Intraoperative microvascular dopplerography in surgery of superficial arteriovenous malformations localized in eloquent areas of the brain

Semenyutin V.B., Nikitin P.I., Govorov B.B.

Russian Polenov Neurosurgical Institute Saint Petersburg, Russia

Modern technologies of intraoperative color duplex sonography (DS) allow to localize AVM, to identify its feeding and draining vessels, as well as to estimate radicality of its removal [1, 10, 15, 21, 22]. At the same time this method has some limitations, as it fails to identify vessels with a diameter of less than 1 mm or superficial vessels [21]. These limitations are of principal importance in surgery of superficial arterrio venous malformation (AVM), localized in eloquent areas, and can be overcome with the help of microvascular Doppler examination [3]. Special probes (a diameter of 1-3 mm and length of 10 mm) permit to study blood flow in vessels with a diameter of 0.5-1 mm. This method can be used while performing interventions for AVM, as a means of identification of transit vessels, which supply functionally important cerebral structures with blood and whose lesion can result in disability of a patient.

The study goal was to estimate potentialities of microvascular dopplerography in identifying afferent (feeding), efferent (draining) and transit vessels and controlling totality of resection of superficial AVM, localized in eloquent areas of the brain.

Material and Methods

We examined 14 patients with superficial cerebral AVM, localized in eloquent areas. Their clinical description is given in table 1.

Table 1

Clinical Description of Patients with Superficial AVM of eloquent areas of the Brain

 

Clinical Data

Age/sex

Localization

Grades accord.
to Spetzler, Martin [18]

Intracranial
hemorrhage

Seizures

Hemiparesis

Visual field defect
(hemianopsia)

Headache

1 (38/f)

occipital

3

+

+

-

+

-

2 (15/m)

frontal

2

+

-

+

-

-

3 (30/m)

temporal

2

-

+

-

-

-

4 (34/m)

frontal

3

-

-

-

-

+

5 (36/m)

frontal

3

+

-

+

-

-

6 (20/m)

frontal - temporal

3

-

+

+

-

-

7 (17/m)

frontal - parietal

3

-

+

-

-

-

8 (45/m)

frontal

2

-

+

-

-

-

9 (35/f)

occipital

2

+

-

-

+

-

10 (12/f)

parietal

2

-

+

+

-

-

11 (31/m)

frontal

2

+

-

-

-

-

12 (27/f)

frontal

2

+

-

+

-

-

13 (21/m)

frontal

3

-

+

-

-

-

14 (43/f)

parietal

3

-

+

-

-

-

All patients underwent microsurgical removal of AVM. Osteoplastic trephination was made in projection of AVM. An operating microscope with 6-12 fold magnification (Opton, Japan) was used. After opening of dura mater, which often adhered to thickened, pale arachnoid, one could see AVM's vessels and body rather well. The adjacent brain was atrophic in many cases and had signs of sustained hemorrhages in the form of hemosiderosis and/or cysts of a different size. The latter facilitated AVM's exposure and allowed to remove it without resection of intact areas of the brain. Sometimes it was impossible to distinguish between afferent and efferent vessels, as they had the same deep-red color due to an effect of arterial blood; their diameter was approximately equal; as for localization (a parallel path), it hampered their identification rather often. Visual diagnosis of transit vessels was a serious problem. Sometimes these vessels were located in cerebral fissures and had an identical color and diameter. Approaching AVM's body and simulating an afferent vessel, a transit vessel could change its direction rather sharply and move into the depth of the brain substance without taking part in blood supply of AVM.

Blood flow velocity (BFV) in afferent, efferent and transit vessels was recorded before and after removal of AVM. It was done with the help of microvascular Doppler [3], using a 20 MHz probe (Multi Dop X system, DWL, Germany) and an original device. The latter allowed to change an angle between the probe axis and a vessel under examination, as well as to fix the probe butt-end on its wall (fig.1).

Results

Data on microvascular 20 MHz dopplerography (MVD), used for examination of afferent, efferent and transit vessels before and after AVM removal, are presented in table 2.

MVD, used before AVM removal. Spectra, representing patterns typical of a shunt and characterized by high parameters of BFV and a low value of pulsatility index (PI), were recorded in afferent vessels of 11 out of 14 patients (fig.2A). The more a diameter of a vessel was, the higher BFV. Mean BFV was within the limits of 33-95 cm/s (56.5±17.3); PI varied from 0.26 up to 0.66 (0.40±0.12). We failed to measure blood flow in afferent vessels in one patient (case 5), as it was impossible to expose them before AVM removal. Identification of afferent vessels on the basis of sharp increase of their BFV turned out to be unachievable in 2 cases (cases 11 and 12), because its value was not higher than 20 cm/s, i.e. it corresponded to normal indices [3, 21]. There was reduction of PI in all examined vessels of both patients; however, we managed to identify afferent vessels only after AVM removal.

Spectra of BFV in draining vessels of all 14 patients were characterized by a marked arterial pattern (fig.2B). Mean BFV and PI varied from 4 up to 44 cm/s and from 0.2 up to 0.65 respectively (table 2).

Transit vessels were identified in 10 out of 14 cases. Values of BFV (13.2±3.9 cm/s) and PI (1.10±0.19) were normal (table 2, fig.2C). The only exception was the 14th case with identified afferent vessels and vessels, in which BFV was three times lower and PI was considerably higher. It appears, that they should be attributed to vessels, defined by Hassler [3] in his classification as "partly AVM supplying".

MVD, used after AVM removal. After AVM removal spectra of BFV in afferent vessels of 9 patients were characterized by low-amplitude spike signals, confirming absence of blood flow (table 2). It seems, that these vessels should be ascribed to a group, defined by Hassler [3] as "exclusively AVM supplying". BFV in afferent vessels of 5 patients reduced to normal and subnormal values (fig.3A). As a rule, PI was considerably higher, than a unity (1.18-1.55). It allowed us to use the terms "mainly AVM supplying" and "partly AVM supplying" (Hassler's classification [3]) for description of afferent vessels in cases 1, 9 and 14 (table 2) and cases 3 and 10 (table 2) respectively.

After AVM removal mean BFV and PI in efferent vessels of all patients reduced up to 5.0±1.0 cm/s and 0.25±0.07 respectively (table 2). Reduction of BFV was accompanied by disappearance of an arterial component in its spectrum. The observed pattern was typical of normal veins (fig.3B). Disappearance of the arterial component in BFV spectrum of efferent vessels was indicative of AVM total removal.

BFV and PI in transit arteries did not undergo considerable changes in 9 out of 10 cases (table 2). Thus, it is possible to conclude, that these arteries supplied only cerebral structures and had nothing to do with AVM (fig.3C). BFV reduction and PI growth in transit vessels of one patient (case 14) confirm an assumption, put forward in MVD examination before AVM removal. According to it, these vessels can be described with the term "partly AVM supplying" (Hassler's classification [3]).

Control angiographic examination, carried out on discharge, was indicative of AVM total exclusion from blood circulation. There was no aggravation of neurologic symptoms; their partial regress in the nearest postoperative period was watched in 9 out of 14 patients. It manifested itself in greater strength in extremities (cases 2, 5, 6, 12), smaller rate of seizures (cases 1, 3, 7, 8), headache absence (case 4).

Discussion

Use of up-to-date microsurgical technique for removal of AVM, localized in eloquent areas of the brain, permits to perform its total resection and to minimize possibility or recurrent hemorrhages from its residues [9, 14, 23]. Thus, maximum preservation of cerebral structures, surrounding AVM, is the first-priority problem. According to various authors, its solution lies in use of different methods for estimating a functional state of these structures [2, 5, 6, 7, 8, 11, 17, 19, 20] and blood flow in vessels of AVM and surrounding areas [1, 3, 4, 13, 15, 16, 24].

Intraoperative identification of AVM is often based on images, obtained with the help of DS. They allow to diagnose AVM and to provide highly precise and safe navigation. Besides, this method helps to identify afferent and efferent vessels of AVM [1, 12, 15, 21, 22]. Some authors emphasize possibility of intraoperative confirmation of AVM resection [1, 15, 21]. At the same time the method has several drawbacks, connected with impossibility to identify vessels with a diameter of less than 1 mm or superficial vessels with a greater diameter. It does not allow to estimate blood flow in afferent and efferent vessels of small AVM, localized in eloquent areas of the brain, as well as in transit arteries, going along the brain surface in the depth of fissures [21].

MVD, carried out according to W. Hassler [3], and use of an original device (fig.1) permitted to identify afferent, efferent and transit vessels on the basis of BFV and PI data; practically, it was irrespective of their localization and diameter. At the same time we failed to get necessary data in some cases, when afferent and draining vessels were localized at a considerable depth. However, it had no effect on results of surgical treatment. DS, used in such cases, was an effective additional modality, which reduced a degree of uncertainty in AVM resection. BFV variations in afferent vessels (33-95 cm/s) were in compliance with their classification, worked out and suggested by W. Hassler [3]. After AVM removal (totality of resection was controlled on the basis of disappearance of an arterial component in all draining vessels) blood flow in vessels, defined as "partly AVM supplying", was reduced to a great extent; but nevertheless it was preserved. This fact, as well as preservation of patency of transit arteries, are of extreme importance from the point of view of normal perfusion of cerebral structures.

Thus, the obtained data and published reports prove expediency of combining MVD with color duplex sonography in intraoperative monitoring, carried out during resection of AVM, localized in different (not only superficial) "functionally important" areas of the brain.

Conclusions

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