Covid-19 Research

Case Series

Combined Sinus Grafting and Lateral Augmentation by a Hyaluronic Acid-Facilitated Guided Bone Regeneration Protocol – Case Series Supported by Human Histologic Analysis

Journal of Biomedical Research & Environmental Sciences article abstract with citation details, DOI, publication dates, subject areas, full text links, and references.

View DOI Submit Manuscript

Article Details

Publication record, authors, dates, abstract, and full text access.

Open Access
Article Type Case Series
Subject Medicine Group
OCLC 9427645896
Anton Friedmann* and Werner Goetz
Issue: Volume3-Issue1
Pages: 065-073
Received: 2022-01-06
Accepted: 2022-01-17
Published: 2022-01-18

Abstract

Guided Bone Regeneration (GBR) is a well-established procedure for the regeneration of alveolar bone defects. In the case of highly complex defect situations, however, inconsistent treatment results are often achieved. Hyaluronic Acid (HA) fulfills several relevant preliminary success criteria for improved regenerative treatment outcomes in complex defects: HA supports the creation of a toxin-free wound area, HA improves wound space stabilization, accelerates wound healing and supports regenerative processes crucial for bone regeneration. The novelty in the reported cases is the use of porcine derived bone substitute particulate hydrated with a cross-linked hyaluronic acid for simultaneous sinus grafting and lateral/vertical ridge augmentation in combination with a ribose cross-linked collagen membrane. The approval of the feasibility is provided with the clinical and histological observations. Three consecutive cases received the abovementioned material combination for staged sinus floor elevation and additional augmentation procedure by one operator according to a standardized protocol. All three sites constantly demonstrate superior clinical outcomes in terms of radiographically impressive tissue enhancement and implant function. The clinical outcomes are supported by qualitative histological analysis reflecting great similarity between samples regarding the observed process of new bone formation and bone substitute behavior. The specific staining allows for detection of osteoclastic activity and indicates the tendency of the particulate bone substitute to degrade over time once integrated.

FullText HTML FullText PDF DOI: 10.37871/jbres1401 Crossmark

Certificate of Publication

Certificate of Publication

Copyright

© 2022 Friedmann A, et al. Distributed under Creative Commons CC-BY 4.0 Creative CommonsAttribution

How to cite this article

Friedmann A, Goetz W. Combined Sinus Grafting and Lateral Augmentation by a Hyaluronic Acid-Facilitated Guided Bone Regeneration Protocol – Case Series Supported by Human Histologic Analysis. J Biomed Res Environ Sci. 2022 Jan 18; 3(1): 065-073. doi: 10.37871/jbres1401, Article ID: JBRES1401, Available at: https://www.jelsciences.com/articles/jbres1401.pdf

Subject area(s)

Dentistry

References

  1. Tatum H Jr. Maxillary and sinus implant reconstructions. Dent Clin North Am. 1986 Apr;30(2):207-29. PMID: 3516738.
  2. Schweikert M, Botticelli D, de Oliveira JA, Scala A, Salata LA, Lang NP. Use of a titanium device in lateral sinus floor elevation: an experimental study in monkeys. Clin Oral Implants Res. 2012 Jan;23(1):100-5. doi: 10.1111/j.1600-0501.2011.02200.x. Epub 2011 Apr 25. PMID: 21518009.
  3. Chiapasco M, Zaniboni M. Methods to treat the edentulous posterior maxilla: implants with sinus grafting. J Oral Maxillofac Surg. 2009 Apr;67(4):867-71. doi: 10.1016/j.joms.2008.11.023. PMID: 19304048.
  4. Handschel J, Simonowska M, Naujoks C, Depprich RA, Ommerborn MA, Meyer U, Kübler NR. A histomorphometric meta-analysis of sinus elevation with various grafting materials. Head Face Med. 2009 Jun 11;5:12. doi: 10.1186/1746-160X-5-12. PMID: 19519903; PMCID: PMC2700082.
  5. Jensen SS, Terheyden H. Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone-substitute materials. Int J Oral Maxillofac Implants. 2009;24 Suppl:218-36. PMID: 19885447.
  6. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants. 2007;22 Suppl:49-70. Erratum in: Int J Oral Maxillofac Implants. 2008 Jan-Feb;23(1):56. PMID: 18437791.
  7. Benic GI, Hämmerle CH. Horizontal bone augmentation by means of guided bone regeneration. Periodontol 2000. 2014 Oct;66(1):13-40. doi: 10.1111/prd.12039. PMID: 25123759.
  8. Dahlin C, Andersson L, Linde A. Bone augmentation at fenestrated implants by an osteopromotive membrane technique. A controlled clinical study. Clin Oral Implants Res. 1991 Oct-Dec;2(4):159-65. doi: 10.1034/j.1600-0501.1991.020401.x. PMID: 8597617.
  9. Esposito M, Grusovin MG, Coulthard P, Worthington HV. The efficacy of various bone augmentation procedures for dental implants: a Cochrane systematic review of randomized controlled clinical trials. Int J Oral Maxillofac Implants. 2006 Sep-Oct;21(5):696-710. PMID: 17066630.
  10. Hämmerle CH, Jung RE, Feloutzis A. A systematic review of the survival of implants in bone sites augmented with barrier membranes (guided bone regeneration) in partially edentulous patients. J Clin Periodontol. 2002;29 Suppl 3:226-31; discussion 232-3. doi: 10.1034/j.1600-051x.29.s3.14.x. PMID: 12787222.
  11. Ohayon L, Taschieri S, Friedmann A, Del Fabbro M. Bone Graft Displacement After Maxillary Sinus Floor Augmentation With or Without Covering Barrier Membrane: A Retrospective Computed Tomographic Image Evaluation. Int J Oral Maxillofac Implants. 2019 May/June;34(3):681–691. doi: 10.11607/jomi.6940. Epub 2018 Dec 5. PMID: 30521657.
  12. Bashutski JD, Wang HL. Biologic Agents to Promote Periodontal Regeneration and Bone Augmentation. Clin Adv Periodontics. 2011 Aug;1(2):80-87. doi: 10.1902/cap.2011.110044. PMID: 32698555.
  13. Tarnow DP, Wallace SS, Froum SJ, Rohrer MD, Cho SC. Histologic and clinical comparison of bilateral sinus floor elevations with and without barrier membrane placement in 12 patients: Part 3 of an ongoing prospective study. Int J Periodontics Restorative Dent. 2000 Apr;20(2):117-25. PMID: 11203554.
  14. Grosso LT, Iha DK, Niu J, Wakabayashi RC, Johnson PW. Protease profiles of cells isolated from regenerative membranes are associated with clinical outcomes. J Periodontol. 1997 Sep;68(9):809-18. doi: 10.1902/jop.1997.68.9.809. PMID: 9379323.
  15. Trimmel B, Gede N, Hegyi P, Szakács Z, Mezey GA, Varga E, Kivovics M, Hanák L, Rumbus Z, Szabó G. Relative performance of various biomaterials used for maxillary sinus augmentation: A Bayesian network meta-analysis. Clin Oral Implants Res. 2021 Feb;32(2):135-153. doi: 10.1111/clr.13690. Epub 2021 Jan 6. PMID: 33230862; PMCID: PMC8247032.
  16. Eliezer M, Imber JC, Sculean A, Pandis N, Teich S. Hyaluronic acid as adjunctive to non-surgical and surgical periodontal therapy: a systematic review and meta-analysis. Clin Oral Investig. 2019 Sep;23(9):3423-3435. doi: 10.1007/s00784-019-03012-w. Epub 2019 Jul 23. PMID: 31338632.
  17. Chen F, Ni Y, Liu B, Zhou T, Yu C, Su Y, Zhu X, Yu X, Zhou Y. Self-crosslinking and injectable hyaluronic acid/RGD-functionalized pectin hydrogel for cartilage tissue engineering. Carbohydr Polym. 2017 Jun 15;166:31-44. doi: 10.1016/j.carbpol.2017.02.059. Epub 2017 Feb 20. PMID: 28385238.
  18. Zhao N, Wang X, Qin L, Zhai M, Yuan J, Chen J, Li D. Effect of hyaluronic acid in bone formation and its applications in dentistry. J Biomed Mater Res A. 2016 Jun;104(6):1560-9. doi: 10.1002/jbm.a.35681. Epub 2016 Apr 9. PMID: 27007721.
  19. Carlson GA, Dragoo JL, Samimi B, Bruckner DA, Bernard GW, Hedrick M, Benhaim P. Bacteriostatic properties of biomatrices against common orthopaedic pathogens. Biochem Biophys Res Commun. 2004 Aug 20;321(2):472-8. doi: 10.1016/j.bbrc.2004.06.165. PMID: 15358200.
  20. Pirnazar P, Wolinsky L, Nachnani S, Haake S, Pilloni A, Bernard GW. Bacteriostatic effects of hyaluronic acid. J Periodontol. 1999 Apr;70(4):370-4. doi: 10.1902/jop.1999.70.4.370. PMID: 10328647.
  21. Kang JH, Kim YY, Chang JY, Kho HS. Influences of hyaluronic acid on the anticandidal activities of lysozyme and the peroxidase system. Oral Dis. 2011 Sep;17(6):577-83. doi: 10.1111/j.1601-0825.2011.01807.x. Epub 2011 Apr 8. PMID: 21477181.
  22. Sasaki T, Watanabe C. Stimulation of osteoinduction in bone wound healing by high-molecular hyaluronic acid. Bone. 1995 Jan;16(1):9-15. doi: 10.1016/s8756-3282(94)00001-8. PMID: 7742090.
  23. Dahiya P, Kamal R. Hyaluronic Acid: a boon in periodontal therapy. N Am J Med Sci. 2013 May;5(5):309-15. doi: 10.4103/1947-2714.112473. PMID: 23814761; PMCID: PMC3690787.
  24. de Brito Bezerra B, Mendes Brazão MA, de Campos ML, Casati MZ, Sallum EA, Sallum AW. Association of hyaluronic acid with a collagen scaffold may improve bone healing in critical-size bone defects. Clin Oral Implants Res. 2012 Aug;23(8):938-42. doi: 10.1111/j.1600-0501.2011.02234.x. Epub 2011 Jun 21. PMID: 21689163.
  25. Kawano M, Ariyoshi W, Iwanaga K, Okinaga T, Habu M, Yoshioka I, Tominaga K, Nishihara T. Mechanism involved in enhancement of osteoblast differentiation by hyaluronic acid. Biochem Biophys Res Commun. 2011 Feb 25;405(4):575-80. doi: 10.1016/j.bbrc.2011.01.071. Epub 2011 Jan 23. PMID: 21266161.
  26. Mendes RM, Silva GA, Lima MF, Calliari MV, Almeida AP, Alves JB, Ferreira AJ. Sodium hyaluronate accelerates the healing process in tooth sockets of rats. Arch Oral Biol. 2008 Dec;53(12):1155-62. doi: 10.1016/j.archoralbio.2008.07.001. Epub 2008 Aug 9. PMID: 18692778.
  27. Deed R, Rooney P, Kumar P, Norton JD, Smith J, Freemont AJ, Kumar S. Early-response gene signalling is induced by angiogenic oligosaccharides of hyaluronan in endothelial cells. Inhibition by non-angiogenic, high-molecular-weight hyaluronan. Int J Cancer. 1997 Apr 10;71(2):251-6. doi: 10.1002/(sici)1097-0215(19970410)71:2<251::aid-ijc21>3.0.co;2-j. PMID: 9139851.
  28. Schwarz F, Sager M, Rothamel D, Herten M, Sculean A, Becker J. Einsatz nativer und quervernetzter Kollagenmembranen für die gesteuerte Gewebe- und Knochenregeneration [Use of native and cross-linked collagen membranes for guided tissue and bone regeneration]. Schweiz Monatsschr Zahnmed. 2006;116(11):1112-23. German. PMID: 17144624.
  29. Sanz-Sánchez I, Ortiz-Vigón A, Sanz-Martín I, Figuero E, Sanz M. Effectiveness of Lateral Bone Augmentation on the Alveolar Crest Dimension: A Systematic Review and Meta-analysis. J Dent Res. 2015 Sep;94(9 Suppl):128S-42S. doi: 10.1177/0022034515594780. Epub 2015 Jul 27. PMID: 26215467.
  30. Oryan A, Moshiri A, Meimandi Parizi AH, Raayat Jahromi A. Repeated administration of exogenous Sodium-hyaluronate improved tendon healing in an in vivo transection model. J Tissue Viability. 2012 Aug;21(3):88-102. doi: 10.1016/j.jtv.2012.06.002. Epub 2012 Jul 4. PMID: 22766020.
  31. Tuncay I, Ozbek H, Atik B, Ozen S, Akpinar F. Effects of hyaluronic acid on postoperative adhesion of tendo calcaneus surgery: an experimental study in rats. J Foot Ankle Surg. 2002 Mar-Apr;41(2):104-8. doi: 10.1016/s1067-2516(02)80033-3. PMID: 11995830.
  32. King SR, Hickerson WL, Proctor KG. Beneficial actions of exogenous hyaluronic acid on wound healing. Surgery. 1991 Jan;109(1):76-84. PMID: 1984639.
  33. Pilloni A, Schmidlin PR, Sahrmann P, Sculean A, Rojas MA. Correction to: Effectiveness of adjunctive hyaluronic acid application in coronally advanced flap in Miller class I single gingival recession sites: a randomized controlled clinical trial. Clin Oral Investig. 2018 Nov;22(8):2961-2962. doi: 10.1007/s00784-018-2567-y. Erratum for: Clin Oral Investig. 2018 Jun 30;: PMID: 30027355.
  34. Yıldırım S, Özener HÖ, Doğan B, Kuru B. Effect of topically applied hyaluronic acid on pain and palatal epithelial wound healing: An examiner-masked, randomized, controlled clinical trial. J Periodontol. 2018 Jan;89(1):36-45. doi: 10.1902/jop.2017.170105. PMID: 28914592.
  35. Humbert P, Mikosinki J, Benchikhi H, Allaert FA. Efficacy and safety of a gauze pad containing hyaluronic acid in treatment of leg ulcers of venous or mixed origin: a double-blind, randomised, controlled trial. Int Wound J. 2013 Apr;10(2):159-66. doi: 10.1111/j.1742-481X.2012.00957.x. Epub 2012 Mar 8. PMID: 22405094; PMCID: PMC7950449.
  36. Juhász I, Zoltán P, Erdei I. Treatment of partial thickness burns with Zn-hyaluronan: lessons of a clinical pilot study. Ann Burns Fire Disasters. 2012 Jun 30;25(2):82-5. PMID: 23233826; PMCID: PMC3506212.
  37. Rajan P, Dusanapudi LN, Kumar CS, Nair D. Hyaluronic acid - a simple, unusual polysaccharide: A potential mediator for periodontal regeneration. Universal Research Journal of Dentistry. 2013;3:113.
  38. Mertens C, Braun S, Krisam J, Hoffmann J. The influence of wound closure on graft stability: An in vitro comparison of different bone grafting techniques for the treatment of one-wall horizontal bone defects. Clin Implant Dent Relat Res. 2019 Apr;21(2):284-291. doi: 10.1111/cid.12728. Epub 2019 Feb 11. PMID: 30741470.
  39. Mir-Mari J, Wui H, Jung RE, Hämmerle CH, Benic GI. Influence of blinded wound closure on the volume stability of different GBR materials: an in vitro cone-beam computed tomographic examination. Clin Oral Implants Res. 2016 Feb;27(2):258-65. doi: 10.1111/clr.12590. Epub 2015 Apr 9. PMID: 25856209.
  40. Meijndert L, Raghoebar GM, Meijer HJ, Vissink A. Clinical and radiographic characteristics of single-tooth replacements preceded by local ridge augmentation: a prospective randomized clinical trial. Clin Oral Implants Res. 2008 Dec;19(12):1295-303. doi: 10.1111/j.1600-0501.2008.01523.x. PMID: 19040446.
  41. Hämmerle CH, Jung RE, Yaman D, Lang NP. Ridge augmentation by applying bioresorbable membranes and deproteinized bovine bone mineral: a report of twelve consecutive cases. Clin Oral Implants Res. 2008 Jan;19(1):19-25. doi: 10.1111/j.1600-0501.2007.01407.x. Epub 2007 Oct 22. PMID: 17956571.
  42. Asparuhova MB, Kiryak D, Eliezer M, Mihov D, Sculean A. Activity of two hyaluronan preparations on primary human oral fibroblasts. J Periodontal Res. 2019 Feb;54(1):33-45. doi: 10.1111/jre.12602. Epub 2018 Sep 27. PMID: 30264516; PMCID: PMC6586051.
  43. Mueller A, Fujioka-Kobayashi M, Mueller HD, Lussi A, Sculean A, Schmidlin PR, Miron RJ. Effect of hyaluronic acid on morphological changes to dentin surfaces and subsequent effect on periodontal ligament cell survival, attachment, and spreading. Clin Oral Investig. 2017 May;21(4):1013-1019. doi: 10.1007/s00784-016-1856-6. Epub 2016 May 19. PMID: 27194052.
  44. Prince CW. Roles of hyaluronan in bone resorption. BMC Musculoskelet Disord. 2004 Apr 29;5:12. doi: 10.1186/1471-2474-5-12. PMID: 15117412; PMCID: PMC411043.
  45. Asparuhova MB, Chappuis V, Stähli A, Buser D, Sculean A. Role of hyaluronan in regulating self-renewal and osteogenic differentiation of mesenchymal stromal cells and pre-osteoblasts. Clin Oral Investig. 2020 Nov;24(11):3923-3937. doi: 10.1007/s00784-020-03259-8. Epub 2020 Mar 31. PMID: 32236725; PMCID: PMC7544712.
  46. Kim JJ, Song HY, Ben Amara H, Kyung-Rim K, Koo KT. Hyaluronic Acid Improves Bone Formation in Extraction Sockets With Chronic Pathology: A Pilot Study in Dogs. J Periodontol. 2016 Jul;87(7):790-5. doi: 10.1902/jop.2016.150707. Epub 2016 Mar 18. PMID: 26991484.
  47. Alcântara CEP, Castro MAA, Noronha MS, Martins-Junior PA, Mendes RM, Caliari MV, Mesquita RA, Ferreira AJ. Hyaluronic acid accelerates bone repair in human dental sockets: a randomized triple-blind clinical trial. Braz Oral Res. 2018;32:e84. doi: 10.1590/1807-3107bor-2018.vol32.0084. Epub 2018 Sep 13. PMID: 30231173.
  48. Stiller M, Kluk E, Bohner M, Lopez-Heredia MA, Müller-Mai C, Knabe C. Performance of β-tricalcium phosphate granules and putty, bone grafting materials after bilateral sinus floor augmentation in humans. Biomaterials. 2014 Mar;35(10):3154-63. doi: 10.1016/j.biomaterials.2013.12.068. Epub 2014 Jan 16. PMID: 24439419.
  49. Danesh-Sani SA, Engebretson SP, Janal MN. Histomorphometric results of different grafting materials and effect of healing time on bone maturation after sinus floor augmentation: a systematic review and meta-analysis. J Periodontal Res. 2017 Jun;52(3):301-312. doi: 10.1111/jre.12402. Epub 2016 Aug 18. PMID: 27534916.
  50. Urban IA, Montero E, Monje A, Sanz-Sánchez I. Effectiveness of vertical ridge augmentation interventions: A systematic review and meta-analysis. J Clin Periodontol. 2019 Jun;46 Suppl 21:319-339. doi: 10.1111/jcpe.13061. PMID: 30667522.
  51. Kivovics M, Szabó BT, Németh O, Iványi D, Trimmel B, Szmirnova I, Orhan K, Mijiritsky E, Szabó G, Dobó-Nagy C. Comparison between Micro-Computed Tomography and Cone-Beam Computed Tomography in the Assessment of Bone Quality and a Long-Term Volumetric Study of the Augmented Sinus Grafted with an Albumin Impregnated Allograft. J Clin Med. 2020 Jan 21;9(2):303. doi: 10.3390/jcm9020303. PMID: 31973237; PMCID: PMC7073646.
  52. Friedmann A, Fickl S, Fischer KR, Dalloul M, Goetz W, Kauffmann F. Horizontal Augmentation of Chronic Mandibular Defects by the Guided Bone Regeneration Approach: A Randomized Study in Dogs. Materials (Basel). 2021 Dec 29;15(1):238. doi: 10.3390/ma15010238. PMID: 35009383; PMCID: PMC8746186.
Publish with JBRES — Peer-reviewed, multidisciplinary Open Access with rapid review, DOI, and global visibility.
Double-Blind CrossRef DOI Discoverable
Submit Manuscript Membership