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Published in: Clinical Oral Investigations 1/2017

01-01-2017 | Original Article

Electrical stimulation enhances tissue reorganization during orthodontic tooth movement in rats

Authors: 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

Published in: Clinical Oral Investigations | Issue 1/2017

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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.
Literature
1.
go back to reference Van Schepdael A, Vander Sloten J, Geris L (2013) A mechanobiological model of orthodontic tooth movement. Biomech Model Mechanobiol 12:249–265CrossRefPubMed Van Schepdael A, Vander Sloten J, Geris L (2013) A mechanobiological model of orthodontic tooth movement. Biomech Model Mechanobiol 12:249–265CrossRefPubMed
2.
go back to reference Krishnan V, Davidovitch Z (2006) Cellular, molecular, and tissue-level reactions to orthodontic force. Am J Orthod Dentofacial Orthop 129(469):e1–32 Krishnan V, Davidovitch Z (2006) Cellular, molecular, and tissue-level reactions to orthodontic force. Am J Orthod Dentofacial Orthop 129(469):e1–32
3.
go back to reference Ren Y, Vissink A (2008) Cytokines in crevicular fluid and orthodontic tooth movement. Eur J Oral Sci 116:89–97CrossRefPubMed Ren Y, Vissink A (2008) Cytokines in crevicular fluid and orthodontic tooth movement. Eur J Oral Sci 116:89–97CrossRefPubMed
4.
go back to reference Krishnan V, Davidovitch Z (2009) On a path to unfolding the biological mechanisms of orthodontic tooth movement. J Dent Res 88:597–608CrossRefPubMed Krishnan V, Davidovitch Z (2009) On a path to unfolding the biological mechanisms of orthodontic tooth movement. J Dent Res 88:597–608CrossRefPubMed
5.
go back to reference 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 89:1135–1141CrossRefPubMedPubMedCentral 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 89:1135–1141CrossRefPubMedPubMedCentral
6.
go back to reference 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 24:565–569CrossRefPubMed 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 24:565–569CrossRefPubMed
7.
go back to reference 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 115:355–362CrossRefPubMed 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 115:355–362CrossRefPubMed
8.
go back to reference 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. 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.
9.
go back to reference 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 19:67–74CrossRefPubMedPubMedCentral 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 19:67–74CrossRefPubMedPubMedCentral
10.
go back to reference 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 49:631–641CrossRef 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 49:631–641CrossRef
11.
go back to reference Sako E, Hosomichi J (2010) Alteration of bFGF expression with growth and age in rat molar periodontal ligament. Angle Orthod 80:904–911CrossRefPubMed Sako E, Hosomichi J (2010) Alteration of bFGF expression with growth and age in rat molar periodontal ligament. Angle Orthod 80:904–911CrossRefPubMed
12.
go back to reference 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 22:405–416CrossRefPubMed 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 22:405–416CrossRefPubMed
13.
go back to reference 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 96:543–551CrossRef 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 96:543–551CrossRef
14.
go back to reference Agren MS, Werthen M (2007) The extracellular matrix in wound healing: a closer look at therapeutics for chronic wounds. Int J Low Extrem Wounds 6:82–97CrossRefPubMed Agren MS, Werthen M (2007) The extracellular matrix in wound healing: a closer look at therapeutics for chronic wounds. Int J Low Extrem Wounds 6:82–97CrossRefPubMed
15.
go back to reference 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 23:035604CrossRef 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 23:035604CrossRef
16.
go back to reference 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 13:17 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 13:17
17.
go back to reference 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 45:275–281CrossRefPubMed 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 45:275–281CrossRefPubMed
18.
go back to reference 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] 17:94–98CrossRef 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] 17:94–98CrossRef
19.
go back to reference 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 67:271–276CrossRefPubMed 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 67:271–276CrossRefPubMed
20.
go back to reference Martin RB, Gutman W (1978) The effect of electric fields on osteoporosis of disease. Calcif Tissue Int 5:23–27CrossRef Martin RB, Gutman W (1978) The effect of electric fields on osteoporosis of disease. Calcif Tissue Int 5:23–27CrossRef
21.
go back to reference 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 23:035605CrossRef 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 23:035605CrossRef
22.
go back to reference Chao PH, Roy R, Mauck ML, Liu W, Valhmu WB, Hung CT (2000) Chondrocyte translocation response to direct current electric fields. J Biomech Eng 122:261–267CrossRefPubMed Chao PH, Roy R, Mauck ML, Liu W, Valhmu WB, Hung CT (2000) Chondrocyte translocation response to direct current electric fields. J Biomech Eng 122:261–267CrossRefPubMed
23.
go back to reference McCaig CD, Rajnicek AM, Song B, Zhao M (2005) Controlling cell behavior electrically:current views and future potential. Physiol Rev 85:943–978CrossRefPubMed McCaig CD, Rajnicek AM, Song B, Zhao M (2005) Controlling cell behavior electrically:current views and future potential. Physiol Rev 85:943–978CrossRefPubMed
24.
go back to reference Funk RH, Monsees TK (2006) Effects of electromagnetic fields on cells: physiological andtherapeutical approaches and molecular mechanisms of interaction. A review. Cells Tissues Organs 182:59–78CrossRefPubMed Funk RH, Monsees TK (2006) Effects of electromagnetic fields on cells: physiological andtherapeutical approaches and molecular mechanisms of interaction. A review. Cells Tissues Organs 182:59–78CrossRefPubMed
25.
go back to reference Poltawski L, Tim Watson T (2009) Bioelectricity and microcurrent therapy for tissue healing—a narrative review. Phys Ther Rev 14:104–114CrossRef Poltawski L, Tim Watson T (2009) Bioelectricity and microcurrent therapy for tissue healing—a narrative review. Phys Ther Rev 14:104–114CrossRef
26.
go back to reference 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 24:150–155CrossRefPubMed 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 24:150–155CrossRefPubMed
27.
go back to reference 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:1–9 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:1–9
28.
go back to reference 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 23:111–120PubMed 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 23:111–120PubMed
29.
go back to reference 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 101:147–153CrossRefPubMed 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 101:147–153CrossRefPubMed
30.
go back to reference 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 18:264–272CrossRefPubMed 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 18:264–272CrossRefPubMed
32.
go back to reference 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 77:33–47CrossRefPubMed 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 77:33–47CrossRefPubMed
33.
go back to reference Kim DH, Park YG, Kang SG (2008) The effects of electrical current from a micro-electrical device on tooth movement. Korean J Orthod 38:337–346CrossRef Kim DH, Park YG, Kang SG (2008) The effects of electrical current from a micro-electrical device on tooth movement. Korean J Orthod 38:337–346CrossRef
34.
go back to reference Hashimoto H (1990) Effect of micro-pulsed electricity on experimental tooth movement. Nihon Kyosei Shika Gakkai Zasshi 49:352–361PubMed Hashimoto H (1990) Effect of micro-pulsed electricity on experimental tooth movement. Nihon Kyosei Shika Gakkai Zasshi 49:352–361PubMed
35.
go back to reference 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 171:264–272 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 171:264–272
36.
go back to reference Becker R (1985) The body electric. Willian Morrow and Co, Inc., New York Becker R (1985) The body electric. Willian Morrow and Co, Inc., New York
37.
go back to reference Basset CA (1993) Beneficial-effects of electromagnetic-fields. J Cell Biochem 51:387–393CrossRef Basset CA (1993) Beneficial-effects of electromagnetic-fields. J Cell Biochem 51:387–393CrossRef
38.
go back to reference Cheng K, Goldman RJ (1998) Electric fields and proliferation in a dermal wound model: cell cycle kinetics. Bioelectromagnetics 19:68–74CrossRefPubMed Cheng K, Goldman RJ (1998) Electric fields and proliferation in a dermal wound model: cell cycle kinetics. Bioelectromagnetics 19:68–74CrossRefPubMed
39.
go back to reference 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 4:23–44CrossRefPubMed 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 4:23–44CrossRefPubMed
40.
go back to reference Mendonça FAS, Santos MTS, Esquissato MAM, Passos LE, Alves AA, Mendonça JS (2005) Efeito da aplicação da microcorrente após fratura. RGO 53:193–197 Mendonça FAS, Santos MTS, Esquissato MAM, Passos LE, Alves AA, Mendonça JS (2005) Efeito da aplicação da microcorrente após fratura. RGO 53:193–197
41.
go back to reference Lee HII, Kim MY, Kwon DR (2009) Therapeutic effect of microcurrent therapy in infants with congenital muscular torticollis. Am J Phys Med Rehabil 1:736–739 Lee HII, Kim MY, Kwon DR (2009) Therapeutic effect of microcurrent therapy in infants with congenital muscular torticollis. Am J Phys Med Rehabil 1:736–739
42.
go back to reference 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 16:8–28 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 16:8–28
43.
go back to reference Thakral G, Lafontaine J, Najafi B, Talal TK, Kim P, Lavery LA (2013) Electrical stimulation to accelerate wound healing. Diabet Foot Ankle 16:1–9 Thakral G, Lafontaine J, Najafi B, Talal TK, Kim P, Lavery LA (2013) Electrical stimulation to accelerate wound healing. Diabet Foot Ankle 16:1–9
44.
go back to reference 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 24:1202–1209CrossRefPubMed 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 24:1202–1209CrossRefPubMed
45.
go back to reference Heller IJ, Nanda R (1979) Effect of metabolic alteration of periodontal fibers on tooth movement: an experimental study. Am J Orthod Dentofac Orthop 75:239–258CrossRef Heller IJ, Nanda R (1979) Effect of metabolic alteration of periodontal fibers on tooth movement: an experimental study. Am J Orthod Dentofac Orthop 75:239–258CrossRef
46.
go back to reference 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 28:217–220CrossRefPubMed 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 28:217–220CrossRefPubMed
47.
go back to reference Dominici M (1902) Sur une methode de technique histologique appropriee a l’etude du systeme hematopoietique. Compt Rend Soc de Biol 54:221–223 Dominici M (1902) Sur une methode de technique histologique appropriee a l’etude du systeme hematopoietique. Compt Rend Soc de Biol 54:221–223
48.
go back to reference Junqueira LCU, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447–455CrossRefPubMed Junqueira LCU, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447–455CrossRefPubMed
49.
go back to reference Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the Biuret reaction. J Biol Chem 177:751–766PubMed Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the Biuret reaction. J Biol Chem 177:751–766PubMed
50.
go back to reference 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 82:460–465CrossRefPubMed 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 82:460–465CrossRefPubMed
51.
go back to reference 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 14:143–157CrossRef 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 14:143–157CrossRef
52.
go back to reference Janssens K, Dijke PT, Janssens S, Hul WV (2005) Transforming growth factor-b1 to the bone. Endocr Rev 26:743–774CrossRefPubMed Janssens K, Dijke PT, Janssens S, Hul WV (2005) Transforming growth factor-b1 to the bone. Endocr Rev 26:743–774CrossRefPubMed
53.
go back to reference Ripamonti U, Ferretti C, Teare J, Blann L (2009) Transforming growth factor-b isoforms and the induction of bone formation. J Craniofac Surg 20:1544–1555CrossRefPubMed Ripamonti U, Ferretti C, Teare J, Blann L (2009) Transforming growth factor-b isoforms and the induction of bone formation. J Craniofac Surg 20:1544–1555CrossRefPubMed
54.
go back to reference Zhao L, Jiang S, Hantash BM (2010) Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells. Tissue Eng Part A 16:725–733CrossRefPubMed Zhao L, Jiang S, Hantash BM (2010) Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells. Tissue Eng Part A 16:725–733CrossRefPubMed
55.
go back to reference Seifi M, Badiee MR, Abdolazimi Z, Amdjadi P (2013) Effect of basic fibroblast growth factor on orthodontic tooth movement in rats. Cell J 15:230–237PubMedPubMedCentral Seifi M, Badiee MR, Abdolazimi Z, Amdjadi P (2013) Effect of basic fibroblast growth factor on orthodontic tooth movement in rats. Cell J 15:230–237PubMedPubMedCentral
57.
go back to reference Wong VW, Crawford JD. Vasculogenic Cytokines in Wound Healing. Biomed Res Int 2013:190486 Wong VW, Crawford JD. Vasculogenic Cytokines in Wound Healing. Biomed Res Int 2013:190486
58.
go back to reference 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 50:489–498CrossRefPubMed 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 50:489–498CrossRefPubMed
59.
go back to reference 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 25:1185–1192CrossRefPubMed 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 25:1185–1192CrossRefPubMed
61.
go back to reference Bates DO (2008) Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 87(2):262–271CrossRef Bates DO (2008) Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 87(2):262–271CrossRef
62.
go back to reference 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 153:347–358CrossRefPubMed 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 153:347–358CrossRefPubMed
63.
go back to reference Aldridge SE, Lennard TW, Willims JR, Birch MA (2005) Vascular endothelial growth factor receptors in osteoclast differentiation and function. Biochem Biophys Res Commun 335:793–738CrossRefPubMed Aldridge SE, Lennard TW, Willims JR, Birch MA (2005) Vascular endothelial growth factor receptors in osteoclast differentiation and function. Biochem Biophys Res Commun 335:793–738CrossRefPubMed
64.
go back to reference 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] 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]
65.
go back to reference Sousa TD, Del Carlo RJ, Viloria MIV (2001) Electrotherapy on the healing process in the articular surface of rabbits. Cienc Rural 31:819–824CrossRef Sousa TD, Del Carlo RJ, Viloria MIV (2001) Electrotherapy on the healing process in the articular surface of rabbits. Cienc Rural 31:819–824CrossRef
66.
go back to reference De Angelis V (1970) Observation on the response of alveolar bone to orthodontic force. Am J Orthod 58:284–294CrossRef De Angelis V (1970) Observation on the response of alveolar bone to orthodontic force. Am J Orthod 58:284–294CrossRef
Metadata
Title
Electrical stimulation enhances tissue reorganization during orthodontic tooth movement in rats
Authors
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
Publication date
01-01-2017
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 1/2017
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-016-1759-6

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