Analysis of 30 Spinal Angiograms Falsely Reported as Normal in 18 Patients with Subsequently Documented Spinal Vascular Malformations

Patient Demographics and Type of Vascular Malformations

This report analyzed 30 spinal angiograms read as normal in 18 patients later diagnosed with a spinal vascular malformation. All of the lesions diagnosed were slow-flow vascular malformations; besides 2 small PmAVFs (Merland Type 1; 10%) located at the conus medullaris, they were either SEAVFs or SDAVFs. This finding is not surprising because the detection of conspicuous anomalies such as spinal arteriovenous malformations or PmAVFs (Merland Type 2 or 3) does not usually represent a challenge for noninvasive imaging, spinal DSA being then used to characterize their angioarchitecture and plan their management.

Our patients' demographic characteristics (predominantly older men) are consistent with previously published data on slow-flow vascular malformations.⁵ From a diagnostic perspective, the high prevalence of elevated CSF proteins (79%) and gadolinium enhancement on MR imaging (83%) probably explains the frequent misdiagnosis of transverse myelitis (83%).⁸ Flow voids, often considered as essential to the diagnosis of vascular malformation, were retrospectively detected in 11 cases (61%) but, because of their subtle nature, were correctly identified at the time of initial MR imaging interpretation in only 7 cases (39%).

Of particular interest is the preponderance of low lumbar and sacral lesions in our cohort; most of the missed SEAVFs/SADVFs (52.9%) were found at or below the L4 level. Besides certain technical considerations discussed separately, this finding seems to correlate with the relatively common misconception that a thoracic myelopathy cannot be accounted for by a pelvic lesion.

In terms of functional outcome, it is important to note that despite the significantly delayed diagnosis (11 months on average) and the clinical worsening caused in some cases by inadequate initial measures (notably steroid therapy), patients did still significantly benefit from the treatment of their vascular malformation. First and foremost, the progressive clinical deterioration typically associated with venous hypertensive myelopathy was stopped in all cases but 1, the exception being a patient who got worse shortly after treatment, likely from spinal venous thrombosis. Besides stopping the disease progression, endovascular or surgical therapy was able to bring a functional improvement in 13 of the 17 patients treated, with a significant difference retrospectively noted between the pre- and posttreatment Aminoff-Logue scores retrospectively (mean follow-up, 20 months; P = .012). This finding is consistent with the previously held view that even patients with severe disabilities can show significant improvement.⁹

Technical Factors Leading to Missed Findings or Inadequate Studies

This review identified several factors behind the missed findings or inadequate results. All were operator-dependent and potentially avoidable. The principal cause of missed diagnoses was a documented yet unrecognized lesion (55.6%). In other words, the anomaly was visible in the recorded images, but not identified as a vascular malformation. The same mechanism was responsible for false-negative studies in 3 additional cases of SDAVFs not included in our cohort because of a lack of detailed clinical information. This finding serves as a strong reminder of the complexity of spinal angiographic images, considering notably that most studies (86.7%) were obtained in academic centers.

The vessel of interest not being investigated was the second most frequent cause of inadequate study (29.6%). In 1 case, the vertebral levels were mislabeled and the feeding artery skipped by mistake. In the other 7 instances (25.9%), the intersegmental artery supplying the lesion was not included in the planned angiogram. Interestingly, the lesion was located at or below L3 in all of these cases. This finding has an important implication besides the fact that low lumbar or sacral vascular malformations are frequent; it suggests that low lumbar and pelvic vessels are often ignored during spinal angiography. Although this may be partly attributed to the technically more demanding catheterization of these branches, notably in older patients, the main reason behind this disregard appears to be the misconception that a pelvic flush angiogram supplemented by selective internal iliac injections is not an integral component of a full spinal angiogram. In our practice, spinal DSA performed in older patients with a suspicion of low-flow vascular malformation starts with a pelvic flush angiogram, which not infrequently establishes the diagnosis during the first few minutes of the procedure. Finally, in 4 cases (14.8%), the vessel of interest was investigated, but the angiograms were technically inadequate. In 1 of the PmAVFs, the feeding artery (left T10) was injected, but considered as normal, and the conus medullaris (site of the lesion) was not included in the field of view. In the other 3 instances, the feeding vessels were studied with nonselective injections, the small amount of contrast passing through the vessel of interest being considered of diagnostic value. In each case, a lesion was subsequently identified by selective angiography.

How to Limit the Risk of Inadequate Spinal Angiograms?

Our findings suggest that missed findings or inadequate studies might be avoided in most cases by the adoption of a rigorous angiographic protocol. The following recommendations—easily implementable in daily angiographic practices—should significantly reduce the risk of false-negative studies:

1. Carefully identify the vertebral levels investigated at the beginning of the procedure. Although the use of a ruler is in our opinion mandatory, it may not prevent skipping a level if one does not meticulously document the progress of the study and record the explored branches.

2. Avoid, as much as possible, poor angiographic visualization related to nonselective injections.¹⁰ It is also critical to document radiculomedullary arteries in their entirety, as exemplified by the PmAVF left out of the field of view during the injection of the artery of Adamkiewicz in 1 of the negative angiograms.

3. In most instances, it is necessary to perform a complete spinal angiogram—even if a lesion has already been documented—including the pelvis and the cervical region and, in selected cases, the carotid arteries as well. There is no strict correlation between the site of an arteriovenous fistula and the location and extent of the resulting spinal cord damage. A cervical SDAVF can, for example, induce midthoracic or lumbar cord edema with a normal MR imaging appearance of the cervical and upper thoracic spinal parenchyma. The potential for multiple synchronous spinal lesions must also be kept in mind.

4. Finally, the fact that most of the missed lesions were actually documented by the initial “negative” studies emphasizes the importance of a meticulous analysis of angiographic images, optimized by electronic means such as best mask selection and pixel shifting. It also stresses the value of second readings and second opinions. Second opinions also represent an educative tool, in keeping with Pinto and Brunese's¹¹ opinion that “a radiology safety culture will only exist when the radiologist who made the error views such feedback positively as a learning experience.” With angiographic images as complex and findings as subtle as the ones acquired during spinal angiography, no level of proficiency can prove completely immune to faulty interpretation.

Spinal Angiography as the “Gold Standard” Spinal Vascular Technique

Although no imaging technique is exempt from the risk of false-negative studies, it seems that various technical and cognitive factors render spinal angiography more prone to misleading interpretation than, for example, cerebral angiography. This fact directly impacts patient care because there is a justified tendency to rely on a “gold standard” technique. The number of patients with vascular malformations who remain misdiagnosed after a spinal angiogram falsely read as normal is unknown but likely not anecdotal. Spinal angiography should therefore only be considered as a “gold standard” technique when performed by experienced angiographers following strict technical guidelines.