Skip to main content

Advertisement

SpringerLink
Log in

Synthesis and characterization of fish scales of hydroxyapatite/ collagen–silver nanoparticles composites for the applications of bone filler

  • Original Article
  • Published:
Journal of the Korean Ceramic Society Aims and scope Submit manuscript

Abstract

The most implanted tissue after blood is a bone, which consists of collagen and hydroxyapatite as the major components. Collagen is a nature-based polymer that is available in skin and tendons, whereas hydroxyapatite is a natural ceramic that is available abundantly in teeth. The composites of hydroxyapatite/collagen (HA/Col) have been reported to be the most encouraging bone graft because of the likenesses with the natural bones. Furthermore, the integration of the nano silvers in the composites’ matrix has been predicted to lead to antimicrobial reactions. This study combined the natural fish scales hydroxyapatite (FsHAp), fish scale collagen (FsCol), and nanosilver (Ag) to develop the composites of FsHAp/FsCol/nAg with various ratios of content. FTIR, XRD, EDX, and SEM were employed to identify the chemical structure and morphology of the tested composites. Similar processes were conducted to study the swelling ratio, biostability, and antibacterial features of the composites. The cytotoxicity of the FsHAp/FsCol/AgNPs composites was evaluated using Alamar blue assay. The outcome revealed that 80:20 of the HA/Col composite showed higher stability than other ratio compositions. The morphology of the composites demonstrated a homogeneous surface with nanosilvers scattered evenly in the matrix. Additionally, the activities of the antimicrobial in the composites were found against Escherichia coli (E. coli) and Staphylococcus aureus (S. aureus). For the cytotoxicity study, the composites showed non-toxic effects on MG-63 human cells at high concentrations.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8.
Fig.9

Similar content being viewed by others

References

  1. S. Batool, U. Liaqat, B. Babar, Z. Hussain, Bone whitlockite: synthesis, applications, and future prospects. J. Korean Ceram. Soc. 58, 1–18 (2021)

    Article  Google Scholar 

  2. S. Swain, R.N. Padhy, T.R. Rautray, Electrically stimulated hydroxyapatite–barium titanate composites demonstrate immunocompatibility in vitro. J. Korean Ceram. Soc. 57(5), 495–502 (2020)

    Article  CAS  Google Scholar 

  3. J. Venkatesan, S.K. Kim, Chitosan composites for bone tissue engineering—an overview. Mar. Drugs 8(8), 2252–2266 (2010)

    Article  CAS  Google Scholar 

  4. S.C. Wu, H.C. Hsu, M.Y. Liu, W.F. Ho, Characterization of nanosized hydroxyapatite prepared by an aqueous precipitation method using eggshells and mulberry leaf extract. J. Korean Ceram. Soc. 58(1), 116–122 (2021)

    Article  CAS  Google Scholar 

  5. T.U. Habibah, H.G. Salisbury, Dental materials, hydroxyapatite (2018)

  6. S. Higashi, T. Yamamuro, T. Nakamura, Y. Ikada, S.H. Hyon, K. Jamshidi, Polymer-hydroxyapatite composites for biodegradable bone fillers. Biomaterials 7(3), 183–187 (1986)

    Article  CAS  Google Scholar 

  7. M.E. Butini, S. Cabric, A. Trampuz, M. Di Luca, In vitro anti-biofilm activity of a biphasic gentamicin-loaded calcium sulfate/hydroxyapatite bone graft substitute. Colloids Surf. B 161, 252–260 (2018)

    Article  CAS  Google Scholar 

  8. C.C. Coelho, R. Araújo, P.A. Quadros, S.R. Sousa, F.J. Monteiro, Antibacterial bone substitute of hydroxyapatite and magnesium oxide to prevent dental and orthopaedic infections. Mater. Sci. Eng. C 97, 529–538 (2019)

    Article  CAS  Google Scholar 

  9. K.R. Mohamed, H.H. Beherei, Z.M. El-Rashidy, In vitro study of nano-hydroxyapatite/chitosan–gelatin composites for bio-applications. J. Adv. Res. 5(2), 201–208 (2014)

    Article  CAS  Google Scholar 

  10. H. Bundela, A.K. Bajpai, Designing of hydroxyapatite-gelatin based porous matrix as bone substitute: correlation with biocompatibility aspects. Express Polym. Lett. 2(3), 201–213 (2008)

    Article  CAS  Google Scholar 

  11. C.C. Coelho, L. Grenho, P.S. Gomes, P.A. Quadros, M.H. Fernandes, Nano-hydroxyapatite in oral care cosmetics: characterization and cytotoxicity assessment. Sci. Rep. 9(1), 1–10 (2019)

    Article  Google Scholar 

  12. I. Zainon, N.M. Alwi, M.Z. Abidin, H.M.Z. Haniza, M.S. Ahmad, A. Ramli, Physicochemical properties of hydroxyapatite extracted from fish scales. Adv Mater Res 545, 235–239 (2012)

    Article  Google Scholar 

  13. X. Liu, C. Zheng, X. Luo, X. Wang, H. Jiang, Recent advances of collagen-based biomaterials: multi-hierarchical structure, modification and biomedical applications. Mater. Sci. Eng. C 99, 1509–1522 (2019)

    Article  CAS  Google Scholar 

  14. X. Chen, L. Zhou, H. Xu, M. Yamamoto, M. Shinoda, M. Kishimoto, T. Tanaka, H. Yamane, Effect of the application of a dehydrothermal treatment on the structure and the mechanical properties of collagen film. Materials 13(2), 377 (2020)

    Article  CAS  Google Scholar 

  15. N. Baheiraei, M.R. Nourani, S.M.J. Mortazavi, M. Movahedin, H. Eyni, F. Bagheri, M.H. Norahan, Development of a bioactive porous collagen/β-tricalcium phosphate bone graft assisting rapid vascularization for bone tissue engineering applications. J. Biomed. Mater. Res. Part A 106(1), 73–85 (2018)

    Article  CAS  Google Scholar 

  16. Y. Guo, Y. Su, R. Gu, Z. Zhang, G. Li, J. Lian, L. Ren, Enhanced corrosion resistance and biocompatibility of biodegradable magnesium alloy modified by calcium phosphate/collagen coating. Surf. Coat. Technol. 401, 126318 (2020)

    Article  CAS  Google Scholar 

  17. J. Wang, X. Sun, Z. Zhang, Y. Wang, C. Huang, C. Yang, L. Liu, Q. Zhang, Silk fibroin/collagen/hyaluronic acid scaffold incorporating pilose antler polypeptides microspheres for cartilage tissue engineering. Mater. Sci. Eng. C 94, 35–44 (2019)

    Article  CAS  Google Scholar 

  18. S. Ullah, I. Zainol, S.R. Chowdhury, M.B. Fauzi, Development of various composition multicomponent chitosan/fish collagen/glycerin 3D porous scaffolds: Effect on morphology, mechanical strength, biostability and cytocompatibility. Int. J. Biol. Macromol. 111, 158–168 (2018)

    Article  CAS  Google Scholar 

  19. C. Zhou, X. Ye, Y. Fan, L. Ma, Y. Tan, F. Qing, X. Zhang, Biomimetic fabrication of a three-level hierarchical calcium phosphate/collagen/hydroxyapatite scaffold for bone tissue engineering. Biofabrication 6(3), 035013 (2014)

    Article  CAS  Google Scholar 

  20. S.S. Liao, F.Z. Cui, In vitro and in vivo degradation of mineralized collagen-based composite scaffold: nanohydroxyapatite/collagen/poly (L-lactide). Tissue Eng. 10(1–2), 73–80 (2004)

    Article  CAS  Google Scholar 

  21. G.E. Dubinenko, A.L. Zinoviev, E.N. Bolbasov, V.T. Novikov, S.I. Tverdokhlebov, Preparation of poly (L-lactic acid)/hydroxyapatite composite scaffolds by fused deposit modeling 3D printing. Mater. Today Proc. 22, 228–234 (2020)

    Article  CAS  Google Scholar 

  22. W. Song, D.C. Markel, S. Wang, T. Shi, G. Mao, W. Ren, Electrospun polyvinyl alcohol–collagen–hydroxyapatite nanofibers: a biomimetic extracellular matrix for osteoblastic cells. Nanotechnology 23(11), 115101 (2012)

    Article  Google Scholar 

  23. H. Xie, X. Chen, X. Shen, Y. He, W. Chen, Q. Luo, W. Ge, W. Yuan, X. Tang, D. Hou, D. Jiang, Preparation of chitosan-collagen-alginate composite dressing and its promoting effects on wound healing. Int. J. Biol. Macromol. 107, 93–104 (2018)

    Article  CAS  Google Scholar 

  24. A. Tampieri, M. Iafisco, M. Sandri, S. Panseri, C. Cunha, S. Sprio, E. Savini, M. Uhlarz, T. Herrmannsdörfer, Magnetic bioinspired hybrid nanostructured collagen–hydroxyapatite scaffolds supporting cell proliferation and tuning regenerative process. ACS Appl. Mater. Interfaces. 6(18), 15697–15707 (2014)

    Article  CAS  Google Scholar 

  25. K. Singh, M. Panghal, S. Kadyan, U. Chaudhary, J.P. Yadav, Green silver nanoparticles of Phyllanthus amarus: as an antibacterial agent against multi drug resistant clinical isolates of Pseudomonas aeruginosa. J. Nanobiotechnol. 12(1), 1–9 (2014)

    Article  Google Scholar 

  26. A. Haider, I.K. Kang, Preparation of silver nanoparticles and their industrial and biomedical applications: a comprehensive review. Adv. Mater. Sci. Eng. 2015(1), 1–17 (2015)

    Article  Google Scholar 

  27. M. Mudhafar, I. Zainol, C.N. Aiza Jaafar, H.A. Alsailawi, A.A. Majhool, Two green synthesis methods to prepared nanoparticles of Ag: two sizes and shapes via using extract of M. dubia leaves. J. Comput. Theor. Nanosci. 17(7), 2882–2889 (2020)

    Article  CAS  Google Scholar 

  28. I. Zainol, N.H. Adenan, N.A. Rahim, C.A. Jaafar, Extraction of natural hydroxyapatite from tilapia fish scales using alkaline treatment. Mater. Today Proc. 16, 1942–1948 (2019)

    Article  CAS  Google Scholar 

  29. R.N. Granito, A.C.M. Renno, H. Yamamura, M.C. de Almeida, P.L.M. Ruiz, D.A. Ribeiro, Hydroxyapatite from fish for bone tissue engineering: a promising approach. Int. J. Mol. Cell. Med. 7(2), 80 (2018)

    CAS  Google Scholar 

  30. Y. Liu, M. Liu, S. Ji, L. Zhang, W. Cao, H. Wang, S. Wang, Preparation and application of hydroxyapatite extracted from fish scale waste using deep eutectic solvents. Ceram. Int. 47(7), 9366–9372 (2021)

    Article  CAS  Google Scholar 

  31. J.A. Da Cruz, W.R. Weinand, A.M. Neto, R.S. Palácios, A.J.M. Sales, P.R. Prezas, M.M. Costa, M.P.F. Graça, Low-cost hydroxyapatite powders from tilapia fish. JOM 72(4), 1435–1442 (2020)

    Article  Google Scholar 

  32. N.N. Panda, K. Pramanik, L.B. Sukla, Extraction and characterization of biocompatible hydroxyapatite from fresh water fish scales for tissue engineering scaffold. Bioprocess Biosyst. Eng. 37(3), 433–440 (2014)

    Article  CAS  Google Scholar 

  33. S. Shahabi, F. Najafi, A. Majdabadi, T. Hooshmand, B. Karimi, S.M. Fatemi, Effect of gamma irradiation on structural and biological properties of a PLGA-PEG-hydroxyapatite composite. Sci. World J. 2014, 420616–420616 (2014)

    Article  Google Scholar 

  34. G. Ramanathan, S. Singaravelu, M.D. Raja, S.S. Sobhana, U.T. Sivagnanam, Extraction and characterization of collagen from the skin of Arothron stellatus fish—a novel source of collagen for tissue engineering. J. Biomater. Tissue Eng. 4(3), 203–209 (2014)

    Article  CAS  Google Scholar 

  35. A.L. Alves, A.L. Marques, E. Martins, T.H. Silva, R.L. Reis, Cosmetic potential of marine fish skin collagen. Cosmetics 4(4), 39 (2017)

    Article  Google Scholar 

  36. M.P. Das, K. Prasad, J.V. Vijaylakshmi, M. Renuka, P.R. Suguna, A study on assessment of propriety of fish scale collagen. Res. J. Pharm. Biol. Chem. Sci. 8(2), 2473–2479 (2017)

    CAS  Google Scholar 

  37. N. Muhammad, G. Gonfa, A. Rahim, P. Ahmad, F. Iqbal, F. Sharif, A.S. Khan, F.U. Khan, Z.U.H. Khan, F. Rehman, I.U. Rehman, Investigation of ionic liquids as a pretreatment solvent for extraction of collagen biopolymer from waste fish scales using COSMO-RS and experiment. J. Mol. Liq. 232, 258–264 (2017)

    Article  CAS  Google Scholar 

  38. A. Saxena, R.M. Tripathi, F. Zafar, P. Singh, Green synthesis of silver nanoparticles using aqueous solution of Ficus benghalensis leaf extract and characterization of their antibacterial activity. Mater. Lett. 67(1), 91–94 (2012)

    Article  CAS  Google Scholar 

  39. A.M. Awwad, N.M. Salem, Green synthesis of silver nanoparticles by Mulberry leaves extract. Nanosci. Nanotechnol. 2(4), 125–128 (2012)

    Article  CAS  Google Scholar 

  40. A.M. Awwad, N.M. Salem, A.O. Abdeen, Green synthesis of silver nanoparticles using carob leaf extract and its antibacterial activity. Int. J. Ind. Chem. 4(1), 29 (2013)

    Article  Google Scholar 

  41. P. Logeswari, S. Silambarasan, J. Abraham, Synthesis of silver nanoparticles using plants extract and analysis of their antimicrobial property. J. Saudi Chem. Soc. 19(3), 311–317 (2015)

    Article  Google Scholar 

  42. Y. Azis, N. Jamarun, S. Arief, H. Nur, Facile synthesis of hydroxyapatite particles from cockle shells (Anadaragranosa) by hydrothermal method. Orient. J. Chem. 31(2), 1099–1105 (2015)

    Article  CAS  Google Scholar 

  43. T. Riaz, R. Zeeshan, F. Zarif, K. Ilyas, N. Muhammad, S.Z. Safi, A. Rahim, S.A. Rizvi, I.U. Rehman, FTIR analysis of natural and synthetic collagen. Appl. Spectrosc. Rev. 53(9), 703–746 (2018)

    Article  CAS  Google Scholar 

  44. M.A. Odeniyi, V.C. Okumah, B.C. Adebayo-Tayo, O.A. Odeniyi, Green synthesis and cream formulations of silver nanoparticles of Nauclea latifolia (African peach) fruit extracts and evaluation of antimicrobial and antioxidant activities. Sustain. Chem. Pharm. 15, 100197 (2020)

    Article  Google Scholar 

  45. Z. Fang, Y. Wang, Q. Feng, A. Kienzle, W.E. Müller, Hierarchical structure and cytocompatibility of fish scales from Carassius auratus. Mater. Sci. Eng. C 43, 145–152 (2014)

    Article  CAS  Google Scholar 

  46. S. Mondal, S. Mahata, S. Kundu, B. Mondal, Processing of natural resourced hydroxyapatite ceramics from fish scale. Adv. Appl. Ceram. 109(4), 234–239 (2010)

    Article  CAS  Google Scholar 

  47. M. Mudhafar, I. Zainol, Medical values, antimicrobial, and anti-fungal activities of Genus. Polyalthia Int. J. Pharm. Res. 11(1), 90–96 (2019)

    Google Scholar 

  48. A. Sionkowska, J. Kozłowska, Characterization of collagen/hydroxyapatite composite sponges as a potential bone substitute. Int. J. Biol. Macromol. 47(4), 483–487 (2010)

    Article  CAS  Google Scholar 

  49. L.A. Sena, M.M. Caraballo, A.M. Rossi, G.A. Soares, Synthesis and characterization of biocomposites with different hydroxyapatite–collagen ratios. J. Mater. Sci. Mater. Med. 20(12), 2395 (2009)

    Article  CAS  Google Scholar 

  50. F. Pishbin, V. Mourino, J.B. Gilchrist, D.W. McComb, S. Kreppel, V. Salih, M.P. Ryan, A.R. Boccaccini, Single-step electrochemical deposition of antimicrobial orthopaedic coatings based on a bioactive glass/chitosan/nano-silver composite system. Acta Biomater. 9(7), 7469–7479 (2013)

    Article  CAS  Google Scholar 

  51. L. Moldovan, O. Craciunescu, E.I. Oprita, M. Balan, O. Zarnescu, Collagen-chondroitin sulfate-hydroxyapatite porous composites: preparation, characterization and in vitro biocompatibility testing. Roum. Biotechnol. Lett. 14(3), 4459–4466 (2009)

    Google Scholar 

  52. S.C. Rodrigues, C.L. Salgado, A. Sahu, M.P. Garcia, M.H. Fernandes, F.J. Monteiro, Preparation and characterization of collagen-nanohydroxyapatite biocomposite scaffolds by cryogelation method for bone tissue engineering applications. J. Biomed. Mater. Res. Part A 101(4), 1080–1094 (2013)

    Article  Google Scholar 

  53. S. Pramanik, P. Agarwala, K. Vasudevan, K. Sarkar, Human-lymphocyte cell friendly starch–hydroxyapatite biodegradable composites: hydrophilic mechanism, mechanical, and structural impact. J. Appl. Polym. Sci. 137(30), 48913 (2020)

    Article  CAS  Google Scholar 

  54. T.T. Li, Y. Zhang, H.T. Ren, H.K. Peng, C.W. Lou, J.H. Lin, Two-step strategy for constructing hierarchical pore structured chitosan–hydroxyapatite composite scaffolds for bone tissue engineering. Carbohydr Polym 260, 117765 (2021)

    Article  CAS  Google Scholar 

  55. F. Ghorbani, A. Zamanian, A. Behnamghader, M.D. Joupari, Bioactive and biostable hyaluronic acid-pullulan dermal hydrogels incorporated with biomimetic hydroxyapatite spheres. Mater. Sci. Eng. C 112, 110906 (2020)

    Article  CAS  Google Scholar 

  56. A. Mocanu, G. Furtos, S. Rapuntean, O. Horovitz, C. Flore, C. Garbo, A. Danisteanu, G. Rapuntean, C. Prejmerean, M. Tomoaia-Cotisel, Synthesis; characterization and antimicrobial effects of composites based on multi-substituted hydroxyapatite and silver nanoparticles. Appl. Surf. Sci. 298, 225–235 (2014)

    Article  CAS  Google Scholar 

  57. C.S. Ciobanu, F. Massuyeau, L.V. Constantin, D. Predoi, Structural and physical properties of antibacterial Ag-doped nano-hydroxyapatite synthesized at 100 C. Nanoscale Res. Lett. 6(1), 1–8 (2011)

    Article  Google Scholar 

  58. G. Ciobanu, M. Harja, Cerium-doped hydroxyapatite/collagen coatings on titanium for bone implants. Ceram. Int. 45(2), 2852–2857 (2019)

    Article  CAS  Google Scholar 

  59. E. Andronescu, A. Ficai, M.G. Albu, V. Mitran, M. Sonmez, D. Ficai, R. Ion, A. Cimpean, Collagen-hydroxyapatite/cisplatin drug delivery systems for locoregional treatment of bone cancer. Technol. Cancer Res. Treat. 12(4), 275–284 (2013)

    Article  CAS  Google Scholar 

  60. R. Vivek, R. Thangam, K. Muthuchelian, P. Gunasekaran, K. Kaveri, S. Kannan, Green biosynthesis of silver nanoparticles from Annona squamosa leaf extract and its in vitro cytotoxic effect on MCF-7 cells. Process Biochem. 47(12), 2405–2410 (2012)

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anesthesia and Intensive Care Techniques, Faculty of Al-Tuff Collage, Karbala, 56001, Iraq

    Mustafa Mudhafar PhD & H. A. Alsailawi

  2. Department of Chemistry, Faculty of Science and Mathematics, Universiti Pendidikan Sultan Idris, Tanjung Malim, Perak, Proton, 35900, Malaysia

    Ismail Zainol

  3. Department of Mechanical and Manufacturing Engineering, Faculty of Engineering, Universiti Putra Malaysia, Serdang Selangor, Karbala, 43000, Malaysia

    C. N. Aiza Jaafar

Authors
  1. Mustafa Mudhafar PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ismail Zainol
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. A. Alsailawi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. N. Aiza Jaafar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mustafa Mudhafar PhD.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mudhafar, M., Zainol, I., Alsailawi, H.A. et al. Synthesis and characterization of fish scales of hydroxyapatite/ collagen–silver nanoparticles composites for the applications of bone filler. J. Korean Ceram. Soc. 59, 229–239 (2022). https://doi.org/10.1007/s43207-021-00154-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43207-021-00154-0

Keywords

Search

Navigation