Review Article

Intraoral Bone Regeneration Using Stem Cells-What a Clinician Needs to Know: Based on a 15-Year MEDLINE Search

Abstract

The choice of an appropriate autogenous source of stem cells has not been adequately addressed especially for intraoral bone regeneration. The current review aims to assess the clinical success of various human stem cells in oral bone regeneration. Articles studying the potential of various stem cells utilized for reconstruction of intraoral bone defects in humans were included in this review. Relevant articles were electronically searched in MEDLINE-PubMed database using keywords with different combinations. Only the articles published in English between 2006 and 2020 were included in this review. It was concluded that intra and extraoral stem cells can be successfully used for bone regeneration of various jaw defects. Depending on the origin, quantity, and quality, each cell type has its own advantages and disadvantages. Also, it brings to the fore the need for more clinical studies to validate and adopt the use of stem cells in regular clinical practice.

 

1. Jamjoom A, Cohen R. Grafts for ridge preservation. J Funct Biomater 2015 Aug;6:833-48.
2. Sybil D, Jain V, Mohanty S, Husain SA. Oral stem cells in intraoral bone formation. J Oral Biosci 2020 Mar;62:36-43.
3. Hansson S, Halldin A. Alveolar ridge resorption after tooth extraction: A consequence of a fundamental principle of bone physiology. J Dent Biomech 2012 Aug;3:1758736012456543.
4. Medina-Solís C, Mendoza-Rodríguez M, Márquez-Rodríguez S, De La Rosa-Santillana R, Islas-Zarazua R, Navarrete-Hernández J, et al. Reasons why erupted third molars are extracted in a public university in Mexico. West Indian Med J 2014 Aug;63:354-8.
5. d’Aquino R, Trovato L, Graziano A, Ceccarelli G, Cusella de Angelis G, Marangini A, et al. Periosteum-derived micro-grafts for tissue regeneration of human maxillary bone. J Transl Sci 2016 Mar;2(2):125-9.
6. Monti M, Graziano A, Rizzo S, Perotti C, Del Fante C, D’Aquino R, et al. In vitro and in vivo differentiation of progenitor stem cells obtained after mechanical digestion of human dental pulp. J Cell Physiol 2017 Mar;232(3):548-55.
7. Giuliani A, Manescu A, Langer M, Rustichelli F, Desiderio V, Paino F, et al. Three years after transplants in human mandibles, histological and in-line holotomography revealed that stem cells regenerated a compact rather than a spongy bone: Biological and clinical implications. Stem Cells Transl Med 2013 Apr;2(4):316-24.
8. d’Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, et al. Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cells Mater 2009 Nov;18:75-83.
9. Barbier L, Ramos E, Mendiola J, Rodriguez O, Santamaria G, Santamaria J, et al. Autologous dental pulp mesenchymal stem cells for inferior third molar post-extraction socket healing: A split-mouth randomized clinical trial. Med Oral Patol Oral y Cir Bucal 2018 Jul;23(4):e469-77.
10. Graziano A, Carinci F, Scolaro S, D’Aquino R. Periodontal tissue generation using autologous dental ligament micro-grafts: case report with 6 months follow-up. Ann Oral Maxillofac Surg 2013 Jun;1(2):1-5.
11. Mahajan A. Periosteum: A Highly underrated tool in dentistry. Int J Dent 2011 Sep;2012:1-6.
12. Kaigler D, Pagni G, Park CH, Braun TM, Holman LA, Yi E, et al. Stem cell therapy for craniofacial bone regeneration: A randomized, controlled feasibility trial. Cell Transplant 2013 Oct;22(5):767-77.
13. Pal US, Sharma NK, Singh RK, Singh N, Mahammad S, Mandhyan D, et al. Direct vs. indirect sinus lift procedure: A comparison. Natl J Maxillofac Surg 2012 Jan-Jun;3(1):31-7.
14. Brunelli G, Alessandro M, Graziano A, D′Aquino R, Zollino I, Carinci F. Sinus lift tissue engineering using autologous pulp micro-grafts: A case report of bone density evaluation. J Indian Soc Periodontol 2013 Sep-Oct;17(5):644-7.
15. Graziano A, D’Aquino R, Brunelli G, Fanali S, Carinci F. Sinus Lift Augmentation Using Pulp Stem Cells: A Case Report and Histological Evaluation. Eur J Inflamm 2011 Jan;9(1):89-93.
16. Pradel W, Mai R, Manolo Hagedorn G, Lauer G, Allegrini S. The biomaterial influences the ossification after sinus floor elevation using tissue-engineered bone grafts. Biomed Tech Eng 2008 Oct;53(5):224-8.
17. Nagata M, Hoshina H, Li M, Arasawa M, Uematsu K, Ogawa S, et al. A clinical study of alveolar bone tissue engineering with cultured autogenous periosteal cells: Coordinated activation of bone formation and resorption. Bone 2012 May;50(5):1123-9.
18. Prins H-J, Schulten EAJM, Ten Bruggenkate CM, Klein-Nulend J, Helder MN. Bone regeneration using the freshly isolated autologous stromal vascular fraction of adipose tissue in combination with calcium phosphate ceramics. Stem Cells Transl Med 2016 Oct;5(10):1362-74.
19. Gonshor A, McAllister BS, Wallace SS, Prasad H. Histologic and histomorphometric evaluation of an allograft stem cell-based matrix sinus augmentation procedure. Int J Oral Maxillofac Implants 2011 Jan-Feb;26(1):123-31.
20. Sauerbier S, Rickert D, Gutwald R, Nagursky H, Oshima T, Xavier SP, et al. Bone marrow concentrate and bovine bone mineral for sinus floor augmentation: A controlled, randomized, single-blinded clinical and histological trial—Per-protocol analysis. Tissue Eng Part A. 2011 Sep;17(17-18):2187-97.
21. Rickert D, Sauerbier S, Nagursky H, Menne D, Vissink A, Raghoebar GM. Maxillary sinus floor elevation with bovine bone mineral combined with either autogenous bone or autogenous stem cells: a prospective randomized clinical trial. Clin Oral Implants Res 2011 Mar;22(3):251-8.
22. Shayesteh YS, Khojasteh A, Soleimani M, Alikhasi M, Khoshzaban A, Ahmadbeigi N. Sinus augmentation using human mesenchymal stem cells loaded into a β-tricalcium phosphate/hydroxyapatite scaffold. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2008 Aug;106(2):203-9.
23. Wildburger A, Payer M, Jakse N, Strunk D, Etchard-Liechtenstein N, Sauerbier S. Impact of autogenous concentrated bone marrow aspirate on bone regeneration after sinus floor augmentation with a bovine bone substitute - a split-mouth pilot study. Clin Oral Implants Res 2014 Oct;25(10):1175-81.
24. Bertolai R. Catelani C, Aversa A, Rossi A, Giannini D, Bani D. Bone graft and mesenchymal stem cells: clinical observations and histological analysis. Clin Cases Miner Bone Metab 2015 May-Aug;12(2):183-7.
25. Dwarakanath C. Carranza’s Clinical Periodontology. 2nd South. Elsevier India; 2016:553-56.
26. Li Y, Zhao S, Nan X, Wei H, Shi J, Li A, et al. Repair of human periodontal bone defects by autologous grafting stem cells derived from inflammatory dental pulp tissues. Stem Cell Res Ther 2016 Sep;7:141.
27. Aimetti M, Ferrarotti F, Cricenti L, Mariani GM, Romano F. Autologous dental pulp stem cells in periodontal regeneration: a case report. Int J Periodontics Restorative Dent 2014 Jun;34 Suppl 3:s27-33.
28. Aimetti M, Ferrarotti F, Mariani GM, Cricenti L, Romano F. Use of dental pulp stem cells/collagen sponge biocomplex in the treatment of non-contained intrabony defects: A case series. Clin Adv Periodontics 2015 May;5:104-9.
29. Aimetti M, Ferrarotti F, Gamba M, Giraudi M, Romano F. Regenerative treatment of periodontal intrabony defects using autologous dental pulp stem cells: A 1-year follow-up case series. Int J Periodontics Restorative Dent 2018 Jan-Feb;38(1):51-8.
30. Ferrarotti F, Romano F, Gamba MN, Quirico A, Giraudi M, Audagna M, et al. Human intrabony defect regeneration with micrografts containing dental pulp stem cells: A randomized controlled clinical trial. J Clin Periodontol 2018 Jul;45(7):841-50.
31. Feng F, Akiyama K, Liu Y, Yamaza T, Wang TM, Chen JH, et al. Utility of PDL progenitors for in vivo tissue regeneration: a report of 3 cases. Oral Dis 2010 Jan;16(1):20-8.
32. Shalini H, Vandana K. Direct application of autologous periodontal ligament stem cell niche in treatment of periodontal osseous defects: A randomized controlled trial. J Indian Soc Periodontol 2018 Nov-Dec;22(6):503-12.
33. Chen FM, Gao LN, Tian BM, Zhang XY, Zhang Y-J, Dong GY, et al. Treatment of periodontal intrabony defects using autologous periodontal ligament stem cells: a randomized clinical trial. Stem Cell Res Ther 2016 Feb;7:33.
34. Manor E, Kachko L, Puterman MB, Szabo G, Bodner L. Cystic lesions of the jaws - A clinicopathological study of 322 cases and review of the literature. Int J Med Sci 2012 Jan;9(1):20-6.
35. Lee ST, Kim SG, Moon SY, Oh JS, You JS, Kim JS. The effect of decompression as treatment of the cysts in the jaws: retrospective analysis. J Korean Assoc Oral Maxillofac Surg 2017 Apr;43(2):83-7.
36. Bertolai R. Catelani C, Signorini M, Rossi A, Giannini D, Mesenchymal stem cells in post-surgical cavities of large maxillary bone lesions. Clin Cases Miner Bone Metab 2016 Sep-Dec;13(3):214-20.
37. Perjuci F, Ademi-Abdyli R, Abdyli Y, Morina E, Gashi A, Agani Z, et al. Evaluation of Spontaneous Bone Healing After Enucleation of Large Residual Cyst in Maxilla without Graft Material Utilization: Case Report. ActaStomatol Croat 2018 Mar;52(1):53-60.
38. Meshram M, Anchlia S, Shah H, Vyas S, Dhuvad J, Sagarka L. Buccal fat pad-derived stem cells for repair of maxillofacial bony defects. J Maxillofac Oral Surg 2019 Mar;18(1):112-23.
39. Pradel W, Eckelt U, Lauer G. Bone regeneration after enucleation of mandibular cysts: Comparing autogenous grafts from tissue-engineered bone and iliac bone. Oral Surg, Oral Med Oral Pathol Oral Radiol Endod. 2006 Mar;101(3):285-90.
40. Redondo LM, García V, Peral B, Verrier A, Becerra J, Sánchez A, et al. Repair of maxillary cystic bone defects with mesenchymal stem cells seeded on a cross-linked serum scaffold. J Cranio-Maxillofacial Surg 2018 Feb;46(2):222-9.
41. Colangeli W, Riccelli U, Giudice A, Barca I, Caruso D, Novembre D, et al. Jaw bones regeneration using mesenchymal stem cells. A single-center experience. Ann Ital Chir 2018 Jan;89:20-3.
42. Tettamanti L, Avantaggiato A, Nardone M, Palmieri A, Tagliabue A. New insights in orofacial cleft: Epidemiological and genetic studies on Italian samples. ORAL Implantol 2017 Jan-Mar;10(1):11-9.
43. Kharbanda OP, Shah B, Shukla DK, Dhaliwal RS, Grover A. Cleft lip and palate anomaly in India: Clinical profile, risk factors and current status of treatment: A hospital-based study. Indian Council of Medical Research Task Force Project Report. 2016:1-74.
44. Esmail AHA, Abdo MAA, Krentz H, Lenz J-H, Gundlach KKH. Centre-based statistics of cleft lip with/without alveolus and palate as well as cleft palate only patients in Aden, Yemen. J Cranio-Maxillofacial Surg 2014 Jun;42(4):297-304.
45. Hibi H, Yamada Y, Ueda M, Endo Y. Alveolar cleft osteoplasty using tissue-engineered osteogenic material. Int J Oral MaxillofacSurg 2006 Jun;35(6):551-5.
46. Khojasteh A, Kheiri L, Behnia H, Tehranchi A, Nazeman P, Nadjmi N, et al. Lateral Ramus Cortical Bone Plate in Alveolar Cleft Osteoplasty with Concomitant Use of Buccal Fat Pad Derived Cells and Autogenous Bone: Phase I Clinical Trial. Biomed Res Int 2017 Dec;2017:1-12.
47. Pradel W, Tausche E, Gollogly J, Lauer G. Spontaneous tooth eruption after alveolar cleft osteoplasty using tissue-engineered bone: a case report. Oral Surgery, Oral Med Oral Pathol Oral RadiolEndodontology 2008 Apr;105(4):440-4.
48. Pradel W, Lauer G. Tissue-engineered bone grafts for osteoplasty in patients with cleft alveolus. Ann Anat - AnatAnzeiger 2012 Nov;194(6):545-8.
49. Bajestan MN, Rajan A, Edwards SP, Aronovich S, Cevidanes LHS, Polymeri A, et al. Stem cell therapy for reconstruction of alveolar cleft and trauma defects in adults: A randomized controlled, clinical trial. Clin Implant Dent Relat Res 2017 Oct;19(5):793-801.
50. Behnia H, Khojasteh A, Soleimani M, Tehranchi A, Khoshzaban A, Keshel SH, et al. Secondary repair of alveolar clefts using human mesenchymal stem cells. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2009 Aug;108(2):e1-6.
51. Gimbel M, Ashley RK, Sisodia M, Gabbay JS, Wasson KL, Heller J, et al. Repair of Alveolar Cleft Defects: reduced morbidity with bone marrow stem cells in a resorbable matrix. J Craniofac Surg 2007 Jul;18(4):895-901.
52. Behnia H, Khojasteh A, Soleimani M, Tehranchi A, Atashi A. Repair of alveolar cleft defect with mesenchymal stem cells and platelet derived growth factors : A preliminary report. J Cranio-Maxillofacial Surg 2012 Jan;40(1):2-7.
53. Manjunath N, Arjun M. An ounce of prevention is worth a pound of cure: A review on ridge augmentation. J Interdiscip Dent 2015 Jan;5:97-104.
54. Khojasteh A, Sadeghi N. Application of buccal fat pad-derived stem cells in combination with autogenous iliac bone graft in the treatment of maxillomandibular atrophy: a preliminary human study. Int J Oral Maxillofac Surg 2016 Jul;45(7):864-71.
55. Gjerde C, Mustafa K, Hellem S, Rojewski M, Gjengedal H, Yassin MA, et al. Cell therapy induced regeneration of severely atrophied mandibular bone in a clinical trial. Stem Cell Res Ther 2018 Aug;9(1):213.
56. Xiao T, Zhao Y, Luo E, Hu J. “Tent-Pole” for reconstruction of large alveolar defects: A case report. J Oral MaxillofacSurg 2016 Jan;74(1):55-67.
57. Rajan A, Eubanks E, Edwards S, Aronovich S, Travan S, Rudek I, et al. Optimized cell survival and seeding efficiency for craniofacial tissue engineering using clinical stem cell therapy. Stem Cells Transl Med 2014 Dec;3(12):1495-503.
58. Khojasteh A, Hosseinpour S, Rad MR, Alikhasi M. Buccal fat pad–derived stem cells in three-dimensional rehabilitation of large alveolar defects: A report of two cases. J Oral Implantol 2019 Feb;45(1):45-54.
59. Behnia H, Mesgarzadeh A, Tehranchi A, Morad G, Samieerad S, Younessian F. Stabilization of premaxilla repositioned during secondary bone grafting in complete bilateral cleft lip and palate patients. J Craniofac Surg 2014 Jul;25(4):1554-7.
IssueVol 18 (Continuously Published Article-Based) QRcode
SectionReview Article
DOI https://doi.org/10.18502/fid.v18i40.7774
Keywords
Adult stem cell Mesenchymal Stem Cells; Review; Bone Regeneration; Cell- and Tissue-Based Therapy

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How to Cite
1.
Jain V, Sybil D, Premchandani S, Krishna M, Singh S. Intraoral Bone Regeneration Using Stem Cells-What a Clinician Needs to Know: Based on a 15-Year MEDLINE Search. Front Dent. 2021;18.