Spinal Infarcts 251 17 Spinal Infarcts

Michael Mull and Armin Thron

CONTENTS spatial and contrast resolution, MRI can show cir- cumscribed regions of ischemic affec- 17.1 Introduction 251 tion. Moreover, the demonstration of blood vessels 17.2 Vascular Anatomy of the Spinal Cord 251 17.2.1 Arterial Supply 251 in and around the spinal cord based on MRI has 17.2.2 Venous Drainage 254 substantially improved recently. Nevertheless, the 17.3 Causes and Symptoms of Spinal Cord 255 spinal arterial system is seldom examined in detail 17.3.1 Pathogenetic Principles 255 by spinal digital subtraction (DSA) 17.3.2 Clinical Aspects 256 during life resulting in a limited understanding 17.4 MR Imaging in Spinal Infarcts 257 17.4.1 Imaging Principles and Differential Diagnoses 257 and fragmentary knowledge of the vascular basis 17.4.2 MR Correlates of Acute Vascular Myelomalacia 258 of spinal circulatory disorders. Our knowledge of 17.4.3 MR Correlates of the spinal cord vascularization remains based on Subacute/Chronic Vascular 261 anatomical and microradiographic studies. 17.4.3.1 Spinal Dural Arteriovenous Fistula 261 The main purpose of this chapter is to define the 17.4.3.2 Arteriovenous Malformations 262 17.5 Spinal Angiography 263 impact of MRI on the diagnosis of vascular diseases 17.5.1 MR Angiography and Spinal Cord Vessels 263 of the spinal cord. 17.5.2 Spinal Angiography (DSA) 264 17.6 Treatment 264 17.7 Summary 265 References 265 17.2 Vascular Anatomy of the Spinal Cord 17.1 Introduction To interpret MR findings in spinal cord ischemia, it is necessary to be aware of the normal arterial The clinical diagnosis of spinal cord ischemia supply and venous drainage of the spine and spinal remains difficult and is mainly based on magnetic cord. Lesion patterns and concomitant signs such resonance imaging (MRI). In the last decade MRI as vertebral body highly depend on the has become the imaging modality of first choice in underlying vascular pathology. Anatomical and confirming the diagnosis of spinal vascular diseases. microangiographic examinations remain the main Spinal cord ischemia is a rare disease accounting basis of our understanding in this field (Kadyi 1889; only for 1%–2% of all vascular neurological patholo- Thron 1988). gies. In contrast to the cerebrovascular system, the arteries directly supplying the spinal cord are not significantly affected by atherosclerotic vessel wall 17.2.1 changes. Even in the first descriptions of the ante- Arterial Supply rior spinal artery syndrome by Preobraschenski (1904) and Spiller (1909), the central arteries were Segmental arteries supply the spine with blood, affected in cases of luetic arteritis. With increasing including the vertebral bodies, paraspinal muscles, dura, nerve roots, and spinal cord. All these tissues, with the exception of the spinal cord, receive their M. Mull, MD blood supply from segmental arteries (one on each A. Thron, MD Department of Neuroradiology, Clinic for Diagnostic side) or their equivalents. In particular, the segmen- Radiology, University Hospital of the Technical University, tal supply of the thoracolumbar region is derived Pauwelsstr. 30, 52074 Aachen, Germany from intercostal and lumbar arteries arising from 252 M. Mull and A. Thron

the (Fig. 17.1). Sources of blood supply in the central arteries, which derive from the segmental cervical and upper thoracic regions are longitudinal and radicular arteries. arteries following intrauterine vascular rearrange- A spinal radicular branch is present at every seg- ments. In this region the vertebral artery, the deep mental level. The number of spinal radicular arteries cervical artery, and the ascending cervical artery that supply as radiculomedullary arteries the spinal give rise to feeders supplying the spinal cord. In cord, is restricted. They follow the anterior and pos- the sacral and lower lumbar region, sacral arteries terior nerve roots. When they reach the anterior or and iliolumbar arteries arise from the internal iliac posterior surface of the spinal cord, they form the arteries and supply the caudal spine. anterior or posterior spinal arteries. Thus, the arte- The radicular arteries are the first branches of rial supply of the entire spinal cord depends on a the dorsal division of the segmental arteries and single anterior spinal artery system and paired pos- their regional equivalents. The blood supply of the terior spinal arteries. The number of anterior radic- bony spine consists of arteries, which come directly ulomedullary arteries ranges from 2 to 17. The larg- off the segmental and radicular arteries. Anterior est ventral radiculomedullary artery which supplies central arteries derive from the segmental artery the thoracolumbar cord enlargement is the arteria and supply the anterior and anterolateral portions radicularis magna of Adamkiewicz (Fig. 17.2). In of the vertebral body. The radicular arteries usually this region large posterior radiculo-pial arteries provide the blood supply to the posterior portion of are also frequently found and form an anastomotic the vertebral body via posterior central arteries and circle around the conus medullaris (arcade of the the arch via prelaminar arteries. Thus, the vertebral conus; Kadyi 1889). The highest density of central body is mainly supplied by posterior and anterior arteries can be found here in microangiograms

Fig. 17.1a,b. Contrast-enhanced spinal MR angiogra- phy, sagittal views. a First phase: the segmental arteries are visible (arrowhead), note the bright enhancement of the aorta. b Second phase: the accompanying arise (arrow)

a b Spinal Infarcts 253

median anastomotic trunc (anterior spinal artery) is 1 mm. The radicular arteries (< 0.4 mm) that run with the posterior nerve root, supply the posterior and posterolateral longitudinal arteries. Their size totals 0.1–0.2 mm, which is beyond the present spa- tial resolution of MR scanners. Together with trans- verse interconnections, these discontinuous trunks supply the network of pial arteries called the “vaso- corona” (Lasjaunias et al. 2001; Thron 1988). The normal intrinsic arteries of the spinal cord are also too small (<0.2 mm) to be detected on CT or MR images. The spinal cord is protected against ischemia by b extra- and intradural longitudinal and transverse Fig. 17.2. a Superfi cial arteries of the spinal cord. X-ray anastomoses. Extradural longitudinal and trans- fi lm of an injected specimen in a.p. view. The anterior verse interconnections between segmental arteries spinal artery system is visible on the ventral surface of can compensate for a focal vessel occlusion at the the cord. b Intrinsic spinal cord arteries. X-ray micro- level of the radicular artery (Fig. 17.3). The anterior angiogram of a transverse section (lumbar enlarge- and posterior spinal arteries represent a system of ment). The sulcal or central artery within the ante- rior fi ssure (arrow) is dominant. Note the posterior longitudinal anastomoses that is reinforced from and posterolateral spinal arteries at both sides of the various segmental levels. The intrinsic anastomotic posterior root entry zone (arrowheads). ASA, anterior system is supplemented by secondary longitudinal spinal artery connections between central arteries and by the pial network of the vasocorona. This specific vascular supply explains why spinal are highly variable, and distinct, predictable vascular territo- ries as present in the brain do not exist (Fig. 17.4). Moreover, the normal arterial vascular system of the spinal cord is not detectable in MRI.

a

reflecting the metabolic demand of the thoracolum- bar enlargement. Those spinal radicular arteries that are radiculo- medullary arteries, supplying nerve root, pial plexus and medulla, branch in a very typical way to form the anterior spinal artery. The ascending branch contin- ues the direction of the radicular artery in the mid- Fig. 17.3. Selective spinal DSA in a 59-year-old woman, p.a. line of the anterior surface. The descending branch, projection. Injection of the 12th left thoracic segmental artery. being the larger one at thoracolumbar levels, forms Filling of the radiculomedullary arteries T12 and T10 on the a hairpin curve as soon as it reaches the midline at left side (arrows) and the anterior spinal artery system. Collat- eral fi lling of the right-sided segmental arteries via retrocorpo- the entrance of the anterior fissure (Fig. 17.3). The ral anastomoses (arrowheads). These extradural anastomoses artery runs above the . The maximum diameter can compensate for focal vessel occlusions at the level of the of a spinal radiculomedullary artery or the anterior radicular artery 254 M. Mull and A. Thron

Fig. 17.4. Axial T2-weighted images in four patients with acute ischemic myelo- malacia of the spinal cord. The hyperin- tense infarctions refl ect different lesion patterns depending on occlusion site and collateral supply

17.2.2 Venous Drainage

Blood from radial veins of the spinal cord paren- chyma and from the small superficial pial veins is collected in two large vessels, the anterior and pos- terior median spinal veins. The anterior median spinal vein accompanies the artery and can be dis- tinguished by its larger diameter. Posterior, the superficial vein is the only midline vessel, as the arteries run in a more lateral position (Fig. 17.5). The transparenchymal anastomoses take a typi- cal course around the central canal and show up- and downward movements in the sagittal plane. They can be seen on MRI. This is also true for the veins of the thoracolumbar enlargement that are the largest vessels of the spinal cord. The transi- tion of a median vein into a radicular vein shows the same hairpin shape like the artery. The super- ficial venous trunks drain into the epidural venous plexus via radicular veins. The number of radicu- lar veins draining the spinal cord is only six to eleven for the anterior and five to ten for the pos- terior systems (Kadyi 1889, Suh and Alexander 1939). The radicular veins reach the inner extra- dural vertebral venous plexus. Drainage of blood from the spine occurs through the internal and external venous vertebral plexus and extends from Fig. 17.5. Normal anterior and posterior median spinal veins of the thoracolumbar cord. Sagittal contrast-enhanced T1- the sacrum to the base of the skull. This system weighted MR images (right side, subtraction image). The is valveless and connected with the azygos and large anterior median vein (arrows) continues with the fi lum hemiazygos venous systems. terminale Spinal Infarcts 255

17.3 (Gravereaux 2001; Mawad et al. 1990; Mikulis Causes and Symptoms of et al. 1992; Naiman et al. 1961; Rosenkranz et al. Spinal Cord Ischemia 2004; Toro et al. 1994; Tosi et al. 1996; Weidauer et al. 2002). 17.3.1 Cartilaginous disc embolism, first described by Pathogenetic Principles Naiman and colleagues in 1961, is meanwhile a widely accepted cause of acute spinal cord ischemia Compared with brain ischemia spinal cord mainly based on postmortem findings (Mikulis are caused by more diverse etiologies. Up-to-now et al. 1992; Toro et al. 1994). Most reported post- there is no satisfactory and accepted classification mortem cases are cervical, but conus medullaris of spinal infarcts. Etiologies include circulatory infarctions are also reported. The exact mechanism arterial and venous disorders. From a clinical and of disc embolism remains unclear and speculative. pathoanatomical point of view it seems reasonable An increased intraosseous pressure within the ver- to differentiate between acute ischemic myeloma- tebral body, due to acute vertical disc herniations lacia and subacute to chronic vascular myelopathy – often after axial trauma – may explain the initial (Table 17.1). In most cases MRI enables the differ- step in a process which ends up in spinal cord isch- entiation of these two main etiologies. A deficient emia (Tosi et al. 1996). In the clinical course of the spinal arterial blood flow generally has various histologically established cases of fibrocartilagi- causes, ranging from the occlusion of intercostal or nous embolism three main characteristics could be lumbar arteries to affection of the intrinsic arteries identified: (1) the sudden severe pain at onset, (2) of the spinal cord . the free interval of neurological signs and symptoms Many causes of acute spinal cord infarction (of (“spinal in progress”), (3) no improvement of arterial and venous origin) have been reported the neurological deficit. In our experience, there is (Table 17.2). They include diseases of the aorta and a surprisingly high rate of disc herniations in close aortic , thromboembolic events and carti- proximity to the vascular lesions of the cord (Mull laginous disc embolism, vasculitis, coagulopathy, et al. 1992). Intravital confirmation of this pathoge- radiation-induced vasculopathy, toxic effects of netic mechanism is difficult. Nevertheless it may be contrast medium, epidural anesthesia, periradicu- that the pathogenetic role of disc material has yet lar nerve root therapy with crystalline corticoids, not been fully realized. decompression illness, shock or cardiac arrest, In contrast to disc embolism, most patients with lumbar artery compression and other etiologies thrombotic or embolic infarctions show at least par- tial recovery in the further course of the disease. Nevertheless, depending on the efforts in diagnos- Table 17.1. Disorders resulting in primary vascular tic work-up, the cause of spinal cord ischemia often myelopathy remains undefined or speculative. • Acute vascular myelomalacia Lumbar artery compression by the diaphragmatic Acute ischemic myelomalacia of arterial and crus has been described as a new etiology for spinal venous origin Rogopoulos • Subacute/chronic vascular myelopathy cord ischemia ( et al. 2000). A pro- Dural AV fi stula longed hyperlordotic position may play a predispos- AVM of the perimedullary fi stula type ing role in this new syndrome. The 1st right and left (AVM of the glomerular type) and the 2nd right lumbar arteries course through an osteotendinous passage between the vertebral body and the diaphragmatic crus. If spinal cord supply- Table 17.2. Causes of acute spinal cord infarction ing arteries arise at the level of the first and second • Surgery for aortoiliac occlusive disease lumbar artery, compromise of the spinal cord arte- • Dissection of the aorta rial supply can result in spinal cord ischemia. • /embolism Suh and Alexander (1939) and later Zülch • Vasculitis • Cardiac arrest and systemic hypotension (1954, 1976) postulated their traditional hypothesis • Fibrocartilaginous embolism of a watershed zone of increased ischemic vulner- • Caisson disease ability near T4. This model was based on the relative • Lumbar artery compression hypovascularity of this region. • Spinal tumor Cheshire et al. (1996) described 44 patients with • Spinal AVM/SDAVF spinal cord infarctions. Surprisingly, the mean sen- 256 M. Mull and A. Thron sory level of the deficits was observed at T8 and T9 vein is reversed and directed to the perimedullary in cases of global ischemia. A review of the clinical veins. The dural shunt is supplied by radiculomen- literature by Cheshire and colleagues (1996) sug- ingeal arteries which normally supply the segmen- gests that the most commonly sensory level found tal nerve roots and dura. They arise from the seg- after spinal cord infarction is centered at T12. mental vessels that persist as intercostal or lumbar Duggal and Lach (2002) analyzed clinical files arteries in the thoracolumbar region. Depending on and neuropathologic specimen in 145 patients with the location of the fistula, the supply may also come well-documented cardiac arrest or severe hypoten- from the sacral or hypogastric arteries (Burguet sion. In this group ischemic myelopathy was found et al. 1985; Heindel et al. 1975; Larsen et al. 1995; in 46% of patients dying after either cardiac arrest Partington et al. 1992; Reinges et al. 2001; Stein or a severe hypotensive episode. Among the patients et al. 1972). In addition, intracranial dural fistulas with myelopathy, predominant involvement of have been described to drain to spinal cord veins the lumbosacral level with relative sparing of tho- and evoke the same symptoms as spinal dural fistu- racic levels was observed in 95% of cardiac arrest las. The cause of the fistulas is unknown so far. and hypotensive patients. None of the examined Functional disturbances within the spinal cord patients developed neuronal limited to the are caused by the venous congestion due to arteriali- thoracic level only. These findings indicate a greater zation and elevated pressure of the medullary veins vulnerability of neurons in the lumbar or lumbosa- (Aminoff et al. 1974). In addition, venous outlets cral spinal cord to ischemia than other levels of the are insufficient and thus reinforcing impairment of spinal cord (Duggal and Lach 2002). the venous circulation and chronic spinal hypoxia. Moreover, analysis of data coming from greater In particular, Merland and coworkers (1980) intro- MR series and our own observations reveal no pre- duced the concept of blocked venous drainage into dominance of infarcts in the upper and mid-thoracic the epidural space. region (Mawad et al. 1990; Weidauer et al. 2002). Thus, the concept of a vulnerable watershed zone at T4 is no longer valid in acute spinal cord ischemia. 17.3.2 Subacute or chronic vascular myelopathy is the Clinical Aspects result of disturbances of microcirculation caused by compromised venous outflow or small-vessel dis- Vascular diseases of the spinal cord are character- ease. ized by transverse cord symptoms and can be differ- Thus, acute, subacute, or chronic impairment of entiated by their clinical features and course. Neu- spinal blood supply can result from a deficient arte- rologic deficits and imaging findings depend on the rial supply and from venous circulatory problems level and extent of spinal cord damage. Acute isch- (Mull and Thron 2004). Spinal vascular malforma- emic myelomalacia has an acute onset and pain is a tions like spinal dural arteriovenous (AV) fistulas common initial complaint. Symptoms may include and AV malformations (AVM) of the perimedullary nerve root deficits or sphincter weakness (Mull and fistula type are the typical disorders associated with Thron 1999). But typical clinical syndromes (i.e., venous congestion of the spinal cord. On the other anterior spinal artery syndrome) are exceptional hand, AVM of the glomerular type are seldom com- presentations in clinical practice. A spinal hemor- bined with a venous outflow disorder. rhage presents with peracute signs and symptoms Spinal dural arteriovenous fistulas (SDAVF) are and always requires prompt diagnostic investiga- the most frequent (acquired) AVM of the spinal canal tion, if necessary on an emergency basis. and its meninges. In 1977 Kendall and Logue were In most cases congestive myelopathy takes a the first to recognize that this disease, which had subacute to chronic course, although acute wors- formerly been described as so-called retromedullary ening may be observed. SDAVF is the prototype of angiomas, in fact is an AV fistula situated within the a congestive myelopathy. The symptoms in SDAVF dura mater. This was confirmed by Merland et al. are slowly progressive and consist of sensory loss in 1980 who pointed out the angiographic character- and paraparesis both of which reflect the extent of istics of the disease in detail (Fig. 17.6). the cord involvement. They are independent of the The AV shunt is located inside the dura mater close location of the fistula (Koenig et al. 1989). An acute to the spinal nerve roots. The arterial blood enters a onset of the disease (11%) or a progressive develop- radicular vein where it passes the dura (Thron et ment interrupted by intermediate remissions (11%) al. 1987; Hassler et al. 1989). Flow in the radicular are the rare forms (Symon et al. 1984). Almost all Spinal Infarcts 257

ab c

Fig. 17.6a–c. Thoracic SDAVF in a 50-year-old man with chronic progressive paraparesis due to congestive myelopathy. a Sagit- tal T2-weighted MRI. The hyperintense lesion (long arrows) involves the thoracic cord indicating vascular damage. b Dilated perimedullary veins are detectable in the thoracic region (right image, arrows) after paramagnetic contrast application (T1- weighted MRI). c DSA, p.a. projection. Selective contrast injection in the 4th left-sided intercostal artery shows the dural AV fi stula (arrowhead) draining slowly in the caudal direction patients have additional sphincter disturbances at MRI is the diagnostic modality of choice, T1- the time of diagnosis. The disease affects men more and T2-weighted images are obligatory. Strongly often than women, most of them being in the middle T2-weighted images (e.g., a CISS sequence) may or older age group. In some cases a relapsing and help to detect pathologic vessels within the bright remitting course of the disease can be observed. . Sagittal and transverse images The symptomatology in SDAVF can cause confusion are more important than coronal views. Fat can be with other disorders like polyneuropathy, spinal ste- suppressed by spectral fat saturation or by using nosis, transverse and . the inversion recovery technique. These sequences are essential in acute spinal cord ischemia to detect associated abnormal bone signals indicating ver- tebral body infarction. Fluid-attenuated inversion 17.4 recovery (FLAIR) sequences suppress signals from MR Imaging in Spinal Infarcts cerebrospinal fluid and, therefore, help to detect intraspinal hemorrhage. Contrast-enhanced T1- 17.4.1 weighted images can reveal abnormal intraspinal Imaging Principles and Differential Diagnoses vessels. Acute spinal cord ischemia is character- ized by a typical time-dependent pattern of contrast The imaging work-up should be guided by a clinical enhancement. MRI can directly depict the cause of assessment of the lesion level. spinal cord ischemia in dissecting aneurysms of the 258 M. Mull and A. Thron aorta. The use of diffusion-weighted MRI (DWI) 17.4.2 has been limited in the spine thus far due to very MR Correlates of Acute Vascular Myelomalacia strong susceptibility artefacts. Nevertheless, diffu- sion imaging has been successfully applied also to Ischemic infarction of the spinal cord is difficult to spinal cord ischemia (Gass et al. 2000). MRI can establish in the early phase, only 50% of the patients directly detect ischemic spinal cord lesions as well as show early demarcation within 24 h. The role of MRI intramedullary, subdural, or epidural hemorrhage. in the acute phase is to exclude hematomyelia, spinal Myelitis and tumor-associated lesions are the most vascular malformation (which requires spinal angi- important clinical and imaging differential diagno- ography in special cases) or a compressive lesion. ses in acute spinal cord ischemia (Table 17.3). CSF Common sites of spinal cord infarction are the examinations are necessary if inflammatory lesions thoracolumbar enlargement and the conus medul- of the spinal cord () and multiple laris in 65%, the cervical region is less commonly sclerosis have to be excluded in the acute phase (de affected (only 11% in our own series). The damage of Seze et al. 2001). the spinal cord is most accurately demonstrated by MRI in T2-weighted sequences (Brown et al. 1989). Table 17.3. Differential diagnosis in acute Hyperintensity in T2-weighted images may be dem- non-traumatic transverse lesion onstrated as early as 8 h after onset (Yuh et al. 1992). • Hematomyelia In most cases pencil-shaped hyperintensive lesions • Multiple sclerosis are visible predominantly in the anterior spinal • artery system at least in follow-up examinations

– (Fig. 17.7). Circumscribed infarctions in the poste- – Disc herniation Mascalchi – Sub-/epidural rior spinal artery system are rare ( et al. • Abscess/empyema 1998). Moderate swelling is generally present in the • Delayed radiation myelopathy acute stage followed by contrast enhancement of the • Acute transverse myelitis cord and the cauda equina in the subacute stage – • Spinal AVM usually after 5 days (Amano et al. 1998; Casselman • Ischemic infarction et al. 1991; Friedman and Flanders 1992). Con-

In the presence of an intraspinal hemorrhage spinal vascular malformation, cavernoma, coagu- lopathy and tumor have to be differentiated. In spinal vascular malformations abnormally thick, often tortuous vessels on the surface of the spinal cord can be identified as well as the angioma- like nidus of the AVM. MRI facilitates the differen- tiation between SDAVF and intramedullary AVM. and post-myelographic computed tomography should only follow MRI if there is a high clinical index of suspicion for a SDAVF. Myelogra- phy is more sensitive than MRI to detect pathologic perimedullary vessels especially in cases of low-flow fistulas (Gilbertson et al. 1995). Spinal angiography remains the gold standard in spinal vascular malformations and can help to elucidate the underlying pathology of acute spinal cord ischemia in selected cases (Di Chiro and Wener 1973; Djindjian et al. 1970; Lasjaunias et al. 2001).

Fig. 17.7. Acute ischemic myelomalacia of the thoracolumbar region in two patients, T2-weighted MR images. The pencil- shaped zone of increased signal represents the acute infarcted cord Spinal Infarcts 259 trast-enhanced images demonstrate enhancement of the infarct up to 3 weeks after the onset (Berlit et al. 1992; Hirono et al. 1992; Yuh et al. 1992). In most cases of the thoracolumbar infarction, the swollen cord shows peripheral enhancement of the central gray matter. The concomitant enhancement of the cauda equina was reported first by Friedman and Flanders in 1992 (Fig. 17.8). This phenomenon is a characteristic finding in the course of spinal cord ischemia which might involve the cord itself and the ventral cauda equina as well, which is composed of motor fibre bundles (Amano et al. 1998). It indicates disruption of the blood–cord barrier as well as reac- tive hyperemia (Friedman and Flanders 1992; Amano et al. 1998). The differential diagnosis of contrast enhancement of the cauda equina includes transverse myelitis, bacterial or viral , and spinal metastasis. Abnormal signal or evolution of signal abnormal- ity in a vertebral body associated with a cord lesion is highly suspicious of an acute spinal infarction (Haddad et al. 1996; Yuh et al. 1992). Due to the vascular supply to the vertebral body, the pattern of signal changes is distinct from degenerative disease. The deep medullary portion and the region of the a endplates are most vulnerable to ischemia. Yuh et al. (1992) reported early hyperintensity in T2-weighted images due to vertebral body infarction after 8 h. As described before, the radicular arteries supply the vertebral bodies and – inconsistently – the spinal cord, if there is a radiculomedullary artery at the same level. Abnormal bone signals indicate this special vascular condition and can be regarded as a confirmatory sign in spinal infarction (Faig et al. 1998; Yuh et al. 1992). In our patient group, the spinal angiography demonstrated that infarction of the vertebral body indicated the origin of the ante- rior spinal artery (Fig. 17.9). Bone marrow abnor- malities are also detectable in posterior spinal cord syndrome (Suzuki et al. 2003). In the chronic stage the affected cord segment may shrink. Early detection of the ischemia is desirable with regard to therapeutic implications. In few studies, DWI is reported to detect spinal cord ischemia in the acute phase (Gass et al. 2000; Bammer et al. 2000; Stepper and Lövblad 2001). Küker and coworkers (2004) recently reported the time course of diffusion abnormality in three patients b with acute spinal cord ischemia. They found diffu- Fig. 17.8a,b. Acute ischemic myelomalacia of the lumbar sion abnormality earliest after 8 h. At this time there enlargement 3 weeks after onset of symptoms. Contrast- enhanced T1-weighted images in sagittal and axial orientation was only a faint hyperintensity visible in the central at different levels. a Enhancement of the ventral cauda equina part of the conus medullaris. Diffusion abnormal- (arrow, arrowhead). b Peripheral ring-like enhancement of the ity did not last for longer than 1 week. Further stud- affected lumbar enlargement (arrow, arrowhead) 260 M. Mull and A. Thron

a b

d Fig. 17.9a–d. Acute ischemic myelomalacia in an 18-year-old man with acute and sphincter disturbances. a Sagittal T2-weighted images show centromedullary multisegmental hyperintensities from T2 to the conus (arrows). b Axial T2-weighted images. c On day 2, a fat-suppressed T2-weighted sequence reveals abnormal signal in the dorsal part of the vertebra T12 cor- responding to vertebral body infarction (arrow). d DSA, p.a. projection, 10 days after onset of symptoms. The radiculomedullary artery originates at T12 level and supplies the anterior spinal axis. At this time the anterior spinal artery is patent. The origin of the cord supplying radiculomedullary artery c corresponds well to the level of the vertebral body infarction Spinal Infarcts 261 ies are necessary to determine its sensitivity in the early phase of spinal cord infarction and to establish its specificity in other causes of myelopathy such as myelitis.

17.4.3 MR Correlates of Subacute/Chronic Vascular Myelopathy

17.4.3.1 Spinal Dural Arteriovenous Fistula

In SDAVF the key findings in MRI are the sequelae of the congestive myelopathy and the detection of the arterialized perimedullary veins (Fig. 17.10). MRI shows in almost all cases a long central intramed- ullary hyperintense lesion in T2-weighted images that spans several cord segments (Koch et al. 1998; Van Dijk et al. 2002). A characteristic finding is a hypointense rim adjacent to the spinal cord lesion.

Fig. 17.11. SDAVF supplied from the left 1st lumbar segmental artery, T2-weighted sagittal and axial MR images. In this case, the perimedullary arterialized veins are not very impressive (arrowhead). Note the peripheral hypointensive rim adjacent to the cord hyperintensity, a typical fi nding in SDAVF (arrows)

This peripheral spinal cord hypointensity was first described by Hurst and Grossman in 2000 and is probably best explained by slow flow of blood containing deoxyhemoglobin related to the venous hypertension (Fig. 17.11). Abnormally enlarged and tortuous perimedullary veins can show flow voids in spin-echo sequences or enhancement after paramagnetic contrast administration (Terwey et al. 1989). Pathologic perimedullary veins are not always detectable in MRI and in some cases diffi- cult to differentiate from CSF pulsations. If contrast enhancement of the spinal cord lesion is present, the cord lesion may be misdiagnosed as tumor. Follow-up MRI after treatment shows regression of the hyperintense lesion and may be followed by atro- phy. If swelling of the cord and/or the pathologic peri- Fig. 17.10. MRI in thoracic SDAVF, sagittal T2- and contrast- medullary vessels persist after treatment, a residual enhanced T1-weighted images. Multisegmental hyperintensive SDAVF needs to be excluded by DSA. lesion of the thoracic cord with swelling indicating congestive Spinal DSA is still required to demonstrate the myelopathy. Flow voids in the dorsal CSF compartment repre- sent the arterialized perimedullary veins (arrow, T2-weighted fistula and the supplying segmental artery. Recent image, left side), which are clearly visible after intravenous developments in MR angiography will help to define contrast application (arrow, T1-weighted image, right side). non-invasively the level of the fistula (Farb et al. 262 M. Mull and A. Thron

2002). In most patients the dural fistula is supplied AVMs of the perimedullary fistula type are direct by a thoracic or lumbar artery. Deep located fistulas AV shunts that are located on the ventral or dorsal of the lumbosacral region are rare and beset with surface of the spinal cord or the conus medullaris, particular diagnostic problems mainly due to the usually in the thoracolumbar area, occasionally unusual anatomic and hemodynamic conditions. thoracic, and rarely cervical. Their location thus In these cases MRI should be focused on the lum- is intradural, intra- or extramedullary. They are bosacral region. The arterialized dilated vein of the always supplied by spinal cord vessels, either by the filum can be detected in 3-mm slices after paramag- anterior spinal artery (ventrally) or by a posterolat- netic contrast administration even if the flow is very eral artery (dorsally), depending on their location. slow. They drain into spinal cord veins (Fig. 17.12). Drain- age may even ascend up to the foramen magnum or into the posterior fossa. 17.4.3.2 AVMs of the glomerular type are more frequent Arteriovenous Malformations and characterized by a nidus similar to those of most cerebral AVMs. They may be located superficially on Spinal AVMs can be mainly divided into AVM of the surface of the spinal cord or deep within the cord the perimedullary fistula type and glomerular parenchyma or extend to both compartments. Due type. Typically, congestive myelopathy is obvious in to the numerous anastomoses between the spinal AVM of the perimedullary type (Heros et al. 1986; cord arteries, the nidus is always supplied by sev- Rosenblum et al. 1987; Thron et al. 2001). eral arteries or branches derived from the anterior

b

Fig. 17.12a,b. Perimedullary AVM of the conus medullaris. a Sagittal T2-weighted MR image. The hyperintensive cord lesion spans several segments (arrows). The draining veins are visible in the neighborhood of the cauda equina. b Selective DSA, opacifi ca- tion of the 1st left lumbar segmental artery (left, lateral view; right, p.a. view). The dilated arteria radicularis magna (arrow) is the main feeder of the AVM. The fi stula a zone is visible at the level L1 (arrowhead) Spinal Infarcts 263 or posterior spinal arteries. Spinal AVMs drain into 17.5 the spinal cord veins and are rarely complicated by Spinal Angiography congestive myelopathy. The principal screening method is MRI 17.5.1 (Dormont et al. 1988; Thron and Caplan 2003). MR Angiography and Spinal Cord Vessels Abnormally dilated vessels in the spinal cord or the subarachnoid space are the main findings. In AVMs The largest blood vessels of the spinal cord are the of the glomerular type, the nidus can be differen- veins of the superficial system, the anterior and pos- tiated from the draining veins. Intradural AVMs terior median vein, the radicular veins, the terminal can be associated with hemorrhage in the spinal vein and, furthermore, the transmedullary venous cord and its surroundings. The hyperintensity in anastomoses. They have an inner vessel diameter T2-weighted images is not the dominant feature in of up to 2 mm compared with a maximum diam- this type of AVM. The signal characteristics vary eter of 1 mm on the arterial side. At present, these over time, comparable with intracerebral hemato- are the vessels most likely to be seen on MRI. They mas. After endovascular treatment, compromise can either be demonstrated on sagittal T1-weighted of the venous outflow may result in a congestive images following contrast enhancement as bright myelopathy. structures or, like in myelography, as dark struc- Perimedullary fistulas type 1 may present with tures within the bright CSF on strongly T2-weighted multisegmental hyperintensive cord lesions on images. Problems arise in “borderline” cases, espe- T2-weighted images due to congestive myelopa- cially at the level of the lumbar enlargement, where thy similar to spinal cord affection in spinal dural it is impossible to decide whether the demonstrated AVF. blood vessels represent still normal or already path-

Fig. 17.13a–c. First-pass con- trast-enhanced MR angiography. a Normal fi nding. b Thoracic SDAVF (T7 left, arrow). c Thoraco- abclumbar spinal AVM (arrows) 264 M. Mull and A. Thron ological findings due to a SDAVF. This is particu- in the routine work-up of spinal vascular pathol- larly true for the thoracolumbar enlargement due ogy will contribute to our understanding of the to a considerable variation of the posterior veins at pathogenetic mechanisms involved. this location that can show varicosity and elongation (Thron and Mull 2004). Even if spatial and contrast resolution of these 17.5.2 imaging modalities will increase in the future, it Spinal Angiography (DSA) might be difficult to differentiate the artery from the vein on the anterior surface of the cord. The ante- Selective spinal angiography provides the basis for rior spinal artery and vein run very close together. classifying spinal vascular malformations by their The branching of a radicular artery or vein has a location, arterial supply and venous drainage pat- very similar hairpin-configuration, and the level at tern. A profound understanding of the AVM archi- which a segmental in- or outflow occurs cannot be tecture is required for the decision regarding which predicted in a given case. treatment option(s) should be taken into consid- The only non-invasive way in which a reliable eration. In SDAVF, spinal DSA remains the gold differentiation of superficial spinal cord arteries standard to identify the fistula-supplying segmen- and veins can be expected, is an MR-based angio- tal artery. In deep lumbosacral SDAVF, only selec- graphic technique with sufficient spatial resolu- tive internal iliac arteriography can identify fistulas tion and with a time resolution that clearly sepa- located in the sacral region supplied by the lateral rates arterial and venous phase. The first MRA sacral or iliolumbar arteries. techniques used were blood flow-dependent, such Selective spinal DSA has a better spatial resolu- as three-dimensional phase contrast angiography tion and plays a main role in the exclusion of spinal and three-dimensional contrast-enhanced time vascular malformations. In selected cases affection of flight imaging (Bowen et al. 1996). The great- of the radicular artery and occlusion of the ante- est disadvantages are the long acquisition time rior spinal artery system can be demonstrated as (10 min) and the limited visualization of normal well as collateral supply even in the later course of intradural arteries. To achieve better visualiza- the ischemia (Mull et al. 2002). Thus, spinal DSA tion without venous overprojection, first-pass MR helps to identify pathologic vascular conditions in angiography with a rapid bolus injection of con- spinal cord ischemia. The main indication remains trast medium and a highly sophisticated acqui- to exclude a spinal vascular malformation. Angio- sition technique, has been proposed (Willinek graphic information about the acute phase of spinal et al. 2002). This technique makes it possible to cord ischemia is not yet available. distinguish the arterial phase from a later phase in which both arteries and veins are enhanced. Verification of the findings by DSA has rarely been performed. Some authors have shown that 17.6 the fistula-supplying segmental artery could be Treatment located by first-pass contrast-enhanced MR angi- ography (Binkert et al. 1999; Farb et al. 2002; In patients with SDAVF the aim of treatment is to Shigematsu et al. 2000). By using a first-pass prevent progression of the spinal cord damage. The technique with two dynamic phases, the arteria goal is the permanent occlusion of the dural shunt radicularis magna of Adamkiewicz could be sep- zone along with the origin of the draining vein. This arated from the anterior median vein and sepa- can be achieved microsurgically or by endovascu- rately visualized in 69% (Yamada et al. 2000a,b). lar treatment using tissue adhesives (Behrens and Recent own investigations comparing MR angi- Thron 1999; Huffmann et al. 1995; Merland et al. ography with DSA findings are encouraging with 1986; Niimi et al. 1997; Song et al. 2001; Thron and regard to the identification of the Adamkiewicz Caplan 2003). Treatment of spinal AVM should be artery and the fistula-supplying segmental artery restricted to specialized centers that are experienced in SDAVF (Backes et al. 2004). Nevertheless, to in this field. date, MRI and MR angiography have not been able To identify the location of cord-supplying seg- to precisely detect small-caliber feeding spinal mental arteries before aortic surgery can help to arteries in spinal AVM (Fig. 17.13). Introduction reduce the risk of spinal cord ischemia. Monitor- of first-pass contrast-enhanced MR angiography ing of somatosensory-evoked responses contrib- Spinal Infarcts 265 utes to identify early signs of spinal cord ischemia References during aortic clamping. Before aortic surgery spinal DSA and MR angiography, as described Amano Y, Machida T, Kumazaki T (1998) Spinal cord infarcts before, can help to identify cord-supplying seg- with contrast enhancement of the cauda equina: two cases. Neuroradiology 40:669–672 mental arteries. Aminoff MJ, Barnard RO, Logue V (1974) The pathophysiology If the diagnosis of a compression of a lumbar of spinal vascular malformations. J Neurol Sci 23:255–263 artery has been established by dynamic spinal DSA Backes W, Nijenhuis R, Mull M, Thron A, Wilmink J (2004) showing complete occlusion of the lumbar artery, Contrast-Enhanced MR Angiography of the Spinal Arter- surgical section of the diaphragmatic crus may ies: Current Possibilities and Limitations. Rivista di Neuro- radiologia 17 (3):282–291 prevent irreversible infarction in this rare condi- Bammer R, Fazekas F, Augustin M, Simbrunner J, Strasser- tion. Fuchs S, Seifert T, Stollberger R, and Hartung HP (2000) At present there are no recognized effective Diffusion-weighted MR imaging of the spinal cord. AJNR treatment strategies for spinal cord stroke (Caplan Am J Neuroradiol 21 (3):587–591 2003; Mull 2005). Nevertheless, if the cord isch- Behrens S, Thron A (1999) Long-term follow-up and outcome in patients treated for spinal dural arteriovenous fistula. 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