Photobiomodulation Effects on Periodontal Ligament Stem Cells: A
Systematic Review of In Vitro Studies

Valina      Mylona; Eugenia      Anagnostaki; Nasim      Chiniforush; Hamidreza      Barikani; Edward      Lynch; Martin      Grootveld

doi:10.2174/1574888X17666220527090321

Abstract

Background: Stem cell therapy has been considered to play a paramount role in the treatment modalities available for regenerative dentistry. The established beneficial effects of photobiomodulation (PBM) at the cellular level have led to the combined use of these two factors (PBM and stem cells). The main goal of this study was firstly to critically appraise the effects of PBM on periodontal ligament stem cells (PDLSCs), and secondly to explore the most effective PBM protocols applied.

Methods: Pubmed, Cochrane, Scopus, Science Direct, and Google Scholar search engines were used to identify experimental in vitro studies in which PBM was applied to cultured PDLSCs. After applying specific keywords, additional filters, and inclusion/exclusion criteria, a preliminary number of 245 articles were narrowed down to 11 in which lasers and LEDs were used within the 630 - 1064 nm wavelength range. Selected articles were further assessed by three independent reviewers for strict compliance with PRISMA guidelines, and a modified Cochrane risk of bias to determine eligibility.

Statistical Analysis: The dataset analysed was extracted from the studies with sufficient and clearly presented PBM protocols. Simple univariate regression analysis was performed to explore the significance of contributions of potential quantitative predictor variables toward study outcomes, and a one-way ANOVA model was employed for testing differences between the laser or LED sources of the treatments. The significance level for testing was set at α = 0.05.

Results: The proliferation rate, osteogenic differentiation, and expression of different indicative genes for osteogenesis and inflammation suppression were found to be positively affected by the application of various types of lasers and LEDs. With regard to the PBM protocol, only the wavelength variable appeared to affect the treatment outcome; indeed, the 940 nm wavelength parameter was found not to exert a favourable effect.

Conclusions: Photobiomodulation can enhance the stemness and differentiation capacities of periodontal ligament stem cells. Therefore, for PBM protocols, there remains no consensus amongst the scientific community. Statistical analyses performed here indicated that the employment of a near-infrared (NIR) wavelength of 940 nm may not yield a significant favourable outcome, although those within the 630 - 830 nm range did so. Concerning the fluence, it should not exceed 8 J/cm² when therapy is applied by LED devices, and 4 J/cm² when applied by lasers, respectively.

Keywords: Laser, low level, LED, periodontal ligament, periodontal ligament stem cells, photobiomodulation, PBM, PDL, PDLSC, systematic review.

« Previous Next »

Graphical Abstract

[1]
Trubiani O, Pizzicannella J, Caputi S, et al. Periodontal ligament stem cells: Current knowledge and future perspectives. Stem Cells Dev  2019; 28(15): 995-1003.
 [http://dx.doi.org/10.1089/scd.2019.0025] [PMID:  31017047]

[2]
Mao AS, Mooney DJ. Regenerative medicine: Current therapies and future directions. Proc Natl Acad Sci USA  2015; 112(47): 14452-9.
 [http://dx.doi.org/10.1073/pnas.1508520112] [PMID:  26598661]

[3]
Gholami L, Nooshabadi VT, Shahabi S, et al. Extracellular vesicles in bone and periodontal regeneration: Current and potential therapeutic applications. Cell Biosci  2021; 11(1): 16.
 [http://dx.doi.org/10.1186/s13578-020-00527-8] [PMID:  33436061]

[4]
Raju R, Oshima M, Inoue M, et al. Three-dimensional periodontal tissue regeneration using a bone-ligament complex cell sheet. Sci Rep  2020; 10(1): 1656.
 [http://dx.doi.org/10.1038/s41598-020-58222-0] [PMID:  32015383]

[5]
Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K. Stem cells in dentistry--part I: Stem cell sources. J Prosthodont Res  2012; 56(3): 151-65.
 [http://dx.doi.org/10.1016/j.jpor.2012.06.001] [PMID:  22796367]

[6]
Caplan AI. Mesenchymal stem cells. J Orthop Res  1991; 9(5): 641-50.
 [http://dx.doi.org/10.1002/jor.1100090504] [PMID:  1870029]

[7]
Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci USA  2000; 97(25): 13625-30.
 [http://dx.doi.org/10.1073/pnas.240309797] [PMID:  11087820]

[8]
Li B, Ouchi T, Cao Y, Zhao Z, Men Y. Dental-Derived Mesenchymal Stem Cells: State of the Art. Front Cell Dev Biol  2021; 9: 654559.
 [http://dx.doi.org/10.3389/fcell.2021.654559] [PMID:  34239870]

[9]
Roato I, Chinigò G, Genova T, Munaron L, Mussano F. Oral Cavity as a Source of Mesenchymal Stem Cells Useful for Regenerative Medicine in Dentistry. Biomedicines  2021; 9(9): 1085.
 [http://dx.doi.org/10.3390/biomedicines9091085] [PMID:  34572271]

[10]
Hollands P, Aboyeji D, Orcharton M. Dental pulp stem cells in regenerative medicine. Br Dent J  2018; 224(9): 747-50.
 [http://dx.doi.org/10.1038/sj.bdj.2018.348] [PMID:  29725075]

[11]
Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet  2004; 364(9429): 149-55.
 [http://dx.doi.org/10.1016/S0140-6736(04)16627-0] [PMID:  15246727]

[12]
Trubiani O, Di Primio R, Traini T, et al. Morphological and cytofluorimetric analysis of adult mesenchymal stem cells expanded ex vivo from periodontal ligament. Int J Immunopathol Pharmacol  2005; 18(2): 213-21.
 [http://dx.doi.org/10.1177/039463200501800204] [PMID:  15888245]

[13]
Mohammed E, Khalil E, Sabry D. Effect of Adipose-Derived Stem Cells and Their Exo as Adjunctive Therapy to Nonsurgical Periodontal Treatment: A Histologic and Histomorphometric Study in Rats. Biomolecules  2018; 8(4): 167.
 [http://dx.doi.org/10.3390/biom8040167] [PMID:  30544734]

[14]
Duan X, Tu Q, Zhang J, et al. Application of induced pluripotent stem (iPS) cells in periodontal tissue regeneration. J Cell Physiol  2011; 226(1): 150-7.
 [http://dx.doi.org/10.1002/jcp.22316] [PMID:  20658533]

[15]
Bartold PM, Shi S, Gronthos S. Stem cells and periodontal regeneration. Periodontol 2000  2006; 40: 164-72.
 [http://dx.doi.org/10.1111/j.1600-0757.2005.00139.x] [PMID:  16398692]

[16]
Chen FM, Gao LN, Tian BM, et al. Treatment of periodontal intrabony defects using autologous periodontal ligament stem cells: A randomized clinical trial. Stem Cell Res Ther  2016; 7: 33.
 [http://dx.doi.org/10.1186/s13287-016-0288-1] [PMID:  26895633]

[17]
Ding G, Liu Y, Wang W, et al. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells  2010; 28(10): 1829-38.
 [http://dx.doi.org/10.1002/stem.512] [PMID:  20979138]

[18]
Park JY, Jeon SH, Choung PH. Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant  2011; 20(2): 271-85.
 [http://dx.doi.org/10.3727/096368910X519292] [PMID:  20719084]

[19]
Glenn JD, Whartenby KA. Mesenchymal stem cells: Emerging mechanisms of immunomodulation and therapy. World J Stem Cells  2014; 6(5): 526-39.
 [http://dx.doi.org/10.4252/wjsc.v6.i5.526] [PMID:  25426250]

[20]
Prockop DJ. The exciting prospects of new therapies with mesenchymal stromal cells. Cytotherapy  2017; 19(1): 1-8.
 [http://dx.doi.org/10.1016/j.jcyt.2016.09.008] [PMID:  27769637]

[21]
Zheng Y, Dong C, Yang J, et al. Exosomal microRNA-155-5p from PDLSCs regulated Th17/Treg balance by targeting sirtuin-1 in chronic periodontitis. J Cell Physiol  2019; 234(11): 20662-74.
 [http://dx.doi.org/10.1002/jcp.28671] [PMID:  31016751]

[22]
Zhao M, Dai W, Wang H, et al. Periodontal ligament fibroblasts regulate osteoblasts by exosome secretion induced by inflammatory stimuli. Arch Oral Biol  2019; 105: 27-34.
 [http://dx.doi.org/10.1016/j.archoralbio.2019.06.002] [PMID:  31247478]

[23]
Wang Y, Chen X, Cao W, Shi Y. Plasticity of mesenchymal stem cells in immunomodulation: Pathological and therapeutic implications. Nat Immunol  2014; 15(11): 1009-16.
 [http://dx.doi.org/10.1038/ni.3002] [PMID:  25329189]

[24]
Liu H, Li D, Zhang Y, Li M. Inflammation, mesenchymal stem cells and bone regeneration. Histochem Cell Biol  2018; 149(4): 393-404.
 [http://dx.doi.org/10.1007/s00418-018-1643-3] [PMID:  29435765]

[25]
Li W, Ren G, Huang Y, et al. Mesenchymal stem cells: A double-edged sword in regulating immune responses. Cell Death Differ  2012; 19(9): 1505-13.
 [http://dx.doi.org/10.1038/cdd.2012.26] [PMID:  22421969]

[26]
Bunte K, Beikler T. Th17 cells and the IL-23/IL-17 axis in the pathogenesis of periodontitis and immune-mediated inflammatory diseases. Int J Mol Sci  2019; 20(14): 3394.
 [http://dx.doi.org/10.3390/ijms20143394] [PMID:  31295952]

[27]
Circu ML, Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med  2010; 48(6): 749-62.
 [http://dx.doi.org/10.1016/j.freeradbiomed.2009.12.022] [PMID:  20045723]

[28]
Paiva CN, Bozza MT. Are reactive oxygen species always detrimental to pathogens? Antioxid Redox Signal  2014; 20(6): 1000-37.
 [http://dx.doi.org/10.1089/ars.2013.5447] [PMID:  23992156]

[29]
Cho H, Tarafder S, Fogge M, Kao K, Lee CH. Periodontal ligament stem/progenitor cells with protein-releasing scaffolds for cementum formation and integration on dentin surface. Connect Tissue Res  2016; 57(6): 488-95.
 [http://dx.doi.org/10.1080/03008207.2016.1191478] [PMID:  27215800]

[30]
Raveau S, Jordana F. Tissue engineering and three-dimensional printing in periodontal regeneration: A literature review. J Clin Med  2020; 9(12): 4008.
 [http://dx.doi.org/10.3390/jcm9124008] [PMID:  33322447]

[31]
Fekrazad R, Asefi S, Allahdadi M, Kalhori KA. Effect of photobiomodulation on mesenchymal stem cells. Photomed Laser Surg  2016; 34(11): 533-42.
 [http://dx.doi.org/10.1089/pho.2015.4029] [PMID:  27070113]

[32]
Fekrazad R, Asefi S, Eslaminejad MB, Taghiar L, Bordbar S, Hamblin MR. Photobiomodulation with single and combination laser wavelengths on bone marrow mesenchymal stem cells: Proliferation and differentiation to bone or cartilage. Lasers Med Sci  2019; 34(1): 115-26.
 [http://dx.doi.org/10.1007/s10103-018-2620-8] [PMID:  30264177]

[33]
Grassia V, Vitale M, d’Apuzzo F, Paiusco A, Caccianiga G, Perillo L. Analysis of changes induced in human periodontal ligament, dental pulp, bone marrow and adipose stem cells by low level laser therapy: A review and new perspectives. Biomed J Sci & Tech Res  2018; 4(2)

[34]
Hamblin M, Pires de Sousa M, Arany P, Carroll J, Patthoff D. Low level laser (light) therapy and photobiomodulation: The path forward. Mechanisms for Low-Level-Light Therapy. Proc SPIE  2015; 9309: 930902-4.
 [http://dx.doi.org/10.1117/12.2084049]

[35]
Amaroli A, Agas D, Laus F, et al. The Effects of photobiomodulation of 808 nm diode laser therapy at higher fluence on the in vitro osteogenic differentiation of bone marrow stromal cells. Front Physiol  2018; 9: 123.
 [http://dx.doi.org/10.3389/fphys.2018.00123] [PMID:  29527174]

[36]
Karu T. Cellular and Molecular Mechanisms of Photobiomodulation (Low-Power Laser Therapy). IEEE J Sel Top Quantum Electron  2014; 20(2): 143-8.
 [http://dx.doi.org/10.1109/JSTQE.2013.2273411]

[37]
Chung H, Dai T, Sharma SK, Huang YY, Carroll JD, Hamblin MR. The nuts and bolts of low-level laser (light) therapy. Ann Biomed Eng  2012; 40(2): 516-33.
 [http://dx.doi.org/10.1007/s10439-011-0454-7] [PMID:  22045511]

[38]
Mester E, Szende B, Gartner P. The effect of laser beams on the growth of hair in mice. Radiobiol Radiother (Berl)  1968; 9(5): 621-6. 5732466 17

[39]
Hamblin MR, Ferraresi C, Huang Y-Y, Freitas De Freitas L, Carroll JD. Low-Level Light Therapy: Photobiomodulation. 2018; 1-390.

[40]
Cronshaw M, Parker S, Anagnostaki E, Mylona V, Lynch E, Grootveld M. Photobiomodulation and Oral Mucositis: A Systematic Review. Dent J  2020; 8(3): 87.
 [http://dx.doi.org/10.3390/dj8030087] [PMID:  32764305]

[41]
Parker S, Cronshaw M, Anagnostaki E, Bordin-Aykroyd SR, Lynch E. Systematic Review of Delivery Parameters Used in Dental Photobiomodulation Therapy. Photobiomodul Photomed Laser Surg  2019; 37(12): 784-97.
 [http://dx.doi.org/10.1089/photob.2019.4694] [PMID:  31573388]

[42]
Gholami L, Asefi S, Hooshyarfard A, et al. Photobiomodulation in Periodontology and Implant Dentistry: Part 1. Photobiomodul Photomed Laser Surg  2019; 37(12): 739-65.
 [http://dx.doi.org/10.1089/photob.2019.4710] [PMID:  31750783]

[43]
Merigo E, Rocca JP, Pinheiro ALB, Fornaini C. Photobiomodulation Therapy in Oral Medicine: A Guide for the Practitioner with Focus on New Possible Protocols. Photobiomodul Photomed Laser Surg  2019; 37(11): 669-80.
 [http://dx.doi.org/10.1089/photob.2019.4624] [PMID:  31589560]

[44]
Ginani F, Soares DM, Barreto MP, Barboza CA. Effect of low-level laser therapy on mesenchymal stem cell proliferation: A systematic review. Lasers Med Sci  2015; 30(8): 2189-94.
 [http://dx.doi.org/10.1007/s10103-015-1730-9] [PMID:  25764448]

[45]
Xu XY, Li X, Wang J, He XT, Sun HH, Chen FM. Concise review: Periodontal tissue regeneration using stem cells: Strategies and translational considerations. Stem Cells Transl Med  2019; 8(4): 392-403.
 [http://dx.doi.org/10.1002/sctm.18-0181] [PMID:  30585445]

[46]
Bayat M, Virdi A, Rezaei F, Chien S. Comparison of the in vitro effects of low-level laser therapy and low-intensity pulsed ultrasound therapy on bony cells and stem cells. Prog Biophys Mol Biol  2018; 133: 36-48.
 [http://dx.doi.org/10.1016/j.pbiomolbio.2017.11.001] [PMID:  29126668]

[47]
Zhu W, Liang M. Periodontal ligament stem cells: Current status, concerns, and future prospects. Stem Cells Int  2015; 2015: 972313.
 [http://dx.doi.org/10.1155/2015/972313] [PMID:  25861283]

[48]
Arany PR, Cho A, Hunt TD, et al. Photoactivation of endogenous latent transforming growth factor-β1 directs dental stem cell differentiation for regeneration. Sci Transl Med  2014; 6(238): 238ra69.
 [http://dx.doi.org/10.1126/scitranslmed.3008234] [PMID:  24871130]

[49]
Feng J, Li X, Zhu S, et al. Photobiomodulation with 808-nm diode laser enhances gingival wound healing by promoting migration of human gingival mesenchymal stem cells via ROS/JNK/NF-κB/MMP-1 pathway. Lasers Med Sci  2020; 35(8): 1831-9.
 [http://dx.doi.org/10.1007/s10103-020-03040-z] [PMID:  32451640]

[50]
Daigo Y, Daigo E, Fukuoka H, Fukuoka N, Ishikawa M, Takahashi K. Wound healing and cell dynamics including mesenchymal and dental pulp stem cells induced by photobiomodulation therapy: An example of socket-preserving effects after tooth extraction in rats and a literature review. Int J Mol Sci  2020; 21(18): 6850.
 [http://dx.doi.org/10.3390/ijms21186850] [PMID:  32961958]

[51]
Borzabadi-Farahani A. Effect of low-level laser irradiation on proliferation of human dental mesenchymal stem cells; a systemic review. J Photochem Photobiol B  2016; 162: 577-82.
 [http://dx.doi.org/10.1016/j.jphotobiol.2016.07.022] [PMID:  27475781]

[52]
Dawoud LE, Hegazy EM, Galhom RA, Youssef MM. Photobiomodulation therapy upregulates the growth kinetics and multilineage differentiation potential of human dental pulp stem cells-an in vitro Study. Lasers Med Sci  2021; 37(3)
 [http://dx.doi.org/10.1007/s10103-021-03461-4] [PMID:  34787763]

[53]
Bidar M, Bahlakeh A, Mahmoudi M, Ahrari F, Shahmohammadi R, Jafarzadeh H. Does the application of GaAlAs laser and platelet-rich plasma induce cell proliferation and increase alkaline phosphatase activity in human dental pulp stem cells? Lasers Med Sci  2021; 36(6): 1289-95.
 [http://dx.doi.org/10.1007/s10103-020-03239-0] [PMID:  33459924]

[54]
Paschalidou M, Athanasiadou E, Arapostathis K, et al. Biological effects of low-level laser irradiation (LLLI) on stem cells from human exfoliated deciduous teeth (SHED). Clin Oral Investig  2020; 24(1): 167-80.
 [http://dx.doi.org/10.1007/s00784-019-02874-4] [PMID:  31069538]

[55]
Vale KLD, Maria DA, Picoli LC, et al. The effects of photobiomodulation delivered by light-emitting diode on stem cells from human exfoliated deciduous teeth: A study on the relevance to pluripotent stem cell viability and proliferation. Photomed Laser Surg  2017; 35(12): 659-65.
 [http://dx.doi.org/10.1089/pho.2017.4279] [PMID:  28937927]

[56]
Wu Y, Zhu T, Yang Y, et al. Irradiation with red light-emitting diode enhances proliferation and osteogenic differentiation of periodontal ligament stem cells. Lasers Med Sci  2021; 36(7): 1535-43.
 [http://dx.doi.org/10.1007/s10103-021-03278-1] [PMID:  33719020]

[57]
Gholami L, Parsamanesh G, Shahabi S, Jazaeri M, Baghaei K, Fekrazad R. The effect of laser photobiomodulation on periodontal ligament stem cells. Photochem Photobiol  2021; 97(4): 851-9.
 [http://dx.doi.org/10.1111/php.13367] [PMID:  33305457]

[58]
Chaweewannakorn C, Santiwong P, Surarit R, Sritanaudomchai H, Chintavalakorn R. The effect of LED photobiomodulation on the proliferation and osteoblastic differentiation of periodontal ligament stem cells: In vitro. J World Fed Orthod  2021; 10(2): 79-85.
 [http://dx.doi.org/10.1016/j.ejwf.2021.03.003] [PMID:  33888447]

[59]
Wang L, Liu C, Wu F. Low-level laser irradiation enhances the proliferation and osteogenic differentiation of PDLSCs via BMP signaling. Lasers Med Sci 2021.
 [http://dx.doi.org/10.1007/s10103-021-03338-6] [PMID:  34247314]

[60]
Gholami L, Hendi SS, Saidijam M, et al. Near-infrared 940-nm diode laser photobiomodulation of inflamed periodontal ligament stem cells. Lasers Med Sci 2021.
 [http://dx.doi.org/10.1007/s10103-021-03282-5] [PMID:  33740139]

[61]
Mohamed Abdelgawad L, Abd El-Hamed MM, Sabry D, Abdelgwad M. Efficacy of photobiomodulation and metformin on diabetic cell line of human periodontal ligament stem cells through Keap1/Nrf2/Ho-1 pathway. Rep Biochem Mol Biol  2021; 10(1): 30-40.
 [http://dx.doi.org/10.52547/rbmb.10.1.30] [PMID:  34277866]

[62]
Abdelgawad LM, Abdelaziz AM, Sabry D, Abdelgwad M. Influence of photobiomodulation and vitamin D on osteoblastic differentiation of human periodontal ligament stem cells and bone-like tissue formation through enzymatic activity and gene expression. Biomol Concepts  2020; 11(1): 172-81.
 [http://dx.doi.org/10.1515/bmc-2020-0016] [PMID:  34233429]

[63]
Yamauchi N, Taguchi Y, Kato H, Umeda M. High-power, red-light-emitting diode irradiation enhances proliferation, osteogenic differentiation, and mineralization of human periodontal ligament stem cells via ERK signaling pathway. J Periodontol  2018; 89(3): 351-60.
 [http://dx.doi.org/10.1002/JPER.17-0365] [PMID:  29528486]

[64]
Hou T, Li S, Zhang G, Li Y. High-fluence low-power laser irradiation promotes odontogenesis and inflammation resolution in periodontitis by enhancing stem cell proliferation and differentiation. Int J Mol Med  2018; 42(4): 2107-19.
 [http://dx.doi.org/10.3892/ijmm.2018.3804] [PMID:  30085334]

[65]
Soares DM, Ginani F, Henriques ÁG, Barboza CA. Effects of laser therapy on the proliferation of human periodontal ligament stem cells. Lasers Med Sci  2015; 30(3): 1171-4.
 [http://dx.doi.org/10.1007/s10103-013-1436-9] [PMID:  24013624]

[66]
Wu JY, Chen CH, Yeh LY, Yeh ML, Ting CC, Wang YH. Low-power laser irradiation promotes the proliferation and osteogenic differentiation of human periodontal ligament cells via cyclic adenosine monophosphate. Int J Oral Sci  2013; 5(2): 85-91.
 [http://dx.doi.org/10.1038/ijos.2013.38] [PMID:  23788285]

[67]
Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ  2021; 372(71): n71.
 [http://dx.doi.org/10.1136/bmj.n71] [PMID:  33782057]

[68]
Higgins JPT, Savović J, Page MJ, Elbers RG, Sterne JAC. Assessing risk of bias in a randomized trial.  Cochrane Handb Syst Rev Interv 2019; pp. 205-28.
 [http://dx.doi.org/10.1002/9781119536604.ch8]

[69]
de Freitas LF, Hamblin MR. Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron  2016; 22(3): 7000417.
 [http://dx.doi.org/10.1109/JSTQE.2016.2561201] [PMID:  28070154]

[70]
Kim WS, Calderhead RG. Is light-emitting diode phototherapy (LED-LLLT) really effective? Laser Ther  2011; 20(3): 205-15.
 [http://dx.doi.org/10.5978/islsm.20.205] [PMID:  24155530]

[71]
Smith KC. Laser (and LED) therapy is phototherapy. Photomed Laser Surg  2005; 23(1): 78-80.
 [http://dx.doi.org/10.1089/pho.2005.23.78] [PMID:  15782040]

[72]
Karu T. Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B  1999; 49(1): 1-17.
 [http://dx.doi.org/10.1016/S1011-1344(98)00219-X] [PMID:  10365442]

[73]
Cronshaw M, Parker S, Anagnostaki E, Mylona V, Lynch E, Grootveld M. Photobiomodulation dose parameters in dentistry: A systematic review and meta-analysis. Dent J (Basel)  2020; 8(4): 114.
 [http://dx.doi.org/10.3390/dj8040114]

[74]
Kreisler M, Christoffers AB, Willershausen B, d’Hoedt B. Effect of low-level GaAlAs laser irradiation on the proliferation rate of human periodontal ligament fibroblasts: An in vitro study. J Clin Periodontol  2003; 30(4): 353-8.
 [http://dx.doi.org/10.1034/j.1600-051X.2003.00001.x] [PMID:  12694435]

[75]
AlGhamdi KM, Kumar A, Moussa NA. Low-level laser therapy: A useful technique for enhancing the proliferation of various cultured cells. Lasers Med Sci  2012; 27(1): 237-49.
 [http://dx.doi.org/10.1007/s10103-011-0885-2] [PMID:  21274733]

[76]
Barboza CA, Ginani F, Soares DM, Henriques AC, Freitas Rde A. Low-level laser irradiation induces in vitro proliferation of mesenchymal stem cells. Einstein (Sao Paulo)  2014; 12(1): 75-81.
 [http://dx.doi.org/10.1590/S1679-45082014AO2824] [PMID:  24728250]

[77]
Hamblin MR, Demidova TN. Mechanisms of low level light therapy. Proceedings of the mechanisms for low-light therapy.  6140-614001.
 [http://dx.doi.org/10.1117/12.646294]

[78]
Hashmi JT, Huang YY, Sharma SK, et al. Effect of pulsing in low-level light therapy. Lasers Surg Med  2010; 42(6): 450-66.
 [http://dx.doi.org/10.1002/lsm.20950] [PMID:  20662021]

[79]
Heiskanen V, Hamblin MR. Photobiomodulation: Lasers vs. light emitting diodes? Photochem Photobiol Sci  2018; 17(8): 1003-17.
 [http://dx.doi.org/10.1039/C8PP00176F] [PMID:  30044464]

[80]
Gupta S, Gupta N, Kumar A, Rathore P, Tyagi AK. Potential of PDL stem cells in periodontal regeneration-review. IOSR J Dent Med Sci  2019; 18(7): 67-74.
 [http://dx.doi.org/10.9790/0853-1807126774]

[81]
Wang L, Shen H, Zheng W, et al. Characterization of stem cells from alveolar periodontal ligament. Tissue Eng Part A  2011; 17(7-8): 1015-26.
 [http://dx.doi.org/10.1089/ten.tea.2010.0140] [PMID:  21186958]

[82]
Silvério KG, Rodrigues TL, Coletta RD, et al. Mesenchymal stem cell properties of periodontal ligament cells from deciduous and permanent teeth. J Periodontol  2010; 81(8): 1207-15.
 [http://dx.doi.org/10.1902/jop.2010.090729] [PMID:  20476882]

[83]
Ji K, Liu Y, Lu W, et al. Periodontal tissue engineering with stem cells from the periodontal ligament of human retained deciduous teeth. J Periodontal Res  2013; 48(1): 105-16.
 [http://dx.doi.org/10.1111/j.1600-0765.2012.01509.x] [PMID:  22881344]

[84]
Song JS, Kim SO, Kim SH, et al. In vitro and in vivo characteristics of stem cells derived from the periodontal ligament of human deciduous and permanent teeth. Tissue Eng Part A  2012; 18(19-20): 2040-51.
 [http://dx.doi.org/10.1089/ten.tea.2011.0318] [PMID:  22571499]

[85]
Zhang J, An Y, Gao LN, Zhang YJ, Jin Y, Chen FM. The effect of aging on the pluripotential capacity and regenerative potential of human periodontal ligament stem cells. Biomaterials  2012; 33(29): 6974-86.
 [http://dx.doi.org/10.1016/j.biomaterials.2012.06.032] [PMID:  22789721]

[86]
Freshney RI. Basic principles of cell culture.  chapter 1 In :  Vunjak-Novakovic G.  Freshney, RI: Eds. Culture of Cells for Tissue Engineering Cult Cells Tissue Eng. 2006; pp. 4-22.
 [http://dx.doi.org/10.1002/0471741817]

[87]
McKee C, Chaudhry GR. Advances and challenges in stem cell culture. Colloids Surf B Biointerfaces  2017; 159: 62-77.
 [http://dx.doi.org/10.1016/j.colsurfb.2017.07.051] [PMID:  28780462]

[88]
Hakki SS, Bozkurt B, Hakki EE, et al. Bone morphogenetic protein-2, -6, and -7 differently regulate osteogenic differentiation of human periodontal ligament stem cells. J Biomed Mater Res B Appl Biomater  2014; 102(1): 119-30.
 [http://dx.doi.org/10.1002/jbm.b.32988] [PMID:  23853066]

[89]
Oortgiesen DA, Walboomers XF, Bronckers AL, Meijer GJ, Jansen JA. Periodontal regeneration using an injectable bone cement combined with BMP-2 or FGF-2. J Tissue Eng Regen Med  2014; 8(3): 202-9.
 [http://dx.doi.org/10.1002/term.1514] [PMID:  22552898]

[90]
Lee JH, Um S, Jang JH, Seo BM. Effects of VEGF and FGF-2 on proliferation and differentiation of human periodontal ligament stem cells. Cell Tissue Res  2012; 348(3): 475-84.
 [http://dx.doi.org/10.1007/s00441-012-1392-x] [PMID:  22437875]

[91]
Fujii S, Maeda H, Tomokiyo A, et al. Effects of TGF-β1 on the proliferation and differentiation of human periodontal ligament cells and a human periodontal ligament stem/progenitor cell line. Cell Tissue Res  2010; 342(2): 233-42.
 [http://dx.doi.org/10.1007/s00441-010-1037-x] [PMID:  20931341]

[92]
Kono K, Maeda H, Fujii S, et al. Exposure to transforming growth factor-β1 after basic fibroblast growth factor promotes the fibroblastic differentiation of human periodontal ligament stem/progenitor cell lines. Cell Tissue Res  2013; 352(2): 249-63.
 [http://dx.doi.org/10.1007/s00441-012-1543-0] [PMID:  23324989]

[93]
Zeng WY, Ning Y, Huang X. Advanced technologies in periodontal tissue regeneration based on stem cells: Current status and future perspectives. J Dent Sci  2021; 16(1): 501-7.
 [http://dx.doi.org/10.1016/j.jds.2020.07.008] [PMID:  33384839]

[94]
Iorio-Siciliano V, Blasi A, Nuzzolo P, Matarasso M, Isola G, Ramaglia L. Treatment of periodontal intrabony defects using enamel matrix derivative: Surgical reentry after an observation period of at least 5 years. Int J Periodont Restor Dent  2019; 39(4): 537-43.
 [http://dx.doi.org/10.11607/prd.4148] [PMID:  31226192]

[95]
Iorio-Siciliano V, Blasi A, Stratul SI, et al. Healing of periodontal suprabony defects following treatment with open flap debridement with or without an enamel matrix derivative: A randomized controlled clinical study. Clin Oral Investig  2021; 25(3): 1019-27.
 [http://dx.doi.org/10.1007/s00784-020-03392-4] [PMID:  32562077]

[96]
Otsu K, Kumakami-Sakano M, Fujiwara N, et al. Stem cell sources for tooth regeneration: Current status and future prospects. Front Physiol  2014; 5: 36.
 [http://dx.doi.org/10.3389/fphys.2014.00036] [PMID:  24550845]

[97]
Cochran DL, Cobb CM, Bashutski JD, et al. Emerging regenerative approaches for periodontal reconstruction: A consensus report from the AAP Regeneration Workshop. J Periodontol  2015; 86(2) (Suppl.): S153-6.
 [http://dx.doi.org/10.1902/jop.2015.140381] [PMID:  25317603]

[98]
Vaquette C, Saifzadeh S, Farag A, Hutmacher DW, Ivanovski S. Periodontal tissue engineering with a multiphasic construct and cell sheets. J Dent Res  2019; 98(6): 673-81.
 [http://dx.doi.org/10.1177/0022034519837967] [PMID:  30971166]

[99]
Abrahamse H. Regenerative medicine, stem cells, and low-level laser therapy: Future directives. Photomed Laser Surg  2012; 30(12): 681-2.
 [http://dx.doi.org/10.1089/pho.2012.9881] [PMID:  23140266]

[100]
Choi EJ, Yim JY, Koo KT, et al. Biological effects of a semiconductor diode laser on human periodontal ligament fibroblasts. J Periodontal 

[101]
Wang Y, Huang YY, Wang Y, Lyu P, Hamblin MR. Photobiomodulation of human adipose-derived stem cells using 810nm and 980nm lasers operates via different mechanisms of action. Biochim Biophys Acta, Gen Subj  2017; 1861(2): 441-9.
 [http://dx.doi.org/10.1016/j.bbagen.2016.10.008] [PMID:  27751953]

[102]
Tassi SA, Sergio NZ, Misawa MYO, Villar CC. Efficacy of stem cells on periodontal regeneration: Systematic review of pre-clinical studies. J Periodontal Res  2017; 52(5): 793-812.
 [http://dx.doi.org/10.1111/jre.12455] [PMID:  28394043]

[103]
Grimm WD, Dannan A, Becher S, et al. The ability of human periodontium-derived stem cells to regenerate periodontal tissues: A preliminary in vivo investigation. Int J Periodont Restor Dent  2011; 31(6): e94-e101.
 [PMID:  22140674]

Rights & Permissions Print Cite

Article Metrics

4

Journal Information

For Authors

For Editors

For Reviewers

Explore Articles

Open Access

Open Access Articles

For Visitors

DOI https://dx.doi.org/10.2174/1574888X17666220527090321	Print ISSN 1574-888X
Publisher Name Bentham Science Publisher	Online ISSN 2212-3946

Current Stem Cell Research & Therapy

Photobiomodulation Effects on Periodontal Ligament Stem Cells: A Systematic Review of In Vitro Studies

Abstract Play Pause

Graphical Abstract

Related Books

Abstract