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Ann Thorac Surg 1995;60:1609-1611
© 1995 The Society of Thoracic Surgeons

Original Articles: General Thoracic

Successful Treatment of Solitary Extracranial Metastases From Non-Small Cell Lung Cancer

James D. Luketich, MD, Nael Martini, MD, Robert J. Ginsberg, MD, David Rigberg, MD, Michael E. Burt, MD, PhD

Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York

Accepted for publication July 27, 1995.


   Abstract
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 Footnotes
 Abstract
Introduction
 Methods and Results
 Comment
 References
 
Background. Recurrence after resection of non-small cell lung carcinoma is generally associated with a poor outcome and is treated with either systemic agents or palliative irradiation. Recently, long-term survival has been reported after resection of isolated brain metastases from non-small cell lung carcinoma, but resection of other metastatic sites has not been explored fully.

Methods. We have identified 14 patients who had solitary extracranial metastases treated aggressively after curative treatment of their non-small cell lung carcinoma. The histology was squamous carcinoma in 5, adenocarcinoma in 8, and large cell carcinoma in 1. Initially, 3 patients had stage I, 5 stage II, and 6 stage IIIa disease.

Results. The sites of metastases included extrathoracic lymph nodes (six), skeletal muscle (four), bone (three), and small bowel (one). The median disease-free interval before metastases was 19.5 months (range, 5 to 71 months). Complete surgical resection of the metastatic site was the treatment in 12 of 14 patients. Two patients received only curative irradiation to the metastatic site, with complete response. The overall 10-year actuarial survival (Kaplan-Meier) was 86%. To date, 11 patients are alive and well after treatment of their metastases (17 months to 13 years), 1 has recurrent disease, 1 died of recurrent widespread metastases, and 2 died of unrelated causes.

Conclusion. Long-term survival is possible after treatment of isolated metastases to various sites from non-small cell lung carcinoma, but patient selection is critical.


   Introduction
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 Abstract
 Introduction
Methods and Results
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The incidence of metastatic recurrence after resection of non-small cell lung cancer (NSCLC) is stage dependent and generally is associated with a poor outcome. Treatment with chemotherapy has only marginally improved survival [1, 2]. Radiation therapy has been used successfully to reduce local recurrence or as a palliative measure for local symptoms such as pain or bleeding. Recently, several reports have confirmed that long-term survival is possible after resection of isolated brain metastases from NSCLC [3–6]. Currently, data regarding resection of other solitary metastatic sites are sparse. The objective of this article is to report our experience with treatment of isolated, extracranial sites of metastases from NSCLC.


   Methods and Results
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 Abstract
 Introduction
 Methods and Results
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A retrospective review from 1983 to 1993 identified 14 patients with lung cancer treated at Memorial Sloan-Kettering Cancer Center who underwent definitive treatment of solitary extracranial metastases from their NSCLC. All patients had previously undergone complete resection of an NSCLC primary tumor and subsequently presented with a solitary site of metastasis. Only those patients who had a solitary extracranial, extraadrenal site of metastasis are included in this report.

All patients had undergone lobectomy and mediastinal lymph node dissection for their primary NSCLC. Histologic types included squamous, adenocarcinoma, and large cell; there were no bronchoalveolar variants. The solitary nature of the metastasis was confirmed by careful physical examination, brain computed tomography scan, chest computed tomography scan including the liver and adrenal glands, and bone scan. The characteristics of these patients at the time of resection of their NSCLC primary tumor are shown in Table 1Go.


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  		Table 1. . Characteristics of Patients With a Solitary Metachronous Metastasis at the Time of Curative Resection of Primary Non-Small Cell Lung Cancer
 
The median metachronous interval was 19.5 months (range, 5 to 71 months). The sites of metastases were extrathoracic lymph nodes (six), skeletal muscle (four), bone (three), and small bowel (one) (Fig 1Go). A histologic examination and comparison with the original NSCLC confirmed that these lesions were metastatic from the previously treated lung cancer. No correlation was present between cell type (ie, adenocarcinoma versus squamous) and location of metastases.



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  		Fig 1. . Sites of isolated extracranial metastases from non-small cell lung carcinoma.

 
Complete surgical resection of the isolated metastases was the primary treatment in 12 of 14 patients. Of these 12, 5 also received postoperative local irradiation to the metastatic site with or without cisplatinum-based chemotherapy (n = 2). Two patients were treated with curative radiation therapy to the metastatic site, with complete response. The overall 10-year actuarial survival was 86% (Fig 2Go). At a median follow-up of 101 months, 11 patients were alive and well after treatment of their metastases (5 months to 13 years). Ten patients had no evidence of locally recurrent disease or metastases, 1 was alive with recurrent disease, 1 had died of recurrent widespread metastases 12 months after resection of the original metastasis, and 2 died of unrelated causes.



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  		Fig 2. . Isolated M1 disease survival after resection of metastases of non-small cell lung carcinoma (NSCLC) (n = 14).

 

   Comment
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 Introduction
 Methods and Results
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References
 
Approximately 44% of patients with NSCLC present with disease apparently limited to the chest [7]. Of those undergoing a potentially curative resection, recurrence rates range from 25% to over 75%, depending upon the stage of disease at initial resection. The site of first recurrence is locoregional in about one third of patients and distant in two thirds. Most patients who have distant recurrent disease have multiple sites of metastases identified, and survival is measured in months despite chemotherapy [8–12]. In the minority, only a single site of metastasis is found. Recent reports of successful treatment of isolated brain metastases from NSCLC have been encouraging.

The Lung Cancer Study Group reported the brain as the sole site of first recurrence in 6.4% of patients after NSCLC resection, accounting for about 20% of all lung cancer recurrences [5]. This is the most frequent site of distant metastasis after complete resection of an NSCLC primary tumor. In nearly half of the patients who present with brain metastases, a solitary lesion is found [13]. If the patient is symptomatic and no treatment is given, median survival is 1 month. Corticosteroids and whole-brain irradiation often palliate symptoms, but survival is increased only modestly by 3 to 6 months [14].

In the presence of a well-controlled or completely resectable primary lung cancer and a negative extensive metastatic workup, surgical removal of a synchronous or metachronous, solitary brain metastasis has resulted in 5-year survival rates ranging from 10% to 30%. In a randomized trial, Patchell and associates [3] compared surgical resection plus radiotherapy with radiotherapy alone in 25 patients with single brain metastases from many primary sites, the majority from the lung. The surgery group lived longer (19 versus 9 months), had fewer recurrences of cancer in the brain, and had a better quality of life compared with radiotherapy alone. We recently reported the retrospective outcome of 185 patients undergoing resection of brain metastases from NSCLC at Memorial Sloan-Kettering Cancer Center [4]. The overall survival rates were as follows: 1 year, 55%; 2 years, 27%; 3 years, 18%; 5 years, 13%; and 10 years, 7%. Complete resection of the primary lung cancer was the major determinant of survival in patients undergoing resection of brain metastases. In two other retrospective reports, Macchiarini and associates [15] and Read and associates [6] studied 37 and 27 patients and found 5-year survival rates of 30% and 21%, respectively.

The adrenal gland is another frequent site of metastases from NSCLC. Autopsy data have shown that adrenal metastases occur in about one third of all patients dying of NSCLC. Routine abdominal computed tomography scans during staging of NSCLC revealed adrenal metastases in 5% to 10% of patients [16–18]. The incidence may be higher because computed tomography has a low sensitivity for detecting metastases in normal-sized glands [19, 21]. It has been generally believed that adrenal metastases preclude any further surgical intervention and are associated with a universally poor outcome. However, several case reports now exist showing that isolated adrenal metastases can be resected with occasional long-term survival [22–24]. We summarized our recent experience with 14 solitary adrenal metastases from NSCLC; 8 patients were treated surgically and 6 received only chemotherapy. Median survival in the surgical group was 22 months, compared with only 8.5 months in the chemotherapy group (p = 0.03) [25].

Only a few case reports have dealt with other sites of metastases from NSCLC [26]. This report summarizes our early experience with patients who have been treated for extracranial, extraadrenal metastases. Although the survival figures are impressive, it is important to recognize that this series represents a highly select group of patients. It is unclear why this group of tumors displayed such an indolent course compared with the typical patient with metastatic NSCLC. We were unable to find an association with survival and cell type or initial stage of disease. Based on our experience, three factors were important in selecting this group of patients for resection of isolated extracranial metastases: (1) The primary NSCLC was completely resected; (2) all patients enjoyed a disease-free interval (median 19.5 months) before metastases developed; and (3) an extensive metastatic and locoregional survey revealed only an isolated extrathoracic metastasis amenable to curative resection or radiotherapy. We are aware that the denominator is missing in this report. Based on our experience and that of others, approximately 7% of patients with metastatic disease from an NSCLC primary will have a solitary metastasis after full evaluation [27].

This retrospective review suggests that a more aggressive approach should be taken in treating patients with apparent solitary sites of metastasis from NSCLC after complete control of their primary site and a complete metastatic survey.


   Footnotes
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 Footnotes
Abstract
 Introduction
 Methods and Results
 Comment
 References
 
Address reprint requests to Dr Burt, Thoracic Surgery Service, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021.


   References
Top
 Footnotes
 Abstract
 Introduction
 Methods and Results
 Comment
 References
 

  1. Schaake-Koning C, Van Den Bogaert W, Dalesio O, et al. Effects of concomitant cisplatin and radiotherapy on inoperable non-small-cell lung cancer. N Engl J Med 1992;326: 524–30.[Abstract]
  2. Kojima A, Shinkai T, Eguchi K, et al. Analysis of three-year survivors among patients with advanced inoperable non-small cell lung cancer. Jpn J Clin Oncol 1991;214:276–81.
  3. Patchell RA, Tibbs PA, Walsh JW, et al. A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med 1990;322:494–500.[Abstract]
  4. Burt M, Wronski M, Arbit E, Galicich JH. Resection of brain metastasis from non-small cell lung carcinoma. J Thorac Cardiovasc Surg 1992;1033:399–411.
  5. Figlin RA, Piantadosi S, Feld R, Lung Cancer Study Group. Intracranial recurrence of carcinoma after complete surgical resection of stage I, II, and III non-small cell lung cancer. N Engl J Med 1988;318:1300–5.[Abstract]
  6. Read RC, Boop WC, Yoder G, Schaefer R. Management of non-small cell lung carcinoma with solitary brain metastasis. J Thorac Cardiovasc Surg 1989;98:884–91.[Abstract]
  7. Cancer patient survival, report no. 5. DHEW publication NIH 77-902. Bethesda, MD: Department of Health, Education, and Welfare, 1977.
  8. Ferguson MK. Diagnosing and staging non-small cell lung cancer. Hematol Oncol Clin North Am 1990;4:1053–68.[Medline]
  9. Stanley KE. Prognostic factors for survival in patients with inoperable lung cancer. J Natl Cancer Inst 1980;65:25–32.[Medline]
  10. Lanzotti VJ, Thomas DR, Boyle L, et al. Survival with inoperable lung cancer. Cancer 1977;39:303–13.[Medline]
  11. O'Connell JP, Kris MG, Gralla RJ, et al. Frequency and prognostic importance of pretreatment clinical characteristics in patients with advanced non-small cell lung cancer treated with combination chemotherapy. J Clin Oncol 1986;4:1604–14.[Abstract/Free Full Text]
  12. Bitran JD, Vokes EE. Chemotherapy for stage IV non-small cell lung cancer. Hematol Oncol Clin North Am 1990;4: 1159–68.[Medline]
  13. Delattre JY, Krol G, Thaler HT, Posner JB. Distribution of brain metastases. Arch Neurol 1988;45:741–4.[Abstract]
  14. Martini N. Rationale for surgical treatment of brain metastasis in non-small cell lung cancer. Ann Thorac Surg 1986;42:357–8.[Medline]
  15. Macchiarini P, Buonaguidi R, Hardin M, Mussi A, Angeletti CA. Results and prognostic factors of surgery in the management of non-small cell lung cancer with solitary brain metastasis. Cancer 1991;68:300–4.[Medline]
  16. Nielsen ME Jr, Heaston DK, Dunnick NR, Korobkin M. Preoperative CT evaluation of adrenal glands in non-small cell bronchogenic carcinoma. AJR 1982;139:317–20.[Abstract/Free Full Text]
  17. Burt ME, Heelan R, Coit D, et al. Prospective evaluation of unilateral adrenal masses in patients with operable non-small-cell lung cancer. Impact of magnetic resonance imaging. J Thorac Cardiovasc Surg 1994;107:584–8.[Abstract/Free Full Text]
  18. Sandler MA, Paerlberg JL, Madrazo BL, et al. Computed tomographic evaluation of the adrenal gland in the preoperative assessment of bronchogenic carcinoma. Radiology 1982;145:733–6.[Free Full Text]
  19. Allard P, Yankaskas BC, Fletcher RH, et al. Sensitivity and specificity of computed tomography for the detection of adrenal metastatic lesions among 91 autopsied lung cancer patients. Cancer 1990;66:457–62.[Medline]
  20. Ettinghausen SE, Burt ME. Prospective evaluation of unilateral adrenal masses in patient with operable non-small cell lung cancer. J Clin Oncol 1991;9:462–6.
  21. Oliver TW, Bernardino ME, Miller JI, et al. Isolated adrenal masses in non-small cell bronchogenic carcinoma. Radiology 1984;153:217–8.[Abstract/Free Full Text]
  22. Raviv G, Klein E, Yellin A, Schneebaum S, Ben-Ari G. Surgical treatment of solitary adrenal metastases from lung carcinoma. J Surg Oncol 1990;43:123–4.[Medline]
  23. Reyes L, Parvez Z, Nemoto T, Regal AM, Takita H. Adrenalectomy for adrenal metastasis from lung carcinoma. J Surg Oncol 1990;44:32–4.[Medline]
  24. Twomey P, Montgomery C, Clark O. Successful treatment of adrenal metastases from large-cell carcinoma of the lung. JAMA 1982;248:581–3.[Abstract]
  25. Luketich JD, Burt ME. Does resection of isolated adrenal metastases from non-small cell lung cancer (NSCLC) improve survival? [Abstract]. 7th World Conference on Lung Cancer, Colorado Springs, CO, June 26–July 1, 1994.
  26. Oka T, Ayabe H, Kawahara K, et al. Esophagectomy for metastatic carcinoma of the esophagus from lung cancer. Cancer 1993;71:2958–61.[Medline]
  27. Albain KS, Crowley JJ, LeBlanc M, Livingston RB. Survival determinants in extensive-stage non-small-cell lung cancer: the Southwest Oncology Group experience. J Clin Oncol 1991;9:1618–26.[Abstract]



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