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Salvage stereotactic radiosurgery for brain metastases Expert Rev. Neurother. 13(11), 1285–1295 (2013)

George Klironomos1 and Mark Bernstein*2 1 Department of surgery, University of Toronto, Clinical Fellow in Neuroncology and Skull Base Neurosurgery, 339 Bathurst Street, Toronto, ON M5T2S8, Canada 2 Department of Surgery, University of Toronto, The Greg Wilkins-Barrick Chair in International Surgery, Neurosurgeon, Toronto Western Hospital, University Health Network, 399 Bathurst Street, 4W451, Toronto, ON M5T 2S8, Canada *Author for correspondence: Tel.: +1 416 603 6499 Fax: +1 416 603 5298 [email protected]

Recurrent or progressive brain metastases after initial treatment represent a common clinical entity mainly due to increased survival of cancer patients. From the various available treatment modalities, salvage stereotactic radiosurgery seems to be the most commonly used. Many clinical studies of class of evidence III have demonstrated satisfied results concerning the local brain control and survival of patients with relapsing brain disease. Also stereotactic radiosurgery is considered a relatively safe modality with low incidence of brain toxicity side effects. It is obvious that well-designed, randomized, prospective studies are necessary for the evaluation of the stereotactic radiosurgery as salvage treatment and for the establishment of guidelines for the selection of patients most suitable for this treatment option. The increasing number of patients with relapsing brain metastatic disease will act as a pressure to this direction. KEYWORDS: brain metastasis • salvage treatment • stereotactic radiosurgery

An overview of brain metastases

Brain metastases (BM) represent the most common intra-axial tumor in adults and exceed the number of primary brain tumors by 5- to 10-times. According to a 2008 report from the American Cancer Society Registry, about 1.5 million Americans are diagnosed with cancer every year and up to 40% of them will develop BM [1]. These numbers will further increase in the coming years due to an aging population, improving diagnostic imaging and earlier detection of BM and continuing improvement in local and systemic cancer therapies. The histology of cancer is one of the most important factors affecting the incidence of BM. Primary tumors that most likely metastasize to the brain are, in decreasing order: lung, breast, melanoma, kidney and gastrointestinal tract tumors [2–4]. The primary site is unknown in up to 15% of patients with BM. In men, lung cancer represents the most common type of primary cancer metastasizing to the brain and is responsible for 30–60% of BM. BM occur in 17–65% of patients with lung cancer and commonly cause the first symptoms of the disease prompting further investigations which

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10.1586/14737175.2013.853445

result in the diagnosis of lung cancer. The incidence of BM from lung cancer has been increasing in women in recent years [5,6]. Breast cancer represents the most common cause of BM in women, occurring in about 30% of patients with breast cancer, and representing 5–30% of BM in the female population [5]. BM from breast cancer usually represents a late event in the course of the disease with a medial interval of about 3 years from the diagnosis of the primary disease to the BM. There has been increasing recognition that patients with HER2-positive and triple negative tumors have a predilection for CNS spread. BM from malignant melanoma are estimated to represent 5–21% of BM [5]. Malignant melanoma is characterized as the tumor with the greatest propensity for metastases to the brain and the incidence of BM among melanoma patients is estimated to be around 90% in autopsy reports [7]. The incidence of BM from renal cell carcinoma is estimated to be 5.5–11% and is more common in men [8]. Colorectal cancer accounts for 1.4–1.8% of BM and about 10% of patients with stage IV cancer develop a metastatic brain tumor [9]. Clinical manifestations of BM include headaches, focal neurological deficits, seizures,

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Table 1. Recursive partitioning analysis classification of patients with brain metastases. Classification

Recursive partitioning analysis

Class I

Age 70, controlled primary malignancy focus and no extracranial metastases

Class II

All patients with clinical and demographic characteristics not included in class I or III

Class III

KPS 60

50–59

70%, no evidence of or male with history of non-small-cell lunger cancer had awake craniotomy for removal of stable systemic disease and previous left parietal tumor. (B) Whole brain radiotherapy was given and MRI at 1 year showed WBRT (except one patient). The authors no evidence of recurrence. (C) About 6 months later, he developed a recurrence at the reported 100% LC in the radiosurgery surgical site and was treated with stereotactic radiosurgery salvage. (D) The recurrent metastasis responded very well to stereotactic radiosurgery treatment. field with median 9 months follow-up and patients with lung adenocarcinoma displayed better responses than patients with melanoma, renal lesion, diameter, volume, radioresistance and pathology of the cell carcinoma and sarcoma [48]. In a prospective Phase I/II primary lesion. The recurrence rate was 5% of the treated study by Davey et al. 1994 [46] for the effectiveness of SRS sal- lesions after a median interval of 24.5 months after SRS. Comvage, a median survival of 6 months after salvage therapy was plications were noticed in only 4/54 patients and related to reported and 9/12 (75%) of the patients developed recurrent headache related to edema 2 and 4 months after SRS, and alometastatic lesion at the site of radiation. A large study by pecia. Sheehan et al. in 2005 [50] evaluated the outcomes and Noe¨l et al. [49] evaluated the effectiveness of SRS salvage in prognostic factors after the use of SRS salvage in retrospective 54 patients with 97 recurrent/progressive metastases using review of 27 patients with 47 recurrent SCLC BM previously 11.8–23 Gy as radiation dose. In a 9-month median follow-up, receiving WBRT. Post-SRS imaging assessment revealed that only 5/97 metastases recurred and the 1- and 2-year LC rates 81% of lesions decreased or remain stable, one patient underwere 91.3 and 84%, respectively. The 1- and 2-year OS were went surgical treatment and in three patients (11%) new meta31 and 28%, respectively and median survival after SRS was stases developed. The OS was 18 months after the diagnosis of 7.8 months. The 1-, 2- and 3-year new brain-free disease sur- BM and prognostic factors affecting OS were KPS, tumor volvival (BFDS) was estimated to be 65, 57 and 28%, respec- ume and time between the diagnosis of lung cancer and BM tively. A univariate analysis in this study revealed that KPS, on the multivariate analysis. Outcomes and prognostic factors RPA class, score index for radiosurgery (SIR) and the interval for the use of SRS salvage in breast cancer patients with recurbetween WBRT and SRS salvage were significant prognostic rent/progressive BM were evaluated in a retrospective study by factors for OS and BFDS. Interval between WBRT and SRS Akyurek et al. in 2007 [51]. In this study, 15 patients who salvage longer that 14 months was associated with longer received SRS salvage for recurrent BM were evaluated, the 1BFDS. The LC rates did not relate to the location of the and 2-year survival rates were 55 and 23%, respectively and the www.expert-reviews.com

1289

1290

17 pts, 21 lesions

12 pts, 20 mets

54 pts, 97 mets

27 pts, 47 mets SCLC

15 pts Breast cancer

79 pts breast cancer

51 pts SCLC

44 pts SCLC

310 pts

111 pts

104 pts

Loeffler et al. (1990)

Davey et al. (1994)

Noe¨l et al. (2001)

Sheehan et al. (2005)

Akyurek et al. (2007)

Kelly et al. (2012)

Harris et al. (2012)

Nakazaki et al. 2013

Caballero et al. (2012)

Chao et al. (2008)

Davey et al. (2007)

NR

NR

NR

4 months

NR

NR

NR

1 year: 68% 2 years: 59%

NR

95% in 4 months

1 year: 57% 2 years: 34%

NR

1 year: 77% 2 year: 46%

81% of lesions

NR

12 months

1 year: 93.1% 2 years: 84%

25% overall

100% in 9 months f/u

Local control rates

9 months

NR

9 months

Median follow-up

7.5 vs 4 months for patients with fractionation or not, respectively

9.9 months after SRS

8.4 months for all pts after SRS

5.8 months

5.9 months median overall survival

9.8 months after SRS

1 year: 55% 2 year: 23% Median: 14 months

4.5 months after SRS

7.8 months after SRS

6 months after SRS

NR

Median survival

[47]

[56]

NR Higher KPS Controlled extracranial disease Fractionation of dose

[55]

3.6% radiation necrosis, seizures, fatigue

NR

[54]

Not related to primary tumor site

Depends on primary location of tumor (see text)

Higher KPS 5 metastases, the presence of carcinomatous meningitis, respectively. Poor prognostic factors for survival time were the KPS 10 metastases, diameter of larger tumor >20 mm and carcinomatous meningitis. Median OS from the time of diagnosis of BM in this study was 16.9 months. Caballero et al. [55] evaluated the prognostic factors for survival for patients who underwent SRS salvage after prior WBRT on the basis of primary pathology. The study included 310 patients (90 breast, 113 NSCLC, 31 SCLC, 42 melanoma, 34 miscellaneous) with a median of 3 BM at salvage, and median interval from WBRT 8.1 months. The median survival time was 8.4 months for all the patients and 12 versus 7.9 months for patients with one vs more than one BM after SRS salvage. However, decreasing survival time wasn’t demonstrated as the number of BM increased beyond one. For breast cancer patients the median survival time was 11.4 months and favorable prognostic factors for survival included age 60 and controlled primary tumor were favorable prognostic factors for survival. Melanoma patients had median survival of 7.2 months and the only favorable factor was the small total target volume. This study is in disagreement with a large study by Chao et al. [47] who evaluated the efficacy of SRS salvage and the prognostic factors for survival in 111 patients who received WBRT as initial treatment. The median OS was 17.7 months and the median survival time after SRS was 9.9 months. The median survival after SRS was 12.3 months in patients who had recurrence more than 6 months after WBRT and 6.8 months in patients with recurrence less than 6 months. The LC rates were 68 and 59% after 1 and 2 years, respectively. Dose 2 cm were predictive for local failure within a median time of 5.2 months and 25% of patients developed local recurrence. In this study, primary tumor site did not appear to be associated with survival time in contrast with the study of Caballero et al. The complications rates in this study were about 3.6% with two patients developing radionecrosis, one patient seizure and one general fatigue. There is also a prospective study evaluating the association between fractionation of SRS salvage and survival [56]. The study examined in a prospective manner 104 patients, 69 of them received a two fraction regimen (total 90% of 29.7 Gy on the surface of the tumor) and 35 received a single-dose treatment (90% isodose of 22.5 Gy on the surface of the tumor) after initial WBRT. Fractionation was revealed to be an independent determinant of survival and the survival rates were 30 and 16 weeks for patients with two fractions and single fraction, respectively. Other positive prognostic factors for survival were the controlled extracranial disease and good performance status. Unfavorable prognostic factors included multiple BM, short period to relapse after WBRT and male gender. SRS salvage in patients whose initial treatment included SRS

There are some published studies evaluating the use of SRS salvage for patients with relapsing BM whose upfront treatment included SRS (SRS alone or combined with surgery). A study published by Chen et al. [57] evaluated the role of SRS salvage in 45 patients with 70. 34 patients had one SRS salvage procedures, 10 patients had two SRS salvage procedure and 1 patient had three SRS salvage procedures. The median survival was 7 months and 92.4% of patients were progression-free at 13-month follow-up period. Another study by Kwon et al. [58] with 43 patients who received SRS salvage reports median survival of 8 months from the salvage SRS. LC rates at 6 months were 90.7% and the RPA class was the main prognostic factor for survival in both initial and salvage SRS. These two studies reported that SRS salvage may offer LC rates and survival time comparable with that of initial SRS and even additional survival benefits in selected patients. A very recent study [59] aimed to evaluate 1292

prognostic factors for survival of patients treated with SRS salvage for recurrent/progressive BM with initial treatment SRS. The authors studied prospectively 251 patients who received SRS salvage for new distal recurrent (DR) BM and report median survival from salvage treatment of 9.6 months, and time of freedom from developing DR after SRS salvage was 7.5 months. The survival time was longer in patients with one DR as compared with patients with multiples (16 vs 8.3 months) and was unrelated to patient’s age, gender, prior WBRT and primary pathology. The authors underline that survival was significantly longer following SRS salvage than initial SRS and this observation makes the prognosis of patients with distal recurrence more favorable than was previously thought. The author suggests a classification system based on clinical impact and treatability of DR metastases in order to select the patients that may benefit from salvage SRS. Shuto et al. [60] in a study of 16 patients with 242 metastatic tumors (mean number 2.9 per patient) reported a median survival of 22.4 months and a correlation of the total number of treated tumors with survival. Yamanaka et al. [61] in a study of 41 patients with recurrent lesions reported a LC rate of 89–93% and OS of 15 months. Radiotherapy-induced edema developed in 4.9% of patients (TABLES 3 & 4). Summary of studies on SRS salvage, data analysis, conclusions

The available studies in the literature dealing with the efficacy of SRS salvage are class III of evidence, retrospective, noncomparative trials and as such the reported results are subjected to selection bias. Despite this fact, the SRS salvage treatment seems to have satisfactory results regarding patients’ survival and LC rates. These satisfactory results are obvious in treating patients with local recurrence or progression of a BM as well as in patients with development of new distal metastases for whom SRS or WBRT included in the upfront treatment plan. Patients who usually are offered SRS salvage are those with long enough survival to suffer a recurrence and have favorable prognosis and performance status. The median survival rates after SRS salvage were determined in some studies to be more than 1 year. [50,51,55]. In some studies, the medial survival after salvage SRS was longer than that after the initial SRS [57]. Additionally, the recent study of Caballero et al. [54] concluded that the number of BM in patients with more than one lesion doesn’t affect the total survival after SRS salvage which seems to be satisfactory (7.9 months). There isn’t evidence in the literature to support a maximum cut off for the number of BM suitable for SRS salvage. The 1- and 2-year survival rates were 31, 28% and 55, 23%, respectively in two large studies [48,50]. The LC rates at 1 and 2 years appears to be very high in some studies (91 and 84%, respectively [48] and 77 and 46%, respectively [50]. The prognostic factors for the efficacy of SRS salvage in patients with recurrent BM are not clear-cut. In general, the extracranial disease status, KPS, total target volume, numbers of metastases and the time from initial treatment to relapse [55] seem to demonstrate a significant prognostic value for patients’ Expert Rev. Neurother. 13(11), (2013)

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Salvage stereotactic radiosurgery for brain metastases

Review

survival. The impact of the pathology of primary site as prognostic factor for survival is conflicted among existing studies. The rate of complications and neurotoxicity of the use of SRS salvage appears to be very low in the literature with the most common complication being the development of radionecrosis and edema. Only in very limited cases was the surgical resection of an area of radionecrosis necessary [52]. There are not definitive guidelines concerning the appropriate dose and safety of SRS, the limitations for treatment of pre-radiated lesions either with WBRT or with SRS, as well as for the use of fractionated radiosurgery. In a study by Gwak et al. in 2009 [62], of 46 patients with 100 recurrent BM acute toxicity (6 months) was reported in 21% of patients. Acute toxicity was correlated with larger tumor size (>10 cm3) and chronic toxicity was correlated with higher cumulative dose (>100 Gy). More data are also necessary concerning the maximum number, the volume of treated BM and the number of treatment for each lesion with SRS.

the existing retrospective descriptive studies are influenced by selection bias and data on quality of life and neurologic are limited. The role of SRS salvage would be best elucidated with prospective randomized trials in order to develop a useful context of guidelines for the selection of patients for SRS salvage.

Expert commentary

Financial & competing interests disclosure

While many randomized clinical studies have established the benefits of upfront SRS treatment, there are no available class I or II comparative studies evaluating the effectiveness of the available salvage therapies. In this context, the use of the available treatment modalities for recurrent/progressive BM is based on the existing class III level of evidence studies and on the personal experience of the particular centers. In addition,

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending or royalties. No writing assistance was utilized in the production of this manuscript.

Five-year view

Salvage SRS has a definite and positive role in the management of patients with recurrent BM. Five years from now, there will hopefully be prospective randomized comparative studies evaluating the efficacy of SRS salvage treatment for BM and its predominance to other treatments modalities. Additionally, more studies evaluating the appropriate and safe radiation dose planning will be available. The increasing number of patients with recurrent/progressive BM and the more effective systematic control of cancer will act as pressing issues requiring the development of guidelines for the appropriate management of relapsing brain metastatic disease.

Key issues • The efficacy of stereotactic radiosurgery salvage on survival and local tumor control needs to be precisely determined. • The prognostic factors for survival and tumor control need to be verified to improve the selection of patients suitable for stereotactic radiosurgery salvage. • Maximum dose, dose planning and safety issues need to be evaluated.

Neurosurg. Clin. North Am. 22(1), 1–6 (2011).

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Kelly PJ, Lin NU, Claus EB, Quant EC, Weiss SE, Alexander BM. Salvage stereotactic radiosurgery for breast cancer

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Salvage stereotactic radiosurgery for brain metastases.

Recurrent or progressive brain metastases after initial treatment represent a common clinical entity mainly due to increased survival of cancer patien...
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