8-year-old female, Irish Sport Horse, Equus caballus, horse.Unilateral left epistaxis for two months, pallor of oral and conjunctival mucosa, anorexia.
Necropsy revealed dried blood on the muzzle, pallor of conjunctival and oral mucosa, bloody and foamy tracheal and bronchial edema, atrophy of the left laryngeal muscles, bloody content in the stomach, and, on the caudodorsal wall of the medial compartment of the left guttural pouch, a proliferative and hemorrhagic lesion with erosion and thrombosis of the internal carotid artery.
Guttural pouch, internal carotid artery and nerves: The guttural pouch mucosa is severely and diffusely eroded and ulcerated and is replaced by a thick coagulum of fibrin, necrotic debris, degenerate neutrophils and hemorrhage.
The necrotic process extends into, and replaces, up to one third of the internal carotid artery wall and extends within the lumen forming a thrombus.Â Palisading on the surface of the coagulum and in association with the necrotic material there are myriad 5 to 8 Î¼m thick, septate, dichotomously branched, PAS-positive fungal hyphae with parallel walls, often associated with abundant brown pigment and numerous bacterial colonies.Â The remaining two thirds of the arterial wall are characterized by diffuse erosion of the endothelium, severe thickening of the intimal, medial and adventitial layers due to fibroblasts, myofibroblasts and muscular cells proliferation, deposition of collagenous and mucinous extracellular matrix, multifocal fibrin deposition, edema and a multifocal inflammatory infiltrate mainly composed of karyolytic and karyorrhectic neutrophils associated with cellular and nuclear debris (necrosis).
The necrotic process extends also into the subepithelial connective tissue where it is associated with a severe and multifocal to coalescent inflammatory infiltrate composed of neutrophils, macrophages, eosinophils, lymphocytes, plasma cells with occasional fungal hyphae.Â There is severe and diffuse edema and multifocal hemorrhages.Â There is multifocal thrombosis. The nerves within the subepithelial connective tissue are characterized by loss of myelin sheaths, spheroid formation, multifocal areas of coagulative necrosis associated with karyolytic and karyorrhectic neutrophils, macrophages, lymphocytes and plasma cells and severe multifocal hemorrhages.
1.Â Guttural pouch: Eustachitis, severe, diffuse, chronic, ulcerative, fibrino-necrotizing, suppurative and macrophagic with intralesional fungal hyphae and bacterial colonies.
2.Â Internal carotid artery: Arteritis, severe, chronic, fibrino-necrotizing, suppurative and proliferative with thrombus formation and fungal hyphae.
3.Â Nerves: neuritis, severe, multifocal chronic, suppurative and necrotizing with demyelination and multifocal hemorrhages, Equus caballus, horse.
Microbiological culture of the proliferative lesion of the guttural pouch was positive for Aspergillus fumigatus.
Guttural pouch mycosis
Guttural pouch mycosis is a rare fungal disease of the upper respiratory tract of horses.(1,4,11) There is no apparent age, sex, breed or geographic predisposition to this disease although it is seen most frequently in stabled horses in temperate climates during the warmer months of the year and is seldom recorded in warmer climatic regions.Â Guttural pouch mycosis shows no predilection for either the right or the left guttural pouch.(1,6,7,8,10,11)
The pathogenesis has not been ascertained; however, it has been speculated that the mucous membrane layer of the guttural pouch is disrupted by trauma, local inflammation, a primary bacterial infection, or all three.Â This disruption allows opportunistic fungi that are present in the normal equine airway, such as Aspergillus spp., to invade into the deeper tissues, including local arteries and nerves.(5) Different species of Aspergillus can be isolated such as A.Â fumigatus, A.Â versicolor, A.Â nidulans and A.Â niger, but A.Â fumigatus is the most frequently isolated.Â (10)
The clinical signs of guttural pouch mycosis can be explained by the fact that fungal growth, and the inflammation associated with it, has a predilection for the roof of the medial and, occasionally, the lateral compartments of the guttural pouch.Â This area is anatomically associated with the external and internal carotid arteries, internal maxillary artery, glossopharyngeal nerve (cranial nerve IX), vagus nerve (X), spinal accessory nerve (XI), hypoglossal nerve (XII), sympathetic nerves, and stylohyoid bone.(1,4,6,7,10,11) Due to this close association, a horse with guttural pouch mycosis can show signs of epistaxis, dysphagia, parotid pain, abnormal head posture, nasal discharge, head shyness, abnormal respiratory noise, sweating and shivering, Horners syndrome, colic, tongue atrophy and facial paralysis.(1,4,6,7,10,11)
Radiographs and clinical pathologic analyses have been determined to be of little value, as radiographic change with guttural pouch mycosis is minimal and clinical pathologic analyses typically will show an anemia, only if a recent significant bleeding episode has occurred.(11)
Gross pathologic examination of the mycotic guttural pouch characteristically reveals a yellow-brown to black mottled dry diphtheritic membrane with dry, dull white fungal plaques growing on it.(1) This membrane and fungal plaques are typically adhered to the tissues of the roof of the medial pouch and found in association with the internal carotid artery, with possible extension onto the roof of the lateral pouch and ventrally to the stylohyoid bone.(6)
If untreated, spontaneous resolution of guttural pouch mycosis has been observed but it may also result in fatal hemorrhage or irreversible neurological signs.(9) Medical treatment generally gives unsatisfactory and doubtful results.(8,9) Therefore, a surgical treatment option is still recommended and is usually successful even though progression of the disease has been described after surgical treatment.(5,8,9) Surgical treatment consisting of a vascular occlusion for prevention of hemorrhage is the recommended procedure and the occlusion must be performed on the cardiac and cerebral sides of the lesion to prevent hemorrhage.(3,5,8,9,12) Complications reported with this technique include recurrence of moderate to profuse epistaxis and retrograde infection.(8,9)
Guttural pouch: Eustachitis, fibrinosuppurative and necrotizing, diffuse, severe, with multifocal arteriolar and venous vasculitis and thrombosis, necrotizing neuritis, and numerous fungal hyphae.
Guttural pouches are ventral diverticulae of the auditory tubes in equids.Â Bacterial infection of the guttural pouch is referred to as guttural pouch empyema, and is most often caused by Streptococcus equi or other streptococci.Â Compared to guttural pouch empyema, guttural pouch mycosis tends to feature more extensive inflammation that invades deeper tissues, and thus leads to more severe complications.Â In addition to the extension into the nerves and arteries described above, guttural pouch mycosis may also result in osteitis and fusion of the stylohyoid and petrous temporal bones.(2)
Conference participants considered the report of left laryngeal muscle atrophy in this horse, and speculated it may be due to damage to the left recurrent laryngeal nerve from extension of the guttural pouch mycosis.Â In horses, laryngeal paralysis is usually a left-sided hemiplegia caused by idiopathic degeneration of the left recurrent laryngeal nerve.Â Although it is thought that neuritis due to extension from guttural pouch disease may play a role in laryngeal paralysis, the extent to which this occurs has yet to be determined.Â Other possible, but unproven, causes of laryngeal hemiplegia are trauma, vitamin deficiency, or neurotoxins.Â Bilateral laryngeal paralysis is more often due to hepatic encephalopathy and general anesthesia.2
There is some slide variation, with some slides exhibiting the described neuritis, which is considered to be secondary to the profound inflammation in surrounding tissue.Â
1.Â Archer RM, Knight CG, Bishop WJ.Â Guttural pouch mycosis in six horses in New Zealand.Â N Zeal Vet J. 2012;60(3):203209.
2.Â Caswell J, Williams KJ.Â Respiratory System.Â In: Maxie MG, ed.Â Jubb, Kennedy and Palmers Pathology of Domestic Animals.Â 5th ed.Â Vol.Â 2.Â Philadelphia, PA: Elsevier Ltd, 2007;537-538.Â
3.Â Delfs KC, Hawkins JF, Hogan DF.Â Treatment of acute apistaxis secondary to guttural pouch mycosis with transarterial nitinol vascular occlusion plugs in three equids. JAVMA.Â 2009;235(2):189-193.Â
4.Â Dixon PM, McGorum BC, Railton DI, Hawe C, Tremaine WH, Pickles K, et al.Â Laryngeal paralysis: a study of 375 cases in a mixed-breed population of horses.Â Eq Vet J. 2001;33(5):452-458.
5.Â Ernst NS, Freeman DE, MacKay RJ.Â Progression of mycosis of the auditory tube diverticulum (guttural pouch) after arterial occlusion in a horse with contralateral temporohyoid osteoarthropathy.Â JAVMA.Â 2006;229(12):1945-1948.
6.Â Hunter B, Nation PN.Â Mycotic encephalitis, sinus osteomyelitis, and guttural pouch mycosis.Â Can Vet J.Â 2011;52(12):1339-41.
7.Â Kipar A, Frese K.Â Hypoglossal neuritis with associated lingual hemiplegia secondary to guttural pouch mycosis.Â Vet Path. 1993;30(6):574-6.
8.Â Lepage OM, Perron MF, Cador JL.Â The mystery of fungal infection in the guttural pouches.Â Vet J. 2004;168: 6064.
9.Â Lepage OM, Piccot-Cr+ï¿½-ï¿½zollet C.Â Transarterial coil embolisation in 31 horses (1999-2002) with guttural pouch mycosis a 2-year follow-up.Â Eq Vet J. 2005;37(5):430-434.Â
10.Â Ludwig A, Gatineau S, Reynaud MC, Cadore-ï¿½ JL, Bourdoiseau G.Â Fungal isolation and identifiaction in 21 cases of guttural pouch mycosis in horses.Â Vet J. 2005;169(3):457-61.
11.Â Millar H.Â Guttural pouch mycosis in a 6-month-old filly.Â Can Vet J. 2006;47(3):259-61.
12.Â Yoshikazu M, Yu N, Yutaka M.Â Occlusion of the internal carotid artery by means of microcoils for preventing epistaxis caused by guttural pouch mycosis in horses.Â J Vet Med Sci.Â 1999;61(3):221-5.