Case Report Ulcerative Glossitis and Gingivitis Associated with Foxtail Grass Awn Irritation in Two Horses P

182 EQUINE VETERINARY EDUCATION / AE / APRIL 2012

Case Report Ulcerative glossitis and gingivitis associated with foxtail grass awn irritation in two horses P. J. Johnson*†, A. M. LaCarrubba†, N. T. Messer† and S. E. Turnquist‡ †Department of Veterinary Medicine and Surgery, Veterinary Medical Teaching Hospital, College of Veterinary Medicine, University of Missouri; and ‡Tifton Veterinary Diagnostic Laboratory, College of Veterinary Medicine, The University of Georgia, USA.

Keywords: horse; glossitis; stomatitis; foxtail awns

Summary Clinical findings

Two horses were presented for diagnosis of lethargy, Two horses from a group of 11 horses were presented to salivation, halitosis, dysphagia, bleeding ulcerative the Veterinary Medical Teaching Hospital for treatment of glossitis, gingivitis, and focal bleeding ulceration along ulcerative stomatitis in the month of October. Both were the mucocutaneous junction of the labial commissures. Quarter Horse fillies: Horse 1 was aged 18 months and In both instances, ulceration was attributed to foxtail awns weighed 470 kg and Horse 2 was a 6-month-old weighing (Setaria geniculata) based on microscopic examination 293 kg. They were in normal body condition, and had been of representative tissue biopsies and identification of administered anthelmintics regularly and vaccinated numerous foxtail seed heads in representative samples of appropriately against tetanus, influenza, eastern equine the available hay. The horses recovered and the lesions encephalomyelitis, western equine encephalomyelitis and resolved completely following removal of the affected West Nile viral encephalomyelitis. All 11 horses in the group source of hay. were accommodated at pasture, supplemented with an alfalfa-grass hay mixture and oats. Introduction Horse 1 exhibited signs of lethargy, ptyalism, bleeding from the oral cavity, ulcerated skin at the inferior labii, The ingestion of forage containing yellow bristle grass tongue ulcers and slightly enlarged mandibular lymph (Setaria lutescens), varieties of triticale, and prairie foxtail nodes of approximately 3 days’ duration. In addition to (Setaria geniculata) (Bankowski et al. 1956; McCosker ptyalism, ulcerated skin at the inferior labii, tongue ulcers Horse 2 and Keenan 1983; Turnquist et al. 2001) may cause a and enlarged mandibular lymph nodes, had characteristic, extensive ulceration of the lips, tongue, oral exhibited signs of lethargy, dysphagia (especially with cavity and nasopharynx of exposed horses. Resulting respect to oats), and had reportedly been adopting clinical observations include reduced appetite, focal, unusual head postures during mastication for almost 2 Horse 2 bleeding ulcers along the commissures of the lips, oedema weeks. was heterozygous for hyperkalaemic and chronic proliferative periodontal gingivitis, thickened periodic paralysis and was being treated preventively per os ulcerative plaques along the gingiva, lingual ulceration, with acetazolamide (250 mg/day ). None of bloody ptyalism, halitosis and (with oropharyngeal the remaining 9 horses had exhibited any notable involvement) coughing. In most cases, ulcerative lesions abnormalities. resolve completely following removal of the offending On presentation, both horses were in normal body forage. The extent to which prairie foxtail awn condition and vital signs were normal. Both horses contamination of hay causes ulcerative gingivitis in horses exhibited bloody ptyalism and halitosis. Well-demarcated in the USA may be increasing because recent drought areas of ulceration were evident at the mid-line of the has reduced the availability of better quality forage for lower lip adjacent to the mucocutaneous junction at horses. This report presents the clinical appearance of 2 several locations. The size of these lesions was variable and Fig 1 Missouri horses that were fed forage contaminated with measured 1–3 cm in diameter ( ). The mucocutaneous prairie foxtail awns. junction that was immediately subjacent to ulcerated skin was oedematous. All of the ulcerated areas were *Corresponding author email: [email protected] characterised by a bed of granulation tissue that would

Fig 1: Horse 1: areas of focal, bleeding ulceration at the Fig 3: Horse 1: focal ulceration and linear ulcers at the dorsal mucocutaneous junction of the lower lip and a pyogranulomatous, surface of the tongue. oedematous bleeding ulcer in the gingiva of the lower mandible. Notice periodontal gingival oedema and bleeding. 2. Results of a serum biochemical profile revealed elevated skeletal muscle enzyme activities for both Horse 1 (creatine kinase 652 u/l, rr 90–565 u/l; aspartate aminotransferase 2334 u/l, rr 205–555 u/l) and Horse 2 (creatine kinase 1929 u/l; aspartate aminotransferase 711 u/l). Results of other serum biochemical tests were normal. In order to determine the extent of the ulcers better, Horse 2 was anaesthetised using xylazine hydrochloride (1.1 mg/kg bwt i.v.) and ketamine hydrochloride (2.2 mg/kg bwt i.v.). An endoscopically assisted examination failed to identify further lesions at the caudal aspect of the oral cavity. Representative samples of ulcerative lesions were obtained from the gingiva and tongue for microscopic inspection and histopathology.

Histopathology

Using a dissecting microscope, spiked grass awns Fig 2: Horse 1: periodontal gingival oedema and bleeding were identified protruding as fine hair-like material ulceration. from the surface of formalin fixed biopsy specimens. The histopathological appearance of both specimens was bleed readily when lightly handled. Periodontal gingiva similar and was characterised by predominantly ulcerated was oedematous and erythematous. A thin line of epithelium, with underlying pyogranulomatous and bleeding granulation tissue was identified at the interface eosinophilic inflammation. Inflammatory foci contained of the periodontal gingiva and the incisors (Fig 2). numerous spiked grass awns in transverse, oblique and The tongue of each horse was also affected by areas longitudinal sections (Fig 4). Adjacent epithelium was of focal ulceration, oedema and granulation tissue hyperplastic. ranging in size from 1.0 ¥ 1.0 cm to 3.0 ¥ 3.0 cm (Fig 3). The dorsal surface of each horse’s tongue was also affected Clinical outcome by the presence of numerous linear ulcers that were associated with focal thickening. Most, but not all, of these The clinical diagnosis of foxtail-induced ulcerative linear ulcers appeared to have re-epithelialised and were stomatitis, glossitis and dermatitis was made and the owner not associated with visibly evident bleeding granulation was instructed to send a sample of the hay for examination. tissue. The length of the linear ulcers varied from This revealed the presence of numerous foxtail seed heads 0.3–2.0 cm. that were identified as prairie foxtail (Setaria geniculata) Results of a complete blood count were normal for (Fig 5). Provision of the hay was discontinued and the 2 Horse 1 and mild hyperfibrinogenaemia (5 g/l; reference horses made an uncomplicated and rapid recovery within range [rr] for our laboratory, 2–4 g/l) was identified in Horse 2 weeks without resort to other treatment strategies. The

and horse pox virus (contagious pustular stomatitis) (Monreal et al. 1995; Letchworth 1996; McCluskey and Mumford 2000). The horses in our report had not been exposed to horses from parts of the country in which VS is sometimes reported, and horse pox viral infections have not been reported in the USA. Moreover, the lesions were atypical for either viral aetiology because a vesicular phase was not identified and the lesions were relatively focal. Infection of horses with VS is restricted to the Americas. Although VS is endemic in Central America and northern South America, there have been a number of VS epizootics reported in horses in the western USA in recent years.

Fig 4: Photomicrograph depicting pyogranulomatous and Outbreaks of an ulcerative stomatitis syndrome have eosinophilic inflammation surrounding a longitudinally aligned also been reported amongst horses in Colorado that were grass awn in the lamina propria of the gingiva. The grass awn is similar in some respects to the clinical manifestation of surrounded by numerous neutrophils and a smaller number of VS, but the specific aetiology was not identified (Kim et al. eosinophils. Magnification ¥400. 2000). Based on these reports, it is believed that there may be other viral causes for ulcerative stomatitis in horses that remain to be identified. Commonly used drugs that cause ulcerative stomatitis and gingivitis in horses include the cyclo-oxygenase inhibitors phenylbutazone and flunixin meglumine. Neither horse had been receiving any drug treatment prior to the development of ulceration. Noxious chemical irritants that have been reported to cause ulcerative stomatitis and glossitis in horses as a result of topical contact include cantharidin (blister beetle poisoning) (Schoeb and Panciera 1978) and quassinoids (irritating components of Quassia spp. that are sometimes inadvertently incorporated into wood shavings used for horse bedding; Campagnolo et al. 1995).

Fig 5: Appearance of foxtail seed heads as seen in the mixed Possible immune-mediated diseases that might cause alfalfa-grass hay with which both horses had been fed. ulcerative lesions include pemphigus foliaceus, pemphigus vulgaris, bullous pemphigoid and systemic lupus erythematosus (Williams et al. 1995). However, these referring veterinarian examined other horses under the conditions are rare and it is unlikely that 2 unrelated horses same management and similar lesions were not identified. It would develop immune-mediated ulceration at the same was concluded that the other horses had not been time. consuming the foxtail-contaminated hay. There are few documented reports of grass awn-associated ulcerative stomatitis in horses. Specific Discussion grass species that have been incriminated include yellow bristle grass (Setaria lutescens), varieties of triticale and Ulceration of the oral cavity and mucocutaneous prairie foxtail (Setaria geniculata) (Bankowski et al. 1956; junctional skin of the lips is an uncommon clinical McCosker and Keenan 1983; Turnquist et al. 2001). In our presentation in mature horses. Differential diagnosis should case, the cause of ulcerative stomatitis was identified include erythema multiforme (Marshall 1991), viral infection as prairie foxtail based on the characteristic distribution (Monreal et al. 1995; Bridges et al. 1997; McCluskey and of ulcerative lesions in 2 horses under the same Mumford 2000), drug reaction (Collins and Tyler 1985), management, identification of grass awns at the topical action of a toxic or noxious substance (Schoeb surface of ulcerative lesions by low-powered microscopy, and Panciera 1978; Campagnolo et al. 1995), squamous histopathological demonstration of foxtail seed heads cell carcinoma (Gardner 1996), paraneoplastic in biopsied tissues, and finding abundant prairie foxtail immune-mediated disease (Williams et al. 1995) and grass awns in the horses’ forage. Simple removal of the awns (Bankowski et al. 1956; McCosker and Keenan 1983; contaminated source of hay resulted in rapid resolution Turnquist et al. 2001). of the ulcers within 2 weeks. Failure to eliminate foxtails Viral causes of ulceration in the oral cavity of horses from the forage can lead to severe proliferative gingival include vesicular stomatitis virus (VS), equine viral arteritis hyperplasia (Fig 6).

Bridges, V.E., McCluskey, B.J., Salman, M.D., Hurd, H.S. and Dick, J. (1997) Review of the 1995 vesicular stomatitis outbreak in the western United States. J. Am. Vet. Med. Ass. 211, 556-560. Campagnolo, E.R., Trock, S.C., Hungerford, L.L., Shumaker, T.J., Teclaw, R., Miller, R.B., Nelson, H.A., Ross, F. and Reynolds, D. (1995) Outbreak of vesicular dermatitis among horses at a midwestern horse show. J. Am. Vet. Med. Ass. 207, 211-213. Collins, L.G. and Tyler, D.E. (1985) Experimentally induced phenylbutazone toxicosis in ponies: Description of the syndrome and its prevention with synthetic prostaglandin E2. Am. J. Vet. Res. 46, 1605-1615. Gardner, D.G. (1996) Spontaneous squamous cell carcinomas of the oral region in domestic animals: A review and consideration of their relevance to human research. Oral Dis. 2, 148-154. Kim, L., Morley, P.S., McCluskey, B.J., Mumford, E.L., Swenson, S.L. and Salman, M.D. (2000) Oral vesicular lesions in horses without evidence of vesicular stomatitis virus infection. J. Am. Vet. Med. Ass. 216, 1399-1404. Letchworth, G.J. (1996) Vesicular stomatitis. In: Virus Infections of Equines, 6, Eds: M.C. Horzinek and M.J. Studdert, Elsevier Science BV, Amsterdam. pp 265-279. Marshall, C. (1991) Erythema multiforme in two horses. J. S. Afr. Vet. Ass. 62, 133-136. McCluskey, B.J. and Mumford, E.L. (2000) Vesicular stomatitis and other vesicular, erosive, and ulcerative diseases of horses. Vet. Clin. N. Am.: Equine Pract. 16, 457-469. McCosker, J.E. and Keenan, D.M. (1983) Ulcerative stomatitis in horses and cattle caused by triticale hay. Aust. Vet. J. 60, 259. Fig 6: A mature horse with chronic foxtail grass awn irritation during Monreal, L., Villatoro, A.J., Hooghuis, H., Ros, I. and Timoney, P.J. (1995) oral examination with speculum. Notice marked hyperplastic Clinical features of the 1992 outbreak of equine viral arteritis in Spain. response of gingival mucosa in close proximity to the incisors Equine Vet. J. 27, 301-304. (photograph credit: Dr Dane Frazier, Lebanon, Missouri, USA). Schoeb, T.R. and Panciera, R.J. (1978) Blister beetle poisoning in horses. J. Am. Vet. Med. Ass. 173, 75-77. Turnquist, S.E., Ostlund, E.N., Kreeger, J.M. and Turk, J.R. (2001) The practice of feeding poor quality hay Foxtail-induced ulcerative stomatitis outbreak in a Missouri stable. (contaminated with weeds) is often a direct consequence J. Vet. Diag. Invest. 13, 238-240. of the relative unavailability of higher quality hay for horses Williams, M.A., Dowling, P.M., Angarano, D.W., Yu, A.A., DiFranco, B.J., following periods of protracted drought. Although the Lenz, S.D. and Anhalt, G.J. (1995) Paraneoplastic bullous stomatitis in a horse. J. Am. Vet. Med. Ass. 207, 331-334. characteristic clinical presentation of grass awn-induced stomatitis, as exemplified by the 2 horses in this report, Supporting Information appears to be quite common in mid-western states, it is under-recognised and frequently confused with other Additional Supporting Information may be found in the online version of possible but less common aetiologies. Although the this article: characteristic clinical presentation of grass awn-induced Fig S1: Severe ulcerative gingivitis and dermatitis resulting from foxtail stomatitis, as exemplified by the 2 horses in this report, grass awn irritation. Notice the discrete areas of haemorrhagic appears to be quite common in mid-western states, it is ulceration and granulation tissue along the lip margins, the focal and under-recognised and frequently confused with other elevated areas of bleeding granulation tissue affecting the gingival possible but less common aetiologies. Representative mucosa and ulceration and hyperplasia affecting the periodontal images of other similarly affected horses depicting gingiva. ulcerative lesions associated with the consumption of Fig S2: Severe ulcerative gingivitis and dermatitis resulting from foxtail grass awn irritation (same horse as depicted in Fig S1). Notice the foxtail-contaminated hay have been provided for the discrete areas of haemorrhagic ulceration and granulation tissue along interested reader (Figs S1–S10). the lip margins, the focal and elevated areas of bleeding granulation tissue affecting the gingival mucosa, and ulceration and hyperplasia affecting the periodontal gingiva. Authors’ declaration of interests Fig S3: Severe ulcerative gingivitis and dermatitis resulting from foxtail grass awn irritation (same horse as depicted in Fig S1). Notice the No conflicts of interest have been declared. discrete areas of haemorrhagic ulceration and granulation tissue along the lip margins, the focal and elevated areas of bleeding granulation tissue affecting the gingival mucosa, and ulceration and hyperplasia References affecting the periodontal gingiva. Fig S4: Severe ulcerative gingivitis and dermatitis resulting from foxtail Bankowski, R.A., Wichman, R.W. and Stuart, E.E. (1956) Stomatitis grass awn irritation (same horse as depicted in Fig 6 in the case report). of cattle and horses due to yellow bristle grass (Setaria lutescens). Notice the focal and elevated areas of bleeding granulation tissue J. Am. Vet. Med. Ass. 129, 149-152. affecting the gingival mucosa with ulceration and hyperplasia

affecting the periodontal gingiva associated with the mandibular case depicts a less haemorrhagic and more chronic manifestation of incisors (photograph credit: Dr Dane Frazier, Lebanon, Missouri, USA). the condition. Fig S5: Extensive ulceration, gingival hyperplasia, and foal raised Fig S9: Ulcerative gingivitis and dermatitis resulting from foxtail grass awn areas of bleeding granulation tissue that resulted from eating hay irritation (same horse as depicted in Fig S6). Notice the discrete areas of contaminated with foxtail grass awns. healing ulceration and granulation tissue along the lip margins, and Fig S6: Ulcerative gingivitis and dermatitis resulting from foxtail grass awn chronic gingival hyperplasia affecting the periodontal gingiva. This irritation. Notice the discrete areas of healing ulceration and case depicts a less haemorrhagic and more chronic manifestation of granulation tissue along the dorsal lip margins, the focal and elevated the condition. areas of granulation tissue affecting the gingival mucosa just dorsal to Fig S10: Ulcerative gingivitis and dermatitis resulting from foxtail grass the right maxillary corner incisor. awn irritation (same horse as depicted in Fig S6). Notice the discrete Fig S7: Severe ulcerative gingivitis and dermatitis resulting from foxtail areas of healing ulceration and granulation tissue along the lip margins, grass awn irritation (same horse as depicted in Fig S6). Notice the and chronic gingival hyperplasia affecting the periodontal gingiva. A discrete areas of healing ulceration and granulation tissue along the lip large area of elevated gingival ulceration, granulation, and epithelial margins, the focal and elevated areas of bleeding granulation tissue hypertrophy is evident on the mandibular gingiva. This case depicts a affecting the gingival mucosa and ulceration, and marked severe less haemorrhagic and more chronic manifestation of the condition. chronic gingival hyperplasia affecting the periodontal gingiva. Fig S8: Ulcerative gingivitis and dermatitis resulting from foxtail grass awn Please note: Wiley-Blackwell are not responsible for the content or irritation (same horse as depicted in Fig S6). Notice the discrete areas of functionality of any supporting materials supplied by the authors. Any healing ulceration and granulation tissue along the lip margins, and queries (other than missing material) should be directed to the chronic gingival hyperplasia affecting the periodontal gingiva. This corresponding author for the article.

Continued from page 170

Ireland, J.L., Clegg, P.D., McGowan, C.M., McKane, S.A. and Orsini, J.A., Baird, D.K. and Ruggles, A.J. (2004) Radiotherapy of a Pinchbeck, G.L. (2011) A cross-sectional study of geriatric horses in recurrent ossifying fibroma in the paranasal sinuses of a horse. J. Am. the United Kingdom. Part 2: Health care and disease. Equine vet. J. vet. med. Ass. 224, 1483-1486. 43, 37-44. Springer, T., Elce, Y.A. and Green, E. (2010) Treatment of an osteoblastic Kowalcyzk, L., Boehler, A., Brunthaler, R., Rathmanner, M. and osteosarcoma in an aged gelding. Equine Vet. Educ. 22, 159-162. Rijkenhuizen, A.B.M. (2011) Squamous cell carcinoma of the paranasal sinuses in two horses. Equine vet. Educ. 23, 435-440. Tremaine, W.H. and Dixon, P.M. (2001) A long-term study of 277 cases of equine sinonasal disease. Part 2: Treatments and results of Kreutzer, R., Wohlsein, U., Staszyk, C., Nowak, M., Sill, V. and treatments. Equine Vet. J. 33, 283-289. Baumgartner, W. (2007) Dental benign cemetomas in three horses. Vet. Pathol. 44, 533-536. Walker, M.A., Schumacher, J., Schmitz, D.G., McMullen, W.C., Ruoff, W.W., Crabill, M.R., Hawkins, J.F., Hogan, P.M., McClure, S.R., Vacel, Matthews, N.S., Hartslield, S.M., Sanders, E.A., Light, G.S. and Walker, J.R., Edwards, J.F., Helman, R.G. and Frelier, P.F. (1998) Cobalt 60 M.A. (1993) Repetitive injectable anesthesia in a 27 year old horse. radiotherapy for treatment of squamous cell carcinoma of the nasal Cornell Vet. 83, 219-225. cavity and paranasal sinuses in three horses. J. Am. vet. med. Ass. McGowan, T.W., Pinchbeck, G., Phillips, C.J.C., Perkins, N., Hodgson, 212, 848-851. D.R. and McGowan, C.M. (2010a) A survey of aged horses in Queensland, Australia. Part 1: management and preventative Witte, S., Mueller, P.O.E., Kosarek, C., Webb, J.L. and Howerth, E.W. health care. Aust. vet. J. 88, 420-427. (2012) Collision tumour affecting the paranasal sinuses of a geriatric donkey. Equine vet. Educ. 24, 163-168. McGowan, T.W., Pinchbeck, G., Phillips, C.J.C., Perkins, N., Hodgson, D.R. and McGowan, C.M. (2010b) A survey of aged horses in Witte, T.H. and Perkins, J.D. (2011) Early diagnosis may hold the key to Queensland, Australia. Part 2: clinical signs and owners’ perceptions the successful treatment of nasal and paranasal sinus neoplasia in of health and welfare. Aust. vet. J. 88, 465-471. the horse. Equine Vet. Educ. 23, 441-447.