Embryology & Development
Beginning at week 4, the tubotympanic sulcus develops as an extension of the endodermal epithelium of the first pharyngeal (branchial) pouch and eventually forms the middle ear canal and the eustachian tube. The tubotympanic recess has elongated and constricted to form the primordial tympanic cavity and eustachian tube by week 8. Simultaneously, the expanding end of the tubotympanic sulcus comes into proximity with the medial aspect of the ectodermal first pharyngeal cleft, the primordial external auditory canal. Although intimately related, the two linings remain separated by a layer of mesenchyme known as the pharyngeal membrane. This trilaminar relationship develops into the adult tympanic membrane, which comprises the outer cutaneous, middle fibrous, and inner mucosal layers. As the middle ear cavity expands, the tympanic sinus is created by the pneumatization of already ossified temporal bone. By 9 months, pneumatization of the tympanum and epitympanum is virtually complete. At the same time, the mastoid antrum is formed by the growth of the tympanic cavity into the mastoid portion of the temporal bone. The attachment of the sternocleidomastoid on the temporal bone promotes the formation of the mastoid process. Although the development of the mastoid air cells begins in fetal life, full maturation does not occur until age 2.
Early in development, the middle ear cavity is filled with loose mesenchyme that spans the gap between the primordial tympanic membrane and oval window. However, during the last 2 months of pregnancy, this mesenchyme is systematically reabsorbed, leaving the nearly mature ossicles suspended in the middle ear cavity. Beginning sometime between weeks 4 and 7, a condensation of neural crest ectoderm embedded within the mesenchyme begins to form the ossicles. Meckel cartilage, which is derived from the first pharyngeal (branchial) arch, gives rise to the head of the malleus and the body of the incus (ossicle portions above the tympanic membrane). The remainder of Meckel cartilage develops into the mandible and sphenomandibular ligament (Meckel ligament). The first pharyngeal arch is also associated with the mandibular division of the trigeminal nerve, the muscles of mastication, the tensor tympani muscle, and the tensor veli palatini muscle. The second pharyngeal arch gives rise to Reichert cartilage, which eventually forms the manubrium of the malleus, the long process of the incus, stapes suprastructure, and the tympanic portion of the stapes footplate (ossicle portions below upper limit tympanic membrane). The vestibular portion of the stapes footplate derives from the otic capsule. The facial nerve, the muscles of facial expression, the stapedius muscle, the upper portion of the hyoid bone, and the stylohyoid ligament are also derived from the second pharyngeal arch mesoderm. It is important to note that although the pharyngeal arches are mesenchymal, the ossicles are derived from neuroectoderm that is embedded within the mesenchyme. This partly explains the association between ossicular malformations and disorders of neuroectoderm.
The stapes requires the longest period of development and is therefore the most frequently malformed. The earliest stages of development begin at 4 weeks, and ossification does not occur until week 26. Development of the stapes footplate is induced by a depression on the otic capsule, the lamina stapedialis. This occurs between weeks 6 and 9. Ultimately, the lamina stapedialis becomes the annular ligament and the vestibular portion of the footplate. Failure of this precise association between the stapes footplate and the lamina stapedialis may result in a malformed or atretic oval window.
The primordial stapes is characterized as a chondral ring. Resorption, periosteal erosion, and ossification shape this cartilaginous precursor into an adult-like ossified stirrup. As a result of this developmental process, the adult stapes is fragile; a “plate” of endosteal bone overlying the original layer of cartilage forms the head and base, and thin periosteal bone makes up the crura. This contrasts with the relatively dense incus and malleus, which form from the repeated layering of endosteal bone on a cartilaginous framework. Furthermore, in contrast to the stapes, the malleus and the incus do not undergo morphologic changes, which minimizes the complexity of the shaping process and the potential for error.
The developmental process of the malleus and incus is rapid. The chondral elements reach adult size by week 15 and are fully ossified skeletal structures by week 25. Before the full development of the ossicular ligaments, projections from the endodermal lining of the middle ear cavity help to support the position of the ossicles. Invaginations of the endodermal lining between the ossicles also serve to separate the developing ossicles from each other and from the walls of the tympanic cavity. Failure of this results in ossicular fusion. The articulations between the ossicles develop early, with the incudomalleolar joint forming at 7 weeks. Adult size and relationships are fully established by the 9th month. Full ossicular mobility, however, does not occur until 2 months after birth, when the mesenchyme of the middle ear cavity is fully reabsorbed.
The developing intracranial vasculature originates from six paired aortic arches and their associated arteries. During the 4th week of development, the stapedial artery arises from the hyoid artery (second aortic arch) near the origin of the proximal internal carotid artery (ICA) (third aortic arch). It enters the anteroinferior quadrant of the middle ear and courses over the promontory and through the primordial stapes to form the obturator foramen. It then proceeds anteriorly to pierce the horizontal facial canal and enter the cranial cavity. The artery subsequently divides into an upper (supraorbital) division and a lower (maxillomandibular) division. The supraorbital division provides the vasculature to the orbit and to the supraorbital areas early in fetal development. However, as the ophthalmic artery matures to assume these distributions, the supraorbital division largely involutes and persists as the middle meningeal artery. The maxillomandibular division exits the cranial cavity through the foramen spinosum and contributes to the fetal vasculature of the lower face, as well as to the inferior alveolar and infraorbital areas. By the third month, this division is largely replaced by branches of the external carotid artery. The proximal trunk of the stapedial artery normally atrophies, whereas the distal portion, the middle meningeal artery, persists and is supplied by the external carotid artery.
Vascular Anomalies
- Dehiscence of the jugular bulb may lead to aberrant position within the middle ear.
- This may be asymptomatic or may lead to tinnitus or conductive hearing loss.
- Visible on CT and MRI/MRA.
- Avoidance is most prudent management.
Between the third and fourth weeks of development, paired cardinal veins first appear in the primordial neck. The cranial portion of the anterior cardinal vein ultimately gives rise to the internal jugular vein, whereas the cephalad portion forms the jugular bulb. The sigmoid sinus and the inferior petrosal sinus converge at the jugular bulb, which drains into the jugular vein in the neck. Normally surrounded by a layer of bone within the jugular fossa, the bulb is subject to congenital dehiscence and an aberrant position within the middle ear. A “high-riding” bulb may be defined anatomically as a bulb that rises above the inferior aspect of the bony annulus or the basal turn of the cochlea. It is present in 5% of temporal bone specimens and may be related to the poor pneumatization of the mastoid air cells and middle ear. The bony covering of the bulb may be thin or absent, resulting in dehiscence and protrusion into the middle ear cavity. Tinnitus, vestibular symptoms, and conductive hearing loss due to ossicular, tympanic membrane, or round window compression have been described. However, dehiscent jugular bulbs are often discovered incidentally on otoscopic examination. Typically, a blue mass is seen in the posteroinferior quadrant of the tympanic membrane.
Contrast-enhanced computed tomography (CT) scanning, magnetic resonance imaging (MRI), and magnetic resonance angiography (MRA) help delineate a vascular mass in the middle ear, whereas a high-definition temporal bone CT scan will reveal a bony defect in the floor of the hypotympanum. Venography may differentiate this lesion from other vascular masses in difficult cases. The lack of a fascial covering over the jugular bulb predisposes it to inadvertent laceration during myringotomy. Therefore, avoidance during middle ear surgery represents the most judicious management of these lesions.
- Agenesis, aneurysm, and aberrancy of the intratemporal carotid artery have been described.
- Symptoms include hearing loss, pulsatile tinnitus, aural fullness, otalgia, and vertigo.
- Pulsatile red mass is seen in the middle ear.
- Imaging studies differentiate this from other vascular lesions.
Anomalies of the intratemporal ICA are extremely rare. Typically, there is a female preponderance, and these anomalies first present in the third decade of life with conductive hearing loss, bloody otorrhea, headache, pulsatile tinnitus, or cranial nerve palsies. Conductive hearing loss is due to impingement by the aneurysm on the ossicles or tympanic membrane. Otoscopic exam may reveal a red and pulsatile mass in the middle ear or blood in the external auditory canal. However, it is presumed that most intratemporal aneurysms of the ICA are asymptomatic and go unrecognized.
The ICA normally enters the carotid canal in the petrous portion of the temporal bone medial to the styloid process. The initial vertical segment is anterior to the cochlea, separated from the internal jugular vein by the carotid ridge and from the tympanic cavity by a thin bony wall, 0.5 mm thick. When laterally displaced, this portion of the ICA is found in the hypotympanum with possible extension over the oval window. Displacement of the tympanic membrane and ossicles, as well as erosion of the cochlear promontory, may also be present. Although temporal bone studies have revealed an incidence of <1% of an aberrant carotid artery, gross and micro-dehiscences of the carotid canal have a reported incidence of 7% and 15%, respectively.
Multiple etiologies for an aberrant ICA have been proposed, including (1) agenesis of the bony carotid canal; (2) lateral traction of the ICA by persistent embryonic vessels (eg, stapedial artery); and (3) agenesis of the vertical ICA with compensatory vascular communication from branches of the developing external carotid artery (ECA) system. The latter theory also explains the association of aberrant ICAs with other vascular anomalies, such as persistent stapedial artery (PSA).
The presenting signs and symptoms of an aberrant ICA include pulsatile tinnitus, otalgia, aural fullness, vertigo, hearing loss (61% conductive, 6% sensorineural, and 33% normal) and a pulsating, red mass in the anteroinferior quadrant of the middle ear. There may be a right-sided predominance of this anomaly, and bilateral involvement has been described.
Although hypoplasia, agenesis, aneurysm, and aberrancy of the ICA have all been reported, the low incidence of these lesions demands a high clinical suspicion if disastrous complications are to be avoided. Agenesis and hypoplasia are most often found incidentally on radiographic imaging and may be unilateral or bilateral. These lesions may remain clinically silent since they may be well compensated by the vertebrobasilar, external carotid, or contralateral internal carotid systems. Alternatively, they may present with neurologic symptoms secondary to cerebral insufficiency or aneurysm formation. The latter occurs in 24–34% of cases.
Radiographic imaging is essential and should include high-resolution CT scanning of the temporal bones (Figure 48–1), MRA, and angiography. CT and MRA are noninvasive and may delineate the vasculature and bony anatomy. A temporal bone CT scan in patients with carotid agenesis shows the complete absence of the petrous carotid canal. Angiographic findings include persistent fetal branches of the ECA, such as the hyoid, caroticotympanic, inferior tympanic, and stapedial arteries, as well as other intracranial vascular anomalies. Findings suggestive of an aberrant ICA include the following: (1) a vascular mass in the hypotympanum, (2) an enlargement of the inferior tympanic canaliculus, and (3) a lack of bony canal wall over the vertical ICA. This last feature helps distinguish aberrancy from a glomus tumor.
Several clinicians advocate angiography as the gold standard in the diagnosis of vascular lesions of the middle ear. The classic angiographic finding of an aberrant ICA is identification lateral to a vertical line drawn through the lateral border of the vestibule. Angiography also allows for occlusion testing to define the adequacy of the contralateral carotid circulation if ligation is to be considered.
The rarity of ICA anomalies dictates that a broad differential diagnosis for vascular masses of the middle ear be considered. Also included in this list are glomus tympanicum, glomus jugulare, vascular tumors of the temporal bone, dehiscent jugular bulbs, arteriovenous malformations, and arterial fistulas.
The treatment of aneurysms and aberrancy of the ICA should be determined on a case-specific basis. Most authors agree that if the patient’s only symptom is pulsatile tinnitus or if the patient is asymptomatic, the lesions may be followed expectantly. Indications for definitive therapy include debilitating or progressive symptoms, the prevention of aneurysm formation, embolic phenomenon from an aneurysm, and the destruction of middle ear structures. Aneurysms may be embolized during angiography. Covering an aberrant vessel with fascia, a bone graft, or a Silastic (ie, polymeric silicone) sheet has been described but carries a significant risk of distal ischemia from compression. Inadvertent injury to an aberrant or aneurysmal ICA during myringotomy or middle ear surgery may result in severe hemorrhage. In these situations, the middle ear should be tightly packed. If this fails, surgical ligation of the internal or common carotid artery may be necessary to prevent exsanguination.
- Usually asymptomatic, but may cause pulsatile tinnitus and hearing loss.
- May be associated with other anomalies and may complicate middle ear surgery.
- Retraction or avoidance may be the most prudent management.
A persistent stapedial artery (PSA) is a rare vascular anomaly of the middle ear. The reported prevalence of 0.48% in cadaveric studies of temporal bones is significantly less than the 0.02–0.05% found in surgical series.
Normally atrophied by 3 months of fetal development, the stapedial artery may persist as a 1.5- to 2.0-mm branch of the petrous ICA. As a result of this anomaly, the middle meningeal artery arises from the stapedial artery, and the foramen spinosum is absent. Although pulsatile tinnitus, conductive hearing loss, and sensorineural hearing loss have been described, most cases are clinically asymptomatic and found incidentally at the time of middle ear surgery. Case series have also noted multiple congenital anomalies associated with PSA, including aberrant ICA, Paget disease, anencephaly, anomalous stapes, anomalous facial nerve, thalidomide deformities, and trisomies 13 and 15.
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