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Satellite Article Diagnosis and management of guttural pouch mycosis P. J. POLLOCK Division of Companion Animal Sciences, Faculty of Veterinary Medicine, University of Glasgow, 464 Bearsden Road, Glasgow G61 1QH, UK. Keywords: horse; guttural; pouch; mycosis; Aspergillus; epistaxis

History, structure and function of the guttural Despite the risks involved in having guttural pouches, it is pouches fair to say that their presence in the equine head offers the clinician a unique view of vital anatomical structures hidden The equine guttural pouches were originally described in Lyon, from view in most mammals. The accessibility of the pouches France in 1764 by Claude Bourgelat, and since then their within the respiratory tract probably leads to increased risk to presence has been noted in a broad range of other mammals, these vital structures for the horse; nevertheless guttural from forest dwelling mice in South America to marine pouch disease is comparatively rare and, as such, large mammals, rhinoceros and (Turner 1850; Brandt 1863; evidence-based studies investigating disease and dysfunction Ellenberger and Baum 1943; Fraser and Purves 1960; are lacking. Hinchcliffe and Pye 1960). Conditions affecting the equine guttural pouches include There have been recent advances in the understanding of empyema, tympany and the topic of this article, mycosis. the anatomy and physiological role of these structures (Figs 1–3) (Baptiste et al. 2000); however, the function of the Guttural pouch mycosis guttural pouches remains a topic of hot debate. The current Guttural pouch mycosis itself was first described by Rivolta belief holds that the pouches act with the intracranial (1868), who named the condition Gutturomyces equi and cavernous venous sinuses to cool the arterial blood en route to concluded that from the appearance of the fungus and the the brain, protecting this sensitive and vital organ from type of lesion that the organism responsible was an thermal shock. Aspergillus sp. fungus. In the years that followed, further The 2 guttural pouches are expansions of the eustachian cases of the disease were reported by a number of authors tubes that connect the to the middle ear and are located and studies of 22 and 32 horses affected by mycosis (Cook side by side, on midline, dorsal to the pharynx, at the base of the 1966, 1968; Cook et al. 1968) described clinical signs, skull. The rostral extent of the pouches is the basisphenoid bone, treatment and outcome. Since then there has been a great ventrally the pharynx, oesophagus and retropharyngeal lymph deal of interest in this condition and many valuable nodes, caudally the atlanto-occipital joint, laterally, the parotid contributions to the literature. and mandibular salivary glands and dorsally the petrous temporal bone, tympanic bulla and auditory meatus. Clinical signs The pouches are separated by a thin membrane rostrally and by the longus capitis and rectus capitis ventralis muscles caudally. Moderate to severe epistaxis (Fig 4), not associated with The guttural pouches are accessed endoscopically through exercise, is by far the most common clinical sign and follows the pharynx via the guttural pouch ostia (also known as the fungal erosion of the wall of the internal carotid (2/3 of cases) plica salpingopharyngium). The stylohyoid bone separates artery or the external carotid and maxillary artery (or its each pouch into a large medial and smaller lateral branches). A bloody mucoid discharge is common for several compartment. A number of structures are found within the days following an acute haemorrhagic episode. Most affected equine guttural pouches including IX, X, XI and horses have several episodes of moderate haemorrhage prior XII (cranial nerves V, VII, VIII run in close proximity to the to a fatal bleed but this is not always the case. pouches and can be affected by guttural pouch disease) the The second most common presenting sign is cranial cervical ganglion, cervical sympathetic trunk, internal (Fig 5), following damage to the glossopharyngeal nerve and carotid, (and its branches, the caudal pharyngeal branch of the . Affected horses are auricular artery, superficial temporal artery and maxillary dull, drool saliva and have food material present at the nares. artery) stylohyoid bone and temporohyoid joint. In severe cases develops. Damage to EQUINE VETERINARY EDUCATION / AE / november 2007 523

other neurological structures within the pouches can lead to Horses presenting with epistaxis should be treated with pharyngeal paralysis, laryngeal hemiplegia and Horner’s extreme care. Endoscopy of the pharynx will often syndrome (Greet 1987). Affected horses may present with demonstrate blood draining from one of the guttural pouch abnormal respiratory noise in the case of damage to the ostia (Fig 6), and if surgical facilities are not close at hand, no recurrent laryngeal nerve, and miosis, ptosis, enophthalmos attempt should be made to enter the guttural pouch itself as and patchy sweating following damage to the cranial cervical the endoscope may dislodge a clot, potentially leading to a ganglion. fatal haemorrhage. In a number of horses, mucopurulent nasal discharge is In horses displaying clinical signs of dysphagia, the nasal the only obvious abnormality. passages and pharynx may contain food material (Fig 7) and the Other less commonly associated clinical signs include facial dorsal wall (roof) of the pharynx is often collapsed. Permanent nerve paralysis, paralysis of the tongue, abnormal head displacement of the may also be a feature. carriage, head-shaking, sweating, colic, exposure keratitis and If endoscopy of the affected pouch is performed, the corneal ulceration, blindness and parotid pain following mycotic lesion usually appears as a yellow/brown/white and palpation at the base of the ear. Infection of the middle ear, black diphtheritic plaque, although the colour and appearance osteitis of the stylohyoid and petrous temporal bones and can be variable, on the roof of the affected pouch (Figs 8a–c). infection (Dixon and Rowlands 1981) or arthropathy of the If there has been haemorrhage it is often difficult to identify any atlanto-occipital joint (Walmsley 1988) have also been structures within the pouch and identification of the damaged reported as possible sequelae to guttural pouch mycosis. vessel can be challenging. In some cases identification of haemorrhage within either the medial or lateral compartment Aetiology may aid in identification of the damaged vessel. Other endoscopic findings include fistulas between the A number of bacterial and fungal organisms are normal pharynx and the pouches or between the pouches themselves inhabitants of the equine guttural pouches. Guttural pouch and in rare cases adhesions (Fig 9) within the pouches. mycosis is caused by many species of fungi (Lepage 1997; Ludwig et al. 2005), although Aspergillus spp. are implicated Treatment in the vast majority of cases. The mechanism of why this fungus, a normal inhabitant of the equine upper airway and If left untreated guttural pouch mycosis may result in a fatal environment, should become a pathogen in animals that are haemorrhage or irreversible neurological signs. Treatment of not debilitated or immunosuppressed is not understood. guttural pouch mycosis has historically been divided into Obtaining positive cultures of early mycotic lesions is difficult medical and surgical options, or in some cases, a combination and this is complicated by the fact that most horses are not of both. The goal of therapy is aimed at occlusion of the sampled until they have clinical signs, by which time the lesion damaged artery and/or elimination of the fungal plaque using is at an advanced stage. Unfortunately the presence of serum topical antifungal agents. It is postulated that occlusion of the antibodies to Aspergillus spp. detected by ELISA cannot affected artery leads to elimination of the fungus through differentiate between healthy horses and those affected by removal of nutrients in the blood substrate on which the the disease. fungus is maintained (Lane 1989). However, cases of Considerable debate exists as to why the fungus seems to spontaneous regression of fungal plaques and fungal plaques confine itself to specific anatomical areas. The presence of in atypical locations that do not involve blood vessels concomitant disease, such as guttural pouch empyema, low (Freeman 1999) may suggest that this hypothesis is too oxygen tension, low light levels, variations in temperature and simplistic a view of what is probably a complex, dynamic humidity have all been suggested although they lack credible process (Baptiste 2004). evidence. The presence of an aneurysm on the affected artery Therefore, choice of treatment modality may be affected has also been proposed as a factor (Colles and Cook 1983); by the area occupied by the fungus, economic factors or however, angiographic studies suggest that only a small personal preference of the clinician involved. proportion of cases have such vascular changes. Erratic larval A variety of agents have been used in the medical migration (Owen 1974) and prolonged treatment with treatment of mycotic lesions including systemic thiabendazole, antimicrobials and corticosteroids (Guillot et al. 1996) have topical nystatin (Caron et al. 1987), natamycin (Greet 1987), also been suggested as possible causes for fungal overgrowth. miconazole (Lane 1980) and enilconazole and topical, or systemic iodides (Owen and McKelvey 1979; Sherlock et al. Diagnosis 2007). Response to such treatments is slow and it is generally accepted that medical treatments give unsatisfactory or Diagnosis of guttural pouch mycosis is usually based on unpredictable results (Speirs et al. 1995) and are not without history, clinical signs and endoscopy of the pharynx and risk to the horse; however, if the fungal plaque does not guttural pouches. In general, mature horses are more involve a blood vessel and/or there are financial restraints, commonly affected; however, the disease has been recorded medical therapy can be an effective option. It should be noted, in animals as young as 6 months of age. There appears to be however, that if the mycotic lesion is in the proximity of a no breed or sex predilection. blood vessel or neurological structure, fatal haemorrhage or 524 EQUINE VETERINARY EDUCATION / AE / november 2007

Fig 1: Normal anatomy. The normal endoscopic appearance of Fig 4: Moderate epistaxis in the horse. Most affected horses the right guttural pouch. Separated into a larger medial have several episodes of moderate haemorrhage prior to a compartment (MC) and smaller lateral compartment (LC) by the fatal bleed but this is not always the case. stylohyoid bone (SH). The external carotid (EC) is noted within the lateral compartment and internal carotid (IC) within the medial compartment. Cranial nerves IX, X and XII can also be identified within the medial compartment although it should be noted that there is some individual variation with regard to identification of these structures.

Fig 5: Horses presenting with dysphagia drool saliva and often have food material present at the nares. A mucoid discharge may also be apparent.

Fig 2: Swallowing. The guttural pouch ostia open during swallowing. The plica salpingopharyngia are clearly identified (R and L), proximal to the soft palate (SP).

Fig 6: Haemorrhage emanating from the left guttural pouch ostium. If surgical facilities are not readily available, no attempt should be made to enter the affected pouch. Fig 3: Normal ostia. The guttural pouch ostia (L and R) can be identified within the pharynx. The dorsal pharyngeal recess is also identified (D). A number of surgical techniques for the treatment of guttural pouch mycosis have been described, particularly for neurological damage are possible complications of these horses presenting with epistaxis or those with fungal lesions treatments, and horse owners should be warned of these overlying blood vessels. Surgical removal of the fungal plaque possible sequelae prior to instigation of medical therapy alone. has been described, although this treatment has led to fatal EQUINE VETERINARY EDUCATION / AE / november 2007 525

Fig 7: Food material, rostral to the epiglottis, and haemorrhage emanating from the left guttural pouch ostium is noted in this horse which presented with a history of dysphagia and epistaxis. Fig 9: Severe adhesions were noted in this guttural pouch, 6 months following successful treatment and resolution of haemorrhage and neurological signs (Johnson et al. 1973) and guttural pouch mycosis. is therefore not recommended. Ligation of the at its origin, at the the face and orally into the palatine artery in order to occlude level of the carotid trifurcation in the parotid region (Johnson all possible sources of retrograde haemorrhage. The balloon et al. 1973; Owen 1974; Greet 1987), although effective at is then removed approximately 14 days after the reducing the risk of fatal epistaxis, is not an effective initial surgical procedure (Freeman and Donawick 1980a,b; treatment option alone, because blood flow in the circle of Freeman et al. 1989). Problems encountered with this Willis maintains arterial blood pressure in the affected technique include the presence of a catheter within the oral segment of the artery, which can lead to retrograde fatal cavity, failure of the balloon section, catheter breakage, haemorrhage (Freeman and Donawick 1980a,b). For this incisional complications, wound infections, prolonged reason a number of techniques were developed to occlude anaesthetic periods, the requirement for a second surgery and blood flow on both sides of the affected portion of artery. the potential for a cosmetic blemish caused by the presence of Open surgical access and ligation of the affected vessels is the catheter subcutaneously (Leveille et al. 2000). A similar difficult or impossible, depending on the vessel affected, and technique using with detachable balloons does not can lead to complications through damage of other vital require a second surgery (Cheramie et al. 1999). structures. As a result several closed surgical techniques have More recently, occlusion of both sides of the affected vessels been developed including balloon tipped catheter placement, using the closed technique of transarterial coil embolisation of in which a catheter is passed into the affected blood vessel at the internal and external carotid and maxillary arteries has been a distant site, peripherally, and passed beyond the lesion, described (Matsuda et al. 1999; Leveille et al. 2000; Lepage and where the balloon is inflated, thereby occluding blood flow. A Piccot-Crezollet 2005). Intravascular platinum microcoils or ligature is then placed on the cardiac side of the vessel where Dacron, fibre-covered, stainless steel spring embolisation coils it is accessible at the level of the carotid trifurcation. If the are passed into the affected vessel under fluoroscopic guidance, maxillary artery in the lateral compartment of the guttural using contrast angiography (Fig 10), through an arterial pouch is affected by a mycotic lesion, a balloon must be catheter. All the surgical procedures described are technically passed into the transverse facial artery on the lateral aspect of demanding, and require specialised equipment and an excellent a) b) c)

Fig 8: The mycotic lesion usually appears as a yellow/brown/white and black diphtheritic plaque, although the colour and appearance can be variable, on the roof of the affected pouch. 526 EQUINE VETERINARY EDUCATION / AE / november 2007

Summary

In summary guttural pouch mycosis is an uncommon but potentially fatal disease affecting horses of all ages, breeds and sex. The most common presenting signs include epistaxis and dysphagia. The condition is caused by invasion of the wall of one or both guttural pouches by Aspergillus spp. fungus, which leads to damage of vital vascular and neurological structures. Surgical treatments carry the highest and most predictable success rates and involve occlusion of the damaged blood vessels. Further investigation into the causative agent is needed if we are to understand why this normal inhabitant of the airway becomes pathological in some horses, what the predisposing factors are and to allow early diagnosis to more effectively prevent fatal haemorrhage and the development of career and Fig 10: A contrast arteriogram obtained during surgery for life-threatening neurological derangements. embolisation coil placement. Several coils can be seen within the vessels proximal to the carotid trifurcation. Acknowledgements knowledge of vascular anatomy. These techniques are further The author gratefully acknowledges the help of Dr Keith complicated by the fact that a percentage of horses exhibit Baptiste, Dr Jim Schumacher and Mr Justin Perkins in the variations in the vascular anatomy of the affected vessels, preparation of this article. particularly the carotid trifurcation (Freeman et al. 1993). For this reason, the use of most of the surgical procedures described References is confined to specialist practices. Complications associated with surgical treatment include Baptiste, K.E. (2004) The mystery of guttural pouch mycosis: failure to prevent epistaxis and the development of the paradox of advancing knowledge of a rare disease. Vet. J. 168, 1-2. neurological disorders and blindness following surgery. The mechanism for the development of these complications is not Baptiste, K.E., Naylor. 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Ass. 191, 345-349. upon early recognition and prompt intervention by attending Cheramie, H.S., Pleasant, R.S., Robertson, J.L., Moll, H.D., Freeman, clinicians. Identification of cases presenting with clinical signs D.E. and Carrig, C.B. (1999) Evaluation of a technique to occlude of epistaxis or fungal plaques overlying major vessels should the internal carotid artery of horses. Vet. Surg. 28, 83-90. be considered an emergency and the owners, trainers or Colles, C.M. and Cook, W.R. (1983) Carotid and cerebral angiography keepers informed of the potentially fatal outcome. Affected in the horse. Vet. Rec. 19, 442-428. animals should be moved to a suitable establishment where Cook, W.R. (1966) Guttural pouch mycosis. Vet. Rec. 78, 396-398. treatment is available. Cook, W.R. (1968) The clinical features of guttural pouch mycosis in Transarterial coil embolisation techniques are the currently the horse. Vet. Rec. 83, 336-345. accepted gold standard for treatment, and using this technique Cook, W.R., Campbell, R.S.F. and Dawson, C. (1968) The pathology Lepage and Piccot-Crézollet (2005) reported a survival rate of and aetiology of guttural pouch mycosis in the horse. Vet. Rec. 87%, with 71% of horses returning to a satisfactory level of 83, 422-428. exercise. Mycotic lesions generally show complete regression Dixon, P.M. and Rowlands, A.C. (1981) Atlanto-occipital joint infection associated with guttural pouch mycosis in a horse. Equine vet. J. within 4 months of treatment with this technique. 13, 260-262. A poor prognosis should be given if there are clinical signs Ellenberger, W. and Baum, H. (1943) Handbuch der vergleichenden of neurological disease, particularly dysphagia, prior to Anatomie der Haustiere. Springer, Berlin. treatment. In some horses with neurological deficits, including Fraser, F.C. and Purves, P.E. (1960) Hearing in Cetaceans. Bulletin of evidence of left recurrent laryngeal nerve dysfunction and the British Museum (Natural History) 7, 1-140. Horner’s syndrome, prior to treatment, complete resolution Freeman, D.E. (1999) Guttural pouch. In: Equine Surgery, 2nd edn., does occur but can take up to 18 months. Eds: J.A. Auer and J.A. Stick, W.B. Saunders, Sydney. pp 372-392. EQUINE VETERINARY EDUCATION / AE / november 2007 527

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