Journal List > J Korean Med Sci > v.35(39) > 1146166

Park, Kim, Park, Chang, and Park: National Trends in the Treatment of Ruptured Cerebral Aneurysms in Korea Using an Age-adjusted Method

Abstract

Background

Two primary treatment methods are used for ruptured cerebral aneurysms, surgical clipping and endovascular coiling. In recent decades, endovascular coiling has shown remarkable progress compared to surgical clipping, along with technological developments. The aim of this study was to investigate the recent trends in treatments for ruptured cerebral aneurysms in Korea.

Methods

The data were obtained from the National Health Insurance database. We evaluated the trends in endovascular coiling and surgical clipping for ruptured aneurysms for the period 2000–2017. We obtained the number of prescriptions with International Classification of Diseases, 9th Revision, clinical modification codes related to nontraumatic subarachnoid hemorrhage and prescription codes S4641/4642 for surgical clipping and M1661/1662 for endovascular coiling. The medical expenses for each prescription were also obtained. The primary outcomes included the cumulative number of patients, patient rates per 100,000 people, and the correlation between patient rates and the percentage of the population in each age group.

Results

In the case of surgical clipping, there were no increasing or decreasing trends in the cumulative number of patients when the population/age group was ignored. When examining the trends in patient rates per 100,000 population at each year in male, there was no increasing or decreasing trend in the number of surgical clippings between the age groups, in spite of a decreasing tendency in the number of surgical clipping in male in their 40s and older than 60. In females, the surgical clipping rates tended to decrease only in patients older than 60 years, but there was no tendency to increase or decrease in the other ages. In contrast, the cumulative number of patients who underwent endovascular coiling for ruptured cerebral aneurysms increased year by year regardless of the population/age group. In both male and female, there was no increasing or decreasing trend only in the group aged 40 or younger and there was an increasing tendency in the rest of the age groups. In the trend of medical expenses, both the cost of surgical clipping and endovascular coiling showed increases. Specifically, the medical expense trend in endovascular coiling increased more rapidly than that for surgical clipping.

Conclusion

There was a significant increase in the proportion of patients with ruptured aneurysms undergoing endovascular coiling between 2010 and 2017, whereas the use of surgical clipping decreased. The endovascular coiling was significantly increased in all age groups and surgical clipping was decreased in all age groups, especially in patients under 50 years of age.

Graphical Abstract

jkms-35-e323-abf001.jpg

INTRODUCTION

Two primary treatment modalities are used for ruptured cerebral aneurysms, surgical clipping and endovascular coiling. Since the introduction of Guglielmi detachable coils (GDCs; Boston Scientific Corp., Marlborough, MA, USA) in the early 1990s, prospective clinical studies, including the International Subarachnoid Aneurysm Trial (ISAT)1 and the Barrow Ruptured Aneurysm Trial,23 have supported an increasing role for coil embolization of ruptured aneurysms. The rapid development of endovascular coiling in recent years has been attributed to the development of coils and instruments that can overcome the shape and location challenges of aneurysms. The results of the analysis of clipping and coiling trends in Korea in recent years also show that the rate of coiling is gradually increasing.45 However, there have been no papers statistically analyzing these trends according to sex and age. Therefore, we tried to investigate recent trends in treatment for ruptured cerebral aneurysms using the age-adjusted method.

METHODS

Data acquisition

We collected data between 2010 and 2017 from the National Health Insurance Service (NHIS), the Korean Statistical Information Service (KOSIS), and the Health Insurance Review and Assessment Service (HIRA) in Korea. Annual reports of statistics from the NHIS of Korea were used. The data were collected according to the Korean Standard Classification of Disease and Cause of Death, 6th edition. We used several codes to identify the samples in this study, S4641-S4642 for surgical clipping and M1661-M1662 for endovascular coiling. We also collected the number of males and females in Korea from 2010 to 2017 from the KOSIS.

Measurement outcomes

The primary outcomes of this study were the relationships between annual trends in operation rates and structural age changes. To investigate these two outcomes, cumulative age-standardized prevalence rates per year according to age groups, cumulative age-standardized operation rates per year according to age groups, age-standardized operation rates/patients per year according to age groups, the correlation between patient rates per year and the percentage of the population, the correlation between operation rates per year and the percentage of the population, and the correlation between operations/patient rates per year and the percentage of the population were measured. We subdivided age into the following groups: less than 40 years old, 40s, 50s, and over 60 years old. We described all outcomes as rates standardized per 100,000 people using the actual general population for the relevant year.

Data analysis

The total number of males per year was calculated for each age group in Korea using data from the National Statistical Office. The total number of operations per year according to the age groups were calculated based on diagnosis codes. The cumulative patient and operation rates were analyzed according to year. Cumulative age-standardized patients and operations according to year and age groups were also analyzed. Generalized linear models (GLMs) were used for the analyses. Poisson regression analysis was used for analysis and stratification analysis by sex was used. In model 1, effect sizes of overall time trend were adjusted for age group. Model 2 was analyzed by adding interaction effect (year × age group) to model 1 to identify whether the time trend estimates differ between age groups.
The results are displayed as estimates with standard errors (SEs) and were plotted as line graphs. For age-standardization, we used the formula as follows: number of patients (for the year) × 10,000/total population (for the year). Analyses were performed for the cumulative age-standardized patient rates per 100,000 people, operation rates per 100,000 people, and procedure/patient rates according to year and age groups. GLM was used and the results were displayed as the estimated with SE and plotted as a line graph. A piecewise linear regression model was used to compare trends before and after 2011. Analyses were performed to derive the correlation coefficients between patient rates and the percentage of the population, between operation rates and the percentage of the population, and between operation rates/patient rates and the percentage of the population per year using Pearson correlation analysis. Statistically significant differences were considered for P values of less than 0.05. All data were analyzed using R software (v3.1.2; R Foundation, Vienna, Austria).

RESULTS

Table 1 shows the procedure trends for all aneurysm patients after age adjustment according to age groups.
Table 1

The trend for procedures of all aneurysm patients after age-adjustment according to age groups

jkms-35-e323-i001
Variables Year Time trend P value
2010 2011 2012 2013 2014 2015 2016 2017 Estimate SE 95% CI
Lower Upper
Endovascular coiling
Male, all 5,828 6,250 6,568 7,714 8,668 8,890 11,205 11,278 0.843 0.079 0.650 1.037 < 0.001
Age adjustmenta 0.994 0.127 0.744 1.243 < 0.001
< 40 1.324 1.385 1.281 1.819 1.935 1.774 2.125 1.904 0.111 0.155 −0.193 0.416 Ref.
40–49 8.530 8.764 9.844 10.042 10.981 12.673 14.101 15.282 0.881 0.220 0.450 1.312 0.001
50–59 13.377 13.725 13.944 16.159 18.076 17.444 23.802 21.278 1.295 0.220 0.864 1.726 < 0.001
≥ 60 12.885 13.992 14.034 16.387 18.098 17.831 21.857 22.977 1.354 0.220 0.923 1.785 < 0.001
Female, all 11,966 14,159 15,147 16,804 18,598 19,196 24,199 23,651 1.737 0.156 1.357 2.118 < 0.001
Age adjustmenta 1.793 0.261 1.281 2.305 < 0.001
< 40 1.045 1.529 1.505 1.704 1.931 1.992 2.370 2.170 0.164 0.265 −0.356 0.684 Ref.
40–49 11.592 12.846 14.749 15.505 16.074 17.710 20.432 19.949 1.097 0.375 0.361 1.832 0.007
50–59 25.288 31.061 30.521 33.332 35.825 35.824 44.302 42.340 2.264 0.375 1.529 3.000 < 0.001
≥ 60 33.589 36.672 38.815 42.205 46.254 45.602 57.669 54.936 3.155 0.375 2.420 3.891 < 0.001
Surgical clipping
Male, all 7,293 7,777 7,430 6,913 6,911 6,778 6,969 6,761 −0.116 0.037 −0.207 −0.025 0.021
Age adjustmenta −0.314 0.072 −0.456 −0.172 < 0.001
< 40 1.683 1.575 1.564 1.455 1.210 1.133 0.991 1.033 −0.107 0.114 −0.331 0.116 Ref.
40–49 13.005 11.818 12.061 10.747 9.770 8.811 9.012 8.807 −0.537 0.161 −0.853 −0.221 0.003
50–59 16.820 19.607 16.830 15.615 15.346 16.038 16.197 14.037 −0.359 0.161 −0.675 −0.043 0.036
≥ 60 12.796 14.049 13.186 12.008 13.393 12.458 12.963 13.232 0.069 0.161 −0.246 0.385 0.670
Female, all 13,342 13,993 13,952 12,550 13,742 12,809 14,833 13,702 0.053 −0.235 0.342 0.453 0.667
Age adjustmenta −0.350 −0.572 −0.127 −3.080 0.005
< 40 1.470 1.387 1.081 1.117 1.053 0.958 0.895 0.833 −0.088 −0.518 0.343 −0.398 Ref.
40–49 13.993 14.972 13.963 11.463 12.632 10.865 10.677 9.543 −0.636 −1.245 −0.027 −2.046 0.052
50–59 30.141 30.422 31.527 27.258 28.321 26.160 29.895 27.941 −0.306 −0.915 0.303 −0.986 0.334
≥ 60 33.973 34.651 33.429 30.100 32.941 30.290 35.903 31.685 −0.107 −0.716 0.502 −0.344 0.734
SE = standard error, CI = confidence interval.
aP value adjusted by age group.

Annual trend in coiling procedure

We presented the overall trends of each procedures in male and female groups in Fig. 1, and the analysis of the patients rate and the percentage of population by year according to each age group in Fig. 2.
Fig. 1

Overall trends of the coiling and clipping procedures in male and female patients. (A) Overall trends of the coiling procedures in male patients. The cumulative number of patients regardless of the population or age group showed an increase over the study period. The patient rate per 100,000 population showed an increase in all age groups, except in patients less than 40 years old. (B) Overall trends of the coiling procedures in female patients. The cumulative number of patients regardless of the population or age group showed an increase. The patient rate per 100,000 population showed an increase in all age groups, except for in patients younger than 40 years, which showed a steady trend. (C) Overall trends of the clipping procedures in male patients. There was no increasing or decreasing trend in the cumulative number of patients over the study period. The patient rates also show trends toward decreases or no change. The patient rates by year showed decreases in all age groups. (D) Overall trends of the clipping procedures in female patients. The cumulative number of patients and the patient rates showed decreases or no change.

jkms-35-e323-g001
Fig. 2

Analysis of the patient rates and the percentage of the population by year according to each age group. (A) Male patients treated by coiling procedure. There was a negative correlation in the under 40 and 40s age groups and a positive correlation in the 50s and over 60-year-old age groups with statistical significance in all age groups. (B) Female patients treated by coiling procedure. There was a negative correlation in the under 40 and 40s age groups and a positive correlation in the 50s and over 60 age groups with statistical significance in all age groups. (C) Male patients treated by clipping procedure. There was a positive correlation in patients under 40 and in the 40s age group and a negative correlation in the 50s and over 60 years age groups. It was statistically significant in the under 40 and 40s age groups. (D) Female patients treated by clipping procedure. There was a positive correlation in the under 40 and 40s age groups and a negative correlation in the 50s and over 60 years old groups. It was statistically significant in the under 40 and 40s age groups.

jkms-35-e323-g002
Fig. 1A shows the overall trends of coiling procedures in male patients. The cumulative number of patients regardless of the population or age group showed an increase over the study period from 5,828 in 2010 to 11,278 in 2017. The patient rate per 100,000 population showed an increase in all age groups, except in patients less than 40 years old. The patient rates by year showed an increase in all age groups indicated by a red line in the figure, as shown in Fig. 2A. The percentage of the population by year showed a decrease in patients under 40 and in the 40s age group and increases in the 50s and over 60-year-old groups. In analysis of the correlation between the patient rates and percentage of the population by year, there was a negative correlation in the under 40 and 40s age groups and a positive correlation in the 50s and over 60-year-old age groups (r = 0.864, P = 0.006 in under 40s; r = 0.974, P = 0 in 40–49; r = 0.834, P = 0.01 in 50–59; and r = 0.977, P = 0 in over 60s). The correlation was statistically significant in all age groups.
Fig. 1B shows the overall trends in coiling procedures in female patients. As with coiling in male patients, the cumulative number of patients regardless of the population or age group showed an increase over the study period from 11,966 in 2010 to 24,199 in 2017. The patient rate per 100,000 population showed an increase in all age groups, except for in patients younger than 40 years, which showed a steady trend. The correlation analysis showed the same result as in male patients, as shown in Fig. 2B. The patient rate by year showed an increase in all age groups and the percentage of the population by year showed a decrease in patients under 40 and the 40s age group and increases in the 50s and over 60 age groups. In the correlation analysis between the patient rates and the percentage of the population by year, there was a negative correlation in the under 40 and 40s age groups and a positive correlation in the 50s and over 60 age groups (r = 0.955, P = 0 in under 40s; r = 0.86, P = 0.006 in 40–49; r = 0.892, P = 0.003 in 50–59; and r = 0.956, P = 0 in patients over 60). The correlation was statistically significant in all age groups.
The results showed that, in both male and female patients, although the populations under 40 and in the 40s decreased, the proportion of patients in those age groups who underwent endovascular coiling increased. The population of patients in their 50s and over 60 increased and the patient rates also increased.

Annual trend in clipping procedures

Fig. 1C shows the overall trends in clipping procedures in male patients. There was no increasing or decreasing trend in the cumulative number of patients over the study period. The patient rates also show trends toward decreases or no change. The patient rates by year showed decreases in all age groups. In the correlation analysis between the patient rates and the percentage of the population by year, there was a positive correlation in patients under 40 and in the 40s age group and a negative correlation in the 50s and over 60 years age groups, as shown in Fig. 2C (r = 0.97, P = 0 in under 40s; r = 0.794, P = 0.019 in 40–49; r = 0.645, P = 0.084 in 50–59; and r = 0.129, P = 0.761 in patients over 60). It was statistically significant in the under 40 and 40s age groups.
Fig. 1D shows the overall trends in clipping procedures in female patients. As with clipping in male patients, the cumulative number of patients and the patient rates showed decreases or no change. The correlation analysis showed the same result as in male patients, as shown in Fig. 2D. There was a positive correlation in the under 40 and 40s age groups and a negative correlation in the 50s and over 60 years old groups (r = 0.958, P = 0 in under 40s; r = 0.765, P = 0.027 in 40–49; r = 0.562, P = 0.147 in 50–59; and r = 0.197, P = 0.64 in patients over 60). It was statistically significant in the under 40 and 40s age groups.
This means, in both male and female patients, the population of patients under 40 and in the 40s group decreased and the rate of patients who underwent surgical clipping also decreased. The population of patients in the 50s and over 60 groups increased, but the patient rate decreased.

Trends in medical expenses

Table 2 shows the trends in medical expenses for endovascular coiling and surgical clipping acquired from HIRA. Fig. 3 shows that both the cost for clipping and coiling increased. Specifically, the increasing trend in medical expenses for endovascular coiling was more rapid than that for surgical clipping.
Table 2

The trend of medical expenses of endovascular coiling and surgical clipping

jkms-35-e323-i002
Variables 2010 2011 2012 2013 2014 2015 2016 2017
Coil Clip Coil Clip Coil Clip Coil Clip Coil Clip Coil Clip Coil Clip Coil Clip
No. of patients
< 40 319 424 383 391 360 345 449 329 484 284 464 259 546 230 486 224
40–49 887 1,193 952 1,182 1,082 1,148 1,135 990 1,204 998 1,342 870 1,515 865 1,530 798
50–59 1,365 1,658 1,684 1,882 1,729 1,881 1,981 1,717 2,209 1,790 2,211 1,753 2,859 1,935 2,693 1,777
≥ 60 1,920 1,934 2,155 2,065 2,358 2,071 2,703 1,940 3,100 2,228 3,220 2,165 4,234 2,607 4,338 2,501
Total 4,491 5,209 5,174 5,520 5,529 5,445 6,268 4,976 6,997 5,300 7,237 5,047 9,154 5,637 9,047 5,300
Total amount, 100 million KRW
< 40 32 84 43 78 46 71 60 70 73 68 83 86 100 78 95 81
40–49 88 239 110 236 139 233 151 205 181 243 241 287 278 292 297 283
50–59 133 323 187 369 220 376 261 345 318 417 383 557 509 638 504 597
≥ 60 186 377 237 396 293 409 351 394 447 524 557 688 748 850 793 844
Total 439 1,023 576 1,080 699 1,090 823 1,014 1,018 1,251 1,264 1,618 1,635 1,858 1,689 1,806
Fig. 3

Overall trend of medical expenses for endovascular coiling and surgical clipping.

jkms-35-e323-g003

DISCUSSION

This research showed the national trend in endovascular coiling and surgical clipping with age shifts over the last eight years. To our knowledge, this is the first study to consider age shifts in comparing the trends between endovascular coiling and surgical clipping.
Since the introduction of endovascular treatment for intracranial aneurysms, there have been considerable changes in its uses and outcomes.67 In 2002, the results of the ISAT study performed as a multicenter phase III trial were published.1 The ISAT study compared endovascular and surgical treatments for 2,143 patients suitable for both treatments. Further patient recruitment was discontinued prematurely because the interim analysis showed a significantly low occurrence of disability and death in the endovascular treatment group. The surgical treatment group showed a higher probability of being dependent or dying compared to the endovascular treatment group (31% of 793 patients vs. 24% of 801 patients). Since the publication of the ISAT results, American and European guidelines have recommended endovascular treatment for ruptured cerebral aneurysms.89 In 2003, the Food and Drug Administration expanded its guidelines to permit the use of GDC coils for all brain aneurysms.10
After that, a steadily increasing percentage of patients have been treated by endovascular methods. The cumulative number of patients, as well as the ratio of patients undergoing endovascular coiling according to the population per year, jumped over the study period.111213 In 2010, Kim et al.14 performed a nationwide multicenter survey and reported the treatment of unruptured aneurysm. In their study, 49.9% of unruptured aneurysms were treated with clipping, 48.6% with coiling, and the remaining 0.5% with combined method. The increase in coiling procedures can be explained by the following reasons. The first reason is technological development. Widespread application of the coiling procedure due to advancements in treatment materials and techniques, as well as assisted coil embolization using stents or balloons, is more common.1516171819 The other cause is an increase in the experience of surgeons and institutions.2021 In recent years, coil embolization has been widely performed in secondary general hospitals and not limited to tertiary university hospitals.2223
Previous studies have compared the trends in endovascular coiling and surgical clipping using HIRA data.24 One study showed that neurointervention, including not only endovascular coiling for aneurysm, but also mechanical thrombectomy for ischemic stroke, and stenting and angioplasty for carotid and intracranial artery stenosis, continued to increase. Our research differed from previous studies in that it reflected changes in demographics by age groups. Our findings showed that the proportion of people under 50 decreased and that of people over 50 increased in the overall demographics. Endovascular coiling was significantly increased in all age groups and surgical clipping was decreased in all age groups, especially in patients under 50 years of age. Moreover, the number of patients undergoing surgical clipping was significantly decreased with a positive correlation. Considering these trends and the increasing trend in the elderly population, the area of endovascular coiling can be expected to increase gradually compared to surgical clipping.
This finding is not just limited to Korea, but is a global trend. In a 25-year observational study in the United States, the percentage of coiling was 3% in 1991 and jumped to 42% in the 2010s.25 In a European study published in the UK, the number of patients undergoing surgical clipping decreased from 51% to 31%, whereas the number of patients receiving endovascular coiling increased from 35% to 68% since the ISAT study results were reported.26
Our study revealed that the medical expense of coiling was higher than that of clipping, in spite of the shorter hospital stay and lower procedure cost in Korea. In Korea, the current procedure charge is 3,040,038 KRW (S4641, simple clipping) and 3,516,663 KRW (S4642, complex clipping) for surgical clipping, which is higher than that of endovascular coiling (M1661, assisted coiling; M1662, simple coiling). The cause of the higher cost of coiling might be associated with the medical devices themselves.2728 Under the current insurance system in Korea, both the total medical cost and the patient burden cost of endovascular coiling are higher than those of surgical clipping.29 In the previous study, it was found that in the case of surgical clipping, the hospitalization fee including the intensive care unit cost, and in the case of endovascular coiling, the cost of surgical material including multiple coils accounted for the largest portion.30
The strength of our study was statistical analysis using age-standardization by year. However, because we used data based on diagnostic codes and billed medical expenses, it did not reflect aneurysm information and cannot exclude the possibility of duplicated or missing data. In addition, because data acquisition was done using prescription codes, a separate analysis of ruptured aneurysms and unruptured aneurysms could not be performed. This is another limitation of this study that the unruptured aneurysms accompanying subarachnoid hemorrhage were not clearly excluded. Coil embolization is currently being performed by both neurosurgeons and interventional neuroradiologists, and selection bias due to the fact that neuroradiologists will prefer coils over clips should be considered. This study does not reflect the size of the hospital, so the fact that the coiling procedure in secondary hospitals has recently increased is another factor that can affect bias. Also, because of the nature of the data obtained from NHIS, KOSIS, and HIRA, we could not analyze procedure-related complications and long-term prognosis according to treatment modality because it was not possible to obtain complete information of the treatment process. In the same vein, because the variables related to the procedural complication were not considered, the cost of each item including procedure charge, medical device, and hospitalization cost, could not be analyzed from the total medical cost.
In conclusion, there was a significant increase in the proportion of patients with ruptured aneurysms undergoing endovascular coiling between 2010 and 2017, whereas the use of surgical clipping decreased. The endovascular coiling was significantly increased in all age groups and surgical clipping was decreased in all age groups, especially in patients under 50 years of age.

Notes

Funding: This research was supported by Soonchunhyang University Research Fund (2020).

Disclosure: The authors have no potential conflicts of interest to disclose.

Author Contributions:

  • Conceptualization: Kim JH, Chang JC.

  • Data curation: Kim JH, Chang JC, Park HR.

  • Formal analysis: Park S, Park HR.

  • Investigation: Park HR.

  • Methodology: Park S, Park SQ.

  • Software: Park S.

  • Validation: Park S.

  • Writing - original draft: Park HR.

  • Writing - review & editing: Park HR, Park SQ, Kim JH.

References

1. Molyneux A, Kerr R. International Subarachnoid Aneurysm Trial (ISAT) Collaborative Group. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomized trial. J Stroke Cerebrovasc Dis. 2002; 11(6):304–314. PMID: 17903891.
crossref
2. McDougall CG, Spetzler RF, Zabramski JM, Partovi S, Hills NK, Nakaji P, et al. The barrow ruptured aneurysm trial. J Neurosurg. 2012; 116(1):135–144. PMID: 22054213.
crossref
3. Spetzler RF, McDougall CG, Zabramski JM, Albuquerque FC, Hills NK, Russin JJ, et al. The barrow ruptured aneurysm trial: 6-year results. J Neurosurg. 2015; 123(3):609–617. PMID: 26115467.
crossref
4. Lee SU, Kim T, Kwon OK, Bang JS, Ban SP, Byoun HS, et al. Trends in the incidence and treatment of cerebrovascular diseases in Korea : Part I. Intracranial aneurysm, intracerebral hemorrhage, and arteriovenous malformation. J Korean Neurosurg Soc. 2020; 63(1):56–68. PMID: 31064041.
crossref
5. Kim JJ, Cho KC, Jung WS, Suh SH. Endovascular treatment for intracranial aneurysms: a nationwide survey in Korea. Neurointervention. 2020; 15(1):18–24. PMID: 31955548.
crossref
6. Qureshi AI. Endovascular treatment of cerebrovascular diseases and intracranial neoplasms. Lancet. 2004; 363(9411):804–813. PMID: 15016492.
crossref
7. Qureshi AI, Janardhan V, Hanel RA, Lanzino G. Comparison of endovascular and surgical treatments for intracranial aneurysms: an evidence-based review. Lancet Neurol. 2007; 6(9):816–825. PMID: 17706565.
crossref
8. Derdeyn CP, Barr JD, Berenstein A, Connors JJ, Dion JE, Duckwiler GR, et al. The International Subarachnoid Aneurysm Trial (ISAT): a position statement from the Executive Committee of the American Society of Interventional and Therapeutic Neuroradiology and the American Society of Neuroradiology. AJNR Am J Neuroradiol. 2003; 24(7):1404–1408. PMID: 12917138.
9. Raabe A, Schmiedek P, Seifert V, Stolke D. German society of neurosurgery section on vascular neurosurgery: position statement on the International Subarachnoid Hemorrhage Trial (ISAT). Zentralbl Neurochir. 2003; 64(3):99–103. PMID: 12975743.
10. Qureshi AI, Hutson AD, Harbaugh RE, Stieg PE, Hopkins LN. North American Trial of Unruptured and Ruptured Aneurysms Planning Committee. Methods and design considerations for randomized clinical trials evaluating surgical or endovascular treatments for cerebrovascular diseases. Neurosurgery. 2004; 54(2):248–264. PMID: 14744272.
11. van der Schaaf I, Algra A, Wermer M, Molyneux A, Clarke M, van Gijn J, et al. Endovascular coiling versus neurosurgical clipping for patients with aneurysmal subarachnoid haemorrhage. Cochrane Database Syst Rev. 2005; (4):CD003085. PMID: 16235314.
crossref
12. Li H, Pan R, Wang H, Rong X, Yin Z, Milgrom DP, et al. Clipping versus coiling for ruptured intracranial aneurysms: a systematic review and meta-analysis. Stroke. 2013; 44(1):29–37. PMID: 23238862.
13. Hwang JS, Hyun MK, Lee HJ, Choi JE, Kim JH, Lee NR, et al. Endovascular coiling versus neurosurgical clipping in patients with unruptured intracranial aneurysm: a systematic review. BMC Neurol. 2012; 12:99. PMID: 22998483.
crossref
14. Kim JE, Lim DJ, Hong CK, Joo SP, Yoon SM, Kim BT. Treatment of unruptured intracranial aneurysms in South Korea in 2006 : a nationwide multicenter survey from the Korean Society of Cerebrovascular Surgery. J Korean Neurosurg Soc. 2010; 47(2):112–118. PMID: 20224709.
crossref
15. Fargen KM, Mocco J, Neal D, Dewan MC, Reavey-Cantwell J, Woo HH, et al. A multicenter study of stent-assisted coiling of cerebral aneurysms with a Y configuration. Neurosurgery. 2013; 73(3):466–472. PMID: 23756744.
crossref
16. Liu KC, Ding D, Starke RM, Geraghty SR, Jensen ME. Intraprocedural retrieval of migrated coils during endovascular aneurysm treatment with the Trevo Stentriever device. J Clin Neurosci. 2014; 21(3):503–506. PMID: 24332812.
crossref
17. Crobeddu E, Lanzino G, Kallmes DF, Cloft HJ. Review of 2 decades of aneurysm-recurrence literature, part 1: reducing recurrence after endovascular coiling. AJNR Am J Neuroradiol. 2013; 34(2):266–270. PMID: 22422180.
crossref
18. Gory B, Klisch J, Bonafé A, Mounayer C, Beaujeux R, Moret J, et al. Solitaire AB stent-assisted coiling of wide-necked intracranial aneurysms: mid-term results from the SOLARE study. Neurosurgery. 2014; 75(3):215–219. PMID: 24818784.
19. Alaraj A, Wallace A, Dashti R, Patel P, Aletich V. Balloons in endovascular neurosurgery: history and current applications. Neurosurgery. 2014; 74(Suppl 1):S163–S190. PMID: 24402485.
20. Bekelis K, Gottlieb D, Labropoulos N, Su Y, Tjoumakaris S, Jabbour P, et al. The impact of hybrid neurosurgeons on the outcomes of endovascular coiling for unruptured cerebral aneurysms. J Neurosurg. 2017; 126(1):29–35. PMID: 26918479.
crossref
21. Lanzino G, Rabinstein AA. Endovascular neurosurgery in the United States: a survey of 59 vascular neurosurgeons with endovascular training. World Neurosurg. 2011; 75(5-6):580–585. PMID: 21704910.
crossref
22. Johnston SC. Effect of endovascular services and hospital volume on cerebral aneurysm treatment outcomes. Stroke. 2000; 31(1):111–117. PMID: 10625724.
crossref
23. Smith GA, Dagostino P, Maltenfort MG, Dumont AS, Ratliff JK. Geographic variation and regional trends in adoption of endovascular techniques for cerebral aneurysms. J Neurosurg. 2011; 114(6):1768–1777. PMID: 21314274.
crossref
24. Suh SH. The annual trends between neurointerventional and neurosurgical procedures in Korea: analysis using HIRA data from 2010 to 2016. Neurointervention. 2017; 12(2):77–82. PMID: 28955509.
crossref
25. Bender MT, Wendt H, Monarch T, Lin LM, Jiang B, Huang J, et al. Shifting treatment paradigms for ruptured aneurysms from open surgery to endovascular therapy over 25 years. World Neurosurg. 2017; 106:919–924. PMID: 28736346.
crossref
26. Gnanalingham KK, Apostolopoulos V, Barazi S, O'Neill K. The impact of the International Subarachnoid Aneurysm Trial (ISAT) on the management of aneurysmal subarachnoid haemorrhage in a neurosurgical unit in the UK. Clin Neurol Neurosurg. 2006; 108(2):117–123. PMID: 16364540.
crossref
27. Halkes PH, Wermer MJ, Rinkel GJ, Buskens E. Direct costs of surgical clipping and endovascular coiling of unruptured intracranial aneurysms. Cerebrovasc Dis. 2006; 22(1):40–45. PMID: 16567936.
crossref
28. Hoh BL, Chi YY, Dermott MA, Lipori PJ, Lewis SB. The effect of coiling versus clipping of ruptured and unruptured cerebral aneurysms on length of stay, hospital cost, hospital reimbursement, and surgeon reimbursement at the university of Florida. Neurosurgery. 2009; 64(4):614–619. PMID: 19197221.
crossref
29. Park KW, Park CW, Jun YI, Yoo CJ, Kim YB, Park CW. Cost analysis for the management of cerebral aneurysms: comparison between clipping and coiling. Korean J Cerebrovasc Surg. 2006; 8(4):260–266.
30. Kim M, Park J, Lee J. Comparative cost analysis for surgical and endovascular treatment of unruptured intracranial aneurysms in South Korea. J Korean Neurosurg Soc. 2015; 57(6):455–459. PMID: 26180615.
crossref
TOOLS
Similar articles