REPORT OF 4 CASES. By I. GAI.IJGIONI, M.I).,* G. C. ANI)Rl0I1, NI.I).,f G. NIARIN, M.I).,* S. BRIAN!, M.D., and G. IRACI, M.I).t

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1 , No. 2 HYPOPLASIA OF THE INTERNAL CAROTID ARTERY ASSOCIATED WITH CEREBRAL PSEUDOANGIOMATOS IS REPORT OF 4 CASES By I. GAI.IJGIONI, M.I).,* G. C. ANI)Rl0I1, NI.I).,f G. NIARIN, M.I).,* S. BRIAN!, M.D., and G. IRACI, M.I).t PARTICULAR variety of cerebrovascubar anomaly, consisting of hvpop!asia of the internal carotid arters (often bilateral) with narrowing at the bevel of the supracbinoiti portion of its siphon anti with an unusual pseudoangiomatous pattern of the cerebral circulation almost resembling an arterio-arterial angioma has been recently describetb.5 #{176} 2 3 Since all patients were Japanese or of mixed Japanese extraction,4 3 this type of cerebral vascular abnormality was considered as being unique to the Japanese,4 2 3 but the feature of racial exclusiveness seems to have been disproveti by more recent observations. We have, therefore, deemed it worthwhile to report 4 cases which recently came to our attention, all belonging to the white, Mediterranean race, anti which presented some angiographic patterns that, in our opinion, may help toward a better understanding and definition of this disease. REPORT OF CASES CASE I. G.M., a 34 year old woman, was admitted with a history of subaracilnoid hemorrhage with residual paresis of the rigilt upper limb of a few hours duration. Upon neurologic examination, she exhibited moderate drowsiness, initial papilledema prevalent on the left side, a right homonymous visual field defect and right facial-brachial paresis. Blood pressure was II 5/70 mm. Hg. There were no signs of meningeai irritation. An eiectroencephaiogram showed a left ceritrai-temporal lesion. Left common carotid arteriograms (l ig. 1, i anti B; and 2 showed a complex abnormality I ADOVA AND FLORENCE, I I ALY of the cerebral circulation on that side, together with angiographic signs of a left temporal space-occupying lesion which was interpreted as an intracerebral hematoma. Improvement of the patient s neurologic status began shortly after admission and continued rapidly during the foiiowing days; a surgical procedure was, therefore, deemed onn ecessarv. Upon discharge a couple of weeks later, the patient had made a complete neuroiogic recovery and her state of consciousness was quite normal. The only residual neurologic deficit consisted of a homonymous right upper quadrant defect of the visual field. About i year later, the patient again suffered a sudden right hemiparesis, without impairment of consciousness and or headache. She was again admitted to our Institute and a repeat left carotid arteriogram showed a similar cerebro-vascular pattern (Fig. ic), without changes but for the disappearance of signs of a temporal intracerebral hematoma. A right carotid arteriogram was obtained and on this side also a complicated abnormality of the cerebral circulation could be seen (Fig. id; and ). During iler second hospital stay, the patient likewise made a complete neuroiogic recovery and she was discharged. CsE 11. R.F., a 44 year old woman, had been complaining for the past 12 months of intermittent, transient episodes of dizziness, drowsiness and left hemiparesis, each of about i week s duration and followed by complete spontaneous recovery. Ipo1l admission, she showed a left hemiparesis more pronounced of the upper limb. Blood pressure was 14o/7c mm. Hg. An electroencephalogram siioweti a slow-wave pattern on * Neuroradiolo,iical Service, OspedaIe ( i vile, P;ulovi, I Ia ly. t Institute of Neurosurgery, University of Padova, Italy. Division of Neurosurgery, Ospedale S. Maria Nuova, Florence, Italy. 251

2 242 Galligioni, Albtirioli, \lariil, Briani albti iraci JINE, 1971 I i;. I. Case I. Left cirotiti arteriograms, arterial phase. (A) Lateral and (B) anteroposterior views. Reduction in caliber throughout the entire length of the vessel and marked stenosis at the distal part of the supraclinoid siphon, distal to the origin c)f the anterior choroidal artery, are noted. Above this, an intricate and dense network of thin arterial vessels can be seen. The anterior choroidal artery is larger than normal and contributes to the replenishment of the middle cerebral artery. The latter is displaced upwards and medially h- a large avascular expanding lesion (hematorna?) in the temporal lobe. The anterior cerebral irterv is filleti bs- a collateral circulation through the ethmoidal branches of the ophthalmic artery. (C) Contrc)l left carotid arteriogram, I year later. There are no signs of an intracerebral expantiing temporal lesion; all other features remain unchangeti. (D) Right carotid arteriogram, arterial phase, oblique view. There is a si-nail aneurysm at the carotid siphon (hollow arrowhead) directed anteriorly and medially anti originating below the ophthalmic artery. There is mild narrowing of the internal carotid artery; an abnormal vascular network is formed b thin arterial vessels, presumably leptomeningeal, originating from the alar tract of the midtilc cerebral artery. The A, (supra-optic) tract of the anterior cerebral artery is formed by separate vessels. resting, localized in the left temporal region. Bilateral carotid arteriograpibies were performed (Fig. 3, 1-I); and 4). Tue patielit recovereti completely in a few das anti was discharged in a normal neurologic state following treatnient with vasodilators. III. \l.\., a 42 ear old woman, was admitted with a history of dull, intermittent headaches for the past years. Ten years previously, she llad sutlered, post partu Ill, a sudden right hemiparesis, thsturbances of motor speech, aiitl mental confusion, which cleareti following vasodilating treatment given elsewhere. After 9 years of gootl health anti I year prior to adilissioli, sue began experiencing again progres-

3 \oi. 112, No. H poplasia of Internal Carotid.Arterv G. 2. Case. Schematic representation of the arteriographic findings shown in Figure 1. The replenishment of the anterior cerebral artery from vessels originating from the ethmoidal branches of the ophthalmic artery was obtained in earlier phases than those shown in l igure I. sive mental confusion, dyspiiasia, and rightsided paresthesias which eventually led to her admission. tpon neurologic examination, she exhibited a marked mental confusion and temporal-spatial disorientation, expression paraphasias, central deficit of tile right facial nerve, right hemiparesis prevalent in the upper limb, impairment of epicritic sensation and loss of stereognosis Ofl the right side of her body. Electroencephalogram, brain scanning and lumbar puncture gave normal findings. Bilateral carotid arteriographies were performed (Fig. c, 11-D; and 6). After treatment witil vasodilating drugs, the patient made a complete recovery and was tlischarged. CASE 1V. P.L., a year old girl who had been delivered 15 days after expected time, showed at birth a severe cyanosis and had to be given an exchange transfusion because of Rh factor incompatibilit. During the following years, her physical growth was normal but her mental development was severer delayed: she suffered a marked oligophrenia and frequent temper tantrums which made her a beilavior probhem witilin the family and at kindergarten. Several times she had suffered minor head 111- juries without any apparent serious consequences; only 2 weeks prior to admission, following a fail, she suffered a clonic Jacksonian seizure affecting her right face and upper limb arid followed by a residual right ilemiparesis. Upon examination, she showed a total inability to speak and to understand, and a marked right hemiparesis. An electroencephalogram revealed a left hemispheric lesion with involvement of the deep cerebral structures. A left carotid arteriographv (Fig. 7, A-C) was done, followed by right cerebral arteriograph via a retrograde injection into the brachial artery (Fig. 8, A-D; and 9). She was discharged in unchanged condition

4 254 (alligioni,.alitirioli, \lariri, lriarii and Iraci., 1)7! 1 ic.. Case 11. (A and B) Left carotid arteriograms in the lateral (A) and anteroposterior (B) views. I here is marked hypoplasia anti narrowing of the carotiti artery with stenosis at the supraclinoid tract of the siphon, immetiiatelv distal to the origin of the anterior choroidal arter (hollow arrowheads). Immediately above the stenosis, there is an abnormal and intricate vascular network formed b thin anti tortuous arterial vessels, showing some tentiency to replenish the internal carotitl artery distal to the stenotic tract (large black arrowheads). This network is only partially formed by branches originating from the initial part of the anterior choroidal artery. Anastornosis can be seen (small black arrows) between branches of the anterior cerebral artery anti mitidle meningeal and superficial temporal arteries at the vertex, allowing refilling of the fronto_polar and calloso-marginal arteries (distal branches). (C anti D) Right carotiti arteriograms in lateral (C) and oblique (D) views. There is a segmental narrowing of the supraclinoid part of the siphon, where a small saccular aneurysm, directeti anteriorly and medially, can be seen originating at a site quite similar to that observed in Case, (large black arrowheads). An intricate, abnormal network of thin vessels, probably (if leptomeningeal origin (large black arrows) is located at the bifurcation of the internal carotid arter anti accompanies the course of the anterior cerebral artery. Note the spontaneous filling of the contralateral anterior cerebral artery through the anterior communicating artery.

5 \oi.. 112, N0, 2 ilvpopbasia of Internal (,arotiti.arterv 2cc I l(,. 4. Case ii. Schematic representation of the arteriographic findings illustrated in l igure,. arid, i year later, re-admitted for a control left carotid arteriography (Fig. 10, A anti B). A control electroencephalogram siiowed no significant change from tue one performed year earlier. I)ISCUS S ION There are 3 aspects of the angiographic findings of our patients which shoulti be considered sepa ra tel v. i. Hypoplasia oj the internal carotid artery with complete stenosis at the suprac/inoid tract oj the siphon. The malformative origin of this abnormality appears to be proveti, in our opinion, by its extension to, anti by its uniformity through, the full length of the vesseb- a fact which should rule out an acquired disease such as arteritis. The findings of Brihave anti Dhaene, Priman anti Christie, 4 anti Van tier Zwan anti Fossen, 7 which are quite similar to tibose observeti in our patients, would appear to confirm tilis il\-pothesis. 2. The abnormal, pseudoangiomatous pattern with its peculiar/eatures, boca ted at the I)ase of the brain near the bifurcation of the internal carotiti artery, has been interpreted 2 as a residual of the rete mirabile which is characteristic of some mammalian species. In fact, in some animals (cat, goat, sheep, ox anti pig), in which blood is supplied to the anterior part of the brain tilrouglb numerous, thin arterial vessels in various forms of anastomoses and intertwining, originating from branches of the external carotitb artery (anastomotic branch and artery from the internal maxilbarv arter\, ascending phar\ ngeal anti accessorv meningeal arteries), a real and true rete mirabile is present. Daniel et al.2 anti Lie stated that the degree of development

6 2#{231}6 Galligioni, Andrioli, Mann, Bniani anti maci JuN., 1971 lu;. c. Case III. (A and B) Left carotid arteriograms in anteroposterior (A) and lateral (B) views. The artery is narrowed along its cnt1re course, with a severe stenosis at the origin of the ophthalmic artery (hollow arrowheatls). Above the stenotic tract anti the sella, and close to the Illitiline, a pseutloangiomatous network formeth by intricate, thin anti tortuous vessels can be seen. I his network tioes not seem to Provitie any collateral circulation. Replenishment of the anterior and mitidle cerebral arteries is instead contributed by the well visible anterior meningeal artery and by some branches of the superficial temporal artery. (C and D) Right carotid arteric)grams in lateral (C) and anteroposterior (D) views. There is hypoplasia of the internal carotiti artery, with marked stenosis (hollow arrowheads) at the origin of the ophthalmic artery, similar to that seen on the left side. A similar abnormal pattern of vascular network is also present (large black arrowheads). Branches of the anterior cerebral artery are filleti through branches from the ophthalmic, mitidle meningeal anti superficial temporal arteries (small black arrows). Some branches coming from the occipital artcr- contribute to a partial filling of the left mitidle cerebral artery. The vertebrobasilar district, thinly filled, gives some collateral circulation to the supratentorial cerebral circulation. This latter finding was later confirmed by aortographv. of such rete mirabile in these animals is inversely proportional to that of the internal carotid artery. Quain with his anatomopa thobogi c studies, and Fields et al.,3 and Minagi and Newton1 with their angiographic studies have given the only proven demonstration and description of a rete mirabile in man. Indeed, the tbense vascular network found in our cases might be the residual of such a rete mirabile, but this hypothesis remains open to dispute because of the lack of an anatomic demon-

7 V01.,ii, No. Hypopbasia of Internal Carotid Artery 257 FIG. 6. Case in. Schematic representation of the arteriographic findings illustrated in 1 igure c. stration of a direct origin from the external carotid artery, with all its functional significance. It cannot be ruled out, however, that the anomalous supraclinoiti circulation network may be formed by tentoriai anti leptomeningeal vessels, originating from the carotid siphon, which in the presence of hypoplasia of the internal carotid artery could undergo an abnormal development. 3. The collateral circulation networks, formed by branches from the external carotid artery (meningeab branches), by the vertebral-basilar system, and by hypertrophic beptomeningeal vessels, are founti (although in greatly varying patterns) in cases of internal carotiti artery stenosis to be more common. They contribute, in varying degrees, to the collateral refilling of the cerebral vessels distal to the site of stenosis. In 2 of our cases, the presence of a saccular aneurysm, contrabateral to the hypc_ plastic internal carotid artery and located at an unusual site along the carotid siphon in both patients, should be added to these angiographic features, as well as tile rare developmental anomaly of the supra-optic anterior cerebral artery formed b 3 separate vessels (Case I). The most important question presented by this anatomic and angiographic appearance of the vessels is whether their origin should be ascribed to congeni tab-malformative, or to acquireti causes. Opinions on this subject are divided. Kudoh5 6 stateti that the condition should be attributed to an acquired disease (arteritis), basing his opinion on the angiographic findings obtained in a year old boy who showed gradual onset and progression of the carotid artery stenosis with parallel devebo#{231}ment of an anomalous vascular network as a collateral

8 258 Galligioni, Antinioli, Mann, Briani anti maci JUNE, 1971.A 1 1 N 11G. 7. Case iv. I.eft carotid arteriograms in (3 and B) anteroposterior views at different stages and (C) lateral view. There is a diffuse and severe stenosis of the supraclinoid tract of the carotid siphon, with marked slowing of the cerebral circulation. Above the stenosis, an intricate and dense vascular network in- Volves the whole region of the basal nuclei, extending anteriorl- as far as the metiial thirti of the orbital roof. Ihie ophthalmic artery has an enlarged caliber; the anterior anti mititile meningeal arteries are also enlargetl, in an attempt to supply collateral circulation. Some tortuous thin vessels can also be seen in the frontal anti parietal regions.

9 Vol.. 112, No. 2 Hypoplasia of Internal Carotiti Arter Ji. 11G. 8. Case iv. Right cerebral angiograms, via retrograde injection into the brachial artery, show a similar pattern in the right carotid circulation anti in the vertebro-basilar district. There is a maximum filling of the basilar artery and Its branches demonstrated in the anteroposterior (4) and lateral (B) views. There is a dense pseudoangiomatous network supplieti by branches of the 2 posterior cerebral arteries, mainly by the posterior choroidal arteries. There is no evident tentlencv to replenishment of the supratentorial vessels. The internal carotid artery is still scarcely filletibut a severe stenosis of its supraclinoid tract is already visible. (C and D) A pseudoangiomatous pattern with the same characteristics can be seen in a deep, paramedian location, immediately above the carotid artery stenosis. There is also a thick network in the territory of the ophthalmic artery anti from the ethmoidal branches. circulation along the carotid siphon. Other authors #{176} 2 6 support a congenital and malformative origin of this disease. On the basis of the information obtaineti in our cases, we are inclined to support this batter viewpoint.2 In 2 of our cases (Cases and ii), alterations of a definitely malformative origin were present (the 2 saccular aneurysms and the abnormality of the A/i tract of the anterior cerebral artery). Further evidence is furnisheti, in our opinion, by the angiographic appearance of the left internal carotid artery in our first anti second patients and of both internal carotiti arteries in our third patient, with a uniform narrowing of the caliber, beginning at their origin and without any of the segmental narrowings or marginal irregularities which I

10 260 Galligioni, Antinioli, Mann, Bniani anti maci JUNE, G.. Schematic representation of the angiographic findings illustrated in l igures 7 anti 8. 11G. 10. Case iv. (A arid 13) Control left carotid arteriograms, 1 year later. The vascular pattern Presents no significant change from the previous examination. The richer filling and more extensive network, as cornpared with the arteriograms shown in Figure 7, are the results of a different phasing of the injection.

11 VOL. 112, No. 2 Hypoplasia of Internal Carotid Artery 261 are characteristic ofarteritis or of acquired arterial thromboses. The pseudoa ngioma totis circuba tion located along the carotid siphon which, according to supporters of the acquired origin of the disease, has the significance of coblateral circulation originating from the antenor choroidab artery, presents such characteristics as to exclude both dependence on the anterior choroidal artery and functional efficacy as a collateral circulation. It shoubti be further noted that, contrary to the patients reporteti by Maki and Nakada, #{176} and by Kudoh, 6 the disease in our cases has presented no tendency to progression, as proved by the arteniographic control stutlies anti by the continuous dinicab follow-up examinations. The fact that symptoms of intermittent cerebral ischemia did not appear in our first 3 cases until adult age is, in our opinion, insufficient evidence against a malformative etiology. It is conceivable that the abnormality of the cerebral circulation becomes clinically evitient only when progressive cerebro-vascular changes, compatible with adult life, result in a diminution of the functional reserves of the intracranial circulation. It should be remembered, furthermore, that the isolated autopsy reports so far available4 have given no substantial contribution to a better knowledge and understanding of this condition. The hypothesis of a malformative cause of this vascular abnormality is thus supported, in our opinion, by the association of other aspects which are clearly of congenital origin, by the characteristics of the stenosis of the internal carotid artery, by the features of the pseudoangiomatous pattern and by the lack of progression of the disease. However, some reservations must be kept in mind because of the complexity of all these angiographic patterns and the several differences found in the cases hitherto reported in the literature. It is possible, for instance, that different etiologic elements may coexist in this condition, or that the functional insufficiency of the carotid artery may eventually lead, in due time, to collateral circulation patterns quite peculiar and unusual. A better explanation to all these factors will be possible only after further clinical, angiographic and autopsy observations. SUMMARY Four cases ofa peculiar cerebral vascular abnormality, consisting of hypoplasia and stenosis of the internal carotid artery, often bilateral, and of an unusual pseudoangiomatous cerebr; b circulation, are reported. Such a condition, originally found in Japanese patients only, has an undetermined cause. The information obtaineti through dinicab and angiographic studies in these 4 cases seems to favor the hypothesis of a congenital and malformative origin of this vascular abnormality. Giorgio Iraci, M.D. Institute of Neurosurgery, University of Padova Ospedale Civile Padova, Italy REFERENCES r. BRIHAYE, J., and DHAENE, R. R#{233}tr#{233}cissement congenital important de l art#{232}re carotide interne. Neurochirurgie, 1962, 8, DANIEL, P. M., DAWE5, J. D. K., and PRICHARD, M. L. Studies of carotid rete and its associated arteries. Philos. Trans. Roy. Soc., Ser. B, 1953, 237, lield5, W. S., BRUETMAN, M. E., and WEIBEL, J. Collateral Circulation of the Brain. Williams & Wilkins Company, Baltimore, KAWAKITA, Y., ABE, K., MIYATA, Y., and HORIKOSHI, S. Spontaneous thrombosis of internal carotid artery in children. Folia Psychiat. Neurol. Jap., 1965, 19, KUDOH, T. Juvenile occlusion of circle of Willis. Clin. Neurology, 1965, 5, Also in Proc. 8th Internat. Congress Neurology, 1966, 4, KUDOH, T. Spontaneous occlusion of circle of Willis; disease apparently confined to Japanese. Neurology, 1968, z8, LEEDS, N. E., and ABBOTT, K. H. Collateral circulation in cerebrovascular disease in childhood via rete mirabile and perforating branches of anterior choroidal and posterior cerebral arteries. Radiology, 1965, 8, LEPOIRE, J.,TRIDON, P., MONTAUT, J., HEPNER,

12 262 Galligioni, Andriobi, Mann, Bniani and Iraci JUNE, 1971 H., RENARD, M., and PICARD, L. Angiomes c#{233}r#{233}braux; malformations angiomateuses artcrio-art#{233}rielles du syst#{232}mecarotidien. Neuro- (hirurgie, 1969, 15, LIE, T. A. Congenital anomalies of carotid arteries (angiographic study and review of the literature). Excerpta Medica Foundation. Williams & Wilkins Company, Baltimore, MAKI, Y., and NAKADA Y. Autopsy case of hemangiomatous malformation of bilateral internal carotid arteries at base of brain. Brain, 1965, 17, ii. MINAGI, H., and NEWTON, T. H. Carotid rete mirabile in man; case report. Radiology, 1966, 86, NI5HIM0T0, A., and TAGEUCHI, S. Abnormal cerebrovascular network relateti to internal carotid arteries. 7. Neurosurg., 1968, 29, NISHIMOTO, A., TAGEUCHI, S., and KATOW, T. Cerebral basal rete mirabile in man; special type of cerebral abnormalities of Japanese. Presented at the Eighth Symposium Neuroradiologicum, Paris, PRIMAN, J., and CHRIsTIE, D.H. Case of abnormal internal carotid artery and associated vascular anomalies. Anat. Rec., 1959, 134, i. QUAIN, R. The Anatomy of Arteries of the Human Body. Taylor & Walton, London, i 8. i6. SANO, K. Cerebral juxta-basal telangiectasia. Brain, 1965, 17, VAN DER ZWAN, A., and FossEx, A. Une m;tlformation du cercle du Willis. Neurochirurgie, 1962, 8, i8. WEIDNER, W., HANAFEE, W., and MARKHAM, C. H. intracranial collateral circulation via leptomeningeal and rete mirabile anastomoses Neurology, 1965, 15,

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