Have a personal or library account? Click to login
Recent progress in sustainable fish byproduct utilisation: unveiling fish collagen as a potential wound healing agent Cover

Recent progress in sustainable fish byproduct utilisation: unveiling fish collagen as a potential wound healing agent

Open Access
|Feb 2025

References

  1. Abe Y., Krimm S., Randall H.M. (1972). Normal vibrations of crystalline polyglycine I. Bioplimers, 11: 1817-1839.
  2. Aðalsteinsdóttir D.B. (2016). Isolation, hydrolysation and bioactive properties of collagen from cod skin. Master Thesis, University of Iceland.
  3. Afzali M., Boateng J.S. (2022). Composite fish collagen-hyaluronate based lyophilized scaffolds modified with sodium alginate for potential treatment of chronic wounds. Polymers, 14: 1550.
  4. Ahmad M., Benjakul S. (2010). Extraction and characterisation of pepsin-solubilised collagen from the skin of unicorn leatherjacket (Aluterus monocerous). Food Chem., 120: 817–824.
  5. Ahmad M., Nirmal N.P., Chuprom J. (2016). Molecular characteristics of collagen extracted from the starry triggerfish skin and its potential in the development of biodegradable packaging film. RSC Adv., 40: 33868–33879.
  6. Ahmed M., Verma A.K., Patel R. (2020). Collagen extraction and recent biological activities of collagen peptides derived from sea-food waste: A review. Sustain. Chem. Pharm., 18: 100315.
  7. Ahmed R., Haq M., Chun B.S. (2019). Characterization of marine derived collagen extracted from the by-products of bigeye tuna (Thunnus obesus). Int. J. Biol. Macromol., 135: 668– 676.
  8. Akita M., Kono T., Lloyd K., Mitsui T., Morioka K., Adachi K. (2019). Biochemical study of type I collagen purified from skin of warm sea teleost Mahi mahi (Coryphaena hippurus), with a focus on thermal and physical stability. J. Food Biochem., 43: e13013.
  9. Arumugam G.K.S., Sharma D., Balakrishnan R.M., Ettiyappan J.B.P. (2018). Extraction, optimization and characterization of collagen from sole fish skin. Sustain. Chem. Pharm. 9: 19–26.
  10. Asaduzzaman A.K.M., Getachew A.T., Cho Y.J., Park J.S., Haq M., Chun B.S. (2020). Characterization of pepsin-solubilised collagen recovered from mackerel (Scomber japonicus) bone and skin using subcritical water hydrolysis. Int. J. Biol. Macromol., 148: 1290–1297.
  11. Bakar J., Hartina U., Razali M., Hashim D., Sazili A.Q. (2013). Properties of collagen from barramundi (Lates calcarifer) skin. Int. Food. Res. J., 20: 835–842.
  12. Benjakul S., Sae-Leaw T., Simpson B.K. (2020). Byproducts from fish harvesting and processing. In: Byproducts from Agriculture and Fisheries: Adding Value for Food, Feed, Pharma and Fuels, Simpson B.K., Aryee A.N.A., Toldrá F. (eds). John Wiley & Sons, pp. 179–217.
  13. Benjakul S., Thiansilakul Y., Visessanguan W., Roytrakul S., Kishimura H., Prodpran T., Meesane, J. (2010). Extraction and characterisation of pepsin-solubilised collagens from the skin of bigeye snapper (Priacanthus tayenus and Priacanthus macracanthus). J. Sci. Food Agric., 90: 132–138.
  14. Bhuimbar M.V., Bhagwat P.K., Dandge P.B. (2019). Extraction and characterization of acid soluble collagen from fish waste: Development of collagen-chitosan blend as food packaging film. J. Environ. Chem. Eng., 7: 102983.
  15. Blanco M., Vázquez J.A., Pérez-Martín R.I., Sotelo C.G. (2019). Collagen extraction optimization from the skin of the small-spotted catshark (S. canicula) by response surface methodology. Mar. Drug., 17.
  16. Boateng J., Catanzano O. (2015). Advanced therapeutic dressings for effective wound healing – a review. J. Pharm. Sci., 11: 3653–3680.
  17. Bratton D.L., Henson P.M. (2011). Neutrophil clearance: When the party is over, clean-up begins. Trends Immunol., 32: 350–357.
  18. 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. J. Aquat. Food Prod., 28: 837–847.
  19. Chen S., Chen H., Xie Q., Hong B., Chen J., Hua F., Bai K., He J., Yi R., Wu H. (2016). Rapid isolation of high purity pepsin-soluble type I collagen from scales of red drum fish (Sciaenops ocellatus). Food Hydrocoll., 52: 468–477.
  20. Chen Y., Jin H., Yang F., Jin S., Liu C., Zhang L., Huang J., Wang S., Yan Z., Cai X., Zhao R., Yu F., Yang Z., Ding G., Tang Y. (2019). Physicochemical, antioxidant properties of giant croaker (Nibea japonica) swim bladders collagen and wound healing evaluation. Int. J. Biol. Macromol., 138: 483–491.
  21. Childs D.R., Murthy A.S. (2017). Overview of wound healing and management. Surg. Clin. North Am., 97: 189–207.
  22. Chotphruethipong L., Battino M., Benjakul S. (2020). Effect of stabilizing agents on characteristics, antioxidant activities and stability of liposome loaded with hydrolyzed collagen from defatted Asian sea bass skin. Food Chem., 328: 127127.
  23. Chuaychan S., Benjakul S., Kishimura H. (2015). Characteristics of acid- and pepsin-soluble collagens from scale of seabass (Lates calcarifer). LWT, 63: 71–76.
  24. Cruz M.A., Araujo T.A., Avanzi I.R., Parisi J.R., de Andrade A.L.M., Rennó A.C.M. (2021). Collagen from marine sources and skin wound healing in animal experimental studies: a systematic review. Mar. Biotechnol., 23: 1–11.
  25. Darby I.A., Laverdet B., Bonté F., Desmoulière A. (2014). Fibroblasts and myofibroblasts in wound healing. Clin. Cosmet. Investig. Dermatol., 6: 301–311.
  26. Dechojarassri D., Okada T., Tamura H., Furuike T. (2023). Evaluation of cytotoxicity of hyaluronic acid/chitosan/bacterial cellulose-based membrane. Materials, 16: 5189.
  27. Deng X., Gould M., Ali M.A. (2022). A review of current advancements for wound healing: Biomaterial applications and medical devices. J. Biomed. Mater. Res. B Appl. Biomater., 110: 2542–2573.
  28. Denis A., Brambati N., Dessauvages B., Guedj S., Ridoux C., Meffre N., Autier C. (2008). Molecular weight determination of hydrolyzed collagens. Food Hydrocoll., 22: 989–994.
  29. Ding D.D., Du B., Zhang C., Zaman F., Huang Y. (2019). Isolation and identification of an antioxidant collagen peptide from skipjack tuna (: Katsuwonus pelamis) bone. RSC Adv., 9: 27032–27041.
  30. Dong Y., Dai Z. (2022). Physicochemical, structural and antioxidant properties of collagens from the swim bladder of four fish species. Mar. Drug., 20: 550.
  31. Dryden S.V., Shoemaker W.G., Kim J.H. (2013). Wound management and nutrition for optimal wound healing. Atlas Oral Maxillofac. Surg. Clin. North Am., 21: 37–47.
  32. Edwards C.A., O’Brien W.D. (1980). Modified assay for determination of hydroxyproline in a tissue hydrolyzate, Clin. Chim. Acta. 104: 161–167.
  33. Elbialy Z.I., Atiba A., Abdelnaby A., Al-Hawary I.I., Elsheshtawy A., El-Serehy H.A., Abdel-Daim M.M., Fadl S.E., Assar D.H. (2020). Collagen extract obtained from Nile tilapia (Oreochromis niloticus L.) skin accelerates wound healing in rat model via up regulating VEGF, bFGF, and α-SMA genes expression. BMC Vet. Res., 16: 352.
  34. Ellis S., Lin E.J., Tartar D. (2018). Immunology of wound healing. Curr. Dermatol. Rep., 7: 350–358.
  35. FAO (2022). The State of World Fisheries and Aquaculture 2022. Towards Blue Transformation. Rome, FAO.
  36. Fatemi M.J., Garahgheshlagh S.N., Ghadimi T., Jamili, S., Nourani M.R., Sharifi A.M., Saberi M., Amini N., Sarmadi V.H., Yazdi-Amirkhiz S.Y. (2021). Investigating the impact of collagen-chitosan derived from scomberomorus guttatus and shrimp skin on second-degree burn in rats model. Regen. Ther., 18: 12–20.
  37. Fatiroi N.S., Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.M., Huda N. (2023). Biochemical and microstructural characteristics of collagen biopolymer from unicornfish (Naso reticulatus Randall, 2001) bone prepared with various acid types. Polymers, 15: 15041054.
  38. Felician F.F., Yu R.H., Li M.Z., Li C.J., Chen H.Q., Jiang Y., Tang T., Qi W.Y., Xu H.M. (2019). The wound healing potential of collagen peptides derived from the jellyfish Rhopilema esculentum. Chin. J. Traumatol., 22: 12–20.
  39. Ferreira A.C., Bomfim M.R.Q., da Costa Sobrinho C.H. de B., Boaz D.T.L., Da Silva Lira R., Fontes V.C., Arruda M.O., Zago P.M.W., Filho C.A.A.D., Dias C.J.M., da Rocha Borges M.O., Ribeiro R.M., Bezerra C.W.B., Penha R.S. (2022). Characterization, antimicrobial and cytotoxic activity of polymer blends based on chitosan and fish collagen. AMB Express, 12: 102.
  40. Firdayanti W., Trilaksani W., Purwaningsih S. (2023). Valorization of emperor fish (Lethrinus lentjan) skin for collagen isolation: effect of acetic acid ratio and extraction time. Proc. IOP Conference Series: Earth and Environmental Science. Institute of Physics.
  41. Gazzarri M., Bartoli C., Mota C., Puppi D., Dinucci D., Volpi S., Chiellini F. (2013). Fibrous star poly(ε-caprolactone) melt-electrospun scaffolds for wound healing applications. J. Bioact. Compat. Polym., 28: 492–507.
  42. Genesi B.P., de Melo Barbosa R., Severino P., Rodas A.C.D., Yoshida C.M.P., Mathor M.B., Lopes P.S., Viseras C., Souto E.B., Ferreira da Silva C. (2023). Aloe vera and copaiba oleoresin-loaded chitosan films for wound dressings: microbial permeation, cytotoxicity, and in vivo proof of concept. Int. J. Pharm., 634: 122648.
  43. Giraud-Guille M.-M., Besseau L., Chopin C., Durand P., Herbage D. (2000). Structural aspects of fish skin collagen which forms ordered arrays via liquid crystalline states. Biomaterials, 21: 899–906.
  44. Gonzalez A.C.D.O., Andrade Z.D.A., Costa T.F., Medrado A.R.A.P. (2016). Wound healing – a literature review. An. Bras. Dermatol., 91: 614–620.
  45. Greenlee-Wacker M.C. (2016). Clearance of apoptotic neutrophils and resolution of inflammation. Immunol. Rev., 273: 357–370.
  46. Hajj W.A., Salla M., Krayem M., Khaled S., Hassan H.F., El Khatib S. (2024). Hydrolyzed collagen: Exploring its applications in the food and beverage industries and assessing its impact on human health – A comprehensive review. Heliyon, 10: e36433.
  47. Hamdan F.S., Sarbon N.M. (2019). Isolation and characterisation of collagen from fringescale sardinella (Sardinella fimbriata) waste material. Int. Food Res. J., 26: 133–140.
  48. Hema G.S., Joshy C.G., Shyni K., Chatterjee N.S., Ninan G., Mathew S. (2017). Optimization of process parameters for the production of collagen peptides from fish skin (Epinephelus malabaricus) using response surface methodology and its characterization. J. Food Sci. Technol., 54: 488–496.
  49. Hou C.Y., Hazeena S.H., Shih M.K., Hsieh S.L., Hsieh C.W., Liu T.T., Chen M.H., Huang Y.W. (2022). Structural characteristics of collagen from cuttlefish skin waste extracted at optimized conditions. Int. J. Food Prop., 25: 2211–2222.
  50. Hou N.T., Chen B.H. (2023). Preparation of nanoemulsions with low-molecular-weight collagen peptides from sturgeon fish skin and evaluation of anti-diabetic and wound-healing effects in mice. Pharmaceutics, 15: 15092304.
  51. Hsieh C.H., Shiau C.Y., Su Y.C., Liu Y.H., Huang Y.R. (2016). Isolation and characterization of collagens from the skin of giant grouper (Epinephelus lanceolatus). J. Aqua. Food Prod. Technol., 25: 93–104.
  52. Hu Z., Yang P., Zhou C., Li S., Hong P. (2017). Marine collagen peptides from the skin of Nile Tilapia (Oreochromis niloticus): Characterization and wound healing evaluation. Mar. Drug., 15.
  53. Iayne K.J., Veis A. (1988). Fourier Transform IR Spectroscopy of Collagen and Gelatin Solutions: Deconvolution of the Amide I Band for Conformational Studies. Biopolymers, 27: 1749–1760.
  54. Iosageanu A., Ilie D., Craciunescu O., Seciu-Grama A.M., Oancea A., Zarnescu O., Moraru I., Oancea F. (2021). Effect of fish bone bioactive peptides on oxidative, inflammatory and pigmentation processes triggered by uv B irradiation in skin cells. Molecules, 26.
  55. Iswariya S., Velswamy P., Uma T.S. (2018). Isolation and characterization of biocompatible collagen from the skin of puffer fish (Lagocephalus inermis). J. Polym. Environ., 26: 2086–2095.
  56. Jafari H., Lista A., Siekapen M.M., Ghaffari-Bohlouli P., Nie L., Alimoradi H., Shavandi A. (2020). Fish collagen: Extraction, characterization, and applications for biomaterials engineering. Polymers, 12: 2230.
  57. Jaziri A.A., Shapawi R., Mohd Mokhtar R.A., Wan W.N., Huda N. (2021). Tropical marine fish surimi by-products: utilisation and potential as functional food application. Food Rev. Int., 39: 3455–3480.
  58. Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.M., Huda N. (2022 a). Biochemical and microstructural properties of lizardfish (Saurida tumbil) scale collagen extracted with various organic acids. Gels, 8: 050266.
  59. Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.M., Huda N. (2022 b). Microstructural and physicochemical analysis of collagens from the skin of lizardfish (Saurida tumbil Bloch, 1795) extracted with different organic acids. Molecules, 27: 082452.
  60. Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.M., Huda N. (2022c). Biochemical analysis of collagens from the bone of lizardfish (Saurida tumbil Bloch, 1795) extracted with different acids. PeerJ., 10: e13103.
  61. Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.M., Huda N. (2022 d). Physicochemical and microstructural analyses of pepsin-soluble collagens derived from lizardfish (Saurida tumbil Bloch, 1795) skin, bone and scales. Gels, 8: 080471.
  62. Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.Md., Huda N. (2023). Extraction and characterization of type I collagen from parrotfish (Scarus sordidus Forsskål, 1775) scale solubilized with the aid of acetic acid and pepsin. Int. J. Biomater., 2023: 1–10.
  63. Jeevithan E., Bao B., Bu Y., Zhou Y., Zhao Q., Wu W. (2014). Type II collagen and gelatin from silvertip shark (Carcharhinus albimarginatus) cartilage: Isolation, purification, physicochemical and antioxidant properties. Mar. Drugs. 12: 3852–3873.
  64. Jongjareonrak A., Benjakul S., Visessanguan W., Nagai T., Tanaka M. (2005 a). Isolation and characterisation of acid and pepsin-solubilised collagens from the skin of Brownstripe red snapper (Lutjanus vitta). Food Chem., 93: 475–484.
  65. Jongjareonrak A., Benjakul S., Visessanguan W., Tanaka M. (2005 b). Isolation and characterization of collagen from bigeye snapper (Priacanthus macracanthus) skin. J. Sci. Food Agric., 85: 1203–1210.
  66. Kittiphattanabawon P., Benjakul S., Visessanguan W., Shahidi F. (2010). Isolation and characterization of collagen from the cartilages of brownbanded bamboo shark (Chiloscyllium punctatum) and blacktip shark (Carcharhinus limbatus). LWT, 43: 792– 800.
  67. Kittiphattanabawon P., Sriket C., Kishimura H., Benjakul S. (2019). Characteristics of acid and pepsin solubilized collagens from Nile tilapia (Oreochromis niloticus) scale. Emir. J. Food Agric., 31: 95–101.
  68. Korteweg C., Gu J. (2008). Pathology, molecular biology, and pathogenesis of avian influenza A (H5N1) infection in humans. Am., J. Pathol., 172: 1155–1170.
  69. Krimm S., Bandekart J. (1986). Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem., 38: 181–364.
  70. Kumar L.V., Shakila R.J., Jeyasekaran G. (2019). In vitro anti-cancer, anti-diabetic, anti-inflammation and wound healing properties of collagen peptides derived from unicorn leatherjacket (Aluterus monoceros) at different hydrolysis. Turk. J. Fish Aquat. Sci., 19: 551–560.
  71. Kurahashi T., Fujii J. (2015). Roles of antioxidative enzymes in wound healing. J. Dev. Biol., 3: 57–70.
  72. Kwon Lee S., Ellen Posthauer M., Dorner B., Redovian V., Jane Maloney M. (2006). Pressure ulcer healing with a concentrated, fortified, collagen protein hydrolysate supplement: a randomized controlled trial. Adv. Skin Wound Care, 19: 94–100.
  73. Lahmar A., RjabM., Sioud F., Selmi M., Salek A., Kilani-Jaziri S., Ghedira L.C. (2022). Design of 3D hybrid plant extract/marine and bovine collagen matrixes as potential dermal scaffolds for skin wound healing. Sci. World J., https://doi.org/10.1155/2022/8788061
  74. Lai C.S., Tu C.W., Kuo H.C., Sun P.P., Tsai M.L. (2020). Type II collagen from cartilage of Acipenser baerii promotes wound healing in human dermal fibroblasts and in mouse skin. Mar. Drug., 18.
  75. Landén N.X., Li D., Ståhle M. (2016). Transition from inflammation to proliferation: a critical step during wound healing. Cell. Mol. Life Sci., 73: 3861–3885.
  76. León-López A., Fuentes-Jiménez L., Hernández-Fuentes A.D., Campos-Montiel R.G., Aguirreálvarez G. (2019 a). Hydrolysed collagen from sheepskins as a source of functional peptides with antioxidant activity. Int. J. Mol. Sci., 20: 163931.
  77. León-López A., Morales-Peñaloza A., Martínez-Juárez V.M., Vargas-Torres A., Zeugolis D.I., Aguirre-Álvarez G. (2019 b). Hydrolyzed collagen-sources and applications. Molecule,. 24: 4031.
  78. Li H., Tian J., Cao H., Tang Y., Huang F., Yang Z. (2023). Preparation of enzyme-soluble swim bladder collagen from sea eel (Muraenesox cinereus) and evaluation its wound healing capacity. Mar. Drug., 21.
  79. Li L.Y., Zhao Y.Q., He Y., Chi C.F., Wang B. (2018). Physicochemical and antioxidant properties of acid- And pepsin-soluble collagens from the scales of Miiuy croaker (Miichthys miiuy). Mar. Drug., 16.
  80. Liao W., Guanghua X., Li Y., Shen X.R., Li C. (2018). Comparison of characteristics and fibril-forming ability of skin collagen from barramundi (Lates calcarifer) and tilapia (Oreochromis niloticus). Int. J. Biol. Macromol., 107: 549–559.
  81. Lim Y.S., Ok Y.J., Hwang S.Y., Kwak J.Y., Yoon S. (2019). Marine collagen as a promising biomaterial for biomedical applications. Mar. Drug., 17.
  82. Lin X., Chen Y., Jin H., Zhao Q., Liu C., Li R., Yu F., Chen Yan, Huang F., Yang Z., Ding G., Tang Y. (2019). Collagen extracted from bigeye tuna (Thunnus obesus) skin by isoelectric precipitation: Physicochemical properties, proliferation, and migration activities. Mar. Drug., 17.
  83. Liu W., Zhang Y., Cui N., Wang T. (2019). Extraction and characterization of pepsin-solubilized collagen from snakehead (Channa argus) skin: Effects of hydrogen peroxide pretreatments and pepsin hydrolysis strategies. Proc. Biochem., 76: 194–202.
  84. López-Otín C., Bond J.S. (2008). Proteases: Multifunctional enzymes in life and disease. J. Biol. Chem., 283: 30433-7.
  85. Man E., Hoskins C. (2020). Towards advanced wound regeneration. Eur. J. Pharm. Sci., 149: 1053607.
  86. Manjushree H.K., Acharya P.P., Bhat G., More S.S., Fasim A. (2023). Biophysical and in vitro wound healing assessment of collagen peptides processed from fish skin waste. J. Bioact. Compat. Polym., 38: 25–40.
  87. Matarsim N.N., Jaziri A.A., Shapawi R., Mokhtar R.A.M., Noordin W.N.M., Huda N. (2023). Type I collagen from the skin of barracuda (Sphyraena sp.) prepared with different organic acids: biochemical, microstructural and functional properties. J. Funct. Biomater., 14.
  88. Matmaroh K., Benjakul S., Prodpran T., Encarnacion A.B., Kishimura H. (2011). Characteristics of acid soluble collagen and pepsin soluble collagen from scale of spotted golden goatfish (Parupeneus heptacanthus). Food Chem., 129: 1179–1186.
  89. Mei F., Liu J., Wu J., Duan Z., Chen M., Meng K., Chen S., Shen X., Xia G., Zhao M. (2020). Collagen peptides isolated from Salmo salar and tilapia nilotica skin accelerate wound healing by altering cutaneous microbiome colonization via upregulated NOD2 and BD14. J. Agric. Food Chem., 68: 1621–1633.
  90. Menezes M. do L.L.R., Ribeiro H.L., Abreu F. de O.M. da S., Feitosa J.P. de A., Filho M. de S.M. de S. (2020). Optimization of the collagen extraction from Nile tilapia skin (Oreochromis niloticus) and its hydrogel with hyaluronic acid. Colloids. Surf. B Biointerfaces., 189: 10852.
  91. Migone C., Scacciati N., Grassiri B., De Leo M., Braca A., Puppi D., Zambito Y., Piras A.M. (2022). Jellyfish polysaccharides for wound healing applications. Int. J. Mol. Sci., 23.
  92. Minh L.T.M., Okazaki E., Osako K. (2014). Isolation and characterization of acid-soluble collagen from the scales of marine fishes from Japan and Vietnam. Food Chem., 149: 264– 270.
  93. Mohammadi R., Mohammadifar M.A., Mortazavian A.M., Rouhi M., Ghasemi J.B., Delshadian Z. (2016). Extraction optimization of pepsin-soluble collagen from eggshell membrane by response surface methodology (RSM). Food Chem., 190: 186–193.
  94. Mosser D.M. (2003). The many faces of macrophage activation. J. Leukoc. Biol., 73: 209–212.
  95. Mullins R.J., Bs M.B. (1996). Allergic reactions to oral, surgical and topical bovine collagen Anaphylactic risk for surgeons. Aust. N. Z. J. Ophthalmol., 24: 257–260.
  96. Muthukumar T., Anbarasu K., Prakash D., Sastry T.P. (2014 a). Effect of growth factors and pro-inflammatory cytokines by the collagen biocomposite dressing material containing Macrotyloma uniflorum plant extract-In vivo wound healing. Colloids. Surf. B Biointerfaces, 121: 178–188.
  97. Muthukumar T., Prabu P., Ghosh K., Sastry T.P. (2014 b). Fish scale collagen sponge incorporated with Macrotyloma uniflorum plant extract as a possible wound/burn dressing material. Colloids. Surf. B Biointerfaces, 113: 207–212.
  98. Muthukumar T., Prakash D., Anbarasu K., Kumar B.S., Sastry T.P. (2014 c). Effect of collagen sponge incorporating Macrotyloma uniflorum extract on full-thickness wound healing by down-regulation of matrix metalloproteinases and inflammatory markers. RSC Adv., 4: 64267–64276.
  99. Naderi Gharahgheshlagh S., Latifi N., Ghadimi T., Farokh Forghani S., Irilouzadian R., Amini N., Larijani G., Hatami S., Taghavian N., Bayat Shahbazi S., Latifi F. (2023). Biochemical and biological characterization of type-I collagen from Scomberomorus commerson skin as a biomaterial for medical applications. Int. J. Pept. Res. Ther., 29.
  100. Nikoo M., Benjakul S., Ocen D., Yang N., Xu B., Zhang L., Xu X. (2013). Physical and chemical properties of gelatin from the skin of cultured Amur sturgeon (Acipenser schrenckii). J. Appl. Ichthyol., 29: 943–950.
  101. Normah I., Afiqah M. (2018). Effect of extraction time on the physico-chemical characteristics of collagen from sin croaker (Johniecop sina) waste. Int. Food Res. J., 25: 1074–1080.
  102. Ogawa M., Portier R.J., Moody M.W., Bell J., Schexnayder M.A., Losso J.N. (2004). Biochemical properties of bone and scale collagens isolated from the subtropical fish black drum (Pogonia cromis) and sheepshead seabream (Archosargus probatocephalus). Food Chem., 88: 495–501.
  103. Ong T.Y., Shaik M.I., Sarbon N.M. (2021). Isolation and characterization of acid and pepsin soluble collagen extracted from sharpnose stingray (Dasyatis zugei) skin. Food Res., 5: 214–224.
  104. 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: 100665.
  105. Pal P., Srivas P.K., Dadhich P., Das B., Maity P.P., Moulik D., Dhara S. (2016). Accelerating full thickness wound healing using collagen sponge of mrigal fish (Cirrhinus cirrhosus) scale origin. Int. J. Biol. Macromol., 93: 1507–1518.
  106. Parenteau-Bareil R., Gauvin R., Berthod F. (2010). Collagen-based biomaterials for tissue engineering applications. Materials, 3: 1863–1887.
  107. Piez K.A., Gross J. (1960). The amino acid composition of some fish collagens: the relation between composition and structure. J. Biol. Chem., 235: 995–998.
  108. Plepis A.M.D.G., Goissis G., Das-Gupta D.K. (1996). Dielectric and pyroelectric characterization of anionic and native collagen. Poly. Eng. Sci., 36: 2932–2938.
  109. Prihanto A.A., Jaziri A.A., Pratomo M.D., Putri S.E., Fajriati C., Nurdiani R., Firdaus M. (2022). Characteristics of collagen from parrotfish (Chlorurus sordidus), tiger grouper (Epinephelus fuscoguttatus) and pink ear emperor (Lethrinus lentjan): Effect of acetic acid concentration and extraction time. Online J. Biol. Sci., 22: 26–35.
  110. Pulidindi K., Ahuja K. (2024). Collagen Market Size. https://www.grandviewresearch.com/industry-analysis/collagen-market#:~:text=The%20global%20collagen%20market%20size%20was%20estimated%20at%20USD%209.12,USD%2019.9%20billion%20by%202030.
  111. Rama S., Chandrakasan G. (1984). Distribution of different molecular species of collagen in the vertebral cartilage of shark (Carcharius acutus). Connect Tissue Res., 12: 111–118.
  112. Ramanathan G., Muthukumar T., Tirichurapalli Sivagnanam U. (2017 a). In vivo efficiency of the collagen coated nanofibrous scaffold and their effect on growth factors and pro-inflammatory cytokines in wound healing. Eur. J. Pharmacol., 814: 45–55.
  113. Ramanathan G., Singaravelu S., Muthukumar T., Thyagarajan S., Rathore H.S., Sivagnanam U.T., Perumal P.T. (2017 b). Fabrication of Arothron stellatus skin collagen film incorporated with Coccinia grandis as a durable wound construct. Int. J. Polym. Mater. Polym. Biomater., 66: 558–568.
  114. 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). Appl. Sci., 12.
  115. Razali U.H.M., Juraimy A.M.M., Jusoh Y.M.M., Dailin D.J., Yaakob H., Zainol N., Zaidel D.N.A. (2023). Effect of ultrasonic amplitude on the yield and properties of barramundi (Lates calcarifer) skin collagen. J. Trop. Life Sci., 13: 247–256.
  116. Ronfard V., Barrandon Y. (2000). Migration of keratinocytes through tunnels of digested fibrin. Biol. Sci., 98: 4504–4509.
  117. Sadowska M., Kolodziejska I., Niecikowska C. (2003). Isolation of collagen from the skins of Baltic cod (Gadus morhua). Food Chem., 81: 257–262.
  118. Sai K.P., Babu M. (2001). Studies on Rana tigerina skin collagen. Comp. Biochem. Physiol. B., 128: 81–90.
  119. Selvaraj S., Inbasekar C., Pandurangan S., Nishter N.F. (2023). Collagen-coated silk fibroin nanofibers with antioxidants for enhanced wound healing. J. Biomater. Sci. Polym. Ed., 34: 35–52.
  120. Senadheera T.R.L., Dave D., Shahidi F. (2020). Sea cucumber derived type I collagen: A comprehensive review. Mar. Drug., 18: 471.
  121. Shaik M.I., Asrul Effendi N.F., Sarbon N.M. (2021). Functional properties of sharpnose stingray (Dasyatis zugei) skin collagen by ultrasonication extraction as influenced by organic and inorganic acids. Biocatal. Agric. Biotechnol., 35.
  122. Shalaby M., Hamouda D., Khedr S.M., Mostafa H.M., Saeed H., Ghareeb A.Z. (2023). Nanoparticles fabricated from the bioactive tilapia scale collagen for wound healing: Experimental approach. PLoS One, 18.
  123. Silvipriya K.S., Krishna Kumar K., Bhat A.R., Dinesh Kumar B., John A., Lakshmanan P. (2015). Collagen: Animal sources and biomedical application. J. Appl. Pharm. Sci., 5: 123–127.
  124. 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.
  125. Sorushanova A., Delgado L.M., Wu Z., Shologu N., Kshirsagar A., Raghunath R., Mullen A.M., Bayon Y., Pandit A., Raghunath M., Zeugolis D.I. (2019). The collagen suprafamily: from biosynthesis to advanced biomaterial development. Adv. Mat., 31: e1801651.
  126. Sousa K. dos S.J., de Souza A., de Lima L.E., Erbereli R., de Araújo Silva J., de Almeida Cruz M., Martignago C.C.S., Ribeiro D.A., Barcellos G.R.M., Granito R.N., Renno A.C.M. (2023). Flounder fish (Paralichthys sp.) collagen a new tissue regeneration: genotoxicity, cytotoxicity and physical–chemistry characterization. Bioprocess Biosyst. Eng., 46: 1053– 1063.
  127. Sulaiman A.W., Sarbon N.M. (2020). Characterization of acid soluble collagen (ASC) and pepsin soluble collagen (PSC) extracted from shortfin scad (Decapterus macrosoma) waste. Food Res., 4: 2272–2280.
  128. Tabriz A.G., Douroumis D. (2022). Recent advances in 3D printing for wound healing: A systematic review. J. Drug Deliv. Sci. Technol., 74: 103564.
  129. Tamilmozhi S., Veeruraj A., Arumugam M. (2013). Isolation and characterization of acid and pepsin-solubilized collagen from the skin of sailfish (Istiophorus platypterus). Food Res. Int., 54: 1499–1505.
  130. Tan Y., Chang S.K.C. (2018). Isolation and characterization of collagen extracted from channel catfish (Ictalurus punctatus) skin. Food Chem., 242: 147–155.
  131. Tsugita A., Scheffler J. J. (1982). A rapid method for acid hydrolysis of protein with a mixture of trifluoroacetic acid and hydrochloric acid. Eur. J. Biochem., 124: 585–588.
  132. Van Hinsbergh V.W.M., Koolwijk P. (2008). Endothelial sprouting and angiogenesis: Matrix metalloproteinases in the lead. Cardiovasc. Res., 78: 203–212.
  133. Velnar T., Bailey T., Smrkolj V. (2009). The wound healing process: An overview of the cellular and molecular mechanisms. J. Int. Medical Res., 37: 1528–1542.
  134. Wang C., Chen Z., He Y., Li L., Zhang D. (2009). Structure, morphology and properties of Fe-doped ZnO films prepared by facing-target magnetron sputtering system. Appl. Surf. Sci., 255: 6881–6887.
  135. Wang J., Xu M., Liang R., Zhao M., Zhang Z., Li Y. (2015). Oral administration of marine collagen peptides prepared from chum salmon (Oncorhynchus keta) improves wound healing following cesarean section in rats. Food Nutr. Res., 59: 26411.
  136. Wang W.Y., Zhao Y.Q., Zhao G.X., Chi C.F., Wang B. (2020). Antioxidant peptides from collagen hydrolysate of redlip croaker (Pseudosciaena polyactis) scales: Preparation, characterization, and cytoprotective effects on H2O2‐damaged HepG2 cells. Mar. Drug., 18.
  137. Wilgus T.A., Roy S., McDaniel J.C. (2013). Neutrophils and wound repair: positive actions and negative reactions. Adv. Wound Care., 2: 379–388.
  138. Woo J.W., Yu S.J., Cho S.M., Lee Y.B., Kim S.B. (2008). Extraction optimization and properties of collagen from yellowfin tuna (Thunnus albacares) dorsal skin. Food Hydrocoll., 22: 879–887.
  139. Woonnoi W., Chotphruethipong L., Tanasawet S., Benjakul S., Sutthiwong N., Sukketsiri W. (2021). Hydrolyzed collagen from salmon skin increases the migration and filopodia formation of skin keratinocytes by activation of fak/src pathway. Pol. J. Food Nutr. Sci., 71: 323–332.
  140. Xiao L., Lv J., Liang Y., Zhang H., Zheng J., Lin F., Wen X. (2023). Structural, physicochemical properties and function of swim bladder collagen in promoting fibroblasts viability and collagen synthesis. LWT, 173: 114294.
  141. Xiong X., Liang J., Xu Y., Liu J., Liu Y. (2020). The wound healing effects of the Tilapia collagen peptide mixture TY001 in streptozotocin diabetic mice. J. Sci. Food Agric., 100: 2848–2858.
  142. Yang F., Qin X., Zhang T., Zhang C., Lin H. (2019). Effect of oral administration of active peptides of Pinctada martensii on the repair of skin wounds. Mar. Drug., 17.
  143. Yang T., Zhang K., Li B., Hou H. (2018). Effects of oral administration of peptides with low molecular weight from Alaska Pollock (Theragra chalcogramma) on cutaneous wound healing. J. Funct. Food., 48: 682–691.
  144. Yu F., Zong C., Jin S., Zheng J., Chen N., Huang J., Chen Y., Huang F., Yang Z., Tang Y., Ding G. (2018). Optimization of extraction conditions and characterization of pepsin-solubilised collagen from skin of giant croaker (Nibea japonica). Mar. Drug., 16.
  145. Zeng S., Yim J., Yang S., Zhang C., Yang P., Wu W. (2012). Structure and characteristics of acid and pepsin-solubilized collagens from the skin of cobia (Rachycentron canadum). Food Chem., 135: 1975–1984.
  146. Zhang B., Chen Y., Wei X., Li M., Wang M. (2010). Optimization of conditions for collagen extraction from the swim bladders of grass carp (Ctenopharyngodon idella) by response surface methodology. Int. J. Food Engin., 6.
  147. Zhang G., Sun A., Li W., Liu T., Su Z. (2006). Mass spectrometric analysis of enzymatic digestion of denatured collagen for identification of collagen type. J. Chromatogr. A., 1114: 274–277.
  148. Zhang X., Xu S., Shen L., Li G. (2020). Factors affecting thermal stability of collagen from the aspects of extraction, processing and modification. J. Leather Sci. Eng., 2: 19.
  149. Zhang Z., Wang J., Ding Y., Dai X., Li Y. (2011). Oral administration of marine collagen peptides from Chum Salmon skin enhances cutaneous wound healing and angiogenesis in rats. J. Sci. Food Agric., 91: 2173–2179.
  150. Zhao W.H., Chi C.F., Zhao Y.Q., Wang B. (2018). Preparation, physicochemical and antioxidant properties of acid- and pepsin-soluble collagens from the swim bladders of miiuy croaker (Miichthys miiuy). Mar. Drug., 16.
  151. Zheng J., Tian X., Xu B., Yuan F., Gong J., Yang Z. (2020). Collagen peptides from swim bladders of giant croaker (Nibea japonica) and their protective effects against H2O2-induced oxidative damage toward human umbilical vein endothelial cells. Mar. Drug., 18.
  152. Zhou T., Sui B., Mo X., Sun J. (2017). Multifunctional and biomimetic fish collagen/bioactive glass nanofibers: Fabrication, antibacterial activity and inducing skin regeneration in vitro and in vivo. Int. J. Nanomedicine., 12: 3495–3507.
DOI: https://doi.org/10.2478/aoas-2025-0026 | Journal eISSN: 2300-8733 | Journal ISSN: 1642-3402
Language: English
Submitted on: Aug 6, 2024
Accepted on: Jan 13, 2025
Published on: Feb 26, 2025
Published by: National Research Institute of Animal Production
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2025 Abdul Aziz Jaziri, Rossita Shapawi, Ruzaidi Azli Mohd Mokhtar, Wan Norhana Md. Noordin, Sukoso, Nurul Huda, published by National Research Institute of Animal Production
This work is licensed under the Creative Commons Attribution 4.0 License.

AHEAD OF PRINT