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Multi-modular bone healing assessment in a randomized controlled clinical trial of root-end surgery with the use of leukocyte- and platelet-rich fibrin and an occlusive membrane

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Abstract

Objectives

The aim of this study was to assess in a multi-modular manner the bone healing 1 year post root-end surgery (RES) with leukocyte- and platelet-rich fibrin (LPRF) and Bio-Gide® (BG; Geistlich Pharma North America, Inc., Princeton, USA) as an occlusive membrane.

Materials and methods

A randomized controlled clinical trial (RCT) of RES +/− LPRF and +/− BG was performed. The follow-up until 1 year post RES was performed by means of ultrasound imaging (UI), periapical radiographs (PR), and cone-beam computed tomography (CBCT).

Results

From the 50 included patients, 6 dropped-out during follow-up. For the 44 assessed patients (34 with UI and 42 with PR and CBCT), there was no evidence (p > 0.05) for an effect of LRPF, neither on UI measurements nor on CBCT assessments. On the contrary, there was an indication for a better outcome with BG. UI presented significant shorter healing time for the bony crypt surface (p = 0.014) and cortical opening (p = 0.006) for the groups with BG. The qualitative CBCT assessment for the combined scores of the apical area and cortical plane was significantly higher for BG (p = 0.01 and 0.02). The quantitative CBCT measurement for bone healing after 1 year was lower with BG (p = 0.019), as well as the percentage of non-zero values (p = 0.026), irrespective of the preoperative lesion size and type. Furthermore, UI seemed to be safer for frequent follow-up during the early postoperative stage (0–3 months), whereas CBCT gave more accurate results 1 year post RES. Amongst the assessors, the qualitative PR analysis was inconsistent for a favorable outcome 1 year post RES with LPRF (p = 0.11 and p = 0.023), but consistent for BG (p = 0.024 and p = 0.023).

Conclusions

There was no evidence for improvement of bone healing when RES was applied with LPRF in comparison with RES without LPRF. However, RES with BG gave evidence for a better outcome than RES without BG.

Clinical relevance

The addition of an occlusive membrane rather than an autologous platelet concentrate improved bone regeneration 1 year post RES significantly, irrespective of the assessment device applied. The accuracy of PR assessment is questionable.

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References

  1. Saunders WP (2008) A prospective clinical study of periradicular surgery using mineral trioxide aggregate as a root-end filling. J Endod 34(6):660–665

    Article  PubMed  Google Scholar 

  2. Wuchenich G, Meadows D, Torabinejad M (1994) A comparison between two root end preparation techniques in human cadavers. J Endod 20(6):279–282

    Article  PubMed  Google Scholar 

  3. Setzer FC, Kohli MR, Shah SB, Karabucak B, Kim S (2012) Outcome of endodontic surgery: a meta-analysis of the literature--part 2: comparison of endodontic microsurgical techniques with and without the use of higher magnification. J Endod 38(1):1–10

    Article  PubMed  Google Scholar 

  4. Setzer FC, Shah SB, Kohli MR, Karabucak B, Kim S (2010) Outcome of endodontic surgery: a meta-analysis of the literature--part 1: comparison of traditional root-end surgery and endodontic microsurgery. J Endod 36(11):1757–1765

    Article  PubMed  Google Scholar 

  5. Tsesis I, Rosen E, Tamse A, Taschieri S, Del Fabbro M (2011) Effect of guided tissue regeneration on the outcome of surgical endodontic treatment: a systematic review and meta-analysis. J Endod 37(8):1039–1045

    Article  PubMed  Google Scholar 

  6. Marx RE (2004) Platelet-rich plasma: evidence to support its use. J Oral Maxillofac Surg 62(4):489–496

    Article  PubMed  Google Scholar 

  7. Choukroun J, Adda F, Schoeffler C (2001) Une opportunité en paro-implantologie: le PRF. 42:55–62

  8. Dohan DM, Choukroun J Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part III: leucocyte activation: a new feature for platelet concentrates? Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2006(101):E51–E55

  9. Dohan DM, Choukroun J, Diss A, Dohan SL, Dohan AJ, Mouhyi J et al (2006) Platelet-rich fibrin (PRF): a second-generation platelet concentrate. Part II: platelet-related biologic features. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 101(3):e45–e50

    Article  PubMed  Google Scholar 

  10. Nyman S, Lindhe J, Karring T, Rylander H (1982) New attachment following surgical treatment of human periodontal disease. J Clin Periodontol 9(4):290–296

    Article  PubMed  Google Scholar 

  11. Nyman S, Gottlow J, Lindhe J, Karring T, Wennstrom J (1987) New attachment formation by guided tissue regeneration. J Periodontal Res 22(3):252–254

    Article  PubMed  Google Scholar 

  12. Caton JG, DeFuria EL, Polson AM, Nyman S (1987) Periodontal regeneration via selective cell repopulation. J Periodontol 58(8):546–552

    Article  PubMed  Google Scholar 

  13. Melcher AH (1976) On the repair potential of periodontal tissues. J Periodontol 47(5):256–260

    Article  PubMed  Google Scholar 

  14. Bashutski JD, Wang HL (2009) Periodontal and endodontic regeneration. J Endod 35(3):321–328

    Article  PubMed  Google Scholar 

  15. Meschi N, Castro AB, Vandamme K, Quirynen M, Lambrechts P (2016) The impact of autologous platelet concentrates on endodontic healing: a systematic review. Platelets 27(7):613–633

    Article  PubMed  Google Scholar 

  16. Meschi N, Fieuws S, Vanhoenacker A, Strijbos O, Van der Veken D, Politis C et al (2018) Root-end surgery with leucocyte- and platelet-rich fibrin and an occlusive membrane: a randomized controlled clinical trial on patients’ quality of life. Clin Oral Investig 22(6):2401–2411

    Article  PubMed  Google Scholar 

  17. Noguchi N, Noiri Y, Narimatsu M, Ebisu S (2005) Identification and localization of extraradicular biofilm-forming bacteria associated with refractory endodontic pathogens. Appl Environ Microbiol 71(12):8738–8743

    Article  PubMed  PubMed Central  Google Scholar 

  18. Ricucci D, Siqueira JF Jr, Bate AL, Pitt Ford TR (2009) Histologic investigation of root canal-treated teeth with apical periodontitis: a retrospective study from twenty-four patients. J Endod 35(4):493–502

    Article  PubMed  Google Scholar 

  19. Molven O, Halse A, Grung B (1987) Observer strategy and the radiographic classification of healing after endodontic surgery. Int J Oral Maxillofac Surg 16(4):432–439

    Article  PubMed  Google Scholar 

  20. Rud J, Andreasen JO, Jensen JE (1972) Radiographic criteria for the assessment of healing after endodontic surgery. Int J Oral Surg 1(4):195–214

    Article  PubMed  Google Scholar 

  21. von Arx T, Janner SF, Hanni S, Bornstein MM (2016) Agreement between 2D and 3D radiographic outcome assessment one year after periapical surgery. Int Endod J 49(10):915–925

    Article  Google Scholar 

  22. von Arx T, Janner SF, Hanni S, Bornstein MM (2016) Evaluation of new cone-beam computed tomographic criteria for radiographic healing evaluation after apical surgery: assessment of repeatability and reproducibility. J Endod 42(2):236–242

    Article  Google Scholar 

  23. EzEldeen M, Van Gorp G, Van Dessel J, Vandermeulen D, Jacobs R (2015) 3-dimensional analysis of regenerative endodontic treatment outcome. J Endod 41(3):317–324

    Article  PubMed  Google Scholar 

  24. Meschi N, EzEldeen M, Torres Garcia AE, Jacobs R, Lambrechts P (2018) A retrospective case series in regenerative endodontics: trend analysis based on clinical evaluation and 2- and 3-dimensional radiology. J Endod 44(10):1517–1525

    Article  PubMed  Google Scholar 

  25. Martin CJ, Sutton DG, Sharp PF (1999) Balancing patient dose and image quality. Appl Radiat Isot 50(1):1–19

    Article  PubMed  Google Scholar 

  26. Farman AG (2005) ALARA still applies. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 100(4):395–397

    Article  PubMed  Google Scholar 

  27. Cotti E, Campisi G, Ambu R, Dettori C (2003) Ultrasound real-time imaging in the differential diagnosis of periapical lesions. Int Endod J 36(8):556–563

    Article  PubMed  Google Scholar 

  28. Curvers F, Meschi N, Vanhoenacker A, Strijbos O, Van Mierlo M, Lambrechts P (2018) Ultrasound assessment of bone healing after root-end surgery: echoes back to patient’s safety. J Endod 44(1):32–37

    Article  PubMed  Google Scholar 

  29. Torabinejad M, Hong CU, McDonald F, Pitt Ford TR (1995) Physical and chemical properties of a new root-end filling material. J Endod 21(7):349–353

    Article  PubMed  Google Scholar 

  30. Torabinejad M, Parirokh M (2010) Mineral trioxide aggregate: a comprehensive literature review--part II: leakage and biocompatibility investigations. J Endod 36(2):190–202

    Article  PubMed  Google Scholar 

  31. Granlund C, Thilander-Klang A, Ylhan B, Lofthag-Hansen S, Ekestubbe A (2016) Absorbed organ and effective doses from digital intra-oral and panoramic radiography applying the ICRP 103 recommendations for effective dose estimations. Br J Radiol 89(1066):20151052

    Article  PubMed  PubMed Central  Google Scholar 

  32. Pauwels R, Zhang G, Theodorakou C, Walker A, Bosmans H, Jacobs R, Bogaerts R, Horner K, The SEDENTEXCT Project Consortium (2014) Effective radiation dose and eye lens dose in dental cone beam CT: effect of field of view and angle of rotation. Br J Radiol 87(1042):20130654

    Article  PubMed  PubMed Central  Google Scholar 

  33. Liang KY, Zeger S (2000;Series B) Longitudinal data analysis of continuous and discrete responses for pre-post designs. Sankhya: The Indian Journa of Statistics 62:134–148

  34. Ludlow JB, Peleaux CP (1994) Comparison of stent versus laser- and cephalostat-aligned periapical film-positioning techniques for use in digital subtraction radiography. Oral Surg Oral Med Oral Pathol 77(2):208–215

    Article  PubMed  Google Scholar 

  35. von Arx T, Cochran DL (2001) Rationale for the application of the GTR principle using a barrier membrane in endodontic surgery: a proposal of classification and literature review. Int J Periodontics Restorative Dent 21(2):127–139

    Google Scholar 

  36. Taschieri S, Del Fabbro M, Testori T, Weinstein R (2007) Efficacy of xenogeneic bone grafting with guided tissue regeneration in the management of bone defects after surgical endodontics. J Oral Maxillofac Surg 65(6):1121–1127

    Article  PubMed  Google Scholar 

  37. von Arx T, Alsaeed M (2011) The use of regenerative techniques in apical surgery: a literature review. Saudi Dent J 23(3):113–127

    Article  Google Scholar 

  38. Dhiman M, Kumar S, Duhan J, Sangwan P, Tewari S (2015) Effect of platelet-rich fibrin on healing of apicomarginal defects: a randomized controlled trial. J Endod 41(7):985–991

    Article  PubMed  Google Scholar 

  39. Kobayashi E, Fluckiger L, Fujioka-Kobayashi M, Sawada K, Sculean A, Schaller B et al (2016) Comparative release of growth factors from PRP, PRF, and advanced-PRF. Clin Oral Investig 20(9):2353–2360

    Article  PubMed  Google Scholar 

  40. Angerame D, De Biasi M, Kastrioti I, Franco V, Castaldo A, Maglione M (2015) Application of platelet-rich fibrin in endodontic surgery: a pilot study. G Ital Endod 29:51–57

    Article  Google Scholar 

  41. Hiremath H, Motiwala T, Jain P, Kulkarni S (2014) Use of second-generation platelet concentrate (platelet-rich fibrin) and hydroxyapatite in the management of large periapical inflammatory lesion: a computed tomography scan analysis. Indian J Dent Res 25(4):517–520

    Article  PubMed  Google Scholar 

  42. Shubhashini N, Kumar RV, Shija AS, Razvi S (2013) Platelet-rich fibrin in treatment of periapical lesions: a novel therapeutic option. Chin J Dent Res 16(1):79–82

    PubMed  Google Scholar 

  43. Singh S, Singh A, Singh R (2013) Application of PRF in surgical management of periapical lesions. Natl J Maxillofac Surg 4(1):94–99

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kapoor S, Bansal P, Chandran S, Agrawal V (2015) Surgical management of a non-healing intra-alveolar root fracture associated with pulpal calcification and root resorption: a case report. J Clin Diagn Res 9(6):Zd03–Zd05

    PubMed  PubMed Central  Google Scholar 

  45. Cortellini S, Castro AB, Temmerman A, Van Dessel J, Pinto N, Jacobs R et al (2018) Leucocyte- and platelet-rich fibrin block for bone augmentation procedure: a proof-of-concept study. J Clin Periodontol 45(5):624–634

    Article  PubMed  Google Scholar 

  46. Musu D, Rossi-Fedele G, Campisi G, Cotti E (2016) Ultrasonography in the diagnosis of bone lesions of the jaws: a systematic review. Oral Surg Oral Med Oral Pathol Oral Radiol 122(1):e19–e29

    Article  PubMed  Google Scholar 

  47. Lizio G, Salizzoni E, Coe M, Gatto MR, Asioli S, Balbi T, Pelliccioni GA (2018) Differential diagnosis between a granuloma and radicular cyst: effectiveness of magnetic resonance imaging. Int Endod J 51(10):1077–1087

    Article  PubMed  Google Scholar 

  48. Salmon B, Le Denmat D (2012) Intraoral ultrasonography: development of a specific high-frequency probe and clinical pilot study. Clin Oral Investig 16(2):643–649

    Article  PubMed  Google Scholar 

  49. Cotti E, Esposito SA, Musu D, Campisi G, Shemesh H (2018) Ultrasound examination with color power Doppler to assess the early response of apical periodontitis to the endodontic treatment. Clin Oral Investig 22(1):131–140

    Article  PubMed  Google Scholar 

  50. Zainedeen O, Al Haffar I, Kochaji N, Wassouf G (2018) The efficacy of ultrasonography in monitoring the healing of jaw lesions. Imaging science in dentistry 48(3):153–160

    Article  PubMed  PubMed Central  Google Scholar 

  51. Barnett CW, Glickman GN, Umorin M, Jalali P (2018) Interobserver and intraobserver reliability of cone-beam computed tomography in identification of apical periodontitis. J Endod 44(6):938–940

    Article  PubMed  Google Scholar 

  52. Christiansen R, Kirkevang LL, Gotfredsen E, Wenzel A (2009) Periapical radiography and cone beam computed tomography for assessment of the periapical bone defect 1 week and 12 months after root-end resection. Dentomaxillofac Radiol 38(8):531–536

    Article  PubMed  Google Scholar 

  53. Su L, Gao Y, Yu C, Wang H, Yu Q (2010) Surgical endodontic treatment of refractory periapical periodontitis with extraradicular biofilm. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 110(1):e40–e44

    Article  PubMed  Google Scholar 

  54. Ricucci D, Siqueira JF Jr, Lopes WS, Vieira AR, Rocas IN (2015) Extraradicular infection as the cause of persistent symptoms: a case series. J. Endod. 41(2):265–273

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to express our gratitude to Prof. Dr. Reinhilde Jacobs and Dr. Ruben Pauwels (KU Leuven, Leuven, Belgium) for their support in establishing the data registration of cone-beam CT scans. We are also grateful for the help of Dr. Mathieu Vandendael (CVORE, Everberg, Belgium) in referral of patients.

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Authors and Affiliations

  1. Department of Oral Health Sciences, UZ Leuven (University Hospitals Leuven), Dentistry, KU Leuven (University of Leuven), Leuven, Belgium

    Nastaran Meschi, Olaf Strijbos, Eléonore Rubbers, Valerie Peeters, Frederik Curvers, Maarten Van Mierlo, Arne Geukens & Paul Lambrechts

  2. Department of Oral Health Sciences, BIOMAT – Biomaterials Research Group, Dentistry, KU Leuven (University of Leuven), Kapucijnenvoer 7 Blok a, Box 7001, 3000, Leuven, Belgium

    Nastaran Meschi, Bernardo Camargo dos Santos & Paul Lambrechts

  3. Stomatology and Maxillofacial Surgery, UZ Leuven (University Hospitals Leuven), Dentistry, KU Leuven (University of Leuven), Leuven, Belgium

    Anke Vanhoenacker

  4. Biostatistics and Statistical Bioinformatics Centre, KU Leuven (University of Leuven), Leuven, Belgium

    Steffen Fieuws

  5. Translational Cell & Tissue Research, KU Leuven (University of Leuven), Leuven, Belgium

    Eric Verbeken

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  1. Nastaran Meschi
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Contributions

All authors contributed to the study conception and design. Dr. Anke Vanhoenacker and Dr. Olaf Strijbos performed the surgical procedures. Material preparation and data collection were performed by Dr. Nastaran Meschi. Radiographic data analysis was performed by Dr. Bernardo Camargo dos Santos, Dr. Valerie Peeters, Dr. Eleonore Rubbers, and Dr. Arne Geukens. Dr. Frederik Curvers and Maarten Van Mierlo performed the ultrasound imaging analysis. Prof. Dr. Eric Verbeken and Dr. Nastaran Meschi performed the histological analysis. The statistical analysis was performed by Dr. Steffen Fieuws. The first draft of the manuscript was written by Dr. Nastaran Meschi and critically corrected by Prof. Dr. Paul Lambrechts. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Nastaran Meschi.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Ethical approval was obtained from the Medical Ethics Committee UZ KU Leuven (KU Leuven, Leuven, Belgium; registration number: S58015/B322201525314). All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Meschi, N., Vanhoenacker, A., Strijbos, O. et al. Multi-modular bone healing assessment in a randomized controlled clinical trial of root-end surgery with the use of leukocyte- and platelet-rich fibrin and an occlusive membrane. Clin Oral Invest 24, 4439–4453 (2020). https://doi.org/10.1007/s00784-020-03309-1

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