Historical Considerations

C O N T E N T S

2.1Arteriovenous Fistula and Pulsating Exophthalmos 3

2.2Angiography 6

2.3Therapeutic Measures 9

2.4Embolization 10

References 11

2.1

Arteriovenous Fistula

and Pulsating Exophthalmos

William Hunter in 1757, is credited with recognizing an arteriovenous aneurysm as direct communication between the artery and vein, while previous observers having interpreted the lesion as a simple aneurysm (Hunter 1762). He studied two patients in whose arms the vessels had been injured by phlebotomy, an operation extensively practiced at that time not only by physicians but also charlatans and barbers. His first accurate appraisal of an arteriovenous communication, described not only the bruit and the palpable thrill at the site of communication but also the marked dilatation and tortuosity of the artery at the site of the fistula:

“In a former paper upon aneurysm, I took notice of a species of that complaint, which, so far as I know, had not been mentioned by any other author; where there is an anstomosis or immediate connection between the artery and the vein at the part where the patient let blood in consequence of the artery being wounded through the vein; so that blood passes immediately from the trunk of the artery into the trunk of the vein and so back into the heart. It will differ in its symptoms from the spurious aneurysm principally thus. The vein will be dilated or become vari-

cose and it will have a pulsatile jarring motion on account of the stream from the artery. It will make a hissing noise, which will be found to correspond with the pulse for the same reason. The blood of the tumor will be altogether or almost entirely fluid because of its constant motion”.

Cleghorn (1769) suggested the name “aneurismal varix” for the direct communication. Without postmortem evidence for his conclusions, Benjamin Travers in 1809 described first pulsating exophthalmos and designated it as “Aneurysma per anstomosin” or “cirsoid aneurysms of the orbit” (Fig. 2.1) (Travers 1811).

Three years later on April 7, 1813, Dalrymple (1815) operated a second, similar case of pulsating exophthalmos and followed Travers’ explanation for its etiology, as did the majority of subsequent writers until 1823.

In these years the French anatomist Breschet (1829) studied in detail the vascular anatomy of the brain and skull, as well as the head and neck area and provided color plates in most outstanding quality (Fig. 2.2).

Guthrie (1827) recorded during the same period the first necropsy of a patient with pulsating exophthalmos and found instead of a “cirsoid aneurysm” an aneurysm of the ophthalmic artery: “On the death of the patient an aneurism of the ophthalmic artery was discovered on each side, of about the size of a large nut”. Thus, he was led to believe erroneously that it was the usual lesion in pulsating exophthalmos and advocated this as etiology of all reported cases of pulsating exophthalmos. This was supported by Busk’s (1839) autopsy findings of another case.

However, in France, four years prior to the Busk report, it was Baron (1835) who is given credit for being the first to discover a direct communication between the internal carotid and the cavernous sinus. Even though his report was so brief that it was

not noticed by many of his colleagues, he in fact established very early on the most important aspect in the etiology of pulsating exophthalmos, namely its intracranial cause. Gendrin (1841) found the same communication, and in 1856, Nelaton (Henry 1959) reported the similar finding.

In 1851, Nelaton (1857) also described the conversion of an arteriovenous aneurysm into a simple aneurysm due to thrombophlebitis and reported that the simple aneurysm was cured by proximal ligation. Broca (1856) applied the name “varicose aneurysm” to the direct communication by way of a false aneurysm sac interposed between artery and vein. Guattanus (1785) is given credit for the first cure of a brachial aneurysmal varix by a combination of direct and indirect methods of compression. In 1833, Breschet described two cases of arteriovenous fistula treated by ligation of the artery proximal to the opening, followed in each instance by gangrene of the limb beyond the fistula.

Baron (1835) first showed that the essential defect of a carotid cavernous sinus fistula was an opening between the internal carotid artery and the cavernous sinus.

Delens (1870) found in cadavers that the carotid artery, injected under pressure, ruptured most often in the segment coursing within the cavernous

sinus. It was also found that, in certain cases, preexisting aneurysms of the ICA had ruptured into the CS either spontaneously or as result of trauma. Direct trauma to the carotid cavernous sinus area by knitting needles, bullets, umbrella staves and similar sharp-pointed objects was also reported to have produced the lesion.

Interestingly, the concept of ruptured carotid artery in its course through the cavernous sinus, as supported by Delens, Nelaton and other French authors, was only reluctantly accepted in England. Travers, Dalrymple, and after them many English physicians, considered pulsating exophthalmos caused by an intraorbital aneurysm. This was in part due to Hulke (1859) and Bowman (1860), who observed a case in which they found all signs of pulsating exophthalmos including a dilated ophthalmic vein on autopsy, but no alterations in the carotid artery. Thus, they continued to suggest the theory of ophthalmic artery aneurysms based on the earlier observation of Guthrie (1827). Nunneley, Chief Surgeon of the Leeds Eye and Ear Infirmary, was the first English author who accepted that pulsating exophthalmos might indeed have an intracranial origin Nunneley (1864).

The excellent thesis of Delens (1870), and the lectures of Timothy Holmes (Holmes 1873) before the

Royal College of Surgeons in England between 1872– 1875 on the “The Surgical Treatment of Aneurism in Its Various Forms” helped the slow acceptance of the intracranial cause for an orbital symptomatology as arteriovenous aneurysm within the cavernous sinus (Fig. 2.3).

Sattler, Professor of Ophthalmology in Erlangen, provided the first detailed review of 106 cases collected to that date (Sattler 1880). He was opposed to the reports of Guthrie, Busk and Hulke and supported the etiology of an arteriovenous communica-

tion that in his opinion must have been frequently overlooked in previous descriptions. One of the interesting findings in his work is that in some cases significant thrombosis of the cavernous sinus or the superior ophthalmic vein was found. Nevertheless, he never assumed this per se could cause or trigger the typical symptoms of pulsating Exophthalmos. Most reports and studies of the following 50 years (including Dandys work) are based on the initial material provided by Sattler (1920, 1930), who continued his work and reported on 322 patients.

Dilated frontal vein (FV)

Dilated superior ophthalmic vein (SOV)

Optic nerve

Optic nerve

Ophthalmic artery (OA)

Internal carotid artery (ICA)

Dilated cavernous sinus (CS), cut open

Tear in the carotid wall (ICA cut open)

Dilated superior petrosal sinus (SPS)

Fractured and dislocated portion of the petrous pyramid

Optic nerve

Internal carotid artery (ICA)

Dilated intercavernous sinus (ICS)

Internal carotid artery (ICA)

Fracture line at the dorsum sellae

Fig. 2.3. Delens’ (1870) case. The second illustrated case of a traumatic CCF from the clinic of Nelaton after an autopsy report of a 17-year-old girl who developed a “pulsating exophthalmos” after a fall out of a carriage in July 1864.

The patient presented 6 months later and died 7 days following an unsuccessful operation due to pyemia. A fracture line running through the posterior and middle cranial fossa is seen, as well as a portion of the petrous apex that is detached and likely penetrated the carotid artery. Drainage into the enlarged intercavernous sinus, superior ophthalmic vein and superior petrosal sinus. (From Sattler 1920, 1930: Pulsierender Exophthalmus. In: Handbuch der Gesamten Augenheilkunde, Springer, pp 114–115)

de Schweinitz and Holloway (1908) in an analysis of 313 previously reported cases found that an abnormal communication between the internal carotid and cavernous sinus was the most frequent cause of unilateral exophthalmos, but that an aneurysm of the ophthalmic, or carotid arteries or even a tumor of the orbit could produce the same symptoms (Fig. 2.4).

Locke (1924) comprehensively reviewed 588 cases of pulsating exophthalmos, of which 126 occurred spontaneously and 418 were of traumatic origin. Conducting careful necropsies, he also found among 33 spontaneous cases that only 16 were caused by a communication between the artery and sinus. Seven cases occurred due to tumor, three due to aneurysm of the ICA, and three due to aneurysm of the ophthalmic artery. In one case no lesion was found. In 17 cases of traumatic origin, autopsies showed that 16 were due to direct communication between the carotid artery and the cavernous sinus and only one case was caused by an aneurysm.

Dandy (1935) and others found in reviews of postmortem examinations that the opening between the artery and sinus had varied in size from 1 mm to 10 mm and (Loehr 1937) that in a few instances the artery had been completely severed, the two ends lying within the sinus but separated by a centimeter or more. In some cases the carotid wall appeared to have weakened by arteriosclerosis and “given way, as do vessels in the brain”.

2.2 Angiography

Only one year after the invention of X-rays by Conrad Roentgen in 1895, Hascheck and Lindenthal (1896) performed the first angiogram on an amputated hand using chalk as contrast agent. On the 28th of June, 1927 during his ninth attempt, Egaz Moniz (Moniz 1927) performed the first cerebral angiogram ever, using strontium bromide in a 20-year-old boy who was blind because of a tumor in the sellar region. This procedure required direct contrast injection after surgical exposure and temporary ligation of the carotid artery. It was the first in vivo radiogram of the cerebral arteries showing displacement and stretching of the vessels by the tumor and represents a milestone in the development of diagnostic radiology.

Terry and Mysel (1934) performed the first angiogram in a patient with pulsating exophthalmos by injecting thorium dioxide sol. They were able to demonstrate the AV fistula between the internal carotid artery and the internal jugular vein in the upper part of the neck.

In the same year, Ziedses des Plantes (1934) presented a thesis in which he introduced two major elements of the twentieth century radiology, film tomography and film subtraction angiography. The

latter, which was the predecessor to X-ray digital subtraction angiography (DSA), was an important step forwards since it allowed for separating the relevant vessel information from superimposing osseous background. Some of the first angiographic images of patients with pulsating exophthalmos were presented by Loehr (1936) and Toennis et al. (1936) in Berlin.

Loehr (1936) initially did not express much enthusiasm when he stated: “Contrary to genuine aneurysms, the traumatic forms at the base of the cranium cannot be demonstrated so well by arteriography, since the blood and with it the contrast substance can pass into the sinus cavernous without coming into the hemisphere.”

Dandy (1937) who felt the clinical signs of pulsating exophthalmos are so striking that confirmation by another diagnostic procedure is not required, was initially very reluctant to see the need for cerebral angiography. Referring to the work of Terry and Mysel he stated “Since the clinical picture of these

aneurysms is unmistakable, one cannot be justified in unnecessary procedures merely to display them more graphically”.

There has been a noteworthy contribution to the subject by Wolff and Schmid (1939) from Wuerzburg in 1939, who carefully studied the venous drainage pattern of carotid cavernous fistulas and developed the first classification for CCFs (Figs. 2.5 and 4.2) that brought more acceptance to cerebral angiography. List and Hodges (1945) confirmed this work and were followed by others (Ramos and Mount 1953; Raney et al. 1948; Alpers et al. 1951). Raney and Raney (1948) recognized the value of arteriography in carotid cavernous fistulas for assessment of the collateral circulation through the circle of Willis; in cases where no dye would fill cerebral vessels, a trapping procedure could probably be performed safely.

Falconer and Hoare (1951) reported on a patient with a traumatic carotico-cavernous fistula that was maintained through the external carotid

artery. They were able to demonstrate angiographic evidence of cerebral arteries filled via the internal maxillary and ophthalmic artery anastomoses.

Parsons et al. (1954) reported the first spontaneous occlusion of a CSF following angiography.

Higazi and El-Bahanwy (1963) demonstrated the value of cerebral angiography for differential diagnosis in cases where other diseases may present the typical clinical picture of a classical carotid cavernous fistula. The authors emphasized its value in several aspects: the presence of a fistula, its exact site, the differentiation between unilateral and bilateral fistula etc.

Hayes (1958) suggested the differentiation in high-flow and low-flow fistulas. It became more obvious that angiography had significant value not only as a new diagnostic tool but also as a measure for efficacy of treatment methods and for development of new strategies. A few years later (Hayes 1963) he showed angiographic evidence in several cases of carotid cavernous fistula that reoccurred after ligation due to collateral flow through external carotid branches.

Possibly the first who observed a DCSF angiographically was Lie in 1961, when he performed an angiogram in a patient with “non-pulsating” exophthalmos (Lie 1968, Fig. 28 there). He noted a bilateral abnormal network near the sellar region, supplied by branches of the internal maxillary and middle meningeal artery. Although he could not

identify a fistula to the CS he commented this must have been an “abnormal form of carotid cavernous shunt”.

Castaigne et al. (1966) were probably the first to recognize and demonstrate the angiographic characteristics of a dural cavernous sinus fistula.

By 1939, Steinberg (1939) and Castellanos et al. (1937) had already investigated the possibility of performing iodine-enhanced angiography using intravenous injection. In the 1970s the development of real-time digital fluoroscopic image processors was begun and led to the introduction of three systems in 1980 (Mistretta and Grist 1998). Because intravenous DSA provided inconsistent image quality and often required repeated injection to overcome artery-vein overlap, a radiologist recognized that digital real time subtraction capabilities could be used with intra-arterial injections (intra-arterial DSA). Intra-arterial DSA has advanced and improved remarkably since, and despite significant technological efforts and investments in non-inva- sive imaging technique, is still the gold standard for vascular diagnosis due to its superior spatial resolution, unmatched time resolution and overall image quality. The development of three-dimensional DSA in the late 1990s has opened a wide range of new possibilities for visualization of cerebral vascular anatomy. Recently, the introduction of FD technology pushes again the limits of high quality vascular imaging (see more detail in Sect. 7.2.5).