Abstract
Periodontal disease is the most common oral disease in cats. The objectives of this study were to determine the relationships between gingivitis and dental calculus thickness (DCT), or dental calculus coverage (DCC); determine the association of gingivitis scores and types of oral bacteria; and to evaluate bacterial co-infection in cats with periodontal disease. Twelve cats that were not infected with feline leukemia or feline immunodeficiency viruses were enrolled in the study. Gingivitis, DCT, and DCC were scored and recorded. A Kruskal-Wallis test was used to compare scores among canine, 2nd premolar, 3rd premolar, 4th premolar, and 1st molar teeth. The relationship between gingivitis and DCT or DCC scores was determined using the Spearman rank sum test (ρ). Subgingival bacteria were cultured and the association between bacterial species and gingivitis score was evaluated using a Fisher’s exact test. The average gingivitis, DCT, and DCC scores for the caudal maxillary teeth were higher for the caudal mandibular teeth and more severe for the 3rd premolar, 4th premolar, and 1st molar teeth than for the canine teeth. A strong relationship between average DCT or DCC score and average gingivitis score was found (ρ = 0.96 and 1, respectively). Aerobic and anaerobic bacterial infections were identified in a large number of cats with periodontal disease (71.1% and 28.9%, respectively). In conclusion, severe gingivitis scores were associated with anaerobic bacterial infection. The caudal teeth are affected with more severe gingivitis, DCT, and DCC than the other teeth. Antibiotic prophylaxis should be prescribed in cats with periodontal disease.
Résumé
La maladie parodontale est la maladie orale la plus fréquente chez les chats. Les objectifs de la présente étude étaient de déterminer les relations entre la gingivite et l’épaisseur du tartre dentaire (ETD), ou la couverture du tartre dentaire (CTD); déterminer l’association des pointages de gingivite et les types de bactéries orales; et d’évaluer les co-infections bactériennes chez les chats avec maladie parodontale. Douze chats qui n’étaient pas infectés par le virus de la leucémie féline ou le virus de l’immunodéficience féline ont été recrutés pour cette étude. La gingivite, l’ETD, et la CTD ont été évalués et notés. Un test de Kruskal-Wallis a permis de comparer les pointages parmi les dents canines, 2e prémolaires, 3e prémolaires, 4e prémolaires et 1ère molaires. La relation entre la gingivite et les pointages d’ETD ou de CTD a été déterminée à l’aide du test de corrélation de Spearman (ρ). Les bactéries sous-gingivales ont été cultivées et l’association entre les espèces bactériennes et le pointage de gingivite a été évaluée à l’aide du test exact de Fisher. Les pointages moyens de gingivite, d’ETD, et de CTD pour les dents maxillaires caudales étaient plus élevés que pour les dents mandibulaires caudales et plus sévères pour les dents 3e prémolaires, 4e prémolaires, et 1ère molaires que pour les canines. Une forte relation entre les pointages moyens d’ETD et de CTD et les pointages moyens de gingivite a été trouvée (ρ = 0,96 et 1, respectivement). Des infections bactériennes aérobies et anaérobies ont été identifiées chez un grand nombre de chats avec maladie parodontale (71,1 % et 28,9 %, respectivement). En conclusion, des pointages élevés de gingivite étaient associés avec des infections par des bactéries anaérobiques. Les dents caudales étaient plus sévèrement affectées de gingivite, d’ETD, et de CTD que les autres dents. Une antibiothérapie prophylactique devrait être prescrite pour des chats avec maladie parodontale.
(Traduit par Docteur Serge Messier)
Introduction
Periodontal disease, an inflammation of the tissues and supportive structures surrounding the teeth, is one of the most common oral diseases in cats (1–4). The periodontium consists of gingiva, periodontal ligament, alveolar bone and cementum (1–4). Continued inflammation can lead to gingival recession and damage to the cementum, periodontal ligament, and/or alveolar bone (5,6), resulting in loss of teeth. The clinical signs of periodontal disease in cats include halitosis, drooling, pain, discomfort, facial swelling, nasal discharge, gingivitis, accumulation of dental calculus, mobile teeth, inappetence, and loss of teeth (2,3,5). The periodontal disease may have a systemic impact that could result in impairment of other organs such as chronic kidney disease, cardiovascular disease, and septicemia (6–10).
Accumulation of bacteria and plaque on the surface of teeth is suggested to be an underlying culprit for periodontal disease (3). Plaque is a white or yellowish biofilm that is formed by bacteria on the teeth (1), whereas dental calculus is formed by the mineralization of minerals in saliva on soft plaque. The inflammation of gingiva may erupt from irritation caused by bacterial toxins from plaque, inflammation from dental calculus deposition, or the inflammation of other periodontal tissues. Dental calculus and gingivitis cause the destruction of teeth and surrounding tissues, which can lead to severe periodontal disease and loss of teeth (6). Certain oral bacteria, including Fusobacterium spp., Eubacterium spp., and Peptostreptococcus spp., have been found in cats with periodontal diseases (11,12). Thus, feline periodontitis may be linked to the presence of specific bacterial species.
To the best of our knowledge, no study has focused on the relationship between gingivitis, dental calculus thickness (DCT), dental calculus coverage (DCC), and oral bacterial infection in cats without feline leukemia virus (FeLV) or feline immunodeficiency virus (FIV). Since FeLV and FIV may affect the host immune response and compromise the normal gingival tissue function (13), only cats which were free of FeLV and FIV infection were selected for the present study. This study sought to i) evaluate the severity of gingivitis, DCT, and DCC for different teeth; ii) determine the putative correlations between gingivitis score and DCT or DCC score in cats without FeLV and FIV; iii) determine the correlation between gingivitis score and type of oral bacteria; and iv) evaluate cultivable bacterial co-infection and drug sensitivity in cats with periodontal disease.
Materials and methods
Twelve cats, 8 female and 4 male, were randomly selected and enrolled in this study during professional dental cleaning procedures. The median age of cats was 5 y (min-max range: 1 to 10 y). Six cats were domestic shorthaired cats and the other 6 were Persians. All cats were negative for FeLV antigen and FIV antibody as assessed by a commercial enzyme-linked immunosorbent assay (ELISA) test (SNAP FIV/FeLV Combo Test; IDEXX Laboratories, Maine, USA). The experimental procedure for this study was approved by the Kasetsart University Animal Committee (ID number: ACKU04859).
All cats underwent general anesthesia with diazepam (Diapine; Atlantic Pharmaceutical, Bangkok, Thailand), 0.02 mg/kg body weight (BW), IV as a premedication and 1% propofol (Anepol injection; Hana Pharmaceutical, Seoul, South Korea), 2 to 4 mg/kg BW, IV for anesthetic induction. The general anesthesia was maintained using 2% isoflurane (Attane; Piramal Critical Care, Pennsylvania, USA) in oxygen. An oral examination was performed on each cat and gingivitis, DCT, and DCC were scored using a modified Silness and Löe scoring system (Table I). All scores were evaluated by a single veterinary dentist (14). The scores were noted for each tooth and then were combined by tooth type and recorded, as canine, 2nd premolar, 3rd premolar, 4th premolar, and 1st molar teeth. The scores for 3rd premolar, 4th premolar, and 1st molar teeth of both the upper and the lower jaw were combined as caudal maxillary teeth and caudal mandibular teeth, respectively.
Table I.
Scoring system for gingivitis, dental calculus thickness, and dental calculus coverage scores
| Gingivitis score | |
|---|---|
| Score | Description |
| 0 | normal |
| 1 | no gingival bleeding on probing examination |
| 2 | gingival bleeding on probing examination |
| 3 | severe inflammation; gingival hypertrophy and spontaneous gingival bleeding |
| Dental calculus thickness score | |
| Score | Description |
| 0 | absence of dental calculus |
| 1 | dental calculus thickness < 0.5 mm |
| 2 | dental calculus thickness 0.5 to 1.0 mm |
| 3 | dental calculus thickness > 1.0 mm |
| Dental calculus coverage score | |
| Score | Description |
| 0 | absence dental calculus |
| 1 | dental calculus coverage at supragingival margin |
| 2 | moderate coverage of dental calculus at supragingival and subgingival margin |
| 3 | wide coverage of dental calculus at supragingival and subgingival margin |
The gingivitis score ranged from 0 to 3, based on the degree of inflammation and bleeding. The gingival score was determined using a sterile blunt probe (Probe CP10; Dental USA, Illinois, USA). A score of 0 indicated a normal gingiva and no inflammation. A score of 1 indicated the presence of mild inflammation of the gingiva, a slight change in color and edema, and no bleeding upon probing. A score of 2 indicated moderate inflammation of the gingiva with the presence of gingival bleeding upon probing. Finally, a score of 3 indicated severe inflammation of the gingiva, severe gingival redness and swelling with the presence of severe and spontaneous gingival bleeding. Gingivitis scores of 0 and 1 were combined as less clinically relevant gingivitis and gingivitis scores of 2 and 3 were combined to a more clinically relevant gingivitis group to determine a possible association among bacterial groups and the severity of gingivitis scores.
Dental calculus thickness scores ranged from 0 to 3. A score of 0 reflected the absence of dental calculus. A score of 1 indicated a dental calculus thickness of up to 0.5 mm, while a score of 2 indicated a dental calculus thickness ranging from 0.5 to 1.0 mm. Finally, a score of 3 indicated a dental calculus thickness of more than 1 mm.
Dental calculus coverage scores were characterized on a scale of 0 to 3. A score of 0 indicated the absence of dental calculus. A score of 1 indicated mild calculus coverage at the supragingival margin (up to 1 mm). A score of 2 indicated a moderate amount of supragingival and subgingival calculus, while a score of 3 indicated wide calculus coverage in both the supragingival and subgingival areas.
Aerobic and anaerobic bacteria were sampled using a sterile absorbent endodontic paper points (Paper points; Shanghai Dental, Bangkok, Thailand). The paper points were inserted and left in the subgingival area for 30 s near the left maxillary and mandibular 4th premolar teeth. The paper points were immediately stored in Amies Transport Medium (Difco Transport Medium Amies; Becton Dickinson, Franklin Lakes, New Jersey, USA) and thioglycolate broth (Fluid thioglycolate medium; Himedia Laboratories Pvt., Mumbai, India) as transport media for both aerobic and anaerobic bacteria, respectively. Aerobic bacteria were cultured on blood agar (BBL blood agar base (infusion agar); Becton Dickinson, Franklin Lakes, New Jersey, USA) and MacConkey agar (Difco MacConkey agar; Becton Dickinson), while the anaerobic bacteria were cultured on thioglycolate medium and anaerobe basal agar (Anaerobe basal agar; Oxoid, Hampshire, England). Drug sensitivities of the bacteria were determined using an elution test.
A commercially available software package (GraphPad Prism version 5.0; GraphPad Software, La Jolla, California, USA) was applied to the data for statistical analysis. A normality test for each score was performed using the Shapiro-Wilk W-test. The severities of gingivitis, DCT, and DCC scores for each tooth were compared using a Kruskal-Wallis test. Dunn’s post-test was used to determine differences among groups. The 3 scores of the caudal maxillary teeth and the mandibular teeth were also compared using a Mann-Whitney U-test. The Spearman rank sum correlation test (ρ) was applied to determine the relationship between the gingivitis score and DCC or DCT score. Fisher’s exact test also was applied to evaluate the association between bacterial groups and the severity of gingivitis score. Results were considered to be statistically significant at P < 0.05.
Results
The median and range of gingivitis, DCT, and DCC scores for all teeth are shown in Table II. The difference in gingivitis, DCT, and DCC scores for different teeth were statistically significantly different (P < 0.0001, 0.0002, and 0.0001, respectively; Figure 1). Dunn’s post-test analysis revealed that gingivitis scores were significantly lower for canine teeth than for 3rd premolar, 4th premolar, or 1st molar teeth (P = 0.0388, 0.0007, and 0.0013, respectively). The gingivitis scores for 2nd premolar teeth were significantly lower than those for the 4th premolar or 1st molar teeth (P = 0.0264 and 0.0256, respectively). Dental calculus thickness scores were significantly higher for 1st molar teeth than for canine teeth (P = 0.0243). Dental calculus thickness scores were significantly higher for 4th premolar teeth than for the canine or 2nd premolar teeth (P = 0.0014 and 0.0222, respectively). Finally, DCC scores were significantly lower for canine teeth than for the 3rd premolar, 4th premolar, or 1st molar teeth (P = 0.0255, 0.0007, and 0.0050, respectively). Dental calculus coverage scores were significantly lower for 2nd premolar teeth than for 4th premolar teeth (P = 0.0456).
Table II.
The median (min to max range) for gingivitis scores, dental calculus thickness (DCT) scores, and dental calculus coverage (DCC) scores for each tooth
| Dental scores | Canine | 2nd Premolar | 3rd Premolar | 4th Premolar | 1st Molar |
|---|---|---|---|---|---|
| Gingivitis | |||||
| Upper teeth | 1.0 (0.5 to 2.0) | 1.0 (0 to 2.0) | 1.8 (1.0 to 3.0) | 2.5 (1.0 to 3.0) | 2.8 (2.0 to 3.0) |
| Lower teeth | 1.0 (0 to 1.5) | N/A | 1.0 (0 to 3.0) | 1.8 (0 to 3.0) | 2.0 (0 to 3.0) |
| Dental calculus thickness | |||||
| Upper teeth | 1.0 (0 to 2.0) | 1.0 (0 to 2.0) | 2.5 (0 to 3.0) | 3.0 (0 to 3.0) | 3.0 (2.0 to 3.0) |
| Lower teeth | 0.8 (0 to 1.0) | N/A | 1.0 (0 to 3.0) | 1.3 (0 to 3.0) | 1.5 (0 to 3.0) |
| Dental calculus coverage | |||||
| Upper teeth | 1.0 (0 to 2.0) | 1.0 (0 to 3.0) | 1.8 (0.6 to 3.0) | 2.5 (0.5 to 3.0) | 1.5 (0 to 3.0) |
| Lower teeth | 1.0 (0 to 3.0) | N/A | 1.0 (0 to 3.0) | 1.8 (0 to 3.0) | 2.0 (0 to 3.0) |
N/A — Not available — the mandibular 2nd premolar tooth is absent in cats.
Figure 1.
Gingivitis, dental calculus thickness (DCT), and dental calculus coverage (DCC) scores for each tooth evaluated. The medians of each score are shown in dashed lines. Columns not sharing a common script are significantly different (P < 0.05).
The gingivitis scores for caudal maxillary teeth were not significantly different from the gingivitis scores for caudal mandibular teeth (P = 0.1862), whereas the DCT and DCC scores for caudal maxillary teeth were more severe than those for caudal mandibular teeth (P = 0.0009 and 0.0042, respectively; Figure 2).
Figure 2.
Comparison of gingivitis, dental calculus thickness (DCT), and dental calculus coverage (DCC) scores of caudal maxillary and mandibular teeth.
A strong relationship between gingivitis scores and DCT scores was found (ρ = 0.8862; P < 0.0001). In addition, a strong relationship between gingivitis scores and DCC scores was found (ρ = 0.8758; P < 0.0001), as shown in Figure 3.
Figure 3.
The linear relationships between gingivitis scores and dental calculus thickness (DCT) or dental calculus coverage (DCC) scores.
The bacterial culture from the gingival sulcus of the left maxillary and mandibular 4th premolar teeth from 12 cats revealed 71.1% and 28.9% aerobic and anaerobic bacterial species, respectively, as shown in Table II. The aerobic bacteria identified in this study were Pasteurella multocida, Streptococcus spp., Enterococcus spp., Staphylococcus spp., Bacillus cereus, Escherichia coli, and Pseudomonas aeroginosa. Meanwhile, anaerobic bacterial species identified included Bacteroides spp., Peptostreptococcus anaerobius, and Eubacterium aerofaciens. Bacteroides spp. was a commonly identified anaerobic bacterium in cats with higher gingivitis scores (P = 0.0278). Associations between bacterial groups and gingivitis scores are shown in Table III.
Table III.
Aerobic and anaerobic bacterial culture results from samples collected from the gingival sulcus of the left maxillary and mandibular 4th premolar in 12 cats and the association between bacterial groups and gingivitis scores
| Bacterial groups | Bacterial species | Number of cats (% of total bacterial species identified) | Gingivitis scores | Fisher’s exact test (P-value) | |
|---|---|---|---|---|---|
|
| |||||
| 0 to 1 (n = 7) | 2 to 3 (n = 5) | ||||
| Aerobic bacteria | Pasteurella multocida | 10 (26.3%) | 7 | 3 | 0.1515 |
| Streptococcus spp. | 7 (18.5%) | 3 | 4 | 0.2929 | |
| Enterococcus spp. | 4 (10.5%) | 1 | 3 | 0.2222 | |
| Staphylococcus spp. | 3 (7.9%) | 2 | 1 | 0.5500 | |
| Bacillus cereus | 1 (2.6%) | 0 | 1 | 0.5500 | |
| Escherichia coli | 1 (2.6%) | 0 | 1 | 0.5500 | |
| Pseudomonas aeruginosa | 1 (2.6%) | 0 | 1 | 0.5500 | |
| Anaerobic bacteria | Bacteroides spp. | 7 (18.5%) | 2 | 5 | 0.0278 |
| Peptostreptococcus anaerobius | 3 (7.9%) | 0 | 3 | 0.1058 | |
| Eubacterium aerofaciens | 1 (2.6%) | 0 | 1 | 0.5500 | |
Antimicrobial sensitivity testing for all anaerobic bacteria species identified in this study is shown in Table IV. All of the anaerobic bacteria were sensitive to clindamycin, chloramphenicol, metronidazole, cefoxitin, or tetracycline. Peptostreptococcus anaerobius and Eubacterium aerofaciens were sensitive to erythromycin and penicillin. Pasteurella multocida, the most abundant aerobic bacterial species, was sensitive to cefoxitin in all cats.
Table IV.
Antimicrobial sensitivity for anaerobic bacteria that were identified from the left maxillary and mandibular 4th premolar gingival sulcus in cats
| Antimicrobials | Bacteroides tectum (n = 3) | Bacteroides buccae (n = 2) | Bacteroides oralis (n = 1) | Eubacterium aerofaciens (n = 1) | Peptostreptococcus anaerobius (n = 3) | Number of cats (%) |
|---|---|---|---|---|---|---|
| Penicillin | S | R | S | S | S | 8 (80%) |
| Cefoxitin | S | S | S | S | S | 10 (100%) |
| Clindamycin | S | S | S | S | S | 10 (100%) |
| Erythromycin | S | S | R | S | S | 9 (90%) |
| Chloramphenicol | S | S | S | S | S | 10 (100%) |
| Tetracycline | S | S | S | S | S | 10 (100%) |
| Metronidazole | S | S | S | S | S | 10 (100%) |
S — susceptible; R — resistant.
Discussion
Periodontal disease has been reported as the most common disease to cause health issues in cats with a prevalence of 13.8% of the cat population (4). In the present study, the association of gingivitis with dental calculus and bacterial infection was evaluated in 12 cats undergoing routine dental cleaning. Accumulation of dental calculus was identified in premolar and 1st molar teeth with the presence of gingivitis. Bacterial culture as well as antimicrobial sensitivity testing was also performed on samples from the gingival sulcus. Interestingly, high gingivitis scores in our cats were significantly associated with the identification of anaerobic bacterial species.
The incisors were not evaluated herein because they are small in cats and commonly lost. These teeth would not be representative of common dental problems found in a clinic. The rostral and caudal teeth were divided by the occlusion of the upper and lower teeth. The interdigitate occlusion was identified on the canine teeth (maxilla and mandible) and 2nd premolar (maxilla) teeth. In addition, the maxillary dental arch is slightly wider than the mandibular dental arch, so that the maxillary 3rd premolar, 4th premolar, and 1st molar teeth slightly overlap those of the mandibular teeth. The results of this study indicate that the canine and 2nd premolar teeth have less severe gingivitis, and lower DCT, and DCC scores than the 3rd premolar, 4th premolar, and 1st molar teeth. This could be explained by the openings of the ducts from the parotid and zygomatic salivary glands that are located near the 4th premolar and the 1st molar teeth (15,16). Mineral deposition from the saliva in this area may cause dental calculus formation. Furthermore, dental calculus formation may lead to the irritation of gingiva thus causing gingivitis.
Dental calculus thickness and DCC scores were significantly higher for the caudal maxillary teeth than for the caudal mandibular teeth. This difference can be attributed to the anatomical occlusion of the caudal maxillary teeth and the caudal mandibular teeth. Because the maxillary dental arch is wider than the mandibular dental arch in cats, the mechanical scrubbing action during mastication helps lower dental calculus build-up of the caudal mandibular teeth.
The relationship between gingivitis scores and DCT or DCC scores was positively correlated. This may support the idea that dental calculus in cats is followed by the development of gingivitis (6). However, the severity of gingivitis may not solely depend on DCT and DCC. In this study, the gingivitis scores for the caudal upper teeth did not differ significantly from those for the caudal lower teeth, suggesting that the underlying causes of gingivitis are multifactorial. As reported in previous studies, cats with resorptive lesions, dental calculus, food allergies, and infectious diseases, such as FeLV, FIV, feline calicivirus, and oral bacteria are predisposed to developing gingivitis (12,17–19).
The aim of this study was to determine the association of gingivitis with DCT or DCC and subgingival bacterial infection. The periodontal pocket depth and oral radiographic evaluation were not fully performed to determine a periodontitis condition; however, the significance of this study should not be affected because bacterial-induced gingivitis has been reported in non-plaque, plaque, or periodontitis conditions (20,21).
The development of gingivitis in cats infected with FeLV and FIV was not evaluated in the present study. Cats infected with either FeLV or FIV are more susceptible to periodontal disease because of the impaired immune system that may further compromise the gingiva of cats that already have dental calculus and bacterial infections (12,22). To eliminate gingivitis that may have been attributed in part to FeLV or FIV infection, all cats with these infections were excluded from this study. One limitation of the present study is that the cats were not tested for feline calicivirus infection. However, calicivirus infections also cause severe stomatitis (23), which was not identified in any of the cats in this study.
Thioglycolate broth is primarily developed for determining the oxygen requirement of microorganisms and also to aid in the isolation of obligate anaerobes when used as a transport medium (24,25). Since sodium thioglycolate in the transport medium utilizes oxygen in the medium, it protects the obligate anaerobes from oxygen damage. Various studies indicated the crucial role of anaerobic infection as an underlying culprit of gingivitis and periodontitis, thus it is recommended that thioglycolate broth be applied as a transport medium, especially in feline patients with severe gingivitis.
The results of this study resemble those of other studies. It has been reported previously that Bacteroides spp. and Peptostreptococcus anaerobius were isolated from cats with severe gingivitis scores and that Pasteurella multocida was isolated from most samples with lower gingivitis scores (26). Similarly, this study found Bacteroides spp. in cats with high gingivitis scores. This study also identified Pasteurella multocida in 10 of the 12 cats (7 cats with lower gingivitis scores and 3 cats with higher gingivitis scores); however, there was no statistical association between Pasteurella multocida and gingivitis scores. Consistent with the present study, anaerobic bacterial infection has been shown to be a risk factor for severe gingivitis (3). Specialized transport media served as an important tool for helping to identify and increase the chance of isolating anaerobic bacteria in our study.
Antibiotic treatment is recommended as an adjunctive treatment for cats after professional dental cleaning and in cats with periodontitis (27,28). The drug sensitivity results in this study suggest that cats with severe gingivitis scores may be given cefoxitin, clindamycin, chloramphenicol, tetracycline, or metronidazole as a first-line antibiotic agent for the treatment of anaerobic bacteria. Routine dental care also should be encouraged to slow down plaque formation and the development of future periodontitis.
In conclusion, the findings of this study indicate that the caudal maxillary and mandibular teeth of cats tend to have more severe gingivitis, DCT, and DCC scores than other teeth. Therefore, cat owners and veterinarians should pay more attention to these areas during dental care. Anaerobic bacterial infection also plays a crucial part in the development of gingivitis in cats. Antibiotic prophylaxis for feline dental procedure is also recommended to minimize risk of local as well as systemic infectious complications originated from gingival bacteria. Future research should be aimed at investigating factors contributing to gingivitis in cats.
Acknowledgments
We thank Dr. Parnchitt Nilkamhang, Dr. Piyaporn Wattanaphan, and Piriyaporn Chontrakool for technical support.
The preliminary result was presented in poster form at the American College of Veterinary Internal Medicine 2011 Forum, Denver, Colorado, USA, June 2011.
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