Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020

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Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020
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
Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020
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
Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020
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
Retrospective Study of Feline Oral Cavity Neoplasms and Non-neoplastic Lesions, Between 2010 and 2020
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
ÖZTÜRK GÜRGEN et al. Feline Oral Pathologies
                                                                 Acta Veterinaria Eurasia 2022; 48(1): 12-17

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