Introduction

The persistent trigeminal artery (PTA) is the most common but rarely reported carotid-basilar anastomosis. Previous studies demonstrated that the incidence of PTA ranged from 0.1-0.6% [1], and the reports of PTA mainly focused on limited sample and case reports. The presence of PTA could combine with many other diseases, such as aneurysm [2,3,4], arteriovenous malformation [5, 6], and trigeminal neuralgia [7,8,9]. Moreover, moyamoya disease (MMD) is a rare disease characterized by occlusion and abnormal proliferation of the cerebral arteries and the formation of moyamoya vessels, which could ultimately lead to the occurrence of cerebral infarction or hemorrhage [10]. The revascularization, which could greatly reduce the incidence of hemorrhage and cerebral infarction, has been proved to be a safe and effective choice for patient with MMD after extensive clinical studies and practices. In very condition, the MMD could combine with PTA, no matter whether this artery is affected [2, 11]. To our knowledge, only 13 cases of MMD associated with PTA were reported in the past decades (including current case).

Case presentation

The case involved a 44-year-old woman who admitted to our department for further treatment. She experienced sudden, severe dizziness and headache three months ago without any identifiable cause. The head computed tomography scan performed at local hospital revealed infarction in the left temporal and basal ganglia, as well as severe stenosis of both internal carotid arteries (ICAs). She was initially treated symptomatically and gradually improved. Three months later, she scheduled for further treatment in our department. The computed tomography perfusion (CTP) imaging showed old infarction and partial liquefaction in the left frontal and temporal lobe. Additionally, the computed tomography angiography (CTA) and digital subtraction angiography (DSA) revealed a PTA arising from cavernous portion of the right ICA, and stenosis or occlusion in the bilateral anterior cerebral arteries (ACA), the M1 segment of bilateral middle cerebral arteries (MCAs), and the C5-C6 segment of bilateral ICAs, combining with many net-like vessels, but the anterior and posterior communicating arteries were patent (Fig. 1). Following thorough preoperative examinations, it was determined that bilateral revascularizations were needed. Considering the characteristics of the disease onset, the left revascularization was performed first. During the surgery, however, we found that all of the potential recipient vessels had a diameter smaller than 0.5 mm, while the superficial temporal artery had a diameter greater than 1.5 mm, a direct bypass would pose a high risk of postoperative hemorrhage. Therefore, an indirect bypass procedure was performed on the left side, the patient recovered well and was discharged within a week. During the follow-up visit three months later, imaging examination revealed severe stenosis of the arteries. However, there were improvements in the intracranial vascular conditions, and collateral vessels had formed on the left side. For similar reason mentioned above, an indirect bypass on the right side was performed during this hospitalization. The patient experienced a smooth recovery and symptom improvement. The most recent CTA, CTP tests and DSA of the head indicated significant improvement in both intracranial and extracranial collateral vessels. However, there was still relatively low cerebral blood flow perfusion in the left frontal and temporal lobe (Fig. 2).

Fig. 1
figure 1

First admission CTP imaging showed old infarction and partial liquefaction in the left frontal and temporal lobe (F), and the CTA and DSA revealed the PTA arises from cavernous portion of the right ICA (A, E) (white arrow), and stenosis or occlusion in the bilateral ACAs, the M1 segments of bilateral MCAs, and the C5-C6 segments of bilateal ICAs, but the anterior and posterior communicating arteries were patent (A, B, C, D, E). Moreover, there were a great mount of moyamoya vessels (A, B, C, D, E). ICA: internal carotid artery; CTP: computed tomography perfusion; CTA: computed tomography angiography; DSA: digital subtraction angiography. ACA: anterior cerebral artery; MCA: middle cerebral artery; PTA: persistent trigeminal artery

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Fig. 2
figure 2

The latest imaging test and DSA (more than two years later after first admission) showed the formation of numerous collateral vessels at the site of bilateral indirect (B, D) and a significant improvement in intracranial blood flow conditions (A, B, C, D) compared to first admission, but there was low cerebral blood flow perfusion in the left frontal and temporal lobe (F)

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Discussion

PTA, otic artery, hypoglossal artery, and proatlantic intersegmental artery are the four persistent embryologic carotid-basilar anastomoses, and PTA is the most common with a very low reported incidence [1]. It was first described in a specimen in 1841 [12] and demonstrated in a live subject in 1950 [13]. Based on its radiological and hemodynamic characteristics, Saltzman classified PTA into three types [14]. Type 1 is the most common, the PTA supplies the bilateral superior cerebellar arteries (SCAs) and the bilateral posterior cerebral arteries. In type 2, the PTA supplies bilateral SCAs. Type 3 represents a variant of PTA, which can be further subdivided into three subtypes: type 3a, where PTA directly drains into the ipsilateral SCA; type 3b, where PTA directly drains into the ipsilateral anterior inferior cerebellar artery (AICA); and type 3c, where PTA directly drains into the ipsilateral posterior inferior cerebellar artery (PICA). Salas classified PTA into lateral and medial types based on the anatomical relationship between PTA and the abducent nerve [15]. Weon further expanded the classification into five types [16]. Types 1 and 2 correspond to Saltzman’s classification, while in types 3 and 4, the PTA drains into the contralateral and ipsilateral posterior cerebral arteries, respectively. Type 5 can be further divided into subtypes based on its terminal arteries: type 5a (SCA), type 5b (AICA), and type 5c (PICA). (Fig. 3). It was reported that the type 1 was the most common [17].

Fig. 3
figure 3

Weon subtyped the PTA into five types based on its hemodynamic characteristics: type 1, the PTA supplies bilateral PCA, and superior cerebellar artery; type 2, the PTA supplies of the bilateral superior cerebellar artery; type 3, the PTA supplies the contralateral PCA; type 4, the PTA supplies ipsilateral PCA; and type 5 can be subclassified as 5a,5b, and 5c according to the terminative artery, the superior cerebellar artery (5a), anterior inferior cerebellar artery (5b), and the posterior inferior cerebellar artery (5c), respectively. PTA: persistent trigeminal artery; ICA: internal carotid artery; SCA: superior cerebellar arteries; AICA: anterior inferior cerebellar artery; PICA: posterior inferior cerebellar artery; BA: basilar artery; VA: vertebral artery; PCA: posterior cerebral artery

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The PTA draws attention for it’s usually reported to be associated with central nervous system disease, such as aneurysm [2,3,4], arteriovenous malformation [5, 6], MMD [2, 11], and trigeminal neuralgia [7,8,9]. It’s reported that the rough incidence of MMD with PTA is 0.0021% [11]. After carefully retrieval in web of science, we found that there were only 13 cases of patients with the coexistence of PTA with MMD (including current case). (Table 1) For the vascular features of MMD and PTA, the PTA could be the collateral vessel of MMD and protect the patients from complications, such as ischemia and hemorrhage (Fig. 4), but also prompt the stage of MMD [18]. Such patients mostly present with ischemia, with a small part with hemorrhage, and no age, gender, or lateralization patterns difference. Patients who underwent revascularization procedures generally achieved favorable outcomes. As the PTA coexistence with MMD is rarely reported, the incidence, clinical feature, and outcome of such condition remain further study.

Fig. 4
figure 4

The figure illustrates the role of PTA in patient with MMD. Under normal blood flow, the ICA supplies blood to the BA via PTA (A). However, in patients with MMD, the ICA get stenosis (B) and even occlusion (C), resulting in the flow of blood from BA to ICA via PTA partially (B) and totally (C). PTA: persistent trigeminal artery; MMD: moyamoya disease; ICA: internal carotid artery; BA: basilar artery

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In addition to PTA, the MMD could be combined with other anomalies, such as arteriovenous malformation [19,20,21], carotid artery absence [22,23,24], ICA hyperplasia [25] and so on. It is more likely that the increased blood to the arteriovenous malformation and increased blood turbulence lead to intimal hyperplasia and progressive occlusion [26]. The anastomotic vessels and their capillaries could open up and become distended in the presence of ischemia, these capillaries could only discharge the increased blood into normal veins which in tum become distended [19]. As the variant of PTA is usually poorly visualized, more attentions should be paid to such patient [25]. In patients with carotid artery abnormality, the presence of PTA could be vital collateral circulation [22, 23]. There is no currently direct etiological evidence show the relationships between MMD and these diseases, but it can be speculated that congenital factors may play an important role [22], as the timeframe in which the PTA regresses during embryonic development coincides with the period in which the vascular condition bears resemblance [27]. Uchino reported the higher incidence of PTA in patient also support this hypothesis [28], but the potential mechanism remains unknown [29]. As the imaging characteristics of MMD, the PTA could be the solely blood supply to the affected brain region [18]. Moreover, this artery could even change the haemodynamics of patients with MMD, and be used as a route for endovascular coiling for aneurysm [2]. Also, the PTA could play a protective role in cases of acquired occlusion of the ipsilateral ICA [30, 31], it could provide compensatory blood to the targeted area. In currtent case, the proximal basilar artery and bilateral vertebral arteries were very thin, the PTA could supply blood to the posterior circulation, especially in patient with MMD, whose cerebral arteries were badly affected. However, further studies are still needed to explore their connections.

Table 1 Summary of the 13 cases of patients with the coexistence of PTA and MMD
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Conclusions

The coexistence of PTA and MMD was rare reported, the pathogenesis of such condition remains yet to be explored. Based on the literature review, we found that the manifestation of such patient showed no classical characteristics. Revascularization might be a feasible choice for patient with PTA combined with MMD.