Extremely Delayed Multiple Brain Metastases from Renal Cell Carcinoma: Remission Achieved with Total Surgical Removal: Case Report and Literature Review

Extremely Delayed Multiple Brain Metastases from Renal Cell Carcinoma: Remission Achieved with Total Surgical Removal: Case Report and Literature Review

Case Report Extremely Delayed Multiple Brain Metastases from Renal Cell Carcinoma: Remission Achieved with Total Surgical Removal: Case Report and Li...

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Case Report

Extremely Delayed Multiple Brain Metastases from Renal Cell Carcinoma: Remission Achieved with Total Surgical Removal: Case Report and Literature Review Yuta Fukushima1, Gakushi Yoshikawa1, Megumi Takasago1, Seiichiro Shimizu2, Kazuo Tsutsumi1

Key words Brain metastasis - Late recurrence - Renal cell carcinoma - Surgery

- BACKGROUND:

Abbreviations and Acronyms LI: Labeling index RCC: Renal cell carcinoma SRS: Stereotactic radiosurgery

- CASE

-

From the Departments of 1Neurosurgery and 2Pathology, Showa General Hospital, Kodaira, Tokyo, Japan To whom correspondence should be addressed: Yuta Fukushima, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.05.065 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.

INTRODUCTION Renal cell carcinoma (RCC) is known for occurrence of late metastasis, at an interval of more than 10 years from nephrectomy.1,2 The mechanisms of such delayed metastasis are still unclear, but late metastasis often occurs as a solitary lesion, which is normally expected to have a good prognosis after surgical removal.2 Only 14 cases of late brain metastasis from RCC have been reported. Total removal of a solitary brain lesion tended to result in favorable outcome, whereas cases of multiple metastases did not achieve remission. We present a case of multiple brain metastases from RCC occurring at 22 years after nephrectomy. Total removal through 2-stage craniotomy achieved remission without adjuvant therapy. CASE PRESENTATION History and Presentation A 60-year-old man was referred to the Showa General Hospital with worsening dizziness over a period of 6 months. He had undergone right nephrectomy for

Late brain metastasis from renal cell carcinoma (RCC), which is generally considered as metastasis occurring more than 10 years after nephrectomy, often occurs as a solitary lesion, and total resection is recommended to achieve remission. DESCRIPTION: We describe a rare case of multiple late brain metastases from RCC in a 60-year-old man who presented with 3 brain metastases from RCC 22 years after nephrectomy. Total removal of the 3 lesions achieved remission without adjuvant therapy.

- CONCLUSIONS:

Total removal of late brain metastasis from RCC, even occurring with multiple lesions, can achieve total remission under specific conditions.

RCC without adjuvant therapy at another hospital 22 years previously. No evidence of metastasis was discovered (stage I, T1, N0, M0), and he had been lost to followup after 3 years. He had no other past medical history. On admission, neurologic examination showed no deficit. Brain T1-weighted magnetic resonance imaging with gadoxetate disodium revealed 3 lesions: a well-enhanced 27-mm tumor on the right cerebellar tonsil that extended into the cerebellomedullary fissure (Figure 1A), a 9.5-mm nodule with cystic component in the left inferior frontal gyrus (Figure 1B), and a 6.0-mm nodule in the left postcentral gyrus (Figure 1C). Whole-body computed tomography with contrast medium showed no abnormal finding other than the right nephrectomy. Digital subtraction angiography showed that the 3 lesions were hypervascular. The patient was scheduled for 2-stage removal. First Operation The patient underwent total resection of the tumor in the posterior cranial fossa through a midline suboccipital craniotomy. At the time of surgery, the reddish tumor had adhered to the right cerebellar tonsil. En bloc resection of the tumor and the tumor bed gliosis was performed. The histologic diagnosis was metastatic clear cell carcinoma with MIB-1 labeling index (LI) of less than 1% (Figure 2).

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Second Operation After 1 month, the patient underwent total resections of the 2 tumors in the left cerebral hemisphere through left frontotemporal craniotomy and left parietal craniotomy. En bloc resections of the 2 tumors were performed. The histologic diagnoses were both metastatic clear cell carcinoma with MIB-1 LI of below 1%. Postoperative Course The patient was discharged without neurologic deficit. Follow-up with brain magnetic resonance imaging, which was performed every 6 months for the first year and then annually, and annual body computed tomography found no recurrence for 36 months (Figure 3). DISCUSSION Distant metastasis is found in about a third of patients at diagnosis of RCC.1,3 About 30% of cases of nonmetastatic RCC at diagnosis resulted in metastasis during the follow-up period after nephrectomy, and many metastases occurred within 5 years.3 Five-year survival rates are reported to be 81% in stage I, in which the tumors are smaller than 7 cm and limited to the kidney, but only 6% in stage IV, in which tumors with metastases are involved.4 Recently, median survival times were reported as 66 months in stage I, 53

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CASE REPORT YUTA FUKUSHIMA ET AL.

DELAYED MULTIPLE BRAIN METASTASES FROM RCC

Figure 1. Preoperative T1-weighted magnetic resonance images with gadoxetate disodium showing 3 lesions (arrow). (A) A 27-mm tumor on the

months in stage II, 53 months in stage III, and 27 months in stage IV.5 Clearly, RCC has a high rate of metastasis, and early metastasis worsens the prognosis. Most deaths as a result of RCC occur within 10 years of the onset.1 Brain metastasis accounts for 5.7% of all cases of metastatic RCC.6 Most metastatic RCCs are resistant to conventional radiotherapy7 and chemotherapy.8 Nevertheless, these therapies have been administered for extensive metastatic RCC or as adjuvant therapy but were mainly ineffective.6 Surgical treatments, including resection and stereotactic radiosurgery (SRS), are limited in effectiveness, and although radical resection is the only curative treatment, the outcome is still not good.6,9

right cerebellar tonsil. (B) A 9.5-mm tumor with cystic component in the left inferior frontal gyrus. (C) A 6.0-mm tumor in the left postcentral gyrus.

Late metastasis of RCC is not necessarily rare. Late metastases occur in 4.7%e11% of patients with RCC who survived more than 10 years after nephrectomy.1,2,10 Various organs are known to be late metastatic sites. The lung is the most frequent metastatic site, followed by the kidney and bone.1,2 Late metastasis tends to occur as a solitary lesion. A solitary lesion was present in 26 of 30 patients with late metastasis of RCC.2 No significant difference was observed in overall survival between patients with and without late recurrence. These findings indicate that late metastasis of RCC differs from early metastasis in clinical behavior and prognosis. Consequently, radical resection of late metastatic lesion, especially in patients with solitary lesion, may be curative.

Figure 2. Photomicrographs of the posterior cranial fossa tumor pathology. (A) The tumor cells showed the characteristic image of clear cytoplasm. Hematoxylin-eosin staining. (B) MIB-1 LI of less than 1%. Immunohistochemical staining with anti-Ki67 antibody.

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Fourteen cases of late brain metastasis have been reported (Table 1).11-21 Nine of the 11 cases of solitary metastasis were totally removed, and many had favorable outcomes. Therefore, total resection must be considered for an accessible solitary lesion. On the other hand, 3 cases of multiple metastases did not achieve remission. Nevertheless, 1 patient with multiple brain metastases survived for 66 months after diagnosis of late multiple brain metastases with resections and SRS, suggesting the need for aggressive treatment to obtain pathologic confirmation and good outcome.11 In the present case, 3 metastatic lesions that occurred after 22 years were totally removed with 2-stage craniotomy, and the patient remained recurrence free for 36 months. There were 2 points during the clinical course when the decisions were made. First, metastatic lesions of RCC are hypervascular tumors, and preoperative embolization was reported to be effective.22 Because the present lesions were fed by the internal carotid artery and vertebral artery, we did not perform preoperative embolization considering the relatively high risk of making cerebral infarction and small tumor size. Second, SRS to tumor bed and surgical cavity after gross total resection was reported to provide effective local tumor control.23-25 Based on the low MIB-1 LIs of the 3 lesions, we selected total removals alone as a treatment strategy because that

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DELAYED MULTIPLE BRAIN METASTASES FROM RCC

Figure 3. T1-weighted magnetic resonance images with gadoxetate disodium showing no recurrence after 36-month follow-up.

Table 1. Reported Cases of Late Brain Metastases from Renal Cell Carcinoma Author

Age (years) Sex Interval (years) Solitary or Multiple

Middleton, 196714 15

Region

Treatment

Outcome (Other Information)

ND

M

14

Solitary

Temporal

Total removal

Alive 17 years

55

F

13

Solitary

Left trigone

Total removal

Alive 4 years

16

Ishikawa et al., 1990

46

F

14

Solitary

Left parietal

Total removal

Alive 28 months

Ammirati et al., 199317

63

F

13

Solitary

Left cerebellum

Total removal

Recurrence after 9 months; alive 18 months after second craniotomy

Radley et al., 199318

78

M

18

Solitary

Left temporal

Total removal

Alive 1 year

18

Radley et al., 1993

60

F

15

Solitary

Left temporal

Total removal, RT ND

Cervoni et al., 199319

61

M

13

Solitary

Right frontal

Total removal

19

Cervoni et al., 1993

65

F

17

Solitary

Right frontal

Total removal

Alive 56 months

Jubelirer, 199620

86

F

15

Solitary

Left frontal

Partial resection

Deceased 6 weeks after craniotomy

Kuroki et al., 199912

86

F

12

Multiple (Lung)

Left temporoparietal Total removal, RT ND

12

Kuroki et al., 1999

67

M

15

Multiple

Left frontal (2 lesions)

Total removals, RT Alive 3 months (right parietal new lesion detected)

Roser et al., 200221

61

M

19

Solitary

Left frontal

Total removal

Alive 14 months (history of brain metastasis after 3 years of nephrectomy)

Sadatomo et al., 200513

77

M

15

Solitary

Left trigone

Partial resection, GRS

Alive 7 months

Choi et al., 201311

76

F

18

Multiple

Parietal, fourth ventricle

Partial resection, GRS

Deceased 66 months after craniotomy

Present case

60

M

22

Multiple

Right cerebellum, left frontal, left parietal

Total removals

Alive 36 months

Killebrew et al., 1983

Alive 49 months

ND, no data; M, male; F, female; RT, radiation therapy; GRS, Gamma Knife radiosurgery.

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could bring about good local control. The strategy also had the advantage of retaining the use of SRS in future recurrence. Recently, basic research using rodent models of cancer metastases has shown evidence that single tumor cells spread to distant sites earlier than previously believed and remain dormant for prolonged periods.26,27 Therefore, it is likely that microscopic metastases occurred before the nephrectomy and grew slowly before becoming symptomatic after long dormancy in the present case. The mechanisms of such long dormancy, especially in RCC, are still unclear, but the present history and pathologic findings indicate that these late multiple metastases differ from the typical clinical behavior of early metastases. As shown in the present case, even if multiple metastatic lesions have occurred, total removal may achieve remission in some cases. Therefore, total removal of accessible brain tumors, whether solitary or multiple, in patients with a history of RCC and long interval from nephrectomy can be considered as a therapeutic option for younger patients with good general condition. Previous reports have suggested that the prognosis is poor for patients after total removal of late multiple brain metastases: 1 case of re-recurrence after total removal of late multiple brain metastases12 and another case of high MIB-1 LI after an interval of 15 years.13 SRS is reported to be effective with high local control rate against brain metastasis from RCC9 and should probably be considered for such cases. In contrast, the present patient had good outcome after total removal of late multiple brain metastases from RCC. The potential for total removal to achieve remission should be evaluated before surgery and may depend on specific conditions such as younger age, good general condition, and accessible lesions. Other patients should probably be treated with less invasive methods such as SRS. No imaging modality can distinguish these patients at present, and further investigation to identify the indications for total removal are needed. The patient should be kept under extended observation.

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DELAYED MULTIPLE BRAIN METASTASES FROM RCC

CONCLUSIONS We report a rare case of extremely delayed multiple brain metastases from RCC in which total removal achieved remission. Multiple brain metastases from RCC occurring after a long interval may be different from early metastases with poor prognosis, and total removal could achieve remission. REFERENCES 1. McNichols DW, Segura JW, DeWeerd JH. Renal cell carcinoma: long-term survival and late recurrence. J Urol. 1981;126:17-23. 2. Miyao N, Naito S, Ozono S, Shinohara N, Masumori N, Igarashi T, et al. Japanese Society of Renal Cancer. Late recurrence of renal cell carcinoma: retrospective and collaborative study of the Japanese Society of Renal Cancer. Urology. 2011;77: 379-384. 3. Ljungberg B, Alamdari FI, Rasmuson T, Roos G. Follow-up guidelines for nonmetastatic renal cell carcinoma based on the occurrence of metastases after radical nephrectomy. BJU Int. 1999;84: 405-411. 4. Sene AP, Hunt L, McMahon RF, Carroll RN. Renal carcinoma in patients undergoing nephrectomy: analysis of survival and prognostic factors. Br J Urol. 1992;70:125-134. 5. ¸ Sims¸ek A, Küçüktopcu O, Akbulut F, Özgör F, Küçüktopcu E, Savun M, et al. Impact of preoperative radiological and postoperative pathological findings on survival of patients after radical nephrectomy performed with the indication of renal cell carcinoma. Turk J Urol. 2015;41:1-6. 6. Wro nski M, Arbit E, Russo P, Galicich JH. Surgical resection of brain metastases from renal cell carcinoma in 50 patients. Urology. 1996;47:187-193. 7. Maor MH, Frias AE, Oswald MJ. Palliative radiotherapy for brain metastases in renal carcinoma. Cancer. 1988;62:1912-1917. 8. Elson PJ, Witte RS, Trump DL. Prognostic factors for survival in patients with recurrent or metastatic renal cell carcinoma. Cancer Res. 1988;48: 7310-7313. 9. Hoshi S, Jokura H, Nakamura H, Shintaku I, Ohyama C, Satoh M, et al. Gamma-knife radiosurgery for brain metastasis of renal cell carcinoma: results in 42 patients. Int J Urol. 2002;9: 618-625. 10. Nakano E, Fujioka H, Matsuda M, Osafune M, Takaha M, Sonoda T. Late recurrence of renal cell carcinoma after nephrectomy. Eur Urol. 1984;10: 347-349.

11. Choi WH, Koh YC, Song SW, Roh HG, Lim SD. Extremely delayed brain metastasis from renal cell carcinoma. Brain Tumor Res Treat. 2013;1:99-102. 12. Kuroki K, Taguchi H, Sumida M, Daimaru Y, Onda J. Cerebral metastasis from a renal cell carcinoma more than 10 years after nephrectomy: report of two cases. No Shinkei Geka. 1999;27:89-93 [in Japanese]. 13. Sadatomo T, Yuki K, Migita K, Taniguchi E, Kodama Y, Kurisu K. Solitary brain metastasis from renal cell carcinoma 15 years after nephrectomy: case report. Neurol Med Chir (Tokyo). 2005;45: 423-427. 14. Middleton RG. Surgery for metastatic renal cell carcinoma. J Urol. 1967;97:973-977. 15. Killebrew K, Krigman M, Mahaley MS, Scatliff JH. Metastatic renal cell carcinoma mimicking a meningioma. Neurosurgery. 1983;13:430-434. 16. Ishikawa J, Umezu K, Yamashita H, Maeda S. Solitary brain metastasis from renal cell carcinoma 14 years after nephrectomy: a case report. Hinyokika Kiyo. 1990;36:1439-1441. 17. Ammirati M, Samii M, Skaf G, Sephernia A. Solitary brain metastasis 13 years after removal of renal adenocarcinoma. J Neurooncol. 1993;15:87-90. 18. Radley MG, McDonald JV, Pilcher WH, Wilbur DC. Late solitary cerebral metastases from renal cell carcinoma: report of two cases. Surg Neurol. 1993;39:230-234. 19. Cervoni L, Salvati M, Delfini R. Late solitary cerebral metastasis from renal carcinoma. J Neurosurg Sci. 1993;37:247-249. 20. Jubelirer SJ. Late solitary cerebral metastasis from renal cell carcinoma: a case report and review of the literature. W V Med J. 1996;92:26-27. 21. Roser F, Rosahl SK, Samii M. Single cerebral metastasis 3 and 19 years after primary renal cell carcinoma: case report and review of the literature. J Neurol Neurosurg Psychiatry. 2002;72:257-258. 22. Terada T. Renal cell carcinoma metastatic to the nasal cavity. Int J Clin Exp Pathol. 2012;5:588-591. 23. Mathieu D, Kondziolka D, Flickinger JC, Fortin D, Kenny B, Michaud K, et al. Tumor bed radiosurgery after resection of cerebral metastases. Neurosurgery. 2008;62:817-823. 24. Jagannathan J, Yen CP, Ray DK, Schlesinger D, Oskouian RJ, Pouratian N, et al. Gamma Knife radiosurgery to the surgical cavity following resection of brain metastases. J Neurosurg. 2009;111: 431-438. 25. Smith TR, Lall RR, Lall RR, Abecassis IJ, Arnaout OM, Marymont MH, et al. Survival after surgery and stereotactic radiosurgery for patients with multiple intracranial metastases: results of a single-center retrospective study. J Neurosurg. 2014; 121:839-845.

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26. Röcken M. Early tumor dissemination, but late metastasis: insights into tumor dormancy. J Clin Invest. 2010;120:1800-1803.

27. Eyles J, Puaux AL, Wang X, Toh B, Prakash C, Hong M, et al. Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth,

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in a mouse model of melanoma. J Clin Invest. 2010; 120:2030-2039. Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 29 February 2016; accepted 18 May 2016

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Citation: World Neurosurg. (2016). http://dx.doi.org/10.1016/j.wneu.2016.05.065 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.

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