Document Type : Research Article-en

Author

National Aquatic Processing Research Center, Inland Aquaculture Research Institute, Fisheries Science Research Institute, Agricultural Education and Extension Research Organization, Anzali, Iran

Abstract

Collagen has diverse general and biomedical applications and its important role in the future of society have made it a key biopolymer for human health and well-being. Therefore, the present study was conducted with the objectives of extracting collagen from the skin of farmed carp, determining the quality characteristics of collagen, and comparing them. Collagen was extracted from the skin of carp fishes by acidic enzymatic method using 0.5 M acetic acid and pepsin in 48 hours. Collagen treatments (5 treatments) included collagen prepared from the skin of common species, grass carp, bighead, silver, and cow (control). Collagen treatments were not capable of hemolysis and did not show toxic effects on human fibroblast cells. Heavy metals (0.01-0.18 ppm) in collagen extracted from cultured carp species were within the standard range. The color (brightness) of experimental collagen (92.74-93.68) and control (92.38) showed no significant difference (p<0.05). Amino acids cysteine and tryptophan were not observed in collagen. Glycine and hydroxylysine amino acids (352 and 3 residues 1000g-1, respectively) had the highest and lowest amounts in collagen. Amino acids profile and collagen production efficiency (10.51-10.59%) did not show significant differences in carp fish species (p<0.05). Based on the results of the present study, production efficiency, safety and quality characteristics of collagen in cultured carp species did not show any significant difference (p<0.05), and no significant difference was observed between these characteristics and the control (p<0.05). Therefore, the skin of these species can be used to produce collagen and introduce it to the industry as a substitute for mammalian collagen.

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Main Subjects

  1. Ahmed, R., Haq, M., & Chun, B.S. (2019). Characterization of marine derived collagen extracted from the by-products of bigeye tuna (Thunnus obesus). International Journal Biological Macromoleculs, 135(1), 668–676. https://doi.org/10.1016/j.ijbiomac.2019.05.213
  2. Andini, A., Prayekti, E., Wulandari, D.D., & Nidianti, E. (2020). Cytotoxicity assay using brine shrimp lethality test on collagen chitosan wound dressing sterilized by ultraviolet Light. Indonesian Journal of Medical Laboratory Science and Technology, 2(1), 21-26. https://doi.org/10.33086/ijmlst.v2i1.1467
  3. Association of Official Analytical Chemists (AOAC). (2000). Fish and Marine Products Treatment and Preparation of Sample. AOAC Standard No. 07. Washington, DC: U.S. Patent and Trademark Office.
  4. Arumugam, G.K.S., Sharma, D., Balakrishnan, R.M., Babu, J., & Ettiyappan, P. (2018). Extraction, optimization, and characterization of collagen from sole fish skin. Sustainable Chemistry and Pharmacy, 9(2018), 19–26. https://idr.nitk.ac.in/jspui/handle/123456789/11243
  5. Blanco, M., Vázquez, J.A., Pérez-Martín, R.I., & Sotelo, C.G. (2017). Hydrolysates of fish skin collagen: an opportunity for valorizing fish industry byproducts. Marine Drugs, 15(5), https://doi.org/10.3390/md15050131
  6. Carvalho, A.M., Marques, A.P., Silva, T.H., & Reis, R.L. (2018). Evaluation of the potential of collagen from Codfish skin as a biomaterial for biomedical applications. Marine Drugs, 16(12), https://doi.org/10.3390/md16120495
  7. Cao, J., Duan, Q., Liu, X., Shen, X., & Li, C. (2019). Extraction and physicochemical characterization of pepsin soluble collagens from golden Pompano (Trachinotus blochii) skin and bone. Journal Aquatic Food Product Technology, 28(3), 837–847. https://doi.org/10.1080/10498850.2019.1652216
  8. Chinh, N.T., Manh, V.Q., Trung, V.Q., Lam, T.D., Huynh, M.D., Tung, N.Q., Trinh, N.D., & Hoang, T. (2019). Characterization of collagen derived from tropical freshwater Carp fish scale Wastes and its amino acid sequence. Natural Product Communications, 14(7), 1–12. https://doi.org/1177/1934578X19866288
  9. Chotphruethipong, L., Hutamekalin, P., Nilsuwan, K., Sukketsiri, W., Aluko, R.E., Abdul, N.R., & Benjakul, S. (2022). Combined effects of defatted hydrolyzed collagen from salmon skin and vitamin C on proliferation and migration of human fibroblast cell. Fishes, 7(5), https://doi.org/10.3390/ fishes7050265
  10. Chuaychan, S. (2016). Production and characterization of collagen, gelatin, and gelatin hydrolysate powder from scales of spotted golden Goatfish. Feculty of Food Science and Technology, Prince of Songkla University, Songkhla, Thailand.
  11. Cumming, M.H., Hall, B., & Hofman, K. (2019). Isolation and characterisation of major and minor collagens from Hyaline Cartilage of Hoki (Macruronus novaezelandiae). Marine Drugs, 17(4), https://doi.org/10.3390/md17040223
  12. Devran, D., & Gulay, O.Y. (2023). Investigation of possible heavy metals and antibiotic residues in commercial collagen. Mehmet Akif Ersoy Üniversitesi Veteriner Fakültesi Dergisi, 8(1), 31–36. https://doi.org/24880/maeuvfd.1218939
  13. Junianto, J., Iskandar, I., Rizal, A., & Damayanti, W. (2018). The influence of concentration of acetic acid and pepsin enzyme in Nilem fish skin collagen extractionto the amount of rendement produced. World News Natural Science, 21(2018), 164–170.
  14. Ferreira, A.C., Bomfim, M.R.Q., & da Costa Sobrinho, C.H.d.B.(2022). Characterization, antimicrobial and cytotoxic activity of polymer blends based on chitosan and fish collagen. AMB Express, 12(1), https://doi.org/10.1186/s13568-022-01433-7
  15. García-Sifuentes, C.O., Lugo-Sánchez, M.E., Scheuren-Acevedo, S., Martínez-Porchas, M., & Peralta-Martínez, V. (2016). Amino acid profile of collagen fractions extracted from by-products of Ophistonemalibertate and Scomberjaponicus, CyTA. Journal of Food, 14(2), 296-301. https://doi.org/10.1080/19476337.2015.1101711
  16. Gauza-Włodarczyk, M., Kubisz, , & Włodarczyk, D. (2017). Amino acid composition in determination of collagen origin and assessment of physical factors effects. International Journal Biology Macromolecule, 104(PtA), 987–991. https://doi.org/10.1016/j.ijbiomac.2017.07.013
  17. Gilbert,W. (2014). Applying the hedonic method. National Institute of Standards and Technology Technical Note 1811. https://doi.org/10.6028/nist.tn.1811
  18. Iranian National Standard No. 12014. (1999). Heavy metal measurement of cosmetic products. Iranian Standard and Industrial Research Institute.
  19. Iranian National Standard No. 10699. (2015). Livestock, poultry, and aquatic feed - measuring the amount of amino acids. Iranian Standard and Industrial Research Institute.
  20. Gómez‑Limia, L., Carballo, J., Rodríguez‑González, M., & Martínez, S. (2022). Proximate composition and amino acid profle of European eel skin: infuence of body weight. European Food Research and Technology, 248(1053–1063), 1437–1446. https://doi.org/10.1007/s00217-022-03978-0
  21. Govindharaj, M., Roopavath, U.K., & Rath, S.N. (2019). Valorization of discarded Marine Eel fish skin for collagen extraction as a 3D printable blue biomaterial for tissue engineering. Journal of Cleaner Production, 230(2), 412–419. https://doi.org/1016/j.jclepro.2019.05.082
  22. ISO 10993-6. (2016). Biological evaluation of medical devices. Part 6: tests for local effects after implantation.
  23. Li, H., Cheng, W., & Liu, K. (2017). Reinforced collagen with oxidized microcrystalline cellulose shows improved hemostatic effects. Carbohydr Polym,165(2), 30–38. https://doi.org/1016/j.carbpol.2017.02.023
  24. Lin, X., Chen, Y., Jin, H., Zhao, Q., Liu, C., Li, R., Yu, F., Chen, Y., Huang, F., Yang, Z., Ding, G., & Tang, Y. (2019). Collagen extracted from bigeye Tuna skin by isoelectric precipitation: physicochemical properties, proliferation, and migration activities. Marine Drugs, 17(5), 261. https://doi.org/10.3390/md17050261
  25. Menezes, M.D.L.L.R., Ribeiro, H.L., Flávia de Oliveira, M., & de Andrade Feitosa, J.P. (2020). Optimization of the collagen extraction from Nile tilapia skin (Oreochromis niloticus) and its hydrogel with hyaluronic acid. Colloids and Surfaces B: Biointerfaces, 189(2), https://doi.org/10.1016/j.colsurfb.2020.110852
  26. Momtahan, N., Panahi, T., Poornejad, N.,  Stewart, M.G., Vance, B.R., Struk, J.A., Castleton, A.A., Roeder, B.L., Sukavaneshvar, S., & Cook, A.D. (2016). Using hemolysis as a novel method for assessment of cytotoxicity and blood compatibility of decellularized heart tissues. ASAIO Journal, 62(3), 340-8. https://doi.org/10.1097/MAT.0000000000000373
  27. Moses, S., Agbaji, E.B., Ajibola, V.O., & Gimba, C.E. (2018). Amino acid composition and proximate analysis in Tilapia (Oreochromis mossambicus) Fish from dams and rivers in Zamfara state, Nigeria. Journal Applied Science Environment Management, 22(6), 8899–905. https://doi.org/4314/jasem.v22i6.10
  28. Mullen, A., Bayon, Y., Pandit, A., & Raghunath, M. (2019). The collagen suprafamiliy: From biosynthesis to advanced biomaterial development. Advanced Materials, 31(1), 6–11. https://doi.org/10.1002/adma.201801651
  29. Nalinanon, S., Benjakul, S., Visessanguan, W., & Kishimura, H. (2007). Use of pepsin for collagen extraction from the skin of bigeye snapper (Priacanthus tayenus). Food Chemistry, 104(2), 593-601. https://doi.org/10.1016/j.foodchem.2006.12.035.
  30. Oslan, S.N.H., Shapawi, R., Mokhtar, R.A.M., Noordin,W.N.M., & Huda, N. (2022). Characterization of acid and pepsin-soluble collagen extracted from the skin of purple-Spotted Bigeye Snapper. Gels, 8(10), 665. https://doi.org/10.3390/gels8100665
  31. Qiu, B., Wei, F., Sun, X., Wang, X., Duan, B., Shi, C., Zhang, J., Zhang, J., Qiu, W., & Mu, W. (2014). Measurement of hydroxyproline in collagen with three different methods. Molecular Medicine Reports, 10(2), 1157–1163. https://doi.org/10.3892/mmr.2014.2267
  32. Raman, M., & Gopakumar, K. (2018). Fish collagen and its applications in food and pharmaceutical industry: A review. EC Nutrition, 13(2018), 752–767. https://api.semanticscholar.org/CorpusID:54176016
  33. Rosmawati, Abustam, E., Tawali, A., & Said, M.I. (2018). Amino acid and collagen content of Snakehead (Channa striata) fish skin and bone. Scientific Research Journal, 6(1), https://api.semanticscholar.org/CorpusID:212409859
  34. Ramle, S.Z., Oslan, S.N.H., Shapawi, R., Mokhtar, R.A.M., Noordin, W.N.M., & Huda, N. (2022). Biochemical characteristics of acid-soluble collagen from food processing by-products of Needlefish Skin (Tylosurus acus melanotus). Appliued Science, 12(24), 12695. https://doi.org/ 10.3390/app122412695
  35. Seifzadeh, M., Golashahi, E., & Safiyari, Sh. (2018). Study the concentrations of lead and cadmium in farmed rainbow trout in Talesh of Guilan. Animal Science Research Journal, 28(2), 65–79. https://sid.ir/paper/365590/en
  36. Song, W.K., Liu, D., Sun, L.L., Li, B.F., & Hou, H. (2019). Physicochemical and biocompatibility properties of type I collagen from the skin of Nile Tilapia (Oreochromis niloticus) for biomedical applications. Marine Drugs, 17(3), 137. https://doi.org/10.3390/md17030137
  37. Sorushanova, A., Delgado, L., Zhuning, W., Shologu, N., Kshirsagar, A., Raghunath, R., Sousa, R.O., Alves, A. L., Carvalho, D.N., Martins, E., Oliveira, C., Silva, T.H., & Reis, R.L. (2020). Acid and enzymatic extraction of collagen from Atlantic cod (Gadus morhua) swim bladders envisaging health-related applications. Journal of Biomaterials Science, Polymer Edition, 31(3), 20–37. https://doi.org/10.1080/09205063.2019.1669313
  38. Sukhikh, S., Noskova, S., Ivanova, S., Ulrikh, E., Izgaryshev, A., Larichev, T., Kozlova, O., Prosekov, A., & Babich, O. (2021). Comparative analysis of collagen-containing waste biodegradation, amino acid, peptide and carbohydrate composition of hydrolysis products. Applied Science, 11(23), 11511. https://doi.org/10.3390/app112311511
  39. Tan, Y., & Chang, S.K.C. (2018). Isolation and characterization of collagen extracted from channel catfish (Ictalurus punctatus) skin. Food Chemistry, 242(1), 147–155. https://doi.org/10.1016/j.foodchem.2017.09.013
  40. Xu, N., Peng, X.L, Li, H.R., Liu, J.X., Cheng, J.S.Y., Qi, X,Y., Ye, S.J, Gong, H.L, Zhao, X.H., Yu, J., Xu, G., & Wei, D.X. (2021). Marine-derived collagen as biomaterials for human health. Frontires Nutrition, 8(3), 702108. https://doi.org/10.3389/fnut.2021.702108
  41. Zhang, W., Zheng, J., Tian, X., Tang, Y., Ding, G., Yang, Z., & Jin, H. (2019). Pepsin-soluble collagen from the skin of Lophius litulo: A preliminary study evaluating physicochemical, antioxidant, and wound healing properties. Marine Drugs, 17(12), 708. https://doi.org/10.3390/md17120708
  42. Wang, T., Yang, L., Wang, G., Han, L., Chen, K., Liu, P., Xu, S., Li, D., Xie, Z., Mo, X., Wang, L., Liang, H., Liu, X., Zhang, S., & Gao, Y. (2021). Biocompatibility, hemostatic properties, and wound healing evaluation of tilapia skin collagen sponges. Journal of Bioactive and Compatible Polymers, 36(1), 44–58. https://doi.org/10.1177/0883911520981705
  43. Weber, M., Steinle, H., Golombek, S., Hann, L., Schlensak, C., Wendel, H. P., & Avci-Adali, M. (2018). Blood-Contacting biomaterials: in vitro evaluation of the Hemocompatibility. Frontires Bioenginering Biotechnology, 6(3), 99. https://doi.org/10.3389/fbioe.2018.00099
  44. Wei, P., Zheng, H., Shi, Z., Li, D., & Xiang, Y. (2019). Isolation and characterization of acid-soluble collagen and pepsin-soluble collagen from the skin of hybrid sturgeon. Journal of Wuhan University of Technology-Mater Science Edition, 34(2019), 950–959. https://doi.org/10.1007/s11595-019-2143-6
  45. Wu, J., Kong, L., Zhang, J., & Chen,W. (2019). Extraction and properties of acid-soluble collagen and pepsin-soluble collagen from silver carp (Hypophthalmichthys molitrix) scales: Prerequisite information for fishery processing waste reuse. Polish Journal Environmental Studies, 28(4), 2923–2930. https://doi.org/10.15244/pjoes/93742
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