INTRODUCTION
Intracranial haemorrhages account for ap- proximately 20% of all cerebral ictuses related to vascular disease, with a higher prevalence of intraaxial localizations (15%) as compared to those principally within the subarachnoid space (5%) (1, 6, 9). Although MRI is highly specific with regard to haemorrhagic lesions, CT remains the examination of choice, espe- cially in emergencies, in part due to the diffi- culty in managing acutely ill patients within the MR scanning unit.
Any physician who acquired an MRI unit in its early stages of clinical application will re- member the sense of confusion experienced with the first acute intracerebral haematoma patient, as initially diagnosed on MRI. In such cases, the lesion MR signal was “ambiguous”, nearly devoid of the specific characterizations seen on CT in patients with haemorrage. In the early stages haemorrhage could appear quite similar to an ischaemic ictus, being differentiat- ed when possible by the differing topography and morphology.
This impact conditioned the attitude of neu- roradiologists against the use of MRI in acute haemorrhagic pathology for some years, and this instinctive wariness has only partly been re-
conditioned by a clear working knowledge of the evolution of the MR signal of parenchymal haemorrhagic collections (13, 15-18).
In this chapter, we will analyse the informa- tion that can be deduced from intracranial haemorrhages using MRI, making a distinction between intraaxial and subarachnoid forms due to the difference in the anatomopathologi- cal and biochemical environment in which the phenomena that influence the haemorrhagic MRI signal occur.
SEMEIOTICS
Intraaxial haemorrhage
Intraaxial cerebral haemorrhages are serious clinical events characterized by a variable alter- ation in the state of consciousness, an often se- vere neurological deficit and by the possible as- sociation with meningeal signs. Alongside this more common presentation, there are more se- rious clinical forms such as sudden decerebra- tion as well as milder forms with relatively mi- nor effects on the state of consciousness and a less serious clinical deficit.
The most frequent cause of intraaxial haem- orrhage, which accounts for more than 50% of
1.7
MRI IN HAEMORRHAGE
L. Simonetti, S. Cirillo, R. Agati
cases, is systemic hypertension associated with intracranial atherosclerotic vessel alterations.
Other causes, in order of frequency, are the rupture of vascular malformations, coagulation disorders, intratumoral haemorrhages (espe- cially neoplastic metastases and malignant gliomas), trauma and postsurgical/iatrogenic causes.
Evolution-based semeiology
Neuroradiological semeiology based on the time elapsed since the onset of the intraaxial bleeding is complex (2, 7, 8, 14, 19): with re- gard to CT, the observations are linked above all to the macroscopic and sub-macroscopic anatomopathological alterations of the haemor- rhagic focus, while with MR the imaging find- ings of haemorrhage must be integrated with varying biochemical factors.
The various steps that take the haematic col- lection from the hyperacute phase, with a prevalence of oxyhaemoglobin, to the outcome and reparation phase, in which the final break- down components such as haemosiderin pre- vail, and the consequent variations in the MR signal are now well understood and catego- rized. It should be remembered that it was pre- cisely the need to explain the dynamic behav- iour of the MR signal of the haematoma that prompted the reconsideration, proper correla- tion and accurate categorization of the stages of haemoglobin metabolism outside the vascular bed. It goes without saying that the state of the haemoglobin within the haemorrhagic focus is of little importance from a diagnostic and ther- apeutic point of view, but it nevertheless pro- vides a very real stimulus for the neuroradiolo- gist to understand clearly this physiological process in order to properly interpret the im- ages.
The temporal evolution of the MR charac- teristics of blood is caused both by alterations of the erythrocytes as well as the haemoglobin present under several differing conditions. As far as the red blood cells are concerned, mem- brane integrity, guaranteed under normal con- ditions by the ATPase/Na-K units dependent
on the membrane and powered by glycolytic energy, is of great importance. Haemoglobin al- terations are influenced by various factors, in- cluding: pH, conditions of osmolarity, temper- ature, partial oxgen pressure (pO2) and the metabolic microenvironment along with the concentration of the oxidizable sublayers. Both oxygenated and deoxygenated haemoglobin circulate inside red blood cells; in such forms of haemoglobin, the heme contains bivalent iron.
If the iron group is oxidized to form trivalent iron, the molecule (metahaemoglobin) loses its ability to bond oxygen; for this reason, through the pentoso-phosphate pathway, a considerable percentage (10%) of the red blood cell’s cata- bolic energy is used to form reducing agents (NADPH and reduced glutathione) capable of preventing or correcting haemoglobin oxida- tion. The same reducing agents also perform the important role of controlling the peroxida- tion of the membrane lipids that would other- wise increase the osmotic fragility of the ery- throcytes. The remaining 90% of the glycidic catabolism of red blood cells follows the gly- colytic pathway, which produces the ATP used to fuel the Na-K dependent ATPase structures.
The proper functioning of these membrane pumps is indispensable for the maintenance of erythrocyte osmolarity and thus the normal bi- concave cellular shape. A sufficient glucose supply is therefore required for several purpos- es: to maintain cellular osmolarity, to keep the haemoglobin properly reduced and to avoid the peroxidation of membrane lipids.
In the light of this, it is easier to interpret the blood’s relaxation parameter alterations using MRI. In the hyperacute phase, in other words in the first 12 hours from onset, intraparenchy- mal haemorrhagic foci are composed of intact red blood cells with high oxygen saturation and therefore containing oxyhaemoglobin. In the absence of paramagnetic molecules or struc- tures, the MR relaxation times are longer than those of the surrounding tissue due to the local alteration in free water content and protein concentration. The resulting oxyhaemoglobin- dominant haemorrhagic lesion on MRI (Fig.
1.71) is complex but includes: relative (as com-
pared to normal brain tissue) minor hypoisoin-
tensity on the T1-weighted images, minor hy- perintensity on PD-weighted images, and mi- nor hyperintensity on the T2-weighted images (in truth, the relative intensity differentials as compared to normal brain are quite small in all routine MR acquisition sequences).
In the oxygen-dependent acute phase (12 hours - 2 days), the pO2 within the extravasat- ed blood starts to drop fairly quickly, and con- sequently there is a reduction in the haemoglo-
bin’s oxygen saturation, with the eventual for- mation of deoxyhaemoglobin. Deoxyhaemo- globin, characterized by high magnetic suscep- tibility and enclosed in the finite intracellular space of the erythrocyte, causes non-homo- geneity of the local magnetic field, thus result- ing in a loss of phase coherence of the resident protons. This translates into a preferential field strength -dependent enhancement of T2 relax- ation. Although deoxyhaemoglobin is para- magnetic, it does not influence T1 relaxation because its heme groups are contained in apo- lar pockets that prevent contact with water pro- tons. The presence of deoxyhaemoglobin in the haemorrhagic lesion translates into (Figs. 1.72, 1.73): relative hypo-isointensity on T1-weight- ed images, iso-hypointensity on PD-weighted images and rather marked hypointensity on T2- weighted images.
The subacute, glucose-dependent phase (2- 14 days) is characterized by two events that oc- cur in parallel but slightly out of phase with one another, partly sharing the same pathogenic mechanisms: the formation of metahaemoglo-
Fig. 1.71 - Hyperacute phase right intracerebral sub-Sylvian haemorrhage (12 hours). Coronal T1-dependent scan (a) and axial T2-dependent scan (b). The lesion presents as hy- pointense in T1 and non-homogeneously hyperintense in T2, where the notably hyperintense oedema halo in formation is al- so visible.
Fig. 1.72 - Acute phase intracerebral haemorrhage (38 hours from onset) in a left thalamo-capsular location. Axial PD (a) and T2 scans: the lesion presents as non-homogeneously hy- pointense with a vast oedematous halo.
a
b
bin (methaemoglobin: 2-7 days) and erythro- cyte lysis (7-14 days).
Methaemoglobinization presupposes the ex- haustion of the oxide-reducing homeostasis of the erythrocyte systems due to a regional re- duction in glucose concentration, the blockage of the catabolitic pentose-phosphate pathway and the progressive reduction of NADPH and reduced glutathione. In addition to an ex- tremely reduced concentration of glucose, haemoglobin oxidation to methaemoglobin is also conditioned by a given pO2 of about 20 mm Hg.
The pathogenesis of red blood cell lysis in- cludes: the exhaustion of erythrocyte ATP re- serves with the stoppage of the Na-K depend- ent membrane pumps and the osmotic swelling of the erythrocytes, the peroxidation of mem- brane lipids and the catabolization of the mem- brane phospholipids by tissue phospholipases.
Being intensely paramagnetic, methaemoglo- bin causes a reduction in T1 relaxation due to the dipole-dipole interaction between the exter- nal shell electrons of the methaemoglobin and water protons. The influence of methaemoglo- bin on T2 relaxation is identical to that de- scribed for deoxyhaemoglobin. Once erythro- cyte lysis has taken place, a loss of T2 relaxation enhancement occurs, as methaemoglobin as- sumes a homogeneous distribution, which translates into hyperintensity of the MR signal on T2-weighted images. At the same time, the intensity on T1-weighted images increases due to the greater T1 relaxation effects of the free methaemoglobin as compared to intracellular methaemoglobin.
To summarize, in the first week of this phase (intact membrane methaemoglobiniza- tion), the MR signal characteristics of the in- tracellular methaemoglobin dominance within the haemorrhagic lesion can be classified as follows: relative hyperintensity on T1-weight- ed images, hyperintensity on PD-weighted im- ages and hypointensity on T2-weighted im- ages. In contrast to this, once erythrocyte lysis has taken place, the extracellular methaemo- globin dominance within the haemorrhage demonstrates: relative hyperintensity on T1- weighted images, hyperintensity on PD-de- pendent images and hyperintensity on T2- weighted images.
For purposes of completeness, we will now describe MR signal alterations in chronic-phase intraparenchymal haematomas (more than two weeks), although, strictly speaking, this goes slightly beyond the temporal limits of this dis- cussion. The chronic phase of haematoma evo- lution is characterized by the phagocytosis of erythrocyte lysis products by microphages around periphery of the haemorrhagic collec- tion. Within the macrophages heme iron accu- mulates primarily within lysosome vacuoles in
Fig. 1.73 - Acute phase intracerebral haemorrhage in left tem- poral location: coronal T1- (a) and T2-dependent (b) scans:
note the marked hypointensity of the lesion and the perilesion- al oedema.
a
b
the form of haemosiderin. The presence of haemosiderin causes increased T2 relaxation and therefore hypointensity on T2-weighted images within the peripheral rim of the haem- orrhagic lesion that persists indefinitely. In
the meantime, methaemoglobin within the haemorrhagic collection continues to cause MR signal hyperintensity on the T1- and T2- weighted images. Subsequently, as months pass, methaemoglobin breaks down into de- rivatives that do not have T1 relaxation effects (Figs. 1.74, 1.75).
Bleeding cause-based semeiology
In addition to the diagnosis of the presence of an intraaxial haemorrhage, MRI can also sometimes provide information that indicates the underlying cause of the bleeding. Apart from arterial hypertension, and excluding trau- ma, intracerebral bleeding typically is caused by vascular malformations or richly vascular- ized intracerebral neoplasias. In such cases the site, morphology, structure and number of blood collections can vary. Therefore, using this information together with the clinical picture, the neuroradiologist is able to suggest the like- ly cause(s) of bleeding.
a) Site
The localization of intraaxial haematomas is represented, in order, by:
– Nucleo-capsular haemorrhages (between the basal ganglia nuclei and the internal cap-
Fig. 1.75 - Sagittal PD-dependent MRI scan: note the thin hy- pointense rim that surrounds the lesion, due to the presence of haemosiderin.
Fig. 1.74 - Left parietal haemorrhage in chronic phase (28 days). Axial CT scan after contrast agent (a): hypodense le- sion with thin hyperdense rim. Axial PD-dependent MR scan: the lesion shows the characteristic hyperintense haema- tic signal.
a
b
sule: 50%). Nucleo-capsular haematomas can be subdivided into capsulo-lenticular (between the internal capsule and the lentic- ular nucleus [globus pallidus plus puta- men]), capsulo-thalamic (between the inter- nal capsule and the thalamus) and capsulo- caudate (between the internal capsule and the caudate nucleus) haematomas. In most cases the haematomas in this position are considered spontaneous, and are linked to arterial hypertension both as a cause of the induced chronic vascular alterations as well as the triggering cause of the acute haemor- rhage. Acute hypertensive crises can also lead to haemorrhages at these locations.
Small capsulo-caudate haematomas are an exception, as the rupture of small periven- tricular arteriovenous malformations more often causes them than does hypertension.
– Lobar haemorrhages (35%). These haem- orrhages are rarely spontaneous. Temporal and occipital lobe haematomas are usually secondary to arteriovenous malformations or haemorrhagic infarcts, mainly due to ve- nous ischaemia. Frontal haematomas are generally caused by ruptures of aneurysms associated with the anterior communicat- ing artery or anterior cerebral artery. All lobar haemorrhages can have a neoplastic origin.
– Infratentorial haemorrhages (10%). These haemorrhages can be subdivided into brain- stem and cerebellar bleeds. The former are frequently caused by vascular malformation ruptures, most commonly cavernous an- giomas; the latter are more typically associ- ated with tumoural bleeding or, less fre- quently, with aneurysm ruptures.
– Intraventricular haemorrhages (5%). Isolat- ed intraventricular haemorrhages devoid of signs of intraaxial haematoma formation are rare. They are generally secondary to the rupture of small paraventricular or choroid plexus arteriovenous malformations.
b) Morphology and structure
Intraaxial haematomas can be round or oval, with well-defined margins, or alternatively ir- regular with dendritic margins or even with completely irregular boundaries having a some-
what map-like appearance. Haematoma mor- phology can be linked to either a vascular mal- formation/aneurysm or a spontaneous aetiolo- gy, however, haematomas with irregular mar- gins are more commonly encountered in pa- tients with blood dyscrasias.
The appearance of the haemorrhage can be homogeneous or heterogeneous, occasionally manifesting a horizontal fluid-fluid level in haemorrhages due to variations in the makeup of the blood clot.
c) Number
Intraaxial blood collections tend to be single in number. The finding of multiple haemor- rhagic foci, usually in a superficial lobar posi- tion (excluding those of traumatic origin), point in the direction of a diagnosis of a blood disorder (including iatrogenic anticoagula- tion), multiple haemorrhagic neoplastic metas- tases (including melanoma) or dural venous si- nus thrombosis with venous infarcts/haemor- rhages.
Semeiotics based on technical MR parameters MR tissue contrast in the presence of blood depends to a great extent on the parameters of the image acquisition sequence used. In gradi- ent-recalled echo (GRE) sequences, the sensi- tivity to paramagnetic constituents is very high. However, this sensitivity requires atten- tion to magnetic susceceptibility “border”
artefacts at the interface of the petrous bones and the paranasal sinuses with the brain parenchyma.
Fast Spin-echo (FSE) sequences differ from
conventional SE sequences in that they use a
train of 180° radiofrequency pulses, which gen-
erate a set of echoes that are individually coded
in the space of a single TR. The implications in
brain examinations are that the effects of mag-
netic susceptibility dephasing are removed and
the effects of diffusion-induced signal loss are
reduced. T2-dependent FSE sequences there-
fore have a lower sensitivity to magnetically sus-
ceptible blood products than do the correspon-
ding conventional spin echo images. The use of
supplementary GRE sequences or T2-weighted
conventional spin echo imaging sequences is recommended in cases where clinical history suggests possible cranial haemorrhage. Echo- planar Imaging (EPI) sequences are becoming increasingly suitable for routine clinical appli- cations. They are very sensitive to magnetic sus- ceptibility in both conventional spin echo and GRE sequences.
Closing comments
The importance of understanding the MR signal characteristics of intraaxial haematomas within the framework of the evolutional phase of the individual blood collections should be underlined: this knowledge is in part intended to provide a means of interpreting MR images in patients with an acute clinical ictus (stroke) who have been inadvertently sent to MRI instead of CT. The greater diagnostic contribution of MRI in patients with intracranial haemorrhage is in the subacute and chronic phases. We refer here to those cases in which the initial clinical and CT findings are ambiguous, thus creating prob- lems of differential diagnosis. In such instances the performance of an MR examination that shows the MR signal characteristics specific for the various evolving blood products dispels di- agnostic doubts.
One piece of additional information that can be gleaned from MRI as compared to CT is the ability of the former to link many “non-sponta- neous” haemorrhages with the underlying pathological condition responsible for the bleed. The better relative sensitivity of MRI in diagnosing vascular malformations (Fig. 1.76), even in the presence of a haematoma, is well known. However, it is less well understood that, in order to be visible when haemorrhage is present, the vascular malformation must be of a rather considerable size. In the presence of acute or subacute haematomas, small vascular malformations are easily overlooked on routine MR images, in part due to the distortion caused by the magnetic field; this applies for both con- ventional MR as well for MR angiography ex- aminations (Fig. 1.77). And, although MR an- giography is an important contribution to pa-
tient treatment planning, it should be comple- mented with a conventional angiographic ex- amination in the pretreatment phase of patient analysis.
Subarachnoid haemorrhage
Haemorrhage into the subarachnoid space (subarachnoid haemorrhage: SAH) has a sud- den clinical onset with headache, nausea, vom- iting, varying degress of disturbance of con- sciousness, widespread cutaneous hyperaesthe- sia and severe meningeal signs. Clinical varia- tions can range from more subtle forms where the meningeal syndrome alone is present, to mixed cerebromeningeal forms associated with clinical symptomatology of the neurological deficit type to more serious forms characterized by coma.
The most frequent cause of SAH is aneurysm rupture, followed, in order of frequency by the rupture of brainstem or cerebral arteriovenous malformations, trauma, blood clotting disorders and, lastly, acute haemorrhagic necrosis of the pituitary gland (5).
Fig. 1.76 - Right temporal-occipital haemorrhage in subacute phase with arteriovenous malformation. Coronal PD-depend- ent scan: the haemorrhagic lesion is very clear, as is the malfor- mation nidus with its characteristic signal void.
Semeiology and variations based on time MR semeiology of SAH is made all the more complex by the continuous alterations being undergone by the blood with relationship to the biological parameters of the subarachnoid space (pH, pO2, glucose concentration). The
variation of these parameters follows different rules that are less easily codified than those that characterize intraparenchymal blood collec- tions (3, 4). For this reason, MRI generally finds little place in the evaluation of acute phase SAH, given CT’s greater sensitivity and rapidity, and its ease of access 24 hours a day.
The interpretation of MR images in patients with non-traumatic SAH is doubtlessly more straightforward in the subacute and chronic phases, and its contribution grows with the passing of time since the “acute” moment of the bleed as the diagnostic efficiency of CT dwindles. In reality however, even during the acute phase a well-planned and executed MR examination can also allow a demonstration of the characteristic signs of SAH.
Variations in the relaxation parameters that distinguish the evolutional phases of haemor- rhagic collections are linked to the structural and functional variations of erythrocytes and the consequent conditions of haemoglobin oxi- dation and oxygenation.
In the subarachnoid space, erythrocyte and haemoglobin alterations follow different dy- namics than those observed in intraparenchy- mal haemorrhages, in part due to the different biochemical-metabolic microenvironment. This makes it somewhat difficult to pinpoint the tem- poral limits of the phases of evolution of SAH.
In the hyperacute phase, there is no length- ening of proton density relaxation times in comparison to the surrounding CSF, but rather a slight shortening of T1 relaxation times due to the increase in protein content; this subtle change is often not detected due to the long re- laxation times of the CSF, which mask the the- oretical effects of the fresh blood, and conse- quently the T1-weighted MR images are usual- ly interpreted as being negative.
In the acute phase it is difficult to perceive the reduction of T2 relaxation times character- istic to parenchymal blood collections, given that the CSF environment is an open system in which the focal variations of pO2 are slowed (relatively higher levels of pO2 are maintained as compared to the cerebral parenchyma).
And, as noted in the preceding paragraph, it is difficult to evaluate small variations in relax-
Fig. 1.77 - Small left frontal intraparenchymal haemorrhage.
Sagittal T1-dependent scan (a) TOF MRA (b). The image con- cerning the haematoma is obvious on the MRA reconstruction:
this would prevent the visualization of any small arteriovenous malformation present.
b
a
ation times in the environment of the CSF, and as a result the T2-weighted MRI tends to be negative.
During the acute phase it is sometimes possible to find some linear hyperintensity on T1-weighted images in an intrafissural loca- tion. Such observations, which indicate SAH, are interpreted to be clotting of the ex- travasated blood within the subarachnoid space. Contact with the CSF is a sufficient stimulus to cause clotting of the blood pres- ent in the subarachnoid spaces. If we then add the fact that the retraction of the clot causes dramatic variations in red blood cell concentration and fibrin structure, we can then explain how it is possible even in an acute phase to visualize SAH in some in- stances. Clotting is therefore the key to visu- alizing blood in the early phases of SAH when using conventional MR sequences. The limit of this semeiological element lies in the tem- poral, quantitative and topographic variabili- ty of clotting processes, the percentage of blood in the CSF, the functionality of the clot- ting mechanisms, the site of the bleed and the biochemical composition of the CSF microen- vironment.
In the subacute phase, a reduction in T1 re- laxation (hyperintensity on T2-weighted im- ages) caused by the presence of methaemoglo- bin is clearly visible. In the subarachnoid space, the reduction in glucose concentration, re- quired for methaemoglobinization and erythro- cyte lysis, also takes place at a slower pace than that observed in parenchymal blood collec- tions. This phase represents the period in which MRI reaches its peak sensitivity for SAH; this is made all the more important if we consider that in this period, the CT density of the extravasated blood tends to decrease, thus consonantly reducing the sensitivity of this technique.
In recent years, we have started to exam- ine SAH with MRI using FLAIR (fluid-at- tenuated inversion recovery) sequences (10, 11). FLAIR images are obtained using an in- version recovery (IR) sequence that has long TI (time to inversion) and TE (time to echo).
These sequences suppress the CSF signal, and
they produce images that are very heavily T2- weighted. This makes FLAIR particularly useful in identifying lesions on the surface of the hemispheres (and overlying subarachnoid spaces), within the basal subarachnoid cis- terns, around the brainstem and at the grey- white matter junction. On the basis of these characteristics it is usually possible to detect SAH. SAH presents as high signal areas on FLAIR images and any associated intraven- tricular haemorrhage is also clearly visible.
FLAIR is also useful in detecting acute SAH in the posterior fossa, which is difficult to study using CT due to the presence of scat- ter artefacts. FLAIR images have been shown to visualize SAH up to 45 days beyond the acute episode.
In the same manner as that mentioned in the preceding section on intraparenchymal collec- tions, MRI can play an important role in the early recognition of the vascular pathology re- sponsible for the SAH.
Closing comments
Given the numerous variables linked to MRI, CT remains the examination of choice in acute phase SAH diagnosis (12). However, in the subacute and chronic phases, the de- creasing sensitivity of CT corresponds with increasing sensitivity of MRI for haemoglobin breakdown products; in particular, chronic leptomeningeal haemosiderin deposits can be recognized even years after bleeding (superfi- cial siderosis).
And, MRI can play an important role in the
early recognition of the vascular pathology re-
sponsible for the bleed. The continuous
progress made in MR angiography has recently
led to a greater diagnostic reliability. In certain
cases, MR angiographic examinations are cur-
rently being proposed as the only presurgical
vascular evaluation in aneurysms responsible
for SAH. However, more experience and fur-
ther technical progress in MRI are required be-
fore it becomes a routine procedure in order to
prove the validity and efficacy of the method in
this area of diagnosis.
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