A 15-year-old 24-kg (53-lb) neutered female Staffordshire Bull Terrier-mix (dog 1) was examined by the ophthalmology department at a referral veterinary hospital for progressive exophthalmos, third eyelid protrusion, and periorbital swelling of the left eye (Figure 1), which had been unresponsive to antimicrobial treatment and extraction of the left maxillary molars by the referring veterinarian. Physical examination findings were unremarkable except for the elicitation of signs of pain when the mouth was opened and the presence of a diffusely soft and compressible swelling surrounding the left orbit. Hematologic and biochemical results were unremarkable. Ultrasonographic examination of the periorbital swelling revealed a hypoechoic fluid-filled compartment with a thin, moderately echogenic wall in the left retrobulbar region. The fluid-filled compartment had no evidence of central blood flow as determined by Doppler ultrasonography, and an ultrasound-guided aspirate of the compartment yielded viscous, translucent, straw-colored fluid. On the basis of the clinical and ultrasonographic findings, the mass was initially presumed to be a sialocele arising from the zygomatic salivary gland.
Photograph of a 15-year-old 24-kg (53-lb) neutered female Staffordshire Bull Terrier-mix (dog 1) that was examined because of exophthalmus, third eyelid protrusion, and periorbital swelling of the left eye that failed to resolve following antimicrobial treatment and extraction of the left maxillary molars by the referring veterinarian.
Citation: Journal of the American Veterinary Medical Association 249, 11; 10.2460/javma.249.11.1301
The fluid-filled compartment was percutaneously drained, which alleviated most of the periorbital swelling, and the dog was discharged from the hospital. The clinical signs recurred during the following 3 months, and the dog was referred to the surgery department for further evaluation.
During the second hospital visit, an aspirate of a soft compressible pharyngeal swelling caudal to the left dental arcade yielded > 10 mL of viscous, translucent, straw-colored fluid similar to that obtained from the retrobulbar space 3 months earlier.
The dog was anesthetized, and CTa examination of the head was performed. Transverse CT images of the head were obtained before and after administration of iohexolb (2 mL/kg, IV), a contrast agent. Evaluation of the resulting CT images revealed the presence of a thin-walled, peripherally enhancing, 5.1 × 2.8-cm, multiloculated, fluid-filled mass that was infiltrating the left retrobulbar space. The mass surrounded the left orbital cone, extended caudomedially to the level of the left TMJ, and caused rostrodorsal displacement of the globe. There was focal lysis of the subchondral bone on either side of the TMJ with no associated sclerosis or periosteal proliferation (Figure 2). The left zygomatic salivary gland was large, whereas the right zygomatic salivary gland was considered clinically normal in size.
Precontrast bone algorithm transverse CT image of the head of the dog in Figure 1 obtained at the level of the TMJs. Notice the cystic lesions (arrow) associated with focal lysis of the subchondral bone of the left TMJ.
Citation: Journal of the American Veterinary Medical Association 249, 11; 10.2460/javma.249.11.1301
Surgical exploration of the left periorbital and pterygopalatine fossa was performed. The left orbit was approached by use of a zygomatic arch osteotomy that hinged ventrally. The thin-walled cystic mass was located and incised. The left zygomatic salivary gland was also excised because its lobes were adherent to and confluent with the cystic structure. Gentle pressure on the globe resulted in the expulsion of approximately 10 mL of brown translucent mucinous fluid (Figure 3), which resolved the exophthalmos. The zygomatic arch was repaired with 2 surgical wires, and the subcutis and skin were closed in a routine manner. Postoperative treatment included IV fluid therapy, opioid administration for analgesia, and daily periodic application of cold packs to the left periorbital region. The dog was discharged from the hospital 2 days after surgery. At that time, the dog had minimal exophthalmos and only mild periorbital swelling of the left eye and was prescribed a 7-day course of tramadolc (2 mg/kg [0.9 mg/lb], PO, q 8 to 12 h) and amoxicillin-clavulanic acidd (20 mg/kg [9 mg/lb], PO, q 12 h).
Intraoperative photograph of the dog in Figure 1 obtained during the first surgical biopsy procedure. The left orbit was approached by a zygomatic arch osteotomy. Retro-pulsion of the left globe resulted in extrusion of > 10 mL of brown, gelatinous, viscous fluid from the retrobulbar space.
Citation: Journal of the American Veterinary Medical Association 249, 11; 10.2460/javma.249.11.1301
Histologic examination was performed on specimens of the cystic mass and excised salivary gland. The pseudocystic wall of the mass consisted of slightly plump spindle cells intermingled with scattered macrophages. The mass contained lightly basophilic mucin, and the macrophages that were present had vacuolated cytoplasm. The loose connective tissue that surrounded the mass and the adjoining salivary gland was expanded by the presence of similar mucin, which resulted in wide separation of cells with small hyperchromatic oval nuclei. A few macrophages were scattered between those cells. Mucinous material was observed within the left salivary ducts, and a few scattered plasma cells and lymphocytes were among the lobular interstitial collagen. Those findings were considered to be most consistent with mild sialoadenitis and sialocele.
The owner reported that the periorbital swelling and exophthalmous recurred within 10 days after surgery, but the dog was not returned to the hospital for further evaluation until 10 weeks later. At that time, the dog was anesthetized and an MRIe examination of the head was performed. Short tau inversion recovery fast-spin echo, T1-weighted, T2-weighted, and PDW sequences were obtained in multiple planes both before and after administration of gadopentetate dimegluminef (0.1 mmol/kg [0.045 mmol/lb], IV), a contrast agent. A well-defined, predominately hyperintense, multiloculated, fluid-filled mass surrounding the left TMJ and orbit causing rostrolateral displacement of the globe was observed on T2-weighted and PDW images (Figure 4). Mild contrast enhancement was present in the central portion of the rostroventral aspect of the mass near the TMJ. Loss of cortical margin definition was observed within the bone of the left TMJ. On the basis of those findings, neoplastic or inflammatory salivary system disruption with subsequent sialocele formation was the suggested etiology for the fluid-filled retrobulbar mass. A CT examination was also performed, and results revealed that there was no evidence of metastatic disease in the regional lymph nodes of the head or lungs.
Axial T2-weighted MRI sequence of the head of the dog in Figure 1 that depicts a well-defined, uniformly hyperintense multiloculated cystic mass surrounding the left TMJ and orbital structures. Notice the hyperintense (white) mass visible throughout the left retrobulbar space causing rostrolateral displacement of the globe. The mass was subsequently diagnosed as a myxoma on the basis of histologic evaluation of specimens obtained during a second surgical biopsy procedure.
Citation: Journal of the American Veterinary Medical Association 249, 11; 10.2460/javma.249.11.1301
Two months later, the clinical signs had progressed and were similar to those present at the initial examination by the ophthalmology department. A second surgical exploration was performed with the intent of obtaining a more targeted biopsy specimen than that obtained during the first surgery. The left mandibular and sublingual salivary chains were removed even though the salivary system did not appear to communicate with the thin-walled viscous fluid-filled cystic mass. The caudal aspect of the zygomatic arch was used as a landmark to locate the condyloid process of the mandible ventrally. Dissection revealed a grossly abnormal bulging TMJ joint capsule from which a biopsy specimen was obtained. The TMJ was explored and contained clumped mucinous material, which extended broadly between the fascial planes of surrounding tissues and the retrobulbar space. Biopsy specimens were also obtained from the periarticular tissues, including the lining of the mucin-filled cavities and the palpably soft bone of the adjacent mandibular shaft. Subcutaneous tissues and skin were closed routinely, and the patient recovered well from surgery with postoperative treatments as previously described.
Histologic evaluation of the biopsy specimens revealed the presence of a sheeted matrix of spindle cells, fine collagen, and mucin in varying proportions, dependent on the area examined, with a few macrophages and small lymphocytes scattered throughout the background. Overall, the cellularity of the specimens was increased, compared with that of the original biopsy specimens. Spindle cells were closely apposed to bone that had a slightly irregular surface. Although those spindle cells were uniform in size, they had slightly larger oval nuclei than expected albeit without any evidence of nuclear atypia or mitosis suggestive of malignancy. The histologic findings were most suggestive of myxoma.
Given the infiltrative nature of the lesion and the neurovascular complexity of the periorbital region, surgical excision of the mass was considered unlikely to be curative and likely to be associated with a high risk of morbidity. The owner declined radiation therapy and chemotherapy. Consequently, no further treatment aside from postoperative analgesia was instituted after the second surgery. Review of the dog's records from the referring veterinary practice revealed that it was seen only twice during the subsequent 3 years for problems unrelated to the periorbital mass. Clinical signs of periorbital swelling, exophthalmos, and third eyelid protrusion recurred soon after the second surgery and persisted, but no other problems associated with the temporomandibular myxoma were reported. Thirty-four months after the initial examination at the referral hospital, the dog was determined to have multicentric lymphoma and was euthanized by the referring veterinary practice.
An 11-year-old 34-kg (75-lb) neutered female Labrador Retriever (dog 2) was examined at a referral veterinary hospital because of recent onset of exophthalmos and third eyelid protrusion of the right eye. Review of information provided by the referring veterinarian indicated that a fine-needle aspirate had been obtained from the swollen periorbital region of the right eye, and cytologic evaluation of the aspirate revealed acellular mucoid material. Plain skull radiographs were also obtained, and results were unremarkable (the radiographs were unavailable for review). The dog was treated with amoxicillin-clavulanic acid (dose unavailable) for 2 weeks, which resulted in no improvement of the clinical signs. Results of the initial physical examination performed at the referral hospital were unremarkable except for the fact that the dog was obese in addition to exophthalmos and third eyelid protrusion of the right eye. Hematologic and biochemical results were unremarkable, as were results of 3-view thoracic radiography.
A transverse CT and MRI examination of the head was performed, which revealed the presence of a cystic mass that extended into the retrobulbar area resulting in dorsolateral deviation of the right globe (Figure 5) in a manner similar to that observed for dog 1. The right zygomatic salivary gland and local lymph nodes appeared clinically normal. Results of the CT examination revealed no evidence of metastatic disease in the regional lymph nodes or lungs. On the basis of the clinical signs, cytologic and diagnostic imaging results, and previous experience with dog 1, the diagnosis considered most likely was a myxomatous neoplastic process involving the right TMJ.
Sagittal-plane PDW MRI image of the head of an 11-year-old 34-kg (75-lb) neutered female Labrador Retriever (dog 2) that was examined because of exophthalmus, third eyelid protrusion, and periorbital swelling of the right eye that failed to resolve following antimicrobial treatment. Notice the retrobulbar mass effect associated with extensive, multiloculated hyperintense (white) fluid accumulation radiating from the right TMJ.
Citation: Journal of the American Veterinary Medical Association 249, 11; 10.2460/javma.249.11.1301
Surgical exploration and targeted surgical biopsy of the right TMJ were performed. The right TMJ was grossly thickened and distended with viscous fluid, similar to dog 1. Biopsy specimens were obtained from the right TMJ synovium, lining of the associated cystic mass, and soft mandibular bone. Histologic evaluation of the biopsy specimens revealed the presence of spindle cells of varying density that formed sheets and some loose streams, which were supported by fine collagen and abundant mucin. Bone surfaces had both large areas of new bone formation and regions of lysis. Distinctive histologic features of the lesion included extensive infiltration of spindle cells between existing collagen bundles and mature but irregular bony trabeculae in adjacent bone. The infiltrating cells were mildly pleomorphic with slightly enlarged euchromatic oval nuclei. A few mitotic figures were present but atypia was minimal. Those histologic features were consistent with a low-grade myxosarcoma. Differentiating between a benign and truly myxoid neoplasm can be difficult, and in retrospect, given that the dog had no evidence of metastatic disease, a diagnosis of myxoma may have been more appropriate.
A recheck examination performed 2 weeks after surgery revealed that the right eye was still moderately exophthalmic. A metronomic chemotherapy regime consisting of cyclophosphamideg (15 mg, PO, q 24 h) and piroxicamh (10 mg, PO, q 24 h) was initiated. Six weeks later, results of a biochemical analysis revealed that the dog had abnormally increased BUN (41.5 mg/dL; reference interval, 7 to 26.9 mg/dL) and creatinine (2.6 mg/dL; reference interval, 0.5 to 1.8 mg/dL) concentrations, and the dosage of cyclophosphamide was decreased to 15 mg, PO, every 48 hours and piroxicam was discontinued. At 12 weeks after surgery, the periorbital swelling around the right eye was similar to that prior to surgery. The periocular swelling continued to slowly increase during the subsequent months despite the administration of various chemotherapeutic agents including cyclophosphamide, piroxicam, chlorambucil,i lomustine,j and toceranib.k However, the patient's demeanor remained good, and 10 months after surgery, the dog was clinically well with prominent but fairly stable swelling of the ventral aspect of the right periorbital region. Eleven months after the dog was initially examined at the referral hospital, the periorbital swelling increased dramatically and the dog developed respiratory stertor. The owners elected to forego further treatment, and the dog was euthanized.
Discussion
In dogs, the retrobulbar space includes tissues contained within the orbital fascial cone (optic nerve, extraocular muscles, lacrimal gland, and fat), zygomatic salivary gland, blood vessels, masticatory muscles, and bones that form the orbit. The orbit is closely associated with the nasal cavity and paranasal sinuses medially and dorsally, the cranial cavity caudomedially, and the TMJs and oral cavity ventrally. Lesions arising from any of those structures can result in signs of retrobulbar disease and rostral displacement of the globe.
Typical signs of retrobulbar disease include exophthalmia, protrusion of the third eyelid, conjunctival congestion, chemosis, and signs of pain during opening of the mouth or palpation of the orbit.1 Clinical signs of retrobulbar disease in conjunction with the presence of sparsely cellular, viscous fluid in the periorbital region can be associated with many pathological processes such as zygomatic sialocele, translocation of vitreous humor following trauma to the globe, extension of mucoid fluid from nasal or sinus disease, or myxomatous neoplasia arising from tissues within the orbit.2–4 Dogs with myxomatous neoplasms arising from the TMJ such as the 2 dogs of this report and those described by Dennis3 frequently develop exophthalmos, periorbital swelling, signs of a retrobulbar mass effect, and fluctuant intraoral swelling. Myxomatous neoplasia of the TMJ synovium can be easily misdiagnosed as a zygomatic sialocele; however, zygomatic sialoceles are rare in veterinary patients, and myxomatous disease arising from the TMJ should be considered for any viscous fluid-filled swelling of the periorbital region. Because the recommended treatment and prognosis for patients with a zygomatic sialocele differ greatly from those for patients with myxomatous neoplasia, every veterinary surgeon, ophthalmologist, dentist, radiologist, oncologist, and pathologist should be familiar with how to differentiate salivary gland derangement from TMJ or retrobulbar myxomatous neoplasms.
The overall prevalence of salivary gland disease is < 0.3% in dogs; only 11% of dogs with salivary gland disease have sialoceles, and disease of the zygomatic salivary gland is even rarer.5–7 Review of diagnostic pathology records for 18 dogs with sialocele and 45 dogs with sialadenitis indicated that the zygomatic salivary gland was not involved in the disease process for any of those cases.5 In another study8 of 60 dogs with sialocele, the zygomatic salivary gland was associated with the sialocele in only 1 dog. Sialoceles are generally the result of aberrations in the sublingual salivary gland or its duct that cause sublingual, cervical, or pharyngeal swelling.8–10 Only 20 dogs with sialoceles arising from the zygomatic salivary gland have been reported in the veterinary literature,1,2,8,10–18 and most of those were the result of known causes such as trauma or surgery (n = 6), sialadenitis (8),1,10 or sialolith (1).18 In contrast, most sublingual sialoceles are idiopathic and do not extend into the retrobulbar region.8
The clinical features of the 2 dogs of this report were similar to those described for 5 dogs with myxosarcoma arising from the TMJ in another report.3 Of the 7 dogs described in this report and that previous report,3 3 had an initial histologic diagnosis of zygomatic sialocele, which was subsequently determined to be wrong. For those 3 dogs, the correct diagnosis of myxomatous neoplasia was confirmed when the clinical signs persisted and advanced diagnostic imaging and targeted surgical biopsy were performed.
Myxomatous neoplasias (myxoma and myxosarcoma) are uncommon in dogs. They are derived from pluripotent mesenchymal cells and have been reported at various sites including the heart, spleen, mesentery, thorax, subcutis, intermuscular fascia, and synovia of multiple joints.19 Although rare, myxomatous neoplasia most commonly affects middle-aged, large-breed dogs of both sexes.20,21 Multiple dogs with myxomatous neoplasia arising from a TMJ have been described,3,22 and 1 investigator3 suggests that the TMJ may be a predilection site for myxomatous neoplasia. Grossly, myxomatous neoplasms are typically soft, pale, poorly defined nodules and cystic masses filled with viscous, clearor straw-colored fluid,3 and most have a solid component.22,23 Local osteolysis may be evident3,20 and neoplastic infiltration along facial planes is common.3,19,20,24
Histologic identification of myxomatous neoplasms is often difficult because of the paucity of tumor cells and the potential for myxomatous changes to develop in other types of neoplasms25–27 or for pluripotent cells to differentiate into > 1 cell line.22,23 Myxomatous neoplasms are histologically categorized as benign myxomas, malignant myxosarcomas, or myxoid liposarcomas. However, definitive differentiation among those variants can be difficult27 because all are infiltrative with a low incidence of metastasis and high incidence of local recurrence after surgical excision.3,19–21,25,27
The difficulty of differentiating myxomatous disease from zygomatic sialocele was highlighted by the erroneous initial histologic findings for dog 1 of this report and 2 of the 5 dogs described by Dennis.3 The initial biopsy specimens obtained from all 3 dogs contained salivary tissues and cystic structures consistent with the reactive fibrous tissue lining of a sialocele. A key observation for dog 1 of the present report was that accumulations of mucinous fluid radiated into the surrounding tissues and were not associated with only neoplastic tissues. Obtaining biopsy specimens of the lining of those radiating cystic masses alone can lead to misdiagnosis, particularly if the attending veterinarian has not encountered this disease syndrome before.
Exophthalmos associated with mucoid acellular fluid accumulation in the periocular region and radiographic evidence of lytic changes in the ipsilateral TMJ should prompt surgical biopsy of the tissues associated with that TMJ.3 In that report,3 plain skull radiographs of the dogs with myxomatous neoplasia of the TMJ revealed evidence of permeative osteolysis of the mandibular fossa of the temporal bone and mandibular condyloid process. In general practice, evaluation of plain radiographs of the TMJ and a sialogram of the zygomatic salivary gland and ultrasonographic examination of the retrobulbar region may be helpful in identifying and differentiating myxomatous neoplasia from a zygomatic sialocele. Advanced diagnostic imaging (CT and MRI) can also help differentiate a neoplastic condition from a zygomatic sialocele and may obviate the need for an invasive biopsy procedure given the guarded long-term prognosis associated with myxomatous neoplasia of the TMJ. Magnetic resonance imaging is considered the modality of choice for differentiation of soft tissues and can be useful for defining areas for targeted surgical biopsy.3,22 Notable MRI findings for the dogs of the present report included the presence of well-defined, mucinous, fluid-filled cystic masses radiating from the TMJ between fascial planes and were consistent with MRI findings reported for other dogs with periorbital myxomatous neoplasia.3,19,22,28 Magnetic resonance imaging also aids in the identification of abnormalities of the zygomatic salivary gland and other periocular structures.1,3,18,29 Additionally, sialadenitis, which is often associated with zygomatic sialocele formation, has highly characteristic MRI features10; however, dogs with myxomatous neoplasia can develop discrete sialadenitis as a secondary lesion, as evidenced by dog 1 of the present report.
Because of the anatomic complexity of the infraorbital region and the difficulty associated with differentiating sialoceles from myxomatous disease clinically, we suggest that advanced cross-sectional diagnostic imaging be performed whenever possible before extirpation of any presumed zygomatic sialocele. In our experience, the solid mass component of myxomatous neoplasms is closely associated with the TMJ and can be difficult to see during surgery. It is imperative that the neoplasm be identified by advanced imaging prior to surgery so the area for biopsy and extirpation can be appropriately targeted. Local bone with pathological changes should also be identified and biopsied. Additionally, retrobulbar mucus accumulation associated with extension of sinus and nasal cavity lesions, another differential for retrobulbar mucocele formation, can be evaluated with advanced imaging.
Recurrence of periocular mucoid fluid accumulation within days to weeks after surgical exploration, drainage, and biopsy was observed for both dogs of the present report and all 5 dogs with myxomatous neoplasia of the TMJ in another report.3 In that other report,3 MRI examination of the head was repeated for 2 dogs 5 and 6 months after surgery, and the results were relatively unchanged, compared with those obtained prior to surgery. Because of their location, surgical drainage and biopsy of myxomatous neoplasms of the TMJ should be considered for diagnostic and palliative treatment purposes only. It remains to be determined whether aggressive surgical resection of those types of TMJ masses is beneficial for the survival of the patient. Chemotherapy may be considered as an adjunct treatment to surgery and radiation22; however, some dogs with myxomatous neoplasia of the TMJ have long survival times despite local recurrence following surgical excision or even without surgical excision or adjunctive postsurgical treatment.25 In a study20 of 39 dogs with synovial myxoma arising from various appendicular joints and vertebrae, the mean survival time was 2.5 years (range, 0 to 7 years) after diagnosis. Of those 39 dogs, 13 underwent surgical biopsy of the mass only, 9 underwent whole-limb amputation, and 4 underwent digital amputation.20 Excision of the mass was histologically incomplete for 7 of the 13 dogs that underwent some type of amputation.20 Of the 27 dogs for which follow-up information was available, 19 died or were euthanized for reasons unrelated to the tumor and none died or were euthanized as a direct consequence of the tumor.20 Unfortunately, information regarding the long-term outcomes for a substantial number of dogs with myxomatous neoplasia of the TMJ is lacking, most likely owing to the paucity of reported cases. In general, the slow progression of the disease suggests that, despite mucocele persistence, long-term survival is possible.
The clinical findings, MRI results, and outcomes for the 2 dogs of the present study were consistent with those reported for 5 dogs with myxomatous neoplasia of the TMJ in another study.3 In dogs, myxomatous neoplasia arising from the TMJ is characterized by the presence of multiloculated cystic masses filled with mucinous fluid in the periorbital area and is frequently misdiagnosed as a zygomatic sialocele. Because of the potential for misdiagnosis, the incidence of myxomatous neoplasia of the TMJ may be higher than previously reported. Dogs with myxomatous neoplasia of the TMJ have characteristic features when the results of physical, radiographic, MRI, ultrasonographic, and cytologic examinations are collectively considered, and veterinarians need to be familiar with those features so they can provide owners of affected dogs with appropriate information regarding treatment options and prognosis. The efficacy of radical tumor resection and adjunct radiation therapy and chemotherapy for the treatment of dogs with myxomatous neoplasia of the TMJ is unknown and warrants further investigation.
Acknowledgments
Supported in part by the Australian College of Veterinary Scientists Geoff Robins Research Grant.
The authors thank Drs. Victoria McEwen and Karon Hoffman for technical assistance.
ABBREVIATIONS
| PDW | Proton density |
| TMJ | Temporomandibular joint |
Footnotes
Lightspeed Plus 4-slice CT Scanner, GE Healthcare Inc, Princeton, NJ.
Omnipaque 300, GE Healthcare Inc, Princeton, NJ.
Tramadol, Apex Laboratories Pty Ltd, Somersby, Australia.
Amoxyclav, Apex Laboratories Pty Ltd, Somersby, Australia.
Gyroscan Intera 1 Tesla, Koninklijke Phillips NV, Eindhoven, The Netherlands.
Magnevist, Bayer HealthCare LLC, Whippany, NJ.
Cyclophosphamide, Bova Compounding Chemist, Caringbah, Australia.
Feldene, Pfizer Inc, West Ryde, Australia.
Leukeran, GlaxoSmithKline Australia Pty Ltd, Bronia, Australia.
Lomustine, Bova Compounding Chemist, Caringbah, Australia.
Palladia, Pfizer Inc, West Ryde, Australia.
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