Hospital and Patient Selection

Hospital participation in the J-ASPECT Study was voluntary. Of the 1369 training institutions certified by the Japan Neurosurgical Society, the Japanese Society of Neurology, and the Japan Stroke Society, 621 agreed to participate in this study. The J-ASPECT Study group analyzed the Diagnosis Procedure Combination (DPC) database to gain new clinical insights into ischemic and hemorrhagic stroke,^13,17–19 an approach we applied again for this cross-sectional survey. The details of the DPC database are shown in Supplementary eAppendix 1.^14,30

We identified patients hospitalized for SAH due to a ruptured aneurysm in the de-identified discharge database using the ICD-10 diagnosis codes related to SAH (I60.0–9). We further selected patients who had been urgently hospitalized between April 1, 2010, and March 31, 2015, and underwent SAH treatment by clipping or coiling (Fig. 1). We then extracted data on age; sex; comorbidities on admission, including those based on Charlson Comorbidity Index (CCI) scores;⁶ level of consciousness on admission, according to the Japan Coma Scale (JCS) (Supplementary eAppendix 2);^13,17–19 and patient transfer status (transferred from another hospital). Data on patient transfer status were available only between April 1, 2013, and March 31, 2015. To maximize the accuracy of the DPC data in the mixed-case patient classification system, at least one responsible physician (e.g., physicians in charge or residents) was required to record the information from each patient’s medical chart regarding diagnoses and therapies received.³⁸

Flowchart of institution and patient selection.

This study was approved by the Kyushu University Institutional Review Board (28-335), which waived the requirement for individual informed consent. We have documented the data, methods, and materials used to conduct the research in this report. The individual patient data are not publicly available because of the memorandum signed by the director of the participating hospitals and the principal investigator of the J-ASPECT Study group.

Assessment of CSC Capabilities Using Institutional Survey

The CSC capabilities of the participating hospitals were assessed using a validated scoring system (CSC score) in 2010. We sent out questionnaires with 25 items, as recommended by the BAC to assess CSC capabilities of facilities to train institutions of the Japan Neurosurgical Society and the Japan Stroke Society that participated in the J-ASPECT Study. The analysis was performed by combining the DPC data of SAH patients admitted between 2010 and 2015 with the CSC score of each participant hospital. The questionnaire items were classified into 5 categories as follows: personnel, diagnostic, specific expertise, infrastructure, and education (Supplementary eAppendix 3).^13,14 One point was assigned to each item, yielding a maximum CSC score of 25. The content, construct, and predictive validity of this scoring system have been previously reported.¹⁸Among the 621 institutions that participated in the J-ASPECT Study, a CSC score was assigned to each of the 447 hospitals that responded to our questionnaire.

Statistical Analysis

For statistical analysis, the modified Rankin Scale (mRS) score at discharge was dichotomized into 0–2 (good functional outcome) and 3–6 (poor functional outcome). The JCS score was treated as a categorical variable of either 0, 1, 2, or 3. The hospitals were classified into quartiles (Q1–Q4) based on the case volume per year of clipping or coiling for SAH and the CSC score. The median (range) values per year for Q1, Q2, Q3, and Q4 for the clipped aneurysm patients were 3 (1–4), 6 (5–7), 10 (8–13), and 18 (14–56), respectively, for case volumes and 12 (6–13), 15 (14–16), 18 (17–18), and 20 (19–24), respectively, for CSC scores, and for the coiled aneurysm patients were 1 (1–2), 3 (3–4), 6 (5–8), and 12 (9–37), respectively, for case volumes and 12 (8–13), 15 (14–16), 18 (17–18), and 20 (19–24), respectively, for CSC scores. We excluded institutions with a case volume of zero.

Univariate analysis was performed with the chi-square, Kruskal-Wallis, Fisher, and Wilcoxon tests. The Kendall tau-b correlation coefficient was used to assess the strength of dependence between case volume and CSC score in the clipping and coiling groups. We used hierarchical logistic regression models to examine the associations between the case volumes of each modality and the CSC capabilities and in-hospital patient outcomes. The model had 2 levels (hospital and patient) and also employed the random effects of hospital variation and the fixed effects of CSC score and patient-related factors (age, sex, JCS score, and fiscal year of hospitalization). The lowest case volume and CSC score quartile (Q1) were used as reference values. For sensitivity analysis, the highest case volume and CSC score (Q4) were also used as references. Analyses were performed using SAS version 9.3 (SAS Institute Inc.), STATA version 12 (STATA Corp.), and SPSS version 12 (SPSS Inc.), and p values < 0.05 were considered statistically significant.

Associations Between Case Volumes and Patient Characteristics or Outcomes

A total of 18,715 (68.3%) clipped and 8775 (31.7%) coiled aneurysm patients were included in the analyses. Patient demographic and outcome data based on hospital case volume are shown in Tables 1 and 2.

Among the clipped aneurysm patients, the overall in-hospital mortality and short-term poor outcomes (discharge mRS score 3–6) were 8.2% and 43.8%, respectively. A high hospital case volume was significantly associated with reduced in-hospital mortality (e.g., Q1 9.5% vs Q4 7.3%) but not short-term poor outcomes.

In coiled aneurysm patients, overall in-hospital mortality and short-term poor outcomes were 13.6% and 47.5%, respectively. A high case volume was significantly associated with reduced in-hospital mortality (e.g., Q1 17.9% vs Q4 12.5%) and short-term poor outcomes (e.g., Q1 54.8% vs Q4 46.1%).

Associations Between CSC Score and Patient Characteristics or Outcomes

A total of 15,783 clipped aneurysm patients and 7114 coiled aneurysm patients were included in this analysis. Patient demographics and outcomes in the clipped and coiled aneurysm patients based on hospital case volume are shown in Tables 3 and 4.

In the clipped aneurysm patients, the overall in-hospital mortality and short-term poor outcomes were 8.1% and 44.0%, respectively. A high CSC score was significantly associated with reduced in-hospital mortality (e.g., Q1 8.5% vs Q4 6.7%) but not with reduced short-term poor outcomes.

In coiled aneurysm patients, the overall in-hospital mortality and short-term poor outcomes were 13.1% and 47.2%, respectively. A high CSC score was significantly associated with reduced in-hospital mortality (e.g., Q1 12.8% vs Q4 12.0%) but not with short-term poor outcomes.

Multivariable Analysis: Associations Between Case Volume and Patient Outcome

In clipped aneurysm patients, in-hospital mortality was significantly lower in the Q4 hospitals (OR 0.71, 95% CI 0.55–0.90), whereas there was no significant difference in short-term poor outcomes based on hospital case volume. In coiled aneurysm patients, in-hospital mortality and short-term poor outcomes were significantly lower in the Q4 hospitals (OR 0.69, 95% CI 0.53–0.90 and OR 0.65, 95% CI 0.51–0.82, respectively). Additionally, the proportion of short-term poor outcomes was significantly lower in the Q3 and Q4 hospitals (OR 0.75, 95% CI 0.59–0.96, and OR 0.65, 95% CI 0.51–0.82, respectively) (Table 5).

Multivariable Analysis: Associations Between CSC Score and Patient Outcomes

In clipped patients, in-hospital mortality was significantly lower in the Q4 hospitals (OR 0.68, 95% CI 0.54–0.86), whereas there was no significant difference in short-term poor outcomes based on hospital case volume. However, in coiled patients, there was no association between in-hospital mortality or short-term poor outcomes (discharge mRS score 3–6) and CSC capabilities (Table 6).

Sensitivity Analysis

Sensitivity analysis using Q4 as the reference demonstrated similar findings in terms of association between case volumes of clipping or coiling (Q1–Q4) and in-hospital mortality and functional outcomes of SAH patients, except for the differences in mortality for coiled aneurysm patients in case volume Q2 versus Q4 hospitals (Supplementary eAppendix 4). Similar associations were also noted between CSC score (Q1–Q4, using Q4 as reference) and in-hospital outcomes, except for the differences in mortality for coiled aneurysm patients in CSC score Q2 versus Q4 hospitals (Supplementary eAppendix 5).

Correlation Between Case Volume and CSC Score in Each Patient Group

In the clipping and coiling groups, the Kendall tau-b correlation coefficients between the case volume and CSC score were 0.23 and 0.22, respectively.

Differences Between Institutions With CSC Score and Institutions Without CSC Score

Significantly more patients were treated with clipping in the 447 institutions with CSC scores than in the remaining 174 institutions without them. As for comorbidity, there were higher rates of hypertension and lower rates of dyslipidemia among SAH patients (Supplementary eAppendix 6).

Multivariable Analysis: Association of Case Volume or CSC Score With Patient Outcomes

There was a low correlation coefficient between CSC score and case volume; hence, we performed analysis after adjusting for both CSC score and case volume in addition to age, sex, and CCI and JCS scores. Except for Q4 of case volume in coiled aneurysm patients, we found similar associations to those found with other analyses after adjusting for each CSC score and case volume as variables (Supplementary eAppendix 7).

Multivariable Analysis: Impact of Treatment Modality

In the 15,783 clipped aneurysm patients and 7114 coiled aneurysm patients, the in-hospital mortality was significantly lower in the clipping group (OR 0.60, 95% CI 0.54–0.67, p < 0.001), whereas there was no significant difference between the 2 groups in discharge mRS score 3–6 (OR 1.02, 95% CI 0.94–1.10, p = 0.651).

Patient Demographics and Outcomes of Clipping and Coiling

In this study, the patient characteristics and unadjusted outcomes after treatment with either the clipping or coiling modality were similar to those of our previously reported SAH cohort in Japan.¹⁸ As for comorbidities, trends reflecting decreased hypertension and diabetes incidence and increased dyslipidemia were generally noted in patients treated at hospitals with increased case volume and CSC capabilities. This finding may be explained by geographical factors, because hospitals with high case volumes and CSC capabilities are more likely to be located in urban areas.¹⁴ Compared with previous nationwide studies in the US and Canada,^8,26,31 SAH patients in our Japanese cohort were almost 10 years older and had lower mortality.

SAH patients treated with coiling had overall higher rates of in-hospital mortality than those treated with clipping. This finding may be attributable to a learning process of the hospital surgical team in the use of endovascular therapy for SAH, as reflected by the higher number of cases treated preferably with clipping between 2010 and 2015 in the Japanese nationwide database used in this study.

Effect of Clipping and Coiling Case Volumes on In-Hospital SAH Patient Outcomes

Numerous studies have reported improved outcomes in SAH patients treated at high-volume centers.^{2–4,7,9,22,24,28,32,34} On the other hand, a previous study in Norway did not find a relationship between treatment at hospitals with high case volume and long-term mortality,²⁵ suggesting that the patient volume-outcome relationship may not be generalizable in other countries. Furthermore, definitions of high and low volume have varied among previous studies.^{2–5,7,9,10,22,24,25,28,32,34} In the US, to obtain CSC certification, institutions are required by the Joint Commission to manage at least 20 cases of SAH and perform at least 15 coiling and/or clipping procedures for ruptured cerebral aneurysms per year.^1,32 However, Pandey et al. suggested that this threshold may be relatively low because according to their study the SAH patient volume-outcome association did not reach a plateau until the institution had managed more than 100 SAH patients per year.³²

Some reported studies have found better functional outcomes in high-volume centers,^2,24,32,34 whereas others have not.^5,10,22 Our results of better functional outcomes in hospitals with Q3 and Q4 case volumes may be attributable to patients being more likely to receive endovascular treatment for vasospasm, such as intraarterial vasodilator infusion or angioplasty.¹¹ On the other hand, the lack of a significant influence of clipping case volume on functional outcomes may be explained by the possibility that cases with a higher level of difficulty are referred to hospital settings with higher levels of surgical team experience, multidisciplinary approaches, and surveillance. However, in Japan, Hattori et al. reported no relationship between case volume and outcomes for clipping for SAH in cases of each World Federation of Neurosurgical Societies (WFNS) severity grade.¹⁰ However, the overall in-hospital mortality rate in clipped SAH patients in that study (9.0%) was similar to the rate in the present study. There are several possible reasons for differences in the former findings compared with the findings of the current study. First, Hattori et al. compared outcomes among institutions accredited by the Japan Neurosurgical Society as class A specialist training facilities (annual neurosurgical procedures > 100 cases/yr), whereas the hospitals in our study varied widely.¹⁰ In fact, the number of clipping cases in the highest-volume center in the previous study was > 50 cases,¹⁰ whereas in the present study it ranged from 14 to 56 cases (Q4). Second, Hattori et al. examined the effect of case volume of clippings performed in 2003.¹⁰ Although clipping remains the mainstay treatment for SAH in Japan,¹⁰ a significant shift from clipping to coiling has been observed since then.³⁵ Thus, our study represents the current status of the volume-outcome relationship of clipping and coiling for SAH in Japan.

As for coiling, a study of 534 cases from 29 tertiary referral centers in Japan examined the determinants of poor outcomes (mRS 3–6 at 12 months) in SAH patients when both clipping and coiling were available.³⁹ The authors reported that the type of treatment modality and the size and location of aneurysms did not influence the outcome. In that report, high-volume centers (> 30 cases/yr, 6 centers) did not affect the outcomes. Taken together, this inconsistency in reported results is most likely due to selection bias in each study.

In the present study, the case volumes in the highest quartiles (Q4) for clipping (> 14) and coiling (> 9), which were associated with better outcomes, almost meet the US CSC criteria of the Joint Commission.^1,32 Generally, SAH patients in high-volume centers are more likely to receive neurointensive care in a multidisciplinary setting.⁴ Greater aggressiveness and effectiveness of aneurysm treatment in high-volume centers may explain their lower mortality figures. Considering there was only a weak association between case volume and CSC capabilities for both the clipping and coiling modalities in this study, further research is required to determine the mechanisms underlying the sole influence of case volume.

In terms of risk reduction, when Q4 hospitals were compared to Q1 hospitals, the risk differences of in-hospital mortality for treatment by coiling and clipping were 5.4% and 2.2%, respectively. This result suggests that, based on case volume characteristics, there is a more substantial difference in benefits in terms of mortality risk reduction when aneurysm patients are treated endovascularly rather than surgically.

Effect of CSC Capabilities on In-Hospital Outcomes of SAH Patients

Unexpectedly, we found that CSC capabilities were associated with decreased in-hospital mortality in clipped, but not coiled, SAH patients. Prior studies have demonstrated that institutional factors such as access to endovascular services and teaching hospital status affect the outcomes of aneurysm treatment.^16,20 Interestingly, the proportion of comatose clipped patients in hospitals with higher CSC capabilities (Q3 and Q4) was relatively higher in this study. Improvements in neurosurgical techniques, such as intraoperative angiography, neurocritical care, and neuroimaging, have allowed neurosurgeons to successfully care for patients who would have previously been considered too sick to treat. The availability of technically trained surgeons and access to facilities with endovascular surgery can also sway prognosis since these institutional factors often dictate treatment and were well represented by the components of the CSC score used in this study.

As subspecialty care becomes more centralized, the availability of both treatment modalities poses a dilemma in terms of patient selection. In both clipped and coiled patients, our study showed that the proportion of transferred patients was highest in hospitals with the highest case volume and the highest CSC capabilities. In this light, it is interesting to note the increasing trends in patient transfer in relation to treatment modality based on either case volume or CSC capabilities.

Previously reported studies on coronary artery bypass graft surgery (CABG)⁴⁰ and esophagectomy³³ demonstrated that case volume alone is a relatively weak predictor of outcome and highlighted the need for greater availability of hospital-specific performance data such as measures of care processes.⁴⁰

In this light, we showed that higher CSC capabilities, measured by the CSC score, are associated with reduced in-hospital mortality in SAH patients with or without surgical or endovascular treatment.^13,14 A previous study in the US confirmed this finding.²⁷ According to the J-ASPECT institutional survey conducted in 2010, 2014, and 2018, there were increasing trends in implementation of items related to endovascular treatment (e.g., board-certified endovascular physicians and 24-hour, 7-day endovascular coverage) and multidisciplinary care (e.g., stroke unit), leading to more widespread use of coiling in Japan. The present findings may be explained by the steep learning curve required to achieve coiling proficiency³⁷ and the rapid development of endovascular technology.²⁹ Further research is necessary to determine which items of the CSC score specifically influence outcomes after surgical clipping for aneurysms.

Study Limitations

Our study has several limitations. First, the DPC database lacks several types of data, such as aneurysm characteristics,¹⁵ delayed cerebral ischemia, treatment of vasospasm, and cause of death. However, similar limitations pertain to all previous administrative database studies using diagnostic coding that examined the relationship between hospital case volume and mortality after aneurysm treatment.³⁴ Moreover, unlike all but one³⁴ of those studies,^{2,3,7,9,22,24,25,28,32} our study included adjustment for severity of SAH. The severity of SAH is an important factor that affects clinical outcome.²¹ Therefore, we think that our analysis allowed a more robust comparison of hospital volume and outcomes in SAH patients. Additionally, we used the JCS score rather than the Hunt and Hess grade or the WFNS scale to measure SAH severity. The JCS is widely used in Japan for the assessment of impaired consciousness in SAH patients,^{13,14,17–19} and JCS scores correlate with stroke outcomes.³⁶ Second, inaccuracies with coding may exist within our DPC database, leading to an underestimation or overestimation of outcomes.⁴¹ However, we performed a validation study on SAH patients in our previous analysis of the J-ASPECT Study,¹⁸ and the high levels of accuracy of diagnoses, treatment modalities, and outcomes of this cohort contained in the DPC database were confirmed by a 2-stage sampling method. Third, this study has potential selection bias from voluntary involvement in the registry, with only about half of the 1369 institutions participating. We previously reported that the hospitals participating in this J-ASPECT Study, rather than nonparticipating hospitals, treated more than 10 cases of intracerebral hemorrhage and SAH per 6 months. Hence, hospitals actively working to improve stroke care were more likely to participate in this study,¹⁴ and therefore the present results may not be generalizable to nonparticipating hospitals. In addition, the results of associations between CSC score and outcomes should be interpreted with caution due to potential selection bias, since the CSC score was available in only 447 among the total 621 institutions. Furthermore, there were some significant differences in hospital and patient backgrounds, and such differences may be explained by the geographical location of the hospitals. Therefore, the results regarding associations between CSC score and outcomes should not be generalized to institutions that did not respond to our questionnaire for CSC capabilities. Additionally, the number of participating hospitals in this study is increasing yearly, and the assessment of CSC capabilities has been performed every 4 years after the period of this study. Thus, we are planning to evaluate the validity of the effects of the case volume and CSC score in SAH patients in the future. Fourth, the CSC score is a self-reported questionnaire and not the result of any formal certification process. In Japan, the official certification of PSC (primary stroke center) just began in 2019. The official certification of CSC in the immediate future will be determined by the Japan Stroke Society; therefore, the results of this study could have a significant impact on the recommended items and criteria for the designation CSCs in Japan. After the official certification of the CSC score, we also plan to reassess the effect of CSC capabilities in SAH patients. Fifth, there is a limitation due to the large imbalance of clipping over coiling. Despite the increasing use of coiling in other countries, clipping remains the mainstay treatment for SAH. In fact, the relative merits of clipping and coiling for SAH, and the ratio of clipping to coiling, were different between Japan and the US at the time of this study.¹⁸ Therefore, our results may not be generalizable to other countries, although the ratio of coiling for SAH has recently increased.³⁹ Therefore, further studies will be needed in the future to assess the effects of the ratio of treatment modalities (clipping vs coiling) on patient outcomes.

Online-Only Content

Supplemental material is available with the online version of the article.

• Supplementary eAppendices 1–8. https://thejns.org/doi/suppl/10.3171/2019.12.JNS192584.