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Original Article

Veterinary Pathology
1-5
Oral Lesions in Captive Nondomestic Felids ª The Author(s) 2020
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With a Focus on Odontogenic Lesions DOI: 10.1177/0300985820943539
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Katherine L. Scott1, Michael M. Garner2, Brian G. Murphy3 ,


and Elise E. B. LaDouceur1,2

Abstract
Odontogenic lesions are well described in domestic cats, but published literature describing these lesions in nondomestic felids is
limited. This study reports oral lesions in 109 captive, non-domestic felids. Ten cases of odontogenic lesions were diagnosed,
including 9 with fibromatous epulis of periodontal ligament origin (FEPLO) and one odontogenic cyst in a cougar. FEPLO was
common in lions. FEPLO did not recur after surgical removal in any of the 3 cases for which follow-up information was available.
Increased occurrences of oral papillomas in snow leopards and eosinophilic granulomas in tigers were identified, which is con-
sistent with the reported literature. With the exception of oral papillomas in snow leopards and FEPLO in lions, the spectrum of
oral lesions in nondomestic felids was similar to what is reported in domestic cats, with squamous cell carcinoma being the most
common oral malignancy, and stomatitis/gingivitis/glossitis accounting for approximately one third of all cases. Rare diagnoses with
one case each included hemangioma, fibrosarcoma, melanoma, cleft palate, and glossal amyloidosis.

Keywords
nondomestic felids, odontogenic, histology, retrospective, fibromatous epulis of periodontal ligament origin, peripheral odonto-
genic fibroma

Odontogenic lesions are well described in animals. Although neoplasms; inflammation included all lesions that were com-
classification schemes in veterinary oral pathology generally posed primarily of inflammation; odontogenic lesions included
closely follow those in human oral pathology, there are nota- all proliferative odontogenic lesions and odontogenic cysts;
ble exceptions of lesions that may be unique to animals, such other diagnoses included non-odontogenic developmental and
as canine acanthomatous ameloblastoma and canine odonto- deposition disorders. Hematoxylin and eosin (HE)-stained his-
genic parakeratinized cyst.1,5,7,13 While recent advances have tologic sections from formalin-fixed paraffin-embedded tissue
been made in the nomenclature and classification of odonto- blocks were reviewed and the diagnoses made by one pathol-
genic tumors in animals, reports on the incidence of odonto- ogist (MMG). Cases of odontogenic lesions were reviewed
genic lesions among various species are generally sparse, histologically by 2 additional pathologists (BGM and EEBL).
particularly for nondomestic species. A recent review of For odontogenic lesions, additional case information, including
reported odontogenic tumors in domestic animals is avail- clinical history, outcome, radiographs, and gross photographs,
able.1 Reports of odontogenic lesions in nondomestic species, was requested from clinicians, and collated when available.
including nondomestic felids, are usually single cases, and are
generally uncommon.
The purpose of this study is to report oral lesions diagnosed Results
in nondomestic felids in human care and compare findings to Oral lesions were diagnosed in 109 captive felids, including 36
those in domestic cats and current literature. This study focused snow leopards (Panthera uncia), 25 tigers (Panthera tigris), 13
on odontogenic lesions, which are not commonly reported in lions (Panthera leo), 12 cheetahs (Acinonyx jubatus), 5 cougars
these animals.

1
Joint Pathology Center, Silver Spring, MD, USA
Materials and Methods 2
Northwest ZooPath, Monroe, WA, USA
3
For this retrospective study, the Northwest ZooPath (Monroe, University of California, Davis, CA, USA
WA) archives were searched for all diagnoses in felids. All
Corresponding Author:
diagnoses of oral lesions were summarized in table format. Elise E. B. LaDouceur, Joint Pathology Center, 606 Stephen Sitter Ave, Silver
Diagnoses were grouped into the following categories: non- Spring, MD 20910, USA.
odontogenic neoplasia included benign and malignant Email: elise.e.ladouceur.civ@mail.mil
2 Veterinary Pathology XX(X)

Table 1. Oral Lesions in 109 Captive Nondomestic Felidsa.

Diagnosis Species affected

Non-odontogenic neoplasia (56; 51%)


Papilloma (39) Snow leopard (30), lion (4), cheetah (3), cougar (1), tiger (1)
SCC (14) Snow leopard (5), tiger (3), lion (2), cougar (1), leopard (1), lynx (1), ocelot (1)
Other (3) Lion (1; hemangioma), ocelot (1; fibrosarcoma), tiger (1; melanoma)
Inflammation (41; 38%)
Stomatitis/gingivitis/glossitis Tiger (12), cheetah (8), leopard (3), cougar (2), lion (2), lynx (1), fishing cat (1), Geoffrey’s cat (1), jaguar
(non-eosinophilic) (33) (1), serval (1), snow leopard (1)
Eosinophilic granuloma (8) Tiger (7), leopard (1)
Odontogenic lesions (10; 9%)
FEPLO (9) Lion (4), jaguar (2), bobcat (1), cheetah (1), serval (1)
Odontogenic cyst (1) Cougar (1)
Other diagnoses (2; 2%)
Cleft palate (1) Tiger (1)
Glossal amyloidosis (1) Ocelot (1)
Abbreviations: SCC, squamous cell carcinoma; FEPLO, fibromatous epulis of periodontal ligament origin.
a
Data in parentheses are number of cases.

(Puma concolor), 5 leopards (Panthera pardus), 3 jaguars mesenchymal cells embedded in fibrous tissue composed of
(Panthera onca), 3 ocelots (Leopardus pardalis), 2 lynx finely bundled collagen with regularly spaced, dilated, small-
(Lynx sp.), 2 servals (Leptailurus serval), 1 Geoffrey’s cat caliber blood vessels (Figs. 2, 3). These lesions often had
(Leopardus geoffroyi), 1 bobcat (Lynx rufus), and 1 fishing cat variable amounts of interspersed odontogenic epithelium, char-
(Prionailurus viverrinus; Table 1). Each animal was diagnosed acterized by small to moderately sized rests or branching plexi-
with only one oral lesion. The most common diagnostic cate- form ribbons of epithelial cells with a peripheral palisade of
gory was neoplasia (56/109; 51%). Papillomas were the most columnar cells in which the nuclei were frequently antibasilar,
common neoplasm diagnosed with 39 cases, and were most with rare cytoplasmic basilar clearing. Islands of cemento-
common in snow leopards (30/39 cases; 77%). At least 19 of osseous matrix (COM) were variably present, and occasionally
the 39 papilloma cases had evidence of viral cytopathic effects abundant. COM demonstrated histologic features consistent
consistent with viral etiology (ie, large cytoplasmic keratohyalin with both osteoid and cementoid matrices, and was sometimes
granules, koilocytes, and/or intracytoplasmic viral inclusions); mineralized and had embedded cells within lacunae. Additional
further diagnostics to confirm papillomavirus infection were not clinical history and follow-up information was available in
available. Squamous cell carcinoma was the second most com- 3 cases (cases 1, 6, and 7). In cases 1 and 7, an excisional
mon neoplasm diagnosed with 14 cases. The second most com- biopsy of the FEPLOs was performed, but surgical margins
mon diagnostic category was inflammation (41/109; 38%) with were incomplete and the FEPLOs extended histologically to
predominantly lymphoplasmacytic (non-eosinophilic) inflam- the deep surgical margins. Despite incomplete excision, surgi-
mation in 33 cases and predominantly eosinophilic inflammation cal removal/debulking was presumably curative in both cases
in 8 cases, 7 of which were tigers. Odontogenic lesions were the as there was no regrowth at annual examinations for 7 years in
third most common diagnostic category (10/109; 9%; see case 1, at which point the animal was euthanized for unrelated
below). Other diagnoses were rare (2/109; 2%). disease, and for 2 years in case 7, at which point the animal was
The most common odontogenic lesion that was diagnosed lost to follow-up. In case 6, an excisional biopsy of the FEPLO
was fibromatous epulis of periodontal ligament origin was performed, and surgical margins were narrow with cells of
(FEPLO), which was diagnosed in 4 lions, including 3 females the FEPLO extending <100 mm from the surgical margin.
and 1 male ranging in age from 13 to 21 years; age for 1 “adult” Despite narrow excision, there was no regrowth of the FEPLO
was not specified. FEPLO was also diagnosed in 2 jaguars, at annual examinations for 3 years, at which point the animal
1 bobcat, 1 cheetah, and 1 serval that included 3 females and died of unrelated disease.
2 males ranging in age from 3 to 12 years. FEPLOs were A single odontogenic cyst was identified in a 20-year-old,
reported to arise from the maxillary or mandibular gingiva female cougar who was euthanized for degenerative joint dis-
around the canine, premolar, or molar teeth. Gross photographs ease and urinary tract disease. Perimortem dental radiographs
of FEPLO were available in 1 cheetah (case 6; Fig. 1) and were performed due to a history of periodontal disease and
revealed an exophytic mass arising from the tooth-associated revealed a periapical lucency associated with the root of one
gingiva that partially entrapped the adjacent tooth. Microsco- of the mandibular canine teeth. A necropsy sample taken from
pically, in all of the FEPLO cases, the majority of the lesion the cyst wall was submitted for histology. Histologically, a cyst
was composed of proliferative periodontal ligament-like expanded the gingival subepithelial stroma (Fig. 4). The lining
stroma with a moderate number of spindle to stellate epithelium of the cyst was non-keratinizing stratified squamous
Scott et al 3

Figures 1–4. Fibromatous epulis of periodontal ligament origin, gingiva. Figure 1. Cheetah, case 6. The buccal gingiva adjacent to a left
maxillary premolar tooth is expanded by a smooth, pink, exophytic mass. Gross photograph courtesy of Holly Haefele. Figure 2. Serval, case 9.
The majority of the neoplasm is composed of periodontal ligament-like stroma (ie, proliferative stellate mesenchymal cells embedded in
abundant collagen arranged in short bundles) with occasional islands of cemento-osseous matrix (arrowheads) and odontogenic epithelium
(arrows). Hematoxylin and eosin (HE), decalcified section. Figure 3. Cheetah, case 6. Periodontal ligament-like stroma is composed of
proliferative stellate mesenchymal cells embedded in abundant collagen arranged in short bundles. There are regularly spaced, dilated, empty
vessels throughout the mesenchyme. The overlying gingiva is at the top of the image. HE, decalcified section. Figure 4. Odontogenic cyst,
gingiva, cougar, case 10. The cyst lining is composed of non-keratinizing stratified squamous epithelium (inset). HE, decalcified section.

epithelium, the basal layer of which was palisading and rarely odontogenic fibroma; the authors prefer the former term, which
exhibited features of odontogenic epithelium (antibasilar nuclei indicates that the lesion originates from the periodontium, as
and basilar clearing). Epithelial thickness varied from 2 to opposed to the latter term, which implies a neoplasm.5 While
10 layers. Lymphocytic and plasmacytic infiltration was mild common in domestic dogs, FEPLO are less common in domes-
in the stroma around the cyst and within the epithelium. tic cats, and the number of cases diagnosed in nondomestic
felids was surprising.5,12 FEPLO was diagnosed in 5 different
species, and lions were the most commonly affected species.
Discussion There is only one previous report of any proliferative odonto-
Odontogenic lesions comprised only 9% of the oral lesions genic lesion in any nondomestic felid, and it was a FEPLO in a
diagnosed in this group of nondomestic felids. Of the odonto- lion.3 Lions may be predisposed to this condition, similar to
genic lesions identified in this population, FEPLO was diag- domestic dogs. Recurrence of FEPLO was not noted in any of
nosed in 9/10 cases. FEPLO is also called peripheral the animals for which follow-up information was available.
4 Veterinary Pathology XX(X)

This is similar to the biologic behavior of FEPLO in domestic cases. The incidence of oral eosinophilic granulomas in tigers
animals, where regrowth is rare even in cases of incomplete reported here is consistent with previous reports suggesting
excision.5 oral eosinophilic granulomas are an underreported and possibly
The only other odontogenic proliferative lesion diagnosed in common lesion of tigers.4,10 Oral eosinophilic granuloma com-
nondomestic felids was a single odontogenic cyst diagnosed plex lesions are fairly common in domestic cats, with which
in a cougar. Odontogenic cysts have been rarely reported in tigers share 95.6% similarity in their genome sequence.2 The
domestic cats and dentigerous cysts are the most common-type genetic relatedness of domestic cats and tigers may make these
reported. 5 The odontogenic cyst in this case was not species similarly predisposed to oral eosinophilic granulomas.
anatomically consistent with a dentigerous cyst as it was asso- Further research is needed to elucidate what role (if any) genet-
ciated with an erupted tooth. The cougar had a history of severe ics plays in the development of oral inflammatory diseases.
dental disease, and the cyst was radiologically associated an Cheetahs accounted for 8/33 cases of stomatitis, gingivitis, or
inflamed tooth root. These findings are consistent with a radi- glossitis. Captive cheetahs have been reported to have a higher
cular cyst, which is uncommon in domestic animals, but occurs incidence of focal palatine erosions compared to other nondo-
secondary to tooth-associated periapical inflammation.5 mestic felids.8 Specific location of biopsy specimens was not
Non-odontogenic neoplasia and oral inflammatory lesions always provided in biopsy submission forms in this study, and
collectively comprised 89% of oral lesions of nondomestic as such incidence of focal palatine erosions could not be deter-
felids. Feline papillomavirus-associated oral papillomas have mined. One of the cases of stomatitis in a cheetah was associ-
been reported in a variety of nondomestic felids and have been ated with intranuclear inclusion bodies; this animal also had
well documented as a relatively common finding in captive rhinotracheitis and was confirmed to have feline herpesvirus-1,
snow leopards.8,9,11 The histologic characteristics of oral to which cheetahs may be predisposed.6 There were multiple
papillomas in captive snow leopards include viral cytopathic limitations of the interpretation of inflammatory lesions in this
changes within the granular cell layer such as large cytoplas- series. Anatomic location of the lesions within the oral cavity,
mic keratohyalin granules, koilocytes, and rare intracytoplas- and/or any associated periodontal disease (eg, dental calculi)
mic viral inclusions. 9,11 This report is consistent with were often not specified. Additionally, polymerase chain reac-
previous literature as oral papillomas were diagnosed in tion or cultures for infectious agents were either not performed
30/36 of snow leopards with oral lesions. The occurrence of or not available to the pathologist.
oral papillomas in snow leopards was more frequent than in
all other nondomestic felids combined. With the exception of Conclusion
snow leopards, oral papillomas were relatively uncommon in
nondomestic felids and accounted for 9/26 of all other non- With the exception of papillomas in snow leopards and FEPLO
odontogenic neoplasms identified. This is similar to domestic in lions, the spectrum of oral lesions in nondomestic felids is
cats, in which oral papillomas are infrequently reported.5 similar to what is reported in domestic cats. Inflammatory
Squamous cell carcinoma (SCC) is the most common oral lesions are the most common oral lesions, SCC is the most
malignancy in domestic cats, and accounts for over 60% of all common oral malignancy, and odontogenic lesions comprised
feline oral tumors.5 Results of this study are consistent with this a minority of the lesions. The results of this study largely agree
finding as 14/17 of the oral malignancies diagnosed in nondo- with the previously reported species-specific data regarding
mestic felids were SCC. The incidence of SCC was higher in well-documented oral lesions in nondomestic felids, specifi-
snow leopards compared with other nondomestic felids in this cally papillomas and SCC in snow leopards and eosinophilic
study and has been previously reported in this species.11 Given granulomas in tigers. As follow-up information was not con-
the high incidence of papillomas in snow leopards, a relation- sistently available in the cases presented here, additional data
ship between SCC and papillomavirus-induced neoplasia has are needed to understand the clinical relevance and prognoses
been suggested.11 However, the role of papilloma virus in the of oral lesions in nondomestic felids.
pathogenesis of oral SCC in domestic cats is controversial as
the incidence of oral SCC in domestic cats is much greater than Authors’ Note
the incidence of oral papillomas.5 The views expressed in this article are those of the authors and do not
Inflammatory lesions are the most common oral lesions in reflect the official policy of the Department of the Army/Navy/Air
Force, Department of Defense, or the US government.
domestic cats and chronic gingivostomatitis is the most com-
monly diagnosed of these lesions.12 The cause of gingivitis is
Acknowledgements
multifactorial and often associated with bacterial plaques/cal-
The authors thank Cathy Minogue and Christie Buie of Northwest
culi.5 With the exception of snow leopards, inflammatory
ZooPath for collection and processing of materials. We also thank
lesions were the most common oral lesion in all species of
Leroy Brown of Histology Consultation Services for specimen prepara-
nondomestic felids in this study; lesions of stomatitis, gingivi- tion. The authors are also grateful to the institutions and individuals who
tis, or glossitis were diagnosed in 33/41 cases of oral inflam- contributed case material and follow-up information, including Fort
matory lesions. The incidence of oral inflammatory lesions was Worth Zoo (especially Kim Rainwater), Fossil Rim Wildlife Center
highest in tigers, which accounted for 12/33 of stomatitis/gin- (especially Holly Haefele), Hendricks County Animal Hospital, India-
givitis/glossitis cases and 7/8 of oral eosinophilic granuloma napolis Zoo (especially Jeff Proudfoot and Abigail Rosenblum),
Scott et al 5

Jacksonville Zoo (especially Tiffany Martin), San Diego Zoo (espe- challenges. In: Proceedings of the Annual Conference of the American Associ-
cially Bruce Rideout), and Zoo Miami (especially Gwen Myers). ation of Zoo Veterinarians; September 19-25, 2020; Nashville, TN.
5. Murphy BG, Bell CM, Soukup JW. Veterinary Oral and Maxillofacial Pathol-
Declaration of Conflicting Interests ogy. Wiley-Blackwell; 2020.
6. Pennings A, Seeley K, Mathieu A, et al. Feline herpesvirus infection in four
The author(s) declared no potential conflicts of interest with respect to
captive cheetahs (Acinonyx jubatus) postvaccination. J Zoo Wildl Med. 2020;
the research, authorship, and/or publication of this article.
51(1):210–216.
7. Soukup JW, Bell CM. Nomenclature and classification of odontogenic
Funding
tumors—part I: historical review. J Vet Dent. 2014;31(4):228–232.
The author(s) received no financial support for the research, author- 8. Steenkamp G, Boy SC, van Staden PJ, et al. Oral, maxillofacial and dental
ship, and/or publication of this article. diseases in captive cheetahs (Acinonyx jubatus). J Comp Pathol. 2018;158:
77–89.
ORCID iD 9. Sunberg JP, Van Ranst M, Montali R, et al. Feline papillomas and papilloma-
Brian G. Murphy https://orcid.org/0000-0003-0057-0604 viruses. Vet Path. 2000;37(1):1–10.
Elise E. B. LaDouceur https://orcid.org/0000-0001-8510-1051 10. Sykes JM 4th, Garner MM, Greer LL, et al. Oral eosinophilic granulomas in
tigers (panther tigris)—a collection of 16 cases. J Zoo Wildl Med. 2007;38(2):
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