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The Subgingival Microbial Community of Feline Periodontitis And www.nature.com/scientificreports OPEN The subgingival microbial community of feline periodontitis and gingivostomatitis: Received: 2 January 2019 Accepted: 14 August 2019 characterization and comparison Published: xx xx xxxx between diseased and healthy cats Marjory Xavier Rodrigues1, Rodrigo Carvalho Bicalho1, Nadine Fiani2, Svetlana Ferreira Lima3 & Santiago Peralta 2 Periodontitis is a common and important health problem in domestic cats. The subgingival microbiota of cats diagnosed with chronic periodontitis (CP), aggressive periodontitis (AP), and feline chronic gingivostomatitis (FCGS) are not well characterized. Thus, the aim of the present study was to characterize and compare the periodontal microbiota of periodontally healthy cats versus cats diagnosed with CP, AP, and FCGS by using next-generation sequencing. In total, 44 domestic cats were enrolled, and 139 subgingival samples were subjected to 16S rRNA gene sequencing to investigate the microbiota composition of each periodontal group evaluated. Our results identifed several key genera previously described in periodontal disease (e.g. Treponema and Filifactor) and in the oral microbiota (e.g. Moraxella and Capnocytophaga) of healthy cats. Phylogenetic beta diversity analysis showed that the microbiota of periodontally healthy cats were distinguishable from diseased cats. Even though most of the genera known to be associated with periodontal disease were also identifed in healthy cats, they were present at signifcantly lower relative abundance. Remarkably, alpha diversity was found to be higher in the disease groups compared to healthy animals. These results suggest a pathological mechanism involving opportunistic behavior. Our fndings corroborate those in the current literature regarding the complexity of the subgingival microbiota of the domestic cat and reveal both diferences and similarities among periodontally healthy and diseased cats. Periodontitis is an infammatory disease that is highly prevalent in domestic cats1,2. It is characterized by loss of periodontal attachment, tooth mobility and eventual tooth loss2,3. It causes pain, gingival bleeding, reduced food intake, and may impact overall health4,5. Given its prevalence, as well as its local and systemic efects, periodonti- tis is a serious animal welfare issue that can impact quality of life. Te pathogenesis of periodontitis involves the presence of subgingival bacterial plaque that initially leads to gingivitis and marginal tissue infammation; if not treated it may progress to loss of periodontal attachment6. Periodontitis can be classifed as chronic or aggressive1,3,7,8. Chronic periodontitis (CP) is the most common form and is characterized by slow progression1; the prevalence of CP increases with age2. In contrast, aggressive periodontitis (AP) has a higher rate of progression and typically begins during early stages of life3,9. Although sub- gingival bacteria play a crucial role in the disease, determination of the causal pathogen(s) has been inconclusive despite advances in the microbiology of subgingival bioflms in health and in diferent forms of periodontal dis- ease9. In humans, it has been suggested that AP is associated with a mixed and complex microbial fora, with het- erogeneity in the types and proportions of microorganisms recovered from individuals with the disease9. On the other hand, the supposed association of AP with an increased load of specifc periodontal bacteria underscores the importance of bacteria to the disease process, and consequently the importance of microbiologic tests10. 1Department of Population Medicine and Diagnostic Sciences, Cornell University, Ithaca, NY, 14853, United States. 2Department of Clinical Sciences, Cornell University, Ithaca, NY, 14853, United States. 3Weill Cornell Medicine, Jill Roberts Institute for Research in Infammatory Bowel Disease, Cornell University, New York City, NY, 10021, United States. Correspondence and requests for materials should be addressed to S.P. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:12340 | https://doi.org/10.1038/s41598-019-48852-4 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Age (years) Body Weight (kg) Status Median Minimum Maximum Median Minimum Maximum Healthy 10.5 2 18 5.2 3.7 9.5 CP 8 3 17 5.5 3.0 7.7 AP 3 2 14 4.8 3.3 6.3 FCGS 4 3 11 3.7 3.2 5.6 Table 1. Median, minimum and maximum age (years) and body weight (kg) of healthy cats and cats afected with afected with chronic periodontitis (CP), aggressive periodontitis (AP), and feline chronic gingivostomatitis (FCGS). Another important disease is feline chronic gingivostomatitis (FCGS), which causes severe pain and distress and is characterized by focal or difuse chronic infammation of the gingiva and oral mucosa11. FCGS may afect cats of any age, and treatment usually involves lifelong medical therapy or extensive surgery. Many cats fail to respond to treatment, and some are euthanized due to a poor quality of life12,13. Even though the etiology of FCGS is unknown, bacteria are thought to play a role in the disease pathogenesis14–16. Additionally, cats with FCGS have been shown to develop more severe and extensive forms of periodontitis compared to cats without the disease17. However, it is unknown whether the latter is due to underlying diferences in the subgingival microbiome com- pared to cats without FGCS. Techniques based on DNA sequencing and advanced bioinformatics tools can help unravel the complexity of the subgingival microbiota in periodontal health and disease10,18. Recent studies have made use of bacterial 16S rDNA sequencing to describe the feline oral microbial composition6,14,19,20. Sturgeon20 and colleagues character- ized the oral microbiota of healthy cats using next-generation sequencing and found it to be highly diverse, rich, and even. Also, comparisons of the feline subgingival microbiota among healthy, gingivitis, and mild periodon- titis cases were recently described based on pyrosequencing6. Porphyromonas was the most abundant genus in healthy cats, along with Moraxella and Fusobacterium, whereas Peptostreptococcaceae was the most abundant fam- ily in gingivitis and mild periodontitis6. Dewhirst et al.19, using bacterial culture and DNA sequencing, showed that for periodontitis as well as for other oral diseases, members of the phyla Spirochaetes and Bacteroidetes are key pathogens19, e.g. Treponema denticola and Porphyromonas gingivalis21, respectively. Pasteurella multocida subsp. multocida was found to be signifcantly more prevalent in afected cats compared to controls when using culture-dependent and independent methods in one study14. In order to better understand the possible role of the subgingival microbiota in periodontal health and disease in cats, we have applied next-generation sequencing techniques to assess and compare the periodontal microbiota from healthy cats and cats with CP, AP, and FCGS. Results Initial descriptive data. Te intrinsic characteristics of enrolled animals were analyzed. Tere was no sta- tistically signifcant diference among disease groups (i.e., AP vs. CP vs. FCGS) regarding sex (male vs female) or breed distribution (domestic vs purebred) using a chi-square test. A Kruskal-Wallis test was used to analyze dif- ferences among groups regarding age and body weight. A statistically signifcant diference was identifed among disease groups regarding age (P-value = 0.005). Comparisons for all pairs using the Dunn method showed that cats with AP were signifcantly younger compared to cats with CP (P-value = 0.0103); signifcant diferences were not found between the other disease groups. No statistically signifcant diferences were found among diseases groups in terms of body weight. Median, minimum and maximum age and body weight are presented in Table 1. Sequencing results. DNA amplifcation using barcoded primers and next-generation sequencing of the V4 region of the 16 rRNA gene were completed for all samples collected. Te sequencing run was performed using a MiSeq sequencer and the reagent kit v2 (300-cycles) (Illumina, Inc., San Diego, CA). Quality fltered reads were de-multiplexed, and the total number of reads was 5,372,557; the average coverage was 38,651 reads per sample, with a standard deviation of 11,454; the number of reads per sample ranged from 8,476 to 82,373 (median = 36,217); and the median length per read was 301 bases. Bacterial distribution based on phylum level. Te relative distributions of bacteria at the phylum level identifed by 16S rDNA gene sequencing are depicted in Fig. 1. Te most prevalent bacterial phyla among all cats were Bacteroidetes, Proteobacteria, Firmicutes, Spirochetes, and Fusobacteria. Proteobacteria was the most abun- dant phylum in the healthy group (mean = 32.88%; median = 34.03%; minimum = 23.57%; maximum = 37.35%), whereas in the disease groups the relative abundance dropped in CP (mean = 21.27%; median = 19.08%; min- imum = 6.22%; maximum = 48.96%), AP (mean = 13.42%; median = 12.92%; minimum = 7.62%; maxi- mum = 19.90%), and FCGS (mean = 9.82%; median = 9.08%; minimum = 6.51%; maximum = 12.78%). Bacteroidetes was the most abundant phylum in the disease groups, having a higher relative abundance in the FCGS group (mean = 40.56%; median = 39.38%; minimum = 17.32%; maximum = 59.16%), followed by AP (mean = 35.62%; median = 30.92%; minimum = 21.56%; maximum = 71.37%) and CP (mean = 33.17%; median = 32.69%; minimum = 14.92%; maximum = 58.19%). In addition, Fusobacteria and Spirochaetes were also more abundant in the diseased individuals.
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