Applied Radiology

Dr. Basak is a Neuroradiologist at Robert Wood Johnson University Hospital, New Brunswick, NJ. Dr. Klufas is an Instructor of Radiology at Harvard Medical School and a Neuroradiologist at Brigham and Women's Hospital, Boston, MA. Dr. Hsu is an Assistant Professor of Radiology at Harvard Medical School and a Neuroradiologist at Brigham and Women's Hospital.

Magnetic resonance imaging (MRI) of the cervical spine is a commonly performed study for evaluation of cervical pain, radiculopathy, and myelopathy. Recognition of less common non-neoplastic disease processes is essential in order to diagnose and properly treat these entities.

Subacute combined degeneration of the cervical spinal cord

Cobalamin or vitamin B12 is an organometallic compound not produced by the human body but is incorporated, instead, into the diet via meat and dairy products. It is bound in the duodenum to intrinsic factor (IF). This cobalamin-IF complex is resistant to proteolysis and is absorbed into the blood stream as it makes its journey to the distal small bowel. ¹ This route of B12 intake is adequate for everyone except for strict vegetarians and their breastfed children. Pernicious anemia is the most common cause of cobalamin deficiency in temperate climates. Other conditions leading to cobalamin deficiency include malabsorption states, ileal resection, massive bacterial colonization of the intestines, and tropical sprue. ¹

Cobalamin deficiency affects not only the blood (megaloblastic anemia) and gastrointestinal tract, but also the nervous system, where it can result in subacute combined degeneration (SCD). The peri-pheral nerves, spinal cord, and cerebrum may also be involved. ¹ In the spinal cord, involvement of the dorsal columns, lateral corticospinal tracts, and, occasionally, the lateral spinothalamic tracts leads to signs and symptoms, such as hand and feet paresthesia, numbness, sensory loss, gait ataxia, and mainly distal lower extremity weakness. If untreated, ataxic paraplegia may develop. ^1,2

Histologically, multifocal demyelination and vacuolization may be found in the posterior, lateral, and, occasionally, anterior columns. ³ Axonal degeneration and, ultimately, axonal death is characteristic. ¹ The progression of demyelination is often from dorsal columns to lateral columns, with subsequent Wallerian degeneration. Cervical and thoracic cord lesions are typical, and the medulla may also be affected. ³

MR imaging of SCD includes expansion of the affected cervical and thoracic cord segments with T2 prolongation, mainly of the dorsal columns and, occasionally, slight enhancement after gadolinium administration ^4,5 (Figure 1). Lateral column involvement on MR imaging is usually not apparent, even though signs and symptoms may be attributable to these tracts. ⁶ Within the brain, multiple confluent areas of white matter T2 prolongation are seen. The differential diagnoses of an intramedullary lesion exhibiting non-
specific characteristics similar to SCD include infectious (herpes virus, HIV vacuolar myelopathy), inflammatory (sarcoid), demyelinating (multiple sclerosis), ischemic, and, to a lesser degree, neoplastic processes (astrocytomas and ependymomas). ⁷ The main findings indicating the diagnosis of SCD are the clinical picture and the dorsal signal abnormality.

Treatment for cobalamin deficiency is intramuscular cyanocobalamin administration and management of any underlying disorder. Although patients show excellent response to treatment with regard to the hematologic manifestations, neurological symptoms may remain refractory. ¹ Early treatment initiation may lead to clinical improvement in myelopathic symptoms with an accompanying decrease in dorsal spinal cord T2 prolongation. ⁷ Early diagnosis is critical, as clinical improvement of SCD is inversely proportional to its duration and severity. ^2,4

Arteriovenous malformations/fistulas of the cervical spinal cord

The nomenclature of spinal vascular lesions has evolved with better understanding of lesional angioarchitecture.
For our discussion, the classification system proposed by Anson and Spetzler ⁸ will be used as follows: type I­­ dural arteriovenous fistulas (DAVFs), type II and III­­intramedullary arteriovenous malformations (AVMs), and type IV­­intradural/extramedullary (peri-medullary) spinal AVMs. Since a discussion of all four types of vascular ab-normalities would be beyond the scope of this text, only type I lesions will be discussed in the context of the cervical spine.

The most common lesions are type I lesions, which comprise up to 80% of all spinal AVMs, and are thought to be secondary and acquired. They are 4 times more common in men, usually between 40 and 70 years of age, and are often found in the lower thoracic or upper lumbar region. The angioarchitecture of these lesions is composed of a radicular artery branch that communicates with an intradural medullary vein via a fistula at the dural root sleeve. This medullary vein then drains cephalad into serpiginous dilated pial veins of the spinal cord. This results in chronic arterialization of veins, leading to elevated pressures and venous engorgement that produce changes in spinal cord parenchyma. Ultimately, there is a decrease in tissue perfusion and a resultant hypoxia due to transmission of these elevated venous pressures to intrinsic spinal cord veins. ^9,10

With time, this progressive spinal venous hypertension manifests clinically as a distinctive chronic myelopathy with progressive weakness and sensory deficits. ^9,11 The most common symptom is progressive lower extremity weakness without upper extremity involvement. Other manifestations also include back pain, sensory deficits, and bowel and bladder dysfunction. Delayed diagnosis is not uncommon, as there is usually a slow progression of symptoms over a 2- to 3-year period. ⁹ The so-called Foix-Alajouanine syndrome or subacute necrotic myelopathy, an eponym associated with type I lesions, is the result of chronic venous ischemia that could potentially lead to cord infarction. ^9,10

Radiographically, prone myelography demonstrates tortuous vessels and cauda equina beading. It is a sensitive test, though not as specific as MRI, which can show cord enlargement, central cord T2 prolongation, dorsal serpentine flow voids (more specific), and dilated vein enhancement ^9-11 (Figure 2). Ill-defined and patchy enhancement of the affected portion of the spinal cord is not uncommon. Nevertheless, catheter-based spinal angiography remains the gold standard for the diagnosis of spinal AVM. ⁹

For the cervical spine, type I lesions are rare, ^12-15 and cervical DAVFs can manifest as a progressive myelopathy, similar to those in the thoracolumbar spine. Interestingly, unlike those in the thoracolumbar region, cervical DAVFs present more often with hemorrhage, such as subarachnoid hemorrhage (SAH) at the craniocervical junction. ^12,16 The angioarchitecture of cervical DAVF can take one of three forms. First, as in the thoracolumbar spine, the feeding radicular artery may drain into a medullary vein along the length of the cervical spinal cord, usually dorsally, and present with myelopathy ^10,13 (Figure 2). Interestingly, the signal abnormality from a cervical DAVF tends not to involve the medulla. ¹⁷

Another pattern is that the DAVFs can decompress entirely into the intracranial venous system and thus decrease venous hypertension in the cervical cord. These patients may not present with myelopathy but with SAH because of intracranial venous enlargement. Alternatively, patients who drain caudally into a medullary vein would be more likely to present with myelopathy than with SAH. ¹⁶

The third scenario involves an intracranial DAVF that produces cervical myelopathy. An intracranial DAVF can drain into spinal veins and produce symptoms secondary to venous hypertension, similar to DAVFs in the thoracolumbar spine. ¹⁰ These lesions can manifest as intracranial hemorrhage, ischemia/infarction, mass effect from enlarged veins, increased intracranial pressure, and cranial neuropathies. T2 prolongation within the cervical cord and medulla, cord enlargement, and flow voids dorsal and ventral to the cervical cord are typical MRI findings. ¹⁷

The initial method of treatment of symptomatic type I DAVFs is primarily endovascular with successful >80% of cases. Permanent liquid agents, such as N-butylcyanoacrylate, are preferred as particulate embolic material results in almost 100% recanalization. If endovascular treatment is unsuccessful or contraindicated, surgical removal of the nidus is usually a safe alternative. ⁹

Cavernous malformations of the cervical spinal cord

The overall incidence of cavernous malformations (CMs) is approximately 4%, ¹⁸ and the spinal cord harbors approximately 3% to 5% of CMs. ¹⁹ They are discrete masses consisting of endothelial-lined sinusoidal vascular channels without intervening neuronal tissue. Cavernous malformations are congenital lesions with a peak incidence in the third and fifth decades. Interestingly, although intracranial lesions show equal male and female predominance, spinal cord CMs are more common in females ¹⁸ and are usually intra-medullary. ¹⁰ Clinically, CMs can present with a wide range of symptoms. Acute symptoms are often secondary to hemorrhage, while a progressive course may be due to microhemorrhages. ¹⁰

Treatment of CMs in the spinal cord depends on the symptoms and age of the patient. Asymptomatic lesions are usually left alone while symptomatic ones can be explored surgically because of the threat of future hemorrhage and resultant neurologic decline. ¹⁰ One study proposes a hemorrhage rate for spinal CMs of 1.6% per year. ²⁰

MRI is the study of choice for imaging for CMs, as arteriovenous (AV) shunting is not characteristic and, thus, remains occult on conventional arteriography. Intracranial and spinal-cord CMs have similar MRI features that classically include central signal heterogeneity (reflecting various stages of blood products) surrounded by a peripheral dark hemosiderin ring without significant edema, mass effect, vascular flow voids, or enhancement (Figure 3). On gradient-recalled images, CMs bloom secondary to blood products within the lesion. On CT, CMs often show focal high attenuation with or without associated calcifications. ^10,18

Cervical spine manifestations of intracranial hypotension

The clinical manifestations of decreased cerebrospinal fluid (CSF) volume and CSF pressure were first described by Schaltenbrand ²¹ in 1938. The findings can be primary from idiopathic spontaneous intracranial hypotension (IH) or secondary due to lumbar puncture or perioperative or posttraumatic causes that allow CSF leakage via meningeal defects. ^22-24 The classic clinical presentation of IH is acute or subacute postural headaches. These, however, may not always be postural, particularly when associated with subdural hygromas or hematomas. ^24-27 Other intracranial manifestations include cranial nerve palsies, visual disturbances, photophobia, dysgeusia, auditory symptoms, facial numbness and weakness, and, rarely, stupor. ²⁷

The manifestations of IH are based on the Monroe-Kelly Rule, which contends that CSF volume varies with intracranial blood volume. This rule states that in the setting of an intact skull, a decreased CSF volume will lead to brain and meningeal vasodilatation. Since there is communication of the intracranial and intraspinal venous systems, it is possible that dilatation of brain meninges and intraspinal venous plexi will occur in concert. ²⁸ It is important to note that CSF pressure is usually low in this condition, but this is not always the case. ^24,27 The intracranial MRI findings include diffuse dural enhancement, prominent dural sinuses, enlarged epidural venous plexus, enlarged pituitary gland, subdural collections (effusions or hematomas), and downward displacement of the optic chiasm, pons, and cerebellar tonsils. ²⁷ Spinal manifestations of IH are similar to those described above, such as dural enhancement (pachymeningeal), epidural venous plexus dilatation, extradural fluid collections, and inferior cerebellar tonsillar displacement, ^22,24,27,28 and are best evaluated with MRI (Figure 4).

Cervical spinal epidural venous engorgement is most prominent at C1-C2, with frequent extension to the clival plexus, and enhances with contrast administration. Flow voids may also be present as hypointense areas on T2-weighted imaging (T2WI). ²⁸ Since there is no posterior epidural vein in the cervical spine, the predominant epidural venous system is situated anterolaterally within the spinal canal. ²⁹ Care must be taken not to mistake an enlarged epidural venous plexus for a meningioma or other dural mass. ²⁷

Another important MRI finding of the spine is the presence of an extradural fluid collection that is usually isointense to CSF on T1-weighted imaging (T1WI) and T2WI. Mild enhancement of the fluid collections or the adjacent dura has been reported when the enhancement may be related to contrast leakage into the collection. ²² The location of these collections is not altogether clear and may be either epidural or subdural. ^22,28 Likewise, the etiology of these extradural collections is uncertain, but may represent the actual site of CSF leakage, ²² secondary to CSF hydrostatic changes, ^25,28 or represent a transudate from spinal meningeal hyperemia. ^28,30

An interesting cervical spinal finding in IH is the presence of a paramedian fluid collection at the C1-C2 level in the posterior soft tissues of the spine that follows CSF signal on both T1WI and T2WI. ²⁸ Three potential etiologies have been suggested. Yousry and colleagues ²⁸ thought that the collection could represent the site of CSF leak, or that it might represent transudate secondary to hydrostatic pressure changes in adjacent rich venous plexi. Alternatively, Dillon ³¹ suggests communication of this cervical fluid collection with the subarachnoid space, as CSF ascends in the epidural space from a site of leakage in a more inferior location and ultimately decompresses into the posterior cervical soft tissues at the C1-C2 level.

Cervical spine sarcoidosis

Sarcoidosis is a multisystem disease that presents histopathologically as noncaseating granulomas of unknown etiology and clinically involves the central nervous system in approximately 5% of affected patients ³² and 16% of cases at autopsy. ³³ This disease often mimics other central nervous system diseases, such as multiple sclerosis, meningioma, tuberculous meningitis, and vasculitis. Intracranial manifestations include dural thickening or masses, enlarged pituitary stalk, leptomeningeal involvement, enhancing and nonenhancing parenchymal lesions, and cranial neuropathies. ^34,35

The cervical manifestations of sarcoidosis are similar to intracranial findings and can have both intramedullary and extramedullary involvement. Intramedullary findings, however, often include an extramedullary component and can mimic spinal cord neoplasms. Sarcoidosis of the cervical spine can be extensive, infiltrative, and expansile, with significant associated hyperintensity on T2-weighted images. The enhancement pattern may be broad-based and peripheral (suggesting inflammatory changes extending from the leptomeninges via perivascular spaces inward), extending from adjacent to the spinal cord surface to the center of the cord ^34,36,37 (Figure 5). In the chronic stages of these intramedullary lesions, cord atrophy without enhancement as well as gliosis may be present. ^36,7

Spontaneous epidural hematoma of the cervical spine

Spontaneous spinal epidural hematomas are not common occurrences. ³⁸ However, with increasing use of MRI, this diagnosis may not be as unusual as initially thought. ³⁹ The most common location of hematomas is in the thoracic spine ^40,41 though Sklar and colleagues ³⁹ reported a predominance of cervical spine hematomas in their study. They propose that this may be due to the fact that the majority of their cases involved trauma that is more common in the cervical spine. ³⁹

Although spinal epidural hematomas are considered to be spontaneous, they may be related to just minor trauma with a male predominance. ^39,42 The epidural venous plexus is thought to be fragile and therefore vulnerable to rupture. ⁴² Other etiologies include coagulopathies, rupture of vascular malformations, vertebral body hemangiomas, hypertension, and pregnancy. ^38,39 Acute pain is a common finding with concomitant neurologic deficit based on the extent of cervical spinal cord compression.

MRI is the modality of choice for evaluation of hematoma, as it gives the clinician information of anterior or posterior location, extent, degree of cord compression, and acuity of the hematoma. It also provides a basis for management and follow-up of potential surgical decompression. ⁴² Signal characteristics can vary, but are isointense to adjacent cord acutely, with conversion to hyperintensity in the subacute stage on T1WI ⁴² (Figure 6). On T2WI, the majority of the signal abnormality is hypointense acutely, ^39,42,43 though hyperintensity has also been described. ⁴⁴ Gradient-echo images have been shown to be useful to demonstrate blooming ³⁹ of hemorrhage, while others report peripheral, linear enhancement of acute spinal epidural hematoma. ⁴⁵

Differential diagnoses from hematoma in the cervical spine include epidural abscess, neoplasm, and lipoma. ⁴² One other diagnostic entity to consider is engorgement of the anterior epidural venous plexus, as was described above in cases of intracranial hypotension. The clincial scenario, with or without contrast MR characteristics, however, should allow accurate diagnosis in most cases. ⁴²

Conclusion

Recognition of the less common non-neoplastic entities of the cervical spine is important in order to diagnose and properly treat these patients and avoid erroneous diagnoses.