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


Cite item

Full Text

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.

About the authors

Valina Mylona

Leicester School of Pharmacy, De Montfort University,

Author for correspondence.
Email: info@benthamscience.net

Eugenia Anagnostaki

Leicester School of Pharmacy, De Montfort University

Email: info@benthamscience.net

Nasim Chiniforush

Laser Research Center, Dentistry Research Institute, Tehran University of Medical Sciences

Email: info@benthamscience.net

Hamidreza Barikani

Dental Implant Research Center, Dentistry Research Institute, Tehran University of Medical Sciences

Email: info@benthamscience.net

Edward Lynch

Leicester School of Pharmacy,, De Montfort University,

Email: info@benthamscience.net

Martin Grootveld

Leicester School of Pharmacy,, De Montfort University

Email: info@benthamscience.net

References

  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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1016/j.jpor.2012.06.001 PMID: 22796367
  6. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9(5): 641-50. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1002/jcp.22316 PMID: 20658533
  15. Bartold PM, Shi S, Gronthos S. Stem cells and periodontal regeneration. Periodontol 2000 2006; 40: 164-72. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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) doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.5978/islsm.20.205 PMID: 24155530
  71. Smith KC. Laser (and LED) therapy is phototherapy. Photomed Laser Surg 2005; 23(1): 78-80. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1002/0471741817
  87. McKee C, Chaudhry GR. Advances and challenges in stem cell culture. Colloids Surf B Biointerfaces 2017; 159: 62-77. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2024 Bentham Science Publishers