Thrombosis of ICA branches: unusual complication of AVM embolization

Svistov D.V., Kandyba D.V., Savello A.V., Fokin V.A., Dolgi V.N., Voznesenskaya N.N.

Chair of Neurosurgery, Chair of Rentgenology and Radiology, Military-medical Academy, Saint Petersburg, Russia.


Differentiated intravascular interventions are an inseparable part of multimodality treatment of patients with a large AVM of the brain. Use of preoperative or preradiation embolization with the purpose of reduction of a malformation size, obliteration of compartments, threatening with rupture, results in considerable improvement of indices of radical malformation elimination. It allows to solve a problem of prevention of intracranial hemorrhages and, to some extent, epileptic syndrome. In some cases, it especially concerns a torpid disease course, intravascular interventions are the only necessary and rather effective means of minimally invasive treatment. Development of modern technologies of intervention neuroradiology permits to perform superselective embolization not only of large, but also small and even micromalformations. It makes a physician review strategy of treatment of such patients. At present we are working at a problem of validity of intravascular intervention, united with diagnostic angiography, as the first stage of therapeutic measures in symptomatic AVM of any size and localization. Thus, we are to study both positive and negative aspects of intravascular interventions in detail. In particular, it concerns a structure and rate of complications. According to our observations, intraoperative neurologic disorders of an ischemic type are rather frequent (31.6%); persistent areflexia is watched in 7.9% of cases. The majority of them are connected with functional importance of embolized afferent vessels of malformation, though sometimes there are complications, which are not typical of this nosologic entity and are caused by brain invasion into a vascular bed. Ascending thrombosis of a catheterized artery is one of such potentially fatal complications.

A Clinical Observation

Patient G., born in 1968, was admitted to the Clinic of Neurosurgery of the Medicomilitary Academy on October 24, 2001 with the following diagnosis: large arteriovenous malformation of the left parietal lobe of the brain.

For the first time the disease manifested itself in June 2001 in the form of secondary generalized seizure. Then the number of seizures increased up to four times a day. Data of CT examination with intravenous enhancement were indicative of AVM. The patient was sent to the Clinic of Neurosurgery of the Medicomilitary Academy for operative treatment.

On admission the patient complained of asthenia, headache, weakness in the right lower extremity and periodic clonospasm in it, accompanied by loss of consciousness.

The patient was compensated somatically. Neurologic examination revealed right-side hemiparesis and reduction of strength in the right lower extremity up to the score of 4.

MRI and magnetic resonance angiography (MRA) of October 29, 2001 were indicative of a large arteriovenous malformation of the left parietal lobe. Blood was supplied via hypertrophic branches of the left ACA and MCA with drainage into the upper sagittal sinus (fig.1). There was suspicion on unruptured aneurysmal widening in the bifurcation of the pericallous artery.

According to findings of Transcranial Doppler examination of November 3, 2001, there were signs of marked arteriovenous shunting in the left ACA and transitory shunting in the left MCA and PCA (fig. 2)..

Selective cerebral angiographic examination of November 5, 2001 demonstrated extensive AVM of the left parietal lobe with a size of 60x50x50 mm. Blood was supplied via hypertrophic branches of the pericallous artery, parietal and frontal branches of MCA, the left anterior ciliary artery, distal branches of the left PCA and posterior ciliary artery. Drainage into the system of the superior sagittal sinus was ensured by sharply delated convexital and basal veins (fig.3). Aneurysmal widening of bifurcation of the pericallous artery was confirmed. Taking into account a size, localization and type of blood supply of AVM, it was decided to embolize it. It was planned to perform embolization of malformation compartments from the ACA region with subsequent estimation of a possibility to embolize branches of the left MCA.

Catheterization of a subcranial segment of ICA with a 5F guide was followed by consecutive superselective catheterization of main arteries, feeding AVM. Afferent branches of ACA and a greater part of malformation (fig.4) were excluded from blood flow (histoacryl mixed with lipidiol in a ratio of 1:1.3 was used as an embolizing material). Amytal test in MCA branches demonstrated transient neurologic deficit. The manipulation was ceased because of a risk of neurologic disorders and a functional importance of preserved feeding arteries. There were no neurologic complications during this manipulation. An operation lasted 1 hour 40 minutes; the guide was in ICA during 1 hour 10 minutes. Systemic heparinization (10 000IU; 2x2500 - bolus administration; 5000 - constant infusion) was carried out.

The patient began to complain of growing numbness in the right part of the face and upper extremity in 3 hours after the operation. Hand paresis aggravated up to the score of 3 within 10 minutes. Block of the sinocarotid area was accompanied by simultaneous development of total aphasia and right-side hemiplegia. There was no displacement of median structures in M-echo. Absence of headache and consciousness disorders allowed not to think about hemorrhage (from aneurysmal widening?). Transcranial Doppler was indicative of sharp reduction of linear blood flow velocity in the left MCA (fig.5), though patency of ICA and ACA was preserved. Thus, acute occlusion (probably, thromboembolic one) of the left MCA was diagnosed.

The patient was taken to an X-ray operating room. Selective angiography demonstrated an intraluminal thrombus of a "rider" type in bifurcation of the left ICA, spreading into M1 segment of the left MCA and its bifurcation. Time of cerebral blood flow increased up to 10 sec. There was bolus administration of heparin in a dose of 10 000 IU. Control angiography, used in 30 min, showed, that in spite of systemic heparinization and increase of coagulation time up to 15 min, there was thrombosis of the descending trunk of MCA (fig.6), It was decided to carry out intraarterial thrombolysis. A zone of subtotal thrombosis occupied a supraclinoid segment of ICA, opening of ACA and MCA, 1-2 segments of MCA. Thus, peculiar localization of thrombi did not allow to bring a microcatheter to a proximal surface of thrombus in the area of total thrombosis (MCA bifurcation) and to perform superselective thrombolysis. It was a cause of streptokinase administration into ICA lumen (selective intraarterial thrombolysis).segments of MCA. Thus, peculiar localization of thrombi did not allow to bring a microcatheter to a proximal surface of thrombus in the area of total thrombosis (MCA bifurcation) and to perform superselective thrombolysis. It was a cause of streptokinase administration into ICA lumen (selective intraarterial thrombolysis). (fig.7). Neurologic deficit regressed by the end of the procedure; the speech restored; locomotive disorders in the right extremities were represented by moderate paresis (the score of 3-4).

The patient received anti-inflammatory, antispasmodic, vasoactive, antibacterial preparations, vitamins, anticoagulants with a direct and indirect effect, symptomatic drugs. Besides, he underwent HBO treatment.

Control dynamic Transcranial Doppler examination showed anterograde changed major blood flow with signs of postischemic reperfusion (fig.8). There was restoration of a hyperemic response in carrying out a compression test. CT examination of November 12, 2001 demonstrated a state, watched after subtotal embolization of AVM of the left parietal lobe. There were foci with reduced density, i.e. signs of ischemia, located paraventricularly at the level of the anterior horn and in projection of central gyruses on the left. Feeding vessels and AVM were filled with an embolizing substance (fig.9).

MRI examination of November 20, 2001 was indicative of subtotal embolization of AVM and ischemic changes, spreading forward from the anterior horn of the left lateral ventricle (fig.10). The patient was compensated somatically at the moment of discharge. As for neurologic findings, there were mild (the score of 4+) right-side hemiparesis, hemihypoesthesia.


The majority of authors consider intra-arterial superselective thrombolysis to be an effective method of restoration of patency of cerebral vessels within the first hours of ischemic stroke onset. The second phase of the randomized multi-center study of intra-arterial fibrinolytic therapy efficacy in ischemic stroke (PROACT II, Abbott Laboratories, 1999) allows to speak of good results, when it is used during the first 6 hours from stroke onset. Recanalization of the artery within 120 min from the beginning of treatment was achieved in 57.7% of patients. Besides, there was outcome improvement in a group of patients, who were subject to intra-arterial fibrinolytic therapy (del Zoppo G.J. et al., 1998) [1].

At the same time thrombolysis in patients with ischemic stroke was supposed to be connected with a risk of hemorrhagic complications. However, it was not proved by statistical data (del Zoppo G.J. et al., 1998; Suarez J.I. et el., 1999) [1, 7].

Thrombosis of AVM feeding arteries after its removal was described as one of possible complications of this intervention (Miyasaka Y. et al., 1990; Sipos E.P. et al., 1992; Miyasaka Y. et al., 1998) [4, 5, 6]. Sipos E.P. et al. (1992) [6] reported a case of successful intra-arterial thrombolysis in retrograde thrombosis of feeding arteries after malformation removal. According to Miyasaka Y. et al. (1990,1998) [4, 5], the causes of retrograde thrombosis of arteries, feeding AVM, could be as follows: atherosclerotic changes, a large size of AVM, widening of a lumen and lengthening of arteries, resulting in slower blood flow after AVM resection against a background of pathologic vascular changes due to a long-term hemodynamic stress.

Jafar J.J. et al. (1991) [3] described a case of successful use of a tissue palsminogen activator in occlusion of MCA by an embolus during AVM embolization. Superselective embolization led to subtotal exclusion of AVM and feeding branches of ACA and preservation of pathologic anastomosis in the MCA region; it implied preservation of the former flow and linear blood flow velocity in the vessel. The case history contained no information on cerebral circulation disorders of an ischemic type and cerebral angiography demonstrated no signs of stenosing lesions of cerebral arteries or artherosclerosis before embolization. Nevertheless, the patient developed a potentially fatal complication against a background of systemic heparinization in three hours after a technically successful procedure.

In spite of preserved arteriovenous anastomosis and high linear blood flow velocity, there was MCA thrombosis. There was no doubt, that the procedure provoked a thromboembolic complication, though manipulation on MCA was limited to short-term passing of a microcatheter and performing Wada test. The most probable thing was ascending thrombosis, which developed from a subcranial segment of ICA and a zone of a guide stay. As for thrombus, it originated between the catheter and artery wall.

Thus, delayed iatrogenic thrombosis of major cerebral arteries should be taken into account as one of possible complications of AVM superselective embolization. Selective intra-arterial thrombolysis is a life-saving method of recanalization in this complication. It is desirable to ensure possibility of its use in a department of intervention neuroradiology.



  1. del Zoppo G.J., Higa shida R.T., Furlan A.J., Pessin M.S., Rowley H.A., Gent M. and the PROACT Investigators. PROACT: A Phase II Randomized Trial of Recombinant Pro-Urokinase by Direct Arterial Delivery in Acute Middle Cerebral Artery Stroke. Stroke. 1998;29:4-11.
  2. Intra-arterial Thrombolysis. Supplement to AJNR:22, September 2001.
  3. Jafar J.J., Tan W.S., Crowell R.M. Tissue plasminogen activator thrombolysis of a middle cerebral artery embolus in a patient with an arteriovenous malformation. Case report. J Neurosurg 1991 May;74(5):808-12.
  4. Miyasaka Y., Kurata A., Tanaka R., Irikura K., Yamada M., Fujii K. The significance of retrograde thrombosis following removal of arteriovenous malformations in elderly patients. Surg Neurol 1998 Apr;49(4):399-405.
  5. Miyasaka Y., Yada K., Ohwada T., Kitahara T., Endoh M., Saito M., Kurata A., Ohtaka H. Retrograde thrombosis of feeding arteries after removal of arteriovenous malformations. J Neurosurg 1990 Apr;72(4):540-5.
  6. Sipos E.P., Kirsch J.R., Nauta H.J., Debrun G., Ulatowski J.A., Bell W.R. Intra-arterial urokinase for treatment of retrograde thrombosis following resection of an arteriovenous malformation. Case report. J Neurosurg. 1992 Jun; 76(6):1004-7.
  7. Suarez J.I., Sunshine J.L., Tarr R., Zaidat O., Selman W.R., Kernich C., Landis D. Predictors of Clinical Improvement, Angiographic Recanalization, and Intracranial Hemorrhage After Intra-Arterial Thrombolysis for Acute Ischemic Stroke. Stroke. 1999;30:2094-2100.