Divided and reunited maxillary artery: developmental and clinical considerations
- First Online:
- Cite this article as:
- Claire, P.G., Gibbs, K., Hwang, S.H. et al. Anat Sci Int (2011) 86: 232. doi:10.1007/s12565-011-0106-x
- 105 Views
We describe an anatomical variation of the right maxillary artery, discovered during dissection of a male human cadaver. The right maxillary artery bifurcates into unequal superficial (larger) and deep (smaller) divisions. Each division gives off several branches that distribute to the muscles of mastication, facial structures, and teeth. The superficial and deep divisions then reunite to form a complete loop, before giving off terminal branches in the pterygopalatine fossa. The entire arterial loop lies superficial to the branches of the mandibular nerve. This case provides further evidence for a network of vascular rings that surround soft tissue structures in the developing infratemporal fossa. Persistence of all or part of these rings determines adult anatomy. Extreme anatomical variations such as this one may complicate major procedures such as radical maxillectomy, as well as simple procedures such as inferior alveolar nerve blocks.
KeywordsAnatomical variationClinical anatomyInfratemporal fossaMaxillary arteryPterygopalatine fossa
The maxillary artery typically arises as one of the terminal branches of the external carotid artery and traverses the infratemporal fossa, ultimately passing through the pterygomaxillary fissure and terminating in the pterygopalatine fossa (e.g., Moore et al. 2011). The artery is usually described as comprising three parts: (1) a mandibular part that lies medial to the ramus and condylar process of the mandible, (2) a pterygoid part related to the lateral pterygoid muscle, and (3) a pterygopalatine part from which the terminal branches emanate in the pterygopalatine fossa (Gilroy et al. 2008). The first part is typically recognized as giving off branches that pass through bony foramina, including the anterior tympanic, deep auricular, middle meningeal, and inferior alveolar arteries. The second part gives off muscular branches to the muscles of mastication and to the buccinator muscle. The third part is usually represented by a terminal bifurcation whose outer (lateral) division gives rise to the infraorbital and posterior superior alveolar arteries. The inner (medial) division of the terminal bifurcation enters the pterygopalatine fossa to end as the descending palatine and sphenopalatine arteries (Stern 1988).
Variability in the pterygoid part of the maxillary artery is particularly well recognized, as this part of the artery may lie either superficial or deep to the lateral pterygoid muscle (Moore et al. 2011). In studies based on Japanese cadavers, most maxillary arteries (between 89.9 and 94%) were found to lie superficial to the muscle, with only 6.3–10.1% running deep to it (Tadokoro et al. 2008, and references therein). In Caucasians, however, a far higher percentage lie deep to the muscle (between 32 and 57.6%), a phenomenon that led Adachi (1928) to characterize the maxillary artery as a “racial blood vessel” (see also Lasker et al. 1951). Considering variations of both the first and second parts of the maxillary artery suggests at least six broad anatomical types (Kim et al. 2010).
Apart from its relationship to the lateral pterygoid muscle, variations of the maxillary artery include unusual sites of origin for some branches, such as the middle meningeal artery (Klisović et al. 1993) and inferior alveolar artery (Jergenson et al. 2005). The branching pattern of the third (pterygopalatine) part of the maxillary artery has also been classified into as many as five types (e.g., Choi and Park 2003; see also Kim et al. 2010). In a more extreme example of anatomical variability, Tadokoro et al. (2008) recently reported a case of a divided maxillary artery comprising two large branches that passed superficial and deep to the lateral pterygoid. Each branch gave off some of the usual branches of the maxillary artery, with no duplication. We report here a case of a divided right maxillary artery that was discovered during routine dissection of a human cadaver in the 1st-year human gross anatomy curriculum at the New York College of Osteopathic Medicine.
The superficial branch gave rise to the inferior alveolar artery, several small muscular (pterygoid) branches, and the posterior and anterior deep temporal arteries. The deep branch gave origin to the middle meningeal and buccal arteries, then passed superficially through the gap between the two heads of the lateral pterygoid. Here, the deep and superficial branches reunited to form a complete loop. The reunited maxillary artery coursed inferiorly and gave off the posterior superior alveolar artery. Finally, the pterygopalatine part of the maxillary artery turned back superiorly to traverse the pterygomaxillary fissure and give off its terminal branches.
Although this maxillary artery consisted of parts that lay superficial and deep to the lateral pterygoid, both branches lay superficial to the mandibular nerve and its branches. The left maxillary artery was relatively unremarkable, in that it maintained a simple course superficial to the lateral pterygoid muscle and did not bifurcate. Because of damage during the superficial dissection, no anastomoses between the maxillary artery and facial artery could be demonstrated.
The variant of the maxillary artery described here is unusual or unique in several respects. First, the superficial and deep branches, after diverging, coalesced to form a complete circuit. In previous descriptions of divided maxillary arteries, the two branches do not reunite (e.g., Lauber 1901; Tadokoro et al. 2008). Second, both branches of the divided maxillary artery coursed superficial to the branches of the mandibular nerve. Such superficial and deep branches, when previously reported, have run superficial and deep to the nerve, respectively. As in previous descriptions of divided maxillary arteries, however, the superficial and deep branches are separated by the lateral pterygoid muscle. Finally, the deep branch of the divided maxillary artery was the smaller of the two, even though it gave off more branches. This differs from the condition reported by Tadokoro et al. (2008), where the deep branch was considered the larger, “main” branch of the maxillary artery.
Embryologically, the maxillary artery originates as a vascular network within the pterygoid mass of myoblasts, forming rings around the developing branches of the mandibular nerve. Parts of these rings persist while others degenerate, typically leaving only the superficial or deep half of each arterial ring (Hogg et al. 1972). The result is usually a discrete maxillary artery that lies either superficial or deep to the lateral pterygoid, but not both. In the case described by Tadokoro et al. (2008), both superficial and deep parts of these vascular rings persisted, becoming a bifurcated maxillary artery that was separated by both the lateral pterygoid muscle and the mandibular nerve branches. The precursors of the maxillary artery branches described here are ambiguous due to their unusual arrangement. Both branches lie superficial to the mandibular nerve, suggesting that they are derived from the superficial halves of vascular precursor rings. However, both branches also passed deep to the lateral pterygoid muscle, indicating that they may be derived from the deep halves of such rings. The fact that the two halves remain connected, forming a complete ring even in the adult, demonstrates that other variations of the primitive vascular network are possible. Separate rings may encircle the neural and muscular Anlagen of the pterygoid region, and in this case, only the portions of vessels superficial to the nerve may have persisted.
The maxillary artery can be injured inadvertently during interventional craniofacial and dental procedures. An anomalous or unpredictable course of the maxillary artery or one of its many branches may increase that risk of iatrogenic injury. As described by Orbay et al. (2007), accidental arterial puncture can occur during procedures to the subcondylar portion of the mandible, such as internal fixation of mandibular fracture, mandibular osteotomy, and temporomandibular joint arthroplasty. It is also placed at risk during percutaneous blocks of the pterygopalatine ganglion and branches of the trigeminal nerve for both routine dental procedures and ablative treatment of intractable craniofacial pain syndromes (e.g., trigeminal neuralgia and cluster headache). Iatrogenic arterial puncture may lead to profuse, difficult-to-manage bleeding and hematoma. Intra-arterial introduction of local anesthetic agents may produce an array of systemic consequences, including neurological manifestations.
A case of facial arteriovenous fistula (AVF) following percutaneous balloon rhizotomy for the treatment of trigeminal neuralgia was reported by Lesley (2007). This procedure for intractable craniofacial pain, which entails balloon compression to the trigeminal ganglia, was performed on a 56-year-old female who subsequently developed pulsatile tinnitus, facial hypesthesia, headaches and orthostatic dizziness. Magnetic resonance angiography confirmed the diagnosis of facial AVF secondary to iatrogenic laceration of the maxillary artery with direct fistulization with the pterygoid venous plexus.
Inadvertent intra-arterial anesthetic injection into the maxillary artery and its branches has been widely described as a complication of routine mandibular and alveolar nerve blocks in dentistry as well. For example, Wilkie (2000) reported a case of instantaneous uniocular blindness and ophthalmoplegia following a mandibular nerve block for elective extraction of a carious molar in a 45-year-old man. Xylocaine and epinephrine had been introduced into the maxillary artery due to its proximity to the mandibular nerve and variable course in the infratemporal fossa, resulting in neurologic dysfunction. A similar case describes transient visual loss, ptosis, diplopia and facial blanching in a 33-year-old woman who underwent an inferior alveolar nerve block during an endodontic procedure (Webber et al. 2001). In both cases, the direct consequence of arterial puncture was paralysis of structures supplied by branches of the maxillary artery, which produced systemic neurovascular symptoms; the arterial punctures themselves could perhaps have been the result of anomalous arterial courses.
Although uncommon, cases of post-traumatic aneurysms occasionally implicate the maxillary artery with resulting hemorrhage and cranial nerve palsies. Rogers et al. (1995) reported two cases, one being a 20-year-old male who sustained a traumatic Le Fort III type fracture and subsequently experienced two significant episodes of maxillofacial hemorrhage. The other was a 23-year-old male who underwent an elective Le Fort I osteotomy for correction of bilateral cleft lip and palate. Both of these patients were diagnosed using highly selective angiographic imaging modalities and treated with interventional embolization. Variations in the course and branching patterns of the maxillary artery may complicate the diagnosis and repair of arterial injury following trauma or surgical osteotomy.
Space-occupying lesions also can significantly affect the maxillary artery and its branches. Neoplastic lesions found in the infratemporal fossa are most commonly contiguous tumors that have spread from neighboring areas such as the paranasal sinuses, nasopharynx, and the parotid gland. Malignant forms include adenoidcystic carcinoma, adenocarcinoma, squamous cell carcinoma, and rhabdomyosarcoma (Tiwari et al. 2000). Benign masses such as nasopharyngeal fibromas, schwannomas, and meningiomas are also known to invade the infratemporal fossa.
With all tumors, the pathology, grade, and stage of the mass determine the treatment. When surgical removal of tumors from the infratemporal fossa or maxillary sinus is recommended, a radical or total maxillectomy is often the procedure of choice (Choi et al. 2004). During this type of procedure, the maxillary artery is ligated in order to control bleeding and, in turn, becomes the vessel most often damaged upon completion of the surgery (Kim et al. 2010). Failure to accurately characterize the specific anatomy of the maxillary artery could easily lead to intraoperative bleeding, post-operative hemorrhage or a post-operative pseudoaneurysm (Kim et al. 2010). Therefore, a complete understanding of the maxillary artery’s path and structure within the infratemporal fossa of the individual patient is imperative for a successful surgical procedure.
Finally, the maxillary and/or sphenopalatine arteries can be ligated to treat intractable posterior epistaxis (Seno et al. 2009). In rare cases, cross-circulation from the branches of the contralateral maxillary artery has resulted in recurrent bleeding, ultimately requiring ligation of both arteries for complete control. In a patient with the anatomy described here, ligation of the superficial (“main”) branch of the right maxillary artery would leave a patent connection to the sphenopalatine artery via the deep anastomosing branch. Recurrent bleeding might then be misinterpreted as emanating from contralateral vessels, when in fact it would be due to the incomplete occlusion of the complex maxillary system on the right side.
This case differs significantly from other instances of divided maxillary arteries in the relative positions of other soft tissue structures and in the coalescence of the deep and superficial branches to form a complete loop. This configuration suggests a complex embryological origin for the vascular network of the infratemporal fossa. The multitude of anatomical variants that can ultimately develop from this network may complicate surgical and other procedures.
We thank James Giannone for helpful comments that improved the manuscript. This research was supported by the New York College of Osteopathic Medicine Office of Research.