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Gamma Knife surgery for patients with brainstem metastases

Clinical article

Takuya Kawabe, Masaaki Yamamoto, Yasunori Sato, Bierta E. Barfod, Yoichi Urakawa, Hidetoshi Kasuya, and Katsuyoshi Mineura

Object

Because brainstem metastases are not deemed resectable, stereotactic radiosurgery (SRS) is the only treatment modality expected to achieve a radical cure. The authors describe their treatment results, focusing particularly on how long patients can survive without neurological deterioration following SRS for brainstem metastases.

Methods

This was an institutional review board–approved, retrospective cohort study in which the authors pulled from their database information on 2553 consecutive patients with brain metastases who underwent Gamma Knife surgery (GKS) at the Mito GammaHouse between July 1998 and July 2011. Among the 2553 patients, excluding cases in which there was meningeal dissemination, 200 cases of brainstem metastases (78 women and 122 men with a mean age of 64 years [range 36–86 years]) were identified and analyzed. The most common primary site was the lung (137 patients) followed by the gastrointestinal tract (24 patients), breast (17 patients), kidney (12 patients), and others (10 patients). Among the 200 patients, 15 patients (7.5%) harbored at least 2 tumors in the brainstem: 11 patients had 2 tumors, 2 patients had 3 tumors, and 1 patient each had 4 or 5 tumors. Therefore, a total of 222 tumors were irradiated. These 222 tumors were located in the pons (121 lesions), the midbrain (65 lesions), and the medulla oblongata (36 lesions). The mean and median tumor volumes were 1.3 and 0.2 cm3 (range 0.005–10.7 cm3), and the median peripheral radiation dose was 18.0 Gy (range 12.0–25.0 Gy).

Results

The overall median survival time (MST) was 6.0 months. Distribution of MSTs across Recursive Partitioning Analysis (RPA) classes showed that the MSTs were 9.4 months in Class I (20 patients), 6.0 months in Class II (171 patients), and 1.9 months in Class III (9 patients). Better Karnofsky Performance Scale score, single metastasis, and well-controlled primary tumor were significant predictive factors for longer survival. The neurological and qualitative survival rates were 90.8% and 89.2%, respectively, at 24 months post-GKS. Better KPS score and smaller tumor volume tended to be associated with prolonged qualitative survival. Follow-up imaging studies were available for 129 patients (64.5%). The tumor control rate was 81.8% at 24 months post-GKS. Smaller tumor volume tended to contribute to tumor control.

Conclusions

The present results indicate that GKS is effective in the treatment of brainstem metastases, particularly from the viewpoint of maintaining a good neurological condition in the patient.

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Letter to the Editor: Aneurysm rupture

Yasuhiro Kuroi, Kazufumi Suzuki, and Hidetoshi Kasuya

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Stereotactic radiosurgery for vestibular schwannomas: average 10-year follow-up results focusing on long-term hearing preservation

Shinya Watanabe, Masaaki Yamamoto, Takuya Kawabe, Takao Koiso, Tetsuya Yamamoto, Akira Matsumura, and Hidetoshi Kasuya

OBJECTIVE

The aim of this study was to reappraise long-term treatment outcomes of stereotactic radiosurgery (SRS) for vestibular schwannomas (VSs). The authors used a database that included patients who underwent SRS with a unique dose-planning technique, i.e., partial tumor coverage designed to avoid excess irradiation of the facial and cochlear nerves, focusing on tumor control and hearing preservation. Clinical factors associated with post-SRS tumor control and long-term hearing preservation were also analyzed.

METHODS

This institutional review board–approved, retrospective cohort study used the authors' prospectively accumulated database. Among 207 patients who underwent Gamma Knife SRS for VSs between 1990 and 2005, 183 (who were followed up for at least 36 post-SRS months) were studied. The median tumor volume was 2.0 cm3 (range 0.05–26.2 cm3). The median prescribed dose at the tumor periphery was 12.0 Gy (range 8.8–15.0 Gy; 12.0 Gy was used in 171 patients [93%]), whereas tumor portions facing the facial and cochlear nerves were irradiated with 10.0 Gy. As a result, 72%–99% of each tumor was irradiated with the prescribed dose. The mean cochlear doses ranged from 2.3 to 5.7 Gy (median 4.1 Gy).

RESULTS

The median durations of imaging and audiometric follow-up were 114 months (interquartile range 73–144 months) and 59 months (interquartile range 33–109 months), respectively. Tumor shrinkage was documented in 110 (61%), no change in 48 (27%), and enlargement in the other 22 (12%) patients. A further procedure (FP) was required in 15 (8%) patients. Thus, the tumor growth control rate was 88% and the clinical control rate (i.e., no need for an FP) was 92%. The cumulative FP-free rates were 96%, 93%, and 87% at the 60th, 120th, and 180th post-SRS month, respectively. Six (3%) patients experienced facial pain, and 2 developed transient facial palsy. Serviceable hearing was defined as a pure tone audiogram result better than 50 dB. Among the 66 patients with serviceable hearing before SRS who were followed up, hearing acuity was preserved in 23 (35%). Actuarial serviceable hearing preservation rates were 49%, 24%, and 12% at the 60th, 120th, and 180th post-SRS month, respectively. On univariable analysis, only cystic-type tumor (HR 3.36, 95% CI 1.18–9.36; p = 0.02) was shown to have a significantly unfavorable association with FP. Multivariable analysis followed by univariable analysis revealed that higher age (≥ 65 years: HR 2.66, 95% CI 1.16–5.92; p = 0.02), larger tumor volume (≥ 8 cm3: HR 5.36, 95% CI 1.20–17.4; p = 0.03), and higher cochlear dose (mean cochlear dose > 4.2 Gy: HR 2.22, 95% CI 1.07–4.77; p = 0.03) were unfavorable factors for hearing preservation.

CONCLUSIONS

Stereotactic radiosurgery achieved good long-term results in this series. Tumor control was acceptable, and there were few serious complications in patients with small- to medium-sized VSs. Unfortunately, hearing preservation was not satisfactory. However, the longer the observation period, the more important it becomes to compare post-SRS hearing decreases with the natural decline in untreated cases.

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Characterization of functional outcome and quality of life following subarachnoid hemorrhage in patients treated with and without nicardipine prolonged-release implants

Clinical article

Martin Barth, Claudius Thomé, Peter Schmiedek, Christel Weiss, Hidetoshi Kasuya, and Peter Vajkoczy

Object

The use of nicardipine prolonged-release implants (NPRIs) is associated with a significant improvement in the therapy of patients suffering from aneurysmal subarachnoid hemorrhage (aSAH) regarding the occurrence and severity of cerebral vasospasm, new infarcts, and functional outcome (FO). Because quality of life (QOL) measurements more reliably seem to describe the patient's true condition, the present study was conducted to assess FO and QOL 1 year after aneurysm rupture in patients with and without NPRIs.

Methods

From the initial series of 32 patients, 18 were assessed 1 year after aSAH (7 of the control and 11 of the NPRI group). The patients underwent neurological investigation, a structured interview followed by a measurement of QOL (Mini-Mental State Examination [MMSE]; 36-Item Short Form Health Survey [SF-36]; and the Hamilton Depression Rating Scale). There were no intergroup differences in the patient characteristics (that is, localization of aneurysm, initial Hunt and Hess grade, or age).

Results

In addition to the previously reported improvement of the National Institutes of Health Stroke Scale and modified Rankin Scale scores, the NPRI group's Karnofsky Performance Scale and the MMSE scores were markedly to significantly improved (p < 0.05 [Karnofsky Performance Scale] and p = 0.053 [MMSE]). In contrast, anxiety, oblivion, and mild symptoms of depression were equally present in both study groups (p = 0.607 [anxiety]; p = 0.732 [oblivion]; and p = 0.509 [Hamilton Depression Rating Scale]). Furthermore, no intergroup differences were observed in any of the SF-36 domains. The scores in the SF-36 domains of Role-Physical, Vitality, and Role-Emotional were significantly reduced in the NRPI group compared with those observed in an age-matched control population (p < 0.001 [Role-Physical]; p = 0.001 [vitality]; and p = 0.01 [Role-Emotional]). Considering consequent costs, no difference was detectable regarding the duration of in- and outpatient rehabilitation (p = 0.135 and 0.171, respectively) or the Prolo score (p = 0.094).

Conclusions

Despite FO improvement in terms of a lower incidence of cerebral vasospasm, new infarcts, morbidity in the treatment of aSAH in patients with NPRIs, a patient's QOL seems to be related to the severity of the aSAH itself.

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Nitric oxide synthase and guanylate cyclase levels in canine basilar artery after subarachnoid hemorrhage

Hidetoshi Kasuya, Bryce K. A. Weir, Masaki Nakane, Jennifer S. Pollock, Lydia Johns, Linda S. Marton, and Kari Stefansson

✓ Endothelium-dependent vasodilation may be impaired during cerebral vasospasm following subarachnoid hemorrhage. Under normal circumstances nitric oxide (NO) released by endothelial cells induces relaxation of smooth muscle by activating the soluble form of guanylate cyclase within muscle cells. In this study the levels of both endothelial NO synthase, the enzyme that produces NO, and soluble guanylate cyclase were determined in canine basilar arteries in a double-hemorrhage model using Western blot immunoassays. Thirty dogs were assigned to three groups: Group D0, control; Group D2, dogs sacrificed 2 days after cisternal injection of blood; and Group D7, dogs given double cisternal injections of blood and sacrificed 7 days after the first injection. Constriction of the basilar artery was confirmed by arterial angiography. Portions of the affected arteries or the corresponding region in control animals were solubilized for sodium dodecylsulfate—polyacrylamide gel electrophoresis and Western blotting. A specific monoclonal antibody against endothelial NO synthase was used. The extract from basilar arteries showed two bands on the blots: 135 kD, characteristic of endothelial NO synthase, and 120 kD, which may be a degradation product of the enzyme. The densitometer values of the bands were presented as percentages of D0 control values. Although the total signal in the D7 group was less than that of the D0 control group (D2, 97% ± 22%; D7, 78% ± 40%), it was not statistically significant. The proportion of the 135-kD form decreased between Groups D0 and D7, but the difference was not significant. A single major band corresponding to the α-subunit of soluble guanylate cyclase was seen at 70 kD in the basilar artery extracts. The signals of D2 and D7 samples were 69%± 40% and 25% ± 18%, respectively. There was a significant difference between D7 and D0 (p < 0.001). The reduced expression of soluble guanylate cyclase may be related to the impairment of endothelium-dependent vasodilation in vasospasm.

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Three-stage Gamma Knife treatment for metastatic brain tumors larger than 10 cm3: a 2-institute study including re-analyses of earlier results using competing risk analysis

Masaaki Yamamoto, Yoshinori Higuchi, Toru Serizawa, Takuya Kawabe, Osamu Nagano, Yasunori Sato, Takao Koiso, Shinya Watanabe, Hitoshi Aiyama, and Hidetoshi Kasuya

OBJECTIVE

The results of 3-stage Gamma Knife treatment (3-st-GK-Tx) for relatively large brain metastases have previously been reported for a series of patients in Chiba, Japan (referred to in this study as the C-series). In the current study, the authors reappraised, using a competing risk analysis, the efficacy and safety of 3-st-GK-Tx by comparing their experience with that of the C-series.

METHODS

This was a retrospective cohort study. Among 1767 patients undergoing GK radiosurgery for brain metastases at Mito Gamma House during the 2005–2015 period, 78 (34 female, 44 male; mean age 65 years, range 35–86 years) whose largest tumor was > 10 cm3, treated with 3-st-GK-Tx, were studied (referred to in this study as the M-series). The target volumes were covered with a 50% isodose gradient and irradiated with a peripheral dose of 10 Gy at each procedure. The interval between procedures was 2 weeks. Because competing risk analysis had not been employed in the published C-series, the authors reanalyzed the previously published data using this method.

RESULTS

The overall median survival time after 3-st-GK-Tx was 8.3 months (95% CI 5.6–12.0 months) in the M-series and 8.6 months (95% CI 5.5–10.6 months) in the C-series (p = 0.41). Actuarial survival rates at the 6th and 12th post–3-st-GK-Tx months were, respectively, 55.1% and 35.2% in the M-series and 62.5% and 26.4% in the C-series (HR 1.175, 95% CI 0.790–1.728, p = 0.42). Cumulative incidences at the 12th post–3-st-GK-Tx, determined by competing risk analyses, of neurological deterioration (14.2% in C-series vs 12.8% in M-series), neurological death (7.2% vs 7.7%), local recurrence (4.8% vs 6.2%), repeat SRS (25.9% vs 18.0%), and SRS-related complications (2.3% vs 5.1%) did not differ significantly between the 2 series.

CONCLUSIONS

There were no significant differences in post–3-st-GK-Tx results between the 2 series in terms of overall survival times, neurological death, maintained neurological status, local control, repeat SRS, and SRS-related complications. The previously published results (C-series) are considered to be validated by the M-series results.

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Prognostic grading system specifically for elderly patients with brain metastases after stereotactic radiosurgery: a 2-institution study

Masaaki Yamamoto, Toru Serizawa, Yoshinori Higuchi, Osamu Nagano, Hitoshi Aiyama, Takao Koiso, Shinya Watanabe, Takuya Kawabe, Yasunori Sato, and Hidetoshi Kasuya

OBJECTIVE

With the aging of the population, increasing numbers of elderly patients with brain metastasis (BM) are undergoing stereotactic radiosurgery (SRS). Among recently reported prognostic grading indexes, only the basic score for brain metastases (BSBM) is applicable to patients 65 years or older. However, the major weakness of this system is that no BM-related factors are graded. This prompted the authors to develop a new grading system, the elderly-specific (ES)–BSBM.

METHODS

For this IRB-approved, retrospective cohort study, the authors used their prospectively accumulated database comprising 3267 consecutive patients undergoing Gamma Knife SRS for BMs during the 1998–2016 period at the Mito GammaHouse. Among these 3267 patients, 1789 patients ≥ 65 years of age were studied (Yamamoto series [Y-series]). Another series of 1785 patients ≥ 65 years of age in whom Serizawa and colleagues performed Gamma Knife SRS during the same period (Serizawa series [S-series]) was used for validity testing of the ES-BSBM.

RESULTS

Two factors were identified as strongly impacting longer survival after SRS by means of multivariable analysis using the Cox proportional hazard model with a stepwise selection procedure. These factors are the number of tumors (solitary vs multiple: HR 1.450, 95% CI 1.299–1.621; p < 0.0001) and cumulative tumor volume (≤ 15 cm3 vs > 15 cm3: HR 1.311, 95% CI 1.078–1.593; p = 0.0067). The new index is the addition of scores 0 and 1 for these 2 factors to the BSBM. The ES-BSBM system is based on categorization into 3 classes by adding these 2 scores to those of the original BSBM. Each ES-BSBM category has 2 possible scores. For the category ES-BSBM 4–5, the score is either 4 or 5; for ES-BSBM 2–3, the score is either 2 or 3; and for ES-BSBM 0–1, the score is either 0 or 1. In the Y-series, the median survival times (MSTs, months) after SRS were 17.5 (95% CI 15.4–19.3) in ES-BSBM 4–5, 6.9 (95% CI 6.4–7.4) in ES-BSBM 2–3, and 2.8 (95% CI 2.5–3.6) in ES-BSBM 0–1 (p < 0.0001). Also, in the S-series, MSTs were, respectively, 20.4 (95% CI 17.2–23.4), 7.9 (95% CI 7.4–8.5), and 3.2 (95% CI 2.8–3.6) (p < 0.0001). The ES-BSBM system was shown to be applicable to patients with all primary tumor types as well as to those 80 years or older.

CONCLUSIONS

The authors found that the addition of the number of tumors and cumulative tumor volume as scoring factors to the BSBM system significantly improved the prognostic value of this index. The present study is strengthened by testing the ES-BSBM in a different patient group.

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Stereotactic radiosurgery for brain metastases: a case-matched study comparing treatment results for patients 80 years of age or older versus patients 65–79 years of age

Clinical article

Shinya Watanabe, Masaaki Yamamoto, Yasunori Sato, Takuya Kawabe, Yoshinori Higuchi, Hidetoshi Kasuya, Tetsuya Yamamoto, Akira Matsumura, and Bierta E. Barfod

Object

Recently, an increasing number of patients with brain metastases, even patients over 80 years of age, have been treated with stereotactic radiosurgery (SRS). However, there is little information on SRS treatment results for patients with brain metastases 80 years of age and older. The authors undertook this study to reappraise whether SRS treatment results for patients 80 years of age or older differ from those of patients who are 65–79 years old.

Methods

This was an institutional review board–approved, retrospective cohort study. Among 2552 consecutive brain metastasis patients who underwent SRS during the 1998–2011 period, we studied 165 who were 80 years of age or older (Group A) and 1181 who were age 65–79 years old (Group B). Because of the remarkable disproportion in patient numbers between the 2 groups and considerable differences in pre-SRS clinical factors, the authors conducted a case-matched study using the propensity score matching method. Ultimately, 330 patients (165 from each group, A and B) were selected. For time-to-event outcomes, the Kaplan-Meier method was used to estimate overall survival and competing risk analysis was used to estimate other study end points, as appropriate.

Results

Although the case-matched study showed that post-SRS median survival time (MST, months) was shorter in Group A patients (5.3 months, 95% CI 3.9–7.0 months) than in Group B patients (6.9 months, 95% CI 5.0–8.1 months), this difference was not statistically significant (HR 1.147, 95% CI 0.921–1.429, p = 0.22). Incidences of neurological death and deterioration were slightly lower in Group A than in Group B patients (6.3% vs 11.8% and 8.5% vs 13.9%), but these differences did not reach statistical significance (p = 0.11 and p = 0.16). Furthermore, competing risk analyses showed that the 2 groups did not differ significantly in cumulative incidence of local recurrence (HR 0.830, 95% CI 0.268–2.573, p = 0.75), rates of repeat SRS (HR 0.738, 95% CI 0.438–1.242, p = 0.25), or incidence of SRS-related complications (HR 0.616, 95% CI 0.152–2.495, p = 0.49). Among the Group A patients, post-SRS MSTs were 11.6 months (95% CI 7.8–19.6 months), 7.9 months (95% CI 5.2–10.9 months), and 2.8 months (95% CI; 2.4–4.6 months) in patients whose disease status was modified–recursive partitioning analysis (RPA) Class(es) I+IIa, IIb, and IIc+III, respectively (p < 0.001).

Conclusions

Our results suggest that patients 80 years of age or older are not unfavorable candidates for SRS as compared with those 65–79 years old. Particularly, even among patients 80 years and older, those with modified-RPA Class I+IIa or IIb disease are considered to be favorable candidates for more aggressive treatment of brain metastases.

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Follow-up results of brain metastasis patients undergoing repeat Gamma Knife radiosurgery

Takao Koiso, Masaaki Yamamoto, Takuya Kawabe, Shinya Watanabe, Yasunori Sato, Yoshinori Higuchi, Tetsuya Yamamoto, Akira Matsumura, and Hidetoshi Kasuya

OBJECTIVE

Stereotactic radiosurgery (SRS) without upfront whole-brain radiotherapy (WBRT) has influenced recent treatment recommendations for brain metastasis patients. However, in brain metastasis patients who undergo SRS alone, new brain metastases inevitably appear with relatively high incidences during post-SRS follow-up. However, little is known about the second SRS results. The treatment results of second SRS were retrospectively reviewed, mainly for newly developed or, uncommonly, for recurrent brain metastases in order to reappraise the efficacy of this treatment strategy with a special focus on the maintenance of neurological status and safety.

METHODS

This was an institutional review board–approved, retrospective cohort study that used a prospectively accumulated database, including 3102 consecutive patients with brain metastases who underwent SRS between July 1998 and June 2015. Among these 3102 patients, 859 (376 female patients; median age 64 years; range 21–88 years) who underwent a second SRS without WBRT were studied with a focus on overall survival, neurological death, neurological deterioration, local recurrence, salvage SRS, and SRS-induced complications after the second SRS. Before the second SRS, the authors also investigated the clinical factors and radiosurgical parameters likely to influence these clinical outcomes. For the statistical analysis, the standard Kaplan-Meier method was used to determine post–second SRS survival and neurological death. A competing risk analysis was applied to estimate post–second SRS cumulative incidences of local recurrence, neurological deterioration, salvage SRS, and SRS-induced complications.

RESULTS

The post–second SRS median survival time was 7.4 months (95% CI 7.0–8.2 months). The actuarial survival rates were 58.2% and 34.7% at 6 and 12 months after the second SRS, respectively. Among 789 deceased patients, the causes of death could not be determined in 24 patients, but were confirmed in the remaining 765 patients to be nonbrain diseases in 654 (85.5%) patients and brain diseases in 111 (14.5%) patients. The actuarial neurological death–free survival rates were 94.4% and 86.6% at 6 and 12 months following the second SRS. Multivariable analysis revealed female sex, Karnofsky Performance Scale score of 80% or greater, better modified recursive partitioning analysis class, smaller tumor numbers, and higher peripheral dose to be significant predictive factors for longer survival. The cumulative incidences of local recurrence were 11.2% and 14.9% at 12 and 24 months after the second SRS. The crude incidence of neurological deterioration was 7.1%, and the respective cumulative incidences were 4.5%, 5.8%, 6.7%, 7.2%, and 7.5% at 12, 24, 36, 48, and 60 months after the second SRS. SRS-induced complications occurred in 25 patients (2.9%) after a median post–second SRS period of 16.8 months (range 0.6–95.0 months; interquartile range 5.6–29.3 months). The cumulative incidences of complications were 1.4%, 2.0%, 2.4%, 3.0%, and 3.0% at 12, 24, 36, 48, and 60 months after the second SRS, respectively.

CONCLUSIONS

Carefully selected patients with recurrent tumors—either new or locally recurrent—are favorable candidates for a second SRS, particularly in terms of neurological status maintenance and the safety of this treatment strategy.

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Influence of endothelial nitric oxide synthase T-786C single nucleotide polymorphism on aneurysm size

Hiroyuki Akagawa, Hidetoshi Kasuya, Hideaki Onda, Taku Yoneyama, Atsushi Sasahara, Chul-Jin Kim, Jung-Chung Lee, Tae-Ki Yang, Tomokatsu Hori, and Ituro Inoue

Object. Among patients with aneurysms, those with heterozygous (T/C) endothelial nitric oxide synthase (eNOS) T-786C single nucleotide polymorphism (SNP), a mutation reducing endothelial nitric oxide synthesis, are reported to have larger ruptured intracranial aneurysms (IAs) than those with homozygous (C/C or T/T) genotype. The authors tested patients harboring aneurysms for eNOS T-786C SNP in two populations—Japanese and Korean.

Methods. The eNOS T-786C SNP was genotyped through direct sequencing in genomic DNA obtained from 336 Japanese and 191 Korean patients with IAs and 214 Japanese and 191 Korean control volunteers. Differences in genotype frequencies among the various aneurysm sizes were evaluated using the Fisher exact test.

There was no significant difference in heterozygous (T/C) eNOS T-786C SNP between aneurysms 5 mm or smaller and those from 6 to 9 mm, and between lesions 5 mm or smaller and those 10 mm or larger in 336 Japanese patients harboring aneurysms—220 with ruptured and 116 with unruptured lesions—and in 191 Korean patients with ruptured aneurysms.

Conclusion. The eNOS T-786C SNP genotype does not influence the size of aneurysms.