Prevalence of feline chronic gingivostomatitis in feral cats and its risk factors

Abstract

Objectives

This study investigated the prevalence of feline chronic gingivostomatitis in urban feral cats in South Korea and analysed its risk factors.

Methods

Three hundred and forty-five feral cats that visited the hospital for neutering using a trap–neuter–return approach were screened for feline chronic gingivostomatitis based on clinical criteria. In addition, we determined if body weight, sex and the presence of tongue lesions are risk factors for feline chronic gingivostomatitis. The difference in severity due to the presence or absence of risk factors, and the relationship between gross findings and histopathological lesions, were analysed by grading lesion severity.

Results

Feline chronic gingivostomatitis was diagnosed in 92 cats. Disease prevalence did not significantly differ with body weight and sex but was significantly related to tongue lesions.

Conclusions and relevance

The prevalence of feline chronic gingivostomatitis in urban feral cats in South Korea was 26.6%. It was significantly more prevalent in cats that had tongue lesions. Severity was also significantly associated with tongue lesions. Feline chronic gingivostomatitis may be associated with an infectious agent that causes tongue lesions.

Introduction

Feline chronic gingivostomatitis (FCGS) is a severe inflammatory syndrome involving the immune system that affects the oral mucosa. ¹ FCGS lesions may occur in multiple areas, from the gums in the oral cavity to the pharynx, and the lesions may be observed as tumour-like nodules due to multiple plasma cell infiltrations. ² This disease was previously called plasma cell stomatitis-pharyngitis, ³ chronic faucitis ⁴ and lymphocytic plasmacytic stomatitis, ⁵ depending on the lesion distribution and pattern. However, according to the latest literature, it is now named FCGS. ⁶

Cats affected by FCGS show clinical signs such as anorexia, bad breath, drooling, reduced grooming and weight loss due to severe pain. ⁷ They can become very debilitated and difficult to treat. Therefore, euthanasia is sometimes considered. In tissue samples of the oral mucosa affected by FCGS, lymphocytes and plasma cells are predominantly observed. In contrast, relatively few neutrophils, mast cells and Mott cells have been observed, thus showing the characteristics of chronic inflammation. ⁸

A biopsy is a valuable method for diagnosing FCGS. However, the disease can only be confirmed by identifying the clinical lesion characteristics. Hence, exclusion of neoplastic lesions is used more than confirmation in clinical practice. ⁹

The oral mucosa of FCGS cats is characterised by a more severe inflammation than that visible in dental diseases or tartar accumulation. If these inflammatory lesions are observed beyond the gingival mucosa, they are subsequently diagnosed as FCGS. ²

FCGS is mostly characterised by bilateral inflammation of the mucosa of the caudal oral cavity, known to distinguish FCGS from other oral diseases.^10,11 Although the cause and mechanism of FCGS have not yet been clearly elucidated, recent immunological studies have reported that FCGS exhibits immunological characteristics caused by intracellular pathogens, such as viruses.^12–14

Many studies have been conducted on the relationship between FCGS and viruses, such as feline calicivirus, feline herpesvirus-1, feline immunodeficiency virus and feline leukaemia virus. Although a causal relationship has not yet been established, many studies have provided consistent evidence that calicivirus may be associated with FCGS.^15–20

Calicivirus is easily transmitted via direct contact, and causes respiratory and acute stomatitis signs. Risk factors for caliciviruses are free-roaming behaviour and environments where many cats live together, such as shelters and kennels. ²¹ Ulcers in the tongue are one of the characteristic clinical signs of calicivirus. In addition, the tongue is a site where the virus is easily detected. ²²

A recent study investigated the relationship between cohabitation environment or external environment accessibility and the prevalence of FCGS. ²³ In that study, the prevalence of FCGS was higher in cats that lived together than in those that lived alone. For each additional cat, the risk of FCGS increased by 70%. As no significant relationship between outdoor accessibility and FCGS was found in the same study, there are likely other FCGS-inducing factors relating to cohabitation in addition to the cause of infection. Therefore, periodic reinfection by chronic carrier cats and stress caused by dense breeding have been suggested as causes. ²³

The prevalence of FCGS ranges from 0.7% to 12%.^24–26 To the best of our knowledge, the prevalence of FCGS in feral cats has not yet been reported. Therefore, this study aimed to investigate the prevalence of FCGS in feral cats and determine whether weight, sex and tongue ulcers, or traces of ulcers – typical signs of calicivirus infection – act as risk factors for FCGS. We hypothesised that the prevalence of FCGS in feral cats would be higher than reported in previous studies, and that a higher prevalence of FCGS would be noted in cats with tongue lesions.

Materials and methods

This study included 345 cats (182 males and 163 females) captured and brought to the Gang-Buk Woori Animal Medical Center in Gangbuk-gu, Seoul, South Korea, for neutering from March to November 2021.

Neutering surgery in the context of a trap–neuter–return operation was performed under general anaesthesia with a combination of ketamine (5 mg/kg), medetomidine (0.03 mg/kg) and butorphanol (0.15 mg/kg) administered intramuscularly. We also used a trap divider to humanely confine the cat at one end of the trap after measuring its body weight. Both FCGS diagnosis and lesion recording were conducted during recovery from anaesthesia.

FCGS was diagnosed by applying the clinical criteria suggested previously. ²⁴ First, inflammation of the mucosa of the oral cavity, including at least one of the visible gingival margins immediately adjacent to the teeth, whole visible gingival mucosa from the teeth to the mucogingival junction, buccal mucosa, caudal oral mucosa, palatoglossal folds, soft palate and pharynx may sometimes be affected. Second, gingivitis usually extends beyond the mucogingival junction. Third, the severity of the inflammation is worse than that visible in other dental diseases. Fourth, the affected areas are frequently oedematous, proliferative and ulcerated. Fifth, the inflamed areas are usually bright red in colour and often bleed spontaneously on very mild trauma (eg, swabbing; Figure 1).

Figure 1

Clinical lesion characteristics of feline chronic gingivostomatitis. (a) Normal mucosal surfaces of the oral cavity, free gingival margin (green arrow), attached gingiva (blue double arrow), mucogingival junction (white arrows) and alveolar mucosa (yellow double arrow). (b) Gingivitis. (c) Alveolar mucositis score 3 (bleeding induced by gentle pressure). (d) Alveolar mucositis score 4 (spontaneous bleeding). (e) Mucosa of the caudal oral cavity (red circle), bordered medially by the palatoglossal folds (asterisk) and fauces, dorsally by the hard (square) and soft palate (triangle) and rostrally by alveolar and buccal mucosa (circle). (f) Caudal stomatitis

Oral inflammatory lesions were graded by the same operator using a previously reported scoring system. ²⁷ Caudal stomatitis and alveolar mucositis intensity scores were evaluated using a five-degree system: grade 0 (no lesion); grade 1 (mild inflammation, non-ulcerative, non-proliferative, not spontaneously bleeding and not bleeding even with slight pressure); grade 2 (moderate inflammation, non-ulcerative, slightly proliferative and not spontaneously bleeding even with slight pressure); grade 3 (moderate, ulcerative or ulceroproliferative inflammation, without spontaneous bleeding, but with bleeding when slight pressure is applied); and grade 4 (severe, ulcerative or ulceroproliferative inflammation with spontaneous bleeding). Surface areas in caudal stomatitis were scored using five degrees: 0 (absence of lesions); 25 (<25% of the total surface area); 50 (25–50%); 75 (50–75%); and 100 (>75%). Finally, the global caudal stomatitis intensity score (GCSIS) was calculated using the following formula: GCSIS = (caudal stomatitis intensity score × surface area score)/100.

Tongue lesions were defined as the loss of tongue papillae due to ulcers on the dorsal aspect of the tongue. Congestion and bleeding on palpation were evaluated as ongoing ulcers. If exfoliated papillae were identified and epithelialised, they were recorded as scars from previous ulcers.

Tissue samples were collected from 10 cats. Histopathological grades were evaluated on a four-grade scale (0, 1, 2 and 3), based on a previous study. ¹² Two cats per severity grade of the mucosa of the caudal oral cavity were selected to determine whether there was a difference between clinical and histopathological severity of lesions in cats with tongue lesions.

Statistical analysis was performed using the commercial programme StatPlus:mac LE (AnalystSoft). A P value <0.05 was considered indicative of statistical significance. The continuous variable (body weight) was assessed for normality via the Shapiro–Wilk test and by visual inspection of Q-Q plots. For those with approximately normal distribution, the sample means were compared between the FCGS and non-FCGS groups via an independent t-test. For dichotomous variables (presence or absence of tongue lesion and sex), the FCGS and non-FCGS groups were compared using the χ² test. The Mann–Whitney one-sided non-parametric test was used to assess the differences in lesion scores according to the presence or absence of tongue lesions in FCGS. The correlation between histopathological grade and clinical intensity score (GCSIS and alveolar mucositis intensity score) was assessed using Spearman’s correlation analysis.

Results

The prevalence of FCGS in urban feral cats in South Korea was 26.7% (92/345 cats). There were no significant differences according to sex and body weight (Table 1).

Table 1

Prevalence (26.7%) of feline chronic gingivostomatitis in 345 cats and comparison between measurements

Variable	FCGS (n = 92)	Non-FCGS (n = 235)	P value
Sex
Male	54	128	0.182
Female	38	125
Weight (kg)
Male	4.37 ± 0.78	4.43 ± 0.95	0.659
Female	3.41 ± 0.72	3.50 ± 0.62	0.457

Data are presented as n or mean ± SD

FCGS = feline chronic gingivostomatitis

As shown in Figure 2, FCGS was identified at significantly higher rates in cats with tongue lesions than in those without. Moreover, a significant difference in the lesion severity scores was observed between cases of FCGS with and without tongue lesions. Table 2 shows the lesion intensity scores in cats diagnosed with FCGS.

Figure 2

Prevalence and severity scores according to the presence of tongue lesions. (a) Normal feline tongue papillae. (b) Tongue ulcers (asterisk). (c) Traces of ulcers, exfoliated papillae (arrows). (d) The presence of tongue lesions is significantly associated with feline chronic gingivostomatitis (FCGS). (e) Severity according to the presence or absence of tongue lesions in FCGS. GCSIS = global caudal stomatitis intensity score; AMIS = alveolar mucositis intensity score

Table 2

Intensity scores of caudal stomatitis and alveolar mucositis in 92 cats with feline chronic gingivostomatitis*

GCSIS 27 *	No. of cats	AMIS 27	No. of cats
0 to <1	46 (50)	0	7 (7.6)
1 to <2	22 (23.9)	1	9 (9.8)
2 to <3	8 (8.7)	2	27 (29.3)
3 to <4	10 (10.9)	3	41 (44.6)
4	6 (6.5)	4	8 (8.7)

Data are presented as n (%) unless otherwise indicated

*

Global caudal stomatitis intensity score (GCSIS) = (caudal stomatitis intensity score × surface area score)/100

AMIS = alveolar mucositis intensity score

Among all FCGS cats, the prevalence of alveolar mucosa inflammation was 92.3%, and that of inflammation of the mucosa of the caudal oral cavity was 79.3% (Table 3).

Table 3

Overall distribution of lesions in 92 cats with feline chronic gingivostomatitis

Lesion location	No. of cats
Alveolar mucosa	85 (92.3)
Mucosa of the caudal oral cavity	73 (79.3)
Palatoglossal fold	66 (71.7)
Soft palate	14 (15.2)
Hard palate	1 (1.0)

Data are presented as n (%)

There was a positive correlation between histopathological severity grade and clinical lesion severity score (ρ = 0.669) (Figure 3).

Figure 3

Histopathological grade according to the caudal stomatitis intensity and surface area score. (a,c,e,g,i) Gross and (b,d,f,h,j) histological findings with haematoxylin and eosin staining. (a,b) Intensity score 0, surface area score 0 and histopathological grade 1. (c,d) Intensity score 1, surface area score 25 and histopathological grade 3. (e,f) Intensity score 2, surface area score 50 and histopathological grade 2. (g,h) Intensity score 3, surface area score 75 and histopathological grade 3. (i,j) intensity score 4, surface area score 100 and histopathological grade 3. Yellow circle indicates the caudal oral mucosa; asterisk indicates the tissue collection site (3 mm biopsy punch); scale bar = 25 µm. (k) Histopathological severity grade based on the clinical lesion score

Discussion

In this study, FCGS was diagnosed in 92/345 feral cats (prevalence rate 26.6%). To the best of our knowledge, this is the first study to report the prevalence of FCGS in feral cats. The prevalence rate of FCGS has been previously reported to be 0.7–12%. In 2004, Verhaert and Van Wetter ²⁵ reported a prevalence rate of 12%; however, the population assessed for oral disease treatment was mixed. In 2007, a study by Healey et al ²⁴ targeted domestic cats that visited a primary hospital and reported a prevalence of 0.7%, while in 2009, Girard et al ²⁶ reported a prevalence of 5.5% in a study of colony cats that had no contact with the external environment. The studies on prevalence reported to date have been performed with groups in which there was a guardian or in which contact with other cats could be controlled. However, as the cats in the present study were exposed to the external environment, contact with other cats could not be controlled. This marks an important difference from other studies. It is known that feral and free-living domestic cats form colonies around food sources. ²⁸ It is also well known that they have a high prevalence of infectious diseases due to their behaviour and lifestyle. ²⁹ Contrary to previous studies, the high prevalence of FCGS in the feral cats in our study suggests that FCGS may have an infectious mechanism.

In this study, no significant difference in the prevalence of FCGS was identified between males and females, similar to most previous studies. However, some studies found high rates of FCGS in neutered males.^24,25 A higher prevalence of FCGS was also identified in males than in females in this study, although the difference was not statistically significant. In addition, the number of males was higher among captured cats, which may be because male feral cats have home territories that are 2–3 times larger than those of females. ²⁹

Anorexia due to oral pain causes weight loss, which is one of the main clinical signs of FCGS. Herein, a significant difference in body weight (P <0.001) was confirmed between males and females. Therefore, we analysed them separately and found that there was no significant difference in body weight between cats with or without FCGS. Possible reasons for these results are as follows: FCGS cats with severe clinical signs may have been eliminated from the wild because they could not eat well or because they were not attracted to food due to oral pain; thus, a relatively small number of cats were captured (Table 2). Alternatively, the weight loss due to FCGS could be smaller than the variation (female body weight SD 0.65, male body weight SD 0.90) in body size between each cat.

Tongue lesions were identified in 112/345 cats. All lesions were identified as traces of ulcers. Tongue lesions were found in 61/92 cats diagnosed with FCGS (66%), which is significantly higher than the proportion in cats not diagnosed with FCGS (51/253 [20%]). Furthermore, the severity scores were significantly higher in FCGS cats with tongue lesions compared with those without lesions. The relationship between calicivirus load and tongue ulcers, but not between viral load and lesion severity, has been found to be statistically significant. ²⁷ Based on previous studies and the findings of this study, the severity of FCGS lesions can be predicted as it tends to increase over time if the virus is severe enough to cause lesions on the tongue. However, in the current study, no cats with tongue ulcers were identified upon examination, probably because no cats with severe clinical signs were captured.

Inflammation of the alveolar mucosa (prevalence 92.3%) and the caudal oral mucosa (79.3%) was identified in FCGS cats, similar to previous studies. ² Inflammation of the soft and hard palates was observed at low rates. Interestingly, in cats with inflammation of the soft and hard palates, inflammation was also observed in all caudal oral mucosa, alveolar mucosa and palatoglossal folds. There was no significant difference in the severity of alveolar mucosal lesions between FCGS cats with and without soft and hard palate inflammation (P = 0.326). However, the severity of the lesion was high in the caudal oral mucosa (P = 0.008). Hence, the soft and hard palate inflammation in FCGS appears to be related to the mechanisms leading to inflammation of the caudal oral mucosa.

A previous study reported a positive correlation between clinical severity score and histopathological severity grade. ¹² Owing to the difference between the clinical severity score scale (0, 1, 2, 3 and 4) used in this study and the histopathological grade scale (0, 1, 2 and 3), which was used in the previous study, a direct comparison was impossible. Additionally, the prediction of the histopathological grade at a low clinical severity score was not well matched (Figure 3). Of the two cats with a clinical severity score of 0, one was diagnosed with FCGS in the alveolar mucosa and the other was not. Although the small sample size prevented generalisation, FCGS can still be histopathologically diagnosed, even if the mucous membrane appears normal when there is a lesion on the tongue. A study with larger sample sizes is necessary to clarify this issue.

A limitation of this study is that the same set-up and study were not conducted with a control group, such as the general population of domestic cats in the same area. In addition, as not all tongue lesions are caused by calicivirus alone (eg, herpesvirus), there is a limitation in that it cannot be confirmed whether there is a history of infection with calicivirus. Although the lesions on the tongue were all traces of ulcers, they may be the clinical signs of FCGS, and they may be considered indicators of severe FCGS.

Conclusions

This is the first study to evaluate the prevalence and risk factors of FCGS in free-roaming street cats in Seoul, South Korea. In this study, the prevalence of FCGS in urban feral cats was 26.6%. Tongue lesions were identified as risk factors for FCGS; sex and weight were not. The present results suggest that FCGS is likely to have an infectious mechanism, and colony breeding should be restricted, as with other infectious diseases, to prevent further disease.