Delayed deterioration after surgical treatment of a spinal dural arteriovenous fistula detected by three spinal angiographies: Case report

Abstract

Spinal dural arteriovenous fistulas (DAVFs) are the most common subtype of spinal arteriovenous malformations, and they often cause progressive myelopathy. Early detection and intervention are critical to preventing irreversible neurological deficits. Selective spinal angiography remains the gold standard for diagnosing this condition. However, for some patients with typical clinical features and magnetic resonance imaging (MRI) findings consistent with DAVF, the initial angiography may fail to detect the lesion. In this article, we report a case of T4 low-flow spinal DAVF that was only identified after three rounds of spinal angiography. The fistula was successfully occluded via surgery, and the patient’s symptoms gradually improved postoperatively. Nevertheless, the patient later developed recurrent, aggravated symptoms. The delayed deterioration of previously resolved symptoms was attributed to venous thrombosis, and the condition improved after systemic anticoagulation therapy with heparin. The patients fluctuating symptoms stabilized one month after combined therapy with anticoagulants and antiplatelet drugs. For patients with a high clinical suspicion of spinal DAVF, required to confirm the final diagnosis. Delayed deterioration can occur secondary to progressive venous thrombosis, so preventive anticoagulation is indicated for selected patient’s, and this intervention should be individualized.

Case report

History and examination

This 65-year-old man presented to an outside hospital with a 4-year history of progressive weakness and numbness in both lower extremities. Spinal MRI showed T2-weighted hyperintensity and swelling of the spinal cord extending from T5 to the conus medullaris, with prominent vascular flow voids detected at the T5 to T7 levels (Figs. 1A and B). Spinal MR angiography identified dilated spinal veins but failed to visualize the fistula (Fig. 1C), leading to clinical suspicion of spinal DAVF.

Fig. 1.

Spinal MRI images obtained before the initial surgery and intraoperative images. (A) Spinal sagittal T2-weighted MR image showing extensive edema within the spinal cord from T5 to the conus medullaris, with marked vascular flow voids on the surface of the T5–T7 levels. (B) Sagittal T1-weighted enhanced MR image showing dilated, tortuous enhanced vessels on the dorsal surface of the T5–T7 spinal cord. (C) Spinal MR angiography showing dilated spinal veins but no evidence of fistula. (D) Intraoperative image showing abnormal dilated and tortuous vessels on the dorsal surface of the spinal cord, with no definitive fistula identified. (E) The abnormal vessels are resected without damaging the spinal cord parenchyma.

The patient underwent selective spinal angiography, which returned a negative result. Based on his clinical presentation and MRI findings, he underwent T3–5 laminoplasty for surgical exploration. During the procedure, numerous dilated, tortuous vessels were observed on the dorsal surface of the spinal cord, but no definitive fistula was identified (Fig. 1D). These abnormal vessels were resected without damaging the spinal cord parenchyma (Fig. 1E).

Postoperatively, the patient’s symptoms improved slightly, but worsened three months later. He was then referred to our hospital for further evaluation and management.

On neurological examination, the patient had spastic paraparesis (grade 3/5) in both lower extremities, accompanied by dysesthesia extending from the T10 dermatome down into both legs. He also presented with urinary incontinence, and bilateral positive Babinski reflexes were detected. Repeat spinal MRI showed persistent spinal cord edema extending from T5 to the conus medullaris, with flow voids no longer visible (Figs. 2A and B). A second spinal angiography still showed no abnormalities, so the patient was transferred to a rehabilitation facility for recovery. Two months later, the patient’s symptoms gradually worsened to the point that he was unable to ambulate. He was readmitted to our hospital with paraparesis, dysesthesia, and complete urinary incontinence. Neurological examination revealed bilateral lower extremity weakness (grade 2/5) and dysesthesia below the T10 level. Repeat spinal MRI still showed spinal cord edema consistent with the previous examination, and no obvious flow voids were detected. However, contrast-enhanced MRI showed dilated, tortuous vessels on the dorsal surface of the spinal cord at the T5–T7 levels (Figs. 2C and D). An angiographically occult spinal DAVF was therefore suspected. A third spinal angiography was performed, which revealed a low-flow DAVF located at the T4 level, supplied by the T4 intercostal artery and draining into the perimedullary vein (Figs. 3A and B).

Fig. 2.

First postoperative MRI images. (A) Spinal T2-weighted MR imaging shows persistent edema in the spinal cord extending from T5 to the conus medullaris, with no residual flow voids. (B) Spinal T1-weighted enhanced MR imaging shows no abnormally enhanced vessels. (C) Spinal T2-weighted MR imaging demonstrates residual edema, without prominent flow voids. (D) T1-weighted enhanced MR imaging shows dilated and tortuous vessels on the dorsal surface of the spinal cord at T5–T7 levels (arrow).

Fig. 3.

Spinal angiography and intraoperative views of the second surgery. (A) Early-phase spinal angiography demonstrates a low-flow fistula supplied by the T4 intercostal artery. (B) Late-phase angiography shows the fistula drains downward into the perimedullary veins. (C) Intraoperative images show the dilated draining vein entering through the inner dura alongside the left T4 nerve root, with a small and narrow proximal segment of the draining vein. (D, E) The fistula is successfully coagulated and divided.

Operation

The patient underwent T4–6 laminoplasty. A dilated arterialized draining vein was found entering the dura alongside the left T4 nerve root. The proximal segment of the draining vein at the dura was small and narrow (Fig. 3C). Laser Doppler flowmetry detected a weak pulsatile signal from this draining vein. The low-flow fistula was then successfully coagulated and transected (Figs. 3D and E).

Postoperative course

The patient had an uneventful postoperative recovery. Within one week after surgery, muscle weakness in the patient's bilateral lower extremities gradually improved, with muscle strength reaching grade 3/5. On the ninth postoperative day, the patient suddenly experienced a decrease in muscle strength to grade 2/5, accompanied by severe pain in both legs. Emergency MRI revealed reduced edema in the spinal cord below T7, as well as disappearance of the dilated venous plexus, with no evidence of acute infarction or hemorrhage (Fig. 4). Progressive venous thrombosis was highly suspected, and systemic anticoagulation therapy with heparin (40 mg twice daily) was initiated immediately. By the second day of treatment, the patient’s leg strength had improved significantly to grade 3+/5. Three days later, the patient’s symptoms worsened again. Increasing the heparin dose to 1 mg/kg of body weight twice daily rapidly restored symptoms to the level they were at before the exacerbation. One week later, heparin was switched to warfarin (1.25 mg/day). Three days after warfarin was initiated, the patient’s gait disturbance worsened again, with muscle strength dropping back to grade 2/5. The treatment plan was adjusted to combine warfarin (1.25 mg/day) with clopidogrel (75 mg/day), targeting an INR of 2–3. Following this adjustment, the patient’s symptoms gradually improved. Three months after surgery, the patient was able to walk with the assistance of a cane, with muscle strength reaching grade 4/5, and urinary incontinence had fully resolved. This combined therapy will be continued for six months after surgery. Fig. 5 illustrates the fluctuation of the patient’s symptoms based on serial muscle strength measurements.

Fig. 4.

Second postoperative MRI images. (A and B) Sagittal T1-weighted and T2-weighted MR imaging show decreased edema within the spinal cord and disappearance of the dilated venous plexus. (C) No abnormally enhanced vessels are observed on the T1-weighted enhanced MR image.

Fig. 5.

The use of anticoagulant medications and muscle strength imaging.

Discussion

Spinal DAVFs are rare lesions characterized by an abnormal connection between a meningeal branch of a segmental artery and an intradural radiculomedullary vein [[1], [2], [3]]. They are the most common subtype of spinal cord vascular malformations and occur most frequently in the thoracolumbar region [1]. Patients with spinal DAVF typically present with slowly progressive myelopathy symptoms resulting from congestive venous hypertension [2,4]. Early diagnosis combined with surgical or endovascular intervention is the key to preventing irreversible neurological impairment.

Spinal DAVF can be successfully managed in most patients when the diagnosis is made before irreversible neurological damage develops. When spinal DAVF is suspected based on clinical manifestations and MRI findings, selective spinal angiography is performed to confirm the diagnosis, accurately localize the fistula, and determine a potential access route for endovascular treatment [3]. While spinal MRI and CT angiography have been proven effective for lesion localization, spinal angiography still remains the gold standard for the diagnosis of DAVF [3,5,[6], [7], [8]].

Even in patients with a high clinical suspicion of spinal DAVF, spinal angiography may fail to detect the fistula [3]. What is more, repeat angiography may also yield a negative result. Aortic atherosclerosis and low-flow fistulas have been identified as potential causes of false-negative results [3,5,6,7]. In this case reported here, the first two angiographies failed to identify the lesion, and the fistula was ultimately detected through the third angiography. During surgery, we observed that the proximal segment of the draining vein adjacent to the nerve root was extremely small and narrow, and Doppler flowmetry confirmed the presence of a low-flow fistula. We therefore conclude that low blood flow is the most likely cause of the negative results from the first two angiographies.

In this case, MRI was obtained 3 months after the first exploratory surgery and showed persistent edema with no definitively enhanced vessels (Figs. 3A and B); however, two months later, when the patient’s symptoms worsened, follow-up MRI revealed enhanced, dilated, tortuous vessels on the surface of the spinal cord at the T5–7 level (Figs. 3C and D). The interval between these two MR examinations was 2 months. These findings indicate that the hemodynamic characteristics of the fistula were dynamic: fistula flow gradually increased and the draining vein enlarged over time, which ultimately enabled the third spinal angiography to detect the previously occult low-flow fistula [9,10]. To our knowledge, this is the first reported case of spinal DAVF that was only detected after three rounds of angiography.

Deterioration of symptoms after a delay following spinal DAVF treatment can occur due to fistula recurrence, venous thrombosis, or spinal cord hemorrhage [[11], [12], [13], [14]]. In our case, symptom aggravation developed on the 9th postoperative day, and repeated MRI showed no evidence of acute infarction or hemorrhage. Fistula recurrence could be ruled out over such a short interval after surgical intervention. Thus, progressive venous thrombosis was determined to be the cause of delayed symptom deterioration in this patient, and the patient’s symptoms gradually improved after initiation of low-dose heparin (40 mg twice daily).

Niimi et al. [5,15] reported that among 49 patients with spinal DAVF treated with embolization, two developed venous thrombosis within one month, and their symptoms resolved after systemic heparinization. They recommended post-embolization heparinization for selected patient’s with significantly compromised spinal cord venous drainage. Ohta et al. [5,11] reported a case of spinal DAVF treated with embolization, in which venous thrombosis developed seven days after prophylactic antithrombotic therapy was discontinued. The patient’s fluctuating symptoms did not stabilize until dual antiplatelet therapy was reinstituted. Knopman et al. [12] described a spinal DAVF patient who experienced delayed neurological aggravation after successful embolization; their symptoms were attributed to venous thrombosis and gradually resolved with systemic anticoagulation. These previously reported cases of neurological deterioration occurred in patients treated with embolization, and the present case is the first report of delayed neurological aggravation after surgical intervention.

Whether all patients with spinal DAVF require systemic anticoagulation after surgical or endovascular therapy remains debated, and the optimal strategy for preventing progressive venous thrombosis during the postoperative period remains unclear [16]. Currently, the most established and effective treatment for venous thrombosis is anticoagulation with heparin or warfarin, rather than antiplatelet agents [12,15]. Stam [17] recommended a six-month course of warfarin for cerebral venous thrombosis, with a target international normalized ratio (INR) of 2.5. In our patient, monotherapy with warfarin failed to stabilize symptoms, but combined treatment with antiplatelet therapy achieved symptom control, with the INR maintained between 2 and 3. This combined therapeutic regimen will be continued for six months.

At our institution, routine systemic anticoagulation is not routinely administered to patients with spinal DAVF, regardless of whether they receive surgical or endovascular treatment. Based on the present case, we recommend that regular systemic anticoagulation be used for selected patients with low-flow fistulas, and that an individualized treatment regimen be developed for each patient.

Conclusions

For patient’s with a high clinical suspicion of spinal DAVF, repeated selective spinal angiography is required to confirm the final diagnosis. Progressive venous thrombosis can develop after surgical treatment of spinal DAVF, leading to delayed neurological deterioration. Systemic anticoagulation should be administered to selected patients, and the treatment regimen should be individualized.

Methodology

• •retrospective;
• •diagnostic or prognostic study;
• •performed at one institution.

Patient consent

Written informed consent was not required for this study because this is a retrospective study.