Results of treatment of aneurysmal subarachnoid hemorrhage in the elderly

Česká verzia

Authors: E. Hovorka ¹; O. Navrátil ¹; K. Ďuriš ^1,2; V. Juráň ¹; K. Svoboda ¹; A. Mrlian ¹; V. Vybíhal ¹ ; J. Hustý ³; M. Smrčka ¹
Authors place of work: Neurochirurgická klinika LF MU a FN Brno ¹; Patofyziologický ústav, LF MU, Brno ²; Klinika radiologie a nukleární medicíny LF MU a FN Brno ³
Published in the journal: Cesk Slov Neurol N 2023; 86(4): 256-261
Category: Původní práce
doi: https://doi.org/10.48095/cccsnn2023256

Summary

Introduction: The aim of our study is to present the treatment outcomes of patients with aneurysmal subarachnoid hemorrhage (SAH) 3 months after the attack who were treated with clipping (MS) or coiling (EV). Materials and methods: The study was based on a retrospective analysis of a database of patients with cerebral aneurysms who were treated at the University Hospital Brno between 2009 and 2019. A total of 499 patients were included in the study. Of these patients, 345 (69%) were treated with surgical MS and 154 (31%) were treated with EV. Patients were divided into 4 groups: according to the age into 0–64 years and 65+ years group, and according to the modality of treatment of aneurysm by MS or EV. We evaluated the effect of the initial Hunt-Hess (HH) score on the treatment outcome according to age and modality and also the relationship between the current age of the patient and the treatment outcome at 3 months after the SAH attack, as assessed by a modified Rankin scale (mRS), where the successful treatment outcome was mRS 0–2 (self-sufficient patient), and the effect of the initial Hunt-Hess score (HH) on the treatment outcome was based on age and modality. Results: Of the 499 patients, 345 (69%) were treated with MS and 154 (31%) with EV, and the average age of MS and EV treated patients was not statistically significantly different (P = 0.2216). In both surgically and endovascularly treated patients in all age categories; we did not observe a statistically significant difference in HH score (P = 0.1664) or in graphical severity of SAH according to the Fischer score (P = 0.5041). Satisfactory treatment outcome (mRS 0–2) at 3 months after the attack was found in 49 (52.88%) in the 65+ years group after MS and 23 (60.61%) in the 65+ years group after EV. Poor treatment outcome (mRS 3–6) at 3 months was found in 43 (47.12%) in MS treated and 15 (39.39%) in EV treated patients, which was statistically significant (P = 0.0002). Satisfactory treatment outcome (mRS 0–2) at 3 months with good clinical status on admission (HH 1–2) was seen in 136 (55%) patients in the 0–64 years group after MS and 28 (33%) in the 65+ years group after MS. Poor treatment outcome (mRS 3–6) after 3 months with poor initial clinical condition (HH 3–5) had 50 (20%) patients treated with MS in the 0 -64 years group and 39 (44%) treated with MS in the 65+ years group, which is statistically significant (P = 0.0001). Conclusion: Elderly (65+ years) after SAH are at a higher risk of poor neurological status 3 months after the attack compared to younger patients, especially if they are in a severe clinical condition on admission. However, a significant proportion of these patients remain in a good clinical condition after treatment of an aneurysm, so the method of treatment and extent of treatment needs to be assessed individually. In elderly patients treated endovascularly, we observed a better treatment outcome at 3 months compared with patients treated by open surgery.

Keywords:

clipping – seniors – subarachnoid hemorrhage – coiling

Introduction

Intracranial aneurysm rupture is responsible for 80% of cases of non-traumatic subarachnoid hemorrhage (SAH) [1]. The purpose of early treatment of the source of bleeding is to prevent re-rupture of the aneurysm with fatal consequences. Cerebral artery aneurysm is standardly treated by one of two modalities - surgical clipping (MS) or endovascular coiling (EV) [2].

The increasing average life expectancy of the population that remains in good physical and mental condition has resulted in an increased number of patients requiring treatment for SAH from ruptured aneurysms, therefore the correct choice of the appropriate modality is very important.

Older age and poor clinical condition on admission are some of the known risk factors for unsatisfactory treatment outcome after SAK [3–9]. The upper limit of age, when it is feasible to treat patients with a ruptured aneurysm and achieve a good treatment outcome, is individual. Therefore, according to the literature it is advisable to actively treat ruptured aneurysms in elderly patients in good or stable clinical condition [10,11].

Indication criteria for modality selection include the patient's clinical condition, age, presence of comorbidities, treatment with blood thinning medications, aneurysm characteristics, and the presence of a significant intracerebral hematoma [3–6]. The modern approach to the management of SAH involves a targeted, strictly individualized assessment of the patient's disease.

The aim of our study is to evaluate the outcomes of elderly patients (over 65 years of age) treated for aneurysmal SAH at University Hospital Brno, to compare them with younger patients and the literature, and to identify potential areas of improvement in the care and treatment of these patients.

Material and methodology

The study was based on a retrospective analysis of a database of patients with cerebral aneurysms who were treated at University Hospital Brno between 2009 and 2019. During that interval, a total of 671 patients were hospitalized at University Hospital Brno with a diagnosis of spontaneous subarachnoid hemorrhage (SAH), and 499 patients were included in the study who were hospitalized with a diagnosis of SAH from cerebral artery aneurysm rupture and were treated with one of the modalities of clipping or coiling or both. Patients with SAK who did not have a diagnosis of aneurysm and those treated conservatively were excluded from the study.

For patients treated with both modalities, we assigned a patient to the modality group that definitively excluded the aneurysm from the circulation. These were primary coiled patients whose aneurysm was inadequately treated (significant sack filling) or who underwent rebleeding after endovascular treatment. Therefore, they were subsequently treated with a clip. We did not have a case of inadequate clip treatment with the possibility of definitive coil treatment in our cohort.

These patients were always treated within 24 h of SAH attack and treatment with both modalities, i.e., MS and EV, was always available. Patients with bleeding in both the anterior and posterior basin, in all sites of the intracranial arteries, were included.

We clipped patients with expansive behaving intracerebral hematoma, aneurysms with wide neck, predominantly in the anterior circulation or where coiling is not technically feasible, e.g., due to anatomical conditions or pathology of the vasculature. Furthermore, we also clipped younger patients up to 65 years and patients in good initial neurostatus (HH 1–2), which was also not absolute.

Coiling was mainly used for elderly (65+), polymorbid patients with a pharmacological history of drugs affecting blood clotting, in poorer clinical condition (HH 3–5), without expansive ICH, posterior basin aneurysms and aneurysms with favorable neck/sack ratio.

We divided the patients into 4 groups. According to age into 0–64 years and 65+ years group. Further according to the modality of aneurysm treatment by clipping or coiling. We evaluated the relationship between the age of the patient and the treatment outcome 3 months after SAH attack, assessed by modified Rankin scale (mRS), in patients hospitalized at University Hospital Brno after treatment of intracranial aneurysm, where the successful treatment outcome was mRS 0–2 (self-sufficient patient), and the effect of initial HH on the treatment outcome according to age and modality.

Data are presented in the form of descriptive statistics including absolute and relative values and subsequent analyses. Categorical data were assessed using the Chi-square test. For continuous data, the distribution of test data was assessed using the D'Agostino-Pearson normality test. Unpaired t-test with Welch's correction, Kruskal-Walisovatestus followed by Dunn's multiple comparison test was used for statistical evaluation of data. The significance level was considered to be α = 0.05. Statistical data processing was performed using GraphPadPrismversion 7.03 for Windows software (GraphPadSoftware, La Jolla,CA, USA, www.graphpad.com).

The study is not subject to ethics committee approval; patients signed a consent form for the diagnostic and treatment process.

Results

Out of 499 patients, 345 (69%) were treated with MS and 154 (31%) with EV, the average age of surgically treated patients was 53.77 (SD 13.69) years, whereas the average age of endovascularly treated patients was 55.35 (SD 13.17) years, which is not a significant difference (P = 0.2216, unpaired t-test with Welch correction).

Table 1 shows the structure of the cohort according to HH, age and type of procedure. In surgically and endovascularly treated patients in all age categories, the clinical condition corresponding to HH2 prevailed (MS 0–64 years 44.1%, MS 65+ 28.57% and MS 65+ 28.57%, respectively EV 0–64 years 38.98%, EV 65+ 47.22%), followed by HH3 score (MS 0–64 years 22.44%, MS 65+ 34.07% and EV 0–64 years 29.66%, EV 65+ 34.7%, respectively). There was no significant difference in the cohort structure according to HH, age and type of surgery (P = 0.1664, Chi-squared test).

Table 2 shows the structure of the cohort according to Fs, age and treatment modality. In both surgically and endovascularly treated patients in all age groups, the predominant graphic severity of SAH on CT was corresponding to Fischer score 3 (MS 0–64 years 54.04%, MS 65+ 48.91% and MS 65+ 48.91%, respectively EV 0–64 years 57.27%, EV 65+ 67.57%), followed by Fischer score 4 (MS 0–64 years 32.81%, MS 65+ 43.48% and EV 0–64 years 32.48%, EV 65+ 29.73%, respectively). Thus, there was no significant difference in the structure of the cohort according to Fs, age and type of surgery (P = 0.5041, Chi-squared test).

The mean mRS at 3 months in the 0–64 years group after MS was 1.852 and in the EV group 1.886, which is not statistically significant (P = 0.9999, Dunn's multiple comparison test).

In both surgically and endovascularly treated patients in all age groups, the predominant outcome in 3 months was mRS 1(MS 0–64 years 60.49%, MS 65+ 37.94% and MS 65+ 37.94% respectively. EV 0–64 years 56.14%, EV 65+ 37.94%) followed by mRS 2(MS 0–64 years 14.40% and EV 0–64 years 12.29%, EV 65+ 27.27% respectively) except in the MS 65+ group where mRS 4 (17.24%) followed as shown in table 3.

Table 4 describes the summary of the number of patients with satisfactory versus unsatisfactory treatment outcome by treatment modality and age. Satisfactory treatment outcome (i.e., mRS 0–2) in 3 months after the attack had 49 (52.88%) patients in the 65+ years group after MS and 23(60.61%) patients in the 65+years group after EV. And poor treatment outcome (mRS 3–6) in 3 months had 43 (47.12%) patients treated with MS and 15(39.39%) treated with EV, which is statistically significant (P = 0.0002, Chi-square test).

The treatment outcome depending on the initial clinical status for each age group and treatment modality is shown in Table 5. Satisfactory outcome (mRS 0–2) in 3 months after the attack in patients in good clinical condition on admission (HH 1–2) in the group 0–64 years after MS had 136 (55%) patients and 9(3%) of these patients ended up in poor clinical condition(mRS 3–6), while 50 (20%) patients were in poor clinical status on admission(HH3-5) with poor treatment outcome(mRS 3–5) and good treatment outcome was seen in 56 (22%) in the HH 3–5 group of young after MS.

In youth in good condition on admission treated EV in 3 months after the attack, successful treatment outcome was seen in 55 (46%) and unsatisfactory treatment outcome in 8 (5%).

In patients 65+ after MS in initial good condition, 28 (33%) had good treatment outcome and 4 (3%) had poor outcome. In elderly patients at initial good condition treated with EV had satisfactory treatment outcome 13 (37%) and unsatisfactory treatment outcome 5 (13%).

And poor treatment outcome (mRS 3–6) after 3 months with poor initial clinical status(HH 3–5) had 50 (20%) patients treated with MS in 0–64 years group and 39 (44%) treated with MS in 65+ group which is statistically significant (P = 0.0001, Chi-square test).

Discussion

The aim of our study is to evaluate the outcomes of treatment of elderly patients (over 65 years), to compare them with younger patients, facts from literature and to identify potential areas of improvement in the care and treatment of these patients.

Our study shows that we have treated more patients surgically over 11 years with a ratio of 345 (69%) MS : 154 (31%) EV.

Higher age and more severe clinical condition on admission of patients with SAH is associated with the risk of poor treatment outcome and therefore worse neurological deficit [4,12–17]. Similarly, in our study, we found out that higher patient age and severe clinical condition at admission were risk factors for poor neurological status in clinical follow-up after 3 months, a relatively short treatment outcome.

Our study focused on the comparison of treatment outcome (assessed by mRS) after microsurgical clipping and endovascular coiling [18–23]. In the follow-up in 3 months after the attack, it was found that in the 65+ group, patients treated with the endovascular method had a better treatment outcome than those who underwent clipping from craniotomy, which is in contrast to Capatano et al. [12], who based on the BRAT study [24–27] and whose study set an age limit also of 65 years, but which implied clipping as a more successful treatment modality.

Similar results to our study were achieved by Ikawa et al. [11] 2018, who also evaluated their results over a similar follow-up horizon and reported endovascular treatment as having a better treatment outcome than open neurosurgical intervention. Furthermore, we learn from this study that there is a general trend in Japan to treat more ruptured aneurysms with clipping, by about 3 : 1, which is a difference from other countries that have leaned more towards coiling after the ISAT study [18]. And this ratio of clip versus coil treatment was similar with our department in 2009–2019, and currently the ratio is 1:1 in our department.

Bekelis et al. [28] in their 2016 study reported no statistically significant difference in treatment outcome between the modalities in the elderly, and the same is true in the 2018 paper by Proust et al. [29]. However, these papers are based on follow-up after one year.

The better treatment outcome after coiling in the elderly is mostly explained by the shorter duration of the procedure and therefore shorter general anesthesia. Also, there is no manipulation of brain tissue and thus no microtraumatization of the edematous brain. Furthermore, elderly patients are at higher risk of surgical complications due to malnutrition and reduced immunity [30]. However, in our study cohort, we did not observe a significant increase in early surgical complications in operated patients over 65 years of age.

Nowadays, we also consider treatment in patients over 80 years of age, especially if we know that their previous quality of life has been satisfactory and they are in good condition after SAH (HH 1–2). Also, according to our results, the blurred line for surgical treatment of aneurysms with a chance of minimum early complications and good treatment outcome is the age around 65 years, taking into account other factors as well. Ohkuma even puts this threshold at 85years of age [10]. In the group 0–64 years, we did not observe a significant difference in treatment outcome between the group of patients treated with clipping or coiling.

According to our results, the Hunt-Hess score and Fischer score, i.e., the clinical and graphic severity of SAH on admission, did not influence the modality chosen to treat the aneurysm. With the exception of expansive behaving intracerebral hematomas, in which clipping from craniotomy was indicated. According to the retrospectively available data, the anatomy of the aneurysm (localization, size, direction of the sack, and width of the neck versus the sack) was most important for the choice of treatment modality. Lavage of the affected area and reduction of the amount of blood thought to be the cause of vasospasm could be beneficial [31]. Another procedure applied in the surgical procedure at our institution is fenestration of the lamina terminalis. According to some authors, fenestration of the lamina terminalis might reduce the risk of hydrocephalus [32–35].

The clinical and graphic status on admission did not have a major influence on the choice of treatment modality is also described by Zanaty et al. [19]. However, in their study, the decision-making is influenced by the fact that the treatment procedure is performed by a neurosurgeon trained in both treatment modalities.

A limitation factor of our study is that we obtained treatment results 3 months after the attack, which for many research may not be a long enough follow-up period, especially if we want to assess quality of life as a treatment outcome. The minimum time to assess treatment outcome is 1 year after the attack by many authors [29,36].

Conclusion

Seniors (65+years) after SAH are at higher risk of poor neurological status 3 months after the attack compared to younger patients, especially if they are in severe clinical condition on admission. However, a significant proportion of these patients remain in good clinical condition after treatment of the aneurysm, so the method of treatment and scope of treatment needs to be assessed on an individual basis. In elderly patients treated endovascularly we observed a better treatment outcome in 3 months compared to patients treated by open surgery.

Zdroje

1. Deutsch BC, Neifert SN, Caridi JM. No disparity in outcomes between surgical clipping and endovascular coiling after aneurysmal subarachnoid hemorrhage. World Neurosurg 2018; 120: e318–e325. doi: 10.1016/ j.wneu.2018.08.060.

2. Solheim O, Eloqayli H, Muller TB et al. Quality of life after treatment for incidental, unruptured intracranial aneurysms. Acta Neurochir (Wien) 2006; 148 (8): 821–830. doi: 10.1007/s00701-006-0804-7.

3. Shimamura N, Naraoka M, Katagai T et al. Analysis of factors that influence long-term independent living for elderly subarachnoid hemorrhage patients. World Neurosurg 2016; 90: 504–510. doi: 10.1016/j.wneu.2016.03. 057.

4. Lanzino G, Kassell NF, Germanson TP et al. Age and outcome after aneurysmal subarachnoid hemorrhage: why do older patients fare worse? J Neurosurg 1996; 85 (3): 410–418. doi: 10.3171/jns.1996.85.3.0 410.

5. Braun V, Rath S, Antoniadis G et al. Treatment and outcome of aneurysmal subarachnoid haemorrhage in the elderly patient. Neuroradiology 2005; 47 (3): 215–221. doi: 10.1007/s00234-005-1356-x.

6. Rosengart AJ, Schultheiss KE, Tolentino J et al. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke 2007; 38 (8): 2315–2321. doi: 10.1161/STROKEAHA.107.484360.

7. Bederson JB, Connolly ES, Batjer HH et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a statement for healthcare professionals from a special writing group of the Stroke Council, American Heart Association. Stroke 2009; 40 (3): 994–1025. doi: 10.1161/STROKEAHA.108.191395.

8. Gonzalez NR, Dusick JR, Duckwiler G et al. Endovascular coiling of intracranial aneurysms in elderly patients: report of 205 treated aneurysms. Neurosurgery 2010; 66 (4): 714–721. doi: 10.1227/01.NEU.0000367451.590 90.D7.

9. Horiuchi T, Hongo K. Clipping surgery for aneurysmal subarachnoid hemorrhage in patients aged 75 years or older. Neurol Res 2011; 33 (8): 853–857. doi: 10.1179/1743132811Y.0000000013.

10. Ohkuma H, Shimamura N, Naraoka M et al. Aneurysmal subarachnoid hemorrhage in the elderly over age 75: a systematic review. Neurol Med Chir (Tokyo) 2017; 57 (11): 575–583. doi: 10.2176/nmc.ra.2017- 0057.

11. Ikawa F, Abiko M, Ishii D et al. Effect of actual age on outcome at discharge in patients by surgical clipping and endovascular coiling for ruptured cerebral aneurysm in Japan. Neurosurg Rev 2018; 41 (4): 1007–1011. doi: 10.1007/s10143-017-0942-9.

12. Catapano JS, Zeoli T, Frisoli FA et al. Long-term independence in older patients with aneurysmal subarachnoid hemorrhage in the Barrow ruptured aneurysm trial. World Neurosurg 2021; 147: e98–e104. doi: 10.1016/ j.wneu.2020.11.139.

13. Goldberg J, Schoeni D, Mordasini P et al. Survival and outcome after poor-grade aneurysmal subarachnoid hemorrhage in elderly patients. Stroke 2018; 49 (12): 2883–2889. doi: 10.1161/STROKEAHA.118.022869.

14. Hütter BO, Kreitschmann-Andermahr I, Gilsbach JM. Health-related quality of life after subarachnoid hemorrhage: impacts of bleeding severity, computerized tomography findings, vasospasm, surgery, and neurological grade. J Neurosurg 2001; 94 (2): 241–251. doi: 10.3171/jns.2001.94.2.0241.

15. Ogilvy CS, Carter BS. A proposed comprehensive grading system to predict outcome for surgical management of intracranial aneurysms. Neurosurgery 1998; 42 (5): 959–968. doi: 10.1097/00006123-199805000-00001.

16. van Donkelaar CE, Bakker NA, Birks J et al. Prediction of outcome after aneurysmal subarachnoid hemorrhage. Stroke 2019; 50 (4): 837–844. doi: 10.1161/STROKEAHA.118. 023902.

17. Pegoli M, Mandrekar J, Rabinstein AA et al. Predictors of excellent functional outcome in aneurysmal subarachnoid hemorrhage. J Neurosurg 2015; 122 (2): 414–418. doi: 10.3171/2014.10.JNS14290.

18. Molyneux AJ, Kerr RSC, Yu LM et al. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005; 366 (9488): 809–817. doi: 10.1016/S0140-6736 (05) 67 214-5.

19. Zanaty M, Chalouhi N, Starke RM et al. Short-term outcome of clipping versus coiling of ruptured intracranial aneurysms treated by dual-trained cerebrovascular surgeon: single-institution experience. World Neurosurg 2016; 95: 262–269. doi: 10.1016/j.wneu.2016.08. 009.

20. Taha MM, Nakahara I, Higashi T et al. Endovascular embolization vs surgical clipping in treatment of cerebral aneurysms: morbidity and mortality with short-term outcome. Surg Neurol 2006; 66 (3): 277–284. doi: 10.1016/j.surneu.2005.12.031.

21. Schwartz C, Aster HC, Al-Schameri R et al. Microsurgical clipping and endovascular treatment of middle cerebral artery aneurysms in an interdisciplinary treatment concept: comparison of long-term results. Interv Neuroradiol 2018; 24 (6): 608–614. doi: 10.1177/1591019918792231.

22. Ikawa F, Abiko M, Ishii D et al. Analysis of outcome at discharge after aneurysmal subarachnoid hemorrhage in Japan according to the Japanese stroke databank. Neurosurg Rev 2018; 41 (2): 567–574. doi: 10.1007/s10143-017-0894-0.

23. Ryttlefors M, Enblad P, Kerr RSC et al. International subarachnoid aneurysm trial of neurosurgical clipping versus endovascular coiling. Stroke 2008; 39 (10): 2720–2726. doi: 10.1161/STROKEAHA.107.506 030.

24. McDougall CG, Spetzler RF, Zabramski JM et al. The Barrow ruptured aneurysm trial. J Neurosurg 2012; 116 (1): 135–144. doi: 10.3171/2011.8.JNS101767.

25. Spetzler RF, McDougall CG, Albuquerque FC et al. The Barrow ruptured aneurysm trial: 3-year results. J Neurosurg 2013; 119 (1): 146–157. doi: 10.3171/2013.3.JNS12 683.

26. Spetzler RF, McDougall CG, Zabramski JM et al. The Barrow ruptured aneurysm trial: 6-year results. J Neurosurg 2015; 123 (3): 609–617. doi: 10.3171/2014.9.JNS141 749.

27. Spetzler RF, McDougall CG, Zabramski JM et al. Ten--year analysis of saccular aneurysms in the Barrow ruptured aneurysm trial. J Neurosurg 2019; 132 (3): 771–776. doi: 10.3171/2018.8.JNS181846.

28. Bekelis K, Gottlieb D, Su Y et al. Surgical clipping versus endovascular coiling for elderly patients presenting with subarachnoid hemorrhage. J Neurointerv Surg 2016; 8 (9): 913–918. doi: 10.1136/neurintsurg-2015-011 890.

29. Proust F, Bracard S, Lejeune JP et al. A randomized controlled study assessing outcome, cognition, autonomy and quality of life in over 70-year-old patients after aneurysmal subarachnoid hemorrhage. Neurochirurgie 2018; 64 (6): 395–400. doi: 10.1016/j.neuchi.2018.08. 004.

30. Soleman J, Ullmann M, Greuter L et al. Mortality and outcome in elderly patients undergoing emergent or elective cranial surgery. World Neurosurg 2021; 146: e575–e589. doi: 10.1016/j.wneu.2020.10.138.

31. Jung SW, Lee CY, Yim MB. The relationship between subarachnoid hemorrhage volume and development of cerebral vasospasm. J Cerebrovasc Endovasc Neurosurg 2012; 14 (3): 186–191. doi: 10.7461/jcen.2012.14.3. 186.

32. Mao J, Zhu Q, Ma Y et al. Fenestration of lamina terminalis during anterior circulation aneurysm clipping on occurrence of shunt-dependent hydrocephalus after aneurysmal subarachnoid hemorrhage: meta-analysis. World Neurosurg 2019; 129: e1–e5. doi: 10.1016/j.wneu.2019.01.270.

33. Vaverka M, Charamza J, Kikalová K et al. Morfologická studie lamina terminalis a její klinický význam. Cesk Slov Neurol N 2006; 69/102 (3): 217–221.

34. Komotar RJ, Olivi A, Rigamonti D et al. Microsurgical fenestration of the lamina terminalis reduces the incidence of shunt-dependent hydrocefalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 2002; 51 (6): 1403–1412.

35. Schmieder K, Koch R, Lücke S et al. Factors influencing shunt dependency after aneurysmal subarachnoid haemorrhage. Zentralbl Neurochir 1999; 60 (3): 133–140.

36. Preiss M, Netuka D, Koblihova J et al. Quality of life 1 year after aneurysmal subarachnoid hemorrhage in good outcome patients treated by clipping or coiling. J Neurol Surg A Cent Eur Neurosurg 2012; 73 (4): 217–223. doi: 10.1055/s-0032-1304215.