AIM: To assess the systemic and local immunological response to subcutaneous implants of a vascular graft covered with collagen extracted from the European carp (freshwater fish) or with collagen of bovine origin. METHODS: Pieces of a vascular graft covered by pure bovine (Bos taurus, BOV, n=14) or carp (Cyprinus carpio, CYP, n=14) collagen 5 mm in size were implanted subcutaneously in the dorsum of a Balb/cOla mice. A sham operation group of 12 animals served as the control. At 7 and 14 days after the operation, one-half of each group was terminated and blood for serum, spleen, and implant with surrounding tissue were collected. Mean cytokine (TNF-α, IL-10, IL-4, IL-1β, IL-13, and IFN-γ) levels in serum were determined using ELISA. Spleen cell cultures were used for in vitro testing of lymphocyte proliferation and cytokine secretion. Local expressions of IL-6, IL-10, TNF-α, TGF-β, CCL-2, and CCL-3 were determined using PCR. RESULTS: We found no significant difference among control, BOV, and CYP groups in mean cytokine serum levels at seven days. At day 14, the BOV group had higher levels of TNF-α (P=.018) and both the BOV and CYP groups had lower levels of IL-4 (P=.011 and P=.047, respectively) compared with the control group. Both tested implants showed only a minimal effect on the production of selected cytokines. Cell proliferation in the CYP group stimulated by CYP gel at 14 days was significantly lower than by BOV gel in BOV group (P=.0031) or by CYP gel in the control group (P=.041). The difference between the groups in the local RNA expression of all the tested mediators both at 7 and at 14 days was not significant apart from a lower level of TNF-α in the BOV group compared to CYP at 14 days (P=.013). CONCLUSIONS: Implants covered with carp collagen induce an immunological response that is comparable to that of bovine collagen covered implants in a mouse model.

Department of Cardiovascular Surgery 1st Faculty of Medicine Charles University and General University Hospital Prague U Nemocnice 2 128 08 Prague 2 Czech Republic

Department of Mechanics Biomechanics and Mechatronics Faculty of Mechanical Engineering Czech Technical University Prague Technicka 4 166 07 Prague 6 Czech Republic

Department of Radiology 1st Faculty of Medicine Charles University and General University Hospital Prague U Nemocnice 2 128 08 Prague 2 Czech Republic

Institute of Immunology and Microbiology 1st Faculty of Medicine Charles University and General University Hospital Prague Studnickova 7 128 00 Prague 2 Czech Republic

Institute of Physiology 1st Faculty of Medicine Charles University Prague Albertov 5 128 00 Prague 2 Czech Republic

Institute of Rock Structure and Mechanics of the Czech Academy of Sciences 5 Holesovickach 41 182 09 Prague 8 Czech Republic

Zobrazit více v PubMed

Ambler G. K., Twine C. P. Graft type for femoro-popliteal bypass surgery. Cochrane Database of Systematic Reviews. 2018;2 doi: 10.1002/14651858.CD001487.pub3.CD001487 PubMed DOI PMC

Grus T., Lambert L., Mlcek M., et al. In vivo evaluation of short-term performance of new three-layer collagen-based vascular graft designed for low-flow peripheral vascular reconstructions. BioMed Research International. 2018;2018:7. doi: 10.1155/2018/3519596.3519596 PubMed DOI PMC

Samson R. H., Morales R., Showalter D. P., Lepore M. R., Nair D. G. Heparin-bonded expanded polytetrafluoroethylene femoropopliteal bypass grafts outperform expanded polytetrafluoroethylene grafts without heparin in a long-term comparison. Journal of Vascular Surgery. 2016;64(3):638–647. doi: 10.1016/j.jvs.2016.03.414. PubMed DOI

Rychlik I. J., Davey P., Murphy J., O'Donnell M. E. A meta-analysis to compare Dacron versus polytetrafluroethylene grafts for above-knee femoropopliteal artery bypass. Journal of Vascular Surgery. 2014;60(2):506–515. doi: 10.1016/j.jvs.2014.05.049. PubMed DOI

Chlupáč J., Filová E., Bacáková L. Blood vessel replacement: 50 years of development and tissue engineering paradigms in vascular surgery. Physiological Research. 2009;58(Suppl 2):S119–S139. PubMed

McClure M. J., Sell S. A., Simpson D. G., Walpoth B. H., Bowlin G. L. A three-layered electrospun matrix to mimic native arterial architecture using polycaprolactone, elastin, and collagen: a preliminary study. Acta Biomaterialia. 2010;6(7):2422–2433. doi: 10.1016/j.actbio.2009.12.029. PubMed DOI

Sarkar S., Salacinski H. J., Hamilton G., Seifalian A. M. The mechanical properties of infrainguinal vascular bypass grafts: their role in influencing patency. European Journal of Vascular and Endovascular Surgery. 2006;31(6):627–636. doi: 10.1016/j.ejvs.2006.01.006. PubMed DOI

Kumar V. A., Caves J. M., Haller C. A., et al. Acellular vascular grafts generated from collagen and elastin analogs. Acta Biomaterialia. 2013;9(9):8067–8074. doi: 10.1016/j.actbio.2013.05.024. PubMed DOI PMC

Sarkar S., Schmitz-Rixen T., Hamilton G., Seifalian A. M. Achieving the ideal properties for vascular bypass grafts using a tissue engineered approach: A review. Medical & Biological Engineering & Computing. 2007;45(4):327–336. doi: 10.1007/s11517-007-0176-z. PubMed DOI

Parenteau-Bareil R., Gauvin R., Berthod F. Collagen-based biomaterials for tissue engineering applications. Materials . 2010;3(3):1863–1887. doi: 10.3390/ma3031863. DOI

Yamamoto K., Igawa K., Sugimoto K., et al. Biological safety of fish (tilapia) collagen. BioMed Research International. 2014;2014:9. doi: 10.1155/2014/630757.630757 PubMed DOI PMC

Ye Q. Molecular and Cellular Mechanisms of Collagen Degradation in the Foreign Body Reaction. University of Groningen; 2013. http://irs.ub.rug.nl/ppn/356097064.

Zanvit P., Tichopád A., Havlíčková M., et al. Adjuvant effect of Bacillus firmus on the expression of cytokines and toll-like receptors in mouse nasopharynx-associated lymphoid tissue (NALT) after intranasal immunization with inactivated influenza virus type A. Immunology Letters. 2010;134(1):26–34. doi: 10.1016/j.imlet.2010.08.006. PubMed DOI

Spacek M., Chlup H., Mitas P., et al. Three-layer collagen-based vascular graft designed for low-flow peripheral vascular reconstructions. Journal of Applied Biomedicine. 2019;17(1) doi: 10.32725/jab.2019.002. PubMed DOI

Jinno C., Morimoto N., Ito R., et al. A comparison of conventional collagen sponge and collagen-gelatin sponge in wound healing. BioMed Research International. 2016;2016:8. doi: 10.1155/2016/4567146.4567146 PubMed DOI PMC

Yamada S., Yamamoto K., Ikeda Ta., Yanagiguchi K., Hayashi Y. Potency of fish collagen as a scaffold for regenerative medicine. BioMed Research International. 2014;2014:8. doi: 10.1155/2014/302932.302932 PubMed DOI PMC

Ogawa M., Moody M. W., Portier R. J., Bell J., Schexnayder M. A., Losso J. N. Biochemical properties of black drum and sheepshead seabream skin collagen. Journal of Agricultural and Food Chemistry. 2003;51(27):8088–8092. doi: 10.1021/jf034350r. PubMed DOI

Kimura S., Miyauchi Y., Uchida N. Scale and bone type I collagens of carp (Cyprinus carpio) Comparative Biochemistry and Physiology -- Part B: Biochemistry and. 1991;99(2):473–476. doi: 10.1016/0305-0491(91)90073-M. PubMed DOI

Subhan F., Kang H. Y., Lim Y., et al. Fish scale collagen peptides protect against CoCl2/TNF-α-induced cytotoxicity and inflammation via inhibition of ROS, MAPK, and NF-κB pathways in HaCaT cells. Oxidative Medicine and Cellular Longevity. 2017;2017:17. doi: 10.1155/2017/9703609.9703609 PubMed DOI PMC

Liu C., Liu X., Xue Y., Ding T., Sun J. Hydrolyzed tilapia fish collagen modulates the biological behavior of macrophages under inflammatory conditions. RSC Advances. 2015;5(39):30727–30736. doi: 10.1039/C5RA02355F. DOI

Foerst J., Vorpahl M., Engelhardt M., Koehler T., Tiroch K., Wessely R. Evolution of coronary stents: from bare-metal stents to fully biodegradable, drug-eluting stents. Combination Products in Therapy. 2013;3(1-2):9–24. doi: 10.1007/s13556-013-0005-7. DOI

Pati F., Datta P., Adhikari B., Dhara S., Ghosh K., Mohapatra P. K. D. Collagen scaffolds derived from fresh water fish origin and their biocompatibility. Journal of Biomedical Materials Research Part A. 2012;100(4):1068–1079. doi: 10.1002/jbm.a.33280. PubMed DOI

Nowack H., Hahn E., David C. S., Timpl R., Götze D. Immune response to calf collagen type I in mice: A combined control of Ir-1A and non H-2 linked genes. Immunogenetics. 1975;2(1):331–335. doi: 10.1007/BF01572302. DOI

Van Dyken S. J., Locksley R. M. Interleukin-4-and interleukin-13-mediated alternatively activated macrophages: Roles in homeostasis and disease. Annual Review of Immunology. 2013;31:317–343. doi: 10.1146/annurev-immunol-032712-095906. PubMed DOI PMC

Kramer M., Dadon S., Hasanreisoglu M., et al. Proinflammatory cytokines in a mouse model of central retinal artery occlusion. Molecular Vision. 2009;15:885–894. PubMed PMC

Lee J., Yang W., Hostetler A., et al. Characterization of the anti-inflammatory Lactobacillus reuteri BM36301 and its probiotic benefits on aged mice. BMC Microbiology. 2016;16(1):p. 69. PubMed PMC

Jiang F., He J., Navarro-Alvarez N., et al. Elongation factor Tu and heat shock protein 70 are membrane-associated proteins from mycoplasma ovipneumoniae capable of inducing strong immune response in mice. PLoS ONE. 2016;11(8)e0161170 PubMed PMC

Qureshi A. A., Reis J. C., Papasian C. J., Morrison D. C., Qureshi N. Tocotrienols inhibit lipopolysaccharide-induced pro-inflammatory cytokines in macrophages of female mice. Lipids in Health and Disease. 2010;9(1):p. 143. PubMed PMC

Blanqué R., Meakin C., Millet S., Gardner C. R. Selective enhancement of LPS-induced serum TNF-α production by carrageenan pretreatment in mice. General Pharmacology: The Vascular System. 1998;31(2):301–306. doi: 10.1016/S0306-3623(97)00434-5. PubMed DOI

Ye Q., Harmsen M. C., van Luyn M. J. A., Bank R. A. The relationship between collagen scaffold cross-linking agents and neutrophils in the foreign body reaction. Biomaterials. 2010;31(35):9192–9201. doi: 10.1016/j.biomaterials.2010.08.049. PubMed DOI

Song E., Yeon Kim S., Chun T., Byun H.-J., Lee Y. M. Collagen scaffolds derived from a marine source and their biocompatibility. Biomaterials. 2006;27(15):2951–2961. doi: 10.1016/j.biomaterials.2006.01.015. PubMed DOI

Friess W. Collagen—biomaterial for drug delivery. European Journal of Pharmaceutics and Biopharmaceutics. 1998;45(2):113–136. doi: 10.1016/s0939-6411(98)00017-4. PubMed DOI

Enhancing Guided Bone Regeneration with a Novel Carp Collagen Scaffold: Principles and Applications

Vascular Damage and Repair - Are Small-Diameter Vascular Grafts Still the "Holy Grail" of Tissue Engineering?

Influence of Biomimetically Mineralized Collagen Scaffolds on Bone Cell Proliferation and Immune Activation

Vancomycin-Loaded Collagen/Hydroxyapatite Layers Electrospun on 3D Printed Titanium Implants Prevent Bone Destruction Associated with S. epidermidis Infection and Enhance Osseointegration

Vancomycin-releasing cross-linked collagen sponges as wound dressings

Rifampin-Releasing Triple-Layer Cross-Linked Fresh Water Fish Collagen Sponges as Wound Dressings