Basal ganglia hemorrhage

B a s a l g a n g l i a h e m o r r h a g e

By: ICD Code

Mark J Alberts and Richard Bernstein I 61.0 I 61.2

Historical note and nomenclature The first cogent description of an intracerebral hemorrhage was published in 1658 by Wepfer in his treatise on apoplexy (Garrison 1969). In that article he noted both intracerebral hemorrhage and subarachnoid hemorrhage in different patients. Through the years, intracerebral hemorrhage has also been termed "cerebral hemorrhage," "intracranial hemorrhage," and "cerebral bleed." The advent of head CT has greatly improved the localization of intracerebral hemorrhages, and this has added to the nomenclature (ie, basal ganglia hemorrhage, versus lobar hemorrhage, versus cerebellar hemorrhage). Clinical manifestations The clinical symptoms and signs vary depending on the size, location, and rate of expansion of the bleed. In about two-thirds of cases the onset is gradual, whereas one-third have a sudden onset of symptoms. Symptoms can evolve over several minutes (10 to 30 minutes) or even hours, contrary to popular belief that the deficit is always maximum at onset. Typical features found in many, but not all, patients include headache, nausea, vomiting, and alterations in the level of consciousness (Hier et al 1977; Kase et al 1992). Elevated blood pressure is found in over 90% of patients acutely, even if there is not a prior history of hypertension (Mohr et al 1978). The most common location for a basal ganglia hemorrhage is the putamen (Mohr et al 1978; Kase et al 1992). Basal ganglia hemorrhages can also occur in the caudate and thalamus (Freytag 1968; Mohr et al 1978; Furlan et al 1979; Kase et al 1992). A putaminal hemorrhage in the dominant hemisphere, if large, can produce an aphasia, contralateral hemiparesis and hemisensory loss, contralateral visual field abnormalities, and gaze deviation (toward the side of the bleed). A putaminal intracerebral hemorrhage in the nondominant hemisphere can produce a neglect syndrome or apraxia, in addition to the motor and visual findings noted above. A large putaminal hemorrhage with mass effect or extension into the frontal horns of the ventricular system can produce obtundation or even coma at presentation. A large bleed producing herniation with uncal compression of the third nerve can cause either partial or complete ipsilateral third nerve palsy. Smaller bleeds produce subsets of these symptoms. Some patients complain of headache, and those with large bleeds or extension into the ventricular system may also have nausea, vomiting, and nuchal rigidity. Rare bilateral putaminal hemorrhages have been reported to cause cortical deafness (Arimura et al 2002) and the combination of amnesia and acalculia (Shu et al 2002). Thalamic hemorrhages account for 10% to 15% of all hemorrhages (Walshe et al 1977; Mohr et al 1978). They can produce contralateral motor and sensory deficits and a pure sensory stroke (Shintani et al 2000). The sensory deficits may be more pronounced than those seen with putaminal hemorrhages. Altered consciousness is

found in 80% to 90% of cases. Oculomotor abnormalities are common, including absent or poor upward gaze and miotic, unreactive pupils. Downward deviation of the eyes is also seen (Walshe et al 1977; Barraquer-Bordas et al 1981). These findings reflect compression of the midbrain tectum by the thalamic hematoma. An anomic aphasia may be present with lesions of the dominant thalamus (Alexander and LoVerme 1980), as may cataleptic posturing (Saposnik et al 2001). Caudate bleeding is relatively uncommon, accounting for 5% to 7% of all intracerebral hemorrhages (Stein et al 1984). Since a hemorrhage in this location is likely to rupture into the ventricular system, common symptoms at presentation include headache, nausea, vomiting, and altered consciousness. Nuchal rigidity from the subarachnoid blood is common. A contralateral hemiparesis can also occur (Stein et al 1984; Kase et al 1992). Transient gaze abnormalities such as horizontal gaze paresis have been reported. Involvement of the nucleus basalis may produce memory impairment (Choi et al 1983; Stein et al 1984). There are reports of extremely small (less than 1.5 cm) hemorrhages that tend to occur in the basal ganglia and internal capsule. Such hemorrhages have symptoms that are similar to those of a lacunar stroke, emphasizing the need for brain imaging in all such patients (Kim et al 1994). Hemorrhages may also occur in other areas of the brain, including the external capsule, periventricular and subependymal, midbrain, and medulla. In each of these cases, as well as in the locations noted above, the specific clinical picture will vary depending on the size of the bleed, rate of expansion, location, and concomitant neurologic diseases. Recurrence of hypertensive hemorrhages was thought to be rare. However, several studies have found that approximately 5% of hypertensive basal ganglionic hemorrhages recur, presumably due to the effects of severe hypertension (Chen et al 1995; Misra and Kalita 1995). Another study found an annual recurrence rate of 2.4%, although some of these cases may have had amyloid angiopathy (Hill et al 2000). Clinical vignette A 56-year-old man of African descent was brought to the emergency room after collapsing at home. He was in his usual state of health until that morning, when he complained of a severe left sided headache. Several minutes later he developed slurred speech and weakness of the right arm and leg. He went to bed hoping that the symptoms would resolve. His wife attempted to awaken him in 1 hour and found him difficult to arouse. When he was moved from the bed he appeared to be confused and had trouble walking. When placed in a chair, he soon collapsed to the floor and was then taken to the emergency room. His past medical history is significant for hypertension for roughly 15 years. He took antihypertensive medications irregularly, and had not been taking his medications for the past 3 weeks. Other problems included smoking roughly 1 pack of cigarettes per day for 30 years. On physical exam he was stuporous, with a blood pressure of 200/105, pulse 66, respirations 20, without fever. He was intubated to control his respirations and protect his airway. His neck was somewhat stiff. Neurologic examination showed no response to verbal stimulation. His pupils were dilated 4 mm and sluggish. Eyes showed left gaze deviation without a response to doll's eyes maneuver. The left corneal response was decreased. Gag reflex was absent. Motor exam showed

absent movements or responses on the right to deep pain, with decorticate posturing of the right upper extremity. Deep tendon reflexes were increased on the right, and both toes were upgoing. A head CT scan showed a 5 cm by 7 cm intracerebral hemorrhage centered in the left putamen, with blood extending into both lateral ventricles. Mild left to right transfalcine shift was also seen. Routine lab studies were normal. The patient was admitted to the Neurosciences Intensive Care Unit. His elevated blood pressure was treated with a nicardipine IV infusion. He was hyperventilated to reduce PCO2 and reduce intracranial pressure. A ventriculostomy was placed to drain blood and cerebrospinal fluid from the right lateral ventricle. The ventriculostomy showed an intracranial pressure of 27 mm Hg. Despite these measures, he did not show any clinical improvement. A repeat head CT scan done 12 hours after admission showed further bleeding into the ventricles and more left to right shift. After discussion with the patient's family, the decision was made to provide supportive measures only. The patient expired 24 hours after admission. Etiology The generally accepted cause of idiopathic (or hypertensive) intracerebral hemorrhage is the rupture of a small blood vessel within the brain parenchyma. The underlying lesion causing vessel rupture is not always known. In one study of 896 cases of spontaneous intracerebral hemorrhage, etiologies included hypertension in 63.5% of the patients, cerebrovascular malformation in 8.5% of the patients, and abnormal hemostasis in 15% of the patients (Rosenow et al 1997). The areas that are most likely to be affected by an intracerebral hemorrhage are also common sites for small vessel ischemic stroke (ie, basal ganglia, thalamus, pons), supporting the concept that an abnormality of small vessels leads to either rupture (producing an intracerebral hemorrhage) or occlusion (producing a lacunar stroke) in these regions. In some cases, the use of anticoagulants (particularly warfarin, if the international normalized ratio is 4 or more), thrombolytic agents, significant alcohol intake, and illicit drugs can cause or precipitate an intracerebral hemorrhage (Da Silva and Bormanis 1992; De Jaegere et al 1992; Hylek and Singer 1994; Juvela et al 1995). Case reports, case series, and a case control study have described an association of intracerebral hemorrhage with the use of sympathomimetic drugs such as phenylpropanolamine and midodrine, although the significance of these reports remains controversial (Kernan et al 2000; Sandroni et al 2001). It is unclear whether these agents cause rupture of a preexisting miliary aneurysm, or produce an intracerebral hemorrhage by another process. Kidney or liver failure (Ozgun and Castillo 1995), lightning strikes (Wang et al 2000), and cerebral edema in the setting of hyperglycemic hypersmolar coma (Cho et al 2002) have also associated been with hemorrhages. Pathogenesis and pathophysiology Several entities have been purported to cause rupture of the small vessels that lead to an intracerebral hemorrhage. Evidence supports the concept that miliary aneurysms (sometimes referred to as Charcot-Buchard aneurysms) form in these vessels, probably due to the effects of long-standing hypertension. These aneurysms rupture and produce an intracerebral hemorrhage. One study found such aneurysms in the brains of 15 of 16 hypertensive patients (Ross 1963). Another study found brain miliary aneurysms in 46% of hypertensives (Cole and Yates 1967). Such aneurysms

were identified in 85% of patients with large intracerebral hemorrhages (Cole and Yates 1967). Other studies have suggested that lipohyalinosis (caused by hypertension) of small vessels leads to vessel rupture and subsequent intracerebral hemorrhage (Fisher 1971). An amyloid angiopathy (due to deposition of amyloid in vessel walls) is presumed to be the cause of some cases of lobar hemorrhages (Wakai et al 1992). One study found that 15% of cases with spontaneous intracerebral hemorrhage had a family history of intracerebral hemorrhage (Graffagnino et al 1994). There are forms of hereditary intracerebral hemorrhage among Dutch and Icelandic populations (Jensson et al 1987; Haan et al 1990). Bleeds in these patients are due to mutations in the amyloid precursor protein gene or the cystatin gene, respectively (Levy et al 1989; 1990). A search for these mutations in patients with sporadic intracerebral hemorrhage was negative (Graffagnino et al 1994). Epidemiology Spontaneous intracerebral hemorrhage is the third most common type of stroke. It is more common in males, in African Americans, and in the elderly (Voelker and Kaufman 1997). The estimated annual incidence is 28 per 100,000 in Caucasians, 50 per 100,000 in those of African descent, and 61 per 100,000 in Asians (Qureshi et al 1999; Kase et al 1992). Overall, the incidence has fallen by approximately 50% during the past 30 years, perhaps due to better treatment of hypertension (Furlan et al 1979). Hypertension is clearly the key risk factor for this type of intracerebral hemorrhage. Some studies found evidence of hypertension in 72% to 81% of patients with intracerebral hemorrhage, whereas others have reported a more modest frequency of 45% to 56% (Mohr et al 1978; Furlan et al 1979; Brott et al 1986; Schutz et al 1990). Other risk factors include alcohol ingestion, cigarette smoking, and low cholesterol levels (reported in Japanese men) (Monforte et al 1990; Fogelholm Murros 1993; Juvela et al 1995). Data from the Nurses Health Study found that low intake of saturated fat and trans unsaturated fat increased the risk of parenchymal cerebral hemorrhage (Iso et al 2001). Diabetes is also an independent risk factor for cerebral hemorrhage (Copeland et al 1999). Anticoagulants and recent thrombolytic therapy increase the risk of intracerebral hemorrhage, particularly among older individuals. Recent liver transplantation has emerged as a risk factor for intracerebral hemorrhage (Wang et al 2000). Low socioeconomic status may also be a risk factor for intracerebral hemorrhage (Jakovljevic et al 2001). Prevention Improved and more aggressive treatment of hypertension is generally accepted as the main reason for the significant declines in incidence and mortality of intracerebral hemorrhage during the past 30 to 40 years (Furlan et al 1979). More judicious use of anticoagulants (lower levels of anticoagulation) and the avoidance of these agents in high-risk populations (alcoholics, elderly, gait instability) may also help to reduce the occurrence of intracerebral hemorrhages. The combination of a thiazide diuretic and an ACE inhibitor has been shown to decrease the risk of recurrent intracerebral hemorrhage by at least 50%, perhaps due in part to the antihypertensive effects of these drugs (PROGRESS Collaborative Group 2001). Treatment of high-risk hypertensive patients with the ACE inhibitor ramipril also decreases the risk

of intracerebral hemorrhage (Heart Outcomes Prevention Evaluation Study Investigators2000). Differential diagnosis Many different entities can either produce an intracerebral hemorrhage or produce findings similar to a hemorrhage. Entities that can be mistaken for a primary hypertensive intracerebral hemorrhage include hemorrhagic transformation of an ischemic stroke, bleeding into a tumor, vascular malformation, aneurysm (mycotic, saccular), abscess or other infectious lesions, trauma, vasculitis or vasculopathy (including amyloid angiopathy and Moyamoya disease), surgery, venous infarction, and acute hemorrhagic leukoencephalopathy (Bogousslavsky et al 1991; Kase 1991; Kase et al 1992; Takeda et al 2002) . Among these various disorders, unsuspected arteriovenous malformations were the most common lesion found after investigation with angiography (Halpin et al 1994). Some tumors have a propensity for undergoing hemorrhagic transformation. Although melanoma and choriocarcinoma are not the most common metastatic brain tumors, they are likely to hemorrhage. Other metastatic tumors likely to hemorrhage include renal cell, thyroid, and breast. Primary brain tumors, particularly grade 4 glioblastomas, are also likely to bleed. Other factors that precipitate an intracerebral hemorrhage include anticoagulants, fibrinolytic agents, antiplatelet agents, head trauma, other inherited or acquired coagulopathies (alcohol abuse, renal failure), and illicit drugs such as cocaine (Levine et al 1990; Anderson et al 1991; Da Silva and Bormanis 1992; De Jaegere et al 1992; Kaufman et al 1993; Melo et al 1993). Diagnostic workup In addition to the clinical presentation and examination, a brain imaging study is crucial for making an accurate diagnosis of intracerebral hemorrhage. Typically, a noncontrast head CT will show a high-density lesion consistent with a hematoma. MRI may show a large intracerebral hemorrhage, although there is some concern that MRI may miss extremely small and acute intracerebral hemorrhages. However, recent studies have found that susceptibility-weighted MRI could detect cerebral hemorrhages within 30 to 80 minutes of onset (Linfante et al 1999). Additional tests may be needed to determine whether the intracerebral hemorrhage is truly idiopathic, or due to one of the previously cited lesions. Using gradient-echo T2* weighted images, researchers have found asymptomatic microbleeds in 54% of patients with symptomatic parenchymal intracerebral hemorrhages (Roob et al 2000). Such patients had an average of 14 microbleeds in various locations. A contrast-enhanced CT or MRI is useful to look for changes suggestive of an arteriovenous malformation, other vascular lesions, or a tumor. A recent study found that MRI was able to identify a new etiology for the intracerebral hemorrhage in 23% of patients (Dylewski et al 2000). Intraoperative ultrasound imaging with color Doppler has been shown to demonstrate the nidus of a ruptured arteriovenous malformation within a massive basal ganglia hemorrhage (Kitazawa et al 1998). An angiogram is sometimes performed for similar reasons. In cases of idiopathic or hypertensive intracerebral hemorrhage, the angiogram will either be negative or show only evidence of the mass effect of the hematoma. The most common structural abnormalities seen with angiography are arteriovenous

malformation and aneurysm (Halpin et al 1994). Rarely, brain biopsy is done to evaluate for the presence of amyloid angiopathy or tumor. In cases of a suspected tumor, a systemic work-up to rule out metastasis from another source (lung, melanoma) is indicated. Coagulation studies to rule out bleeding diathesis should be performed. Prognosis and complications Complications of an intracerebral hemorrhage can be divided into direct and indirect effects. Direct effects are those that are caused by the intracerebral hemorrhage and its local effects. These local effects arise from the mass of the bleed, as well as the cerebral edema that often forms around the bleed. Complications include brain herniation (transfalcine, uncal), as well as midbrain compression (from a thalamic intracerebral hemorrhage). Obstructive hydrocephalus can occur if a basal ganglia hemorrhage kinks or obstructs the foramen of Monro or cerebral aqueduct. Another complication of intracerebral hemorrhage that was not fully appreciated until a few years ago is an expansion of the clot that evolves several hours after the onset of bleeding (Broderick et al 1990; Bae et al 1992). Although the frequency of such expansion is unclear, there is agreement that growth of the hematoma can be associated with neurologic worsening. It is uncommon for basal ganglionic intracerebral hemorrhage to cause seizures. Some studies have suggested that such clot expansion is caused by elevated blood pressure, although this remains unclear (Maruishi et al 2001). The prognosis for intracerebral hemorrhage patients relates to the size and location of the bleed, expansion of the original clot, presenting status, and age of the patient (Lisk et al 1994; Rosenow et al 1997). The 30-day mortality is 40% to 50% (Bamford et al 1990; Broderick et al 1993b). Clots larger than 60 cc, or more than 3 cm in diameter, have a poor prognosis, especially when accompanied by intraventricular hemorrhage (Broderick et al 1993a). In such cases the mortality is 80% to 90%. The ICH Score," a novel, standardized severity score combines Glasgow coma score, age, presence of infratentorial hemorrhage, and presence of IVH into a composite factor which effectively predicts mortality (Hemphill et al 2001). Age is an important factor, as older patients have a higher mortality than younger adults (Daverat et al 1991). Patients presenting in a coma have a poor prognosis (Radberg et al 1991). Mortality is higher in patients of African descent than in Caucasians (Sacco et al 1991). Patients with a recurrent hemorrhage have a poor outcome, with a mortality of 26% and severe disability in 51% (Chen et al 1995). Fever within the first few days of an intracerebral hemorrhage is also an independent predictor of a poor prognosis (Schwarz et al 2000). One study correlated outcome with initial mean arterial blood pressure. Patients with mean arterial blood pressure more than 145 mm Hg had a worse outcome than patients with lower pressures (Dandapani et al 1995). However, since this was a retrospective study, definitive conclusions cannot be made about an independent role for blood pressure in prognosis. Another study of 173 patients with cerebral cavernous malformations showed that location was the most important factor for predicting neurologic deterioration, with significantly higher rates (10.6% per year) for deeply located lesions (basal ganglia, thalamus, brainstem, cerebellar nuclei) compared to superficially located lesions (0% per year) (Porter et al 1997).

Management Treatment of intracerebral hemorrhage remains problematic, with no clear evidence of efficacy for any medical or surgical intervention. The goals of therapy are to prevent hematoma expansion and recurrent hemorrhage, reduce intracranial pressure while optimizing cerebral perfusion, prevent tissue shifts, and preserve or improve neurologic function. Measures that can reduce bleeding include reversal of any coagulopathy that may have precipitated the bleed. This might include the administration of protamine for heparin-induced bleeding, vitamin K for warfarin-associated intracerebral hemorrhages, and cryoprecipitate for bleeds due to thrombolytics. The use of a prothrombin complex concentrate may reverse anticoagulation more rapidly than fresh frozen plasma (Fredriksson et al 1992; Cartmill et al 2000). In all cases, fresh frozen plasma also may be used to correct an acquired coagulopathy. Reduction of increased intracranial pressure caused by the intracerebral hemorrhage is similar to steps used in other conditions (Ropper 1993). The placement of an intracranial pressure monitor in patients with a Glasgow coma score of less than 9 facilitates optimization of intracranial pressure and cerebral perfusion pressure when level of consciousness can not be closely followed clinically. Supportive measures include, maintaining a straight neck position, reducing agitation, and keeping the patient slightly dehydrated. Other aggressive steps include hyperventilation, osmotic diuretics such as mannitol, and a ventriculostomy to measure intracranial pressure and remove cerebrospinal fluid to reduce intracranial pressure (Ropper 1993). Agents such as thiopental (discussed above) may reduce intracranial pressure and protect neurons by reducing brain metabolism. In all cases, careful attention must be given to the cerebral perfusion pressure, which is calculated as follows: cerebral perfusion pressure = mean arterial blood pressure - intracranial pressure Interventions that reduce cerebral perfusion pressure below 50 mm Hg to 60 mm Hg may have deleterious effects on neuronal function. The use of antihypertensive agents in patients with intracerebral hemorrhage is somewhat controversial. Although some believe that gentle lowering of the blood pressure may reduce the risk and extent of expansion of the hematoma, there is no clear proof that this is effective. One study did show that patients with higher blood pressures had a worse prognosis (Dandapani et al 1995), but any causal link between blood pressure and outcome remains unproven. One group has suggested keeping the mean arterial blood pressure less than 130 mm Hg (Broderick et al 1999). An important concern has been that lowering the blood pressure acutely may induce worsening ischemia in a penumbral region around the hematoma. However, recent studies in animal models and humans with cerebral hemorrhage have failed to identify a penumbral region (Qureshi et al 1999; Diringer et al 1998). A recent study did not detect any clinical worsening when hypertension was treated (Adams et al 1999). Another study found that cerebral autoregulation appeared normal around most cerebral hemorrhages (Powers et al 2001). Based on these data, lowering of the blood pressure may be safe and reasonable in such patients. In general, we attempt to keep mean arterial pressure around 110 mm Hg to 120 mm Hg, and follow the exam carefully during any manipulation of blood pressure. This

is consistent with recent American Heart Association guidelines, which recommend a mean arterial pressure of less than 130 after hypertensive intracerebral hemorrhage, with mean arterial pressure of less than 110 after evacuative surgery (Broderick et al 1999). The choice of antihypertensive agents is important. Some commonly used antihypertensives, particularly the nitrate-based drugs (nitroprusside, nitroglycerin) and certain calcium channel blockers (nifedipine) can cause a significant increase in intracranial pressure (Cottrel et al 1978; Hayashi et al 1988). Such an effect can be deleterious in patients with large intracerebral hemorrhages who already have increased intracranial pressure. Antihypertensives that are less likely to increase intracranial pressure include beta-blockers (labetalol, esmolol) and the angiotensin converting enzyme inhibitors (enalapril, captopril). Thiopental reduces blood pressure, cerebral metabolism, and intracranial pressure. Most experts feel that patients with intracerebral hemorrhage should be cared for in neuroscience intensive care units, as opposed to general ICUs. Two recent studies have found that such patients have a reduced mortality when cared for in a neuroscience ICU compared to a general ICU (Ronning et al 2001; Diringer and Edwards 2001). The efficacy of surgical removal of the hematoma has been a subject of much debate (Radberg et al 1991; Kalff et al 1992; Zumkeller et al 1992). Several studies have produced somewhat conflicting results (Kanno et al 1984; Kanaya 1990). Patients with small intracerebral hemorrhages typically do well, whether the hematoma is removed or allowed to resolve spontaneously. Therefore, conservative medical therapy is appropriate in this group (Broderick et al 1999). Cases with large hematomas tend to do poorly with either surgical or medical therapy. Moderate-sized hematomas that expand and cause clinical deterioration may be most amenable to surgical removal, particularly if the bleed is superficial and in the nondominant hemisphere or a noncritical region (Maiuri et al 1990; Broderick et al 1999). The Cochrane Stroke Group did a metaanalysis of surgical treatment for intracerebral hemorrhage, and did not find any evidence of efficacy, even with endoscopic or aspiration removal of the clot (Prasad and Shrivastava 2000). Another recent study found that early surgery was associated with rebleeding and a high mortality rate (Morgenstern et al 2001). Several studies have evaluated stereotactic removal of hematomas, either with or without the use of local thrombolytics to enhance clot removal (Liu et al 1991; Miller et al 1993; Montes et al 2000). A typical protocol includes hematoma aspiration, followed by the instillation of 5,000 units to 10,000 units of urokinase (Montes et al 2000). There is no clear proof of the safety or efficacy of this approach, although with additional experience and technical refinements it may become more widely used. The use of local thrombolytics is associated with a 4% to 5% rate of bleeding complications (Kaufman 1993; Broderick et al 1999). An antiischemic therapy, muscimol, has been shown to improve the outcome after intracerebral hematoma in preclinical models (Lyden et al 1997); no data are yet available from clinical trials. Pregnancy There is no clear evidence that pregnancy contributes to, or causes, basal ganglia hemorrhage.

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