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 Table of Contents  
Year : 2021  |  Volume : 9  |  Issue : 1  |  Page : 25-28

Visual techniques in microsurgery for intra-cranial arteriovenous malformations

Department of Neurosurgery, National Neurosciences Mission, Adarsha Super-Specialty Hospital, Manipal-Udupi, Karnataka, India

Date of Submission17-Jul-2021
Date of Decision18-Jul-2021
Date of Acceptance29-Jul-2021
Date of Web Publication27-Aug-2021

Correspondence Address:
Dr. Sumeet Narang
Department of Neurosurgery, National Neurosciences Mission, Adarsha Super-Specialty Hospital, Manipal-Udupi, Karnataka
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcvs.jcvs_18_21

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Arterio-venous malformations (AVMs) are anomalous shunts between the arterial and venous systems, acting as a major risk factor for intra-cerebral haemorrhage, seen in 38%–71% of patients harbouring the pathology. Current techniques in the management of AVMs include observation, microsurgery, embolisation and radiosurgery, or combination therapy. AVMs are classically categorised based on the Spetzler-Martin grading and it is generally accepted that Grades I and II are best managed by microsurgical resection. To discuss the technique of astute visual inspection of AVM malformations on the operating table in microsurgical management of AVMs, and the surgical importance and significance of the valuable inferences derived from this routine. It is of utmost importance to visually distinguish between the arterial and venous ends of the nidus, and this can be effectively accomplished through eyeballing techniques by looking at the appearance of the vessels and noticing its colour, thickness, and underlying blood; and the variations in the turgor pressure of the nidus with changes in compression of the arterial and venous ends. It is equally important to visually identify the safe and effective plane to approach the target lesion by identifying the gliotic plane, the discoloured vertex of the underlying haematoma, or the widened subarachnoid spaces. Microsurgical resection is a definite mode of treatment of intra-cranial AVMs and flawless execution of surgery is vital. Eyeballing techniques must be aimed at correctly identifying the nature of the lesion and creating a mind-map before setting out to manipulate the AVM. A good initial visual inspection and survey is a crucial measure of safety and efficiency in AVM surgery.

Keywords: Arteriovenous malformation, microsurgery, technique

How to cite this article:
Narang S, Dil JS, Raja A. Visual techniques in microsurgery for intra-cranial arteriovenous malformations. J Cerebrovasc Sci 2021;9:25-8

How to cite this URL:
Narang S, Dil JS, Raja A. Visual techniques in microsurgery for intra-cranial arteriovenous malformations. J Cerebrovasc Sci [serial online] 2021 [cited 2023 Mar 28];9:25-8. Available from: http://www.jcvs.in/text.asp?2021/9/1/25/324814

  Introduction Top

Arteriovenous malformations (AVMs) of the brain are anomalous arteriovenous shunts comprising tangles of dysplastic cerebral arteries and veins that converge at a vascular nidus without normal intervening parenchyma.[1]

Intracerebral haemorrhage is the most common clinical presentation of AVMs, followed by seizures, headaches or focal neurological deficits.[1],[2]

The determinant for the treatment of brain AVMs is the balance between the cumulative risk of morbidity and mortality if the pathology is allowed to take its natural course, versus if it is treated. This is an ongoing discussion in neurological practice.

The goal of AVM intervention is complete endo-luminal closure or obliteration of the nidus. To achieve this, current management options for patients with AVM include observation, surgical resection, embolisation and stereotactic radiosurgery (SRS), or multimodality treatment strategies.

Microsurgical resection is a mainstay in the treatment of AVMs, and is most widely carried out based on the gold standard Spetzler-Martin 5-tier grading of AVMs [Figure 1], which serves as a classification of the lesion and a prognosticator for the surgical outcome, and has now been modified into the Spetzler-Ponce 3-tier classification.[1],[2],[3],[4]
Figure 1: Spetzler and martin grading of arterio venous malformations[3]

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The microsurgical approach to AVMs is interesting and also technically challenging when dealing with the nidus. A rightly approached lesion and thoughtfully executed procedure could bring about highly favourable results.


To discuss the technique of astute visual inspection of AVMs on the operating table in microsurgical management of AVMs, and the surgical importance and significance of the valuable inferences derived from this routine.

  Methods Top

Hospital-Based Retrospective Observational Study of patients admitted to the National Neurosciences Mission, Adarsha Super-specialty Hospital, (Manipal-Udupi, Karnataka, India), with intracranial AVMs as diagnosed clinically and radiologically through computed tomography, magnetic resonance imaging and angiograms, managed by microsurgical approach.

  Discussion Top

The basic pathophysiology of an AVM that is allowed to follow its natural course, arises from the disturbances in the normal vascular pattern of the brain. The direct communication of arteries to the veins, without the presence of arterioles, capillaries and venules, allows the arterial blood to bypass the pressure regulating vascular bed, and directly enter the thin-walled, wide lumen veins. The nidus becomes a ticking time bomb pre-disposed to rupture due to the high pressure within it, leading to intracerebral haemorrhage. Intra-cerebral haemorrhage is the most common clinical presentation of AVMs, seen in 38%–71% of patients with AVMs. Intracerebral haemorrhage has been seen to occur in 2.2% of unruptured AVMs and 4.5% of ruptured AVMs. Apart from this, disturbances in the normal vasculature exerts loco-regional effects on the brain due to hypo-perfusion and 'cerebral steal' causing other clinical manifestations such as seizures, which is the second-most common clinical presentation of AVMs is seizures, seen in 18%–40% of cases, with a 58% risk of developing epilepsy. Other presentations include headache and focal neurological deficits.[1],[2]

The primary intention of treatment of AVMs is to reduce the risk of life-threatening haemorrhage occurring spontaneously with the AVM in situ, or to prevent them from recurring in patients diagnosed after experiencing symptoms.[1],[2],[3]

The technical goal to achieve satisfactory treatment is to eliminate the abnormal shunt by completely obliterating the flow in the nidus while preserving the vascularity of the surrounding brain.

The major determinant for the treatment rests upon the objective comparison between the risks of developing morbidity or mortality from the pathology versus what may occur from the planned therapeutic procedure.

The oldest standard approach to treat identified AVMs, was once upon a time, always surgery. In the year 1986, Spetzler and Martin published their grading of AVMs which classified the nature of the lesion while also categorically defining the degree of difficulty of surgical approach for resection. AVMs were classified based on their size, pattern of venous drainage, and neurological eloquence of the surrounding brain, each parameter assigned a numerical score value, so that they were classified into six types, which were also correlated with the surgical results [Figure 1]. Patients who had lower scores had better post-operative results, and vice versa.[3],[4]

With time and advancement in medical technology, embolisation and SRS became acceptable techniques for treatment as they could achieve the same technical goals, and were implemented as stand-alone approaches and also as part of combined approaches, each having their advantages and disadvantages.[1],[2],[3]

The availability of more options than guidelines led to the initiation of several large-scale studies to deliver data for consensus in the management of AVMs, notable amongst them being 'A Randomised trial of Unruptured Brain Arteriovenous malformations' (ARUBA) trial, the Scottish Audit of Intracranial Vascular Malformations (SAIVM) and the Multicenter AVM Research Study are notable.[5],[6],[7],[8],[9]

Although the ARUBA study showed that medical management alone was superior to intervention in the prevention of stroke in unruptured AVMs, microsurgical resection remains preferred and reliable and even indicated in achieving complete obliteration with minimal morbidity and mortality. Surgical series of unruptured AVMs reported superior outcomes compared with ARUBA for low-grade AVMs, with obliteration rates of nearly 100% and permanent neurologic deficits rates of <4%. Compared with other interventions, resection affords the highest rate of seizure freedom, as well as the shortest interval to achieving this endpoint, in patients with AVM with pre-treatment seizures. In the SAIVM AVM study, the obliteration rates for embolisation versus resection were 45% versus 83%, respectively. In ARUBA, the obliteration rates for embolisation versus resection were 50% versus 100%, respectively.[5],[6],[7],[8],[9]

It has been generally concluded by most studies and accepted that Spetzler-Martin Grades I and II have low surgical risk and microsurgery is recommended. Spetzler-Martin Grade III has intermediate risk, for which multimodality treatment is recommended, and Spetzler-Martin Grades IV and V have high risk for which observation is preferred.[3],[10],[11],[12],[13],[14],[15],[16]

Realising that microsurgical resection is here to stay, as seen from the positive results from the series of stalwarts such as Drake, Spetzler and Martin, Yasargil, Hernesniemi, and even from current data, we do not intend to argue on the pros and cons of other modalities of treatment or seek to assert any superior, or lay down an iron fist on the management of AVMs, but to focus on few key things about microsurgery that must be reiterated and reinforced for the practicing cerebrovascular surgeon.[10],[11],[12],[13],[14],[15],[16]

As previously mentioned, AVM surgery is technically challenging. The stepwise goals of this intervention are wide exposure of the relevant anatomy, occlusion of the feeding arteries while preserving en-passage vessels, circumferential dissection of the lesion, disconnection of the draining veins, and finally en-bloc extirpation of the nidus.[10],[11],[12],[13],[14],[15],[16]

The major difficulties arise from operating on a highly vascular site with limited anatomical access. Therefore, focused and trained inspection of the AVM nidus itself and the surrounding brain is not just important but also extremely useful in allowing the surgeon to proceed with certainty. Correct observation and re-observation as much as possible leads to proper identification of the vascular structures and recognition of the operative target and the nature of the lesion.

The first distinction that must be made, is visual differentiation of the arteries and the veins in the AVM nidus. Certain differences are obvious and basic, but must not be under-valued.

Externally, arteries appear thicker, attributable to the tunica media, unlike veins, which, in contrast, appear to have thinner walls.

Though one expects the veins to appear bluish, this is not the case with an AVM. Arterial blood directly enters the wide lumen, thin-walled veins, and hence the veins appear to be redder from the blood flowing within it, while arteries appear white as the blood within is not visible. Under the operating microscope, it is even possible to see the flow of the blood within the vein, while it is not possible to see the blood within the artery.

This information, though valuable, is not enough for the surgeon to proceed with definitive manual steps such as ligation of the vessels. To be sure, one may employ temporary clips and observe the changes in the turgor pressure of the nidus. Placing a clip on the arterial side of the nidus prevents it from filling, and hence the turgor pressure of the nidus is reduced and the lesion appears comparatively flaccid. On the other hand, if the clip is placed towards the venous side, this would prevent only the outflow from the nidus, but not the inflow from the arterial end, and therefore, the turgor pressure of the nidus appears to be increased and the lesion appears to be more turgid. Similarly, this can also be appreciated, if the vessel is held between the prongs of a bipolar cauteriser: Filling up of the lesion suggests that one has obstructed its outflow, and is therefore handling a venous channel exiting the lesion.

One might have grossly recognised the lesion and constructed a mental plan on how to deal with it, but how does one approach the malformation? The location of an AVM is not constant and this variability and the association of the AVM with the neurological eloquence, is such an important surgical parameter, as is obvious from its incorporation into the Spetzler-Martin grading system.

In the case of an AVM that has previously ruptured and bled either once or repeatedly, the surrounding brain undergoes gliotic changes which results in the formation of a visually distinct appearance in comparison with the normal brain. In AVM surgery, identifying the gliotic plane and approaching the AVM through this plane, is the safest and best method of approach.

If an AVM has ruptured and resulted in an intracerebral haemorrhage, correlating the site of the haemorrhage from radiological findings with that of the brain on-table, one might notice that there is a physiological discolouration at the vertex of the location of the haematoma. This vertex also serves as a safe point of entry to the lesion.

Old AVMs and the associated regional effects that it has produced through its natural course, cause atrophic changes in the brain. Such regions of the brain, especially at the surface, that have undergone cortical atrophy, reveals grossly visible dilated subarachnoid spaces. These regions provide more space to enter.

All the above points have been reviewed [Table 1] to highlight the importance as correctly approaching an AVM and mindfully dealing with such a lesion. This is not only to prevent undue retraction in attempting to reach the lesion, or reduce untoward circumstances and minimise surgical complications but also to remind the surgeon, the necessity of proper planning and having a mind-map in place, in performing excellent surgery.
Table 1: Summary of eyeballing techniques in arterio-venous malformations microsurgery

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  Conclusion Top

Although the management of AVMs is still a topic of discussion with space for more data and research, microsurgical resection is a definite mode of treatment and flawless execution of surgery is vital in bringing about faith in its effectiveness.

Stringent obedience to classical rules and basic surgical teaching is important. Visual cues and eyeballing techniques cannot be undermined in the surgeon's approach to the pathology. Eyeballing must be aimed at correctly identifying the nature of the lesion and creating a mind-map before setting out to manipulate the AVM. A good initial visual inspection and survey is a crucial measure of safety and efficiency in AVM surgery.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Chen CJ, Ding D, Derdeyn CP, Lanzino G, Friedlander RM, Southerland AM, et al. Brain arteriovenous malformations: A review of natural history, pathobiology, and interventions. Neurology 2020;95:917-27.  Back to cited text no. 1
Unnithan A. Overview of the current concepts in the management of arteriovenous malformations of the brain. Postgrad Med J 2020;96:212-20.  Back to cited text no. 2
Spetzler RF, Martin NA. A proposed grading system for arteriovenous malformations. J Neurosurg 1986;65:476-83.  Back to cited text no. 3
Spetzler RF, Ponce FA. A 3-tier classification of cerebral arteriovenous malformations. Clinical article. J Neurosurg 2011;114:842-9.  Back to cited text no. 4
Mohr JP, Koennecke HC, Hartmann A. Management of brain arteriovenous malformations: Still a long and winding road ahead. Neurology 2020;95:899-900.  Back to cited text no. 5
Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, et al. Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): A multicentre, non-blinded, randomised trial. Lancet 2014;383:614-21.  Back to cited text no. 6
Mohr JP, Overbey JR, Hartmann A, Kummer RV, Al-Shahi Salman R, Kim H, et al. Medical management with interventional therapy versus medical management alone for unruptured brain arteriovenous malformations (ARUBA): Final follow-up of a multicentre, non-blinded, randomised controlled trial. Lancet Neurol 2020;19:573-81.  Back to cited text no. 7
Al-Shahi Salman R, White PM, Counsell CE, du Plessis J, van Beijnum J, Josephson CB, et al. Outcome after conservative management or intervention for unruptured brain arteriovenous malformations. JAMA 2014;311:1661-9.  Back to cited text no. 8
Kim H, Al-Shahi Salman R, McCulloch CE, Stapf C, Young WL; MARS Coinvestigators. Untreated brain arteriovenous malformation: Patient-level meta-analysis of hemorrhage predictors. Neurology 2014;83:590-7.  Back to cited text no. 9
Drake CG. Cerebral arteriovenous malformations: Considerations for and experience with surgical treatment in 166 cases. Clin Neurosurg 1979;26:145-208.  Back to cited text no. 10
Yasargil MG. Microsurgery Applied to Neurosurgery. Stuttgart, Georg Thieme; 1969. p. 105 19.  Back to cited text no. 11
Hernesniemi J, Romani R, Lehecka M, Isarakul P, Dashti R, Celik O, et al. Present state of microneurosurgery of cerebral arteriovenous malformations. Acta Neurochir Suppl 2010;107:71-6.  Back to cited text no. 12
Raja A. Musings about surgery for intra-cranial arterio-venous malformations. J Cerebrovasc Sci 2020;8:55-7.  Back to cited text no. 13
  [Full text]  
Söderman M, Andersson T, Karlsson B, Wallace MC, Edner G. Management of patients with brain arteriovenous malformations. Eur J Radiol 2003;46:195-205.  Back to cited text no. 14
Mattle HP, Schroth G, Seiler RW. Dilemmas in the management of patients with arteriovenous malformations. J Neurol 2000;247:917-28.  Back to cited text no. 15
Lawton MT, Lang MJ. The future of open vascular neurosurgery: Perspectives on cavernous malformations, AVMs, and bypasses for complex aneurysms. J Neurosurg 2019;130:1409-25.  Back to cited text no. 16


  [Figure 1]

  [Table 1]


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