Chapter 10 Spontaneous Intraparenchymal Hemorrhage

Alejandro A. Rabinstein, Steven J. Resnick

The ability to image the brain using computed tomography (CT) and magnetic resonance imaging (MRI) has greatly enhanced our understanding of intraparenchymal hemorrhages (IPH) in the central nervous system. Before the advent of these modalities, the diagnosis of IPH was based on clinical presentation and indirect angiographic findings. Certainty could only be reached at the time of necropsy. CT and MRI now provide us with means to characterize the hematoma size, its location, and its effect on adjacent structures. Furthermore, they allow us to follow the evolution of the hematomas and taught us that these lesions are highly dynamic and have a dangerous tendency to expand early after their development.^1,² Brott et al. reported substantial hematoma growth (greater than one third of the baseline volume) in 26% of patients within 1 hour of the initial CT scan and in an additional 12% within the first 20 hours among patients presenting for emergency evaluation within 3 hours of symptom onset.¹

The cause responsible for the production of the hematoma can often be gleaned from brain imaging, such as in cases of associated tumors and vascular anomalies. Timing and adequacy of interventions may be guided by serial imaging, as is often the case with progressive hydrocephalus requiring ventriculostomy or expanding cerebellar hemorrhages demanding surgical evacuation. Various radiological features predict functional outcome after IPH. Hematoma volume greater than 60 cc, pronounced midline shift, infratentorial location, presence of hydrocephalus, and intraventricular hemorrhage have been shown to be prognosticators of death or poor recovery.^3,⁴

Because hematoma volume carries such remarkable prognostic weight, it is essential to be familiar with the pragmatic technique used to estimate volume on the basis of CT scan appearance. This technique, known as the ABC/2 method and reliably validated in the literature, is simply based on the measurement of the three maximal diameters of the hematoma.⁵ It is illustrated on Figure 10-1. This measurement method can be applied using axial cuts of MRI sequences, but MRI-based measurements may lead to overestimation of lesion size.⁶

Figure 10-1 An estimation of hematoma volume (cc) can be calculated with the formula (A × B × C)/2.⁵ First, identify the slice with the largest area of intracerebral hematoma. A represents the longest diameter (cm) to be measured in the slice showing the largest hematoma size. B represents the longest diameter (cm) perpendicular to A. C represents the height of the hematoma, calculated by multiplying the number of slices involved by the slice thickness (cm). To measure the number of slices involved, comparisons should be made to the largest diameter slice using percentages: if the diameter of the hematoma in the slice is greater than 75% of the largest diameter in the scan, that slice is counted as one full slice; if the diameter of the hematoma in the slice is between 25% and 75% of the largest diameter in the scan, that slice is counted as half, if the diameter is less than 25% of the largest diameter, the slice is not counted. The figure exemplifies how hematoma volume can be estimated. Slice 5 was identified as the largest area of intracerebral hematoma. The longest diameter (A) is measured as 6.5 cm. The longest perpendicular diameter (B) is 5.5 cm. C can be measured by calculating the slice thickness (0.5 cm) by the number of slices involved (10) (0.5 × 10=5). Slices 1, 2, and 16 were not counted because the diameter of the hematoma in those slices was less than 25% of the largest diameter in the scan. Slices 3, 9, 12, 13, 14, 15 were counted as half (total of 3); slices 4, 5, 6, 7, 8, 10, 11 were counted as one (total of 7). Values A(6.5) × B(5.5) × C(5) were then multiplied and divided by 2 to reach an estimated volume of 89 cc.

Traditionally, CT scan was considered the modality of choice for the diagnosis of hyperacute IPH.⁷ However, MRI has now been shown to be as accurate as CT scan for the detection of acute hematomas and offers greater sensitivity for the recognition and temporal staging of chronic hemorrhages.⁸^–¹⁰ Susceptibility-weighted sequences, such as gradient-recalled echo (GRE) T2^*-weighted imaging, are particularly useful for the detection of acute hemorrhage. GRE also allows optimal visualization of chronic hemorrhages and microhemorrhages.

Figure 10-2 depicts how changes in MRI appearance help determine the age of intraparenchymal hemorrhage.

Figure 10-2 Stages of intraparenchymal hemorrhages as depicted by different magnetic resonance imaging sequences. GRE, gradient-recalled echo.

Trying to establish whether there is an area surrounding the hematoma that is at risk for ischemia (penumbra) has lately been the focus of intensive research. Perfusion- and diffusion-weighted MRI, CT perfusion, single photon emission computed tomography (SPECT), and positron emission tomography have been used as tools to address this question. Most evidence thus far appears to indicate that hematomas are surrounded by a region of hypoperfusion that corresponds to a metabolically quiescent area.¹¹^–¹⁴ Serial imaging with perfusion-weighted MRI has shown that the hypoperfusion surrounding the hematoma resolves by the second week.¹⁵ However, some studies support the notion that hematomas may be surrounded by ischemic penumbra.^11,¹⁶ Thus, more research is necessary to reach a final answer.

Determining the volume of perihematomal edema and following the evolution of edema over time has important practical implications. Perihematomal edema appears early and, on average, increases by 75% during the first 24 hours in patients with acute spontaneous IPH.¹⁷ The volume of baseline relative edema on initial CT scan correlates inversely with the subsequent accumulation of edema in the following hours of the first day.¹⁷ More interestingly, presence of greater volume of baseline relative edema (but not of absolute edema) has been found to be associated with better functional outcome at 3 months in patients with IPH without intraventricular extension.¹⁸ These observations await confirmation, and their meaning is unclear at present, but they nonetheless highlight the likely importance of edema formation in the outcome of patients with IPH. Late neurological deterioration (in the second and third weeks after acute IPH) from a delayed increase in edema volume is not infrequently encountered in practice and may provoke unexpected brain herniation. For that reason, patients with large hematomas may require serial imaging even many days after the bleeding. The pathophysiology of this late edema demands further investigation.

Classification of IPH is typically based on its anatomical location. The most common sites of origin of spontaneous IPH in the largest imaging series are ^19,²⁰:

♦ Striatocapsular (30%–50%)

♦ Lobar (20%–40%)

♦ Thalamic (10%–20%)

♦ Cerebellar (7%–12%)

♦ Pontine (2%–8%)

♦ Intraventricular (1%–3%)

The following sections of the chapter discuss the value of neuroimaging in the diagnostic assessment, clinical management, and prognostication of patients with spontaneous IPH on each of these locations.

STRIATOCAPSULAR HEMORRHAGES

The striatocapsular region comprises the lenticular and caudate nuclei, the internal capsule, and the external capsule and subinsular area. The presentation and prognosis of striatocapsular hemorrhages depend on the epicenter of the bleeding. Chung and colleagues have proposed a detailed classification that divides these hemorrhages into six types, as listed in Table 10-1.²⁴

TABLE 10-1 Anatomical classification of striatocapsular hemorrhages.

Type	Site of bleeding	Arterial territory
Anterior	Caudate nucleus	Heubner’s artery
Middle	Globus pallidus or medial putamen	Medial lenticulostriates
Posteromedial	Posterior limb of internal capsule	Anterior choroidal
Posterolateral	Posterior putamen	Lateral lenticulostriates (posteromedial branches)
Lateral	External capsule, subinsular region	Lateral lenticulostriates (lateral branches)
Massive	Entire area (may spare caudate and anterior limb of internal capsule)	Variable

Most putaminal hemorrhages encountered in practice tend to be lateral and remain localized in the region of the lenticular nucleus or expand toward the insula. Medial hemorrhages occur less often, and, when large, they may be difficult to differentiate at first glance from external thalamic hematomas. Massive hemorrhages may obscure the center of origin and extend both medially and laterally; herniation is often present early.

Impaired level of consciousness at presentation and large hematoma size consistently predict poor functional outcome in patients with striatocapsular hemorrhage. Additionally, hydrocephalus and intraventricular extension are markers of large hematoma size in patients with putaminal hemorrhage (unlike in those with bleedings emanating from the caudate) and thus also forecast death or dependency.²¹^–²³ Capsular involvement is strongly associated with persistent hemiparesis, but weakness tends to be severe only in patients with larger hematomas.

Lateral Putaminal Hemorrhage

Case Vignette

A 48-year-old Hispanic woman with recent diagnosis of hypertension presented with sudden onset of headache and left-sided weakness. Examination revealed an alert patient with a blood pressure of 210/124 mm Hg, mild right horizontal gaze palsy, and severe left hemiparesis. She appeared relatively unconcerned about her weakness and paid less attention to activity occurring over her left visual field. The patient had no complications during her acute hospitalization. Her CT scan of the brain revealed a right lateral putaminal hemorrhage, later confirmed on MRI (Figure 10-3, upper two rows). No underlying vascular anomalies or masses were found. Six months later, she had residual weakness but recovered the ability to walk independently with minimal support and had partial functional use of her left arm. Follow-up imaging is shown in the lower row of Figure 10-3.

Figure 10-3 Computed tomography scan of the brain showing a lateral putaminal hemorrhage of moderate size exerting mild mass effect over the lateral ventricle. The hypodense rim surrounding the hematoma represents edema (A). Magnetic resonance imaging (MRI) shows that the hemorrhage is isointense on T1-weighted sequence (B) and hyperintense on T2-weighted sequence (C), denoting the acuteness of the lesion. Note that edema is better delineated by MRI. Gradient-recalled echo (GRE) shows the acute hemorrhage as a dark signal, whereas edema appears bright as in T2-weighted images (D). Six months later, repeat MRI shows a relatively small, linear residual scar seen on T1-weighted (E) and GRE images (F).

♦ Lateral striatocapsular hemorrhages are lens-shaped lesions that remain typically contained within the deep brain parenchyma; thus they are not readily accessible for surgical drainage.

♦ Although often deemed putaminal in origin, these hemorrhages typically arise from rupture of lateral lenticulostriate branches into more lateral structures (external capsule, claustrum) and may actually spare the putamen itself when not large.

♦ Most patients have preserved or minimally impaired level of consciousness. The severity of weakness depends on extension into the posterior limb of the internal capsule. Some degree of dysphasia is seen in nearly half of the cases with hematomas in the dominant hemisphere but is usually transient. Neglect and anosognosia can occasionally be observed in patients with hemorrhages in the nondominant side, and they also tend to improve rather rapidly in most cases. Mild to moderate conjugate gaze paresis may be present in the acute phase.²⁴

♦ These hematomas can rarely rupture into the anterior horn of the lateral ventricle.

♦ They exert pressure on more medial structures, and their expansion may cause subfalcine herniation.

♦ Good functional recovery can be expected in the majority of cases.

Massive Striatocapsular Hemorrhage

♦ Massive hemorrhages may occur at onset or develop after hematoma growth in the first few hours following the original bleeding (Figure 10-4).

♦ Patients with massive striatocapsular hemorrhage present with stupor or coma, contralateral hemiplegia, and marked ocular movement abnormalities. Signs of subfalcine and transtentorial (diencephalic or uncal) herniation are obvious on initial examination or appear shortly after.

♦ Ventricular extension is characteristically present, and hydrocephalus (often in the form of trapping of the contralateral ventricle) is a frequent complication.

♦ Outcome is typically poor, with high rates of mortality.

♦ There is no evidence that surgical evacuation improves outcome.²⁵

Figure 10-4 A 68-year-old woman with history of hypertension presented with coma and right-sided hemiparesis. Her computed tomography scan of the head showed a massive putaminal hemorrhage invading the anterior horn of the lateral ventricle and producing mass effect with midline shift and early subfalcine herniation.

Posterolateral Striatocapsular Hemorrhage

♦ Posterolateral striatocapsular hemorrhages, the most common type of striatocapsular hemorrhage, primarily affect the posterior putamen and tend to spread ventrally or dorsally (Figure 10-5). However, rostrocaudal extension may also occur and produce mass effect over diencephalic structures.

♦ Patients are most commonly awake but hemiparetic because of frequent involvement (direct or indirectly by compression) of the posterior limb of the internal capsule. Transient dysphasia or neglect and gaze deviation (ipsilateral or, rarely, “wrong way”) may be present. Sensory deficits are relatively frequent.

♦ Intraventricular extension occurs very rarely.

♦ In the absence of enlargement, death is exceptional, but functional recovery is often limited because of persistent hemiparesis.

Figure 10-5 A 65-year-old man with history of hypertension presented with lethargy and right-sided hemiparesis. Initial computed tomography (CT) scan of the head (left and middle) showed a large left posterolateral putaminal hemorrhage with expansion into the ipsilateral temporal lobe. After craniectomy, a repeat CT scan confirmed successful hematoma evacuation (right). The patient had good clinical outcome.

Middle-Posteromedial Striatocapsular Hemorrhage

♦ Middle striatocapsular hemorrhages are relatively uncommon and arise from rupture of middle lenticulostriate branches. Posteromedial striatocapsular hemorrhages may be caused by rupture of terminal branches of the anterior choroidal artery.

♦ Patients are most often alert and may present with abnormal ocular movements and mild to moderate hemiparesis.

♦ They usually spread laterally toward the lateral aspect of the lenticular nucleus and the external capsule (Figure 10-6).

♦ Large hemorrhages with epicenter in the globus pallidus or the medial putamen may be indistinguishable from hematomas originating from the lateral portions of the lenticular nucleus.

♦ Ventricular rupture is distinctly infrequent.

♦ Functional prognosis tends to be good to fair, with more than half of patients recovering independence.²⁴

Figure 10-6 A 72-year-old hypertensive man presented with sudden onset of right sided hemiparesis. Head computed tomography scan revealed a left middle striatocapsular hemorrhage with typical lateral extension. Notice the medial putaminal epicenter of the hematoma without rupture into the lateral ventricle.

Caudate Hemorrhage

♦ Hemorrhages arising from the head or body of the caudate constitute the anterior group of striatocapsular hemorrhages and are caused by rupture of the recurrent artery of Heubner.

♦ Caudate hemorrhages are invariably associated with intraventricular hemorrhage (Figure 10-7).

♦ They represent an obligatory differential diagnosis in any case of intraventricular hemorrhage.

♦ Hematoma volume tends to be relatively small to moderate.

♦ Patients present with sudden severe headache and neck stiffness but usually have only mild neurological impairment. Memory problems, abulia and perseveration, or, less frequently, restless agitation may be noted during the first few months but later tend to resolve. Larger hematomas may produce focal deficits in the acute phase that are most often mild and transient.

♦ Functional outcome is characteristically favorable.^24,²⁶

Figure 10-7 A 62-year-old woman with history of diabetes and hypertension developed a sudden, severe headache and presented in the emergency department with a blood pressure of 260/100. Computed tomography scan of the head showed a left caudate hemorrhage with extension into the left lateral ventricle.

LOBAR HEMORRHAGES

Lobar spontaneous IPH may be less frequent than is traditionally estimated. In recent years, enhanced technology, mainly in the form of MRI and highly improved angiographic equipment, has demonstrated that cases previously believed to be due to hypertension are actually caused by other conditions, such as occult vascular anomalies, venous thrombosis, or, most often, amyloid angiopathy. Secondary causes of IPH are discussed in the next chapter but must be carefully excluded before concluding that a lobar hemorrhage is spontaneous even in a hypertensive patient (Table 10-2). Neuroimaging is an extremely valuable and in fact irreplaceable tool to recognize the correct etiology of bleeding in patients with lobar IPH.

TABLE 10-2 Causes of lobar intracerebral hemorrhage other than primary arterial hypertension

Cause	Diagnosis
Ruptured saccular aneurysm	Angiography
AVM	Angiography
Cavernous angioma	MRI
Cerebral amyloid angiopathy	MRI (GRE)
Tumor	MRI with gadolinium
Hemorrhagic transformation of ischemic infarction	CT, MRI with DWI
Cerebral venous thrombosis	MRV or angiography
Coagulopathy (intrinsic or iatrogenic)	History, blood work, CT
Recreational drugs (amphetamines, cocaine)	History, toxicology screening
Trauma	History, CT
Vasculitis	History, blood work, CSF, angiography, cultures if suspicion of infection
Ruptured mycotic aneurysm	Angiography, blood cultures, TEE
Moyamoya syndrome	Angiography

AVM, arteriovenous malformation; CSF, cerebrospinal fluid; CT, computed tomography; DWI, diffusion-weighted imagery; GRE, gradient-recall echo; MRI, magnetic resonance imaging; TEE, transesophageal echocardiography.

Lobar hemorrhages tend to originate from the cortical-subcortical or gray-white matter junction and extend into the adjacent white matter. Any lobe can be involved, and the location and laterality of the hematoma determines the clinical manifestations. Seizures, typically of focal onset with secondary generalization, occur frequently occur at onset and during the acute phase.^27,²⁸ Multiple hemorrhage locations, simultaneous or sequential, may occur because of hypertension but must be regarded as a potential indicator of an alternative cause (mainly amyloid angiopathy in the elderly with cortical hemorrhages or cavernous malformations in young patients with deep hemorrhages).

The overall outcome of patients with lobar IPH is deemed to be comparatively more favorable than after ganglionic hemorrhages.^29,³⁰ Once again, one has to be cautious when analyzing older series reporting favorable outcomes because they may have included patients with more benign secondary hemorrhages in the group of spontaneous lobar IPH. Size is still the most powerful predictor of outcome, and intraventricular extension remains a prognosticator of reduced chances of survival and poor recovery.