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Ann Thorac Surg 1996;62:213-216
© 1996 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Role of Video-Assisted Thoracic Surgery in the Treatment of Pulmonary Metastases: Results of a Prospective Trial

Patricia M. McCormack, MD, Manjit S. Bains, MD, Colin B. Begg, PhD, Michael E. Burt, MD, PhD, Robert J. Downey, MD, David M. Panicek, MD, Valerie W. Rusch, MD, Maureen Zakowski, MD, Robert J. Ginsberg, MD

Departments of Diagnostic Radiologya, Pathologyb, Epidemiology & Biostatisticsc, and Thoracic Surgeryd, Memorial Sloan-Kettering Cancer Center, New York, New York USA


    Abstract
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Background. A retrospective review revealed a 42% error rate between computed tomographic scan reports and thoracotomy findings; therefore, a prospective study was designed to compare the value of computed tomographic scans, video-assisted thoracoscopic exploration, and open thoracotomy in the management of pulmonary metastases.

Methods. Eligibility included any patient with only one or two ipsilateral pulmonary metastases identified on computed tomographic scan who was being considered for surgical resection. Initially video-assisted thoracic surgery was performed and all lesions identified were resected. A thoracotomy adequate for complete lung palpation was then carried out and any additional lesions found were removed.

Results. Eighteen patients of a planned 50 were treated before closure of the study. Four patients (22%) had no additional lesions found at thoracotomy. The primary sites of tumor were colon (10), breast (3), and one patient each skin (squamous), cervix, kidney, melanoma, and sarcoma. Four patients (22%) did have additional lesions at thoracotomy, which were benign. In the remaining 10 patients (56%) additional malignant lesions were found at thoracotomy after video-assisted thoracoscopic exploration. After 18 patients were entered, analysis of the early results disclosed a 56% failure rate of a computed tomographic scan and video-assisted thoracic surgery to detect all lesions. Being within the 95% confidence interval (32% to 78%), the study was abandoned.

Conclusions. We conclude that video-assisted thoracic surgery should be used only as a diagnostic tool in managing lung metastasis. A thoracotomy is required to achieve complete resection, which is the major survival prognosticator for satisfactory long-term results.


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See also page 216.

Pulmonary metastases, when found as the only site of metastatic disease in patients where the primary tumor has been controlled, are often best treated by metastasectomy. The most consistent prognostic factor predicting survival has been complete surgical removal of all metastatic foci.

When video-assisted thoracic surgery (VATS) was introduced, it was quickly adapted to metastasectomy. Concern was expressed by us that identification of all metastatic tumors to the lung might not be possible when the VATS technique is used, as manual palpation of the entire collapsed lung has been deemed essential. The use of a probe, or single digit might not suffice as a substitute for the surgeon's hand [1].

Because the estimation of the number and location of metastases and planned operation is based on computed tomographic (CT) scan images, initially we retrospectively compared the radiologic findings with the surgical findings of 72 patients with primary colon cancer metastatic to lung [1]. Computed tomographic scans underestimated surgical findings in 42% (30 of 72 patients). In those with one or two lesions on the CT scan the "missed lesion rate" was 28%. To validate this retrospective review a prospective study was initiated to determine the accuracy of CT scan and video-assisted surgery as compared to open thoracotomy in identifying metastatic lesions in patients with no more than two presumed pulmonary metastases, believing that these would be the patients eligible for a VATS approach.


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Any patient who fit the general eligibility criteria for operation for lung metastases, and whose CT scan showed no more than two lesions in one lung was eligible. The selection criteria for metastasectomy are primary tumor under control; no tumor sites outside the lungs; CT scan demonstrates complete resectability; no better proven method of treatment is available; and medical condition allows planned resection. The prospective study was approved by the IRB (93-42) and informed consent was obtained from every patient.

Operative decisions made by each surgeon were based on scans carried out no more than 3 weeks before the planned operation. The official radiologic report, consultation with radiology staff, and personal review of all imaging material by the surgeon were used for preoperative planning. All CT scans were performed with current generation scanners. Only two scans were obtained helically. Computed tomographic scans more than 3 weeks old or judged unreadable were repeated. The scans were reviewed subsequently by a single member of the Radiology Staff (D.M.P.). A data form was used to record the number and locations of all suspected lung nodules seen on lung windows. The degree of confidence in findings was graded on a 5-point scale (0 = normal; 1 = probably normal; 2 = indeterminate; 3 = probably abnormal; 4 = abnormal).

Initially thoracoscopy was performed. Any lesion identified was resected using standard VATS techniques and instrumentation. Finger palpation and solid probes attempted to identify other nodules. Ultrasonography was not used. Under the same anesthetic a formal thoracotomy was then carried out to allow the surgeon to palpate the entire lung and resect any additional lesions found.

All resected specimens were reviewed by one pathologist (M.Z.) and were confirmed to have been completely resected before closure.


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There was no mortality or morbidity in this group of patients and the average postoperative stay was 4.5 days. This was before "same-day admission" policy was in use. Eighteen patients were treated in this fashion before concluding the study.

The primary sites were colon in 10 patients, breast in 3, squamous carcinoma of skin, leiomyosarcoma of uterus, cervix, kidney and melanoma were one patient each. In 14 patients, one lesion was noted on CT scan, and in 4 others, two lesions.

In 15 patients, all nodules noted on preoperative scans were located at thoracoscopy. In 2 patients with a single lesion on the CT scan, no lesions were identified at the video-assisted procedure. In a third patient only one of two lesions was found and removed at thoracoscopy. All three "missing" lesions were ultimately found and removed at thoracotomy. They were not detectable at VATS because of their deep location and technical problems related to pleural adhesions.

Only 22% of patients (4 of 18) had no new lesions found. In 22% (4 of 18) additional benign lesions were found at thoracotomy. In 56% of patients (10 of 18) additional malignant tumors were identified at thoracotomy (Fig 1Go). In only 1 patient was an additional lesion found at VATS.



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Fig 1. . Results of pilot study in 18 patients.

 
Of the 14 patients with solitary lesions on CT scan, 7 had additional malignant lesions found (14 nodules). In 3 additional patients five nodules were identified that were benign.

In only 8 of 18 patients identified preoperatively as having no more than two ipsilateral lesions was the CT scan correct and confirmed by VATS.

In two of the four "two-lesion" patients, only one lesion was found at thoracoscopy. The second malignancy was located at thoracotomy in both patients, one of which had three additional benign lesions discovered. In the other 2 patients both lesions were removed at VATS, but in both additional malignancies were identified and removed at thoracotomy (Table 1Go).


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Table 1. . Results of Study
 
In the single cases with skin, cervix, sarcoma and melanoma primaries, no additional malignant lesions were found at thoracotomy.

Twelve of the CT scans were available for retrospective review (Table 2Go). In 7 of these (58%) our results show a misread, 3 overread, and 4 underread.


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Table 2. . Retrospective Analysis of Computed Tomographic Scans (12 Scans)
 

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Pulmonary metastasectomy was first reported in the Scandinavian literature by Divis in 1927 [2] and subsequently in North America by Barney and Churchill in 1939 [3]. However, by 1960, 264 cases of successful resection with long-term survival were reported [4]. In 1971 Martini and colleagues reported 29% 5-year survival rates in osteogenic sarcoma patients where none had survived 3 years before metastasectomy was begun [5, 6]. Multiple nodules were resected and multiple thoracotomies were required to achieve these results.

Resection of pulmonary metastases is now the recognized standard of care for selected patients who meet specific criteria. Thoracotomy has been proven to be exceedingly safe with minimal morbidity and mortality [7]. Advanced surgical techniques, first median sternotomy [8] and later the clamshell incision [9] have also made bilateral resections at one operation a safe and efficient approach. This study was designed to compare VATS versus thoracotomy, which is best done with the lateral incision. Therefore, all these patients had thoracotomies. It is our practice to use the median sternotomy and clamshell approach when we are concerned about bilaterality. In sarcoma, with a solitary lesion, we do not explore both lungs.

Video-assisted thoracic surgery was introduced as an approach offering a less painful incision, and a shorter hospital stay. It was quickly applied to the treatment of lung metastases [10]. Our initial retrospective study identified the potential problems of missing small metastatic lesions, resulting in the institution of this present prospective study.

The prognostic significance of several variables in the presentation of these patients has been analyzed to improve the selection of potentially curable patients and avoid operation when it would not help the patient. These variables include length of tumor doubling time and disease-free interval, number of metastases, site of the primary tumor, and completeness of the pulmonary resection. All variables have had inconsistent prognostic significance except one: complete resection of all metastatic lesions [7].

After analyzing the results of the first 18 of a proposed 50-patient study, this protocol was closed to accrual because the estimated probability that cancer will be missed if VATS alone is used is 56% (95% confidence interval, 27% to 75%), and was sufficiently high to warrant termination of the study. Even for patients with only one lesion detected on CT the error rate is estimated to be 50% (95% confidence interval, 23% to 77%).

The results of this prospective study are somewhat surprising but do confirm our retrospective analysis-that in patients with solitary metastases and even more with two metastases-thoracotomy will frequently identify more malignant lesions. Our ability to identify these lesions with a VATS approach alone was less than satisfactory.

It is unlikely that the higher accuracy found in the sites other than colorectal, breast, and kidney reflect anything but a sampling error.

In this study CT scans were used from a wide variety of referring facilities and represents current clinical practice. It was not practical, due to cost and scheduling, to re-scan each patient with our own helical scanner. We acknowledge that this approach may underestimate the accuracy of CT that can be achieved by consistent, optimized CT technique and a dedicated radiologist comparing old films. It was the only pragmatic solution in our practice climate. In a prospective study of 39 patients, Remy-Jardin and colleagues [11] found 42% more nodules on helical CT scans as compared to conventional scanners. Increased identification of smaller nodules, however, lessens their specificity for being cancers [12]. Retrospective analysis as part of a study favors overreading and our results show a misread in the 7 of 12 patients we analyzed (58%) (Table 2Go).

In conclusion, we firmly believe that metastasectomy has a proven efficacy in treating these stage IV patients with 5-year survival rates in our hands shown to be 80% in testicular primary, 50% in colon or breast, 60% in renal, 40% in osteosarcoma, 25% in soft tissue sarcoma and melanoma primary sites. Patients should be offered operation as an option when they fit the selection criteria.

Therefore, we have concluded that the CT scan is not accurate in detecting all pulmonary metastases. The VATS technique as now practiced will fail to detect and remove all pulmonary metastases. Manual palpation of the lung is still required to locate all metastatic foci. Video-assisted thoracic surgery should be used for diagnosis only in metastasectomy. Until newer imaging and localization techniques allow a greater accuracy for the VATS approach, thoracotomy and manual palpation must remain the gold standard in treating even solitary pulmonary metastases.


    Footnotes
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Presented at the Thirty-second Annual Meeting of The Society of Thoracic Surgeons, Orlando, FL, January 29–31, 1996.

Address reprint requests to Dr McCormack, 1275 York Ave, New York, NY 10021.


    References
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 Abstract
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 Material and Methods
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 Comment
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  1. McCormack PM, Ginsberg KB, Bains MS, et al. Accuracy of lung imaging in metastases with implications for the role of thoracoscopy. Ann Thorac Surg 1993;56:863–7.[Abstract]
  2. Divis G. Einbertrag zur operativen, behandlung der lungengschuuilste. Acta Chir Scand 1927;62:329.
  3. Barney JD, Churchill ET. Adenocarcinoma of the kidney with metastasis to the lung cured by nephrectomy and lobectomy. J Urol 1939;42:269–76.
  4. Gliedman M, Horowitz S, Lewis FJ. Lung resection for metastatic cancer. Surgery 1957;42:521–32.
  5. Marcove RC, Mike V, Hajek JV, et al. Osteogenic sarcoma under the age of 21: a review of 145 operative cases. J Bone Joint Surg (Am) 1970;51:411–21.
  6. Martini N, Huvos AG, Mike V, et al. Multiple pulmonary resections in the treatment of osteogenic sarcoma. Ann Thorac Surg 1971;12:271–80.
  7. McCormack PM, Martini N. A current view of surgical management of pulmonary metastases. In: Economou SAu: need initial, ed. Adjuncts to cancer therapy. Philadelphia: Lea & Febiger, 1991:246–52.
  8. Johnston MR. Median sternotomy for resection of pulmonary metastases. J Thorac Cardiovasc Surg 1983;85:516–22.[Abstract]
  9. Bains MS, Ginsberg RJ, Jones WG III, et al. The clamshell incision: an improved approach to bilateral pulmonary and mediastinal tumor. Ann Thorac Surg 1994;58:30–3.[Abstract]
  10. Landreneau RJ, Hazelrigg SR, Ferson PF, et al. Thoracoscopic resection of 85 pulmonary lesions. Ann Thorac Surg 1992;54:415–9.[Abstract]
  11. Remy-Jardin M, Remy J, Giraud F, Marquette C-H. Pulmonary nodules: detection with thick-section spiral CT versus conventional CT. Radiology 1993;187:513–20.[Abstract/Free Full Text]
  12. Chang AE, Schaner EG, Conkle DM, Flye MW, Dappman JL, Rosenberg SA. Evaluation of computed tomography in the detection of pulmonary metastases: a prospective study. Cancer 1994;43:913–6.



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Patricia M. McCormack
Manjit S. Bains
Michael E. Burt
Valerie W. Rusch
Robert J. Ginsberg
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