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Activated complement components C3a and C4a in cerebrospinal fluid and plasma following subarachnoid hemorrhage

Hidetoshi Kasuya and Takashi Shimizu

✓ The cerebrospinal fluid (CSF) and plasma levels of the complement components C3a and C4a in 40 patients suffering from subarachnoid hemorrhage (SAH) were quantitated by radioimmunoassay. Serial measurements of the lumbar CSF levels revealed that the C3a and C4a levels were significantly elevated in the initial stage of SAH, but decreased rapidly. Within 48 hours after SAH, the mean C3a and C4a levels in the cisternal, lumbar, and ventricular CSF were significantly higher in patients with delayed ischemic neurological deficits (DIND) than in those without DIND. The serially measured plasma levels of C3a and C4a in patients with DIND were elevated more than in those without DIND, but they did not show a significant change over time. Simultaneous levels of fibrinopeptide A (FPA), an indicator of thrombin activity in CSF, were also measured by radioimmunoassay. There was a significant correlation between CSF-activated complement components and CSF FPA. These results suggest that complement activation occurred in the subarachnoid space soon after SAH, chiefly due to activation of the coagulation system. The higher CSF levels of C3a and C4a in patients with DIND may indicate a relationship between these components and the pathogenesis of cerebral vasospasms.

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Change in circulating blood volume following craniotomy

Kenichi Hirasawa, Hidetoshi Kasuya, and Tomokatsu Hori

Object. The importance of monitoring circulating blood volume (CBV) during perioperative management is widely recognized in critically ill patients. The purpose of this study was to investigate the change in CBV following craniotomy by using indocyanine-green pulse spectrophotometry.

Methods. Circulating blood volume and plasma hormones related to stress and fluid regulation were measured five times: preoperatively, immediately postoperatively, and 1, 2, and 7 days after craniotomy was performed in 17 patients with a brain tumor or an unruptured aneurysm.

The mean value of CBV preoperatively was 82 ml/kg, which decreased to 64 ml/kg (78%) immediately postoperatively and gradually recovered to 82 ml/kg on Day 7 postsurgery (p = 0.0069). The mean values of adrenaline, noradrenaline, arginine vasopressin, renin, and aldosterone were highest immediately postoperatively. The mean intraoperative balances of water and sodium were 1090 ml and 113 mEq, respectively. Partial correlation coefficients of CBV to noradrenaline and serum sodium during the entire study were −0.430 (p = 0.0036) and 0.418 (p = 0.0048), respectively.

Conclusions. Attention should be paid to decreased CBV following craniotomy, which is caused by the shift of fluid to interstitial spaces due to surgical stress. Hypovolemia can be suspected from a postoperative decrease in serum sodium.

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Diagnosis of vascular compression in facial spasm by stereoscopic short-range magnetic resonance angiography

Technical note

Takashi Shimizu, Hiroto Kawasaki, Hidetoshi Kasuya, and Koki Kurita

✓ The authors describe the use of stereoscopic short-range magnetic resonance (MR) angiography to diagnose whether and by what means the brainstem is compressed in a case of facial spasm. The MR images were obtained on a 1.5-tesla imaging system with three-dimensional time-of-flight pulse sequence (repetition time 39 msec, echo time 9 msec). Six-source MR images, in which the internal acoustic meatuses were described, were processed using a maximum-intensity projection technique to reconstruct the MR angiograms. The internal acoustic meatuses, the posterior fossa, and the nearby arteries are shown on a single MR angiogram. When two MR angiograms with projection angles 10° apart are placed side by side and observed through polarized glasses, a stereoscopic view of the compressing artery can easily be seen.

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Mechanism of oxyhemoglobin-induced release of endothelin-1 from cultured vascular endothelial cells and smooth-muscle cells

Hidetoshi Kasuya, Bryce K. A. Weir, David M. White, and Kari Stefansson

✓ Release of endothelin-1 from cultured endothelial cells can be induced with oxyhemoglobin (oxyHb). The present study was conducted to explore whether oxyHb affects the release of endothelin-1 and the induction of endothelin-1 messenger ribonucleic acid (mRNA) and to examine the mechanism whereby oxyHb induces endothelin-1 production in cultured vascular smooth-muscle cells as well as in cultured endothelial cells.

Oxyhemoglobin produces concentration-dependent (0.1 to 10 µM) and time-dependent (0 to 24 hours) increases in immunoreactive endothelin-1 in conditioned medium from bovine arterial endothelial cells. Oxyhemoglobin induces immunoreactive endothelin-1 in rat aortic smooth-muscle cells in the same fashion, although the rate is 30-fold less than that of endothelial cells. This promoting effect is much higher than that of other stimulators such as thrombin and phorbol 12-myristate 13-acetate. Northern blot analysis of total RNA from endothelial cells also showed endothelin-1 mRNA induction. Staurosporine, a protein kinase C (PKC) inhibitor inhibited oxyHb-induced endothelin-1 production in both vascular endothelial and smooth-muscle cells, whereas an increase of intracellular cyclic adenosine monophosphate (cAMP) by forskolin or an addition of 8-bromo-cAMP only inhibited this effect in smooth-muscle cells.

These findings suggest that oxyHb-induced endothelin-1 production in endothelial cells is regulated by PKC, and in smooth-muscle cells by both PKC and the cAMP-dependent pathway. The production of endothelin, the most potent vasoconstrictor, in both vascular endothelial and smooth-muscle cells by oxyHb may have significance in the pathogenesis of cerebral vasospasm.

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Fisher's Classification

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Statistical Techniques and Vasospasm

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Using endothelial nitric oxide synthase gene polymorphisms to identify intracranial aneurysms more prone to rupture in Japanese patients

Boris Krischek, Hidetoshi Kasuya, Hiroyuki Akagawa, Atsushi Tajima, Akira Narita, Hideaki Onda, Tomokatsu Hori, and Ituro Inoue

Object

Recent investigators found that the presence of three tandem polymorphisms of the endothelial nitric oxide synthase (eNOS) gene—promoter single nucleotide polymorphism (SNP) T-786C, intron-4 27-bp variable number of tandem repeats, and the G894T SNP in exon 7—was indicative of intracranial aneurysms more prone to rupture in a Caucasian patient sample. In the present study, the authors sought to determine whether the presence of these eNOS polymorphisms could indicate which Japanese patients with aneurysms were more endangered by a subarachnoid hemorrhage (SAH).

Methods

The three eNOSpolymorphisms were genotyped in 297 patients with ruptured aneurysms (RAs), 108 patients with unruptured aneurysms (UAs), and 176 healthy volunteers by using polymerase chain reaction.

The distribution of the variant alleles did not differ significantly (p > 0.05) between the RA group and the UA group. The frequency of the corresponding genotypes between the two groups and a haplotype analysis did not show any significant differences. Further comparisons of the RA and UA groups with the control group did not yield any significant allele or genotype frequency differences.

Conclusions

These data show that the examined set of eNOS polymorphisms were not indicative of which Japanese patients with intracranial aneurysms would suffer an SAH. The presence of eNOS polymorphisms is not useful in identifying intracranial aneurysms that are more prone to rupture in a Japanese patient sample.

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Long-term follow-up results of intentional 2-stage Gamma Knife surgery with an interval of at least 3 years for arteriovenous malformations larger than 10 cm3

Clinical article

Masaaki Yamamoto, Atsuya Akabane, Yuji Matsumaru, Yoshinori Higuchi, Hidetoshi Kasuya, and Yoichi Urakawa

Object

Little information is available on staged Gamma Knife surgery (GKS) with an interval of 3 years or more when used to treat arteriovenous malformations (AVMs) with volumes larger than 10 cm3. The goal of this study was to increase knowledge in this area by reporting the authors' experience.

Methods

The authors describe an institutional review board–approved retrospective study in which they examined databases including information on 250 patients who consecutively underwent GKS for cerebral AVMs during a 16-year period (1988–2004). Among the 250 patients the authors identified 31 patients (12.4%, 15 female and 16 male patients with a mean age of 29 years [range 10–63 years]) in whom 2-stage GKS was intentionally planned at the time of initial treatment because the volume of the AVM nidus was larger than 10 cm3. The most common presentation was bleeding (14 patients), followed by seizures (9 patients), incidental findings (7 patients), and headache with scintillation (1 patient). One patient underwent GKS for the treatment of 2 AVMs simultaneously, and thus 32 AVMs are included in this study. The mean nidus volume was 16.2 cm3 (maximum 55.8 cm3). In all 31 patients, relatively low radiation doses (12–16 Gy directed at the periphery of the lesion) were intentionally used for the first GKS. The second GKS was scheduled for at least 36 months after the first.

Results

Complete nidus obliteration was obtained after the first GKS in 1 patient. To date, 26 patients have undergone a second procedure with a post-GKS mean interval of 41 months (range 24–83 months); 2 other patients refused to undergo the second GKS, and no further treatment was given because of severe morbidity in 1 case and death due to bleeding in the other case. Among the 26 patients who did undergo a second procedure, 3 patients refused follow-up digital subtraction (DS) angiography, another is scheduled for follow-up DS angiography, and 2 patients died, one of bleeding and the other of an unknown cause. The remaining 20 patients underwent follow-up DS angiography. Complete nidus obliteration was confirmed in 13 patients (65.0%) and remarkable nidus shrinkage in the other 7 patients (35.0%). In 2 of these 7 patients, a third GKS achieved complete nidus obliteration. Therefore, the cumulative complete obliteration rate in this series was 76.2% (16 of 21 eligible patients). Seven patients (22.6%) experienced bleeding. The bleeding rates were 9.7%, 16.1%, 16.1%, and 26.1%, respectively, at 1, 2, 5, and 10 years post-GKS. There were 2 deaths and 3 cases of morbidity (persistent coma, mild hemimotor weakness, and hemianopsia in 1 patient each). Hemorrhage did not produce neurological deficits in the other 2 patients. During the mean post-GKS follow-up period of 105 months (range 42–229 months) to date, mild symptomatic GKS-related complications occurred in 2 patients (6.5%); these were classified as Radiation Oncology Group Neurotoxicity Grade 1 in 1 patient and Grade 2 in the other. Among various pre-GKS clinical factors, univariate analysis showed only patient age to impact complications (hazard ratio 0.675, 95% CI 0.306–0.942, p = 0.0085). The rate of complications in the pediatric cases was 33.3%, whereas that in the adolescent and adult cases was 0% (p = 0.0323).

Conclusions

Although a final conclusion awaits further studies and patient follow-up, these results suggest 2-stage GKS to be beneficial even for relatively large AVMs.

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A case-matched study of stereotactic radiosurgery for patients with multiple brain metastases: comparing treatment results for 1–4 vs ≥ 5 tumors

Clinical article

Masaaki Yamamoto, Takuya Kawabe, Yasunori Sato, Yoshinori Higuchi, Tadashi Nariai, Bierta E. Barfod, Hidetoshi Kasuya, and Yoichi Urakawa

Object

Although stereotactic radiosurgery (SRS) alone for patients with 4–5 or more tumors is not a standard treatment, a trend for patients with 5 or more tumors to undergo SRS alone is already apparent. The authors' aim in the present study was to reappraise whether SRS results for ≥ 5 tumors differ from those for 1–4 tumors.

Methods

This institutional review board–approved retrospective cohort study used the authors' database of prospectively accumulated data that included 2553 consecutive patients who underwent SRS, not in combination with concurrent whole-brain radiotherapy, for brain metastases (METs) between 1998 and 2011. These 2553 patients were divided into 2 groups: 1553 with tumor numbers of 1–4 (Group A) and 1000 with ≥ 5 tumors (Group B). Because there was considerable bias in pre-SRS clinical factors between Groups A and B, a case-matched study was conducted. Ultimately, 1096 patients (548 each in Groups A and B) were selected. The standard Kaplan-Meier method was used to determine post-SRS survival and the post-SRS neurological death–free survival times. Competing risk analysis was applied to estimate cumulative incidences of local recurrence, repeat SRS for new lesions, neurological deterioration, and SRS-induced complications.

Results

The post-SRS median survival time was significantly longer in the 548 Group A patients (7.9 months, 95% CI 7.0–8.9 months) than in the 548 Group B patients (7.0 months 95% [CI 6.2–7.8 months], HR 1.176 [95% CI 1.039–1.331], p = 0.01). However, incidences of neurological death were very similar: 10.6% in Group A and 8.2% in Group B (p = 0.21). There was no significant difference between the groups in neurological death–free survival intervals (HR 0.945, 95% CI 0.636–1.394, p = 0.77). Furthermore, competing risk analyses showed that there were no significant differences between the groups in cumulative incidences of local recurrence (HR 0.577, 95% CI 0.312–1.069, p = 0.08), repeat SRS (HR 1.133, 95% CI 0.910–1.409, p = 0.26), neurological deterioration (HR 1.868, 95% CI 0.608–1.240, p = 0.44), and major SRS-related complications (HR 1.105, 95% CI 0.490–2.496, p = 0.81).

In the authors' cohort, age ≤ 65 years, female sex, a Karnofsky Performance Scale score ≥ 80%, cumulative tumor volume ≤ 10 cm3, controlled primary cancer, no extracerebral METs, and neurologically asymptomatic status were significant factors favoring longer survival equally in both groups.

Conclusions

This retrospective study suggests that increased tumor number is an unfavorable factor for longer survival. However, the post-SRS median survival time difference, 0.9 months, between the two groups is not clinically meaningful. Furthermore, patients with 5 or more METs have noninferior results compared to patients with 1–4 tumors, in terms of neurological death, local recurrence, repeat SRS, maintenance of good neurological state, and SRS-related complications. A randomized controlled trial should be conducted to test this hypothesis.

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Stereotactic radiosurgery for patients with multiple brain metastases: a case-matched study comparing treatment results for patients with 2–9 versus 10 or more tumors

Clinical article

Masaaki Yamamoto, Takuya Kawabe, Yasunori Sato, Yoshinori Higuchi, Tadashi Nariai, Shinya Watanabe, and Hidetoshi Kasuya

Object

Although stereotactic radiosurgery (SRS) alone is not a standard treatment for patients with 4–5 tumors or more, a recent trend has been for patients with 5 or more, or even 10 or more, tumors to undergo SRS alone. The aim of this study was to reappraise whether the treatment results for SRS alone for patients with 10 or more tumors differ from those for patients with 2–9 tumors.

Methods

This was an institutional review board–approved, retrospective cohort study that gathered data from the Katsuta Hospital Mito GammaHouse prospectively accumulated database. Data were collected for 2553 patients who consecutively had undergone Gamma Knife SRS alone, without whole-brain radiotherapy (WBRT), for newly diagnosed (mostly) or recurrent (uncommonly) brain metastases during 1998–2011. Of these 2553 patients, 739 (28.9%) with a single tumor were excluded, leaving 1814 with multiple metastases in the study. These 1814 patients were divided into 2 groups: those with 2–9 tumors (Group A, 1254 patients) and those with 10 or more tumors (Group B, 560 patients). Because of considerable bias in pre-SRS clinical factors between groups A and B, a case-matched study, which used the propensity score matching method, was conducted for clinical factors (i.e., age, sex, primary tumor state, extracerebral metastases, Karnofsky Performance Status, neurological symptoms, prior procedures [surgery and WBRT], volume of the largest tumor, and peripheral doses). Ultimately, 720 patients (360 in each group) were selected. The standard Kaplan-Meier method was used to determine post-SRS survival times and post-SRS neurological death–free survival times. Competing risk analysis was applied to estimate cumulative incidence for local recurrence, repeat SRS for new lesions, neurological deterioration, and SRS-induced complications.

Results

Post-SRS median survival times did not differ significantly between the 2 groups (6.8 months for Group A vs 6.0 months for Group B; hazard ratio [HR] 1.133, 95% CI 0.974–1.319, p = 0.10). Furthermore, rates of neurological death were very similar: 10.0% for group A and 9.4% for group B (p = 0.89); neurological death–free survival times did not differ significantly between the 2 groups (HR 1.073, 95% CI 0.649–1.771, p = 0.78). The cumulative incidence of local recurrence (HR 0.425, 95% CI 0.0.181–0.990, p = 0.04) and repeat SRS for new lesions (HR 0.732, 95% CI 0.554–0.870, p = 0.03) were significantly lower for Group B than for Group A patients. No significant differences between the groups were found for cumulative incidence for neurological deterioration (HR 0.994, 95% CI 0.607–1.469, p = 0.80) or SRS-related complications (HR 0.541, 95% CI 0.138–2.112, p = 0.38).

Conclusions

Post-SRS treatment results (i.e., median survival time; neurological death–free survival times; and cumulative incidence for local recurrence, repeat SRS for new lesions, neurological deterioration, and SRS-related complications) were not inferior (neither less effective nor less safe) for patients in Group B than for those in Group A. We conclude that carefully selected patients with 10 or more tumors are not unfavorable candidates for SRS alone. A randomized controlled trial should be conducted to test this hypothesis.