Posttraumatic bilateral middle cerebral artery occlusion Case report SKIP JACQUES, M.D., C. HUNTER SHELDEN, M.D., D. THOMAS ROGERS, JR., M.D., AND ANTHONY C. TRIPPI,M.D.
Department of Neurological Surgery, Huntington Memorial Hospital and the Huntington Institute of Applied Medical Research, Pasadena, California v' The authors report a case of bilateral posttraumatic middle cerebral artery occlusion. Previously reported unilateral cases are reviewed and possible pathophysiological mechanisms disscussed. KEY WORDS m i d d l e cerebral artery embolism 9 dissecting a n e u r y s m ~
W
, HILE posttraumatic occlusion of the extracranial vertebral and carotid arteries is well known, reports of occlusion of intracranial vessels following closed head trauma are rare; 7'8 in fact, only 21 cases have been adequately documented? We believe this occurrence is much more common than generally recognized and needs to be stressed because of the clinical similarity to other intracranial posttraumatic mass lesions. This communication will describe a single case of bilateral middle cerebral artery occlusion following closed head injury and comment on possible pathophysiological mechanisms. C a s e Report
A 53-year-old male physician was admitted through the emergency room at another hospital on June 17, 1973, following an automobile accident. He was comatose, had a
J. Neurosurg. / Volume 42 / February, 1975
9 occlusion
9 thrombosis
9
flaccid right arm and leg, contusions of the left thorax, and multiple left rib fractures. An endotracheal tube was introduced, following which he was placed on a volume respirator. Over the ensuing 48 hours he became progressively more responsive. On the fourth day after admission he became much more lethargic and was transferred to the Huntington Memorial Hospital for neurosurgical care. Examination. The patient responded to pain with purposeful movements; vital signs were normal. The pupils were 2 mm, equal, and reacted slowly to light. There was no papilledema or retinal hemorrhage. No external evidence of facial fracture, hemotympanum, or trauma to the neck was present; no bruits were heard. There were contusions over the lower midline sternum and auscultation revealed rhonchi and decreased breath sounds over the lower lobe of the left lung. Examination disclosed a deformity of the splinted right 217
S. Jacques, C. H. Shelden, D. T. Rogers, Jr., and A. C. Trippi
FIG. 1. Angiographic studies made June 21, 1973. Upper Left: Right lateral brachial retrograde angiogram reveals complete obstruction of the right middle cerebral artery distal to take-off of ascending frontoparietal branch. Upper Right: Left lateral percutaneous carotid angiogram shows complete obstruction of the left middle cerebral artery at its origin from the left internal carotid artery. Lower Left." Anteroposterior view of left lateral percutaneous carotid angiogram.
tibia and a sutured 2" laceration in the frontal scalp. Neurological examination revealed a right central facial palsy and a right hemiparesis, more pronounced in the leg than in the arm. Reflexes were 2 + on the right side of the body and 1 + on the left. The patient had a right Babinski sign. Initial x-ray films revealed a fracture of the right tibia and multiple rib fractures with a left pneumothorax and lung contusion. 218
Hospital Course. The patient had a tracheostomy and treatment with dexamethasone and antibiotics. On June 21, 1973, percutaneous right brachial and left carotid angiograms demonstrated complete occlusion of both middle cerebral arteries. The right middle cerebral artery (Fig. 1 upper left and right) was obstructed just distal to the take-off of the ascending frontoparietal branch. Angiograms demonstrated good fillJ. Neurosurg. / Volume 42 / February, 1975
Bilateral middle cerebral artery occlusion
FJc. 2. Angiogram made July 5, 1973. Left." Right lateral brachial retrograde angiogram shows some collateral circulation developing. Right." Left lateral percutaneous carotid angiogram shows retrograde collateral circulation from terminal arterial cerebral branches. ing of the right posterior cerebral and right anterior cerebral arteries as well as a prolonged arterial phase with increased intracranial pressure. The left middle cerebral artery (Fig. 1 lower left) showed complete obstruction at its origin from the left internal carotid artery. The left posterior cerebral and left anterior cerebral arteries were well-filled and in normal position. There was no evidence of subdural or intracerebral hematoma. Repeat angiography (Fig. 2) on July 5, 1973, again demonstrated occlusion of both middle cerebral arteries and no evidence of hematoma. The patient improved to the point of understanding a few simple commands although he still showed marked expressive aphasia and right hemiplegia. He was discharged on August 6, 1973, to an extended-care facility without further neurological improvement. Discussion
Twenty-one cases of middle cerebral artery occlusion attributed to nonpenetrating head injuries have been adequately described in the literature,1 8,9-. In 1942 DeVeer and Browde? reported a 42-year-old man who developed stupor and hemiplegia 12 hours J. Neurosurg. / Volume 42 / February, 1975
after a closed bead injury; autopsy revealed that a dissecting aneurysm involving the middle cerebral artery resulted in complete occlusion of the vessel. Of the 21 cases of unilateral occlusion previously reported, the patients ranged in age from 6 to 67 years with an average age of 38 years. 6 Many of the patients had suffered relatively minor head injuries, often without loss of consciousness. The interval from the time of injury to the onset of occlusive symptoms varied; 14 patients developed coma following lucid intervals as long as 2 weeks. In 33% of the cases the injury proved fatal; the prognosis is generally poor. Angiography has consistently demonstrated an occlusion of the main stem or horizontal portion of the middle cerebral artery although two out of the 10 cases reviewed by Hollin, et al., ~ visualized occlusion of more distal middle cerebral artery branches. Displacement of the anterior cerebral artery has been rare. Collateral circulation with retrograde filling of the middle cerebral artery by the anterior or posterior cerebral arteries has been documented; this also occurred with our patient. Three patients in Hollin's review had associated defects in the 219
S. J a c q u e s , C. H . S h e l d e n , D. T. R o g e r s , J r . , a n d A. C. T r i p p i cervical portion of the carotid artery; one also had abnormalities in the supraclinoid portion of the same vessel. Follow-up angiography has been performed in 10 patients at intervals ranging from 24 hours to 9 months; significant clearing had occurred in all except one patient in this group. This clearing appeared in our case, although significant collaterals had developed. Seven patients had postmortem examinations. Three of these had been diagnosed as having a dissecting aneurysm of the middle cerebral artery. In one case thrombosis of the middle cerebral artery was found and attributed to transient occlusion of the cervical portion of the carotid artery. In a case reviewed by Lear, et al., e postmortem examination revealed emboli in all of the major branches of the middle cerebral artery; their origin was a mural thrombus in the proximal internal carotid artery. In the remaining two cases with postmortem examinations, the involved arteries were found to be completely patent, despite previous angiographic demonstration of complete middle cerebral artery occlusions. Death in these cases was attributed to cerebral edema and increased intracranial pressure. The pathogenesis of middle cerebral artery occlusion following nonpenetrating head trauma is not clearly understood, especially since so few cases have been examined at autopsy. However, several plausible explanations exist: . Spasm. A number of authors have emphasized the role of spasm of the carotid artery in the neck as a possible cause of posttraumatic angiographic occlusion of the intracranial arteries. Frantzen, et al.? have hypothesized the release by reflex of arterial spasm from the carotid artery in the neck, secondary to trauma. Arteriograms of patients with head injuries have shown areas of arterial narrowing attributed to spasm; the spasm was presumably secondary to movement of the brain during trauma. The distal segment of the siphon is fixed to the brain by the anterior and middle cerebral branches and moves with it, while the proximal carotid artery remains fixed at the cavernous sinus. This over-stretching could cause spasm and thus give the illusion of thrombosis. ~ 220
2. Emboli from the cervical portion o f the internal carotid artery. Posttraumatic thrombus formation in the cervical portion of the internal carotid artery may result from direct contusion of the arterial wall or shearing and stretching of the vessel by sudden hyperextension of the neck and traction across the transverse process of the third cervical vertebra or the lateral mass of the atlas. 7 Embolization of mural thrombus fragments to the middle cerebral artery could readily occur and is well documented in atherosclerotic carotid disease. 6 3. Dissecting aneurysm. This seems the most likely mechanism in a bilateral occlusion. The impact of a blow on the head could cause damage to intracranial arteries and separation of the intima from the outer layers of the vessel wall. Thus, an intramural hematoma could cause progressive narrowing and occlusion of the affected vessel. Cerebral arteries have relatively thin walls and only one elastic membrane and are therefore much more fragile and probably more susceptible to separation between the intima and media than vessels elsewhere. 4. Thrombus formation. Mechanical injury to any vessel can affect the intimal charge secondarily attracting platelets and cause subsequent clot formation. Although direct contusion of the middle cerebral artery is probably not common, the internal carotid and proximal middle cerebral arteries could conceivably be bruised against adjacent bony structures.
References 1. DeVeer JA, Browder J: Post-traumatic cerebral thrombosis and infarction. Report of a case and discussion of its bearing on the problem of immediate and delayed posttraumatic apoplexy. J Neuropathol Exp Neurol 1:24-31, 1942 2. Duman S, Stephens JW: Post-traumatic middle cerebral artery occlusion. Neurology (Minneap) 13:610-616, 1963 3. Frantzen E, Jacobsen HH, Therkelsen J: Cerebral artery occlusions in children due to trauma to the head and neck. Neurology (Minneap) 11:695-700, 1961 J. Neurosurg. / Volume 42 / February, 1975
Bilateral middle cerebral artery occlusion 4. Gunning A J, Pickering GW, Robb-Smith AHT, et al: Mural thrombosis of the internal carotid artery and subsequent embolism. Q J Med 3:155-195, 1964 5. Hollin SA, Sukoff MH, Silverstein A, et al: Post-traumatic middle cerebral artery occlusion. J Neurosurg 25:526-535, 1966 6. Loar CR, Chadduck WM, Nugent GR: Traumatic occlusion of the middle cerebral artery. Case report. J Neurosurg 39:753-756, 1973 7. Lyness SS, Wagman AD: Neurologic deficit following cervical manipulation. Surg Neurol 2:121-124, 1974 8. Mehalic T, Farhat SM: Vertebral artery injury from chiropractic manipulation of the neck. Surg Neurol 2:125-129, 1974
J. Neurosurg. / Volume 42 / February, 1975
9. Sakamoto K, Sumikawa Y: (Traumatic middle cerebral artery occlusion.) Brain Nerve (Tokyo) 21:983-991, 1969 (Jap) 10. Takahashi S, Honda T: (Traumatic middle cerebral artery occlusion: report of a case with review of literature.) Brain Nerve (Tokyo) 21:1128-1131, 1970 (.lap) 11. Wolpert SM, Schechter MM: Traumatic middle cerebral artery occlusion. Radiology 87:671-677, 1966
Address reprint requests to: Skip Jacques, M.D., Huntington Institute of Applied Medical Research, 734 Fairmount Avenue, Pasadena, California 91105.
221
Department of Neurological Surgery, Huntington Memorial Hospital and the Huntington Institute of Applied Medical Research, Pasadena, California v' The authors report a case of bilateral posttraumatic middle cerebral artery occlusion. Previously reported unilateral cases are reviewed and possible pathophysiological mechanisms disscussed. KEY WORDS m i d d l e cerebral artery embolism 9 dissecting a n e u r y s m ~
W
, HILE posttraumatic occlusion of the extracranial vertebral and carotid arteries is well known, reports of occlusion of intracranial vessels following closed head trauma are rare; 7'8 in fact, only 21 cases have been adequately documented? We believe this occurrence is much more common than generally recognized and needs to be stressed because of the clinical similarity to other intracranial posttraumatic mass lesions. This communication will describe a single case of bilateral middle cerebral artery occlusion following closed head injury and comment on possible pathophysiological mechanisms. C a s e Report
A 53-year-old male physician was admitted through the emergency room at another hospital on June 17, 1973, following an automobile accident. He was comatose, had a
J. Neurosurg. / Volume 42 / February, 1975
9 occlusion
9 thrombosis
9
flaccid right arm and leg, contusions of the left thorax, and multiple left rib fractures. An endotracheal tube was introduced, following which he was placed on a volume respirator. Over the ensuing 48 hours he became progressively more responsive. On the fourth day after admission he became much more lethargic and was transferred to the Huntington Memorial Hospital for neurosurgical care. Examination. The patient responded to pain with purposeful movements; vital signs were normal. The pupils were 2 mm, equal, and reacted slowly to light. There was no papilledema or retinal hemorrhage. No external evidence of facial fracture, hemotympanum, or trauma to the neck was present; no bruits were heard. There were contusions over the lower midline sternum and auscultation revealed rhonchi and decreased breath sounds over the lower lobe of the left lung. Examination disclosed a deformity of the splinted right 217
S. Jacques, C. H. Shelden, D. T. Rogers, Jr., and A. C. Trippi
FIG. 1. Angiographic studies made June 21, 1973. Upper Left: Right lateral brachial retrograde angiogram reveals complete obstruction of the right middle cerebral artery distal to take-off of ascending frontoparietal branch. Upper Right: Left lateral percutaneous carotid angiogram shows complete obstruction of the left middle cerebral artery at its origin from the left internal carotid artery. Lower Left." Anteroposterior view of left lateral percutaneous carotid angiogram.
tibia and a sutured 2" laceration in the frontal scalp. Neurological examination revealed a right central facial palsy and a right hemiparesis, more pronounced in the leg than in the arm. Reflexes were 2 + on the right side of the body and 1 + on the left. The patient had a right Babinski sign. Initial x-ray films revealed a fracture of the right tibia and multiple rib fractures with a left pneumothorax and lung contusion. 218
Hospital Course. The patient had a tracheostomy and treatment with dexamethasone and antibiotics. On June 21, 1973, percutaneous right brachial and left carotid angiograms demonstrated complete occlusion of both middle cerebral arteries. The right middle cerebral artery (Fig. 1 upper left and right) was obstructed just distal to the take-off of the ascending frontoparietal branch. Angiograms demonstrated good fillJ. Neurosurg. / Volume 42 / February, 1975
Bilateral middle cerebral artery occlusion
FJc. 2. Angiogram made July 5, 1973. Left." Right lateral brachial retrograde angiogram shows some collateral circulation developing. Right." Left lateral percutaneous carotid angiogram shows retrograde collateral circulation from terminal arterial cerebral branches. ing of the right posterior cerebral and right anterior cerebral arteries as well as a prolonged arterial phase with increased intracranial pressure. The left middle cerebral artery (Fig. 1 lower left) showed complete obstruction at its origin from the left internal carotid artery. The left posterior cerebral and left anterior cerebral arteries were well-filled and in normal position. There was no evidence of subdural or intracerebral hematoma. Repeat angiography (Fig. 2) on July 5, 1973, again demonstrated occlusion of both middle cerebral arteries and no evidence of hematoma. The patient improved to the point of understanding a few simple commands although he still showed marked expressive aphasia and right hemiplegia. He was discharged on August 6, 1973, to an extended-care facility without further neurological improvement. Discussion
Twenty-one cases of middle cerebral artery occlusion attributed to nonpenetrating head injuries have been adequately described in the literature,1 8,9-. In 1942 DeVeer and Browde? reported a 42-year-old man who developed stupor and hemiplegia 12 hours J. Neurosurg. / Volume 42 / February, 1975
after a closed bead injury; autopsy revealed that a dissecting aneurysm involving the middle cerebral artery resulted in complete occlusion of the vessel. Of the 21 cases of unilateral occlusion previously reported, the patients ranged in age from 6 to 67 years with an average age of 38 years. 6 Many of the patients had suffered relatively minor head injuries, often without loss of consciousness. The interval from the time of injury to the onset of occlusive symptoms varied; 14 patients developed coma following lucid intervals as long as 2 weeks. In 33% of the cases the injury proved fatal; the prognosis is generally poor. Angiography has consistently demonstrated an occlusion of the main stem or horizontal portion of the middle cerebral artery although two out of the 10 cases reviewed by Hollin, et al., ~ visualized occlusion of more distal middle cerebral artery branches. Displacement of the anterior cerebral artery has been rare. Collateral circulation with retrograde filling of the middle cerebral artery by the anterior or posterior cerebral arteries has been documented; this also occurred with our patient. Three patients in Hollin's review had associated defects in the 219
S. J a c q u e s , C. H . S h e l d e n , D. T. R o g e r s , J r . , a n d A. C. T r i p p i cervical portion of the carotid artery; one also had abnormalities in the supraclinoid portion of the same vessel. Follow-up angiography has been performed in 10 patients at intervals ranging from 24 hours to 9 months; significant clearing had occurred in all except one patient in this group. This clearing appeared in our case, although significant collaterals had developed. Seven patients had postmortem examinations. Three of these had been diagnosed as having a dissecting aneurysm of the middle cerebral artery. In one case thrombosis of the middle cerebral artery was found and attributed to transient occlusion of the cervical portion of the carotid artery. In a case reviewed by Lear, et al., e postmortem examination revealed emboli in all of the major branches of the middle cerebral artery; their origin was a mural thrombus in the proximal internal carotid artery. In the remaining two cases with postmortem examinations, the involved arteries were found to be completely patent, despite previous angiographic demonstration of complete middle cerebral artery occlusions. Death in these cases was attributed to cerebral edema and increased intracranial pressure. The pathogenesis of middle cerebral artery occlusion following nonpenetrating head trauma is not clearly understood, especially since so few cases have been examined at autopsy. However, several plausible explanations exist: . Spasm. A number of authors have emphasized the role of spasm of the carotid artery in the neck as a possible cause of posttraumatic angiographic occlusion of the intracranial arteries. Frantzen, et al.? have hypothesized the release by reflex of arterial spasm from the carotid artery in the neck, secondary to trauma. Arteriograms of patients with head injuries have shown areas of arterial narrowing attributed to spasm; the spasm was presumably secondary to movement of the brain during trauma. The distal segment of the siphon is fixed to the brain by the anterior and middle cerebral branches and moves with it, while the proximal carotid artery remains fixed at the cavernous sinus. This over-stretching could cause spasm and thus give the illusion of thrombosis. ~ 220
2. Emboli from the cervical portion o f the internal carotid artery. Posttraumatic thrombus formation in the cervical portion of the internal carotid artery may result from direct contusion of the arterial wall or shearing and stretching of the vessel by sudden hyperextension of the neck and traction across the transverse process of the third cervical vertebra or the lateral mass of the atlas. 7 Embolization of mural thrombus fragments to the middle cerebral artery could readily occur and is well documented in atherosclerotic carotid disease. 6 3. Dissecting aneurysm. This seems the most likely mechanism in a bilateral occlusion. The impact of a blow on the head could cause damage to intracranial arteries and separation of the intima from the outer layers of the vessel wall. Thus, an intramural hematoma could cause progressive narrowing and occlusion of the affected vessel. Cerebral arteries have relatively thin walls and only one elastic membrane and are therefore much more fragile and probably more susceptible to separation between the intima and media than vessels elsewhere. 4. Thrombus formation. Mechanical injury to any vessel can affect the intimal charge secondarily attracting platelets and cause subsequent clot formation. Although direct contusion of the middle cerebral artery is probably not common, the internal carotid and proximal middle cerebral arteries could conceivably be bruised against adjacent bony structures.
References 1. DeVeer JA, Browder J: Post-traumatic cerebral thrombosis and infarction. Report of a case and discussion of its bearing on the problem of immediate and delayed posttraumatic apoplexy. J Neuropathol Exp Neurol 1:24-31, 1942 2. Duman S, Stephens JW: Post-traumatic middle cerebral artery occlusion. Neurology (Minneap) 13:610-616, 1963 3. Frantzen E, Jacobsen HH, Therkelsen J: Cerebral artery occlusions in children due to trauma to the head and neck. Neurology (Minneap) 11:695-700, 1961 J. Neurosurg. / Volume 42 / February, 1975
Bilateral middle cerebral artery occlusion 4. Gunning A J, Pickering GW, Robb-Smith AHT, et al: Mural thrombosis of the internal carotid artery and subsequent embolism. Q J Med 3:155-195, 1964 5. Hollin SA, Sukoff MH, Silverstein A, et al: Post-traumatic middle cerebral artery occlusion. J Neurosurg 25:526-535, 1966 6. Loar CR, Chadduck WM, Nugent GR: Traumatic occlusion of the middle cerebral artery. Case report. J Neurosurg 39:753-756, 1973 7. Lyness SS, Wagman AD: Neurologic deficit following cervical manipulation. Surg Neurol 2:121-124, 1974 8. Mehalic T, Farhat SM: Vertebral artery injury from chiropractic manipulation of the neck. Surg Neurol 2:125-129, 1974
J. Neurosurg. / Volume 42 / February, 1975
9. Sakamoto K, Sumikawa Y: (Traumatic middle cerebral artery occlusion.) Brain Nerve (Tokyo) 21:983-991, 1969 (Jap) 10. Takahashi S, Honda T: (Traumatic middle cerebral artery occlusion: report of a case with review of literature.) Brain Nerve (Tokyo) 21:1128-1131, 1970 (.lap) 11. Wolpert SM, Schechter MM: Traumatic middle cerebral artery occlusion. Radiology 87:671-677, 1966
Address reprint requests to: Skip Jacques, M.D., Huntington Institute of Applied Medical Research, 734 Fairmount Avenue, Pasadena, California 91105.
221
