Aneurysm location and clipping versus coiling for development of secondary normal-pressure hydrocephalus after aneurysmal subarachnoid hemorrhage: Japanese Stroke DataBank

Full access

OBJECT

The present study aimed to investigate aneurysm locations and treatments for ruptured cerebral aneurysms associated with secondary normal-pressure hydrocephalus (sNPH) after subarachnoid hemorrhage (SAH) by using comprehensive data from the Japanese Stroke DataBank.

METHODS

Among 101,165 patients with acute stroke registered between 2000 and 2013, 4693 patients (1482 men, 3211 women) were registered as having had an SAH caused by a ruptured saccular aneurysm. Of them, 1448 patients (438 men and 1010 women; mean age 61.9 ± 13.4 years) who were confirmed to have or not have coexisting acute hydrocephalus and sNPH were included for statistical analyses. Locations of the ruptured aneurysms were subcategorized into 1 of the following 4 groups: middle cerebral artery (MCA; n = 354), anterior communicating artery and anterior cerebral artery (ACA; n = 496), internal carotid artery (ICA; n = 402), and posterior circulation (n = 130). Locations of 66 of the ruptured aneurysms were unknown/unrecorded. Treatments included craniotomy and clipping alone in 1073 patients, endovascular coil embolization alone in 285 patients, and a combination of coiling and clipping in 17 patients. The age-adjusted and multivariate odds ratios from logistic regression analyses were calculated after stratification using the Fisher CT scale to investigate the effects of the hematoma volume of SAH.

RESULTS

Acute hydrocephalus was confirmed in 593 patients, and 521 patients developed sNPH. Patients with a ruptured ACA aneurysm had twice the risk for sNPH over those with a ruptured MCA aneurysm. Those with an ACA aneurysm with Fisher Grade 3 SAH had a 9-fold-higher risk for sNPH than those with an MCA aneurysm with Fisher Grade 1 or 2 SAH. Patients with a ruptured posterior circulation aneurysm did not have any significant risk for sNPH. Clipping of the ruptured aneurysm resulted in twice the risk for sNPH over coil embolization alone.

CONCLUSIONS

Patients with low-grade SAH caused by a ruptured MCA aneurysm had a low risk for the development of sNPH. In contrast, patients with high-grade SAH caused by a ruptured ACA aneurysm had a higher risk for sNPH. Endovascular coiling might confer a lower risk of developing sNPH than microsurgical clipping.

ABBREVIATIONSACA = anterior cerebral artery; ICA = internal carotid artery; MCA = middle cerebral artery; NPH = normal-pressure hydrocephalus; SAH = subarachnoid hemorrhage; sNPH = secondary NPH; WFNS = World Federation of Neurological Societies.

OBJECT

The present study aimed to investigate aneurysm locations and treatments for ruptured cerebral aneurysms associated with secondary normal-pressure hydrocephalus (sNPH) after subarachnoid hemorrhage (SAH) by using comprehensive data from the Japanese Stroke DataBank.

METHODS

Among 101,165 patients with acute stroke registered between 2000 and 2013, 4693 patients (1482 men, 3211 women) were registered as having had an SAH caused by a ruptured saccular aneurysm. Of them, 1448 patients (438 men and 1010 women; mean age 61.9 ± 13.4 years) who were confirmed to have or not have coexisting acute hydrocephalus and sNPH were included for statistical analyses. Locations of the ruptured aneurysms were subcategorized into 1 of the following 4 groups: middle cerebral artery (MCA; n = 354), anterior communicating artery and anterior cerebral artery (ACA; n = 496), internal carotid artery (ICA; n = 402), and posterior circulation (n = 130). Locations of 66 of the ruptured aneurysms were unknown/unrecorded. Treatments included craniotomy and clipping alone in 1073 patients, endovascular coil embolization alone in 285 patients, and a combination of coiling and clipping in 17 patients. The age-adjusted and multivariate odds ratios from logistic regression analyses were calculated after stratification using the Fisher CT scale to investigate the effects of the hematoma volume of SAH.

RESULTS

Acute hydrocephalus was confirmed in 593 patients, and 521 patients developed sNPH. Patients with a ruptured ACA aneurysm had twice the risk for sNPH over those with a ruptured MCA aneurysm. Those with an ACA aneurysm with Fisher Grade 3 SAH had a 9-fold-higher risk for sNPH than those with an MCA aneurysm with Fisher Grade 1 or 2 SAH. Patients with a ruptured posterior circulation aneurysm did not have any significant risk for sNPH. Clipping of the ruptured aneurysm resulted in twice the risk for sNPH over coil embolization alone.

CONCLUSIONS

Patients with low-grade SAH caused by a ruptured MCA aneurysm had a low risk for the development of sNPH. In contrast, patients with high-grade SAH caused by a ruptured ACA aneurysm had a higher risk for sNPH. Endovascular coiling might confer a lower risk of developing sNPH than microsurgical clipping.

The natural history of secondary normal-pressure hydrocephalus (sNPH) occurring 1 or 2 months after subarachnoid hemorrhage (SAH) is becoming clear. The prevalence of sNPH has been reported to be 8.9%–48% in patients with SAH.1–7,11,12,16,18,22,23 Acute hydrocephalus coexisting with SAH is known to be one of the most important predictors for sNPH.3–6,11,16 Previous studies have shown that severe symptoms at SAH onset and a large amount of subarachnoid blood seen on admission CT images are associated with the development of sNPH.3–11,12,16,18,23 A posterior circulation location of the ruptured aneurysm and endovascular coil embolization have been reported to be significantly associated with sNPH.1,4–7,12,15,16,22 However, this relationship is controversial, because SAH caused by a posterior circulation aneurysm frequently occurs with severe initial symptoms and acute hydrocephalus, compared to SAH caused by a ruptured anterior circulation aneurysm, which is known to occur with mild symptoms and/or no acute hydrocephalus.14 In addition, most ruptured posterior circulation aneurysms have been treated with endovascular coil embolization.3,5 This selection bias in previous hospital-based studies might have influenced the risk for development of sNPH after coil embolization among patients with a ruptured posterior circulation aneurysm. In the present study, by taking an advantage of a large nationwide registration study, we investigated the risk of sNPH associated with aneurysm location and treatment (clipping or coil embolization) for the ruptured cerebral aneurysm.

Methods

Population

Between 2000 and 2013, the Japanese Standard Stroke Registry Study accumulated data on 101,165 patients with acute stroke treated in 163 institutions across Japan.10,20 This nationwide stroke database was established with support from the Japanese Ministry of Health, Labor and Welfare to provide evidence for the standardization of Japanese stroke management. The present study was approved by the ethics committee of the Shimane Medical University. Details of data collection and management have been published elsewhere.10,20 A total of 5344 patients (5.3% of the registered population; 1772 men and 3572 women; mean age 62.5 ± 14.4 years) were registered as having had an SAH. Among them, 4693 patients were diagnosed with a ruptured saccular aneurysm, 196 had a dissecting aneurysm, 27 had an infectious or traumatic pseudo-aneurysm, and 428 had an aneurysm for which the origin was unknown or not recorded. In this study, the patients confirmed to have had a ruptured cerebral saccular aneurysm were included because of the different pathological characteristics of dissecting and pseudoaneurysms. In addition, to clarify the relationship between acute hydrocephalus and sNPH, this study included the patients who were confirmed to have or not have coexisting acute hydrocephalus and sNPH, as diagnosed by the attending neurosurgeons at the registered hospitals. We also gathered data on patients diagnosed with acute hydrocephalus who experienced neurological deterioration and underwent immediate CSF diversion by placement of an external ventricular or lumbar drain on admission. The records of patients with sNPH after SAH were also reviewed to note their symptoms and whether they underwent ventriculoperitoneal or lumboperitoneal shunt placement for permanent CSF diversion. Finally, 1448 patients (438 men and 1010 women; mean age 61.9 ± 13.4 years) were included for statistical analyses. The database recorded age, sex, medical history, medication status, family history of stroke, lifestyle factors, neurological severity grading at SAH onset (NIH Stroke Scale, World Federation of Neurological Societies [WFNS] scale, and Hunt and Kosnik scale), Fisher CT scale grade (from the admission CT scan), and treatment for the ruptured cerebral aneurysm (neurosurgical clipping and/or endovascular coil embolization). Locations of the ruptured cerebral aneurysms were categorized as follows: middle cerebral artery (MCA; n = 354), anterior communicating artery (n = 416), anterior cerebral artery (ACA; n = 80), internal carotid-posterior communicating artery (n = 395), other internal carotid artery (ICA; n = 7), posterior cerebral artery (n = 14), basilar tip (n = 48), basilar-superior cerebellar artery (n = 21), vertebral artery-posterior inferior cerebellar artery (n = 47), and unknown or unrecorded (n = 66). The aneurysm locations were subcategorized into 1 of the following 4 groups: MCA, ACA (which included the ACA and the anterior communicating artery), ICA (which included the ICA-posterior communicating artery and other ICAs), and posterior circulation (which included the posterior cerebral artery, basilar tip, basilarsuperior cerebellar artery, and vertebral artery-posterior inferior cerebellar artery).

Statistical Analysis

Odds ratios and 95% CIs for the development of sNPH were calculated. Using logistic regression analyses, we investigated the association between sNPH and the following variables: age (< 60 or ≥ 60 years), sex, acute hydrocephalus, craniotomy and microsurgical clipping or endovascular coil embolization, hypertension, diabetes, dyslipidemia, smoking habit, alcohol consumption, WFNS scale grade, Hunt and Kosnik scale grade, and Fisher CT scale grade. All analyses were adjusted by the continuous variable of age at registration. To assess the effects of modification and interaction, we conducted multivariate analyses after adjusting for age, sex, hypertension, smoking habit, acute hydrocephalus, and Fisher CT scale grade. In addition, to investigate the effects of acute hydrocephalus and hematoma volume, age-adjusted and multivariate odds ratios were analyzed after stratification according to acute hydrocephalus (versus no acute hydrocephalus) and Fisher CT scale grade. All missing variables were treated as deficit data that did not change the other variables. Statistical significance was assumed at a Fisher exact test probability value (p) of < 0.05. Statistical analyses were performed using R software (version 3.1.2, R Foundation for Statistical Computing; http://www.R-project.org).

Results

The clinical characteristics of the 1448 patients diagnosed with SAH caused by a ruptured cerebral saccular aneurysm are summarized in Table 1. Of them, 521 were registered as having had sNPH after aneurysmal SAH, and 444 (85%) of these patients underwent shunt surgery. SAH caused by ACA aneurysm rupture tended to have lower grades on the WFNS and Hunt and Kosnik scales and was seen in younger males, and 78% of the aneurysms were treated with clipping alone. SAH caused by posterior circulation aneurysms occurred more often in older females, had a higher concurrence of acute hydrocephalus, had higher grades on the WFNS, Hunt and Kosnik, and Fisher scales, and was treated more often with endovascular coiling rather than with microsurgical clipping. Table 2 lists the age-adjusted and multivariate odds ratios for the development of sNPH. Significant independent predictors for the development of sNPH were age of 60 years or older, concurrence of acute hydrocephalus, and high grades on the WFNS, Hunt and Kosnik, and Fisher scales. Patients with a ruptured ACA aneurysm had twice the risk for sNPH than those with a ruptured MCA aneurysm; ruptured posterior circulation aneurysms did not confer any significant risk for sNPH (Table 2). The sNPH risk in patients with an ACA aneurysm did not change even after stratification for the coexistence of acute hydrocephalus (data not shown). For patients with Fisher CT Group 1 or 2 SAH, which indicates a small hematoma volume, the ACA and ICA aneurysms conferred a 5.5- and 2.5-times-higher risk for sNPH than MCA aneurysms, respectively (Table 3). In the subgroup of patients with Fisher Group 3 SAH, the sNPH risk conferred by ACA aneurysms was 1.8 times higher than that by the MCA aneurysms. In the subgroup of patients with Fisher Group 4 SAH, however, there was no significant difference among the 4 aneurysm locations. ACA aneurysms in patients with Fisher Group 3 SAH conferred a 9-fold-higher risk for sNPH than MCA aneurysms in patients with Fisher Group 1 or 2 SAH.

TABLE 1.

Clinical characteristics in each location of ruptured cerebral aneurysm on admission*

CharacteristicAneurysm Location
AllMCAACAICAPosterior CirculationUnknown/Unrecorded
No.144835449640213066
Age (yrs)61.9 ± 13.461.6 ±12.760.8 ±13.462.6 ± 14.264.1 ± 13.262.8 ± 12.2
Female sex1010 (70)248 (70)288 (58)322 (80)113 (87)39 (59)
Acute hydrocephalus593 (41.0)120 (33.9)218 (44.0)152 (37.8)79 (60.8)24 (36.4)
Clipping alone1073 (74.1)320 (90.4)385 (77.6)296 (73.6)51 (39.2)21 (31.8)
Coiling alone285 (19.7)20 (5.7)97 (19.6)91 (22.6)70 (53.9)7 (10.6)
Hypertension718 (49.6)189 (53.4)241 (48.6)181 (45.0)74 (56.9)33 (50.0)
Diabetes mellitus112 (7.7)20 (5.7)34 (6.9)34 (8.5)11 (8.5)13 (19.7)
Dyslipidemia180 (12.4)39 (11.0)65 (13.1)54 (13.4)17 (13.1)5 (7.6)
Smoking habit444 (30.7)114 (32.2)177 (35.7)102 (25.4)33 (25.4)18 (27.3)
Alcohol consumption499 (34.5)135 (38.1)192 (38.7)117 (29.1)30 (23.1)25 (37.9)
NIH stroke scale13.2 ± 16.113.29 ± 15.712.4 ± 16.212.5 ± 16.116.1 ± 16.415.1 ± 17.9
WFNS scale
 Grade I484 (33.4)116 (32.8)169 (34.1)145 (36.1)27 (20.8)27 (40.9)
 Grade II360 (24.9)71 (20.1)134 (27.0)100 (24.9)41 (31.5)14 (21.2)
 Grade III124 (8.6)35 (9.9)45 (9.1)32 (8.0)9 (6.9)3 (4.6)
 Grade IV282 (19.5)86 (24.3)79 (15.9)76 (18.9)33 (25.4)8 (12.1)
 Grade V194 (13.4)44 (12.4)69 (13.9)47 (11.7)20 (15.4)14 (21.2)
Hunt & Kosnik scale
 Grade I160 (11.0)36 (10.2)61 (12.3)40 (10.0)9 (6.9)14 (21.2)
 Grade II568 (39.2)132 (37.3)198 (39.9)168 (41.8)46 (35.4)24 (36.4)
 Grade III326 (22.5)76 (21.5)110 (22.2)93 (23.1)38 (29.2)9 (13.6)
 Grade IV248 (17.1)78 (22.0)76 (15.3)69 (17.2)19 (14.6)6 (9.1)
 Grade V144 (9.9)32 (9.0)51 (10.3)30 (7.5)18 (13.8)13 (19.7)
Fisher CT scale
 Grade 141 (2.8)7 (2.0)10 (2.0)14 (3.5)5 (3.9)5 (7.6)
 Grade 2220 (15.2)49 (13.8)66 (13.3)77 (19.2)16 (12.3)12 (18.2)
 Grade 3957 (66.1)217 (61.3)345 (69.6)263 (65.4)95 (73.1)37 (56.1)
 Grade 4227 (15.7)81 (22.9)73 (14.7)47 (11.7)14 (10.8)12 (18.2)

Values are mean ± SD or number (%).

Data for some patients were not recorded: treatment methods (clipping or coiling), 9 patients (3 with MCA aneurysm, 3 with ACA aneurysm, 2 with ICA aneurysm, 1 with no aneurysm location information); history of hypertension, 41 patients (9 with MCA aneurysm, 16 with ACA aneurysm, 13 with ICA aneurysm, 3 with no aneurysm location information); history of diabetes mellitus, 29 patients (11 with MCA aneurysm, 6 with ACA aneurysm, 11 with ICA aneurysm, 1 with posterior circulation aneurysm); history of dyslipidemia, 108 patients (24 with MCA aneurysm, 34 with ACA aneurysm, 38 with ICA aneurysm, 8 with posterior circulation aneurysm, 4 with no aneurysm location information); smoking habits, 249 patients (66 with MCA aneurysm, 90 with ACA aneurysm, 63 with ICA aneurysm, 22 with posterior circulation aneurysm, 8 with no aneurysm location information); alcohol consumption, 248 patients (64 with MCA aneurysm, 91 with ACA aneurysm, 62 with ICA aneurysm, 24 with posterior circulation aneurysm, 7 with no aneurysm location information); WFNS scale, 4 patients (2 with MCA aneurysm, 2 with ICA aneurysm); Hunt & Kosnik scale, 2 patients (with ICA aneurysm); and Fisher CT scale, 3 patients (2 with ACA aneurysm, 1 with ICA aneurysm).

TABLE 2.

Risk of coexisting sNPH after aneurysmal SAH

VariablesNPHNosNPHaOR* (95% CI)p ValuemOR (95% CI)p Value
Age (≥60 yrs)3664562.44 (1.94–3.10)<0.0011.96 (1.47–2.62)<0.001
Acute hydrocephalus3212723.62 (2.87–4.57)<0.0013.60 (2.77–4.69)<0.001
Aneurysm location
 MCA104250ReferenceReference
 ACA2112851.93 (1.42–2.61)<0.0012.02 (1.39–2.92)<0.001
 ICA1432591.12 (0.96–1.32)0.1601.14 (0.94–1.39)0.180
 Posterior circulation47831.06 (0.91–1.23)0.4501.06 (0.88–1.28)0.530
Treatment
 Coiling alone95190ReferenceReference
 Clipping alone3956781.59 (1.18–2.14)0.0021.97 (1.36–2.85)<0.001
Hunt & Kosnik scale
 Grade I or II159569ReferenceReference
 Grade III1501762.92 (2.17–3.91)<0.0012.32 (1.63–3.29)<0.001
 Grade IV or V2121803.78 (2.88–4.96)<0.0012.62 (1.85–3.73)<0.001
Fisher CT rating scale
 Grade 1 or 252209ReferenceReference
 Grade 33625952.15 (1.53–3.01)<0.0011.95 (1.30–2.91)0.001
 Grade 41061213.34 (2.21–5.05)<0.0012.99 (1.75–5.10)<0.001

aOR indicates the age-adjusted OR from logistic regression analysis.

Boldface indicates statistically significant variables.

mOR indicates the multivariate OR for sNPH after adjustment for age, sex, hypertension, smoking habit, acute hydrocephalus, and Fisher grade.

TABLE 3.

Risk of coexisting sNPH after aneurysmal SAH in the Fisher CT rating scale subgroups

VariablesNPHNo sNPHmOR* (95% CI)p Value
Fisher Grade 1 or 252209
 Age (≥60 yrs)36932.28 (0.96–5.4)0.061
 Acute hydrocephalus353411.1 (4.64–26.5)<0.001
 MCA aneurysm452Reference
 ACA aneurysm16605.50 (1.20–25.4)0.028
 ICA aneurysm22692.50 (1.10–5.70)0.029
 Posterior circulation aneurysm5160.92 (0.39–2.20)0.848
 Coiling alone839Reference
 Clipping alone361581.67 (0.47–6.00)0.430
 Hunt & Kosnik scale Grade I or II33189Reference
 Hunt & Kosnik scale Grade III9151.70 (0.46–6.28)0.420
 Hunt & Kosnik scale Grade IV or V1047.00 (6.10–790)<0.001
Fisher Grade 3362595
 Age (≥60 yrs)2593011.94 (1.38–2.74)<0.001
 Acute hydrocephalus2171953.04 (2.24–4.14)<0.001
 MCA aneurysm70147Reference
 ACA aneurysm1541911.76 (1.15–2.70)0.009
 ICA aneurysm921711.03 (0.82–1.29)0.820
 Posterior circulation aneurysm36591.05 (0.85–1.29)0.670
 Coiling alone76140Reference
 Clipping alone2574191.90 (1.28–2.83)0.002
 Hunt & Kosnik scale Grade I or II107343Reference
 Hunt & Kosnik scale Grade III1291382.41 (1.64–3.56)<0.001
 Hunt & Kosnik scale Grade IV or V1261142.42 (1.61–3.64)<0.001
Fisher Grade 4106121
 Age (≥60 yrs)70612.40 (1.12–5.05)0.024
 Acute hydrocephalus68433.29 (1.63–6.66)<0.001
 MCA aneurysm3051Reference
 ACA aneurysm40332.28 (0.88–5.90)0.090
 ICA aneurysm29181.49 (0.88–2.52)0.140
 Posterior circulation aneurysm680.93 (0.53–1.60)0.786
 Coiling alone1111Reference
 Clipping alone91935.00 (0.86–29.2)0.073
 Hunt & Kosnik scale Grade I or II1836Reference
 Hunt & Kosnik scale Grade III12232.09 (0.54–8.02)0.284
 Hunt & Kosnik scale Grade IV or V76622.56 (1.10–5.96)0.029

mOR indicates the multivariate OR for sNPH after adjustment for age, sex, hypertension, smoking habit, acute hydrocephalus, and Fisher CT rating scale grade.

Boldface indicates statistically significant variables.

Among these 1448 patients, 1073 were treated with craniotomy and clipping alone, 285 were treated with coil embolization alone, and 17 underwent a combination of coiling and clipping. Microsurgical clipping conferred a 2-fold-increased risk for sNPH over coil embolization alone (Table 2). This advantage of coil embolization for the reduction of sNPH risk did not change in the subgroup of patients with Fisher Grade 3 SAH (Table 3). In the subgroup of patients with Fisher Grade 1, 2, or 4 SAH, however, there was no statistically significant difference between clipping and coiling in terms of sNPH risk.

Discussion

Our large registration study revealed that ruptured ACA aneurysms conferred a significantly higher risk of sNPH than ruptured MCA aneurysms. Gruber et al.7 reported that ruptured aneurysms located in the anterior communicating artery conferred a significant increased risk for the development of sNPH compared with those in other locations (p < 0.001). Other previous studies concluded that patients with a ruptured posterior circulation aneurysm most frequently developed sNPH;1,5,6,12,16,17,21 3 of these 7 studies reported that patients with an anterior communicating artery or ACA aneurysm are the second-most frequent to develop sNPH and that developing sNPH after an MCA aneurysm is rare.6,17,21 The other 4 studies did not further categorize the anterior circulation aneurysms as being located in the ACA, MCA, or ICA.1,5,12,16 The sNPH risk conferred by posterior circulation aneurysms may be affected by the other modified variables, such as intraventricular hemorrhage and acute hydrocephalus, for which the frequency was reported to be the highest in patients with a ruptured posterior circulation aneurysm.9,21 We confirmed that posterior circulation aneurysms cooccurred with acute hydrocephalus more frequently and were treated more often with endovascular coiling than aneurysms in the other locations in this study. Although the patients’ characteristics were similar to those in the previous studies, posterior circulation aneurysms did not confer any significantly increased risk for the development of sNPH. SAH in the interhemispheric fissure may contribute to the pathogenesis of a higher prevalence of sNPH with ruptured ACA aneurysms, because it would become an obstacle to the CSF-drainage pathway into the nasal lymphatic system via the perineural subarachnoid space enveloping the olfactory nerve rootlets.13,24

In addition, we also confirmed that increasing age, severe initial symptoms, a large-volume diffuse subarachnoid hematoma, and concurrence of acute hydrocephalus were correlated significantly with the development of sNPH; these findings are supported by previous studies.3–7,11,12,16,18,23 On the basis of the evidence of an association between the severity of SAH and the prevalence of subsequent sNPH, many neurosurgeons have believed that several surgical manipulations for facilitating CSF dynamics, such as hematoma evacuation, widening the opening of the cisterns, and fenestration of the lamina terminalis, might help to reduce the subsequent occurrence of sNPH after the surgical treatment of SAH. However, the authors of a recent meta-analysis of 11 nonrandomized studies in which data from 1973 patients were pooled concluded that there was no significant difference in the prevalence of sNPH between the 975 patients who had undergone fenestration of the lamina terminalis and the 998 who had not (p = 0.09).11 On the basis of this evidence, guidelines for the management of chronic hydrocephalus after aneurysmal SAH from the American Heart Association recommend that fenestration of the lamina terminalis not be routinely performed.2 Another meta-analysis of 5 nonrandomized studies with data from 1718 patients pooled3 reported that 1336 patients treated with microsurgical clipping had a significantly lower risk of sNPH than 382 patients treated with endovascular coiling (relative risk 0.74; 95% CI 0.58–0.94; p = 0.01); however, 3 of the 5 studies found no significant difference between clipping and coiling for the predictive risk of sNPH.8,15,19 Our results provide the first evidence that, compared with microsurgical clipping alone, coil embolization alone significantly decreased the risk for the development of sNPH. This finding may support the view that microsurgical manipulation accelerates inflammation of CSF in the subarachnoid space and leads to stagnating CSF that results from thickness and fibrosis of the arachnoid and pia mater.

The advantage of this study includes a much larger sample size than those of previous studies. Despite this advantage, a register-based study also has some limitations, such as recording bias. In fact, one-third of the 4693 patients registered as having had aneurysmal SAH were included in this study, and 95% of them were treated with coiling or clipping.

Conclusions

Our findings indicate that sNPH after SAH frequently occurs among patients with high-grade SAH caused by a ruptured ACA aneurysm and patients treated with microsurgical clipping. On the contrary, patients with low-grade SAH caused by a ruptured MCA aneurysm and patients treated with endovascular coiling might be less likely to develop sNPH. Studies are needed to elucidate the mechanisms by which ruptured ACA aneurysms and microsurgical treatment can increase the risk for developing sNPH after SAH.

Author Contributions

Conception and design: Yamada, Ishikawa, Kobayashi. Acquisition of data: Kobayashi. Analysis and interpretation of data: Yamada, Ishikawa, Yamamoto, Kobayashi. Drafting the article: Ishikawa, Yamamoto, Kobayashi. Approved the final version of the manuscript on behalf of all authors: Yamada. Statistical analysis: Yamada, Ishikawa, Kobayashi. Administrative/technical/material support: Ishikawa, Ino, Kimura, Kobayashi. Study supervision: Ishikawa, Yamamoto, Ino, Kimura, Kobayashi. Organized the Japanese Stroke DataBank: Kobayashi.

Supplemental Information

Current Affiliation

Dr. Kimura: Rakuwakai Otowa Rehabilitation Hospital, Kyoto, Japan.

Appendix: Japan Standard Stroke Registry Study Group

The institutions that presently contribute to the registration of hospital records for cerebral strokes are as follows:

  1. Teine Keijinnkai Hospital, Department of Neurosurgery

  2. Hakodate Neurosurgical Hospital, Department of Neurosurgery

  3. Hokkaido Neurosurgical Memorial Hospital, Department of Neurosurgery

  4. Nakamura Memorial Hospital, Stroke Center

  5. Hokkaido University Hospital, Department of Neurosurgery

  6. Keiwakai Ebetsu Hospital, Department of Neurosurgery

  7. Asahikawa Medical University Hospital, Department of Neurology

  8. Rumoi Central Clinic, Department of Neurosurgery

  9. Iwate Medical University, Department of Neurology and Neurosurgery

  10. Iwate Prefectural Kuji Hospital, Department of Neurosurgery

  11. Southern Tohoku Research Institute for Neuroscience Hospital, Stroke Center

  12. Kohnan Hospital, Stroke Center

  13. Research Institute for Brain and Blood Vessels Akita, Stroke Center

  14. Saiseikai Central Hospital, Department of Neurology

  15. Kanto Medical Center NTT East Corporation, Department of Neurosurgery

  16. Keio University School of Medicine, Department of Neurology

  17. National Center for Global Health and Medicine, Neurosurgery

  18. Hatanodai Neurosurgical Hospital, Department of Neurosurgery

  19. Metroporitan Ohkubo Hospital, Department of Neurosurgery

  20. Tokyo Women’s Medical University Hospital, Department of Neurology

  21. Kyorin University Hospital, Department of Neurosurgery

  22. Akiru Municipal Medical Center, Department of Neurosurgery

  23. Tokyo Medical University Hachioji Medical Center, Department of Neurosurgery

  24. Yokohama Rosai Hospital, Department of Neurology

  25. Kawasaki Saiwai Hospital, Department of Neurosurgery

  26. Sagamihara Kyoudo Hospital, Department of Neurosurgery

  27. Yokohama Stroke & Brain Center

  28. Yokohama City University Hospital, Stroke Center

  29. Shonankamakura General Hospital, Stroke Center

  30. Tokai University, Department of Oiso Hospital, Department of Neurology

  31. Tokai University Hospital, Department of Neurology

  32. Tokyo Dental College Ichikawa General Hospital, Department of Neurosurgery

  33. Jisenkai Yoshida Hospital, Department of Neurosurgery

  34. Chiba Rosai Hospital, Department of Neurosurgery

  35. Chiba Cardiovascular Center, Stroke Center

  36. Dokkyo University School of Medicine, Department of Neurology

  37. Ryugasaki Saiseikai Hospital, Department of Neurology

  38. Saitama International Medical Research Center Hospital, Stroke Center

  39. Hiratsuka Kyosai Hospital, Stroke Center

  40. Saitama Medical University Hospital, Department of Neurology

  41. Fukui University Hospital, Department of Neurology

  42. Toyama University Hospital, Department of Neurology and Neurosurgery

  43. Shizuoka General Hospital, Department of Neurology

  44. Matsunami General Hospital, Department of Neurosurgery

  45. Shiga University of Medical Science Hospital, Department of Neurology and Neurosurgery

  46. Osaka University Faculty of Medicine, Department of Neurology

  47. National Cardiovascular Center, Department of Cerebrovascular Disease

  48. Hoshigaoka Koseinenkin Hospital, Department of Neurology

  49. Kyoto Second Red Cross Hospital, Department of Neurology

  50. Kyoto Prefectural University of Medicine, Department of Neurology

  51. Otowa Hospital, Department of Neurology

  52. Itami City Hospital, Department of Neurosurgery

  53. Kobe City General Hospital, Stroke Center

  54. Hyogo Brain and Heart Center, Department of Neurology

  55. Matsue City Hospital, Department of Neurosurgery

  56. Shimane Prefectural Central Hospital, Department of Neurology and Neurosurgery

  57. Shimane University Hospital, Department of Neurology and Neurosurgery

  58. Okayama Rosai Hospital, Department of Neurosurgery

  59. Matsue Red Cross Hospital, Department of Neurology

  60. Ohda Municipal Hospital, Department of Neurology

  61. Masuda Red Cross Hospital, Department of Neurology

  62. Kawasaki Medical School Hospital, Stroke Center

  63. National Okayama Medical Center, Department of Neurology

  64. Okayama Kyokuto Hospital, Department of Cerebrovascular Disease

  65. Konan Central Hill Hospital, Department of Neurosurgery

  66. Oota Memorial Hospital, Department of Neurology

  67. Okayama University Hospital, Department of Neurology

  68. National Hospital Organization Okayama Medical Center, Department of Neurology

  69. Kajikawa Hospital, Department of Neurology

  70. Hiroshima University Hospital, Department of Neurology

  71. National Hospital Organization Kure Medical Center, Department of Neurology

  72. Higashihiroshima Medical Center, Department of Neurology

  73. Yamaguchi University Hospital, Department of Neurosurgery

  74. Kagawa University Hospital, Department of Neurology

  75. Osaka Neurosurgical Hospital, Department of Rehabilitation

  76. Tokushima University Hospital, Department of Neurosurgery

  77. Ehime University Hospital, Department of Neurosurgery

  78. Chikamori Hospital, Department of Neurology

  79. Saiseikai Fukuoka General Hospital, Department of Neurology

  80. Kyusyu University Hospital, Stroke Center

  81. Kyusyu National Medical Center Hospital, Department of Neurology

  82. Iizuka Hospital, Department of Neurology

  83. St. Mary’s Hospital, Cerebral Stroke Center

  84. Saga Prefectural Hospital, Department of Neurosurgery

  85. Saiseikai Kumamoto Hospital, Department of Neurology

  86. Kumamoto City Hospital, Department of Neurology

  87. Kumamoto Red Cross Hospital, Department of Neurology

  88. Fukuoka Red Cross Hospital, Department of Neurology

  89. Oita Almedia Hospital, Department of Neurosurgery

  90. Miyakonojo Regional Medical Center, Department of Neurosurgery

  91. Ryukyu University Hospital, Department of Neurology

  92. Okinawa Prefectural Yaeyama Hospital, Department of Neurosurgery

  93. Fukuoka Tokusyukai Hospital, Department of Neurology

  94. Kohase Hospital, Department of Neurosurgery

References

  • 1

    Chan MAlaraj ACalderon MHerrera SRGao WRuland S: Prediction of ventriculoperitoneal shunt dependency in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 110:44492009

    • Search Google Scholar
    • Export Citation
  • 2

    Connolly ES JrRabinstein AACarhuapoma JRDerdeyn CPDion JHigashida RT: Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43:171117372012

    • Search Google Scholar
    • Export Citation
  • 3

    de Oliveira JGBeck JSetzer MGerlach RVatter HSeifert V: Risk of shunt-dependent hydrocephalus after occlusion of ruptured intracranial aneurysms by surgical clipping or endovascular coiling: a single-institution series and metaanalysis. Neurosurgery 61:9249342007

    • Search Google Scholar
    • Export Citation
  • 4

    Dehdashti ARRilliet BRufenacht DAde Tribolet N: Shunt-dependent hydrocephalus after rupture of intracranial aneurysms: a prospective study of the influence of treatment modality. J Neurosurg 101:4024072004

    • Search Google Scholar
    • Export Citation
  • 5

    Dorai ZHynan LSKopitnik TASamson D: Factors related to hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 52:7637712003

    • Search Google Scholar
    • Export Citation
  • 6

    Graff-Radford NRTorner JAdams HP JrKassell NF: Factors associated with hydrocephalus after subarachnoid hemorrhage. A report of the Cooperative Aneurysm Study. Arch Neurol 46:7447521989

    • Search Google Scholar
    • Export Citation
  • 7

    Gruber AReinprecht ABavinzski GCzech TRichling B: Chronic shunt-dependent hydrocephalus after early surgical and early endovascular treatment of ruptured intracranial aneurysms. Neurosurgery 44:5035121999

    • Search Google Scholar
    • Export Citation
  • 8

    Jartti PKarttunen AIsokangas JMJartti AKoskelainen TTervonen O: Chronic hydrocephalus after neurosurgical and endovascular treatment of ruptured intracranial aneurysms. Acta Radiol 49:6806862008

    • Search Google Scholar
    • Export Citation
  • 9

    Kallmes DFLanzino GDix JEDion JEDo HWoodcock RJ: Patterns of hemorrhage with ruptured posterior inferior cerebellar artery aneurysms: CT findings in 44 cases. AJR Am J Roentgenol 169:116911711997

    • Search Google Scholar
    • Export Citation
  • 10

    Kobayashi S: International experience in stroke registry: Japanese Stroke DataBank. Am J Prev Med 31:6 Suppl 2S240S2422006

  • 11

    Komotar RJHahn DKKim GHStarke RMGarrett MCMerkow MB: Efficacy of lamina terminalis fenestration in reducing shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage: a systematic review. Clinical article. J Neurosurg 111:1471542009

    • Search Google Scholar
    • Export Citation
  • 12

    Little ASZabramski JMPeterson MGoslar PWWait SDAlbuquerque FC: Ventriculoperitoneal shunting after aneurysmal subarachnoid hemorrhage: analysis of the indications, complications, and outcome with a focus on patients with borderline ventriculomegaly. Neurosurgery 62:6186272008

    • Search Google Scholar
    • Export Citation
  • 13

    McComb JG: Recent research into the nature of cerebrospinal fluid formation and absorption. J Neurosurg 59:3693831983

  • 14

    Mehta VHolness ROConnolly KWalling SHall R: Acute hydrocephalus following aneurysmal subarachnoid hemorrhage. Can J Neurol Sci 23:40451996

    • Search Google Scholar
    • Export Citation
  • 15

    Mura JRojas-Zalazar DRuíz AVintimilla LCMarengo JJ: Improved outcome in high-grade aneurysmal subarachnoid hemorrhage by enhancement of endogenous clearance of cisternal blood clots: a prospective study that demonstrates the role of lamina terminalis fenestration combined with modern microsurgical cisternal blood evacuation. Minim Invasive Neurosurg 50:3553622007

    • Search Google Scholar
    • Export Citation
  • 16

    O’Kelly CJKulkarni AVAustin PCUrbach DWallace MC: Shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: incidence, predictors, and revision rates. Clinical article. J Neurosurg 111:102910352009

    • Search Google Scholar
    • Export Citation
  • 17

    Pietilä TAHeimberger KCPalleske HBrock M: Influence of aneurysm location on the development of chronic hydrocephalus following SAH. Acta Neurochir (Wien) 137:70731995

    • Search Google Scholar
    • Export Citation
  • 18

    Rincon FGordon EStarke RMBuitrago MMFernandez ASchmidt JM: Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 113:7747802010

    • Search Google Scholar
    • Export Citation
  • 19

    Sethi HMoore ADervin JClifton AMacSweeney JE: Hydrocephalus: comparison of clipping and embolization in aneurysm treatment. J Neurosurg 92:9919942000

    • Search Google Scholar
    • Export Citation
  • 20

    Takizawa SShibata TTakagi SKobayashi S: Seasonal variation of stroke incidence in Japan for 35631 stroke patients in the Japanese Standard Stroke Registry, 1998–2007. J Stroke Cerebrovasc Dis 22:36412013

    • Search Google Scholar
    • Export Citation
  • 21

    Tapaninaho AHernesniemi JVapalahti MNiskanen MKari ALuukkonen M: Shunt-dependent hydrocephalus after subarachnoid haemorrhage and aneurysm surgery: timing of surgery is not a risk factor. Acta Neurochir (Wien) 123:1181241993

    • Search Google Scholar
    • Export Citation
  • 22

    Varelas PHelms ASinson GSpanaki MHacein-Bey L: Clipping or coiling of ruptured cerebral aneurysms and shunt-dependent hydrocephalus. Neurocrit Care 4:2232282006

    • Search Google Scholar
    • Export Citation
  • 23

    Yang TCChang CHLiu YTChen YLTu PHChen HC: Predictors of shunt-dependent chronic hydrocephalus after aneurysmal subarachnoid haemorrhage. Eur Neurol 69:2963032013

    • Search Google Scholar
    • Export Citation
  • 24

    Weller ROKida SZhang ET: Pathways of fluid drainage from the brain—morphological aspects and immunological significance in rat and man. Brain Pathol 2:2772841992

    • Search Google Scholar
    • Export Citation

If the inline PDF is not rendering correctly, you can download the PDF file here.

Article Information

Correspondence Shigeki Yamada, Department of Neurosurgery and Stroke Center, Normal Pressure Hydrocephalus Center, Rakuwakai Otowa Hospital, Otowachinji-cho 2, Yamashina-ku, Kyoto 607–8602, Japan. email: shigekiyamada3@gmail.com.

* See Appendix for listing of institutions participating in the Japan Standard Stroke Registry Study Group.

INCLUDE WHEN CITING Published online July 31, 2015; DOI: 10.3171/2015.1.JNS142761.

DISCLOSURE Dr. Ishikawa has received honoraria from Medtronic Japan Co., Ltd. (Japan). Dr. Yamada declares no disclosures and no conflicts of interest. Drs. Yamamoto, Ino, Kimura, and Kobayashi report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. All authors have made substantial contributions to the intellectual content of the paper, have approved the final manuscript, and agree with submission to this journal. Dr. Yamada is the corresponding author for this study and the principal investigator. He takes responsibility for data management, accuracy of statistical analysis, conduct of the research, and drafting of the manuscript. The following grants funded this study: “21st Century Type Promoting Development of Clinical Research Fund” from the Japanese of Health, Labor and Welfare during 1999 to 2001.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1

    Chan MAlaraj ACalderon MHerrera SRGao WRuland S: Prediction of ventriculoperitoneal shunt dependency in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg 110:44492009

    • Search Google Scholar
    • Export Citation
  • 2

    Connolly ES JrRabinstein AACarhuapoma JRDerdeyn CPDion JHigashida RT: Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 43:171117372012

    • Search Google Scholar
    • Export Citation
  • 3

    de Oliveira JGBeck JSetzer MGerlach RVatter HSeifert V: Risk of shunt-dependent hydrocephalus after occlusion of ruptured intracranial aneurysms by surgical clipping or endovascular coiling: a single-institution series and metaanalysis. Neurosurgery 61:9249342007

    • Search Google Scholar
    • Export Citation
  • 4

    Dehdashti ARRilliet BRufenacht DAde Tribolet N: Shunt-dependent hydrocephalus after rupture of intracranial aneurysms: a prospective study of the influence of treatment modality. J Neurosurg 101:4024072004

    • Search Google Scholar
    • Export Citation
  • 5

    Dorai ZHynan LSKopitnik TASamson D: Factors related to hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 52:7637712003

    • Search Google Scholar
    • Export Citation
  • 6

    Graff-Radford NRTorner JAdams HP JrKassell NF: Factors associated with hydrocephalus after subarachnoid hemorrhage. A report of the Cooperative Aneurysm Study. Arch Neurol 46:7447521989

    • Search Google Scholar
    • Export Citation
  • 7

    Gruber AReinprecht ABavinzski GCzech TRichling B: Chronic shunt-dependent hydrocephalus after early surgical and early endovascular treatment of ruptured intracranial aneurysms. Neurosurgery 44:5035121999

    • Search Google Scholar
    • Export Citation
  • 8

    Jartti PKarttunen AIsokangas JMJartti AKoskelainen TTervonen O: Chronic hydrocephalus after neurosurgical and endovascular treatment of ruptured intracranial aneurysms. Acta Radiol 49:6806862008

    • Search Google Scholar
    • Export Citation
  • 9

    Kallmes DFLanzino GDix JEDion JEDo HWoodcock RJ: Patterns of hemorrhage with ruptured posterior inferior cerebellar artery aneurysms: CT findings in 44 cases. AJR Am J Roentgenol 169:116911711997

    • Search Google Scholar
    • Export Citation
  • 10

    Kobayashi S: International experience in stroke registry: Japanese Stroke DataBank. Am J Prev Med 31:6 Suppl 2S240S2422006

  • 11

    Komotar RJHahn DKKim GHStarke RMGarrett MCMerkow MB: Efficacy of lamina terminalis fenestration in reducing shunt-dependent hydrocephalus following aneurysmal subarachnoid hemorrhage: a systematic review. Clinical article. J Neurosurg 111:1471542009

    • Search Google Scholar
    • Export Citation
  • 12

    Little ASZabramski JMPeterson MGoslar PWWait SDAlbuquerque FC: Ventriculoperitoneal shunting after aneurysmal subarachnoid hemorrhage: analysis of the indications, complications, and outcome with a focus on patients with borderline ventriculomegaly. Neurosurgery 62:6186272008

    • Search Google Scholar
    • Export Citation
  • 13

    McComb JG: Recent research into the nature of cerebrospinal fluid formation and absorption. J Neurosurg 59:3693831983

  • 14

    Mehta VHolness ROConnolly KWalling SHall R: Acute hydrocephalus following aneurysmal subarachnoid hemorrhage. Can J Neurol Sci 23:40451996

    • Search Google Scholar
    • Export Citation
  • 15

    Mura JRojas-Zalazar DRuíz AVintimilla LCMarengo JJ: Improved outcome in high-grade aneurysmal subarachnoid hemorrhage by enhancement of endogenous clearance of cisternal blood clots: a prospective study that demonstrates the role of lamina terminalis fenestration combined with modern microsurgical cisternal blood evacuation. Minim Invasive Neurosurg 50:3553622007

    • Search Google Scholar
    • Export Citation
  • 16

    O’Kelly CJKulkarni AVAustin PCUrbach DWallace MC: Shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: incidence, predictors, and revision rates. Clinical article. J Neurosurg 111:102910352009

    • Search Google Scholar
    • Export Citation
  • 17

    Pietilä TAHeimberger KCPalleske HBrock M: Influence of aneurysm location on the development of chronic hydrocephalus following SAH. Acta Neurochir (Wien) 137:70731995

    • Search Google Scholar
    • Export Citation
  • 18

    Rincon FGordon EStarke RMBuitrago MMFernandez ASchmidt JM: Predictors of long-term shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage. Clinical article. J Neurosurg 113:7747802010

    • Search Google Scholar
    • Export Citation
  • 19

    Sethi HMoore ADervin JClifton AMacSweeney JE: Hydrocephalus: comparison of clipping and embolization in aneurysm treatment. J Neurosurg 92:9919942000

    • Search Google Scholar
    • Export Citation
  • 20

    Takizawa SShibata TTakagi SKobayashi S: Seasonal variation of stroke incidence in Japan for 35631 stroke patients in the Japanese Standard Stroke Registry, 1998–2007. J Stroke Cerebrovasc Dis 22:36412013

    • Search Google Scholar
    • Export Citation
  • 21

    Tapaninaho AHernesniemi JVapalahti MNiskanen MKari ALuukkonen M: Shunt-dependent hydrocephalus after subarachnoid haemorrhage and aneurysm surgery: timing of surgery is not a risk factor. Acta Neurochir (Wien) 123:1181241993

    • Search Google Scholar
    • Export Citation
  • 22

    Varelas PHelms ASinson GSpanaki MHacein-Bey L: Clipping or coiling of ruptured cerebral aneurysms and shunt-dependent hydrocephalus. Neurocrit Care 4:2232282006

    • Search Google Scholar
    • Export Citation
  • 23

    Yang TCChang CHLiu YTChen YLTu PHChen HC: Predictors of shunt-dependent chronic hydrocephalus after aneurysmal subarachnoid haemorrhage. Eur Neurol 69:2963032013

    • Search Google Scholar
    • Export Citation
  • 24

    Weller ROKida SZhang ET: Pathways of fluid drainage from the brain—morphological aspects and immunological significance in rat and man. Brain Pathol 2:2772841992

    • Search Google Scholar
    • Export Citation

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 455 455 35
PDF Downloads 294 294 19
EPUB Downloads 0 0 0

PubMed

Google Scholar