Isolated origin of the left internal carotid artery from the pulmonary artery
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1 J Neurosurg Pediatrics 2: , 2008 Isolated origin of the left internal carotid artery from the pulmonary artery Case report MICHAEL C. HURLEY, M.D., 1,2 PAMELA H. NGUYEN, M.D., 1 ARTHUR J. DIPATRI, M.D., 2 AND ALI SHAIBANI, M.D. 1,2 Departments of 1 Neuroradiology and 2 Neurosurgery, Children s Memorial Hospital, Chicago, Illinois The authors describe what is, to their knowledge, the first reported case of the anomalous origin of an internal carotid artery from the pulmonary artery. An otherwise asymptomatic 6-year-old girl, who presented with headaches and hypertension, underwent a comprehensive workup that revealed extensive meningeal and cerebral artery anastomoses to the left internal carotid artery itself arising from the origin of the left pulmonary artery. This unique anatomical anomaly, caused by a disturbed pattern of aortic arch regression, resulted in a right-to-left vascular shunt into the pulmonary artery and a disturbance of intracranial artery flow patterns, complicating the management options. (DOI: /PED/2008/2/9/207) KEY WORDS aortic arch internal carotid artery pulmonary artery D ISTORTED, primitive aortic arch regression can result in anomalous origins of the subclavian, innominate, or CCA from the PA. Five reports of anomalous CCA origin from the PA exist. We describe what we believe to be the first reported case of an anomalous left ICA originating from the left PA with an independent left ECA origin as the first aortic arch branch. Pathogenesis is discussed and illustrated, and clinical implications and management issues are considered. Case Report History and Presentation. This otherwise healthy 6-yearold girl was referred to her family physician with a complaint of mild, but troublesome, recurring headaches. Examination revealed mild hypertension, which was persistent on repeated assessments. Her remaining examination was normal with no neurological deficits or cervical or precordial bruits. Imaging Examination. Magnetic resonance images of the Abbreviations used in this paper: CA = carotid artery; CCA = common CA; ECA = external CA; ICA = internal CA; MCA = middle cerebral artery; PA = pulmonary artery; TOF = time of flight. patient s head were obtained and the standard sequences were unremarkable. However, unenhanced 3D TOF MR angiography failed to demonstrate a normal left ICA flow signal despite a normal corresponding flow void on the T2- weighted axial sequence (Fig. 1A and B). Subsequent CT arteriography images revealed a well-opacified left ICA at the skull base. We deduced that the TOF MR angiographic appearance was a result of signal nulling of reversed flow in the left ICA caused by the cranial presaturation pulses which are routinely applied to eliminate potential venous contamination of the arteriogram. Computed tomography angiography also demonstrated an enlarged left internal maxillary and ascending pharyngeal arteries feeding a fine network of vessels centered in the dura mater of the left cavernous sinus and communicating with the cavernous ICA via the inferolateral and meningohypophyseal trunks (Fig. 1 C and D). The left ICA was ectatic at the skull base, becoming more narrow distally. The left posterior communicating artery and left anterior cerebral artery A1 segment were small and tortuous, and the left middle cerebral artery appeared normal. Contrast-enhanced MR angiography demonstrated vascular anatomy from the aortic arch to the skull base, independent of flow direction. The right aortic arch branched in 207
2 M. C. Hurley et al. FIG. 1. Axial TOF MR (A and B) and CT angiography (C and D) images of the anastamoses through the skull base. A and B: Flow signal in the left ICA (*) is absent below the skull base (A) and reduced in the carotid canal (B) due to reversed and turbulent flow, respectively. Compare to normal right ICA (curved arrow). Enlarged left ECA collateral vessels: left STA (double arrowheads) and middle meningeal artery (arrow) arising from the left internal maxillary artery (A), middle meningeal artery in the foramen spinosum (arrow, B), distal internal maxillary artery in the pterygopalatine fossa (triple arrowheads, B), left APA branches (arrowheads, A) and bilateral hypoglossal branches (zig-zag arrows) indentifiable as they pass through the hypoglossal canals, and branch into clival dural anastomoses (B), and left accessory meningeal artery entering the foramen ovale (double arrows, B). C and D: Images through the normally opacified cavernous segment of the ICA (*) show a prominent cavernous dural network of vessels composed of branches of the artery of the foramen rotundum converging on the inferolateral trunk (double arrows, both panels), joined by branches of the middle and accessory meningeal arteries (arrow, C). Clival dural branches (zig-zag arrows, D) ascend to anastomose with the meningohypophyseal trunk (arrowhead, D). The STA gives a zygomatico-orbital branch (double arrowheads, C), which anastomoses with the palpebral artery (not shown) and communicates with an enlarged ophthalmic artery (curved arrow). the following sequence: a grossly enlarged left ECA, right CCA, right subclavian artery, and an aberrant left subclavian artery arising from the right-sided descending aorta. The left ICA arose from the proximal left pulmonary artery but had a normal course above the thoracic outlet. An echocardiogram was performed to screen for cardiac defects but showed no such abnormalities. Conventional arch aortography confirmed the branching order and early retrograde flow down the left ICA to the left PA (Fig. 2). Selective angiography did not include the left ECA due to difficult catheterization. On right CCA injection (Fig. 3), flow crossed the anterior communicating artery and left the A1 segment to the left ICA with minimal M1 opacification. Right internal maxillary and ascending pharyngeal arteries intracranial branches ramified into dural anastomoses, crossing the midline to the left cavernous ICA. Massive supply from equivalent left-sided ECA branches was apparent from the axial imaging described above. Vertebral angiography showed some left posterior communicating artery supply to the left ICA; the left M1 segment of the MCA filled retrogradely via pial collaterals, predominantly from the temporal left posterior cerebral artery to MCA territories (Fig. 3). A synopsis of the imaging findings is illustrated in Figs. 4 and 5. Follow-Up. We discussed the long-term implications of this left-to-right shunt with the patient s parents. Given her minimal symptoms, they decided to avoid the immediate FIG. 2. Left: Arch aortography early arterial phase shows the order of branching of the major vessels. The origin of the first branch (enlarged left ECA [LECA], white arrowhead) overlaps the right CCA (RCCA) origin. The steep left anterior oblique projection view projects the descending aorta to the left. Arrow = pigtail catheter in the ascending aorta; * = right subclavian artery; LSUB = left subclavian artery; RVERT = right vertebral artery. Right: Slightly delayed phase from the same angiographic run shows retrograde filling of the left ICA (LICA) down to the origin of the left PA (arrowhead). Contrast opacifies the left PA (double arrowheads) and refluxes into the main pulmonary trunk. Note pigtail catheter in ascending aorta (arrow). 208
3 Isolated ICA from the pulmonary artery risks of shunt occlusion for now, and the child remains well to this time, 9 months after her initial presentation. FIG. 3. Left: Right common carotid angiography with left anterior oblique projection centered on the skull base. Reconstitution of the left ICA occurs through the anterior communicating artery and a tortuous left A1 segment (zig-zag arrow) as well as branches of the right anterior PA (double arrows) and internal maxillary artery (curved arrow) via the middle meningeal artery (arrowhead) and artery of the foramen rotundum (double arrowheads). Inferior hypophyseal arteries cross the midline to the left meningohypophyseal trunk (arrow). Right: Pial collaterals to the left MCA arise from the left anterior cerebral artery (arrowhead) and the left posterior cerebral artery territories (double arrows) are shown. There is delayed filling of the left M1 MCA with retrograde flow into the left ICA (arrow). Discussion Normal aortic arch development requires selective segmental regression of paired ventral and dorsal aortic segments and arches. Aortic branch isolation results from abnormal segmental regression both proximal and distal to its origin. Persistent ductus arteriosus patency enables communication with the PA (Fig. 6). The affected arteries are usually the more distal branches of the arch, such as the subclavian, innominate, and potentially the CCA if there is an associated aberrant subclavian artery. 7 Only 5 reports of the latter exist, including Fong and Venable s original 1987 paper. 2,3,5,6,8 All previously reported cases were left CCA isolations associated with right-sided aortic arches, and in all cases additional cardiovascular developmental anomalies were described including ostium primum defect, ostium secundum defect, left superior vena cava draining into the coronary sinus, and 2 cases of tetralogy of Fallot. During open surgery, Kaushik et al. 6 directly visualized a left CCA arising from the pulmonary trunk rather than the left PA, and the left ligamentum arteriosum was identified to be separate, intact, and in its normal location. The authors proposed that this anomaly was caused by truncoaortic sac FIG. 4. Left: Contrast-enhanced MR angiogram demonstrating right-sided aortic arch with ascending (arrow) and descending (arrowhead) aorta. The left ECA is the first branch from the arch (single arrowhead) and is similar in size to the ICAs. The left ICA (single arrow) passes down to the origin of the left PA (*). Other vessels shown: right vertebral artery (curved arrow) and CCA (double arrowheads). Right: Artist s illustration of right aotic arch anatomy and major vessels. Blood flow in the left ICA is retrograde to the left PA. L. Sub. = left subclavian artery; R. Sub. = right subclavian artery. 209
4 M. C. Hurley et al. FIG. 5. Illustration of the angiographically identified collaterals through circle of Willis and dural and pial anastomoses. A For. Rot. = artery of the foramen rotundum; Acc. Men. = accessory meningeal artery; ACOM = anterior communicating artery; Asc. Pha. A. = ascending pharyngeal artery; F* = foramina traversed by branches of the APA (hypoglossal canal, jugular foramen, foramen lacerum); FO = foramen ovale; FR = foramen rotundum; FS = foramen spinosum; ILT = inferolateral trunk; IMAX = internal maxillary artery; LECA = left external carotid artery; LMCA = left MCA; LPCA = left posterior cerebral artery; M. Men. = middle meningeal; MHT = meningohypophyseal trunk; O.A. = occipital artery; PCOM = posterior communicating artery; RICA = right ICA; RMCA = right MCA; RPCA = right posterior cerebral artery; STA = superficial temporal artery. malseptation, a disorder of neural crest migration rather than anomalous arch regression. 1,4 However, on careful assessment of our contrast-enhanced MR angiography source images, our isolated ICA origin can be traced to the left PA. Selective left ICA isolation additionally requires a separate left ECA origin from the arch, itself a rare consequence of anomalous arch regression. 1,7 Isolated ICA origin from the PA has not been reported previously. The late presentation in a relatively asymptomatic child and the lack of associated cardiac and genetic syndromes in our patient is also remarkable. Unlike previously described CCA-to-PA shunts receiving extracranial input via the ECA and carotid bifurcation, the anomalous ICA has no extracranial branches and obligates intracranial anastomoses from pathways including the circle of Willis (anterior and posterior communicating arteries), ECA meningeal anastomoses, and even retrograde left MCA flow with pial recruitment from neighboring cerebral terriories. Intracranial anastomotic recruitment increases the risk of acute shunt closure, particularly intracranial hemorrhage and cerebral edema. Propagation of the thrombus from the occlusion site into the intracranial ICA could result in thromboembolic complications. To avoid the complications of pulmonary hypertension, a controlled closure of the shunt would be desirable. This could be accomplished either surgically by graded ligature occlusion, or by endovascular staged stent-within-stent placement in the ICA over several months and coiling of any residual lumen. We would follow the impact of shunt occlusion with Doppler ultrasonography and MR angiogra- 210
5 Isolated ICA from the pulmonary artery FIG. 6. Left: Illustration of normal embryological evolution of the aortic arch and great vessels through programmed segmental regression (dotted lines) of the primitive arches (center inset: VA = ventral aorta; DA = dorsal aorta). The resulting order of branches is enumerated adjacent to their respective origins. Vestigial ligamentum arteriosum (LA) connects the PA to the aortic arch; the ligamentum caroticus (LC) (remnant of the primitive dorsal aorta between the third and fourth primitive arches) connects the ICA to the arch. Right: Illustration of the abnormal developmental pattern in our patient. White arrows point to sites of anomalous regression (* = sites responsible for causing isolation of the left ICA from the arch). Black arrows indicate segments with anomalous persistence. Note the patent ductus caroticus (PDC) and ductus arteriosum (PDA). The anomalous branching order is enumerated. SUB = subclavian artery. phy of the cervical CA, and through cerebral MR perfusion assessments. Conclusions This unique case of an isolated left ICA arising from the PA results from a combination of rare primitive aortic regression anomalies and presents phenotype-specific management issues. References 1. Bryan RN, Drewyer RG, Gee W: Separate origins of the left internal and external carotid arteries from the aorta. AJR Am J Roentgenol 130: , Fong L, Venables AW: Isolation of the left common carotid or left innominate artery. Br Heart J 57: , Ghalili K, Issenberg HJ, Freeman NJ, Brodman RF: Isolated left carotid artery in CHARGE association: diagnosis and repair. Ann Thorac Surg 50: , Horrowitz M, Bansal S, Dastur K: Aortic arch origin of the left external carotid artery and type II proatlantal fetal anastomosis. AJNR Am J Neuroradiol 24: , Huang SF, Wu MH: Left common carotid artery arising from the pulmonary artery in a patient with DiGeorge syndrome. Heart 76:82 83, Kaushik N, Saba Z, Rosenfeld H, Patel HT, Martin K, Reinhartz O, et al: An isolated left common carotid artery from the main pulmonary artery: possible malseptation of the truncoaortic sac. Pediatr Cardiol 26: , Moes CA, Freedom RM: Rare types of aortic arch anomalies. Pediatr Cardiol 14:93 101, Tozzi R, Hernanz-Schulman M, Kiley R, Genieser N, Ambrosino M, Pinto R, et al: Congenital pulmonary steal associated with Tetralogy of Fallot, right aortic arch and an isolated left carotid artery. Pediatr Radiol 19: , 1989 Manuscript submitted March 2, Accepted May 23, Sources of support: none reported. Address correspondence to: Ali Shaibani, M.D., Department of Radiology, Children s Memorial Hospital, 2300 Children s Plaza, Chicago, Illinois ashaibani@radiology.north western.edu. 211
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