Preoperative Embolization of Extra- and Intracranial Tumors

D.V. Svistov, D.V. Kandyba, A.V. Savello, A.U. Benshaban, S.A. Landik

Medicomilitary Academy Saint Petersburg, Russia

 

Introduction

Despite development of modern surgical technologies, removal of hypervascularized tumors of the brain and skull base is still a complicated problem. The rates of postoperative mortality and disability are rather high and equal 3-7% [5, 7].

Main causes of unfavorable outcomes in removal of meningeal-vascular tumors and hypervascularized neoplasms of a skull base include marked blood loss, intraoperative damage of major arteries, impaired blood supply and brain edema, secondary disorders of hemostasis. The most severe bleeding is watched at the stage of performing an approach and during menigioma removal [2, 3, 6, 8].

Many authors stick to the opinion, that preoperative embolization of hypervascularized extra-intracranial tumors is a method, preventing intraoperative bleeding. Its main purpose is selective obliteration of a tumor vascular network and preservation of blood supply in intact tissues. Preoperative exsanguination of neoplasms is of particular importance, when they are localized in difficult-of-access areas, for example a skull base.

Preoperative embolization leads to diminishing a tumor volume and, as a result, its easier removal and a smaller risk of tumor cells' penetration into systemic blood flow during intervention. Besides, it allows to perform more extensive resection, to avoid double-stage interventions, to reduce operation time and intraoperative blood loss and to make an intervention less traumatic. In case of incurable tumors embolization can be used as a palliative means, permitting to inhibit a tumor growth, to achieve temporary stabilization of clinical symptoms, to eliminate a risk of bleeding, to reduce severity of pain syndrome [11, 12, 14].

The Study's Goal: Retrospective analysis of results, obtained after preoperative embolization of neoplasms of the brain and skull base.

Materials and Methods

There were 52 patients (30 males and 22 females) with hypervascularized extra- and intracranial tumors, treated at the Chair of Neurosurgery of the Medicomilutary Academy in 1998-2003. They were 14-74 years old (a mean age - 42 years). All the cases were divided into two groups.

The first group comprised 35 patients with intracranial neoplasms (a mean age - 49 years). The majority of them had meningiomas (91%). Their distribution was as follows: meningiomas of a skull base - 13 cases (37%), meningiomas of a skull fornix - 11 cases (31%), parasagittal meningiomas - 5 cases (14%), meningiomas of a cerebellar tentorium - 3 cases (9%). Two patients (6%) had chemodectoma of a jugular glomus. There was meningomatosis of a cerebral hemisphere in 1 case.

The second group consisted of 17 patients (a mean age - 28 years), who had neoplasms of a skull base, characterized mainly by extracranial spread. There were nasopharyngeal angiofibromas (14 cases, 82%), hemangiomas (2 cases) and cancer of an upper jaw (1 case).

On admission all the patients underwent CT- and MRI-examinations of the brain and skull base. Their purpose was as follows: Tumor primary diagnosis; determination of its localization; estimation of its topographic- anatomic version and relationships with adjacent bone structures, major vessels, brain and its meninges; assessment of localization and spread of exophytic growth foci; planning of angiographic study. Contrast study helped to evaluate a degree of tumor vascularization on the basis of the enhancement index increase (growth of neoplasm density by more than 20 HU) and to reveal presence of big vessel and vascular regions, involved into a tumor. In some cases perfusion CT with determining blood flow indices in a tumor was used for estimation of a degree of its blood supply. "Fervid" tumor nodes with volumetric blood flow velocity of more than 60ml/min/100 ml of tissue and tissue blood volume, exceeding 6%, were considered to be indications for angiography with probable embolization.

Digital subtraction angiography was used in all the cases. It was carried out with the help of Polystar-II and Angiostar Plus apparatus (Siemens). The purpose was determining a degree of intensity of tumor blood supply, sources of blood supply and estimating a state of major cerebral arteries and veins.

Selective angiography was performed transfemorally according to Seldinger's method with applying 4-6 F diagnostic catheters. Catheterization and angiography of regions of the internal (ICA) and external (ECA) carotid arteries were carried out separately. If there were indications for embolization of branches of the ICA cavernous segment, a state of collateral blood supply in the same region was estimated. When blood supply sources and peculiarities of tumor vascular anatomy had been determined, a diagnostic catheter was replaced by a cerebral guide. Superselective catheterization and angiography of the ECA separate branches were performed under conditions of systemic heparinization (2500-5000 U). MAGIC 3 F/1.8 F-1.2 F catheters, Prowler 1.9-2.3 F (Cordis), Vasco 10-18 (Balt) rigid catheters were used with SORCERER 0.007"-1.012" microguides.

Selective angiography allowed to obtain information on tumor blood supply (a type, quantity, geometry of feeding arteries, blood flow parameters), a degree of compartmentalization of tumor blood supply, presence/absence of arteriovenous anastomoses within a tumor, a direction and type of blood drainage from a tumor, presence of arteriovenous anastomoses in a system of carotid and vertebral arteries, participation of dermal or neural vessels in tumor blood supply.

Superselective embolization (SSE) was carried out immediately after angiographic examination and pharmacological testing (if necessary) of functional significance of an embolized region. SSE was performed with polyvinylacetate microparticles (Trufill 45-350m), gelatin microspheres (Embosphere 40-300m), liquid embolizing materials (a mixture of Hystoacryl with Lipiodol, being a liposoluble contrast substance, in a ratio of 1:2-1:6; Embolin), microspirals.

Embolization results were estimated on the basis of rentgenologic findings. Angiographic examination of the carotid region was carried out just after embolization. Control CT-examination with enhancing, MRI- and perfusion CT-examinations took place during the first 7 days after embolization. Clinical assessment lied in observing changes of neurologic symptoms during and after embolization. Intraoperative evaluation included a surgeon's subjective opinion and determining a degree of blood loss. Conventional methods were used for histological study of a removed substrate.

Results

Intracranial tumors, watched in the first group, were supplied mainly from the ECA region (25 cases); both external carotid arteries took part in blood supply in 4 of these patents. A tumor, localized in medial segments of the sphenoid bone wing and watched in 2 cases, was supplied with blood from the meningohypophyseal trunk only. Mixed blood supply from the ICA and ECA regions was observed in 8 patients.

Tumors of all the patents of the second group were supplied with blood from the ECA region; both ECA took part in this process in 4 of them. The distribution of participants of blood supply was as follows: maxillary arteries - 13 cases, ascending pharyngeal arteries - 4 cases, branches of the facial artery - 5 cases, the superior thyroid artery - 1 case.

A number of catheterizations and a type of catheterized arteries are presented in Table 1. As for embolization of itracranial tumors in patients of the first group (29 cases), the most frequent object of superselective catheterization was the middle meningeal artery (Fig.1). SSE of this artery was performed on both sides in 4 cases (Fig.2). Catheterzaton and embolization of the middle meningeal artery was accompanied by embolizaton of the deep maxillary artery or its branches in 4 patients. Simultaneous embolizaton of the middle meningeal artery and branches of the deep temporal artery, feeding a tumor, was performed in 2 cases. Superselective catheterization and embolization of the maxillary artery was carried out in 7 cases. One patient underwent catheterization and embolization of the ascending pharyngeal and occipital arteries. Embolization of the hypertrophied meningohypophyseal trunk, feeding meningioma of medial segments of the sphenoid bone wing, was performed in 3 cases (Fig.3), (Fig.4).

Table 1

A Number of Catheterizations of Feeding Arteries

The Artery's Name

The First Group

The Second Group

a. meningea media

33

-

a. maxillaris

7

16

a. pharyngea ascendens

1

5

a. facialis

1

2

a. carotis interna, r.meningohypophysalis

3

-

a. temporalis superficialis

1

-

a. temporalis profunda

2

-

a. auricularis posterior

1

-

a. occipitalis

1

-

a. thyroidea superior

-

1

a. sphenopalatina

-

2

TOTAL

50

26

The maxillary artery was catheterized most frequently (16 times) in 13 patients of the second group (.5). Catheterizaton and embolization was performed on both sides in 3 cases. The ascending pharyngeal artery was catheterized 5 times (4 patients). The sphenopalatine and facial arteries were subject to catheterization 2 times. Catheterization of the superior thyroid artery was performed only once (Table 1).

A tumor vascular network was embolized either by one embolizing substance or a combination of different substances. These substances and their combinations are described in Table 2.

Trufill 45-350m microspheres of polyvinylacetate (Cordis, USA), a glue composition, being a mixture of Hystoacryl with liposoluble Lipiodol (a ratio of 1:2-1:6), were used for embolization most frequently. Among other applied substances one can mention Embolin, Tungstene (microemboli) and Embosphere (microspheres). A substance was introduced until there appeared a "contrast-stop" phenomenon in a feeding artery. Embolization of branches of the ICA cavernous segment with TruFill 45-150m microemboli (Cordis, USA) was performed under conditions of temporary balloon-occlusion of the ICA in 3 cases. SSE of tumor vessels with free microspirals was carried out in 1 case, as use of microparticles could result in embolism of the central artery of the retina. As for the rest cases, microspirals were used for reduction of intraoperative bleeding from the maxillary artery after SSE of a tumor vascular network.

Table 2

Substances for Embolization of a Tumor Vascular Network

 

The First Group

The Second Group

TruFill

10

3

Hystoacryl + Lipiodol

10

2

Embolin

11

1

Free microspirals

-

1

Combinations:

4

8

TruFill + microspirals

2

4

Hystoacryl:Lipiodol + microspirals

1

-

EVAL + hemostatic sponge

1

-

Trufill + Hystoacryl:Lipiodol

-

1

Embolin + microspirals

-

1

TruFill + balloon-occlusion

-

1

Tangstene + hemostatic sponge

-

1

TOTAL

35

17

A degree, to which a tumor vascular network was filled, presence of a "contrast-stop" phenomenon in a vessel under embolization, position of radiopaque deposits of an embolizing substance in tumor tissue served visual signs of radical embolization in control angiographic study.

Total embolization of a tumor vascular network was achieved in 29 cases (56%). It was watched in 18 patients (51%) of the first group. The rate of total embolization in cases of the second group was much higher (11 cases, 65%). Preservation of tumor blood supply from major afferent arteries in the first and second groups was watched 8.5% and 17.5% of cases respectively. Residual blood supply of meningiomas from pial sources was observed in 5.5% of patients of the first group. Thus, SSE ensured effective ensanguination of a tumor node in 60% of cases of the first group and 82.3% of patients of the second group.

Insufficient tumor embolization was caused by giving up SSE of the following structures:

SSE was followed by control CT- or MRI-examination, perfusion CT-study were carried out in 7 cases of the first group at different intervals (in 3-14 days). Control tomograms of all the patients showed structural changes of a tumor's central part (hypoperfusion, ischemia and degeneration zones), its smaller size, regression of a mass effect. It promoted improvement of a clinical state of the patients under discussion (Fig.6).

The patients were operated on the 1-13 day after embolization. As for the first group, a tumor was removed on the1-2 day, the 3-5 day and the 6-13 day in 12, 9 and 8 cases respectively. Interventions were not performed in 6 patients: 2 of them did not give their consent to the operation and 4 cases were taken to another hospital for surgical treatment or radiotherapy. All the patients of the second group were operated on the 1-3 day. Radical and subtotal interventions were performed respectively in 21 and 8 out of 29 operated cases of the first group. As for 17 operated patients of the second group, total and subtotal resections were made in 14 and 3 of them respectively.

Intensity of arterial bleeding was much smaller both at the stage of surgical approach and tumor removal in all operated patients. A degree of blood loss decreased in comparison with analogous cases, operated without preceding embolization. An indirect index of reduced intensity of intraoperative bleeding was less need of intra- and postoperative hemotransfusion. It was necessary in 15% of cases of the first group; this rate was equal to 15-25% in conventional tactics [7]. Preoperative embolization had no effect on intensity of venous bleeding; it was especially typical of such stages as performing an approach in parasagittal meningiomas and their removal.

Neoplasm consistency underwent considerable changes. When an operation was made on the 4-6 day after total embolization, a tumor was soft and pliable; it had clotted consistency and was aspirated easily. There were necrotic areas in a tumor matrix; stroma and a tumor vascular network looked like a bloodless net of tubular structures, whose resection was not accompanied by bleeding. Thus, use of embolization promoted necrosis of central areas of a tumor node. This made removal of neoplasms without applying neurosurgical spatulas a much easier procedure. As a result, an intervention was less traumatic.

Complications of Intravascular Operations

Neurologic complications during performing SSE were watched in 5 cases (10%). They were persistent and transient in 2 (4%) and 3 (6%) patients respectively. Neurologic complications developed in 4 cases of the first and 1 patient of the second groups.

These complications were caused by embolism of functionally eloquent branches of the ECA (3) or ICA (2) region. Embolism of the ECA branches was characterized by an orthograde direction; embolism of ICA branches was conditioned by reflux of an embolizing substance into the ICA.

One female patient with meningioma of the sphenoid bone wing on the right developed amaurosis and paresis of the abducent nerve immediately after partial embolization of a tumor vascular network with Embolin. It demanded carrying out vasoconstrictive antiedematous therapy. The complication development was considered to be caused by reflux of an embolizing substance into the ophthalmic artery system through orbital branches of the middle meningeal artery. It happened against a background of anatomic peculiarities of the involved vascular structures of the orbit and due to appearance of a tumor pathologic vascular network.

If embolism of functionally eloquent (neural) branches of the ECA or anastomoses with the ICA was suspected, drug tests with administration of 30-50 mg of Thiopental and/or 10 mg of Lidocaine were carried out. According to our data, a drug test with Lidocaine administration did not possess high specificity for prognostication of ischemic neuropathy. In 3 patients administration of 2% Lidocaine solution (2 ml) into the middle meningeal artery for reducing pain syndrome, caused by introduction of DMSO-soluble embolizing materials, resulted in peripheral paresis of the facial nerve due to retrograde reflux of the anesthetic into the stylomastoid artery. However, there was no paresis of mimic muscles in all these cases after embolization.

Discussion

The less bleeding from a tumor the smaller blood loss during its removal. It makes an intervention more radical. The first preoperative endovascular embolization of an organ artery was performed in 1973. Since then this method has been used successfully in urooncology, pulmonary and abdominal surgery. All the authors agree, that an effect of preoperative embolization demonstrates itself in smaller operative blood loss and shorter duration of an operation [1, 4, 9, 10, 13, 15].

An effect of embolization on a tumor is supposed to be mediated by mechanisms of ischemic necrosis and programmed death of cells (apoptosis). It is accompanied by reduction of a tumor cellular mass, less rapid proliferation, decrease of a tumor volume and retardation of its growth [16].

As for neurosurgery, preoperative embolization is used widely in cerebral meningiomas, supplied with blood mainly from a region of meningeal arteries. A risk of embolization is conditioned by presence of permanent anastomoses between the ECA branches and the ICA, participation of the ECA branches in blood supply of craniocerebral nerves.

There is no doubt, that removal of a bloodless tumor causes less technical difficulties and promotes quicker recovery of a patient. However, invasiveness of preoperative embolization, a risk of complications demand discussion of some problems. Among them one can mention:

Medical literature considers two main goals of embolization: preoperative (facilitation of neoplasm removal, reduction of its volume, smaller operative blood loss) and mitigating (temporary decrease of a tumor volume, control of its growth) [16].

In our opinion, the most important indication for preoperative embolization is intracranial and craniobasal tumors (chiefly meningiomas), characterized by:

Usually embolizaton is indicated in intensive blood supply of a tumor by branches of the ECA and ICA, which can be subject to selective catheterization by microcatheters. Possibility and efficacy of embolization are conditioned by a type of tumor blood supply. A. Valavanis distinguishes several types of neoplasm blood supply:

A degree of tumor blood supply compartmentalization has an effect on possibility of its radical exclusion from blood flow. Mono- and multicompartmental types are watched in 15% and 85% respectively [16].

Despite technical progress, angioarchitectonics of intracerebral tumors conditions a risk of embolization to a great extent. It can be justified in hypervascularized hemangioblastomas or glioblastomas with marked intraneoplastic shunting. A list of histological types of tumors, which can be possible objects of preoperative embolization, is given below in accordance with their localizaton [16].

Extracerebral
(demarcated from the brain around them)

Intracerebral
(inseparable from the brain around them)

Meningioma

Hemangioblastoma

Meningosarcoma

Glioblastoma

Hemangiopericytoma

Choriopapilloma

Neurilemoma

Intraventricular meningioma

Paraganglioma

Ependymoma

Angiofibroma

Pituitary adenoma

Chordoma

Metastases

Esthesioblastoma

 

Metastases

 

Possible embolization of pial sources of meningioma's blood supply is limited by functional significance of brain areas, adjacent to a tumor. Possible embolization of ethmoidal branches of the ophthalic artery, feeding meningiomas of the anterior cranial fossa, demands further discussion.

Medical literature does not give exact definition of hypervascularization criteria. Usually such tumors have an abundant vascular network, often characterized by presence of arteriovenous anastomoses, high velocity of blood flow, hypertrophy of afferent arteries. Thus, these criteria are referred to an angiographic picture. It limits possibility of performing embolization in case a department's activity is not organized properly (availability of necessary instruments and embolizing materials). Taking this into account, it is important to determine specific properties of such tumors on the basis of findings of CT- and MRI-examinations, carried out either in outpatient departments or at the first stage of admission to a hospital. According to our data, such criteria can include increase of a tumor density by 20 HU and more in intravenous enhancement; indices of tumor blood flow, exceeding those of the brain. Thorough analysis of CT and MRI data allows to optimize angiographic diagnosis so that to perform simultaneous SSE.

SSE of a tumor is an optimum method, as it ensures obliteration of an intraneoplastic vascular network. Proximal occlusion of an afferent artery promotes development of anastomoses, providing a high level of tumor perfusion. It does not allow to achieve a necessary degree of bloodlessness.

SSE is characterized by a lower level of complications, as the majority of functionally eloquent branches run from proximal segments of major arteries. SSE can be performed only in case of selective catheterization of afferent arteries under conditions of preserved orthograde blood flow of sufficient intensity for ensuring distal penetration of an embolizing substance. Embolization of a vascular network is to precede that of a main trunk of a feeding artery; this principle is compulsory. Factors, effecting delivery of an embolizing material to a tumor and its distribution within it, are its adequate choice and proper composition, absence of spasm of feeding or major arteries. When adequate bloodlessness of a tumor vascular network is achieved, it is possible to occlude an afferent artery in its opening, using free microspirals. It reduces bleeding intensity at the stage of performing a surgical access. Use of solid emboli for preoperative embolization is conventional. As for "liquid" embolizing substances, they are considered to be more dangerous. According to our data, a negative pharmacological test allows to use them without any considerable growth of a complication rate. If a test is positive, it is expedient to use bigger solid microemboli (>500m). The majority of complications in our series was connected with applying liquid embolizing materials and underestimation of angioarchitectonics of afferent arteries. In other words, they had a rather marked "subjective" character and were not conditioned by a choice of an embolizing material.

Embolization precedes surgical intervention; a term of the latter is determined by dynamics of necrobiotic processes. An optimum result (the least degree of blood loss, decrease of a tumor volume, softening of a node) is achieved in operations, performed on the 6-7 day after embolizaton. Long-term follow-up of patients, who refused to be operated on, is indicative of regression of mass-effect symptoms due to node necrosis and decrease of its volume. It is worth mentioning, that "total" embolization does not prevent recurrences. We watched them in 2 cases; however, there was no marked vascular network in neoplastic nodes and the patients did not demand repeated embolization before reoperations.

Preoperative embolization of craniobasal tumors needs further improvement. The most prospective ways are developing methods of safe embolization of branches of the ICA cavernous segment and combined chemoembolization of these neoplasms.

Conclusions

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