Transcranial Doppler Sonography in Carotid-Cavernous Fistulas:Analysis of Five Cases

Zainal Muttagin, M .D., Kazunori Arita, M.D., Tohru Uozumi, M.D.,Satoshi Kuwabara, M .D., Shuichi Oki, M.D., Sinji Ohba, M.D., Kaoru Kurisu, M.D .,Toshinori Nakahara, M.D ., Hiroaki Kohno, M.D., and Hideki Satoh, M .D.Department of Neurosurgery, Hiroshima University School of Medicine, Hiroshima, Japan

Muttagin Z, Arira K, Uozumi T, Kuwabara S, Oki S, Ohba S,Kutisu K, Nakahara T, Kohno H, Satoh H . Transcranial dopplersonography in carotid-cavernous fistulas : analysis of five cases . SurgNeurol 1992 ;38:179-85 .

Transcranial doppler sonography was performed transor-bitally in five patients clinically diagnosed as unilateralcarotid-cavernous fistula. Dural arteriovenous malfor-mation related-shunts were detected in all the patients .In the normal eyes, the only doppler signals observed atan insonation depth of 45 to 55 mm were those of theophthalmic artery . In the affected eyes, abnormal dopplersignals with relatively higher flow velocity and lower re-sistance were observed . In three of the cases, these abnor-mal signals showed a flow directed anteriorly or awayfrom the cavernous sinus, consistent with changes in theophthalmic veins caused by the presence of the shunts .In two cases, however, the observed flows were directedposteriorly, the normal direction of these veins . The possi-ble explanations for this discrepancy are discussed in rela-tion with angiographic findings . The use of transcranialdoppler might provide a better understanding about he-modynamic changes in carotid cavernous fistulas .

KEY WORDS : Transcranial doppler; Carotid-cavernous fistula

The introduction of a high-energy, pulsed doppler sys-tem by Aaslid et al [1,2] enables one particular vessel tobe examined in isolation, at a defined depth, and this isworked out by means of an electronic gate, in whichdoppler shifts are registered only at certain distancesfrom the probe, within a defined sample volume [1] .Aaslid et al [21 and Hennerici et al [10] recommendedthe mean flow velocity values to be used to discriminatenormal from abnormal conditions . Using one of thethree transcranial windows mentioned by many authors

Address reprint requests to : Zaina[ Muttagin, M.D., Department ofNeurosurgery, Hiroshima University School of Medicine, 1-2-3 Ka-sumi, Minami-ku, Hiroshima 734, Japan .

Received October 25, 1991 ; accepted February 21, 1992 .

® 1992 by Elsevier Science Publishing Co ., Inc .

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[1,2,8,14], it is possible to measure the normal flowvelocity of the basal cerebral arteries and their mainbranches. The orbital window may be used to insonatethe carotid siphon, ipsilateral ophthalmic artery, andsometimes even the precommunicating segment of thecontralateral anterior cerebral artery [1,7,14] . The oph-thalmic artery can normally be sampled at a depth of 40to 55 mm, with its characteristic of higher resistance thanother intracranial vessels and its flow directed towardthe doppler probe [6,7,14] . Normal mean flow velocityof the ophthalmic artery is 21 + 5 cm/second [14] .

Carotid-cavernous fistulas (CCF5) are abnormal com-munications between the carotid artery or its duralbranches and the cavernous sinus. Symptoms and signsare usually related to orbital congestion caused by retro-grade filling of the ophthalmic veins from the cavernoussinus [3,4] . The diagnosis of CCF can be made by com-puted tomographic (CT) scan or magnetic resonanceimaging (MRI) scan [5,12], but the clear definition de-pends on the demonstration of direct or indirect shunt-ing from the carotid artery or its dural branches intothe cavernous sinus on cerebral angiography [8,14] . Itsclassification into high or low flow still depends on angio-graphic results alone [3,4] . On the other hand, angiogra-phy is invasive and has some potential risks that make itimpractical for continuous monitoring and for repeatedfollow-up in patients with CCF. Transarterial injectionof contrast material also gives an additional pressure,which may cause a temporary hemodynamic change lo-cally, and therefore influences the real angiographic pic-tures, especially in low-flow arteriovenous shunts . Re-ported here are the results of transcranial dopplerexamination in five CCF cases ; they are analyzed in rela-tion to the clinical and radiological findings .

Subjects and MethodsThe study involved five patients clinically diagnosed ashaving unilateral, spontaneous CCF . They were all ad-mitted to the Department of Neurosurgery, Hiroshima

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TCD in Carotid-Cavernous Fistulas

Figure 1 ; Case 1 . (A) MRI angiography (upper left) showed the rightsuperior ophthalmic vein asterisk) . Angiograpby, showed the early opacifi-cation of the right cavernous sinus (small arrow) and the right superiorophthalmic vein (large arrow), and revealed that this dural AVM-relatedCCF is fed by the ducal branches of the right internal and external carotidarteries directly, and also by the left external and internal carotid arteriesthrough intercavernous sinus. (B) Transcranial doppler result of the righteye showed a relatively high flow velocity and low resistance signals directedanteriorly (notice the direction of the small arrow away from doppler probeon the upper right side of each recording), which is consistent with thearterialized right superior ophthalmic vein . That of the left eye demonstratedonly signals of the normal ophthalmic artery . Normal signals of the rightophthalmic artery were seen overlapped by the higher signal of the shuntedvein (large white arrow).

University Hospital, between July 1990 and June 1991 .Transarterial carotid angiography using conventional ordigital subtraction angiography was performed, selec-tively if possible, on all patients. Transcranial dopplerexaminations were done through the orbital window, insupine position, using a TC2-64 Transcranial Doppler(EME, Uberlingen, Germany) . Insonations were donefrom the superior palpebrae, over a closed eye, withdepths of 45, 50, and 55 mm . Doppler intensity was setat 10% of spatial peak temporal average, as recom-mended by the Bioeffect Committee of the AmericanInstitute of Ultrasound in Medicine [8) . Doppler signalsof the ophthalmic arteries in the normal eyes served asnormal controls .

The patients consisted of three men and two women,age 56 to 67 years (mean 61 .6 years). All had spontane-ous, unilateral, ducal arteriovenous malformation(AVM)-related CCFs, four on the right side and one onthe left side. All patients complained of orbital conges-tion of the involved eyes . Exophthalmos was found intwo patients, but they all experienced or had once expe-

Table 1 . Characteristics of Patients with Carotid-Cavernous Fistula

rienced some kind of tinnitus or bruit, four ipsilaterallyand one contralaterally (case 1) . Table 1 describes detailsof patients' signs and symptoms and their angiographicfindings . CT had been performed in two patients andMRI angiography in another one, and all the resultsshowed an enlarged intraorbital vein in the affected side .

ResultsThe results of transcranial doppler examination weredetailed in Table 2 . In all cases, normal signals from theophthalmic artery were the only flow signals observedin the healthy side. These were directed anteriorly andhad mean flow velocities between 16 and 32 cm/s (mean23.6 em/s) and pulsatility indices between 1 .0 and 1 .9(mean 1 .32) . On the pathological side, besides signals ofthe normal ophthalmic artery, there were other signalswith relatively higher flow velocity and lower resistance .These abnormal signals were seen to overlap the signalsof the normal ophthalmic artery (cases 1 and 2) or wereseen as separate signals by moving the insonation angleslightly (cases 3, 4, and 5) . In the first three cases, theseabnormal signals indicated anteriorly directed flow, or adirection away from the cavernous sinus (Figure 1 B) .In the other two cases, however, the abnormal signalsindicated a posteriorly directed flow, exactly the same asthe normal flow direction of the normal ophthalmic vein(Figure 3 B). The vessel's resistance, as shown by thepulsatility index values, ranges from 0 .39 to 0.89 (mean0.62), and flow velocity varies between 20 to 70 cm/s(mean 42.4 cm/s). In case 4, internal carotid angiographyshowed a slight opacification of the superior ophthalmicvein in the late arterial phase (Figure 3 A) . External

Signs and symptoms

Present

Orbital headache,chemosis of right eye

Chemosis, exophthalmos,and rerroorbital pain

Bruit, chemosis, doublevision, and mild ptosisof the left eye

Chemosis, exophthalmos

Chemosis, bruit(preauricular), doublevision, mild ptosis

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Feeding arteries

Cavernous branches ofbilateral ICAs, bilateralIMAs, bilateral MMAs

Cavernous branch ofright ICA

Cavernous branch(es) ofleft ICA

Cavernous branch ofright ICA, right IMA,right MMA

Right ascendingpharyngeal, right IMA

Abbreviations . CCF, carotid-cavernous fistula ; M, male ; ICA, internal carotid artery ; IMA, internal maxillary artery; MMA, middle meningeal artery ; F, female .

Case Sex Age, yr CCF side Initial

I M 56 Right Bruit (contralateral),

F 61 Right

orbital headache,chemosis of right eye

Chemosis, exophthalmos,

3 M 67 Left

double vision, andright retroorbital pain

Bruit, chemosis, double

F 59 Right

vision, and mild ptosisof the left eye

Bruit, chemosis,

5 M 65 Right

exophthalmos, andretroorbital pain of theright eye

Bruit, chemosis, doublevision, and mild prosisof the right eye

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TCD in Carotid-Cavernous Fistulas

Figure 2 ; Case 4. (A) Right internal carotid arteriography opacifiedipsilateral superior ophthalmic vein (large arrow) in the laterarterial phase.Right external carotid arteriograpby showed feeding arteries from the inter-nal maxillary artery and middle meningeal arteries . The right cavernoussinus (small arrow) was weakly opacified, and drained posteriorly to theinferior pet royal sinus and the jugular vein (arrowhead) . (B) Signals of thenormal ophthalmic arteries were observed in both eyes 4eLt and middle) .However, a little change of the insonation angle in the right eye revealedrelatively high flow velocity and low resistance signals and indicated aposteriorlydirectedflow ri bt toward the cavernous sinus (notice The direc-tion of the small arrow in the right upper corner) . Thisflow direction is inaccordance with the normal flora direction of the superior ophthalmic vein .

carotid angiography opacified the cavernous sinusslightly, and it drained posteriorly into the inferior petro-sal vein . There was no opacification of the superior oph-thalmic vein . In case 5, angiography revealed numeroussmall abnormal vessels from the right ascending pharyn-geal and the right internal maxillary arteries without aclear visualization of the cavernous sinus itself. In thiscase, the inferior ophthalmic vein drained first to theinferior petrosal sinus and then to the internal jugularvein .

DiscussionAngiographically, CCFs can be classified according to,first, the velocity of the blood flow through the shuntand, second, the anatomical origin of the artery supply-ing the CCFs [3,4] . Most of the CCF cases result fromtrauma, but about 25%-30% of all cases occur sponta-neously [3,4,111 . Using the above criteria, Barrow et al

Table 2 . Results of Angiography and Transcranial Doppler Sonography

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[3) mentioned four types of CCFs . Among these types,their type D includes most of the dural AVM-relatedCCFs. They characteristically have insidious onset, arefed by dural branches of both external and internal ca-rotid arteries, have a low flow, and about 10%-60%have the tendency to resolve without treatment. Sponta-neous CCFs will result in enlargement of the superiorophthalmic vein, accompanied by arterialization and re-versal of its flow away from the cavernous sinus [4,6,9) .

Under normal conditions, superior ophthalmic veinswere difficult to insonate, as shown by the result ofinsonation of the normal eyes in our cases . Dopplersignals recorded at the depth of 45 to 55 mm of thenormal eyes were merely those of the normal ophthalmicarteries . Abnormal doppler signals found in the CCFside of cases 1, 2, and 3, which indicated anteriorlydirected flow, showed changes of flow patterns-the so-called arterialization-of the superior ophthalmic veinscaused by the presence of arteriovenous shunt in thecavernous sinus . Compared to the normal signals of theophthalmic arteries, these abnormal doppler signals ofthe ophthalmic veins had almost twice the mean flowvelocity values and less than half of pulsatility indexvalues. The same observation had also been reported byGomez et al (6) .

Contrary to this "classic" picture, cases 4 and 5showed the presence of posteriorly directed abnormalflow, or the same flow direction as the normal ophthalmicvein (Figures 2B) . This unusual flow direction of theophthalmic vein involved in CCF may be explained withthe following hypothesis: The direct draining vein of

Abbreviations : TCD, transcranial doppler: MFV, mean flow velocity ; Pl. pulsatility index; Rt, right; Lt, left, ICAG, internal carotid arreriography ; ECAG, externalcarotid arteriography.

Opacihcation of the cavernous sinus and its draining veins during angiography (timing and thickness of staining) .Gosling's pulsatility index = peak systolic velocity - end diastolic velocity/time mean velocity .

TCD signalsof normal eye

Abnormal signalsof affected eye

Normal signalsof affected eye

Case Angiography" MFV, cm/s PI° Direction MFV, cm/s Pt" Direction MFV, cm/s PP Direction

I Rt cavernous sinus and ophthalmic veinwere seen on midarterial phase .

16 1 .0 Anterior 42 0.41 Anterior Overlapped by abnormalsignal

2 Rt cavernous sinus was seen on earlyarterial phase, but superior ophthalmicvein was weakly stained later .

16 1 .9 Anterior 70 0.39 Anterior Overlapped by abnormalsignal

3 Is cavernous sinus, ophthalmic vein, andinferior petrosal vein were stronglystained at early arterial phase .

32 1 .2 Anterior 20 0.89 Anterior 26 1.15 Anterior

4 Rr cavernous sinus and superiorophthalmic vein were weakly stainedat late arterial phase of ICAG, butECAG didn't opacify any ophthalmicvein .

30 1 .3 Anterior 0.53 Posterior 28 1 .3 Anterior

5 Rt inferior ophthalmic vein and inferiorpetrosal vein were weakly stained atmidarterial phase of ECAG .

24 1 .2 Anterior 36 0.89 Posterior 26 1 .113 Anterior

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Figure 3 : Case 3 . (A) CT scan (lam) showed the enlarged left superior ophthalmic vein, while angiography revealed the presence of a large shunt fromdural branches of the left internal carotid artery to the left cavernous sinus (open arrow) . which then drained anteriorly to the ipsilateral superiorophthalmic vein (arrow and posteriorly to the inferior petrosal sinus (arrowhead) . Note the opacification of the ptetygopalatine plexus (double arrows) .(B) Insonation of the right (normal) eye showed only doppler signals of the right ophthalmic artery !right) . In the left eye, besides signals of the left ophthalmicartery (lt), a little change of the insonation angle disclosed signals with relatively low resistance directed away from the cavernous sinus, presumed to bethe signals of the left superior ophthalmic vein (middle) .

TCD in Carotid-Cavernous Fistulas

a CCF, such as the ophthalmic vein, will gradually bearterialized [4,6,9] . It is possible that this pressure-related physical change of the venous wall will providenegative feedback for the shunt itself, especially the verylow flow type. This consideration might be related to thefact that some low-flow CCFs tend to resolve spontane-ously, without treatment or after repeated manual com-

pression of the carotid artery and internal jugular vein

in the neck . Transarterial injection of contrast material,especially during selective carotid angiography, gives anadditional flow pressure temporarily as noted by Greitzand Tornell [7] . This additional pressure changed thelocal hemodynamics temporarily and, as a consequence,resulted in opacification of an otherwise "balanced"shunt. Cases 4 and 5 might represent some of the low-flow, dural AVM-related carotid-cavernous fistulacases with arrested or balanced arteriovenous shunts .

The present clinical presentations of cases 4 and 5 were

very mild and were far better than the initial signs andsymptoms as described by the patients . On angiography,

the ophthalmic veins and/or the cavernous sinus wereweakly opacified during the mid to late arterial phase ofboth of these cases . Angiography with contrast materialinjected transvenously or at a more proximal arterialtrunk would be agood method of obtaining a real pictureof the very low flow arteriovenous shunt without givingany additional pressure to the shunt itself.

Case 3 showed an intense opacification of the cavern-ous sinus and all its draining veins in the early arterialphase on angiography (Figure 2 A) . Doppler signals ofthe ophthalmic vein, however, showed a relatively lowflow velocity (Table 2) . This is related to the principle

that transcranial doppler measures flow velocity, not flowvolume, so it will be difficult to relate transcranial dopp-ler results to the volume of the shunted blood .

From this observation, it seemed that transcranialdoppler has the ability to record changes of the flowvelocity, the vessel's resistance, and direction of flow inthe ophthalmic vein in patients with CCF, and it is the

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only noninvasive means to evaluate hemodynamic

changes in CCF .

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