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50TH ANNIVERSARY ARTICLE Neurological Critical Care: The Evolution of Cerebrovascular Critical Care Cherylee W. J. Chang, MD, FCCM, KEY WORDS: acute ischemic stroke; cerebrovascular disease; critical FACP, FNCS1 care medicine; history; intracerebral hemorrhage; neurocritical care; Jose Javier Provencio, MD, FCCM, subarachnoid hemorrhage FNCS2 Shreyansh Shah, MD1 n 1970, when 29 physicians first met in Los Angeles, California, to found the Society of Critical Care Medicine (SCCM), there was little to offer for the acute management of a patient suffering from an acute cerebrovascular Icondition except supportive care. Stroke patients were not often found in the ICU. Poliomyelitis, and its associated neuromuscular respiratory failure, cre- ated a natural intersection of neurology with critical care; such was not the case for stroke patients. Early textbooks describe that the primary decision in the emergency department was to ascertain whether a patient could swallow. If so, the patient was discharged with the advice that nothing could be done for the stroke. If unable to swallow, a nasogastric tube was inserted and then the patient was discharged with the same advice. In the 50 intervening years, many advances in stroke care have been made. Now, acute cerebrovascular patients are not infrequent admissions to an ICU for neurologic monitoring, observa- tion, and aggressive therapy (Fig. 1). HISTORY Over 50 years ago, stroke, previously called “apoplexy” which means “struck down with violence” or “to strike suddenly,” was a clinical diagnosis that was confirmed by autopsy as a disease of the CNS of vascular origin (1). In the 1960s, approximately 25% of stroke patients died within 24 hours and nearly half died within 2 to 3 weeks. Of those that survived the acute stroke, nearly half were dead within 4 to 5 years (2). In 1970, the World Health Organization (WHO) convened a group in Monaco for 4 days to address the topic of stroke, which was the third lead- ing cause of death (behind infectious/parasitic disease and ischemic heart disease) in 40 of 57 countries represented by the WHO, including the United States, and the top 10 causes of death in 54 countries (3, 4). Nearly 50 years later, globally, stroke is the second leading cause of death behind ischemic heart disease with 6.2 million deaths in 2017 attributed to cerebrovascular disease and a prevalence of 79% ischemic, 17% hemorrhagic, and 9% suba- rachnoid hemorrhage (SAH) (5, 6). In the United States, stroke has fallen to the fifth leading cause of death but remains the leading cause of serious long- term disability (5). Copyright © 2021 by the Society of Mortality is higher following hemorrhagic stroke than ischemic stroke, and Critical Care Medicine and Wolters this gap is widening. Advances in acute treatment for acute ischemic stroke (AIS), Kluwer Health, Inc. All Rights such as revascularization and management, has led to decrease in the AIS mor- Reserved. tality rate from 29 per 100 person-years to 11 per 100 person-years, but mortality DOI: 10.1097/CCM.0000000000004933 Critical Care Medicine www.ccmjournal.org 881 Copyright © 2021 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved. Chang et al Figure 1. Notable events in the evolution of cerebrovascular critical care. ABA = American Board of Anesthesiology, ABIM = American Board of Internal Medicine, ABS = American Board of Surgery, AIS = acute ischemic stroke, ATACH = Antihypertensive Treatment of Acute Cerebral Hemorrhage, BP = blood pressure, CSC = Comprehensive Stroke Center, DAWN = Diffusion Weighted Imaging or Computerized Tomography Perfusion Assessment with Clinical Mismatch in the Triage of Wake Up and Late Presenting Strokes Undergoing Neurointervention, DEFUSE 3= Diffusion and Perfusion Imaging Evaluation for Understanding Stroke Evolution 3, FDA = U.S. Food and Drug Administration, ICH = intracerebral hemorrhage, INTERACT2 = Second Intensive Blood Pressure Reduction in Acute Cerebral Hemorrhage Trial, MISTIE = Minimally Invasive Surgery plus Alteplase in Intracerebral Hemorrhage Evacuation, PSC = primary stroke center, SAH = subarachnoid hemorrhage, SCCM = Society of Critical Care Medicine, STICH = Surgical Trial in Intracerebral Hemorrhage, t-PA = tissue plasminogen activator, UCNS=United Council for Neurologic Subspecialties. is essentially unchanged following intracerebral hemor- The development of thrombolytic therapy for AIS has rhage (ICH) (from 25 to 30 per 100 person-years) (7). begun to change the attitudes of practitioners toward In the intervening years, advances in imaging and more aggressive care. treatment have changed it from a condition where the stroke victim was triaged as the last to be seen in the RISK FACTORS AND PREVENTION emergency department, to a “stroke code” where ur- Ischemic Stroke gency is sought not only in the emergency department, but in the prehospital arena with a high priority for Fifty years ago, given the lack of treatment and high critical care admission and management. rate of mortality, initially, prevention was the natural It is important to mention an important obstacle to priority, although there was limited understanding of the improvement of care that has bedeviled neurologi- preventable risk factors. Advances in cardiovascular cally injured patients for more than 50 years is nihilism. epidemiological research had a key transformative Since neurologic damage associated with cerebrovas- impact. In 1970, based on the landmark Framingham cular disease: 1) was thought to be complete prior to study, hypertension was identified as “the most com- admission to the hospital and 2) this damage affects mon and potent precursor of atherothrombotic brain aspects of the human condition that healthcare work- infarction” and recognized that early detection and ers value, there has been a trend of clinician pessimism blood pressure control was a key factor in stroke pre- that permeates decisions. This has led to less aggressive vention (8, 9). Data from existing studies of the asso- treatment and early withdrawal of life-saving measures ciation of stroke and serum cholesterol or smoking that impact the ability to understand the true outcome were conflicting (10). At the time, smoking remained cerebrovascular diseases and the benefit of treatments. popular with approximately 43% of men and 31% of 882 www.ccmjournal.org June 2021 • Volume 49 • Number 6 Copyright © 2021 by the Society of Critical Care Medicine and Wolters Kluwer Health, Inc. All Rights Reserved. 50th Anniversary Article women, an estimated 48.8 million cigarette smokers in $30,000 to $60,000 (United States) per event, depending the United States. (11). As a point of reference, in 2018, on the patient’s weight (18). New guidelines have been the year with the most up-to-date statistics, the preva- developed to address the reversal of antiplatelet and lence of smoking has dropped to 13.7% (12). antithrombotic agents (19). The reversal of these newer Other advances included the 1978 Framingham Heart agents is an important area of research and under- study that demonstrated that diabetes increased stroke standing for the critical care provider when addressing risk and that nonvalvular atrial fibrillation was clearly as- intracerebral and other life-threatening hemorrhages. sociated with a 5.6-fold increase in the risk of stroke (13). The advanced electrophysiology ablation of atrial fibril- Subarachnoid Hemorrhage lation, interventional cardiac procedures, and develop- ment of the direct-acting oral anticoagulants (DOACs) Compared with AIS and ICH, aneurysmal SAH occurs provides additional pharmacological strategies other at a relatively young age with poorer outcome. Studies than warfarin to prevent cardioembolic stroke (14). over the last 50 years have confirmed immutable risk factors include hereditary preponderance, female sex, Intracerebral Hemorrhage and older age, but also drawn attention to modifiable In 1971, there was already a trend toward a decrease in the risk factors such as hypertension, smoking, and exces- overall prevalence of ischemic and hemorrhagic stroke sive alcohol intake have the potential to decrease an (15). The use of thiazide diuretics beginning in late 1950s individual’s risk for hemorrhage (20, 21). and a multicenter Veterans Administration Cooperative study (phase 1 and 2) between 1964 and 1971 showed for ADVANCES IN NEURODIAGNOSTIC the first time that treating diastolic hypertension (rang- IMAGING ing between 90 and 129 mm Hg) reduced cardiovascular When addressing the issue of treatment, a key bar- events such as stroke and heart failure and improved rier to effective treatment has been accurate diagnosis. mortality (16, 17). Hypertension treatment to prevent Prior to advanced imaging, it was unclear what pro- ICH remains the mainstay of therapy. portion of strokes were ischemic and hemorrhagic. In Risk factors for spontaneous ICH in 2021 expand the United States in 2020, 87% of strokes are ischemic, beyond hypertension and vascular abnormalities such 10% are hemorrhagic, and 3% SAH (5). However, in as vascular malformations and dural arteriovenous 1970, of 207,166 deaths reported, cerebral thrombosis fistulas known in 1971. In 2021, other risk factors in- reportedly accounted for 57,845 (28%) deaths, cerebral clude the more frequent use of illicit sympathomimet- embolism 884 (< 1%), cerebral hemorrhage 41,379 ics such as cocaine and methamphetamine, and, in our (20%), and “all other cerebrovascular disease” 107,068 aging population, cerebral

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