RGNS Child's Nerv Syst (1985) 1:363-366 © Springer-Verlag 1985 A case of internal carotid artery occlusion successfully treated by encephalo-duro-arterio-synangiosis Yoshiharu Matsushima *, Yoshio Takasato, Tohoru Fukumoto, Shin Tsuruoka, Takekane Yamaguchi and Yutaka Inaba Department of Neurosurgery, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo, 113 Japan Abstract. In m a n y cases, intracranial occlusive strokes in children are treated symptomatically, with a diagnosis o f acute infantile hemiplegia. This is because a n g i o g r a p h y is more difficult in children and, even if occlusive cerebral arterial disease is diagnosed, there is no definite therapeutic procedure. A case is reported o f left internal carotid artery occlusion presenting with acute infantile hemiplegia and followed by r e p e a t e d transient ischemic attacks. Encephalo-duro-arterio-synangiosis - d e v e l o p e d as an operation for m o y a m o y a disease - was p e r f o r m e d on this patient, resulting in a m a r k e d revascularization o f the brain in 8 postoperative months with good i m p r o v e m e n t in symptoms. This suggests that the operation m a y be effective in chronic cerebral ischemic diseases other than m o y a m o y a disease. Key words: Acute infantile hemiplegia - Pediatric stroke Internal carotid synangiosis. occlusion - Case report A 3-year-old boy was apathetic for 1 day before 3 April 1981, when he could not stand up in the morning, suffering weakness in the extremities. He had no appetite and could not talk. There were no remarkable fmdings on the first computed tomography (CT) examination. After the attack, he began to take meals on the 3rd day, to talk on the 5th day, to sit on the floor on the 7th day and to stand up on the 8th day. CT performed on 13 May 1981 revealed a low-density area in the left. frontal lobe. On 30 June 1981, it became difficult for him to walk, again for 2 days, but his gait returned to normal within a week. Cerebral angiography performed on 19August 1981 revealed that the left internal carotid artery was completely occluded just distal to the origin of the ophthalmic artery (Fig. 1). The left cerebral arteries were opacified by the right internal carotid artery via the anterior communicating artery. On 6 May 1982, it again became difficult for him to stand up, but he returned to normal the following afternoon. On 5 October 1982 he had an attack of weakness following blood drawing, but returned to normal within 15 min. Encephalo-duro-arterio- Intracranial occlusive cerebral arterial disease in children is a c o m m o n cause o f pediatric stroke. In most cases, treatment is palliative with a diagnosis o f acute infantile hemiplegia, without the establishment o f a definite etiology. This is p r o b a b l y because cerebral a n g i o g r a p h y is less easily p e r f o r m e d in children, a n d also because there is no c o m m o n l y accepted t h e r a p y for occlusive cerebral arterial disease. Recently, we treated a child with left internal carotid artery occlusion, who h a d r e p e a t e d attacks o f reversible ischemic neurologic deficit or transient cerebral ischemia by encephalo-duro-arterio-synangiosis (EDAS) [9], a treatment developed for pediatric m o y a m o y a disease. The result was a r e m a r k a b l e revascularization, confirmed by cerebral angiography p e r f o r m e d 8 months after the operation. * To whom offprint requests should be addressed Fig. 1. Preoperative left common carotid angiogram (19 August 1981), 0.5 s after the injection of the contrast medium. Complete obstruction of the internal carotid artery (arrow) visible at the site immediately distal to the origin of the ophthalmic artery 364 Fig. 2A-C. Postoperative selective left external carotid angiograms (5 September 1983) 10 mouths after EDAS. Revascularization of left middle cerebral zone is visible, A = 0.5, B = 1.5, and C = 3.5 s after the injection of contrast medium On 15 October 1982, he was admitted to our hospital. His blood pressure was 129/90mmHg and his pulse rate was 112/rain. Overall general examination was not remarkable, with no cardiomegaly or audible murmurs. The positive neurological signs included slightly hyperactive deep tendon reflexes on the left side, mild right-sided hemiparesis with slightly hemiparetic gait, and awkward usage of the right hand with no grasping power. Skull radiographs revealed a slightly smaller left cranial vault. CT showed slight widening of the left frontal subarachnoid spaces and a larger left lateral ventricle, probably indicating left frontal lobe atrophy. On 29 October 1982, we performed EDAS [9] using the parietal branch of the left superficial temporal artery. The postoperative course was uneventful, and he was discharged on 13 November 1982. No transient ischemic attacks were observed thereafter, and the right hemiparesis has improved. On 5 September 1983, selective angiography of the left external carotid artery (Fig. 2) was performed: left cerebral revascularization from the donor scalp artery was clearly seen. Discussion It has been reported by m a n y investigators that cerebral arterial disease is a c o m m o n part of the etiology o f acute hemiplegia in childhood [1, 2, 3, 11]. A m o n g these reports, the largest series is reported in the textbook by HarwoodNash [2], who diagnosed 65 cases o f cerebral arterial occlusion with idiopathic or acute onset ofhemiplegia who had previously been quite normal, with no evidence o f intracranial or systemic disease of any kind. They classified them into three types (types I - I I I ) from the viewpoint o f cerebral angiography. Our case was confirmed to have unilateral intracranial internal carotid occlusion and belonged to their type IIa. According to Bickerstaff [1] and other investigators [2, 12], cases corresponding to type II a often recanalize, and the symptoms improve with time. In contrast, our case manifested repeated transient ischemic attacks without recanalization during the 1-year observa- tion period. There was complete occlusion o f the left internal carotid artery (Fig. 1). Since the anterior circulation of the left cerebrum was supplied by the blood flow from the opposite anterior cerebral artery through the anterior communicating artery, sufficient blood flow could not be maintained when the d e m a n d for blood in the left cerebrum increased or when PaCO2 was decreased by hyperventilation, resulting in a decrease in the total cerebral blood flow. Transient ischemic attacks were induced on such occasions. Thus, we thought that EDAS [9] - developed by us for the treatment of m o y a m o y a disease, a typical chronic progressive cerebral ischemia in childhood - might be effective for the chronic ischemia in this case. In order to explain this, we should describe our concept of collateral circulation in the case o f chronic cerebral ischemia. According to our classification [6], the collaterals of the brain are composed o f seven systems referred to as A - G surrounding the brain in laminar layers (Fig. 3): the A, B, and C systems are o f the internal carotid artery, and the D and E systems are of the external carotid artery. These systems assume different functions during cerebral ischemia. For-example, in m o y a m o y a disease, which is a progressive failure of the B system, the collaterals of the A and C systems belonging to the same internal carotid artery system act immediately to compensate for the failure. Although the well-developed picture of the A system is noticed as the m o y a m o y a vessels because of its distinguishing feature, the C system is not so noticeable because it is composed of the cortical arteries seen on a normal cerebral angiogram. When the D and E systems o f the external carotid artery serve as collaterals through transdural anastomoses, the m o y a m o y a vessels of the A system become reduced or disappear: spontaneous cure o f pediatric m o y a m o y a disease occurs [13]. This process 365 CSF: XER Fig. 3. Schematic illustration of collaterals to the brain. A system, Anastomosis intracerebralis; B system, basal communications; C system, cortical leptomeningeal anastomosis; D system, dural networks; E system, extracranial networks; (F system, functional collaterals); G system, ground communications requires a great deal of time, because the layer of CSF in the subarachoid spaces between the C and D systems interrupts their physical continuity. Also, the skull is a barrier between the D and E systems, inhibiting the formation or growth of collaterals. Therefore, in order to treat moyamoya disease surgically and successfully, one must both minimize the damage to the D and E systems and eliminate the obstacle, i.e., the subarachnoid fluid space and the skull. Thus, it is possible to produce the spontaneous healing of this disease by establishing the condition i n which failure of the B system is completely compensated for by the D and E systems, without waiting for the lapse of time. Since EDAS is an indirect E C / I C bypass operation based on the above-mentioned concept [6], and is designated to cause minimal damage to the D and E systems, it was expected that this operation would probably be effective for our case with the already described chronic ischemic condition. EDAS involves making a linear scalp incision along a donor scalp artery and freeing the artery for a certain length with a strip of Galea attached. The artery then is sutured with the strip of Galea onto the linear dural opening through a narrow cranial window made in the skull. The donor scalp artery is not cut, and the blood flow of this artery is not obstructed throughout the procedure. In this operation, incisions made on the D and E systems are all linear and parallel to the direction of thick arteries, minimizing damage to these systems [7, 9]. Although encephalo-myo-synangiosis (EMS) [4], and superficial temporal-middle cerebral artery (STA-MCA) anastomosis [5] seem to be similar to EDAS, these methods are quite different in that they cause too much damage to the E and D systems, sacrificing the naturally and already formed, collaterals and reserve collaterals by making large scalp and dural flap and/or cutting the superficial temporal artery, which is the main artery of the E system. EMS has further disadvantages in its use of muscle, from muscle contractile action, electrical potential activity, extensive adhesions, compression over the brain as subdural hematoma, wide bone defect to pass the muscle flap, and so on. STA-MCA anastomosis also has some disadvantages. In children, both the donor scalp artery and the recipient cortical artery are quite narrow. Skill in the technique is required, and thus the operative results are variable. Since it is necessary to close off the recipient artery for a period of time, focal brain circulation may be impaired. Furthermore, if anastomotic failure occurs, the vessels with abundant blood flow may be lost by thrombosis. EDAS was developed to eliminate the disadvantages of these two methods and has been proved to work well in the treatment of moyamoya disease in children [7, 8, 10]. It seems that omental transplantation has been widely performed in China [14], but this method has the disadvantages of both EMS and STA-MCA anastomosis from the viewpoint of our concept of collateral formation, and should not be used as a therapeutic method for cerebral ischemia in children. References 1. Bickerstaff ER (1964) Aetiology of acute hemiplegia in childhood. Br Med J II: 82-87 2. Harwood-Nash DC, Fitz CR (1976) Neuroradiology in infants and children. Mosby, St Louis, Mo, pp 929-955 3. Hilal SK, Solomon GE, Gold AP, Carter S (1870) Primary cerebral arterial occlusive disease in children. I. Acute acquired hemiplegia. Radiology 99:71-86 4. Karasawa J, Kikuchi H, Furuse S, Sakaki T; Yoshida Y, Ohnishi H, Taki W (1977) A surgical treatment of "Moyamoya" disease, "encephalo-myo-synangiosis." Neurol Med Chir (Tokyo) 17:29-37 5. Karasawa J, Kikuchi H, Furuse S, Kawamura J, Sakaki T (1978) Treatment of moyamoya disease with STA-MCA anastomosis. J Neurosurg 49:679-688 6. Matsushima Y, Inaba Y (1983) Dynamics of formation of collaterals in pediatric moyamoya disease and it's surgical treatment. I. Collateral circulation to the brain and dynamics of collateral formation in moyamoya disease (in Japanese). Nerv Syst Child 8:57-65 7. Matsushima Y, Inaba Y (1984) Moyamoya disease in children and its surgical treatment. Introduction of a new surgical procedure and its follow-up angiograms. Child's Brain 11: 155-170 8. Matsushima Y, l_naba Y (1985) Expeoence in eneephaloduro-arterio-synangiosis, a new surgiear procedure to treat moyamoya disease in children. Microsurgical anastomoses for cerebral ischemia. Igaku-Shoin, New York Tokyo, pp 275-277 9. Matsushima Y, Fukai N, Tanaka K, Tsuruoka S, Inaba Y, Aoyagi M, Ohno K (1981) A new surgical treatment of 366 moyamoya disease in children: a preliminary report. Surg Neurol 15:313-320 10. Matsushima Y, Tomita H, Takei H, Yamaguchi T, Takasato Y, Tsuruoka S, Fukumoto T, Kuroiwa T, Takada Y, Niimi Y, Inaba Y (1985) Changes in symptoms after encephalo-duroarterio-synangiosis (EDAS) in pediatric moyamoya disease. Cerebral revascularisation for stroke. ~[hieme-Stratton, New York, pp 578-583 11. Shillito J (1966) Carotid arteritis: a cause of hemiplegia in childhood. J Neurosurg 21:540-551 12. Solomon GE, Hilal SK, Gold AP, Carter S (1970) Natural history of acute hemiplegia of childhood. Brain 93: 107-120 13. Suzuki J, Kodama M (1983) Moyamoya disease - a review. Stroke 14:104-109 14. Wu PHT (ed) (1983) Abstracts of the 6th Asian-Australian Congress of Neurological Surgery, Hong Kong, pp 168-170 A nnouncement The 14th Scientific Meeting of the International Society for Pediatric Neurosurgery will take place in Madrid, Spain, September 30-October 3, 1986. Chairman: Francisco J. Villarejo, Prado del Rey, 65, Somosaguas, 28023 Madrid, Spain.