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Association of Baseline Hyperglycemia with Outcomes Of Diabetes Volume 68, September 2019 1861 Association of Baseline Hyperglycemia With Outcomes of Patients With and Without Diabetes With Acute Ischemic Stroke Treated With Intravenous Thrombolysis: A Propensity Score–Matched Analysis From the SITS-ISTR Registry Georgios Tsivgoulis,1,2 Aristeidis H. Katsanos,1,3 Dimitris Mavridis,4,5 Vaia Lambadiari,6 Christine Roffe,7 Mary Joan Macleod,8 Petr Sevcik,9 Manuel Cappellari,10 Miroslava Nevšímalová,11 Danilo Toni,12 and Niaz Ahmed13,14 Diabetes 2019;68:1861–1869 | https://doi.org/10.2337/db19-0440 Available data from observational studies on the asso- with patients without aHG. Similarly, in the DM group, ciation of admission hyperglycemia (aHG) with outcomes patients with aHG had lower rates of 3-month favor- COMPLICATIONS of patients with acute ischemic stroke (AIS) treated with able functional outcome (mRS scores 0–1, 34.1% vs. intravenous thrombolysis (IVT) are contradictory, espe- 39.3%, P < 0.001) and FI (48.2% vs. 52.5%, P < 0.001), cially when stratified by diabetes mellitus (DM) history. higher 3-month mortality rates (23.7% vs. 19.9%, P < We assessed the association of aHG (‡144 mg/dL) with 0.001), and similar SICH rates (2.2% vs. 2.7%, P = 0.224) outcomes stratified by DM history using propensity compared with patients without aHG. In conclusion, aHG score–matched (PSM) data from the SITS-ISTR. The was associated with unfavorable 3-month clinical out- primary safety outcome was symptomatic intracranial comes in patients with and without DM and AIS treated hemorrhage (SICH); 3-month functional independence with IVT. (FI) (modified Rankin Scale [mRS] scores 0–2) repre- sented the primary efficacy outcome. Patients with and without aHG did not differ in baseline characteristics More than one-third of patients with acute ischemic stroke both in the non-DM (n = 12,318) and DM (n = 6,572) (AIS) present with increased plasma glucose on hospital PSM subgroups. In the non-DM group, patients with admission (1,2). Hyperglycemia (HG) after AIS has been aHG had lower 3-month FI rates (53.3% vs. 57.9%, P < acknowledged as an independent predictor of poor out- 0.001), higher 3-month mortality rates (19.2% vs. 16.0%, come for .20 years (3), and more recently, several ob- P < 0.001), and similar symptomatic intracerebral hem- servational studies suggested that increased plasma orrhage (SICH) rates (1.7% vs. 1.8%, P = 0.563) compared glucose on presentation is also an independent predictor 1Second Department of Neurology, Attikon University Hospital, School of Medicine, 11Department of Neurology, Hospital Ceske Budejovice, Statutory City, Czech Republic National and Kapodistrian University of Athens, Athens, Greece 12Neurovascular Unit, Policlinico Umberto I, Department of Human Neurosciences, 2Department of Neurology, University of Tennessee Health Science Center, University of Rome, “La Sapienza,” Rome, Italy Memphis, TN 13Department of Neurology, Karolinska University Hospital Solna, Stockholm, Sweden 3Department of Neurology, St. Josef-Hospital, Ruhr University, Bochum, Germany 14Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden 4 Department of Primary Education, University of Ioannina, Ioannina, Greece Corresponding author: Georgios Tsivgoulis, [email protected] 5Faculté de Médecine, Université Paris Descartes, Paris, France Received 30 April 2019 and accepted 17 June 2019 6Research Unit and Diabetes Center, Second Department of Internal Medicine, Attikon University Hospital, National and Kapodistrian University of Athens, Athens, This article contains Supplementary Data online at http://diabetes Greece .diabetesjournals.org/lookup/suppl/doi:10.2337/db19-0440/-/DC1. 7University Hospital of North Midlands, Stoke-on-Trent, U.K., and Keele University, © 2019 by the American Diabetes Association. Readers may use this article as Keele, U.K. long as the work is properly cited, the use is educational and not for profit, and the 8Division of Applied Medicine, University of Aberdeen, Foresterhill, U.K. work is not altered. More information is available at http://www.diabetesjournals 9Department of Neurology, Faculty of Medicine in Pilsen, Charles University in .org/content/license. Prague, Pilsen, Czech Republic 10Stroke Unit, Azienda Ospedaliera Universitaria Integrata Verona, Verona, Italy 1862 Hyperglycemia in IVT for AIS Diabetes Volume 68, September 2019 outcome assessment using the mRS score. Patients who have had endovascular treatment, alone or following ad- ministration of tissue plasminogen activator (tPA), were excluded from the present analysis. We also excluded patients enrolled in the SITS-ISTR before January 2010 because the data of these patients have been included in previous studies investigating the association of aHG with outcomes in patients with AIS treated with IVT (10). The primary safety outcome was the difference in SICH rates according to the Safe Implementation of Thrombol- ysis in Stroke-Monitoring Study (SITS-MOST) defini- tion (local or remote parenchymal hemorrhage type 2 on 22- to 36-h post-IVT imaging scans combined with a Na- tional Institutes of Health Stroke Scale [NIHSS] score increase $4 points or leading to death within 24 h) (12), while the primary efficacy outcome was the difference in functional independence (FI) rates at 3 months (defined as mRS scores 0–2) between patients with and without aHG. Secondary outcome events of interest included Figure 1—Flowchart presenting the selection of eligible and PSM 1) mortality rates at 3 months, 2) favorable functional patients. outcome (FFO) rates at 3 months (defined as mRS scores of 0 or 1), 3) SICH rates according to the European Co- operative Acute Stroke Study (ECASS) II definition (any intracranial bleed with $4 points worsening on for symptomatic intracerebral hemorrhage (SICH) and the NIHSS score) (13), 4) rates of any parenchymal unfavorable clinical outcomes in patients with AIS treated hemorrhage (PH), and 5) the distribution of the 3-month with intravenous thrombolysis (IVT) (4–7). Interestingly, mRS scores (functional improvement) between patients this association of HG with poor clinical outcomes has also with and without aHG. All outcomes were evaluated sep- been reported in patients with successful recanalization arately for patients with and without DM, and all analyses following IVT (8). were performed in both the unmatched and the PSM However, when stratified by the history of diabetes populations. mellitus (DM), data from observational studies on the association of HG with IVT outcomes yield contradictory Statistical Analyses fi ndings. In the Canadian Alteplase for Stroke Effective- After dichotomization according to the history of DM and . ness Study (CASES), admission HG (aHG) ( 144 mg/dL) the presence of aHG ($144 mg/dL) before tPA bolus (14), was independently associated with poor outcomes follow- patients in the active group (presence of aHG) were ing IVT administration in patients with and without DM matched to those in the control group (absence of aHG) (9), while in the Safe Implementation of Treatments in using a structured, iterative propensity score model with Stroke International Stroke Thrombolysis Register (SITS- the primary objective to maximize the balance in the ISTR), aHG was associated with a higher risk of SICH and distribution of possible confounders between the two mortality in patients without a history of DM but not in groups. The PSM was performed separately for patients fi patients with DM (10). In view of these discrepant nd- with and without DM. In the PSM algorithm, we included ings, we sought to assess the association of HG with early all baseline characteristics except for the history of DM fi outcomes of patients with AIS treated with IVT, strati ed and aHG. The corresponding propensity score of the aHG – by history of DM, using propensity score matched (PSM) variable was then calculated for each patient, and a nearest data from the SITS-ISTR. neighbor matching algorithm was then used to match patients with aHG to patients in the control group (pa- RESEARCH DESIGN AND METHODS tients without aHG) on a 1:1 ratio (with no replacement) We analyzed prospectively collected data from the SITS- within 0.2 ∗ SD of the logit of the propensity score. The ISTR from participating centers that treat patients with process of PSM has been described in detail in similar AIS with IVT using the IVT register platform, as previously analyses of the SITS-ISTR (15). To determine whether described (11). We included all IVT-treated patients with PSM achieved balance in all potential confounders, we AIS registered in the SITS-ISTR standard data set between compared all baseline characteristics of patients with aHG January 2010 and December 2017 if they had available to their PSM counterparts. data regarding their 1) history of DM, 2) baseline plasma Statistical comparisons were performed between the glucose values, 3) disability before stroke onset (modified aforementioned PSM groups using the x2 test (or the Rankin Scale [mRS] scores .1), and 4) 3-month functional Fisher exact test) and the unpaired t test (or Mann-Whitney diabetes.diabetesjournals.org Tsivgoulis and Associates 1863 U test), where appropriate. The distributions of the mRS In the unmatched cohort, patients without DM with aHG scores at 3 months between the PSM groups were com- were older (P , 0.001) and more likely to be female (P , 0.001) pared using the Cochran-Mantel-Haenszel test. The asso- with greater neurological severity on admission (P , ciations of aHG and DM history with the outcomes
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