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persistent trigeminal artery variant and coexisting variants of the head and neck vessels diagnosed using 3 T MRA
Clinical Radiology 68 (2013) e578ee585
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Persistent trigeminal artery/persistent trigeminal artery variant and coexisting variants of the head and neck vessels diagnosed using 3 T MRA M. Bai a, *, Q. Guo b, S. Li a a
Department of Radiology, Liaocheng People’s Hospital and Liaocheng Clinical School of Taishan Medical University, Liaocheng, Shandong, PR China b Department of Neurosurgery, Liaocheng People’s Hospital and Liaocheng Clinical School of Taishan Medical University, Liaocheng, Shandong, PR China
article in formation Article history: Received 10 March 2013 Received in revised form 9 May 2013 Accepted 29 May 2013
AIM: To report the prevalence and characteristic features of persistent trigeminal artery (PTA), PTA variant (PTAV), and other variants of the head and neck vessels, identified using magnetic resonance angiography (MRA). MATERIALS AND METHODS: The three-dimensional (3D) time of flight (TOF) MRA and 3D contrast-enhanced (CE) MRA images of 6095 consecutive patients who underwent 3 T MRA at Liaocheng People’s Hospital from 1 September 2008 through 31 May 2012 were retrospectively reviewed and analysed. Thirty-two patients were excluded because of suboptimal image quality or internal carotid artery (ICA) occlusion. RESULTS: The prevalence of both PTA and PTAV was 0.63% (PTA, 26 cases; PTAV, 12 cases). The prevalence of coexisting variants of the head and neck vessels in cases of PTA/PTAV was 52.6% (20 of 38 cases). The vascular variants that coexisted with cases of PTA/PTAV were as follows: the intracranial arteries varied in 10 cases, the origin of the supra-aortic arteries varied in nine cases, the vertebral artery (VA) varied in 14 cases, and six cases displayed fenestrations. Fifteen of the 20 cases contained more than two types of variants. CONCLUSION: The prevalence of both PTA and PTAV was 0.63%. Although PTA and PTAV are rare vascular variants, they frequently coexist with other variants of the head and neck vessels. Multiple vascular variations can coexist in a single patient. Recognizing PTA, PTAV, and other variants of the head and neck vessels is crucial when planning a neuroradiological intervention or surgery. Recognizing the medial PTA is very important in clinical practice when performing trans-sphenoidal surgery on the pituitary as failure to do so could result in massive haemorrhage. Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Carotidevertebrobasilar anastomoses include the persistent primitive trigeminal artery (PPTA), the persistent * Guarantor and correspondent: M. Bai, Department of Radiology, Liaocheng People’s Hospital, Dongchang West Road 67, Liaocheng, Shandong Province 252000, PR China. Tel.: þ86 13563588802. E-mail address: [email protected] (M. Bai).
primitive otic artery, the persistent primitive hypoglossal artery, and the persistent primitive pro-atlantal artery. These anastomoses, which are named according to their associated anatomy, link the primitive internal carotid artery (ICA) and basilar artery (BA) systems, and exist in early foetal life (4e5 mm embryonic stage).1 As the vascular system evolves, they are quickly remodelled, with the trigeminal artery being the last to disappear (7e14 mm embryonic stage).1 Rarely, the anastomoses persist into adulthood.
0009-9260/$ e see front matter Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2013.05.099
M. Bai et al. / Clinical Radiology 68 (2013) e578ee585
Persistent trigeminal artery (PTA) is the most common remnant of embryonic communication between the ICA and the vertebrobasilar system. The PTA originates from the cavernous segment of the ICA and communicates with the BA. The angiographic anatomy and classification of PTAs were first described by Saltzman and Wollschlaeger.2 In Saltzman type 1 PTA, the PTA supplies the BA, posterior cerebral arteries (PCA), and superior cerebellar arteries (SCAs). Segments of the BA proximal to the insertion of the PTA may be hypoplastic and the posterior communicating artery (PComA) may be absent. In Saltzman type 2 PTA, the PTA joins the BA below the origin of the SCA, and the PCA receives its blood supply predominantly through the patent PComA. PTA is also divided into two types, depending on where in the cavernous ICA the artery originates: lateral PTA originates in the posterolateral aspect, whereas medial PTA originates in the posteromedial aspect. Direct anastomoses between the precavernous portion of the ICA and the cerebellar arteries, without interposition of the BA, are described as PTA variants (PTAV).3e5 Cases in which the anomalous artery arises from the ICA and joins the ipsilateral SCA or the BA have been named “PTAV type A,” whereas those in which the anomalous artery arises from the ICA and joins the ipsilateral SCA have been named “PTAV type B”.6 The reported incidence of PTA/PTAV is about 0.2e0.76%.4e7 Numerous anatomical and embryological studies of PTA and PTAV have been reported.4e8 Several previous studies have shown that PTA often coexists with aortic arch anomalies and variation of the intracranial vasculature, the VA, and the carotid artery.3,5,6,8e11 Being aware of these variations is crucial for interpreting the findings of magnetic resonance angiography (MRA), because they can influence surgical and interventional procedures. Three-dimensional (3D) time of flight (TOF) MRA of the supra-aortic arteries has been used as a non-invasive, safe, and fast method for evaluating the vasculature of the head and neck. The purpose of the present study was to describe the prevalence and characteristic features of PTA/PTAV and coexisting variants of the head and neck vessels identified using MRA at 3 T.
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Materials and methods Patients Using either a picture archiving and communication system (PACS) or the Aquarius workstation (TeraRecon, Foster City, CA, USA), the findings of 3D TOF MRA and contrast-enhanced (CE) MRA examinations of the head and neck vessels of 6095 consecutive Chinese patients who had or were suspected of having an ischaemic cerebrovascular disease on physical examination were retrospectively reviewed. The examinations were carried out from 1 September 2008 to 31 May 2012. After excluding 32 patients whose images were of suboptimal quality or showed ICA occlusion, the images of 6063 patients were ultimately reviewed and analysed. The mean age of the patients was 64 years, and the range was 15e75 years. Fifteen of the 38 patients with PTA or PTAV were men; 23 were women. Patients were both asymptomatic and symptomatic. The reported symptoms included dizziness, headache, vomiting, asthenia, hemiparalysis, and trigeminal neuralgia. This study was approved by the institutional review board of Liaocheng People’s Hospital.
MRA All MRA imaging was performed using a 3 T scanner (Achieva; Philips Medical Systems, The Netherlands) using a 16-channel sensitivity-encoding head and neck coil and a strong gradient system (maximal gradient amplitude, 80 mT/m; slew rate, 150 T/m/s). For 3D TOF MRA, a 3D fast-field echo sequence with a multichunk technique was used. The imaging parameters of the head, neck, and supra-aortic arch are shown in Table 1. The total acquisition time was 11 min, 39 s. The original 3D TOF MRA images of the head, neck, and supra-aortic arteries were scanned, and then analysed with a maximum-intensity projection (MIP) post-processing algorithm. The separate images of the head, neck, and supra-aortic arteries were fused using MobiView software (Philips Healthcare, USA) to create one image that extended from the top of the head to the aortic arch. All images were of diagnostic quality.
Table 1 Sequence parameters of three-dimensional time of flight magnetic resonance angiography. Parameter
Head
Neck
Supra-aortic arch
Repetition time (ms) Echo time (ms) Field of view (mm mm mm) Flip angle ( ) Matrix Voxel size (mm mm mm) Sections Section thickness (cm) Gap (cm) Chunks SENSE factor Acquisition time
15 3.5 220 191 96 18 368 40 0.6 1.0 0.6 160 2 1 5 2 2 min, 52 s
20 3.5 160 129 135 20 260 84 0.85 0.52 0.75 180 2 1 6 3 2 min, 24 s
22 3.5 250 238 96 22 252 142 1.0 1.6 0.8 120 1 1 5 2 4 min, 48 s
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For 3D CE MRA, an electronic power injector (Spectris Solaris EP, MEDRAD, USA) was used to inject the contrast material. The contrast agent injection protocol specified 0.2 mmol gadodiamide per kilogram body weight administered at a flow rate of 1.5 ml/s, followed by 20 ml saline at the same rate. Subsequently, high-spatial-resolution CE MRA was performed in the coronal plane using a fast sequence.
Image analysis The MRA images were reviewed by one experienced radiologist using either the PACS or the Aquarius workstation. Partial MIP and volume rendering (VR) were used to visualize the head and neck vessel variants.
Results Among the 6063 patients, 26 cases of PTA (10 men, 16 women; 0.43% prevalence) were identified. Right PTA was more common than left PTA (right PTA, 15 cases; left PTA, nine cases). Twelve cases of PTAV (five men, seven women; 0.2% prevalence) were also identified. The prevalence of both PTA and PTAV was 0.63%. The ratio of men with PTA/ PTAV to women with PTA/PTAV was 1:1.5. Twenty-three cases of PTA were lateral types (Fig 1; 88.5% prevalence); three cases were medial types (Fig 2; 11.5% prevalence). Nine cases of PTAV were type A (Fig 3; 75% prevalence) and three cases were type B (Fig 4; 25% prevalence). As described in Table 2, 20 cases of PTA/PTAV (52.6% total prevalence) displayed additional coexisting variants of the head and neck vessels. The coexisting variants that were observed in the present study are described in Table 3. More than two types of head and neck vessel variations in 15 of the 20 cases of PTA/PTAV were detected. The region of the BA proximal to the site of convergence with the PTA was hypoplastic in six cases and completely absent in one case. Although one case of PTA was associated with an aneurysm, and six cases with arterial stenosis, other vascular diseases, such as arteriovenous malformations, Moyamoya disease, or SturgeeWeber syndrome, were not detected. However, 16 cases were associated with cerebral infarctions, and one case with trigeminal neuralgia.
Discussion 3D TOF MRA technique is a multichunk 3D inflow MRA, in which visualization of the arteries lumen is achieved by the inflow of unsaturated blood through an image section with pre-saturated static tissue. It is a 3D inflow where the 3D volume is divided into overlapping sub-volumes or chunks acquired in an interleaved mode using chunk acquisition and reconstruction method (CHARM; Philips Medical Systems).The chunk overlap to avoid signal decrease between chunks. CHARM is an algorithm used to merge the chunk borders and reduce venetian blind artefacts. An increase in the magnetic field intensity and improvement of the performance of the gradient system contribute to decreasing the acquisition time. Artefacts
Figure 1 MIP-reformatted 3D TOF MRA image (a) and a 3D TOF MRA axial source image (b) of a case of right, lateral PTA in a 63-year-old woman. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the BA. The distal portion of the BA can be observed, but the portion proximal to the site of BA/PTA convergence is very faint (white short arrow). In addition, the VA is bilaterally hypoplastic, and a foetal-type right PCA is observed. A 3D TOF MRA axial source image (b) shows that the PTA trunk branches from the cavernous ICA, which courses around the dorsum sellae at the right (white arrowhead).
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Figure 3 MIP-reformatted 3D TOF MRA image of a case of right PTAV, type B, in a 64-year-old man. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the right SCA. In addition, the left VA branches directly from the aortic arch, and the foetal-type PCA (white arrow) arises from the C7 segment of the ICA bilaterally.
Figure 2 A MIP-reformatted 3D TOF MRA image (a) and a 3D TOF MRA axial source image (b) of a case of left lateral PTA in a 39-yearold woman. The left PTA (white arrowhead) arises from the C4 portion of the left ICA and joins the BA. The diameter of the BA from the proximal portion to the site of BA/PTA convergence is slightly smaller than that of the distal portion (white arrow). A 3D TOF MRA axial source image (b) shows that the PTA trunk branches from the cavernous ICA and runs through the dorsum sellae (white arrowhead).
arising from respiratory and vessel pulsation can be minimized at 3 T MRA. Sensitivity encoding (SENSE) imaging using a SENSE 16-channel neurovascular coil (Philips) has greatly shortened the acquisition time and increased the spatial resolution. 3D TOF MRA more clearly visualizes the intracranial arteries than 3D CE MRA. 3D CE MRA images can be used to visualize the PTA/PTAV; however, they cannot be used to easily identify medial and lateral type PTAs. 3D TOF MRA axial source images more clearly visualize the medial type PTA trunk, which originates from the ICA, through the cavernous sinus, and are connected to the BA, than CE MRA images. Quain12 first described the anatomy of the PTA in an autopsy case in 1844, and Sutton13 reported the first angiographic case in 1950. PTA is frequently reported as an incidental finding at MRA, computed tomography (CT) angiography, or digital subtraction angiography (DSA). Based on a large MRA series, the incidence of PTA/PTAV has been reported to be 0.1e0.76%. Similar to previous reports,6 the incidence of PTA/PTAV in the present study was 0.63%. In the present cohort, PTA/PTAV was more frequent
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Figure 4 MIP-reformatted 3D TOF MRA image of a case of right PTAV, type A, in a 64-year-old woman. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and without joins the BA.
on the right side of the body. The present study revealed that women with PTA were more numerous than males, which is in accordance with other reports.6 Medial type PTA has been reported to occur more rarely than lateral PTA.6 In cases of medial PTA, the PTA courses medially to the abducens nerve and pierces the dura near the BA. Recognizing medial PTA is very important in clinical practice: preoperative MRA will define the course of the medial PTA and enable the neurosurgeon to appropriately plan the surgery to avoid a fatal haemorrhage following trans-sphenoidal resection of pituitary adenomas. PTA and other variants of the head and neck vessels are usually incidental findings. Although the presence of PTA may be completely asymptomatic, it may have certain clinical implications. PTA can be associated with aneurysms,14e17 arteriovenous malformations,18 Moyamoya disease,19 and SturgeeWeber syndrome.20 The reported incidence of intracranial aneurysms with PTA/PTAV is 4.2%, which is similar to that of the general population. Although PTA-associated aneurysms have been reported to occur on the cavernous ICA, the PTA trunk, and the PTA/BA junction, few were located on the PTA itself. There were no arteriovenous malformations or cases of Moyamoya disease or
Figure 5 A MIP-reformatted 3D TOF MRA image of a case of right PTAV in a 61-year-old man. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the BA. In addition, the innominate artery and the left common carotid artery share a common origin (white short arrow), which is located above the aorta and the region where the absent right ACA A1 segment should be (white arrow).
SturgeeWeber syndrome associated with cases of PTA in the present study. This is most likely due to selection bias, because MRA was routinely performed on patients that had or were suspected of having ischaemic cerebrovascular diseases. Several previous studies have shown that PTA/PTAV often coexists with intracranial vascular variants, VA, and carotid artery variants, and aortic arch anomalies.5,6,8e14 The present study determined that PTA/PTAV frequently (52.6%) coexists with other variants of the head and neck vessels, and that more than one type of vascular variation can exist in the same case (46.9%). Among all of the present cases of PTA/PTAV, variants of the intracranial arteries were detected in 10, supra-aortic arteries with variant origins in nine, and variants of the VA in 14. Six cases also displayed fenestrations. Although PTAs are discovered incidentally, it is important to recognize these associated vascular anomalies, particularly before undertaking endovascular and surgical treatment of the head and neck.
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Figure 6 MIP-reformatted 3D TOF MRA image of a case of left PTA in a 51-year-old man. The left PTA (white arrowhead) arises from the C4/5 portion of the left ICA and joins the BA. In addition, the innominate artery and the left common carotid artery share a common origin, which is located above the aorta arch. In this case, there are three pericallosal arteries (white arrow), and the right VA is hypoplastic.
Figure 7 MIP-reformatted 3D TOF MRA image of a case of right PTAV in a 74-year-old man. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the BA. In addition, the right VA is hypoplastic, the VA terminates in the posterior inferior cerebellar artery bilaterally (white long arrow), and the structure of the right subclavian artery is aberrant (white short arrow).
Variants of the supra-aortic arteries in cases of PTA/PTAV
The second most frequent supra-aortic arch variation that occurred together with PTA is found within the left VA. Normally, this vessel arises as a separate branch of the left subclavian artery, but the variant form arises from the aortic artery. The reported incidence of this variant in the normal population is 2.4e5.8%.22 In the present study, the incidence of variant-origin left VAs in cases of PTA/PTAV was 5.3%, which is similar to that of the general population. An aberrant right subclavian artery was found in one case that displayed right VA hypoplasia and had a bilateral variant of the VA, with the VA abnormally terminating in the posterior inferior cerebellar artery. An incidence of 7.9% for varianttermination VAs was calculated in cases of PTA/PTAV.
There are a number of common variations in the anatomy of the great vessels, some of which occur at the vessels’ origins in the aortic arch. The most frequent variant that coexisted with PTA in the cases examined was an ostium that gave rise to both the right innominate artery and the left common carotid artery. This variant is present in approximately 13% of normal individuals.21 A similar proportion (13.2%) was detected in cases of PTA/PTAV. Another common anomaly is a bifurcation of the right innominate artery and the left common carotid artery from a shared point of origin. The bifurcation occurs immediately above the aorta. A similar but less common variant is a left common carotid artery that originates directly from the innominate artery. The reported incidence of this vascular pattern is 9%. In the present study, the incidence in cases of PTA/ PTAV was 2.6%, which is lower than that of the general population.
VA hypoplasia in PTA/PTAV The hypoplastic VA has a uniform but narrow size from its origin to the base of the skull. In the normal population, the reported prevalence of VA hypoplasia detected at angiography is 10e40%. VA hypoplasia has been reported in
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Table 2 Patient demographics and coexisting variants of the head and neck vessels in cases of persistent trigeminal artery/persistent trigeminal artery variant (PTA/PTAV) diagnosed using magnetic resonance angiography (MRA). Age (years) 63 39 64 65 61 56 74 38 58 39 60 54 73 69 60 15 72 34 64 66
(Fig (Fig (Fig (Fig (Fig (Fig (Fig
1) 2) 3) 4) 5) 6) 7)
Gender
Laterality
Type of PTA
Saltzman type
Types of coexisting variants
F F F M M M M
Right Right Right Right Right Left Right
Lateral Medial PTA B PTA A Lateral Lateral Lateral
1 2 None None 1 2 2
F F F M F F F M M M F F F
Right Left Left Right Left Right Left Right Left Right Right Left Left
Lateral Lateral Lateral Medial Lateral Lateral Lateral Lateral Lateral Lateral Lateral Lateral Lateral
1 2 1 1 1 2 1 1 1 2 2 2 1
1, 2 2 3, 4 5 2, 6a, 7 6a, 8, 9 6a, 9, 10, 11, 12,13 2, 9 2, 9, 14 2, 9 9 3, 5 6b, 7, 9, 13 5, 6a 9 5, 10 2, 9, 14 5, 12, 15 10 5, 6a
1, Double middle cerebral artery; 2, hypoplasia of the basilar artery (BA) proximal to the site of BA/PTA convergence; 3, the left vertebral artery (VA) branches directly from the aortic arch; 4, azygos anterior cerebral artery (ACA); 5, fenestration; 6a, the innominate artery and the left common carotid artery share a common origin above the aorta; 6b, the left common carotid artery originates directly from the innominate artery; 7, the ACA A1 segment is absent; 8, triple pericallosal artery; 9, the VA is hypoplastic; 10, the VA terminates in the posterior inferior cerebellar artery; 11, the right subclavian artery is aberrant; 12, double posterior cerebral artery; 13, the BA is absent proximal to site of BA/PTA convergence; 14, the ACA A1 segment is hypoplastic; 15, the right ACA A1 segment and the right M1 segment have anastomosed.
many previous reports. In the present study, the prevalence of this condition in cases of PTA was 23.7%.
Variants of the intracranial arteries in cases of PTA/PTAV Uchino et al.5 and Eluvathingal Muttikkal et al.8 reported azygos anterior cerebral arteries in cases of PTA,5,8 and in the present study, this variant was detected in one case of PTA. Wismer9 and Takase et al.10 reported ACA A1 segment hypoplasia in cases of PTA.9,10 The absence of the ACA A1 segment was also reported.11 The reported prevalence of ACA A1 segment hypoplasia and absence in autopsy cases were 10% and 1e2%, respectively.23 In the present study, the prevalence of ACA A1 segment hypoplasia and absence in cases of PTA was 5.3%, which is slightly higher than that of general population. The reported prevalence of a triple pericallosal artery in the general population was 5.3%24; the prevalence in the present cohort of PTA was 2.6%, which is slighter lower. O’uchi and O’uchi6 documented five cases of PTA with double middle cerebral artery and one case with double PCA.6 In the present study, the prevalence of double middle cerebral artery and double PCA cerebral artery in cases of PTA was 2.6% and 5.3%, respectively.
Fenestration in cases of PTA/PTAV
Type of variant
Number of occurrences
ACA A1 segment hypoplasia Absent ACA A1 segment Azygos ACA Triple pericallosal artery Double middle cerebral artery Double posterior cerebral artery Anastomosis of the right ACA A1segment and the right M1 segment The innominate artery and left common carotid artery originate from a common location above the aorta The left common carotid artery originates directly from the innominate artery VA hypoplasia The VA terminates in the posterior inferior cerebellar artery The left VA branches directly from the aortic arch Fenestration Aberrant right subclavian artery BA hypoplasia proximal to the union with the PTA
2 2 (Fig 5) 1 1 (Fig 6) 1 2 1
Fenestrations are most common in the intracranial arteries and in the vertebrobasilar system. They can be found in any of the segments of the head and neck arteries, including the anterior cerebral artery, anterior communicating artery, middle cerebral arteries, PCAs, VA, BA, and ICA. Fenestrations of the basilar system are believed to be due to partial failure of fusion of the paired longitudinal neural arteries of the 5e7 mm embryo.25 The reported prevalence of fenestrations in the normal population, determined by 3D CTA and MRA, was 11e28%.26 O’uchi and O’uchi6 documented two cases of PTA with fenestration of segment A2 of the ACA, one case of PTAV type A with fenestration of the proximal portion of the BA, and two cases of PTA with fenestration of the distal portion of the BA.6 Six cases of PTA with coexisting fenestrations were documented in the present study. In these cases, fenestration was detected in one BA, two left A1 segments, one M1 segment of the right cerebral middle artery, and two VAs. The prevalence of fenestrations in these cases of PTA was 15.8%.
5 (Figs 5 and 6)
The condition of the BA in cases of PTA
Table 3 Coexisting variants of the head and neck vessels in cases of persistent trigeminal artery/persistent trigeminal artery variant (PTA/PTAV).
1 9 (Figs 1and 6) 3 (Fig 7) 2 (Fig 3) 6 1 (Fig 7) 7
ACA, anterior cerebral artery; BA, basilar artery; VA, vertebral artery.
Hypoplasia of the BA proximal to the location where it joins the PTA has been reported.6 O’uchi and O’uchi6 categorized the degree of hypoplasia as follows: no hypoplasia, moderate hypoplasia, and severe hypoplasia. “No hypoplasia” indicated that the diameter of the BA proximal to or distal to the site of convergence with the PTA had not changed. “Moderate hypoplasia” indicated that the diameter of the BA proximal to the site of BA/PTA convergence was smaller than that of the distal portion, but the proximal portion could still be identified at MRA. “Severe hypoplasia” indicated that although the distal portion of the BA was
M. Bai et al. / Clinical Radiology 68 (2013) e578ee585
easily observed, the portion that was proximal to the site of BA/PTA convergence was very faint. In the present study, the prevalence of BA hypoplasia in cases of PTA was 18.4%. In addition, the BA proximal to the site of BA/PTA convergence was absent in two cases of PTA (5.3%). A limitation of the present study is that it was a retrospective clinical study, and only one neuroradiologist analysed the MRA images. In addition, there may have been some selection bias in the study materials and results, because most of the enrolled patients had or were suspected of having ischaemic cerebrovascular disease. In conclusion, the prevalence of both PTA and PTAV was 0.63%. Although PTA and PTAV were rare vascular variants in the patient population, these conditions frequently coexisted with other variants of the head and neck vessels. More than one vascular variant can be present in a single case of PTA. Recognizing PTA, PTAV, and the associated variants of the head and neck vessels is crucial when planning a neuroradiological intervention or surgery. Recognizing the medial PTA is very important in clinical practice when performing trans-sphenoidal surgery on the pituitary, as failure to do so could result in massive haemorrhage.
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Persistent trigeminal artery/persistent trigeminal artery variant and coexisting variants of the head and neck vessels diagnosed using 3 T MRA M. Bai a, *, Q. Guo b, S. Li a a
Department of Radiology, Liaocheng People’s Hospital and Liaocheng Clinical School of Taishan Medical University, Liaocheng, Shandong, PR China b Department of Neurosurgery, Liaocheng People’s Hospital and Liaocheng Clinical School of Taishan Medical University, Liaocheng, Shandong, PR China
article in formation Article history: Received 10 March 2013 Received in revised form 9 May 2013 Accepted 29 May 2013
AIM: To report the prevalence and characteristic features of persistent trigeminal artery (PTA), PTA variant (PTAV), and other variants of the head and neck vessels, identified using magnetic resonance angiography (MRA). MATERIALS AND METHODS: The three-dimensional (3D) time of flight (TOF) MRA and 3D contrast-enhanced (CE) MRA images of 6095 consecutive patients who underwent 3 T MRA at Liaocheng People’s Hospital from 1 September 2008 through 31 May 2012 were retrospectively reviewed and analysed. Thirty-two patients were excluded because of suboptimal image quality or internal carotid artery (ICA) occlusion. RESULTS: The prevalence of both PTA and PTAV was 0.63% (PTA, 26 cases; PTAV, 12 cases). The prevalence of coexisting variants of the head and neck vessels in cases of PTA/PTAV was 52.6% (20 of 38 cases). The vascular variants that coexisted with cases of PTA/PTAV were as follows: the intracranial arteries varied in 10 cases, the origin of the supra-aortic arteries varied in nine cases, the vertebral artery (VA) varied in 14 cases, and six cases displayed fenestrations. Fifteen of the 20 cases contained more than two types of variants. CONCLUSION: The prevalence of both PTA and PTAV was 0.63%. Although PTA and PTAV are rare vascular variants, they frequently coexist with other variants of the head and neck vessels. Multiple vascular variations can coexist in a single patient. Recognizing PTA, PTAV, and other variants of the head and neck vessels is crucial when planning a neuroradiological intervention or surgery. Recognizing the medial PTA is very important in clinical practice when performing trans-sphenoidal surgery on the pituitary as failure to do so could result in massive haemorrhage. Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
Introduction Carotidevertebrobasilar anastomoses include the persistent primitive trigeminal artery (PPTA), the persistent * Guarantor and correspondent: M. Bai, Department of Radiology, Liaocheng People’s Hospital, Dongchang West Road 67, Liaocheng, Shandong Province 252000, PR China. Tel.: þ86 13563588802. E-mail address: [email protected] (M. Bai).
primitive otic artery, the persistent primitive hypoglossal artery, and the persistent primitive pro-atlantal artery. These anastomoses, which are named according to their associated anatomy, link the primitive internal carotid artery (ICA) and basilar artery (BA) systems, and exist in early foetal life (4e5 mm embryonic stage).1 As the vascular system evolves, they are quickly remodelled, with the trigeminal artery being the last to disappear (7e14 mm embryonic stage).1 Rarely, the anastomoses persist into adulthood.
0009-9260/$ e see front matter Ó 2013 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.crad.2013.05.099
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Persistent trigeminal artery (PTA) is the most common remnant of embryonic communication between the ICA and the vertebrobasilar system. The PTA originates from the cavernous segment of the ICA and communicates with the BA. The angiographic anatomy and classification of PTAs were first described by Saltzman and Wollschlaeger.2 In Saltzman type 1 PTA, the PTA supplies the BA, posterior cerebral arteries (PCA), and superior cerebellar arteries (SCAs). Segments of the BA proximal to the insertion of the PTA may be hypoplastic and the posterior communicating artery (PComA) may be absent. In Saltzman type 2 PTA, the PTA joins the BA below the origin of the SCA, and the PCA receives its blood supply predominantly through the patent PComA. PTA is also divided into two types, depending on where in the cavernous ICA the artery originates: lateral PTA originates in the posterolateral aspect, whereas medial PTA originates in the posteromedial aspect. Direct anastomoses between the precavernous portion of the ICA and the cerebellar arteries, without interposition of the BA, are described as PTA variants (PTAV).3e5 Cases in which the anomalous artery arises from the ICA and joins the ipsilateral SCA or the BA have been named “PTAV type A,” whereas those in which the anomalous artery arises from the ICA and joins the ipsilateral SCA have been named “PTAV type B”.6 The reported incidence of PTA/PTAV is about 0.2e0.76%.4e7 Numerous anatomical and embryological studies of PTA and PTAV have been reported.4e8 Several previous studies have shown that PTA often coexists with aortic arch anomalies and variation of the intracranial vasculature, the VA, and the carotid artery.3,5,6,8e11 Being aware of these variations is crucial for interpreting the findings of magnetic resonance angiography (MRA), because they can influence surgical and interventional procedures. Three-dimensional (3D) time of flight (TOF) MRA of the supra-aortic arteries has been used as a non-invasive, safe, and fast method for evaluating the vasculature of the head and neck. The purpose of the present study was to describe the prevalence and characteristic features of PTA/PTAV and coexisting variants of the head and neck vessels identified using MRA at 3 T.
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Materials and methods Patients Using either a picture archiving and communication system (PACS) or the Aquarius workstation (TeraRecon, Foster City, CA, USA), the findings of 3D TOF MRA and contrast-enhanced (CE) MRA examinations of the head and neck vessels of 6095 consecutive Chinese patients who had or were suspected of having an ischaemic cerebrovascular disease on physical examination were retrospectively reviewed. The examinations were carried out from 1 September 2008 to 31 May 2012. After excluding 32 patients whose images were of suboptimal quality or showed ICA occlusion, the images of 6063 patients were ultimately reviewed and analysed. The mean age of the patients was 64 years, and the range was 15e75 years. Fifteen of the 38 patients with PTA or PTAV were men; 23 were women. Patients were both asymptomatic and symptomatic. The reported symptoms included dizziness, headache, vomiting, asthenia, hemiparalysis, and trigeminal neuralgia. This study was approved by the institutional review board of Liaocheng People’s Hospital.
MRA All MRA imaging was performed using a 3 T scanner (Achieva; Philips Medical Systems, The Netherlands) using a 16-channel sensitivity-encoding head and neck coil and a strong gradient system (maximal gradient amplitude, 80 mT/m; slew rate, 150 T/m/s). For 3D TOF MRA, a 3D fast-field echo sequence with a multichunk technique was used. The imaging parameters of the head, neck, and supra-aortic arch are shown in Table 1. The total acquisition time was 11 min, 39 s. The original 3D TOF MRA images of the head, neck, and supra-aortic arteries were scanned, and then analysed with a maximum-intensity projection (MIP) post-processing algorithm. The separate images of the head, neck, and supra-aortic arteries were fused using MobiView software (Philips Healthcare, USA) to create one image that extended from the top of the head to the aortic arch. All images were of diagnostic quality.
Table 1 Sequence parameters of three-dimensional time of flight magnetic resonance angiography. Parameter
Head
Neck
Supra-aortic arch
Repetition time (ms) Echo time (ms) Field of view (mm mm mm) Flip angle ( ) Matrix Voxel size (mm mm mm) Sections Section thickness (cm) Gap (cm) Chunks SENSE factor Acquisition time
15 3.5 220 191 96 18 368 40 0.6 1.0 0.6 160 2 1 5 2 2 min, 52 s
20 3.5 160 129 135 20 260 84 0.85 0.52 0.75 180 2 1 6 3 2 min, 24 s
22 3.5 250 238 96 22 252 142 1.0 1.6 0.8 120 1 1 5 2 4 min, 48 s
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For 3D CE MRA, an electronic power injector (Spectris Solaris EP, MEDRAD, USA) was used to inject the contrast material. The contrast agent injection protocol specified 0.2 mmol gadodiamide per kilogram body weight administered at a flow rate of 1.5 ml/s, followed by 20 ml saline at the same rate. Subsequently, high-spatial-resolution CE MRA was performed in the coronal plane using a fast sequence.
Image analysis The MRA images were reviewed by one experienced radiologist using either the PACS or the Aquarius workstation. Partial MIP and volume rendering (VR) were used to visualize the head and neck vessel variants.
Results Among the 6063 patients, 26 cases of PTA (10 men, 16 women; 0.43% prevalence) were identified. Right PTA was more common than left PTA (right PTA, 15 cases; left PTA, nine cases). Twelve cases of PTAV (five men, seven women; 0.2% prevalence) were also identified. The prevalence of both PTA and PTAV was 0.63%. The ratio of men with PTA/ PTAV to women with PTA/PTAV was 1:1.5. Twenty-three cases of PTA were lateral types (Fig 1; 88.5% prevalence); three cases were medial types (Fig 2; 11.5% prevalence). Nine cases of PTAV were type A (Fig 3; 75% prevalence) and three cases were type B (Fig 4; 25% prevalence). As described in Table 2, 20 cases of PTA/PTAV (52.6% total prevalence) displayed additional coexisting variants of the head and neck vessels. The coexisting variants that were observed in the present study are described in Table 3. More than two types of head and neck vessel variations in 15 of the 20 cases of PTA/PTAV were detected. The region of the BA proximal to the site of convergence with the PTA was hypoplastic in six cases and completely absent in one case. Although one case of PTA was associated with an aneurysm, and six cases with arterial stenosis, other vascular diseases, such as arteriovenous malformations, Moyamoya disease, or SturgeeWeber syndrome, were not detected. However, 16 cases were associated with cerebral infarctions, and one case with trigeminal neuralgia.
Discussion 3D TOF MRA technique is a multichunk 3D inflow MRA, in which visualization of the arteries lumen is achieved by the inflow of unsaturated blood through an image section with pre-saturated static tissue. It is a 3D inflow where the 3D volume is divided into overlapping sub-volumes or chunks acquired in an interleaved mode using chunk acquisition and reconstruction method (CHARM; Philips Medical Systems).The chunk overlap to avoid signal decrease between chunks. CHARM is an algorithm used to merge the chunk borders and reduce venetian blind artefacts. An increase in the magnetic field intensity and improvement of the performance of the gradient system contribute to decreasing the acquisition time. Artefacts
Figure 1 MIP-reformatted 3D TOF MRA image (a) and a 3D TOF MRA axial source image (b) of a case of right, lateral PTA in a 63-year-old woman. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the BA. The distal portion of the BA can be observed, but the portion proximal to the site of BA/PTA convergence is very faint (white short arrow). In addition, the VA is bilaterally hypoplastic, and a foetal-type right PCA is observed. A 3D TOF MRA axial source image (b) shows that the PTA trunk branches from the cavernous ICA, which courses around the dorsum sellae at the right (white arrowhead).
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Figure 3 MIP-reformatted 3D TOF MRA image of a case of right PTAV, type B, in a 64-year-old man. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the right SCA. In addition, the left VA branches directly from the aortic arch, and the foetal-type PCA (white arrow) arises from the C7 segment of the ICA bilaterally.
Figure 2 A MIP-reformatted 3D TOF MRA image (a) and a 3D TOF MRA axial source image (b) of a case of left lateral PTA in a 39-yearold woman. The left PTA (white arrowhead) arises from the C4 portion of the left ICA and joins the BA. The diameter of the BA from the proximal portion to the site of BA/PTA convergence is slightly smaller than that of the distal portion (white arrow). A 3D TOF MRA axial source image (b) shows that the PTA trunk branches from the cavernous ICA and runs through the dorsum sellae (white arrowhead).
arising from respiratory and vessel pulsation can be minimized at 3 T MRA. Sensitivity encoding (SENSE) imaging using a SENSE 16-channel neurovascular coil (Philips) has greatly shortened the acquisition time and increased the spatial resolution. 3D TOF MRA more clearly visualizes the intracranial arteries than 3D CE MRA. 3D CE MRA images can be used to visualize the PTA/PTAV; however, they cannot be used to easily identify medial and lateral type PTAs. 3D TOF MRA axial source images more clearly visualize the medial type PTA trunk, which originates from the ICA, through the cavernous sinus, and are connected to the BA, than CE MRA images. Quain12 first described the anatomy of the PTA in an autopsy case in 1844, and Sutton13 reported the first angiographic case in 1950. PTA is frequently reported as an incidental finding at MRA, computed tomography (CT) angiography, or digital subtraction angiography (DSA). Based on a large MRA series, the incidence of PTA/PTAV has been reported to be 0.1e0.76%. Similar to previous reports,6 the incidence of PTA/PTAV in the present study was 0.63%. In the present cohort, PTA/PTAV was more frequent
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Figure 4 MIP-reformatted 3D TOF MRA image of a case of right PTAV, type A, in a 64-year-old woman. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and without joins the BA.
on the right side of the body. The present study revealed that women with PTA were more numerous than males, which is in accordance with other reports.6 Medial type PTA has been reported to occur more rarely than lateral PTA.6 In cases of medial PTA, the PTA courses medially to the abducens nerve and pierces the dura near the BA. Recognizing medial PTA is very important in clinical practice: preoperative MRA will define the course of the medial PTA and enable the neurosurgeon to appropriately plan the surgery to avoid a fatal haemorrhage following trans-sphenoidal resection of pituitary adenomas. PTA and other variants of the head and neck vessels are usually incidental findings. Although the presence of PTA may be completely asymptomatic, it may have certain clinical implications. PTA can be associated with aneurysms,14e17 arteriovenous malformations,18 Moyamoya disease,19 and SturgeeWeber syndrome.20 The reported incidence of intracranial aneurysms with PTA/PTAV is 4.2%, which is similar to that of the general population. Although PTA-associated aneurysms have been reported to occur on the cavernous ICA, the PTA trunk, and the PTA/BA junction, few were located on the PTA itself. There were no arteriovenous malformations or cases of Moyamoya disease or
Figure 5 A MIP-reformatted 3D TOF MRA image of a case of right PTAV in a 61-year-old man. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the BA. In addition, the innominate artery and the left common carotid artery share a common origin (white short arrow), which is located above the aorta and the region where the absent right ACA A1 segment should be (white arrow).
SturgeeWeber syndrome associated with cases of PTA in the present study. This is most likely due to selection bias, because MRA was routinely performed on patients that had or were suspected of having ischaemic cerebrovascular diseases. Several previous studies have shown that PTA/PTAV often coexists with intracranial vascular variants, VA, and carotid artery variants, and aortic arch anomalies.5,6,8e14 The present study determined that PTA/PTAV frequently (52.6%) coexists with other variants of the head and neck vessels, and that more than one type of vascular variation can exist in the same case (46.9%). Among all of the present cases of PTA/PTAV, variants of the intracranial arteries were detected in 10, supra-aortic arteries with variant origins in nine, and variants of the VA in 14. Six cases also displayed fenestrations. Although PTAs are discovered incidentally, it is important to recognize these associated vascular anomalies, particularly before undertaking endovascular and surgical treatment of the head and neck.
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Figure 6 MIP-reformatted 3D TOF MRA image of a case of left PTA in a 51-year-old man. The left PTA (white arrowhead) arises from the C4/5 portion of the left ICA and joins the BA. In addition, the innominate artery and the left common carotid artery share a common origin, which is located above the aorta arch. In this case, there are three pericallosal arteries (white arrow), and the right VA is hypoplastic.
Figure 7 MIP-reformatted 3D TOF MRA image of a case of right PTAV in a 74-year-old man. The right PTA (white arrowhead) arises from the C4 portion of the right ICA and joins the BA. In addition, the right VA is hypoplastic, the VA terminates in the posterior inferior cerebellar artery bilaterally (white long arrow), and the structure of the right subclavian artery is aberrant (white short arrow).
Variants of the supra-aortic arteries in cases of PTA/PTAV
The second most frequent supra-aortic arch variation that occurred together with PTA is found within the left VA. Normally, this vessel arises as a separate branch of the left subclavian artery, but the variant form arises from the aortic artery. The reported incidence of this variant in the normal population is 2.4e5.8%.22 In the present study, the incidence of variant-origin left VAs in cases of PTA/PTAV was 5.3%, which is similar to that of the general population. An aberrant right subclavian artery was found in one case that displayed right VA hypoplasia and had a bilateral variant of the VA, with the VA abnormally terminating in the posterior inferior cerebellar artery. An incidence of 7.9% for varianttermination VAs was calculated in cases of PTA/PTAV.
There are a number of common variations in the anatomy of the great vessels, some of which occur at the vessels’ origins in the aortic arch. The most frequent variant that coexisted with PTA in the cases examined was an ostium that gave rise to both the right innominate artery and the left common carotid artery. This variant is present in approximately 13% of normal individuals.21 A similar proportion (13.2%) was detected in cases of PTA/PTAV. Another common anomaly is a bifurcation of the right innominate artery and the left common carotid artery from a shared point of origin. The bifurcation occurs immediately above the aorta. A similar but less common variant is a left common carotid artery that originates directly from the innominate artery. The reported incidence of this vascular pattern is 9%. In the present study, the incidence in cases of PTA/ PTAV was 2.6%, which is lower than that of the general population.
VA hypoplasia in PTA/PTAV The hypoplastic VA has a uniform but narrow size from its origin to the base of the skull. In the normal population, the reported prevalence of VA hypoplasia detected at angiography is 10e40%. VA hypoplasia has been reported in
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Table 2 Patient demographics and coexisting variants of the head and neck vessels in cases of persistent trigeminal artery/persistent trigeminal artery variant (PTA/PTAV) diagnosed using magnetic resonance angiography (MRA). Age (years) 63 39 64 65 61 56 74 38 58 39 60 54 73 69 60 15 72 34 64 66
(Fig (Fig (Fig (Fig (Fig (Fig (Fig
1) 2) 3) 4) 5) 6) 7)
Gender
Laterality
Type of PTA
Saltzman type
Types of coexisting variants
F F F M M M M
Right Right Right Right Right Left Right
Lateral Medial PTA B PTA A Lateral Lateral Lateral
1 2 None None 1 2 2
F F F M F F F M M M F F F
Right Left Left Right Left Right Left Right Left Right Right Left Left
Lateral Lateral Lateral Medial Lateral Lateral Lateral Lateral Lateral Lateral Lateral Lateral Lateral
1 2 1 1 1 2 1 1 1 2 2 2 1
1, 2 2 3, 4 5 2, 6a, 7 6a, 8, 9 6a, 9, 10, 11, 12,13 2, 9 2, 9, 14 2, 9 9 3, 5 6b, 7, 9, 13 5, 6a 9 5, 10 2, 9, 14 5, 12, 15 10 5, 6a
1, Double middle cerebral artery; 2, hypoplasia of the basilar artery (BA) proximal to the site of BA/PTA convergence; 3, the left vertebral artery (VA) branches directly from the aortic arch; 4, azygos anterior cerebral artery (ACA); 5, fenestration; 6a, the innominate artery and the left common carotid artery share a common origin above the aorta; 6b, the left common carotid artery originates directly from the innominate artery; 7, the ACA A1 segment is absent; 8, triple pericallosal artery; 9, the VA is hypoplastic; 10, the VA terminates in the posterior inferior cerebellar artery; 11, the right subclavian artery is aberrant; 12, double posterior cerebral artery; 13, the BA is absent proximal to site of BA/PTA convergence; 14, the ACA A1 segment is hypoplastic; 15, the right ACA A1 segment and the right M1 segment have anastomosed.
many previous reports. In the present study, the prevalence of this condition in cases of PTA was 23.7%.
Variants of the intracranial arteries in cases of PTA/PTAV Uchino et al.5 and Eluvathingal Muttikkal et al.8 reported azygos anterior cerebral arteries in cases of PTA,5,8 and in the present study, this variant was detected in one case of PTA. Wismer9 and Takase et al.10 reported ACA A1 segment hypoplasia in cases of PTA.9,10 The absence of the ACA A1 segment was also reported.11 The reported prevalence of ACA A1 segment hypoplasia and absence in autopsy cases were 10% and 1e2%, respectively.23 In the present study, the prevalence of ACA A1 segment hypoplasia and absence in cases of PTA was 5.3%, which is slightly higher than that of general population. The reported prevalence of a triple pericallosal artery in the general population was 5.3%24; the prevalence in the present cohort of PTA was 2.6%, which is slighter lower. O’uchi and O’uchi6 documented five cases of PTA with double middle cerebral artery and one case with double PCA.6 In the present study, the prevalence of double middle cerebral artery and double PCA cerebral artery in cases of PTA was 2.6% and 5.3%, respectively.
Fenestration in cases of PTA/PTAV
Type of variant
Number of occurrences
ACA A1 segment hypoplasia Absent ACA A1 segment Azygos ACA Triple pericallosal artery Double middle cerebral artery Double posterior cerebral artery Anastomosis of the right ACA A1segment and the right M1 segment The innominate artery and left common carotid artery originate from a common location above the aorta The left common carotid artery originates directly from the innominate artery VA hypoplasia The VA terminates in the posterior inferior cerebellar artery The left VA branches directly from the aortic arch Fenestration Aberrant right subclavian artery BA hypoplasia proximal to the union with the PTA
2 2 (Fig 5) 1 1 (Fig 6) 1 2 1
Fenestrations are most common in the intracranial arteries and in the vertebrobasilar system. They can be found in any of the segments of the head and neck arteries, including the anterior cerebral artery, anterior communicating artery, middle cerebral arteries, PCAs, VA, BA, and ICA. Fenestrations of the basilar system are believed to be due to partial failure of fusion of the paired longitudinal neural arteries of the 5e7 mm embryo.25 The reported prevalence of fenestrations in the normal population, determined by 3D CTA and MRA, was 11e28%.26 O’uchi and O’uchi6 documented two cases of PTA with fenestration of segment A2 of the ACA, one case of PTAV type A with fenestration of the proximal portion of the BA, and two cases of PTA with fenestration of the distal portion of the BA.6 Six cases of PTA with coexisting fenestrations were documented in the present study. In these cases, fenestration was detected in one BA, two left A1 segments, one M1 segment of the right cerebral middle artery, and two VAs. The prevalence of fenestrations in these cases of PTA was 15.8%.
5 (Figs 5 and 6)
The condition of the BA in cases of PTA
Table 3 Coexisting variants of the head and neck vessels in cases of persistent trigeminal artery/persistent trigeminal artery variant (PTA/PTAV).
1 9 (Figs 1and 6) 3 (Fig 7) 2 (Fig 3) 6 1 (Fig 7) 7
ACA, anterior cerebral artery; BA, basilar artery; VA, vertebral artery.
Hypoplasia of the BA proximal to the location where it joins the PTA has been reported.6 O’uchi and O’uchi6 categorized the degree of hypoplasia as follows: no hypoplasia, moderate hypoplasia, and severe hypoplasia. “No hypoplasia” indicated that the diameter of the BA proximal to or distal to the site of convergence with the PTA had not changed. “Moderate hypoplasia” indicated that the diameter of the BA proximal to the site of BA/PTA convergence was smaller than that of the distal portion, but the proximal portion could still be identified at MRA. “Severe hypoplasia” indicated that although the distal portion of the BA was
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easily observed, the portion that was proximal to the site of BA/PTA convergence was very faint. In the present study, the prevalence of BA hypoplasia in cases of PTA was 18.4%. In addition, the BA proximal to the site of BA/PTA convergence was absent in two cases of PTA (5.3%). A limitation of the present study is that it was a retrospective clinical study, and only one neuroradiologist analysed the MRA images. In addition, there may have been some selection bias in the study materials and results, because most of the enrolled patients had or were suspected of having ischaemic cerebrovascular disease. In conclusion, the prevalence of both PTA and PTAV was 0.63%. Although PTA and PTAV were rare vascular variants in the patient population, these conditions frequently coexisted with other variants of the head and neck vessels. More than one vascular variant can be present in a single case of PTA. Recognizing PTA, PTAV, and the associated variants of the head and neck vessels is crucial when planning a neuroradiological intervention or surgery. Recognizing the medial PTA is very important in clinical practice when performing trans-sphenoidal surgery on the pituitary, as failure to do so could result in massive haemorrhage.
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