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ORIGINAL ARTICLE
Year : 2020  |  Volume : 68  |  Issue : 1  |  Page : 118-123

Patient Outcomes Following Obliteration of Spinal Dural Arteriovenous Fistula and the Role of Indocyanine Green Angiography Videoangiography (ICG‑VA) During Surgery


Department of Neurosurgery, All India Institute of Medical Sciences, New Delhi, India

Date of Web Publication28-Feb-2020

Correspondence Address:
Dr. Manoj Phalak
Department of Neurosurgery All India Institute of medical Sciences, New Delhi
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.279705

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 » Abstract 


Background: Spinal dural arteriovenous fistula (SDAVF) is a known cause of progressive myelopathy which can be treated either by surgery or embolization. Indocyanine green angiography videoangiography (ICG-VA) during surgery can locate the exact location of AV shunting.
Objective: To determine the clinical outcome following obliteration of the fistula and to study the role of ICG in identifying the presence and location of SDAVF; to add a comparative study of patients treated by embolization.
Materials and Methods: Patients treated for SDAVF in our centre from 2005 to 2015 were studied for clinical and radiological features, and outcome following obliteration of fistula.
Results: Of the total 33 patients (27 males, six females), 19 patients were operated without the use of ICG, nine were operated with the use of ICG and successful embolization was done in five. Acute presentation was seen in five. Single feeder was seen in 20 patients, multiple in 13. Mean follow-up was 58 months. All patients in ICG group improved. Three out of 19 patients in the non-ICG group (15.78%) required re-operation. With the use of ICG, the improvement in Aminoff Logue score was significantly better (P < 0.005). Embolization was tried in 13 cases, but successful in five (38%).
Conclusions: Surgery with intraoperative ICG shows the exact location of AVF. This decreases the chance of postoperative clinical deterioration and improves patient outcome.


Keywords: Embolisation, ICG, spinal dural arteriovenous fistula, surgery
Key Messages: Our study emphasizes that intraoperative ICG is indispensible in the surgical management of SDAVF.


How to cite this article:
Koyalmantham V, Kale SS, Devarajan LJ, Phalak M, Chandra P S, Suri A, Kumar R, Tandon V. Patient Outcomes Following Obliteration of Spinal Dural Arteriovenous Fistula and the Role of Indocyanine Green Angiography Videoangiography (ICG‑VA) During Surgery. Neurol India 2020;68:118-23

How to cite this URL:
Koyalmantham V, Kale SS, Devarajan LJ, Phalak M, Chandra P S, Suri A, Kumar R, Tandon V. Patient Outcomes Following Obliteration of Spinal Dural Arteriovenous Fistula and the Role of Indocyanine Green Angiography Videoangiography (ICG‑VA) During Surgery. Neurol India [serial online] 2020 [cited 2020 Mar 28];68:118-23. Available from: http://www.neurologyindia.com/text.asp?2020/68/1/118/279705




Spinal dural arteriovenous fistula (SDAVF) is a network of acquired low-flow abnormal arteriovenous (AV) shunt in the dural sheet, usually supplied by the meningeal branch of a radicular artery and refluxing into the perimedullary venous system through a medullary vein.[1] Despite being a treatable cause of myelopathy, they are often under-diagnosed because of the non-specific nature of the clinical presentation and lack of awareness of the clinical condition among the practicing physicians. Recent advances in magnetic resonance imaging (MRI), superselective spinal angiography, microsurgical techniques, and endovascular therapy have enabled early detection and potential cure of these lesions. Even though embolization is increasingly being performed in these lesions, surgical disconnection of SDAVF is still a treatment option with high success rates. With the use of indocyanine green (ICG), the exact point of shunting the arterial ICG into abnormal venous malformation, refluxing medullary vein and early perimedullary venous filling are clearly visualized [Figure 1]a, [Figure 1]1b and [Figure 2]d, [Figure 2]e. Clipping of the refluxing medullary vein and then re-injecting the ICG dye will demonstrate the absence of early perimedullary venous filling there by confirming the presence and location of medullary vein draining the AV fistula [Figure 1]c, [Figure 1]d and [Figure 4]f. This vein can then be coagulated to obliterate the fistula. Postoperative DSA can be avoided by this.
Figure 1: (a) Intraoperative picture showing dilated coronary venous plexus and possible site of AV shunting (b) ICG angiography confirms the site of fistulous communication (arrow) (c) After application of temporary clip, shows decrease in the engorgement of veins. (d) Post-clipping ICG-VA shows absence of fluorescence from coronary venous plexus

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 » Materials and Methods Top


Patients who were treated for SDAVF in our center from 2005 to 2015 were included. Ethics committee approval was taken prior to the study (IESC/T-12/28.10.2015, RT-11/27.11.2015). The patients who had clinical features of myelopathy underwent MRI [Figure 1]a. Spinal DSA was done in patients who showed intradural T2 flow voids with or without cord edema, to identify the exact type of malformation and level and number of feeding arteries by selective spinal angiography. Management included either surgical ligation or embolization and was decided based on morphology of fistula, feasibility of embolization and patients' choice. The choice of ICG during surgery was decided by availability of a microscope integrated with ICG technology. Details of patients were obtained from hospital records. Follow-up details were obtained from OPD file records, by telephonic questionnaire and by clinical examination.

Microneurosurgery

Surgery involved performing a wide laminectomy, opening the dura, and following the dorsal radiculomeningeal artery as it heads towards the dorsal nerve root and ligating the artery–vein connection by coagulation or clipping. In case of usage of ICG, this arteriovenous connection was clearly visualized under microscope and this area was clipped. ICG angiography was repeated and proper clipping was visualized in the form of absence of early venous filling.

Primary outcome measures

Follow-up was performed by clinical examination, and functional status was measured by use of Aminoff- Logue Scale[2] [Table 1]. Total score is sum of all three variables.
Table 1: Showing Aminoff Logue Score

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Assessment

Analysis I

Group A: Patients treated by any modality without use of ICG

Group B: Patients treated by surgery with ICG.

Analysis II

Group 1: Patients treated by surgery without the use of ICG

Group 2: Patients treated successfully by embolization

Group 3: Patients treated by surgery using ICG.


 » Results Top


A total of 40 patients were treated in the department of neurosurgery and intervention neuroradiology during the period of study. Out of these patients, a total of 33 patients were incorporated in the study as seven patients were lost to follow-up. Of the 33 patients, 27 were male and 6 female. The sex difference between different groups were not statistically significant. The mean age of presentation of the disease was 51 years and did not vary in the individual groups with statistical difference.

Clinical features

The most common presenting symptom was weakness in lower limbs and it was seen in all patients. Urinary symptoms were present in 32 patients (96%), bowel disturbance in 31 patients (93.9%), back pain in 10 patients (30.3%), and sensory loss in 9 patients (27.2%). Upper limbs were not involved in any patient. There was no statistical difference in the presenting symptoms among various groups.

MRI Findings

The most consistent MRI findings were T2 flow voids and T2 cord edema and were seen in all patients [Figure 2]a and [Figure 3]a. Some patients showed patchy enhancement in the cord (33%).
Figure 2: (a) Preoperative MRI sagittal view showing multiple flow voids at dorsal sub arachnoid space, cord hyperintensities, 3 months postoperative image shows no flow voids and resolution of cord changes. (b) AP (c) Lateral view of selective spinal DSA of left internal iliac artery showing fistula with multiple feeders (arrows). (d) Intraoperative picture (e) ICG angiography showing feeder (arrow) (f) No feeders seen following coagulation of all feeders (g) AP (h) Lateral views of postoperative DSA shows no residual

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Figure 3: (a) Preoperative MRI sagittal view showing multiple flow voids at dorsal sub arachnoid space. (b and c) DSA pictures showing location of fistula at RD5 level (arrow)

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DSA Findings

The most common location of the feeder for the fistula was L1 followed by D11 and D6 [Figure 4]. In 20 patients (60.6%) there was a single feeder [Figure 2]b and [Figure 2]2c and in 13 patients (39.39%) there was more than 1 feeder [Figure 4]b and 4c] (Two feeders in eight, three feeders in three, and more than three feeders in two patients).
Figure 4: Bar chart depicting the level of fistula

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Embolization

Among the 33 patients, 13 patients underwent an attempt at embolization at-least once. Among these 13 patients, embolization was not successful in eight patients (61.53%) and these eight patients ultimately needed surgery. Difficult access (38%), multiple feeders (15%), and residual fistula (8%) were the reasons for failure of attempted embolization.

Follow-up

The median duration of follow-up was 58 months; there was no difference in follow-up period of individual groups. The mean change in ALS, gait, bowel function, power, and sensory loss was analyzed statistically and P value was obtained. The improvement was statistically significant irrespective of the mode of intervention.

Analysis I

Comparison between Group A and B: As both the group of patients showed clinical improvement, statistical comparison was carried out using two-sample Wilcoxon rank-sum (Mann-Whitney) test and P value was noted. In view of large standard deviation, median (p50) was used for comparison. We observed that patients treated by surgery using ICG-VA had better improvement in gait, bowel function, ALS and sensory loss which was statistically significant. The improvement in micturition was comparable in both the groups [Table 2].
Table 2: Statistical comparison using two-sample Wilcoxon rank-sum (Mann-Whitney) test between group A and group B

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Analysis II

Comparison of improvement in outcome among the three groups: In order to find out any difference in the group of patients who are treated by any modality without the use of ICG, this group was further subdivided into those treated by surgery without ICG and by successful embolization. The mean change in ALS, gait, bowel function, power and sensory loss was analyzed statistically and P value was obtained. Further inter-group comparison was also carried out. Post-hoc comparison is done by two-sample Wilcoxon rank-sum test by adjusting the level of significance to 0.05÷3=0.0017. Hence a P value of 0.0017 was considered significant in this intergroup comparison and is summarized in the table shown below [Table 3].
Table 3: Comparison of various clinical parameters among group 1, 2 and 3

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The improvement in ALS is better in the patients treated by surgery using ICG compared to the patients treated by embolization or by surgery without ICG usage [Table 4]. But, there was no statistical difference in the outcome of patients treated either by embolization or surgery without using ICG.
Table 4: Table showing inter group comparison of ALS

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Re-intervention after primary procedure: Among the 19 patients treated by surgery without the use of ICG, three patients (15.78%) required reoperation and 1 patient out of the 5 patients treated successfully by embolization required another sitting of embolization, because of an angiographic residual fistula. All the 9 patients treated by surgery with the use of ICG either improved or remained stable.


 » Discussion Top


SDAVFs are the most frequently encountered spinal vascular lesions and one of the treatable vascular causes of progressive myelopathy.[1],[3] SDAVFs are fistulae between dural branch of a radicular artery and a radicular vein along the inner dural sleeve of the dorsal spinal root at the intervertebral foramen.[4] Recent microsurgical study of anatomy of SDAVF by Takai et al. revealed that multiple AV connections from meningeal feeding artery join to form a single proximal radicomedullary draining vein at the inner surface of dural sleeve.[5] The pathologic AV shunt leads to arterialization of the valveless perimedullary venous plexus with resultant reduction in AV gradient and retrograde venous drainage [Figure 5]. The resultant venous hypertension decreases spinal cord perfusion and leads to ischemia and edema, resulting in progressive myelopathy and sometimes, in the spinal cord infarction.[6] The natural history of untreated patients is progressive myelopathy, with 50% of untreated patients likely to be severely disabled at 3 years.[7] Foix and Alajouanine described the clinical entity of subacute myelopathy due to thrombosis of pathologic spinal cord vessels in 1926.[8] Di Chiro et al. proposed the most commonly accepted scheme of classifying them as Type I lesions in 1967.[9]
Figure 5: Diagram showing Type I dural AVF

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It was Aminoff and Logue who were credited with the first large clinical series of patients with SDAVFs in 1974 with its pathophysiology of venous hypertension and proposal of the widely accepted disability scale[2] The classification and terminology of SDAVFs was further modified by Spetzler et al. in 2002 to dorsal intradural AV fistula, in contrast to the high flow (perimedullary) ventral intradural AV fistula.[10]

Dural AV fistulas first become symptomatic in later adult life. The strong male preponderance is well known.[3],[6],[7] Delay in the diagnosis and management leading to very poor clinical status at presentation was observed in our series. Often, patients are diagnosed as degenerative spine disease and have been operated multiple times by other surgeons with obviously no clinical improvement [Figure 6].
Figure 6: Patient diagnosed as Degenerative spine disease with disc prolapse and have been operated multiple times in other centres showing a deformed spine at presentation to us (a and b). DSA done later shows a dural AVF (arrow)

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Song JK et al. in 2001 suggested early treatment of dural AVF as soon as diagnosed because of the progression of spinal deficits once the lesion becomes symptomatic.[11] Early intervention was associated with better outcomes in our study also.

Endovascular intervention carries the limitations of high cost which is a significant factor in developing countries. In our center, many of these patients were from a poor economic background who could not afford the high cost associated with embolization. Endovascular therapy has been associated with a lower initial success rate and higher rate of recurrence than microsurgical therapy.[12] Van Dijk JM et al. in 2002 found a success rate of endovascular therapy to vary between 25% and 75%,[13] whereas a recent meta-analysis suggested complete occlusion of the fistula following surgery in 98%.[12] Andres et al. concluded that both endovascular and surgical treatment of SDAVFs resulted in a good and lasting clinical outcome in the majority of cases, but, when a secondary neurosurgical approach was required after endovascular treatment, the clinical outcome was rather poor.[14] If the glue does not reach the venous site, Krings et al. strongly advocate early surgical intervention because a recent study has shown that patients in whom the endovascular occlusion was incomplete and who required surgical intervention had a bad clinical outcome, which was likely due to the delay of the secondary intervention.[1]

In our study, we found that embolization was not possible in many cases because the embolic agent must pass the nidus and reach and occlude the proximal segment of the draining vein to prevent subsequent intradural collateral filling of the fistula. A spinal DAVF usually consists of multiple dural arterial vessels with a single draining vein. Thus, occlusion of a feeding arterial vessel may lead to recanalization or collateral development in the early postoperative period. Another important consideration is the identification of patients with conditions that would make them unsuitable for endovascular therapy. Embolization therapy may not be feasible if the arterial feeder is too small to catheterize and arterial damage due to catheter manipulation is likely, as in patients with severe arteriosclerosis, or if the anterior spinal  Artery of Adamkiewicz More Details and feeding artery of the fistula originate from the same segmental artery.[7]

Once surgery is planned, usage of ICG is another factor to consider. The advantages of using ICG are that it is noninvasive and considered quite safe, so it can be repeated as needed without associated morbidity. There is no radiation hazard, and it does not require another medical instrument such as a C-arm fluoroscopy. Furthermore, it is very easy to perform ICG-VA, so it can reduce operation time. Finally, because ICG-VA is real-time imaging, rapid feedback is available for vascular intervention to prevent spinal cord ischemic damage. Also, ICG is not nephrotoxic (whereas intravenous contrast used for DSA is nephrotoxic). Hence it can even be used in patients with renal failure. However, it takes time for the ICG to be washed out; therefore, repeat studies are somewhat tedious and time consuming, especially in spinal AVFs with multiple shunts/drainer. In this setting also, using ICG pooling technique, Thorsteinsdottir et al. were able to detect the location of SDAVF more easily.[15] Horie et al., reported two patients of SDAVF treated with the help of intra-arterial ICG angiography to detect the residual shunt/drainer and confirm complete obliteration.[16]

Fontes et al. reported a case of minimally invasive treatment which was aided by ICG.[17] In case of wrong level laminectomy also, the direction of flow of ICG can help in proceeding with the appropriate surgical correction.[18] Killory et al. could identify the location of SDAVF using ICG, in three patients where the fistula was not identified by spinal DSA.[19] Jae Keun Oh et al. in 2011 observed that the only added advantage of intraoperative DSA would be in potentially providing a complete picture of the circulation in the operative field, whereas the ICG technique demonstrates only the vessels visible to the naked eye.[20]

To our knowledge, there are no trials comparing the outcome of surgery without the use of ICG and with use of ICG. Various publications have just emphasized that ICG was crucial in identifying the fistula. But whether it causes any change in the outcome was not shown.

In our study we found better improvement in ALS, gait, bowel and bladder function, sensory improvement in patients who underwent surgery using ICG compared to patients operated without ICG or by embolization.

We observed 0% reoperation rate in patients whom ICG was used, where as it was 15% in patients whose surgery was done without the use of ICG. One patient embolized successfully needed another sitting of embolization. Redo embolization or reoperation was needed either because of clinical recurrence of symptoms or because of angiographic residual.


 » Conclusions Top


The natural course of untreated SDAVF is progressive myelopathy, with loss of bowel and bladder function and if left untreated, patients become permanently disabled and bed ridden. Early diagnosis and treatment of SDAVF can either halt or reverse the progression of disease. Intra-arterial Spinal DSA is a prerequisite for exact localization of the fistula. The treatment can be endovascular or surgical with both causing improvement and stabilization of symptoms. There was a significantly better outcome in patients operated using ICG, than with embolization or surgery without ICG. We found a higher rate of redo surgery in patients operated without the usage of intraoperative ICG. Hence, we suggest that ICG must be used routinely used during surgery in all cases as it objectively shows the exact location of arteriovenous shunting and can tackle multiple feeders effectively. Another advantage of ICG is that there is no need for postoperative check DSA.

Embolization in suitable cases can be tried as an initial treatment option, bearing in mind the higher chance of the procedure being unsuccessful.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

1.
Krings T, Geibprasert S. Spinal dural arteriovenous fistulas. AJNR Am J Neuroradiol 2009; 30:639-48.  Back to cited text no. 1
    
2.
Aminoff MJ, Logue V. The prognosis of patients with spinal vascular malformations. Brain 1974;97:211-8.  Back to cited text no. 2
    
3.
Koch C. Spinal dural arteriovenous fistula. Curr Opin Neurol 2006;19:69-75.  Back to cited text no. 3
    
4.
Jellema K, Tijssen CC, van Gijn J. Spinal dural arteriovenous fistulas: A congestive myelopathy that initially mimics a peripheral nerve disorder. Brain 2006;129:3150-64.  Back to cited text no. 4
    
5.
Takai K, Komori T, Taniguchi M. Microvascular anatomy of spinal dural arteriovenous fistulas: Arteriovenous connections and their relationships with the dura mater. J Neurosurg Spine 2015;23:526-33.  Back to cited text no. 5
    
6.
Dhandapani S, Gupta A, Singh J, Sharma BS, Mahapatra AK, Mehta VS. Spinal dural arterio-venous fistula: Clinico-radiological profile and outcome following surgical occlusion in an Indian neurosurgical center. Neurol India 2013;61:406-10.  Back to cited text no. 6
[PUBMED]  [Full text]  
7.
Thron A, Caplan LR. Vascular malformations and interventional neuroradiology of the spinal cord. In: Brandt T, Caplan LR, editors. Neurological Disorders: Course and Treatment. 2nd ed. Amsterdam: Academic Press; 2003. p. 517-28.  Back to cited text no. 7
    
8.
Foix CH, Alajouanine T. La myelite necrotique subaigue. Rev Neurol 1926;46:1-42.  Back to cited text no. 8
    
9.
Di Chiro G, Doppman J, Ommaya AK. Selective arteriography of arteriovenous aneurysms of spinal cord. Radiology 1967;88:1065-77.  Back to cited text no. 9
    
10.
Spetzler RF, Detwiler PW, Riina HA, Porter RW. Modified classification of spinal cord vascular lesions. J Neurosurg 2002;96(Suppl 2):145-56.  Back to cited text no. 10
    
11.
Song JK, Gobin YP, Duckwiler GR, Murayama Y, Frazee JG, Martin NA, et al. N-butyl 2-cyanoacrylate embolization of spinal dural arteriovenous fistulae. AJNR Am J Neuroradiol 2001;22:40-7.  Back to cited text no. 11
    
12.
Steinmetz MP, Chow MM, Krishnaney AA, Andrews-Hinders D, Benzel EC, Masaryk TJ, et al. Outcome after the treatment of spinal dural arteriovenous fistulae: A contemporary single-institution series and meta-analysis. Neurosurgery 2004;55:77-87, discussion 87-88.  Back to cited text no. 12
    
13.
Van Dijk JM, TerBrugge KG, Willinsky RA, Farb RI, Wallace MC. Multidisciplinary management of spinal dural arteriovenous fistulas: Clinical presentation and longterm follow-up in 49 patients. Stroke 2002;33:1578-83.  Back to cited text no. 13
    
14.
Andres RH, Barth A, Guzman R, Remonda L, El-Koussy M, Seiler RW, et al. Endovascular and surgical treatment of spinal dural arteriovenous fistulas. Neuroradiology 2008;50:869-76.  Back to cited text no. 14
    
15.
Thorsteinsdottir J, Siller S, Dorn F, Briegel J. Use of a new indocyanine green pooling technique for improved visualization of spinal dural AV Fistula: A single-center case series. World Neurosurg 2019;125:e67-73.  Back to cited text no. 15
    
16.
Horie N, So G, Debata A, Hayashi K, Morikawa M. Intra-arterial indocyanine green angiography in the management of spinal arteriovenous fistulae: Technical case reports. Spine (Phila Pa 1976) 2012;37:E264-7.  Back to cited text no. 16
    
17.
Fontes RB, Tan LA, O'Toole JE. Minimally invasive treatment of spinal dural arteriovenous fistula with the use of intraoperative indocyanine green angiography. Neurosurg Focus 2013;35 (2 Suppl):Video 5. doi: 10.3171/2013.V2.FOCUS13191  Back to cited text no. 17
    
18.
Paolini S, Severino R, Cardarelli G, Missori P, Bartolo M, Esposito V. Indocyanine green videoangiography in the surgical treatment of spinal dural arterovenous fistula: A useful application. World Neurosurg 2019;122:508-11.  Back to cited text no. 18
    
19.
Killory BD, Nakaji P, Maughan PH, Wait SD, Spetzler RF. Evaluation of angiographically occult spinal dural arteriovenous fistulae with surgical microscope-integrated intraoperative near-infrared indocyanine green angiography: Report of 3 cases. Neurosurgery 2011;68:781-7.  Back to cited text no. 19
    
20.
Oh JK, Shin HC, Kim TY, Choi GH, Ji GY, Yi S, et al. Intraoperative indocyanine green video-angiography-spinal dural arteriovenous fistula. Spine (Phila Pa 1976) 2011;36:E1578-80.  Back to cited text no. 20
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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