Anatomy of the temporomandibular joint in the cat: a study by microdissection, cryosection and vascular injection

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1 462704JFM / X Journal of Feline Medicine and SurgeryArredondo et al 2012 Original Article Anatomy of the temporomandibular joint in the cat: a study by microdissection, cryosection and vascular injection Journal of Feline Medicine and Surgery 15(2) ISFM and AAFP 2012 Reprints and permission: sagepub.co.uk/journalspermissions.nav DOI: / X jfms.com Jorge Arredondo 1, Amalia Agut 2, María Jesús Rodríguez 2, Ricardo Sarriá 3 and Rafael Latorre 3 Abstract The minute anatomy of the temporomandibular joint (TMJ) is of great clinical relevance in cats owing to a high number of lesions involving this articulation. However, the precise anatomy is poorly documented in textbooks and scientific articles. The aim of this study was to describe, in detail, the TMJ anatomy and its relationship with other adjacent anatomical structures in the cat. Different anatomical preparations, including vascular and articular injection, microdissection, cryosection and plastination, were performed in 12 cadaveric cats. All TMJ anatomical structures were identified and described in detail. A thorough understanding of the TMJ anatomy is essential to understand the clinical signs associated with TMJ disorders, to locate lesions precisely and to accurately interpret the results in all diagnostic imaging techniques. Accepted: 4 September 2012 Introduction Imaging of the temporomandibular joint (TMJ) is an essential part of the diagnostic work-up of dogs and cats with mandibular trauma, dental malocclusion, and pain or inability to open or close the mouth. 1 TMJ ankylosis secondary to fracture, joint luxation, dysplasia and osteoarthritis are relatively common TMJ lesions in cats. 2 Clinical signs associated with TMJ lesions include painful mandibular movement, dental malocclusion and excessive salivation. A frequently concurrent injury associated with TMJ trauma is mandibular symphyseal separation. 3 For decades, radiography has been the primary method of imaging the canine and feline TMJ, but the complex anatomy of the carnivore skull represents a technical and diagnostic challenge for the radiographer and radiologist. 1 In recent years, other diagnostic techniques, such as computed tomography (CT), 1,4 6 have been used to assess the TMJ structures in the cat. It is important to emphasise that a deep knowledge of conventional and sectional TMJ anatomy is a prerequisite to accurately interpret tomographic diagnostic techniques, as well as to achieve good results minimising iatrogenic lesions during corrective surgery procedures. Despite its clinical relevance in small animal practice, the study of the cat TMJ has received little attention and its specific anatomy is poorly documented. The feline TMJ is a synovial condylar joint formed between the condyloid process of the mandible and the mandibular fossa of the temporal bone. 7 The retroarticular process is a caudoventral extension of the mandibular fossa, which cups and prevents the caudal luxation of the condyloid process. At the rostral margin of the mandibular fossa, a pronounced articular eminence is described. 8 The TMJ is stabilised by an articular capsule, which is reinforced by a lateral ligament in the cat. 8 Although the masticatory muscles are also referred to as stabilisers of the TMJ, 7 only the lateral pterygoid muscle has been found to be attached to the medial part of the capsule in the cat. 8,9 1 Department of Anatomy and Physiology, Faculty of Veterinary Medicine and Zootechny, Autonomous University of the State of Mexico, Toluca, Mexico 2 Department of Medicine and Surgery, Veterinary Faculty, University of Murcia, Spain 3 Department of Anatomy and Comparative Pathology, Veterinary Faculty, University of Murcia, Spain Corresponding author: Jorge Arredondo DVM, PhD, Faculty of Veterinary Medicine and Zootechny, El Cerrillo Campus, Toluca, 5000 Mexico jarredondor@uaemex.mx

2 112 Journal of Feline Medicine and Surgery 15(2) Owing to a slight articular surface incongruity, an articular disc has developed, 7 which is a non-vascularised thin membrane. 8 Its entire perimeter is attached to the articular capsule, 7 dividing the articular cavity into two different spaces dorsal and ventral. 8 Descriptions in the literature of the vascular and nervous supply to the TMJ are brief. The only quoted vascular supply to the TMJ is given by the temporomandibular articular branches of the maxillary artery, by the masseteric artery 8,10 and by the masseteric branch of the superficial temporal artery; 10 TMJ innervation is described as coming from sensitive afferent fibres from the lateral trigeminal ganglion of the trigeminal nerve. 11 The aim of this article was to describe, in detail, the clinical anatomy of the TMJ in cats in order to possibly explain its potential relationship with some clinical signs of joint or ear pathology in this species. Materials and methods Animals The project was approved by the Animal Care and Ethics Committee of the University of Murcia. Twelve cats (nine male and three female) from the Murcia University Animal House [mean age 2.5 years (range: ), mean weight 3.5 kg (range: )] underwent euthanasia for reasons other than TMJ disorders. Dental occlusion was considered normal and none of the cats had a history of maxillofacial trauma. A radiographic study of each cat s head consisting of a dorsoventral view, and left and right lateral oblique 10º views was performed to rule out gross osseous pathological conditions affecting this joint. Vascular and synovial injection For vascular injection, the common carotid artery was approached by placing an arterial 5 F introducer sheath (Check-flo; William Cook Europe, Bjaeverskov, Denmark) into the brachiocephalic trunk. Three heads were injected with 2.5 ml red epoxy (Araldit CY 223, Aradur HY2967; Huntsman Advanced Materials Europe, Everberg, Belgium) and then frozen at -30 o C for 48 h. One of them was corroded using sodium hydroxide (NaOH) and the other two were processed by enzymatic digestion using the pancreatin technique. 12 Another four heads were also injected with red latex to enhance arterial structures during microdissection. The TMJ synovial cavities in two heads were injected with 0.2 ml green latex using a 25 gauge 0.5 ml needle. The anatomical landmarks when performing the arthrocentesis were the zygomatic process and the retroarticular process of the temporal bone and the masseteric muscle. Microdissection The four heads injected with red latex were used for microdissection. A stereoscope with magnification of 3.2 (Stemi DV4; Carl Zeiss Microimaging, Barcelona, Spain) was used. The zygomatic arch, the external auditory meatus and the angular process were the principal landmarks when achieving the lateral microdissection. To perform the medial microdissection, heads were sectioned in the midline sagittal plane by cryosection. Each microdissection was started craneocaudally and proceeded from superficial to deeper anatomical structures. Cryosection A total of five heads (two of them with intra-articular latex and three without injection) were frozen at -70ºC for 1 week and sectioned into 3 mm-thick slices. For sectioning, a marker and a high-speed band saw were used. Cryosections were obtained on transverse, sagittal or dorsal planes (one plane per articulation). Plastination After cryosectioning the five specimens were preserved by the P40 and E12 plastination methods. 13,14 Results Microdissections The lateral microdissection (Figure 1A) revealed that the transverse facial artery and the facial nerve were related to the lateral aspect of the TMJ, and the superficial temporal artery and the auriculotemporal nerve were identified to be related caudolaterally to the joint. In a deeper microdissection (Figure 1B), the tight relation between the caudal aspect of the TMJ and the styloauricular muscle was noticed. A reinforcement of the lateral aspect of the articular capsule was also identified. A connective tissue band was differentiated attaching the dorsocaudal aspect of the articular capsule to the lateral part of the annular cartilage in the external ear. In addition, a tendinous band connection running caudally between the caudal part of the angular process of the mandible and the ventromedial aspect of the annular cartilage was seen. After incision of the joint capsule (Figure 1C), the articular disc was observed attached around its entire periphery to the capsule dividing the synovial cavity into two separate spaces dorsal and ventral. The periphery of the disc was irrigated by small branches from the articular temporomandibular artery. On medial microdissection, the close proximity of the TMJ to the tympanic bulla and to the stylohyoid bone was observed. Some fibre bundles of the lateral and medial pterygoid muscles were found attaching to the medial aspect of the articular capsule. The mandibular nerve arose from the oval foramen and was closely related to the joint capsule. Branches from the mandibular nerve, such as the pterygoid, the auriculotemporal, the masseteric and the inferior alveolar nerves, were also close to the medial aspect of the joint.

3 Arredondo et al 113 Figure 1 (A) Lateral view of the left masseter muscle of the cat after removal of the parotid gland. (B) Lateral view of the left TMJ of the cat after removal of the superficial and middle portions of the masseter muscle. (C) Lateral view of the left TMJ of the cat after removal of the superficial and middle portions of the masseter muscle. The joint capsule has been opened in its lateral surface. Note the fixation of the disc to the joint capsule and the vascular supply to the disc given by the TMJ branch of maxillary artery. (D) Medial view of the left TMJ after removal of the pterygoid muscles. (A flat metal tip has been placed between the maxillary artery and the chordae tympani, and forceps have been introduced from the lateral aspect of the joint to push and expose the medial wall of the joint capsule.) (1) Mandibular condyle, (2) mandibular neck, (3) angular process, (4) zygomatic process of temporal bone, (5) tympanic bulla, (6) joint capsule, (7) articular disc, (8) dorsal synovial space, (9) ventral synovial space, (10) temporal muscle, (11) masseter muscle, (12) styloauricular muscle insertion, (13) medial pterygoid nerve, (14) lingual nerve, (15) chordae tympani, (16) inferior alveolar nerve, (17) maxillary artery, (18) superficial temporal artery, (19) transverse facial artery, (20) temporomandibular joint branch of maxillary artery, (21) maxillary branches for the joint capsule, (22) inferior alveolar artery, (23) pterygoid artery, (24) masseteric artery, (25) annular cartilage, (arrowhead) tendinous fascicle between the angular process of the mandible and the tympanic bulla, (*) connective tissue between the joint capsule and the external ear canal The chorda tympani was visualised over the medial aspect of the TMJ capsule. The maxillary artery was closely adjacent to the medial aspect of the capsule where some direct small branches emerged to supply this structure (Figure 1D). Vascular injection TMJ vascularisation was better studied in the enzymatic corrosion specimens (Figure 2). Articular temporomandibular branches which arose from the dorsal part of the maxillary artery supplied the caudolateral and lateral aspect of the TMJ. The masseteric artery covering the rostrolateral aspect of the joint arose from the caudal deep temporal artery. The transverse facial and the masseteric branches from the superficial temporal artery also contributed to the lateral vascularisation of this joint. Medially, the TMJ received small branches from the maxillary, the inferior alveolar, the rostral tympanic and the medium meningeal arteries (Figure 2A, B). All these injected vessels enhanced the peripheral vascularisation identified in the articular disc. Plastination E12 plastinated cryosections showed clear anatomical details. The articular surfaces of the TMJ were congruent. The mandibular condyle was found aligned in the

4 114 Journal of Feline Medicine and Surgery 15(2) Figure 2 (A) Ventral view of an arterial corrosion of a cat s head. (B) Amplified detail of the TMJ area. (1) Mandibular condyle, (2) angular process, (3) zygomatic process of temporal bone, (4) maxillary artery, (5) superficial temporal artery, (6) transverse facial artery, (7) temporomandibular branches of maxillary artery, (8) maxillary branches for the joint capsule, (9) inferior alveolar artery, (10) masseteric artery transversal plane and slightly inclined towards the caudal and medial direction. Its rostral articular surface was observed to be more developed in its lateral half, corresponding with the major expansion of the articular eminence, while the caudal articular surface of the condyle was more extended in its medial part, corresponding with the presence of the retroarticular process. The plastinated sagittal sections through the medial part of the joint showed the proximity with the retroarticular foramen and the middle ear (Figure 3A). The articular disc was identified between the articular surfaces and attached around its entire periphery to the articular capsule. The central part of the disc was slightly thinner than the reinforced periphery. Intra-articular injections of green latex confirmed the division of the articular cavity by the articular disc into two articular compartments dorsal and ventral. Each of them presented a rostral and caudal synovial pouch (Figure 3B). Muscular attachments to the joint capsule and the disc were most easily assessed in plastinated slices. Some fibres of the masseter muscle were fixed onto the rostrolateral, the lateral and the caudolateral aspects of the articular capsule; part of the temporal muscle attached onto the rostromedial aspects of the capsule; the lateral pterygoid muscle was divided into two fascicles rostral and caudal and both inserted into the medial aspect of the capsule; the medial pterygoid muscle was in close relation to the rostromedial aspect of the capsule as the styloauricular muscle was to the caudal aspect of the capsule (Figure 3D). On the sagittal plane it was possible to observe some fibres of the masseter muscle attaching onto the rostral aspect of the articular disc. Plastinated specimens allowed the identification of the pterygoid plexus located medially to both pterygoid muscles and also offered the possibility of a thorough evaluation of the nerves related to the TMJ. The mandibular nerve was adjacent to the medial aspect of the joint. Branches from this nerve close to the articular capsule were the auriculotemporal nerve passing between the TMJ and the styloauricular muscle, the pterygoid nerve running through the lateral pterygoid muscle and medially to the articular capsule, and the masseteric nerve running mediorostrally to the joint and passing through the mandibular notch (Figure 3C). Discussion A thorough knowledge of the TMJ anatomy is essential to understand TMJ pathological processes and to interpret the results of diagnostic imaging procedures accurately. The anatomical techniques used in this study provided outstanding anatomical details of the TMJ and vital related structures. Contrary to the findings of Knospe and Ross, 8 a great congruence between the articular surfaces of the TMJ was observed on sagittal sections in our study. 8 The presence of the articular eminence projecting laterally in this species was confirmed. Knospe and Ross 8 had also previously described the presence of a lateral capsular reinforcement. However, the caudal capsular reinforcement described in this work had not been mentioned before for this species. We consider both reinforcements analogous to the lateral and caudal ligaments referred to in the horse. 15 Minute details of the relationship between the TMJ and the external and middle ear were also observed by microdissection in this study, and were similar to those mentioned for the horse 15 and for humans. 16 The connective tissue between the caudal aspect of the TMJ capsule

5 Arredondo et al 115 Figure 3 Plastinated cryosections of the TMJ in the cat. For each image the plane of section is shown on a dry skull. (A) Sagittal ultrathin section through the medial end of the mandibular condyle. (B) Sagittal section through the mid-point of the mandybular condyle. The articular spaces have been filled with green latex. (C) Transversal section. (D) Dorsal section. (1) Mandibular condyle, (2) pterygoid fovea, (3) coronoid process, (4) zygomatic process of temporal bone, (5) articular eminence, (6) retroarticular process, (7) retroarticular foramen, (8) petrosal portion of temporal bone, (9) external auditory meatus, (10) joint capsule, (11) articular disc, (12) dorsal synovial space, (13) ventral synovial space, (14) rostro-dorsal synovial pouch, (15) rostro-ventral synovial pouch, (16) caudo-dorsal synovial pouch, (17) caudo-ventral synovial pouch, (18) masseter muscle, (19) medial pterygoid muscle, (20) lateral pterygoid muscle, (20 ) rostral head of the lateral pterygoid muscle, (20 ) caudal head of the lateral pterygoid muscle, (21) styloauricular muscle, (22) mandibular nerve, (23) auriculotemporal nerve, (24) masseteric nerve, (25) lateral pterygoid nerve, (26) cerebral fossa, (27) pterygoid plexus, (28) emissary vein of the temporal meatus, (29) annular cartilage, (30) parotid gland and the annular cartilage could be analogous to the disco-malleolar ligament described for humans, 16 but histological studies should be performed to corroborate this finding. We concur with Knospe and Ross 8 in the presence of two articular spaces for this joint dorsal and ventral. However, our results went further and demonstrated that these spaces did not communicate and also showed the presence of rostral and caudal synovial pouches for each compartment. This fact had been described before for the horse, 15 but no mention had been found of the cat or dog. We agree with Nickel et al, 10 who described the lateral vascular supply to this joint by the temporomandibular articular branches of the maxillary artery, the masseteric artery and by the masseteric branch of the superficial temporal artery. No information regarding the irrigation to the medial aspect to the TMJ had, however, been made before. Our study presented new information on this subject for this species and gave more details of the medial supply to the articular capsule by small branches from the maxillary artery and by the inferior alveolar, the rostral tympanic and the medium meningeal arteries, similar to humans. 17,18 We also observed the vascular supply to the periphery of the articular disc which is contrary to the references of Knospe and Ross who mentioned that the articular disc is a non-vascularised structure. 8 Our results showed the relationship of the TMJ with the pterygoid plexus, which had not been mentioned before for this species.

6 116 Journal of Feline Medicine and Surgery 15(2) Of the masticatory muscles, the lateral pterygoid muscle was the only one reported to be attached to the articular capsule of the TMJ in the cat. 8,9 Nevertheless, our results yield new information, as we identified attachments from most of these muscles to the joint capsule, as occurs in the horse. 15 Studies in humans have shown that the lateral pterygoid muscle could have one, two (inferior and superior) or three (inferior, superior or medial) heads; 19 in the dog, the pterygoid muscle only has one head, which seems to be analogous to the inferior head observed in humans. 20 Our results show the presence of two muscular points of origin or heads of the lateral pterygoid muscle, which is new information for this species. 9 Yoshino et al 11 described the TMJ innervation in the cat arising from the mandibular ganglion of the trigeminal nerve. Our results concur with this and also showed the specific relation of the TMJ with the mandibular nerve and its branches, and the proximity with the chorda tympani and the facial nerve. 21 The relationship of the TMJ to other adjacent structures, such as the parotid gland, temporal superficial artery, transverse facial artery, and facial and auriculotemporal nerves, have been described previously in the horse, 15,22,23 but no mention has been found of cats. Conclusions The close proximity of the TMJ with the mandibular nerve, the maxillary artery and the middle ear should be borne in mind during diagnosis and treatment of TMJ pathologies. In addition, the highly detailed information about the sectional anatomy of the TMJ in the cat should be useful for a clear interpretation of images obtained by tomographic diagnostic techniques such as CT and magnetic resonance imaging. Funding This research received no grant from any funding agency in the public, commercial or not-for-profit sectors. Conflict of interest The authors do not have any potential conflicts of interest to declare. Acknowledgements The authors are grateful to M Orenes and J Albarracin for technical support. References 1 Schwarz T, Weller R, Dickie AM, et al. Imaging of the canine and feline temporomandibular joint: a review. Vet Radiol Ultrasound 2002; 43: Gatineau M, El-Warrak AO, Marretta SM, et al. Locked jaw syndrome in dogs and cats: 37 cases ( ). J Vet Dent 2008; 25: Ticer J and Spencer C. Injury of the temporomandibular joint: radiographic signs. Vet Radiol Ultrasound 2005; 19: Maas CP and Theyse LF. Temporomandibular joint ankylosis in cats and dogs. A report of 10 cases. Vet Comp Orthop Traumatol 2007; 20: Beam RC, Kunz DA, Cook CR, et al. Use of threedimensional computed tomography for diagnosis and treatment planning for open-mouth jaw locking in a cat. 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