the diagnosis and prognosis of atypical carotid-cavernous fistula (red-eyed shunt syndrome)

THE DIAGNOSIS AND PROGNOSIS OF ATYPICAL CAROTID-CAVERNOUS FISTULA (RED-EYED SHUNT SYNDROME)

CHARLES D. PHELPS, M.D., H. STANLEY THOMPSON, M.D., AND KARL C. OSSOINIG, M.D.

Iowa City, Iowa

Nineteen patients who complained of red eyes had the characteristic clinical signs of an atypical carotid-cavernous fistula. Episcleral veins were dilated, intraocular pressure and episcleral venous présure were high, and blood filled Schlemm's canal during gonioscopy. Most of the patients had mild exophthalmos, but in none was the exophthalmos obviously pulsatile, and in only two patients could a bruit be heard. Orbital echography disclosed either a dilated superior ophthalmic vein or congestion of the orbital soft tissues. Selective carotid angiography, done in seven patients, disclosed the fistula to be a dural-cavernous fistula.

The only serious complication of the fistulas was open-angle glaucoma resulting from the high episcleral venous pressure. None of the fistulas was treated surgically, but six closed spontaneously and three closed soon after carotid angiography.

The dramatic clinical signs of a typical large carotid-cavernous fistula form a classic and easily recognized neuro-ophthalmologic syndrome.110 More often than not, the patient is a young man who soon after a severe head injury develops a bruit, pulsating exophthalmos, conjuncti-val Chemosis, engorgement of epibulbar veins, motility restriction, and evidence of ocular ischemia. This constellation of signs points unmistakably to the diagno-sis of a large carotid-cavernous fistula.

In other patients, however, the clinical manifestations of carotid-cavernous fistu-la are much less spectacular and the diag-nosis is less obvious.11'14 These patients, often middle-aged to elderly women,

Accepted for publication Dec. 29, 1981. From the Department of Ophthalmology, Univer-

sity of Iowa Hospitals and Clinics, Iowa City, Iowa. Reprint requests toC. S. O'Brien Library, Depart-

ment of Ophthalmology, University of Iowa Hospi-tals, Iowa City, IA 52242.

usually lack a history of trauma. They have no bruit, their proptosis is minimal, and their eyes do not pulsate. Prominent congestion of episcleral and conjunctival veins is usually the patient's chief con-cern and the initial diagnostic clue.

Although physicians have known for years that some patients with carotid-cavernous fistula are affected less severe-ly than others, the anatomic basis for the different degrees of severity did not be-come clear until the past decade when sophisticated modern angiographic tech-niques became available. Methods such as selective internal and external carotid angiography, magnification, stereopsis, and subtraction have disclosed that a pa-tient with the classic severe syndrome usually has a large fistula between the internal carotid artery and the surround-ing cavernous sinus venous plexus. A patient with the mild or atypical syn-drome, however, almost always has a dural-cavernous fistula.11'1315"21 This is a

©AMERICAN JOURNAL OF OPHTHALMOLOGY 93:423-436, 1982 423

424 AMERICAN JOURNAL OF OPHTHALMOLOGY APRIL, 1982

fistula fed by small meningeal branches of either the intracavernous internal carotid artery11,22"26 or the external carotid ar-t e r y 11,20,25-37 j t j s 0 f t e n fed by more than

one vessel, because anastomoses be-tween the various dural arteries are com-mon and extensive.38"40 The fistula may empty directly into the cavernous sinus or, less frequently, into an adjacent dural vein that connects with the cavernous sinus. In general, a dural-cavernous fis-tula is small, and the arteriovenous shunting of blood is "low flow and low pressure" compared with the "high flow and high pressure" shunting typical of true internal carotid-cavern-ous fistulas.

Since most patients with low-flow fistu-las visit an ophthalmologist because an eye appears red, we call the condition the "red-eyed shunt syndrome." The patients usually consult an ophthalmologist first. The ophthalmologist may be unfamiliar with the condition because it has only recently been described in published re-ports and has received little attention in standard textbooks. Thus, the diagnosis is frequently missed. The patient is mis-takenly thought to have conjunctivi-tis, thyroid ophthalmopathy, scleritis, or orbital pseudotumor. Ineffective and potentially deleterious treatment with antibiotics or corticosteroids may be pre-scribed.

Correct diagnosis is important, not only to avoid unnecessary treatment and diagnostic studies, but also because low-flow fistulas cause potentially serious sec-ondary open-angle glaucoma. Intraocular pressure is increased in nearly every pa-tient, and in some the glaucoma is severe enough to cause blindness. Prompt rec-ognition and appropriate treatment may prevent glaucomatous loss of vision.

We describe herein the clinical findings and course of 19 patients who had low-flow fistulas. Three points must be em-phasized: (1) The clinical signs and symp-

toms, although less florid than those of high-flow fistulas, are sufficiently charac-teristic that the condition should at least be suspected by the clinician. (2) Orbital echography and measurement of epi-scleral venous pressure, two noninvasive ancillary tests, are particularly helpful in confirming the diagnosis. (3) With the exception of secondary glaucoma, the condition is usually benign. We believe that this good prognosis must be kept in mind when potentially hazardous diag-nostic tests or surgical intervention are being considered.

SUBJECTS AND METHODS

From January 1972 through December 1979 we diagnosed an atypical carotid-cavernous fistula or "red-eyed shunt" in 19 patients. Each patient was examined by at least two of us. To put the frequency of the condition into perspective, during the same period we examined six other patients who had the typical signs of the classic internal carotid-cavernous fistula syndrome. Because there is no distinct boundary separating the atypical from the typical syndrome, in some patients our clinical classification was arbitrary. In general, we included patients in the study and classified them as having the atypical syndrome if they had mild clini-cal manifestations and if a red eye was the sole or major complaint. We classified patients as having the classic syndrome and excluded them if they had an acute onset with severe proptosis, conjunctival Chemosis, ocular pulsations, and immedi-ate loss of vision or other signs of severe ocular ischemia.

The diagnosis of fistula was confirmed by carotid angiography in seven patients. In the other 12 patients the diagnosis was made on clinical grounds and, because surgical repair of the fistula was not con-templated, angiography was not per-formed.

If information regarding the patient's

VOL. 93, NO. 4 ATYPICAL CABOTID-CAVERNOUS FISTULA 425

history or subsequent course was incom-plete, the patient was either questioned by telephone or was brought back for re-examination. We obtained the follow-ing data for each patient: chief complaint, onset of symptoms, antecedent trauma or illnesses (including diabetes, high blood pressure, other cardiovascular disease, and family history), and symptoms (red eye, noise in head, headache, ocu-lar pain, proptosis, and diplopia). Oph-thalmologic examination included visual acuity and perimetric testing, motility assessment, slit-lamp examination, oph-thalmoscopy, applanation tonometry, aus-cultation of the head for a bruit, goni-oscopy (16 patients), orbital echography (16 patients), measurement of episcleral venous pressure (15 patients), Hertel ex-ophthalmometry (14 patients), and ton-ography (eight patients). Twelve patients were also examined by a neurologist. The other seven patients had no neurologic symptoms or obvious deficit.

We measured episcleral venous pres-sure with a membrane-capped pressure chamber connected to a manometer.41

Echographic examination included A-scan, B-scan, and Doppler evaluations (standardized echography42).

Of the 19 patients, five were men and 14 were women. The age at onset of symptoms ranged from 16 to 77 years (Table 1). Twelve patients were over 55 years of age. Four of the seven youngest patients had a history of trauma (Table 2), but none of the 12 oldest patients had

TABLE 1

AGE AT ONSET OF LOW-FLOW CAROTID-CAVERNOUS FISTULA

Age (yrs) Men Women

Less than 40 2 3 40 to 49 1 1 50 to 59 0 3 60 to 69 2 2 70 to 79 0 5

TABLE 2

CLINICAL HISTORIES OF PATIENTS WITH LOW-FLOW CAROTID-CAVERNOUS FISTULAS

No. of History Patients

Head trauma 4 Termination of pregnancy 1 Diabetes 3 Cardiovascular disease 6* None 7

"Two patients had diabetes.

such a history. One patient had been struck on the forehead by a load of corn sliding down a chute. That evening his eye became red. The other three patients had had head injuries one to three years before the onset of the red eye. Only one was injured severely enough to lose con-sciousness.

One 37-year-old woman developed symptoms after an abortion. Six patients had major vascular diseases; three had carotid stenosis and three had coronary artery disease. Three patients were dia-betic.

The complaint that caused the patient to seek medical care was redness of the eye in 16 cases. The other three patients also had red eyes but were chiefly con-cerned about headache (two cases) and ocular pain (one case). In five patients both eyes were red, in eight the right eye was red, and in six the left eye was red. The redness usually began gradually and increased during a two- to three-week period, so that the patient was rarely able to date its onset precisely. There was no associated mattering, photophobia, or blurring of vision.

Although the red eye was usually the complaint that led to the diagnosis, three patients had been examined by physi-cians for neurologic problems several months before their eyes became red. A 58-year-old woman had had a left hemi-paresis that had partially resolved; six


months later her left eye became red and 11 months later her right eye became red. A 60-year-old man had had left-sided headaches and a left superior oblique muscle palsy that had slowly resolved; five months later his left eye became red. A 59-year-old diabetic woman had had a right third nerve palsy that had slowly improved; six months later both of her eyes became red.

Concomitant with the onset of the ocu-lar redness, two patients also noted a noise in their head, 12 patients observed that the involved eye bulged forward, four complained of headache, and one complained of ocular pain, and seven (including the two patients with resolving cranial nerve palsies) complained of di-plopia (Table 3).

RESULTS

Extraocular signs—We listened for a bruit in all patients but were able to hear one in only two patients (Table 3). Exoph-thalmos was present in 13 patients and absent in six. Hertel exophthalmometer

TABLE 3

SYMPTOMS AND SIGNS OF LOW-FLOW CAROTID-CAVERNOUS FISTULAS

No. of Symptoms and Signs Patients

Red eye 19 Noise in head 2 Proptosis 12 Pain 5 Diplopia 8 Dilated episcleral vessels 19

Bilateral 5 Right eye 8 Left eye 6

Bruit 2 Exophthalmos 13 Motility limitation 7 Increased intraocular pressure 19 Visual acuity

6/7.5 (20/25) or better 16* 6/15 (20/50) or worse 2* Hand motions 1

'Includes four patients with bilateral fistulas. * Includes one patient with bilateral fistulas.

readings ranged from 16 to 25 mm (mean, 19.6 ± 3.0 mm). The difference between the two eyes (excluding the six patients who had no differences) ranged from 1 to 11 mm (mean, 5.2 ± 2.7 mm). No ocular pulsations were observed. Seven patients had mild to moderate restriction of ocular motility, but in only three patients was there a definite cranial nerve palsy. In the others it was difficult to distinguish paresis from restriction caused by orbital congestion.

Visual acuity—The fistula decreased the visual acuity of only one patient. This was a woman who had had symptoms for nine years and who could see only hand movements with her involved eye be-cause of severe glaucomatous optic nerve damage. Two other patients (three in-volved eyes) had moderate decreases in visual acuity (6/12 to 6/18 [20/40 to 20/60]), but in each the blurring was the result of cataracts that had been present for more than a year before the eyes became red. The remaining 16 patients (20 involved eyes) had normal visual acui-ties.

Intraocular pressure—Intraocular pressure was at least slightly increased in all of the red eyes (Table 4). Usually it was between 20 and 35 mm Hg. In one excep-tional patient with bilateral involvement, the intraocular pressure was 57 mm Hg in one eye but only 27 mm Hg in the other. One patient with a unilateral red eye had a slightly increased intraocular pres-sure in the fellow eye because of ex-foliation syndrome. In the remaining patients with unilateral involvement, the intraocular pressures in the fellow eyes were normal.

Gonioscopy—Sixteen of the 19 patients (including three with bilateral involve-ment) underwent gonioscopy. The proce-dure often provided an important indica-tion that the episcleral venous pressure was high. The anterior chamber angles were open, appeared to be structurally normal, and resembled the angles in the

VOL. 93, NO. 4 ATYPICAL CAROTID-CAVERNOUS FISTULA 427

TABLE 4

SIGNS OF GLAUCOMA IN PATIENTS WITH LOW-FLOW CAROTID-CAVERNOUS FISTULAS

Signs Involved Eye Uninvolved Eye

Intraocular pressure (mm Hg) No. tested 24 14 Range 20 to 57 10 to 23 Mean ± S.D. 27.1 ± 7.4 14.5 ± 3.9

Blood reflux in Schlemm's canal 17 of 19 Oof 13 Episcleral venous pressure (mm Hg)

No. tested 19 13 Range 9.5 to 26 6 to 12 Mean ± S.D. 18.4 ± 4.2 9.2 ± 2.2

C value (uJ/mm Hg/min) No. tested 10 6 Range 0.05 to 0.34 0.18 to 0.54 Mean ± S.D. 0.213 ± 0.087 0.340 ± 0.120

Glaucomatous cupping 6 of 24 l o f 14 Glaucomatous visual field defect 4 of 24 l o f 14

fellow uninvolved eyes. However, in 18 of the 19 involved eyes, it was easy to make blood reflux into Schlemm's canal, whereas in the fellow eyes, despite a much lower intraocular pressure, blood reflux either could not be induced or was induced with difficulty. We sometimes failed to observe blood reflux when the involved eye was examined with a lens that lacked a flange, such as the Zeiss gonioprism. In these eyes blood reflux occurred only when it was induced by pressing the flange of a goniolens, such as the Allen-Thorpe lens, against the epi-scleral veins. In other instances, howev-er, blood reflux appeared in one or more quadrants of the angle even when it was not induced by compression of the epi-scleral veins.

Episcleral venous pressure—In all pa-tients the episcleral veins were markedly congested and prominent. In normal eyes, the episcleral arteries are larger in caliber and more tortuous than the veins. In affected eyes, the opposite was true. We measured the episcleral venous pres-sure in 15 patients (19 involved eyes). In normal eyes, the episcleral venous pres-sure, measured with our instrument, av-erages 9.0 ± 1.5 mm Hg.41 It exceeded 12 mm Hg in all but one of the involved

eyes (Table 4). The sole exception was a patient who had had a unilateral fistula for six years; in this case the episcleral venous pressure was 9.5 mm Hg in the involved eye and 6 mm Hg in the fellow eye.

As the fistulas became chronic, they evolved in an interesting way. During the first few months, many episcleral veins were engorged (Fig. 1, left). The epi-scleral venous pressure was increased at the same level wherever along the vessel the measurement was made and did not vary greatly from vessel to vessel. With time, the appearance of the eyes changed (Fig. 1, right). Fewer episcleral vessels were dilated, although a number of ves-sels remained prominent near the cor-neoscleral limbus. The episcleral venous pressure remained high near the corneo-scleral limbus, but further away from the corneoscleral limbus it decreased in some, but not all, of the vessels. Some of the vessels that showed this decrease in pressure could be moved over the under-lying sclera, although they were obvious-ly subconjunctival. These were probably veins in Tenon's capsule that anasto-mosed near the corneoscleral limbus with the episcleral veins and were carrying arterialized blood into the low-pressure


Fig. 1 (Phelps, Thompson, and Ossoinig). Left eye of 60-year-old woman soon after the onset of a dural-cavernous fistula (left) and several years later (right). Initially the episcleral and conjunctival veins are all prominent but the dilation is later limited to a wreath of veins near the corneoscleral limbus and a few large collateral veins in Tenon's capsule and the conjunctiva.

Fig. 2 (Phelps, Thompson, and Ossoinig). Standardized A-scan echograms of the dilated and arterialized superior ophthalmic vein in a high-flow arteriovenous fistula. These transocular echograms were obtained with the probe placed behind the corneoscleral limbus at the 6 o'clock position with the sound beam aimed through the globe into the superior orbit and the instrument at the "tissue sensitivity" setting. Left, Normal echogram obtained from the unaffected, healthy orbit of the patient (high, overloaded orbital spikes; superior ophthalmic vein not demonstrated). Right, A large defect within the orbital pattern represents the cross-section of the dilated superior ophthalmic vein in the affected orbit. I, initial spike indicating the

Erobe-eye interface at the 6 o'clock position behind the corneoscleral limbus; V, clear vitreous (intact aseline); F, fundus signals (retinal, choroidal, and scleral surfaces); A, arterialized, dilated superior

ophthalmic vein producing a sharply outlined defect in the orbital pattern (the low blurred spikes represent fast moving blood within the vein); arrows, inferior (left) and superior (right) walls of the dilated vein; O, normal orbital tissues. The orbital spikes behind the superior ophthalmic vein (on the right end of the echogram at right) are lower and less regular than those in the normal orbital echogram at left because of the oblique interception of the sound beam by more posterior sections of the superior ophthalmic vein.


venous channels that drain into the facial vein.

Tonography—We measured outflow fa-cility in eight patients, including two with bilateral involvement (Table 4). The C value was normal (> 0.15 jxl/mm Hg/min) in nine of the ten involved eyes. In one patient who had had signs of a low-flow fistula for 30 years the C value was re-duced to 0.05 |xl/mm Hg/min. The ocular pulse amplitude, depicted on the tono-graphy tracing, was often greater in the affected than the normal eyes, a finding also observed by others.43

Glaucoma—In general, the secondary glaucoma was mild, and optic nerve dam-age did not develop in most patients. In six patients, however, the optic disk cup was larger in the involved eye. These six eyes had a typical glaucomatous visual field defect.

Echography—Sixteen patients under-went orbital echography. This procedure was helpful in ruling out other orbital conditions and, in most patients, dis-closed abnormalities that were either pa-thognomonic for, or characteristic of, carotid-cavernous fistula. In only two pa-tients, neither of whom had proptosis, were the results normal.

High-flow fistulas produce echograms that are pathognomonic for carotid-cavernous fistula (Fig. 2) . 4 2 , 4 4 , 4 6 The stand-ardized A-scan shows a sharply outlined defect that corresponds with the cross-section of the dilated superior ophthalmic vein. The steeply rising and falling sur-face spikes on either side of the defect indicate the vessel wall. Within the de-fect, low spikes show spontaneous, con-tinuous, fast, flickering, vertical motion of limited extent; this motion is produced by the arterialized blood flow within the dilated vein. These blood spikes appear blurred in Figure 2 because of the fast motion. Although these A-scan findings occur not only in high-flow fistulas, but also in orbital arteriovenous malforma-tions, a topographic evaluation with ei-

ther A-scan or B-scan (which provides better documentation) clearly shows that the orbital lesion is a dilated superior ophthalmic vein rather than an orbital arteriovenous malformation (Fig. 3). By simply shifting the A-scan beam or, even better, the B-scan acoustic section across

Fig. 3 (Phelps, Thompson, and Ossoinig). Contact B-scan echograms of a dilated and arterialized superi-or ophthalmic vein in a high-flow arteriovenous fistula using a vertical acoustic section through the globe and orbit (top) and a horizontal acoustic sec-tion that was tilted upwards through the globe and

Xrior orbit (bottom). The probe was placed verti-along the temporal corneoscleral limbus of the

globe (top) and horizontally behind the inferior cor-neoscleral limbus (bottom). Top, A long-section of the optic nerve and a cross-section of the dilated superior ophthalmic vein as it crosses over the nerve. Bottom, A long-section of the superior ophthalmic vein as it meanders from the anteronasal (AN) to the posterotemporal (PT) superior orbit (toward superior orbital fissure). V, clear vitreous (acoustically empty space); F, fundus signals; A, arterialized, dilated superior ophthalmic vein producing sharply outlined defect in the echograms; ON, optic nerve (long-section).


Fig. 4 (Phelps, Thompson, and Ossoinig). Maximum thickness of the optic nerve and the extraocular muscles in both orbits (measured by the standardized A-scan method) in a patient with right unilateral signs of a low-flow arteriovenous fistula. All the echograms were obtained during a transocular examination so that the first spike on the left corresponds with the probe-eye interface opposite the structure examined, and the baseline indicates normal vitreous. The defects in the orbital A-scan patterns are outlined by steeply rising and falling surface spikes, indicating the maximum thickness cross-section of the optic nerve (N), and the medial rectus (M), lateral rectus (L), superior rectus (S), inferior rectus (I), and superior oblique (O) muscles. Note that all the identified structures, as well as the overall width of the orbital tissues, are wider on the affected right side (left) than on the normal left side (right, on facing page).

the superior orbit, one can easily demon-strate the anteronasal to posterotemporal direction and often meandering course of the dilated superior ophthalmic vein. In addition to these pathognomonic echo-graphic findings, A-scan measurements of the extraocular muscles demonstrate swelling of the adjacent muscles from hyperemia.

Low-flow fistulas, at least those near the lower end of the range of flow, fail to open orbital and facial drainage channels and present a different echographic pic-ture (Fig. 4) . 4 2 A standardized A-scan

shows that all orbital structures, and the extraocular muscles and the sheaths of the optic nerve in particular, are slightly but clearly thickened. This can be ex-plained by venous congestion in the orbit caused by the low-flow fistula. In contrast to the high-flow fistulas, no dilatation or arterialization of the superior ophthalmic vein is present.

We detected a greatly dilated superior ophthalmic vein in six of our patients with red-eyed shunt syndrome, indicating that these patients had greater flow than their clinical signs suggested. In all 14 patients


for whom echographic findings were posi-tive, we detected diffuse swelling of the extraocular muscles and optic nerve sheaths. This hyperemia was found adja-cent to the superior ophthalmic vein in the six patients who had high-flow fistulas whereas it was detected in all the extraoc-ular muscles and affected the entire orbit, including the optic nerve sheaths, in the eight patients who did not show any dilatation of the superior ophthalmic vein. Doppler examination disclosed the reversal of the usual direction of orbital venous blood flow in all patients.

Neurologic deficits—Twelve patients were examined by a neurologist or a neurosurgeon. Two patients had a sixth cranial nerve palsy, one a fourth cranial nerve palsy, and one a mild left hemi-paresis. These latter two were included in the three patients whose neurologic

deficits began several months before any signs of a fistula had developed. Nine patients had normal neurologic findings. The seven patients who did not undergo neurologic examinations had no neuro-logic symptoms or obvious deficits.

Carotid angiography—Carotid angiog-raphy was performed in seven patients and attempted unsuccessfully in an eighth. The other 11 patients did not undergo angiography because of iodine allergy (one patient), patient refusal (one patient), or benign clinical signs (nine patients). A dural cavernous shunt was demonstrated in each of the seven pa-tients who had angiograms. In three pa-tients, a transient neurologic deficit fol-lowed the angiography. In one of these and in two other patients, the fistula closed shortly after angiography; this was shown by a reduction of proptosis, lessen-


ing of redness, and return of intraocular pressure and episcleral venous pressure to normal levels.

Follow-up—None of the fistulas were treated surgically. However, in nine pa-tients the fistula closed between four and 24 months after the onset of symptoms. Closure followed angiography in three patients and was spontaneous in six of the 11 patients who did not undergo angiog-raphy.

The fistulas remained patent in ten patients. These ten, whose symptoms had lasted for six months to 34 years, showed no ill effects other than the secondary glaucoma mentioned earlier. In some pa-tients, spontaneous fluctuations of epi-scleral venous pressure and intraocular pressure suggested that blood flow through the fistula waxes and wanes or that the venous pathways draining the fistula vary from time to time.

The glaucoma responded poorly to all types of pressure-decreasing medication. Presently available glaucoma medica-tions, of course, can only diminish the gap between intraocular pressure and episcleral venous pressure. They cannot decrease the intraocular pressure to less than the episcleral venous pressure.

Three of our patients had undergone filtering operations, all performed else-where, to allow the aqueous to bypass the episcleral veins. Two succeeded; in the third case a filtering bleb was present for a few months but later stopped function-ing. The surgeons had encountered no intraoperative problems, such as the sud-den choroidal effusions observed by Bel-lows and associates.46

DISCUSSION

Terminology and classification—Ca-rotid-cavernous fistula is a general term that refers to any abnormal shunting of arterial blood from a branch of the common carotid artery into the cavernous sinus. Carotid-cavernous fistulas can be

classified in at least three ways. An etio-logic classification differentiates posttrau-matic from spontaneous fistulas. An ana-tomic classification differentiates direct internal carotid-cavernous fistulas from various types of dural-cavernous fistulas. A clinical classification, which depends on the severity of symptoms and signs, differentiates high-flow from low-flow syndromes and also contains intermedi-ate gradations.

Although, as a general rule, low-flow fistulas are spontaneous and originate in dural vessels and high-flow fistulas are traumatic and originate in the internal carotid artery, the three classifications do not always exactly coincide. For instance, some relatively high-flow fistulas origi-nate in meningeal arteries, and some low-flow fistulas are traumatic in origin. Which classification to use depends on one's purpose. An epidemiologist may use the etiologic classification, a neuro-surgeon contemplating surgery may pre-fer a precise anatomic definition, and the ophthalmologist charged with deciding whether or not to embark on potentially hazardous diagnostic tests and therapeu-tic interventions is probably best served by the clinical classification.

The clinical classification, in which carotid-cavernous fistulas are separated into low-flow and high-flow syndromes on the basis of the severity of symptoms and signs, is sometimes arbitrary. In some patients the condition is midway on the spectrum and cannot be classified easily. We found that the clinical assessment and echographic findings were not always in perfect agreement. Patients may have echographic evidence of a dilated superi-or ophthalmic vein and Doppler evidence of high blood flow, resembling the echo-graphic findings in the classic high-flow syndrome, yet be affected only mildly. Most cases, however, can be placed at one end of the clinical spectrum or the other. In these cases this classification


serves several useful purposes. It allows the clinician to predict the anatomic site of the fistulas, to judge the prognosis, and to determine the need for angiography and surgery.

Diagnosis—The diagnosis of low-flow carotid-cavernous fistula can be made clinically and, unless surgical treatment is contemplated, does not require angiog-raphy. The principal ocular signs include dilated and tortuous episcleral veins, a mild to moderate increase in intraocular pressure, and blood in Schlemm's canal. Mild or moderate exophthalmos is com-mon, and motility restriction occurs in some patients. A bruit, the traditional pathognomonic sign of a carotid-cav-ernous fistula, may be difficult or imr

possible to hear. Headache and orbital pain, frequent complaints of patients with high-flow fístulas, are uncommon.

None of our patients with the red-eyed shunt syndrome showed signs of ocular ischemia (keratitis, iritis, rubeosis, iris atrophy, cataract, hypotony, and hemor-rhages of the optic nerve head and reti-na), whereas these signs occur frequently in the high-flow syndrome.47 When pres-ent, they indicate that blood intended for the ophthalmic artery is being diverted instead into the fistula; the low ophthal-mic artery pressure and the high orbital venous pressure combine to slow the ocular blood flow. Apparently the flow of blood through low-flow fistulas is insuffi-cient to embarrass ocular blood flow. Vi-sion, which in the high-flow syndrome is often reduced by the various manifesta-tions of ocular ischemia, is rarely im-paired in low-flow fistulas.

Intraocular pressure—High intraocu-lar pressure, secondary to high episcleral venous pressure, is a common complica-tion of all types of carotid-cavernous fistu-las. The normal direction of blood flow in the episcleral veins, which receive aque-ous humor as it leaves the eye, is posteri-orly through anterior ciliary veins into

the ophthalmic veins. If a fistula is pres-ent, the high pressure in the superior ophthalmic vein is transmitted anteriorly to the episcleral veins. The relationship of intraocular pressure (P0) and episcleral venous pressure (Pe v) is most simply de-scribed in Goldmann's classic formula-tion of aqueous humor dynamics (where F = flow and R = outflow resistance):

P, = F X R + Pe v.

If episcleral venous pressure is high, as it is in patients with carotid-cavernous fis-tulas, intraocular pressure must be even higher for circulation of aqueous to con-tinue.4 8'4 9 It is higher by an amount pro-portional to the rate of aqueous formation and the resistance to outflow.

Intraocular pressure was increased in the affected eyes of all of the patients included in this report, although previous studies have not always found such a high frequency of increased intraocular pressure.3,6 However, these reports de-scribed patients at the high-flow end of the spectrum, many of whom probably had enough ocular ischemia to impair aque-ous humor formation. Also, we have ob-served a few patients with carotid-cavernous fistulas in whom angiography and echography showed involvement of the superior ophthalmic vein but who had no clinical signs of orbital congestion and who had normal (although above average) episcleral and intraocular pressures. These patients may have had larger-than-normal anastomoses between the superior ophthalmic vein and the angular facial vein that allowed a large volume of blood to pass through the orbit without causing much congestion.

Tonography in low-flow fistulas demon-strates a relatively normal outflow facili-ty.4 8 , 4 9 However, the outflow facilities in our patients with unilateral involvement were somewhat lower in affected than in fellow eyes. The reasons for this are un-


clear, but may involve secondary changes in outflow resistance, pseudofacility, or ocular rigidity.

Episcleral venous pressure—Episcleral venous pressure can be measured easily with a simple pressure-chamber device.4 1

This measurement is helpful in distin-guishing eyes with high episcleral venous pressure from eyes with normal episcler-al venous pressure and episcleral vasodi-lation caused by medications, inflamma-tion, exposure, thyroid ophthalmopathy, or some other cause. The causes of high episcleral venous pressure are few. Sturge-Weber syndrome50 and superior vena caval obstruction,51,52 both easily identified simply by examining the pa-tient, are two of the best documented causes. Rare causes include orbital arte-riovenous fistula and orbital vein throm-bosis.5 3 Some cases in which the cause was unknown54,55 may have been the re-sult of unrecognized low-flow carotid-cavernous fistulas.

Orbital echography—Orbital echog-raphy easily and quickly provides conclu-sive proof that a fistula is present, and helps to distinguish high-flow from low-flow fistulas. It also distinguishes both types of fistulas from other causes of proptosis and orbital congestion such as pseudotumor and Graves' disease.56

The two major echographic signs of fistulas are a dilated and arterialized su-perior ophthalmic vein and congestion of the orbital tissues. Dilatation of the supe-rior ophthalmic vein is a characteristic echographic finding in patients who have clinical signs of a high-flow fistula and is always associated with Doppler evidence that blood is flowing from posterior to anterior. When found in patients whose conditions are toward the low-flow end of the clinical spectrum, it shows that the blood flow is somewhat higher than sus-pected. Diffuse congestion of orbital soft tissues, although present in high-flow fis-tulas, is more pronounced and typical in low-flow fistulas.

Standardized echography is particular-ly helpful in those high-flow fistulas that do not produce the classic neuro-ophthalmologic syndrome and in those fistulas that clinically appear to be low-flow but which echography shows have sufficient flow to produce dilatation of the superior ophthalmic vein and drainage through the orbital and facial veins. In these patients, the pathognomonic pat-tern disclosed by standardized A-scan can usually be recognized within the first 30 seconds of the echographic examination. Standardized echography is also helpful in confirming low-flow fistulas by detect-ing diffuse orbital hyperemia with thick-ening of the extraocular muscles and the optic nerve sheaths, as well as orbital fat tissues. Even in bilateral cases of such hyperemia, echography is helpful in dis-tinguishing the diffuse, mild thickening that affects all extraocular muscles to an equal degree from other bilateral condi-tions such as Graves' disease, lympho-mas, or pseudotumor. Graves' disease, for instance, causes a thickening of extra-ocular muscles that varies from muscle to muscle, and the thickened muscles have a heterogeneous high-reflective internal structure.

Prognosis and treatment—The progno-sis for eventual recovery in our patients was good. Nearly one half of the fistulas closed without surgical intervention. In the other patients, the condition has been compatible with a normal life. The pa-tients are not bothered by an intolerable bruit, as is often the case in high-flow fistulas. Except for secondary glaucoma, which has been a serious problem in only a few patients, there have been no vision-threatening complications. Cerebral is-chemia and life-threatening intracranial or nasal hemorrhages, which are occa-sional problems in patients with high-flow fistulas, have not occurred in our patients with the low-flow syndrome. Thus, there appears to be no pressing need for surgical treatment of low-flow

VOL. 93 , NO. 4 ATYPICAL CAROTID-CAVERNOUS FISTULA 4 3 5

fístulas, especially if the potential compli-cations of fistula surgery5,47,57"69 and its not infrequent failures are considered.

Angiography may be indicated even if surgery is not contemplated. It confirms the diagnosis and pinpoints the site of the fistula, possibly identifying an unusual fistula that can be repaired easily. Occa-sionally, angiography seems to cure the fistula.11,60 The signs and symptoms of the fistula may remit permanently soon after the angiogram. The mechanism of closure is unknown.

However, angiography is not without risk. A transient neurologic deficit follow-ing angiography is common in patients with cerebral vascular disease and oc-curred in several of our patients. A per-manent deficit occurs occasionally.61,62

Angiography requires hospitalization and is expensive and spontaneous cures occur in some patients who do not undergo angiography. Thus, whether or not to perform angiography depends on the se-verity of symptoms and the attitude of the patient toward his disease.

REFERENCES

1. Locke, C. E., Jr.: Internal carotid arteriove-nous aneurysm or pulsating exophthalmos. Ann. Surg. 80:1, 1924.

2. Dandy, W. E.: Carotid-cavernous aneurysms (pulsating exophthalmos). Zentralbl. Neurochir. 2:77, 1937.

3. Sugar, H. S., and Meyer, S. J . : Pulsating ex-ophthalmos. Arch. Ophthalmol. 23:1288, 1940.

4. Martin, J. D., and Mabon, R. F.: Pulsating exophthalmos. Review of all reported cases. J.A.M.A. 121:330, 1943.

5. Walker, A. E., and Allègre, E. E.: Carotid-cavernous fistulas. Surgery 39:411, 1956.

6. Henderson, J. W., and Schneider, R. C : The ocular findings in carotid-cavernous fistula in a series of 17 cases. Trans. Am. Ophthalmol. Soc. 56:123, 1958.

7. Hamby, W. R.: Carotid-Cavemous Fistula. Springfield, Charles C Thomas, 1966, pp. 35-62.

8. Arseni, C , Ghitescu, M., Cristescu, A., Mihai-la, C , and Dragutoiu, E.: Traumatic carotido-cavernous fistulas. Psychiatr. Neurol. Neurochir. 73:237, 1970.

9. Madsen, P. H.: Carotid-cavernous fistulae. A study of 18 cases. Acta Ophthalmol. 48:731, 1970.

10. Parkinson, D.: Carotid cavernous fistulae. In Vinken, P. J . , and Bruyn, G. W. (eds.): Handbook of

Clinical Neurology. Amsterdam, North Holland Pub-lishing Co., 1972, vol. 12, pp. 267-288.

11. Newton, T. H., and Hoyt, W. F.: Dural arte-riovenous shunts in the region of the cavernous sinus. Neuroradiology 1:71, 1970.

12. Taniguchi, R. M., Goree, J. A., and Odom, G. L.: Spontaneous carotid-cavernous shunts pre-senting diagnostic problems. J. Neurosurg. 35:384, 1971.

13. Clay, C , Ramée, A., and Vignaud, J. : Fistules carotido-cavemeuses cliniquement atypiques. Neu-rochirurgia 19:49, 1973.

14. DeKeizer, R. J. W.: Spontaneous carotico-cavernous fistulas. The importance of the typical limbal vascular loops for the diagnosis, the recogni-tion of glaucoma, and the uses of conservative thera-py in this condition. Doc. Ophthalmol. 46:403,1979.

15. Aminoff, M. J . : Vascular anomalies in the in-tracranial dura mater. Brain 96:601, 1973.

16. Siu, K., and Henderson, K.: Dural arteriove-nous shunts in the region of the cavernous sinus. Aust. N.Z. J. Surg. 44:264, 1974.

17. Clay, C , Vignaud, J . , Lasjaunias, P., and Moret, J . : Problèmes actuels posés par les fistules artério-veineuses carotido-cavemeuses. Arch. Oph-talmol. 35:639, 1975.

18. Klepach, G. L. , Wray, S. H., Roberson, G. H., and Dallow, R. L.: Bilateral dural arteriove-nous malformations simulating dysthyroid ophthal-mopathy. Ann. Ophthalmol. 10:1519, 1978.

19. Dilenge, £>.: Angiography of spontaneous carotido-cavernous communications. Mod. Probl. Ophthalmol. 14:110, 1975.

20. Costin, J. A., Weinstein, M. A., Berlin, A. J . , Hardy, R. W., and Gutman, F. A.: Dural arterio-venous malformations involving the cavernous sinus. À case report. Br. J. Ophthalmol. 62:478, 1978.

21. Slusher, M. M., Lennington, B. R., Weaver, R. G., and Davis, C. H.: Ophthalmic findings in dural arteriovenous shunts. Ophthalmology 86:720, 1979.

22. Djindjian, R., Picard, L. , and Manelfe, C.: Fistules artérioveineuses carotide inteme-sinus cav-erneux. Aspects radio-anatomiques actuels et per-spectives thérapeutiques. Neurochirurgia 19:75, 1973.

23. Katsiotis, P., Kiriakopoulous, C , and Taptas, J. : Carotid-cavernous sinus fistulae and dural arterio-venous shunts. Vase. Surg. 8:60, 1974.

24. Obrador, S., Gomez-Bueno, J . , and Silvela, J . : Spontaneous carotid-cavernous fistula produced by ruptured aneurysm of the meningohypophyseal branch of the internal carotid artery. J. Neurosurg. 40:539, 1974.

25. Lobato, R. D., Escudero, L. , and Lamas, E.: Bilateral dural arteriovenous fistula in the region of the cavernous sinus. Neuroradiology 15:39, 1978.

26. Hayes, G. J . : External carotid-cavernous sinus fistulas. J. Neurosurg. 20:692, 1963.

27. Takekawa, S. D., and Holman, C. B.: Roent-genographic diagnosis of anomalous communication between the external carotid artery and intracranial veins. Am. J. Roentgenol. Radium Ther. Nucl. Med. 95:822, 1965.

28. Castaigne, P., Laplane, D., Djindjian, R.,


Bories, J . , and Augustin, P.: Communication artério-veineuse spontanée entre la carotide externe et le sinus caverneux. Rev. Neurol. 114:5, 1966.

29. Mingrino, S., and Moro, F.: Fistula between the external carotid artery and cavernous sinus. Case report. J. Neurosurg. 27:157, 1967.

30. Clemens, F. , and Lodin, H.: Non-traumatic external carotid-cavernous sinus fistula. Clin. Radiol. 19:201, 1968.

31. Schlezinger, N. S., and Schatz, N. J . : Exter-nal carotid cavernous fistula. Trans. Am. Neurol. Assoc. 98:159, 1973.

32. Djindjian, R., Manelfe, C , and Picard, L.: Fistules artérioveineuses carotide externe-sinus cav-erneux. Etude angiographique à propos de 6 obser-vations et revue de la littérature. Neurochirurgia 19:91, 1973.

33. Edwards, S., and Connolly, S.: Cavernous sinus syndrome produced by communications be-tween external carotid artery and cavernous sinus. J. Neurosurg. 46:92, 1977.

34. Pradat, P., Piganiol, G., Navarro-Artiles, C , and David, M.: Revascularisation d'un anévrysme carotido-caverneux post-traumatique par l'intemédi-aire de l'artèrie méningée moyenne. Neurochirurgia 14:875, 1968.

35. Mahalley, M. S., Jr., and Boone, S. C : Exter-nal carotid-cave mous fistula treated by arterial em-bolization. J. Neurosurg. 40:110, 1974.

36. Newton, T. H., and Hoyt, W. F.: Spontane-ous arteriovenous fistula between dural branches of the internal maxillary artery and the posterior cav-ernous sinus. Radiology 91:1147, 1968.

37. Rosenbaum, A. E. , and Schechter, M. M.: External carotid-cavernous fistulae. Acta Radiol. 9:440, 1969.

38. Parkinson, D. : Collateral circulation of cavern-ous carotid artery. Anatomy. Can. J. Surg. 7:251, 1964.

39. Margolis, M. T., and Newton, T. H.: Collat-eral pathways between the cavernous portion of the internal carotid and external carotid arteries. Radiol-ogy 93:834, 1969.

40. Houser, O. W., Baker, H. L., Jr. , Rhoton, A. L., Jr. , and Okazaki, H.: Intracranial dural arte-riovenous malformations. Radiology 105:55, 1972.

41. Phelps, C. D., and Armaly, M. F.: Measure-ment of episcleral venous pressure. Am. J. Ophthal-mol. 85:35, 1978.

42. Ossoinig, K. C : Standardized echography. Basic principles, clinical applications and results. Int. Ophthalmol. Clin. 19:127, 1979.

43. Calin, M. A., and Harris, L. : The ocular pulse in carotid-cavernous sinus fistula. Am. J. Ophthal-mol. 61:1472, 1966.

44. Valencak, E. , and Ossoinig, K. C. : Les fistules artérioveineuses de l'orbite aux échogrammes A et B. Neurochirurgia 14:951, 1968.

45. Ossoinig, K. C. : A-scan echography and orbit-al disease. Mod. Probl. Ophthalmol. 14:203, 1975.

46. Bellows, A. R., Chylack, L. T., Jr., Epstein,

D. L., and Hutchinson, B. T.: Choroidal effu-sion during glaucoma surgery in patients with prom-inent episcleral vessels. Arch. Ophthalmol. 97:493, 1979.

47. Sanders, M. D., and Hoyt, W. F.: Hypoxic ocular sequelae of carotid-cavernous fistulae. Study of the causes of visual failure before and after neuro-surgical treatment in a series of 25 cases. Br. J. Ophthalmol. 53:82, 1969.

48. Weekers, R., and Delmarcelle, Y.: Pathogene-sis of intraocular hypertension in cases of arteriove-nous aneurysm. Arch. Ophthalmol. 48:338, 1952.

49. Nordmann, J . , Lobstein, A., Gerhard, J. P., and Levy, J. P. : A propos de 14 cas de glaucome par hypertension veineuse d'origine extraoculaire. Oph-thalmologica 142(suppl.):501, 1961.

50. Phelps, C. D.: The pathogenesis of glaucoma in Sturge-Weber syndrome. Trans. Am. Acad. Oph-thalmol. 85:276, 1978.

51. Bedrossian, E. H. : Increased intraocular pres-sure secondary to mediastinal syndrome. Arch. Oph-thalmol. 47:641, 1952.

52. Alfano, J. E.: Glaucoma following ligation of the superior vena cava. Am. J. Ophthalmol. 60:412, 1967.

53. Bietti, G. B., and Vanni, V.: Glaucoma secon-daire à une obstruction veineuse extra-oculaire. Oph-thalmologica 142:227, 1961.

54. Bigger, J. F.: Glaucoma associated with ele-vated episcleral venous pressure. South. Med. J. 68:1444, 1975.

55. Radius, R. L. , and Maumenee, A. E.: Dilated episcleral vessels and open-angle glaucoma. Am. J. Ophthalmol. 86:31, 1978.

56. Bettelheim, H., and Till, P.: Diagnosis of orbital vascular disorders by ophthalmodynamogra-phy and echo-orbitography. Mod. Probl. Ophthal-mol. 14:299, 1975.

57. Renpenning, H. J . , and Wacaser, L. E.: Ipsi-lateral blindness after common carotid ligation for carotid-cavernous fistula. Arch. Ophthalmol. 69:186, 1963.

58. Perret, G., and Nishioka, H.: Report on the cooperative study of intracranial aneurysms and sub-arachnoid hemorrhage. VI. Arteriovenous malforma-tions. J. Neurosurg. 25:467, 1966.

59. Stem, W. E. , Brown, W. J . , and Alksne, J. F.: The surgical challenge of carotid-cavernous fistula. The critical role of intracranial circulatory dynamics. J. Neurosurg. 27:298, 1967.

60. Voigt, K., Sauer, M., and Dichgans, J . : Spon-taneous occlusion of a bilateral caroticocavemous fistula studied by serial angiography. Neuroradiology 2:207, 1971.

61. Taveras, J. M., and Wood, E. H.: Diagnostic Neuroradiology, 2nd ed. Baltimore, Wilhams and Wilkins, 1976, pp. 567-575.

62. Faught, E. , Trader, S. D., and Hanna, G. R.: Cerebral complications of angiography for transient ischemia and stroke. Prediction of risk. Neurology 29:4, 1979.

the diagnosis and prognosis of atypical carotid-cavernous fistula (red-eyed shunt syndrome)

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