Nephro Urol Mon. 2014 May; 6(3): e17258. DOI: 10.5812/numonthly.17258 Research Article Published online 2014 May 3.

Pulmonary and Chest Wall Metastasectomy in Urogenital Tumors: A Single Center Experience and Review of Literature

1 2,* 3 Seyd Hossein Fattahi Masoum ; Behzad Feizzdeh Kerigh ; Alireza Goreifi

1Transplant Research Center, Imam Reza Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, IR Iran 2Minimally Invasive Surgery Research Center, Kidney Transplantation Complications Research Center, Ghaem Medical Hospital, Faculty of Medicine, Mashhad University of Medi- cal Sciences, Mashhad, IR Iran 3Department of Urology, Mashhad University of Medical Sciences, Mashhad, IR Iran *Corresponding author : Behzad Feizzdeh Kerigh, Minimally Invasive Surgery Research Center, Kidney Transplantation Complications Research Center, Ghaem Medical Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, IR Iran. Tel: +98-5118012857, Fax: +98-5118417404, E-mail: [email protected] Received: ; Accepted: January 7, 2014 March 15, 2014

Background: Pulmonary metastases are often found in advanced malignancies. Urogenital malignancies originating from kidney, prostate, testes, and bladder all metastasize preferentially to the lungs. Objectives: This retrospective study aimed to evaluate the results of pulmonary and chest wall metastasectomy in patients with primary urogenital Tumors. Patients and Methods: The patients who underwent pulmonary metastasectomy in Ghaem Hospital from 1996 to 2011 were examined. Thirteen out of 79 patients referred for pulmonary metastasectomy to a single thoracic surgeon had metastases from urogenital tumors; two cases with from urogenital tumors were inoperable. We reviewed their demographic data and also clinicopathological features. Disease free interval (DFI) was defined as the time between the first curative surgery and the appearance of the signs and symptoms of pulmonary metastasis. Results: Among 11 patients who underwent surgery consisted of eight males and three females. Their metastasis originated from testis tumors (n = 5), renal cell (RCC; n = 4), bladder tumor (n = 1), and prostate (n = 1). Their mean age was 41.27 years (range, 21-67). The mean age of the patients with RCC and testis tumor at the time of diagnosing metastasis was 54 and 24.8 years, respectively. There were two other patients (a 62-year-old female and a 54-year-old male) with pleural effusion due to metastatic RCC whose tumor was inoperable because of their poor general condition and hence, were referred for . Conclusions: Pulmonary metastasectomy is feasible in selected cases. Keywords: Pulmonary; Thoracic Wall; urogenital ; Neoplasm Metastasis

1. Background

Pulmonary metastases are often found in advanced sis or in those whose lesions are technically or function- malignancies. Urogenital malignancies originating from ally inoperable, local interventions such as surgery and kidney, prostate, testicles, and bladder tumors metasta- radiotherapy are at best palliative. The standard proce- size preferentially to the lungs. The diagnosis of lung me- dure is a circumscribed atypical (lung tissue sparing) re- tastasis is often associated with a very poor prognosis and section; rarely, anatomical resection such as pulmonary a short survival time. Consequently, few patients survive segmentectomy or lobectomy is required (1, 3). more than one year after diagnosis. In these situations, palliative chemotherapy is usually initiated; however, 2. Objectives the possibility of metastasectomy should be considered In this study, we presented our single center experience (1, 2). Many studies have been conducted on pulmonary with pulmonary and chest wall metastasectomy of uro- metastasectomy and it has become the standard of thera- genital and reviewed the studies concerning this py for various lungs metastases from solid malignancies. issue. Metastases of the primary tumors that do not respond well to chemotherapy, radiotherapy, or a combination of 3. Patients and Methods them are especially well suited for surgical resection. If metastases are restricted to the lungs, the use of surgery We retrospectively examined patients who underwent along with the overall oncological treatment is justified. pulmonary metastasectomy in Ghaem Hospital from In patients with widespread diffuse pulmonary metasta- 1996 to 2011. From 79 patients referred for pulmonary me

Implication for health policy/practice/research/medical education: This study may help for evaluation and treatment of metastatic urogenital cancers. Copyright © 2014, Nephrology and Urology Research Center; Published by Kowsar Corp. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Fattahi Masoum SH et al.

Table 1. Summary of Patients Dataa Case Age, y/Gender DFI Initial Pathology Site of Metastasis/Type of Surgery 1 60/M 3 RCC Chest wall/resection and reconstruction 2 56/F 3 RCC Lt lung/sup lobectomy and wedge resection 3 45/F 6 RCC Both lungs/metastasectomy 4 55/M 1 RCC chest wall/resection and reconstruction 5 67/F 4 Bladder TCC Lt lung (sup lobe)/lobectomy 6 47/M 4 Prostate Lt lung (sup lobe)/lobectomy 7 26/M 6 Rt lung/Rt lung pneumonectomy 8 32/M 4 Mixed GCT of testis Lt lung/wedge resection and segmentectomy 9 22/M 5 Mixed GCT of testis Rt lung/metastasectomy 10 23/M 3 Mixed GCT of testis Rt lung/Inf and Mid segmentectomy 11 21/M 2 Mixed GCT of testis Rt lung/metastasectomy a Abbreviation: M, male; F, female; RCC, ; TCC, transitional cell carcinoma (urothelial carcinoma); DFI, disease free interval; GCT, ; Rt, right; Lt, left; Sup, superior; Inf, inferior; and Mid, middle. tastasectomy to a single thoracic surgeon, there were 13 patient; Table 1). cases of urogenital metastases of which two cases were No major complication occurred during surgery and in inoperable. We reviewed their demographic data as well postoperation period. All patients were discharged with as clinicopathological features. Disease free interval (DFI) good condition. One patient (case 6 in Table 1) had hemo- was defined as the time between the first curative surgery philia that was prepared for surgery with 100 IU of factor and the appearance of signs and symptoms of pulmo- VIII and did not experience any complication in periop- nary metastasis. erative period. 4. Results 5. Discussion

Patients with metastases originating from urogenital Systemic metastases occur in about 20% of testicular cancers who underwent surgery consisted of eight males germ cell tumors (GCTs), 25% to 30% of prostate cancers, and three females. Their was testis tumor 30% of urothelial carcinoma with muscle , and (n = 5), RCC (n = 4), bladder tumor (n = 1), and prostate 50% of RCCs; in addition, all of them metastasize prefer- cancer (n = 1). Their mean age was 41.27 years (range, entially to the lungs (4). We reviewed the studies concern- 21-67). The mean age of patients with RCC and testis tu- ing pulmonary metastasectomy in urogenital tumors as mor at the time of diagnosing the metastasis was 54 and well as presenting our experience in this issue. 24.8 years, respectively. There were two other patients (A 5.1. Renal Cell Carcinoma 62-year-old female and a 54-year-old male) with pleural effusion due to metastatic RCC who were found inopera- RCC metastasizes preferentially to the lung either he- ble due to their poor general condition and were referred matogenous or via lymphatic route (1). At the time of di- for chemotherapy. agnosis, about 20% of patients show regional or systemic Clinical presentation of the metastasis was dyspnea and metastases and up to 30% of them present with metasta- cough in five patients and hemoptysis in one patient. Five ses after radical nephrectomy (5). Lung and lymph nodes patients were asymptomatic and their metastasis was are the most frequent sites of metastasis (62%-77% and diagnosed in their routine follow-up. Mean DFI was 3.73 34%-58%, respectively); the skeletal system and liver are years (range, 1-6) in all patients and 2.75 and four years in involved less frequently (18%-30%) (4, 6). patients with RCC and testis tumor, respectively. Although development of new drugs like tyrosine The site of metastasis was chest wall in two, right lung in kinase inhibitors and mTOR (mammalian target of ra- four, and left lung in four patients. One patient had bilat- pamycin) inhibitors is associated with an improvement eral lung metastases. All surgeries were done by a single in progression-free survival, lung metastasectomy re- thoracic surgeon. Two patients with chest wall involve- mains as an acceptable choice for curative treatment ment underwent tumor resection. Chest wall was recon- (7). In 21 studies published from 1961 to 2011, the five-year structed using latissimus dorsi muscle and Mersilene survival after RCC pulmonary metastasectomy ranged mesh. The other types of surgical procedures included from 21% to 60% (8). on the other hand, in a study of eight lobectomy (three cases), metastasectomy (three cases), selected patients without extrapulmonary metastases segmentectomy (two cases), and pneumonectomy (one who underwent complete resection of solitary or mul-

2 Nephro Urol Mon. 2014;6(3):e17258 Fattahi Masoum SH et al. tiple unilateral or bilateral RCC pulmonary metastases, others had lung involvement. Moreover, we had two pa- five-year survival was 83% (9). In most studies, complete tients with pleural effusion due to metastatic RCC who resection of metastasis was a good prognostic factor. Al- were inoperable. though resectability itself may be associated with better prognosis, reduction of tumor burden may also play a 5.2. Testicular Tumors significant role. Higher number of metastases and lymph node involvement indicate advanced disease and may The lung is the most common site of metastases in pa- compromise complete resectability (8, 10). Other good tients with testicular GCTs (16). Pulmonary metastasec- prognostic factors include solitary metastasis (vs. mul- tomy in GCTs results in five-year survival rate of 65% (12), tiple), smaller number of metastases (< 3 or < 7), smaller the best survival rate in comparison to the rates from size of metastases (< 3 cm), metachronous (vs. synchro- metastasectomy of other tumor types including epithe- nous) metastases, longer DFI (> 12-36 months), absence of lial tumors, , and . The role of pul- positive hilar and/or mediastinal lymph nodes, absence monary metastasectomy in the treatment of testicular of pleural infiltration, and absence of positive lymph GCT has been evolving with the introduction of cisplatin nodes at initial nephrectomy (8). Simultaneous metasta- to chemotherapy regimens. Before cisplatin era, the five- sis of thoracic lymph nodes occurs in 30% to 45% of cases year survival rate for patients after pulmonary metasta- and is associated with a much less favorable prognosis. sectomy was 41% that increased to 65% after introducing Mean survival of these patients has been reported as 26 cisplatin (17). to 29 months, which is shorter in comparison to 64 to Numerous studies have demonstrated the prognostic 92 months in patients without lymph node metastases. value of the resected residual lesions histology. In their Therefore, patients with mediastinal lymph node metas- study, Einhorn et al. concluded that surgical resection tases are not suitable for curative surgery (11). Surgery of residual disease following chemotherapy-induced cy- should resect all existing metastases, which may leads to toreduction with platinum combination chemotherapy a five-year survival rate of 40% to 50% and a mean survival may be therapeutic in some cases and helps to define the time from 35 to 55 months, with low surgical mortality optimal subsequent treatment strategy (18). In nonsemi- and morbidity rates (0%-2% and 1.5%-10%, respectively) (4). nomatous , all lesions that remain after Pastorino et al. reported that the five- and ten-year sur- chemotherapy should be removed because in up to 35% of vival rates of patients who underwent complete surgi- cases, their histopathological findings are inconsistent cal resection were 36% and 26%, respectively, which were with their retroperitoneal findings (1, 4). Normalization longer in comparison with the rates in those with incom- of the tumor markers after chemotherapy does not im- plete resections (13% and 7% in five- and ten-years rates, ply that removing the residual tumors in the lungs and respectively) (12). Tanguay et al. reported the potential mediastinum is not needed (1). Patients with elevated se- benefits of combining surgery with systemic therapy. Me- rum markers were traditionally believed as unresectable dian time to relapse was six months in patients treated and not suitable for surgery; however, a few studies have with initial surgery and 8.5 months in patients treated demonstrated that salvage surgery may have potential with delayed surgery, although the latter group of pa- for cure in a selected patients with lesions limited to one tients had substantially more sever disease. Among the site (17). Murphy et al. reported that six patients with dis- patients who underwent initial surgery, 55% had survived ease limited to the lung parenchyma and mediastinum after median follow-up of 48 months while 66% of pa- had no evidence of disease with a minimum follow-up tients who received initial systemic therapy had survived period of 31 months (19). Wood et al. reported that me- 27 months. The authors emphasized that the disease tastasectomy was performed for three patients with lung burden was much greater in patients who had received metastases and one with mediastinal disease of which initial systemic therapy; however, the promising results two patients were disease-free at 16-month later follow- seem to support initial systemic therapy for patients with up (20). Moreover, in a study by Liu et al., eight patients greater disease burden (13). Although DFI, defined as the had persistently elevated serum tumor markers after time interval between nephrectomy and pulmonary me- chemotherapy prior to pulmonary metastasectomy. After tastasectomy or between nephrectomy and diagnosis of metastasectomy, five patients survived without evidence pulmonary metastases, varies in metachronous metasta- of disease, three of which were considered as cured with ses, it does not exceed five years in the majority of cases. follow-up period of longer than 15 years (17). However, some others reported a maximum DFI of longer In general, indications of resecting lung metastatic foci than 15 years (14, 15). Very late metastasectomy has been include residual tumors after chemotherapy and nor- rarely reported, and the long-term results are practically malization of tumor marker values, lack of response to lacking (8). chemotherapy, partial response to chemotherapy, and In our experience, we had four cases of metastatic recurrence after chemotherapy (1). The histological dis- RCC with mean DFI of 2.75 years, and the mean age of cordance between the two lungs is only 5%; hence, the patients at the time of diagnosis of metastasis was 54 decision for or against surgical resection of contralateral years. Two patients had chest wall involvement and two metastasis may be made on the basis of histological find-

3 Nephro Urol Mon. 2014;6(3):e17258 Fattahi Masoum SH et al. ings of the first procedure (4). site who had responded well to chemotherapy and had In our study we had five cases of testicular tumor, four no evidence of rapid progression elsewhere. In addition, cases of mixed GCTs and one case of seminoma. All of before considering surgical consolidation, they observed them had normal tumor markers before metastasectomy patients for three to six months following chemotherapy and their mean DFI was four years. to exclude rapid progression (29). In our experience, we had only one case of bladder car- 5.3. Urothelial Carcinoma cinoma that underwent pulmonary lobectomy with DFI of four years. Locoregional or systemic recurrence may be seen re- spectively in 5% and 35% of patients with muscle-invasive 5.4. Prostate Carcinoma urothelial carcinoma (transitional cell carcinoma) of the urinary bladder after radical cystectomy (21, 22). The Pulmonary metastases are found in 5% to 27% of prostate standard treatment consists of systemic chemotherapy cancer cases and usually only after bone metastasis (30, which leads to partial or complete remission in 70% of 31). These metastases may present in a diffuse interstitial patients with mean progression-free interval of seven pattern representing lymphatic spread, which is the most months, and shorter than 14 months mean survival time common form, or a multinodular pattern representing (23). Recurrences occur usually at the site of the primary hematogenous spread, which is seen in 8% to 20% of those metastasis, which indicates persistence of active cancer- with positive radiographic findings. Solitary pulmonary ous cells; hence, metastasectomy is reasonable to im- nodules have been reported but are extremely rare (32). prove the prognosis (4). Recently, modern diagnostic imaging methods such as Cowles et al. reported surgery for metastatic urothelial choline PET/CT (positron emission tomography/comput- cancer for the first time. They observed a long-term dis- ed tomography) have become essential tools by enabling ease control in six patients after the resection of a solitary early diagnosis of isolated metastases in patients with pulmonary metastasis (24). Siefker-Radtke et al. reported low-PSA recurrence, which can raises patients’ hopes outcomes of 31 patients undergoing postchemotherapy of cure (33). Salvage metastasectomy is a surgical treat- resection of metastases of which 77% were lung metas- ment of locoregional or solitary systemic metastases that tases. Overall survival (OS) since the time of surgery was are confirmed by imaging studies after local primary or 23 months and five-year survival rate was 33% (25). Abe systemic therapy. The aim of salvage metastasectomy in et al. observed a median survival time of 42 months in is to gain time before initiating systemic 12 patients, with visible cancer in 83% of them, who un- androgen deprivation, which is associated with marked derwent metastasectomy at multiple sites including the side effects that are time-limited. This treatment is not lungs (26). In a recent study by Lehmann et al., outcomes helpful to increase the survival time. Due to the limited of 44 patients from 15 different centers in Germany were life expectancy, visceral metastasectomy or, alternatively, reported. The patients had distant metastases of the uro- radiotherapy should be performed only if the patient’s thelial or upper urinary tract tumors and underwent symptoms cannot be controlled by conservative manage- complete resection of all detectable metastases. OS from ment or if his function is threatened (4). the time of resection was 27 months and 7 (15.9%) pa- In our experience we had only one case of prostate sar- tients survived for more than two years without disease coma which underwent lobectomy with DFI of four years. progression (27). Recently, Siefker-Radtke et al. presented The patient has been operated because of his severe respi- data from a phase II clinical trial of sequential neoadju- ratory symptoms that could not be controlled by conser- vant chemotherapy with ifosfamide, doxorubicin, and vative management. gemcitabine followed by cisplatin, gemcitabine, and ifos- The diagnosis of lung metastases in urogenital tumors famide in locally advanced urothelial carcinoma. In their is often associated with a very poor prognosis and a short report, 35 patients underwent surgical consolidation, in- survival time. The primary treatment in these patients is cluding 24 with nodal metastasis, six with tumor fixed to palliative chemotherapy. However, an interdisciplinary the pelvic sidewall, and five with metastasis to other or- tumor board should also discuss the possibility of metas- gans such as lung, brain, abdominal wall, or ileum. Five- tasectomy. The aim of treatment in these situations is pal- year OS for these patients was 29%; moreover, the greatest liative local radical resection and symptom control. Sur- improvement was seen in patients undergoing surgical vival after lung metastasectomy depends on the nature consolidation after a 90% or greater response to chemo- of the primary tumor. In the case of urogenital tumors, therapy (28). pulmonary metastasectomy can be performed in select- The available evidence suggests that a selected group of ed patients and may improve the survival rate as well as patients benefit from surgical consolidation of visceral quality of life. Therefore, the decision for or against me- metastases, most frequently in the setting of lung me- tastasectomy must be made on a case-by-case basis. tastasis. Although there is no standard guideline in this Acknowledgements setting, Svatek et al. considered surgical consolidation of visceral metastases for patients with tumor at one distant We thank Mrs. Yaghouti for her excellent cooperation.

4 Nephro Urol Mon. 2014;6(3):e17258 Fattahi Masoum SH et al.

Author’s Contribution 16. Kawamukai K, Di Saverio S, Antonacci F, Lacava N, Boaron M. Mediastinal germ cell tumour with massive pulmonary involve- BMJ Case Rep. 2011 Both authors worked equally. ment. 2011; . 17. Liu D, Abolhoda A, Burt ME, Martini N, Bains MS, Downey RJ, et al. Financial Disclosure Pulmonary metastasectomy for testicular germ cell tumors: A 28- The Annals of Thoracic Surgery. 66 year experience. 1998; (5):1709–14. There was no financial interest. 18. Einhorn LH, Williams SD, Mandelbaum I, Donohue JP. Surgical re- section in disseminated testicular cancer following chemothera- Cancer. 48 Funding/Support peutic cytoreduction. 1981; (4):904–8. 19. Murphy BR, Breeden ES, Donohue JP, Messemer J, Walsh W, Roth J BJ, et al. Surgical salvage of chemorefractory germ cell tumors. There was no funding source. Clin Oncol. 11 1993; (2):324–9. References 20. Wood DP, Herr HW, Motzer RJ, Reuter V, Sogani PC, Morse MJ, et al. Surgical resection of solitary metastases after chemotherapy in 1. Pfannschmidt J, Egerer G, Bischof M, Thomas M, Dienemann H. patients with nonseminomatous germ cell tumors and elevated Dtsch Arztebl Cancer. 70 Surgical intervention for pulmonary metastases. serum tumor markers. 1992; (9):2354–7. Int. 109 2012; (40):645–51. 21. Giannarini G, Kessler TM, Thoeny HC, Nguyen DP, Meissner C, 2. Younes RN, Haddad F, Ferreira F, Gross JL. [Surgical removal of Studer UE. Do patients benefit from routine follow-up to detect Rev As- pulmonary metastasis: prospective study in 182 patients]. recurrences after radical cystectomy and ileal orthotopic blad- soc Med Bras. 44 Eur Urol. 58 1998; (3):218–25. der substitution? 2010; (4):486–94. 3. Kim JJ, Park JK, Wang YP. Surgical resection of pulmonary metas- 22. Volkmer BG, Kuefer R, Bartsch GC, Jr, Gust K, Hautmann RE. On- Korean J Thorac Cardiovasc Surg. tasis from renal cell carcinoma. cological followup after radical cystectomy for -is 44 J Urol. 181 2011; (2):159–64. there any benefit? 2009; (4):1587–93. 4. Heidenreich A, Wilop S, Pinkawa M, Porres D, Pfister D. Surgical 23. von der Maase H, Hansen SW, Roberts JT, Dogliotti L, Oliver T, resection of urological tumor metastases following medical Moore MJ, et al. Gemcitabine and cisplatin versus methotrexate, Dtsch Arztebl Int. 109 treatment. 2012; (39):631–7. vinblastine, doxorubicin, and cisplatin in advanced or metastat- 5. Beisland C, Medby PC, Beisland HO. Presumed radically treated ic bladder cancer: results of a large, randomized, multinational, J Clin Oncol. 18 renal cell carcinoma--recurrence of the disease and prog- multicenter, phase III study. 2000; (17):3068–77. Scand J Urol Nephrol. nostic factors for subsequent survival. 24. Cowles RS, Johnson DE, McMurtrey MJ. Long-term results fol- 38 Urology. 2004; (4):299–305. lowing thoracotomy for metastatic bladder cancer. 20 6. Mekhail TM, Abou-Jawde RM, Boumerhi G, Malhi S, Wood L, Elson 1982; (4):390–2. P, et al. Validation and extension of the Memorial Sloan-Ketter- 25. Siefker-Radtke AO, Walsh GL, Pisters LL, Shen Y, Swanson DA, ing prognostic factors model for survival in patients with pre- Logothetis CJ, et al. Is there a role for surgery in the management J Clin Oncol. viously untreated metastatic renal cell carcinoma. of metastatic urothelial cancer? The M. D. Anderson experience. 23 J Urol. 171 2005; (4):832–41. 2004; (1):145–8. 7. Staehler M. The role of metastasectomy in metastatic renal cell 26. Abe T, Shinohara N, Harabayashi T, Sazawa A, Maruyama S, Suzuki Nat Rev Urol. 8 carcinoma. 2011; (4):180–1. S, et al. Impact of multimodal treatment on survival in patients Eur Urol. 52 8. Tsakiridis K, Visouli AN, Zarogoulidis P, Mpakas A, Machairiotis with metastatic urothelial cancer. 2007; (4):1106–13. N, Stylianaki A, et al. Lost in time pulmonary metastases of re- 27. Lehmann J, Suttmann H, Albers P, Volkmer B, Gschwend JE, Fech- nal cell carcinoma: complete surgical resection of metachro- ner G, et al. Surgery for metastatic urothelial carcinoma with J Thorac Dis. Eur Urol. nous metastases, 18 and 15 years after nephrectomy. curative intent: the German experience (AUO AB 30/05). 4 55 2012; (Suppl 1):69–73. 2009; (6):1293–9. 9. Chen F, Fujinaga T, Shoji T, Miyahara R, Bando T, Okubo K, et al. 28. Siefker-Radtke AO, Dinney CP, Shen Y, Williams DL, Kamat AM, Pulmonary resection for metastasis from renal cell carcinoma. Grossman HB, et al. A phase 2 clinical trial of sequential neoad- Interact Cardiovasc Thorac Surg. 7 2008; (5):825–8. juvant chemotherapy with ifosfamide, doxorubicin, and gem- 10. Pogrebniak HW, Haas G, Linehan WM, Rosenberg SA, Pass HI. Re- citabine followed by cisplatin, gemcitabine, and ifosfamide Cancer. nal cell carcinoma: Resection of solitary and multiple metasta- in locally advanced urothelial cancer: final results. The Annals of Thoracic Surgery. 54 119 ses. 1992; (1):33–8. 2013; (3):540–7. 11. Pfannschmidt J, Klode J, Muley T, Dienemann H, Hoffmann H. 29. Svatek RS, Siefker-Radtke A, Dinney CP. Management of metastat- Nodal involvement at the time of pulmonary metastasectomy: ic urothelial cancer: the role of surgery as an adjunct to chemo- Ann Thorac Surg. 81 Can Urol Assoc J. 3 experiences in 245 patients. 2006; (2):448–54. therapy. 2009; (6 Suppl 4):S228–31. 12. Pastorino U, Buyse M, Friedel G, Ginsberg RJ, Girard P, Gold- 30. Fabozzi SJ, Schellhammer PF, El-Mahdi AM. Pulmonary metasta- Cancer. 75 straw P, et al. Long-term results of lung metastasectomy: Prog- ses from prostate cancer. 1995; (11):2706–9. J Thoracic Cardiovasc Surg. nostic analyses based on 5206 cases. 31. Saitoh H, Hida M, Shimbo T, Nakamura K, Yamagata J, Sa- 113 1997; (1):37–49. toh T. Metastatic patterns of prostatic cancer: Correla- Cancer. 13. Tanguay S, Swanson DA, Putnam JBJ. Renal Cell Carcinoma Meta- tion between sites and number of organs involved. 54 static to the Lung: Potential Benefit in the Combination of Bio- 1984; (12):3078–84. J Urol. 156 logical Therapy and Surgery. 1996; (5):1586–9. 32. Goto T, Maeshima A, Oyamada Y, Kato R. Solitary pulmonary me- World J Surg Oncol. 14. Kanzaki R, Higashiyama M, Fujiwara A, Tokunaga T, Maeda J, tastasis from prostate sarcomatoid cancer. 8 Okami J, et al. Long-term results of surgical resection for pul- 2010; :101. monary metastasis from renal cell carcinoma: a 25-year single- 33. Picchio M, Briganti A, Fanti S, Heidenreich A, Krause BJ, Messa Eur J Cardiothorac Surg. 39 institution experience. 2011; (2):167–72. C, et al. The role of choline positron emission tomography/ 15. Shiono S, Yoshida J, Nishimura M, Nitadori J, Ishii G, Nishiwaki Y, computed tomography in the management of patients with et al. Late pulmonary metastasis of renal cell carcinoma resected prostate-specific antigen progression after radical treatment of Jpn J Clin Oncol. 34 Eur Urol. 59 25 years after nephrectomy. 2004; (1):46–9. prostate cancer. 2011; (1):51–60.

5 Nephro Urol Mon. 2014;6(3):e17258