A symptomatic atherosclerotic persistent pharyngo-hyo-stapedial artery: Treatment management and embryological considerations

Abstract

The stapedial artery (SA) is an embryonic vessel connecting the internal carotid artery (ICA) to the branches of the future external carotid artery (ECA). It passes through the primordium of the stapes that progressively develops around the SA. Normally, SA disappears during the tenth week in utero. Approximately 0.4% of the population can have a persistent SA. It can persist as four types of embryological variations, of which the pharyngo-hyo-stapedial variant has been rarely described before. We reported a case of a 61-year-old woman presented with transient ischemic attacks (TIAs). Computed tomography angiography showed an unusual “duplicated” aspect of the left ICA. Digital subtraction angiography depicted a persistent pharyngo-hyo-stapedial artery with an atherosclerotic wall and was considered the cause of the TIAs. After failure of the antiplatelet therapy in preventing recurrent TIAs, stenting of the artery was planned and successfully performed. Patient was asymptomatic during 12-month follow-up. The pharyngo-hyo-stapedial artery is a very rare variation in which the SA is supplied by the inferior tympanic (rising from the ascending pharyngeal artery) and the hyoid artery (rising from the ICA). To our knowledge, this is a unique case of a pharyngo-hyo-stapedial artery in a patient presenting associated ischemic symptoms. Radiological and embryological findings are discussed.

Introduction

The stapedial artery (SA) is an embryonic vessel which normally regresses around the 10th week of gestation. It connects the internal carotid artery (ICA) to the branches of the future external carotid artery (ECA). Around the SA, the primordium of the stapes progressively develops during the 16th–20th stage of Carnegie (9–18mm embryo).^1–3 The first case of a persistent stapedial artery (SA) was reported in 1836 by Hyrtl.⁴ After the first description, many other cases were published, and this congenital vascular variation of the middle ear has been reported as a cause of pulsatile tinnitus or conductive hearing loss.⁵ The prevalence of this embryological variation has been estimated around 0.4%.⁶ However, SA can persist as four types of developmental variations (Figure 1): (1) a persistent SA (also called hyoido-stapedial), the most common type; (2) a pharyngo-stapedial artery; (3) a pharyngo-hyo-stapedial artery; and (4) a persistent SA with an aberrant ICA.⁷ In our case of pharyngo-hyo-stapedial variant, the SA originated from the hyoid artery (rising from the petrous ICA) that was anastomosed with the inferior tympanic artery (a branch of the ascending pharyngeal artery) originating from the common carotid artery bifurcation⁸ (Figures 1 to 4). An irregular atherosclerotic wall of the pharyngo-hyo-stapedial vessel was likely the cause of the transient ischemic attacks (TIAs). Endovascular treatment, embryological and anatomical aspects of this rare case are discussed.

Figure 1.

(a, b, c, d, e, f) Embryology of the stapedial artery (SA) and anatomic variations (modified from Hitier et al.⁵). The SA and the hyoid artery originate from the second aortic arch (pharyngeal arch). During the 14th stage of Carnegie (5–6 mm embryo), the dorsal part of this arch becomes the hyoid artery. The hyoid artery rises from the primitive ICA and gives rise to the SA that goes through the stapes (week 6) (a). The middle meningeal artery (MMA) originates from the SA. The foramen spinosum grows around the link between the SA and the ventral pharyngeal artery (primordium of the internal maxillary artery, IMA). The inferior tympanic artery, passing through the inferior tympanic canaliculus, anastomoses with the hyoid artery. Five types of evolution are possible. (1) Normal evolution with regression of the SA (b): the MMA rises from the IMA (previous ventral pharyngeal artery), passing through the foramen spinosum. (2) Persistent SA, forming a hyoido-stapedial artery (c), rising from the ICA, with no foramen spinosum. (3) Persistent pharyngo-stapedial artery (d): SA originates from the ascending pharyngeal artery. (4) Persistent SA from the inferior tympanic artery (originating from the ascending pharyngeal artery) that joined the hyoid artery forming a pharyngo-hyo-stapedial artery (e). This variation corresponds to our case. (5) Persistent stapedial artery with an aberrant carotid artery (f): agenesis of the cervical part of ICA with the intracranial carotid supplied by the inferior tympanic artery.

Figure 2.

(a, b, c, d, e, f) 61-year-old female with recurrent episodes of TIAs (transient right arm weakness and left amaurosis) and negative DWI images (a) at admission. Neck CTA showed a “duplicated” aspect of the left internal carotid artery (ICA) (b, c): yellow arrowhead depicts a normal external carotid artery (ECA); red arrowhead indicates the ICA, while black arrowhead shows an “additional” vessel rising, together with the ascending pharyngeal artery, from the origin of the ICA at the level of the common carotid artery (CCA) bifurcation. This artery is an inferior tympanic artery presenting calcifications and an irregular wall likely related to the atherosclerosis of the vessel (b, c, d black arrowheads). Axial CT scan of the skull base and the petrous bone showing a normal right carotid foramen (red ring) (e); on the left side, red and black arrowheads indicate the left carotid foramen and an enlarged inferior tympanic canaliculus, respectively (e). On the left side, the foramen spinosum was not identified (f) (red star).

Figure 3.

(a, b, c, d) Digital subtraction angiography with lateral (a) view showing the ECA (yellow arrowhead) and the ICA (red arrowhead). A large inferior tympanic artery (presenting a common origin with the ascending pharyngeal artery from the ICA at the bifurcation point of the CCA) courses parallel, laterally and posteriorly to the ICA, joining the hyoid artery that anastomoses with the ICA (a). A persistent stapedial artery (SA), rising from the hyoid artery (hyoido-stapedial artery) supplies the MMA (a). This rare embryological variation is a persistent pharyngo-hyo-stapedial artery. Frontal (b) view depicting the intracranial ICA with an agenesis of the A1 segment. 3D angiography (c) depicting the pharyngo-hyo-stapedial artery: the inferior tympanic artery crosses the skull base through the tympanic foramen (Jacobson’s canal), joining the hyoid artery. The irregular wall of the inferior tympanic artery, likely related to an atherosclerosis of the vessel, could be seen in (b and e) (black arrowheads). Stenting (Xact 8/6 x 40 mm) (Abbott Park, IL, USA) of the inferior tympanic artery was performed. Lateral view (d) showing vessel wall remodeling after stenting (black arrowhead) with a flow competition (red arrow) between the inferior tympanic artery and the ICA (red arrowhead). Slow flow was seen in the original ICA (d), but it was normal during the following angiographic images (e, red arrow). A spasm of the inferior tympanic artery, immediately after the distal part of the stent, was visualized (red arrowhead). 12-months CTA control depicting the patency of the stent (f) and the normal flow in the ICA.

Figure 4.

Schematic representation of the persistent pharyngo-hyo-stapedial artery (modified from Lefournier et al.⁸ and Lasjaunias et al.²).

Case report

A 61-year-old woman was admitted because of recurrent transient right arm weakness and left amaurosis. During the final 10 days, she experienced multiple regressive episodes, lasting 20-30 minutes. On admission, the neurological and physical examinations were normal. Past medical and family history were unremarkable. She was a current smoker. Symptoms were considered as TIAs and Clopidogrel (75 mg) and Aspirin (75 mg) were given. Platelet inhibition was tested with VerifyNow test, showing 43% rate of platelet inhibition (platelet reactivity unit, PRU = 121). In addition, head and neck computed tomography (CT) angiography and brain MR were performed to investigate the cause of the TIAs. DWI sequences excluded recent ischemic lesions (Figure 2(a)). CT angiography depicted a “duplicated” aspect of the left cervical ICA (Figure 2(b) to (d)). Axial CT scan of the skull base and the petrous bone demonstrated a normal right carotid foramen and a duplication of the left one: red and black arrowheads indicate the left carotid foramen and an enlarged inferior tympanic canaliculus, respectively (Figure 2(e)). The ipsilateral foramen spinosum was not identified (Figure 2(f)). Digital subtraction angiography (DSA) from the left common carotid artery (CCA) depicted a normal ICA and ECA, with the presence of an additional parallel vessel running laterally and posteriorly to the ICA, from the cervical segment to the petrous bone (Figure 3(a) to (c)). On the ECA, the middle meningeal artery (MMA) was not identified. This anatomical variation is consisted in a persistent pharyngo-hyo-stapedial artery (Figure 4): a large inferior tympanic artery (presenting a common origin with the ascending pharyngeal artery from the ICA at the origin of the CCA bifurcation) crossed the skull base through the tympanic foramen (Jacobsen’s canal), joining the hyoid artery that anastomoses the ICA at the junction of the vertical and horizontal segments, during its course into the carotid canal (Figure 3(c)). A persistent SA, rising from the hyoid artery (hyoido-stapedial artery), passes through the stapes into the middle ear, supplying the MMA (Figure 3(a) to (c)). Thus, foramen spinosum was absent because of the aberrant origin of the MMA.

DSA showed an irregular aspect of the lumen of the inferior tympanic artery likely related to an atherosclerotic plaque that has been considered the cause of the TIAs. Accordingly, stenting of the vessel was successfully performed with reconstruction of the arterial wall (Figure 3(d) to (f)).

Patient was under dual antiplatelet therapy until the 6-month follow-up. At 12-month follow-up, the stent was patent, the patient was asymptomatic (Figure 4), and single antiplatelet therapy with Aspirin was maintained.

Discussion

To our knowledge, this is the second described case of a persistent pharyngo-hyo-stapedial artery. In the only case reported by Lefournier et al.,⁸ this variant was diagnosed after a hemorrhagic complication of a tympanotomy on a 3-year-old girl. In our case, patient presented recurrent TIAs likely due to an atherosclerotic wall of the proximal segment of the inferior tympanic artery that has been successfully stented. The decision to perform a stenting of the aberrant artery was mainly based on the following considerations: (1) the origin of the persistent pharyngo-hyo-stapedial artery was straight (Figure 3(a) and (c)), and stenting was quite straightforward and fast to perform; (2) in addition, stenting is quite effective to assure vessel wall reconstruction of the atherosclerotic artery. Indeed, patient was completely asymptomatic during follow-up, and the 12-months computed tomography angiography (CTA) showed the patency of both ICA and the pharyngo-hyo-stapedial artery. However, it is important to underline that occlusion of the inferior tympanic artery could a possible alternative option. A temporary flow impairment on the covered ICA was seen immediately after stent deployment (Figure 3(d)), with a complete reconstitution of the flow in the following angiographic images (Figure 3(e)), and during follow-up (Figure 3(f)).

In general, the SA can persist as different embryological variations.⁷ During the embryogenesis, the first and the second aortic arch (also called pharyngeal arches) connect the primordia of the ICA and ECA. The second arch, linked with the ICA, becomes the hyoid artery: the SA is an extension of the hyoid artery (hyoido-stapedial artery), going into the primordium of the stapes (fifth week of gestation) (Figure 1(a)). The first arch participates in the genesis of the internal maxillary artery (IMA) (primitive mandibular artery) and anastomoses with the SA. At this stage, the MMA rises from the SA (Figure 1(a)). During the 10th week of gestation, the SA normally disappears, and the MMA becomes a branch of the IMA, passing through the foramen spinosum (Figure 1(b)). In the typical embryological variation, the hyoido-stapedial artery persists, and the MMA rises from the SA^7,9 (Figure 1(c)). In our case, similarly to the case of Lefournier et al.,⁸ the inferior tympanic branch of the ascending pharyngeal artery enters into the tympanic cavity through the Jacobson’s canal (inferior tympanic canaliculus) and anastomoses with the hyoid artery (which normally regresses, becoming the caroticotympanic artery), that is connected to the ICA (Figure 1(e)). This rare embryological variation is called pharyngo-hyo-stapedial artery and it can explain the “duplicated” aspect of the ICA.

It is interesting to underline that our case of a persistent pharyngo-hyo-stapedial artery was associated with the agenesis of the homolateral A1 (Figure 3(b)). Celebi et al.¹⁰ described a case of a persistent SA associated with an aberrant carotid artery in the left temporal bone, with an hypoplastic A1 segment of the left anterior cerebral artery. The author argued that, despite hypoplasia of the A1 segment is reported in about 10% of autopsies,¹¹ an association with the persistence of the SA can be supposed because the development of the SA and ophthalmic arterial system are closely related.^10,12 However, another hypothesis is that the contralateral ICA supply of both anterior cerebral arteries may result from the ipsilateral hypoperfusion due to the anomalous ICA during embryonic stages.

Other anatomical variations are reported in the literature. The persistent pharyngo-stapedial artery (or pharyngo-tympano-stapedial artery) has been reported by Lasjaunias and Moret.^3,13 In this variant, the hyoid artery has regressed at the level of its origin from the ICA; a persistent SA is supplied by the inferior tympanic artery (coming from the ascending pharyngeal artery) that runs through the inferior tympanic canaliculus (accompanying the Jacobson’s nerve then the middle ear and the stapes) to supply the MMA (Figure 1(d)). This variant has been also described by Jehl et al.¹⁴: the author reported a case of bilateral persistent pharyngo-stapedial arteries revealed during evaluation of a carotid-cavernous fistula.

The SA has been also reported associated with an aberrant carotid artery (Figure 1(f)). In this variant, the inferior tympanic artery seems to be associated with absence of the first portion of the carotid canal (partially or totally absent in its proximal portion) because of the absence of the ICA; the flow in the intracranial carotid is given by the inferior tympanic artery (a branch of the ascending pharyngeal artery) and the carotido-tympanic artery (hyoid artery).^7,14 The persistent SA can be associated to the aberrant carotid artery (30-60%) and originates from the aberrant ICA at the junction of the carotid-tympanic and inferior tympanic arteries (Figure 1(f)).^7,10

Finally, bilateral aberrant ICA (with bilateral persistent SA), and bilateral duplicated internal carotid arteries have been described by Roll et al.¹⁵ in a 5-year-old boy evaluated for a retrotympanic mass.

Knowledge of these anatomical variations is important when planning surgical or endovascular interventions of the carotid artery.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Informed consent

The patients have consented to the submission of these case reports to the journal.

ORCID iDs

Federico Cagnazzo https://orcid.org/0000-0003-3159-1678

Imad Derraz https://orcid.org/0000-0003-0632-3399