Periodontal disease burden and pathological changes in organs of dogs

Bacterial plaque associated periodontal disease is the most common chronic infection in man and dogs. In man, there is an association between periodontal disease and myocardial infarction and stroke, while in dogs it has also been associated with changes in internal organs. Inflamed periodontal tissues present a 'periodontal disease burden' to the host and the extent of this inflammatory disease burden is likely to affect the degree of associated pathological change in distant organs. This hypothesis was investigated in dogs with naturally occurring periodontal disease. Post-mortem investigations including periodontal assessment, standard necropsy, and organ histology were performed on 44 mature toy and miniature Poodles (related, periodontitis predisposed breeds) that died naturally or were euthanized based on clinical disease. Animals with gross primary organ pathology were excluded. The periodontal disease burden was estimated from the total surface area of periodontal pocket epithelium using six measurements of probing depth for each tooth and the tooth circumferences. Ordinal logistic regression (OR) analysis established that for each square centimeter of periodontal disease burden there was a 1.4-times higher likelihood of greater changes being present in the left atrio-ventricular valves (OR = 1.43), plus 1.2 and 1.4 times higher likelihoodfor greater liver and kidney pathology (OR = 1.21; OR = 1.42), respectively The results show that there is a link between the estimated 'periodontal disease burden' resulting from plaque-bacteria associated periodontal disease and the level of internal pathology in this population, implying that periodontitis might contribute to the development of systemic pathology in dogs.     

犬牙周病的临床研究进展

牙周病(periodontal disease, PD)是由细菌在牙齿表面聚集形成的牙菌斑和牙结石逐渐侵蚀牙周组织,引发周围组织炎症的一类疾病。根据疾病的发展进程,可分为齿龈炎与牙周炎2个阶段。在小动物临床疾病中牙周病尤为常见,世界范围内约有80%的成年犬患有该病。由于饲主对于犬的口腔保健意识薄弱且该疾病隐秘性较高,患犬就诊时往往已出现牙周支持组织不可逆的损伤,细菌及其毒力因子通过血液循环进入全身从而引发系统性疾病的风险大大提高。但目前犬牙周病的核心致病菌属、菌群失调的原因与发病机制尚不明确。因此,笔者基于高通量测序方法的病原学研究结果,分析与疾病发展相关的微生物群。同时,整合目前世界通用的最新犬牙周病临床诊断分级标准及犬牙周病的中西医防治方案,分析犬牙周病与全身系统性疾病之间的相关性,系统综述犬牙周病在国内外小动物临床领域的研究进展,以期为该类疾病的临床诊疗提供理论参考,推进兽医师在临床实践中更高效地开展该类疾病的诊疗工作,并为犬牙周病相关的临床研究提供思路。     

Pigmented-anaerobic bacteria associated with canine periodontitis

The etiology of human periodontal disease has been the focus of considerable research, yet relatively little is known about the causative agents of companion animal periodontitis. In humans, Porphyromonas gingivalis, a black-pigmented anaerobic bacteria (BPAB), has been implicated as the primary periopathogen. It has been demonstrated that BPAB are also found in companion animal periodontal pockets. While some animal BPAB have been individually identified, a study to identify the most frequently isolated subgingival BPAB has not been completed using genetic tools. The objective of this work was to identify the types and relative frequencies of pigmented anaerobic bacteria found in the periodontal pockets of dogs. Porphyromonas salivosa, Porphyromonas denticanis (a novel species) and Porphyromonas gulae were found to be the most frequently isolated BPAB associated with canine periodontitis.     

Clinical and patho-morphological investigation of spontaneously occurring Seriodontal isease in dogs

Diagnostic evaluation of, and treatment planning for, different periodontal diseases of dogs are a common problem in veterinary dentistry. Therefore the aim of the present study was to propose a classification for inflammatory periodontal disease. One hundred and twenty-three male and female poodles (from two to over 12 years) were used for the clinical investigations; 120 periodontitis teeth were analysed for pathomorphological signs of inflammation. The recorded data made it possible to differentiate five forms of gingivitis (gingivitis simplex, hyperplastica, ulcerosa, granulomatosa and desquamativa) and three forms of periodontitis (juvenile, rapidly progressive adult and chronic adult periodontitis). The pathomorphological investigations allowed a differentiation between acute progressive inflammation, chronic nonprogressive inflammation, chronic proliferative inflammation and chronic resorptive inflammation. It is concluded that standardised diagnoses as well as the pathomorphological background may be helpful tools for providing effective treatment strategies.     

Measurement of total antioxidant capacity in gingival crevicular fluid and serum in dogs with periodontal disease

OBJECTIVE: To determine whether gingival crevicular fluid (GCF) and serum total antioxidant capacities (TACs) correlate with the degree of severity of periodontal disease in dogs. ANIMALS: 41 Toy and Miniature Poodles. PROCEDURES: After assessment of the degree of severity of naturally occurring periodontitis, GCF samples from both maxillary fourth premolars and a blood sample were collected from each dog. The condition of the periodontium of the entire dentition and at each site of GCF collection was recorded. Clinical parameters assessed included plaque index, gingival index, and probing depth. Radiographic analysis of alveolar bone level was also performed. Total antioxidant capacity was measured in GCF and serum samples by use of a commercial kit. RESULTS: Dogs with gingivitis and minimal periodontitis had significantly higher TAC in GCF than dogs with advanced periodontitis. Bivariate regression analysis revealed significant negative correlations between TAC in GCF and clinical parameters and age. The TAC in serum was significantly negatively correlated with the degree of gingival inflammation but was not significantly correlated with age. CONCLUSIONS AND CLINICAL RELEVANCE: TAC in GCF is related to the degree of severity of periodontal disease in dogs. This is likely the result of release of reactive oxygen species by activated phagocytes and fibroblasts in the inflamed periodontal tissues. The results of our study suggest that the local delivery of antioxidants may be a useful adjunctive treatment for periodontitis in dogs.     

Evaluation of cross-protection by immunization with an experimental trivalent companion animal periodontitis vaccine in the mouse periodontitis model

Companion animal periodontal disease is one of the most prevalent diseases seen by veterinarians. The goal of this study was to evaluate the vaccine performance of a trivalent canine periodontitis vaccine in the mouse oral challenge model of periodontitis. Mice vaccinated subcutaneously with an inactivated, whole-cell vaccine preparation of Porphyromonas denticanis, Porphyromonas gulae, and Porphyromonas salivosa displayed significantly reduced alveolar bone loss in response to heterologous and cross-species challenges as compared to sham vaccinated animals. Based on the results of these studies, a periodontitis vaccine may be a useful tool in preventing the initiation and progression of periodontitis caused by the most commonly isolated pigmenting anaerobic bacteria in animals.     

Association between chronic azotemic kidney disease and the severity of periodontal disease in dogs

Naturally occurring periodontal disease affects >75% of dogs and has been associated with cardiac lesions and presumptive endocarditis. However, the relationships between periodontal disease and chronic kidney disease (CKD) in dogs have not been studied. In a retrospective longitudinal study the incidence of azotemic CKD was compared between a cohort of 164,706 dogs with periodontal disease and a cohort of age-matched dogs with no periodontal disease from a national primary care practice. These dogs contributed 415,971 dog-years of follow-up from 2002 to 2008. Hazard ratios and 95% confidence intervals from Cox regression were used to compare the incidence of azotemic CKD in dogs with stage 1, 2, or 3/4 periodontal disease to dogs with no periodontal disease. The hazard ratio for azotemic CKD increased with increasing severity of periodontal disease (stage 1 hazard ratio=1.8, 95% confidence interval: 1.6, 2.1; stage 2 hazard ratio=2.0, 95% confidence interval: 1.7, 2.3; stage 3/4 hazard ratio=2.7, 95% confidence interval: 2.3, 3.0; P(trend)=<0.0001) after adjustment for age, gender, neuter status, breed, body weight, number of hospital visits, and dental procedures. Increasing severity of periodontal disease was also associated with serum creatinine >1.4 mg/dl and blood urea nitrogen >36 mg/dl, independent of a veterinarian's clinical diagnosis of CKD.     

Repair of experimental plaque-induced periodontal disease in dogs

Forty mongrel dogs were used in this study for induction of periodontal disease by placing subgingival silk ligatures affecting maxillary and mandibular premolar teeth during a 12-month period. Experimental premolar teeth received monthly clinical, radiographic, and histometric/pathologic assessments. The results demonstrated significant increases in scores and values of periodontal disease parameters associated with variable degrees of alveolar bone loss. The experimental maxillary premolar teeth exhibited more severe and rapid rates of periodontal disease compared with mandibular premolar teeth. Histometric analysis showed significant reduction in free and attached gingiva of the experimental teeth. Histopathological examination of buccolingual sections from experimental premolar teeth showed the presence of rete pegs within the sulcular epithelium with acanthosis and erosive changes, widening of the periodontal ligament, and alveolar bone resorption. Various methods for periodontal repair were studied in 194 experimental premolar teeth exhibiting different degrees of periodontal disease. The treatment plan comprised non-surgical (teeth scaling, root planing, and oral hygiene) and surgical methods (closed gingival curettage, modified Widman flap, and reconstructive surgery using autogenous bone marrow graft and canine amniotic membrane). The initial non-surgical treatment resulted in a periodontal recovery rate of 37.6% and was found effective for treatment of early periodontal disease based on resolution of gingivitis and reduction of periodontal probing depths. Surgical treatment by closed gingival curettage to eliminate the diseased pocket lining resulted in a recovery rate of 48.8% and proved effective in substantially reducing deep periodontal pockets. Open root planing following flap elevation resulted in a recovery rate of 85.4% and was effective for deep and refractory periodontal pockets. Autogenous bone graft implantation combined with canine amniotic membrane as a biodegradable membrane was used in 18 premolar teeth and failed to improve advanced furcation defects in most teeth.     

Oral flora of mongrel and beagle dogs with periodontal disease

The plaque flora was studied in adult mongrel and beagle dogs with periodontal disease. Gingival plaque from maxillary premolars was removed and cultured on various growth media. The flora in all dogs was composed of mostly anaerobic gram negative rods. Bacteroides asaccharolyticus was found in the highest proportion of plaque samples from mongrel dogs, and decomposed hydrogen peroxide suggesting catalase activity. Fusobacterium nucleatum was found in higher proportion in the plaque of beagle dogs as compared to B. asaccharolyticus. With the increasing numbers of obligative anaerobic gram negative organisms such as B. asaccharolyticus, the proportions of Streptococcus, Enterococcus and Staphylococcus decreased in the dogs with periodontal disease. The salivary flora was different from the plaque flora of the dogs with periodontal disease. It was constant regardless with the disease. The salivary flora of beagle dogs with the healthy gingiva was different from that of mongrel dogs. Enterococcus, Lactobacillus, Eubacterium and black-pigmented Bacteroides (BPB, mainly B. asaccharolyticus) were higher proportion in the flora of beagle dogs as compared to mongrel dogs, while Fusobacterium, Enterobacteriaceae, yeast and molds were lower in the flora. The results reveal that B. asaccharolyticus and F. nucleatum are common pathogens and uniquely contribute to the development of gingival inflammation in dog.     

A review of the frequency and impact of periodontal disease in dogs

Periodontal disease is a frequent problem seen in veterinary practices. Primary-care veterinary practices, where diagnosis of periodontal disease is predominantly based on visual oral assessment of conscious dogs, report an average prevalence of 9.3 to 18.2% within the dog population. Detailed examinations of anaesthetised dogs report much higher prevalence of between 44 and 100%. The prevalence and severity of periodontitis varies between sizes of dogs, breeds and individuals. The lack of robust evaluation of these variances opens the opportunity for a review of the topic. A literature search was therefore undertaken to determine the frequency and extent (severity and oral location) of periodontal disease in the dog population. Both clinical and retrospective data based surveys of veterinary records, show there is an increased likelihood of developing periodontitis as age increases and with bodyweight decreases. The maxillary and mandibular incisors, fourth premolars and first molars are likely to develop the disease first although in some breeds the canines may also be involved. Poor oral care is a significant risk factor for the development of periodontal disease although diet, behaviour, environment and genetics are also likely to play a role. The information provided in this review can be used by veterinarians to improve the effectiveness of their diagnosis, treatments and interventions by focussing their efforts on the sizes, breeds and individuals most at risk. Given the potential link between periodontal disease and systemic health, veterinarians have the opportunity to positively impact the quality of life of a large number of dogs and therefore their owners.     

Anaerobes in periodontal disease in the dog: a review

As anaerobic sampling and culture techniques improved, the documented prevalence of anaerobic bacteria in periodontal disease has increased. The anaerobic bacteria have become more well-known in humans and consequently in dogs, since this species is a major model in periodontal studies. A review of the literature related to anaerobic flora is described.     

Assessment of Alloxan-Induced Diabetic Rats as a Periodontal Disease Model Using a Selective Cyclooxygenase (COX)-2 Inhibitor

Several recent studies have reported that alloxan-treated rats with long-term hyperglycemia can develop naturally occurring periodontal disease (PD). Our previous studies detected dental caries in the same model. Therefore, these two lesions of different etiologies are expected to occur concurrently. In this study, we evaluated the use of diabetic rats as a PD model by employing a selective COX-2 inhibitor reported to be effective against PD. Six-week-old female F344 rats were divided into 3 groups: intact rats (control), alloxan-induced diabetic rats fed a standard diet (AL) and alloxan-induced diabetic rats fed a diet containing 0.01% etodolac (AL+Et). The animals were euthanized at 26 weeks of age, and their oral tissues were examined histopathologically. Gingivitis, marginal periodontitis and alveolar bone resorption were markedly enhanced along with dental caries in the AL group compared with the control group. However, the COX-2 inhibitor had no effect on periodontal inflammation in the AL+Et group. In addition, in the AL group, periodontitis was notably nonexistent around the normal molars, and gingivitis was scarcely worse than that in the control group. In the diabetic rats, the progression of periodontal inflammation was closely correlated with the severity of adjacent dental caries, and marginal periodontitis was frequently continuous with apical periodontitis. In conclusion, an alloxan-induced diabetic rat is not a model of PD but of dental caries. It is probable that in this model, hyperglycemia may enable crown caries to progress to apical periodontitis, while the associated inflammation may rostrally expand to surrounding periodontal tissue.     

Diet and periodontal disease in dogs and cats

SUMMARY A review of relevant literature was undertaken because of concerns about a possible relationship between pet foods, development of periodontal disease, and secondary adverse effects on general health. It was concluded that, while changes in feeding methods in recent decades have arguably improved pet health by reducing or preventing diseases associated with nutritional deficiencies and excesses, periodontal disease remains a serious, diet-related problem. There is reasonable evidence that soft diets are associated with increased frequency and severity of periodontal disease, and that harder foods requiring vigorous prehension and mastication are preferable for dogs and cats. While it is plausible that periodontal disease could cause diseases in other organs and tissues, the evidence for this is limited at present. Further research is needed to better define the relationship between diet types and oral health. In the meantime, veterinarians and pet owners should pay attention to the physical qualities (textures, abrasiveness, ‘chewiness’) of foods they provide for dogs and cats, as well as to their nutrient content, and should consider additional methods to control plaque and prevent periodontal disease where necessary.     

Dietary influences on periodontal health in dogs and cats.

A pet cannot be healthy without oral health. Periodontal is a significant disease that has local and systemic ramifications. It has been stated earlier that effective plaque control prevents gingivitis. In human beings, 90% of periodontitis occurs as the result of progression gingivitis, and this type of periodontitis can be completely prevented by plaque control. It is reasonable that dogs and cats react similarly and that effective plaque control could prevent a large percentage of periodontitis cases. Proper nutrition and effective oral hygiene are necessary components of oral health and should be jointly promoted in the management of oral disease in dogs and cats.     

Mandibulectomy for treatment of fractures associated with severe periodontal disease

Six cases of mandibular fractures associated with severe periodontal disease that had been treated by mandibulectomy, due to intense bone loss, were evaluated retrospectively. The dogs were mainly older, small breed dogs that had suffered a traumatic event. Four dogs had a bilateral mandibulectomy and 2 a unilateral mandibulectomy.     

Histological evaluation of the pulp in teeth from dogs with naturally occurring periodontal disease

The purpose of this investigation was to evaluate the pulp of dog teeth affected by advanced periodontal disease. Histological examination was done on demineralized teeth extracted during clinical treatment of mature, client owned small and medium-size breed dogs with either good periodontal health or with advanced naturally occurring periodontal disease. Routinely stained sections from 5 clinically normal teeth and 22 teeth with advanced periodontitis from dogs between 5 and 12-years of age were examined using light microscopy. The pulp cavities of most teeth were narrow with low cellularity and some fibrosis of the pulp. Findings specific to periodontally affected teeth included acute and chronic pulpitis, vascular congestion, and pulp necrosis. A glomus body was identified in the pulp of one tooth and areas of poorly mineralized cementum were seen in both normal and diseased teeth. Age related changes in dog teeth appear similar to those reported for man and the rat. In addition to age related changes, the pulp of dog teeth with advanced periodontal disease were frequently inflamed or necrotic. This may reflect the advanced periodontitis affecting these teeth or a mechanical effect related to excessive tooth mobility. Further study is required to determine the etiology and significance of these findings and to investigate pulp status in less severely diseased teeth.     

Efficacy of enamel matrix protein applied to spontaneous periodontal disease in two dogs

Enamel matrix protein (EMP) was applied for regeneration of periodontal tissue in 2 dogs with spontaneous periodontal disease. Case 1 had bony resorption around the root and root apex of the maxillary fourth premolars. Case 2 had vertical resorption of bone between the mandibular first and second molars. A flap was formed in the buccal gingiva, and EMP was applied onto the surface of the exposed root. One or 4 months postoperatively, increased bone level and clinical attachment were recognized. EMP was therefore suggested to be effective to induce regeneration of periodontal tissues in the cases with periodontal disease.     

Ecology of genus Porphyromonas in canine periodontal disease.

Asaccharolytic pigmented Porphyromonas species, including P. endodontalis, P. gingivalis, P. circumdentaria and unclassified species, were isolated from the plaque of adult dogs, but not from any oral sites of puppies and adolescent dogs. With age-dependency, the proportion of Porphyromonas species in the flora of plaque increased. Isolation of the genus Porphyromonas was clearly associated with the progress of periodontol disease. We suggested that Porphyromonas is the exogenous organism and obligate pathogen for canine periodontal diseases.     

Association of Treponema spp. with canine periodontitis

To evaluate the association of oral Treponema (T.) spp. with severity of canine periodontitis, subgingival plaque samples of dogs of various breeds undergoing surgery were investigated. A wide range of oral Treponema spp. was analysed by a molecular and culture-independent approach applying DNA-DNA dot blot hybridization analysis and fluorescence in situ hybridization using Treponema specific oligonucleotide probes specific for phylogenetic groups I-VII of oral treponemes as well as probes specific for T. socranskii and T. denticola. To assess the periodontal status of affected dogs clinical parameters were measured and the periodontal status was classified from grade 0 (physiological periodont) to 3 (severe periodontitis). The periodontal status correlated significantly with an increasing concentration of volatile sulfur compounds (VSC, r=0.854) determined with a Halimeter, indicating a positive correlation between the presence of VSC-producing bacteria and periodontitis. In this study Treponema spp. of phylogenetic groups III, V-VII were not detected in any sample, whereas T. denticola-like treponemes were found only in 2 of 51 animals. However, treponemes belonging to phylogenetic groups I, II and IV of oral treponemes or T. socranskii were found in up to 64.84% of the dogs. The detection rate of Treponema spp. was significantly associated with an increased periodontal status. Treponemes present in periodontal lesions were also visualized by fluorescence in situ hybridization of gingival biopsies showing Treponema spp. not only in the microbial biofilm but also within the gingival tissue. The data presented here indicate that oral Treponema spp. are associated with canine periodontitis. Similar to human periodontitis, treponemes of groups I, II and IV and T. socranskii were found more frequently the higher the degree of periodontitis was.     

A longitudinal assessment of periodontal health status in 53 Labrador retrievers

Objectives

To determine the incidence and rates of progression of gingivitis and periodontitis in Labrador retrievers.

Materials and Methods

Fifty‐three dogs, aged 1·1 to 5·9 years, had their periodontal health assessed every 6 months for up to 2 years. The extent of gingivitis and periodontitis was measured around the whole gingival margin of every tooth under general anaesthesia.

Results

All dogs had gingivitis at the initial assessment. The majority (64·2%) of tooth aspects had very mild gingivitis. The palatal/lingual aspect of all tooth types was most likely to show bleeding when probed: 63·0% of these aspects had mild or moderate gingivitis. Over 2 years, 56·6% of dogs developed periodontitis and dogs as young as 1·9 years were affected. There was a significant positive correlation between the proportion of teeth with periodontitis and age. In total, 124 teeth (5·7%) developed periodontitis; 88 (71·0%) of these were incisors. The palatal/lingual aspect of the incisors developed the disease first (2·8% of incisor aspects).

Clinical Significance

Periodontitis developed in regions that are difficult to see in conscious dogs implying that detection and treatment of disease requires periodic sedation or anaesthesia.