Nanosurfaces Modulate the Mechanism of Peri-implant Endosseous Healing by Regulating Neovascular Morphogenesis

Overview

Journal Commun Biol

Specialty Biology

Date 2018 Oct 2

PMID 30271953

Citations 16

Authors

Niloufar Khosravi

Azusa Maeda

Ralph S DaCosta

John E Davies

Affiliations

Soon will be listed here.

Abstract

Nanosurfaces have improved clinical osseointegration by increasing bone/implant contact. Neovascularization is considered an essential prerequisite to osteogenesis, but no previous reports to our knowledge have examined the effect of surface topography on the spatio-temporal pattern of neovascularization during peri-implant healing. We have developed a cranial window model to study peri-implant healing intravitally over clinically relevant time scales as a function of implant topography. Quantitative intravital confocal imaging reveals that changing the topography (but not chemical composition) of an implant profoundly affects the pattern of peri-implant neovascularization. New vessels develop proximal to the implant and the vascular network matures sooner in the presence of an implant nanosurface. Accelerated angiogenesis can lead to earlier osseointegration through the delivery of osteogenic precursors to, and direct formation of bone on, the implant surface. This study highlights a critical aspect of peri-implant healing, but also informs the biological rationale for the surface design of putative endosseous implant materials.

Citing Articles

Surface modifications and coatings to improve osseointegration and antimicrobial activity on titanium surfaces: A statistical review over the last decade.

Raju K, Biswas A J Orthop. 2025; 67:68-87.

PMID: 39902142 PMC: 11787716. DOI: 10.1016/j.jor.2025.01.002.

Cell-based therapy in the treatment of musculoskeletal diseases.

Trapana J, Weinerman J, Lee D, Sedani A, Constantinescu D, Best T Stem Cells Transl Med. 2024; 13(10):959-978.

PMID: 39226104 PMC: 11465182. DOI: 10.1093/stcltm/szae049.

Multifunctional surface of the nano-morphic PEEK implant with enhanced angiogenic, osteogenic and antibacterial properties.

Zhang J, Ma T, Liu X, Zhang X, Meng W, Wu J Regen Biomater. 2024; 11:rbae067.

PMID: 38974666 PMC: 11226884. DOI: 10.1093/rb/rbae067.

3D printing metal implants in orthopedic surgery: Methods, applications and future prospects.

Meng M, Wang J, Huang H, Liu X, Zhang J, Li Z J Orthop Translat. 2023; 42:94-112.

PMID: 37675040 PMC: 10480061. DOI: 10.1016/j.jot.2023.08.004.

Multiscale morphological analysis of bone microarchitecture around Mg-10Gd implants.

Sefa S, Espiritu J, Cwieka H, Greving I, Flenner S, Will O Bioact Mater. 2023; 30:154-168.

PMID: 37575877 PMC: 10412723. DOI: 10.1016/j.bioactmat.2023.07.017.

References

Kassab G . Scaling laws of vascular trees: of form and function. Am J Physiol Heart Circ Physiol. 2005; 290(2):H894-903. DOI: 10.1152/ajpheart.00579.2005. View

Winkler I, Barbier V, Wadley R, Zannettino A, Williams S, Levesque J . Positioning of bone marrow hematopoietic and stromal cells relative to blood flow in vivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood. 2010; 116(3):375-85. DOI: 10.1182/blood-2009-07-233437. View

Holstein J, Becker S, Fiedler M, Garcia P, Histing T, Klein M . Intravital microscopic studies of angiogenesis during bone defect healing in mice calvaria. Injury. 2010; 42(8):765-71. DOI: 10.1016/j.injury.2010.11.020. View

Crisan M, Chen C, Corselli M, Andriolo G, Lazzari L, Peault B . Perivascular multipotent progenitor cells in human organs. Ann N Y Acad Sci. 2009; 1176:118-23. DOI: 10.1111/j.1749-6632.2009.04967.x. View

Bauer S, Bauer R, Velazquez O . Angiogenesis, vasculogenesis, and induction of healing in chronic wounds. Vasc Endovascular Surg. 2005; 39(4):293-306. DOI: 10.1177/153857440503900401. View

Mantripragada V, Lecka-Czernik B, Ebraheim N, Jayasuriya A . An overview of recent advances in designing orthopedic and craniofacial implants. J Biomed Mater Res A. 2013; 101(11):3349-64. PMC: 4854641. DOI: 10.1002/jbm.a.34605. View

Davies J . Mechanisms of endosseous integration. Int J Prosthodont. 1999; 11(5):391-401. View

Djonov V, Andres A, Ziemiecki A . Vascular remodelling during the normal and malignant life cycle of the mammary gland. Microsc Res Tech. 2001; 52(2):182-9. DOI: 10.1002/1097-0029(20010115)52:2<182::AID-JEMT1004>3.0.CO;2-M. View

Patan S, Tanda S, Roberge S, Jones R, Jain R, Munn L . Vascular morphogenesis and remodeling in a human tumor xenograft: blood vessel formation and growth after ovariectomy and tumor implantation. Circ Res. 2001; 89(8):732-9. PMC: 2752899. DOI: 10.1161/hh2001.097872. View

10.

Guimaraes-Camboa N, Cattaneo P, Sun Y, Moore-Morris T, Gu Y, Dalton N . Pericytes of Multiple Organs Do Not Behave as Mesenchymal Stem Cells In Vivo. Cell Stem Cell. 2017; 20(3):345-359.e5. PMC: 5337131. DOI: 10.1016/j.stem.2016.12.006. View

11.

Tonnesen M, Feng X, Clark R . Angiogenesis in wound healing. J Investig Dermatol Symp Proc. 2001; 5(1):40-6. DOI: 10.1046/j.1087-0024.2000.00014.x. View

12.

McKenzie J, Fruttiger M, Abraham S, Lange C, Stone J, Gandhi P . Apelin is required for non-neovascular remodeling in the retina. Am J Pathol. 2011; 180(1):399-409. PMC: 3244602. DOI: 10.1016/j.ajpath.2011.09.035. View

13.

Bennett R, Robbins A, Hu M, Cao X, Betensky R, Clark T . Tau induces blood vessel abnormalities and angiogenesis-related gene expression in P301L transgenic mice and human Alzheimer's disease. Proc Natl Acad Sci U S A. 2018; 115(6):E1289-E1298. PMC: 5819390. DOI: 10.1073/pnas.1710329115. View

14.

Peng L, Barczak A, Barbeau R, Xiao Y, LaTempa T, Grimes C . Whole genome expression analysis reveals differential effects of TiO2 nanotubes on vascular cells. Nano Lett. 2009; 10(1):143-8. PMC: 2833360. DOI: 10.1021/nl903043z. View

15.

Liddell R, Ajami E, Davies J . Tau (τ): A New Parameter to Assess the Osseointegration Potential of an Implant Surface. Int J Oral Maxillofac Implants. 2016; 32(1):102-112. DOI: 10.11607/jomi.4746. View

16.

Kochhan E, Lenard A, Ellertsdottir E, Herwig L, Affolter M, Belting H . Blood flow changes coincide with cellular rearrangements during blood vessel pruning in zebrafish embryos. PLoS One. 2013; 8(10):e75060. PMC: 3795766. DOI: 10.1371/journal.pone.0075060. View

17.

Kim T, Singh R, Kang M, Kim J, Kim H . Gene delivery nanocarriers of bioactive glass with unique potential to load BMP2 plasmid DNA and to internalize into mesenchymal stem cells for osteogenesis and bone regeneration. Nanoscale. 2016; 8(15):8300-11. DOI: 10.1039/c5nr07933k. View

18.

Nygren H, Eriksson C, Lausmaa J . Adhesion and activation of platelets and polymorphonuclear granulocyte cells at TiO2 surfaces. J Lab Clin Med. 1997; 129(1):35-46. DOI: 10.1016/s0022-2143(97)90159-1. View

19.

Maeda A, Leung M, Conroy L, Chen Y, Bu J, Lindsay P . In vivo optical imaging of tumor and microvascular response to ionizing radiation. PLoS One. 2012; 7(8):e42133. PMC: 3425534. DOI: 10.1371/journal.pone.0042133. View

20.

Umoh J, Sampaio A, Welch I, Pitelka V, Goldberg H, Underhill T . In vivo micro-CT analysis of bone remodeling in a rat calvarial defect model. Phys Med Biol. 2009; 54(7):2147-61. DOI: 10.1088/0031-9155/54/7/020. View