Volumetric response to radiosurgery for brain metastasis varies by cell of origin

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Object

The aim of this study was to evaluate the imaging response of brain metastases after radiosurgery and to correlate the response with tumor type and patient survival.

Methods

The authors conducted a retrospective review of patients who had undergone Gamma Knife radiosurgery for brain metastases from non–small cell lung cancer (NSCLC), breast cancer, or melanoma. The imaging volumetric response by tumor type was plotted at 3-month intervals and classified as a sustained decrease in tumor volume (Type A), a transient decrease followed by a delayed increase in tumor volume (Type B), or a sustained increase in tumor volume (Type C). These imaging responses were then compared with patient survival and tumor type.

Results

Two hundred thirty-three patients with metastases from NSCLC (96 patients), breast cancer (98 patients), and melanoma (39 patients) were eligible for inclusion in this study. The patients with NSCLC were most likely to exhibit a Type A response; those with breast cancer, a Type B response; and those with melanoma, a Type C response. Among patients with NSCLC, the median overall survival was 11.2 months for those with a Type A response (76 patients), 8.6 months for those with a Type B response (6 patients), and 10.5 months for those with a Type C response (14 patients). Among patients with breast cancer, the median overall survival was 16.6 months in those with a Type A response (65 patients), 18.1 months in those with a Type B response (20 patients), and 7.5 months in those with a Type C response (13 patients). For patients with melanoma, the median overall survival was 5.2 months in those with a Type A response (26 patients) and 6.7 months in those with a Type C response (13 patients). None of the patients with melanoma had a Type B response. The imaging response was significantly associated with survival only in patients with breast cancer.

Conclusions

The various types of imaging responses of metastatic brain tumors after stereotactic radiosurgery depend in part on tumor type. However, the type of response only correlates with survival in patients with breast cancer.

Abbreviations used in this paper:GKRS = Gamma Knife radiosurgery; NSCLC = non–small cell lung cancer; WBRT = whole-brain radiation therapy.

Object

The aim of this study was to evaluate the imaging response of brain metastases after radiosurgery and to correlate the response with tumor type and patient survival.

Methods

The authors conducted a retrospective review of patients who had undergone Gamma Knife radiosurgery for brain metastases from non–small cell lung cancer (NSCLC), breast cancer, or melanoma. The imaging volumetric response by tumor type was plotted at 3-month intervals and classified as a sustained decrease in tumor volume (Type A), a transient decrease followed by a delayed increase in tumor volume (Type B), or a sustained increase in tumor volume (Type C). These imaging responses were then compared with patient survival and tumor type.

Results

Two hundred thirty-three patients with metastases from NSCLC (96 patients), breast cancer (98 patients), and melanoma (39 patients) were eligible for inclusion in this study. The patients with NSCLC were most likely to exhibit a Type A response; those with breast cancer, a Type B response; and those with melanoma, a Type C response. Among patients with NSCLC, the median overall survival was 11.2 months for those with a Type A response (76 patients), 8.6 months for those with a Type B response (6 patients), and 10.5 months for those with a Type C response (14 patients). Among patients with breast cancer, the median overall survival was 16.6 months in those with a Type A response (65 patients), 18.1 months in those with a Type B response (20 patients), and 7.5 months in those with a Type C response (13 patients). For patients with melanoma, the median overall survival was 5.2 months in those with a Type A response (26 patients) and 6.7 months in those with a Type C response (13 patients). None of the patients with melanoma had a Type B response. The imaging response was significantly associated with survival only in patients with breast cancer.

Conclusions

The various types of imaging responses of metastatic brain tumors after stereotactic radiosurgery depend in part on tumor type. However, the type of response only correlates with survival in patients with breast cancer.

The imaging response of brain metastases after stereotactic radiosurgery is complex and dynamic. Stereotactic radiosurgery leads to tumor control in 70%–90% of metastatic brain tumors.1,3,4,8,10 The clinical effectiveness of radiosurgery relates in part to the histological tumor source. Tumor control is adequate if serial imaging after radiosurgery reveals stable or reduced tumor volumes. A transient increase in tumor volume may not preclude the possibility of long-term tumor inactivation5 and is inadequate to predict the eventual radiosurgical response at a single follow-up imaging time point. In an effort to better define the effect of radiosurgery on different tumor pathologies, we evaluated the quantitative volumetric response of lung, breast, and melanoma metastases in the brain following Gamma Knife radiosurgery (GKRS). We then correlated this response to patient survival.

Methods

Institutional review board approval was acquired at the University of Pittsburgh for data review and presentation. We conducted a retrospective review of patients who had undergone GKRS for brain metastases from non–small cell lung cancer (NSCLC), breast cancer, and melanoma between 2002 and 2010 at our institution. To be included in the study, patients had to have undergone follow-up imaging at our institution so that volumetric measurements could be made on the same imaging software. Brain metastases were confirmed on CT or MRI studies, and the histopathological tumor subtype was confirmed from the site of the primary cancer. Gamma Knife radiosurgery was performed as previously described, with all patients undergoing stereotactic head frame–based, same-day MRI- or CT-guided radiosurgery.6,9,11 Magnetic resonance imaging studies were obtained 4–8 weeks after radiosurgery and at regular 3-month intervals thereafter. Patients without imaging at least 3 months after radiosurgery were excluded from the study. Images of any lesion following repeat radiosurgery were excluded from analysis. For patients with more than one metastasis, only the largest treated metastasis was selected for evaluation. Any tumor for which resection had been performed or attempted prior to radiosurgery was excluded.

The volumetric response of the three tumor pathologies to radiosurgery was serially measured, beginning with the imaging studies obtained during radiosurgery. Using software (Stentor Inc.), we determined the tumor volumes by multiplying the sum of the tumor area for each axial Gd-enhanced T1-weighted MR image by the slice thickness, which varied from 0.2 to 0.5 cm. Tumor areas were automatically generated for each closed, nonintersecting hand-drawn contour around the region of enhancement. Posttreatment tumor volumes were expressed as a fraction of the pretreatment contrast-enhanced tumor volume. Patients were divided into groups depending on their primary malignancy, and the imaging response to treatment was measured and plotted as the volumetric change over the course of 3-month intervals after radiosurgery.

Tumor volume response categories were classified as a sustained reduction in tumor volume (Type A), a transient reduction followed by a subsequent increase in tumor volume (Type B), or a sustained increase in tumor volume (Type C). Specifically, patients with a Type A response experienced an overall volume decrease of more than 10% from the initial volume without ever having more than a 10% volume increase; those with a Type B response had an initial decrease in tumor volume of more than 10%, followed by a more than 10% volume increase above the initial volume; and those with a Type C response never experienced more than a 10% decrease in tumor volume. To determine whether a pattern of response was more likely in one primary malignancy than others, the numbers of patients who fell into each category were compared individually by pathology using a chi-square test. For each pathology, we then compared the Kaplan-Meier survival curves of patients demonstrating response Types A, B, and C. Survival curves were compared using the log-rank test. Statistical significance was defined as a p value < 0.05.

Results

After applying our exclusion and inclusion criteria, we had a final cohort of 233 patients whose brain metastases from NSCLC (96 patients), breast cancer (98 patients), and melanoma (39 patients) had been treated with GKRS. The study population, which consisted of 29.4% of males, had a mean age of 57.6 years at the time of treatment. Patient demographics are summarized in Table 1. Among the three pathologies, the NSCLC group was most likely to contain patients with a Type A response; the breast cancer group, those with a Type B response; and the melanoma group, those with a Type C response (p < 0.01, chi-square test).

TABLE 1:

Summary of characteristics in 233 patients with brain metastases*

ParameterOverallBreastLungMelanomap Value
mean age in yrs57.6 ± 10.954.6 ± 10.560.8 ± 9.557.0 ± 12.6<0.001
% female70.61006129.2<0.001
mean KPS score88.3 ± 11.789.6 ± 12.137.2 ± 11.187.7 ± 12.40.116
RPA class (% of patients)
 110.212.66.414.60.143
 284.281.192.379.20.551
 35.66.31.36.30.176
% patients w/ active extracranial disease at radiosurgery65597977<0.001
% patients w/ history of WBRT38572233<0.001
mean tumor margin dose in Gy17.1 ± 3.317.4 ± 2.216.7 ± 4.217.5 ± 2.70.642
mean isodose line (%)51.8 ± 6.451.5 ± 5.651.8 ± 5.552.8 ± 9.20.358

Values represent the mean ± standard deviation, unless indicated otherwise. KPS = Karnofsky Performance Scale; RPA = recursive partitioning analysis.

Non–Small Cell Lung Cancer

Patients with NSCLC received between 16 and 20 Gy to the tumor margin. Sixteen patients (17%) received whole-brain radiation therapy (WBRT) before radiosurgery. Patients were imaged from 0.4 to 42.4 months after radiosurgery (mean 9 months). The mean reduction in tumor volume occurred most rapidly in the first 3 months after GKRS (mean treated tumor reduction 45%), followed by a less steep decline in volume over the subsequent 2 years (mean reduction 32%). Response by category is shown in Fig. 1A. Median overall survival among patients with NSCLC was 11.2 months for those with a Type A response (76 patients), 8.6 months for those with Type B (6 patients), and 10.5 months for those with Type C (14 patients; Table 2). The imaging response category was not associated with survival in patients with NSCLC (p = 0.996, log-rank test, pooled over strata; Fig. 2A).

Fig. 1.
Fig. 1.

Volumetric response curve for each primary pathology—NSCLC (A), breast cancer (B), melanoma (C)—according to response type: Group A, sustained responders; Group B, mixed responders; Group C, nonresponders.

TABLE 2:

Median survival in each group*

GroupSurvival (mos)
breast
 Group A16.6 ± 3.9
 Group B18.1 ± 3.6
 Group C7.5 ± 1.2
NSCLC
 Group A11.2 ± 1.8
 Group B8.6 ± 7.2
 Group C10.5 ± 0.9
melanoma
 Group A5.2 ± 0.8
 Group BNA
 Group C6.7 ± 1.7

Values represent the median ± standard deviation. NA = not applicable.

Fig. 2.
Fig. 2.

Kaplan-Meier plots showing overall survival after radiosurgery for each primary pathology, according to response type: Group A, sustained response; Group B, transient response; Group C, sustained tumor progression.

Breast Cancer

Patients with breast cancer received between 12 and 20 Gy to the tumor margin. Fifty-seven patients (58%) had received prior WBRT. Patients underwent imaging from 0.3 to 53.3 months after radiosurgery (mean 9.2 months). The mean reduction in tumor volume occurred most rapidly in the first 3 months after GKRS (mean treated tumor reduction 41%) and then again after 15 months in those who underwent follow-up imaging (mean treated tumor reduction between 15 and 21 months was 41%). Response by category is shown in Fig. 1B. Median overall survival among the patients with breast cancer was 16.6 months for those with Type A response (65 patients), 18.1 months for those with Type B (20 patients), and 7.5 months for those with Type C (13 patients; Table 2). The imaging response category was significantly associated with survival in breast cancer (Fig. 2B). Patients with a Type B response survived the longest, and those with a Type C response survived the shortest amount of time (p = 0.011, log-rank test, pooled over strata). Twenty patients whose receptor status was triple negative (ER−, PR−, and Her-2Neu−) had a Type A response, 5 had a Type B response, and 7 had a Type C response. A triple-negative receptor status did not correlate significantly with the imaging response category (p = 0.35, Fisher-exact test; Table 3).

TABLE 3:

Pathological findings in breast cancer metastases by response group*

GroupERPRHer2Neu
Group A
 negative362036
 positive292529
 unknown0200
Group B
 negative785
 positive9810
 unknown445
Group C
 negative7810
 positive320
 unknown333

ER = estrogen receptor; PR = progesterone receptor.

Melanoma

Patients with melanoma received between 16 and 20 Gy to the tumor margin. Twenty-two patients (56%) received WBRT prior to radiosurgery. Patients were imaged from 1 to 20 months after radiosurgery (mean 3 months). For patients with a Type A response, the reduction in tumor volume occurred most rapidly in the first 3 months after GKRS (mean reduction 56%). For the melanoma group, however, the mean tumor volume increased to an average of 1.8 times the original volume in the first 3 months, suggesting a nonlinear relationship between tumor volume changes in responders versus nonresponders to radiosurgery. Response by category is shown in Fig. 1C. Median overall survival among patients with melanoma was 5.2 months for those with a Type A response (26 patients) and 6.7 months for those with a Type C response (13 patients; Table 2). For melanoma patients, the imaging response category was not associated with overall patient survival (p = 0.608; Fig. 2C).

Discussion

Stereotactic radiosurgery is highly efficacious and safe in the management of single and multiple brain metastases. Although the overall median survival of patients with brain metastases remains less than 1 year, the prevalence of longer-term survivors continues to increase. Attempts to increase our understanding of the radiobiological response to radiosurgery should improve outcomes further. Volumetric changes in neoplasms after radiosurgery provide some insight into a specific tumor's radiobiological response. Prior small clinical series have evaluated such responses to radiosurgery in meningiomas, schwannomas, pituitary adenomas, and gliomas, as well as metastatic lesions.2,5,12,16 Some of these studies are limited to a degree by a simplified methodology for volumetric measurement, that is, volumetric calculation by multiplying maximum length and width by height. Lesional irregularities can compromise such methods. More recently, computer-assisted segmentation has been implemented to assist in more accurately measuring tumor volumes. Tumors have been traditionally measured as ellipsoids, in which the volume is estimated as x × y × z × π/6, where x, y, and z represent the largest diameter on contrast enhancement in each dimension. The error in calculating tumor volumes using this method has been reported to be as high as 20%.13,17 Here, we described a more precise method of determining tumor volumes over time to further help to elucidate the response to radiosurgery.

Our methodology involved using software to contour tumor areas across multiple axial MRI slices to accurately define tumor volume. Other major studies evaluating metastatic volumetric response to radiosurgery have classified response types in general terms, such as reduced, stable, or increased in size, using various parameters or thresholds for each outcome. We categorized volumetric outcomes as sustained reduction, reduction followed by increase, or progression; we then assessed the frequency of these outcomes and plotted the mean fractional volumetric change after radiosurgery. Each tumor type must be studied separately. Indeed, inclusion of multiple tumor types in any study of brain metastases ignores the inherent biological differences among the various cancers. Our choice of the largest tumor in each patient allowed for more accurate serial responses. Given the limitations of MRI and CT slice thicknesses, using the largest tumor resulted in the least measurement variability.

Patients with NSCLC had the greatest likelihood of sustained tumor reduction, whereas those with breast cancer were more likely to have a volumetric increase after a transient decrease. Melanoma patients were the most likely to show a volume increase after radiosurgery. As in prior reports, for all primary pathologies, a tumor volume increase was most likely to be identified 3–6 months after radiosurgery and was much less likely to be identified thereafter. In addition, a volume reduction followed by an increase occurred between the 3- and 6-month interval in the majority of patients who had available imaging. However, the frequency variations in patterns of response between pathologies may represent important and not yet well-understood biological differences in response to radiosurgery for these tumors. Data on categorical volumetric response by metastatic pathology are somewhat limited, although Rahman et al.15 recently published results suggesting that melanoma is less responsive to linear accelerator radiosurgery than breast cancer or NSCLC. An important evaluation of this finding should also include hemorrhagic potential, another variable that determines volumetric change.

We determined whether survival correlated with the type of brain tumor response. Given that survival also depends on the response of extracranial cancer to therapy, such an analysis must be interpreted cautiously. For patients with NSCLC, the median overall survival was 11.2 months for those with a Type A response (76 patients), 8.6 months for those with a Type B response (6 patients), and 10.5 months for those with a Type C response (14 patients). For patients with breast cancer, the median overall survival was 16.6 months for those with Type A response (65 patients), 18.1 months for those with Type B (20 patients), and 7.5 months for those with Type C (13 patients). For patients with melanoma, the median overall survival was 5.2 months for those with a Type A response (26 patients) and 6.7 months for those with a Type C response (13 patients). The imaging response was significantly associated with survival only in patients with breast cancer.

An increase in contrast-enhancing volume does not necessarily indicate tumor growth. Indeed, it can reflect enhancement from blood-brain barrier changes and inflammation as part of the tumor response. Thus, clinical interpretation of these volumetric responses to radiosurgery is a topic of ongoing investigation. One can safely assume that tumors that decrease in size (or regress entirely) on follow-up imaging are well controlled. However, how to clinically interpret an increase in apparent contrast enhancement following irradiation remains unknown. Differentiation between tumor regrowth and radiation effects resulting in contrast enhancement can be made to a degree by comparing T1- and T2-weighted MRI sequences.7 Interestingly, as part of an analysis on the volumetric response of metastases to GKRS, Patel et al.14 recently reported that patients who experienced a sustained increase in tumor volume had an overall longer survival than patients with tumors that decreased in size. Certainly, only patients who are still alive and can undergo imaging will show any such changes. Thus, despite this bias, the authors suggested that imaging-defined enlargement may be a result of inflammatory changes (as opposed to actual tumor growth) as a rationale for these counterintuitive results.14 The frequency of patients belonging to each response type depends on the primary pathology, which in turn determines whether the response type will have an effect on patient survival.

Some authors have found no correlation between volumetric response and patient survival.2 For the most part, survival depends more on systemic factors than on response to therapy for brain metastases. Regardless, as survival trends increase in metastatic disease and remain somewhat unpredictable on an individual basis, so does the need to better understand the relevance of postradiosurgical lesion responses. This understanding can factor in decisions regarding further irradiation or the potential need for other interventions.

Lastly, describing volumetric response patterns for a given radiosurgical methodology aids comparisons for future technique and device development. We present a large series of patients with tumor margin doses of 12–20 Gy (breast) and 16–20 Gy (NSCLC and melanoma) delivered on Gamma Knife 4C and Perfexion units. Although some variability in tumor margin dose exists, the relative frequencies of outcome patterns are potentially useful for future analyses of radiosurgical efficacy in metastatic tumors. Will a higher dose increase the slope of initial tumor regression or perhaps lead to later adverse radiation effects with more enhancement? Is a lower central dose (higher tumor margin isodose) more likely to be associated with late failure?

Limitations of this study include its retrospective nature and inhomogeneity of imaging follow-up for the target population. Given that we are a regional referral center, not all patients could have imaging at 3-month intervals. In addition, some selection bias may also be inherent in that excluded patients who had no imaging follow-up at all may have been more likely to die of disease or suffer progression, systemically or intracranially (that is, tumor volume increase). Although the overall size of the population is large, there is some limitation when divided by pathology for response pattern analysis. For instance, only 2 melanoma patients experienced a volume reduction followed by an increase.

Conclusions

Analysis of the categorical volumetric response of metastases to stereotactic radiosurgery reveals that the appearance of the response curves varies with tumor histology. Volume increases, whether preceded by volume reductions, are most likely to occur 3–6 months after radiosurgery and are unlikely thereafter. We hope that clinicians who evaluate new brain metastasis therapies will use this approach to compare management techniques and tumor responses.

Disclosure

Dr. Lunsford is a consultant for and stockholder in AB Elekta. Dr. Weiner is a stockholder in AB Elekta. The work described in this report was funded by a research grant from the Osaka Medical Research Foundation for Incurable Diseases (H.K.). The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Kano. Acquisition of data: Iyer, Harrison, Weiner. Analysis and interpretation of data: Iyer. Drafting the article: Kano, Iyer, Harrison, Luther, Lunsford, Kondziolka. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Kano. Statistical analysis: Iyer. Study supervision: Kano, Lunsford, Kondziolka.

A portion of this work was presented in poster form at the Congress of Neurological Surgeons 2012 Annual Meeting held in Chicago, Illinois, on October 6–10, 2012.

References

  • 1

    Bhatnagar AKFlickinger JCKondziolka DLunsford LD: Stereotactic radiosurgery for four or more intracranial metastases. Int J Radiat Oncol Biol Phys 64:8989032006

  • 2

    Feigl GCSamii MHorstmann GA: Volumetric follow-up of meningiomas: a quantitative method to evaluate treatment outcome of gamma knife radiosurgery. Neurosurgery 61:2812872007

  • 3

    Grandhi RKondziolka DPanczykowski DMonaco EA IIIKano HNiranjan A: Stereotactic radiosurgery using the Leksell Gamma Knife Perfexion unit in the management of patients with 10 or more brain metastases. Clinical article. J Neurosurg 117:2372452012

  • 4

    Hasegawa TKondziolka DFlickinger JCGermanwala ALunsford LD: Brain metastases treated with radiosurgery alone: an alternative to whole brain radiotherapy?. Neurosurgery 52:131813262003

  • 5

    Hayhurst CZadeh G: Tumor pseudoprogression following radiosurgery for vestibular schwannoma. Neuro Oncol 14:87922012

  • 6

    Kano HIyer AKondziolka DNiranjan AFlickinger JCLunsford LD: Outcome predictors of gamma knife radiosurgery for renal cell carcinoma metastases. Neurosurgery 69:123212392011

  • 7

    Kano HKondziolka DLobato-Polo JZorro OFlickinger JCLunsford LD: T1/T2 matching to differentiate tumor growth from radiation effects after stereotactic radiosurgery. Neurosurgery 66:4864922010

  • 8

    Kondziolka DFlickinger JCLunsford LD: Radiosurgery for brain metastases. Prog Neurol Surg 25:1151222012

  • 9

    Kondziolka DKano HHarrison GLYang HCLiew DNNiranjan A: Stereotactic radiosurgery as primary and salvage treatment for brain metastases from breast cancer. Clinical article. J Neurosurg 114:7928002011

  • 10

    Kondziolka DMartin JJFlickinger JCFriedland DMBrufsky AMBaar J: Long-term survivors after gamma knife radiosurgery for brain metastases. Cancer 104:278427912005

  • 11

    Mathieu DKondziolka DCooper PBFlickinger JCNiranjan AAgarwala S: Gamma knife radiosurgery for malignant melanoma brain metastases. Clin Neurosurg 54:2412472007

  • 12

    Pamir MNKiliç TBelirgen MAbacioğlu UKarabekiroğlu N: Pituitary adenomas treated with gamma knife radiosurgery: volumetric analysis of 100 cases with minimum 3 year follow-up. Neurosurgery 61:2702802007

  • 13

    Pan HCCheng FCSun MHChen CCSheehan J: Prediction of volumetric data errors in patients treated with gamma knife radiosurgery. Stereotact Funct Neurosurg 85:1841912007

  • 14

    Patel TRMcHugh BJBi WLMinja FJKnisely JPChiang VL: A comprehensive review of MR imaging changes following radiosurgery to 500 brain metastases. AJNR Am J Neuroradiol 32:188518922011

  • 15

    Rahman MCox JBChi YYCarter JHFriedman WA: Radiographic response of brain metastasis after linear accelerator radiosurgery. Stereotact Funct Neurosurg 90:69782012

  • 16

    Wowra BStummer W: Efficacy of gamma knife radiosurgery for nonfunctioning pituitary adenomas: a quantitative follow up with magnetic resonance imaging-based volumetric analysis. J Neurosurg 97:5 Suppl4294322002

  • 17

    Yang DYSheehan JLiu YSChangLai SPPan HCChen CJ: Analysis of factors associated with volumetric data errors in gamma knife radiosurgery. Stereotact Funct Neurosurg 87:172009

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Article Information

Address correspondence to: Hideyuki Kano, M.D., Ph.D., Department of Neurological Surgery, University of Pittsburgh Medical Center, Suite B-400, 200 Lothrop St., Pittsburgh, PA 15213. email: kanoh@upmc.edu.

Please include this information when citing this paper: published online May 30, 2014; DOI: 10.3171/2014.4.JNS131502.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Volumetric response curve for each primary pathology—NSCLC (A), breast cancer (B), melanoma (C)—according to response type: Group A, sustained responders; Group B, mixed responders; Group C, nonresponders.

  • View in gallery

    Kaplan-Meier plots showing overall survival after radiosurgery for each primary pathology, according to response type: Group A, sustained response; Group B, transient response; Group C, sustained tumor progression.

References

  • 1

    Bhatnagar AKFlickinger JCKondziolka DLunsford LD: Stereotactic radiosurgery for four or more intracranial metastases. Int J Radiat Oncol Biol Phys 64:8989032006

  • 2

    Feigl GCSamii MHorstmann GA: Volumetric follow-up of meningiomas: a quantitative method to evaluate treatment outcome of gamma knife radiosurgery. Neurosurgery 61:2812872007

  • 3

    Grandhi RKondziolka DPanczykowski DMonaco EA IIIKano HNiranjan A: Stereotactic radiosurgery using the Leksell Gamma Knife Perfexion unit in the management of patients with 10 or more brain metastases. Clinical article. J Neurosurg 117:2372452012

  • 4

    Hasegawa TKondziolka DFlickinger JCGermanwala ALunsford LD: Brain metastases treated with radiosurgery alone: an alternative to whole brain radiotherapy?. Neurosurgery 52:131813262003

  • 5

    Hayhurst CZadeh G: Tumor pseudoprogression following radiosurgery for vestibular schwannoma. Neuro Oncol 14:87922012

  • 6

    Kano HIyer AKondziolka DNiranjan AFlickinger JCLunsford LD: Outcome predictors of gamma knife radiosurgery for renal cell carcinoma metastases. Neurosurgery 69:123212392011

  • 7

    Kano HKondziolka DLobato-Polo JZorro OFlickinger JCLunsford LD: T1/T2 matching to differentiate tumor growth from radiation effects after stereotactic radiosurgery. Neurosurgery 66:4864922010

  • 8

    Kondziolka DFlickinger JCLunsford LD: Radiosurgery for brain metastases. Prog Neurol Surg 25:1151222012

  • 9

    Kondziolka DKano HHarrison GLYang HCLiew DNNiranjan A: Stereotactic radiosurgery as primary and salvage treatment for brain metastases from breast cancer. Clinical article. J Neurosurg 114:7928002011

  • 10

    Kondziolka DMartin JJFlickinger JCFriedland DMBrufsky AMBaar J: Long-term survivors after gamma knife radiosurgery for brain metastases. Cancer 104:278427912005

  • 11

    Mathieu DKondziolka DCooper PBFlickinger JCNiranjan AAgarwala S: Gamma knife radiosurgery for malignant melanoma brain metastases. Clin Neurosurg 54:2412472007

  • 12

    Pamir MNKiliç TBelirgen MAbacioğlu UKarabekiroğlu N: Pituitary adenomas treated with gamma knife radiosurgery: volumetric analysis of 100 cases with minimum 3 year follow-up. Neurosurgery 61:2702802007

  • 13

    Pan HCCheng FCSun MHChen CCSheehan J: Prediction of volumetric data errors in patients treated with gamma knife radiosurgery. Stereotact Funct Neurosurg 85:1841912007

  • 14

    Patel TRMcHugh BJBi WLMinja FJKnisely JPChiang VL: A comprehensive review of MR imaging changes following radiosurgery to 500 brain metastases. AJNR Am J Neuroradiol 32:188518922011

  • 15

    Rahman MCox JBChi YYCarter JHFriedman WA: Radiographic response of brain metastasis after linear accelerator radiosurgery. Stereotact Funct Neurosurg 90:69782012

  • 16

    Wowra BStummer W: Efficacy of gamma knife radiosurgery for nonfunctioning pituitary adenomas: a quantitative follow up with magnetic resonance imaging-based volumetric analysis. J Neurosurg 97:5 Suppl4294322002

  • 17

    Yang DYSheehan JLiu YSChangLai SPPan HCChen CJ: Analysis of factors associated with volumetric data errors in gamma knife radiosurgery. Stereotact Funct Neurosurg 87:172009

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