associated with shorter survival times (p = 0.002; see Fig 7). Of course, the extent of excision could be dictated by factors that carried unfavorable influence by themselves, eg, a pneumonectomy for a hilar lesion.

Multivariate Analysis
Multivariate analysis was performed with the following variables: histology, sex, free interval, side of deposits (unilateral versus bilateral), number of metastases, and type of excision performed (Table 1). Size of the largest metastasis excised was not taken into account because it was not available in 46 patients and did not provide contributive information within each histologic category. It appears that most of the predictive information contained within the aforementioned data could be obtained by considering the histologic process. This information was improved slightly by adding the number of metastases excised (p = 0.032). The relative importance of the histologic process compared with the number of metastases appears in Table 2 and is expressed in terms of the hazard ratio. Furthermore, when considering only carcinomas and sarcomas, none of the preceding variables appeared to affect survival in a significant fashion.

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

Common sense would suggest that outcome is directly related to the duration of the disease-free interval [6], with death expected rapidly when the time elapsed between primary tumor and the appearance of lung metastases is short. This was confirmed in two large European series totaling nearly 700 patients. Considering a 6-month cutoff for the free interval, a Paris team found a drop from 30% to 14% in 5-year survival rates [7], whereas a Heidelberg group reported 52% and 27% survival rates when the free interval was set at 3 years or less and more than 3 years, respectively [8] (p < 0.01 in both series). Similar conclusions were reached in a smaller Japanese series with a free-interval cutoff at 1 year [9]. In another cancer group comprising 234 patients, median survival was proportional to the free interval, except for melanoma [10].

One should bear in mind, however, that spurious deductions (or first-kind errors) may be reached with the choice of single, occasionally arbitrary, cutoff values. In this respect, comparing several groups of free-interval periods of comparable sizes is certainly a more valid way to identify tendencies—if not significant trends—and may account for the opposite conclusions reached by the present study and by two American series [11, 12]. The latter two studies, published in the mid-1980s, were similar in histologic distribution and nearly as large as the French and German series combined. Close examination of yearly free-interval subgroups in these reports shows survival rates to vary erratically and leads one to infer that free intervals, for unknown reasons, should not be relied upon for prognosis.

Paradoxes also prevail when considering the number of resected pulmonary metastases. One would expect numerous deposits to behave less favorably than single ones [13, 14], as shown in the 1981 report from a cancer center in Buffalo [10]. This was shown to be the case for osteogenic and soft tissue sarcomas, for instance [15], and was confirmed in the present report (p = 0.032), which also showed that bilaterality of lesions was hardly more detrimental than one-sided disease (p = 0.11). However, several large series have noted comparable 5-year survival rates after excision of solitary and multiple metastases [3, 7–9, 16]. The exception to the rule may be for melanoma metastatic to the lung [17]. Based on a thorough multivariate analysis in 945 patients, a group from Duke University has recently decided to limit lung metastasectomy to patients with one or two nodules only, as three nodules or more were found to be associated with a dismal outcome [18].

Unlike the free interval and number of metastases, the size of lung metastases is seldom discussed, and when it is, its predictive value is usually dismissed [2, 8, 19]. The M.D. Anderson group did find a correlation, but for melanoma only [11], whereas a Japanese series of 100 cases found a significant 28% drop in 5-year survival rates with a 30-mm diameter cutoff [9]. In the Brompton experience and despite incomplete information in some cases, the size of the largest metastasis excised at first metastasectomy appeared highly predictive (p = 0.0004) when considering four subgroups of size (<10, 11 to 30, and >31 mm; and size missing). This finding is likely due to the fact that most teratomas had small metastases.

Opinions on the predictive influence of histologic findings converge on at least two points. (1) Melanoma metastatic to the lung carries an awful prognosis despite metastasectomy and adjuvant therapy. The median survival in a group of 17 patients barely exceeded 7 months [10]. These and other dismal figures explain why many centers, including Brompton [20], have become reluctant to perform lung metastasectomy in this subgroup. (2) At the opposite extreme, the outcome after excision of metastatic teratoma is excellent; the 10-year survival reached 72% in the present report. These cases obviously benefited from preoperative platinum-based chemotherapy [20], reported to sterilize lung metastases in up to 26% of cases [21] or to induce differentiation into tissues of benign appearance [22]. Such favorable transformations also occurred in the present series, with two thirds of the cases displaying either total necrosis (29%) or differentiation into tissues of benign appearance (38%) and one third having degeneration into predominantly undifferentiated tumor.

In our univariate analysis, the histologic process appeared highly predictive when all categories were considered (p < 0.0001), but remained a highly significant discriminator when we excluded melanomas and compared teratomas, sarcomas, and carcinomas together. Finally, no clear advantage seems to emerge when the matching is limited to sarcomas and carcinomas [8, 11, 12], the two subgroups that predominate in most reports [16] (some series include optimizing teratomas in the group of carcinomas with caval propagation [8]). The predominant role of histology is obvious in the present study; multivariate analysis showed that it outranked disease-free interval and size and number of resected metastases. Its predictive impact was improved slightly by adding the number of metastases excised.

In conclusion, actuarial survival in this series after the first metastasectomy was 50% at 5 years and 36% at 10 years. These results confirm the benefit of lung metastasectomy in selected cases and show that short disease-free intervals, numerous metastases, or even lung deposits recurring after metastasectomy are not contraindications for this procedure.

	Acknowledgments

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
We thank Joan and Marcel Robert and Robert Lemoine, MD, from the Department of Pathology of Geneva University Hospital.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Doctor Ambrogi was a Visiting Fellow from the Division of Thoracic Surgery, Tor Vergete University, Rome, Italy.

Address reprint requests to Dr Robert, Unité de Chirurgie Thoracique, Hôpital Cantonal Universitaire, CH-1211 Genève 14, Switzerland.

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Vincenzo Ambrogi Peter Goldstraw Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Robert, J. H. Articles by Goldstraw, P. Search for Related Content PubMed PubMed Citation Articles by Robert, J. H. Articles by Goldstraw, P. Related Collections Related Article