DOI QR코드

DOI QR Code

Effect of Epidermal Growth Factor with Collagen Matrix on Increasing Gingival Thickness: A Pilot Preclinical Investigation

  • Hyun-Chang Lim (Department of Periodontology, Kyung Hee University College of Dentistry, Periodontal-Implant Clinical Research Institute, Kyung Hee University Medical Center) ;
  • Yeek Herr (Department of Periodontology, Kyung Hee University College of Dentistry, Periodontal-Implant Clinical Research Institute, Kyung Hee University Medical Center) ;
  • Jong-Hyuk Chung (Department of Periodontology, Kyung Hee University College of Dentistry, Periodontal-Implant Clinical Research Institute, Kyung Hee University Medical Center) ;
  • Seung-Yun Shin (Department of Periodontology, Kyung Hee University College of Dentistry, Periodontal-Implant Clinical Research Institute, Kyung Hee University Medical Center) ;
  • Seung-Il Shin (Department of Periodontology, Kyung Hee University College of Dentistry, Periodontal-Implant Clinical Research Institute, Kyung Hee University Medical Center) ;
  • Ji-Youn Hong (Department of Periodontology, Kyung Hee University College of Dentistry, Periodontal-Implant Clinical Research Institute, Kyung Hee University Medical Center)
  • Received : 2023.06.14
  • Accepted : 2023.08.02
  • Published : 2023.12.30

Abstract

Purpose: To investigate the effect of epidermal growth factor (EGF) with collagen matrix (CM) for increasing gingival thickness. Materials and Methods: In five mongrel dogs, bilateral gingival defects were surgically made on the maxillary canines. After two months, either a subepithelial connective tissue graft (group SCTG) or CM with EGF (0.1 ug/ml, group EGF) was grafted, and the flap was coronally positioned to cover the graft materials. The animals were sacrificed after three months. Intraoral scanning was performed for soft tissue analysis. Histologic and histomorphometric analyses were performed. Result: Two animals exhibited wound dehiscence during the healing phase, leaving three for analysis. No statistically significant difference was found in soft tissue changes (P>0.05). The level of gingival margin (GM) increased in both groups (1.02±0.74 mm in group SCTG vs. 1.24±0.83 mm in group EGF). Linear increases at the GM pre-augmentation in the soft tissue profile were 1.08±0.58 mm in group SCTG and 0.96±0.73 mm in group EGF. Histomorphometric parameters (keratinized tissue height, tissue thickness, and rete peg density) were not significantly different between the groups (P>0.05). Conclusion: EGF loaded onto CM led to comparable gingival phenotype enhancement to SCTG.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (No.2020R1C1C1008201). Epidermal growth factor (EGF) was kindly provided by Daewoong, Seoul, Korea. Collagen matrices were kindly provided by Genoss, Seoul, Korea.

References

  1. Barootchi S, Tavelli L, Zucchelli G, Giannobile WV, Wang HL. Gingival phenotype modification therapies on natural teeth: a network meta-analysis. J Periodontol. 2020; 91: 1386-99. https://doi.org/10.1002/JPER.19-0715
  2. Rasperini G, Acunzo R, Cannalire P, Farronato G. Influence of periodontal biotype on root surface exposure during orthodontic treatment: a preliminary study. Int J Periodontics Restorative Dent. 2015; 35: 665-75. https://doi.org/10.11607/prd.2239
  3. Cortellini P, Bissada NF. Mucogingival conditions in the natural dentition: Narrative review, case definitions, and diagnostic considerations. J Clin Periodontol. 2018; 45(Suppl 20): S190-8. https://doi.org/10.1111/jcpe.12948
  4. Song YW, Kim S, Waller T, Cha JK, Cho SW, Jung UW, Thoma DS. Soft tissue substitutes to increase gingival thickness: histologic and volumetric analyses in dogs. J Clin Periodontol. 2019; 46: 96-104. https://doi.org/10.1111/jcpe.13034
  5. Zucchelli G, Tavelli L, McGuire MK, Rasperini G, Feinberg SE, Wang HL, Giannobile WV. Autogenous soft tissue grafting for periodontal and periimplant plastic surgical reconstruction. J Periodontol. 2020; 91: 9-16. https://doi.org/10.1002/JPER.19-0350
  6. Chambrone L, Sukekava F, Araujo MG, Pustiglioni FE, Chambrone LA, Lima LA. Root-coverage procedures for the treatment of localized recession-type defects: a Cochrane systematic review. J Periodontol. 2010; 81: 452-78. https://doi.org/10.1902/jop.2010.090540
  7. Chambrone L, Tatakis DN. Periodontal soft tissue root coverage procedures: a systematic review from the AAP Regeneration Workshop. J Periodontol. 2015; 86(2 Suppl): S8-51. https://doi.org/10.1902/jop.2015.130674
  8. Zuhr O, Baumer D, Hurzeler M. The addition of soft tissue replacement grafts in plastic periodontal and implant surgery: critical elements in design and execution. J Clin Periodontol. 2014; 41(Suppl 15): S123-42. https://doi.org/10.1111/jcpe.12185
  9. Tavelli L, Barootchi S, Rasperini G, Giannobile WV. Clinical and patient-reported outcomes of tissue engineering strategies for periodontal and peri-implant reconstruction. Periodontol 2000. 2023; 91: 217-69. https://doi.org/10.1111/prd.12446
  10. Pietruska M, Skurska A, Podlewski L, Milewski R, Pietruski J. Clinical evaluation of Miller class I and II recessions treatment with the use of modified coronally advanced tunnel technique with either collagen matrix or subepithelial connective tissue graft: a randomized clinical study. J Clin Periodontol. 2019; 46: 86-95. https://doi.org/10.1111/jcpe.13031
  11. Lee KS, Shin SY, Hammerle CHF, Jung UW, Lim HC, Thoma DS. Dimensional ridge changes in conjunction with four implant timing protocols and two types of soft tissue grafts: a pilot pre-clinical study. J Clin Periodontol. 2022; 49: 401-11. https://doi.org/10.1111/jcpe.13594
  12. Schmitt CM, Matta RE, Moest T, Humann J, Gammel L, Neukam FW, Schlegel KA. Soft tissue volume alterations after connective tissue grafting at teeth: the subepithelial autologous connective tissue graft versus a porcine collagen matrix - a pre-clinical volumetric analysis. J Clin Periodontol. 2016; 43: 609-17. Erratum in: J Clin Periodontol. 2018; 45: 392.
  13. Ben Amara H, Thoma DS, Schwarz F, Song HY, Capetillo J, Koo KT. Healing kinetics of oral soft tissue wounds treated with recombinant epidermal growth factor: translation from a canine model. J Clin Periodontol. 2019; 46: 105-17. https://doi.org/10.1111/jcpe.13035
  14. Kim JM, Bak EJ, Chang JY, Kim ST, Park WS, Yoo YJ, Cha JH. Effects of HB-EGF and epiregulin on wound healing of gingival cells in vitro. Oral Dis. 2011; 17: 785-93. https://doi.org/10.1111/j.1601-0825.2011.01836.x
  15. Pansani TN, Basso FG, Turrioni AP, Soares DG, Hebling J, de Souza Costa CA. Effects of low-level laser therapy and epidermal growth factor on the activities of gingival fibroblasts obtained from young or elderly individuals. Lasers Med Sci. 2017; 32: 45-52. https://doi.org/10.1007/s10103-016-2081-x
  16. Park JW, Hwang SR, Yoon IS. Advanced growth factor delivery systems in wound management and skin regeneration. Molecules. 2017; 22: 1259.
  17. Kim JW, Kim MG, Lee HJ, Koh Y, Kwon JH, Kim I, Park S, Kim BK, Oh JM, Kim KI, Yoon SS. Topical recombinant human epidermal growth factor for oral mucositis induced by intensive chemotherapy with hematopoietic stem cell transplantation: final analysis of a randomized, double-blind, placebo-controlled, phase 2 trial. PLoS One. 2017; 12: e0168854.
  18. Kim KI, Kim JW, Lee HJ, Kim BS, Bang SM, Kim I, Oh JM, Yoon SS, Lee JS, Park S, Kim BK. Recombinant human epidermal growth factor on oral mucositis induced by intensive chemotherapy with stem cell transplantation. Am J Hematol. 2013; 88: 107-12. https://doi.org/10.1002/ajh.23359
  19. Wu HG, Song SY, Kim YS, Oh YT, Lee CG, Keum KC, Ahn YC, Lee SW. Therapeutic effect of recombinant human epidermal growth factor (RhEGF) on mucositis in patients undergoing radiotherapy, with or without chemotherapy, for head and neck cancer: a double-blind placebo-controlled prospective phase 2 multi-institutional clinical trial. Cancer. 2009; 115: 3699-708. https://doi.org/10.1002/cncr.24414
  20. Kao RT, Curtis DA, Kim DM, Lin GH, Wang CW, Cobb CM, Hsu YT, Kan J, Velasquez D, Avila-Ortiz G, Yu SH, Mandelaris GA, Rosen PS, Evans M, Gunsolley J, Goss K, Ambruster J, Wang HL. American Academy of Periodontology best evidence consensus statement on modifying periodontal phenotype in preparation for orthodontic and restorative treatment. J Periodontol. 2020; 91: 289-98. https://doi.org/10.1002/JPER.19-0577
  21. Park JS, Herr Y, Chung JH, Shin SI, Lim HC. Retrospective analysis of keratinized tissue augmentation using a xenogeneic collagen matrix for resolving peri-implant mucositis and peri-implantitis. J Periodontal Implant Sci. 2023; 53: 145-56. https://doi.org/10.5051/jpis.2200700035
  22. Lim HC, An SC, Lee DW. A retrospective comparison of three modalities for vestibuloplasty in the posterior mandible: apically positioned flap only vs. free gingival graft vs. collagen matrix. Clin Oral Investig. 2018; 22: 2121-8.
  23. De Angelis P, Rella E, Manicone PF, Liguori MG, De Rosa G, Cavalcanti C, Galeazzi N, D'Addona A. Xenogeneic collagen matrix versus connective tissue graft for soft tissue augmentation at immediately placed implants: a prospective clinical trial. Int J Oral Maxillofac Surg. 2023; 52: 1097-105. https://doi.org/10.1016/j.ijom.2023.01.019
  24. Qiu X, Li X, Li F, Hu D, Wen Z, Wang Y, Zhang J. Xenogeneic collagen matrix versus free gingival graft for augmenting keratinized mucosa around posterior mandibular implants: a randomized clinical trial. Clin Oral Investig. 2023; 27: 1953-64. https://doi.org/10.1007/s00784-022-04853-8
  25. Wallace SC, Pikos MA, Prasad H. De novo bone regeneration in human extraction sites using recombinant human bone morphogenetic protein-2/ACS: a clinical, histomorphometric, densitometric, and 3-dimensional cone-beam computerized tomographic scan evaluation. Implant Dent. 2014; 23: 132-7. https://doi.org/10.1097/ID.0000000000000035
  26. Cochran DL, Jones AA, Lilly LC, Fiorellini JP, Howell H. Evaluation of recombinant human bone morphogenetic protein-2 in oral applications including the use of endosseous implants: 3-year results of a pilot study in humans. J Periodontol. 2000; 71: 1241-57. https://doi.org/10.1902/jop.2000.71.8.1241
  27. Jo DW, Cho YD, Seol YJ, Lee YM, Lee HJ, Kim YK. A randomized controlled clinical trial evaluating efficacy and adverse events of different types of recombinant human bone morphogenetic protein-2 delivery systems for alveolar ridge preservation. Clin Oral Implants Res. 2019; 30: 396-409. https://doi.org/10.1111/clr.13423
  28. Fiorellini JP, Howell TH, Cochran D, Malmquist J, Lilly LC, Spagnoli D, Toljanic J, Jones A, Nevins M. Randomized study evaluating recombinant human bone morphogenetic protein-2 for extraction socket augmentation. J Periodontol. 2005; 76: 605-13. https://doi.org/10.1902/jop.2005.76.4.605
  29. Cha JK, Sun YK, Lee JS, Choi SH, Jung UW. Root coverage using porcine collagen matrix with fibroblast growth factor-2: a pilot study in dogs. J Clin Periodontol. 2017; 44: 96-103. https://doi.org/10.1111/jcpe.12644
  30. Kim YS, Ji JH, Oh SY, Lee S, Huh SJ, Lee JH, Song KH, Son CH, Roh MS, Lee GW, Lee J, Kim ST, Kim CK, Jang JS, Hwang IG, Ahn HK, Park LC, Oh SY, Kim SG, Lee SC, Lim DH, Lee SI, Kang JH. A randomized controlled trial of epidermal growth factor ointment for treating epidermal growth factor receptor inhibitor-induced skin toxicities. Oncologist. 2020; 25: e186-93. https://doi.org/10.1634/theoncologist.2019-0221
  31. Moon HS, Li L, Yoon HJ, Ji YS, Yoon KC. Effect of epidermal growth factor ointment on persistent epithelial defects of the cornea. BMC Ophthalmol. 2020; 20: 147.
  32. Lim HC, Paeng KW, Kim MJ, Jung RE, Hammerle CH, Jung UW, Thoma DS. Immediate implant placement in conjunction with guided bone regeneration and/or connective tissue grafts: an experimental study in canines. J Periodontal Implant Sci. 2022; 52: 170-80. https://doi.org/10.5051/jpis.2104040202
  33. Thoma DS, Naenni N, Benic GI, Hammerle CH, Jung RE. Soft tissue volume augmentation at dental implant sites using a volume stable three-dimensional collagen matrix - histological outcomes of a preclinical study. J Clin Periodontol. 2017; 44: 185-94. https://doi.org/10.1111/jcpe.12635
  34. Avila-Ortiz G, Couso-Queiruga E, Pirc M, Chambrone L, Thoma DS. Outcome measures and methods of assessment of soft-tissue augmentation interventions in the context of dental implant therapy: a systematic review of clinical studies published in the last 10 years. Clin Oral Implants Res. 2023; 34(Suppl 25): 84-96. https://doi.org/10.1111/clr.13927
  35. Noh K, Thoma DS, Park JC, Lee DW, Shin SY, Lim HC. A case series of profilometric changes in two implant placement protocols at periodontally compromised non-molar sites. Sci Rep. 2021; 11: 1714.