Clin Neuroradiol DOI 10.1007/s00062-014-0300-z

Correspondence

Quantitative Measurements of Cerebral Circulation in Spontaneously Regressing Traumatic Carotid-Cavernous Sinus Fistula with Velocity-Encoded Magnetic Resonance Imaging H. K. Kim · S. W. Youn · J. Lee

Received: 31 July 2013 / Accepted: 17 March 2014 © Springer-Verlag Berlin Heidelberg 2014

Introduction Carotid-cavernous sinus fistula (CCF) is an abnormal communication between the carotid artery and the cavernous sinus. Among the various subtypes, direct CCF (or Barrow type A CCF) is caused by a traumatic tear of the cavernous internal carotid artery (ICA) or rupture of a pseudoaneurysm within it [1, 2]. Pseudoaneurysm of the ICA may arise rarely from complete tearing of the arterial wall and the formation of a perivascular haematoma [3, 4]. The goal of treatment for direct CCF is to occlude the site of shunt flow while preserving the patency of the ICA [2], which can be accomplished by using coils [5, 6] and/or stent-graft placement [7, 8]. The clinical manifestations of CCF, such as exophthalmos, cephalic bruit, and conjunctival congestion, are related to the reflux of highly pressurized arterial blood directly into extradural veins such as the cavernous sinus and superior ophthalmic vein [2, 3, 9, 10]. However, there is currently very little information regarding the effect of shunt flow on cerebral vessels in direct CCF. Unlike dural arteriovenous fistulae, the severity of direct CCFs has never been graded based upon the haemodynamic impairment of cerebral veins [11]. Although it might be suggested by post-interventional angiographic findings, there have been no reports of direct

and quantitative evidence for whether endovascular occlusion would remove the shunts connected to extradural venous drainage alone, or further resolve the disturbance of cerebral venous flow. It is not known how cerebral vessels would change in the long-term as a result of obstructing this shunt flow, or how the clinical symptoms are related to the haemodynamic changes in the rare cases of spontaneous regression. The understanding of the pathophysiology of CCF can be enhanced by correlating the clinical symptoms and MRI findings during a long observational period. Velocity-encoded magnetic resonance imaging (VENCMRI) has shown excellent diagnostic accuracy and reliability for the measurement of the flow volumes (FVs) in cerebral vessels [12]. Furthermore, VENC-MRI does not require contrast medium administration or invasive catheterization, and is considered a safe and appropriate followup imaging technique [13]. However, this tool has never been used for quantifying the shunt volume and cerebral circulation related to CCF. A case in which VENC-MRI was used to measure the shunt volume of and FVs in the cerebral vessels in a direct CCF patient is presented herein. The temporal changes during spontaneous regression are demonstrated, and the relationships between the patient’s clinical symptoms and the measured cerebral haemodynamics are discussed. Clinical Details

S. W. Youn () · H. K. Kim Department of Radiology, Catholic University of Daegu School of Medicine, Daegu, Korea e-mail: [email protected] J. Lee Department of Radiology, Kyungpook National University School of Medicine, Daegu, Korea

A 38-year-old male driver was transferred to an emergency care centre after a motor-vehicle collision. He had severe chest discomfort, and a chest CT scan revealed aneurysmal dilatation of the aortic arch with concomitant haemothorax and fractures of multiple ribs and the sternum. He was alert and had no focal neurological deficit. However, he was

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found to have ptosis and diplopia 1 week after the motorvehicle collision when he was about to undergo stent-graft placement for traumatic arch aneurysm with transposition of the left common carotid artery. Conventional MRI revealed small signal voids in the left cavernous sinus and mild engorgement of the left superior ophthalmic vein. Time-of-flight (TOF) magnetic resonance angiography (MRA) revealed flow-related enhancements, mostly on the left side, in the cavernous sinus, superior ophthalmic vein, and inferior petrosal sinus (Fig. 1). In addition to these findings, which are suggestive of arteriovenous shunts, there was a pseudoaneurysm-like outpouching in the cavernous segment of the left ICA. The diagnosis of traumatic CCF with pseudoaneurysm of the ICA was made before catheter angiography. Catheter angiography was therefore delayed as far as possible since the patient was in the acute postoperative period with a transposed left common carotid artery, having undergone insertion of a stentgraft on the aortic arch, and most of his symptoms were non-urgent. FVs were measured at several locations with the aid of peripherally gated VENC-MRI (1.5 T; Signa, GE, Milwaukee, WI, USA), as described previously [13, 14]. The acquisition planes were at each level of the first and second cervical spine (C1 and C2), distal ICA, and coronal plane covering the superior ophthalmic vein or transverse sinus (Fig.  2). The MRI parameters were as follows: echo/repetition time, 4.4–7.1/12.0–14.5 ms; flip angle, 28°; field of view, 28 mm2; matrix, 256 × 128; slice thickness, 5  mm; encoding velocity, 80 cm/s. The images were processed using software (ReportCARD, GE) that manually extracts

the region of interest and calculates its flow curves over the 30 segments of the cardiac cycle. The combined FV in the ICAs and the vertebral arteries was 1,039 ml/min at C1/C2, and that of the ICAs and the basilar artery was 800 ml/min at the distal ICA level. The flow in the ICA on the patient’s affected side was higher than in an age- and sex-matched normal subject selected from the VENC-MRI database of our institution (616 ml/ min versus 290 ml/min). The FV of the extradural venous drainage associated with CCF was 171 ml/min at the cavernous sinus, 58 ml/min at the left superior ophthalmic vein, and 241 ml/min at the inferior petrosal sinus (versus 103 ml/ min in the normal subject). The FV measured at the pseudoaneurysmal sac was 316 ml/min. In the normal subject, the flow at the cavernous sinus was within undetectable ranges at an encoding velocity of 80 cm/s; ophthalmic vein data were unavailable. The sum of the FV in the superior sagittal and straight sinuses was 361 ml/min in the distal ICA plane (versus 460 ml/min in the normal subject) and 376 ml/min in the coronal plane covering the transverse sinus. TOF-MRA performed 1 week later revealed a dramatically decreased flow-related enhancement in the cavernous sinus. Catheter angiography performed at 3 weeks after stent-graft placement (i.e., 4 weeks after the collision) revealed no demonstrable CCF and a small residual sac of the pseudoaneurysm. The treatment plan was thus revised to repeat follow-up imaging instead of endovascular intervention. The sac disappeared and the shunt flow was absent at the 5-month follow-up imaging. The patterns of interval changes in FVs were observed at 1 week, 2 weeks, 1 month, and 5 months after the collision.

Fig. 1  Imaging in a 38-year-old male who presented with ptosis and diplopia after a motor-vehicle injury. a Projection view and b source image of initial time-of-flight (TOF) magnetic resonance angiography (MRA) showed flow-related enhancement in the left cavernous sinus (solid arrow), superior ophthalmic vein (arrowhead) and inferior petrosal sinus (broken arrow). A saccular pseudoaneurysm (asterisk)

arises anteriorly from the left internal carotid artery (ICA). c A 3Dreconstructed image obtained 3 weeks after the initial examination via rotational catheter angiography, revealed a small pseudoaneurysm (asterisk) arising from the petrous ICA. A carotid-cavernous sinus fistula (CCF) was not found. d TOF-MRA performed 5 months after the collision revealed no visible CCF or pseudoaneurysm

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Fig. 2  Acquisition of velocity-encoded magnetic resonance imaging and image analysis. a T2-weighted midline sagittal image was used for localizing the plane. b&c, plane for the distal ICAs, basilar artery and cavernous sinus; c1-2, plane for the proximal ICA and vertebral arteries; sov, coronal plane perpendicular to the superior ophthalmic vein; cor, coronal plane perpendicular to the transverse sinus. b, c At the plane covering the distal ICA and basilar artery, the regions of inter-

est (ROIs) were drawn on the cavernous sinus (blue line) and inferior petrosal sinus (white ellipse). Separate ROIs are drawn on the right and left ICAs and the pseudoaneurysm on the left side (asterisk). d An ellipsoid ROI drawn on the coronal plane perpendicular to the superior ophthalmic vein to indicate the engorged left-side vein with flow in the anterior direction

Fig. 3  Temporal changes of flow volumes (FVs, ml/min) in the CCF and its venous drainage during the 5-month follow-up period. a CCF and its related extradural venous drainage. The FVs in the cavernous sinus, inferior petrosal sinus, and left superior ophthalmic vein decreased rapidly at 1 week, and those of the pseduoaneurysm gradually decreased during the follow-up period. CAV cavernous sinus, PseudoA pseudoaneurysmal sac, SOV left superior ophthalmic vein, IPS inferior

petrosal sinus. b The FVs in the ICAs plus the vertebral arteries (ICAs + VAs) decreased during the first 2 weeks of the follow-up period, and then rebounded and stabilized. The FVs in the straight sinus plus the superior sagittal sinus (SS + SSS) and the transverse sinus (TS) increased gradually during the follow-up period. c The ratio of FVs between (SS + SSS) or TS and (ICAs + VAs) also improved gradually over time

With regard to the extradural venous drainage associated with the CCF, there was a rapid reduction in the flows in the cavernous sinus (from 171 to 59 ml/min), inferior petrosal sinus (from 241 to − 7 ml/min), and left superior ophthalmic vein (from 58 to − 8  ml/min) at 1 week, and those of the pseduoaneurysm gradually decreased during the measurement period (from 316  ml/min to 130  ml/min at 1 week, 78 ml/min at 2 weeks and 0 ml/min at both 1 and 5 months; Fig. 3a). The FV in the cerebral arteries decreased as the FVs in the CCF and its extradural venous drainage decreased (Fig.  3b). However, that of the cerebral veins exhibited a gentle increment during the measurement period, resulting

in a remarkable increment of the FV ratios between venous sinus and the cerebral arteries (Fig. 3c). The patient’s symptoms of ptosis and diplopia started to improve at the 1 week follow-up imaging, and disappeared gradually during the subsequent 5 months of clinical follow-up. Discussion In this study, we used serial TOF-MRA and VENC-MRI to demonstrate the haemodynamic features of traumatic CCF with pseudoaneurysm of the ICA, and its spontane-

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ous regression in a survivor of a road-traffic collision. To the best of our knowledge, this is the first use of VENCMRI to depict the improvements in cerebral circulation in a spontaneously regressing direct CCF. Approximately 2.7 % (4/148) of CCFs close spontaneously [15], and prompt endovascular embolization is generally performed for this high-flow lesion, without waiting for spontaneous closure [2–5, 7, 8]. Although catheter angiography is the gold-standard confirmative diagnostic method and planning imaging modality for endovascular embolization, it requires invasive catheterizations and carries with it a radiation hazard. Therefore, catheter angiography and endovascular treatment were delayed in the present patient to avoid catheterization through the transposed common carotid artery with its vulnerable orifice. This clinical situation necessitated the diagnosis of CCF without performing catheter angiography and provided the chance to observe its natural course non-invasively. The use of VENC-MRI provides confidence for noninvasive diagnosis by adding quantitative information to the presumptive diagnosis based on TOF-MRA. The flowrelated enhancement of the cavernous sinus, superior ophthalmic vein, and inferior petrosal sinus on TOF-MRA was not mistaken as normal variations, such as venous reflux of the internal jugular vein [16–18], and measurement of the FVs in the aforementioned structures on VENC-MRI further supported the presence of an arteriovenous shunt. The initially high FV in the cerebral arteries seemed to contribute greatly to the shunt flow and the related extradural venous engorgement, rather than to compensate for deficient cerebral veins. Ptosis and diplopia were the main symptoms in this patient, and the initial high FV in the cerebral arteries, shunt volume, and its related extradural venous drainage vessels was strongly correlated with these symptoms. While redeye is associated with congestion of anterior drainage vessels such as the ophthalmic veins and extraocular muscles, ptosis and diplopia are related to cranial nerve palsy close to the posterior drainage into the inferior petrosal sinus [9, 10]. The FV was greater in the inferior petrosal sinus (241 ml/ min) than in the left superior ophthalmic vein (58 ml/min) at the initial examination, which suggested that his cranial nerve palsy was associated with engorgement of the posterior venous drainage. The oculomotor nerve is known to be the most commonly compromised nerve in shunts with posterior venous drainage, of which the potential causes include nerve compression, dural arterial steal, and venous congestion [10]. Non-invasive TOF-MRA and VENC-MRI have advantages over catheter angiography, especially when used for follow-up imaging. On the follow-up imaging, arrest or spontaneous regression was noted from the disappearance of flow-related enhancement on TOF-MRA and decreasing

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shunt volumes on VENC-MRI. Interestingly, the improvement of the symptoms and disappearance of flow-related enhancement at the cavernous sinus coincided temporally with the decrease in the volume and extradural venous drainage of the shunt. In contrast, the cerebral venous flow increased gently during that period, and the ratios between venous sinus flows and cerebral arterial flows had improved remarkably, suggesting that the spontaneous closure of the shunt exerted a beneficial effect on the cerebral circulation both by improving the proper cerebral arterial supply and removing cerebral vein disturbances. Notwithstanding the limitation that the data reported herein were obtained from observations of a single patient, it appears that VENC-MRI could be useful as an adjunct to TOF-MRA for assessing and monitoring shunt volume and the impaired cerebral circulation of CCF patients. Acknowledgements  This work was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by Ministry of Education, Science and Technology (grant number NRF-2011-0014573). Otherwise the authors have no conflicts of interest to declare. Conflict of Interest  The authors have no conflict of interest.

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Quantitative Measurements of Cerebral Circulation in Spontaneously Regressing Traumatic Carotid-Cavernous Sinus Fistula with Velocity-Encoded Magnetic Resonance Imaging.

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