Skip to main content
Top
Published in: International Journal of Implant Dentistry 1/2019

Open Access 01-12-2019 | Growth Factors | Research

Effect of platelet-rich and platelet-poor plasma on peri-implant innervation in dog mandibles

Authors: Dandan Song, Yan Huang, Jeroen Van Dessel, Sohaib Shujaat, Kaan Orhan, Tim Vangansewinkel, Kathleen Van den Eynde, Ivo Lambrichts, Tania Roskams, Constantinus Politis, Reinhilde Jacobs

Published in: International Journal of Implant Dentistry | Issue 1/2019

Login to get access

Abstract

Background

Autologous plasma fractions, such as platelet-rich plasma (PRP) and platelet-poor plasma (PPP), contain growth factors that can enhance neural cell survival and are therefore likely to have the ability to promote nerve regeneration. The present study compared the effect of PRP and PPP application on myelinated nerve density and diameter in the peri-implant bone region. In addition, the effect of healing time on nerve regeneration was assessed.

Materials and methods

Nine beagle dogs randomly received 54 dental implants in the bilateral mandible according to a split-mouth design. Each implant was randomly assigned to one of three implant protocols: delayed implant placement with delayed loading (DIP + DL) with local application of PRP, DIP + DL with local application of PPP and DIP + DL without any plasma additive. The animals were euthanized at 1, 3, and 6 months after loading (3 dogs per time point). Block biopsies were prepared for histomorphometry in the peri-implant bone within 500 μm around the implants.

Results

Myelinated nerve fibers were identified in the trabecular bone and in the osteons near the implants surface. The nerve fibers in the PRP group (median ± IQR; 2.88 ± 1.55 μm) had a significantly (p < 0.05) greater diameter compared to the PPP (2.40 ± 0.91 μm) and control (2.11 ± 1.16 μm) group. The nerve diameter after 6 months healing (3.18 ± 1.58 μm) was significantly (p < 0.05) greater compared to 1 (2.08 ± 0.89 μm) and 3 (2.49 ± 1.22 μm) months. No significant difference was found for myelinated nerve density between groups and healing time.

Conclusions

The present study showed that the healing time significantly influenced the diameter of the myelinated nerve fibers in peri-implant bone. PRP exerted a significant effect on the diameter of the myelinated nerve fibers as compared to PPP. Large-scale animal studies and longer follow-up periods are needed to confirm these findings and to verify whether platelet plasma can facilitate nerve regeneration process.
Literature
1.
go back to reference Gallucci GO, Hamilton A, Zhou W, Buser D, Chen S. Implant placement and loading protocols in partially edentulous patients: A systematic review. Clin Oral Implants Res. 2018;29:106–34.PubMedCrossRef Gallucci GO, Hamilton A, Zhou W, Buser D, Chen S. Implant placement and loading protocols in partially edentulous patients: A systematic review. Clin Oral Implants Res. 2018;29:106–34.PubMedCrossRef
2.
go back to reference Pietrokovski J, Kaffe I, Arensburg B. Retromolar ridge in edentulous patients: clinical considerations. J Prosthodont. 2007;16(6):502–6.PubMedCrossRef Pietrokovski J, Kaffe I, Arensburg B. Retromolar ridge in edentulous patients: clinical considerations. J Prosthodont. 2007;16(6):502–6.PubMedCrossRef
3.
go back to reference Hughes FJ. Chapter 34 - Periodontium and Periodontal Disease. In: Vishwakarma A, Sharpe P, Shi S, Ramalingam M, editors. Stem Cell Biology and Tissue Engineering in Dental Sciences. Boston: Academic Press; 2015. p. 433–44.CrossRef Hughes FJ. Chapter 34 - Periodontium and Periodontal Disease. In: Vishwakarma A, Sharpe P, Shi S, Ramalingam M, editors. Stem Cell Biology and Tissue Engineering in Dental Sciences. Boston: Academic Press; 2015. p. 433–44.CrossRef
4.
go back to reference Wadhwa S, Nanda R, Pilbeam C. Chapter 26-Mechanotransduction of Orthodontic Forces. In: Nanda R, Kapila S, editors. Current Therapy in Orthodontics. Saint Louis: Mosby; 2010. p. 339–52.CrossRef Wadhwa S, Nanda R, Pilbeam C. Chapter 26-Mechanotransduction of Orthodontic Forces. In: Nanda R, Kapila S, editors. Current Therapy in Orthodontics. Saint Louis: Mosby; 2010. p. 339–52.CrossRef
5.
go back to reference Lambrichts I, Creemers J, van Steenberghe D. Morphology of neural endings in the human periodontal ligament: an electron microscopic study. J Periodontol Res. 1992;27(3):191–6.CrossRef Lambrichts I, Creemers J, van Steenberghe D. Morphology of neural endings in the human periodontal ligament: an electron microscopic study. J Periodontol Res. 1992;27(3):191–6.CrossRef
6.
go back to reference Jacobs R, van Steenberghe D. Role of periodontal ligament receptors in the tactile function of teeth: a review. J Periodontol Res. 1994;29(3):153–67.CrossRef Jacobs R, van Steenberghe D. Role of periodontal ligament receptors in the tactile function of teeth: a review. J Periodontol Res. 1994;29(3):153–67.CrossRef
7.
go back to reference Mühlbradt L, Ulrich R, Möhlmann H, Schmid H. Mechanoperception of natural teeth versus endosseous implants revealed by magnitude estimation. Int J Oral Maxillofac Implants. 1989;4(2):125–30.PubMed Mühlbradt L, Ulrich R, Möhlmann H, Schmid H. Mechanoperception of natural teeth versus endosseous implants revealed by magnitude estimation. Int J Oral Maxillofac Implants. 1989;4(2):125–30.PubMed
8.
go back to reference Jacobs R, van Steenberghe D. Comparative evaluation of the oral tactile function bv means of teeth or implant-supported prostheses. Clin Oral Implants Res. 1991;2(2):75–80.PubMedCrossRef Jacobs R, van Steenberghe D. Comparative evaluation of the oral tactile function bv means of teeth or implant-supported prostheses. Clin Oral Implants Res. 1991;2(2):75–80.PubMedCrossRef
9.
go back to reference Jacobs R, van Steenberghe D. Comparison between implant-supported prostheses and teeth regarding passive threshold level. Int J Oral Maxillofac Implants. 1993;8(5):549–54.PubMed Jacobs R, van Steenberghe D. Comparison between implant-supported prostheses and teeth regarding passive threshold level. Int J Oral Maxillofac Implants. 1993;8(5):549–54.PubMed
10.
go back to reference Hämmerle CH, Wagner D, Brägger U, Lussi A, Karayiannis A, Joss A, et al. Threshold of tactile sensitivity perceived with dental endosseous implants and natural teeth. Clin Oral Implants Res. 1995;6(2):83–90.PubMedCrossRef Hämmerle CH, Wagner D, Brägger U, Lussi A, Karayiannis A, Joss A, et al. Threshold of tactile sensitivity perceived with dental endosseous implants and natural teeth. Clin Oral Implants Res. 1995;6(2):83–90.PubMedCrossRef
11.
12.
go back to reference Jacobs R, van Steenberghe D. From osseoperception to implant-mediated sensory-motor interactions and related clinical implications. J Oral Rehabil. 2006;33(4):282–92.PubMedCrossRef Jacobs R, van Steenberghe D. From osseoperception to implant-mediated sensory-motor interactions and related clinical implications. J Oral Rehabil. 2006;33(4):282–92.PubMedCrossRef
13.
go back to reference Van Loven K, Jacobs R, Swinnen A, Van Huffel S, Van Hees J, Van Steenberghe D. Sensations and trigeminal somatosensory-evoked potentials elicited by electrical stimulation of endosseous oral implants in humans. Arch Oral Biol. 2000;45(12):1083–90.PubMedCrossRef Van Loven K, Jacobs R, Swinnen A, Van Huffel S, Van Hees J, Van Steenberghe D. Sensations and trigeminal somatosensory-evoked potentials elicited by electrical stimulation of endosseous oral implants in humans. Arch Oral Biol. 2000;45(12):1083–90.PubMedCrossRef
14.
go back to reference Wang Y-HKT, Ando H, Nakanishi E, Yoshizawa H, Zhang M, Fukuyama H, Wada S, Uchida Y. Nerve regeneration after implantation in peri-implant area. A histological study on different implant materials in dogs. Osseoperception. In: Jacobs R. (editor) Osseoperception. Leuven. 1998. p.3-11. Wang Y-HKT, Ando H, Nakanishi E, Yoshizawa H, Zhang M, Fukuyama H, Wada S, Uchida Y. Nerve regeneration after implantation in peri-implant area. A histological study on different implant materials in dogs. Osseoperception. In: Jacobs R. (editor) Osseoperception. Leuven. 1998. p.3-11.
15.
go back to reference Lambrichts I. Histological and ultrastructural aspects of bone innervation. In: Jacobs R. (editor) Osseoperception. Leuven. 1998. p.13-20 Lambrichts I. Histological and ultrastructural aspects of bone innervation. In: Jacobs R. (editor) Osseoperception. Leuven. 1998. p.13-20
16.
go back to reference Corpas LD, Lambrichts I, Quirynen M, Collaert B, Politis C, Vrielinck L, et al. Peri-implant bone innervation: Histological findings in humans. Eur J Oral Implantol. 2014;7(3):283–92. Corpas LD, Lambrichts I, Quirynen M, Collaert B, Politis C, Vrielinck L, et al. Peri-implant bone innervation: Histological findings in humans. Eur J Oral Implantol. 2014;7(3):283–92.
17.
go back to reference Choi B-H. Periodontal ligament formation around titanium implants using cultured periodontal ligament cells: a pilot study. Int J of Oral Maxillofac Implants. 2000;15(2). Choi B-H. Periodontal ligament formation around titanium implants using cultured periodontal ligament cells: a pilot study. Int J of Oral Maxillofac Implants. 2000;15(2).
18.
go back to reference Yuan Q, Gong P, Tan Z. Schwann cell graft: a method to promote sensory responses of osseointegrated implants. Med Hypotheses. 2007;69(4):800–3.PubMedCrossRef Yuan Q, Gong P, Tan Z. Schwann cell graft: a method to promote sensory responses of osseointegrated implants. Med Hypotheses. 2007;69(4):800–3.PubMedCrossRef
19.
go back to reference Ma L, Xiang L, Yao Y, Yuan Q, Li L, Gong P. CGRP-alpha application: a potential treatment to improve osseoperception of endosseous dental implants. Med Hypotheses. 2013;81(2):297–9.PubMedCrossRef Ma L, Xiang L, Yao Y, Yuan Q, Li L, Gong P. CGRP-alpha application: a potential treatment to improve osseoperception of endosseous dental implants. Med Hypotheses. 2013;81(2):297–9.PubMedCrossRef
20.
go back to reference Huang Y, Jacobs R, Van Dessel J, Bornstein MM, Lambrichts I, Politis C. A systematic review on the innervation of peri-implant tissues with special emphasis on the influence of implant placement and loading protocols. Clin Oral Implants Res. 2015;26(7):737–46.PubMedCrossRef Huang Y, Jacobs R, Van Dessel J, Bornstein MM, Lambrichts I, Politis C. A systematic review on the innervation of peri-implant tissues with special emphasis on the influence of implant placement and loading protocols. Clin Oral Implants Res. 2015;26(7):737–46.PubMedCrossRef
21.
go back to reference Martínez CE, González SA, Palma V, Smith PC. Platelet-poor and platelet-rich plasma stimulate bone lineage differentiation in periodontal ligament stem cells. J Periodontol. 2016;87(2):e18–26.PubMedCrossRef Martínez CE, González SA, Palma V, Smith PC. Platelet-poor and platelet-rich plasma stimulate bone lineage differentiation in periodontal ligament stem cells. J Periodontol. 2016;87(2):e18–26.PubMedCrossRef
22.
go back to reference Shahidi M, Vatanmakanian M, Arami MK, Shirazi FS, Esmaeili N, Hydarporian S, et al. A comparative study between platelet-rich plasma and platelet-poor plasma effects on angiogenesis. Med Mol Morphol. 2018;51(1):21–31.PubMedCrossRef Shahidi M, Vatanmakanian M, Arami MK, Shirazi FS, Esmaeili N, Hydarporian S, et al. A comparative study between platelet-rich plasma and platelet-poor plasma effects on angiogenesis. Med Mol Morphol. 2018;51(1):21–31.PubMedCrossRef
23.
go back to reference Zheng C, Zhu Q, Liu X, Huang X, He C, Jiang L, et al. Improved peripheral nerve regeneration using acellular nerve allografts loaded with platelet-rich plasma. Tissue Eng. Part A. 2014;20(23-24):3228–40.PubMedPubMedCentralCrossRef Zheng C, Zhu Q, Liu X, Huang X, He C, Jiang L, et al. Improved peripheral nerve regeneration using acellular nerve allografts loaded with platelet-rich plasma. Tissue Eng. Part A. 2014;20(23-24):3228–40.PubMedPubMedCentralCrossRef
24.
go back to reference Dhurat R, Sukesh M. Principles and methods of preparation of platelet-rich plasma: a review and author's perspective. J Cutan Aesthet Surg. 2014;7(4):189.PubMedPubMedCentralCrossRef Dhurat R, Sukesh M. Principles and methods of preparation of platelet-rich plasma: a review and author's perspective. J Cutan Aesthet Surg. 2014;7(4):189.PubMedPubMedCentralCrossRef
25.
go back to reference Huang Y, van Dessel J, Martens W, Lambrichts I, Zhong WJ, Ma GW, et al. Sensory innervation around immediately vs. delayed loaded implants: a pilot study. Int J Oral Sci. 2015;7(1):49–55.PubMedCrossRef Huang Y, van Dessel J, Martens W, Lambrichts I, Zhong WJ, Ma GW, et al. Sensory innervation around immediately vs. delayed loaded implants: a pilot study. Int J Oral Sci. 2015;7(1):49–55.PubMedCrossRef
26.
go back to reference Faul F, Erdfelder E, Lang A-G, Buchner A. G* Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–91.PubMedCrossRef Faul F, Erdfelder E, Lang A-G, Buchner A. G* Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39(2):175–91.PubMedCrossRef
27.
go back to reference Lee JW, Kwon OH, Kim TK, Cho YK, Choi KY, Chung HY, et al. Platelet-rich plasma: quantitative assessment of growth factor levels and comparative analysis of activated and inactivated groups. Arch Plast Surg. 2013;40(5):530.PubMedPubMedCentralCrossRef Lee JW, Kwon OH, Kim TK, Cho YK, Choi KY, Chung HY, et al. Platelet-rich plasma: quantitative assessment of growth factor levels and comparative analysis of activated and inactivated groups. Arch Plast Surg. 2013;40(5):530.PubMedPubMedCentralCrossRef
28.
go back to reference Huang Y, Corpas LS, Martens W, Jacobs R, Lambrichts I. Histomorphological study of myelinated nerve fibres in the periodontal ligament of human canine. Acta Odontol Scand. 2011;69(5):279–86.PubMedCrossRef Huang Y, Corpas LS, Martens W, Jacobs R, Lambrichts I. Histomorphological study of myelinated nerve fibres in the periodontal ligament of human canine. Acta Odontol Scand. 2011;69(5):279–86.PubMedCrossRef
29.
go back to reference Weiner S, Klein M, Doyle JL, Brunner M. Identification of axons in the peri-implant region by immunohistochemistry. Int J of Oral Maxillofac Implants. 1995;10(6):689–95. Weiner S, Klein M, Doyle JL, Brunner M. Identification of axons in the peri-implant region by immunohistochemistry. Int J of Oral Maxillofac Implants. 1995;10(6):689–95.
30.
go back to reference Linden R, Scott B. The effect of tooth extraction on periodontal ligament mechanoreceptors represented in the mesencephalic nucleus of the cat. Arch Oral Biol. 1989;34(12):937–41.PubMedCrossRef Linden R, Scott B. The effect of tooth extraction on periodontal ligament mechanoreceptors represented in the mesencephalic nucleus of the cat. Arch Oral Biol. 1989;34(12):937–41.PubMedCrossRef
31.
go back to reference Anjayani S, Wirohadidjojo YW, Adam AM, Suwandi D, Seweng A, Amiruddin MD. Sensory improvement of leprosy peripheral neuropathy in patients treated with perineural injection of platelet-rich plasma. Int J Dermatol. 2014;53(1):109–13.PubMedCrossRef Anjayani S, Wirohadidjojo YW, Adam AM, Suwandi D, Seweng A, Amiruddin MD. Sensory improvement of leprosy peripheral neuropathy in patients treated with perineural injection of platelet-rich plasma. Int J Dermatol. 2014;53(1):109–13.PubMedCrossRef
32.
go back to reference Khojasteh A, Hosseinpour S, Nazeman P, Dehghan M. The effect of a platelet-rich fibrin conduit on neurosensory recovery following inferior alveolar nerve lateralization: a preliminary clinical study. Int J Oral Maxillofac Surg. 2016;45(10):1303–8.PubMedCrossRef Khojasteh A, Hosseinpour S, Nazeman P, Dehghan M. The effect of a platelet-rich fibrin conduit on neurosensory recovery following inferior alveolar nerve lateralization: a preliminary clinical study. Int J Oral Maxillofac Surg. 2016;45(10):1303–8.PubMedCrossRef
33.
go back to reference Whitman DH, Berry RL, Green DM. Platelet gel: an autologous alternative to fibrin glue with applications in oral and maxillofacial surgery. J of Oral Maxillofac Surg. 1997;55(11):1294–9.CrossRef Whitman DH, Berry RL, Green DM. Platelet gel: an autologous alternative to fibrin glue with applications in oral and maxillofacial surgery. J of Oral Maxillofac Surg. 1997;55(11):1294–9.CrossRef
34.
go back to reference Dolder JVD, Mooren R, Vloon AP, Stoelinga PJ, Jansen JA. Platelet-rich plasma: quantification of growth factor levels and the effect on growth and differentiation of rat bone marrow cells. Tissue Eng. 2006;12(11):3067–73.PubMedCrossRef Dolder JVD, Mooren R, Vloon AP, Stoelinga PJ, Jansen JA. Platelet-rich plasma: quantification of growth factor levels and the effect on growth and differentiation of rat bone marrow cells. Tissue Eng. 2006;12(11):3067–73.PubMedCrossRef
35.
go back to reference Wada S, Kojo T, Wang YH, Ando H, Nakanishi E, Zhang M, et al. Effect of loading on the development of nerve fibers around oral implants in the dog mandible. Clin Oral Implants Res. 2001;12(3):219–24.PubMedCrossRef Wada S, Kojo T, Wang YH, Ando H, Nakanishi E, Zhang M, et al. Effect of loading on the development of nerve fibers around oral implants in the dog mandible. Clin Oral Implants Res. 2001;12(3):219–24.PubMedCrossRef
36.
go back to reference Yamazaki T, Sabit H, Oya T, Ishii Y, Hamashima T, Tokunaga A, et al. Activation of MAP kinases, Akt and PDGF receptors in injured peripheral nerves. J Peripher Nerv Syst. 2009;14(3):165–76.PubMedCrossRef Yamazaki T, Sabit H, Oya T, Ishii Y, Hamashima T, Tokunaga A, et al. Activation of MAP kinases, Akt and PDGF receptors in injured peripheral nerves. J Peripher Nerv Syst. 2009;14(3):165–76.PubMedCrossRef
37.
go back to reference Anitua E, Sánchez M, Orive G, Andia I. Delivering growth factors for therapeutics. Trends Pharmacol Sci. 2008;29(1):37–41.PubMedCrossRef Anitua E, Sánchez M, Orive G, Andia I. Delivering growth factors for therapeutics. Trends Pharmacol Sci. 2008;29(1):37–41.PubMedCrossRef
38.
go back to reference Graziani F, Ivanovski S, Cei S, Ducci F, Tonetti M, Gabriele M. The in vitro effect of different PRP concentrations on osteoblasts and fibroblasts. Clin Oral Implants Res. 2006;17(2):212–9.PubMedCrossRef Graziani F, Ivanovski S, Cei S, Ducci F, Tonetti M, Gabriele M. The in vitro effect of different PRP concentrations on osteoblasts and fibroblasts. Clin Oral Implants Res. 2006;17(2):212–9.PubMedCrossRef
39.
go back to reference Cho HH, Jang S, Lee SC, Jeong HS, Park JS, Han JY, et al. Effect of neural-induced mesenchymal stem cells and platelet-rich plasma on facial nerve regeneration in an acute nerve injury model. The Laryngoscope. 2010;120(5):907–13.PubMed Cho HH, Jang S, Lee SC, Jeong HS, Park JS, Han JY, et al. Effect of neural-induced mesenchymal stem cells and platelet-rich plasma on facial nerve regeneration in an acute nerve injury model. The Laryngoscope. 2010;120(5):907–13.PubMed
40.
go back to reference Albanese A, Licata ME, Polizzi B, Campisi G. Platelet-rich plasma (PRP) in dental and oral surgery: from the wound healing to bone regeneration. Immun Ageing. 2013;10(1):23.PubMedPubMedCentralCrossRef Albanese A, Licata ME, Polizzi B, Campisi G. Platelet-rich plasma (PRP) in dental and oral surgery: from the wound healing to bone regeneration. Immun Ageing. 2013;10(1):23.PubMedPubMedCentralCrossRef
41.
go back to reference Tabrizi R, Pourdanesh F, Jafari S, Behnia P. Can platelet-rich fibrin accelerate neurosensory recovery following sagittal split osteotomy? A double-blind, split-mouth, randomized clinical trial. Int J Oral Surg. 2018;47(8):1011–4.CrossRef Tabrizi R, Pourdanesh F, Jafari S, Behnia P. Can platelet-rich fibrin accelerate neurosensory recovery following sagittal split osteotomy? A double-blind, split-mouth, randomized clinical trial. Int J Oral Surg. 2018;47(8):1011–4.CrossRef
42.
go back to reference Sánchez M, Anitua E, Delgado D, Sanchez P, Prado R, Orive G, et al. Platelet-rich plasma, a source of autologous growth factors and biomimetic scaffold for peripheral nerve regeneration. Expert Opin Biol Ther. 2017;17(2):197–212.PubMedCrossRef Sánchez M, Anitua E, Delgado D, Sanchez P, Prado R, Orive G, et al. Platelet-rich plasma, a source of autologous growth factors and biomimetic scaffold for peripheral nerve regeneration. Expert Opin Biol Ther. 2017;17(2):197–212.PubMedCrossRef
43.
go back to reference Sánchez M, Garate A, Bilbao AM, Oraa J, Yangüela F, Sánchez P, et al. Platelet-Rich Plasma for Injured Peripheral Nerves: Biological Repair Process and Clinical Application Guidelines. IntechOpen: Neuropathies; 2018. Sánchez M, Garate A, Bilbao AM, Oraa J, Yangüela F, Sánchez P, et al. Platelet-Rich Plasma for Injured Peripheral Nerves: Biological Repair Process and Clinical Application Guidelines. IntechOpen: Neuropathies; 2018.
44.
go back to reference Bastami F, Vares P, Khojasteh A. Healing Effects of Platelet-Rich Plasma on Peripheral Nerve Injuries. J Craniofac Surg. 2017;28(1):e49–57.PubMedCrossRef Bastami F, Vares P, Khojasteh A. Healing Effects of Platelet-Rich Plasma on Peripheral Nerve Injuries. J Craniofac Surg. 2017;28(1):e49–57.PubMedCrossRef
Metadata
Title
Effect of platelet-rich and platelet-poor plasma on peri-implant innervation in dog mandibles
Authors
Dandan Song
Yan Huang
Jeroen Van Dessel
Sohaib Shujaat
Kaan Orhan
Tim Vangansewinkel
Kathleen Van den Eynde
Ivo Lambrichts
Tania Roskams
Constantinus Politis
Reinhilde Jacobs
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Implant Dentistry / Issue 1/2019
Electronic ISSN: 2198-4034
DOI
https://doi.org/10.1186/s40729-019-0193-3

Other articles of this Issue 1/2019

International Journal of Implant Dentistry 1/2019 Go to the issue