Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020
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Original Article Acta Veterinaria Eurasia 2022; 48(1): 12-17 Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020 Hazal ÖZTÜRK GÜRGEN1 , Pembe Dilara KEÇİCİ2 , Gülay YÜZBAŞIOĞLU ÖZTÜRK1 , Aydın GÜREL1 1 Department of Pathology, İstanbul University-Cerrahpaşa, Faculty of Veterinary Medicine, İstanbul, Turkey 2 Department of Animal Breeding and Husbandry, İstanbul University-Cerrahpaşa, Faculty of Veterinary Medicine, İstanbul, Turkey Cite this article as: Öztürk Gürgen, H., Dilara Keçici, P., Yüzbaşıoğlu Öztürk, G., & Gürel, A. (2022). Retrospective study of feline oral cavity neoplasms and non-neoplastic lesions, between 2010 and 2020. Acta Veterinaria Eurasia, 48(1), 12-17. ORCID iDs of the authors: H.O-G. 0000-0003-2748-6189; P.D.K. 0000-0003-1151-179X; G.Y-O. 0000-0002-1761-0409; A.G. 0000-0002-0266-8771 Abstract Oral pathologies are common in cats, and a histopathological examination (n = 21/59; 35.59%), respectively. The patient profiles indicated that adult is important for their diagnosis. In this study, it was aimed to statistically patients have a greater predilection for oral pathologies. Female patients determine the prevalence of oral diseases diagnosed in the pathology (n = 72/143; 50.34%) were found slightly more predisposed than males department, between 2010 and 2020. The oral pathologies were divided (n = 59/143; 41.25%). Moreover, the number of mixed breeds (n = 103/143; into malignant and benign neoplasms and non-neoplastic lesions, diagno- 72.02%) was significantly higher in comparison with the pure breeds. sed by the hematoxylin and eosin (HE) staining method. The findings reve- These findings were also statistically confirmed by the chi-square test. The aled that malignant neoplasms (n = 69/143; 48.25%) and non-neoplastic most commonly affected anatomical site was determined as the gingiva lesions (n = 59/143; 41.25%) constituted most of the cases, whereas benign (n = 41/143; 28.67%). In conclusion, this study presents the prevalence and neoplasms (n = 15/143; 10.48%) were very limited. The malignant neop- statistical confirmations of the most commonly encountered feline oral pat- lasms and non-neoplastic lesions were predominantly composed of oral hologies with patient profiles. squamous cell carcinoma (n = 44/69; 63.76%), feline chronic gingivostoma- titis (FCGS) (n = 27/59; 45.76%), and eosinophilic granuloma complex (EGC) Keywords: Feline, oral lesions, prevalence Introduction the oral pathologies encountered in cats with different patient pro- files, and the most commonly affected anatomical sites. Feline oral pathologies are common, presenting a varying severity of disorders that can affect the oral mucosa, such as inflammation Methods associated with infectious etiology, idiopathic or immune-mediated responses, and neoplastic conditions (Lommer, 2013; Verhaert & A total of 143 cases between 2010 and 2020 were documented from Van Wetter, 2004). The chronic and recurrent non-neoplastic diseases the databases of the Department of Pathology, İstanbul University- can be localized to inflammation within the oral mucosa (Lommer, Cerrahpaşa, Faculty of Veterinary Medicine, İstanbul, Turkey. The 2013) or can be derived from other underlying systemic conditions biopsy samples were mostly obtained from the small animals’ clinic (Dokuzeylül et al., 2016; Lommer, 2013). All these pathological enti- of the faculty and some private small-animal veterinary clinics in ties cause several health problems, including an increase of saliva, a Istanbul. reluctance to eat, and weight loss, which lead to the loss of energy, lethargy, and anorexia (Verhaert, 2010). A histopathological exami- The cases were classified based on breed, sex, life stage, and the nation is always required to eliminate similar macroscopic entities anatomical site of the lesions. The patients were categorized as and to achieve a definitive diagnosis of non-neoplastic lesions and male or female, and no information about neutering was available. neoplastic diseases (Verhaert, 2010). The purpose of this retrospec- The life stages were classified as kitten (0–6 months old), young tive study is to statistically analyze and demonstrate the incidence of (7 months–2 years old), adult (3–6 years old), mature (7–10 years Corresponding Author: Hazal ÖZTÜRK GÜRGEN • E-mail: hazal.ozturkgurgen@iuc.edu.tr This work is licensed under a Creative Received: February 22, 2021 • Accepted: June 17, 2021 • Available Online Date: September 9, 2021 • DOI: 10.5152/actavet.2021.21018 Commons Attribution-NonCommercial 4.0 International License. Available online at actavet.org 12
ÖZTÜRK GÜRGEN et al. Feline Oral Pathologies Acta Veterinaria Eurasia 2022; 48(1): 12-17 old), senior (11–14 years old), and geriatric (≥15 years old) (Vogt et al., 2010). Table 1 Distribution of Cat Oral Lesions According to the Type of Lesion, Breed, Sex, and Histopathological diagnoses had been performed on HE-stained tis- Age sue sections, along with Giemsa staining (10 mL Giemsa stain and Factor Number Percentage of Total Lesions 50 mL 0.1% acetic acid solution) for suspected cases of mast cell tumors by three different pathologists, regarding the histopatholog- Tumor type ical properties of each of the oral pathologies described previously Malign 52 44.8a (Head et al., 2003; Munday et al., 2017; Uzal et al., 2016). Non-neoplastic 49 42.2a Statistical Analyses Benign 15 12.9b Statistical analyses could be performed in 116/143 cases. The cases p
ÖZTÜRK GÜRGEN et al. Feline Oral Pathologies Acta Veterinaria Eurasia 2022; 48(1): 12-17 The rest of the non-neoplastic cases consisted of granulomatous lesions (n = 4; 6.77%), feline progressive histiocytosis (n = 3; 5.08%), fibrous osteodystrophy (n = 1; 1.69%), hyperostosis (n = 1; 1.69%), peripheral giant cell granuloma (n = 1; 1.69%), and non-neoplastic polyp (n = 1; 1.69%). Detailed information about non-neoplastic lesions, patient profiles, and the most commonly affected anatomi- cal sites are given in Table 3. The benign tumors mainly consisted of odontogenic tumors, such as peripheral odontogenic fibroma (POF) (n = 7; 46.66%) and amelo- blastoma (AM) (n = 4; 26.66%). The other remaining benign tumors were extramedullary plasmacytoma (n = 2; 13.33%), osteoma, (n = 1; 6.66%), and papilloma (n = 1; 6.66%). The benign neoplasm group was composed of nine male (60%) and six female (40%) patients. No differences in age-groups were observed for benign neoplasms. Mixed breeds were the most commonly affected breeds. The detailed information about benign tumors, patient profiles, and the Figure 1 most commonly affected anatomical sites are given in Table 4. Feline Oral Squamous Cell Carcinoma, Maxilla, Male, 10 Years Old, Mixed Breed Cat. Islands of Neoplastic Squamous Cells (Stars). Discussion, Conclusion and Recommendations determined as the most commonly affected anatomical site (n = 16 This retrospective study presents the prevalence and statistical 59.25%). The occurrence of EGC in female patients was twice as analyses of the most common feline oral pathologies encountered common as in males, and there was no information about gender in the patient profiles and the commonly affected anatomical sites. for three patients (male: 6; 28.57%; female: 12; 57.14%). Young cats The results statistically showed that malignant neoplasms and non- were found to be more prone to the disease (n = 9; 47.36%), but a neoplastic lesions constituted the biggest proportion of the cases, few older patients increased the mean age, which was determined which was consistent with the previous studies (Falcão et al., 2020; as 5.31 years. Mixed breeds constituted most of the cases (n = 13; Mikiewicz et al., 2019; Wingo, 2018). Female patients seemed to have 61.90%). The other affected breeds were Persian (n = 3; 14.28%), slightly higher prevalence than males. Adult, mature, and senior cats Chinchilla (n = 2; 9.52%), Scottish Fold (n = 2; 9.52%), and Sphynx seemed to be the most affected patient groups for the development (n = 1; 4.76%). The most commonly affected site was the tongue of oral pathologies. Surprisingly, there were no kitten patients in this (n = 9, 42. 85%). study. Mixed breeds and the domestic short and long hair breeds Table 2 Malignant Neoplasms Seen in the Oral Cavity in Patients Number of Cases; Commonly Gender Percentage of the Total Most Common Mean Age Predominant Affected Malignant Neoplasms Lesions Life Stage (Year) Breed Localization Male Female Unk. OSCC n = 44; 30.76 Mature 10.07 Mixed breed Mandible–tongue 16 22 6 Und. Sarc. n = 5; 3.49 Mature-Senior 11.6 Mixed breed Oral cavity 1 3 1 Fibrosarcoma n = 3; 2.09 NA 9.66 Mixed breed Lips - 2 1 Osteosarcoma n = 3; 2.09 Senior 11.66 Mixed breed Gingiva 2 1 - Vascular neoplasms n = 3; 2.09 Mature 6.33 Mixed breed NA 2 1 - Leiomyosarcoma n = 1; 0.69 Geriatric 15 Mixed breed Tongue - 1 - Chondrosarcoma n = 1; 0.69 Geriatric 15 Mixed breed Maxilla 1 - - Neurofibrosarcoma n = 1; 0.69 Adult 5 Mixed breed Mandible - 1 - Fibromyxosarcoma n = 1; 0.69 Mature 7 Mixed breed Oral cavity 1 - - Mast cell tumor n = 1; 0.69 Mature 10 Mixed breed Gingiva - 1 - Lymphoma n = 1; 0.69 NA NA Persian Gingiva 1 - - Malignant melanoma n = 2; 1.39 NA 4 NA NA 1 1 - Anaplastic carcinoma n = 2; 1.39 NA 6.5 NA NA 1 1 - Malignant fibrous n = 1; 0.69 NA NA Mixed breed Mandible - - 1 histiocytoma Note: NA = not applicable; Unk = unknown; Und. Sarc. = undifferentiated sarcoma. 14
ÖZTÜRK GÜRGEN et al. Feline Oral Pathologies Acta Veterinaria Eurasia 2022; 48(1): 12-17 (Bilgiç et al., 2015). In this retrospective study, no information about the metastatic condition was available in any of the cases. The most commonly affected life stage is defined to be older cats (Stebbins, et al., 1989; Vos & Van der Gaag, 1987; Wingo, 2018). Similarly, the mean affected age in this study was found to be over 10 years (10.07 years), indicating the borderline of mature and senior stages, according to the guideline of feline life stages (Vogt et al., 2010). No sex predilection was found in this study, as previously indicated (Stebbins et al., 1989). OSCC can occur in any site of the oral cavity, but the lingual/sublingual area, the mandible, and max- illa show higher prevalence (Bilgiç et al., 2015), which was consistent with this study. Fibrosarcoma has been reported as one of the most common malig- nancies for feline oral pathology (Northrup et al., 2006; Stebbins et Figure 2 al., 1989), but recent studies do not correlate with this assumption Feline Chronic Gingivostomatitis, Oral Cavity, Female, 8 Years Old, (Falcão et al., 2020; Mikiewicz et al., 2019; Wingo, 2018), which was Mixed Breed Cat. Severe Infiltration Of Lymphocytes And Plasma confirmed in this study. Fibrosarcoma was determined only in a few Cells (Star). cases and shared the same ratio with osteosarcoma and hemangio- sarcoma as the other mesenchymal tumors. constituted almost three-quarters of the cases, and this was found In this study, non-neoplastic lesions have an important place fol- compatible with the other studies (Falcão et al., 2020; Mikiewicz lowing malignant neoplasms (or OSCC). The most commonly seen et al., 2019; Wingo, 2018). non-neoplastic lesions were FCGS and EGC. In recent studies, inflam- matory lesions show higher prevalence in comparison with the Oral squamous cell carsinomas were the most common tumors OSCC (Falcão et al., 2020; Mikiewicz et al., 2019; Wingo, 2018). FCGS among malignant neoplasms, as reported previously. (Bonfanti has recently been found to be the most commonly encountered et al., 2015; Falcão et al., 2020; Hayes et al., 2007; Mikiewicz et al., pathological entity (Falcão et al., 2020). Patient profiles of FCGS can 2019; Stebbins et al., 1989; Verhaert, 2010; Wingo, 2018). This is a be in any of the age-groups and show no sex predilection (Munday very agrresive and locally invasive neoplasm (Stebbins et al., 1989). et al., 2017). In this study, adult patients were predominant, as previ- Although its metastatic rate has been noted to have a very low ously indicated by Rolim et al. (2017), and the disease showed no potential (Stebbins et al., 1989), metastasis into the mandibular sex predilection. lymph nodes has been reported (Gendler et al., 2010). The reason metastasis has not been commonly observed could be associated The etiological causes for FCGS may be multifactorial. Bacterial dis- with the early death or euthanasia of the patient due to the aggres- eases caused by Gram-negative bacteria arising from dental plaques sive behavior of the neoplasm itself, before any signs of metastasis (Love et al., 1989; Mallonee et al.,1988; Sims et al., 1990), especially Pasteurella multocida subsp. multocida (Dolieslager et al., 2011; Southerden, 2010), the feline calicivirus infection (FCV) (Dowers et al., 2010; Thompson et al., 1984), periodontal diseases, or a hyper- sensitive reaction to the diet (Winer et al., 2016) have been reported as the common etiological factors for oral inflammatory lesions. Besides these, systemic viral infections caused by viruses such as the feline immunodeficiency virus (FIV) or the feline leukemia virus (FELV) can have a negative effect, resulting in oral diseases (Williams & Aller, 1992). An epidemiological study performed in North America has determined higher seropositivity for FELV and FIV in cats with oral diseases (Burling et al., 2017). In this retrospective study, only one patient was found to be registered with FIV positivity, and we have no information about the suspected etiologies for any of the other patients. EGC is subdivided into the three different forms, observed in cuta- neous and oral lesions: indolent ulcer, eosinophilic plaque, and eosinophilic granuloma (Power & Ihrke, 1995). Eosinophilic granu- Figure 3 loma is actually a histopathologic term to confirm the clinical enti- Feline Eosinophilic Granuloma, Sublingual Area, Female, 7 Years Old, ties (Power & Ihrke, 1995). The mucocutaneous junctions of the Scottish Fold Cat. Granulomatous Inflammation With Increased lip are more prone to indolent ulcers, whereas EGC appears most Number of Eosinophils (Arrow) Surrounded by Macrophages, commonly on the tongue and hard palate (Munday et al., 2017). In Lymphocytes, and Fibrocytes. this study, cases diagnosed with EGC indicated oral eosinophilic 15
ÖZTÜRK GÜRGEN et al. Feline Oral Pathologies Acta Veterinaria Eurasia 2022; 48(1): 12-17 Table 3 Non-neoplastic Lesions Seen in the Oral Cavity Number of Cases; Most Commonly Sex Percentage of the Common Mean Age Predominant Affected Non-neoplastic Lesions Total Lesions Life Stage (Years) Breed Localization Male Female Unk. FCGS n = 27; 18.88 Adult 6.75 Mixed breed Gingiva 12 15 - EGC n = 21; 14.68 Young 5.31 Mixed breed Tongue 6 12 3 Granulomatous n = 4; 2.79 Mature 6.5 Persian Tongue 2 2 - inflammation Feline progressive n = 3; 2.09 Adult 4.66 Mixed breed NA 2 1 - histiocytosis Fibrous osteodystrophy n = 1; 0.69 Senior 12 Mixed breed Maxilla - 1 - Inflammatory polyp n = 1; 0.69 Mature 7 Mixed breed Larynx 1 - - Hyperostosis and fibrosis n = 1; 0.69 NA NA Mixed breed Mandible - 1 - of bone Peripheral giant cell n = 1; 0.69 Mature 10 Mixed breed Mandible 1 - - granuloma Note: NA= not applicable; Unk = unknown. granuloma and indolent ulcers. They were mostly found in the lin- Patients with oral pathology generally show no signs of pain, but gual/sublingual areas. The etiologic causes for EGC may be auto- this may differ when the tongue is affected or problems in mas- immune and/or allergic, and mostly, secondary bacteria play a role tication occur (Verhaert, 2010). These kinds of problems cause in triggering the inflammatory reaction (Buckley & Nuttall, 2012). severe pain and lead to the loss of appetite and deterioration in None of the cases in this study had an available history for etiologi- the general condition of the patient (Bilgiç et al., 2015; Verhaert, cal causes. 2010; Wingo, 2018). Concerning these oral health problems, a large part of the OSCC cases are diagnosed during physical exami- Benign neoplasms comprised a very low percentage of the oral nations (Hayes et al., 2007). However, most of the oral pathologies pathologies in this study. Among them, odontogenic tumors com- show macroscopic appearances similar to OSCC. The differential prised the highest proportion. In fact, they are very rare entities diagnoses include non-neoplastic lesions such as gingival hyper- in cats (Falcão et al., 2020; Mikiewicz et al., 2019; Stebbins et al., plasia, EGC, FCGS, or periodontal diseases (Bilgiç et al., 2015; 1989; Vos & Van der Gaag, 1987; Wingo, 2018). Nevertheless, POF Stebbins et al., 1989). Therefore, a histopathological examination was determined as the fourth most common oral pathology, which is required for a definitive diagnosis (Lommer, 2013; Stebbins et al., differed in comparison with the recent studies (Wingo, 2018; 1989; Wingo, 2018). Mikiewicz et al., 2019). The other forms of the odontogenic lesions encountered in this study were AM, and the peripheral giant cell In conclusion, this retrospective study presents the prevalence of oral granuloma and also which was seen in a single case and was clas- lesions encountered in cats in Istanbul, and presents the patient profiles sified under non-neoplastic lesions, since it is not actually a benign and commonly affected anatomical sites of the oral cavity. A clinical tumor and is considered as a tumor-like proliferation (Munday diagnosis based on macroscopic appearances and clinical symptoms et al., 2017). may be challenging for oral pathologies, therefore histopathology Table 4 Benign Neoplasms Seen in the Oral Cavity Sex Benign Number of Cases; Percentage of Most Common Mean Age Predominant Commonly Affected Neoplasms the Total Lesions Life Stage (Years) Breed Localization Male Female Unk. POF n = 7; 4.89 Senior-geriatric 10.3 Mixed breed Gingiva 1 6 - AM n = 4; 2.79 Adult-mature 5.75 Mixed Gingiva 4 - - breed-British EP n = 2; 1.39 NA 6.5 Mixed breed Oral cavity 2 - - Osteoma n = 1; 0.69 Mature 10 Chinchilla Mandible 1 - - Papilloma n = 1; 0.69 Geriatric 17 Siamese Gingiva 1 - - Note: POF= peripheral odontogenic fibroma; AM = ameloblastoma; EP = extramedullary plasmacytoma; NA = not applicable; Unk = unknown. 16
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