Journal of Clinical Neuroscience xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment Charles Kulwin, Bradley N. Bohnstedt, Troy D. Payner, Thomas J. Leipzig, John A. Scott, Andrew J. DeNardo, Aaron A. Cohen-Gadol ⇑ Goodman Campbell Brain and Spine, Indiana University Department of Neurological Surgery, 355 W. 16th Street, Suite 5100, Indianapolis, IN 46202, USA
a r t i c l e
i n f o
Article history: Received 2 December 2013 Accepted 6 December 2013 Available online xxxx Keywords: Acute subdural hematoma Evacuation Intracranial aneurysm Prognosis
a b s t r a c t Acute subdural hematoma is an uncommon presentation of aneurysmal hemorrhage that has been identified as a poor prognostic sign. Current series are small, have short follow-up, or were collected over a long period during which treatment evolved. To evaluate prognostic factors, we analyzed a large modern series of aneurysmal subdural hematoma (aSDH) with long-term follow-up. A prospectively maintained database was queried for patients presenting with aSDH from 2001–2013. Thirty patients met the study criteria. Statistical analysis was performed with unpaired t-test or Fisher’s exact test. Aneurysm treatment involved open clipping (n = 18), endosaccular coiling (n = 8), both (n = 1), or no treatment (n = 3). Good Glasgow Outcome Scale score at discharge was present in 20% and increased to 40% at 6–12 months postoperatively. Good clinical presentation was associated with good final outcome in 75%, whereas poor clinical presentation correlated with good outcome in 30%. Good outcome correlated with younger age (p = 0.04), smaller aneurysm (p = 0.04), and lower Hunt-Hess score (HH) at intervention (p = 0.04). Favorable outcome did not correlate with sex, race, presence of subarachnoid or intraparenchymal hemorrhage, size or laterality of hemorrhage, midline shift, aneurysm treatment modality, or HH at admission (p > 0.15). There was no difference between good and poor outcomes in terms of time to treatment or hematoma evacuation. Poor clinical presentation may be exaggerated by mass effect of hematoma; aggressive treatment is not futile. Presenting neurological status, age, and aneurysm size are predictors of outcome, while laterality and size of hematoma and extent of midline shift are not, suggesting that clinical status is more important than radiographic findings. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Acute subdural hematoma (SDH) is an uncommon presentation of aneurysmal hemorrhage. Published series up to 10 years ago suggested that poor prognosis accompanied the generally poor clinical grade at presentation [1–5]. This outcome was considered inferior to those for patients suffering from traditional aneurysmal subarachnoid hemorrhage (SAH). These series were generally small and retrospective. However, more recent studies suggest that despite poor clinical presentation, a reasonable clinical outcome can be achieved with aggressive management even among poor grade patients [6–10]. Other studies have reported a mixed prognosis [11]. Nonetheless, the available data are confounded by inclusion of small patient cohorts and short follow-up outcome assessments. In addition, these patient series were collected over a long period of time during ⇑ Corresponding author. Tel.: +1 317 362 8760; fax: +1 317 924 8472. E-mail address: [email protected] (A.A. Cohen-Gadol).
which treatment options may have evolved, given the shift in published outcomes. To assess the indications for treatment and outcomes in this patient population, we reviewed our single institution prospectively collected aneurysm database and herein present, to our knowledge, the largest series of aneurysmal acute subdural hemorrhage managed through modern microsurgical and endovascular techniques and report a long-term follow-up.
2. Methods We queried our institution’s prospectively maintained aneurysm database for all patients presenting with aneurysmal hemorrhage and any form of SDH from 2001 to 2013. During this period of time, microsurgical techniques remained consistent. Of 1564 patients, 41 patients were identified for possible inclusion. Inclusion criteria included the presence of at least one cerebral aneurysm and nontraumatic convexity acute SDH. Exclusion criteria included age younger than 18 years (two patients), isolated falcine (one patient) or
http://dx.doi.org/10.1016/j.jocn.2013.12.010 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
2
C. Kulwin et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
tentorial (five patients) SDH, pseudoaneurysm (one patient), or lack of available initial imaging (two patients). The resultant 30 patients composed the study population. Baseline demographic information including clinical status at the time of presentation and intervention, radiographic features of both the SDH (size, laterality, midline shift) and the aneurysm (size, location, laterality), medical and surgical (endovascular, microsurgical and hematoma evacuation) management, and clinical outcome at discharge, 6, and 12 months were analyzed. Long-term (6–12 month) follow-up was prospectively available among 23 of 30 patients; the remaining seven patients’ outcomes were collected retrospectively through chart review, death registry, and/or telephone survey. All patients received an initial head CT scan as well as digital subtraction angiography and/or computed tomography angiography. These patients were treated at a tertiary care hospital with a high volume of aneurysmal SAH, a dedicated neurocritical care unit, and surgical and endovascular staff with significant aneurysm management experience. Admission and preprocedural clinical grade was assessed using the Hunt-Hess (HH) grading system; discharge and long-term clinical outcomes were assessed using the Glasgow Outcome Scale (GOS). Treatment modality was based on a multidisciplinary assessment, taking into consideration clinical status, mass effect of SDH, physical characteristics of the aneurysm, and overall medical condition. Long-term (6–12 month) follow-up was available for 23 of 30 patients. Patients without follow-up were presumed to have maintained the discharge GOS score for data analysis. For analysis of prognostic factors for outcome, a dichotomized outcome was chosen, with good clinical outcome defined as GOS score 4–5 and poor clinical outcome defined as GOS score 1–3. Statistical analysis was performed with unpaired t-test or Fisher’s exact test when appropriate. We did not feel multivariate analysis was valuable due to the small number of patients in each subgroup. The Indiana University Institutional Review Board approved this study. 3. Results Presenting characteristics are described in Table 1. The average age of patients was 61 years (range 39–86). Eighty percent of patients were female, and 80% were Caucasian. The average HH grade at presentation was 3.8 (range 1–5), and at intervention, it was 3.9. The average initial SDH maximum thickness was 6.7 mm (range 3– 20 mm), and the average midline shift was 5.9 mm (range 1– 15 mm), as measured at the level of the foramen of Monro. Of these, 21 (70%) SDH were on the right, 26 (87%) presented additionally with SAH, and 19 (63%) had intraparenchymal hematomas. Aneurysm characteristics and treatment modality are summarized in Table 2. Locations of aneurysms by frequency were as follows: posterior communicating artery, 10 (33%); anterior communicating artery, six (20%); middle cerebral artery, six (20%); anterior choroidal artery, four (13%); and ophthalmic, four
Table 2 Aneurysm characteristics and treatment modality
n
% or (range)
61 24% 24% 3.8 3.9 6.7 5.9 21 26 19
(39–86) 80 80 (1–5) (1–5) (3–20) (1–15) 70 87 63
HH = Hunt-Hess score, IPH = intraparenchymal hematoma, MLS = midline shift, SAH = subarachnoid hemorrhage, SDH = subdural hematoma.
% or (range)
Aneurysm location Pcomm Acomm MCA AchoA Ophth Anterior circulation Interval to treatment, days Aneurysm size, mm
10 6 6 4 4 30 0.78 8.1
33 20 20 13 13 100 (0–3) (3–19)
Aneurysm treatment Clipping Coiling Both None
18 8 1 3
60 27 3 10
Hematoma treatment Craniotomy Craniectomy None
24 4 6
80 13 20
AchoA = anterior choroidal artery, Acomm = anterior communicating artery, MCA = middle cerebral artery, Ophth = ophthalmic, Pcomm = posterior communicating artery.
(13%). All aneurysms were in the anterior circulation. Average aneurysm size was 8.1 mm (range 3–19 mm). Eighteen patients (60%) underwent aneurysm clipping, eight (27%) received endosaccular coiling, one (3%) underwent both, and three (10%) were not treated due to their poor neurologic status. Twenty-four patients (80%) underwent surgical hematoma evacuation, and four (13%) underwent decompressive craniectomy. Six (20%) did not undergo surgical hematoma evacuation. In other words, among the 24 patients who underwent craniotomy for hematoma evacuation, 18 underwent simultaneous clip ligation of their aneurysm, one underwent partial coil embolization followed by clip ligation of the residual aneurysm at the time of hematoma evacuation, and five underwent coil embolization followed by hematoma evacuation. Among the four patients who underwent craniectomies, one patient underwent clip ligation and three patients had endosaccular coiling. The calculated frequency of aneurysmal SDH at our institution is 1.9% of all patients presenting with aneurysmal SAH. Outcomes are depicted in Tables 3 and 4. Nine patients (30%) died prior to discharge, and two subsequently died after discharge in poor neurologic state. Good (GOS score 4–5) discharge condition occurred in six (20%) patients. The rate of good outcome increased to 40% (12 of 30) at 6–12 month follow-up evaluation. Seventy percent of patients presenting in good (HH 1–2) clinical condition achieved a good outcome (three of four patients; one patient declined to HH 5 Table 3 Outcomes following aneurysm management at discharge and 6–12 month follow-up
Table 1 Demographic and clinical characteristics of the study population at presentation
Age, years Sex, female Race, Caucasian HH admission HH intervention SDH width, mm MLS, mm Laterality, right Presence of SAH Presence of IPH
n
Clinical characteristic
Outcome
Mortality In-hospital mortality Post-discharge mortality
9 (30%) 0
Clinical outcome GOS 4–5 GOS 1–3
Discharge 6 (20%) 24 (80%)
6–12 month follow-up 12 (40%) 18 (60%)
Admission HH 1–2 (n = 4) GOS 4–5 GOS 1–3
3 (75%) 1 (25%)*
Admission HH 4–5 (n = 23) GOS 4–5 GOS 1–3
8 (35%) 15 (65%)
Data are presented as n (%). One patient presented HH 1 with subsequent rehemorrhage. GOS = Glasgow Outcome Scale, HH = Hunt-Hess score.
*
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
C. Kulwin et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx Table 4 Outcome by admission clinical grade
HH HH HH HH HH
1 2 3 4 5
*
(n = 2) (n = 2) (n = 3) (n = 15) (n = 8)
GOS 1
GOS 2
GOS 3
GOS 4
GOS 5
1 – 1 3 6
– – – 1 –
– – 1 5 –
– – – 3 2
1 2 1 3 –
* One patient presented HH 1 with subsequent rehemorrhage. GOS = Glasgow Outcome Scale, HH = Hunt-Hess score.
prior to intervention due to rehemorrhage with subsequent poor outcome). Patients presenting in poor (HH 4–5) clinical condition achieved a good outcome in 35% (eight of 23 patients) (Fig. 1). The subgroup with a good outcome at 6–12 month follow-up were younger (p = 0.04), had smaller aneurysm size (p = 0.04), and better clinical grade (lower HH) at the time of intervention (p = 0.04). The HH at the time of admission was not a predictor of outcome (p = 0.05). The dramatic change in one patient who suffered a rehemorrhage caused HH at the time of intervention to be related to outcome. Analysis excluding this patient shows a better correlation between clinical grade at admission and outcome (p = 0.048). There was no significant difference between the two
3
subgroups with respect to sex, race/ethnicity, presence of SAH or intraparenchymal hemorrhage, size or laterality of hemorrhage, midline shift, the need for hematoma evacuation, timing of intervention, or treatment modality (p > 0.15) (Table 5).
4. Discussion Although rare (1.9% of all aneurysmal SAH in our series), aneurysmal SDH is increasingly recognized in the recent literature. Our series of 30 patients confirms the findings of a recently published review of existing smaller series [8]. Our incidence of aneurysmal SDH was similar to their rate of 1.8%. Clinical grade and aneurysm size were prognostic in both studies. Our overall rate of good outcome (40%) is slightly more desirable than theirs of 34%, and our rate of good outcome among poor grade patients (35%) is similarly better than their cited rate of 23%. Both studies identified aneurysmal SDH only in anterior circulation aneurysms. A number of factors, however, were not available in the pooled population, including size and mass effect of the hematoma, rate of craniectomy, and time to treatment, which we were able to describe and evaluate. Patients with an aneurysmal SDH present in poor clinical grade compared with large historical controls suffering from aneurysmal
Fig. 1. Illustrative patient. This patient presented in Hunt-Hess grade 4 with aneurysmal subdural hematoma. She underwent urgent craniotomy and aneurysm clip ligation. She recovered with rehabilitation to a Glasgow Outcome Scale score of 4 by her 6 month follow-up visit. (A) Axial CT scan at the level of the foramen of Monro demonstrating an 8 mm aneurysmal subdural hematoma and 11 mm of midline shift. (B) Preoperative anteroposterior early arterial angiogram demonstrated an 8 mm anterior choroidal aneurysm. (C) Postoperative axial CT scan demonstrates adequate evacuation of hematoma and placement of an external ventricular drain. (D) Postoperative anteroposterior early arterial angiogram demonstrating clip ligation of the previously noted aneurysm. (E) One month postoperative axial CT scan shows resolution of preoperative findings and hemispheric edema.
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
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C. Kulwin et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
Table 5 Clinical outcome subgroup characteristics Outcome at 6–12 month follow-up
GOS 1–3
GOS 4–5
p value
Age, years Sex, % female Race/ethnicity, % white HH at admission* HH at intervention SDH width, mm MLS, mm Laterality, % right Presence of SAH, % Presence of IPH, % Interval to treatment, days Aneurysm size, mm Aneurysm coiled, % Hematoma evacuation, % Craniectomy, %
66 83 83 4.1 4.2 7.6 6.3 62 94 67 0.6 9.6 11 72 17
54 75 75 3.5 3.4 5.5 5.3 83 75 58 1 5.8 8 92 8
0.04 >0.2 >0.2 0.19 0.04 0.15 >0.2 >0.2 >0.2 >0.2 0.18 0.04 >0.2 >0.2 >0.2
Significant p values are in bold. With exclusion of one patient with postadmission rehemorrhage p = 0.048. HH = Hunt-Hess score, IPH = intraparenchymal hematoma, MLS = midline shift, SAH = subarachnoid hemorrhage, SDH = subdural hematoma.
*
SAH – a good presentation clinical grade was seen in 23% of patients in our study, 25% in Schuss et al., [8] and 35% in Biesbroek et al., [11] compared with 73% in Kassell et al. [12]. Previously this poor presentation was thought to portend a poor prognosis. Given the noted shift in the recent reported data toward the possibility of good outcomes in spite of poor presentation in this population, it is likely that poor-grade patients with aneurysmal SDH may differ from those with poor-grade aneurysmal SAH. The outcome of the former is influenced by the presence of SDH mass effect and cerebral herniation. These factors may render traditional SAH grading schemata less applicable [6]. In aneurysmal SAH, poor grade (HH 4–5) at presentation led to a good (modified Rankin Scale score 0–3) outcome in 39 of 148 patients (26%) at 1 year [13]. Biesbroek et al. recently concluded that aneurysmal SDH is an independent risk factor for poor outcome [11]. Subsequently, one would expect even poorer outcomes in poor clinical grade aneurysmal SDH, leading the surgeon to assume a less aggressive approach to management. However, upon detailed inspection of this study, it is important to note that this correlation was no longer significant when adjusted for clinical grade (in either the whole cohort or the modern subgroup). The above findings, as well as our own, suggest that clinical presentation may be exaggerated by the surgically treatable mass effect of the hematoma rather than reflecting the diffuse (surgically untreatable) injury present in poor-grade SAH. This decline due to a mass lesion may be responsive to early evacuation, potentially resulting in better than expected outcomes in aneurysmal SDH. A representative patient demonstrates the mass effect that can be surgically improved, resulting in a good outcome despite a poor clinical presentation (Fig. 1). Similar to traditional aneurysmal SAH, we found that younger patients presenting in better neurological status and with smaller aneurysms showed better outcomes. Our protocol of aggressive early (on average within 24 hours) aneurysm treatment and hematoma evacuation has contributed to the finding of no treatment modality differences between subgroups with good and poor outcomes, as nearly all (24 of 27 treated patients) underwent an emergent craniotomy. Also notable was that radiographic presentation, including hematoma size or midline shift, did not affect outcome. Given our high rate of early hematoma evacuation, one can conclude that hematoma-related decline is reversible surgically; were it not, then larger hematoma size should correlate with worse outcomes. Therefore, prognosis and treatment should be based on clinical presentation rather than radiographic factors.
In our series, more than one-third of poor-grade patients and 40% of all patients demonstrated good clinical outcome at 6– 12 months despite an average HH admission grade of nearly 4. A meta-analysis by Schuss et al. showed a similar 34% overall favorable outcome in spite of only 25% of patients having a good clinical grade at presentation [8]. This suggests that SDH itself may not worsen outcomes and may in fact mask a less severely injured patient than one with a similar HH grade suffering from aneurysmal SAH. 4.1. Limitations There are numerous limitations to this study. First, the biases inherent in any non-randomized, non-blinded study are present. Additionally, although still one of the largest published series to our knowledge, the sample size is relatively small, which limits subgroup analysis and some clinically important findings may not be statistically identified. In spite of this, clinical outcomes were comparable if not better than modern series of aneurysmal SAH, so if an underestimation did occur, it would further strengthen our findings that a good clinical outcome is possible with aggressive treatment in spite of an initial poor-grade presentation. 5. Conclusions Patients with aneurysmal SDH present in poor clinical grade compared to historical controls without hematomas. However, poor-grade presentation resulted in a good clinical outcome in 35% of patients. Clinical grade at the time of intervention, aneurysm size, and age correlated with outcome. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Barnett HJ. Some clinical features of intracranial aneurysms. Clin Neurosurg 1969;16:43–72. [2] Inamasu J, Saito R, Nakamura Y, et al. Acute subdural hematoma caused by ruptured cerebral aneurysms: diagnostic and therapeutic pitfalls. Resuscitation 2002;52:71–6. [3] Kamiya K, Inagawa T, Yamamoto M, et al. Subdural hematoma due to ruptured intracranial aneurysm. Neurol Med Chir (Tokyo) 1991;31:82–6. [4] Ohkuma H, Shimamura N, Fujita S, et al. Acute subdural hematoma caused by aneurysmal rupture: incidence and clinical features. Cerebrovasc Dis 2003;16:171–3. [5] Weir B, Myles T, Kahn M, et al. Management of acute subdural hematomas from aneurysmal rupture. Can J Neurol Sci 1984;11:371–6. [6] Westermaier T, Eriskat J, Kunze E, et al. Clinical features, treatment, and prognosis of patients with acute subdural hematomas presenting in critical condition. Neurosurgery 2007;61:482–7 [discussion 487–8]. [7] Marbacher S, Fandino J, Lukes A. Acute subdural hematoma from ruptured cerebral aneurysm. Acta Neurochir (Wien) 2010;152:501–7. [8] Schuss P, Konczalla J, Platz J, et al. Aneurysm-related subarachnoid hemorrhage and acute subdural hematoma: single-center series and systematic review. J Neurosurg 2013;118:984–90. [9] Otani N, Takasato Y, Masaoka H, et al. Clinical characteristics and surgical outcomes of patients with aneurysmal subarachnoid hemorrhage and acute subdural hematoma undergoing decompressive craniectomy. World Neurosurg 2011;75:73–7. [10] Kocak A, Ates O, Durak A, et al. Acute subdural hematomas caused by ruptured aneurysms: experience from a single Turkish center. Turk Neurosurg 2009;19:333–7. [11] Biesbroek JM, van der Sprenkel JW, Algra A, et al. Prognosis of acute subdural haematoma from intracranial aneurysm rupture. J Neurol Neurosurg Psychiatry 2013;84:254–7. [12] Kassell NF, Torner JC, Haley Jr EC, et al. The international cooperative study on the timing of aneurysm surgery. Part 1: overall management results. J Neurosurg 1990;73:18–36. [13] Mocco J, Ransom ER, Komotar RJ, et al. Preoperative prediction of long-term outcome in poor-grade aneurysmal subarachnoid hemorrhage. Neurosurgery 2006;59:529–38 [discussion 529–8].
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical Study
Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment Charles Kulwin, Bradley N. Bohnstedt, Troy D. Payner, Thomas J. Leipzig, John A. Scott, Andrew J. DeNardo, Aaron A. Cohen-Gadol ⇑ Goodman Campbell Brain and Spine, Indiana University Department of Neurological Surgery, 355 W. 16th Street, Suite 5100, Indianapolis, IN 46202, USA
a r t i c l e
i n f o
Article history: Received 2 December 2013 Accepted 6 December 2013 Available online xxxx Keywords: Acute subdural hematoma Evacuation Intracranial aneurysm Prognosis
a b s t r a c t Acute subdural hematoma is an uncommon presentation of aneurysmal hemorrhage that has been identified as a poor prognostic sign. Current series are small, have short follow-up, or were collected over a long period during which treatment evolved. To evaluate prognostic factors, we analyzed a large modern series of aneurysmal subdural hematoma (aSDH) with long-term follow-up. A prospectively maintained database was queried for patients presenting with aSDH from 2001–2013. Thirty patients met the study criteria. Statistical analysis was performed with unpaired t-test or Fisher’s exact test. Aneurysm treatment involved open clipping (n = 18), endosaccular coiling (n = 8), both (n = 1), or no treatment (n = 3). Good Glasgow Outcome Scale score at discharge was present in 20% and increased to 40% at 6–12 months postoperatively. Good clinical presentation was associated with good final outcome in 75%, whereas poor clinical presentation correlated with good outcome in 30%. Good outcome correlated with younger age (p = 0.04), smaller aneurysm (p = 0.04), and lower Hunt-Hess score (HH) at intervention (p = 0.04). Favorable outcome did not correlate with sex, race, presence of subarachnoid or intraparenchymal hemorrhage, size or laterality of hemorrhage, midline shift, aneurysm treatment modality, or HH at admission (p > 0.15). There was no difference between good and poor outcomes in terms of time to treatment or hematoma evacuation. Poor clinical presentation may be exaggerated by mass effect of hematoma; aggressive treatment is not futile. Presenting neurological status, age, and aneurysm size are predictors of outcome, while laterality and size of hematoma and extent of midline shift are not, suggesting that clinical status is more important than radiographic findings. Ó 2014 Elsevier Ltd. All rights reserved.
1. Introduction Acute subdural hematoma (SDH) is an uncommon presentation of aneurysmal hemorrhage. Published series up to 10 years ago suggested that poor prognosis accompanied the generally poor clinical grade at presentation [1–5]. This outcome was considered inferior to those for patients suffering from traditional aneurysmal subarachnoid hemorrhage (SAH). These series were generally small and retrospective. However, more recent studies suggest that despite poor clinical presentation, a reasonable clinical outcome can be achieved with aggressive management even among poor grade patients [6–10]. Other studies have reported a mixed prognosis [11]. Nonetheless, the available data are confounded by inclusion of small patient cohorts and short follow-up outcome assessments. In addition, these patient series were collected over a long period of time during ⇑ Corresponding author. Tel.: +1 317 362 8760; fax: +1 317 924 8472. E-mail address: [email protected] (A.A. Cohen-Gadol).
which treatment options may have evolved, given the shift in published outcomes. To assess the indications for treatment and outcomes in this patient population, we reviewed our single institution prospectively collected aneurysm database and herein present, to our knowledge, the largest series of aneurysmal acute subdural hemorrhage managed through modern microsurgical and endovascular techniques and report a long-term follow-up.
2. Methods We queried our institution’s prospectively maintained aneurysm database for all patients presenting with aneurysmal hemorrhage and any form of SDH from 2001 to 2013. During this period of time, microsurgical techniques remained consistent. Of 1564 patients, 41 patients were identified for possible inclusion. Inclusion criteria included the presence of at least one cerebral aneurysm and nontraumatic convexity acute SDH. Exclusion criteria included age younger than 18 years (two patients), isolated falcine (one patient) or
http://dx.doi.org/10.1016/j.jocn.2013.12.010 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
2
C. Kulwin et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
tentorial (five patients) SDH, pseudoaneurysm (one patient), or lack of available initial imaging (two patients). The resultant 30 patients composed the study population. Baseline demographic information including clinical status at the time of presentation and intervention, radiographic features of both the SDH (size, laterality, midline shift) and the aneurysm (size, location, laterality), medical and surgical (endovascular, microsurgical and hematoma evacuation) management, and clinical outcome at discharge, 6, and 12 months were analyzed. Long-term (6–12 month) follow-up was prospectively available among 23 of 30 patients; the remaining seven patients’ outcomes were collected retrospectively through chart review, death registry, and/or telephone survey. All patients received an initial head CT scan as well as digital subtraction angiography and/or computed tomography angiography. These patients were treated at a tertiary care hospital with a high volume of aneurysmal SAH, a dedicated neurocritical care unit, and surgical and endovascular staff with significant aneurysm management experience. Admission and preprocedural clinical grade was assessed using the Hunt-Hess (HH) grading system; discharge and long-term clinical outcomes were assessed using the Glasgow Outcome Scale (GOS). Treatment modality was based on a multidisciplinary assessment, taking into consideration clinical status, mass effect of SDH, physical characteristics of the aneurysm, and overall medical condition. Long-term (6–12 month) follow-up was available for 23 of 30 patients. Patients without follow-up were presumed to have maintained the discharge GOS score for data analysis. For analysis of prognostic factors for outcome, a dichotomized outcome was chosen, with good clinical outcome defined as GOS score 4–5 and poor clinical outcome defined as GOS score 1–3. Statistical analysis was performed with unpaired t-test or Fisher’s exact test when appropriate. We did not feel multivariate analysis was valuable due to the small number of patients in each subgroup. The Indiana University Institutional Review Board approved this study. 3. Results Presenting characteristics are described in Table 1. The average age of patients was 61 years (range 39–86). Eighty percent of patients were female, and 80% were Caucasian. The average HH grade at presentation was 3.8 (range 1–5), and at intervention, it was 3.9. The average initial SDH maximum thickness was 6.7 mm (range 3– 20 mm), and the average midline shift was 5.9 mm (range 1– 15 mm), as measured at the level of the foramen of Monro. Of these, 21 (70%) SDH were on the right, 26 (87%) presented additionally with SAH, and 19 (63%) had intraparenchymal hematomas. Aneurysm characteristics and treatment modality are summarized in Table 2. Locations of aneurysms by frequency were as follows: posterior communicating artery, 10 (33%); anterior communicating artery, six (20%); middle cerebral artery, six (20%); anterior choroidal artery, four (13%); and ophthalmic, four
Table 2 Aneurysm characteristics and treatment modality
n
% or (range)
61 24% 24% 3.8 3.9 6.7 5.9 21 26 19
(39–86) 80 80 (1–5) (1–5) (3–20) (1–15) 70 87 63
HH = Hunt-Hess score, IPH = intraparenchymal hematoma, MLS = midline shift, SAH = subarachnoid hemorrhage, SDH = subdural hematoma.
% or (range)
Aneurysm location Pcomm Acomm MCA AchoA Ophth Anterior circulation Interval to treatment, days Aneurysm size, mm
10 6 6 4 4 30 0.78 8.1
33 20 20 13 13 100 (0–3) (3–19)
Aneurysm treatment Clipping Coiling Both None
18 8 1 3
60 27 3 10
Hematoma treatment Craniotomy Craniectomy None
24 4 6
80 13 20
AchoA = anterior choroidal artery, Acomm = anterior communicating artery, MCA = middle cerebral artery, Ophth = ophthalmic, Pcomm = posterior communicating artery.
(13%). All aneurysms were in the anterior circulation. Average aneurysm size was 8.1 mm (range 3–19 mm). Eighteen patients (60%) underwent aneurysm clipping, eight (27%) received endosaccular coiling, one (3%) underwent both, and three (10%) were not treated due to their poor neurologic status. Twenty-four patients (80%) underwent surgical hematoma evacuation, and four (13%) underwent decompressive craniectomy. Six (20%) did not undergo surgical hematoma evacuation. In other words, among the 24 patients who underwent craniotomy for hematoma evacuation, 18 underwent simultaneous clip ligation of their aneurysm, one underwent partial coil embolization followed by clip ligation of the residual aneurysm at the time of hematoma evacuation, and five underwent coil embolization followed by hematoma evacuation. Among the four patients who underwent craniectomies, one patient underwent clip ligation and three patients had endosaccular coiling. The calculated frequency of aneurysmal SDH at our institution is 1.9% of all patients presenting with aneurysmal SAH. Outcomes are depicted in Tables 3 and 4. Nine patients (30%) died prior to discharge, and two subsequently died after discharge in poor neurologic state. Good (GOS score 4–5) discharge condition occurred in six (20%) patients. The rate of good outcome increased to 40% (12 of 30) at 6–12 month follow-up evaluation. Seventy percent of patients presenting in good (HH 1–2) clinical condition achieved a good outcome (three of four patients; one patient declined to HH 5 Table 3 Outcomes following aneurysm management at discharge and 6–12 month follow-up
Table 1 Demographic and clinical characteristics of the study population at presentation
Age, years Sex, female Race, Caucasian HH admission HH intervention SDH width, mm MLS, mm Laterality, right Presence of SAH Presence of IPH
n
Clinical characteristic
Outcome
Mortality In-hospital mortality Post-discharge mortality
9 (30%) 0
Clinical outcome GOS 4–5 GOS 1–3
Discharge 6 (20%) 24 (80%)
6–12 month follow-up 12 (40%) 18 (60%)
Admission HH 1–2 (n = 4) GOS 4–5 GOS 1–3
3 (75%) 1 (25%)*
Admission HH 4–5 (n = 23) GOS 4–5 GOS 1–3
8 (35%) 15 (65%)
Data are presented as n (%). One patient presented HH 1 with subsequent rehemorrhage. GOS = Glasgow Outcome Scale, HH = Hunt-Hess score.
*
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
C. Kulwin et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx Table 4 Outcome by admission clinical grade
HH HH HH HH HH
1 2 3 4 5
*
(n = 2) (n = 2) (n = 3) (n = 15) (n = 8)
GOS 1
GOS 2
GOS 3
GOS 4
GOS 5
1 – 1 3 6
– – – 1 –
– – 1 5 –
– – – 3 2
1 2 1 3 –
* One patient presented HH 1 with subsequent rehemorrhage. GOS = Glasgow Outcome Scale, HH = Hunt-Hess score.
prior to intervention due to rehemorrhage with subsequent poor outcome). Patients presenting in poor (HH 4–5) clinical condition achieved a good outcome in 35% (eight of 23 patients) (Fig. 1). The subgroup with a good outcome at 6–12 month follow-up were younger (p = 0.04), had smaller aneurysm size (p = 0.04), and better clinical grade (lower HH) at the time of intervention (p = 0.04). The HH at the time of admission was not a predictor of outcome (p = 0.05). The dramatic change in one patient who suffered a rehemorrhage caused HH at the time of intervention to be related to outcome. Analysis excluding this patient shows a better correlation between clinical grade at admission and outcome (p = 0.048). There was no significant difference between the two
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subgroups with respect to sex, race/ethnicity, presence of SAH or intraparenchymal hemorrhage, size or laterality of hemorrhage, midline shift, the need for hematoma evacuation, timing of intervention, or treatment modality (p > 0.15) (Table 5).
4. Discussion Although rare (1.9% of all aneurysmal SAH in our series), aneurysmal SDH is increasingly recognized in the recent literature. Our series of 30 patients confirms the findings of a recently published review of existing smaller series [8]. Our incidence of aneurysmal SDH was similar to their rate of 1.8%. Clinical grade and aneurysm size were prognostic in both studies. Our overall rate of good outcome (40%) is slightly more desirable than theirs of 34%, and our rate of good outcome among poor grade patients (35%) is similarly better than their cited rate of 23%. Both studies identified aneurysmal SDH only in anterior circulation aneurysms. A number of factors, however, were not available in the pooled population, including size and mass effect of the hematoma, rate of craniectomy, and time to treatment, which we were able to describe and evaluate. Patients with an aneurysmal SDH present in poor clinical grade compared with large historical controls suffering from aneurysmal
Fig. 1. Illustrative patient. This patient presented in Hunt-Hess grade 4 with aneurysmal subdural hematoma. She underwent urgent craniotomy and aneurysm clip ligation. She recovered with rehabilitation to a Glasgow Outcome Scale score of 4 by her 6 month follow-up visit. (A) Axial CT scan at the level of the foramen of Monro demonstrating an 8 mm aneurysmal subdural hematoma and 11 mm of midline shift. (B) Preoperative anteroposterior early arterial angiogram demonstrated an 8 mm anterior choroidal aneurysm. (C) Postoperative axial CT scan demonstrates adequate evacuation of hematoma and placement of an external ventricular drain. (D) Postoperative anteroposterior early arterial angiogram demonstrating clip ligation of the previously noted aneurysm. (E) One month postoperative axial CT scan shows resolution of preoperative findings and hemispheric edema.
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
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C. Kulwin et al. / Journal of Clinical Neuroscience xxx (2014) xxx–xxx
Table 5 Clinical outcome subgroup characteristics Outcome at 6–12 month follow-up
GOS 1–3
GOS 4–5
p value
Age, years Sex, % female Race/ethnicity, % white HH at admission* HH at intervention SDH width, mm MLS, mm Laterality, % right Presence of SAH, % Presence of IPH, % Interval to treatment, days Aneurysm size, mm Aneurysm coiled, % Hematoma evacuation, % Craniectomy, %
66 83 83 4.1 4.2 7.6 6.3 62 94 67 0.6 9.6 11 72 17
54 75 75 3.5 3.4 5.5 5.3 83 75 58 1 5.8 8 92 8
0.04 >0.2 >0.2 0.19 0.04 0.15 >0.2 >0.2 >0.2 >0.2 0.18 0.04 >0.2 >0.2 >0.2
Significant p values are in bold. With exclusion of one patient with postadmission rehemorrhage p = 0.048. HH = Hunt-Hess score, IPH = intraparenchymal hematoma, MLS = midline shift, SAH = subarachnoid hemorrhage, SDH = subdural hematoma.
*
SAH – a good presentation clinical grade was seen in 23% of patients in our study, 25% in Schuss et al., [8] and 35% in Biesbroek et al., [11] compared with 73% in Kassell et al. [12]. Previously this poor presentation was thought to portend a poor prognosis. Given the noted shift in the recent reported data toward the possibility of good outcomes in spite of poor presentation in this population, it is likely that poor-grade patients with aneurysmal SDH may differ from those with poor-grade aneurysmal SAH. The outcome of the former is influenced by the presence of SDH mass effect and cerebral herniation. These factors may render traditional SAH grading schemata less applicable [6]. In aneurysmal SAH, poor grade (HH 4–5) at presentation led to a good (modified Rankin Scale score 0–3) outcome in 39 of 148 patients (26%) at 1 year [13]. Biesbroek et al. recently concluded that aneurysmal SDH is an independent risk factor for poor outcome [11]. Subsequently, one would expect even poorer outcomes in poor clinical grade aneurysmal SDH, leading the surgeon to assume a less aggressive approach to management. However, upon detailed inspection of this study, it is important to note that this correlation was no longer significant when adjusted for clinical grade (in either the whole cohort or the modern subgroup). The above findings, as well as our own, suggest that clinical presentation may be exaggerated by the surgically treatable mass effect of the hematoma rather than reflecting the diffuse (surgically untreatable) injury present in poor-grade SAH. This decline due to a mass lesion may be responsive to early evacuation, potentially resulting in better than expected outcomes in aneurysmal SDH. A representative patient demonstrates the mass effect that can be surgically improved, resulting in a good outcome despite a poor clinical presentation (Fig. 1). Similar to traditional aneurysmal SAH, we found that younger patients presenting in better neurological status and with smaller aneurysms showed better outcomes. Our protocol of aggressive early (on average within 24 hours) aneurysm treatment and hematoma evacuation has contributed to the finding of no treatment modality differences between subgroups with good and poor outcomes, as nearly all (24 of 27 treated patients) underwent an emergent craniotomy. Also notable was that radiographic presentation, including hematoma size or midline shift, did not affect outcome. Given our high rate of early hematoma evacuation, one can conclude that hematoma-related decline is reversible surgically; were it not, then larger hematoma size should correlate with worse outcomes. Therefore, prognosis and treatment should be based on clinical presentation rather than radiographic factors.
In our series, more than one-third of poor-grade patients and 40% of all patients demonstrated good clinical outcome at 6– 12 months despite an average HH admission grade of nearly 4. A meta-analysis by Schuss et al. showed a similar 34% overall favorable outcome in spite of only 25% of patients having a good clinical grade at presentation [8]. This suggests that SDH itself may not worsen outcomes and may in fact mask a less severely injured patient than one with a similar HH grade suffering from aneurysmal SAH. 4.1. Limitations There are numerous limitations to this study. First, the biases inherent in any non-randomized, non-blinded study are present. Additionally, although still one of the largest published series to our knowledge, the sample size is relatively small, which limits subgroup analysis and some clinically important findings may not be statistically identified. In spite of this, clinical outcomes were comparable if not better than modern series of aneurysmal SAH, so if an underestimation did occur, it would further strengthen our findings that a good clinical outcome is possible with aggressive treatment in spite of an initial poor-grade presentation. 5. Conclusions Patients with aneurysmal SDH present in poor clinical grade compared to historical controls without hematomas. However, poor-grade presentation resulted in a good clinical outcome in 35% of patients. Clinical grade at the time of intervention, aneurysm size, and age correlated with outcome. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication. References [1] Barnett HJ. Some clinical features of intracranial aneurysms. Clin Neurosurg 1969;16:43–72. [2] Inamasu J, Saito R, Nakamura Y, et al. Acute subdural hematoma caused by ruptured cerebral aneurysms: diagnostic and therapeutic pitfalls. Resuscitation 2002;52:71–6. [3] Kamiya K, Inagawa T, Yamamoto M, et al. Subdural hematoma due to ruptured intracranial aneurysm. Neurol Med Chir (Tokyo) 1991;31:82–6. [4] Ohkuma H, Shimamura N, Fujita S, et al. Acute subdural hematoma caused by aneurysmal rupture: incidence and clinical features. Cerebrovasc Dis 2003;16:171–3. [5] Weir B, Myles T, Kahn M, et al. Management of acute subdural hematomas from aneurysmal rupture. Can J Neurol Sci 1984;11:371–6. [6] Westermaier T, Eriskat J, Kunze E, et al. Clinical features, treatment, and prognosis of patients with acute subdural hematomas presenting in critical condition. Neurosurgery 2007;61:482–7 [discussion 487–8]. [7] Marbacher S, Fandino J, Lukes A. Acute subdural hematoma from ruptured cerebral aneurysm. Acta Neurochir (Wien) 2010;152:501–7. [8] Schuss P, Konczalla J, Platz J, et al. Aneurysm-related subarachnoid hemorrhage and acute subdural hematoma: single-center series and systematic review. J Neurosurg 2013;118:984–90. [9] Otani N, Takasato Y, Masaoka H, et al. Clinical characteristics and surgical outcomes of patients with aneurysmal subarachnoid hemorrhage and acute subdural hematoma undergoing decompressive craniectomy. World Neurosurg 2011;75:73–7. [10] Kocak A, Ates O, Durak A, et al. Acute subdural hematomas caused by ruptured aneurysms: experience from a single Turkish center. Turk Neurosurg 2009;19:333–7. [11] Biesbroek JM, van der Sprenkel JW, Algra A, et al. Prognosis of acute subdural haematoma from intracranial aneurysm rupture. J Neurol Neurosurg Psychiatry 2013;84:254–7. [12] Kassell NF, Torner JC, Haley Jr EC, et al. The international cooperative study on the timing of aneurysm surgery. Part 1: overall management results. J Neurosurg 1990;73:18–36. [13] Mocco J, Ransom ER, Komotar RJ, et al. Preoperative prediction of long-term outcome in poor-grade aneurysmal subarachnoid hemorrhage. Neurosurgery 2006;59:529–38 [discussion 529–8].
Please cite this article in press as: Kulwin C et al. Aneurysmal acute subdural hemorrhage: Prognostic factors associated with treatment. J Clin Neurosci (2014), http://dx.doi.org/10.1016/j.jocn.2013.12.010
