Clinical Oral Investigations

, Volume 21, Issue 1, pp 111–120 | Cite as

Electrical stimulation enhances tissue reorganization during orthodontic tooth movement in rats

  • Gisele Sampaio Spadari
  • Ewerton Zaniboni
  • Silvia Amelia Scudeler Vedovello
  • Mauro Pedrine Santamaria
  • Maria Esméria Corezola do Amaral
  • Gláucia Maria Tech dos Santos
  • Marcelo Augusto Marretto Esquisatto
  • Fernanda Aparecida Sampaio Mendonca
  • Milton Santamaria-Jr
Original Article

Abstract

Objective

This study evaluated the effects of a low-intensity electric current on tissue reorganization during experimental orthodontic tooth movement.

Materials and methods

Thirty-two animals were divided into two groups evaluated on days 3 and 7: OTM—orthodontic tooth movement and OTM + MC—orthodontic tooth movement and microcurrent application (10 μA/5 min). The samples were processed for histological, morphometric, and Western blotting analysis.

Results

Analysis of the periodontal ligament (PL) showed a significantly smaller number of granulocytes in the OTM + MC group on day 7.The number of fibroblasts was significantly higher in the OTM + MC group on days 3 and 7. The area of birefringent collagen fibers was more organized in the OTM + MC group on days 3 and 7. The number of blood vessels was significantly higher in the OTM + MC group on day 7. Microcurrent application significantly increased the number of osteoclasts in the compression region of the PL. In the OTM + MC group on day 7 of tooth movement, the expression of TGF-β1 and VEGF was significantly reduced whereas the expression of bFGF was increased in PL.

Conclusions

Electrical stimulation enhances tissue responses, reducing the number of granulocytes and increasing the number of fibroblasts, blood vessels, and osteoclasts and modulates the expression of TGF-β1, VEFG, and bFGF.

Clinical relevance

This technique is used in many areas of medicine, but poorly explored in dentistry and orthodontics. This treatment is cheap and non-invasive and can be applied by own orthodontist, and it can improve the treatment with a faster and safe tooth movement, without pain.

Keywords

Microcurrent application Low-intensity electric current Orthodontic tooth movement 

Notes

Compliance with ethical standards

Funding

This study was funded by the National Council for Scientific and Technological Development - CAPES/PNPD (process no. 23038.008192/2013-01) and Heminio Ometto University Center.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in the present research were in accordance with the ethical standards of the Research Ethics Committee of Herminio Ometto University Center (permit no. 095/2011) and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

The studied experimental model involves animals (rats), thus informed consent is not necessary.

References

  1. 1.
    Van Schepdael A, Vander Sloten J, Geris L (2013) A mechanobiological model of orthodontic tooth movement. Biomech Model Mechanobiol 12:249–265CrossRefPubMedGoogle Scholar
  2. 2.
    Krishnan V, Davidovitch Z (2006) Cellular, molecular, and tissue-level reactions to orthodontic force. Am J Orthod Dentofacial Orthop 129(469):e1–32Google Scholar
  3. 3.
    Ren Y, Vissink A (2008) Cytokines in crevicular fluid and orthodontic tooth movement. Eur J Oral Sci 116:89–97CrossRefPubMedGoogle Scholar
  4. 4.
    Krishnan V, Davidovitch Z (2009) On a path to unfolding the biological mechanisms of orthodontic tooth movement. J Dent Res 88:597–608CrossRefPubMedGoogle Scholar
  5. 5.
    Teixeira CC, Khoo E, Tran J, Chartres I, Liu Y, Thant LM, Khabensky I, Gart LP, Cisneros G, Alikhani M (2010) Cytokine expression and accelerated tooth movement. J Dent Res 89:1135–1141CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bismar H, Klöppinger T, Schuster EM, Balbach S, Diel I, Ziegler R, Pfeilschifter J (1999) Transforming growth factor beta (TGF-beta) levels in the conditioned media of human bone cells: relationship to donor age, bone volume, and concentration of TGF-beta in human bone matrix in vivo. Bone 24:565–569CrossRefPubMedGoogle Scholar
  7. 7.
    Garlet TP, Coelho U, Silva JS, Garlet GP (2007) Cytokine expression pattern in compression and tension sides of the periodontal ligament during orthodontic tooth movement in humans. Eur J Oral Sci 115:355–362CrossRefPubMedGoogle Scholar
  8. 8.
    Di Domenico M, D’apuzzo F, Feola A, Cito L, Monsurrò A, Pierantoni GM, Berrino L, De Rosa A, Polimeni A, Perillo L (2012) Cytokines and VEGF induction in orthodontic movement in animal models J Biomed Biotechnol 201689.Google Scholar
  9. 9.
    Salomão MFLS, Reis SRA, Vale VLC, Machado CV, Meyer R, Nascimento ILO (2014) Immunolocalization of FGF-2 and VEGF in rat periodontal ligament during experimental tooth movement. Dental Press J Orthod 19:67–74CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Derringer KA, Linden RW (2004) Vascular endothelial growth factor, fibroblast growth factor 2, platelet derived growth factor and transforming growth factor beta released in human dental pulp following orthodontic force. Arch Biol Oral 49:631–641CrossRefGoogle Scholar
  11. 11.
    Sako E, Hosomichi J (2010) Alteration of bFGF expression with growth and age in rat molar periodontal ligament. Angle Orthod 80:904–911CrossRefPubMedGoogle Scholar
  12. 12.
    Feito MJ, Lozano RM, Alcaide M, Ramírez-Santillán C, Arcos D, Vallet-Regí M, Portolés MT (2011) Immobilization and bioactivity evaluation of FGF-1 and FGF-2 on powdered silicon-doped hydroxyapatite and their scaffolds for bone tissue engineering. J Mater Sci Mater Med 22:405–416CrossRefPubMedGoogle Scholar
  13. 13.
    Qu D, Li J, Li Y, Gao Y, Zuo Y, Hsu Y, Hu J (2011) Angiogenesis and osteogenesis enhanced by bFGF ex vivo gene therapy for bone tissue engineering in reconstruction of calvarial defects. J Biomed Mater Res 96:543–551CrossRefGoogle Scholar
  14. 14.
    Agren MS, Werthen M (2007) The extracellular matrix in wound healing: a closer look at therapeutics for chronic wounds. Int J Low Extrem Wounds 6:82–97CrossRefPubMedGoogle Scholar
  15. 15.
    Neves LMG, Matheus RL, Santos GMT, Esquisatto MAM, Amaral MEC, Mendonça FAS (2013) Effects of microcurrent application and 670 nm InGaP low-level laser irradiation on experimental wound healing in healthy and diabetic Wistar rats. Laser Phys 23:035604CrossRefGoogle Scholar
  16. 16.
    Campos Ciccone C, Zuzzi DC, Neves LMG, Mendonça JS, Paulo Pinto Joazeiro PP, Esquisatto MAM (2013) Effects of microcurrent stimulation on Hyaline cartilage repair in immature male rats (Rattus norvegicus) BMC Complement. Altern Med 13:17Google Scholar
  17. 17.
    Zuzzi DC, Ciccone CC, Neves LM, Mendonça JS, Joazeiro PP, Esquisatto MA (2013) Evaluation of the effects of electrical stimulation on cartilage repair in adult male rats. Tissue Cell 45:275–281CrossRefPubMedGoogle Scholar
  18. 18.
    Fujita M, Hukuda S, Doida Y (1992) The effect of constant direct electrical current on intrinsic healing in the flexor tendon in vitro. An ultrastructural study of differing attitudes in epitenon cells and tenocytes. J Hand Surg [Br] 17:94–98CrossRefGoogle Scholar
  19. 19.
    Lin YL, Moolenaar H, van Weeren PR, van de Lest CH (2006) Effect of microcurrent electrical tissue stimulation on equine tenocytes in culture. Am J Vet Res 67:271–276CrossRefPubMedGoogle Scholar
  20. 20.
    Martin RB, Gutman W (1978) The effect of electric fields on osteoporosis of disease. Calcif Tissue Int 5:23–27CrossRefGoogle Scholar
  21. 21.
    Mendonça JS, Neves LMG, Esquisatto MAM, Mendonça FAS, Santos GMT (2013) Comparative study of the application of microcurrent and AsGa 904 nm laser radiation in the process of repair after calvaria bone excision in rats. Laser Phys 23:035605CrossRefGoogle Scholar
  22. 22.
    Chao PH, Roy R, Mauck ML, Liu W, Valhmu WB, Hung CT (2000) Chondrocyte translocation response to direct current electric fields. J Biomech Eng 122:261–267CrossRefPubMedGoogle Scholar
  23. 23.
    McCaig CD, Rajnicek AM, Song B, Zhao M (2005) Controlling cell behavior electrically:current views and future potential. Physiol Rev 85:943–978CrossRefPubMedGoogle Scholar
  24. 24.
    Funk RH, Monsees TK (2006) Effects of electromagnetic fields on cells: physiological andtherapeutical approaches and molecular mechanisms of interaction. A review. Cells Tissues Organs 182:59–78CrossRefPubMedGoogle Scholar
  25. 25.
    Poltawski L, Tim Watson T (2009) Bioelectricity and microcurrent therapy for tissue healing—a narrative review. Phys Ther Rev 14:104–114CrossRefGoogle Scholar
  26. 26.
    Mendonça FAS, Passarini Junior JR, Esquisatto MA, Mendonça JS, Franchini CC, Santos GM (2009) Effects of the application of Aloe vera (L.) and microcurrent on the healing of wounds surgically induced in Wistar rats. Acta Cir Bras 24:150–155CrossRefPubMedGoogle Scholar
  27. 27.
    De Gaspi FOG, Foglio MA, Carvalho JE, Santos GMT, Testa M, Passarini JR Jr, Moraes CP, Esquisatto MAM, Mendonça JS, Mendonça FAS (2011) Effects of the topical application of hydroalcoholicleaf extract of Oncidium flexuosum Sims. (Orchidaceae) and microcurrent on the healing of wounds surgically induced in Wistar rats. Evid Based Complement Alternat Med:1–9Google Scholar
  28. 28.
    Migliato KF, Chiosini MA, Mendonça FAS, Esquisatto MAM, Salgado HR, Santos GMT (2011) Effect of glycolic extract of Dillenia indica L combined with microcurrent stimulation on experimental lesions in Wistar rats. Wounds 23:111–120PubMedGoogle Scholar
  29. 29.
    Castro FCB, Magre A, Cherpinski R, Zelante PM, Neves LMG, Esquisatto MAM, Mendonça FAZ, Santos GMT (2012) Effects of microcurrent application alone or in combination with topical Hypericum perforatum L and Arnica montana L on surgically induced wound healing in Wistar rats. Homeopathy 101:147–153CrossRefPubMedGoogle Scholar
  30. 30.
    Blumenthal NC, Ricci J, Breger L, Zychlinsky A, Solomon H, Chen GG, Kuznetsov D, Dorfman R (1997) Effects of low-intensity AC and/or DC electromagnetic fields on cell attachment and induction of apoptosis. Bioelectromagnetics 18:264–272CrossRefPubMedGoogle Scholar
  31. 31.
    Watson T (2002) Current concepts in electrotherapy. Haemophilia 8:413–418CrossRefPubMedGoogle Scholar
  32. 32.
    Davidovitch Z, Finkelson MD, Steigman S, Shanfeld JL, Montgomery PC, Korostoff E (1980) Electric currents, bone remodeling, and orthodontic tooth movement increase in rate of tooth movement and periodontal cyclic nucleotide levels by combined force and electric current. Am J Orthod 77:33–47CrossRefPubMedGoogle Scholar
  33. 33.
    Kim DH, Park YG, Kang SG (2008) The effects of electrical current from a micro-electrical device on tooth movement. Korean J Orthod 38:337–346CrossRefGoogle Scholar
  34. 34.
    Hashimoto H (1990) Effect of micro-pulsed electricity on experimental tooth movement. Nihon Kyosei Shika Gakkai Zasshi 49:352–361PubMedGoogle Scholar
  35. 35.
    Cheng N, Van Hoof H, Bockx E, Hoogmartens MJ, Mulier JC, De Dijcker FJ, Sansen WM, De Loecker W (1982) The effects of electrical currents on ATP generation, protein synthesis, and membrane transport in rat skin. Clin Orthop Relat Res 171:264–272Google Scholar
  36. 36.
    Becker R (1985) The body electric. Willian Morrow and Co, Inc., New YorkGoogle Scholar
  37. 37.
    Basset CA (1993) Beneficial-effects of electromagnetic-fields. J Cell Biochem 51:387–393CrossRefGoogle Scholar
  38. 38.
    Cheng K, Goldman RJ (1998) Electric fields and proliferation in a dermal wound model: cell cycle kinetics. Bioelectromagnetics 19:68–74CrossRefPubMedGoogle Scholar
  39. 39.
    Kloth LC (2005) Electrical stimulation for wound healing: a review of evidence from in vitro studies, animal experiment, and clinical trials. Int J Low Extrem Wounds 4:23–44CrossRefPubMedGoogle Scholar
  40. 40.
    Mendonça FAS, Santos MTS, Esquissato MAM, Passos LE, Alves AA, Mendonça JS (2005) Efeito da aplicação da microcorrente após fratura. RGO 53:193–197Google Scholar
  41. 41.
    Lee HII, Kim MY, Kwon DR (2009) Therapeutic effect of microcurrent therapy in infants with congenital muscular torticollis. Am J Phys Med Rehabil 1:736–739Google Scholar
  42. 42.
    Balakatounis KC, Angoules AG (2008) Low-intensity electrical stimulation in wound healing: review of the efficacy of externally applied currents resembling the current of injury. Eplasty 16:8–28Google Scholar
  43. 43.
    Thakral G, Lafontaine J, Najafi B, Talal TK, Kim P, Lavery LA (2013) Electrical stimulation to accelerate wound healing. Diabet Foot Ankle 16:1–9Google Scholar
  44. 44.
    Lee BY, Wendell K, AL-Waili N, Butler G (2007) Ultra-low microcurrent therapy: a novel approach for treatment of chronic resistant wounds. Adv Ther 24:1202–1209CrossRefPubMedGoogle Scholar
  45. 45.
    Heller IJ, Nanda R (1979) Effect of metabolic alteration of periodontal fibers on tooth movement: an experimental study. Am J Orthod Dentofac Orthop 75:239–258CrossRefGoogle Scholar
  46. 46.
    Santamaria M Jr, Milagres D, Stuani AS, Stuani MBS, Ruellas ACO (2006) Initial changes in pulpal microvasculature during orthodontic tooth movement: a stereological study. Eur J Orthod 28:217–220CrossRefPubMedGoogle Scholar
  47. 47.
    Dominici M (1902) Sur une methode de technique histologique appropriee a l’etude du systeme hematopoietique. Compt Rend Soc de Biol 54:221–223Google Scholar
  48. 48.
    Junqueira LCU, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447–455CrossRefPubMedGoogle Scholar
  49. 49.
    Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the Biuret reaction. J Biol Chem 177:751–766PubMedGoogle Scholar
  50. 50.
    Lara VS, Figueiredo F, Silva TA, Cunha FQ (2003) Dentin-induced in vivo inflammatory response and in vitro activation of murine macrophages. J Dent Res 82:460–465CrossRefPubMedGoogle Scholar
  51. 51.
    Fracalossi AC, Santamaria M Jr, Consolaro MFMO, Consolaro A (2009) Experimental tooth movement in murines: study period and direction of microscopic sections. Rev Dent Press Ortod Ortop Facial 14:143–157CrossRefGoogle Scholar
  52. 52.
    Janssens K, Dijke PT, Janssens S, Hul WV (2005) Transforming growth factor-b1 to the bone. Endocr Rev 26:743–774CrossRefPubMedGoogle Scholar
  53. 53.
    Ripamonti U, Ferretti C, Teare J, Blann L (2009) Transforming growth factor-b isoforms and the induction of bone formation. J Craniofac Surg 20:1544–1555CrossRefPubMedGoogle Scholar
  54. 54.
    Zhao L, Jiang S, Hantash BM (2010) Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells. Tissue Eng Part A 16:725–733CrossRefPubMedGoogle Scholar
  55. 55.
    Seifi M, Badiee MR, Abdolazimi Z, Amdjadi P (2013) Effect of basic fibroblast growth factor on orthodontic tooth movement in rats. Cell J 15:230–237PubMedPubMedCentralGoogle Scholar
  56. 56.
    Murakami M, Simons M (2008) Fibroblast growth factor regulation of neovascularization. Curr Opin Hematol 15:215–220CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Wong VW, Crawford JD. Vasculogenic Cytokines in Wound Healing. Biomed Res Int 2013:190486Google Scholar
  58. 58.
    Asadi MR, Torkaman G, Hedayati M, Mofid M (2013) Role of sensory and motor intensity of electrical stimulation on fibroblastic growth factor-2 expression, inflammation, vascularization, and mechanical strength of full-thickness wounds. J Rehabil Res Dev 50:489–498CrossRefPubMedGoogle Scholar
  59. 59.
    Dahl J, Li J, Bring DK, Renström P, Ackermann PW (2007) Intermittent pneumatic compression enhances neurovascular ingrowth and tissue proliferation during connective tissue healing: a study in the rat. J Orthop Res 25:1185–1192CrossRefPubMedGoogle Scholar
  60. 60.
    Wise GE, King GJ (2008) Mechanisms of tooth eruption and orthodontic tooth movement. J Dent Res 87:414–434CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Bates DO (2008) Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 87(2):262–271CrossRefGoogle Scholar
  62. 62.
    Bao P, Kodra A, Tomic-Canic M, Golinko MS, Ehrlich HP, Brem H (2009) The role of vascular endothelial growth factor in wound healing. J Surg Res 153:347–358CrossRefPubMedGoogle Scholar
  63. 63.
    Aldridge SE, Lennard TW, Willims JR, Birch MA (2005) Vascular endothelial growth factor receptors in osteoclast differentiation and function. Biochem Biophys Res Commun 335:793–738CrossRefPubMedGoogle Scholar
  64. 64.
    Di Alberti L, Rossetto A, Albanese M, D’Agostino A, De Santis D, Bertossi D, Nocini PF. Expression of vascular endothelial growth factor (VEGF) mRNA in healthy bone tissue around implants and in peri-implantitis Minerva Stomatol. 2013;11 [Epub ahead of print]Google Scholar
  65. 65.
    Sousa TD, Del Carlo RJ, Viloria MIV (2001) Electrotherapy on the healing process in the articular surface of rabbits. Cienc Rural 31:819–824CrossRefGoogle Scholar
  66. 66.
    De Angelis V (1970) Observation on the response of alveolar bone to orthodontic force. Am J Orthod 58:284–294CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Gisele Sampaio Spadari
    • 1
  • Ewerton Zaniboni
    • 2
  • Silvia Amelia Scudeler Vedovello
    • 1
  • Mauro Pedrine Santamaria
    • 4
  • Maria Esméria Corezola do Amaral
    • 3
  • Gláucia Maria Tech dos Santos
    • 3
  • Marcelo Augusto Marretto Esquisatto
    • 3
  • Fernanda Aparecida Sampaio Mendonca
    • 3
  • Milton Santamaria-Jr
    • 1
    • 3
  1. 1.Graduate Program of OrthodonticsHeminio Ometto University Center, UNIARARASArarasBrazil
  2. 2.School of DentistryHeminio Ometto University Center, UNIARARASArarasBrazil
  3. 3.Graduate Program of Biomedical SciencesHeminio Ometto University Center, UNIARARASArarasBrazil
  4. 4.Division of Periodontics, College of DentistryState University of São Paulo, UNESPSão José dos CamposBrazil

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