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Persistent hypoglossal artery associated with arteriovenous malformation: a case report
European Journal of Radiology 33 (2000) 59 – 62 www.elsevier.nl/locate/ejrad
Case report
Persistent hypoglossal artery associated with arteriovenous malformation: a case report Chikako Nishida *, Ryuichiro Ashikaga, Yutaka Araki, Kiyoshi Nakamatsu, Yukihiko Ono, Kouichi Fujii, Yasumasa Nishimura Department of Radiology, Kinki Uni6ersity School of Medicine, 377 -2, Ohno-Higashi, Osaka-Sayama, Osaka 589 -8511, Japan Received 16 December 1998; accepted 26 March 1999
Abstract A rare case of persistent hypoglossal artery in conjunction with arteriovenous malformation was presented. MRA could delineate persistent hypoglossal artery and arteriovenous malformation very clearly. The patient suffered from intracranial hemorrhage from in the 37th week of pregnancy. MRI, MRA, angiography, and CT of this rare condition are reported. © 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Persistent hypoglossal artery; Arteriovenous malformation; MRA; MRI
1. Case report A 30-year-old woman in the 37th week of pregnancy was admitted to our hospital because of sudden onset of a severe headache on October 16, 1994. As a past history, she experienced operation of patent ductus arteriosus at 5-years of age. On admission, she showed loss of consciousness and the right hemiplagia. CT revealed intracranial hemorrhage in the right temporal region (Fig. 1). The right internal carotid angiograms showed the persistent hypoglossal artery originating from the right internal carotid artery at the level of the third cervical vertebra (Fig. 2a). The arteriovenous malformation was located in the distal portion of the right middle cerebral artery (Fig. 2a). The selective persistent hypoglossal artery angiogram showed that the persistent hypoglossal artery fed the basilar artery and the left middle cerebral artery via the left posterior communicating artery (Fig. 2b). The right vertebral artery was not seen at the right subclavian angiogram. The left common carotid angiogram demonstrated the * Corresponding author. Tel.: +81-723-675173; fax: + 81-723682388. E-mail address: radiol@med. kindai. ac. jp (C. Nishida)
hypoplastic left internal carotid artery, which was severely stenosed at the entrance of the carotid siphon. In addition, the left vertebral artery was also hypoplastic. Thus, the persistent hypoglossal artery was the only artery feeding the basilar artery. MRA also could show the persistent hypoglossal artery originating from the right internal carotid artery as shown on angiography (Fig. 3). A source image of MRA showed that the right persistent hypoglossal artery ran through the right hypoglossal canal (Fig. 4). Intracranial hemorrhage was considered to be due to rupture of the arteriovenous malformation. Four days after onset, she gave birth by Cesarean section, giving her a healthy baby. After Cesarean section, the cerebral hematoma was removed. One week after the onset, arteriovenous malformation was resected during the operation following transcatheter embolization of the arteriovenous malformation.
2. Discussion The first description of persistent hypoglossal artery was reported by Batujeff in 1889 [1], and the first angiographic demonstration of persistent hypoglossal
0720-048X/99/$ - see front matter © 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 7 2 0 - 0 4 8 X ( 9 9 ) 0 0 0 5 8 - 3
60
C. Nishida et al. / European Journal of Radiology 33 (2000) 59–62
artery was presented by Begg in 1961 [2]. Persistent hypoglossal artery is occurring in less than 0.5% of routine cerebral angiography [3]. There was no significant sex predominance. The age at diagnosis ranged mainly in between 20 and 40-years-old [4]. In most instance, the persistent hypoglossal artery were incidentally discovered by cerebral angiography [5]. The embryological origin was precisely described by Padget in 1948 [6]. In a 4-mm human embryo, the internal carotid artery is anastomosed with the longitudinal neural artery, which later becomes the basilar artery, by four vessels; the trigeminal, optic, hypoglossal, and proatlantal intersegmental arteries. As the posterior communicating artery develops, these primitive anastomotic vessels disappear in between 5–6 mm and 7–12 mm human embryo. Thus the normal life span of the hypoglossal artery is thought less than 1 week [8]. However, they rarely persist and become anomalies of the carotid-basilar anastomosis at birth. Lie proposed the anatomical diagnostic criteria of persistent hypoglossal artery [7]: (a) It arises as a robust branch of the cervical internal carotid artery at the first cervical vertebra to third cervical vertebra level, (b) It proceeds in a tortuous fashion through the Fig. 1. Precontrast CT scan demonstrates cerebral bleeding in the right temporal lobe, ruptured into bilateral lateral ventricles.
Fig. 2. (a) Right internal carotid angiogram on antero-posterior view shows the right temporal arteriovenous malformation fed by the right middle cerebral artery. The persistent hypoglossal artery (arrow) arises from the internal carotid artery at level of third cervical vertebra. (b) Selective persistent hypoglossal angiogram on antero-posterior view reveals that persistent hypoglossal artery originates from the right internal carotid artery at level of third cervical vertebra and feeds the left middle cerebral artery via the posterior communicating artery.
C. Nishida et al. / European Journal of Radiology 33 (2000) 59–62
61
Fig. 3. MRA demonstrates persistent hypoglossal artery (arrow) arises from the internal carotid artery and ending at the left middle cerebral artery. The left internal carotid artery is hypoplastic(arrow head).
anterior condyloid foramen (the hypoglossal canal) to the posterior cranial fossa, (c) The basilar artery is seen only beyond the point of anastomosis with the hypoglossal artery, (d) The posterior communicating arteries are not visible arteriographically. In the present case, the persistent hypoglossal artery arises from the internal carotid artery at level of second cervical vertebra. Persistent hypoglossal artery runs through the hypoglossal canal. The basilar artery is seen only beyond the point of anastomosis with the hypoglossal artery. The posterior communicating arteries are visible. The present case met three of the four criteria of persistent hypoglossal artery. Later, Brismar revised these criteria of persistent hypoglossal artery in 1976 when he reported a case of persistent hypoglossal artery in which a well-developed posterior communicating artery was found [8]. He suggested that only the first two anatomic criteria (a, b) could reliably identify the anomalous hypoglossal artery. Karasawa reported the first case of persistent hypoglossal artery associated with arteriovenous malformation in 1973 [11]. Only six cases of persistent hypoglossal artery with arteriovenous malformation, to our knowledge, have been reported since then [4,5,9–12]. Yamanaka et al., described that the incidence of arteriovenous malformation in patients was 3.0% [12]. Among the six patients reported, five patients suffered severe headache because of cerebral hemorrhage from arteriovenous malformation. In the remaining one case, initial symptom of the patient was epilepsy. As the etiology of the combination of persistent hypoglossal artery and arteriovenous malformation, Shibata et al. suggested that arteriovenous
Fig. 4. An axial MRI shows that the persistent hypoglossal artery runs through the hypoglossal canal (arrow).
malformation may disturb the regression of the carotid-basilar anastomosis because the arteriovenous malformation requires a high blood flow [4]. Intracranial hemorrhage from arteriovenous malformation occurred during pregnancy in the present case. The occurrence rate of bleeding from arteriovenous malformation raised up to 87% during pregnancy [13]. On the other hand, there are reports that pregnancy dose not increase the rate of first cerebral hemorrhage from arteriovenous malformation [14,15]. In addition, the present case was also associated with patent ductus arteriosus. To our best knowledge, there is no report the association of persistent hypoglossal artery with patent ductus arteriosus. In conclusion, the persistent hypoglossal artery is an unusual feature, but its preoperative recognition is necessary in order to minimize neurological deficits during carotid surgery [16]. Because MRI and MRA were very safe to perform without any contrast medium, we therefore think MRA and MRI are the modality of choice in the diagnosis of persistent hypoglossal artery. MRA and MRI were enough to detect the persistent hypoglossal artery in the present case.
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C. Nishida et al. / European Journal of Radiology 33 (2000) 59–62
References [1] Batujeff N. Eine seltene Arterienanomalie. Anat Anz 1889;4:282 – 5. [2] Begg AC. Radiographic demonstration of the hypoglossal artery. A rare type of persistent anomalous carotid-basilar anastomosis. Clin Radiol 1961;12:187–9. [3] Ouriel K, Green RM, DeWeese JA. Anomalous carotid-basilar anastomoses in cerebrovascular surgery. J Vasc Surg 1988;7:774 – 7. [4] Shibata Y, Hyodo A, Saito A, Yoshii Y, Nose T. Large arteriovenous malformation associated with persistent primitive hypoglossal artery: case report. Neurol Med Chir 1991;31:804 – 8. [5] Garza MR, Cavazos E, Urrutia G. Persistent hypoglossal artery in combination with multifocal arteriovenous malformations of the brain: case report. Neurosurgery 1990;26:871–6. [6] Padget DH. The development of the cranial arteries in the human embryo. Contr Embryol Carneg Inst 1948;205:212 – 32. [7] Lie TA. Congenital abnormalities of the carotid arteries. Amsterdam. Excerpta Medica: 1968: 76–83. [8] Brismar J. Persistent hypoglossal artery, diagnostic criteria. Acta Radiol Diag 1976;17:160–6. [9] Karasawa J, Kikuchi H, Furuse S, Kawai S, Uchida Y, Sakai T.
.
[10] [11]
[12]
[13] [14]
[15]
[16]
Studies on 2 cases of a persistent primitive hypoglossal artery: case reports on a 9-year-old male patient with arteriovenous malformation and a 55-year-old male patient with brain stem syndrome. Brain Nerve (No To Shinkei) 1973;24:91 – 8. Stanley OS. Unilateral sudden hearing loss as a result of anomalous carotid anatomy. J Vascular Surg 1990;12:341 – 4. Yamanaka K, Noguchi K, Hayasaki K, Matsuoka Y. Persistent primitive hypoglossal artery associated with arteriovenous malformation: case report. Neurol Med Chir 1990;30:949 –55. Sahoo Y, Mathai KV, Mallikarjunaiah GS, David BS, Parida S. Persistent hypoglossal artery. Indian J Radiol Imag 1988;42:144 – 6. Robinson JL, Hall CS, Sedzimir CB. Arteriovenous malformations, aneurysms, and pregnancy. J Neurosurg 1974;41:63–70. Horton JC, Chambers WA, Lyons SL, Adams RD, Kiellberg RN. Pregnancy and the risk of hemorrhage from cerebral arteriovenous malformation. Neurosurgery 1990;27:867 – 71. Fujita K, Tsunoda H, Shigemitsu S, Kubo T. Clinical study on the intracranial arteriovenous malformation associated with pregnancy. Acta Obstet Gynaecol Jap 1995;47(12):1359–64. Cartier R. Combined endarterectomy of the internal carotid artery and persistent hypoglossal artery: an unusual case of carotid revascularization. Can J Surg 1996;39(2):159– 62.
Case report
Persistent hypoglossal artery associated with arteriovenous malformation: a case report Chikako Nishida *, Ryuichiro Ashikaga, Yutaka Araki, Kiyoshi Nakamatsu, Yukihiko Ono, Kouichi Fujii, Yasumasa Nishimura Department of Radiology, Kinki Uni6ersity School of Medicine, 377 -2, Ohno-Higashi, Osaka-Sayama, Osaka 589 -8511, Japan Received 16 December 1998; accepted 26 March 1999
Abstract A rare case of persistent hypoglossal artery in conjunction with arteriovenous malformation was presented. MRA could delineate persistent hypoglossal artery and arteriovenous malformation very clearly. The patient suffered from intracranial hemorrhage from in the 37th week of pregnancy. MRI, MRA, angiography, and CT of this rare condition are reported. © 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Persistent hypoglossal artery; Arteriovenous malformation; MRA; MRI
1. Case report A 30-year-old woman in the 37th week of pregnancy was admitted to our hospital because of sudden onset of a severe headache on October 16, 1994. As a past history, she experienced operation of patent ductus arteriosus at 5-years of age. On admission, she showed loss of consciousness and the right hemiplagia. CT revealed intracranial hemorrhage in the right temporal region (Fig. 1). The right internal carotid angiograms showed the persistent hypoglossal artery originating from the right internal carotid artery at the level of the third cervical vertebra (Fig. 2a). The arteriovenous malformation was located in the distal portion of the right middle cerebral artery (Fig. 2a). The selective persistent hypoglossal artery angiogram showed that the persistent hypoglossal artery fed the basilar artery and the left middle cerebral artery via the left posterior communicating artery (Fig. 2b). The right vertebral artery was not seen at the right subclavian angiogram. The left common carotid angiogram demonstrated the * Corresponding author. Tel.: +81-723-675173; fax: + 81-723682388. E-mail address: radiol@med. kindai. ac. jp (C. Nishida)
hypoplastic left internal carotid artery, which was severely stenosed at the entrance of the carotid siphon. In addition, the left vertebral artery was also hypoplastic. Thus, the persistent hypoglossal artery was the only artery feeding the basilar artery. MRA also could show the persistent hypoglossal artery originating from the right internal carotid artery as shown on angiography (Fig. 3). A source image of MRA showed that the right persistent hypoglossal artery ran through the right hypoglossal canal (Fig. 4). Intracranial hemorrhage was considered to be due to rupture of the arteriovenous malformation. Four days after onset, she gave birth by Cesarean section, giving her a healthy baby. After Cesarean section, the cerebral hematoma was removed. One week after the onset, arteriovenous malformation was resected during the operation following transcatheter embolization of the arteriovenous malformation.
2. Discussion The first description of persistent hypoglossal artery was reported by Batujeff in 1889 [1], and the first angiographic demonstration of persistent hypoglossal
0720-048X/99/$ - see front matter © 2000 Elsevier Science Ireland Ltd. All rights reserved. PII: S 0 7 2 0 - 0 4 8 X ( 9 9 ) 0 0 0 5 8 - 3
60
C. Nishida et al. / European Journal of Radiology 33 (2000) 59–62
artery was presented by Begg in 1961 [2]. Persistent hypoglossal artery is occurring in less than 0.5% of routine cerebral angiography [3]. There was no significant sex predominance. The age at diagnosis ranged mainly in between 20 and 40-years-old [4]. In most instance, the persistent hypoglossal artery were incidentally discovered by cerebral angiography [5]. The embryological origin was precisely described by Padget in 1948 [6]. In a 4-mm human embryo, the internal carotid artery is anastomosed with the longitudinal neural artery, which later becomes the basilar artery, by four vessels; the trigeminal, optic, hypoglossal, and proatlantal intersegmental arteries. As the posterior communicating artery develops, these primitive anastomotic vessels disappear in between 5–6 mm and 7–12 mm human embryo. Thus the normal life span of the hypoglossal artery is thought less than 1 week [8]. However, they rarely persist and become anomalies of the carotid-basilar anastomosis at birth. Lie proposed the anatomical diagnostic criteria of persistent hypoglossal artery [7]: (a) It arises as a robust branch of the cervical internal carotid artery at the first cervical vertebra to third cervical vertebra level, (b) It proceeds in a tortuous fashion through the Fig. 1. Precontrast CT scan demonstrates cerebral bleeding in the right temporal lobe, ruptured into bilateral lateral ventricles.
Fig. 2. (a) Right internal carotid angiogram on antero-posterior view shows the right temporal arteriovenous malformation fed by the right middle cerebral artery. The persistent hypoglossal artery (arrow) arises from the internal carotid artery at level of third cervical vertebra. (b) Selective persistent hypoglossal angiogram on antero-posterior view reveals that persistent hypoglossal artery originates from the right internal carotid artery at level of third cervical vertebra and feeds the left middle cerebral artery via the posterior communicating artery.
C. Nishida et al. / European Journal of Radiology 33 (2000) 59–62
61
Fig. 3. MRA demonstrates persistent hypoglossal artery (arrow) arises from the internal carotid artery and ending at the left middle cerebral artery. The left internal carotid artery is hypoplastic(arrow head).
anterior condyloid foramen (the hypoglossal canal) to the posterior cranial fossa, (c) The basilar artery is seen only beyond the point of anastomosis with the hypoglossal artery, (d) The posterior communicating arteries are not visible arteriographically. In the present case, the persistent hypoglossal artery arises from the internal carotid artery at level of second cervical vertebra. Persistent hypoglossal artery runs through the hypoglossal canal. The basilar artery is seen only beyond the point of anastomosis with the hypoglossal artery. The posterior communicating arteries are visible. The present case met three of the four criteria of persistent hypoglossal artery. Later, Brismar revised these criteria of persistent hypoglossal artery in 1976 when he reported a case of persistent hypoglossal artery in which a well-developed posterior communicating artery was found [8]. He suggested that only the first two anatomic criteria (a, b) could reliably identify the anomalous hypoglossal artery. Karasawa reported the first case of persistent hypoglossal artery associated with arteriovenous malformation in 1973 [11]. Only six cases of persistent hypoglossal artery with arteriovenous malformation, to our knowledge, have been reported since then [4,5,9–12]. Yamanaka et al., described that the incidence of arteriovenous malformation in patients was 3.0% [12]. Among the six patients reported, five patients suffered severe headache because of cerebral hemorrhage from arteriovenous malformation. In the remaining one case, initial symptom of the patient was epilepsy. As the etiology of the combination of persistent hypoglossal artery and arteriovenous malformation, Shibata et al. suggested that arteriovenous
Fig. 4. An axial MRI shows that the persistent hypoglossal artery runs through the hypoglossal canal (arrow).
malformation may disturb the regression of the carotid-basilar anastomosis because the arteriovenous malformation requires a high blood flow [4]. Intracranial hemorrhage from arteriovenous malformation occurred during pregnancy in the present case. The occurrence rate of bleeding from arteriovenous malformation raised up to 87% during pregnancy [13]. On the other hand, there are reports that pregnancy dose not increase the rate of first cerebral hemorrhage from arteriovenous malformation [14,15]. In addition, the present case was also associated with patent ductus arteriosus. To our best knowledge, there is no report the association of persistent hypoglossal artery with patent ductus arteriosus. In conclusion, the persistent hypoglossal artery is an unusual feature, but its preoperative recognition is necessary in order to minimize neurological deficits during carotid surgery [16]. Because MRI and MRA were very safe to perform without any contrast medium, we therefore think MRA and MRI are the modality of choice in the diagnosis of persistent hypoglossal artery. MRA and MRI were enough to detect the persistent hypoglossal artery in the present case.
62
C. Nishida et al. / European Journal of Radiology 33 (2000) 59–62
References [1] Batujeff N. Eine seltene Arterienanomalie. Anat Anz 1889;4:282 – 5. [2] Begg AC. Radiographic demonstration of the hypoglossal artery. A rare type of persistent anomalous carotid-basilar anastomosis. Clin Radiol 1961;12:187–9. [3] Ouriel K, Green RM, DeWeese JA. Anomalous carotid-basilar anastomoses in cerebrovascular surgery. J Vasc Surg 1988;7:774 – 7. [4] Shibata Y, Hyodo A, Saito A, Yoshii Y, Nose T. Large arteriovenous malformation associated with persistent primitive hypoglossal artery: case report. Neurol Med Chir 1991;31:804 – 8. [5] Garza MR, Cavazos E, Urrutia G. Persistent hypoglossal artery in combination with multifocal arteriovenous malformations of the brain: case report. Neurosurgery 1990;26:871–6. [6] Padget DH. The development of the cranial arteries in the human embryo. Contr Embryol Carneg Inst 1948;205:212 – 32. [7] Lie TA. Congenital abnormalities of the carotid arteries. Amsterdam. Excerpta Medica: 1968: 76–83. [8] Brismar J. Persistent hypoglossal artery, diagnostic criteria. Acta Radiol Diag 1976;17:160–6. [9] Karasawa J, Kikuchi H, Furuse S, Kawai S, Uchida Y, Sakai T.
.
[10] [11]
[12]
[13] [14]
[15]
[16]
Studies on 2 cases of a persistent primitive hypoglossal artery: case reports on a 9-year-old male patient with arteriovenous malformation and a 55-year-old male patient with brain stem syndrome. Brain Nerve (No To Shinkei) 1973;24:91 – 8. Stanley OS. Unilateral sudden hearing loss as a result of anomalous carotid anatomy. J Vascular Surg 1990;12:341 – 4. Yamanaka K, Noguchi K, Hayasaki K, Matsuoka Y. Persistent primitive hypoglossal artery associated with arteriovenous malformation: case report. Neurol Med Chir 1990;30:949 –55. Sahoo Y, Mathai KV, Mallikarjunaiah GS, David BS, Parida S. Persistent hypoglossal artery. Indian J Radiol Imag 1988;42:144 – 6. Robinson JL, Hall CS, Sedzimir CB. Arteriovenous malformations, aneurysms, and pregnancy. J Neurosurg 1974;41:63–70. Horton JC, Chambers WA, Lyons SL, Adams RD, Kiellberg RN. Pregnancy and the risk of hemorrhage from cerebral arteriovenous malformation. Neurosurgery 1990;27:867 – 71. Fujita K, Tsunoda H, Shigemitsu S, Kubo T. Clinical study on the intracranial arteriovenous malformation associated with pregnancy. Acta Obstet Gynaecol Jap 1995;47(12):1359–64. Cartier R. Combined endarterectomy of the internal carotid artery and persistent hypoglossal artery: an unusual case of carotid revascularization. Can J Surg 1996;39(2):159– 62.