IMAGING OF intracranial hemorrhage

IMAGING OF INTRACRANIAL HEMORRHAGE Camilo R Gomez ABSTRACT Intracranial hemorrhages represent serious neurologic emergencies, whose diagnosis and treatment must be carried out rapidly and decisively Their diagnosis, categorization, and appropriate treatment allocation can be easily guided by current imaging techniques Although computed tomography (CT) has traditionally been considered the imaging modality of choice in the management of these patients, recent technologic advances have placed magnetic resonance imaging in an advantageous position to become a very important diagnostic tool, in some cases likely to replace CT KEY POINT: Ⅲ Intracranial hemorrhage has potential devastating consequences, and its management is closely linked to the effectiveness of the diagnostic algorithm utilized by the clinical team Continuum Lifelong Learning Neurol 2008;14(4):37–56 INTRODUCTION Intracranial hemorrhage constitutes a heterogeneous group of disorders that share, as a common pathogenic denominator, the sudden extravasation of blood into the brain parenchyma, one of the surrounding meningeal spaces, or both As such, intracranial hemorrhages may occur spontaneously or as a result of direct trauma to the cranium Regardless of its root cause, intracranial bleeding has potentially devastating consequences, and its management is closely linked to the effectiveness of the diagnostic algorithm utilized by the clinical team At present, such diagnostic algorithm revolves around the appropriate application and interpretation of imaging techniques to characterize the hemor- rhagic process, monitor it over time, and assess the impact of therapeutic measures This chapter includes: (1) an overview of the practical considerations that become a prerequisite for the appropriate utilization of imaging techniques, (2) a discussion of the different imaging techniques available to study patients with intracranial hemorrhage, and (3) a description of their application in the context of the different types of intracranial hemorrhagic processes PURPOSE OF IMAGING: TASKORIENTED CHOICES The most practical approach to a discussion of the application of imaging techniques to study intracranial hemorrhages is to first address the tasks, diagnostic or therapeutic, that require Relationship disclosure: Dr Gomez has received personal compensation for activities with Alsius Corporation, Boston Scientific Corporation, Bristol-Myers Squibb Company, Cordis Corporation, Guidant Corporation, Sanofi-Aventis Pharmaceuticals, Inc., WL Gore, and Accumetrics as a consultant and scientific advisory board member Dr Gomez has received research support from Abbott Laboratories, Inc., Alsius Corporation, AstraZeneca Pharmaceuticals, Bayer Pharmaceuticals, Boston Scientific Corporation, BristolMyers Squibb Company, Guidant Corporation, Parke-Davis, and Sanofi-Aventis Pharmaceuticals, Inc Unlabeled Use of Products/Investigational Use Disclosure: Dr Gomez has nothing to disclose Copyright © 2008, American Academy of Neurology All rights reserved 37 ‹ INTRACRANIAL HEMORRHAGE KEY POINTS: Ⅲ Ⅲ 38 Since the overwhelming majority of intracranial hemorrhages occur as sudden events that require urgent care, imaging techniques provide the best way for rapid and accurate identification of the hemorrhagic process Since the cerebral vasculature is implicated in the pathogenic process of intracerebral hemorrhages, the assessment of the cerebral arteries and veins becomes an additional benefit of imaging utilization the utilization of imaging This is the optimal approach to properly guide how neurologists choose the most appropriate technique for each clinical situation From this perspective, the scenarios in which imaging techniques are likely to be needed must be assessed along the following lines: (1) What information is being sought, and how quickly is it needed?; (2) Which of the available imaging techniques is most likely to answer the question being asked?; and (3) How will the information obtained by imaging impact further diagnostic algorithms, prognosis, and treatment of the patient? Based on these considerations, tasks that require the utilization of imaging during clinical care of cerebrovascular patients include those listed below Initial Diagnosis Since the overwhelming majority of intracranial hemorrhages occur as sudden events that require urgent care, imaging techniques provide the best way for rapid and accurate identification of the hemorrhagic process In particular, the last decades have brought technologic advances that translate into faster imaging acquisition and processing, and have allowed imaging techniques to provide the necessary diagnostic information in a matter of minutes Categorization and Therapeutic Allocation Once the diagnosis of an intracranial hemorrhage is made, a more precise definition of the condition has enormous therapeutic implications, both immediate and long-term The same technologic advances described above have extended to improvements in image resolution, with better signal-noise ratios and a superior definition of the pathologic processes Furthermore, since the cerebral vasculature is so often implicated in the pathogenic process, imaging of the cerebral arteries and Continuum: Lifelong Learning Neurol 2008;14(4) veins becomes an additional dimension in the categorization of these patients Assessment of Prognosis Following identification and categorization of the intracranial hemorrhage, it is possible to use the imaging information to “best fit” the potential outlook and final outcome of each patient It is often possible to make predictions about the potential benefit of a specific treatment strategy Clearly, this characteristic of imaging relates to the fact that the existing techniques represent the equivalent of “bedside neuropathology,” and that they have direct correspondence with the natural history of every type of intracranial hemorrhage Monitoring of Evolution Regardless of how the patient is being treated, the time continuum that follows initial evaluation and treatment demands that the clinical team follows the evolution of the patient in order to make on-the-fly decisions about which aspects of treatment to continue and which ones to change In certain situations, such as in the intensive care unit, when clinical assessment may not be easy or feasible because of the need for deep sedation, imaging becomes of paramount importance to assess changes and guide therapy (Joo et al, 2006) IMAGING TECHNIQUES: RELEVANCE TO THE INFORMATION NEEDED CT Techniques Every discussion about imaging techniques for intracranial hemorrhages must begin with CT The introduction of CT in the 1970s changed the way many neurologic diseases are diagnosed and treated Suddenly, it was possible to directly look at the brain tissue and document any tissue damage incurred Furthermore, CT allowed a rapid differentiation among the various forms of intracranial hemorrhage KEY POINT: Ⅲ Case 2-1 A 55-year-old man presented to the emergency department following the sudden onset of headache, nausea, and vomiting These symptoms were promptly followed by lethargy and weakness of the left side of the body He had preexisting hypertension and had not been followed by a physician for several years On admission, his blood pressure was 220/110 mm Hg, and he was found lethargic, with a left gaze paresis, a left hemiparesis, and a left perceptual deficit His urgent CT is shown in Figure 2-1 He was admitted to the intensive care unit, his blood pressure was rapidly controlled with IV nicardipine, and after weeks, he was discharged to inpatient rehabilitation Comment This patient demonstrates a typical presentation of a ‘‘hypertensive’’ acute parenchymal hemorrhage (Figure 2-1A), evolving into a subacute hemorrhage (Figure 2-1B) The Evolution of the appearance of FIGURE 2-1 rate of resolution intracranial hemorrhage on CT A, depends on the During the acute phase, the hemorrhage shown is significantly hyperdense with respect size of the to the surrounding tissue (large arrow) B, Several weeks hematoma, usually later, the density of the hemorrhage has largely dissipated within to (small arrow) with the exception of the core weeks, and it absorbs from the outside toward the center The ability to visualize an acute hemorrhagic process using CT depends on the increased density of fresh blood because of its hemoglobin content (Case 2-1) This results in the hemorrhage averaging 60 HU to 100 HU (Hounsfield units), and renders it as a “whiter” tissue (ie, hyperdense) than the normal brain (about 40 HU to 45 HU) (Figures 2-1A and 2-2) As time elapses, the globin molecule of the blood breaks down, and the blood progressively loses its high-density appearance (Figure 2-1B) This change occurs centripetally, and its speed de- The ability to visualize an acute hemorrhagic process using CT depends on the increased density of fresh blood because of its hemoglobin content, averaging 60 HU to 100 HU 39 Relationship among the various tissues and their corresponding Hounsfield units (HUs) in CT Density increases as the HUs increase Note that the HU (and the density of intracranial hemorrhage [ICH]) is greater than that of white matter (WM) and gray matter (GM) FIGURE 2-2 Continuum: Lifelong Learning Neurol 2008;14(4) ‹ INTRACRANIAL HEMORRHAGE 40 pends largely on the size of the original hemorrhage Subacute hemorrhages are typically isodense with the brain, while chronic ones present as remnant hypodensities that replace the injured tissue The routine utilization of IV contrast as part of the CT examination of the patient with an acute intracranial hemorrhage is unwarranted The demonstration of possible enhancement of any of the tissue in these patients generally serves no clinical purpose and typically does not help guide treatment In the context of certain clinical scenarios, such a practice may be dangerous For example, the intense nausea that can be produced by IV contrast administration can jeopardize the fate of patients with increased intracranial pressure secondary to the intracranial hemorrhage It is possible to argue about the potential benefit of discovering hidden metastases that can only be visualized as they enhance with contrast administration However, as discussed below, better methods exist for finding this type of information, which in fact is rarely needed with urgency Finally, a special mention must be made of the use of contrast to obtain additional information about the brain blood vessels (Carstairs et al, 2006; Joo et al, 2006; Nijjar et al, 2007; Westerlaan et al, 2007) CT angiography is a relatively noninvasive technique that couples helical CT scanning with contrast enhancement to obtain vascular images (Carstairs et al, 2006; Joo et al, 2006; Nijjar et al, 2007; Westerlaan et al, 2007) It is performed by first obtaining a series of helical axial images following the injection of about 100 mL of iodinated contrast over about 20 minutes These are then reconstructed using 1.25-mm-thick slices and 0.5-mm to 1.0-mm increments This protocol allows three-dimensional rendering of the angiographic images The development of this technique required the Continuum: Lifelong Learning Neurol 2008;14(4) introduction of a scanner that allowed patients to be translated through a continuously rotating gantry with very rapid data acquisition The operator controls several variables that determine the protocol to be used for each region of interest to be imaged, including duration of the scan, speed of movement of the table, and collimation As with any other technique, CT angiography has advantages and disadvantages On one hand, it is not susceptible to flow perturbations and complex flow patterns like magnetic angiography On the other hand, it utilizes ionizing radiation and contrast administration, which limit its use in patients with azotemia and contrast allergy, while resulting in a more limited field of view per study The latter is very important because it requires that the planning and postprocessing of the study take into consideration the question being asked Furthermore, postprocessing and three-dimensional rendering typically involve “sculpting out” some of the tissue that surrounds the vessels, based on its density When not carefully carried out, this process can conceivably lead to the exclusion of important structures or pathologic findings (Figure 2-3) Another practical aspect of CT in the management of patients with intracranial hemorrhage is the ease with which it allows follow-up imaging in patients as they evolve, either positively or negatively Examples of such practical dimension of the technique abound, from monitoring the resolution of hydrocephalus in patients who require ventriculostomy following intraventricular hemorrhages, to the close follow-up required for patients at risk of rebleeding following the rupture of a saccular aneurysm More recently, CTA has been proposed for the assessment of vasospasm in patients with subarachnoid hemorrhage (Joo et al, 2006) Finally, a special mention must be made about traumatic intracranial hemorrhage in this context Recent publications suggest that routine repeated use of CT is not warranted except in cases of clinical change (Schuster and Waxman, 2005; Smith et al, 2007) MRI Techniques The utilization of magnetic resonance imaging (MRI) in clinical medicine became widespread during the 1980s The increased sensitivity of this technique, as compared with CT, for the detection of abnormalities in brain structure made it an immediate candidate for the imaging modality of choice in almost all clinical circumstances At first, however, intracranial hemorrhage was the exception due to the difficulty in differentiating acute blood from other tissue using the original spin-echo (SE) sequences More recently, the introduction of additional MRI sequences has resulted in the ability to image intracranial hemorrhages more reliably (Chalela and Gomes, 2004; Evans et al, 2005; Greer et al, 2004; Griffiths and Wilkinson, 2006; Lee et al, 2006; Schellinger and Fiebach, 2004) These new techniques will be described later in this discussion, but first, it is imperative to cover the fundamental concepts of MRI examination of intracranial hemorrhages The MRI appearance of intracranial hemorrhages over time is one of the most interesting subjects in neuroimaging because it largely depends on the natural evolution of hemoglobin degradation within the tissue and the strength of the magnetic field Typically, the sequence of conversion from oxyhemoglobin to deoxyhemoglobin, followed by that from deoxyhemoglobin to methemoglobin (first intracellular and then extracellular, as the erythrocytes disappear) and, finally, to hemosiderin, occurs as a continuum that evolves over weeks to months (Figures 2-4A and 2-4B) (Chalela and Gomes, 2004; Griffiths and Wilkinson, 2006) Hyperacute hemorrhage (ie, a few hours) in the form of oxyhemoglobin is isointense with the brain parenchyma on T1weighted SE images and hyperintense on T2-weighted SE images (Figures 2-4A and 2-4B) After a few hours, the oxyhemoglobin evolves into deoxyhemoglobin within the hematoma The latter predominantly shortens T2, and this leads to low signal on T2-weighted images After to days, deoxyhemoglobin is progressively converted to methemoglobin, which is a paramagnetic substance that shortens both T1 and T2, although its predominant effect is KEY POINT: Ⅲ The MRI appearance of intracranial hemorrhages over time largely depends on the natural evolution of hemoglobin degradation within the tissue and the strength of the magnetic field 41 Potential incorrect postprocessing of CT angiography (CTA) during the search for an aneurysm The patient had suffered a subarachnoid hemorrhage A, B, The original CTA produced quite good three-dimensional images of the major cerebral arteries No aneurysm is visualized in these, but note that the intracranial portions of the internal carotid arteries are incomplete C, Review of the axial acquisition images clearly shows the presence of a left internal carotid artery aneurysm arising from its medial wall (black arrow) D, Additional postprocessing with three-dimensional rendering shows the aneurysm from behind (large white arrow) Note that in order to see it, a compromise has been made to allow more of the skull bone to show in the rendering (small white arrows) FIGURE 2-3 Continuum: Lifelong Learning Neurol 2008;14(4) ‹ INTRACRANIAL HEMORRHAGE shortening T1 As a result, at this stage hematomas display high signal in both T1- and T2-weighted images (Figures 2-4A and 2-4B) Over the next few months, the methemoglobin is slowly broken down into hemichromes, which produce only mild T1 shortening Hematomas at this end stage have a slightly high signal on T1-weighted images but retain a high signal on the T2-weighted images Finally, around the periphery of hematomas, macrophage activity results in degradation of the 42 FIGURE 2-4 Schematic representation of the appearance of intracranial hemorrhages at their various stages using spin-echo MRI techniques in terms of their intensity in the images T1W ϭ T1 weighted; T2W ϭ T2 weighted; RBC ϭ Red blood cells; Hgb ϭ hemoglobin Continuum: Lifelong Learning Neurol 2008;14(4) methemoglobin and conversion of the iron moiety to hemosiderin, which shortens T2 and produces a black ring around the hematoma on T2weighted images (Figures 2-4A and 2-4B) This can be observed within weeks after hemorrhage, and it has a tendency to become thicker over time In small hematomas (less than cm), the low-signal intensity from hemosiderin may essentially occupy the entire ultimate volume of the cavity In my experience, the length of time that the hemosiderin will remain in the area of a hematoma mimics autopsy findings many years after an intracerebral hemorrhage, and I suspect that by using high-field MRI, the residual of the hemorrhage can be readily identified over the lifetime of the patient The concepts outlined above result in a very practical approach to assessing the age of an intracranial hemorrhage using MRI (Figure 2-5) The first step is to look at its appearance on T1weighted images Hyperintensity in this sequence automatically classifies the hematoma as subacute If so, concurrent hyperintensity on T2-weighted images places the hematoma in the late subacute category; otherwise it is an early subacute lesion If the hematoma is isointense on T1-weighted images, the next step is to identify the presence of a conspicuous hypointense rim on T2-weighted sequences, since this is characteristic of chronic lesions Finally, if the hypointense rim is absent and the hematoma is hyperintense, the lesion is clearly hyperacute Otherwise, the hematoma must be considered acute Gradient-Refocused Echo MRI Techniques The discussion above is largely applicable to SE techniques Over the last decade, however, as more knowledge has accumulated about the various methods of applying MRI to clinical practice, sequences that are more sensitive to intracranial hemorrhages have been introduced In general, different materials vary in their ability to support magnetic fields within them This property, known as magnetic susceptibility, is significantly different between some of the hemoglobin breakdown products (ie, deoxyhemoglobin and methemoglobin) and the surrounding brain tissue Such a difference exists because the substances in question have unpaired electrons that superimpose their own magnetic field on the external field This creates field inhomogeneities that increase magnetic susceptibility artifacts and make these substances stand out against the background tissue The presence of magnetic susceptibility artifacts can be emphasized by using techniques that are T2* weighted As an MRI parameter, T2* is the time constant that describes the decay of transverse magnetization, taking into account the inhomogeneities of the static magnetic field and the spin-spin relaxation in the human body This interaction results in rapid loss of phase coherence and MRI signal The T2* is always less than the T2 time, a characteristic that will be of benefit when studying intracranial hemorrhage The gradient-refocused echo imaging sequences use a refocusing gradient in the phase-encoding direction during the end module to maximize (refocus) remaining transverse magnetization at the time when the next excitation pulse is due, while the other two gradients are balanced These sequences can be identified by various acronyms, used by the different companies to identify them (Table 2-1), but fundamentally, all rely on the increased susceptibility artifact displayed by intracerebral hemorrhages at nearly any stage for their rapid detection due to their low-signal appearance (Figure 2-6) Indeed, the literature describing the increased Continuum: Lifelong Learning Neurol 2008;14(4) 43 ‹ INTRACRANIAL HEMORRHAGE sensitivity of gradient-refocused echo techniques for detecting acute intracranial hemorrhages continues to grow, both in the acute and chronic care settings (Chalela and Gomes, 2004; Evans et al, 2005; Greer et al, 2004) The latter relates to the ability to detect microhemorrhages in patients with conditions that place them at risk for additional future hemorrhages (eg, amyloid angiopathy) (Walker et al, 2004) Vascular MRI Techniques: Magnetic Resonance Angiography From the perspective of clinical practice, no discussion of the use of MRI 44 FIGURE 2-5 Flowchart of a step-wise approach to assessing the age of an intracranial hemorrhage (ICH) in spin-echo MRI sequences T1W ϭ T1 weighted; T2W ϭ T2 weighted Continuum: Lifelong Learning Neurol 2008;14(4) for studying patients with intracranial hemorrhage would be complete without describing the sequences that allow the assessment of the cerebral vasculature In general, magnetic resonance angiography (MRA) adds to the ability to assess all aspects of intracranial hemorrhages by helping to identify vascular anomalies that may be causally related to the hemorrhagic process (eg, aneurysms and vascular malformations) Originally, the use of SE MRI sequences produced images in which there was “negative” visualization of the cerebral blood vessels, due to their characteristic signal void relative to the speed of flowing blood This was recognized early in the utilization of MRI but did not seem to provide a reliable method for studying the cerebral vasculature The advent of fast-scanning MRI pulse sequencing, particularly gradient echo and bipolar flow-encoding gradient, has allowed direct vascular imaging and the widespread utilization of MRA At present and specifically for imaging intracranial vessels, either timeof-flight or phase-contrast (PC) techniques can be applied The technique of time-of-flight angiography is based on the phenomenon of flow-related enhancement, and it can be performed with either two- or three dimensional volume acquisitions It utilizes flip angles of less than 60° and no refocusing 180° pulse (the echo is refocused by reversing the readout gradient) This type of MRA can be carried out using one of several gradient-refocused echo methods, including fast low-angle shot (FLASH), fast imaging with steady precession (FISP) and gradientrecalled acquisition in steady state (GRASS) (Table 2-1) On the other hand, PC angiography is based on the detection of velocity-induced phase shifts to distinguish flowing blood from the surrounding stationary tissue TABLE 2-1 Different Techniques for T2* Brain Imaging Acronym Sequence Name FAST Fourier acquired steady-state technique FFE Fast-field echo FISP Fast imaging with steady precession FLASH Fast low-angle shot GRASS Gradient-recalled acquisition in steady state SSFP Steady-state free precession 45 The appearance of an acute cortical hemorrhage using various types of images A, CT clearly shows the hemorrhage as an area of increased density (arrow) B, MRI using spin-echo (SE) FLAIR sequences clearly shows the hemorrhage (arrow) but does not allow its differentiation from other chronic ischemic lesions C, T1-weighted SE imaging does not clearly show the lesion, which is isointense (arrow) D, T2*-weighted sequence using gradient refocused echo clearly shows the lesion as hypointense (arrow) FIGURE 2-6 Continuum: Lifelong Learning Neurol 2008;14(4) ‹ INTRACRANIAL HEMORRHAGE KEY POINTS: Ⅲ The advantages of MR angiography are that it can be carried out as part of the entire MRI evaluation of the patient and, for the intracranial circulation, it does not require contrast administration Ⅲ Intraparenchymal hemorrhages in the context of arterial hypertension have a predictable localization due to their underlying pathophysiology By using bipolar flow-sensitized gradients it is possible to subtract the two acquisitions of opposite polarity and no net phase (stationary tissue) from one another The data that remains reflect the phase shift induced by flowing blood The use of cardiac gating helps overcome the sensitivity of PC angiography to pulsatile and non-uniform flow The advantages of MRA are obvious: it can be carried out as part of the entire MRI evaluation of the patient, and, for the intracranial circulation, it does not require contrast administration Furthermore, in the context of using very high-field (ie, 3.0 tesla) instruments, the vascular detail is simply exquisite, with an ability to resolve very small pathologic structures (Figure 2-7) The main disadvantage is the fact that it is not widely understood that MRA represents an anatomic rendering of flow dynamics, not vessel anatomy This results in common misinterpretations of the images due to wrongful expectations and assumptions Ultrasonic Imaging Techniques Despite the fact that CT and MRI are the two most sensitive and widespread imaging techniques used for the study of patients with intracranial hemorrhages, a smaller body of literature describes the use of transcranial colorcoded sonography in these patients The work, primarily having been done in Europe and Japan, has never really gained popularity in the United States, but it is mentioned here for the sake of completion and because it may be helpful within the constraint of very limited applications (Cheung, 1999; Woydt et al, 1996) CLINICAL APPLICATIONS OF IMAGING: MATCHING THE TOOL TO THE NEED Intraparenchymal Hemorrhage Bleeding directly into a portion of the brain parenchyma most commonly results from hypertensive arteriolopathy, but it can be also produced by other vasculopathies (eg, amyloid angiopathy), ruptured vascular anomalies (eg, arteriovenous malformations), or coagulopathies (eg, hemophilia) Imaging techniques not only allow the identification of the hemorrhagic process but also its categorization and staging Intraparenchymal hemorrhages in the context of arterial hypertension have a predictable localization be- 46 FIGURE 2-7 Normal three-dimensional magnetic resonance angiography obtain at 3.0 tesla using time-of-flight A, Axial and (B) left anterior oblique views demonstrate the exquisite detail not only of the primary brain arteries but also of the second- and third-order branches Continuum: Lifelong Learning Neurol 2008;14(4) cause of their underlying pathophysiology Understanding this basic principle assists considerably in their imaging evaluation Figure 2-8 illustrates the relationship between the progressive branching of the cerebral arterial system and the intraluminal mean arterial pressures of each caliber vessel In general, the mean arterial pressures in the first-order cerebral arteries (eg, middle cerebral artery) approximate 90% of the body’s mean arterial blood pressure (MABP) measured in the aortic arch (ie, mean arterial pressure [first-order artery] ϭ arch MABP ϫ 0.9) Through progressive branching, however, the arterial tree dissipates such high pressures among more numerous yet smaller vessels, the end result being that the mean pressure in the brain capillaries is only about 5% of the MABP (Figure 2-8A) Such pressure differential takes place over a much longer distance in the circumferential arterial branching system than in the perforator system (Figure 2-8B) As a consequence, the latter arteries are under considerably more stress from the intraluminal pressures than those over the circumference of the brain Such an enhanced stress creates a selective vulnerability for the perforators to be affected over time by the elevated pressures of systemic hypertension and predisposes them to lipohyalinosis, fibrinoid necrosis, and overall arterial wall fragility These are the characteristics of hypertensive arteriolopathy and explain why almost invariably, hypertensive intraparenchymal hemorrhages occur in regions of the brain supplied by perforators: the basal ganglia, thalamus, pons, and deep nuclei of the cerebellum The selective localization of hypertensive hemorrhages allows the imaging specialist to quickly identify them while differentiating them from those that have a predilection for occurring in different locations The remaining forms of intrapa- Relationship between the mean arterial blood pressure (MABP) measured in the aortic arch and the mean pressure of the different caliber arteries of the brain A, The mean arterial pressure of the progressively branching arteries slowly declines from about 95% of the MABP in the primary arteries to about 5% in the capillaries B, Comparison between the distance over which the pressure decrement between arteries and capillaries takes place in the circumferential and the perforator territories FIGURE 2-8 renchymal hemorrhages have a less predictable localization with a few exceptions Perhaps the most common is amyloid angiopathy, which is characteristic of relatively elderly individuals and most commonly affects the posterior portions of the cerebral hemispheres (Figure 2-9) (Walker et al, 2004) Another exception involves hemorrhages produced by metastatic tumors, which are characteristically localized at the gray-white matter interface The reason for such predilection also obeys their pathogenesis since metastatic lesions spread to the brain in the form of neoplastic emboli that get lodged in the gray-white matter interface where they continue to grow In these patients, contrast-enhanced imaging is likely to uncover smaller Continuum: Lifelong Learning Neurol 2008;14(4) 47 ‹ INTRACRANIAL HEMORRHAGE Posterior hemisphere acute hemorrhage, such as those observed in patients with amyloid angiopathy A, The CT shows a small hemorrhage outside of the perforator territories B, The hemorrhage is hardly visible in T1-weighted imaging, as would be expected in the acute phase C, Gradient-refocused echo imaging clearly displays the hemorrhage FIGURE 2-9 48 hidden metastases that otherwise would not be seen Finally, hemorrhages associated with coagulopathic processes have a tendency to be more unpredictable and widespread (Figure 2-10), often extending into the ventricular system, or displaying fluid levels indicative of repeated bleeding (Case 2-2) Irrespective of their location and etiology, intraparenchymal hemorrhages have similar appearance when imaged using CT or MRI As noted earlier, CT displays acute hemorrhages as areas of increased density, which may also have adjacent or surrounding areas of hypodensity corresponding to cerebral edema, displacement of adjacent structures (ie, mass effect), and ventricular enlargement due to obstruction of CSF flow An important aspect of the care of patients with hypertensive intraparenchymal hemorrhages is the possibility of issuing prognostic statements based on imaging assessment In the mid-1990s, a method for approximating the volume of intracerebral hematomas using CT was introduced and correlated with the 30-day outcome of the patients The method involved a simplification of the formula for calculating the volContinuum: Lifelong Learning Neurol 2008;14(4) ume of an ellipsoid, as follows: 4/3 ␲ (A/2) (B/2) (C/2), where A, B, and C are the maximal diameters in three planes Considering this, if the value of ␲ is approximated to 3, then the simplified formula becomes: A ϫ B ϫ C/2 The application of this formula to the volumetric assessment of intraparenchymal hemorrhages by CT is illustrated in Figure 2-11 In the original reports, the volume of the hemorrhage combined with the Glasgow Coma Scale (GCS) predicted 30-day mortality with a sensitivity and specificity greater than 96% As such, patients with hemorrhages of more than 60 cc plus a GCS less than or equal to had a predicted 30-day mortality of greater than 90%, while those with hemorrhages of less than 30 cc plus a GCS greater than or equal to had a predicted 30-day mortality of less than 20% However, these reports only relate to the natural evolution of patients as they present and not take into account some of the more recent approaches to aggressive management of these patients Subarachnoid Hemorrhage Although the most common cause of subarachnoid hemorrhages is trauma, KEY POINT: Case 2-2 Ⅲ A 63-year-old man with preexisting atrial fibrillation and treated with chronic anticoagulation (ie, warfarin) was found unresponsive on his recliner Upon arrival, paramedics confirmed his stupor and transported him immediately to the local emergency department Here, he was found to have a blood pressure of 160/90 mm Hg, and to be barely and temporarily arousable His international normalized ratio (INR) was 4.1 His CT is shown in Figure 2-10 He was admitted to the intensive care unit and required placement of a ventriculostomy after his INR was corrected via administration of coagulation blood products He remained hospitalized for about weeks prior to going to inpatient rehabilitation The method for calculating the volume of a hematoma involves a simplification of the formula for calculating the volume of an ellipsoid: A X B X C/2, where A, B, and C are the maximal diameters in three planes Intraparenchymal hemorrhage in the context of a coagulopathy A, The location and appearance of the hemorrhage is rather uncharacteristic of any particular pathologic process (arrow) Note the ventricular enlargement B, There is clearly intraventricular extension, with well-defined blood-fluid level (arrows) C, In addition, a large hemorrhage is present in the right hemisphere, also displaying a blood-fluid level (arrow) FIGURE 2-10 Comment This case represents a bleeding diathesis from an elevated INR caused by warfarin overuse Intracranial hemorrhage from coagulopathies is unpredictable and widespread, often extending into the ventricular system or displaying fluid levels indicative of repeated bleeding those that present spontaneously most commonly result from ruptured saccular (“berry”) aneurysms In general, it is considered one of the most severe forms of stroke, with 10% to 15% of patients dying before ever reaching the hospital and the overall first-week mortality approximating 40% The rapid and decisive diagnosis of subarachnoid hemorrhage is therefore of considerable importance if its management is to have a beneficial impact Traditionally, CT has been considered the initial imaging study of choice with a reported sensitivity that varies between 90% and 100% in the first 24 hours, depending on the series False- 49 FIGURE 2-11 Volumetric analysis of intraparenchymal hemorrhages using a modified ellipsoid formula Continuum: Lifelong Learning Neurol 2008;14(4) ‹ INTRACRANIAL HEMORRHAGE Subarachnoid hemorrhages of various severities A, Small perimesencephalic hemorrhage (arrow), typically associated with good prognosis B, Hemorrhage involving the basal cisterns and fissures (arrows) Note the enlargement of the temporal horns of the ventricles C, More severe hemorrhage involving the cisterns, the convexity sulci, and displaying intraventricular extension (arrows) D, Very severe hemorrhage from a ruptured left middle cerebral artery aneurysm involving the sylvian fissure (large arrow) and extending into the parenchyma (small arrow) FIGURE 2-12 50 TABLE 2-2 negative CT in patients with subarachnoid hemorrhage can occur when the volume of hemorrhage is very small or in patients with severe anemia The typical appearance is one of hyperdensity within the subarachnoid space (ie, following the convolutions and sulci of the cortex), and that can vary between a small focal area around a specific region and an extensive process involving the basal cisterns, even rupturing into the ventricular system (Figure 2-12) An important aspect that derives from the concepts just exposed is that of predicting the risk of vasospasm (ie, one of the most dreaded complications of subarachnoid hemorrhage) from the original CT appearance The admission CT can be used to calculate the Fisher Scale grade of the patient (Table 2-2) This scale has been used for years with fairly good results More recently, however, a modified version has been introduced and validated in large prospective trials (Suarez et al, 2006) Following the identification of the subarachnoid hemorrhage, additional imaging is required to identify the source of the hemorrhage and properly plan the therapeutic approach Clearly, the traditional vascular imag- Comparison Between the Original Fisher Scale for CT Categorization and the Modified Version Grade Classic Fisher Definition Modified Fisher Definition Risk No blood detected Minimal blood in cisterns 10% Diffuse blood (1-mm layers) Thin basal blood ϩ bilateral IVH 20% Thick blood (Ͼ mm) in cisterns Thick blood (Ͼ mm) in cisterns 30% Intracranial hemorrhage or IVH present Thick blood ϩ IVH 40% IVH ϭ intraventricular hemorrhage Continuum: Lifelong Learning Neurol 2008;14(4) ing diagnostic procedure of choice has been cerebral catheterization and angiography, a test for which there is no substitute It has the additional benefit of the planning and execution of endovascular treatment strategies However, the literature of the last few years includes an increasing number of reports regarding the use of CTA, piggybacked to the diagnostic noncontrast CT to identify aneurysms and vascular malformations (Carstairs et al, 2006; Nijjar et al, 2007; Westerlaan et al, 2007) Current CTA technology provides exquisite three-dimensional rendering of the intracranial vasculature, typically within a narrow field of view In practice, the use of either catheter angiography or CTA must be guided by the clinical situation since each has advantages and disadvantages I recommend, whenever possible, to follow the initial noncontrast CT used to diagnose the subarachnoid hemorrhage with a CTA before moving the patient off the table (Figure 2-13) The information derived from this approach is useful in any case Identification of an aneurysm, for example, provides a three-dimensional view that facilitates assessment of the aneurysm neck and the parent vessel and helps guide the endovascular treatment strategy On the other hand, a negative CTA does not overcome the need for catheter angiography but simply alerts the interventionist about pursuing a broader angiographic search as well as extra care in assessing vessels outside of the field of view of the CTA The main downside of CTA involves its need for relatively large amounts of iodinated contrast (ie, about 100 cc) and the nausea that IV administration of these compounds can produce Furthermore, once that contrast has been administered, it limits by the same amount the contrast that can be used during catheter angiography, particularly if this is carried out promptly thereafter Along Use of CT angiography (CTA) to diagnose aneurysms A, This patient suffered a mild subarachnoid hemorrhage that has discrete hyperdensity of the left sylvian fissure (large arrow) and intraventricular blood-fluid level (small arrow) B, Three-dimensional rendering of the CTA clearly identifies the left posterior communicating artery aneurysm (arrow) FIGURE 2-13 these lines, all possible vessels implicated in the common location of aneurysms must be properly imaged by one method and/or the other Finally, I recommend repeating the vascular imaging after weeks in patients with subarachnoid hemorrhage whose original evaluation failed to uncover a source Finally, the role of MRI in the assessment and follow-up of patients with subarachnoid hemorrhage is a matter of discussion Traditionally, as noted earlier, MRI was thought to be very insensitive to this condition in the first 48 hours However, the introduction of T2*-weighted imaging techniques and the widespread utilization of fluid-attenuated inversion recovery sequences have allowed MRI to have an important role in identifying even small hemorrhages (Figure 2-14) Furthermore, the possibility to use time-offlight MRA of the intracranial vessels is of importance in detecting aneurysms In fact, current use of very high-field (eg, 3.0 tesla) instruments allows clear definition of even 1-mm to 2-mm aneurysms, as well as three-dimensional postprocessing (Figure 2-15) Continuum: Lifelong Learning Neurol 2008;14(4) 51 ‹ INTRACRANIAL HEMORRHAGE Role of MRI in assessing a discrete cortical subarachnoid hemorrhage A, CT barely shows the area of hyperdensity (arrow) B, T1-weighted images fail to show the hemorrhage at all (arrow) C, Fast low-angle inversion recovery imaging clearly shows the hemorrhage (arrow) FIGURE 2-14 Epidural and Subdural Hemorrhages Unlike subarachnoid hemorrhages, bleeding in the epidural and subdural spaces invariably results from trauma (although in elderly persons sometimes this is trivial) Fundamental dif- 52 Intracranial magnetic resonance angiography of a small left middle cerebral artery aneurysm A, Threedimensional rendering allows clear visualization of the aneurysm (arrow) B, Postprocessing allows even better assessment of the aneurysm geometry FIGURE 2-15 Continuum: Lifelong Learning Neurol 2008;14(4) ferences between these two conditions exist in terms of the vascular structures involved and their imaging appearance They are discussed together to facilitate their individual recognition and management Epidural hemorrhages occur when blood accumulates between the inner table of the skull and the stripped-off dura, which normally is firmly attached to the skull covering the dural branches of the external carotid artery and their venous counterparts The overwhelming majority of these patients suffer a fracture of the skull overlying the hemorrhage, and the arterial vessels in close proximity are typically the source of the hemorrhage They are most common in the temporoparietal region and only infrequently are the result of venous bleeding Subdural hemorrhages, on the other hand, are most commonly the result of venous bleeding in the space between the dura and the arachnoid Because of their venous origin, their temporal evolution is slower, not infrequently being accompanied by an asymptomatic period between the original insult and the presentation In fact, a number of subdural hemorrhages become chronic, and their imaging appearance changes accordingly In some instances, patients with chronic subdural hemorrhages can display imaging evidence of multiple rebleeding episodes Another major difference between these two conditions is the degree of injury sustained by the underlying brain In the case of epidural hemorrhages, the impact is largely absorbed by the skull, and the underlying brain may be considerably spared Subdural hemorrhages, however, can be associated with significant parenchymal injury In any case, considering the fact that they are essentially traumatic injuries, both epidural and subdural hemorrhages can be seen in association with other traumatic brain injuries, in- FIGURE 2-16 CT appearance of an acute epidural hematoma (arrow) with mild midline shift cluding subarachnoid hemorrhages, parenchymal contusions, and axonal injuries The traumatic nature of these two conditions leads to significant experi- ence with using CT for their diagnosis Indeed, the bulk of the literature pertains to the use of CT because of its speed and widespread utilization in the evaluation of trauma patients The pathogenesis and different aspects described above about each of them help one to understand their CT appearance Epidural hematomas are characterized by a lenticular appearance, particularly in axial images (Figure 2-16) This is because the hemorrhagic process “peels” or “strips” the dura from the inner table of the skull as it grows, but the latter remains largely attached in regions not affected On the other hand, subdural hemorrhages have a more semilunar appearance in axial images, since the blood spreads along the inner surface of the dura, sometimes following its unfolding (eg, tentorial or falcial subdural hemorrhages) (Figure 2-17) (Case 2-3) In the acute phase, KEY POINT: Ⅲ Epidural hematomas are characterized by a lenticular appearance, particularly in axial images Instead, subdural hematomas have a semilunar appearance Case 2-3 A 72-year-old woman sustained a fall while going to pick up her mail She got up with difficulty, noticing that she had struck her head on the pavement of her driveway She immediately called her children, who brought her urgently to the emergency department for evaluation On arrival, her blood pressure was 140/85 mm Hg, and she displayed no neurologic deficit Her CT is shown in Figure 2-17 She was admitted to the intensive care unit for observation of her subdural hematomas She spent week in the hospital and was discharged home without any neurologic sequelae FIGURE 2-17 CT appearance of Comment This patient had a bilateral subdural typical presentation of a bilateral hematomas (small acute subdural hematoma, arrows), with tentorial treated conservatively Risk extension (large arrow) factors associated with a subdural hematoma include older age, alcoholism, use of anticoagulants, and bleeding diathesis Continuum: Lifelong Learning Neurol 2008;14(4) 53 ‹ INTRACRANIAL HEMORRHAGE both the epidural and subdural hemorrhages are displayed as having the high density typical of acute blood Depending on their size, they may show displacement of adjacent structures (ie, mass effect) Unlike epidural hemorrhages, those in the subdural space may evolve so slowly as to have characteristic appearances during their subacute or chronic stages In the same way as it was described above for intraparenchymal hemorrhages, the degradation of the acute blood over time renders the subdural hemorrhage isodense during the subacute stage and hypodense during the chronic stage At times, repeated episodes of bleeding can be seen in chronic subdural hemorrhages as a hyperdense fluid level within the subdural space Finally, chronic subdural hemorrhages must be distinguished from subdural hygro- mas, accumulations of CSF between the dural and the arachnoid resulting from involutional brain changes that separate the two Considerably less information is available about the use of MRI in the study of patients with either epidural or subdural hemorrhages The main reason is the need for expeditious examination of these patients in the emergency setting However, occasionally MRI may be useful in differentiating chronic subdural hemorrhages from hygromas (Figure 2-18) The magnetic susceptibility of hemoglobin products renders the chronic subdural hemorrhage significantly different than the CSF In addition, evidence of subacute rebleeding in the form of the typical T1-weighted hyperintensity of methemoglobin is seldom present Clearly though, in cases where either of these types of lesions is associated 54 Role of MRI of a subacute subdural hemorrhage A, The CT scan shows bilateral subdural hemorrhages with a somewhat isodense/hypodense appearance B, T2-weighted imaging does not allow distinction between a hemorrhage and a hygroma C, T1-weighted and (D) FLAIR images clearly show the subdural hemorrhages with intensity different than that of spinal fluid FIGURE 2-18 Continuum: Lifelong Learning Neurol 2008;14(4) with small subarachnoid or parenchymal hemorrhages (ie, contusions), MRI is superior in defining the overall status of the brain More recently, the use of diffusionweighted MRI has been suggested as the means to differentiate solid from liquid subdural hematomas (Kuwahara et al, 2004; Kuwahara et al, 2005a; Kuwahara et al, 2005b) CONCLUSIONS The utilization of imaging techniques for the evaluation of patients with intracranial hemorrhages is of paramount importance in their management, but the choices must be guided by the specific needs of the clinical situation Although CT has been the traditional image modality of choice, advances in MRI have resulted in additional dimensions in the assessment of these patients In fact, MRI is rapidly becoming the de facto “bedside neuropathology,” providing exquisite detail about the diagnosis as well as a unique perspective on prognosis In addition, both CT and MRI techniques allow evaluation of the cerebral vasculature, an important aspect of studying these patients and identifying the root cause of their hemorrhagic event Finally, although CT is preferred in the evaluation of patients with traumatic hemorrhages, MRI may also add information relevant to their care REFERENCES Carstairs SD, Tanen DA, Duncan TD, et al Computed tomographic angiography for the evaluation of aneurysmal subarachnoid hemorrhage Acad Emerg Med 2006;13(5):486 – 492 Chalela JA, Gomes J Magnetic resonance imaging in the evaluation of intracranial hemorrhage Expert Rev Neurother 2004;4(2):267–273 Cheung RT Differentiation between intracerebral hemorrhage and ischemic stroke by transcranial duplex sonography Stroke 1999;30(8):1735–1736 Evans AL, Coley SC, Wilkinson ID, Griffiths PD First-line investigation of acute intracerebral hemorrhage using dynamic magnetic resonance angiography Acta Radiol 2005;46(6):625– 630 Greer DM, Koroshetz WJ, Cullen S, et al Magnetic resonance imaging improves detection of intracerebral hemorrhage over computed tomography after intra-arterial thrombolysis Stroke 2004;35(2):491– 495 Griffiths PD, Wilkinson ID MR imaging of recent non-traumatic intracranial hemorrhage: early experience at T Neuroradiology 2006;48(4):247–254 Joo SP, Kim TS, Kim YS, et al Clinical utility of multislice computed tomographic angiography for detection of cerebral vasospasm in acute subarachnoid hemorrhage Minim Invasive Neurosurg 2006;49(5):286 –290 Kuwahara S, Fukuoka M, Koan Y, et al Subdural hyperintense band on diffusionweighted imaging of chronic subdural hematoma indicates bleeding from the outer membrane Neurol Med Chir (Tokyo) 2005a;45(3):125–131 Kuwahara S, Fukuoka M, Koan Y, et al Diffusion-weighted imaging of traumatic subdural hematoma in the subacute stage Neurol Med Chir (Tokyo) 2005b;45(9):464 – 469 Continuum: Lifelong Learning Neurol 2008;14(4) 55 ‹ INTRACRANIAL HEMORRHAGE Kuwahara S, Miyake H, Fukuoka M, et al Diffusion-weighted magnetic resonance imaging of organized subdural hematoma— case report Neurol Med Chir (Tokyo) 2004; 44(7):376 –379 Lee SW, Choi SH, Hong Y, Kim W Effects of magnetic resonance imaging diffusion gradient recalled echo on a patient with an intracranial hemorrhage presenting to the emergency department Eur J Emerg Med 2006;13(2):117–118 Nijjar S, Patel B, McGinn G, West M Computed tomographic angiography as the primary diagnostic study in spontaneous subarachnoid hemorrhage J Neuroimaging 2007;17(4): 295–299 Schellinger PD, Fiebach JB Intracranial hemorrhage: the role of magnetic resonance imaging Neurocrit Care 2004;1(1):31– 45 Schuster R, Waxman K Is repeated head computed tomography necessary for traumatic intracranial hemorrhage? Am Surg 2005;71(9):701–704 Smith JS, Chang EF, Rosenthal G, et al The role of early follow-up computed tomography imaging in the management of traumatic brain injury patients with intracranial hemorrhage J Trauma 2007;63(1):75– 82 Suarez JI, Tarr RW, Selman WR Aneurysmal subarachnoid hemorrhage N Engl J Med 2006;354(4):387–396 Walker DA, Broderick DF, Kotsenas AL, Rubino FA Routine use of gradient-echo MRI to screen for cerebral amyloid angiopathy in elderly patients AJR Am J Roentgenol 2004; 182(6):1547–1550 Westerlaan HE, Gravendeel J, Fiore D, et al Multislice CT angiography in the selection of patients with ruptured intracranial aneurysms suitable for clipping or coiling Neuroradiology 2007;49(12):997–1007 Woydt M, Greiner K, Perez J, et al Transcranial duplex-sonography in intracranial hemorrhage Evaluation of transcranial duplex-sonography in the diagnosis of spontaneous and traumatic intracranial hemorrhage Zentralbl Neurochir 1996;57(3): 129 –135 56 Continuum: Lifelong Learning Neurol 2008;14(4) ... fundamental concepts of MRI examination of intracranial hemorrhages The MRI appearance of intracranial hemorrhages over time is one of the most interesting subjects in neuroimaging because it largely... routine utilization of IV contrast as part of the CT examination of the patient with an acute intracranial hemorrhage is unwarranted The demonstration of possible enhancement of any of the tissue in... equivalent of “bedside neuropathology,” and that they have direct correspondence with the natural history of every type of intracranial hemorrhage Monitoring of Evolution Regardless of how the