1887

Journal of Medical Microbiology logo

Volume 70, Issue 4

Microbiome analysis of feline odontoclastic resorptive lesion (FORL) and feline oral health Open Access

Abstract

Feline odontoclastic resorptive lesion (FORL) is one of the most common and painful oral diseases of the cat. It is characterised by tooth resorption due to destructive activity of odontoclasts. FORL can result in tooth loss. While the aetiology of FORL is not clearly understood, it is thought to be multifactorial and bacteria are likely to play a major role.

Dysbiosis of the normal feline oral microbiota leads to an alteration in commensal bacteria populations, which results in the development of FORL.

The purpose of the current study was to determine the composition of the microbiomes associated with feline oral health and FORL.

Supragingival plaque was collected from 25 cats with a healthy oral cavity and 40 cats with FORL. DNA was extracted from each sample, the V4 region of the 16S rRNA gene amplified by polymerase chain reaction and amplicons sequenced. Diversity and species richness analyses were performed, principal component analysis was used to explore differences between the oral microbiomes of healthy cats and those with FORL, and linear discriminant analysis effect size was used to assess differences between the groups.

The six most abundant bacterial genera identified were , , , and . Two-step cluster analysis of the data identified two FORL sub-groups (FORL-1, FORL-2). The FORL-2 sub-group was very similar to the healthy group, whilst the FORL-1 sub-group was clearly different from both the FORL-2 sub-group and the healthy groups. In this analysis, ( <0.001) and ( <0.01) were found at significantly lower levels and at a slightly higher level in the FORL-1 sub-group compared to the healthy and FORL-2 sub-groups. Microbial diversity was found to be less in the FORL-1 sub-group than in the healthy group. sp., a phosphate-accumulating oral commensal species, was significantly lower in the FORL-1 sub-group.

The oral microbiota associated with the FORL-1 sub-group is distinct from that found in the healthy group and FORL-2 sub-group. species may influence the local calcium-phosphate ratio, which could be a factor in tooth and bone resorption observed in FORL.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacteria , feline , high-throughput sequencing , microbiome and odontoclastic resorptive lesion
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001353
2021-04-15
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/4/jmm001353.html?itemId=/content/journal/jmm/10.1099/jmm.0.001353&mimeType=html&fmt=ahah

References

  1. Lyon KF. Subgingival odontoclastic resorptive lesions. classification, treatment, and results in 58 cats. Vet Clin N Am Small Anim Pract 1992; 22:1417–1432 [View Article][PubMed]
     [Google Scholar]
  2. Reiter AM, Mendoza KA. Feline odontoclastic resorptive lesions an unsolved enigma in veterinary dentistry. Vet Clin N Am Small Anim Pract 2002; 32:791–837 [View Article][PubMed]
     [Google Scholar]
  3. Mestrinho LA, Runhau J, Bragança M, Niza MM. Risk assessment of feline tooth resorption: a Portuguese clinical case control study. J Vet Dent 2013; 30:78–83 [View Article][PubMed]
     [Google Scholar]
  4. Girard N, Servet E, Biourge V, Hennet P. Feline tooth resorption in a colony of 109 cats. J Vet Dent 2008; 25:166–174 [View Article][PubMed]
     [Google Scholar]
  5. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature 2003; 423:337–342 [View Article][PubMed]
     [Google Scholar]
  6. Patel S, Kanagasingam S, Pitt Ford T. External cervical resorption: a review. J Endod 2009; 35:616–625 [View Article][PubMed]
     [Google Scholar]
  7. DuPont GA. Radiographic evaluation and treatment of feline dental resorptive lesions. Vet Clin North Am Small Anim Pract 2005; 35:943–962 [View Article][PubMed]
     [Google Scholar]
  8. Gorrel C. Tooth resorption in cats: pathophysiology and treatment options. J Feline Med Surg 2015; 17:37–43 [View Article][PubMed]
     [Google Scholar]
  9. Booij-Vrieling HE. Tooth resorption in cats: contribution of vitamin D and inflammation. PhD thesis Utrecht University, The Netherlands;
     [Google Scholar]
  10. Girard N, Servet E, Hennet P, Biourge V. Tooth resorption and vitamin D3 status in cats fed premium dry diets. J Vet Dent 2010; 27:142–147 [View Article][PubMed]
     [Google Scholar]
  11. Reiter AM, Lewis JR, Okuda A. Update on the etiology of tooth resorption in domestic cats. Vet Clin North Am Small Anim Pract 2005; 35:913–942 [View Article][PubMed]
     [Google Scholar]
  12. Zupan J, Jeras M, Marc J. Osteoimmunology and the influence of pro-inflammatory cytokines on osteoclasts. Biochem Med 2013; 23:43–63 [View Article][PubMed]
     [Google Scholar]
  13. DeLaurier A, Allen S, deFlandre C, Horton MA, Price JS. Cytokine expression in feline osteoclastic resorptive lesions. J Comp Pathol 2002; 127:169–177 [View Article][PubMed]
     [Google Scholar]
  14. Booij-Vrieling HE, Tryfonidou MA, Riemers FM, Penning LC, Hazewinkel HAW. Inflammatory cytokines and the nuclear vitamin D receptor are implicated in the pathophysiology of dental resorptive lesions in cats. Vet Immunol Immunopathol 2009; 132:160–166 [View Article][PubMed]
     [Google Scholar]
  15. Mallonee DH, Harvey CE, Venner M, Hammond BF. Bacteriology of periodontal disease in the cat. Arch Oral Biol 1988; 33:677–683 [View Article][PubMed]
     [Google Scholar]
  16. Davis IJ, Wallis C, Deusch O, Colyer A, Milella L et al. A cross-sectional survey of bacterial species in plaque from client owned dogs with healthy gingiva, gingivitis or mild periodontitis. PLoS One 2013; 8:e83158 [View Article][PubMed]
     [Google Scholar]
  17. Kennedy R, Lappin DF, Dixon PM, Buijs MJ, Zaura E et al. The microbiome associated with equine periodontitis and oral health. Vet Res 2016; 47:49 [View Article][PubMed]
     [Google Scholar]
  18. Dolieslager SMJ, Riggio MP, Lennon A, Lappin DF, Johnston N et al. Identification of bacteria associated with feline chronic gingivostomatitis using culture-dependent and culture-independent methods. Vet Microbiol 2011; 148:93–98 [View Article][PubMed]
     [Google Scholar]
  19. Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq illumina sequencing platform. Appl Environ Microbiol 2013; 79:5112–5120 [View Article][PubMed]
     [Google Scholar]
  20. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article][PubMed]
     [Google Scholar]
  21. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013; 10:996–998 [View Article][PubMed]
     [Google Scholar]
  22. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335–336 [View Article][PubMed]
     [Google Scholar]
  23. Cole JR, Wang Q, Cardenas E, Fish J, Chai B et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009; 37:D141–D145 [View Article][PubMed]
     [Google Scholar]
  24. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T et al. The Silva ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 2013; 41:D590–D596 [View Article][PubMed]
     [Google Scholar]
  25. Hammer Ø, Harper DAT, Ryan PD. PAST: PAleontological STatistics software package for education and data analysis. Palaeontol Electronica 2001; 4:9
     [Google Scholar]
  26. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011; 12:R60 [View Article][PubMed]
     [Google Scholar]
  27. Sturgeon A, Pinder SL, Costa MC, Weese JS. Characterization of the oral microbiota of healthy cats using next-generation sequencing. Vet J 2014; 201:223–229 [View Article][PubMed]
     [Google Scholar]
  28. Adler CJ, Malik R, Browne GV, Norris JM. Diet may influence the oral microbiome composition in cats. Microbiome 2016; 4:23 [View Article][PubMed]
     [Google Scholar]
  29. Harris S, Croft J, O'Flynn C, Deusch O, Colyer A et al. A pyrosequencing investigation of differences in the feline subgingival microbiota in health, gingivitis and mild periodontitis. PLoS One 2015; 10:e0136986 [View Article][PubMed]
     [Google Scholar]
  30. Dewhirst FE, Klein EA, Bennett ML, Croft JM, Harris SJ et al. The feline oral microbiome: a provisional 16S rRNA gene based taxonomy with full-length reference sequences. Vet Microbiol 2015; 175:294–303 [View Article][PubMed]
     [Google Scholar]
  31. Stante L, Cellamare CM, Malaspina F, Bortone G, Tilche A. Biological phosphorus removal by pure culture of Lampropedia spp. Water Res 1997; 31:1317–1324 [View Article]
     [Google Scholar]
  32. Tripathi C, Mahato NK, Singh AK, Kamra K, Korpole S et al. Lampropedia cohaerens sp. nov., a biofilm-forming bacterium isolated from microbial mats of a hot water spring, and emended description of the genus Lampropedia . Int J Syst Evol Microbiol 2016; 66:1156–1162 [View Article][PubMed]
     [Google Scholar]
  33. Dorn ES, Tress DB, Suchodolski JS, Nisar T, Ravindran P et al. Bacterial microbiome in the nose of healthy cats and in cats with nasal disease. PLoS One 2017; 12:e0180299 [View Article][PubMed]
     [Google Scholar]
  34. Reiter AM, Lyon KF, Nachreiner RF, Shofer FS. Evaluation of calciotropic hormones in cats with odontoclastic resorptive lesions. Am J Vet Res 2005; 66:1446–1452 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001353
Loading
Microbiome analysis of feline odontoclastic resorptive lesion (FORL) and feline oral health
J. Med. Microbiol. 70, 001353 (2021); https://doi.org/10.1099/jmm.0.001353
/content/journal/jmm/10.1099/jmm.0.001353
/content/journal/jmm/10.1099/jmm.0.001353
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error