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Original research
Intraoperative spinal digital subtraction angiography: indications, technique, safety, and clinical impact
  1. Emanuele Orru’1,
  2. Danielle E Sorte1,
  3. Lydia Gregg1,
  4. Jean-Paul Wolinsky2,
  5. George I Jallo2,
  6. Ali Bydon2,
  7. Rafael J Tamargo2,
  8. Philippe Gailloud1
  1. 1Division of Interventional Neuroradiology, Department of Radiology, The Johns Hopkins Hospital, Baltimore, Maryland, USA
  2. 2Department of Neurological Surgery, The Johns Hopkins Hospital, Baltimore, Maryland, USA
  1. Correspondence to Dr Emanuele Orru’, Division of Interventional Neuroradiology, Department of Radiology, The Johns Hopkins Hospital, 1800 Orleans St, Bloomberg 7218, Baltimore, MD 21287, USA; eorru1{at}jhmi.edu

Abstract

Background Cerebral intraoperative DSA (IODSA) is a well-described, routinely performed procedure that allows the effectiveness of cerebrovascular interventions to be evaluated in the operating room. Spinal IODSA, on the other hand, is infrequently obtained and has received less attention.

Objective To discuss the indications, technique, safety, and clinical impact of spinal IODSA.

Materials and methods Twenty-three patients underwent 45 thoracic and/or lumbar spinal IODSA between 2005 and 2016, either immediately before surgery for lesion localization or after the intervention to evaluate its effectiveness. Indications included 21 vascular malformations and 2 diaphragmatic crus compression syndromes. A long femoral arterial sheath with its hub positioned on the lateral surface of the thigh was used to allow catheter manipulations in the prone position.

Results All targeted intersegmental arteries (ISAs) were successfully catheterized. The course of surgery was changed in 6 instances (26.1%). In 4 cases of epidural or perimedullary arteriovenous fistulae (AVFs), a residual lesion required additional intervention. In one case of epidural AVF, initial IODSA revealed spontaneous resolution of the lesion, preventing unnecessary surgery. Finally, angiography performed in a case of diaphragmatic crus syndrome showed thrombosis of the ISA and non-visualization of the artery of Adamkiewicz. Recanalization was obtained by IA thrombolysis, with excellent clinical outcome. No intraprocedural or postprocedural complication was noted.

Conclusions Spinal IODSA is a safe technique that offers an immediate assessment of the effectiveness of a spinovascular surgical procedure, notably epidural and perimedullary AVFs. Spinal IODSA was technically successful in all cases, influencing the surgical strategy in 6 of 23 patients, including one patient who benefited from intraoperative endovascular therapy.

  • Spinal cord
  • Vascular Malformation
  • Angiography
  • Fistula
  • Arteriovenous Malformation
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Introduction

Cerebral intraoperative DSA (IODSA) allows the effectiveness of a cerebrovascular surgical procedure to be evaluated while the patient is still in the operating room. Developed during the 1960s,1 ,2 cerebral IODSA is now a routinely performed procedure with well-established safety profile and clinical value.3–5 IODSA can also be used to assess the efficacy of surgical interventions dealing with the spinal vasculature. Less commonly obtained than cerebral IODSA, spinal IODSA has to our knowledge been mentioned in only eight articles so far,6–13 including five specifically dedicated publications,6–10 including a total of 42 patients (range 1–9). We present our experience with 45 procedures performed in 23 patients, and discuss the technique, safety, and clinical impact of spinal IODSA.

Materials and methods

This retrospective study identified 23 patients who underwent spinal IODSA at our institution between May 2005 and April 2016. Only procedures involving the selective catheterization of thoracic and/or lumbosacral intersegmental arteries (ISAs) were included in this review (cervical vascular lesions were excluded as intraoperative vertebral angiography is not technically different from standard cerebral IODSA). Electronic records, angiographic images, and procedural reports were reviewed for each patient. All patients were investigated with spine MRI and a full diagnostic spinal angiogram was obtained before surgery. The total number of intraoperative angiograms and their impact on the surgical intervention were documented. The number and level of catheterized vessels, duration of the procedure, mean catheterization and imaging time for each studied vessel, and the total number of injections were recorded for angiograms evaluating more than one branch (17 cases). These various times were calculated by analyzing the procedural report generated by the C-arm at the end of each procedure. Instead of simply collecting fluoroscopy times, which would be shorter than the actual procedural times, the duration of the angiograms was calculated as the time between the first and last DSA acquisitions. The mean catheterization and imaging times were then obtained by dividing the procedural time by the number of vessels catheterized and by the number of DSA acquisitions, respectively. The occurrence of periprocedural or postprocedural adverse events, including groin or retroperitoneal hematoma, femoral artery injury, access site infection, vessel rupture/dissection, and spinal thromboembolic complications, was also recorded.

Angiography technique

Femoral arterial access was obtained in the operating room with the patient under general anesthesia in the supine position using a single-wall puncture technique. A long arterial sheath (5F, 55 cm or 4F, 30 cm for pediatric patients) was then introduced over a 0.035 wire, keeping an extra-arterial segment of the sheath curved backward and secured with transparent waterproof dressing on the lateral aspect of the thigh, allowing for subsequent access with the patient in the prone position (figure 1). Continuous flushing with heparinized saline (4000 IU/L, 30 mL/hour) was maintained throughout the surgical procedure.

Figure 1

Picture of a patient's left groin area showing the hub of the long arterial sheath placed on the lateral aspect of the thigh, a position that offers easy access when the patient subsequently lies in the prone position for the surgical procedure.

IODSA was performed in a sterile fashion with the patient in the prone position on a radiolucent carbon fiber Jackson table using a mobile C-arm (ARCADIS Varis, Siemens, Germany). In preparation for angiography, the operative field was covered with sterile towels and drapes, the area around the sheath's hub re-prepped, and the hub accessed by cutting a hole in the transparent sterile dressing. A 5F Cobra 2 catheter was used in the vast majority of cases, at times supplemented by a 5F Mickelson catheter. Depending on the operating room configuration, the operators were either positioned to the left or right of the patient, near the hub of the arterial sheath, facing the C-arm unit, and angiography monitors placed on the other side (figure 2). For optimal radioprotection, the operating table was raised as high as possible and the image intensifier-to-patient distance kept to a minimum. Tight collimation and limited magnification factors were used. Presurgical spinal IODSA, typically limited to the catheterization of a single ISA, was generally performed to confirm the presence of the targeted pathology and assist with surgical access planning. Most postoperative studies included ISAs located above and below the lesion in order to detect potential collateral supply to the treated anomaly (figure 3). Patients with documented residual lesions underwent further surgical manipulations, followed by one or more additional IODSAs. Arterial sheaths were either removed in the operating room at the end of the intervention or immediately after arrival in the intensive care unit.

Figure 2

Artistic representation of the operating room setup during spinal intraoperative digital subtraction angiography (IODSA).

Figure 3

Patient with a spinal dural arteriovenous fistula (AVF) supplied by the left T6 intersegmental arteries (ISAs). (A) DSA, left T6 injection, posteroanterior view, showing the radiculomeningeal artery feeding the lesion located along the left T6 nerve root (large black arrow) as well as an anterior radiculomedullary artery (white arrow). The small black arrows point at the perimedullary drainage of the dural AVF. (B) Intraoperative DSA (IODSA), left T6 injection, posteroanterior view, performed in the operating room immediately before surgery, confirming the presence of the lesion and assisting with laminectomy planning (same legend keys). (C) IODSA, left T6 injection, posteroanterior view, documenting successful obliteration of the spinal dural AVF with preservation of the anterior radiculomedullary artery (white arrow).

Results

Forty-five IODSAs were performed by the neurointerventional service between May 2005 and April 2016 in 23 patients (17 men and 6 women, age range: pre-teens to late-70s, median 52.8), including 10 preoperative angiograms for lesion localization and 35 postoperative studies. The indications included seven (30.4%) spinal dural arteriovenous fistulae (AVFs), five (21.7%) spinal epidural AVFs, eight perimedullary AVFs (34.8%), one spinal AVM (4.3%), and two cases of diaphragmatic crus compression syndrome (8.7%).14 Anonymized patient data are shown in table 1. All the targeted ISAs were successfully catheterized. The following results were deduced by analysis of the data for the 17 IODSAs which included multiple vessels catheterizations. The mean number of investigated vessels during IODSA was 6.1 (range 2–13, median 5). The mean number of injections performed for each study was 7.4 (range 2–17, median 6). The mean duration of IODSAs involving more than one vessel was 7.5 min (range 3–22, median 7). The mean catheterization and imaging time for each studied vessel was 1.3 min (range 0.4–3.1, median 1.1). No intra- or postprocedural complications related to IODSA were seen. The procedure directly affected the course of surgery in six cases (26.1%), as summarized below:

  • Case 1—A patient in the middle 50s with a T12 perimedullary AVF necessitating five clip repositionings, each followed by IODSA, before complete exclusion of the lesion.

  • Case 2—A septuagenarian patient treated for an L1 epidural AVF; IODSA after obliteration of the main feeder showed residual fistula fed by minute meningeal branches. The second angiogram performed after ligation of these branches confirmed complete obliteration of the lesion.

  • Case 3—A patient in the late 60s treated for a perimedullary AVF of the conus medullaris; initial IODSA documented residual arteriovenous shunting, but complete obliteration was confirmed by a second angiogram.

  • Case 4—A patient in the early 40s treated for spinal cord ischemia secondary to severe diaphragmatic compression of the left L1 ISA. IODSA obtained after section of the diaphragmatic crus revealed left L1 ISA occlusion. Complete recanalization was achieved by selective infusion of nicardipine (3.5 mg) and recombinant tissue plasminogen activator (rtPA; 8 mg), with normal appearance of the artery of Adamkiewicz and absence of residual L1 stenosis. Additional angiography was obtained immediately after completion of the surgical treatment, revealing recurrent intraluminal clot successfully treated with an additional IA dose of rtPA (4 mg), with excellent functional outcome (figure 4).

  • Case 5—A patient in the middle 60s with an epidural AVF supplied by the T8, T9, and T10 ISAs, in whom three IODSAs were performed before complete obliteration of the lesion was obtained.

  • Case 6—A patient in the early 40s with a left T9 spinal epidural AVF documented by angiography; immediate presurgical IODSA revealed spontaneous resolution of the lesion. Twelve-vessel IODSA confirmed the absence of residual lesion and the surgery was canceled.

Table 1

Patient demographics, number and level of catheterized intersegmental arteries (ISAs) and brief description of the way in which IODSA altered the course of surgery

Figure 4

Patient with diaphragmatic crus syndrome. (A) Schematic representation of the anatomical configuration leading to a diaphragmatic crus syndrome in this patient, in a projection corresponding to the angiographic views described below. (B) Intraoperative DSA (IODSA), left L1 injection, posteroanterior view, performed at the beginning of the procedure, confirming near-occlusive stenosis of the intersegmental artery (ISA) at its point of passage through the left diaphragmatic crus (black arrow). Note the opacification of the artery of Adamkiewicz (small white arrow). (C) IODSA, left L1 injection, posteroanterior view, obtained after section of the portion of the crus compressing the L1 ISA. The stenosis has resolved (black arrow), but the vessel is occluded distally, and the artery of Adamkiewicz is not opacified. (D) IODSA, left L1 injection, posteroanterior view, documenting full patency of the left L1 ISA after superselective administration of recombinant tissue plasminogen activator and nicardipine, with complete resolution of the crus compression (black arrow) and normal opacification of the artery of Adamkiewicz (small white arrow) and anterior spinal artery.

Discussion

Cerebral IODSA is now a well-established, routinely performed procedure, but spinal IODSA is less commonly carried out and has been discussed in only a few articles.6–13 The main technical particularity of spinal IODSA is the need to perform the procedure with the patient in the prone position. Arterial access therefore requires the placement of a long femoral sheath with its hub secured to the side of the thigh before positioning the patient prone for the surgical procedure. This approach has been described with minor differences in previous reports.8–10 After sheath placement, a presurgical angiogram is sometimes obtained in the operating room at the start of the surgical procedure to confirm the presence of the lesion and assist with its localization before skin incision. Alternatively, the presurgical study can be obtained in the angiography suite before transferring the patient to the operating room.13 Grams et al6 reported the only known instance in which the whole surgery was carried out in the angiography suite. Although this approach provides better image quality than angiography obtained in the operating room with a portable C-arm, it requires an angiography suite with operating room sterility.

For radioprotection, the rigorous use of optimal geometric factors—that is, high table position, short detector–patient distance, and avoidance of oblique projections unless absolutely necessary, is important to keep the dose to the minimum. The use of protective lead screens and optimized angiography protocols help to limit exposure of both the patient and the caring team. Of note, owing to the prone position of the patient, spinal IODSA is performed in an anteroposterior rather than posteroanterior projection, which may expose patients to a slightly higher effective dose according to a recent computational human phantom study.15

In our series, selective catheterization of the targeted ISAs was always possible, with relatively short fluoroscopy and DSA times (mean procedural times 7.5 min). It should be noted that these various times were calculated using the cumulative procedural duration recorded by the C-arm between the first and last acquisitions, which includes the time spent reviewing images and moving the X-ray tube from one level to the next, and therefore represents an overestimation of the actual fluoroscopy time. No intraprocedural or postprocedural complication was noted, a finding consistent with prior studies that showed a similar safety profile.6–10

At our institution, IODSA is carried out in all instances of cerebrovascular and spinovascular interventions. At the spinal level, in addition to vascular malformations, indications now also include cases of surgical correction of the diaphragmatic crus syndrome.

Mourier et al16 remarked that fistulous connections were often difficult to detect during surgery. This led some teams to preoperatively mark the fistulous point with coils or glue in patients for whom endovascular therapy was not an option.17 In our experience, either the use of bony landmarks was considered sufficient (13 cases) or IODSA was carried out immediately before surgical access, with the patient in the supine position to confirm the lesion localization, without the need for more invasive methods (10 cases).

Spinal IODSA has in our series altered the course of surgery in nearly a third of patients, generally by documenting a residual lesion, which was often supplied by vessels not previously identifiable, notably in cases of spinal epidural and perimedullary AVFs. In one instance, presurgical IODSA carried out in the operating room prevented an unnecessary multilevel laminectomy by revealing the spontaneous resolution of a spinal epidural AVF previously diagnosed by angiography.

As an alternative to IODSA, the surgical obliteration of spinal vascular malformations can be assessed by indocyanine green videoangiography (ICGV),18–21 which is less invasive and time consuming. This report shows that IODSA can be performed quickly and safely and offers significant advantages over ICGV, including (1) the visualization of vascular structures located outside the operative field of view or deep vessels that cannot be directly appreciated, (2) a higher sensitivity for the detection of spinal arteries, and (3) a better assessment of the angioarchitecture of residual lesions.22 ,23

As another alternative to spinal IODSA, some authors recommend performing postoperative spinal angiography 24–72 hours after the surgical procedure.18 ,19 ,24 However, by identifying a residual lesion or other potential complication when the patient is still in the operating room, before surgical closure, IODSA authorizes immediate adjustments, preventing the burden of re-operation and of additional invasive diagnostic procedures in the immediate postoperative period.

Finally, with spinal IODSA comes the ability to use endovascular measures to deal with intraoperative events that cannot be managed surgically. As part of this series, we report what we believe to be the first instance of emergent intraoperative spinal IA thrombolysis performed to salvage an occluded ISA providing the artery of Adamkiewicz.

Pre- and post-surgical IODSA can significantly influence the surgical outcome of spinal vascular disorders, notably when dealing with complex lesions such as epidural and perimedullary AVFs or with less common disorders (eg, diaphragmatic crus syndrome). The ability to immediately identify and deal with residual fistulous connections or unexpected and possibly catastrophic complications justifies, in our opinion, the prolonged anesthesia time and additional costs. IODSA did not in our series directly modify the surgical technique in cases of spinal dural AVFs. However, dural AVFs managed surgically at our institution are typically lesions deemed less favorable for endovascular management, usually because of the presence of a prominent radiculomedullary artery originating from the ISA suppling the AVF, but IODSA still had an important role by confirming the patency of these critical branches. The usefulness of IODSA for simpler dural AVFs, in particular those not associated with significant radiculomedullary branches, is not established by our series, a conclusion consistent with the excellent obliteration rates reported for dural AVFs in surgical series not using IODSA.25

Two limitations of our study need to be mentioned. First, even though it is the largest cohort published so far, our retrospective series remains relatively small, preventing a meaningful statistical analysis. Second, the mean recorded procedural time (7.5 min) represents only the time between the first and last acquisitions, and does not take into account the time for sheath placement before the start of the surgery or the time needed to access and prepare the catheter hub at the beginning of the angiography itself. Although these times are not routinely recorded, our best estimation, based on observations made in recent cases, is that they are about 15 and 10 min, respectively.

Conclusions

We present our single-center experience with spinal IODSA in 23 patients. The procedure was technically successful and uncomplicated in all instances, significantly changed the course of surgery, and eliminated the need for further angiographic assessments in the immediate postoperative period.

Spinal IODSA is the most sensitive tool for intraoperative assessment of the spinal vasculature. Considering its high safety profile and reported advantages, we suggest that spinal IODSA should routinely complement spinovascular surgical procedures—notably, complex or unusual lesions.

References

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Footnotes

  • Contributors All authors contributed equally to the manuscript and its reviews.

  • Competing interests None declared.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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