A6-year-old Appaloosa mare in good physical condition was referred to the University of Florida Veterinary Medical Center because of acute onset of inappetence and difficulty eating. The mare had undergone prophylactic dentistry 3 months prior to referral. The mare was reported to be 27 days in gestation and was being treated with orally administered altrenogest.a Flunixin meglumine had been administered before referral.
On arrival at the medical center, the right eye had a moderate volume of mucopurulent discharge, and the conjunctiva was hyperemic and swollen. Ophthalmologic examination revealed a fibrotic scar and a small superficial corneal ulcer in the right eye. A CBC and serum biochemical analysis revealed no important findings. Gastroscopic examination revealed no abnormal findings, and results of a reproductive tract examination were consistent with a 23- to 24-day pregnancy.
The mare was treated with flunixin meglumine (1.1 mg/kg [0.5 mg/lb], IV) and housed in a stall overnight for observation. Physical examination on the following morning again revealed no abnormalities except that a large quantity of hay was held in the mouth and the mare grew agitated when examination of the oral cavity was attempted.
Endoscopic examination of the upper portion of the respiratory tract and auditory tube diverticula (guttural pouches) revealed the right stylohyoid bone to be abnormally thick, consistent with THO (Figure 1). In the caudomedial portion of the roof of the left guttural pouch, a yellow and white plaque on the internal carotid artery was detected (Figure 2). Radiography revealed moderate right-sided otitis media, consistent with mild to moderate right-sided THO. On the basis of these findings, THO in the right guttural pouch and mycosis in the left guttural pouch were diagnosed. Medical and surgical treatment options were discussed with the owner, and the horse underwent unilateral ceratohyoidectomy (right side) and surgical occlusion of the left internal carotid artery.
Endoscopic photograph of the right auditory tube diverticulum (guttural pouch) of a 6-year-old horse with dysphagia. Notice that the contours of the right stylohyoid bone are abnormally thick in the area of the tympanohyoid articulation (between arrows).
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the right auditory tube diverticulum (guttural pouch) of a 6-year-old horse with dysphagia. Notice that the contours of the right stylohyoid bone are abnormally thick in the area of the tympanohyoid articulation (between arrows).
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the right auditory tube diverticulum (guttural pouch) of a 6-year-old horse with dysphagia. Notice that the contours of the right stylohyoid bone are abnormally thick in the area of the tympanohyoid articulation (between arrows).
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the medial compartment of the left guttural pouch in the same horse as in Figure 1. Notice that the plaque adherent to the segment of the internal carotid artery coursing through the pouch does not involve the stylohyoid bone.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the medial compartment of the left guttural pouch in the same horse as in Figure 1. Notice that the plaque adherent to the segment of the internal carotid artery coursing through the pouch does not involve the stylohyoid bone.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the medial compartment of the left guttural pouch in the same horse as in Figure 1. Notice that the plaque adherent to the segment of the internal carotid artery coursing through the pouch does not involve the stylohyoid bone.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Preoperative treatment included administration of single doses of potassium penicillin G (22,000 U/kg [10,000 U/lb], IV), gentamicin sulfate (6.6 mg/kg [3 mg/lb], IV), and tetanus toxoid (IM). Flunixin meglumine and altrenogesta treatment were continued, and the corneal ulcer was treated with 1 dose (0.2 mL) of topically administered atropine solution and neomycin-polymyxin-gramicidin ophthalmic solutionb (0.2 mL, q 4 h). The mare was sedated with xylazine hydrochloride (200 mg, IV), and anesthesia was induced with diazepam (12 mg, IV) and ketamine hydrochloride (1.2 g, IV) and maintained with isoflurane in oxygen. An electrolyte solution (5 mL/kg/h [2.3 mL/lb/h], IV) was administered during anesthesia. The horse was positioned in dorsal recumbency and prepared for aseptic surgery.
Ceratohyoidectomy was performed on the right side through a 10-cm incision medial to the right linguofacial vein and centered over the basihyoid bone in a method that has been described.1 The right hypoglossal nerve and lingual branches of the right mandibular and glossopharyngeal nerves were retracted with Penrose drains to protect them during dissection and removal of the ceratohyoid bone. Incisional closure was routine.
With the horse still in dorsal recumbency, a sufficient length of the left internal carotid artery (6 cm) was exposed through a 10-cm-long incision parallel and cranial to the wing of the atlas to locate aberrant branches, a finding that has been reported.2–4 No arterial branches were found; the artery was ligated close to its origin from the common carotid artery, and a small arteriotomy was made distal to the ligature. A 6-F single-end-hole nylon catheterc was introduced rostrally into the internal carotid artery through the arteriotomy and advanced approximately 13 cm. A polyethylene terephthalate fiber–covered, stainless-steel occluding spring embolization coil (5-mm diameter and 5 cm long)c was inserted in the catheter, and a 0.038-inch guidewire was used to push the coil into the artery at the sigmoid flexure. A second embolization coil of the same size was inserted in the same manner until backflow of blood through the arteriotomy ceased. The catheter was withdrawn, and the absence of backflow confirmed arterial occlusion.3,5,6 The artery was ligated distal to the arteriotomy site, and the incision was closed routinely.
The mare recovered from anesthesia without complications and was treated postoperatively with orally administered phenylbutazone (2.2 mg/kg [1.0 mg/lb], q 24 h) and altrenogesta during hospitalization. All physical examination variables remained within reference range. Clinical signs of difficult prehension and mastication were not observed, and the mare was discharged 3 days after surgery. During the 3 weeks after surgery, the owner reported that the mare continued to improve and was able to eat without difficulty.
Fifty-three days after surgery, the mare was returned to the medical center with a 3-week history of dysphagia (including discharge of food material and water from the nostrils) and weight loss. Endoscopy revealed left laryngeal hemiplegia and persistent displacement of the soft palate. The mycotic plaque in the left guttural pouch was more extensive than on the previous examination but had not invaded the structures or vasculature of the lateral compartment (Figure 3). The mare had left-sided Horner syndrome and atrophy of the right side of the tongue (Figure 4) but no tongue protrusion. Because of the worsening clinical condition and unfavorable prognosis, the mare was euthanatized, and necropsy was performed.
Endoscopic photograph of the medial compartment of the left guttural pouch of the horse in Figure 1 53 days after occlusion of the left internal carotid artery. Enlargement of the lesion on the internal carotid artery and extension onto the stylohyoid bone are evident.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the medial compartment of the left guttural pouch of the horse in Figure 1 53 days after occlusion of the left internal carotid artery. Enlargement of the lesion on the internal carotid artery and extension onto the stylohyoid bone are evident.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Endoscopic photograph of the medial compartment of the left guttural pouch of the horse in Figure 1 53 days after occlusion of the left internal carotid artery. Enlargement of the lesion on the internal carotid artery and extension onto the stylohyoid bone are evident.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Photograph of the tongue in the horse in Figure 1 53 days after occlusion of the left internal carotid artery. Notice the wrinkling from muscle atrophy on the right side of the tongue.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Photograph of the tongue in the horse in Figure 1 53 days after occlusion of the left internal carotid artery. Notice the wrinkling from muscle atrophy on the right side of the tongue.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
Photograph of the tongue in the horse in Figure 1 53 days after occlusion of the left internal carotid artery. Notice the wrinkling from muscle atrophy on the right side of the tongue.
Citation: Journal of the American Veterinary Medical Association 229, 12; 10.2460/javma.229.12.1945
The most important gross abnormality was the finding of gray to yellow flocculent material adhered to the roof of the medial compartment of the left guttural pouch and overlying the left internal carotid artery. The left internal carotid artery contained a complete and mature thrombus from the level of the ligature to the cerebral arterial circle, and the 2 microcoils were found incorporated in the thrombus at the first bend of the sigmoid flexure in the internal carotid artery. There was no evidence of an aberrant branch from the internal carotid artery. The right stylohyoid bone was moderately thick close to and involving the articulation with the temporal bone, and the right side of the tongue was atrophied. The right hypoglossal nerve was intact and was surrounded by fibrous tissue at the ceratohyoidectomy site.
Histologic examination of the plaque revealed complete mucosal necrosis with overlying neutrophils; fibrin; bacteria; necrotic debris; and septate, branching fungal hyphae. Histologic examination also revealed extensive inflammation and nerve injury characterized by swollen myelin sheaths, swollen axons, and axonal and myelin degeneration that was extensive and advanced with complete necrosis in some nerve sections. No attempt had been made beforehand to identify specific nerves for histologic examination. A mature and extensive thrombus with areas of fibrous connective tissue filled the lumen of the left internal carotid artery. The right half of the tongue was severely atrophied, and the left half was moderately atrophied, characterized by different degrees of myocyte atrophy within myocyte bundles. Histologic examination confirmed incorporation of the right hypoglossal nerve in the area of fibrosis and granulation tissue at the ceratohyoidectomy site. Mild to moderate atrophy of the left laryngeal muscles was observed, and chronic diffuse and marked bone proliferation of the right stylohyoid bone was detected.
Discussion
Noteworthy findings in this horse were progression of the mycotic lesion in the left guttural pouch and associated development of dysphagia and Horner syndrome after occlusion of the left internal carotid artery. The fungal lesion was associated with clinical, endoscopic, and histologic signs of damage to at least 3 sets of nerves at the site of infection, including the sympathetic nerve trunk or cranial cervical ganglion (resulting in Horner syndrome), the vagus nerve and branches (resulting in pharyngeal and laryngeal dysfunction), the hypoglossal nerve (resulting in multifocal and moderate atrophy of the left half of the tongue), and possibly the glossopharyngeal nerve (resulting in pharyngeal dysfunction). None of these signs had been evident at the time of initial examination. These findings indicated that there was expansion of the mycotic lesion and continued fungal invasion of adjacent structures after occlusion of the underlying artery, a development that was contrary to the claim that vascular occlusion hastens resolution of guttural pouch mycosis and can eliminate the need for antifungal treatment.7 This claim is supported by a report7 involving 6 horses in which endoscopic examination revealed that mycotic lesions began to regress within a week of vascular occlusion and were fully resolved in ≤ 4 months. In a recent report8 involving 31 horses with guttural pouch mycosis that underwent transarterial coil embolization, complete regression of the mycotic lesion was evident between 30 and 180 days in 14 horses that had endoscopic follow-up. Incomplete regression of the lesion was observed in 3 other horses in that study8 that were evaluated 51, 251, and 269 days after vascular occlusion, and 9 of 19 horses that had neurologic signs recovered completely after vascular occlusion, although there was no relationship between rate of resolution and severity of signs. In another study,9 2 of 3 horses treated by means of ligation of the affected internal carotid artery still had a fungal lesion when reexamined endoscopically 18 months after surgery.
Collectively, these findings suggest that the time required for lesion regression after vascular occlusion can vary, as is true for lesions that are not treated.10 The horse in the present report was different from horses in previous reports in that the mycotic lesion was an incidental finding, whereas most lesions must erode to a critical tissue depth before clinical signs of hemorrhage or neurologic dysfunction are induced. This horse therefore represented a suitable test of the efficacy of complete vascular occlusion in resolving the disease process. Although the mare was being treated with a synthetic progesterone for a brief period, it is unlikely that the immunosuppressive effects of the drug were of clinical importance.11
The horse of this report was also unusual because it had 2 apparently unrelated diseases concurrently affecting the guttural pouches. On initial examination, clinical signs and findings led to a diagnosis of rightsided THO as a cause of corneal ulceration and difficulty in prehension and chewing. Although the classic signs of THO attributable to facial nerve and vestibulocochlear nerve dysfunction were absent, corneal ulceration and difficulty chewing have been described in association with this disease.1 The left guttural pouch mycosis was considered to be an incidental finding because none of the clinical signs were referable to this disease at the time of initial examination. The initial favorable response to ceratohyoidectomy was interpreted as further evidence that THO was responsible for the original clinical signs.1
Because the risk of fatal hemorrhage from guttural pouch mycosis on the left internal carotid artery was considered unacceptable by the owner, the affected internal carotid artery was occluded. Although the use of angiography is important for verification of vascular anatomy, assessment of microcoil coiling and placement, and confirmation of complete occlusion of affected vessels,12 microcoils can be placed accurately by a cutdown procedure in the internal carotid artery as was performed in this horse, provided that arterial anatomy is typical.5 At necropsy, we confirmed that the internal carotid artery was free of aberrant branching, that it was the only major artery underlying the mycotic plaque, and that it had been completely occluded by the microcoils.
Ceratohyoidectomy1 was chosen over partial ostectomy of the stylohyoid bone13 because it is considered to be a safer, easier, and more permanent surgical alternative that is free of the risk of eventual healing of the stylohyoid bone and recurrence of clinical signs.1 The goal of ceratohyoidectomy is to decrease the forces generated by tongue movement on the ankylosed temporohyoid joint and thereby prevent future fractures and neurologic signs associated with bony callus encroaching on adjacent cranial nerves.1,13 Injury to the hypoglossal nerve after ceratohyoidectomy in the horse of this report was evident as atrophy of the ipsilateral lingual muscles, a finding that was not evident at initial examination. Despite attempts to protect the hypoglossal nerve from dissection and damage by retractors, the hypoglossal nerve was damaged at the time of surgery or during subsequent compression within the surgical scar.
Vascular occlusion of the artery to which the lesion is attached may not necessarily be a reliable method of resolving guttural pouch mycosis. Although this conclusion is made on the basis of findings in 1 horse, the marked change in that horse's clinical course after vascular occlusion warrants reevaluation of the concept that this surgery hastens resolution of the disease. A more accurate assessment may be that expansion of the lesion and development of new clinical signs are rare after initial clinical signs appear7–10,12 and lesions can resolve over time with or without antifungal treatment.
ABBREVIATIONS
| THO | Temporohyoid osteoarthropathy |
Regu-mate solution 0.22%, Intervet Inc, Millsboro, Del.
Neopolygram, Bausch & Lomb Pharmaceuticals Inc, Tampa, Fla.
Embolization coils, Cook Inc, Bloomington, Ind.
References
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