Original Article Clinical characteristics of internal carotid artery aplasia
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1 Int J Clin Exp Med 2017;10(10): /ISSN: /IJCEM Original Article Clinical characteristics of internal carotid artery aplasia Jian-Jun Tang, Yong-Bo Zhao, You-Yu Lu, Guo-Dong Wang, Qing Zhang, Xiao-Lin Zhou, Xiang Shen, Xiao-Yan Song, Hai-Yan Lv, Qiao-Shu Wang, Yun-Cheng Wu Department of Neurology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, No.100, Haining Road, Shanghai , P.R. China Received March 31, 2017; Accepted August 4, 2017; Epub October 15, 2017; Published October 30, 2017 Abstract: The rarity of internal carotid artery aplasia (ICA) limits the research of this condition. As the endovascular treatment of cerebrovascular diseases is applied more and more widely, further understanding of ICA aplasia is important. We reviewed 4 consecutive internal carotid artery (ICA) aplasia patients admitted in our department between June 1, 2015 and December 31, The presentations were: ipsilateral hemisphere ischemic symptoms in 2 patients, headache in 1 patient, unfixed numbness in 1 patient and ischemic stroke in the contralateral middle cerebral artery (MCA) territory in 1 patient. Collateral channels to the ipsilateral hemisphere include the ophthalmic artery from the middle meningeal artery (MMA), the muscle branch from the ipsilateral vertebral artery (VA), anterior communicating arteries (ACOM), posterior communicating arteries (PCOM) and leptomeningeal arteries. Associated anomalies were: varied origins of common carotid artery (CCA) or VA, ipsilateral CCA hypoplasia, agenesis or aplasia of bone carotid cannels, hypoplasia of posterior cranial fossa, the extremely hypertrophic VA. MCA or anterior cerebral artery (ACA) aplasia was confirmed in 2 of 4 cases. Fusiform aneurysms were found in 2 cases. Distinguishing ICA aplasia, associated anomalies and collateral channels are important for preparing the endovascular treatment and surgery of head and neck. Keywords: Internal carotid artery, aplasia, cerebrovascular disease, collateral channel, angiography Introduction Internal carotid artery (ICA) aplasia, alternatively used with ICA hypoplasia or ICA agenesis, refers to the failure development of ICA. The rarity of this entity limited our understanding of this condition. Lie defined ICA agenesis as complete failure in ICA development, ICA aplasia as lack of development of ICA with its precursor once existed, and hypoplasia as incomplete development of the organ [1]. Case reports suggested intracranial arteriovenous malformations (AVMs), intracranial aneurysms as well as several types of collateral channels were associated with ICA aplasia [2-9]. We analyzed the medical records of 4 cases of ICA aplasia in order to prompt the understanding of this condition and improve the safety of endovascular treatment of cerebrovascular disease as well as head and neck surgery. Materials and methods Medical records of 4 cases of ICA aplasia consecutively admitted into our department be- tween June 1, 2015 and December 31, 2016 were reviewed and analyzed. This study was approved by the Institutional Review Board of our hospital and informed consents were obtained from all the research subjects. Results There were 2 males and 2 females summarized (Table 1). The age ranged from 30 to 53 years with the mean age of 43 years. Among the 4 cases, there was 1 case of ICA agenesis, 1 case of ICA aplasia and 2 cases of ICA hypoplasia according to Lie s theory [1]. Case 1 (Figure 1) complained of mild dizziness. Then computed tomography angiography (CTA) confirmed the absence of the whole left ICA. Case 2 (Figure 2) was admitted for ischemic stroke then the CTA occasionally found the hypoplastic ICA contralateral to the stroke foci, which was confirmed with angiography. Case 3 (Figure 3) was admitted for recurrent serious left headache and right weakness. Then digital subtraction angiography (DSA) revealed the left ICA aplasia. Case 4 (Figure 4) complained of unfixed nu-
2 Table 1. Clinical characteristics of 4 cases of ICA aplasia Case 1 Case 2 Case 3 Case 4 Sex Age Male Male Female Female ICA status Lt agenesis Rt hypoplasia Lt aplasia Lt hypoplasia Chief complain Dizzy Rt side Rt side weakness, slurred speaking, Lt side Unfixed numbness weakness,seizure headache Aortic arch Normal Lt CCA origins from brachiocephalic trunk Normal Lt VA origins from aotic arch Ipsilateral CCA Hypoplasia Normal Hypoplasia Hypoplasia Bone carotid canal Ipsilateral agenesis, contralateral Bilateral intact Ipsilateral hypoplasia, contralateral incomplete Bilateral intact intact bone wall Collateral channel ACOM, PCOM ACOM, PCOM Ophthalmic artery from MMA, leptomeningeal artery from Lt PCA, internal carotid artery remnant from vertebral artery branch ACOM, leptomeningeal artery from Lt ACA and Lt PCA Perfusion Mild delayed MMT and TTP NA NA Mild delayed MMT and TTP Aneurysm No No Ipsilateral MCA Ipsilateral ACA Other associated anomaly No No Hypertrophic VA, hypoplastic posterior cranial fossa and Lt cerebellum Hypoplastic ipsilateral MCA, hypertrophic ipsilateral ACA and PCA Atherosclerosis No No No No Ipsilateral stroke/tia No No Yes Yes Contralateral stroke No Yes No No Risk factors of stroke Tobacco use No Yes No No Alcohol degestion No No No No Hypertention No No Yes No Hyperlipidemia No No No No Diabetes No No No No Hyperhomocysteinemia No Yes No No Follow up duration 18 months 8 months 6 months 6 months 0utcome Stable Stable Stable Stable Notes: Lt: left; Rt: right; ICA: internal carotid artery; CCA: common carotid artery; VA: vertebral artery; ACOM: anterior communicating artery; PCOM: posterior communicating artery; MMA: middle meningeal artery; ACA: anterior cerebral artery; PCA: posterior cerebral artery; MTT: mean transit time; TTP: time to peak; NA: not available. TIA: transient ischemic attack Int J Clin Exp Med 2017;10(10):
3 Figure 1. Case 1: A 52 years old male patient with the symptom of dizzy. A. Cervical CTA suggested the absence of left ICA. B. Collateral channels via the ACOM and the PCOM. C. CTP suggested no significant abnormality. D. TBCT showed absence of ipsilateral CBC (rectangular arrow). mbness and magnetic resonance angiograph (MRA) revealed a fainted ICA, and the ICA hypoplasia was confirmed with DSA. In the 4 cases, lacunar infarction foci were found in 1 territory of 4 hypoplastic ICAs, in which case the MCA distal to the affected ICA was also aplastic. During the follow-up, no stroke happened in all 4 cases. Collateral channels In these 4 cases, collateral channels through anterior communicating arteries (ACOMs) were found in 3 cases (Figures 1, 2 and 4). Collateral channels through posterior communicating arteries (PCOMs) were found in 2 cases (Figures 1 and 2). An ophthalmic artery from the MMA Int J Clin Exp Med 2017;10(10):
4 Figure 2. Case 2: A 30 years old male patient with right side weakness and aphasia diagnosed as ischemic stroke in left MCA territory. A. Cervical CTA suggested the right ICA hypoplasia and the left CCA originated from the brachiocephalic trunk. B. Lateral projection of angiography revealed the right ICA ending as the ophthalmic artery. C, D. Angiography showed the collateral channels via the right PCA and the ACA, and one of the right MCA branches was blocked. (middle meningeal artery) as a collateral channel was confirmed in 1 case (Figure 3). Leptomeningeal arteries as collateral channels were documented in 2 cases (Figures 3 and 4). A rare collateral channel originating from the muscular branch of vertebral artery (VA) to the remnant of ICA was confirmed in 1 case with angiography (Figure 3). CT perfusion (CTP) completed in 2 cases and revealed almost normal cerebral blood flow (CBF) and cerebral blood volume (CBV) but slightly delayed mean transit time (MTT) and time to peak (TTP). Carotid bone canals In the patient with ICA agenesis, ipsilateral carotid bone canal (CBC) agenesis was confirmed with scull base CT (SBCT) scan. In the patient with ICA aplasia, ipsilateral CBC hypoplasia and incompletement of the contralateral CBC were confirmed with SBCT. In the 2 cases of ICA hypoplasia, the ipsilateral CBCs were both intact. Associated abnormalities Fusiform intracranial aneurysms were seen in 2 patients. No saccular aneurysms were found. Aortic variations were seen in 2 cases. Posterior cranial fossa hypoplasia was found in one patient with ICA aplasia. MCA hypoplasia and ACA hypoplasia were respectively confirmed in two patients. An extremely hypertrophic VA was confirmed in one patient with ICA aplasia. Discussion The incidence of ICA aplasia is less than 0.01% with the ratio between right:left:both being 1:3:1 [10]. Tode discovered carotid agenesis on postmortem examination in 1787 [11]. ICA aplasia can be associated with congenital combined pituitary hormone deficiency [12], neurofibromatosis [13, 14], intracranial aneurysms [2]. The mechanism of ICA aplasia is still to be determined. ICA develops at 4- to 5-mm embryonic stage and completes by 6 weeks of fetal life [15, 16]. The basilar artery is formed at the 7-12 mm stage of embryonic development and the circle of Willis is complete when the anterior communicating artery is formed at the 24 mm stage [17]. The skull base begins to form since the fifth or sixth week of fetal life [18]. Lie illustrated six types of collateral channels in ICA aplasia. Type A - Unilateral ICA aplasia with collateral circulation to the ipsilateral ACA through an ACOM and the collateral channel to the ipsilateral MCA through a PCOM, Type B - Unilateral ICA absence with the collateral channel to the ipsilateral hemisphere through an ACOM, Type C - Bilateral ICA agenesis with collateral channels to anterior circulation Int J Clin Exp Med 2017;10(10):
5 Figure 3. Case 3: A 53 years old female patient with recurrent left headache, intermittent right side weakness and slurred speech. A. Frontal projection of angiography showed the small caliber of the right CCA and the enlarged left VA. B. Lateral projection of left CCA angiography revealed one collateral channel through the ophthalmic artery from the MMA (hollow arrow). C. Lateral projection of left VA angiography revealed the remnant of ICA supported with a muscular branch of VA (black triangles) and a fusiform aneurysm of left MCA (star). D. CTA showed the absence of A1 segment of right ACA and a fusiform aneurysm of left MCA (star). E. CT of scull base revealed ipsilateral CBC aplasia, incompletement of bone wall (white arrow) of the contralateral CBC and hypoplasia of posterior fossa and left cerebellum (curved white arrow). through carotid-vertebrobasilar anastomoses and PCOMs, Type D - Unilateral cervical portion ICA agenesis with collateral flow through intercavernous communication from the contralateral ICA, Type E - Bilateral ICA hypoplasia with collateral channels through bilateral PCOMs, Type F - ICA hypoplasia with collateral flow through rete mirabile [1, 7]. Associated collateral channels may reflect the time and nature of ICA occlusion. If ICA absence happens before embryonic arteries regression, the embryonic vessels will become the collateral channels. On the contrary, if the ICA regresses after the regression of embryonic arteries, they can t be the collateral channel [19]. Supposed mechanism of unilateral ICA aplasia may be due to the mechanical stress such as exaggerated embryo folding and amniotic bands constriction [20]. In our case 3, the patient had a remnant of distal ICA while the initial segment was absent. Additionally, hypoplasia of the patient s posterior fossa and bilateral CBCs was documented. These appearances were consistent with the mechanical pressure theory. In case 4, the collateral channels mainly through leptomeningeal arteries suggested the blockage of ICA happened at a late embryonic stage. The coincidence of ICA hypoplasia and MCA hypoplasia on 1 patient is difficult to be explained with mechanical pressure. We proposed that the mechanism of thromboembolism at the terminal of the developed ICA at the fetal stage should be taken into account. CBCs develop depending upon the presence of ICAs at 5-6 weeks gestation. Absence of CBC indi Int J Clin Exp Med 2017;10(10):
6 Figure 4. Case 4: A 37 years old female patient with unfixed numbness. A. Aortic arch angiography showed the left VA originated from the arch and small caliber of left CCA. B. Left CCA angiography showed the hypoplastic ICA as well as the hypoplastic left MCA (long black arrow). C. MR revealed 2 lacunar infarction fuci in the ipsilateral hemisphere. D. CTP suggested slightly delayed TTP and MTT with CBF and CBV normal. E. A fusiform aneurysm was found at the ipsilateral ACA (curved black arrow). cates ICA agenesis [21]. If ICAs occlude after the scull base development, the CBCs will be normal. Otherwise the CBCs will be hypoplastic or absent. 2 of our 4 cases have normal CBCs, which suggests that their ICAs were once full developed. Whether the reduced blood flow may induce the atrophy of ICA is to be determined. In our case 3, we identified collateral channels through the remnant of ICA from the muscular branch of VA and the ophthalmic artery from the MMA which was documented in some case reports of intracranial aneurysms [22]. Two patients received CTP scan and the results suggested normal CBV and CBF, while MTT and TTP slightly delayed. Since ICA aplasia happened at the early stage of life, compensatory blood flow can be established well and special treatment is not necessary for ICA aplasia. However, the collateral channels may be more vulnerable as ageing and non-specific neurologic symptoms such as dizzy, headache or weakness may appear after middle age Int J Clin Exp Med 2017;10(10):
7 Prevalence of aneurysms reported in ICA aplasia patients was 24-67%, which is significantly higher than in general population, 2-4% [2, 21, 23]. Paschoal et al. reviewed patients of ICA hypoplasia and concomitant rete mirabile, and found the initial symptom was most frequently subarachnoid hemorrhage (SAH) (34.2%) [6]. Among the Lee et al. reported series of ICA aplasia, 3 out of 9 patients presented with SAH [2]. In our 4 cases, 2 unruptured fusiform aneurysms were found in 2 cases. No saccular aneurysms were found. The aneurysms seem to be related to increased blood flow and changed hemodymatics. No SAH was presented. Similar to the cases reported before, in 3 of our 4 cases, calibers of ipsilateral CCAs were significantly smaller than the contralateral ones. The diameter difference between bilateral CCAs may be used as an indication of ICA aplasia in future [3], which worth further research. Some cases of hypoplastic ICA should be differentiated from MOYAMOYA disease, which presented as stenosis or occlusion at the terminal of ICA with abnormal vascular network nearby [24]. It is important to distinguish the ICA aplasia from ICA acute occlusion when the guide wire goes through the blockage to treat ischemic stroke. In preparing for head and neck surgery, documenting the ICA aplasia and related collateral channels is of great significance. Since this is a small scale retrospective study, the mechanism of ICA aplasia and the risk of associated anomalies including intracranial artery aplasia and scull base hypoplasia need further research. Patients with ICA aplasia may have risks of hypoplasia of intracranial arteries, scull bases and cerebellums as well as intracranial aneurysms. In addition to mechanical oppression, ICA system thromboembolism in the early life stage should be taken into account when the mechanism is studied. It s important to detect the collateral channels and accompanied anomalies for surgery or endovascular therapy of head and neck in these patients. Disclosure of conflict of interest None. Address correspondence to: Drs. Yun-Cheng Wu and Qiao-Shu Wang, Department of Neurology, Shanghai General Hospital, Shanghai Jiao Tong University School of Medicine, No.100, Haining Road, Shanghai , P.R. China. Tel: ; Fax: ; yunchw@ medmail.com.cn (YCW); qiaoshuwang@gmail.com (QSW) References [1] TA L. Congenital anomalies of the carotid arteries. Excerpta Medica, Amsterdam 1968; 6. [2] Lee JH, Oh CW, Lee SH and Han DH. Aplasia of the internal carotid artery. Acta Neurochir (Wien) 2003; 145: ; discussion 125. [3] Kaya O, Yilmaz C, Gulek B, Soker G, Cikman G, Inan I and Demirduzen S. An important clue in the sonographic diagnosis of internal carotid artery agenesis: ipsilateral common carotid artery hypoplasia. Case Rep Radiol 2014; 2014: [4] Kim CH, Cho YD, Kang HS, Kim JE, Jung SC, Ahn JH and Han MH. Anomalous external carotid artery-internal carotid artery anastomosis in two patients with proximal internal carotid arterial remnants. Korean J Radiol 2015; 16: [5] Mohan D, Moisa H and Ciurea AV. Surgical difficulties in a case of left ophthalmic artery ruptured aneurysm associated with right ICA hypoplasia - case report. Chirurgia (Bucur) 2015; 110: [6] Paschoal EH, Yamaki VN, Junior FM, Piske RL, Teixeira MJ and Bor-Seng-Shu E. Carotid rete mirabile associated with subarachnoid hemorrhage from intracranial aneurysm: a case report and systematic review. Interv Neuroradiol 2015; 21: [7] Alurkar A, Karanam LS, Oak S and Kori S. Congenital absence of internal carotid artery with rare type of intercavernous anastamosis and ruptured cerebral aneurysm. J Clin Diagn Res 2016; 10: TD [8] Cruz ESV and Brito M. Bilateral absence of the internal carotid artery and basilar aneurysm. Br J Neurosurg 2016; 1-5. [9] Oz, II, Serifoglu I, Yazgan O and Erdem Z. Congenital absence of internal carotid artery with intercavernous anastomosis: Case report and systematic review of the literature. Interv Neuroradiol 2016; 22: [10] Florio F, Balzano S, Nardella M, Strizzi V, Cammisa M, Bozzini V, Catapano G and D Angelo V. Congenital absence of the internal carotid artery. Cardiovasc Intervent Radiol 1999; 22: [11] Midkiff RB, Boykin MW, McFarland DR and Bauman JA. Agenesis of the internal carotid artery with intercavernous anastomosis. AJNR Am J Neuroradiol 1995; 16: Int J Clin Exp Med 2017;10(10):
8 [12] Lamine F, Kanoun F, Chihaoui M, Saveanu A, Menif E, Barlier A, Enjalbert A, Brue T and Slimane H. Unilateral agenesis of internal carotid artery associated with congenital combined pituitary hormone deficiency and pituitary stalk interruption without HESX1, LHX4 or OTX2 mutation: a case report. Pituitary 2012; 15 Suppl 1: S [13] Wali AR, Santiago-Dieppa DR, Steinberg JA, Alattar A, Cheung VJ, Modir R, Khalessi AA and Pannell JS. Hypoplastic internal carotid artery co-presenting with neurofibromatosis and intracranial masses. Cureus 2016; 8: e750. [14] Ohta H, Hashimoto M, Urasaki E and Yokota A. [Hypoplasia of internal carotid artery at cervical portion associated with neurofibromatosis type I]. No To Shinkei 2002; 54: [15] Czarnecki EJ, Silbergleit R, Mehta BA and Sanders WP. Absence of the supraclinoid internal carotid artery in association with intracranial aneurysms. Neuroradiology 1998; 40: [16] DH P. The development of the cranial arteries in the human embryo. Contrib Embryol 1948; 32: 56. [17] Worthington C, Olivier A and Melanson D. Internal carotid artery agenesis: correlation by conventional and digital subtraction angiography, and by computed tomography. Surg Neurol 1984; 22: [18] Quint DJ, Silbergleit R, Young WC. Absence of the carotid canals at skull base CT. Radiology 1992; 182: 5. [19] Sahin H, Cinar C and Oran I. Carotid and vertebrobasilar rete mirabile: a case report. Surg Radiol Anat 2010; 32: [20] Given CA 2nd, Huang-Hellinger F, Baker MD, Chepuri NB and Morris PP. Congenital absence of the internal carotid artery: case reports and review of the collateral circulation. AJNR Am J Neuroradiol 2001; 22: [21] Quint DJ, Boulos RS and Spera TD. Congenital absence of the cervical and petrous internal carotid artery with intercavernous anastomosis. AJNR Am J Neuroradiol 1989; 10: [22] Yi Z, Sasaki T, Satoh D, Muruta T, Kitazawa K and Kobayashi S. Carotid-anterior cerebral artery anastomosis associated with paraclinoid aneurysm and ophthalmic artery originating from middle meningeal artery: case report and consideration of terminology. World Neurosurg 2016; 88: 689 e [23] Afifi AK, Godersky JC, Menezes A, Smoker WR, Bell WE and Jacoby CG. Cerebral hemiatrophy, hypoplasia of internal carotid artery, and intracranial aneurysm. A rare association occurring in an infant. Arch Neurol 1987; 44: [24] M F. Guidelines for the diagnosis and treatment of spontaneous occlusion of the circle of Willis ( moyamoya disease). Clin Neurol Neurosurg 1997; 99: Int J Clin Exp Med 2017;10(10):
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