Normal Venous Phase Documented during Angiography in Patients with Spinal Vascular Malformations: Incidence and Clinical Implications

Classification and Diagnosis of Spinal Vascular Malformations

Spinal vascular anomalies with arteriovenous shunts can pragmatically be divided into 2 main categories. The high-flow lesions include the SAVMs, the fast perimedullary arteriovenous fistulas (Merland types 2 and 3),⁹ and some high-output SEAVFs, generally of congenital or traumatic nature. The slow-flow lesions include SDAVFs, SEAVFs, and the slow perimedullary arteriovenous fistula (Merland type 1).

From a diagnostic viewpoint, high-flow SVMs are usually easily identified by noninvasive imaging methods. On the other hand, the nonspecific MR imaging changes associated with slow-flow arteriovenous fistulas can be deceptive, particularly in the absence of typical flow voids. A recent study found that the sensitivity and positive predictive value of MR imaging for SVMs in general could be as low as 51% and 48%, respectively.¹⁰ Our cohort similarly suggested a limited value for MR imaging, notably for slow-flow lesions, which were associated with an inaccurate initial diagnosis in 65% of cases.¹¹ This low predictive value may be related to the importance generally attributed to the absence of detectable flow voids, which were only noted in 49 of our 81 patients (60.5%). This situation is particularly relevant to our report because the angiographic documentation of a normal venous phase is generally used to rule out the presence of a slow-flow arteriovenous fistula in patients with inconclusive MR imaging findings.

Spinal Angiography Technique

The fundamental principles of selective spinal angiography established by its pioneers remain valid to this day.^12⇓–14 While partial studies may be performed in certain circumstances (eg, the limited diagnostic portion of a therapeutic procedure or follow-up angiograms), a typical diagnostic study includes at least the selective catheterization of each pair of intersegmental arteries and a pelvic flush aortogram (documenting an SVM does not rule out the presence of additional lesions¹), often complemented by selective injections of the internal iliac, subclavian, vertebral, supreme intercostal, and (in some instances) carotid arteries.^4,6,15 The appropriate technique and equipment allow performing a complete spinal angiogram with the patient under conscious sedation with short procedure durations, reasonable radiation and contrast agent doses, and extremely low complication rates.¹⁰ However, a sign reliably permitting terminating the procedure early, such as the observation of a normal venous phase, would carry an important clinical value. The emphasis placed on reliability is particularly important because it has been estimated that about 50% of so-called false-negative findings on spinal angiograms result from a failure to investigate the vessel supplying the SVM.¹⁶

Normal Venous Phase of Spinal Angiography

Multiple factors influence the detectability of normal venous structures during the injection of the artery of Adamkiewicz, including the quality of the angiographic equipment, the patient's age and body habitus, the use of general anesthesia or conscious sedation (including the use of paralytic agents or the patient's ability to breath-hold when studied awake), and the presence of significant motion and/or bowel artifacts. The presence of a normal venous phase may, therefore, be underestimated by our retrospective study, in which a substantial portion of angiograms (28.4%) were technically inadequate for the detection of small venous structures, principally because of respiratory and gastrointestinal motion artifacts or limited angiographic sequences in patients generally studied under conscious sedation. It is possible that performing diagnostic SpDSA with the patient under general anesthesia (by using paralytics and pausing the ventilator during injections) would reduce motion artifacts, particularly at the end of long angiographic sequences, and increase the visibility of small venous structures and the number of normal venous phases identified in patients with spinal vascular malformations. Yet, despite these drawbacks, 43% of all the reviewed SVMs were associated with a normal venous phase, including 40% of slow-flow lesions. The venous phase was analyzed at the lower thoracic and lumbosacral levels of the spinal cord (ie, the venous return of the anterior spinal artery after injection of the artery of Adamkiewicz). Some of the SVMs were, therefore, remotely located normal venous structures, such as a cervical cord SAVM (case 1) or an upper thoracic SDAVF (case 6), but most drained at the levels opacified during the observed normal venous phase. An interesting point made by Trop et al in 1998⁸ in regard to their cranial arteriovenous fistula with perimedullary drainage but associated with a normal venous phase was the normal MR imaging appearance of the lower spinal cord in their patient, which led them to conclude that “venous compartmentalization accounted for the isolated abnormal signal of the cervical cord and the normal venous drainage of the lower cord at MR imaging.” This idea of a “longitudinal compartmentalization“ could certainly apply to our 3 cases with remotely located SVMs.

Cases in which the normal and abnormal venous phases were documented at the same vertebral levels may suggest a relative functional independence of the anterior and posterior longitudinal venous systems, one preferentially participating in the drainage of the SVM while the other is involved in the visualization of a normal venous phase. Due to the 2D nature of SpDSA, however, the distinction between anterior and posterior spinal veins is generally not possible without the acquisition of lateral projections, which were generally not obtained in our patients. The existence of a “transverse compartmentalization” of the perimedullary venous drainage, therefore, remains hypothetic.

The Mechanisms Underlying the Visualization or Nonvisualization of a Spinal Venous Phase in Perimedullary Venous Hypertension

In our series, the lack of a spinal venous phase was slightly more common in SDAVFs than SEAVFs and in lesions located at the lumbar level. Both factors seem to favor a role for locoregional venous pressure variations. Hence, the observation of a venous phase, typically made at the level of the conus medullaris, would be more likely prevented by the pressure gradient produced by a closely rather than remotely located fistula (ie, lumbar versus sacral or thoracic). Similarly, the pressure gradient associated with an SDAVF, which consists of an arteriovenous shunt directly involving a radiculomedullary vein, should have a more significant locoregional impact than the gradient resulting from an SEAVF, in which the arteriovenous shunt is located on an epidural venous pouch with secondary drainage into a radiculomedullary vein (and other possible venous outflow pathways).

Case illustration 5 (Fig 6) suggests that the visualization of a normal venous phase may also depend on the existence of a patent radiculomedullary vein locally available to drain the perimedullary venous blood. In terms of venous timing, this case was a clear outlier (first documentation at 29 seconds, best delineation at 39 seconds) and could have easily been considered as lacking a normal venous phase without a long angiographic acquisition. Most interesting, this “transitional case” is also the one in which a patent lumbosacral radiculomedullary vein was not documented. It is, therefore, reasonable to think that a disappearing venous phase correlates with increasing venous drainage impairment and venous hypertension, a phenomenon typical of slow-flow arteriovenous fistulas well-described by Merland et al in 1980:¹⁷ “Hyperpressure is due to the presence of the shunt but also to impaired venous return, which in turn probably depends upon the absence of the veins normally draining into the epidural space.”