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Clinical oral investigations
Mar 22, 2025;29 (4): 201.

Efficacy of collagenated bone substitutes for bone regeneration in two-wall-damaged extraction sockets without barrier membranes.

Seungho Jeong, Franz J Strauss, Hae Jee Shin, Jin-Young Park, Jae-Kook Cha, Jung-Seok Lee
Author Information
  1. Seungho Jeong: Department of Periodontology, Research Institute for Periodontal Regeneration, College of Dentistry, Yonsei University, 50 Yonsei-Ro, Seodaemun-Gu, Seoul, 03722, South Korea. ORCID
  2. Franz J Strauss: Clinic of Reconstructive Dentistry, Center for Dental Medicine, University of Zurich, Zurich, Switzerland. ORCID
  3. Hae Jee Shin: Department of Periodontology, Research Institute for Periodontal Regeneration, College of Dentistry, Yonsei University, 50 Yonsei-Ro, Seodaemun-Gu, Seoul, 03722, South Korea. ORCID
  4. Jin-Young Park: Department of Periodontology, Research Institute for Periodontal Regeneration, College of Dentistry, Yonsei University, 50 Yonsei-Ro, Seodaemun-Gu, Seoul, 03722, South Korea. ORCID
  5. Jae-Kook Cha: Department of Periodontology, Research Institute for Periodontal Regeneration, College of Dentistry, Yonsei University, 50 Yonsei-Ro, Seodaemun-Gu, Seoul, 03722, South Korea. ORCID
  6. Jung-Seok Lee: Department of Periodontology, Research Institute for Periodontal Regeneration, College of Dentistry, Yonsei University, 50 Yonsei-Ro, Seodaemun-Gu, Seoul, 03722, South Korea. cooldds@gmail.com. ORCID
PMID: 40119996 DOI: 10.1007/s00784-025-06281-w

Abstract

OBJECTIVES: To evaluate ridge dimensional changes following alveolar ridge augmentation in two-wall-damaged extraction sockets without a barrier membrane, using two types of collagenated bone substitutes i. cross-linked (CL-CB) and ii. non-cross-linked (NCL-CB).
MATERIALS AND METHODS: Two-wall defects were created in mandibles of seven beagle dogs and treated in three groups: (i) no grafting (control), (ii) sockets filled with NCL-CB, and (iii) sockets filled with CL-CB. No barrier membrane was used. One animal was sacrificed after 1 week of healing for tissue assessments (n = 1), and the other six were sacrificed after 8 weeks of healing for microcomputed tomography (micro-CT) and histological analyses (n = 6).
RESULTS: Compared to unextracted sites, radiographic analysis revealed that the alveolar ridge dimension decreased to 83.29 ± 24.96% in group NCL-CB, 73.46 ± 16.59% in group CL-CB and 55.41 ± 12.95% in non-grafted sites (intergroup p = 0.062). Histological analysis showed that compared to baseline values the ridge area decreased to 68.75 ± 14.20% in the non-grafted group, 79.88 ± 20.05% in the NCL-CB group and 76.10 ± 21.09% in the CL-CB group with no significant differences between the groups (p > 0.05). Qualitative histological analyses revealed significantly less mineralized tissue in both test groups, amounting to 25.28 ± 10.40% in group NCL-CB, 29.86 ± 12.04% in group CL-CB, and 67.15 ± 14.35% in non-grafted sites (intergroup p < 0.05).
CONCLUSION: The efficacy of alveolar ridge augmentation using either cross-linked or non-cross-linked collagenated bone substitutes alone might be limited in severely damaged sockets such as those with two-wall defects.
CLINICAL RELEVANCE: In situations where sockets are extensively damaged, like those with two-wall defects, relying solely on soft-type bone block substitutes without a barrier membrane may not provide sufficient bone regeneration. This study highlights the importance of considering additional regenerative strategies, such as the use of barrier membranes, to enhance clinical outcomes.

Keywords

Animal model Bone regeneration Bone substitutes Tooth extraction

References

  1. Araújo MG, Lindhe J (2005) Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol 32:212–218. https://doi.org/10.1111/j.1600-051X.2005.00642.x [DOI: 10.1111/j.1600-051X.2005.00642.x]
  2. Jonker BP, Strauss FJ, Naenni N, Jung RE, Wolvius EB, Pijpe J (2021) Early implant placement with or without alveolar ridge preservation in single tooth gaps renders similar esthetic, clinical and patient-reported outcome measures: one-year results of a randomized clinical trial. Clin Oral Implants Res 32:1041–1051. https://doi.org/10.1111/clr.13796 [DOI: 10.1111/clr.13796]
  3. Strauss FJ, Fukuba S, Naenni N, Jung R, Jonker B, Wolvius E, Pijpe J (2024) Alveolar ridge changes 1-year after early implant placement, with or without alveolar ridge preservation at single-implant sites in the aesthetic region: A secondary analysis of radiographic and profilometric outcomes from a randomized controlled trial. Clin Implant Dent Relat Res 26:356–368. https://doi.org/10.1111/cid.13297 [DOI: 10.1111/cid.13297]
  4. Jung RE, Philipp A, Annen BM, Signorelli L, Thoma DS, Hämmerle CH, Attin T, Schmidlin P (2013) Radiographic evaluation of different techniques for ridge preservation after tooth extraction: a randomized controlled clinical trial. J Clin Periodontol 40:90–98. https://doi.org/10.1111/jcpe.12027 [DOI: 10.1111/jcpe.12027]
  5. Cardaropoli G, Araújo M, Hayacibara R, Sukekava F, Lindhe J (2005) Healing of extraction sockets and surgically produced - augmented and non-augmented - defects in the alveolar ridge. An experimental study in the dog. J Clin Periodontol 32:435–440. https://doi.org/10.1111/j.1600-051X.2005.00692.x [DOI: 10.1111/j.1600-051X.2005.00692.x]
  6. Araújo MG, Sukekava F, Wennström JL, Lindhe J (2006) Tissue modeling following implant placement in fresh extraction sockets. Clin Oral Implants Res 17:615–624. https://doi.org/10.1111/j.1600-0501.2006.01317.x [DOI: 10.1111/j.1600-0501.2006.01317.x]
  7. Araújo M, Linder E, Wennström J, Lindhe J (2008) The influence of Bio-Oss Collagen on healing of an extraction socket: an experimental study in the dog. Int J Periodontics Restor Dent 28:123–135
  8. Araújo MG, Lindhe J (2009) Ridge preservation with the use of Bio-Oss collagen: a 6-month study in the dog. Clin Oral Implants Res 20:433–440. https://doi.org/10.1111/j.1600-0501.2009.01705.x [DOI: 10.1111/j.1600-0501.2009.01705.x]
  9. Araújo MG, Liljenberg B, Lindhe J (2010) Dynamics of Bio-Oss Collagen incorporation in fresh extraction wounds: an experimental study in the dog. Clin Oral Implants Res 21:55–64. https://doi.org/10.1111/j.1600-0501.2009.01854.x [DOI: 10.1111/j.1600-0501.2009.01854.x]
  10. Lindhe J, Cecchinato D, Donati M, Tomasi C, Liljenberg B (2014) Ridge preservation with the use of deproteinized bovine bone mineral. Clin Oral Implants Res 25:786–790. https://doi.org/10.1111/clr.12170 [DOI: 10.1111/clr.12170]
  11. Barootchi S, Tavelli L, Majzoub J, Stefanini M, Wang HL, Avila-Ortiz G (2023) Alveolar ridge preservation: complications and cost-effectiveness. Periodontol 2000 92:235–262. https://doi.org/10.1111/prd.12469 [DOI: 10.1111/prd.12469]
  12. Mardas N, Macbeth N, Donos N, Jung RE, Zuercher AN (2023) Is alveolar ridge preservation an overtreatment? Periodontol 2000 93:289–308. https://doi.org/10.1111/prd.12508 [DOI: 10.1111/prd.12508]
  13. Avila-Ortiz G, Chambrone L, Vignoletti F (2019) Effect of alveolar ridge preservation interventions following tooth extraction: a systematic review and meta-analysis. J Clin Periodontol 46(Suppl 21):195–223. https://doi.org/10.1111/jcpe.13057 [DOI: 10.1111/jcpe.13057]
  14. Avila-Ortiz G, Gubler M, Romero-Bustillos M, Nicholas CL, Zimmerman MB, Barwacz CA (2020) Efficacy of alveolar ridge preservation: a randomized controlled trial. J Dent Res 99:402–409. https://doi.org/10.1177/0022034520905660 [DOI: 10.1177/0022034520905660]
  15. Araujo MG, Hurzeler MB, Dias DR, Matarazzo F (2023) Minimal invasiveness in the alveolar ridge preservation, with or without concomitant implant placement. Periodontol 2000 91:65–88. https://doi.org/10.1111/prd.12441 [DOI: 10.1111/prd.12441]
  16. Koo TH, Song YW, Cha JK, Jung UW, Kim CS, Lee JS (2020) Histologic analysis following grafting of damaged extraction sockets using deproteinized bovine or porcine bone mineral: a randomized clinical trial. Clin Oral Implants Res 31:93–102. https://doi.org/10.1111/clr.13557 [DOI: 10.1111/clr.13557]
  17. Araújo MG, Dias DR, Matarazzo F (2023) Anatomical characteristics of the alveolar process and basal bone that have an effect on socket healing. Periodontol 2000 93:277–288. https://doi.org/10.1111/prd.12506 [DOI: 10.1111/prd.12506]
  18. Buser D, Urban I, Monje A, Kunrath MF, Dahlin C (2023) Guided bone regeneration in implant dentistry: basic principle, progress over 35 years, and recent research activities. Periodontol 2000 93:9–25. https://doi.org/10.1111/prd.12539 [DOI: 10.1111/prd.12539]
  19. Siawasch SAM, Yu J, Castro AB, Dhondt R, Teughels W, Temmerman A, Quirynen M (2025) Autologous platelet concentrates in alveolar ridge preservation: a systematic review with meta-analyses. Periodontol 2000 97:104–130. https://doi.org/10.1111/prd.12609 [DOI: 10.1111/prd.12609]
  20. Calciolari E, Corbella S, Gkranias N, Vigano M, Sculean A, Donos N (2023) Efficacy of biomaterials for lateral bone augmentation performed with guided bone regeneration. A network meta-analysis. Periodontol 2000 93:77–106. https://doi.org/10.1111/prd.12531 [DOI: 10.1111/prd.12531]
  21. Mizraji G, Davidzohn A, Gursoy M, Gursoy U, Shapira L, Wilensky A (2023) Membrane barriers for guided bone regeneration: an overview of available biomaterials. Periodontol 2000 93:56–76. https://doi.org/10.1111/prd.12502 [DOI: 10.1111/prd.12502]
  22. Severi M, Trombelli L, Heitz-Mayfield L, Farina R, Simonelli A (2023) Minimal invasiveness in lateral bone augmentation with simultaneous implant placement: a systematic review. Periodontol 2000 91:113–125. https://doi.org/10.1111/prd.12481 [DOI: 10.1111/prd.12481]
  23. Hämmerle CH, Karring T (1998) Guided bone regeneration at oral implant sites. Periodontol 2000 17:151–175. https://doi.org/10.1111/j.1600-0757.1998.tb00132.x [DOI: 10.1111/j.1600-0757.1998.tb00132.x]
  24. Wang HL, Boyapati L (2006) “PASS” principles for predictable bone regeneration. Implant Dent 15:8–17. https://doi.org/10.1097/01.id.0000204762.39826.0f [DOI: 10.1097/01.id.0000204762.39826.0f]
  25. Mir-Mari J, Benic GI, Valmaseda-Castellón E, Hämmerle CHF, Jung RE (2017) Influence of wound closure on the volume stability of particulate and non-particulate GBR materials: an in vitro cone-beam computed tomographic examination. Part II Clin Oral Implants Res 28:631–639. https://doi.org/10.1111/clr.12845 [DOI: 10.1111/clr.12845]
  26. Mir-Mari J, Wui H, Jung RE, Hämmerle CHF, Benic GI (2016) 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 27:258–265. https://doi.org/10.1111/clr.12590 [DOI: 10.1111/clr.12590]
  27. Zuercher AN, Mancini L, Naenni N, Thoma DS, Strauss FJ, Jung RE (2023) The L-shape technique in guided bone regeneration with simultaneous implant placement in the esthetic zone: a step-by-step protocol and a 2–14 year retrospective study. J Esthet Restor Dent 35:197–205. https://doi.org/10.1111/jerd.12965 [DOI: 10.1111/jerd.12965]
  28. Llanos AH, Sapata VM, Jung RE, Hämmerle CH, Thoma DS, César Neto JB, Pannuti CM, Romito GA (2019) Comparison between two bone substitutes for alveolar ridge preservation after tooth extraction: cone-beam computed tomography results of a non-inferiority randomized controlled trial. J Clin Periodontol 46:373–381. https://doi.org/10.1111/jcpe.13079 [DOI: 10.1111/jcpe.13079]
  29. Park JY, Hong KJ, Ko KA, Cha JK, Gruber R, Lee JS (2023) Platelet-rich fibrin combined with a particulate bone substitute versus guided bone regeneration in the damaged extraction socket: an in vivo study. J Clin Periodontol 50:358–367. https://doi.org/10.1111/jcpe.13742 [DOI: 10.1111/jcpe.13742]
  30. Tien HK, Lee WH, Kim CS, Choi SH, Gruber R, Lee JS (2021) Alveolar ridge regeneration in two-wall-damaged extraction sockets of an in vivo experimental model. Clin Oral Implants Res 32:971–979. https://doi.org/10.1111/clr.13791 [DOI: 10.1111/clr.13791]
  31. Lee JS, Choe SH, Cha JK, Seo GY, Kim CS (2018) Radiographic and histologic observations of sequential healing processes following ridge augmentation after tooth extraction in buccal-bone-deficient extraction sockets in beagle dogs. J Clin Periodontol 45:1388–1397. https://doi.org/10.1111/jcpe.13014 [DOI: 10.1111/jcpe.13014]
  32. Percie du Sert N, Ahluwalia A, Alam S et al (2020) Reporting animal research: explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biol 18:e3000411. https://doi.org/10.1371/journal.pbio.3000411 [DOI: 10.1371/journal.pbio.3000411]
  33. Percie du Sert N, Hurst V, Ahluwalia A et al (2020) The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol 18:e3000410. https://doi.org/10.1371/journal.pbio.3000410 [DOI: 10.1371/journal.pbio.3000410]
  34. Schenk RK, Buser D, Hardwick WR, Dahlin C (1994) Healing pattern of bone regeneration in membrane-protected defects: a histologic study in the canine mandible. Int J Oral Maxillofac Implants 9:13–29 [PMID: 8150509]
  35. Hong JY, Lee JS, Pang EK, Jung UW, Choi SH, Kim CK (2014) Impact of different synthetic bone fillers on healing of extraction sockets: an experimental study in dogs. Clin Oral Implants Res 25:e30–37. https://doi.org/10.1111/clr.12041 [DOI: 10.1111/clr.12041]
  36. Rothamel D, Schwarz F, Sager M, Herten M, Sculean A, Becker J (2005) Biodegradation of differently cross-linked collagen membranes: an experimental study in the rat. Clin Oral Implants Res 16:369–378. https://doi.org/10.1111/j.1600-0501.2005.01108.x [DOI: 10.1111/j.1600-0501.2005.01108.x]
  37. Naenni N, Lim HC, Strauss FJ, Jung RE, Hämmerle CHF, Thoma DS (2020) Local tissue effects of various barrier membranes in a rat subcutaneous model. J Periodontal Implant Sci 50:327–339. https://doi.org/10.5051/jpis.2000380019 [DOI: 10.5051/jpis.2000380019]
  38. Tal H, Kozlovsky A, Artzi Z, Nemcovsky CE, Moses O (2008) Long-term bio-degradation of cross-linked and non-cross-linked collagen barriers in human guided bone regeneration. Clin Oral Implants Res 19:295–302. https://doi.org/10.1111/j.1600-0501.2007.01424.x [DOI: 10.1111/j.1600-0501.2007.01424.x]
  39. Lee JH, Lee JS, Baek WS, Lim HC, Cha JK, Choi SH, Jung UW (2015) Assessment of dehydrothermally cross-linked collagen membrane for guided bone regeneration around peri-implant dehiscence defects: a randomized single-blinded clinical trial. J Periodontal Implant Sci 45:229–237. https://doi.org/10.5051/jpis.2015.45.6.229 [DOI: 10.5051/jpis.2015.45.6.229]
  40. Lee JS, Cha JK, Kim CS (2018) Alveolar ridge regeneration of damaged extraction sockets using deproteinized porcine versus bovine bone minerals: a randomized clinical trial. Clin Implant Dent Relat Res 20:729–737. https://doi.org/10.1111/cid.12628 [DOI: 10.1111/cid.12628]
  41. Benic GI, Thoma DS, Muñoz F, Sanz Martin I, Jung RE, Hämmerle CH (2016) Guided bone regeneration of peri-implant defects with particulated and block xenogenic bone substitutes. Clin Oral Implants Res 27:567–576. https://doi.org/10.1111/clr.12625 [DOI: 10.1111/clr.12625]
  42. Kim C-S, Choi S-H, Chai J-K, Cho K-S, Moon I-S, Wikesjö UME, Kim C-K (2004) Periodontal repair in surgically created intrabony defects in dogs: influence of the number of bone walls on healing response. J Periodontol 75:229–235. https://doi.org/10.1902/jop.2004.75.2.229 [DOI: 10.1902/jop.2004.75.2.229]
  43. Jovanovic SA, Hunt DR, Bernard GW, Spiekermann H, Wozney JM, Wikesjö UM (2007) Bone reconstruction following implantation of rhBMP-2 and guided bone regeneration in canine alveolar ridge defects. Clin Oral Implants Res 18:224–230. https://doi.org/10.1111/j.1600-0501.2006.01324.x [DOI: 10.1111/j.1600-0501.2006.01324.x]
  44. Kaushal S, Kumar A, Khan MA, Lal N (2016) Comparative study of nonabsorbable and absorbable barrier membranes in periodontal osseous defects by guided tissue regeneration. J Oral Biol Craniofac Res 6:111–117. https://doi.org/10.1016/j.jobcr.2015.12.001 [DOI: 10.1016/j.jobcr.2015.12.001]
  45. Hämmerle CH, Schmid J, Lang NP, Olah AJ (1995) Temporal dynamics of healing in rabbit cranial defects using guided bone regeneration. J Oral Maxillofac Surg 53:167–174. https://doi.org/10.1016/0278-2391(95)90396-8 [DOI: 10.1016/0278-2391(95)90396-8]
  46. Shin HJ, Park JY, Tien HK, Strauss FJ, Cha JK, Lee JS (2024) In vivo experimental study comparing alveolar ridge preservation versus guided bone regeneration after unassisted socket healing at intact and damaged sites in narrow alveolar ridges. J Periodontol. https://doi.org/10.1002/jper.24-0125

MeSH Term

Animals
Dogs
Tooth Socket
Bone Regeneration
X-Ray Microtomography
Alveolar Ridge Augmentation
Bone Substitutes
Collagen
Mandible
Tooth Extraction
Wound Healing

Chemicals

Bone Substitutes
Collagen
Journal Article

Word Cloud

Created with Highcharts 10.0.0groupsocketsboneridgebarriersubstitutesCL-CBNCL-CBalveolarextractionwithoutmembranecollagenateddefectssitesnon-graftedregenerationaugmentationtwo-wall-damagedusingcross-linkediinon-cross-linkedfilledsacrificedhealingtissuehistologicalanalysesanalysisrevealeddecreasedintergroupgroups05damagedtwo-wallmembranesBoneOBJECTIVES:evaluatedimensionalchangesfollowingtwotypesMATERIALSANDMETHODS:Two-wallcreatedmandiblessevenbeagledogstreatedthreegroups:graftingcontroliiiusedOneanimal1 weekassessmentsn = 1six8 weeksmicrocomputedtomographymicro-CTn = 6RESULTS:Comparedunextractedradiographicdimension8329 ± 2496%7346 ± 1659%5541 ± 1295%p = 0062Histologicalshowedcomparedbaselinevaluesarea6875 ± 1420%7988 ± 2005%7610 ± 2109%significantdifferencesp > 0Qualitativesignificantlylessmineralizedtestamounting2528 ± 1040%2986 ± 1204%6715 ± 1435%p < 0CONCLUSION:efficacyeitheralonemightlimitedseverelyCLINICALRELEVANCE:situationsextensivelylikerelyingsolelysoft-typeblockmayprovidesufficientstudyhighlightsimportanceconsideringadditionalregenerativestrategiesuseenhanceclinicaloutcomesEfficacyAnimalmodelTooth

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