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Utilizing biodegradable alloys as guided bone regeneration (GBR) membrane: Feasibility and challenges

使用可降解金属材料制备定向骨再生膜的可行性与 挑战

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Abstract

Guided bone regeneration (GBR) is a therapeutic procedure used to enhance alveolar bone volume before dental implants. Commercial non-absorbable membranes (i.e., titanium membranes) typically require a second surgery to remove, whereas absorbable membranes (i.e., collagen membranes) will fail when put over extensive bone lesions due to their low mechanical strength. The GBR membrane that has been sought is still being developed. Biodegradable metals (BMs), particularly Mg and Zn, have recently been postulated as promising barrier membrane candidates. Herein, the goal of this research is to evaluate the mechanical and biological feasibility of using BMs as GBR membranes. It shows that BMs have a wide range of potential applications as GBR membranes, owing to their benign biocompatibility, sufficient mechanical support, tunable degradation rate, good osteogenic capabilities, broad-spectrum antibacterial behavior, and improved wound healing ability. The rapid degradation rate, hydrogen evolution impact, and stress corrosion cracking behavior all pose obstacles to the use of Mg-based membranes, which can be improved by surface modifications, heat treatment, alloying, etc. Due to its acceptable degradation rate and lack of gas production, Zn appears to be a better candidate for usage as a GBR membrane. In general, advances in the development of BMs have paved the door for BMs to be used as GBR membranes in oral clinical trials.

摘要

定向骨再生手术是一种用于增加牙槽骨体积的治疗手段. 目前, 商用的不吸收薄膜(钛膜等)需要二次手术去除, 而可吸收薄膜(胶原膜 等), 由于强度较低, 在覆盖大部分病变骨骼时可能会失效. 理想的定向 骨再生薄膜仍处于发展中. 近年来, 生物可降解金属被认为是潜在的骨 再生薄膜候选材料. 因此, 本文主要从力学和生物学角度评估了可降解 金属作为定向骨再生薄膜的可行性. 结果表明, 可降解金属具有良好的 生物相容性、足够的机械强度、可控的降解速率、良好的成骨性能、 广谱抗菌能力和较好的创面愈合能力等优点, 能够被用于制备定向骨 再生薄膜. 然而, 对于镁合金来说, 其较快的降解速率、析氢行为和应 力腐蚀现象制约了其应用. 对于锌合金而言, 其降解速率适中且无氢气 产生, 似乎具有更好的应用前景. 目前, 可降解金属的发展已经为其在 口腔临床中的应用奠定了一定的基础.

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References

  1. Aprile P, Letourneur D, Simon-Yarza T. Membranes for guided bone regeneration: A road from bench to bedside. Adv Healthc Mater, 2020, 9: 2000707

    Article  CAS  Google Scholar 

  2. Elgali I, Omar O, Dahlin C, et al. Guided bone regeneration: Materials and biological mechanisms revisited. Eur J Oral Sci, 2017, 125: 315–337

    Article  Google Scholar 

  3. Bottino MC, Thomas V, Schmidt G, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration—A materials perspective. Dent Mater, 2012, 28: 703–721

    Article  CAS  Google Scholar 

  4. Jung RE, Windisch SI, Eggenschwiler AM, et al. A randomized-controlled clinical trial evaluating clinical and radiological outcomes after 3 and 5 years of dental implants placed in bone regenerated by means of GBR techniques with or without the addition of BMP-2. Clin Oral Implant Res, 2009, 20: 660–666

    Article  Google Scholar 

  5. Meloni SM, Jovanovic SA, Urban I, et al. Horizontal ridge augmentation using GBR with a native collagen membrane and 1:1 ratio of particulated xenograft and autologous bone: A 1-year prospective clinical study. Clin Implant Dent Relat Res, 2017, 19: 38–45

    Article  Google Scholar 

  6. Beitlitum I, Artzi Z, Nemcovsky CE. Clinical evaluation of particulate allogeneic with and without autogenous bone grafts and resorbable collagen membranes for bone augmentation of atrophic alveolar ridges. Clin Oral Implant Res, 2010, 21: 1242–1250

    Article  Google Scholar 

  7. Mandelli F, Traini T, Ghensi P. Customized-3D zirconia barriers for guided bone regeneration (GBR): Clinical and histological findings from a proof-of-concept case series. J Dent, 2021, 114: 103780

    Article  CAS  Google Scholar 

  8. Ueyama Y, Ishikawa K, Mano T, et al. Usefulness as guided bone regeneration membrane of the alginate membrane. Biomaterials, 2002, 23: 2027–2033

    Article  CAS  Google Scholar 

  9. Mirzaali MJ, Schwiedrzik JJ, Thaiwichai S, et al. Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone, 2016, 93: 196–211

    Article  Google Scholar 

  10. Staiger MP, Pietak AM, Huadmai J, et al. Magnesium and its alloys as orthopedic biomaterials: A review. Biomaterials, 2006, 27: 1728–1734

    Article  CAS  Google Scholar 

  11. Park JY, Lee JH, Kim CH, et al. Fabrication of polytetrafluoroethylene nanofibrous membranes for guided bone regeneration. RSC Adv, 2018, 8: 34359–34369

    Article  CAS  Google Scholar 

  12. Nishio S, Kosuga K, Igaki K, et al. Long-term (>10 years) clinical outcomes of first-in-human biodegradable poly-l-lactic acid coronary stents. Circulation, 2012, 125: 2343–2353

    Article  CAS  Google Scholar 

  13. Bowen PK, Shearier ER, Zhao S, et al. Biodegradable metals for cardiovascular stents: From clinical concerns to recent Zn-alloys. Adv Healthc Mater, 2016, 5: 1121–1140

    Article  CAS  Google Scholar 

  14. Huang D, Niu L, Li J, et al. Reinforced chitosan membranes by microspheres for guided bone regeneration. J Mech Behav Biomed Mater, 2018, 81: 195–201

    Article  CAS  Google Scholar 

  15. Li G, Yang H, Zheng Y, et al. Challenges in the use of zinc and its alloys as biodegradable metals: Perspective from biomechanical compatibility. Acta Biomater, 2019, 97: 23–45

    Article  CAS  Google Scholar 

  16. Mostaed E, Sikora-Jasinska M, Drelich JW, et al. Zinc-based alloys for degradable vascular stent applications. Acta Biomater, 2018, 71: 1–23

    Article  CAS  Google Scholar 

  17. Gu XN, Zheng YF. A review on magnesium alloys as biodegradable materials. Front Mater Sci China, 2010, 4: 111–115

    Article  Google Scholar 

  18. Pan H, Qin G, Huang Y, et al. Development of low-alloyed and rare-earth-free magnesium alloys having ultra-high strength. Acta Mater, 2018, 149: 350–363

    Article  CAS  Google Scholar 

  19. Chen J, Tan L, Yu X, et al. Mechanical properties of magnesium alloys for medical application: A review. J Mech Behav Biomed Mater, 2018, 87: 68–79

    Article  CAS  Google Scholar 

  20. Song J, She J, Chen D, et al. Latest research advances on magnesium and magnesium alloys worldwide. J Magnes Alloys, 2020, 8: 1–41

    Article  CAS  Google Scholar 

  21. Windisch P, Orban K, Salvi GE, et al. Vertical-guided bone regeneration with a titanium-reinforced d-PTFE membrane utilizing a novel split-thickness flap design: A prospective case series. Clin Oral Invest, 2021, 25: 2969–2980

    Article  Google Scholar 

  22. Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: A systematic review. Clin Oral Implant Res, 2009, 20: 113–123

    Article  Google Scholar 

  23. Polimeni G, Koo KT, Pringle GA, et al. Histopathological observations of a polylactic acid-based device intended for guided bone/tissue regeneration. Clin Implant Dent Rel Res, 2008, 10: 99–105

    Article  Google Scholar 

  24. Kim BN, Ko YG, Yeo T, et al. Guided regeneration of rabbit calvarial defects using silk fibroin nanofiber-poly(glycolic acid) hybrid scaffolds. ACS Biomater Sci Eng, 2019, 5: 5266–5272

    Article  CAS  Google Scholar 

  25. Wang J, Qu Y, Chen C, et al. Fabrication of collagen membranes with different intrafibrillar mineralization degree as a potential use for GBR. Mater Sci Eng-C, 2019, 104: 109959

    Article  CAS  Google Scholar 

  26. Xia D, Yang F, Zheng Y, et al. Research status of biodegradable metals designed for oral and maxillofacial applications: A review. Bioactive Mater, 2021, 6: 4186–4208

    Article  CAS  Google Scholar 

  27. Liu Y, Zheng Y, Chen XH, et al. Fundamental theory of biodegradable metals-definition, criteria, and design. Adv Funct Mater, 2019, 29: 1805402

    Article  CAS  Google Scholar 

  28. Francis A, Yang Y, Virtanen S, et al. Iron and iron-based alloys for temporary cardiovascular applications. J Mater Sci-Mater Med, 2015, 26: 138

    Article  CAS  Google Scholar 

  29. Zheng YF, Gu XN, Witte F. Biodegradable metals. Mater Sci Eng-R-Rep, 2014, 77: 1–34

    Article  Google Scholar 

  30. Vojtěch D, Kubásek J, Serák J, et al. Mechanical and corrosion properties of newly developed biodegradable Zn-based alloys for bone fixation. Acta Biomater, 2011, 7: 3515–3522

    Article  CAS  Google Scholar 

  31. Yang H, Wang C, Liu C, et al. Evolution of the degradation mechanism of pure zinc stent in the one-year study of rabbit abdominal aorta model. Biomaterials, 2017, 145: 92–105

    Article  CAS  Google Scholar 

  32. Yang H, Qu X, Lin W, et al. In vitro and in vivo studies on zinc-hydroxyapatite composites as novel biodegradable metal matrix composite for orthopedic applications. Acta Biomater, 2018, 71: 200–214

    Article  CAS  Google Scholar 

  33. Qu X, Yang H, Jia B, et al. Biodegradable Zn-Cu alloys show antibacterial activity against MRSA bone infection by inhibiting pathogen adhesion and biofilm formation. Acta Biomater, 2020, 117: 400–417

    Article  CAS  Google Scholar 

  34. Chen K, Xie X, Tang H, et al. In vitro and in vivo degradation behavior of Mg-2Sr-Ca and Mg-2Sr-Zn alloys. Bioactive Mater, 2020, 5: 275–285

    Article  Google Scholar 

  35. Ge W, Chen K, Tang H, et al. Degradability and in vivo biocompatibility of micro-alloyed Mg-Ca-La alloys as orthopedic implants. Mater Lett, 2022, 310: 131510

    Article  CAS  Google Scholar 

  36. Tang H, Wang F, Li D, et al. Mechanical properties, degradation behaviors and biocompatibility of micro-alloyed Mg-Sr-RE alloys for stent applications. Mater Lett, 2020, 264: 127285

    Article  CAS  Google Scholar 

  37. Rapetto C, Leoncini M. Magmaris: A new generation metallic sirolimus-eluting fully bioresorbable scaffold: Present status and future perspectives. J Thorac Dis, 2017, 9: S903–S913

    Article  Google Scholar 

  38. Esmaily M, Svensson JE, Fajardo S, et al. Fundamentals and advances in magnesium alloy corrosion. Prog Mater Sci, 2017, 89: 92–193

    Article  CAS  Google Scholar 

  39. Hoornaert A, d’Arros C, Heymann MF, et al. Biocompatibility, resorption and biofunctionality of a new synthetic biodegradable membrane for guided bone regeneration. Biomed Mater, 2016, 11: 045012

    Article  CAS  Google Scholar 

  40. Oh SH, Kim JH, Kim JM, et al. Asymmetrically porous PLGA/Pluronic F127 membrane for effective guided bone regeneration. J Biomater Sci Polym Ed, 2006, 17: 1375–1387

    Article  CAS  Google Scholar 

  41. Shim JH, Jeong JH, Won JY, et al. Porosity effect of 3D-printed polycaprolactone membranes on calvarial defect model for guided bone regeneration. Biomed Mater, 2017, 13: 015014

    Article  Google Scholar 

  42. Jung RE, Herzog M, Wolleb K, et al. A randomized controlled clinical trial comparing small buccal dehiscence defects around dental implants treated with guided bone regeneration or left for spontaneous healing. Clin Oral Impl Res, 2017, 28: 348–354

    Article  Google Scholar 

  43. Omar O, Elgali I, Dahlin C, et al. Barrier membranes: More than the barrier effect? J Clin Periodontol, 2019, 46: 103–123

    Article  Google Scholar 

  44. Seo SJ, Kim JJ, Kim JH, et al. Enhanced mechanical properties and bone bioactivity of chitosan/silica membrane by functionalized-carbon nanotube incorporation. Compos Sci Tech, 2014, 96: 31–37

    Article  CAS  Google Scholar 

  45. Costa EM, Silva S, Veiga M, et al. A review of chitosan’s effect on oral biofilms: Perspectives from the tube to the mouth. J Oral Biosci, 2017, 59: 205–210

    Article  Google Scholar 

  46. Liu Y, Li H, Xu J, et al. Biodegradable metal-derived magnesium and sodium enhances bone regeneration by angiogenesis aided osteogenesis and regulated biological apatite formation. Chem Eng J, 2021, 410: 127616

    Article  CAS  Google Scholar 

  47. Li W, Qiao W, Liu X, et al. Biomimicking bone-implant interface facilitates the bioadaption of a new degradable magnesium alloy to the bone tissue microenvironment. Adv Sci, 2021, 8: 2102035

    Article  CAS  Google Scholar 

  48. Yang H, Jia B, Zhang Z, et al. Alloying design of biodegradable zinc as promising bone implants for load-bearing applications. Nat Commun, 2020, 11: 401

    Article  CAS  Google Scholar 

  49. Leonhardt H, Ziegler A, Lauer G, et al. Osteosynthesis of the mandibular condyle with magnesium-based biodegradable headless compression screws show good clinical results during a 1-year follow-up period. J Oral Maxil Surg, 2021, 79: 637–643

    Article  Google Scholar 

  50. Wu S, Jang YS, Kim YK, et al. Surface modification of pure magnesium mesh for guided bone regeneration: In vivo evaluation of rat calvarial defect. Materials, 2019, 12: 2684

    Article  CAS  Google Scholar 

  51. Byun SH, Lim HK, Kim SM, et al. The bioresorption and guided bone regeneration of absorbable hydroxyapatite-coated magnesium mesh. J Craniofac Surg, 2017, 28: 518–523

    Article  Google Scholar 

  52. Peng W, Chen JX, Shan XF, et al. Mg-based absorbable membrane for guided bone regeneration (GBR): A pilot study. Rare Met, 2019, 38: 577–587

    Article  CAS  Google Scholar 

  53. Zhang S, Sun X, Kang C, et al. Study on repairing canine mandibular defect with porous Mg-Sr alloy combined with Mg-Sr alloy membrane. Regen Biomater, 2020, 7: 331–336

    Article  CAS  Google Scholar 

  54. Guo Y, Liu W, Ma S, et al. A preliminary study for novel use of two Mg alloys (WE43 and Mg3Gd). J Mater Sci-Mater Med, 2016, 27: 82

    Article  CAS  Google Scholar 

  55. Guo Y, Yu Y, Han L, et al. Biocompatibility and osteogenic activity of guided bone regeneration membrane based on chitosan-coated magnesium alloy. Mater Sci Eng-C, 2019, 100: 226–235

    Article  CAS  Google Scholar 

  56. Chen Y, Ye SH, Sato H, et al. Hybrid scaffolds of Mg alloy mesh reinforced polymer/extracellular matrix composite for critical-sized calvarial defect reconstruction. J Tissue Eng Regen Med, 2018, 12: 1374–1388

    Article  CAS  Google Scholar 

  57. Si J, Shen H, Miao H, et al. In vitro and in vivo evaluations of Mg-Zn-Gd alloy membrane on guided bone regeneration for rabbit calvarial defect. J Magnes Alloys, 2021, 9: 281–291

    Article  CAS  Google Scholar 

  58. Zhao M, Liu G, Li Y, et al. Degradation behavior, transport mechanism and osteogenic activity of Mg-Zn-RE alloy membranes in critical-sized rat calvarial defects. Coatings, 2020, 10: 496

    Article  CAS  Google Scholar 

  59. Lin DJ, Hung FY, Lee HP, et al. Development of a novel degradation-controlled magnesium-based regeneration membrane for future guided bone regeneration (GBR therapy. Metals, 2017, 7: 481

    Article  CAS  Google Scholar 

  60. Guo H, Xia D, Zheng Y, et al. A pure zinc membrane with degradability and osteogenesis promotion for guided bone regeneration: In vitro and in vivo studies. Acta Biomater, 2020, 106: 396–409

    Article  CAS  Google Scholar 

  61. Chen K, Zhou G, Li Q, et al. In vitro degradation, biocompatibility and antibacterial properties of pure zinc: Assessing the potential of Zn as a guided bone regeneration membrane. J Mater Chem B, 2021, 9: 5114–5127

    Article  CAS  Google Scholar 

  62. Li P, Zhang W, Dai J, et al. Investigation of zinc-copper alloys as potential materials for craniomaxillofacial osteosynthesis implants. Mater Sci Eng-C, 2019, 103: 109826

    Article  CAS  Google Scholar 

  63. Zhang W, Li P, Shen G, et al. Appropriately adapted properties of hot-extruded Zn-0.5Cu-xFe alloys aimed for biodegradable guided bone regeneration membrane application. Bioact Mater, 2021, 6: 975–989

    Article  CAS  Google Scholar 

  64. Wang X, Shao X, Dai T, et al. In vivo study of the efficacy, biosafety, and degradation of a zinc alloy osteosynthesis system. Acta Biomater, 2019, 92: 351–361

    Article  CAS  Google Scholar 

  65. Zhuang Y, Liu Q, Jia G, et al. A biomimetic zinc alloy scaffold coated with brushite for enhanced cranial bone regeneration. ACS Biomater Sci Eng, 2021, 7: 893–903

    Article  CAS  Google Scholar 

  66. Zhang Y, Yan Y, Xu X, et al. Investigation on the microstructure, mechanical properties, in vitro degradation behavior and bio-compatibility of newly developed Zn-0.8%Li-(Mg, Ag) alloys for guided bone regeneration. Mater Sci Eng-C, 2019, 99: 1021–1034

    Article  CAS  Google Scholar 

  67. Kubásek J, Dvorský D, Šedý J, et al. The fundamental comparison of Zn-2Mg and Mg-4Y-3RE alloys as a perspective biodegradable materials. Materials, 2019, 12: 3745

    Article  CAS  Google Scholar 

  68. Chen K, Dai J, Zhang X. Improvement of corrosion resistance of magnesium alloys for biomedical applications. Corros Rev, 2015, 33: 101–117

    Article  CAS  Google Scholar 

  69. Skalny AV, Skalnaya MG, Grabeklis AR, et al. Zinc deficiency as a mediator of toxic effects of alcohol abuse. Eur J Nutr, 2018, 57: 2313–2322

    Article  CAS  Google Scholar 

  70. Fu J, Su Y, Qin YX, et al. Evolution of metallic cardiovascular stent materials: A comparative study among stainless steel, magnesium and zinc. Biomaterials, 2020, 230: 119641

    Article  CAS  Google Scholar 

  71. Wang J, Witte F, Xi T, et al. Recommendation for modifying current cytotoxicity testing standards for biodegradable magnesium-based materials. Acta Biomater, 2015, 21: 237–249

    Article  CAS  Google Scholar 

  72. Ma J, Zhao N, Zhu D. Endothelial cellular responses to biodegradable metal zinc. ACS Biomater Sci Eng, 2015, 1: 1174–1182

    Article  CAS  Google Scholar 

  73. Tang H, Li S, Zhao Y, et al. A surface-eroding poly(1,3-trimethylene carbonate) coating for magnesium based cardiovascular stents with stable drug release and improved corrosion resistance. Bioact Mater, 2022, 7: 144–153

    Article  CAS  Google Scholar 

  74. Zhang Z, Jia B, Yang H, et al. Zn0.8Li0.1Sr: A biodegradable metal with high mechanical strength comparable to pure Ti for the treatment of osteoporotic bone fractures: In vitro and in vivo studies Biomaterials, 2021, 275: 120905

    Article  CAS  Google Scholar 

  75. Yuan W, Xia D, Zheng Y, et al. Controllable biodegradation and enhanced osseointegration of ZrO2-nanofilm coated Zn-Li alloy: In vitro and in vivo studies Acta Biomater, 2020, 105: 290–303

    Article  CAS  Google Scholar 

  76. Chen K, Lu Y, Tang H, et al. Effect of strain on degradation behaviors of WE43, Fe and Zn wires. Acta Biomater, 2020, 113: 627–645

    Article  CAS  Google Scholar 

  77. Winzer N, Atrens A, Song G, et al. A critical review of the stress corrosion cracking (SCC) of magnesium alloys. Adv Eng Mater, 2005, 7: 659–693

    Article  CAS  Google Scholar 

  78. Törne K, Örnberg A, Weissenrieder J. Influence of strain on the corrosion of magnesium alloys and zinc in physiological environments. Acta Biomater, 2017, 48: 541–550

    Article  CAS  Google Scholar 

  79. Bian D, Zhou W, Liu Y, et al. Fatigue behaviors of HP-Mg, Mg-Ca and Mg-Zn-Ca biodegradable metals in air and simulated body fluid. Acta Biomater, 2016, 41: 351–360

    Article  CAS  Google Scholar 

  80. Chen Y, Xu Z, Smith C, et al. Recent advances on the development of magnesium alloys for biodegradable implants. Acta Biomater, 2014, 10: 4561–4573

    Article  CAS  Google Scholar 

  81. Wang JL, Xu JK, Hopkins C, et al. Biodegradable magnesium-based implants in orthopedics—A general review and perspectives. Adv Sci, 2020, 7: 1902443

    Article  CAS  Google Scholar 

  82. Zhang Y, Xu J, Ruan YC, et al. Implant-derived magnesium induces local neuronal production of CGRP to improve bone-fracture healing in rats. Nat Med, 2016, 22: 1160–1169

    Article  CAS  Google Scholar 

  83. Yoshizawa S, Brown A, Barchowsky A, et al. Magnesium ion stimulation of bone marrow stromal cells enhances osteogenic activity, simulating the effect of magnesium alloy degradation. Acta Biomater, 2014, 10: 2834–2842

    Article  CAS  Google Scholar 

  84. Zhai Z, Qu X, Li H, et al. The effect of metallic magnesium degradation products on osteoclast-induced osteolysis and attenuation of NF-κB and NFATc1 signaling. Biomaterials, 2014, 35: 6299–6310

    Article  CAS  Google Scholar 

  85. Yuan Z, Wei P, Huang Y, et al. Injectable PLGA microspheres with tunable magnesium ion release for promoting bone regeneration. Acta Biomater, 2019, 85: 294–309

    Article  CAS  Google Scholar 

  86. Hung CC, Chaya A, Liu K, et al. The role of magnesium ions in bone regeneration involves the canonical Wnt signaling pathway. Acta Biomater, 2019, 98: 246–255

    Article  CAS  Google Scholar 

  87. Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature, 2014, 507: 323–328

    Article  CAS  Google Scholar 

  88. Liu WC, Chen S, Zheng L, et al. Angiogenesis assays for the evaluation of angiogenic properties of orthopaedic biomaterials: A general review. Adv Healthc Mater, 2017, 6: 1600434

    Article  CAS  Google Scholar 

  89. Yamaguchi M. Role of nutritional zinc in the prevention of osteoporosis. Mol Cell Biochem, 2010, 338: 241–254

    Article  CAS  Google Scholar 

  90. Nagata M, Lönnerdal B. Role of zinc in cellular zinc trafficking and mineralization in a murine osteoblast-like cell line. J Nutral Biochem, 2011, 22: 172–178

    Article  CAS  Google Scholar 

  91. Yamaguchi M, Kishi S. Zinc compounds inhibit osteoclast-like cell formation at the earlier stage of rat marrow culture but not osteoclast function. Mol Cell Biochem, 1996, 158: 171–177

    Article  CAS  Google Scholar 

  92. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutral Biochem, 2010, 21: 297–303

    Article  CAS  Google Scholar 

  93. Kwun IS, Cho YE, Lomeda RAR, et al. Zinc deficiency suppresses matrix mineralization and retards osteogenesis transiently with catchup possibly through Runx 2 modulation. Bone, 2010, 46: 732–741

    Article  CAS  Google Scholar 

  94. Yamaguchi M, Goto M, Uchiyama S, et al. Effect of zinc on gene expression in osteoblastic MC3T3-E1 cells: enhancement of Runx2, OPG, and regucalcin mRNA expressions. Mol Cell Biochem, 2008, 312: 157–166

    Article  CAS  Google Scholar 

  95. Fong L, Tan K, Tran C, et al. Interaction of dietary zinc and intracellular binding protein metallothionein in postnatal bone growth. Bone, 2009, 44: 1151–1162

    Article  CAS  Google Scholar 

  96. Ovesen J, MØller-Madsen B, Thomsen JS, et al. The positive effects of zinc on skeletal strength in growing rats. Bone, 2001, 29: 565–570

    Article  CAS  Google Scholar 

  97. Yousef MI, El Hendy HA, El-Demerdash FM, et al. Dietary zinc deficiency induced-changes in the activity of enzymes and the levels of free radicals, lipids and protein electrophoretic behavior in growing rats. Toxicology, 2002, 175: 223–234

    Article  CAS  Google Scholar 

  98. Kim JT, Baek SH, Lee SH, et al. Zinc-deficient diet decreases fetal long bone growth through decreased bone matrix formation in mice. J Med Food, 2009, 12: 118–123

    Article  CAS  Google Scholar 

  99. Cho YE, Lomeda RAR, Ryu SH, et al. Zinc deficiency negatively affects alkaline phosphatase and the concentration of Ca, Mg and P in rats. Nutr Res Pract, 2007, 1: 113

    Article  CAS  Google Scholar 

  100. Zhu D, Su Y, Young ML, et al. Biological responses and mechanisms of human bone marrow mesenchymal stem cells to Zn and Mg biomaterials. ACS Appl Mater Interfaces, 2017, 9: 27453–27461

    Article  CAS  Google Scholar 

  101. Li HF, Xie XH, Zheng YF, et al. Development of biodegradable Zn-1X binary alloys with nutrient alloying elements Mg, Ca and Sr. Sci Rep, 2015, 5: 10719

    Article  CAS  Google Scholar 

  102. Arciola CR, Campoccia D, Speziale P, et al. Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials, 2012, 33: 5967–5982

    Article  CAS  Google Scholar 

  103. Lin Z, Sun X, Yang H. The role of antibacterial metallic elements in simultaneously improving the corrosion resistance and antibacterial activity of magnesium alloys. Mater Des, 2021, 198: 109350

    Article  CAS  Google Scholar 

  104. Robinson DA, Griffith RW, Shechtman D, et al. In vitro antibacterial properties of magnesium metal against Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus. Acta Biomater, 2010, 6: 1869–1877

    Article  CAS  Google Scholar 

  105. Padan E, Bibi E, Ito M, et al. Alkaline pH homeostasis in bacteria: New insights. Biochim Biophys Acta, 2005, 1717: 67–88

    Article  CAS  Google Scholar 

  106. Rahim MI, Eifler R, Rais B, et al. Alkalization is responsible for antibacterial effects of corroding magnesium. J Biomed Mater Res B Appl Biomater, 2015, 103: 3526–3532

    Article  CAS  Google Scholar 

  107. Li Y, Liu G, Zhai Z, et al. Antibacterial properties of magnesium in vitro and in an in vivo model of implant-associated methicillin-resistant Staphylococcus aureus infection. Antimicrob Agents Chemother, 2014, 58: 7586–7591

    Article  CAS  Google Scholar 

  108. Demishtein K, Reifen R, Shemesh M. Antimicrobial properties of magnesium open opportunities to develop healthier food. Nutrients, 2019, 11: 2363

    Article  CAS  Google Scholar 

  109. Matevosyan L, Bazukyan I, Trchounian A. Comparative analysis of the effect of Ca and Mg ions on antibacterial activity of lactic acid bacteria isolates and their associations depending on cultivation conditions. AMB Expr, 2019, 9: 32

    Article  CAS  Google Scholar 

  110. Rodríguez-Sánchez J, Pacha-Olivenza MÁ, González-Martín ML. Bactericidal effect of magnesium ions over planktonic and sessile Staphylococcus epidermidis and Escherichia coli. Mater Chem Phys, 2019, 221: 342–348

    Article  CAS  Google Scholar 

  111. Liu C, Fu X, Pan H, et al. Biodegradable Mg-Cu alloys with enhanced osteogenesis, angiogenesis, and long-lasting antibacterial effects. Sci Rep, 2016, 6: 27374

    Article  CAS  Google Scholar 

  112. Wolf FI, Cittadini A. Chemistry and biochemistry of magnesium. Mol Aspects Med, 2003, 24: 3–9

    Article  CAS  Google Scholar 

  113. Wang G, Jiang W, Mo S, et al. Nonleaching antibacterial concept demonstrated by in situ construction of 2D nanoflakes on magnesium. Adv Sci, 2020, 7: 1902089

    Article  CAS  Google Scholar 

  114. Malagurski I, Levic S, Pantic M, et al. Synthesis and antimicrobial properties of Zn-mineralized alginate nanocomposites. Carbohydr Polym, 2017, 165: 313–321

    Article  CAS  Google Scholar 

  115. Ashfaq M, Verma N, Khan S. Highly effective Cu/Zn-carbon micro/nanofiber-polymer nanocomposite-based wound dressing biomaterial against the P. aeruginosa multi- and extensively drug-resistant strains. Mater Sci Eng-C, 2017, 77: 630–641

    Article  CAS  Google Scholar 

  116. Ghorbani FM, Kaffashi B, Shokrollahi P, et al. PCL/chitosan/Zn-doped nHA electrospun nanocomposite scaffold promotes adipose derived stem cells adhesion and proliferation. Carbohydr Polym, 2015, 118: 133–142

    Article  CAS  Google Scholar 

  117. Ning C, Wang X, Li L, et al. Concentration ranges of antibacterial cations for showing the highest antibacterial efficacy but the least cytotoxicity against mammalian cells: Implications for a new antibacterial mechanism. Chem Res Toxicol, 2015, 28: 1815–1822

    Article  CAS  Google Scholar 

  118. Sirelkhatim A, Mahmud S, Seeni A, et al. Review on zinc oxide nanoparticles: Antibacterial activity and toxicity mechanism. Nano-Micro Lett, 2015, 7: 219–242

    Article  CAS  Google Scholar 

  119. Hu H, Zhang W, Qiao Y, et al. Antibacterial activity and increased bone marrow stem cell functions of Zn-incorporated TiO2 coatings on titanium. Acta Biomater, 2012, 8: 904–915

    Article  CAS  Google Scholar 

  120. Xie Y, Li S, Zhang T, et al. Titanium mesh for bone augmentation in oral implantology: Current application and progress. Int J Oral Sci, 2020, 12: 37

    Article  Google Scholar 

  121. Lin DJ, Hung FY, Yeh ML, et al. Microstructure-modified biodegradable magnesium alloy for promoting cytocompatibility and wound healing in vitro. J Mater Sci-Mater Med, 2015, 26: 248

    Article  CAS  Google Scholar 

  122. Grzesiak JJ, Pierschbacher MD. Changes in the concentrations of extracellular Mg++ and Ca++ down-regulate E-cadherin and up-regulate α2β1 integrin function, activating keratinocyte migration on type I collagen. J Invest Dermatol, 1995, 104: 768–774

    Article  CAS  Google Scholar 

  123. Sasaki Y, Sathi GA, Yamamoto O. Wound healing effect of bioactive ion released from Mg-smectite. Mater Sci Eng-C, 2017, 77: 52–57

    Article  CAS  Google Scholar 

  124. Zhu Y, Zhang CN, Gu YX, et al. The responses of human gingival fibroblasts to magnesium-doped titanium. J Biomed Mater Res, 2020, 108: 267–278

    Article  CAS  Google Scholar 

  125. Ogawa Y, Kawamura T, Shimada S. Zinc and skin biology. Arch Biochem Biophys, 2016, 611: 113–119

    Article  CAS  Google Scholar 

  126. Ogawa Y, Kinoshita M, Shimada S, et al. Zinc and skin disorders. Nutrients, 2018, 10: 199

    Article  CAS  Google Scholar 

  127. Schwartz JR, Marsh RG, Draelos ZD. Zinc and skin health: Overview of physiology and pharmacology. Dermatol Surg, 2005, 31: 837–847

    Article  CAS  Google Scholar 

  128. Xu Q, Zheng Z, Wang B, et al. Zinc ion coordinated poly(ionic liquid) antimicrobial membranes for wound healing. ACS Appl Mater Interfaces, 2017, 9: 14656–14664

    Article  CAS  Google Scholar 

  129. Coger V, Million N, Rehbock C, et al. Tissue concentrations of zinc, iron, copper, and magnesium during the phases of full thickness wound healing in a rodent model. Biol Trace Elem Res, 2019, 191: 167–176

    Article  CAS  Google Scholar 

  130. Celiksoy V, Moses RL, Sloan AJ, et al. Evaluation of the in vitro oral wound healing effects of pomegranate (Punica granatum) rind extract and punicalagin, in combination with Zn(II). Biomolecules, 2020, 10: 1234

    Article  CAS  Google Scholar 

  131. Yao S, Chi J, Wang Y, et al. Zn-MOF encapsulated antibacterial and degradable microneedles array for promoting wound healing. Adv Healthc Mater, 2021, 10: 2100056

    Article  CAS  Google Scholar 

  132. Król A, Pomastowski P, Rafińska K, et al. Zinc oxide nanoparticles: Synthesis, antiseptic activity and toxicity mechanism. Adv Colloid Interface Sci, 2017, 249: 37–52

    Article  CAS  Google Scholar 

  133. Mehranpour MS, Heydarinia A, Emamy M, et al. Enhanced mechanical properties of AZ91 magnesium alloy by inoculation and hot deformation. Mater Sci Eng-A, 2021, 802: 140667

    Article  CAS  Google Scholar 

  134. Heimann RB. Magnesium alloys for biomedical application: Advanced corrosion control through surface coating. Surf Coat Tech, 2021, 405: 126521

    Article  CAS  Google Scholar 

  135. Atrens A, Shi Z, Mehreen SU, et al. Review of Mg alloy corrosion rates. J Magnes Alloy, 2020, 8: 989–998

    Article  CAS  Google Scholar 

  136. Song MS, Zeng RC, Ding YF, et al. Recent advances in biodegradation controls over Mg alloys for bone fracture management: A review. J Mater Sci Tech, 2019, 35: 535–544

    Article  CAS  Google Scholar 

  137. Zhang AM, Lenin P, Zeng RC, et al. Advances in hydroxyapatite coatings on biodegradable magnesium and its alloys. J Magnes Alloy, 2022

  138. Cai L, Mei D, Zhang ZQ, et al. Advances in bioorganic molecules inspired degradation and surface modifications on Mg and its alloys. J Magnes Alloy, 2022, 10: 670–688

    Article  CAS  Google Scholar 

  139. Zhang ZQ, Yang YX, Li JA, et al. Advances in coatings on magnesium alloys for cardiovascular stents—A review. Bioact Mater, 2021, 6: 4729–4757

    Article  CAS  Google Scholar 

  140. He LJ, Shao Y, Li SQ, et al. Advances in layer-by-layer self-assembled coatings upon biodegradable magnesium alloys. Sci China Mater, 2021, 64: 2093–2106

    Article  CAS  Google Scholar 

  141. Yin ZZ, Qi WC, Zeng RC, et al. Advances in coatings on biodegradable magnesium alloys. J Magnes Alloy, 2020, 8: 42–65

    Article  CAS  Google Scholar 

  142. Shao Y, Zeng RC, Li SQ, et al. Advance in antibacterial magnesium alloys and surface coatings on magnesium alloys: A review. Acta Metall Sin (Engl Lett), 2020, 33: 615–629

    Article  CAS  Google Scholar 

  143. Zhang ZQ, Wang HY, Wang L, et al. Protein conformation and electric attraction adsorption mechanisms on anodized magnesium alloy by molecular dynamics simulations. J Magnes Alloy, 2021

  144. Zhang ZQ, Wang L, Zeng MQ, et al. Biodegradation behavior of micro-arc oxidation coating on magnesium alloy—from a protein perspective. Bioact Mater, 2020, 5: 398–409

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Key R&D Program of China (2018YFC1106600), the National Natural Science Foundation of China (52071008, and U20A20390), and Beijing Natural Science Foundation (2192027).

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Authors and Affiliations

  1. Key Laboratory of Biomechanics and Mechanobiology (Beihang University), Ministry of Education, Beijing Advanced Innovation Center for Biomedical Engineering, School of Biological Science and Medical Engineering, Beihang University, Beijing, 100083, China

    Xuenan Gu  (顾雪楠), Chenyang Huang  (黄晨阳), Haoran Su  (苏皓然) & Yubo Fan  (樊瑜波)

  2. Beijing Advanced Innovation Center for Materials Genome Engineering, Institute for Advanced Materials and Technology, University of Science and Technology Beijing, Beijing, 100083, China

    Kai Chen  (陈凯) & Li Zhao  (赵莉)

  3. Department of Stomatology, The Fifth Medical Center, Chinese PLA General Hospital, Beijing, 100036, China

    Jie Sun  (孙洁)

Authors
  1. Kai Chen  (陈凯)
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  2. Li Zhao  (赵莉)
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  3. Jie Sun  (孙洁)
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  4. Xuenan Gu  (顾雪楠)
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  5. Chenyang Huang  (黄晨阳)
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  6. Haoran Su  (苏皓然)
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  7. Yubo Fan  (樊瑜波)
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Contributions

Chen K came up with the concept of this manuscript, summarized the information and literature, and prepared the manuscript. Zhao L finished the introduction section. Sun J was also involved in the collection of data and original draft preparation. Huang C and Su H discussed actively the original idea of this review, and polished the manuscript. Gu X advised the first author in the writing and provided many meaningful recommendations. Fan Y advised the idea of the review and the discussion.

Corresponding authors

Correspondence to Xuenan Gu  (顾雪楠) or Yubo Fan  (樊瑜波).

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Conflict of interest

The authors declare that they have no conflict of interest.

Kai Chen is a PhD candidate in biological science and medical engineering at Beihang University, China. His main research interests focus on the microstructure, corrosion, mechanical properties and biocompatibility of Mg and Zn-based alloys.

Xuenan Gu received her PhD degree in mechanics (bio-mechanics and biomedical engineering) from Peking University in 2011. Her research interests focus on the development of degradable metallic biomaterials and surface modification of biomedical magnesium and zinc alloys.

Yubo Fan received his PhD degree in biomechanics from Sichuan University in 1992. His research interests focus on biomechanics and mechanobiology, medical appliances, biomaterials and tissue engineering.

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Chen, K., Zhao, L., Sun, J. et al. Utilizing biodegradable alloys as guided bone regeneration (GBR) membrane: Feasibility and challenges. Sci. China Mater. 65, 2627–2646 (2022). https://doi.org/10.1007/s40843-022-2118-3

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  • DOI: https://doi.org/10.1007/s40843-022-2118-3

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