SMASH-U A Proposal for Etiologic Classification of Intracerebral Hemorrhage
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SMASH-U A Proposal for Etiologic Classification of Intracerebral Hemorrhage Atte Meretoja, MD, PhD, MSc(Stroke Med); Daniel Strbian, MD, PhD; Jukka Putaala, MD, PhD; Sami Curtze, MD, PhD; Elena Haapaniemi, MD, PhD; Satu Mustanoja, MD, PhD, MSc(Stroke Med); Tiina Sairanen, MD, PhD, MSc(Stroke Med); Jarno Satopää, MD; Heli Silvennoinen, MD, PhD; Mika Niemelä, MD, PhD; Markku Kaste, MD, PhD; Turgut Tatlisumak, MD, PhD Background and Purpose—The purpose of this study was to provide a simple and practical clinical classification for the etiology of intracerebral hemorrhage (ICH). Methods—We performed a retrospective chart review of consecutive patients with ICH treated at the Helsinki University Central Hospital, January 2005 to March 2010 (n⫽1013). We classified ICH etiology by predefined criteria as structural vascular lesions (S), medication (M), amyloid angiopathy (A), systemic disease (S), hypertension (H), or undetermined (U). Clinical and radiological features and mortality by SMASH-U (Structural lesion, Medication, Amyloid angiopathy, Systemic/other disease, Hypertension, Undetermined) etiology were analyzed. Results—Structural lesions, namely cavernomas and arteriovenous malformations, caused 5% of the ICH, anticoagulation 14%, and systemic disease 5% (23 liver cirrhosis, 8 thrombocytopenia, and 17 various rare conditions). Amyloid angiopathy (20%) and hypertensive angiopathy (35%) were common, but etiology remained undetermined in 21%. Interrater agreement in classifying cases was high (, 0.89; 95% CI, 0.82– 0.96). Patients with structural lesions had the smallest hemorrhages (median volume, 2.8 mL) and best prognosis (3-month mortality 4%), whereas anticoagulation- related ICHs were largest (13.4 mL) and most often fatal (54%). Overall, median ICH survival was 51⁄2 years, varying strongly by etiology (P⬍0.001). After adjustment for baseline characteristics, patients with structural lesions had the lowest 3-month mortality rates (OR, 0.06; 95% CI, 0.01– 0.37) and those with anticoagulation (OR, 1.9; 1.0 –3.6) or other systemic cause (OR, 4.0; 1.6 –10.1) the highest. Conclusions—In our patients, performing the SMASH-U classification was feasible and interrater agreement excellent. A plausible etiology was determined in most patients but remained elusive in one in 5. In this series, SMASH-U based etiology was strongly associated with survival. (Stroke. 2012;43:2592-2597.) Key Words: amyloid angiopathy 䡲 anticoagulation 䡲 etiology 䡲 hypertension 䡲 ICH 䡲 stroke E tiologic classifications help in evaluating patients, choos- ing purposeful diagnostic tests, predicting prognosis, and planning secondary preventive measures. Furthermore, uni- Methods This report is based on the Helsinki ICH Study, a retrospective analysis of all consecutive patients with ICH treated at the Helsinki University Central Hospital from January 2005 to March 2010. form classification systems help in comparing patient popu- Helsinki University Central Hospital is the only university teaching lations across different series and in standardizing research. hospital in the province of Uusimaa with a catchment population of Several classifications exist for ischemic stroke according to 1.5 million and the only neurological emergency department with infarct localization1 or etiology.2,3 However, an established 24/7 service in the province. We performed a retrospective chart review, including province- etiologic classification for intracerebral hemorrhage (ICH) wide electronic patient records and imaging databases for all does not exist, but developing one has been recently consecutive patients who at any time during their hospital stay or acknowledged as a research priority.4 In the present work, outpatient visit had a diagnosis of ICH, International Classification we describe a novel classification system for ICH etiology of Diseases, 10th Revision code I61, recorded. All patient records were retrieved. This study has been approved by institutional using our consecutive single-center registry of 1013 pa- authorities. As a routine observational quality registry with no tients with ICH and evaluate the validity and prognostic patient contact, consent for registration was not required by Finnish value of this classification. legislation. Received May 21, 2012; final revision received June 20, 2012; accepted July 2, 2012. From the Departments of Neurology (A.M., D.S., J.P., S.C., E.H., S.M., T.S., M.K., T.T.), Neurosurgery (J.S., M.N.), and Radiology (H.S.), Helsinki University Central Hospital, Helsinki, Finland; and Melbourne Brain Centre at the Royal Melbourne Hospital, Department of Medicine, University of Melbourne, Florey Neuroscience Institutes, and Department of Neurology, The Royal Melbourne Hospital, Melbourne, Australia (A.M.). Louis Caplan, MD, was the guest editor for this article. Correspondence to Atte Meretoja, MD, PhD, MSc(Stroke Med), Department of Neurology, Helsinki University Central Hospital, PO Box 340, FI-00029 HUS, Finland. E-mail atte.meretoja@fimnet.fi © 2012 American Heart Association, Inc. Stroke is available at http://stroke.ahajournals.org DOI: 10.1161/STROKEAHA.112.661603 Downloaded from http://stroke.ahajournals.org/ 2592 by guest on September 24, 2015
Meretoja et al SMASH-U: An Etiologic Classification of ICH 2593 History, imaging or pathology of: • Traumatic ICH, Yes • Sub- / epidural hemorrhage or NON-STROKE • Hemorrhage from co-localized tumor No Imaging or pathology of primary: • Subarachnoid hemorrhage or Yes • Ischemic stroke (IS) with STROKE, NON-ICH hemorrhagic transformation, also after thrombolytic therapy No Imaging or pathology confirmed Yes structural vascular malformation STRUCTURAL LESION diagnosed at ICH site No Systemic or other determined cause for ICHa, except for Yes SYSTEMIC/OTHER DISEASE anticoagulation, hypertension or amyloid angiopathy No Warfarin with INR≥2.0, novel oral Figure 1. Classification scheme for the SMASH-U anticoagulants within 3 days, Yes MEDICATION ICH etiology. ICH indicates intracerebral hemor- full-dose heparin, or non-IS systemic thrombolysis rhage; SMASH-U, Structural lesion, Medication, Amyloid angiopathy, Systemic/other disease, Hypertension, Undetermined. No Lobar, cortical, or corticosubcortical Yes hemorrhage and AMYLOID ANGIOPATHY age ≥55 No Deep or infratentorial hemorrhage Yes HYPERTENSION with pre-ICH hypertensionb No UNDETERMINED a Liver cirrhosis implicated when known liver disease combined with spontaneously elevated INR or liver enzymes >3 x upper limit of the reference range, and thrombocytopenia when thrombocyte count
2594 Stroke October 2012 multiple ICHs during the study period were included several times in tuted the ICH etiology in one fourth of our patients. Amyloid the study only if there were ⬎28 days between the 2 ICHs. No angiopathy (n⫽205 [20%]) and hypertension (n⫽354 [35%]) children aged ⬍18 years were treated at our hospital. were common classifications, whereas 21% of our patients Although many concomitant pathological processes lead to blood extravasation, we tried to provide rules for classifying the most likely did not fulfill any of the definitions (n⫽213, of which 54 cause for each patient assuming certain pathologies as causal and were cortical ⬍55 years old and the rest deep with no known others merely as contributing factors. We preferred the risk factors hypertension). Interrater reliability was high with 92 of 100 that could be definitely demonstrated such as structural malforma- patients rated identically by 2 raters (, 0.89; 95% CI, tions, coagulation disorders, and anticoagulation to those that cannot: 0.82– 0.96; P⬍0.001). Baseline parameters, treatment, and the hypertensive and amyloid angiopathies without pathology. We developed a strict definition for hypertensive etiology (Figure 1). For outcome of the patients by SMASH-U class are presented in amyloid angiopathy, we used the Boston criteria8 except for patients Table 1. who had their stroke due to medication or other systemic disease. The identified structural lesions were either cavernomas The etiologic classification was done by one of 3 stroke neurologists (n⫽31) or arteriovenous malformations (n⫽19). The most (A.M., D.S., J.P.) blinded to patients’ 3-month outcome. A set of 100 common other defined etiologies were hepatopathy (n⫽23; patients was rated independently by 2 raters to test for interrater reliability. 3-month mortality 48%) and thrombocytopenia (n⫽8 [75%]). Rare etiologies consisted of cerebral venous thrombosis Data Retrieval (n⫽2), intravenous amphetamine use (n⫽2), coagulopathy All data were retrospectively retrieved from medical records. Every due to carcinoma (n⫽2), and one patient each of hyperper- patient had been seen by a neurologist with accordingly diligent chart fusion syndrome after carotid endarterectomy, cerebral vas- notes. The Glasgow Coma Scale was systematically registered for culitis without infarction, Staphylococcus aureus sepsis, hem- patients at the emergency department and the National Institutes of Health Stroke Scale for those presenting as thrombolysis candidates orrhagic meningitis, Wernicke encephalopathy, reversible and reconstructed from chart notes for others. In intubated patients, cerebral vasoconstriction syndrome, and presumably heredi- the National Institutes of Health Stroke Scale and Glasgow Coma tary factor VII deficiency. None of these rare cases were fatal Scale were evaluated before intubation. Information on comorbidi- by 3 months. One patient with endocarditis and one with ties and previous medications were retrieved from the provincewide thalassemia-related ICH died as did one of the 2 patients with hospital notes of all specialties and general practice referral notes. All scans were evaluated by neuroradiologists at our hospital, and we eclampsia included in our series. included all subsequent scans after the ICH in our analysis. Lesion Of the patients with anticoagulation-related ICH (n⫽143), volumes were estimated with the ABC/2 method.9 64 had warfarin within the therapeutic international normalized We recorded the modified Rankin Scale at discharge but did not ratio (INR) range of 2.0 to 3.0 and a high 3-month mortality rate have systematic follow-up visits, wherefore functional outcome (52%), 56 had INR ⬎3.0 (56%, P⫽0.58 compared with the could not be evaluated after discharge. For this reason, we used mortality at 3 months as our primary outcome with date of death therapeutic range), and the remaining 23 patients had full-dose retrieved from Statistics Finland in October 2011 for all residents of low-molecular-weight heparin, standard heparin, or our province. thrombolytic therapy for noncerebral thrombosis at the time of their ICH (52%). The 8 patients with subtherapeutic warfarin Statistical Analyses (INR ⬍2.0) at baseline were not classified as anticoagulation- Due to nonnormal distribution of all continuous variables, median related and none died in 3 months. with interquartile range are reported. Groups were compared with the Among the patients classified as ICH due to amyloid independent-samples Kruskal-Wallis test or the Pearson 2 test where appropriate with 2-sided statistical significance set at 0.05. angiopathy (n⫽205), only 10 (5%) had definite cerebral Interrater agreement was evaluated using absolute agreement and amyloid angiopathy (CAA) according to the Boston criteria,8 nonweighted Cohen . Long-term survival is described as a Kaplan- a further 2 (1%) had pathology confirmed probable CAA, 36 Meier graph and difference in survival tested for with the log rank (18%) had clinically probable CAA with multiple hemor- test. To test the independent prognostic value of the SMASH-U rhages, whereas in most (n⫽157 [77%]), the hemorrhage was etiologic classification on 3-month mortality, a logistic regression model was constructed with the previously identified10 covariates of single and without pathology. In the latter group, 58% had intraventricular or infratentorial hemorrhage, sex, and, as continuous hypertension, representing a competing etiology. Hyperten- variables, age, arrival National Institutes of Health Stroke Scale, sion was less common with cortical ICH than with ICH of any Glasgow Coma Scale, and baseline ICH volume. The relative other location (56% versus 68%, P⬍0.001). significance of the model covariates was compared using the Wald Etiology was classified as undetermined in 21% of patients statistic, and the overall performance of the model was analyzed with the receiver operating characteristic area under the curve. Analyses based on the SMASH-U classification. If also patients with were performed on IBM SPSS 20 (IBM Corp, Armonk, NY). several risk factors for ICH would have been classified as undetermined, this would have increased to 58%. Results Twenty-nine patients were lost to 3-month mortality Between January 1, 2005, and March 31, 2010, a total of 1013 follow-up due to nonresidence in Finland (n⫽14) or residence patients with ICH were treated at our hospital. Of these, 33 outside our province. The overall 3-month mortality rate was had a history of ICH before the study period, and 16 had more 32%. Long-term mortality after the acute phase was stable than one separate episodes of ICH during the study period. with median survival at 5.6 years. Survival strongly varied by Overall, 25% of the patients had angiography performed (CT SMASH-U etiology (Figure 2; P⬍0.001). In multivariable angiography, MR angiography, or digital subtraction angiog- analysis, SMASH-U etiology was a strong predictor of raphy) and 6% had their ICH evacuated. 3-month mortality (Table 2; receiver operating characteristic Structural lesions (n⫽50 [5%]), systemic disease (n⫽48 area under the curve, 0.911). Based on the Wald statistic, [5%]), and anticoagulation (n⫽143 [14%]) together consti- SMASH-U etiology was a stronger predictor of mortality Downloaded from http://stroke.ahajournals.org/ by guest on September 24, 2015
Meretoja et al SMASH-U: An Etiologic Classification of ICH 2595 Table 1. Baseline Characteristics and Selected Clinical, Laboratory, and Imaging Parameters, Procedures, and Outcome by SMASH-U Etiology Structural Amyloid Systemic Hypertensive All Patients Lesion Medication Angiopathy Disease Angiopathy Undetermined P (n⫽1013) (n⫽50) (n⫽143) (n⫽205) (n⫽48) (n⫽354) (n⫽213) Value Age, y 68 (58 –78) 55 (38 – 64) 76 (68 – 82) 73 (66 – 80) 60 (51– 68) 66 (57–78) 62 (54 –73) ⬍0.001 Male sex 582 (57%) 22 (44%) 88 (62%) 100 (49%) 32 (67%) 204 (58%) 136 (64%) 0.006 Hypertension 637 (63%) 14 (28%) 111 (78%) 117 (57%) 24 (50%) 354 (100%) 17 (8%) ⬍0.001 Diabetes 143 (14%) 4 (8%) 31 (22%) 26 (13%) 7 (15%) 64 (18%) 10 (5%) ⬍0.001 Coronary heart 128 (13%) 4 (8%) 41 (29%) 35 (17%) 3 (7%) 43 (12%) 2 (1%) ⬍0.001 disease Peripheral artery 19 (2%) 0 6 (4%) 5 (2%) 0 6 (2%) 2 (1%) 0.20 disease Atrial fibrillation 142 (14%) 1 (2%) 98 (70%) 10 (5%) 5 (11%) 26 (7%) 2 (1%) ⬍0.001 Previous stroke 146 (15%) 7 (14%) 29 (20%) 34 (17%) 5 (11%) 55 (16%) 16 (8%) 0.02 Previous ICH 54 (5%) 5 (10%) 5 (4%) 20 (10%) 2 (4%) 19 (5%) 3 (1%) 0.004 Antiplatelet 265 (26%) 8 (16%) 24 (17%) 64 (31%) 9 (19%) 131 (37%) 29 (14%) ⬍0.001 Oral anticoagulation 132 (13%) 2 (4%) 122 (85%) 2 (1%) 1 (2%) 5 (1%) 0 ⬍0.001 Antihypertensive 489 (48%) 12 (24%) 103 (72%) 94 (46%) 23 (48%) 247 (70%) 9 (4%) ⬍0.001 Statin 191 (19%) 12 (24%) 39 (27%) 42 (21%) 4 (9%) 84 (24%) 10 (5%) ⬍0.001 NIHSS 11 (4–20) 3 (1–7) 14 (6–25) 6 (3–14) 11 (3–20) 13 (5–21) 12 (5–19) ⬍0.001 GCS 14 (10–15) 15 (15–15) 14 (7–15) 15 (12–15) 14 (10–15) 14 (10–15) 14 (11–15) 0.002 INR 1.0 (1.0–1.2) 1.0 (0.9–1.0) 3.0 (2.5–3.8) 1.0 (0.9–1.1) 1.3 (1.1–1.5) 1.0 (0.9–1.1) 1.0 (0.9–1.0) ⬍0.001 Thrombocytes, E9/L 209 (171–253) 231 (190–265) 197 (154–235) 208 (172–253) 123 (52–212) 214 (174–257) 215 (182–260) ⬍0.001 ICH volume, mL 9.8 (3.8–28) 2.8 (0.8–5.7) 14 (4.8–46) 14 (4.5–34.4) 9.8 (3.0–32) 9.3 (3.6–22) 9.1 (4.4–24.6) ⬍0.001 Any repeat imaging 631 (62%) 47 (94%) 83 (58%) 131 (64%) 31 (65%) 201 (57%) 138 (65%) ⬍0.001 MRI performed at 153 (15%) 29 (58%) 7 (5%) 42 (20%) 12 (25%) 24 (7%) 38 (18%) ⬍0.001 any time Cortical/subcortical/ 394 (39%) 27 (54%) 62 (43%) 205 (100%) 29 (60%) 17 (5%) 54 (25%) ⬍0.001 lobar* Deep supratentorial* 544 (54%) 11 (22%) 72 (50%) 11 (5%) 15 (31%) 293 (83%) 142 (67%) ⬍0.001 Intraventricular* 416 (41%) 9 (18%) 67 (47%) 39 (19%) 17 (35%) 182 (52%) 102 (48%) ⬍0.001 Infratentorial* 142 (14%) 15 (30%) 18 (13%) 1 (0%) 9 (19%) 70 (20%) 29 (14%) ⬍0.001 In-hospital mortality 244 (24%) 1 (2%) 64 (45%) 27 (13%) 18 (38%) 83 (23%) 41 (19%) ⬍0.001 Lost to 3-mo follow-up 29 (3%) 0 1 (1%) 7 (3%) 0 15 (4%) 6 (3%) 0.16 Mortality at 3 mo 317 (32%) 2 (4%) 77 (54%) 43 (22%) 21 (44%) 111 (33%) 63 (30%) ⬍0.001 All values are median (interquartile range) or n (%). ICH indicates intracerebral hemorrhage; NIHSS, National Institutes of Health Stroke Scale; GCS, Glasgow Coma Scale; INR, international normalized ratio. *SMASH-U classification in patients with multiple locations based on main focus of hemorrhage. than either the patient’s age or ICH volume, next only to We applied the World Health Organization clinical defini- baseline National Institutes of Health Stroke Scale score. The tion of stroke solidly established since the 1970s.5 In ischemic variance in the mortality rates among different etiologies stroke, modern imaging has provided tools to challenge the arose from the secondary ICH types only. Hypertensive, World Health Organization time-based definition with tissue- amyloid, and undetermined ICH 3-month mortality rates based ones,11 but with ICH, even the original World Health differed in univariate (P⫽0.02) but not in multivariable Organization definition has not been quite uniformly inter- (P⫽0.25) analysis from each other. preted. A recent review of epidemiology of ICH concluded that among high-quality population-based studies (n⫽40), Discussion half did not define ICH in detail (n⫽17), whereas many We presented a simple highly reproducible etiologic classifi- excluded ICH due to trauma (n⫽15), tumor (n⫽10), or even cation for ICH in a large consecutive patient cohort. We arteriovenous malformation (n⫽3).12 The World Health Or- classified 55% of ICH as due to hypertensive or amyloid ganization definition term “vascular cause” has been inter- angiopathy; one fourth secondary to underlying lesions, preted to exclude extracerebral intracranial ICH and ICH due diseases, or medication; and finally one fifth as cryptogenic. to malignancy or trauma,12 as we did. This SMASH-U classification was strongly and indepen- With inconsistency in classifying certain ICH as stroke or dently associated with survival. nonstroke, there has been even less consensus on defining Downloaded from http://stroke.ahajournals.org/ by guest on September 24, 2015
2596 Stroke October 2012 1.0 able. Similarly, full anticoagulation may be more important than assumed angiopathy, although both may contribute. Structural lesion Hypertension often exists with lobar hemorrhages,13,18 0.8 although less commonly than with deep ICH both in our series (56% versus 68%) and in others (48% versus 70%).19 The difference between assumed hypertensive and amyloid Cumulative Survival 0.6 etiology is based on deep versus superficial hemorrhage Undetermined location, as per the Boston criteria.8 In the absence of Hypertension Amyloid angiopathy pathology, or even with it, solid differentiation between 0.4 amyloid and hypertensive ICH is difficult. Indeed, 38% of patients with possible CAA by the Boston criteria show no 0.2 Systemic cause pathological findings of CAA.8 Similarly, the distinction Medication between hypertensive and undetermined etiology is vague and depends on the definition of hypertension. We, as have 0.0 others,13 classified deep hemorrhages as hypertensive only 0 1 2 3 4 5 6 7 when previous definite hypertension could be demonstrated. Follow-up, years Many studies have included anticoagulation-related ICH as Figure 2. Long-term survival of patients by SMASH-U etiology, “primary” ICH, not separating this subgroup.8,13,20 Based on Kaplan-Meier analysis. our data, anticoagulation-related ICH, even when within the therapeutic range as was the case in most of our patients and ICH subtypes. It is known that hypertension,13 amyloid those of other series,15,21,22 follows a much grimmer progno- angiopathy,8 anticoagulation,14 –16 and several other second- sis than other “primary” ICH. The Boston criteria may classify anticoagulation-related ICH as CAA when INR is up ary causes17 are risk factors for ICH and often coexist. We to 3.0. In our series, subtherapeutic INR ⬍2.0 was not aimed to develop a simple and practical etiology-oriented associated with increased mortality. Classifying patients with classification system that is easy to learn, quick to perform, subtherapeutic INR as anticoagulation-related ICH, as many and has high interrater agreement. For this purpose we have done,22,23 might be incorrect for prognostic purposes. preferred to avoid classifying patients as undetermined due to Although secondary prevention of ICH is not determined multiple possible etiologies, recognizing this as a practical by etiology as much as it is with ischemic stroke, ICH simplification. In reality, few patients presented with a etiology has a strong prognostic value. Based on previous definite single cause of ICH. Should all risk factors be literature, prognosis of ICH related to arteriovenous malfor- considered equal, 58% of our patients would have been of mation was known to be better24 and that of anticoagulation- undetermined etiology and the classification less useful. Our related ICH worse than with other ICH.14 –16 The ICH score preference of certain risk factors was based on presumption. developed by Hemphill and coworkers has been validated and Assuming an arteriovenous malformation at the ICH site to used to evaluate the outcome of patients with ICH.10,25 In be causal, rather than coexisting hypertension, seems reason- their small cohort of 152 patients, etiology defined as “im- pression of the treating physician” did not predict patient Table 2. Predictors of 3-Mo Mortality in outcome. Prognostic factors included in our model have been Multivariable Analysis previously prospectively validated to produce a good receiver operating characteristic area under the curve of 0.88.25 In our P Predictors OR (95% CI) Value Wald series, adding etiology produced an even more discriminatory model (receiver operating characteristic area under the curve, Age, y per decade 1.63 (1.37–1.95) ⬍0.001 29.7 0.91). Etiology seems to be a major determinant of mortality. Male sex 1.74 (1.17–2.61) 0.007 7.3 Our study has limitations. First, this is a retrospective NIHSS on arrival per point 1.12 (1.08–1.16) ⬍0.001 46.7 analysis of consecutive patients with ICH in routine practice. GCS on arrival per point 0.96 (0.89–1.04) 0.29 1.1 Management and diagnostics varied, and there was no sys- ICH volume per 10 mL 1.28 (1.17–1.41) ⬍0.001 27.7 tematic follow-up for functional outcome. However, early Intraventricular hemorrhage 2.12 (1.42–3.17) ⬍0.001 13.4 death is common in ICH and the outcome of mortality robust. Infratentorial hemorrhage 2.16 (1.19–3.91) 0.01 6.5 Second, our study is hospital-based and single-center. In Finland, a hospital-based approach imposes a smaller selec- SMASH-U ⬍0.001 32.4 tion than in most countries with 97% of our patients with Structural lesion* 0.06 (0.01–0.37) 0.002 9.2 stroke treated as inpatients and 94% sensitivity of Interna- Medical anticoagulation* 1.92 (1.03–3.60) 0.04 4.2 tional Classification of Diseases, 10th Revision I61 to capture Amyloid angiopathy* 0.61 (0.32–1.18) 0.14 2.2 population-based ICH.26,27 However, referral bias is possible Systemic cause* 3.97 (1.57–10.05) 0.004 8.5 with one third of the patients with ICH in our province being Hypertension* 0.82 (0.49–1.37) 0.45 0.6 treated in other hospitals.28 Over the study period, the NIHSS indicates National Institutes of Health Stroke Scale; GCS, Glasgow 3-month mortality rate of all patients with ICH in Finland was Coma Scale; ICH, intracerebral hemorrhage. 35% and median survival 41⁄2 years compared with our 32% *Compared with undetermined etiology. and 51⁄2 years.29 The difference may hint a selection bias or Downloaded from http://stroke.ahajournals.org/ by guest on September 24, 2015
Meretoja et al SMASH-U: An Etiologic Classification of ICH 2597 simply reflect quality of care. Third, this classification was 8. Knudsen KA, Rosand J, Karluk D, Greenberg SM. Clinical diagnosis of developed echoing our preconceived ideas of most likely cerebral amyloid angiopathy: validation of the Boston criteria. Neurology. 2001;56:537–539. etiologies. Lacking pathological verification, some true brain 9. Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuc- pathology and specific etiologies have certainly been misclas- carello M, et al. The ABCs of measuring intracerebral hemorrhage sified. Finally, this etiologic classification has to be validated volumes. Stroke. 1996;27:1304 –1305. 10. Hemphill JC III, Bonovich DC, Besmertis L, Manley GT, Johnston SC. in an external data set preferably in a prospective series. The ICH score: a simple, reliable grading scale for intracerebral hemor- In summary, the SMASH-U classification for ICH etiology rhage. Stroke. 2001;32:891– 897. is practical to perform, has excellent interrater agreement, and 11. Albers GW, Caplan LR, Easton JD, Fayad PB, Mohr JP, Saver JL, et al. was in our series strongly associated with patient outcome. Transient ischemic attack—proposal for a new definition. N Engl J Med. 2002;347:1713–1716. 12. van Asch CJ, Luitse MJ, Rinkel GJ, van der Tweel I, Algra A, Klijn Sources of Funding CJ. Incidence, case fatality, and functional outcome of intracerebral This study was supported by the Helsinki University Central Hos- haemorrhage over time, according to age, sex, and ethnic origin: a pital Research Funds (EVO). Additional support was received from systematic review and meta-analysis. Lancet Neurol. 2010;9:167–176. Yrjö Jahnsson and Biomedicum Helsinki Foundations and the 13. Lovelock CE, Molyneux AJ, Rothwell PM. Change in incidence and National Health and Medical Research Council of Australia Centre aetiology of intracerebral haemorrhage in Oxfordshire, UK, between for Research Excellence Grant 1001216 (Dr Meretoja), Maire 1981 and 2006: a population-based study. Lancet Neurol. 2007;6: Taponen Foundation (Drs Meretoja, Haapaniemi, Satopää, and 487– 493. Tatlisumak), Sigrid Jusélius Foundation (Drs Meretoja and Tatlisu- 14. Hart RG, Boop BS, Anderson DC. Oral anticoagulants and intracranial mak), and the Academy of Finland (Dr Tatlisumak). hemorrhage. Facts and hypotheses. Stroke. 1995;26:1471–1477. 15. Steiner T, Rosand J, Diringer M. Intracerebral hemorrhage associated with oral anticoagulant therapy: current practices and unresolved Disclosures questions. Stroke. 2006;37:256 –262. Dr Meretoja has received compensation for consultancy from Boeh- 16. Huhtakangas J, Tetri S, Juvela S, Saloheimo P, Bode MK, Hillbom M. ringer-Ingelheim (modest). Dr Putaala has received travel expenses Effect of increased warfarin use on warfarin-related cerebral hemorrhage: from Boehringer-Ingelheim and Genzyme and honoraria from Boeh- a longitudinal population-based study. Stroke. 2011;42:2431–2435. ringer-Ingelheim (all modest). Dr Sairanen has received honoraria 17. Al-Shahi Salman R, Labovitz DL, Stapf C. Spontaneous intracerebral from Boehringer Ingelheim for speaking and industry-funded travel haemorrhage. BMJ. 2009;339:b2586. for scientific meetings from Boehringer Ingelheim and Allergan (all 18. Hirohata M, Yoshita M, Ishida C, Ikeda SI, Tamaoka A, Kuzuhara S, et modest). Dr Kaste has received honoraria and travel expenses for al. Clinical features of non-hypertensive lobar intracerebral hemorrhage participating on the Steering Committee meetings of the Terutroban related to cerebral amyloid angiopathy. Eur J Neurol. 2010;17:823– 829. versus aspirin in patients with cerebral ischaemic events, carbamy- 19. Jackson CA, Sudlow CL. 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SMASH-U: A Proposal for Etiologic Classification of Intracerebral Hemorrhage Atte Meretoja, Daniel Strbian, Jukka Putaala, Sami Curtze, Elena Haapaniemi, Satu Mustanoja, Tiina Sairanen, Jarno Satopää, Heli Silvennoinen, Mika Niemelä, Markku Kaste and Turgut Tatlisumak Stroke. 2012;43:2592-2597; originally published online August 2, 2012; doi: 10.1161/STROKEAHA.112.661603 Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 2012 American Heart Association, Inc. All rights reserved. Print ISSN: 0039-2499. Online ISSN: 1524-4628 The online version of this article, along with updated information and services, is located on the World Wide Web at: http://stroke.ahajournals.org/content/43/10/2592 Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. Further information about this process is available in the Permissions and Rights Question and Answer document. Reprints: Information about reprints can be found online at: http://www.lww.com/reprints Subscriptions: Information about subscribing to Stroke is online at: http://stroke.ahajournals.org//subscriptions/ Downloaded from http://stroke.ahajournals.org/ by guest on September 24, 2015
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