Bilateral superior ophthalmic vein enlargement associated with diffuse cerebral swelling
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1 J Neurosurg 86: , 1997 Bilateral superior ophthalmic vein enlargement associated with diffuse cerebral swelling Report of 11 cases ROHIT K. KHANNA, M.D., CHRISTOPHER J. PHAM, D.O., GHAUS M. MALIK, M.D., ERIC M. SPICKLER, M.D., BHARAT MEHTA, M.D., AND MARK L. ROSENBLUM, M.D. Departments of Neurosurgery and Radiology (Neuroradiology), Henry Ford Hospital, Detroit, Michigan Bilateral superior ophthalmic vein (SOV) enlargement has rarely been shown to occur in patients with septic and aseptic cavernous sinus thrombosis, Graves disease due to obstruction of the SOV by enlarged extraocular muscles, or carotid cavernous fistulas caused by retrograde flow. The authors describe 11 patients with bilateral SOV enlargement associated with cerebral swelling as detected by computerized tomography scanning. The bilaterally enlarged SOVs returned to a normal size following resolution of cerebral swelling and elevated intracranial pressure. To the authors knowledge, this is the first report of bilateral SOV enlargement associated with diffuse cerebral swelling that subsequently resolved after treatment of the cerebral edema. The authors believe that the bilateral SOV enlargement was caused by mechanical cavernous sinus venous stagnation due to cerebral swelling, a syndrome that occurs more commonly than currently appreciated. KEY WORDS cavernous sinus cerebral edema computerized tomography head injury intracranial aneurysm superior ophthalmic vein enlargement U NILATERAL superior ophthalmic vein (SOV) enlargement has been reported in patients with carotid cavernous fistulas, intraorbital pathology, and (infrequently) parasellar tumors. 3,7,10 12 The syndrome is associated with increased retrograde SOV flow, SOV obstruction, or cavernous sinus compression. Except for some patients with cavernous sinus thrombosis, 5 Graves disease, 10 or carotid cavernous fistulas, 1,9 SOV enlargement is almost always unilateral. We report on 11 patients with bilateral SOV enlargement associated with cerebral edema that resolved after treatment. Clinical Review A comprehensive review of over 500 computerized tomography (CT) scans obtained in patients admitted to the neurosurgical intensive care unit at Henry Ford Hospital in Detroit, Michigan, over a 2-year period was undertaken. The CT scans of the head included sections through the orbits, thus allowing for evaluation of the SOVs as well as any intracranial pathology. Patients whose bilateral SOV enlargement could be evaluated on serial CT scans were included. Patients with unilateral SOV enlargement, those in whom one scan showed SOV enlargement but in whom no other CT scans offered good orbital sections for evaluation of their SOVs, and those with a known cause for bilateral SOV enlargement were excluded from the study. Because variability exists in the size of SOVs among different patients, only patients with transient SOV enlargement were included and these patients served as their own controls. Generally, an SOV size of greater than 2 mm on axial CT scanning was considered to be a possible indication of enlargement, 3 mm or more a likely indication of enlargement, and 4 mm or more a definite indication of enlargement. A total of 55 patients met the inclusion criteria. Results Of the 55 patients meeting the inclusion criteria, intracranial pressure (ICP) was monitored in 40 and was found to be elevated ( 20 mm Hg) at some point in 21. Our review identified 11 patients with bilateral SOV enlargement associated with cerebral edema that returned to normal size after the cerebral edema resolved. Table 1 shows the clinical presentation, surgical treatment, hospital course, and outcome for each patient. Four patients were placed on a ventilator during initial CT scanning, but the positive end-expiratory pressure (PEEP) did not rise above 5 mm Hg during this time. The findings on initial and follow-up head CT scans are listed in Table 2. Of the 21 patients with intracranial hypertension, transient bilat- 893
2 R. K. Khanna, et al. TABLE 1 Clinical characteristics, hospital course, and outcome in 11 patients with enlarged SOVs* Highest Case Age GCS ICP (mm No. (yrs) Diagnosis Score Hg) Complications Surgical Procedure Outcome 1 15 closed head injury 3 25 none subdural hematoma evacuation w/ severe deficits temporal craniectomy, ventriculostomy 2 54 ruptured middle cerebral artery aneurysm uncal herniation, aneurysm clipping, temporal lobec- moderate hydrocephalus tomy,vp shunt deficits 3 38 ruptured middle cerebral artery aneurysm 6 NM hydrocephalus aneurysm clipping, VP shunt severe deficits 4 29 ruptured posterior communicating artery severe symptomat- aneurysm clipping, VP shunt good recovery aneurysm ic vasospasm 5 19 ruptured basilar tip aneurysm hydrocephalus, aneurysm clipping, VP shunt mild deficits vasospasm 6 22 posterior fossa ependymoma hydrocephalus, ependymoma resection, VP shunt vegetative status epilepticus state 7 59 frontotemporal & subarachnoid 5 20 uncal herniation, intracerebral hematoma evacuation, death hemorrhage hydrocephalus temporal lobectomy, ventriculostomy 8 39 ruptured ACoA aneurysm hydrocephalus aneurysm clipping, VP shunt mild deficits 9 49 large basal ganglia hypertensive hemorrhage 6 38 seizure, hydro- intracerebral hematoma evacuation, severe deficits cephalus ventriculostomy closed head injury 11 NM seizure temporal lobectomy w/ intracerebral good recovery hematoma evacuation ruptured large frontal & basal ganglia AVM none AVM resection, ventriculostomy mild deficits * ACoA = anterior communicating artery; AVM = arteriovenous malformation; GCS = Glasgow Coma Scale; ICP = intracranial pressure; NM = not monitored; VP = ventriculoperitoneal. eral SOV enlargement was seen in eight (38.1%); of 19 patients with normal ICP, only one (5.3%) had transient bilateral SOV enlargement, and even this patient exhibited increased ICP (up to 16 mm Hg) during the period of bilateral SOV enlargement. Two (13.3%) of the 15 patients who did not undergo monitoring had transient bilateral SOV enlargement associated with cerebral swelling. The bilateral SOV enlargement usually followed ICP elevations, either immediately or up to several hours later. Case Report History. This 41-year-old man (Case 10) was brought to the emergency room by his family members 4 hours after receiving an injury to the head during an assault. The patient suffered a generalized seizure in the emergency room prior to evaluation. His medical history was significant for moderate-to-severe alcohol consumption. Examination. On examination the patient was combative, exhibited slurred speech, and moved all four extremities spontaneously. His left pupil was reactive; his right pupil could not be evaluated because of a ruptured globe sustained 7 years previously. The patient exhibited no chemosis, palpebral swelling, or cranial nerve deficits, and no intracranial bruits were heard. A CT scan of the head showed diffuse cerebral swelling of the brain and FIG. 1. Initial CT scans in a patient with bilateral SOV enlargement. Left: Note the enlarged right superior ophthalmic vein (arrow) as well as the right temporal hemorrhage. The ethmoid air cells, sphenoid sinus, and mastoid air cells are clear. Right: The left superior ophthalmic vein is also enlarged (arrow). FIG. 2. Higher sections from the initial CT in the same patient. Left: There is diffuse cerebral swelling with loss of cisternal space as well as right frontal and left temporal lobe hemorrhages. The frontal sinuses are clear. Right: Note the diffuse cerebral swelling with obliteration of the sulcal pattern. 894
3 Bilateral SOV enlargement with cerebral edema TABLE 2 Serial CT findings in 11 patients with enlarged SOVs* Case No. Initial Head CT Scan First Follow-Up CT Scan Second Follow-Up CT Scan 1 bilat SOV enlargement, acute rt frontotemporoparietal 8-mm- 2 days later: smaller SOVs, resolved subdural thick subdural hemorrhage, 5-mm midline shift, entrapped hemorrhage & hydrocephalus, moderate lt lat ventricle diffuse cerebral swelling, no midline shift 2 bilat SOV enlargement, diffuse cerebral swelling, SAH 18 hours later: smaller SOVs w/ mild cere- 2 days later: smaller SOVs w/ mild in rt sylvian fissure, acute rt temporoparietal lobe hemor- bral swelling, rt temporal lobectomy w/ cerebral swelling & resolving rt rhage w/ 1.5-cm midline shift to lt side, rt lat IVH hemorrhage evacuation, persistent rt lat IVH ventricle hemorrhage, no midline shift 3 bilat SOV enlargement, diffuse cerebral swelling, impinge- 12 hours later: same findings as initial CT 1 day later: smaller SOVs w/ rt ment of rt lat ventricle w/ no midline shift, SAH in rt basal ganglia infarct & resolving sylvian fissure & bilat ambient cisterns rt sylvian fissure hemorrhage 4 small SOVs; mild hydrocephalus; SAH in rt sylvian fissure; 3 days later: bilat SOV enlargement w/ 6 days later: small SOVs w/ no suprasellar, perimesencephalic & ambient cisterns; diffuse cerebral swelling cerebral swelling fourth ventricle hemorrhage 5 bilat SOV enlargement; moderate hydrocephalus; SAH in 12 days later: smaller SOVs w/ resolved prepontine, suprasellar, bilat ambient cisterns & sylvian hydrocephalus, SAH, & fourth ventricle fissures; fourth ventricle hemorrhage hemorrhage 6 bilat SOV enlargement, diffuse edema especially in cere- 1 day later: bilat SOV enlargement, im- 6 days later: smaller SOVs, rebellum, mild hydrocephalus, SAH along folia of cere- proving edema, moderate hydrocephalus, solving edema, SAH, & IVH bellum & ambient cisterns lt lat ventricle hemorrhage 7 bilat SOV enlargement; SAH in prepontine, suprasellar, 4 days later: smaller SOVs, resolving ICH, lt ambient cistern & sylvian fissure; lt frontotemporal IVH, & SAH, no hydrocephalus hemorrhage; lt lat ventricle; third & fourth ventricle hemorrhage; moderate hydrocephalus 8 bilat SOV enlargement, rt frontal hemorrhage, bilat lat 1 day later: smaller SOVs, resolved frontal ventricle hemorrhage, moderate hydrocephalus hemorrhage, persistent ventricular hemorrhage, & hydrocephalus 9 bilat SOV enlargement, large lt frontotemporoparietal hemor- 1 day later: bilat SOV enlargement, resolving 7 days later: smaller SOVs, lt rhage, lt lat ventricle hemorrhage, midline shift of 7 cerebral hemorrhage & hydrocephalus, frontotemporoparietal mm, moderate hydrocephalus persistent lt frontotemporal edema, & 5-mm encephalomalacia midline shift 10 bilat SOV enlargement, diffuse cerebral swelling, acute bilat 10 days later: smaller SOVs w/ mild cerebral temporal rt frontal & lt parietal lobe hemorrhages swelling & rt temporal lobectomy w/ hemorrhage evacuation 11 bilat SOV enlargement; resected rt frontal/basal ganglia rup- 11 days later: smaller SOVs, resolved IVH & tured arteriovenous malformation; diffuse IVH & hydro- SAH, no hydrocephalus cephalus; SAH in rt frontal sulci, perimesencephalic, prepontine, & rt ambient cistern * ICH = intracerebral hemorrhage; IVH = intraventricular hemorrhage; SAH = subarachnoid hemorrhage. acute intracerebral hemorrhages in the temporal lobes bilaterally (much more pronounced in the right side) and in the right frontal and high left parietal lobes (Figs. 1 and 2). The routine thin CT sections through the posterior fossa also included the orbits and showed bilaterally enlarged SOVs with no evidence of cavernous sinus thrombosis (Fig. 1). The paranasal sinuses and the mastoid air cells were not opacified, and there was no evidence of any other intraorbital pathology. Operation. The patient was immediately taken to the operating room where the right temporal hematoma was evacuated and a decompressive right temporal lobectomy was performed. The patient received mannitol for his cerebral edema both pre- and postoperatively but an effort was made to avoid dehydration. Postoperative Course. Ten days postsurgery a repeated CT scan showed a normal-sized SOV bilaterally (Fig. 3) with a significant decrease in diffuse cerebral swelling (Fig. 4). At this time the patient was neurologically intact except for some mild cognitive impairment. Discussion Enlargement of an SOV can be detected reliably by high-resolution CT scanning. 2,7,10,11 Unilateral SOV enlargement has been reported secondary to cavernous sinus thrombosis, carotid cavernous fistula, Graves orbitopathy, orbital pseudotumor (idiopathic orbital inflammation), orbital varices and arteriovenous malformations, and parasellar tumors. 3,7,10 12 The SOV provides major orbital venous drainage into the cavernous sinus via the superior orbital fissure. Because of the lack of valves in this vein, retrograde flow from a carotid cavernous fistula or impaired venous outflow caused by cavernous sinus compression or thrombosis can lead to its enlargement. Compression of the SOV by enlarged extraocular muscles secondary to Graves disease, as well as intraorbital inflammation, infection, or neoplasm, can also cause SOV enlargement. Although unilateral SOV enlargement is more common, bilateral SOV enlargement has been reported infrequently in patients with Graves orbitopathy, cavernous sinus thrombosis, and carotid cavernous fistulas. 1,6,9,10 895
4 R. K. Khanna, et al. FIG. 3. Follow-up CT scans in the same patient. Left: The right superior ophthalmic vein (arrow) has returned to its normal size. Note the right temporal lobectomy. Right: The left superior ophthalmic vein (arrow) has also returned to its normal size. FIG. 4. Follow-up CT scans in the same patient. Left: Section at the same level as shown as Fig. 2 left. Note the decreased cerebral swelling and the presence of the cisternal spaces. Right: Section at the same level as shown in Fig. 2 right illustrating the decreased cerebral swelling with the normal appearance of the sulci and gyral pattern. Unlike the dural venous sinuses, the cavernous sinus is not formed by splits in the dura and therefore is easily compressible. The cavernous sinus is a venous plexus located on each side of the sphenoid bone beginning at the superior orbital fissure and extending to the petrous apex of the temporal bone. The two cavernous sinuses communicate via the intercavernous sinuses, which pass anteriorly and posteriorly to the sella turcica and pituitary gland. Generalized cerebral edema can lead to intracranial hypertension with consequent compression of the cavernous sinuses. Because the cerebral veins and venous sinuses do not have valves, blood within them can flow in either direction depending on the pressure gradients. Yasargil and Damur 14 have previously documented the phenomenon of mechanical venous stagnation with thrombosis of pial veins in patients with cerebral edema following closed head injury. Early appearance of SOV on carotid angiography also has been shown to occur in patients with increased ICP from brain tumors. 5 The reversibility of bilateral SOV enlargement in our patients after resolution of cerebral edema indicates that mechanical venous stagnation rather than venous thrombosis in the cavernous sinus was the cause of their condition, although initial cavernous sinus thrombosis secondary to intracranial hypertension with subsequent recanalization is another possible cause that cannot be excluded. This phenomenon of thrombosed cerebral vein recanalization has been documented by magnetic resonance imaging. 8 Prolonged intracranial hypertension accompanied by dehydration could easily lead to cavernous sinus and pial vein thrombosis, further exacerbating the cerebral swelling. We initially considered posttraumatic carotid cavernous fistulas as the likely cause of the bilaterally enlarged SOVs in patients with closed head injury. However, we subsequently ruled out this possibility based on the clinical picture and because both SOVs returned to normal size after resolution of the cerebral swelling. Posttraumatic fistulas usually do not disappear spontaneously. 9 Septic cavernous sinus thrombosis was also excluded as a possible cause because these patients had no predisposing infections. 4 Increased cerebral blood volume secondary to hyperemia from a generalized seizure could have led to cerebral swelling and/or bilaterally enlarged SOVs, but this is unlikely because no CT scan was obtained either during or immediately after a seizure, and any hyperemia should have resolved by the time the CT scans were obtained. Arteriovenous shunt placement for treatment of cerebral arteriovenous malformations can cause bilateral SOV enlargement in some patients; however, this was not the case in our patient with an arteriovenous malformation because the bilateral SOV enlargement was seen after resection of the malformation, at which time no arteriovenous shunting was present. The effect of PEEP on central venous pressure elevations and venous engorgement with subsequent SOV enlargement in some of our intubated patients also seems unlikely because the PEEP in our intubated patients was 5 mm Hg or less, thus exerting a negligible effect on central venous pressure elevations and/or venous engorgement. Conclusions We believe that bilateral enlargement of the SOVs occurs more commonly in patients with cerebral edema than is currently appreciated. When corroborated by other clinical criteria and by CT scanning for increased ICP, this finding usually reflects significant intracranial hypertension and may call for early aggressive treatment. A prospective analysis with magnetic resonance imaging and venography should ultimately provide a better understanding of the pathophysiological mechanism(s) involved in this syndrome. References 1. Ahmadi J, Teal JS, Segall HD, et al: Computed tomography of carotid-cavernous fistula. AJNR 4: , Bacon KT, Duchesneau PM, Weinstein MA: Demonstration of the superior ophthalmic vein by high resolution computed tomography. Radiology 124: ,
5 Bilateral SOV enlargement with cerebral edema 3. Brismar G, Brismar J: Thrombosis of the intraorbital veins and cavernous sinus. Acta Radiol Diag 18: , DiNubile MJ: Septic thrombosis of the cavernous sinuses. Arch Neurol 45: , Hacker H, Porrero M: Demonstration and significance of the superior ophthalmic vein in carotid angiography. Radiology 94:717, 1970 (Abstract) 6. Hasso AN, Lasjaunias P, Thompson JR, et al: Venous occlusions of the cavernous area a complication of crushing fractures of the sphenoid bone. Radiology 132: , Howard GR, Nerad JA, Carter KD: Superior ophthalmic vein enlargement and proptosis caused by middle cranial fossa lipoma. Am J Ophthalmol 110: , 1990 (Letter) 8. Macchi PJ, Grossman RI, Gomori JM, et al: High field MR imaging of cerebral venous thrombosis. J Comput Assist Tomogr 10:10 15, Mullan S: Carotid-cavernous fistulas and intracavernous aneurysms, in Wilkins RH, Rengachary SS (eds): Neurosurgery. New York: McGraw-Hill, 1985, pp Nugent RA, Belkin RI, Neigel JM, et al: Graves orbitopathy: correlation of CT and clinical findings. Radiology 177: , Peyster RG, Savino PJ, Hoover ED, et al: Differential diagnosis of the enlarged superior ophthalmic vein. J Comput Assist Tomogr 8: , Scotti LN, Goldman RL, Hardman DR, et al: Venous thrombosis in infants and children. Radiology 112: , Teasdale G, Jennett B: Assessment of coma and impaired consciousness. A practical scale. Lancet 2:81 84, Yasargil MG, Damur M: Thrombosis of the cerebral veins and dural sinuses, in Newton TH, Potts DG (eds): Radiology of the Skull and Brain. St. Louis: Mosby, 1974, pp Manuscript received September 18, Accepted in final form December 19, Address reprint requests to: Ghaus M. Malik, M.D., c/o Editorial Office, Department of Neurosurgery, Henry Ford Hospital, 2799 West Grand Boulevard, Detroit, Michigan
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