Skip to main content
SpringerLink
Log in

Collagen from Atlantic cod (Gadus morhua) skins extracted using CO2 acidified water with potential application in healthcare

  • Original Paper
  • Published:
Journal of Polymer Research Aims and scope Submit manuscript

Abstract

The extraction of collagen from fish skins is being proposed as strategy for valorization of marine origin by-products, being a sustainable alternative to mammal collagen. The method commonly uses solutions of organic acids, but new methodologies are arising, aiming to improve process yields and/or the properties of the resulting products. In this work, skins removed from salt brine Atlantic cod (Gadus morhua) were used to extract collagen, using water acidified with CO2, obtaining an extraction yield of 13.8% (w/w). Acidified water extracted collagen (AWC) presented a total content of proline-like amino acids of 151/1000 residues, with a degree of hydroxylation of 38%, and its SDS-PAGE profile is compatible with type I collagen. Moreover, FTIR, CD and XRD results suggest the presence of preserved triple helix, having a denaturation temperature of 32.3 °C as determined by micro-DSC. AWC exhibited a typical shear thinning behavior, interesting regarding their further processing, namely in jelly-like formulations. Additionally, the presence of AWC in MRC-5 human fibroblasts culture did not affect cell viability, demonstrating the non-cytotoxic behavior. Overall, the results support the efficiency of the proposed approach for collagen extraction and further enable the design of methodologies to address AWC use in biomedical or cosmetic context.

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

Similar content being viewed by others

References

  1. Ottera H (2004) FAO cultured aquatic species information programme - Gadus morhua. In: Cult. Aquat. Species Inf. Program. FAO Fish. Aquac. Dep

  2. ALIF-Associação da Indústria Alimentar pelo Frio (2014) Necessidades da indústria relativamente à valorização de subprodutos de pescado. IPMA

  3. Rustad T, Storrø I, Slizyte R (2011) Possibilities for the utilisation of marine by-products. Int J Food Sci Technol 46:2001–2014. https://doi.org/10.1111/j.1365-2621.2011.02736.x

    Article  CAS  Google Scholar 

  4. Gestsson HM, Guðjónsson J (2014) Turning waste into value. Icelandic Fish Mag 24

  5. Alves A, Marques A, Martins E et al (2017) Cosmetic potential of marine fish skin collagen. Cosmetics 4:39. https://doi.org/10.3390/cosmetics4040039

    Article  CAS  Google Scholar 

  6. Carvalho A, Marques A, Silva T et al (2018) Evaluation of the potential of collagen from codfish skin as a biomaterial for biomedical applications. Mar Drugs 16:495. https://doi.org/10.3390/md16120495

    Article  CAS  PubMed Central  Google Scholar 

  7. Zelechowska E, Sadowska M, Turk M (2010) Isolation and some properties of collagen from the backbone of Baltic cod (Gadus morhua). Food Hydrocoll 24:325–329. https://doi.org/10.1016/j.foodhyd.2009.10.010

    Article  CAS  Google Scholar 

  8. Moreira-Silva J, Diogo GS, Marques APL et al (2016) Marine collagen isolation and processing envisaging biomedical applications. In: biomaterials from nature for advanced devices and therapies, pp 16–36. https://doi.org/10.1002/9781119126218.ch2

  9. Silva TH, Alves A, Ferreira BM et al (2012) Materials of marine origin: a review on polymers and ceramics of biomedical interest. Int Mater Rev 57:276–306. https://doi.org/10.1179/1743280412Y.0000000002

    Article  CAS  Google Scholar 

  10. Silva TH, Moreira-Silva J, Marques ALP, Domingues A, Bayon Y, Reis RL (2014) Marine origin collagens and its potential applications. Mar Drugs 12:5881–5901. https://doi.org/10.3390/md12125881

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Shoulders MD, Raines RT (2009) Collagen structure and stability. Annu Rev Biochem 78:929–958. https://doi.org/10.1146/annurev.biochem.77.032207.120833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Ehrlich H (2015) Marine collagens. In: Biological materials of marine origin: vertebrates, pp 321–341. https://doi.org/10.1007/978-94-007-5730-1_8

  13. Ferraro V, Anton M, Santé-Lhoutellier V (2016) The “sisters” α-helices of collagen, elastin and keratin recovered from animal by-products: functionality, bioactivity and trends of application. Trends Food Sci Technol 51:65–75. https://doi.org/10.1016/j.tifs.2016.03.006

    Article  CAS  Google Scholar 

  14. Barros AA, Aroso IM, Silva TH et al (2015) Water and carbon dioxide: green solvents for the extraction of collagen/gelatin from marine sponges. ACS Sustain Chem Eng 3:254–260. https://doi.org/10.1021/sc500621z

    Article  CAS  Google Scholar 

  15. Rita A, Duarte C, Santo VE et al (2013) The journal of supercritical fluids unleashing the potential of supercritical fluids for polymer processing in tissue engineering and regenerative medicine. J Supercrit Fluids 79:177–185. https://doi.org/10.1016/j.supflu.2013.01.004

    Article  CAS  Google Scholar 

  16. Jung Y, Kim S (2014) A biocompatible tissue scaffold produced by supercritical fluid processing for cartilage tissue engineering. https://doi.org/10.1089/ten. TEC.2012.0170

  17. Silva JC, Barros AA, Aroso IM et al (2016) Extraction of collagen/gelatin from the marine demosponge Chondrosia reniformis (Nardo, 1847) using water acidified with carbon dioxide - process optimization. Ind Eng Chem Res 55:6922–6930. https://doi.org/10.1021/acs.iecr.6b00523

    Article  CAS  Google Scholar 

  18. Reis RLG, Duarte ARC, Silva JFCLM et al (2015) Method to obtain collagen/gelatin from marine sponges. PCT patent, WO2015/151030A1

  19. Zhu J, Kaufman LJ (2014) Collagen i self-assembly: revealing the developing structures that generate turbidity. Biophys J 106:1822–1831. https://doi.org/10.1016/j.bpj.2014.03.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sousa RO, Alves AL, Carvalho DN, Martins E, Oliveira C, Silva TH, Reis RL (2019) Acid and enzymatic extraction of collagen from Atlantic cod (Gadus Morhua) swim bladders envisaging health-related applications. J Biomater Sci Polym Ed 31:20–37. https://doi.org/10.1080/09205063.2019.1669313

    Article  CAS  PubMed  Google Scholar 

  21. Wang L, An X, Xin Z et al (2007) Isolation and characterization of collagen from the skin of deep-sea redfish (Sebastes mentella). J Food Sci 72:450–455. https://doi.org/10.1111/j.1750-3841.2007.00478.x

    Article  CAS  Google Scholar 

  22. Foegeding EA, Lanier TC, Hultin HO (1996) Characteristics of edible muscle tissues. In: Owen Fennema R (ed) Food chemistry, Chapter 15, vol. 3, pp 879–942

  23. Nagai T, Araki Y, Suzuki N (2002) Collagen of the skin of ocellate puffer fish (Takifugu rubripes). Food Chem 78:173–177. https://doi.org/10.1016/S0308-8146(01)00396-X

    Article  CAS  Google Scholar 

  24. Tylingo R, Mania S (2016) Isolation and characterization of acid soluble collagen from the skin of African catfish (Clarias gariepinus), Salmon (Salmo salar) and Baltic cod (Gadus morhua). J Biotechnol Biomater 6. https://doi.org/10.4172/2155-952X.1000234

  25. Sun L, Hou H, Li B, Zhang Y (2017) Characterization of acid- and pepsin-soluble collagen extracted from the skin of Nile tilapia (Oreochromis niloticus). Int J Biol Macromol 99:8–14. https://doi.org/10.1016/j.ijbiomac.2017.02.057

    Article  CAS  PubMed  Google Scholar 

  26. Skierka E, Sadowska M (2007) The influence of different acids and pepsin on the extractability of collagen from the skin of Baltic cod (Gadus morhua). Food Chem 105:1302–1306. https://doi.org/10.1016/j.foodchem.2007.04.030

    Article  CAS  Google Scholar 

  27. Yang H, Wang H, Zhao Y, Wang H, Zhang H (2015) Effect of heat treatment on the enzymatic stability of grass carp skin collagen and its ability to form fibrils in vitro. J Sci Food Agric 95:329–336. https://doi.org/10.1002/jsfa.6724

    Article  CAS  PubMed  Google Scholar 

  28. Bak SY, Lee SW, Choi CH, Kim HW (2018) Assessment of the influence of acetic acid residue on type I collagen during isolation and characterization. Materials (Basel) 10. https://doi.org/10.3390/ma11122518

  29. Ma J, Lin Y, Chen X et al (2014) Flow behavior, thixotropy and dynamical viscoelasticity of sodium alginate aqueous solutions. Food Hydrocoll 38:119–128. https://doi.org/10.1016/j.foodhyd.2013.11.016

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has received funding from European Union, under the scope of European Regional Development Fund (ERDF) through the Structured Project NORTE-01-0145-FEDER-000021 (Norte2020) and under the scope of the European Union Seventh Framework Programme (FP7/2007-2013) through grant agreement ERC-2012-ADG 20120216-321266 (ERC Advanced Grant ComplexiTE). The Portuguese Foundation for Science and Technology is also acknowledged for the grant of A.L.A under Doctoral Programme Do* Mar (PD/BD/127995/2016) and for the PhD grant of C. O. (Norte-08-5369-000037) with financial support by Norte 2020. The authors would like to acknowledge Frigoríficos da Ermida, Lda. (Gafanha da Nazaré, Portugal) for the kind offer of Atlantic cod skins and to Dr. Manuela Pintado, Dr. Raquel Madureira and Joana Costa (Universidade Católica Portuguesa, Porto) for the use of microDSC and assistance during measurements. The authors also thank to Dr. Catarina Marques and Dr. Sandra Pina (3B’s Research Group) for assistance on XRD measurements, to Dr. Rita Lopez-Cebral (3B’s Research Group) for assistance on SEC measurements and to Dr. Alexandre Barros for discussions.

Author information

Author notes

  1. Ana Rita C. Duarte

    Present address: Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Campus da Caparica, 2829-516, Caparica, Portugal

Authors and Affiliations

  1. 3B’s Research Group, I3Bs – Research Institute on Biomaterials, Biodegradables and Biomimetics, University of Minho, Headquarters of the European Institute of Excellence in Tissue Engineering and Regenerative Medicine Avepark, Parque de Ciência e Tecnologia, Zona Industrial da Gandra, 4805-017, Barco – Guimarães, Portugal

    Rita O. Sousa, Eva Martins, Duarte Nuno Carvalho, Ana L. Alves, Catarina Oliveira, Ana Rita C. Duarte, Tiago H. Silva & Rui L. Reis

  2. ICVS/3B’s – PT Government Associate Laboratory, Braga/Guimarães, Portugal

    Rita O. Sousa, Eva Martins, Duarte Nuno Carvalho, Ana L. Alves, Catarina Oliveira, Ana Rita C. Duarte, Tiago H. Silva & Rui L. Reis

  3. The Discoveries Centre for Regenerative and Precision Medicine, Headquarters at University of Minho, Avepark, Barco, 4805-017, Guimarães, Portugal

    Rui L. Reis

Authors
  1. Rita O. Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Duarte Nuno Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ana L. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Catarina Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ana Rita C. Duarte
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tiago H. Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rui L. Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tiago H. Silva.

Ethics declarations

Conflict of interest

The authors declare no competing financial interest.

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

Sousa, R.O., Martins, E., Carvalho, D.N. et al. Collagen from Atlantic cod (Gadus morhua) skins extracted using CO2 acidified water with potential application in healthcare. J Polym Res 27, 73 (2020). https://doi.org/10.1007/s10965-020-02048-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10965-020-02048-x

Keywords

Search

Navigation