Renal Cell Carcinoma: Resection of Solitary and Multiple Metastases Helen W. Pogrebniak, MD, Gabe Haas, MD, W. Marston Linehan, MD, Steven A. Rosenberg, MD, PhD, and Harvey I. Pass, MD Thoracic Oncology Section, Urologic Oncology Section, and Surgery Branch, National Cancer Institute, National Institutes of Health, Bethesda, Maryland

Between 1985 and 1991, 23 patients underwent resection of pulmonary metastases from renal cell carcinoma, of whom 18 had previously received interleukin-2 based immunotherapies. Mean survival from exploration in all patients was 43 months. Survival after resection did not correlate with the number of nodules on preoperative tomograms, the number of nodules resected, or the disease-free interval. Patients who underwent complete resection of metastatic disease (n = 15), however, had a

significantly longer survival (mean, 49 months; median not yet achieved) compared with patients with incomplete resection (median, 16 months) (pa = 0.02). Two of the 15 patients who underwent curative resections are presently free of disease greater than 45 months after exploration. These data support surgical resection of isolated pulmonary metastatic disease from renal cell cancer. (Ann Thorac Surg 1992;54:33-8)

I

efficacy of interleukin-2 based immunotherapies. During that time, 23 patients underwent 28 resections for pulmonary metastases from renal cell cancer and are the subject of this review. Follow-up data are available on all 23 patients, with a median potential follow-up of 32 months. Ages ranged from 37 to 70 years with a median of 54 years. There were 17 male and 6 female patients, and all patients were determined to have the clear cell variant of renal cell cancer as analyzed by the Surgical Pathology Section of the National Cancer Institute. The majority of patients were asymptomatic with pulmonary nodules detected by routine roentgenographic screening for extrarenal metastases. The 4 symptomatic patients complained of hemoptysis (n = 2) and chest wall pain (n = 2). All patients had extensive preoperative staging before attempted resection including chest roentgenograms, thoracic computed tomography or full-lung linear tomograms, computed tomography of the head and abdomen, and radionuclide bone scans. Exploration was undertaken with curative intent in 17 patients. In these patients the primary tumor was controlled, extrapulmonary metastases were absent, and the amount of lung tissue remaining would provide the patients with sufficient pulmonary parenchymal reserve. The indications for exploration in the other 6 patients included palliation of hemoptysis (l), diagnosis (l),treatment with photodynamic therapy under the auspices of a phase I trial at the Surgery Branch of the National Cancer Institute/NIH (l), and procurement of tumor-infiltrating lymphocytes (3).

t is only recently that the selective use of the resection of pulmonary metastases in patients with favorable histologies has been generally accepted to prolong survival. Barney and Churchill [l]in 1939 were the first to demonstrate the value of resecting a pulmonary metastasis in a patient with renal cell cancer. That patient survived 23 years after lobectomy and ultimately died of coronary artery disease [2]. This anecdotal success prompted others to consider more aggressively the resection of metastatic pulmonary lesions, chiefly osteogenic sarcoma [3] and soft tissue sarcoma [4]. Nevertheless, the efficacy of pulmonary metastasectomy for renal cell cancer remains indeterminate. This report examines the impact on survival of pulmonary resection in the treatment of renal cell cancer that has metastasized to the lung. The influence of several prognostic factors on survival including synchronicity of metastases with the primary lesion, disease-free interval, the number of nodules on preoperative studies, the number of nodules resected, and the effect of preoperative immunotherapy was considered in this select series of patients.

Patients and Methods Patient Population and Preoperative Evaluation Between 1985and 1991, 426 patients with metastatic renal cell cancer were admitted to the Surgical Branch, National Cancer Institute, National Institutes of Health, with the diagnosis of metastatic renal cell cancer. All patients were initially screened for inclusion in clinical protocols of the Surgery Branch, National Cancer Institute, evaluating the Presented at the Thirty-Eighth Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 7-9, 1991. Address reprint requests to Dr Pass, Thoracic Oncology Section, Surgery Branch, National Cancer InstituteiNIH, Building 10, Room 2807, Bethesda, MD 20892.

Operative Procedure Conduct of the operation was as previously described [4]. All patients were monitored by an indwelling arterial line and on-line arterial digital oximetry. Briefly, the metastases were resected through a median sternotomy or lateral

34

POGREBNIAK ET AL RENAL CANCER PULMONARY METASTASECTOMY

thoracotomy using double-lumen endotracheal anesthesia. The entire thoracic cavity, including the mediastinum, chest wall, and hilar nodes, was thoroughly examined. The right and left lungs were individually explored by bimanual palpation of the collapsed lung. Palpable abnormalities that did not appear to be obvious granulomas or intrapulmonary lymph nodes were excised with automatic stapling devices. Formal pulmonary resection was undertaken in patients whose nodules were not amenable to wedge or segmental resections if they could be rendered free of disease, if lymph node sampling did not reveal metastatic renal cell carcinoma, and if discontinuous pleural metastatic disease was not present. The number of metastases was determined and recorded for each operation.

Roentgenographic Monitoring A nodule was defined as a focus of increased density that was spherical, based on either the pleura or parenchyma, and unassociated with linear densities. Newly developing nodules were considered highly suggestive of renal cell cancer metastases and served as an absolute indication for exploration. Chest computed tomographic examinations were performed with a GE 8800 CT/C scanner (General Electric Company, Fairfield, CT) by scanning the entire thorax in transaxial slices at 10-mm-thick intervals. The images were displayed on a 256 by 256 matrix. Contiguous 1-cm linear tomograms were obtained in the coronal plane throughout the entire depth of the lungs.

Statistical Analysis Survival durations were computed from the date of operation until the date of last known follow-up or date of death. Probabilities of survival were computed actuarially by the method of Kaplan and Meier [5]. The statistical significance of the difference between groups was determined by the generalized Wilcoxon test of Gehan. All p values are two-sided.

Results Operative Findings From 1985 to 1991, 23 patients underwent 28 thoracic explorations for presumptive metastatic renal cell cancer. Histologically confirmed pulmonary metastases were found at all 28 explorations. At the 23 initial explorations, median sternotomy was the most common approach (n = 14). Lateral thoracotomies (n = 7) or combined sternotomies/thoracotomies (n = 2) were performed in the remaining patients. All 5 patients undergoing a second operation were explored through a lateral thoracotomy. Fifteen patients could be rendered free of disease at exploration, with 49% of these resections (n = 7) involving wedge only. However, formal anatomic resections were required in the remainder: wedge and segmentectomy, 4; wedge and lobectomy, 1; wedge and chest wall resection, 1; lobectomy only, 1; and bilobectomy, wedge, and chest wall resection, 1. Eight of 23 patients were not rendered free of disease at thoracotomy, but only 2 of

Ann Thorac Surg 1992;54:33-8

these 8 were explored with curative intent, both of whom were found to have unresectable disease via wedge biopsy confirmation of recurrence. The 6 patients not explored with curative intent underwent thoracotomy for diagnosis (wedge, l), palliation of hemoptysis (wedge segmentectomy, l), treatment with photodynamic therapy (wedge and pleural resection, l), and procurement of tumor-infiltrating lymphocytes (3). Overall, 91 wedge resections, 5 segmentectomies, 3 lobectomies, 2 chest wall resections, and 1 bilobectomy were performed. Four patients had additional procedures at exploration. Two underwent simultaneous resection of their primary and metastatic lesions. In both instances the patients were able to be rendered free of disease. One patient required placement of an arteriovenous hemodialysis graft, and a patient with discontinuous pleurally based disease received photodynamic therapy.

Operative Mortality and Morbidity There were no operative or perioperative deaths. In the 28 explorations there were two complications (7%):atelectasis (1) and a third-degree skirt burn (1) requiring split thickness skin grafting. The burn occurred in a patient who had received the photosensitizer Photofrin I1 in anticipation of the delivery of photodynamic therapy; however, because the patient was able to have complete resection, no intrapleural light was administered. Operative duration ranged from 1.5 hours for simple wedge resections to 5 hours for the more complicated anatomic resections (mean, 3.2 ? 0.2 hours). Mean estimated blood loss was 544 ? 100 mL (range, 100 to 1,500 mL), with only 1 patient requiring replacement. No patient remained intubated longer than 24 hours, and mean hospitalization was 8 ? 1 days (range, 6 to 17 days).

Actuarial Survival After Resection Long-term survival data were available on all 23 patients. The mean survival after exploration in all 23 patients was 43 months (Fig 1).The 15 patients rendered free of disease at thoracotomy had significantly longer postthoracotomy survival (mean, 49 months; median not yet achieved) compared with patients with incomplete resection (median, 16 months; p2 = 0.02) (Fig 2). Two of the 15 patients who underwent curative reseciions are presently free of disease greater than 4.5 years after exploration.

Possible lnfluence of Prognostic Factors METASTASES. Of the 15 patients who underwent complete resection, 7 had pulmonary metastases at the time of diagnosis and 8 had metastases that developed subsequently. There was no significant difference in postoperative survival between these two groups ( p 2 = 0.60) (Fig 3). The mean postoperative survival for patients who had metastases at the time of diagnosis was 44 months, versus 47 months for patients whose nodules developed later. SYNCHRONOUS VERSUS METACHRONOUS

NUMBER

OF NODULES ON PREOPERATIVE ROENTGENO-

EVALUATION. All 17 patients explored with curative intent underwent preoperative evaluation by either GRAPHIC

POGREBNIAK ET AL RENAL CANCER PULMONARY METASTASECTOMY

Ann Thorac Surg 1992;54:3%8

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Fig 1. Survival after resection for pulmona y metastases in all 23 patients with renal cell cancer from the time of pulmonary resection.

Fig 3. Survival after resection for pulmonay metastases from renal cell cancer: synchronous versus metachronous pulmonary metastases.

full-lung linear tomography, thoracic computed tomography, or both. The number of nodules detected was not a significant predictor of survival after thoracotomy ( p 2 = 0.65) (Fig 4). Patients with only one nodule detected had a mean postthoracotomy survival of 47.5 months versus 45.4 months for those with greater than one imageable lesion. Because of the superiority of computed tomography in the detection of pulmonary metastases compared with conventional full-lung linear tomography [6], the influence on survival of the number of nodules on preoperative computed tomography was analyzed. This also was not a predictor of survival (data not shown).

and cryptococcus. The absolute number of metastases resected in the 15 patients who could be rendered free of disease at exploration was not a predictor of postthoracotomy survival (Fig 5). Patients with only one metastasis resected had a mean survival of 46 months, whereas for patients with more than one nodule resected, mean survival was 47 months ( p 2 = 0.79).

NUMBER OF NODULES RESECTED. The mean number of nodules resected was 6 f 1 (range, 1 to 19) of which 3 f 1 were malignant (range, 1 to 16). The histologies of benign disease included granulomatous disease, pneumonitis, hematoma, fibrosis, calcified nodules, hamartoma,

PREOPERATIVE IMMUNOTHERAPY. The majority (78%) of patients in this study received preoperative immunotherapy. Of patients able to have complete resection, there was no difference in postthoracotomy survival between patients who had received immunotherapy (mean postoperative survival, 42.4 months) versus patients not pretreated (32.2 months; p2 = 0.73) (Fig 6).

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Fig 4 . Survival after resection for pulmonary metastases from renal cell cancer: influence of number of nodules on preoperdtive roentgenographic studies. (CT = computed tomography; FLT = full-lung linear tomography.)

36

Ann Thorac Surg 1992;54:33-8

POGREBNIAK ET AL RENAL CANCER PULMONARY METASTASECTOMY

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Fig 5. Survival after resection for pulmonary metastases from renal cell cancer: influence of number of metastases resected.

Comment Renal cell cancer accounts for 3% of adult malignancies. Each year in the United States, approximately 25,300 people will develop, and 10,600 will die of, renal cell cancer [7]. Almost one-third of renal cell cancer patients have metastatic disease at diagnosis (8,9], and metastases will develop in one-half of the patients who undergo nephrectomy for apparently isolated disease [lo]. Moreover, 75% of stage IV patients will have pulmonary metastases [ll].The magnitude of this problem can be appreciated from these statistics, which point to the fact that one half of all patients with renal cell cancer will have initial or developing pulmonary metastases. Some surgeons have advocated an aggressive surgical approach for the treatment of pulmonary metastatic disease from renal cell cancer in select patients due to

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anecdotal reports of long-term survival after resection, and due to the absence of effective standard systemic therapy. Since Barney and Clmrchill's original case report, several studies have reported improved survival after resection of renal cell cancer pulmonary metastases (Table 1). Reported 5-year survivals range from 13% to 50%, and median survivals range from 23 to 33 months. Unfortunately, in addition to analyzing patients who had resection of pulmonary metastases, the majority of these studies also included patients who underwent resection of isolated extrapulmonary metastases in the brain, bone, adrenal, subcutaneous, and other sites. As is documented in other series of pulmonary metastasectomy, these thoracotomies, even when repeated, can be performed with acceptable mortality and morbidity. This probably is the single most important caveat that must be upheld before considering any patients for metastasectomy. In this particular series, with regard to survival once the patient undergoes such an exploration, the median postoperative survival of patients successfully undergoing resection was significantly longer than patients not capable of being surgically rendered free of disease. Thus, the ability to surgically resect pulmonary metastatic disease may significantly prolong the survival of renal cell cancer patients; however, from this retrospective review, it is not possible to determine whether resectability itself indicates a more favorable prognosis or whether surgical resection influences the outcome. It is probable that both the biologic behavior of the tumor and cytoreduction of the tumor burden are important. In patients who underwent complete resection no significant difference in survival was detected between those with pulmonary metastases at the time of diagnosis and those in whom metastases developed later. These findings are in agreement with the results of Dineen and associates [19] and Pontes arid co-workers [20]. In both series the presence or absence of metastases at the time of diagnosis did not influence survival. ODea and colleagues [16] stated that patients who had metastases after nephrectomy survived longer than patients with synchronous metastatic lesions; however, when survival was calculated from the time of excision of pulmonary metastases, not from the time of the primary renal resection, there was no such survival advantage. Skinner and associates [13] and Jett and co-workers [18] reported improved postthoracotomy survival in patients with a prolonged disease-free interval. The influence of disease-free interval could not be determined in our series because of the small sample size; however, the similarity in survival of patients with synchronous and metachronous disease implies that disease-free interval did not significantly influence survival in this series. In contrast to several series that have shown an inverse relationship between the number of malignant nodules resected and postoperative survival [13, 141, neither the number of nodules on preoperative tomograms nor the number of metastases resected correlated with survival as long as the patient was able to be rendered free of disease at exploration. Thus, there are no absolute criteria as to the number of nodules imaged on preoperative studies

POGREBNIAK ET AL RENAL CANCER PULMONARY METASTASECTOMY

Ann Thorac Surg 1992;543=

37

Table 1. Previous Studies of Resection of Renal Cell Cancer Pulmonay Metastases First Author

Reference

Year

Wilkins Middleton Skinner

[21 [I21 1131~

1961 1967 1971

Dekernion Katzenstein Mountain ODea Morrow Jett Dineen Pontes

[81 ~ 4 1 ~ 5 1 [I61 ~ 7 1

1978 1978 1978 1978 1980 1983 1988 1989

a

P I

~ 9 1 [201

No. of Patients

Solitary Lesions Only

Pulmonary Metastases Only"

Survival

16 59 20 41 12 17 16 44 25 44 29 35

No Yes No No No No No Yes No No Yes No

Yes No Yes No Yes Yes (unilateral) Yes No Yes Yes No No

31% 5-year 34% 5-year 25% 5-year 29% 5-year 25% 5-year 38 mo mean 50% 5-year Nonevaluable 24% 5-year 33 mo median 13%5-year 23 mo median

Some series included patients who underwent resection of isolated extrapulmonary metastases in the brain, bone, adrenal, subcutaneous, and other sites. This series is subsetted as patients with and without isolated pulmonary metastatic involvement.

t h a t w o u l d contraindicate exploration of these patients. Therefore, a t o u r institution we explore selected patients w i t h as many a s six or seven c o m p u t e d tomographic abnormalities if it is believed t h a t (1)s u c h resection w o u l d render t h e patient free of disease, (2) t h e patient's primary lesion was controlled or controllable, and (3) resection would leave t h e patient with sufficient pulmonary reserve. W e c a n n o t c o m m e n t on t h e influence of intrathoracic nodal metastases as a prognostic factor in these patients. Patients chosen t o undergo potentially curative resection m u s t have no evidence of segmental or mediastinal nodal enlargement on preoperative studies, and therefore routine nodal sampling is n o t performed a t t h e time of resection. The improved survival observed i n o u r series (mean survival, 43 m o n t h s ) for all patients could be due t o a number of factors including referral pattern, good performance status, o r t h e r a p y w i t h biologic response modifiers. Treatment w i t h biologic response modifiers m a y offer m o r e promise t h a n conventional chemotherapy. T h e response rate for single or multidrug chemotherapy regimens is 9% t o 17% versus 22% t o 35% for interleukin-2 and 15% to 20% for interferon-based therapies [21, 221. Seventy-eight percent of o u r patients w e r e treated with biologic response modifiers. Because pretreatment w i t h i m m u n o t h e r a p y did n o t i m p r o v e survival compared w i t h t h e patients i n this series who were n o t pretreated, t h e impact of i m m u n o t h e r a p y on survival is difficult t o quantitate. In some patients, however, t h e ability of immunotherapy t o cause t u m o r regression may r e n d e r patients w i t h formerly unresectable disease amenable t o operation. T o definitively demonstrate t h a t resection of pulmonary metastases from renal cell cancer improves survival a prospective, randomized s t u d y is needed; however, because of t h e bias of t h e medical community, it is unlikely to be performed. Further studies w i t h a larger n u m b e r of patients m u s t a d d r e s s t h e impact of s u c h neoadjuvant o r

postoperative adjunctive therapies i n a prospective fashion. Nevertheless, i n carefully selected patients, an aggressive approach t o isolated p u l m o n a r y metastases m a y be justified. It is possible t h a t w i t h newer therapies, includi n g immunotherapy, there will be an expanded role for t h e thoracic oncologist i n the m a n a g e m e n t of these patients.

References 1. Barney JD, Churchill EJ. Adenocarcinoma of the kidney with metastasis to the lung. J Urology 1939;42:269-76. 2. Wilkins EW Jr, Burke JF, Head JM. The surgical management of metastatic neoplasms in the lung. J Thorac Cardiovasc Surg 1961;42:29%309. 3. Putnam JB Jr, Roth JA, Wesley MN, Johnston MR, Rosenberg SA. Survival following aggressive resection of pulmonary metastases from osteogenic sarcoma: analysis of prognostic factors. Ann Thorac Surg 1983;36:516-23. 4. Jablons D, Steinberg SM, Roth J, Pittaluga S, Rosenberg SA, Pass HI. Metastasectomy for soft tissue sarcoma. J Thorac Cardiovasc Surg 1989;97:695-705. 5. Kaplan EL, Meier P. Non-parametric estimation from incomplete observation. J Am Stat Assoc 1958;53:457-81. 6. Pass HI, Dwyer A, Makuch R, Roth JA. Detection of pulmonary metastases in patients with osteogenic and soft tissue sarcoma: the superiority of CT scan compared with conventional linear tomograms using dynamic analyses. J Clin Oncol 1985;3:1261-5. 7. Boring CC, Squires TS, Tong T. Cancer statistics, 1991. CA 1991;41:19-36. 8. Dekernion JB, Ramming KP, Smith RB. The natural history of metastatic renal cell carcinoma: a computer analysis. J Urol 1978;120:14%52. 9. Patel NP, Lavengood RW. Renal cell carcinoma: natural history and results of treatment. J Urol 1978;119:722-6. 10. Swanson DA, Johnson DE. The management of renal carcinoma. Weekly Urology Update Service 1978;1:2. 11. Maldazys JD, Dekernion JB. Prognostic factors in metastatic renal carcinoma. J Urol 1986;136:376-9. 12. Middleton RG. Surgery for metastatic renal cell carcinoma. J Urol 1967;97:97>7. 13. Skinner DG, Colvin RB, Vermillion CD, Pfister RC, Leadbet-

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14. 15. 16. 17. 18.

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ter WF. Diagnosis and management of renal cell carcinoma. Cancer 1971;28:1165-77. Katzenstein AL, Purvis R Jr, Gmelich J, Askin F. Pulmonary resection for metastatic renal adenocarcinoma. Cancer 1978; 41:712-23. Mountain CF, Khalil KG, Hermes KE, Frazier OH. The contribution of surgery to the management of carcinomatous pulmonary metastases. Cancer 1978;41:833-40. ODea MJ, Zincke H, Utz DC, Bernatz PE. The treatment of renal cell carcinoma with solitary metastasis. J Urol 1978;120: 54Cb2. Morrow CE, Vassilopoulos PP, Grage TB. Surgical resection for metastatic neoplasms of the lung: experience at the University of Minnesota Hospitals. Cancer 1980;45:2981-5. Jett JR, Hollinger CG, Zinsmeister AR, Pairolero PC. Pulmo-

19. 20. 21. 22.

nary resection of metastatic renal cell carcinoma. Chest 1983;84:442-5. Dineen MK, Pastore RD, Emiich LJ, Huben RP. Results of surgical treatment of renal cell carcinoma with solitary metastasis. J Urol 1988;140:277-9. Pontes JE, Huben R, Novick A, Montie J. Salvage surgery for renal cell carcinoma. Semin Surg Oncol 1989;5:282-5. Rosenberg SA, Lotze MT, Yang JC, et al. Experience with the use of high-dose interleukin-2 in the treatment of 652 cancer patients. Ann Surg 1989;210:474-85. Linehan WM, Shepley W, Longo DL. Cancer of the kidney and ureter. In: Devita VT, Hellman S , Rosenberg SA, eds. Cancer: principles and practices of oncology. Philadelphia: J. 8 . Lippincott, 1989:979-1007.

DISCUSSION DR JOE B. PUTNAM, JR (Houston, TX): At The University of Texas M. D. Anderson Cancer Center, we have resected pulmonary metastases for a long time. More recently the genitourinary oncologists have become even more aggressive than before in encouraging resection of these nodules. One indication for pulmonary metastasectomy in this patient population, which is implied but not stated, is to assess the response to preoperative chemotherapy, as many of these patients will have some form of chemotherapy before operation. In these patients who had resectable disease, did any receive postoperative chemotherapy? And, of patients with unresectable disease who had an assessment of their tumor response to chemotherapy, did these patients receive additional chemotherapy after operation?

DR POGREBNIAK: None of the 15 patients who had complete resection received postoperative, adjuvant Chemotherapy. Those patients who subsequently had recurrence received various therapies including reresection, chemotherapy, irradiation, and immunotherapy. Only 2 patients explored with curative intent were found to have unresectable disease, and neither of these patients initially received additional therapy. Finally, in terms of assessing response to therapy, 12 patients who had previously received immunotherapy were explored with curative intent. Before immunotherapy, the mean number of nodules on roentgenographic evaluation was six; after immunotherapy, but preoperatively, this shrunk to a mean of two nodules, and at exploration a solitary nodule was found in 9 of the 12 patients.

DR KAMAL A. MANSOUR (Atlanta, GA): I really have a big problem with mediastinal nodes with renal cell metastases. I would like to know if you have treated any patients with mediastinal or subcarinal nodes, as I have had disappointing experience with operation in this setting. What d o you d o if you find mediastinal or subcarinal nodes on computed tomographic scan? Do you operate? And if you do operate, d o you d o lobectomy or pneumonectomy with radical node dissection? DR POGREBNIAK: We do not perform routine nodal sampling at the time of resection in patients chosen to undergo potentially curative resections; however, we carefully review the computed tomograms and full-lung tomograms preoperatively to exclude patients with evidence of segmental or mediastinal nodal enlargement. A subcarinal nodal resection was performed in 1patient in this series. This patient had previously received immunotherapy, but nevertheless, the operation itself was uncomplicated. The purpose of the operation was to procure tumor-infiltrating lymphocytes, and thus other metastatic foci were left behind. DR WILLIAM A. COOK (North Andover, MA): I am happy to see this group of patients being analyzed with resection for various kinds of metastatic disease. It is one of the areas we need to look at further in our work. There is another good reason to d o a resection of renal tumors, particularly if the patient can well tolerate it, which is that some of the immune therapy strategies require enough tissue to create the immune material.

Renal cell carcinoma: resection of solitary and multiple metastases.

Between 1985 and 1991, 23 patients underwent resection of pulmonary metastases from renal cell carcinoma, of whom 18 had previously received interleuk...
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