The study monitored in vitro early response of connective tissue cells and immunocompetent cells to enosseal implant materials coated by different blood components (serum, activated plasma, and plasma/platelets) to evaluate human osteoblast proliferation and synthetic activity and inflammatory response presented as a cytokine profile of peripheral blood mononuclear cells (PBMCs) under conditions imitating the situation upon implantation. The cells were cultivated on coated Ti-plasma-sprayed (Ti-PS), Ti-etched (Ti-Etch), Ti-hydroxyapatite (Ti-HA), and ZrO2 surfaces. The plasma/platelets coating supported osteoblast proliferation only on osteoconductive Ti-HA and Ti-Etch whereas activated plasma enhanced proliferation on all surfaces. Differentiation (BAP) and IL-8 production remained unchanged or decreased irrespective of the coating and surface; only the serum and plasma/platelets-coated ZrO2 exhibited higher BAP and IL-8 expression. RANKL production increased on serum and activated plasma coatings. PBMCs produced especially cytokines playing role in inflammatory phase of wound healing, that is, IL-6, GRO-α, GRO, ENA-78, IL-8, GM-CSF, EGF, and MCP-1. Cytokine profiles were comparable for all tested surfaces; only ENA-78, IL-8, GM-CSF, and MCP-1 expression depended on materials and coatings. The activated plasma coating led to uniformed surfaces and represented a favorable treatment especially for bioinert Ti-PS and ZrO2 whereas all coatings had no distinctive effect on bioactive Ti-HA and Ti-Etch.

Institute of Macromolecular Chemistry Academy of Sciences of the Czech Republic Heyrovskeho Namesti 2 162 06 Prague Czech Republic

Rheumatological Institute Na Slupi 4 128 50 Prague Czech Republic

School of Dental Medicine General University Hospital Prague 1st Faculty of Medicine Charles University Prague Karlovo Namesti 32 121 11 Prague Czech Republic

The Institute of Hematology and Blood Transfusion U Nemocnice 2094 1 128 20 Prague Czech Republic

Zobrazit více v PubMed

Jemat A., Ghazali M. J., Razali M., Otsuka Y. Surface modifications and their effects on titanium dental implants. BioMed Research International. 2015;2015:11. doi: 10.1155/2015/791725.791725 PubMed DOI PMC

Vlcak P., Cerny F., Weiss Z., et al. The effect of nitrogen ion implantation on the surface properties of Ti6Al4V alloy coated by a carbon nanolayer. Journal of Nanomaterials. 2013;2013:8. doi: 10.1155/2013/475758.475758 DOI

Kubies D., Himmlova L., Riedel T., et al. The interaction of osteoblasts with bone-implant materials: 1. The effect of physico-chemical surface properties of implant materials. Physiological Research. 2011;60(1):95–111. PubMed

Dohan Ehrenfest D. M., Coelho P. G., Kang B.-S., Sul Y.-T., Albrektsson T. Classification of osseointegrated implant surfaces: materials, chemistry and topography. Trends in Biotechnology. 2010;28(4):198–206. doi: 10.1016/j.tibtech.2009.12.003. PubMed DOI

Tejero R., Anitua E., Orive G. Toward the biomimetic implant surface: biopolymers on titanium-based implants for bone regeneration. Progress in Polymer Science. 2014;39(7):1406–1447. doi: 10.1016/j.progpolymsci.2014.01.001. DOI

Goodman S. B., Yao Z., Keeney M., Yang F. The future of biologic coatings for orthopaedic implants. Biomaterials. 2013;34(13):3174–3183. doi: 10.1016/j.biomaterials.2013.01.074. PubMed DOI PMC

Schliephake H. Clinical efficacy of growth factors to enhance tissue repair in oral and maxillofacial reconstruction: a systematic review. Clinical Implant Dentistry and Related Research. 2015;17(2):247–273. doi: 10.1111/cid.12114. PubMed DOI

Yoo D., Tovar N., Jimbo R., et al. Increased osseointegration effect of bone morphogenetic protein 2 on dental implants: an in vivo study. Journal of Biomedical Materials Research Part A. 2014;102(6):1921–1927. doi: 10.1002/jbm.a.34862. PubMed DOI

Thor A. L., Hong J., Kjeller G., Sennerby L., Rasmusson L. Correlation of platelet growth factor release in jawbone defect repair—a study in the dog mandible. Clinical Implant Dentistry and Related Research. 2013;15(5):759–768. doi: 10.1111/j.1708-8208.2011.00405.x. PubMed DOI

Davis V. L., Abukabda A. B., Radio N. M., et al. Platelet-rich preparations to improve healing. Part I: workable options for every size practice. Journal of Oral Implantology. 2014;40(4):500–510. doi: 10.1563/aaid-joi-d-12-00104. PubMed DOI

Davis V. L., Abukabda A. B., Radio N. M., et al. Platelet-rich preparations to improve healing. Part II: platelet activation and enrichment, leukocyte inclusion, and other selection criteria. Journal of Oral Implantology. 2014;40(4):511–521. doi: 10.1563/aaid-joi-d-12-00106. PubMed DOI

Ahmad Z., Howard D., Brooks R. A., et al. The role of platelet rich plasma in musculoskeletal science. Journal of the Royal Society of Medicine Short Reports. 2012;3(6):40–48. doi: 10.1258/shorts.2011.011148. PubMed DOI PMC

Albanese A., Licata M. E., Polizzi B., Campisi G. Platelet-rich plasma (PRP) in dental and oral surgery: from the wound healing to bone regeneration. Immunity and Ageing. 2013;10(1, article 23) doi: 10.1186/1742-4933-10-23. PubMed DOI PMC

Harnack L., Boedeker R. H., Kurtulus I., Boehm S., Gonzales J., Meyle J. Use of platelet-rich plasma in periodontal surgery—a prospective randomised double blind clinical trial. Clinical Oral Investigations. 2009;13(2):179–187. doi: 10.1007/s00784-008-0223-7. PubMed DOI

Christo S. N., Diener K. R., Bachhuka A., Vasilev K., Hayball J. D. Innate immunity and biomaterials at the nexus: friends or foes. BioMed Research International. 2015;2015:23. doi: 10.1155/2015/342304.342304 PubMed DOI PMC

Baier R. E., Dutton R. C. Initial events in interactions of blood with a foreign surface. Journal of Biomedical Materials Research. 1969;3(1):191–206. doi: 10.1002/jbm.820030115. PubMed DOI

Everts P. A. M., Knape J. T. A., Weibrich G., et al. Platelet-rich plasma and platelet gel: a review. Journal of Extra-Corporeal Technology. 2006;38(2):174–187. PubMed PMC

Kanthan S. R., Kavitha G., Addi S., Choon D. S. K., Kamarul T. Platelet-rich plasma (PRP) enhances bone healing in non-united critical-sized defects: a preliminary study involving rabbit models. Injury. 2011;42(8):782–789. doi: 10.1016/j.injury.2011.01.015. PubMed DOI

Peerbooms J. C., Colaris J. W., Hakkert A. A., et al. No positive bone healing after using platelet rich plasma in a skeletal defect. An observational prospective cohort study. International Orthopaedics. 2012;36(10):2113–2119. doi: 10.1007/s00264-012-1603-9. PubMed DOI PMC

Findikcioglu K., Findikcioglu F., Yavuzer R., Elmas C., Atabay K. Effect of platelet-rich plasma and fibrin glue on healing of critical-size calvarial bone defects. Journal of Craniofacial Surgery. 2009;20(1):34–40. doi: 10.1097/SCS.0b013e318190ddb9. PubMed DOI

Badr M., Coulthard P., Alissa R., Oliver R. The efficacy of platelet-rich plasma in grafted maxillae. A randomised clinical trial. European Journal of Oral Implantology. 2010;3(3):233–244. PubMed

Ogundipe O. K., Ugboko V. I., Owotade F. J. Can autologous platelet-rich plasma gel enhance healing after surgical extraction of mandibular third molars? Journal of Oral and Maxillofacial Surgery. 2011;69(9):2305–2310. doi: 10.1016/j.joms.2011.02.014. PubMed DOI

Frelinger A. L., III, Torres A. S., Caiafa A., et al. Platelet-rich plasma stimulated by pulse electric fields: platelet activation, procoagulant markers, growth factor release and cell proliferation. Platelets. 2016;27(2):128–135. doi: 10.3109/09537104.2015.1048214. PubMed DOI

Farrugia A. Albumin usage in clinical medicine: tradition or therapeutic? Transfusion Medicine Reviews. 2010;24(1):53–63. doi: 10.1016/j.tmrv.2009.09.005. PubMed DOI

Ghuman J., Zunszain P. A., Petitpas I., Bhattacharya A. A., Otagiri M., Curry S. Structural basis of the drug-binding specificity of human serum albumin. Journal of Molecular Biology. 2005;353(1):38–52. doi: 10.1016/j.jmb.2005.07.075. PubMed DOI

Deeb O., Rosales-Hernández M. C., Gómez-Castro C., Garduño-Juárez R., Correa-Basurto J. Exploration of human serum albumin binding sites by docking and molecular dynamics flexible ligand—protein interactions. Biopolymers. 2010;93(2):161–170. doi: 10.1002/bip.21314. PubMed DOI

Weszl M., Skaliczki G., Cselenyák A., et al. Freeze-dried human serum albumin improves the adherence and proliferation of mesenchymal stem cells on mineralized human bone allografts. Journal of Orthopaedic Research. 2012;30(3):489–496. doi: 10.1002/jor.21527. PubMed DOI

Skaliczki G., Schandl K., Weszl M., et al. Serum albumin enhances bone healing in a nonunion femoral defect model in rats: A computer tomography micromorphometry study. International Orthopaedics. 2013;37(4):741–745. doi: 10.1007/s00264-012-1770-8. PubMed DOI PMC

Mosesson M. W. Fibrinogen and fibrin structure and functions. Journal of Thrombosis and Haemostasis. 2005;3(8):1894–1904. doi: 10.1111/j.1538-7836.2005.01365.x. PubMed DOI

Whelan D., Caplice N. M., Clover A. J. P. Fibrin as a delivery system in wound healing tissue engineering applications. Journal of Controlled Release. 2014;196:1–8. doi: 10.1016/j.jconrel.2014.09.023. PubMed DOI

Silver F. H., Wang M.-C., Pins G. D. Preparation and use of fibrin glue in surgery. Biomaterials. 1995;16(12):891–903. doi: 10.1016/0142-9612(95)93113-R. PubMed DOI

Gasparotto V. P. O., Landim-Alvarenga F. C., Oliveira A. L. R., et al. A new fibrin sealant as a three-dimensional scaffold candidate for mesenchymal stem cells. Stem Cell Research & Therapy. 2014;5, article 78 doi: 10.1186/scrt467. PubMed DOI PMC

Filová E., Brynda E., Riedel T., et al. Improved adhesion and differentiation of endothelial cells on surface-attached fibrin structures containing extracellular matrix proteins. Journal of Biomedical Materials Research Part A. 2014;102(3):698–712. doi: 10.1002/jbm.a.34733. PubMed DOI

Naik B., Karunakar P., Jayadev M., Marshal V. R. Role of Platelet rich fibrin in wound healing: a critical review. Journal of Conservative Dentistry. 2013;16(4):284–293. doi: 10.4103/0972-0707.114344. PubMed DOI PMC

Davalos D., Akassoglou K. Fibrinogen as a key regulator of inflammation in disease. Seminars in Immunopathology. 2012;34(1):43–62. doi: 10.1007/s00281-011-0290-8. PubMed DOI

Trindade R., Albrektsson T., Tengvall P., Wennerberg A. Foreign body reaction to biomaterials: on mechanisms for buildup and breakdown of osseointegration. Clinical Implant Dentistry and Related Research. 2016;18(1):192–203. doi: 10.1111/cid.12274. PubMed DOI

Owens D. K., Wendt R. C. Estimation of the surface free energy of polymers. Journal of Applied Polymer Science. 1969;13(8):1741–1747. doi: 10.1002/app.1969.070130815. DOI

Křížová P., Mášová L., Suttnar J., et al. The influence of intrinsic coagulation pathway on blood platelets activation by oxidized cellulose. Journal of Biomedical Materials Research Part A. 2007;82(2):274–280. doi: 10.1002/jbm.a.31060. PubMed DOI

Bellavite P., Andrioli G., Guzzo P., et al. A colorimetric method for the measurement of platelet adhesion in microtiter plates. Analytical Biochemistry. 1994;216(2):444–450. doi: 10.1006/abio.1994.1066. PubMed DOI

Vaníčková M., Suttnar J., Dyr J. E. The adhesion of blood platelets on fibrinogen surface: comparison of two biochemical microplate assays. Platelets. 2006;17(7):470–476. doi: 10.1080/09537100600758875. PubMed DOI

Laughton C. Quantification of attached cells in microtiter plates based on Coomassie brilliant blue G-250 staining of total cellular protein. Analytical Biochemistry. 1984;140(2):417–423. doi: 10.1016/0003-2697(84)90187-8. PubMed DOI

Piattelli A., Scarano A., Corigliano M., Piattelli M. Effects of alkaline phosphatase on bone healing around plasma-sprayed titanium implants: a pilot study in rabbits. Biomaterials. 1996;17(14):1443–1449. doi: 10.1016/0142-9612(96)87288-7. PubMed DOI

Price C. P. Multiple forms of human serum alkaline phosphatase: detection and quantitation. Annals of Clinical Biochemistry. 1993;30(4):355–372. doi: 10.1177/000456329303000403. PubMed DOI

Yamashita T., Takahashi N., Udagawa N. New roles of osteoblasts involved in osteoclast differentiation. World Journal of Orthopaedics. 2012;3(11):175–181. doi: 10.5312/wjo.v3.i11.175. PubMed DOI PMC

Fritz E. A., Glant T. T., Vermes C., Jacobs J. J., Roebuck K. A. Titanium particles induce the immediate early stress responsive chemokines IL-8 and MCP-1 in osteoblasts. Journal of Orthopaedic Research. 2002;20(3):490–498. doi: 10.1016/S0736-0266(01)00154-1. PubMed DOI

Quirynen M., Bollen C. M. L. The influence of surface roughness and surface free energy on supra- and subgingival plaque formation in man. A review of the literature. Journal of Clinical Periodontology. 1994;22(1):1–20. PubMed

Milleding P., Gerdes S., Holmberg K., Karlsson S. Surface energy of non-corroded and corroded dental ceramic materials before and after contact with salivary proteins. European Journal of Oral Sciences. 1999;107(5):384–392. doi: 10.1046/j.0909-8836.1999.eos107510.x. PubMed DOI

Pešáková V., Kubies D., Hulejová H., Himmlová L. The influence of implant surface properties on cell adhesion and proliferation. Journal of Materials Science: Materials in Medicine. 2007;18(3):465–473. doi: 10.1007/s10856-007-2006-0. PubMed DOI

Barrientos S., Stojadinovic O., Golinko M. S., Brem H., Tomic-Canic M. Growth factors and cytokines in wound healing. Wound Repair and Regeneration. 2008;16(5):585–601. doi: 10.1111/j.1524-475X.2008.00410.x. PubMed DOI

Ding J., Tredget E. E. The role of chemokines in fibrotic wound healing. Advances in Wound Care. 2015;4(11):673–686. doi: 10.1089/wound.2014.0550. PubMed DOI PMC

Behm B., Babilas P., Landthaler M., Schreml S. Cytokines, chemokines and growth factors in wound healing. Journal of the European Academy of Dermatology & Venereology. 2012;26(7):812–820. doi: 10.1111/j.1468-3083.2011.04415.x. PubMed DOI

Jones J. A., Chang D. T., Meyerson H., et al. Proteomic analysis and quantification of cytokines and chemokines from biomaterial surface-adherent macrophages and foreign body giant cells. Journal of Biomedical Materials Research—Part A. 2007;83(3):585–596. doi: 10.1002/jbm.a.31221. PubMed DOI

Kearns A. E., Khosla S., Kostenuik P. J. Receptor activator of nuclear factor κB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocrine Reviews. 2008;29(2):155–192. doi: 10.1210/er.2007-0014. PubMed DOI PMC

Weibrich G., Hansen T., Kleis W., Buch R., Hitzler W. E. Effect of platelet concentration in platelet-rich plasma on peri-implant bone regeneration. Bone. 2004;34(4):665–671. doi: 10.1016/j.bone.2003.12.010. PubMed DOI

Choi B.-H., Im C.-J., Huh J.-Y., Suh J.-J., Lee S.-H. Effect of platelet-rich plasma on bone regeneration in autogenous bone graft. International Journal of Oral & Maxillofacial Surgery. 2004;33(1):56–59. doi: 10.1054/ijom.2003.0466. PubMed DOI

Massini P., Käser-Glanzmann R., Luscher E. F. Movement of calcium ions and their role in the activation of platelets. Thrombosis and Haemostasis. 1978;40(2):212–218. PubMed

Ogino Y., Ayukawa Y., Kukita T., Atsuta I., Koyano K. Platelet-rich plasma suppresses osteoclastogenesis by promoting the secretion of osteoprotegerin. Journal of Periodontal Research. 2009;44(2):217–224. doi: 10.1111/j.1600-0765.2008.01109.x. PubMed DOI

Orman M. A., Nguyen T. T., Ierapetritou M. G., Berthiaume F., Androulakis I. P. Comparison of the cytokine and chemokine dynamics of the early inflammatory response in models of burn injury and infection. Cytokine. 2011;55(3):362–371. doi: 10.1016/j.cyto.2011.05.010. PubMed DOI PMC

Huang R.-P., Burkholder B., Sloane Jones V., et al. Cytokine antibody arrays in biomarker discovery and validation. Current Proteomics. 2012;9(1):55–70. doi: 10.2174/157016412799746209. DOI

Zaja-Milatovic S., Richmond A. CXC chemokines and their receptors: a case for a significant biological role in cutaneous wound healing. Histology and Histopathology. 2008;23(11):1399–1407. PubMed PMC

Mackiewicz A., Kushner I., Baumann H. Acute Phase Proteins Molecular Biology, Biochemistry, and Clinical Applications. Boca Raton, Fla, USA: CRC Press; 1993.

Lee C. Y. S., Rohrer M. D., Prasad H. S. Immediate loading of the grafted maxillary sinus using platelet rich plasma and autogenous bone: a preliminary study with histologic and histomorphometric analysis. Implant Dentistry. 2008;17(1):59–73. doi: 10.1097/id.0b013e318166ce3c. PubMed DOI

Rees P. A., Greaves N. S., Baguneid M., Bayat A. Chemokines in wound healing and as potential therapeutic targets for reducing cutaneous scarring. Advances in Wound Care. 2015;4(11):687–703. doi: 10.1089/wound.2014.0568. PubMed DOI PMC

Özkurt Z., Kazazoğlu E. Zirconia dental implants: a literature review. Journal of Oral Implantology. 2011;37(3):367–376. doi: 10.1563/aaid-joi-d-09-00079. PubMed DOI

Anand U., Mehta D. S. Evaluation of immediately loaded dental implants bioactivated with platelet-rich plasma placed in the mandibular posterior region: a clinico-radiographic study. Journal of Indian Society of Periodontology. 2012;16(1):89–95. doi: 10.4103/0972-124x.94612. PubMed DOI PMC

Anitua E. A. Enhancement of osseointegration by generating a dynamic implant surface. Journal of Oral Implantology. 2006;32(2):72–76. doi: 10.1563/736.1. PubMed DOI

Titanium and Other Metal Hypersensitivity Diagnosed by MELISA® Test: Follow-Up Study