| OCR Text |
Show ORIGINAL CONTRIBUTION Restricted Diffusion in the Superior Ophthalmic Vein and Cavernous Sinus in a Case of Cavernous Sinus Thrombosis Hemant Parmar, MD, Dheeraj Gandhi, MD, Suresh K. Mukherji, MD, and Jonathan D. Trobe, MD Abstract: A previously healthy 14-year-old boy developed headache, stiff neck, fever, diplopia, right proptosis, and right complete sixth and partial third cranial nerve palsies. Orbital CT showed features of pansinusitis and orbital fat stranding. An initial diagnosis of orbital cellulitis was made. However, closer inspection of the CT disclosed nonfilling of the right superior ophthalmic vein (SOV) and both cavernous sinuses, suggesting cavernous sinus thrombosis (CST). CT venography (CTV) confirmed these features and disclosed nonobstructing thrombus within the left sigmoid sinus and proximal segments of both internal jugular veins. MRI with diffusion imaging disclosed evidence of restricted diffusion within the SOV and cavernous sinuses. These diffusion imaging findings, which may be analogous to those reported with brain parenchymal hematoma, have been described sparingly in intravascular hematoma. (J Neuro-Ophthalmol 2009;29:16-20) Cavernous sinus thrombosis (CST) is a relatively rare but life-threatening cause of a cavernous sinus syndrome in immunocompetent patients (1). The primary source of sepsis may be a distant focus or contiguous regions (2). The dural sinuses and the cerebral and emissary veins have no valves, allowing blood to flow in either direction according to pressure gradients in the vascular system. This feature, together with the extensive direct and indirect vascular connections of the centrally located cavernous sinuses, makes these structures vulnerable to septic thrombosis from infected tributary sites such as the Department of Radiology (HP, DG, SKM), Division of Neuroradiology, and Departments of Ophthalmology and Neurology (JDT), University of Michigan Health System, Ann Arbor, Michigan. Address correspondence to Hemant Parmar, MD, Department of Radiology, University of Michigan, 1500 East Medical Center Drive, Ann Arbor, MI; E-mail: parurad@hotmail.com/hparmar@umich.edu face, nose, tonsils, soft palate, teeth, and ears. Once antibiotic therapy became widely available, however, the sphenoid sinus emerged as the most common primary source of infection predisposing to CST. We report a patient who presented with clinical features initially suggesting orbital cellulitis as the primary process. Careful analysis of the clinical and imaging features led to the diagnosis of CST with secondary thrombosis of the right superior ophthalmic vein (SOV) and ipsilateral orbital congestion. We also report MRI evidence of restricted diffusion within the thrombosed cavernous sinuses and SOV, a feature not previously described. CASE REPORT A 14-year-old boy developed headache, diplopia, proptosis, and swelling of the right eyelids and redness of the right eye. One day later, he complained of neck pain. His mother noted him to be feverish, confused, and hallucinating. For the preceding 2 days, he had lost appetite and had had a few bouts of vomiting. He complained of marked photophobia. He had felt weak and had diarrhea for 1 week earlier, manifestations attributed to a ‘‘flu-like'' illness circulating among family members. His past medical history was unremarkable except for a chronic postnasal drip. Oph-thalmologic examination 6 years earlier had been normal. Emergency room examination disclosed a tempera-ture of 102F with 80% oxygen saturation, blood pressure of 110/60 mmHg, pulse of 140, and respirations of 20. His neck was stiff. General physical examination findings were otherwise normal. Ophthalmologic examination was difficult because of the patient's extreme photophobia and irritability. However, it disclosed normal visual acuity and confrontation visual fields in both eyes. There were no abnormalities of the left eye. There was incomplete right upper lid ptosis and upper and lower eyelid edema with 8 mm of right proptosis but no tenderness to palpation or resistance to retropulsion of the right eye. The conjunctiva of the right eye was mildly hyperemic but not edematous. The right eye was deviated 16 J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 Cavernous Sinus Thrombosis J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 inward and could not be abducted beyond the midline. Adduction and infraduction were normal. Supraduction was 50% of normal. The pupils measured 4 mm in dim light and constricted briskly and equally to direct light without afferent defect. Intraocular pressures were 17 mmHg in the right eye and 14 mmHg in the left eye. Portable slit-lamp examination was normal and ophthalmoscopy showed clear media and no abnormalities of the retina or optic nerves. Neurologic examination disclosed that the patient was disoriented to time and place, irritable, and inattentive. There were no focal deficits apart from those affecting the eyes. Postcontrast CT of the orbits showed right proptosis and ‘‘fat stranding'' in the right orbit (Fig. 1A-B). The right FIG. 1. Initial CT. A. Axial view shows right proptosis and opacification of paranasal sinuses. B. Coronal view shows inhomogeneous attenuation of fat in the right orbit (arrows); there is no subperiosteal or intraorbital abscess. superior ophthalmic vein (SOV) was enlarged and did not enhance normally, suggesting thrombosis. Poor contrast enhancement was noted within both cavernous sinuses (right more than left). The maxillary, ethmoid, frontal, and sphenoid sinuses showed mucosal thickening, and there was an air-fluid level in the frontal sinuses. The initial emergency room diagnosis was orbital cellulitis. However, the ophthalmic findings of complete right sixth cranial nerve palsy and superior division right third cranial nerve palsy, together with the orbital CT findings, were more consistent with a retro-orbital (cavernous sinus) than with an orbital process. Hemoglobin was 11.2 g, white cell count was 18,300 with neutrophil predominance, and standard chemistry results were normal, including hepatic and renal panels and urinalysis. Lumbar puncture without a recording of opening pressure disclosed protein of 142 mg/dL, glucose of 42 mg/dL (serum glucose of 100 mg/dL), red cell count of 2,037, white cell count of 303 (neutrophils 65%), and a negative Gram stain. Blood and spinal fluid culture results were negative. CT venography (CTV) did not show the expected contrast opacification of the right cavernous sinus and showed only minimal contrast opacification of the anterior aspect of the left cavernous sinus (Fig. 2A-B). There was mass effect with narrowing of cavernous segments of both internal carotid arteries. The right SOV was enlarged and showed no contrast (Fig. 2C). The left SOV was normal. There was also no contrast within the left superior petrosal sinus (Fig. 2D), and there were nonobstructive filling defects within the left sigmoid sinus (Fig. 2E) and proximal segments of both internal jugular veins (Fig. 2F). MRI of the brain and orbits was performed 1 day later with a 3.0-T Achieva magnetic resonance system (Philips Medical Systems, Best, The Netherlands) using an 8-channel SENSE head coil. Diffusion imaging data were obtained using an echo-planar single-shot technique with the shortest TR, 49 ms TE and a 90 flip angle, and a b value of 1,000 seconds/mm2. The data were recorded on a 128 128 matrix and were zero-filled for a final resolution of 128 256. Axial slices with 4-mm slice thickness and a 1-mm interslice gap were obtained. A SENSE P factor of 3 was used. The total imaging time was 49 seconds. MRI confirmed the CT findings. T2 (Fig. 3A) and precontrast T1 (Fig. 3B) images showed heterogeneous signal within these regions. On postcontrast T1 images, there were filling defects within both cavernous sinuses. There was also extensive thickening and enhancement of the walls of the cavernous sinuses, adjacent tentorium (Fig. 3C), and dural lining of the cerebral hemispheres. The dural enhancement was attributed to reactive dural conges-tion or changes due to recent lumbar puncture. Diffusion images revealed high signal and corresponding apparent 17 J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 Parmar et al FIG. 2. CT venography. A. Axial view shows lack of expected enhancement of both cavernous sinuses (arrows). B. Coronal view also shows lack of enhancement of cavernous sinuses, which have bulging lateral walls (arrows). There is mass effect and narrowing of cavernous segments of the internal carotid arteries. C. Coronal view through the mid orbit shows a dilated and nonenhancing right superior ophthalmic vein (SOV) (arrow). Compare with the normal caliber and enhancing fellow SOV (arrowhead). D. Coronal view shows no enhancement of the left superior petrosal sinus (arrows). Compare with the normal superior petrosal sinus on the opposite side (arrow). E. Axial view shows a nonobstructive filling defect in the left sigmoid sinus (arrow). Compare with the normal right sigmoid sinus (arrowhead). F. Axial view shows nonobstructive filling defects in both internal jugular veins (arrows). coefficient diffusion (ADC) low signal within both cavern-ous sinuses (Fig. 4A-B) and the right SOV (Fig. 4C-D). These diffusion abnormalities were attributed to thrombosis. When added to the clinical findings, these imaging findings led to a change in diagnosis from orbital cellulitis to sphenoid sinusitis causing CST and meningitis with secondary SOV thrombosis and right orbital congestion. The signal abnormalities in the jugular and left sigmoid sinuses were believed to represent propagated clot from the cavernous sinuses. The patient was treated with intravenous 10 mg/kg vancomycin every 6 hours, 4 g piperacillin/tazobactam FIG. 3. MRI performed 1 day later. A. T2 axial. B. Precontrast T1 axial. These images show mild heterogeneous signal abnormality within both cavernous sinuses. C. Postcontrast T1 image shows lack of normal enhancement within the cavernous sinuses (arrows). There is diffuse reactive enhancement of the walls of cavernous sinuses and adjacent tentorium (arrowheads) partially attributable to a recent lumbar puncture. 18 q 2009 Lippincott Williams & Wilkins Cavernous Sinus Thrombosis J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 FIG. 4. A, B. Both cavernous sinuses show hyperintensity (A, arrows) with corresponding apparent diffusion coefficient (ADC) hypointensity (B, arrows). C, D. The anterior segment of the right superior ophthalmic vein (SOV) shows hyperintensity (C, bracketed by arrows) with corresponding ADC hypointensity (D, bracketed by arrows). These signal abnormalities reflect restricted diffusion owing to thrombosis. every 6 hours, and 5 mg/kg metronidazole every 6 hours and heparin (later enoxaparin). Within 2 days, his mental status had normalized and the lid edema, ptosis, and supraduction deficit had improved. All other ophthalmic findings persisted at discharge 1 week after admission. Follow-up brain MRI after 3 months showed interval improvement in the right cavernous sinus opacification. There was, however, some residual narrowing of the right internal carotid artery and the right SOV still did not show complete opacification. The diffusion images were not reliable as the follow-up examination was performed on the MRI sequence without parallel imaging. DISCUSSION Our patient had typical clinical and imaging features of CST, but bacterial orbital cellulitis spreading from adjacent ethmoid sinusitis was the initial diagnosis because unilateral proptosis and ptosis in a young patient are much more likely to represent this process. It was only after we carefully analyzed the clinical and full imaging features that we determined the diagnosis of CST. Absent abduction and impaired supraduction and ptosis in the presence of spared adduction and infraduction favored a retro-orbital rather than an orbital process. The lack of contrast opacification in both cavernous sinuses, the right SOV, and the left superior petrosal sinus, together with filling defects in the sigmoid sinuses and internal jugular veins, confirmed that CST was the cause of the proptosis. The imaging evidence of bilateral CST, even when clinical manifestations are limited to one side, is consistent with previous reports demon-strating up to 75% incidence of bilateral imaging findings with unilateral clinical presentations (3). 19 J Neuro-Ophthalmol, Vol. 29, No. 1, 2009 Parmar et al Although CT imaging provides ample evidence of CST, MRI is critical for evaluation of potential complica-tions of CST such as intracranial dissemination of infection or cerebral infarction. In our patient, MRI also unex-pectedly revealed abnormalities on diffusion imaging that have not been previously described in CST or in any cases of intravascular thrombosis in the head and neck. Although restricted diffusion has been described within the optic nerve owing to venous ischemia from CST (4-6), restricted diffusion within the SOV and cavernous sinuses was not mentioned in those reports. Diffusion imaging is a relatively new technique for evaluating the diffusion properties of tissue water mole-cules and has been used widely to study ischemia, tumors, infections, and white matter disorders (7,8). There are few reports of its use in lesions of the skull base and orbits, perhaps because these regions contain inhomogeneous tissues (bone, air, fat, and soft tissue) that produce severe susceptibility artifacts (9). Wider availability and applica-tion of sensitivity encoding (SENSE), the technique we applied, may enhance the quality of echo-planar diffusion imaging by reducing the blurring and off-resonance artifacts at the skull base and posterior fossa (9). Diffusion imaging has been evaluated previously for intraparenchymal brain hematoma, for which it produces a variety of signal abnormalities depending on the stage of the hematoma (10,11). In the hyperacute stage, the diffusion imaging signal is high owing to restricted diffusion from shrinkage of the extracellular space caused by clot retraction, plasma resorption, and conformational changes in the hemoglobin molecule. In the acute, early subacute, and chronic stages, the diffusion imaging signal is hypointense owing to magnetic inhomogeneity from intracellular deoxyhemoglobin (acute stage), paramagnetic intracellular methemoglobin (subacute stage), and hemo-siderin (chronic stage). Because a susceptibility artifact from this inhomogeneity causes marked diffusion imaging hypointensity, ADC measurements in these stages cannot be reliably calculated (7,11). The only exception to the uniformly hypointense signal in these periods occurs in the late subacute stage, in which red blood cell lysis, distribution of intracellular contents in the extracellular space, and high viscosity from inflammatory cell and macrophage infiltration may contribute to restricted diffusion and diffusion imaging hyperintensity (11). Favrole et al (12) reported restricted diffusion within intravascular clots in 12 (41%) of 28 patients with cerebral venous thrombosis on MRI examination performed between 1 and 30 days after clinical onset. None of their cases involved the cavernous sinus or superior ophthalmic veins. Moreover, they did not attempt to date the thrombus based on the diffusion imaging findings. Our patient demonstrated mostly a very high diffusion imaging signal, which should correspond to the hyperacute stage of brain parenchymal hematoma. Yet the diffusion imaging study was performed several days into his illness. Perhaps intravascular thrombi do not undergo the evolutionary stages described for intraparenchymal hematoma. We have seen similarly high diffusion imaging signal abnormalities well after the hyperacute stage in intramural hematoma in arterial dissection (unpublished data) and as recently reported by Choi et al (13). Our report suggests that diffusion imaging may be helpful in the diagnosis of cavernous sinus and superior ophthalmic vein thrombosis. The absence of restricted diffusion, however, should not exclude the diagnosis. Correlation of clinical signs with conventional imaging signs remains important in this regard. Further studies of diffusion imaging signal abnormalities in patients with intravascular thrombosis and arterial and venous hemato-mas will be helpful to validate our findings. REFERENCES 1. Ebright JR, Pace MT, Niazi AF. Septic thrombosis of the cavernous sinuses. Arch Intern Med 2001;161:2671-6. 2. Pavlovich P, Looi A, Rootman J. Septic thrombosis of the cavernous sinus: two different mechanisms. Orbit 2006;25:39-43. 3. Mukherji SK, Tart RP, Mancuso AA. Septic cavernous sinus thrombosis revisited. Appl Radiol 1995;24:35-8. 4. Chen JS, Mukherjee P, Dillon WP, et al. Restricted diffusion in bilateral optic nerves and retinas as an indicator of venous ischemia caused by cavernous sinus thrombophlebitis. AJNR Am J Neuroradiol 27:1815-6 5. Al-Shafai LS, Mikulis DJ. Diffusion MR imaging in a case of acute ischemic optic neuropathy. AJNR Am J Neuroradiol 2006;27:255-7. 6. Mathur S, Karimi A, Mafee MF. Acute optic nerve infarction demonstrated by diffusion-weighted imaging in a case of rhinocere-bral mucormycosis. AJNR Am J Neuroradiol 2007;28:489-90. 7. Schaefer PW, Grant PE, Gonzalez RG. Diffusion-weighted MR imaging of the brain. Radiology 2000;217:331-45. 8. Rowley HA, Grant PE, Roberts TP. Diffusion MR imaging: theory and applications. Neuroimaging Clin N Am 1999;9:343-61. 9. Jaermann T, Crelier G, Pruessmann KP, et al. SENSE-DTI at 3 T. Magn Reson Med 2004;51:230-6. 10. Atlas SW, DuBois P, Singer MB, et al. Diffusion measurements in intracranial hematomas: implications for MR imaging of acute stroke. AJNR Am J Neuroradiol 2000;21:1190-4. 11. Kang BK, Dong GN, Ryoo JW, et al. Diffusion-weighted MR imaging of intracerebral hemorrhage. Korean J Radiol 2001;2: 183-91. 12. Favrole P, Guichard JP, Crassard I, et al. Diffusion-weighted imaging of intravascular cerebral venous thrombosis. Stroke 2004;35:99-103. 13. Choi KD, Jo JW, Park KP, et al. Diffusion-weighted imaging of intramural hematoma in vertebral artery dissection. J Neurol Sci 2007;253:81-4. 20 q 2009 Lippincott Williams & Wilkins |
