Postoperative administration of mesenchymal stem cells enhances peri-implant tissue healing in a medication-related osteonecrosis of the jaw model
Source abstract
Abstract
Patients undergoing antiresorptive therapy are generally advised against dental surgical procedures, particularly implant placement, due to the high risk of medication-related osteonecrosis of the jaw (MRONJ). Mesenchymal stem cells (MSCs) are multipotent cells capable of differentiating into multiple lineages; they also regulate immune responses and tissue repair. Previous studies have demonstrated that MSCs alleviate MRONJ symptoms and promote peri‑implant tissue healing, although their activation depends on specific in vivo conditions. In this study, we compared the effects of MSC administration before and after implantation on peri‑implant hard and soft tissue healing in a rat MRONJ model. In vivo, preoperative MSC treatment did not result in significant differences in peri‑implant bone or soft tissue healing compared with the drug-only group, whereas postoperative MSC treatment significantly improved multiple parameters; some reached levels comparable to those of controls. In vitro, postoperative MSC treatment modified the biological characteristics of primary oral epithelial cells and influenced the secretion of key reparative proteins. These findings suggest that postoperative MSC administration enhances peri‑implant tissue healing and modulates epithelial cell function, providing new experimental evidence for preventing and treating implant-associated MRONJ. STATEMENT OF SIGNIFICANCE: Medication-related osteonecrosis of the jaw (MRONJ) limits safe implant therapy in patients taking antiresorptive drugs. Using a reproducible MRONJ-like rat model, we show that postoperative, but not preoperative, mesenchymal stem cell (MSC) administration improves peri‑implant healing. Postoperative MSCs strengthen epithelial sealing, enhance angiogenesis, reduce neutrophil infiltration, and lessen necrotic bone, with congruent micro-CT and histology. We also report the first isolation and analysis of primary oral epithelial cells from MRONJ peri‑implant tissue, revealing MSC-driven gains in proliferation, survival, and barrier proteins. These findings identify therapeutic timing as a key design parameter for MSC-based interventions and provide translational guidance for mitigating implant-associated MRONJ risk, while informing broader biomaterials strategies that couple immunomodulation with repair of the epithelial-implant interface.
Source: openalex_inverted_index · Quality: baseline
Research context
OpenAlex topics: Bone health and treatments · Oral health in cancer treatment · Mesenchymal stem cell research
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (84)
Show source-provided references
1. A systematic review of studies comparing conventional complete denture and implant retained overdenture10.1016/j.jpor.2017.06.004 ↗
2. Mitigating osteonecrosis of the jaw (ONJ) through preventive dental care and understanding of risk factors10.1038/s41413-020-0088-1 ↗
3. American Association of Oral and Maxillofacial Surgeons' Position Paper on medication-related osteonecrosis of the jaws-2022 update10.1016/j.joms.2022.02.008 ↗
4. Effect of antiresorptive drugs on osseointegrated dental implants: a systematic review10.3390/jcm13072091 ↗
5. Mesenchymal stem cell immunomodulation: mechanisms and therapeutic potential10.1016/j.tips.2020.06.009 ↗
6. Mesenchymal stem cell-conditioned medium accelerates skin wound healing: an in vitro study of fibroblast and keratinocyte scratch assays10.1016/j.yexcr.2010.02.026 ↗
7. Cell-based immunotherapy with mesenchymal stem cells cures bisphosphonate-related osteonecrosis of the jaw-like disease in mice10.1002/jbmr.37 ↗
8. Mesenchymal stem cells in the treatment of osteonecrosis of the jaw10.5125/jkaoms.2021.47.2.65 ↗
9. Treatment of medication-related osteonecrosis of the jaw with cell therapy10.3389/fcell.2024.1338376 ↗
10. Therapeutic interaction of systemically-administered mesenchymal stem cells with peri-implant mucosa10.1371/journal.pone.0090681 ↗
11. Alveolar bone regeneration by transplantation of periodontal ligament stem cells and bone marrow stem cells in a canine peri-implant defect model: a pilot study10.1902/jop.2009.090249 ↗
12. Mesenchymal stromal cell 'licensing': a multistep process10.1038/leu.2011.108 ↗
13. Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotype10.4049/jimmunol.0803864 ↗
14. Mechanisms of mesenchymal stromal cell immunomodulation10.1038/icb.2012.56 ↗
15. Human mesenchymal stem cells stimulated by TNF-alpha, LPS, or hypoxia produce growth factors by an NF kappa B- but not JNK-dependent mechanism10.1152/ajpcell.00437.2007 ↗
16. Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells10.1186/s13287-018-1007-x ↗
17. Mesenchymal stem cell durotaxis depends on substrate stiffness gradient strength10.1002/biot.201200205 ↗
18. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: role in homing efficiency in NOD/SCID mice10.3324/haematol.10669 ↗
19. Mesenchymal stem cells: a new trend for cell therapy10.1038/aps.2013.50 ↗
20. Concise review: mesenchymal stem cells and translational medicine: emerging issues10.5966/sctm.2011-0019 ↗
21. Impact of timing and dose of mesenchymal stromal cell therapy in a preclinical model of acute myocardial infarction10.1016/j.cardfail.2013.03.011 ↗
22. Multipotent mesenchymal stromal cell sheet therapy for bisphosphonate-related osteonecrosis of the jaw in a rat model10.1016/j.actbio.2016.06.022 ↗
23. Changes in the distribution of laminin-5 during peri-implant epithelium formation after immediate titanium implantation in rats10.1016/j.biomaterials.2004.05.033 ↗
24. Limitations of using micro-computed tomography to predict bone-implant contact and mechanical fixation10.1111/j.1365-2818.2011.03541.x ↗
25. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography10.1002/jbmr.141 ↗
26. Zoledronate impairs socket healing after extraction of teeth with experimental periodontitis10.1177/0022034517732770 ↗
27. Epithelial and connective tissue sealing around titanium implants with various typical surface finishes10.1021/acsbiomaterials.9b00499 ↗
28. Pamidronate (Aredia) and zoledronate (Zometa) induced avascular necrosis of the jaws: a growing epidemic10.1016/S0278-2391(03)00720-1 ↗
29. Endothelial progenitor cells inhibit jaw osteonecrosis in a rat model: a major adverse effect of bisphosphonate therapy10.1038/s41598-019-55383-5 ↗
30. Oral fibroblasts rescue osteogenic differentiation of mesenchymal stem cells after exposure to zoledronic acid in a paracrine effect10.3389/fphar.2023.1172705 ↗
31. Dynamic polarization shifting from M1 to M2 macrophages in reduced osteonecrosis of the jaw-like lesions by cessation of anti-RANKL antibody in mice10.1016/j.bone.2020.115560 ↗
32. Multilineage potential of adult human mesenchymal stem cells10.1126/science.284.5411.143 ↗
33. Efficacy of stem cells on the healing of peri-implant defects: systematic review of preclinical studies10.1002/cre2.16 ↗
34. Bisphosphonate-related osteonecrosis. application of adipose-derived stem cells in an experimental murine model
35. Evaluation of the therapeutic effects of conditioned media from mesenchymal stem cells in a rat bisphosphonate-related osteonecrosis of the jaw-like model10.1016/j.bone.2015.01.011 ↗
36. Exosomes from adipose-derived stem cells can prevent medication-related osteonecrosis of the jaw10.12659/MSM.929684 ↗
37. Extracellular vesicles of stem cells to prevent BRONJ10.1177/0022034520906793 ↗
38. Establishment and assessment of rodent models of medication-related osteonecrosis of the jaw (MRONJ)10.1038/s41368-022-00182-4 ↗
39. Preventive effect of fluvastatin on the development of medication-related osteonecrosis of the jaw10.1038/s41598-020-61724-6 ↗
40. Alveolar wound healing and ridge remodeling after tooth extraction in the rat: a histologic, radiographic, and histometric study10.1016/0278-2391(85)90257-5 ↗
41. Intra-oral PTH administration promotes tooth extraction socket healing10.1177/0022034513487558 ↗
42. The effects of hyperglycaemia on peri-implant tissues after osseointegration10.1016/j.jpor.2019.07.007 ↗
43. Stem cell transplantation: the lung barrier10.1016/j.transproceed.2006.12.019 ↗
44. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion10.3389/fimmu.2012.00297 ↗
45. Pulmonary passage is a major obstacle for intravenous stem cell delivery: the pulmonary first-pass effect10.1089/scd.2008.0253 ↗
46. To serve and protect: hydrogels to improve stem cell-based therapies10.1016/j.stem.2015.12.004 ↗
47. MSCs mediate long-term efficacy in a Crohn's disease model by sustained anti-inflammatory macrophage programming via efferocytosis10.1038/s41536-024-00347-1 ↗
48. Alendronate/dexamethasone combination therapy worsens soft and hard tissue wound healing around implants in rat maxillae10.1016/j.bone.2021.115942 ↗
49. Effect of zoledronate on oral wound healing in rats10.1158/1078-0432.CCR-10-1614 ↗
50. Cytokine mixtures mimicking secretomes from mesenchymal stem cells improve medication-related osteonecrosis of the jaw in a rat model10.1002/jbm4.10013 ↗
51. Small extracellular vesicles derived from adipose tissue prevent bisphosphonate-related osteonecrosis of the jaw by promoting angiogenesis10.2147/IJN.S305361 ↗
52. The modulatory effects of mesenchymal stem cells on osteoclastogenesis10.1155/2016/1908365 ↗
53. The influence of systemically or locally administered mesenchymal stem cells on tissue repair in a rat oral implantation model10.1186/s40729-017-0112-4 ↗
54. The role of hepatocyte growth factor in mesenchymal stem cell-induced recovery in spinal cord injured rats10.1186/s13287-020-01691-x ↗
55. Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-3710.1002/stem.544 ↗
56. Antibacterial activity of human mesenchymal stem cells mediated directly by constitutively secreted factors and indirectly by activation of innate immune effector cells10.1002/sctm.19-0092 ↗
57. Therapeutic strategies for enhancing angiogenesis in wound healing10.1016/j.addr.2018.09.010 ↗
58. Bisphosphonate effects on the behaviour of oral epithelial cells and oral fibroblasts10.1016/j.archoralbio.2010.11.003 ↗
59. Effect of zoledronic acid on oral fibroblasts and epithelial cells: a potential mechanism of bisphosphonate-associated osteonecrosis10.1111/j.1365-2141.2008.07504.x ↗
60. In vivo effects of zoledronic acid on oral mucosal epithelial cells10.1111/j.1601-0825.2010.01739.x ↗
61. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing10.1371/journal.pone.0001886 ↗
62. Laminins: roles and utility in wound repair10.1089/wound.2014.0533 ↗
63. Laminin-5 expression is independent of the injury and the microenvironment during reepithelialization of wounds10.1177/002215549804600309 ↗
64. The role of a recombinant fragment of laminin-332 in integrin alpha3beta1-dependent cell binding, spreading and migration10.1016/j.biomaterials.2010.03.003 ↗
65. Evaluation of carbonate apatite as a bone substitute in rat extraction sockets from the perspective of mesenchymal stem cells10.4012/dmj.2022-040 ↗
66. Therapeutic interactions between mesenchymal stem cells for healing medication-related osteonecrosis of the jaw10.1186/s13287-016-0367-3 ↗
67. Hepatocyte growth factor is required for mesenchymal stromal cell protection against bleomycin-induced pulmonary fibrosis10.5966/sctm.2015-0337 ↗
68. Intra-arterial cell transplantation provides timing-dependent cell distribution and functional recovery after stroke10.1161/STROKEAHA.112.677328 ↗
69. Therapeutic potential of mesenchymal stem cells on early and late experimental hepatic schistosomiasis model10.1645/15-754.1 ↗
70. Early injection of human adipose tissue-derived mesenchymal stem cell after inflammation ameliorates dextran sulfate sodium-induced colitis in mice through the induction of M2 macrophages and regulatory T cells10.1007/s00441-018-02981-w ↗
71. Mesenchymal stem cells can prevent or promote the progression of colon cancer based on their timing of administration10.1186/s12967-023-04028-3 ↗
72. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli10.1182/blood.V99.10.3838 ↗
73. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide10.1182/blood-2002-07-2104 ↗
74. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype10.4049/jimmunol.0902007 ↗
75. Human mesenchymal stem cells modulate B-cell functions10.1182/blood-2005-07-2657 ↗
76. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation10.1182/blood-2005-07-2775 ↗
77. Mesenchymal stem cells inhibit dendritic cell differentiation and function by preventing entry into the cell cycle10.1097/01.tp.0000244572.24780.54 ↗
78. Human mesenchymal stem cells inhibit neutrophil apoptosis: a model for neutrophil preservation in the bone marrow niche10.1634/stemcells.2007-0416 ↗
79. The role of mesenchymal stem cells in haemopoiesis10.1016/j.blre.2005.11.002 ↗
80. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes10.3324/haematol.12857 ↗
81. Bone marrow-derived mesenchymal stem cells induce both polyclonal expansion and differentiation of B cells isolated from healthy donors and systemic lupus erythematosus patients10.1634/stemcells.2007-0528 ↗
82. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells10.1634/stemcells.2005-0008 ↗
83. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide10.1016/j.stem.2007.11.014 ↗
84. Determination of the molecular mechanism by which macrophages and γδ-T cells contribute to ZOL-induced ONJ10.18632/aging.104006 ↗