Abstract
Fish collagen is reported with an increased bioavailability as compared to other sources, the extraction being performed on secondary sources as skin, bones, scales, or fins resulted after fish processing. The aim of the present study was to obtain biocompatible collagen hydrolysates from waste Cyprinus carpio skin, the main aquaculture species in Romania using an inexpensive and “green” neutral hydrolysis process. Neutral hydrolysis of pretreated fish skins performed for 6 h at a temperature of 135 °C and a pressure of 315 kPa produced collagen hydrolysates in 24.6–35.5% yields depending on the adopted pretreatment procedure. The extensive characterization of hydrolysate samples revealed a high purity degree (98% protein content, undetected ash content, pH value in the range 6–7), also confirmed by the absence of undesired aggregates in the characteristic fibril structure as determined by electronic microscopy. A specific collagen hydrolysate random coil structure and the absence of triple helix was determined by FTIR analysis and sustained by CD spectroscopy and X-Ray diffraction. The biocompatibility assessment for the obtained fish collagen hydrolysates revealed no cytotoxic effect on Human keratinocytes, with an 80% cell viability, superior as compared to conventional bovine collagen hydrolysate. Neutral hydrolysis of waste Cyprinus carpio skin yielded collagen hydrolysates with determined characteristics and biocompatibility superior to bovine collagen, suitable for application in foods, cosmetics and pharmaceutical industry.
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Gelsea, K., Poschlb, E., Aigner, T.: Collagens—structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55, 1531–1546 (2003). https://doi.org/10.1016/j.addr.2003.08.002
Myllyharju, J., Kivirikko, K.I.: Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20, 33–43 (2004). https://doi.org/10.1016/j.tig.2003.11.004
Hong, H., Fan, H., Chalamaiah, M., Wu, J.: Preparation of low-molecular-weight, collagen hydrolysates (peptides): Current progress, challenges, and future perspectives. Food Chem. 301, 125222 (2019). https://doi.org/10.1016/j.foodchem.2019.125222
Soderhall, C., Marenholz, I., Kerscher, T., Ruschendorf, F., Esparza-Gordillo, J., Worm, M., Gruber, C., Mayr, G., Albrecht, M., Rohde, K., Schulz, H., Wahn, U., Hubner, N., Lee, Y.A.: Variants in a novel epidermal collagen gene (COL29A1) are associated with atopic dermatitis. PLOS Biol. 5(9), e242 (2007). https://doi.org/10.1371/journal.pbio.0050242
Schmidt, M.M., Dornelles, R.C.P., Mello, R.O., Kubota, E.H., Mazutti, M.A., Kempka, A.P., Demiate, I.M.: Collagen extraction process. Int. Food Res. J. 23, 913–922 (2016). http://www.ifrj.upm.edu.my/23%20(03)%202016/(1).pdf
Alves, A.L., Marques, A.L.P., Martins, E., Silva, T.H., Reis, R.L.: Cosmetic potential of marine fish skin collagen. Cosmetics 4, 39 (2017). https://doi.org/10.3390/cosmetics4040039
Subhan, F., Hussain, Z., Tauseef, I., Shehzad, A., Wahid, F.: A review on recent advances and applications of fish collagen. Crit. Rev. Food Sci. Nutr. 61, 1027–1037 (2021). https://doi.org/10.1080/10408398.2020.1751585
Jafari, H., Lista, A., Mafosso, S.M., Ghaffari-Bohlouli, P., Nie, L., Alimoradi, H., Shavandi, A.: Fish collagen: extraction, characterization, and applications for biomaterials engineering. Polymers 12, 2230 (2020). https://doi.org/10.3390/polym12102230
Aguirre-Cruz, G., León-López, A., Cruz-Gómez, V., Jiménez-Alvarado, R., Aguirre-Álvarez, G.: Collagen hydrolysates for skin protection: oral administration and topical formulation. Antioxidants 9, 181 (2020). https://doi.org/10.3390/antiox9020181
Silva, T.H., Moreira-Silva, J., Marques, A.L.P., Domingues, A., Bayon, Y., Reis, R.L.: Marine origin collagens and its potential applications. Mar. Drugs. 12, 5881–5901 (2014). https://doi.org/10.3390/md12125881
Nasri, M.: Bioactive peptides from fish collagen byproducts: a review, in byproducts from agriculture and fisheries: adding value for food, feed, pharma, and fuels. In: Simpson, B.K., Aryee, A.N.A., Toldra, F. (eds.) John Wiley & Sons Ltd., 309–333 (2019). https://doi.org/10.1002/9781119383956.ch13
Gao, R., Yu, Q., Shen, Y., Chu, Q., Chen, G., Fen, S., Yang, M., Yuan, L., McClements, D.J., Sun, Q.: Production, bioactive properties, and potential applications of fish protein hydrolysates: developments and challenges. Trends Food Sci. Technol. 110, 687–699 (2021). https://doi.org/10.1016/j.tifs.2021.02.031
Boonmaleerat, K., Wanachewin, O., Phitak, T., Pothacharoen, P., Kongtawelert, P.: Fish collagen hydrolysates modulate cartilage metabolism. Cell Biochem. Biophys. 76, 279–292 (2018). https://doi.org/10.1007/s12013-017-0817-2
Sanchez, A., Blanco, M., Correa, B., Perez-Martin, R.I., Sotelo, C.G.: Effect of fish collagen hydrolysates on type I collagen mRNA levels of human dermal fibroblast culture. Mar. Drugs 16, 144 (2018). https://doi.org/10.3390/md16050144
Aberoumand, A.: Comparative study between different methods of collagen extraction from fish and its properties. World Appl. Sci. J. 16, 316- 319 (2012). http://www.idosi.org/wasj/wasj16(3)12/1.pdf
Ishak, N.H., Sarbon, N.M.: A review of protein hydrolysates and bioactive peptides deriving from wastes generated by fish processing. Food Bioproc Tech. 11, 2–16 (2018). https://doi.org/10.1007/s11947-017-1940-1
Zamorano-Apodaca, J.C., García-Sifuentes, C.O., Carvajal-Millán, E., Vallejo-Galland, B., Scheuren-Acevedo, S.M., Lugo-Sánchez, M.E.: Biological and functional properties of peptide fractions obtained from collagen hydrolysate derived from mixed by-products of different fish species. Food Chem. 331, 127350 (2020). https://doi.org/10.1016/j.foodchem.2020.127350
Marcet, I., Álvarez, C., Paredes, B., Díaz, M.: The use of sub-critical water hydrolysis for the recovery of peptides and free amino acids from food processing wastes. Review of sources and main parameters. J. Waste Manag. 49, 364–371 (2016). https://doi.org/10.1016/j.wasman.2016.01.009
Ahmed, R., Chun, B.-S.: Subcritical water hydrolysis for the production of bioactive peptides from tuna skin collagen. J. Supercrit Fluids. 141, 88–96 (2018). https://doi.org/10.1016/j.supflu.2018.03.006
Carvalho, A.M., Marques, A.P., Silva, T.H., Reis, R.L.: Evaluation of the potential of collagen from codfish skin as a biomaterial for biomedical applications. Mar. Drugs. 16, 495 (2018). https://doi.org/10.3390/md16120495
Kittiphattanabawon, P., Benjakul, S., Sinthusamran, S., Kishimura, H.: Characteristics of collagen from the skin of clown featherback (Chitala ornata). J. Food Sci. Technol. 50, 1972–1978 (2015). https://doi.org/10.1111/ijfs.12864
Morais, H.A., Silvestre, M.P.C., Silva, V.D.M., Silva, M.R., Simoes e Silva, A.C., Silveira, J.N.: Correlation between the degree of hydrolysis and the peptide profile of whey protein concentrate hydrolysates: effect of the enzyme type and reaction time. Am. J. Food Technol. 8, 1–16 (2013). https://doi.org/10.3923/ajft.2013.1.16
Berridge, M.V., Herst, P.M., Tan, A.S.: Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol. Annu. Rev. 11, 27–152 (2005). https://doi.org/10.1016/S1387-2656(05)11004-7
Khiari, Z., Rico, D., Martin-Diana, A.B., Barry-Ryan, C.: Valorization of fish by-products: rheological, textural and microstructural properties of mackerel skin gelatins. J. Mater. Cycles Waste Manag. 19, 180–191 (2017). https://doi.org/10.1007/s10163-015-0399-2
Duan, R., Zhang, J., Dua, X., Yao, X., Konno, K.: Properties of collagen from skin, scale and bone of carp (Cyprinus carpio). Food Chem. 112, 702–770 (2009). https://doi.org/10.1016/j.foodchem.2008.06.020
Haibo, W., Yanping, L., Haiyin, W., Hanjun, Z., Min, W., Liangzhong, L.: Physical-chemical properties of collagens from skin, scale, and bone of grass carp (Ctenopharyngodon idellus). J. Aquat. Food Prod. Technol. 23, 264–277 (2014). https://doi.org/10.1080/10498850.2012.713450
Mahboob, S., Haider, S., Sultana, S., Al-Ghanim, K.A., Al-Misned, F., Al-Kahem Al-Balawi, H.F., Ahmad, Z.: Isolation and characterization of collagen from the waste material of two important freshwater fish species. J. Anim. Plant Sci. 24(6), 1802–1810 (2014). http://www.thejaps.org.pk/docs/v-24-6/33.pdf
Trandafir, V., Popescu, G., Albu, M.G,., Iovu, H., Georgescu, M.: Bio- products based on collagen (“Bioproduse pe bazã de colagen”). Ars Docendi Publishing House, Bucharest, 119–147 (2007).
Niculescu, M., Bajenaru, S., Gaidau, C., Simion, D., Filipescu, L.: Extraction of the protein components as amino-acids hydrolysates from chrome leather wastes through hydrolytic processes. Rev. Chim. 60, 1070–1078 (2009)
Riaz, T., Zeeshan, R., Zarif, F., Ilyas, K., Muhammad, N., Zaman Safi, S., Rahim, A., Rizvi, S.A.A., Ur Rehman, I.: FTIR analysis of natural and synthetic collagen. Appl. Spectrosc. Rev. 53(9), 703–746 (2018). https://doi.org/10.1080/05704928.2018.1426595
Muyonga, J.H., Cole, C.G.B., Duodu, K.G.: Fourier transform infrared (FTIR) spectroscopic study of acid soluble collagen and gelatin from skins and bones of young and adult Nile perch (Lates niloticus). Food Chem. 86, 325–332 (2004). https://doi.org/10.1016/j.foodchem.2003.09.038
Rabotyagova, O.S., Cebe, P., David, L.: Collagen structural hierarchy and susceptibility to degradation by ultraviolet radiation. Mater. Sci. Eng. C. 28, 1420–1429 (2008). https://doi.org/10.1016/j.msec.2008.03.012
Kelly, S.M., Price, N.C.: The use of circular dichroism in the investigation of protein structure and function. Curr. Protein Pept. Sci. 1, 349–384 (2000). https://doi.org/10.2174/1389203003381315
Yang, L., Yanwen, L., Zongliang, D., Guoying, L.: Comparison of dynamic denaturation temperature of collagen with its static denaturation temperature and the configuration characteristics in collagen denaturation processes. Thermochim. Acta. 469, 71–76 (2008). https://doi.org/10.1016/j.tca.2008.01.006
Sun, L., Hou, H., Li, B., Zhang, Y.: Characterization of acid- and pepsin- soluble collagen extracted from the skin of Nile tilapia (Oreochromis niloticus). Int. J. Biol. Macromol. 99, 8–14 (2017). https://doi.org/10.1016/j.ijbiomac.2017.02.057
Woo, J.W., Yu, S.J., Cho, S.M., Lee, Y.B., Kim, S.B.: Extraction optimization and properties of collagen from yelowfin tuna (Thunnus albacares) dorsal skin. Food Hydrocoll. 22, 879–887 (2008). https://doi.org/10.1016/j.foodhyd.2007.04.015
Hee-Seok, J., Jayachandran, V., Se-Kwon, K.: Isolation and characterization of collagen from marine fish (Thunnus obesus). Biotechnol. Bioprocess Eng. 18, 1185–1191 (2013). https://doi.org/10.1007/s12257-013-0316-2
Yaowen, L., Donghui, M., Yihao, W., Wen, Q.: A comparative study of the properties and self-aggregation behavior of collagens from the scales and skin of grass carp (Ctenopharyngodon idella). Int. J. Biol. Macromol. 106, 516–522 (2018). https://doi.org/10.1016/j.ijbiomac.2017.08.044
Zhang, H., Pan, D., Dong, Y., Su, W., Su, H., Wei, X., Yang, C., Jing, L., Tang, X., Li, X., Daqing, Z., Liwei, S., Bin, Q.: Transdermal permeation effect of collagen hydrolysates of deer sinew on mouse skin, ex vitro, and antioxidant activity, increased type I collagen secretion of percutaneous proteins in NIH/3T3 cells. J. Cosmet. Dermatol. 19(2), 519–528 (2019). https://doi.org/10.1111/jocd.13041
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The work has been funded by the Operational Program Human Capital of the Ministry of European Funds through the Financial Agreement 51668/09.07.2019, SMIS code 124705.
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Dănilă, E., Stan, R., Kaya, M.A. et al. Valorization of Cyprinus Carpio Skin for Biocompatible Collagen Hydrolysates with Potential Application in Foods, Cosmetics and Pharmaceuticals. Waste Biomass Valor 13, 917–928 (2022). https://doi.org/10.1007/s12649-021-01569-w
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DOI: https://doi.org/10.1007/s12649-021-01569-w