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Aneurysmal subarachnoid hemorrhage in patients under 35-years-old: A single-center experience
Clinical Neurology and Neurosurgery 115 (2013) 665–668
Contents lists available at SciVerse ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Aneurysmal subarachnoid hemorrhage in patients under 35-years-old: A single-center experience Nohra Chalouhi a , Sonia Teufack a , Sid Chandela a , Richard Dalyai a , Stavropoula Tjoumakaris a , David M. Hasan b , Aaron S. Dumont a , L. Fernando Gonzalez a , Robert H. Rosenwasser a , Pascal M. Jabbour a,∗ a b
Department of Neurological Surgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, Philadelphia, PA, United States Department of Neurosurgery, University of Iowa, Iowa City, Iowa, USA
a r t i c l e
i n f o
Article history: Received 10 February 2012 Received in revised form 2 July 2012 Accepted 15 July 2012 Available online 2 August 2012 Key words: Aneurysm Endovascular Intracranial Subarachnoid hemorrhage Young
a b s t r a c t Objective: Aneurysmal subarachnoid hemorrhage (SAH) is relatively uncommon in young adults. There is a paucity of data pertaining to the management of aneurysmal SAH in young patients, especially with endovascular therapy. Methods: We reviewed all SAH patients under the age of 35 years treated at Jefferson Hospital for Neuroscience, Philadelphia, USA, from 2004 to 2009. Results: A total of 40 patients (15 males and 25 females) under the age of 35 were treated for aneurysmal SAH. The average patient age was 30 years (17–35 yo); 25 (62.5%) were smokers. Seventeen patients presented with a Hunt and Hess Grade I or II (42.5%), 20 with a Grade III (50%), and 3 with a Grade IV (7.5%). Thirty-two aneurysms (80%) were located in the anterior circulation and 8 (20%) in the posterior circulation. Thirty-five patients (87.5%) were treated with coil embolization versus 5 with craniotomy and clipping. The endovascular and microsurgical occlusion rates were 90.6% and 100%, respectively. There were no procedural complications with endovascular therapy. Of 35 patients undergoing endovascular treatment, 24 (68.6%) had excellent outcomes at time of discharge with a Glasgow outcome scale of 5. There were no deaths in the series. No patient experienced a rehemorrhage after endovascular treatment. Conclusion: Smoking, female sex, and anterior circulation aneurysms are highly prevalent in young adults with SAH. Endovascular treatment resulted in an overall favorable outcome with no rehemorrhages in patients under the age of 35 years. Our results suggest that endovascular therapy is a reasonable treatment for young patients with SAH. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Aneurysmal subarachnoid hemorrhage (SAH) is relatively uncommon in young adults and typically observed in patients between the ages of 40 and 60 years [1,2]. Despite extensive literature discussing the subject of cerebral aneurysms in the general population, there remains a paucity of data pertaining specifically to the occurrence, clinical features, management, and outcome of SAH in young adults [3,4]. Given its greater durability compared to endovascular coiling, surgical clipping is considered by many as the preferred treatment modality for ruptured aneurysms in young patients. In previous studies, surgical clipping was the main treatment modality used in this patient population [4,3,5]. The role
∗ Corresponding author at: Department of Neurosurgery, Thomas Jefferson University, 901 Walnut, 3rd Floor, Philadelphia, PA 19107, United States. Tel.: +1 215 955 7000; fax: +1 215 503 9170. E-mail address: [email protected] (P.M. Jabbour). 0303-8467/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2012.07.016
of endovascular therapy in this setting has not been well documented. In this study, we performed an analysis on a series of young patients with SAH treated primarily by endovascular techniques at our institution.
2. Materials and methods 2.1. Patient population We conducted a review of a prospectively maintained database of SAH admissions at Jefferson Hospital for Neuroscience. A total of 40 patients with aneurysmal SAH under the age of 35 years were admitted from January 2004 to January 2009. Patients with traumatic and mycotic aneurysms were excluded. Our initial evaluation was geared toward the classification of patients based on Hunt and Hess grade, Fisher scale and presence or
666
N. Chalouhi et al. / Clinical Neurology and Neurosurgery 115 (2013) 665–668 Table 1 Clinical characteristic of patients under 35-year-old presenting with aneurysmal subarachnoid hennorrhage in our study. Clinical Characteristics
Fig. 1. Clinical presentation by Hunt and Hess grade of patients under 35-year-old with aneurysmal subarachnoid hemorrhage.
absence of hydrocephalus. Socio-economic factors such as smoking and family history of cerebral aneurysms were also obtained. All initial surgical interventions were performed within 48 h of admission by five skull base vascular and endovascular-trained neurosurgeons. Treatment modalities included endovascular coil embolization, endovascular stent-assisted coil embolization, and open craniotomy with clip ligation of the aneurysm. The clinical course was also reviewed with particular attention given to the development of persistent hydrocephalus requiring placement of a ventriculo-peritoneal shunt, vasospasm requiring surgical intervention, and rehemorrhage. Patients’ outcomes were measured based on Glasgow Outcome Scale (GOS) at the time of discharge.
Number
Age 17–20 21–24 25–28 29–32 33–35 Sex Female Male Hunt and Hess grade H&H I H&H II H&H III H&H IV H&H V Aneurysm location Anterior Anterior communicating Internal carotid – posterior communicating Middle cerebral Internal carotid – other Posterior Aneurysm size <7 mm 7–15 mm 15–25 mm >25 mm Smoking Yes No
Percent
1 (1M) 2 (2F) 13 (11F, 2M) 17 (9F, 8M) 7 (3F, 4M)
2.5% 5% 32.5% 42.5% 17.5%
25 15
62.5% 37.5%
14 3 20 3 0
35% 7.5% 50% 7.5% 0%
32 12 10 6 4 8
80% 30% 25% 15% 10% 20%
23 15 1 1
57.5% 37.5 2.5% 2.5%
25 15
62.5% 37.5%
F: Female, M: Male.
3. Results From January 2004 to January 2009, 40 patients under the age of 35 were admitted for aneurysmal SAH. Twenty-five were female (62.5%) and 15 were male (37.5%, RR = 1.5). The average age was 29 years for females and 31 years for males. Twenty-five patients (62.5%) were active smokers (14 women and 11 men). The percentage of smokers was 60% (15/25) among women and 66.7% (10/15) among men. 3.1. Clinical presentation
Table 2 Hospital course and clinical outcome of patients under 35-year-old with aneurysmal subarachnoid hennorrhage in our study. Clinical characteristics Hydrocephalus (HCP) No hydrocephalus HCP requiring EVD but no VPS HCP requiring EVD and VPS Treatment modality Endovascular coiling Endovascular stent assisted coiling Craniotomy and clipping Vasospasm requiring intervention Aneurysm re-rupture Outcome by Glasgow outcome scale GOS 1 GOS 2 GOS 3 GOS 4 GOS 5
Number
Percentage
17 16 7
42.5% 40% 17.5%
32 3 5 3 0
80% 7.5% 12.5% 7.5% 0%
0 0 6 7 27
0% 0% 15% 17.5% 67.5%
All patients underwent a full neurological evaluation at their arrival and were classified in accordance to the Hunt and Hess grading system [6]. Fourteen patients (35%) were H&H Grade I, 3 (7.5%) were grade II, 20 (50%) were grade III, 3 (7.5%) were grade IV, and none were grade V (Fig. 1). All patients with H&H grade III and above had a ventriculostomy catheter placed. Patients were also assessed by CT scan for the extent of hemorrhage and the presence of hydrocephalus. A total of 23 patients (57.5%) developed hydrocephalus and underwent ventriculostomy catheter placement. All patients subsequently underwent cerebral angiography to localize and characterize their aneurysms. Thirty-two aneurysms (80%) were located in the anterior circulation, with the most common being anterior (30%) and posterior communicating aneurysms (25%). Only 8 (20%) aneurysms were in the posterior circulation. Twenty-three (57.5%) patients had aneurysms less than 7 mm, 15 (37.5%) patients had aneurysms 7 to 15 mm, and only 2 (5%) had aneurysms larger than 15 mm (Table 1).
placement of a ventriculo-peritoneal shunt due to persistent hydrocephalus (Table 2). Three patients developed clinically significant vasospasm, defined as neurological deterioration and/or increased Lindegaar ratio (mean MCA velocity/mean ICA velocity on transcranial Doppler examination) over 3.0. All 3 patients subsequently had vasospasm confirmed by angiography. Two patients underwent angioplasty and one required injection of intra-arterial nicardipine. No patients had a re-rupture during their admission. The average length of stay was 14.8 days (6–42 days).
3.2. Hospital course
3.3. Clinical outcome
Thirty-two (80%) patients were treated by coil embolization, 3 (7.5%) by stent-assisted coil embolization, and 5 (12.5%) by craniotomy and clip ligation. Seven patients (17.5%) required
Outcome was measured at the time of discharge and graded based on GOS. Of 5 patients treated with surgical clipping, 3 (60%) had a GOS of 5, 1 (20%) had a GOS of 4, and 1 (20%) had a GOS of 3.
N. Chalouhi et al. / Clinical Neurology and Neurosurgery 115 (2013) 665–668
Fig. 2. Clinical outcome by Glasgow outcome scale of patients under 35-year-old with aneurysmal subarachnoid hemorrhage.
Of 35 patients undergoing endovascular treatment, 24 (68.6%) had a GOS of 5, 6 (17.1%) had a GOS of 4, and 5 (14.3%) had a GOS of 3. Overall, 27 (67.5%) patients in this series had excellent outcome with GOS of 5, 7 (17.5%) had a moderate disability with GOS of 4, and 6 (15%) had a severe disability with GOS of 3 (Fig. 2). No patients developed persistent vegetative state or died. 3.4. Efficacy of endovascular treatment Of 32 patients treated with coil embolization, 29 (90.6%) patients had complete obliteration of the aneurysm dome; the remaining 3 patients had greater than 80% aneurysm obliteration. Three aneurysms with wider necks that were not amenable to coil embolization alone were successfully treated with stent-assisted coil embolization (>95% occlusion). There were no procedurerelated complications with endovascular therapy. Angiographic follow-up was available in 25 patients (digital subtraction angiography in 16 and magnetic resonance angiography in 9) at a mean time point of 18.1 months (range 6–60 months). Two of the previously known near-completely obliterated aneurysms remained stable at follow-up. One patient had a 50% recanalization at 8 months and underwent a craniotomy for clipping of the residual aneurysm. Another patient had a 25% recurrence at 8 months and underwent surgical clipping. Lastly, one patient presented 4 years later with a SAH from a de novo aneurysm; the previously coiled aneurysm was still completely occluded. No patient experienced a rehemorrhage from a previously coiled aneurysm in the present series. 4. Discussion Aneurysmal SAH is rare in patients under the age of 35 [1,7]. Young patients account for 5–17% of the SAH population [4,8,9]. Our study showed a female predominance in young patients presenting with SAH. These findings are congruent with previously published data by Kamitani [1] and Ogungbo [4]. However, several other studies have shown a male predominance [3,9]. This inconsistency may be accounted for by the differences in the population examined and reflects the need for further investigation of the multi-factorial etiologies of aneurysmal SAH in the young adult. One such factor thought to influence the incidence of SAH is smoking [10–12]. Our study showed an increased prevalence of smoking in the SAH population under 35 years, compared to the general population. Sixty-two percent of our patients were active smokers versus 20.8% of the United States adult population [13]. The population-based study conducted by Woo et al. [11] also produced similar results with a smoking prevalence of 62.6% among acute subarachnoid patients. The high percentage of smokers among female patients (60%) may partly account for the
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observed female predominance in the present study [12], though a similarly high percentage was noted among male patients (66.7%). Most aneurysms in our study were located in the anterior circulation with a slight predominance of all ICA over ACA aneurysms. Previous authors postulate that younger patients tend to have more proximal aneurysms involving the ICA, as opposed to older patients who have an increased incidence of ACA aneurysms [3,14]. A formerly suggested hypothesis argues that this difference stems from an embryological process whereby the ICA develops before the ACA and the MCA; therefore hemodynamic stress would cause a defect in a congenitally fragile ICA earlier than in the ACA. Our overall outcome for SAH patients under the age of 35 was very favorable; all patients had a GOS greater than 3 at the time of discharge. These findings are consistent with previous series that showed that outcomes in aneurysmal SAH were generally better in young adults in comparison to older patients [1,9]. We speculate that younger patients fare better than their older counterparts, at least in part, because they have less comorbidity and have an overall lower likelihood of developing complications. The uniqueness of our series resides in the fact that most patients were treated by an endovascular approach, as opposed to an open craniotomy and clip ligation approach in previous studies [4,5]. In their series on SAH in the young population, Ogungbo et al. [4] treated 171 patients with surgical clipping and only 25 with endovascular embolization. The authors reported good outcome (GOS 4 or 5) in up to 92% of patients treated with either modalities. Horiushi et al. [3] reported on 25 patients with SAH presenting in the third decade of life and 106 patients in the fourth decade. All patients in their series were treated with open surgery and the authors reported favorable outcomes. In general, surgical clipping is preferred in young patients because of its long-term durability and the absence of medical comorbidities in this population which minimizes the surgical risk. We bring a new perspective in the treatment of young patients with SAH. Patients treated with endovascular therapy in the present study had excellent early clinical outcome with no perioperative mortality. There were no procedural complications with endovascular treatment and complete aneurysm occlusion was achieved in more than 90% of cases. Our results suggest that endovascular therapy is a viable option in young patients with SAH as it seems to provide excellent clinical outcomes with high aneurysm occlusion rates and adequate protection against rehemorrhage. However, we admit that the durability of endovascular treatment could be a concern especially in a young population. In fact, the Cerebral Aneurysm Re-rupture After Treatment (CARAT) study [15] and the International Subarachnoid Aneurysm Trial (ISAT) [16,17] have highlighted the higher risk of rehemorrhage with endovascular compared to surgical treatment. The authors of the ISAT also noted that the advantage of coiling over surgical clipping is lower in patients <50 years of age than it is for those >50 years of age [17]. They concluded that the long term protection from SAH afforded by surgical clipping could give this treatment modality an advantage in life expectancy over coiling for young patients [17]. However, the same group has also suggested that recoiling in the few cases where it was mandated has a low complication rate and did not negate the original benefit of endovascular treatment [18]. Furthermore, the advantages of initial endovascular treatment by not subjecting the injured brain to craniotomy, retraction, and other secondary injuries is likely to result in a benefit that, as suggested above, may override the risks associated with further treatment – including craniotomy for clip ligation – in a small subset of patients. Patients managed with endovascular means should be regularly followed to detect and treat aneurysm recanalization thus minimizing the risk of rehemorrhage. The rate of recanalization (8%, 2/25) was acceptable in the present series. In our institution, as the results of this study show, young patients presenting with SAH are treated
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primarily with endovascular therapy. This management strategy is based on the results of the ISAT study and recently the Barrow Ruptured Aneurysm Trial that invariably showed an outcome benefit in patients treated with endovascular therapy as compared to open surgery [16,19]. There are several limitations to the present study. First, this is a retrospective review of a single-institution experience which could potentially introduce bias. Second, we had a sub-optimal angiographic follow-up in the endovascular group. This constitutes an essential criterion in the determination of long-term efficacy of endovascular treatment. Third, we chose to examine clinical outcome at discharge, which is an early time point. This is unlikely to influence our results, however, as patients tend to improve clinically over time. At this early time point, all patients had a GOS score of greater than 3 at discharge and deteriorations beyond the period of vasospasm are rare. 5. Conclusion In young adults, aneurysmal SAH occurs more often in women and the underlying aneurysm is generally located in the anterior circulation. The prevalence of smoking is significantly higher in the young subarachnoid population compared to the general public. Treatment with a predominant endovascular approach limits periprocedural morbidity and results in an overall favorable outcome with adequate protection against rehemorrhage. Our results suggest that endovascular therapy is a reasonable treatment option in young patients with SAH. References [1] Kamitani H, Masuzawa H, Kanazawa I, Kubo T. Saccular cerebral aneurysms in young adults. Surgical Neurology 2000;54:59–66. [2] van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 2001;124:249–78. [3] Horiuchi T, Tanaka Y, Hongo K, Kobayashi S. Aneurysmal subarachnoid hemorrhage in young adults: a comparison between patients in the third and fourth decades of life. Journal of Neurosurgery 2003;99:276–9. [4] Ogungbo B, Gregson B, Blackburn A, Barnes J, Vivar R, Sengupta R, et al. Aneurysmal subarachnoid hemorrhage in young adults. Journal of Neurosurgery 2003;98:43–9.
[5] Kamitani H, Masuzawa H, Kanazawa I, Kubo T. Saccular cerebral aneurysms in young adults. Surgical Neurology 2000;54:59–66 [discussion 66–57]. [6] Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. Journal of Neurosurgery 1968;28: 14–20. [7] Osawa M, Hongo K, Tanaka Y, Nakamura Y, Kitazawa K, Kobayashi S. Results of direct surgery for aneurysmal subarachnoid haemorrhage: outcome of 2055 patients who underwent direct aneurysm surgery and profile of ruptured intracranial aneurysms. Acta Neurochirurgica 2001;143:655–63 [discussion 663–654]. [8] Bonita R, Beaglehole R, North JD. Subarachnoid hemorrhage in New Zealand: an epidemiological study. Stroke 1983;14:342–7. [9] Park SK, Kim JM, Kim JH, Cheong JH, Bak KH, Kim CH. Aneurysmal subarachnoid hemorrhage in young adults: a gender comparison study. Journal of Clinical Neuroscience 2008;15:389–92. [10] Nguyen TV, Chandrashekar K, Qin Z, Parent AD, Zhang J. Epidemiology of intracranial aneurysms of Mississippi: a 10-year (1997–2007) retrospective study. Journal of Stroke and Cerebrovascular Diseases 2009;18: 374–80. [11] Woo D, Khoury J, Haverbusch MM, Sekar P, Flaherty ML, Kleindorfer DO, et al. Smoking and family history and risk of aneurysmal subarachnoid hemorrhage. Neurology 2009;72:69–72. [12] Longstreth Jr WT, Nelson LM, Koepsell TD, van Belle G. Cigarette smoking, alcohol use, and subarachnoid hemorrhage. Stroke 1992;23:1242–9. [13] Sakaki S, Ohta S, Ohue S, Kohno K, Matsuoka K. Outcome in elderly patients with ruptured intracranial aneurysm. Clinical Neurology and Neurosurgery 1989;91:21–7. [14] Kongable GL, Lanzino G, Germanson TP, Truskowski LL, Alves WM, Torner JC, et al. Gender-related differences in aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery 1996;84:43–8. [15] Rates of delayed rebleeding from intracranial aneurysms are low after surgical and endovascular treatment. Stroke 2006;37:1437–42. [16] Molyneux AJ, Kerr RS, Birks J, Ramzi N, Yarnold J, Sneade M, et al. Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the International Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurology 2009;8: 427–33. [17] Mitchell P, Kerr R, Mendelow AD, Molyneux A. Could late rebleeding overturn the superiority of cranial aneurysm coil embolization over clip ligation seen in the International Subarachnoid Aneurysm Trial? Journal of Neurosurgery 2008;108:437–42. [18] Renowden SA, Koumellis P, Benes V, Mukonoweshuro W, Molyneux AJ, McConachie NS. Retreatment of previously embolized cerebral aneurysms: the risk of further coil embolization does not negate the advantage of the initial embolization. American Journal of Neuroradiology 2008;29: 1401–4. [19] McDougall CG, Spetzler RF, Zabramski JM, Partovi S, Hills NK, Nakaji P, et al. The barrow ruptured aneurysm trial. Journal of Neurosurgery 2012;116: 135–44.
Contents lists available at SciVerse ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Aneurysmal subarachnoid hemorrhage in patients under 35-years-old: A single-center experience Nohra Chalouhi a , Sonia Teufack a , Sid Chandela a , Richard Dalyai a , Stavropoula Tjoumakaris a , David M. Hasan b , Aaron S. Dumont a , L. Fernando Gonzalez a , Robert H. Rosenwasser a , Pascal M. Jabbour a,∗ a b
Department of Neurological Surgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, Philadelphia, PA, United States Department of Neurosurgery, University of Iowa, Iowa City, Iowa, USA
a r t i c l e
i n f o
Article history: Received 10 February 2012 Received in revised form 2 July 2012 Accepted 15 July 2012 Available online 2 August 2012 Key words: Aneurysm Endovascular Intracranial Subarachnoid hemorrhage Young
a b s t r a c t Objective: Aneurysmal subarachnoid hemorrhage (SAH) is relatively uncommon in young adults. There is a paucity of data pertaining to the management of aneurysmal SAH in young patients, especially with endovascular therapy. Methods: We reviewed all SAH patients under the age of 35 years treated at Jefferson Hospital for Neuroscience, Philadelphia, USA, from 2004 to 2009. Results: A total of 40 patients (15 males and 25 females) under the age of 35 were treated for aneurysmal SAH. The average patient age was 30 years (17–35 yo); 25 (62.5%) were smokers. Seventeen patients presented with a Hunt and Hess Grade I or II (42.5%), 20 with a Grade III (50%), and 3 with a Grade IV (7.5%). Thirty-two aneurysms (80%) were located in the anterior circulation and 8 (20%) in the posterior circulation. Thirty-five patients (87.5%) were treated with coil embolization versus 5 with craniotomy and clipping. The endovascular and microsurgical occlusion rates were 90.6% and 100%, respectively. There were no procedural complications with endovascular therapy. Of 35 patients undergoing endovascular treatment, 24 (68.6%) had excellent outcomes at time of discharge with a Glasgow outcome scale of 5. There were no deaths in the series. No patient experienced a rehemorrhage after endovascular treatment. Conclusion: Smoking, female sex, and anterior circulation aneurysms are highly prevalent in young adults with SAH. Endovascular treatment resulted in an overall favorable outcome with no rehemorrhages in patients under the age of 35 years. Our results suggest that endovascular therapy is a reasonable treatment for young patients with SAH. © 2012 Elsevier B.V. All rights reserved.
1. Introduction Aneurysmal subarachnoid hemorrhage (SAH) is relatively uncommon in young adults and typically observed in patients between the ages of 40 and 60 years [1,2]. Despite extensive literature discussing the subject of cerebral aneurysms in the general population, there remains a paucity of data pertaining specifically to the occurrence, clinical features, management, and outcome of SAH in young adults [3,4]. Given its greater durability compared to endovascular coiling, surgical clipping is considered by many as the preferred treatment modality for ruptured aneurysms in young patients. In previous studies, surgical clipping was the main treatment modality used in this patient population [4,3,5]. The role
∗ Corresponding author at: Department of Neurosurgery, Thomas Jefferson University, 901 Walnut, 3rd Floor, Philadelphia, PA 19107, United States. Tel.: +1 215 955 7000; fax: +1 215 503 9170. E-mail address: [email protected] (P.M. Jabbour). 0303-8467/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2012.07.016
of endovascular therapy in this setting has not been well documented. In this study, we performed an analysis on a series of young patients with SAH treated primarily by endovascular techniques at our institution.
2. Materials and methods 2.1. Patient population We conducted a review of a prospectively maintained database of SAH admissions at Jefferson Hospital for Neuroscience. A total of 40 patients with aneurysmal SAH under the age of 35 years were admitted from January 2004 to January 2009. Patients with traumatic and mycotic aneurysms were excluded. Our initial evaluation was geared toward the classification of patients based on Hunt and Hess grade, Fisher scale and presence or
666
N. Chalouhi et al. / Clinical Neurology and Neurosurgery 115 (2013) 665–668 Table 1 Clinical characteristic of patients under 35-year-old presenting with aneurysmal subarachnoid hennorrhage in our study. Clinical Characteristics
Fig. 1. Clinical presentation by Hunt and Hess grade of patients under 35-year-old with aneurysmal subarachnoid hemorrhage.
absence of hydrocephalus. Socio-economic factors such as smoking and family history of cerebral aneurysms were also obtained. All initial surgical interventions were performed within 48 h of admission by five skull base vascular and endovascular-trained neurosurgeons. Treatment modalities included endovascular coil embolization, endovascular stent-assisted coil embolization, and open craniotomy with clip ligation of the aneurysm. The clinical course was also reviewed with particular attention given to the development of persistent hydrocephalus requiring placement of a ventriculo-peritoneal shunt, vasospasm requiring surgical intervention, and rehemorrhage. Patients’ outcomes were measured based on Glasgow Outcome Scale (GOS) at the time of discharge.
Number
Age 17–20 21–24 25–28 29–32 33–35 Sex Female Male Hunt and Hess grade H&H I H&H II H&H III H&H IV H&H V Aneurysm location Anterior Anterior communicating Internal carotid – posterior communicating Middle cerebral Internal carotid – other Posterior Aneurysm size <7 mm 7–15 mm 15–25 mm >25 mm Smoking Yes No
Percent
1 (1M) 2 (2F) 13 (11F, 2M) 17 (9F, 8M) 7 (3F, 4M)
2.5% 5% 32.5% 42.5% 17.5%
25 15
62.5% 37.5%
14 3 20 3 0
35% 7.5% 50% 7.5% 0%
32 12 10 6 4 8
80% 30% 25% 15% 10% 20%
23 15 1 1
57.5% 37.5 2.5% 2.5%
25 15
62.5% 37.5%
F: Female, M: Male.
3. Results From January 2004 to January 2009, 40 patients under the age of 35 were admitted for aneurysmal SAH. Twenty-five were female (62.5%) and 15 were male (37.5%, RR = 1.5). The average age was 29 years for females and 31 years for males. Twenty-five patients (62.5%) were active smokers (14 women and 11 men). The percentage of smokers was 60% (15/25) among women and 66.7% (10/15) among men. 3.1. Clinical presentation
Table 2 Hospital course and clinical outcome of patients under 35-year-old with aneurysmal subarachnoid hennorrhage in our study. Clinical characteristics Hydrocephalus (HCP) No hydrocephalus HCP requiring EVD but no VPS HCP requiring EVD and VPS Treatment modality Endovascular coiling Endovascular stent assisted coiling Craniotomy and clipping Vasospasm requiring intervention Aneurysm re-rupture Outcome by Glasgow outcome scale GOS 1 GOS 2 GOS 3 GOS 4 GOS 5
Number
Percentage
17 16 7
42.5% 40% 17.5%
32 3 5 3 0
80% 7.5% 12.5% 7.5% 0%
0 0 6 7 27
0% 0% 15% 17.5% 67.5%
All patients underwent a full neurological evaluation at their arrival and were classified in accordance to the Hunt and Hess grading system [6]. Fourteen patients (35%) were H&H Grade I, 3 (7.5%) were grade II, 20 (50%) were grade III, 3 (7.5%) were grade IV, and none were grade V (Fig. 1). All patients with H&H grade III and above had a ventriculostomy catheter placed. Patients were also assessed by CT scan for the extent of hemorrhage and the presence of hydrocephalus. A total of 23 patients (57.5%) developed hydrocephalus and underwent ventriculostomy catheter placement. All patients subsequently underwent cerebral angiography to localize and characterize their aneurysms. Thirty-two aneurysms (80%) were located in the anterior circulation, with the most common being anterior (30%) and posterior communicating aneurysms (25%). Only 8 (20%) aneurysms were in the posterior circulation. Twenty-three (57.5%) patients had aneurysms less than 7 mm, 15 (37.5%) patients had aneurysms 7 to 15 mm, and only 2 (5%) had aneurysms larger than 15 mm (Table 1).
placement of a ventriculo-peritoneal shunt due to persistent hydrocephalus (Table 2). Three patients developed clinically significant vasospasm, defined as neurological deterioration and/or increased Lindegaar ratio (mean MCA velocity/mean ICA velocity on transcranial Doppler examination) over 3.0. All 3 patients subsequently had vasospasm confirmed by angiography. Two patients underwent angioplasty and one required injection of intra-arterial nicardipine. No patients had a re-rupture during their admission. The average length of stay was 14.8 days (6–42 days).
3.2. Hospital course
3.3. Clinical outcome
Thirty-two (80%) patients were treated by coil embolization, 3 (7.5%) by stent-assisted coil embolization, and 5 (12.5%) by craniotomy and clip ligation. Seven patients (17.5%) required
Outcome was measured at the time of discharge and graded based on GOS. Of 5 patients treated with surgical clipping, 3 (60%) had a GOS of 5, 1 (20%) had a GOS of 4, and 1 (20%) had a GOS of 3.
N. Chalouhi et al. / Clinical Neurology and Neurosurgery 115 (2013) 665–668
Fig. 2. Clinical outcome by Glasgow outcome scale of patients under 35-year-old with aneurysmal subarachnoid hemorrhage.
Of 35 patients undergoing endovascular treatment, 24 (68.6%) had a GOS of 5, 6 (17.1%) had a GOS of 4, and 5 (14.3%) had a GOS of 3. Overall, 27 (67.5%) patients in this series had excellent outcome with GOS of 5, 7 (17.5%) had a moderate disability with GOS of 4, and 6 (15%) had a severe disability with GOS of 3 (Fig. 2). No patients developed persistent vegetative state or died. 3.4. Efficacy of endovascular treatment Of 32 patients treated with coil embolization, 29 (90.6%) patients had complete obliteration of the aneurysm dome; the remaining 3 patients had greater than 80% aneurysm obliteration. Three aneurysms with wider necks that were not amenable to coil embolization alone were successfully treated with stent-assisted coil embolization (>95% occlusion). There were no procedurerelated complications with endovascular therapy. Angiographic follow-up was available in 25 patients (digital subtraction angiography in 16 and magnetic resonance angiography in 9) at a mean time point of 18.1 months (range 6–60 months). Two of the previously known near-completely obliterated aneurysms remained stable at follow-up. One patient had a 50% recanalization at 8 months and underwent a craniotomy for clipping of the residual aneurysm. Another patient had a 25% recurrence at 8 months and underwent surgical clipping. Lastly, one patient presented 4 years later with a SAH from a de novo aneurysm; the previously coiled aneurysm was still completely occluded. No patient experienced a rehemorrhage from a previously coiled aneurysm in the present series. 4. Discussion Aneurysmal SAH is rare in patients under the age of 35 [1,7]. Young patients account for 5–17% of the SAH population [4,8,9]. Our study showed a female predominance in young patients presenting with SAH. These findings are congruent with previously published data by Kamitani [1] and Ogungbo [4]. However, several other studies have shown a male predominance [3,9]. This inconsistency may be accounted for by the differences in the population examined and reflects the need for further investigation of the multi-factorial etiologies of aneurysmal SAH in the young adult. One such factor thought to influence the incidence of SAH is smoking [10–12]. Our study showed an increased prevalence of smoking in the SAH population under 35 years, compared to the general population. Sixty-two percent of our patients were active smokers versus 20.8% of the United States adult population [13]. The population-based study conducted by Woo et al. [11] also produced similar results with a smoking prevalence of 62.6% among acute subarachnoid patients. The high percentage of smokers among female patients (60%) may partly account for the
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observed female predominance in the present study [12], though a similarly high percentage was noted among male patients (66.7%). Most aneurysms in our study were located in the anterior circulation with a slight predominance of all ICA over ACA aneurysms. Previous authors postulate that younger patients tend to have more proximal aneurysms involving the ICA, as opposed to older patients who have an increased incidence of ACA aneurysms [3,14]. A formerly suggested hypothesis argues that this difference stems from an embryological process whereby the ICA develops before the ACA and the MCA; therefore hemodynamic stress would cause a defect in a congenitally fragile ICA earlier than in the ACA. Our overall outcome for SAH patients under the age of 35 was very favorable; all patients had a GOS greater than 3 at the time of discharge. These findings are consistent with previous series that showed that outcomes in aneurysmal SAH were generally better in young adults in comparison to older patients [1,9]. We speculate that younger patients fare better than their older counterparts, at least in part, because they have less comorbidity and have an overall lower likelihood of developing complications. The uniqueness of our series resides in the fact that most patients were treated by an endovascular approach, as opposed to an open craniotomy and clip ligation approach in previous studies [4,5]. In their series on SAH in the young population, Ogungbo et al. [4] treated 171 patients with surgical clipping and only 25 with endovascular embolization. The authors reported good outcome (GOS 4 or 5) in up to 92% of patients treated with either modalities. Horiushi et al. [3] reported on 25 patients with SAH presenting in the third decade of life and 106 patients in the fourth decade. All patients in their series were treated with open surgery and the authors reported favorable outcomes. In general, surgical clipping is preferred in young patients because of its long-term durability and the absence of medical comorbidities in this population which minimizes the surgical risk. We bring a new perspective in the treatment of young patients with SAH. Patients treated with endovascular therapy in the present study had excellent early clinical outcome with no perioperative mortality. There were no procedural complications with endovascular treatment and complete aneurysm occlusion was achieved in more than 90% of cases. Our results suggest that endovascular therapy is a viable option in young patients with SAH as it seems to provide excellent clinical outcomes with high aneurysm occlusion rates and adequate protection against rehemorrhage. However, we admit that the durability of endovascular treatment could be a concern especially in a young population. In fact, the Cerebral Aneurysm Re-rupture After Treatment (CARAT) study [15] and the International Subarachnoid Aneurysm Trial (ISAT) [16,17] have highlighted the higher risk of rehemorrhage with endovascular compared to surgical treatment. The authors of the ISAT also noted that the advantage of coiling over surgical clipping is lower in patients <50 years of age than it is for those >50 years of age [17]. They concluded that the long term protection from SAH afforded by surgical clipping could give this treatment modality an advantage in life expectancy over coiling for young patients [17]. However, the same group has also suggested that recoiling in the few cases where it was mandated has a low complication rate and did not negate the original benefit of endovascular treatment [18]. Furthermore, the advantages of initial endovascular treatment by not subjecting the injured brain to craniotomy, retraction, and other secondary injuries is likely to result in a benefit that, as suggested above, may override the risks associated with further treatment – including craniotomy for clip ligation – in a small subset of patients. Patients managed with endovascular means should be regularly followed to detect and treat aneurysm recanalization thus minimizing the risk of rehemorrhage. The rate of recanalization (8%, 2/25) was acceptable in the present series. In our institution, as the results of this study show, young patients presenting with SAH are treated
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primarily with endovascular therapy. This management strategy is based on the results of the ISAT study and recently the Barrow Ruptured Aneurysm Trial that invariably showed an outcome benefit in patients treated with endovascular therapy as compared to open surgery [16,19]. There are several limitations to the present study. First, this is a retrospective review of a single-institution experience which could potentially introduce bias. Second, we had a sub-optimal angiographic follow-up in the endovascular group. This constitutes an essential criterion in the determination of long-term efficacy of endovascular treatment. Third, we chose to examine clinical outcome at discharge, which is an early time point. This is unlikely to influence our results, however, as patients tend to improve clinically over time. At this early time point, all patients had a GOS score of greater than 3 at discharge and deteriorations beyond the period of vasospasm are rare. 5. Conclusion In young adults, aneurysmal SAH occurs more often in women and the underlying aneurysm is generally located in the anterior circulation. The prevalence of smoking is significantly higher in the young subarachnoid population compared to the general public. Treatment with a predominant endovascular approach limits periprocedural morbidity and results in an overall favorable outcome with adequate protection against rehemorrhage. Our results suggest that endovascular therapy is a reasonable treatment option in young patients with SAH. References [1] Kamitani H, Masuzawa H, Kanazawa I, Kubo T. Saccular cerebral aneurysms in young adults. Surgical Neurology 2000;54:59–66. [2] van Gijn J, Rinkel GJ. Subarachnoid haemorrhage: diagnosis, causes and management. Brain 2001;124:249–78. [3] Horiuchi T, Tanaka Y, Hongo K, Kobayashi S. Aneurysmal subarachnoid hemorrhage in young adults: a comparison between patients in the third and fourth decades of life. Journal of Neurosurgery 2003;99:276–9. [4] Ogungbo B, Gregson B, Blackburn A, Barnes J, Vivar R, Sengupta R, et al. Aneurysmal subarachnoid hemorrhage in young adults. Journal of Neurosurgery 2003;98:43–9.
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