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A 2-plane micro-computed tomographic alveolar bone measurement approach in mice

  • Catunda, Raisa Queiroz (Department of Dentistry, Faculty of Medicine and Dentistry, School of Dentistry, University of Alberta) ;
  • Ho, Karen Ka-Yan (Department of Dentistry, Faculty of Medicine and Dentistry, School of Dentistry, University of Alberta) ;
  • Patel, Srushti (Department of Dentistry, Faculty of Medicine and Dentistry, School of Dentistry, University of Alberta) ;
  • Febbraio, Maria (Department of Dentistry, Faculty of Medicine and Dentistry, School of Dentistry, University of Alberta)
  • Received : 2021.03.11
  • Accepted : 2021.06.11
  • Published : 2021.12.31

Abstract

Purpose: This study introduces a standardized 2-plane approach using 8 landmarks to assess alveolar bone levels in mice using micro-computed tomography. Materials and Methods: Bone level differences were described as distance from the cemento-enamel junction (CEJ) to alveolar bone crest (ABC) and as percentages of vertical bone height and vertical bone loss, comparing mice infected with Porphyromonas gingivalis (Pg) to controls. Eight measurements were obtained per tooth: 2 in the sagittal plane (mesial and distal) and 6 in the coronal plane (mesiobuccal, middle-buccal, distobuccal, mesiolingual, middle-lingual, and distolingual). Results: Significant differences in the CEJ-to-ABC distance between Pg-infected mice and controls were found in the coronal plane (middle-lingual, mesiobuccal, and distolingual for the first molar; and mesiobuccal, middle-buccal, and distolingual for the second molar). In the sagittal plane, the distal measurement of the second molar was different. The middle-buccal, mesiobuccal, and distolingual sites of the first and second molars showed vertical bone loss relative to controls; the second molar middle-lingual site was also different. In the sagittal plane, the mesial sites of the first and second molars and the distal site of the second molar showed loss. Significantly different vertical bone height percentages were found for the mesial and distal sites of the second molar (sagittal plane) and the middle-lingual and distolingual sites of the first molar(coronal plane). Conclusion: A reliable, standardized technique for linear periodontal assessments in mice is described. Alveolar bone loss occurred mostly on the lingual surface of the coronal plane, which is often omitted in studies.

Keywords

Acknowledgement

The authors gratefully acknowledge Dr. Manuel Lagravere-Vich for his support with Avizo software and for his advice in developing landmarks for this protocol. We also acknowledge Dr. Maria Alexiou and Pranidhi Baddam for support in scanning and reconstructing the animal heads.

References

  1. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et al. Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 2018; 89 Suppl 1: S173-82. https://doi.org/10.1002/JPER.17-0721
  2. Moore WE, Moore LV. The bacteria of periodontal diseases. Periodontol 2000 1994; 5: 66-77. https://doi.org/10.1111/j.1600-0757.1994.tb00019.x
  3. Ebbers M, Lubcke PM, Volzke J, Kriebel K, Hieke C, Engelmann R, et al. Interplay between P. gingivalis, F. nucleatum and A. actinomycetemcomitans in murine alveolar bone loss, arthritis onset and progression. Sci Rep 2018; 8: 15129. https://doi.org/10.1038/s41598-018-33129-z
  4. Hiyari S, Atti E, Camargo PM, Eskin E, Lusis AJ, Tetradis S, et al. Heritability of periodontal bone loss in mice. J Periodontal Res 2015; 50: 730-6. https://doi.org/10.1111/jre.12258
  5. Saadi-Thiers K, Huck O, Simonis P, Tilly P, Fabre JE, Tenenbaum H, et al. Periodontal and systemic responses in various mice models of experimental periodontitis: respective roles of inflammation duration and Porphyromonas gingivalis infection. J Periodontol 2013; 84: 396-406. https://doi.org/10.1902/jop.2012.110540
  6. Myneni SR, Settem RP, Connell TD, Keegan AD, Gaffen SL, Sharma A. TLR2 signaling and Th2 responses drive Tannerella forsythia-induced periodontal bone loss. J Immunol 2011; 187: 501-9. https://doi.org/10.4049/jimmunol.1100683
  7. Wilensky A, Gabet Y, Yumoto H, Houri-Haddad Y, Shapira L. Three-dimensional quantification of alveolar bone loss in Porphyromonas gingivalis-infected mice using micro-computed tomography. J Periodontol 2005; 76: 1282-6. https://doi.org/10.1902/jop.2005.76.8.1282
  8. Lalla E, Lamster IB, Feit M, Huang L, Schmidt AM. A murine model of accelerated periodontal disease in diabetes. J Periodontal Res 1998; 33: 387-99. https://doi.org/10.1111/j.1600-0765.1998.tb02335.x
  9. Oz HS, Puleo DA. Animal models for periodontal disease. J Biomed Biotechnol 2011; 2011: 754857. https://doi.org/10.1155/2011/754857
  10. Madden TE, Caton JG. Animal models for periodontal disease. Methods Enzymol 1994; 235: 106-19. https://doi.org/10.1016/0076-6879(94)35135-X
  11. Wiebe CB, Adkins CA, Putnins EE, Hakkinen L, Larjava HS. Naturally occurring periodontal bone loss in the wild deer mouse, genus Peromyscus. J Periodontol 2001; 72: 620-5. https://doi.org/10.1902/jop.2001.72.5.620
  12. Monasterio G, Castillo F, Ibarra JP, Guevara J, Rojas L, Alvarez C, et al. Alveolar bone resorption and Th1/Th17-associated immune response triggered during Aggregatibacter actinomycetemcomitans-induced experimental periodontitis are serotype-dependent. J Periodontol 2018; 89: 1249-61. https://doi.org/10.1002/jper.17-0563
  13. Fujita Y, Maki K. High-fat diet-induced obesity triggers alveolar bone loss and spontaneous periodontal disease in growing mice. BMC Obes 2016; 3: 1. https://doi.org/10.1186/s40608-016-0082-8
  14. Hajishengallis G, Lamont RJ, Graves DT. The enduring importance of animal models in understanding periodontal disease. Virulence 2015; 6: 229-35. https://doi.org/10.4161/21505594.2014.990806
  15. Li D, Feng Y, Tang H, Huang L, Tong Z, Hu C, et al. A simplified and effective method for generation of experimental murine periodontitis model. Front Bioeng Biotechnol 2020; 8: 444. https://doi.org/10.3389/fbioe.2020.00444
  16. Lalla E, Lamster IB, Hofmann MA, Bucciarelli L, Jerud AP, Tucker S, et al. Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice. Arterioscler Thromb Vasc Biol 2003; 23: 1405-11. https://doi.org/10.1161/01.ATV.0000082462.26258.FE
  17. Rowsell HC. The Canadian Council on Animal Care - its guidelines and policy directives: the veterinarian's responsibility. Can J Vet Res 1991; 55: 205.
  18. Park CH, Abramson ZR, Taba M Jr, Jin Q, Chang J, Kreider JM, et al. Three-dimensional micro-computed tomographic imaging of alveolar bone in experimental bone loss or repair. J Periodontol 2007; 78: 273-81. https://doi.org/10.1902/jop.2007.060252
  19. Glowacki AJ, Yoshizawa S, Jhunjhunwala S, Vieira AE, Garlet GP, Sfeir C, et al. Prevention of inflammation-mediated bone loss in murine and canine periodontal disease via recruitment of regulatory lymphocytes. Proc Natl Acad Sci U S A 2013; 110: 18525-30. https://doi.org/10.1073/pnas.1302829110
  20. Gehlot P, Volk SL, Rios HF, Jepsen KJ, Holoshitz J. Spontaneous destructive periodontitis and skeletal bone damage in transgenic mice carrying a human shared epitope-coding HLA-DRB1 allele. RMD Open 2016; 2: e000349. https://doi.org/10.1136/rmdopen-2016-000349
  21. Marchesan J, Girnary MS, Jing L, Miao MZ, Zhang S, Sun L, et al. An experimental murine model to study periodontitis. Nat Protoc 2018; 13: 2247-67. https://doi.org/10.1038/s41596-018-0035-4
  22. Struillou X, Boutigny H, Soueidan A, Layrolle P. Experimental animal models in periodontology: a review. Open Dent J 2010; 4: 37-47. https://doi.org/10.2174/1874210601004010037
  23. Settem RP, Honma K, Sharma A. Neutrophil mobilization by surface-glycan altered Th17-skewing bacteria mitigates periodontal pathogen persistence and associated alveolar bone loss. PLoS One 2014; 9: e108030. https://doi.org/10.1371/journal.pone.0108030
  24. Yuan H, Zelkha S, Burkatovskaya M, Gupte R, Leeman SE, Amar S. Pivotal role of NOD2 in inflammatory processes affecting atherosclerosis and periodontal bone loss. Proc Natl Acad Sci U S A 2013; 110: E5059-68.
  25. Lubcke PM, Ebbers MNB, Volzke J, Bull J, Kneitz S, Engelmann R, et al. Periodontal treatment prevents arthritis in mice and methotrexate ameliorates periodontal bone loss. Sci Rep 2019; 9: 8128. https://doi.org/10.1038/s41598-019-44512-9
  26. Zhang L, Meng S, Tu Q, Yu L, Tang Y, Dard MM, et al. Adiponectin ameliorates experimental periodontitis in diet-induced obesity mice. PLoS One 2014; 9: e97824. https://doi.org/10.1371/journal.pone.0097824
  27. Srinivasan M, Kodumudi KN, Galli DM. Aggregatibacter actinomycetemcomitans modulates toll-like receptors 2 and 4 in gingival epithelial cells in experimental periodontitis. J Int Clin Dent Res Organ 2010; 2: 24-9. https://doi.org/10.4103/2231-0754.89992
  28. Gully N, Bright R, Marino V, Marchant C, Cantley M, Haynes D, et al. Porphyromonas gingivalis peptidylarginine deiminase, a key contributor in the pathogenesis of experimental periodontal disease and experimental arthritis. PLoS One 2014; 9: e100838. https://doi.org/10.1371/journal.pone.0100838
  29. Fine DH, Patil AG, Loos BG. Classification and diagnosis of aggressive periodontitis. J Clin Periodontol 2018; 45 Suppl 20: S95-111. https://doi.org/10.1111/jcpe.12942
  30. Theil EM, Heaney TG. The validity of periodontal probing as a method of measuring loss of attachment. J Clin Periodontol 1991; 18: 648-53. https://doi.org/10.1111/j.1600-051X.1991.tb00105.x
  31. Al Shayeb KN, Turner W, Gillam DG. Periodontal probing: a review. Prim Dent J 2014; 3: 25-9. https://doi.org/10.1308/205016814812736619
  32. Ansai T, Awano S, Soh I. Problems and future approaches for assessment of periodontal disease. Front Public Health 2014; 2: 54. https://doi.org/10.3389/fpubh.2014.00054
  33. Hong HH, Mei CC, Liu HL, Liang CH, Lin CK, Lee FY, et al. The correspondence of 3D supporting bone loss and crownto-root ratio to periodontitis classification. J Clin Periodontol 2020; 47: 825-33. https://doi.org/10.1111/jcpe.13296
  34. Papathanasiou E, Kantarci A, Konstantinidis A, Gao H, Van Dyke TE. SOCS-3 regulates alveolar bone loss in experimental periodontitis. J Dent Res 2016; 95: 1018-25. https://doi.org/10.1177/0022034516645332