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Original Articles: General Thoracic

Resection of Pulmonary Metastases From Sarcoma: Can Some Patients Benefit From a Less Invasive Approach?

^a Thoracic Department, Institut Mutualiste Montsouris, Paris
^b Pathology Department, Institut Mutualiste Montsouris, Paris
^c Institut Gustave Roussy, Villejuif, France

Accepted for publication September 16, 2008.

^_* Address correspondence to Dr Gossot, Thoracic Department, Institut Mutualiste Montsouris, 42 Bd Jourdan, Paris, F-75014, France (Email: dominique.gossot{at}imm.fr).

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
Background: Although video-assisted metastasectomy has been proposed for some solitary metastases, its value has not been investigated in patients with pulmonary metastases from sarcoma for which open resection remains the usual approach.

Methods: In all, 113 consecutive patients underwent curatively intended lung resection for metastases from sarcomas. Of these 113 patients, 31 were selected for a thoracoscopic wedge resection (group TS). These patients were compared with 29 patients operated on by thoracotomy but whose features could have made them possible candidates for a thoracoscopic resection (group TT). Follow-up was complete for all patients (mean follow-up, 34 months).

Results: No mortality occurred. No morbidity was observed in group TT, and 1 complication occurred in group TS. The mean postoperative hospital stay was 3.7 days for group TS and 6.2 days for group TT (p < 0.0001). Overall survival rates at 1, 3, and 5 years were, respectively, 87.4%, 70.9%, and 52.5% in group TS, and 82.3%, 63.6%, and 34% in group TT (p = 0.20). Disease-free survival rates at 1 and 3 years were, respectively, 50.5% and 26.4% in group TS and 60% and 24.8% in group TT (p = 0.74). Local recurrence occurred in 1 patient in each group. Survival without a homolateral recurrence (i.e., in the operated lung) at 1 and 3 years was 66.7% and 44.4% in group TS and 83.5% and 45% in group TT, respectively (p = 0.54).

Conclusions: In selected patients with a maximum of two pulmonary nodules, thoracoscopic resections yield survival rates similar to open resections while being less invasive and preserving the patient's ability to undergo possible repeat operations.

	Introduction

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The lungs are the most common sites of metastatic sarcoma. Pulmonary resection (PR), alone or combined with anthracycline-based chemotherapy, has been proven beneficial for a subgroup of patients with isolated and resectable pulmonary metastases (PM) [1]. As most of these patients are young and have no respiratory disorders, the morbidity of PR is low, and the average 5-year survival rate is between 20% and 40%, depending on the pathologic type, the number of PM, and the disease-free interval before developing PM [2, 3]. This survival rate exceeds that obtained with chemotherapy alone or when surgery is unfeasible [1, 2]. This has prompted surgeons to attempt an aggressive surgical approach in these patients.

Over the past years, surgery for sarcoma, especially those of extremities, has attempted to be less invasive by avoiding amputation and using conservative treatments. Meanwhile, surgical management of pulmonary metastatic disease consisted of an open metastasectomy, through either a thoracotomy or sternotomy and even a clamshell incision [2]. This attitude is based on the principle that an efficient PR should be as radical as possible, namely, any pulmonary lesion should be removed, even if it is tiny and undetectable by currently available imaging methods. However, a less invasive approach could be considered taking into account the following characteristics of these patients: (1) at least 40% of patients operated on for PM from sarcoma will relapse in the lung [4]; (2) many of these patients will be reoperated on, undergoing an average of two operations per patient [5]; and (3) resectability of PM decreases in proportion to the number of thoracotomies, and consequently, some patients end up abandoning surgery after two to three reoperations, and even in case of a single relapse. Thus, obviating a thoracotomy and its consequences at the time of the first PR may deserve consideration for a subgroup of patients.

Bearing this in mind, for selected patients, we have gradually shifted from a "classic" approach (through thoracotomy), to its less invasive counterpart (through thoracoscopy), whenever possible. To evaluate whether a less invasive approach is advisable for some patients, we compared the perioperative course and survival rate of supposedly similar patients who underwent PR by thoracoscopy (TS) or thoracotomy (TT).

	Material and Methods

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Patient Selection
From January 2000 to July 2007, 113 consecutive patients underwent curatively intended lung resection for metastatic disease from sarcomas. Patients were selected for surgery if there was no recurrence at the primary site, no other metastastic sites, if all the detected pulmonary nodules were resectable without major functional compromise, and if they had increased in size but not in number during a surveillance period of at least 2 months. Among these 113 patients, we retrospectively identified 60 patients who shared the following characteristics: number of nodules two or fewer per lung field, maximal nodule diameter 30 mm or less, wedge resections feasible, and no mediastinal or chest wall involvement.

Because the study was retrospective and the patients were anonymous, no consent was requested. The study was approved by the Institutional Review Board at the Institut Gustave Roussy. Among the 60 patients, 31 had undergone at least one PR by thoracoscopy (group TS), and 29 patients had undergone a PR by thoracotomy alone (group TT). Patient characteristics and the histologic type of the primary tumor are summarized in Table 1. Both groups were similar in terms of age, sex ratio, and histologic type of the primary tumor (Table 1). There was no statistical difference in the profile of resected nodules, except for the largest diameter, which was greater in group TT (p < 0.05; Table 2). The choice of technique—open versus thoracoscopic—was mainly dependent on the location of the nodule (deep or subpleural) and on the surgeon's preference. At the beginning, some surgeons felt more confident with thoracotomy and applied the rule that metastasis from sarcoma had to be approached through thoracotomy. Gradually, considering the better postoperative course and results, more patients were selected for a thoracoscopic approach. This is a bias in the present study.

Data Collection
Hospital records were reviewed retrospectively for patient demographic characteristics, preoperative status, and intraoperative and postoperative course. Follow-up information was obtained by correspondence or telephone interview of the patient, the patient's relatives, or the referring physician. Follow-up was complete for all the patients with a mean of 34 months (95% CI: 27 to 41). A local recurrence was defined as a tumor relapse at the staples site.

Statistical Analysis
Statistical analysis was done using GraphPad Prism 4 statistical software (GraphPad Software, San Diego, CA). Continuous variables were expressed as means and the 95% confidence interval (CI) of the mean (95% CI) or range. Categorical variables were expressed as percentages. The Mann-Whitney U test and Fisher exact test were used to compare continuous and categorical variables, respectively. Survival data were analyzed with standard Kaplan-Meier techniques to estimate survival probabilities and expressed with the corresponding 95% CI. The log rank test was used to compare survival curves. Survival was calculated from the date of the first thoracoscopy or from the date of the first thoracotomy to the last follow-up in the TS and TT group, respectively. Disease-related deaths were treated as an endpoint for survival. All other deaths unrelated to sarcoma or its treatment were treated as censored observations.

Finally, to compare recurrence in an operated lung field—named homolateral recurrence—between the two groups, we considered each lung field as an independent unit. Thus, a period free of recurrence was calculated from the date of the initial resection from a lung field to the date of recurrence in the same lung field or the last follow-up.

	Results

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The 31 patients in group TS had a total of 63 operations, 42 by thoracoscopy and 21 by thoracotomy. Staged bilateral resections were performed within less than a month in 11 patients (35%): in 7 patients, one side was treated by thoracoscopy and the other side by thoracotomy; and 4 patients underwent bilateral thoracoscopy. A total of 11 patients in group TS also had at least one resection performed by thoracotomy: in 7 patients before, and in 4 patients after, their thoracoscopic operation. The reason was a contraindication to a thoracoscopic approach because of either a large diameter or the location.

Repeat resections (unilateral or bilateral at more than a month apart) were performed in 36% of patients in group TS. The 29 patients in group TT underwent a total of 60 thoracotomies. Staged bilateral resections were performed within less than a month in 12 patients (41%). Repeat resections were performed in 41% of patients in group TT (Table 2). No mortality occurred. All resection margins were tumor free at frozen section examination and at final pathologic examination. No morbidity was observed in group TT. One patient from group TS, operated on in a context of chemotherapy-induced thrombocytopenia, was readmitted 1 week after discharge for hemopneumothorax. He was managed conservatively by drainage and intrapleural thrombolysis. The mean chest drain duration (Fig 1) was 1.5 days (95% CI: 1.2 to 1.8) in group TS and 3 days (95% CI: 2.5 to 3.5) in group TT (p < 0.0001). The mean postoperative hospital stay (Fig 1) was 3.7 days (95% CI: 3.1 to 4.2) in group TS and 6.2 days (95% CI: 5.5 to 6.8) in group B (p < 0.0001).

View larger version (18K): [in this window] [in a new window]   Fig 1. Mean chest tube duration and postoperative hospital stay in the thoracoscopy (TS) group and thoracotomy (TT) group. ***p < 0.0001. (Solid bar = chest tubes TS; open bar = chest tubes TT; hatched bar = hospital stay TS; shaded bar = hospital stay TT.)

View larger version (11K): [in this window] [in a new window]   Fig 2. Overall survival rate with the number of patients at risk in the thoracoscopy (TS) group (solid line) and thoracotomy (TT) group (dashed line [p = 0.20]).

View larger version (9K): [in this window] [in a new window]   Fig 3. Disease-free survival rate after the initial pulmonary metastasis resection in the thoracoscopy group (solid line) and the thoracotomy group (dashed line [p = 0.74]).

View larger version (9K): [in this window] [in a new window]   Fig 4. Homolateral pulmonary recurrence-free survival rate in the thoracoscopy group (solid line) and the thoracotomy group (dashed line [p = 0.54]).

	Comment

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However, very few authors have so far recommended a thoracoscopic approach for PM from sarcoma. In three recent series, all patients were operated on by thoracotomy or sternotomy whatever the number of lesions [12–14]. Some authors have suggested that a thoracoscopic approach could be a valid option, but only in patients with a solitary lesion that is resected for diagnostic purposes. If the metastatic nature of the lesion is confirmed, then thoracoscopy should be followed by thoracotomy [15, 16].

The main reason for preferring an open approach is the fear of overlooking a small lesion and the belief that manual palpation of the lung is better than computed tomography (CT) scan. This concern is particularly true of some metastases from sarcoma that are difficult to individualize, even by thorough digital examination [17]. Kayton and colleagues [17] analyzed 54 thoracotomies for suspected PM from sarcoma. All patients had a CT performed at a median of 20 days before surgery. They found that in 35% of thoracotomies the number of pathologically proven, viable, or nonviable metastases was underestimated by CT. In addition, half of the pulmonary lesions were located 5 mm or further below the pleural surface, meaning that they would not have been detected by thoracoscopy. They concluded that only thoracotomy with manual palpation was advisable in these patients.

In a smaller series of 17 patients, Mutsaerts and colleagues [10] confirmed that in patients who underwent resection for PM by TS, confirmatory TT found residual lesions that were missed during TS. However, in patients with only one lesion detected on preoperative CT, confirmatory TT did not find additional nodules. They advocated TS for a radiologically solitary metastasis. Similar conclusions were reached by Ludwig and colleagues [18], who compared the number of PM found on preoperative CT and at thoracotomy in 276 patients. In their series, patients with suspected PM had fewer lesions than expected preoperatively in 38% and more than expected in 25%. For patients with a single nodule on preoperative CT, only 7% had more than one metastasis, whereas 16% had no evidence of metastasis at the final pathologic examination. The authors concluded that for patients with a solitary nodule on preoperative CT, TS could be recommended.

There is no doubt that, even with the use of high performance helical CT, open surgical exploration can detect skipped nodules. That is the main argument put forward by the prothoracotomy surgeons, but there is no evidence that the excision of these digitally detected micronodules results in a demonstrated benefit in terms of life expectancy [19]. One cannot assert that removing a 1- to 2-mm PM (which could be detected by the surgeon's fingers) results in a survival gain, whereas overlooking a 0.5-mm nodule (which cannot be detected by the surgeon's fingers) has no consequence. The belief that a pulmonary metastasectomy by thoracotomy can always guarantee a complete resection is not supported by pathologic examinations. Shiono and colleagues [20] studied 96 specimens of wedge resections for PM. They found lesions exhibiting 10 or more cancer cell clusters remote from the main tumor in 19% of the cases. They also demonstrated that micrometastases, vascular spread, and lymphatic spread were present in 22%, 43%, and 31% of the specimens, respectively. Patients with cell clusters had a significantly higher risk of local recurrence.

Another reason for preferring TT over TS might be that lymphadenectomy—when associated with metastasectomy—is easier to perform through TT. However, sarcomas are seldom associated with lymph node metastases [21]. To our knowledge, only the series of PM reported by Pfannschmidt and colleagues [22] included a systematic hilar and mediastinal dissection. In their series of 69 PR for metastases from sarcoma, mediastinal lymphatic involvement was found in 10% of cases. However, in the most recent series of PR for PM from sarcoma, there is no mention of lymphadenectomy as part of the operation [12, 13, 15, 23], and nodal involvement was not investigated as a factor influencing the prognosis [23]. Lymph node dissection provides information on staging, but there is no evidence that this has any clinical impact. In two recent series, none of the patients with PM and mediastinal lymphatic spread survived more than 5 years [24, 25]. In the case of sarcoma, the discovery of mediastinal lymph node metastasis will probably not change the medical management of these lesions.

Similar homolateral recurrence rates were obtained in our series for patients treated by thoracoscopic or open resections. With similar disease-free survival rates after these two procedures, it could be contended that thoracoscopy does not result in higher recurrence rates than thoracotomy in these selected patients.

The last argument for preferring a TS approach in patients with a single lesion is preserving the ability to undergo repeat operations in patients who are highly likely to relapse in the lung. In the series by Bricoli and colleagues [4] including 267 patients with PM from sarcoma, 94 (35%) required pulmonary reoperation. It is now admitted from the results of several series of repeat resections that acceptable survival rates can be obtained by reoperations: 22.6% at 5 years for Harting and colleagues [12] and 36% at 5 years for Weiser and associates [13], and 31% at 3 years for Liebl and colleagues [26]. Thus, when reoperation combined with chemotherapy is technically feasible and does not compromise respiratory function, it should be attempted [4]. However, the more rethoracotomies are performed, the more complications are likely to occur, including pulmonary tears, pleural hemorrhage, and impairment of pulmonary function. In addition, a complete and extensive examination of the pulmonary parenchyma is usually impossible after the third homolateral operation. On the other hand, it is admitted that a thoracoscopic wedge resection results in far fewer pleural adhesions and does not complicate a potential reoperation by thoracotomy [18]. In addition, as demonstrated by the significantly shorter drainage duration and hospital stay in our series (Fig 4), TS is better tolerated. In our series, the mean duration of stay after TS was significantly shorter than after TT (Fig. 1). Other authors have mentioned the benefit of TS for lung nodule resection in terms of hospital stay [7, 8]. Although shortening the hospital stay is not a goal per se in patients suffering from a severe and potentially life-threatening disease, this short stay is an indicator of low morbidity and of better tolerance than TT. That should be taken into account for patients who experience aggressive and sometimes disabling treatments. In the series by Harting and colleagues [12], more than 10% of the patients did not undergo PR because they refused surgery.

In conclusion, although open resection through thoracotomy remains the standard approach for most patients presenting with PM from sarcoma, our series supports a less invasive approach for selected patients fulfilling the following criteria: two or fewer nodules, and subpleural nodules that are suitable for a thoracoscopic resection, which means that free margins can be obtained. In our series, the survival rate of these patients is comparable to that of patients operated on through thoracotomy and to other published data (Table 3). If confirmed by other studies, this attitude would be beneficial for patients who undergo several invasive treatments and are candidates for repeat pulmonary resections.

	Acknowledgments

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The authors thank Lorna Saint Ange (Institut Gustave Roussy) for editing the manuscript. Members of the Comité de Pathologie Thoracique at Institut Gustave Roussy, including Drs C. Le Pechoux, B. Besse and D. Grunenwald, participated in the treatment of some patients of the series.

	References

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This Article Abstract Full Text (PDF) 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): Dominique Gossot Costin Radu Mohamed Sadok Boudaya Pierre Magdeleinat Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gossot, D. Articles by Magdeleinat, P. Search for Related Content PubMed PubMed Citation Articles by Gossot, D. Articles by Magdeleinat, P. Related Collections Lung - other Related Article