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Pulpal outcomes in orthodontic tooth movement in diabetes mellitus

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Abstract

Diabetes mellitus impairs angiogenesis and tissue reorganization during orthodontic tooth movement (OTM). Thus, this study evaluated pulpal outcomes in orthodontic tooth movement through metabolic changes in diabetes. Male Wistar rats were used, and the in vivo study design consisted of four groups (n = 10/group): C—non-diabetic animals not subjected to orthodontic tooth movement; D—diabetic animals not subjected to orthodontic tooth movement; OTM—non-diabetic animals subjected to orthodontic tooth movement; and D + OTM—diabetic animals subjected to orthodontic tooth movement. In addition, the pulps of the distovestibular root (DV) and mesiovestibular root (MV) were assessed by histomorphometric analyses and immunoexpression of the RANKL/OPG system. Pulpal analysis of the MV root showed an increase in blood vessels in diabetic animals. Inflammatory infiltrate and fibroblastic cells were elevated in diabetic animals with tooth movement in the DV and MV roots. In the DV and MV roots, diabetic rats with OTM showed a reduction in birefringent collagen fibers. The immunostaining for RANKL was higher in the pulp tissue of OTM in diabetic and non-diabetic animals. It was concluded that the pulp tissue has less adaptive and repair capacity during OTM in diabetes. Orthodontic strength can alter the inflammatory processes in the pulp.

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References

  1. Hassan AH, Al-Fraidi AA, Al-Saeed SH. Corticotomy–assisted orthodontic treatment: review. Open Dent J. 2010;4:159–64. https://doi.org/10.2174/1874210601004010159.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bensch L, Braem M, Van Acker K, Willems G. Orthodontic treatment considerations in patients with diabetes mellitus. Am J Orthod Dentofacial Orthop. 2003;123(1):74–8. https://doi.org/10.1067/mod.2003.53.

    Article  PubMed  Google Scholar 

  3. Ferreira CL, da Rocha VC, da Silva Ursi WJ, De Marco AC, Santamaria M, Santamaria MP, et al. Periodontal response to orthodontic tooth movement in diabetes-induced rats with or without periodontal disease. J Periodontol. 2018;89(3):341–50. https://doi.org/10.1002/JPER.17-0190.

    Article  PubMed  Google Scholar 

  4. Camargo WA, de Vries R, van Luijk J, Hoekstra JW, Bronkhorst EM, Jansen JA, et al. Diabetes mellitus and bone regeneration: a systematic review and meta-analysis of animal studies. Tissue Eng Part B Rev. 2017;23(5):471–9. https://doi.org/10.1089/ten.TEB.2016.0370.

    Article  PubMed  Google Scholar 

  5. Fatehi F, Nafissi S, Basiri K, Amiri M, Soltanzadeh A. Chronic inflammatory demyelinating polyneuropathy associated with diabetes mellitus. J Res Med Sci. 2013;18(5):438–41 (PMID: 24174953).

    PubMed  PubMed Central  Google Scholar 

  6. Gilbert RE. Endothelial loss and repair in the vascular complications of diabetes: pathogenetic mechanisms and therapeutic implications. Circ J. 2013;77(4):849–56 (PMID: 23503045).

    Article  Google Scholar 

  7. Li Y, Jacox LA, Little SH, Ko CC. Orthodontic tooth movement: the biology and clinical implications. Kaohsiung J Med Sci. 2018;34(4):207–14. https://doi.org/10.1016/j.kjms.2018.01.007.

    Article  PubMed  Google Scholar 

  8. Kohli SS, Kohli VS. Role of RANKL–RANK/osteoprotegerin molecular complex in bone remodeling and its immunopathologic implications. Indian J Endocrinol Metab. 2011;15(3):175–81. https://doi.org/10.4103/2230-8210.83401.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Calsa B, Masiero BC, Esquisatto MAM, Catisti R, Santamaria M Jr. Gestational protein restriction alters the RANKL/OPG system in the dental germ of offsprings. J Oral Biol Craniofac Res. 2020;10(4):743–6. https://doi.org/10.1016/j.jobcr.2020.10.007.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Popescu MR, Surlin P, Rauten AM, Dragomir L, Olteanu M. Histological analysis of collagen fibers in patients with diabetes mellitus and periodontal disease. J Cytol Histol. 2014;S4:008. https://doi.org/10.4172/2157-7099.S4-008.

    Article  Google Scholar 

  11. Park HJ, Baek KH, Lee HL, Kwon A, Hwang HR, Qadir AS, et al. Hypoxia inducible factor-1α directly induces the expression of receptor activator of nuclear factor-κB ligand in periodontal ligament fibroblasts. Mol Cells. 2011;31(6):573–8. https://doi.org/10.1007/s10059-011-1055-x.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Neves LMG, Matheus RL, Santos GMT, Esquisatto MAM, Amaral MEC, Mendonça FAS. Effects of microcurrent application and 670 nm InGaP low-level laser irradiation on experimental wound healing in healthy and diabetic Wistar rats. Laser Phys. 2013. https://doi.org/10.1088/1054-660X/23/3/035604.

    Article  Google Scholar 

  13. Villarino ME, Lewicki M, Ubios AM. Bone response to orthodontic forces in diabetic Wistar rats. Am J Orthod Dentofacial Orthop. 2011;139(4 Suppl):S76-82. https://doi.org/10.1016/j.ajodo.2010.06.021.

    Article  PubMed  Google Scholar 

  14. Najeeb S, Siddiqui F, Qasim SB, Khurshid Z, Zohaib S, Zafar MS. Influence of uncontrolled diabetes mellitus on periodontal tissues during orthodontic tooth movement: a systematic review of animal studies. Prog Orthod. 2017;18(1):5. https://doi.org/10.1186/s40510-017-0159-z.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Javed F, Al-Keraif AA, Romanos EB, Romanos GE. Influence of orthodontic forces on human dental pulp: a systematic review. Arch Oral Biol. 2015;60(2):347–56. https://doi.org/10.1016/j.archoralbio.2014.11.011.

    Article  PubMed  Google Scholar 

  16. Von Böhl M, Ren Y, Kuijpers-Jagtman AM, Fudalej PS, Maltha JC. Age-related changes of dental pulp tissue after experimental tooth movement in rats. PeerJ. 2016;4:e1625. https://doi.org/10.7717/peerj.1625.

    Article  Google Scholar 

  17. Santamaria-Jr M Jr, Bagne L, Zaniboni E, Santamaria MP, Jardini MAN, Felonato M, et al. Diabetes mellitus and periodontitis: inflammatory response in orthodontic tooth movement. Orthod Craniofac Res. 2020;23:27–34. https://doi.org/10.1111/ocr.12340.

    Article  PubMed  Google Scholar 

  18. Zaniboni E, Vedovello Filho M, Santamaria MP, Jardini MAN, Martins-Ortiz MF, Consolaro A, et al. Root morphology can be a risk factor for periodontal damage and root resorption in orthodontic movement. Braz J Oral Sci. 2017;16:1–8. https://doi.org/10.20396/bjos.v16i0.8651188.

    Article  Google Scholar 

  19. Tannenbaum J, Bennett BT. Russell and Burch’s 3Rs then and now: the need for clarity in definition and purpose. J Am Assoc Lab Anim Sci. 2015;54:120–32 (PMID: 25836957).

    PubMed  PubMed Central  Google Scholar 

  20. Santamaria M Jr, Milagres D, Stuani AS, Stuani MBS, Ruellas ACO. Initial changes in pulpal microvasculature during orthodontic tooth movement: a stereological study. Eur J Orthod. 2006;28:217–20. https://doi.org/10.1093/ejo/cji117.

    Article  PubMed  Google Scholar 

  21. Spadari GS, Zaniboni E, Vedovello SA, Santamaria MP, do Amaral ME, Dos Santos GM, et al. Electrical stimulation enhances tissue reorganization during orthodontic tooth movement in rats. Clin Oral Investig. 2017;21:111–20. https://doi.org/10.1007/s00784-016-1759-6.

    Article  PubMed  Google Scholar 

  22. Franzoni JS, Soares FMP, Zaniboni E, Filho MV, Santamaria MP, Dos Santos GMT, et al. Zoledronic acid and alendronate sodium and the implications in orthodontic movement. Orthod Craniofac Res. 2017;20:164–9. https://doi.org/10.1111/ocr.12192.

    Article  PubMed  Google Scholar 

  23. Gonzalez-Suarez E, Jacob AP, Jones J, Miller R, Roudier-Meyer MP, Erwert R, et al. RANK ligand mediates progestin-induced mammary epithelial proliferation and carcinogenesis. Nature. 2010;468(7320):103–7. https://doi.org/10.1038/nature09495.

    Article  PubMed  Google Scholar 

  24. Zaniboni E, Bagne L, Camargo T, do Amaral MEC, Felonato M, de Andrade TAM, et al. Do electrical current and laser therapies improve bone remodeling during an orthodontic treatment with corticotomy? Clin Oral Investig. 2019;23(11):4083–97. https://doi.org/10.1007/s00784-019-02845-9.

    Article  PubMed  Google Scholar 

  25. Toms A, Gannon B, Carati C. The immunohistochemical response of the rat periodontal ligament endothelium to an inflammatory stimulus. Aust Orthod J. 2000;16(2):61–8 (PMID: 11201966).

    PubMed  Google Scholar 

  26. Murphy A, Biringanine M, Roberts B, Stringer B, Perel P, Jobanputra K. Diabetes care in a complex humanitarian emergency setting: a qualitative evaluation. BMC Health Serv Res. 2017;17(1):431. https://doi.org/10.1186/s12913-017-2362-5.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27(5):1047–53. https://doi.org/10.2337/diacare.27.5.1047.

    Article  PubMed  Google Scholar 

  28. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014;103(2):137–49. https://doi.org/10.1016/j.diabres.2013.11.002.

    Article  PubMed  Google Scholar 

  29. Hellsing E, Hammarström L. The hyaline zone and associated root surface changes in experimental orthodontics in rats: a light and scanning electron microscope study. Eur J Orthod. 1996;18(1):11–8. https://doi.org/10.1093/ejo/18.1.11.

    Article  PubMed  Google Scholar 

  30. Cuoghi OA, Aiello CA, Consolaro A, Tondelli PM, Mendonça MR. Resorption of roots of different dimension induced by different types of forces. Braz Oral Res. 2014;28(1):1–7. https://doi.org/10.1590/1807-3107BOR-2014.vol28.0013.

    Article  Google Scholar 

  31. Maltha JC, van Leeuwen EJ, Dijkman GE, Kuijpers-Jagtman AM. Incidence and severity of root resorption in orthodontically moved premolars in dogs. Orthod Craniofac Res. 2004;7(2):115–21. https://doi.org/10.1111/j.1601-6343.2004.00283.x.

    Article  PubMed  Google Scholar 

  32. Weltman B, Vig KWL, Fields HW, Shanker S, Kaizar EE. Root resorption associated with orthodontic tooth movement: a systematic review. Am J Orthod Dentofacial Orthop. 2010;137(4):462–76. https://doi.org/10.1016/j.ajodo.2009.06.021 (discussion 12A).

    Article  PubMed  Google Scholar 

  33. Santamaria M Jr, Milagres D, Iyomasa MM, Stuani MBS, Ruellas ACO. Initial pulp changes during orthodontic movement: histomorphological evaluation. Braz Dent J. 2007;18(1):34–9 (PMID: 17639198).

    Article  Google Scholar 

  34. Massaro CS, Consolaro RB, Santamaria M Jr, Consolaro MF, Consolaro U. Analysis of the dentin-pulp complex in teeth submitted to orthodontic movement in rats. J Appl Oral Sci. 2009;17(Suppl):35–42. https://doi.org/10.1590/S1678-77572009000700007.

    Article  PubMed Central  Google Scholar 

  35. Amatyakul S, Chakraphan D, Chotpaibulpan S, Patumraj S. The effect of long-term supplementation of vitamin C on pulpal blood flow in streptozotocin-induced diabetic rats. Clin Hemorheol Microcirc. 2003;29(3–4):313–9 (PMID: 14724356).

    PubMed  Google Scholar 

  36. Garber SE, Shabahang S, Escher AP, Torabinejad M. The effect of hyperglycemia on pulpal healing in rats. J Endod. 2009;35(1):60–2. https://doi.org/10.1016/j.joen.2008.09.010.

    Article  PubMed  Google Scholar 

  37. Moraru AI, GheorghiŢa LM, Dascălu IT, Bătăiosu M, Manolea HO, Agop Forna D, et al. Histological and immunohistochemical study on the dental pulp of patients with diabetes mellitus. Rom J Morphol Embryol. 2017;58(2):493–9 (PMID: 28730235).

    PubMed  Google Scholar 

  38. Tyrovola JB. The “mechanostat theory” of frost and the OPG/RANKL/RANK system. J Cell Biochem. 2015;116(12):2724–9. https://doi.org/10.1002/jcb.25265.

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Council for Scientific and Technological Development–CAPES/PNPD (Process no 23038.008192/2013‐01) and the Hermínio Ometto Foundation.

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Correspondence to Milton Santamaria-Jr.

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Santamaria-Jr, M., do Nascimento, E.R.A., Bagne, L. et al. Pulpal outcomes in orthodontic tooth movement in diabetes mellitus. Odontology 109, 921–929 (2021). https://doi.org/10.1007/s10266-021-00609-0

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