SpringerLink
Log in

Biologically enhanced 3D printed micro-nano hybrid scaffolds doped with abalone shell for bone regeneration

  • Research
  • Published:
Advanced Composites and Hybrid Materials Aims and scope Submit manuscript

Abstract

The formation of nacreous layers of abalone shell (Aba) is a similar process to the deposition of calcium salts in human bone, with the main mechanism being the orderly mineralization of inorganic matter mediated by organic bioactive components. In this study, 3D printing technology was employed to use the abundant calcium sources and bioactive substances in Aba to enhance the osteoinductive and remineralization capacity of materials in implants for bone regeneration. The novel hybrid scaffolds were successfully 3D-printed from polycaprolactone (PCL), which has good toughness and processability, doped with powdered Aba. When the Aba particle do** was increased from 0 to 15%, the physicochemical properties of PCL were virtually unchanged, while the surfaces of scaffolds became rough, and Aba particles were gradually exposed. The Aba/PCL scaffolds had an interconnected pore structure with a pore size of approximately 200 μm and over 50% porosity, which was convenient for the transport of nutrients. With the addition of Aba, the thermodynamic stability and mechanical properties of the scaffolds significantly improved, and the maximum compressive strength and modulus reached 1.34 and 1.89 MPa, respectively, because Aba provided nucleation sites for nanohydroxyapatite (nHAP) to promote mineralization. In vitro cell experiments showed that the hybrid scaffolds had good biocompatibility and promote the proliferation of osteoblasts. In vivo results revealed that the hydroxyapatite of organic matter and trace elements in Aba particles induced the migration of stem cells and active factors to the site of a bone defect. The implantation of 3D-printed scaffolds offered a microenvironment for osteoblast attachment and proliferation, which further promotes osteogenesis-related gene expression, such as bone gamma carboxyglutamate protein (BGLAP), type I collagen (COL1A1), and secreted phosphoprotein 1 (SPP1), and facilitated the repair of a skull defect. This high-value applications of Aba have the potential to improve environmental pollution and provide potentially low-cost, high-performance bone repair materials for clinical use.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Scheme 1
Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Hou Y, Shavandi A, Carne A, Bekhit AA, Ng TB, Cheung RCF, Bekhit AE-dA (2016) Marine shells: potential opportunities for extraction of functional and health-promoting materials. Crit Rev Env Sci Tec 46:1047–1116

    Article  CAS  Google Scholar 

  2. Mokhtari S, Eftekhari Yekta B, Marghussian V, Ahmadi PT (2020) Synthesis and characterization of biodegradable AZ31/calcium phosphate glass composites for orthopedic applications. Adv Compos Hybrid Ma 3(3):390–401

    Article  CAS  Google Scholar 

  3. Pei J, Wang Y, Zou X, Ruan H, Tang C, Liao J, Si G, Sun P (2021) Extraction, purification, bioactivities and application of matrix proteins from pearl powder and nacre powder: a review. Front Bioeng Biotechnol 9:649665

    Article  Google Scholar 

  4. Long J, Zhang W, Chen Y, Teng B, Liu B, Li H, Yao Z, Wang D, Li L, Yu X-F, Qin L, Lai Y (2021) Multifunctional magnesium incorporated scaffolds by 3D-Printing for comprehensive postsurgical management of osteosarcoma. Biomaterials 275:120950

    Article  CAS  Google Scholar 

  5. Lin H, Shi S, Lan X, Quan X, Xu Q, Yao G, Liu J, Shuai X, Wang C, Li X, Yu M (2021) Scaffold 3D-printed from metallic nanoparticles-containing ink simultaneously eradicates tumor and repairs tumor-associated bone defects. Small Methods 5:e2100536

    Article  Google Scholar 

  6. Yang C, Ma H, Wang Z, Younis MR, Liu C, Wu C, Luo Y, Huang P (2021) 3D printed wesselsite nanosheets functionalized scaffold facilitates NIR-II photothermal therapy and vascularized bone regeneration. Adv Sci 8:e2100894

    Article  Google Scholar 

  7. Pan P, Yue Q, Li J, Gao M, Yang X, Ren Y, Cheng X, Cui P, Deng Y (2021) Smart cargo delivery system based on mesoporous nanoparticles for bone disease diagnosis and treatment. Adv Sci 8:e2004586

    Article  Google Scholar 

  8. Espinosa HD, Rim JE, Barthelat F, Buehler MJ (2009) Merger of structure and material in nacre and bone–perspectives on de novo biomimetic materials. Prog Mater Sci 54:1059–1100

    Article  CAS  Google Scholar 

  9. Macha IJ, Ben-Nissan B (2018) Marine skeletons: towards hard tissue repair and regeneration. Mar Drugs 16:225

    Article  Google Scholar 

  10. **ng H, Yang F, Sun S, Pan P, Wang H, Wang Y, Chen J (2022) Green efficient ultrasonic-assisted extraction of abalone nacre water-soluble organic matrix for bioinspired enamel remineralization. Colloids Surf B 212:112336

    Article  CAS  Google Scholar 

  11. Ma J, Li ZJ, Xue YZB, Liang XY, Tan ZJ, Tang B (2020) Novel PEEK/nHA composites fabricated by hot-pressing of 3D braided PEEK matrix. Adv Compos Hybrid Ma 3(2):156–166

    Article  CAS  Google Scholar 

  12. Mount AS, Wheeler AP, Paradkar RP, Snider D (2004) Hemocyte-mediated shell mineralization in the eastern oyster. Science 304:297–300

    Article  CAS  Google Scholar 

  13. Zhang G, Brion A, Willemin AS, Piet MH, Moby V, Bianchi A, Mainard D, Galois L, Gillet P, Rousseau M (2017) Nacre, a natural, multi-use, and timely biomaterial for bone graft substitution. J Biomed Mater Res A 105:662–671

    Article  CAS  Google Scholar 

  14. Carson MA, Clarke SA (2018) Bioactive compounds from marine organisms: potential for bone growth and healing. Mar Drugs 16:304

    Article  Google Scholar 

  15. Barthelat F, Yin Z, Buehler MJ (2016) Structure and mechanics of interfaces in biological materials. Nat Rev Mater 1:16007

    Article  CAS  Google Scholar 

  16. Hu Y, Cao S, Chen J, Zhao Y, He F, Li Q, Zou L, Shi C (2020) Biomimetic fabrication of icariin loaded nano hydroxyapatite reinforced bioactive porous scaffolds for bone regeneration. Chem Eng J 394:124895

    Article  CAS  Google Scholar 

  17. Zhao Y, Chen J, Zou L, Xu G, Geng Y (2019) Facile one-step bioinspired mineralization by chitosan functionalized with graphene oxide to activate bone endogenous regeneration. Chem Eng J 378:122174

    Article  CAS  Google Scholar 

  18. Yang Y, Yao Q, Pu X, Hou Z, Zhang Q (2011) Biphasic calcium phosphate macroporous scaffolds derived from oyster shells for bone tissue engineering. Chem Eng J 173:837–845

    Article  CAS  Google Scholar 

  19. Du M, Li Q, Chen J, Liu K, Song C (2021) Design and characterization of injectable abalone shell/calcium sulfate bone cement scaffold for bone defect repair. Chem Eng J 420:129866

    Article  CAS  Google Scholar 

  20. Kakisawa H, Sumitomo T (2011) The toughening mechanism of nacre and structural materials inspired by nacre. Sci Technol Adv Mater 12:064710

    Article  Google Scholar 

  21. Kim H, Lee K, Ko CY, Kim HS, Shin HI, Kim T, Lee SH, Jeong D (2012) The role of nacreous factors in preventing osteoporotic bone loss through both osteoblast activation and osteoclast inactivation. Biomaterials 33:7489–7496

    Article  CAS  Google Scholar 

  22. Dimas LS, Bratzel GH, Eylon I, Buehler MJ (2013) Tough composites inspired by mineralized natural materials: computation, 3D printing, and testing. Adv Funct Mater 23:4629–4638

    Article  CAS  Google Scholar 

  23. Li L, Lu H, Zhao Y, Luo J, Yang L, Liu W, He Q (2019) Functionalized cell-free scaffolds for bone defect repair inspired by self healing of bone fractures: a review and new perspectives. Mater Sci Eng C 98:1241–1251

    Article  CAS  Google Scholar 

  24. Vaquette C, Bock N, Tran PA (2020) Layered antimicrobial selenium nanoparticle-calcium phosphate coating on 3d printed scaffolds enhanced bone formation in critical size defects. ACS Appl Mater Interfaces 12:55638–55648

    Article  CAS  Google Scholar 

  25. Wang Q, Ma Z, Wang Y, Zhong L, **e W (2020) Fabrication and characterization of 3D printed biocomposite scaffolds based on PCL and zirconia nanoparticles. Bio Des Manuf 4:60–71

    Article  Google Scholar 

  26. Yan Y, Chen H, Zhang H, Guo C, Yang K, Chen K, Cheng R, Qian N, Sandler N, Zhang YS, Shen H, Qi J, Cui W, Deng L (2019) Vascularized 3D printed scaffolds for promoting bone regeneration. Biomaterials 190:97–110

    Article  Google Scholar 

  27. Bartnikowski M, Dargaville TR, Ivanovski S, Hutmacher DW (2019) Degradation mechanisms of polycaprolactone in the context of chemistry, geometry and environment. Prog Poly Sci 96:1–20

    Article  CAS  Google Scholar 

  28. Yang T, Hu Y, Wang C, Binks BP (2017) Fabrication of hierarchical macroporous biocompatible scaffolds by combining pickering high internal phase emulsion templates with three-dimensional printing. ACS Appl Mater Interfaces 9:22950–22958

    Article  CAS  Google Scholar 

  29. Ahn J-H, Kim J, Han G, Kim D, Cheon K-H, Lee H, Kim H-E, Kim Y-J, Jang T-S, Jung H-D (2021) 3D-printed biodegradable composite scaffolds with significantly enhanced mechanical properties via the combination of binder jetting and capillary rise infiltration process. Addit Manuf 41:101988

    CAS  Google Scholar 

  30. Kuang T, Chen S, Gu Z, Shen Z, Hejna A, Saeb MR, Chen F, Zhong M, Liu T (2022) A facile approach to fabricate load-bearing porous polymer scaffolds for bone tissue engineering. Adv Compos Hybrid Ma 3(4):170–181

    Google Scholar 

  31. Kim D, Lee J, Min Seok J, Jung J-Y, Hee Lee J, Sik Lee J, Lee K, Park SA (2021) Three-dimensional bioprinting of bioactive scaffolds with thermally embedded abalone shell particles for bone tissue engineering. Mater Des 212:110228

    Article  CAS  Google Scholar 

  32. Zou L, Hu L, Pan P, Tarafder S, Du M, Geng Y, Xu G, Chen L, Chen J, Lee CH (2022) Icariin-releasing 3D printed scaffold for bone regeneration. Compos B Eng 232:109625

    Article  CAS  Google Scholar 

  33. Dadhich P, Srivas PK, Das B, Pal P, Dutta J, Maity P, Guha Ray P, Roy S, Das SK, Dhara S (2021) Direct 3D printing of seashell precursor toward engineering a multiphasic calcium phosphate bone graft. ACS Biomater Sci Eng 7:3806–3820

    Article  CAS  Google Scholar 

  34. Liu D, Nie W, Li D, Wang W, Zheng L, Zhang J, Zhang J, Peng C, Mo X, He C (2019) 3D printed PCL/SrHA scaffold for enhanced bone regeneration. Chem Eng J 362:269–279

    Article  CAS  Google Scholar 

  35. Ahmed MK, Zayed MA, El-Dek SI, Hady MA, El Sherbiny DH, Uskokovic V (2021) Nanofibrous epsilon-polycaprolactone scaffolds containing Ag-doped magnetite nanoparticles: physicochemical characterization and biological testing for wound dressing applications in vitro and in vivo. Bioact Mater 6(7):2070–2088

    Article  CAS  Google Scholar 

  36. Wang H, Yan K, **ng H, Chen J, Lu R (2021) Effective removal of Cu2+ from aqueous solution by synthetic abalone shell hydroxyapatite microspheres adsorbent. Environ Technol Inno 23:101663

    Article  CAS  Google Scholar 

  37. Lai Y, Cao H, Wang X, Chen S, Zhang M, Wang N, Yao Z, Dai Y, **e X, Zhang P, Yao X, Qin L (2018) Porous composite scaffold incorporating osteogenic phytomolecule icariin for promoting skeletal regeneration in challenging osteonecrotic bone in rabbits. Biomaterials 153:1–13

    Article  CAS  Google Scholar 

  38. Peng C, Zheng J, Chen D, Zhang X, Deng L, Chen Z, Wu L (2018) Response of hPDLSCs on 3D printed PCL/PLGA composite scaffolds in vitro. Mol Med Rep 18:1335–1344

    CAS  Google Scholar 

Download references

Funding

This work was supported by Natural Science Foundation of Shandong Province (no. ZR2022QD057), the Open Project Fund for Hubei Key Laboratory of Oral and Maxillofacial Development and Regeneration (No. 2021kqhm003), the State Key Laboratory of Advanced Technology for Materials Synthesis and Processing (Wuhan University of Technology), the Physical Chemical Materials Analytical and Testing Center of Shandong University at Weihai, China Postdoctoral Science Foundation (2022M722434) and the Science Fund of Shandong Laboratory of Advanced Materials and Green Manufacturing (Yantai, No. AMGM2021F02).

Author information

Authors and Affiliations

  1. Marine College, Shandong University, Weihai, 264209, China

    Panpan Pan, Le Hu, Qing Liu, Man Liu, Meiqi Cheng & **gdi Chen

  2. Weihai Changqing Ocean Science Technology Co., Ltd., Rongcheng, 264300, China

    Panpan Pan

  3. Shandong Laboratory of Advanced Materials and Green Manufacturing, Yantai, 265599, China

    **gdi Chen

  4. Hubei Province Key Laboratory of Oral and Maxillofacial Development and Regeneration, Wuhan, 430022, China

    Panpan Pan

  5. College of Biological Science and Technology, Fuzhou University, Fuzhou, 350108, China

    Yusheng Geng & Li Chen

Authors
  1. Panpan Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yusheng Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Le Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Man Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meiqi Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Li Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. **gdi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.P. wrote the main manuscript text. Y.G. and L.H. conceived and designed research. Q.L., M.L., L.C., and M.C. conducted experiments. J.C. contributed new reagents or analytical tools. All authors reviewed the manuscript.

Corresponding author

Correspondence to **gdi Chen.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 964 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pan, P., Geng, Y., Hu, L. et al. Biologically enhanced 3D printed micro-nano hybrid scaffolds doped with abalone shell for bone regeneration. Adv Compos Hybrid Mater 6, 10 (2023). https://doi.org/10.1007/s42114-022-00593-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s42114-022-00593-1

Keywords

Search

Navigation