Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

Comparison of early wound healing using modified papilla preservation technique between enamel matrix derivative and recombinant human fibroblast growth factor

  • Yohei Nakayama (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Shinichi Tabe (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Kazuma Igarashi (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Satoshi Moriya (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Tsuyoshi Katsumata (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Ryo Kobayashi (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Shuta Nakagawa (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Tomoko Nishino (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Namiko Fukuoka (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Kota Hosono (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Mai Yamasaki (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Yosuke Yamazaki (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Moe Ogihara-Takeda (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Shoichi Ito (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Yumi Saito (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Arisa Yamaguchi (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Yuto Tsuruya (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Mizuho Yamazaki-Takai (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Shoichi Yoshino (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Hideki Takai (Department of Periodontology, Nihon University School of Dentistry at Matsudo) ;
  • Yorimasa Ogata (Department of Periodontology, Nihon University School of Dentistry at Matsudo)
  • Received : 2023.07.04
  • Accepted : 2023.10.05
  • Published : 2024.08.31
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: Enamel matrix derivative (EMD) has demonstrated beneficial effects on wound healing following surgery. However, the effects of recombinant human fibroblast growth factor 2 (rhFGF-2) in periodontal regeneration therapy have not been extensively studied. This retrospective study was conducted to compare the wound healing outcomes of the modified papilla preservation technique (mPPT) between EMD and rhFGF-2 therapies. Methods: A total of 79 sites were evaluated for early wound healing using the modified early wound healing index (mEHI), which included 6 items: incision, fibrin clotting, step, redness, swelling, and dehiscence. A numeric analog scale, along with postoperative images of the 6 mEHI items, was established and used for the evaluations. The inter-rater reliability of the mEHI was assessed via intraclass correlation coefficients (ICCs). After adjusting for factors influencing the mPPT, the differences in mEHI scores between the EMD and rhFGF-2 groups were statistically analyzed. Additionally, radiographic bone fill (RBF) was evaluated 6 months after surgery. Results: The ICC of the mEHI was 0.575. The mEHI, redness score, and dehiscence scores were significantly higher in the rhFGF-2 group (n=33) than in the EMD group (n=46). Similar results were observed in the subgroup of patients aged 50 years or older, but not in those younger than 50 years. In the subgroup with non-contained bone defects, related results were noted, but not in the subgroup with contained bone defects. However, early wound healing did not correlate with RBF at 6 months after surgery. Conclusions: Within the limitations of this study, the findings suggest that early wound healing following the use of mPPT with rhFGF-2 is somewhat superior to that observed after mPPT with EMD. However, mEHI should be improved for use as a predictive tool for early wound healing and to reflect clinical outcomes after surgery.

Keywords

Acknowledgement

This study received partial support from the Japan Society for the Promotion of Science (Chiyoda, Tokyo, Japan) through the KAKENHI Grants-in-Aid for Scientific Research (C), No. 21K09921, awarded to Y. N. We extend our thanks to Emiri Wada and Ayako Kato for their evaluation of wound healing by modified early wound healing index (mEHI).

References

  1. Heijl L, Heden G, Svardstrom G, Ostgren A. Enamel matrix derivative (EMDOGAIN) in the treatment of intrabony periodontal defects. J Clin Periodontol 1997;24:705-14. https://doi.org/10.1111/j.1600-051X.1997.tb00253.x
  2. Lyngstadaas SP, Wohlfahrt JC, Brookes SJ, Paine ML, Snead ML, Reseland JE. Enamel matrix proteins; old molecules for new applications. Orthod Craniofac Res 2009;12:243-53. https://doi.org/10.1111/j.1601-6343.2009.01459.x
  3. Kitamura M, Nakashima K, Kowashi Y, Fujii T, Shimauchi H, Sasano T, et al. Periodontal tissue regeneration using fibroblast growth factor-2: randomized controlled phase II clinical trial. PLoS One 2008;3:e2611.
  4. Kitamura M, Akamatsu M, Kawanami M, Furuichi Y, Fujii T, Mori M, et al. Randomized placebo-controlled and controlled non-inferiority phase III trials comparing trafermin, a recombinant human fibroblast growth factor 2, and enamel matrix derivative in periodontal regeneration in intrabony defects. J Bone Miner Res 2016;31:806-14. https://doi.org/10.1002/jbmr.2738
  5. Cortellini P, Prato GP, Tonetti MS. The simplified papilla preservation flap. A novel surgical approach for the management of soft tissues in regenerative procedures. Int J Periodontics Restorative Dent 1999;19:589-99.
  6. Cortellini P, Tonetti MS, Lang NP, Suvan JE, Zucchelli G, Vangsted T, et al. The simplified papilla preservation flap in the regenerative treatment of deep intrabony defects: clinical outcomes and postoperative morbidity. J Periodontol 2001;72:1702-12. https://doi.org/10.1902/jop.2001.72.12.1702
  7. Takei HH, Han TJ, Carranza FA Jr, Kenney EB, Lekovic V. Flap technique for periodontal bone implants. Papilla preservation technique. J Periodontol 1985;56:204-10. https://doi.org/10.1902/jop.1985.56.4.204
  8. Cortellini P, Prato GP, Tonetti MS. The modified papilla preservation technique. A new surgical approach for interproximal regenerative procedures. J Periodontol 1995;66:261-6. https://doi.org/10.1902/jop.1995.66.4.261
  9. Murphy KG. Interproximal tissue maintenance in GTR procedures: description of a surgical technique and 1-year reentry results. Int J Periodontics Restorative Dent 1996;16:463-77.
  10. Trombelli L, Simonelli A, Pramstraller M, Wikesjo UM, Farina R. Single flap approach with and without guided tissue regeneration and a hydroxyapatite biomaterial in the management of intraosseous periodontal defects. J Periodontol 2010;81:1256-63. https://doi.org/10.1902/jop.2010.100113
  11. Retzepi M, Tonetti M, Donos N. Comparison of gingival blood flow during healing of simplified papilla preservation and modified Widman flap surgery: a clinical trial using laser Doppler flowmetry. J Clin Periodontol 2007;34:903-11. https://doi.org/10.1111/j.1600-051X.2007.01119.x
  12. Cortellini P, Tonetti MS. A minimally invasive surgical technique with an enamel matrix derivative in the regenerative treatment of intra-bony defects: a novel approach to limit morbidity. J Clin Periodontol 2007;34:87-93. https://doi.org/10.1111/j.1600-051X.2006.01020.x
  13. Cortellini P, Tonetti MS. Improved wound stability with a modified minimally invasive surgical technique in the regenerative treatment of isolated interdental intrabony defects. J Clin Periodontol 2009;36:157-63. https://doi.org/10.1111/j.1600-051X.2008.01352.x
  14. Moreno Rodriguez JA, Ortiz Ruiz AJ, Caffesse RG. Periodontal reconstructive surgery of deep intraosseous defects using an apical approach. Non-incised papillae surgical approach (NIPSA): a retrospective cohort study. J Periodontol 2019;90:454-64. https://doi.org/10.1002/JPER.18-0405
  15. Wachtel H, Schenk G, Bohm S, Weng D, Zuhr O, Hurzeler MB. Microsurgical access flap and enamel matrix derivative for the treatment of periodontal intrabony defects: a controlled clinical study. J Clin Periodontol 2003;30:496-504. https://doi.org/10.1034/j.1600-051X.2003.00013.x
  16. Maycock J, Wood SR, Brookes SJ, Shore RC, Robinson C, Kirkham J. Characterization of a porcine amelogenin preparation, EMDOGAIN, a biological treatment for periodontal disease. Connect Tissue Res 2002;43:472-6. https://doi.org/10.1080/03008200290000880
  17. Mercado F, Hamlet S, Ivanovski S. Subepithelial connective tissue graft with or without enamel matrix derivative for the treatment of multiple class III-IV recessions in lower anterior teeth: a 3-year randomized clinical trial. J Periodontol 2020;91:473-83. https://doi.org/10.1002/JPER.19-0058
  18. Discepoli N, Mirra R, Ferrari M. Efficacy of enamel derivatives to improve keratinized tissue as adjunct to coverage of gingival recessions: a systematic review and meta-analysis. Materials (Basel) 2019;12:2790.
  19. Graziani F, Peric M, Marhl U, Petrini M, Bettini L, Tonetti M, et al. Local application of enamel matrix derivative prevents acute systemic inflammation after periodontal regenerative surgery: a randomized controlled clinical trial. J Clin Periodontol 2020;47:747-55. https://doi.org/10.1111/jcpe.13270
  20. Johnson DL, Carnes D, Steffensen B, Cochran DL. Cellular effects of enamel matrix derivative are associated with different molecular weight fractions following separation by size-exclusion chromatography. J Periodontol 2009;80:648-56. https://doi.org/10.1902/jop.2009.070420
  21. Okumura M, Okuda T, Nakamura T, Yajima M. Acceleration of wound healing in diabetic mice by basic fibroblast growth factor. Biol Pharm Bull 1996;19:530-5. https://doi.org/10.1248/bpb.19.530
  22. Baffour R, Berman J, Garb JL, Rhee SW, Kaufman J, Friedmann P. Enhanced angiogenesis and growth of collaterals by in vivo administration of recombinant basic fibroblast growth factor in a rabbit model of acute lower limb ischemia: dose-response effect of basic fibroblast growth factor. J Vasc Surg 1992;16:181-91. https://doi.org/10.1016/0741-5214(92)90106-I
  23. Murakami S. Periodontal tissue regeneration by signaling molecule(s): what role does basic fibroblast growth factor (FGF-2) have in periodontal therapy? Periodontol 2000 2011;56:188-208. https://doi.org/10.1111/j.1600-0757.2010.00365.x
  24. Canalis E, Centrella M, McCarthy T. Effects of basic fibroblast growth factor on bone formation in vitro. J Clin Invest 1988;81:1572-7. https://doi.org/10.1172/JCI113490
  25. Bertl K, An N, Bruckmann C, Dard M, Andrukhov O, Matejka M, et al. Effects of enamel matrix derivative on proliferation/viability, migration, and expression of angiogenic factor and adhesion molecules in endothelial cells in vitro. J Periodontol 2009;80:1622-30. https://doi.org/10.1902/jop.2009.090157
  26. Kasaj A, Meister J, Lehmann K, Stratul SI, Schlee M, Stein JM, et al. The influence of enamel matrix derivative on the angiogenic activity of primary endothelial cells. J Periodontal Res 2012;47:479-87. https://doi.org/10.1111/j.1600-0765.2011.01456.x
  27. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 2005;16:159-78. https://doi.org/10.1016/j.cytogfr.2005.01.004
  28. Nakayama Y, Matsuda H, Itoh S, Iwai Y, Takai H, Mezawa M, et al. Impact of adjunctive procedures on recombinant human fibroblast growth factor-2-mediated periodontal regeneration therapy: a retrospective study. J Periodontol 2021;92:983-94. https://doi.org/10.1002/JPER.20-0481
  29. Bell WB, Boegel PN, Keene JC. The use of autogenous bone grafts in the treatment of infrabony periodontal defects. J Hawaii State Dent Assoc 1969;2:6-10.
  30. Schei O, Waerhaug J, Lovdal A, Arno A. Alveolar bone loss as related to oral hygiene and age. J Periodontol 1959;30:7-16. https://doi.org/10.1902/jop.1959.30.1.7
  31. Lindhe J, Socransky S, Nyman S, Westfelt E, Haffajee A. Effect of age on healing following periodontal therapy. J Clin Periodontol 1985;12:774-87. https://doi.org/10.1111/j.1600-051X.1985.tb01403.x
  32. Ashcroft GS, Mills SJ, Ashworth JJ. Ageing and wound healing. Biogerontology 2002;3:337-45. https://doi.org/10.1023/A:1021399228395
  33. Martin P. Wound healing--aiming for perfect skin regeneration. Science 1997;276:75-81. https://doi.org/10.1126/science.276.5309.75
  34. Smith PC, Caceres M, Martinez C, Oyarzun A, Martinez J. Gingival wound healing: an essential response disturbed by aging? J Dent Res 2015;94:395-402. https://doi.org/10.1177/0022034514563750
  35. Okuda K, Miyazaki A, Momose M, Murata M, Nomura T, Kubota T, et al. Levels of tissue inhibitor of metalloproteinases-1 and matrix metalloproteinases-1 and -8 in gingival crevicular fluid following treatment with enamel matrix derivative (EMDOGAIN). J Periodontal Res 2001;36:309-16. https://doi.org/10.1034/j.1600-0765.2001.360506.x
  36. Miron RJ, Bosshardt DD, Hedbom E, Zhang Y, Haenni B, Buser D, et al. Adsorption of enamel matrix proteins to a bovine-derived bone grafting material and its regulation of cell adhesion, proliferation, and differentiation. J Periodontol 2012;83:936-47. https://doi.org/10.1902/jop.2011.110480
  37. Fujihara C, Kanai Y, Masumoto R, Kitagaki J, Matsumoto M, Yamada S, et al. Fibroblast growth factor-2 inhibits CD40-mediated periodontal inflammation. J Cell Physiol 2019;234:7149-60. https://doi.org/10.1002/jcp.27469
  38. Zeldich E, Koren R, Nemcovsky C, Weinreb M. Enamel matrix derivative stimulates human gingival fibroblast proliferation via ERK. J Dent Res 2007;86:41-6. https://doi.org/10.1177/154405910708600106
  39. Schlueter SR, Carnes DL Jr, Cochran DL. In vitro effects of enamel matrix derivative on microvascular cells. J Periodontol 2007;78:141-51. https://doi.org/10.1902/jop.2007.060111
  40. Aspriello SD, Zizzi A, Spazzafumo L, Rubini C, Lorenzi T, Marzioni D, et al. Effects of enamel matrix derivative on vascular endothelial growth factor expression and microvessel density in gingival tissues of periodontal pocket: a comparative study. J Periodontol 2011;82:606-12. https://doi.org/10.1902/jop.2010.100180