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Antithrombotic Protein Filter Composed of Hybrid Tissue-Fabric Material has a Long Lifetime

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Abstract

There are recent reports of hybrid tissue–fabric materials with good performance—high biocompatibility and high mechanical strength. In this study, we demonstrate the capability of a hybrid material as a long-term filter for blood proteins. Polyester fabrics were implanted into rats to fabricate hybrid tissue–fabric material sheets. The hybrid materials comprised biological tissue grown on the fabric. The materials were extracted from the rat’s body, approximately 100 days post-implantation. The tissues were decellularized to prevent immunological rejection. An antithrombogenicity test was performed by dropping blood onto the hybrid material surface. The hybrid material showed lesser blood coagulation than polysulfone and cellulose. Blood plasma was filtered using the hybrid material to evaluate the protein removal percentage and the lifetime of the hybrid material in vitro. The hybrid material showed a comparable performance to conventional filters for protein removal. Moreover, the hybrid material could work as a protein filter for 1 month, which is six times the lifetime of polysulfone.

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References

  1. Chandran, K. B., D. Gao, G. Han, H. Baraniewski, and J. D. Corson. Finite-element analysis of arterial anastomoses with vein, Dacron and PTFE grafts. Med. Biol. Eng. Comput. 30:413–418, 1992.

    Article  CAS  PubMed  Google Scholar 

  2. Dungel, P., N. Long, B. Yu, Y. Moussy, and F. Moussy. Study of the effects of tissue reactions on the function of implanted glucose sensors. J. Biomed. Mater. Res. A 85(3):699–706, 2008.

    Article  PubMed  Google Scholar 

  3. Funamoto, S., K. Nam, T. Kimura, A. Murakoshi, Y. Hashimoto, K. Niwaya, and A. Kishida. The use of high-hydrostatic pressure treatment to decellularize blood vessels. Biomaterials 31:3590–3595, 2010.

    Article  CAS  PubMed  Google Scholar 

  4. Fung, Y. C. Biomechanics: Mechanical Properties of Living Tissues (2nd ed.). New York: Springer, 1993.

    Book  Google Scholar 

  5. Gough, D. A., L. S. Kumosa, T. L. Routh, J. T. Lin, and J. Y. Lucisano. Function of an implanted tissue glucose sensor for more than 1 year in animals. Sci. Transl. Med. 2:42–53, 2010.

    Article  Google Scholar 

  6. Honge JL, Funder J, Hansen E, Dohmen PM, Konertz W, Hasenkam JM. Recellularization of aortic valves in pigs. Eur. J. Cardiothorac. Surg. 39:829–834, 2011.

    Article  PubMed  Google Scholar 

  7. Iatridis, J. C., J. Wu, J. A. Yandow, and H. M. Langevin. Subcutaneous tissue mechanical behavior is linear and viscoelastic under uniaxial tension. Connect. Tissue Res. 44:208–217, 2003.

    Article  PubMed  Google Scholar 

  8. Ishihara, K., H. Fujita, T. Yoneyama, and Y. Iwasaki. Antithrombogenic polymer alloy composed of 2-methacryloyloxyethyl phosphorylcholine polymer and segmented polyurethane. J. Biomater. Sci. Polym. Ed. 11:1183–1195, 2000.

    Article  CAS  PubMed  Google Scholar 

  9. Jia, W. Z., K. Wang, and X. H. Xia. Elimination of electrochemical interferences in glucose biosensors. TrAC Trends Anal. Chem. 29:306–318, 1994.

    Article  Google Scholar 

  10. Ju, Y. M., B. Yu, L. West, Y. Moussy, and F. Moussy. A novel porous collagen scaffold around an implantable biosensor for improving biocompatibility. II. Long term in vitro/in vivo sensitivity characteristics of sensors with NDGA or GA crosslinked collagen scaffolds. J. Biomed. Mater. Res. A 92:650–658, 2010.

    PubMed  Google Scholar 

  11. Kaltenbrunner, M., T. Sekitani, J. Reeder, T. Yokota, K. Kuribara, T. Tokuhara, and T. Someya. An ultra-lightweight design for imperceptible plastic electronics. Nature 499:458–463, 2013.

    Article  CAS  PubMed  Google Scholar 

  12. Kawase, Y., Y. Inoue, T. Isoyama, I. Saito, H. Nakagawa, T. Ono, and H. Kumagai. Development of hybrid blood removal cannula use of titan rigid for ventricular assist device (VAD). Seitai Ikougaku 51:R-229, 2013.

    Google Scholar 

  13. Kim, W. G., J. K. Park, and W. Y. Lee. Tissue-engineered heart valve leaflets: an effective method of obtaining acellularized valve xenografts. Int. J. Artif. Organs 25:791–797, 2002.

    CAS  PubMed  Google Scholar 

  14. Kingshott, P., H. Thissen, and H. J. Griesser. Effects of cloud-point grafting, chain length, and density of PEG layers on competitive adsorption of ocular proteins. Biomaterials 23:2043–2056, 2002.

    Article  CAS  PubMed  Google Scholar 

  15. Kishi, A., T. Isoyama, I. Saito, H. Miura, H. Nakagawa, A. Kouno, and M. Noshiro. Use of in vivo insert molding to form a jellyfish valve leaflet. Artif. Organs 34(12):1125–1131, 2010.

    Article  CAS  PubMed  Google Scholar 

  16. Le Tissier, P., J. P. Stoye, Y. Takeuchi, C. Patience, and R. A. Weiss. Two sets of human-tropic pig retrovirus. Nature 389:681–682, 1997.

    Article  PubMed  Google Scholar 

  17. Leypoldt, J. K. Fouling of ultrafiltration and hemodialysis membranes by plasma proteins. Blood Purif. 12:285–291, 1994.

    Article  CAS  PubMed  Google Scholar 

  18. Liu, G. F., Z. J. He, D. P. Yang, X. F. Han, T. F. Guo, C. G. Hao, and C. L. Nie. Decellularized aorta of fetal pigs as a potential scaffold for small diameter tissue engineered vascular graft. Chin. Med. J. (Engl.) 121:1398–1406, 2008.

    Google Scholar 

  19. Morais, J. M., F. Papadimitrakopoulos, and D. J. Burgess. Biomaterials/tissue interactions: possible solutions to overcome foreign body response. AAPS J. 12:188–196, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Murase, Y., Y. Narita, H. Kagami, K. Miyamoto, Y. Ueda, M. Ueda, and T. Murohara. Evaluation of compliance and stiffness of decellularized tissues as scaffolds for tissue-engineered small caliber vascular grafts using intravascular ultrasound. ASAIO J. 52:450–455, 2006.

    Article  CAS  PubMed  Google Scholar 

  21. Nakayama, Y., and T. Tsujinaka. Acceleration of robust “Biotube” vascular graft fabrication by in-body tissue architecture technology using a novel eosin Y-releasing mold. J. Biomed. Mater. Res. B Appl. Biomater. 102(2):231–238, 2014.

    Article  PubMed  Google Scholar 

  22. Nakayama, Y., S. Yamaoka, M. Yamanami, M. Fujiwara, M. Uechi, K. Takamizawa, and H. Yaku. Water-soluble argatroban for antithrombogenic surface coating of tissue-engineered cardiovascular tissues. J. Biomed. Mater. Res. B Appl. Biomater. 99:420–430, 2011.

    Article  PubMed  Google Scholar 

  23. Nauli, A. M., Y. Sun, J. D. Whittimore, S. Atyia, G. Krishnaswamy, and S. M. Nauli. Chylomicrons produced by Caco-2 cells contained ApoB-48 with diameter of 80–200 nm. Physiol. Rep. 2:e12018, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Nishida, K., M. Sakakida, K. Ichinose, T. Uemura, M. Uehara, K. Kajiwara, and N. Nakabayashi. Development of a ferrocene-mediated needle-type glucose sensor covered with newly designed biocompatible membrane, 2-methacryloyloxyethyl phosphorylcholine-co-n-butyl methacrylate. Med. Prog. Technol. 21:91–103, 1995.

    CAS  PubMed  Google Scholar 

  25. Novak, M. T., F. Yuan, and W. M. Reichert. Modeling the relative impact of capsular tissue effects on implanted glucose sensor time lag and signal attenuation. Anal. Bioanal. Chem. 398:1695–1705, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Onuki, Y., U. Bhardwaj, F. Papadimitrakopoulos, and D. J. Burgess. A review of the biocompatibility of implantable devices: current challenges to overcome foreign body response. J. Diabetes Sci. Technol. 2:1003–1015, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Patience, C., Y. Takeuchi, and R. A. Weiss. Infection of human cells by an endogenous retrovirus of pigs. Nat. Med. 3:282–286, 1997.

    Article  CAS  PubMed  Google Scholar 

  28. Patil, S., N. F. Martinez, J. R. Lozano, and R. Garcia. Force microscopy imaging of individual protein molecules with sub-pico Newton force sensitivity. J. Mol. Recognit. 20:516–523, 2007.

    Article  CAS  PubMed  Google Scholar 

  29. Quinn, C. P., C. P. Pathak, A. Heller, and J. A. Hubbell. Photo-crosslinked copolymers of 2-hydroxyethyl methacrylate, poly(ethylene glycol) tetra-acrylate and ethylene dimethacrylate for improving biocompatibility of biosensors. Biomaterials 16:389–396, 1995.

    Article  CAS  PubMed  Google Scholar 

  30. Ranieri, J. P., D. L. Hern-Anderson, A. M. J. Gonin, and B. K. McIlroy Processed ratite carotid arteries as xenogeneic small bore vascular grafts. U.S. Patent No. 20,020,077,697, 2002.

  31. Reach, G., and G. S. Wilson. Can continuous glucose monitoring be used for the treatment of diabetes? Anal. Chem. 64:381A–386A, 1992.

    CAS  PubMed  Google Scholar 

  32. Reddy, S. M., and P. M. Vagama. Surfactant-modified poly(vinyl chloride) membranes as biocompatible interfaces for amperometric enzyme electrodes. Anal. Chim. Acta 350:77–89, 1997.

    Article  CAS  Google Scholar 

  33. Reichert, W. M., and S. S. Saavedra. Materials consideration in the selection, performance, and adhesion of polymeric encapsulants for implantable sensors. Mater. Sci. Technol. 64(6):A381–A386, 1992.

    Google Scholar 

  34. Reichert, W. M. and A. A. Sharkawy. Biosensors. In: Handbook of Biomaterials Evaluation: Scientific, Technical, and Clinical Testing of Implant Materials. Philadelphia: Taylor & Francis, pp. 439–459, 1999.

  35. Sakai, O., K. Kanda, K. Takamizawa, T. Sato, H. Yaku, and Y. Nakayama. Faster and stronger vascular “Biotube” graft fabrication in vivo using a novel nicotine-containing mold. J. Biomed. Mater. Res. B Appl. Biomater. 90:412–420, 2009.

    PubMed  Google Scholar 

  36. Shaw, G. W., D. J. Claremont, and J. C. Pickup. In vitro testing of a simply constructed, highly stable glucose sensor suitable for implantation in diabetic patients. Biosens. Bioelectron. 6:401–406, 1991.

    Article  CAS  PubMed  Google Scholar 

  37. Sheller, N. B., S. Petrash, M. D. Foster, and V. V. Tsukruk. Atomic force microscopy and X-ray reflectivity studies of albumin adsorbed onto self-assembled monolayers of hexadecyltrichlorosilane. Langmuir 14:4535–4544, 1998.

    Article  CAS  Google Scholar 

  38. Tanaka, M., T. Hayashi, and S. Morita. The roles of water molecules at the biointerface of medical polymers. Polym. J. 45:701–710, 2013.

    Article  CAS  Google Scholar 

  39. Tanaka, M., T. Motomura, M. Kawada, T. Anzai, Y. Kasori, T. Shiroya, K. Shimura, and A. Mochizuki. Blood compatible aspects of poly(2-methoxyethylacrylate)(PMEA)—relationship between protein adsorption and platelet adhesion on PMEA surface. Biomaterials 21(14):1471–1481, 2000.

    Article  CAS  PubMed  Google Scholar 

  40. Tinkilic, N., O. Cubuk, and I. Isildak. Glucose and urea biosensors based on all solid-state PVC–NH2 membrane electrodes. Anal. Chim. Acta 452:29–34, 2002.

    Article  CAS  Google Scholar 

  41. Toscano, A., and M. M. Santore. Fibrinogen adsorption on three silica-based surfaces: conformation and kinetics. Langmuir 22:2588–2597, 2006.

    Article  CAS  PubMed  Google Scholar 

  42. Vadgama, P. M., and G. Reach. Advances in Biosensors: Chemical Sensors for In Vivo Monitoring. London: JAI Press, 1993.

    Google Scholar 

  43. Valdes, T. I., and F. Moussy. A ferric chloride pre-treatment to prevent calcification of Nafion membrane used for implantable biosensors. Biosens. Bioelectron. 14(6):579–585, 1999.

    Article  CAS  PubMed  Google Scholar 

  44. Wisniewski, N., F. Moussy, and W. M. Reichert. Characterization of implantable biosensor membrane biofouling. Fresenius J. Anal. Chem. 366:611–621, 2000.

    Article  CAS  PubMed  Google Scholar 

  45. Xu, Y., G. Zhang, Y. Chang, Y. X. Qiu, and C. Wang. The preparation of acellular dermal matrices by freeze-thawing and ultrasonication process and the evaluation of its antigenicity. Cell Biochem. Biophys. 73(1):27–33, 2015.

    Article  CAS  PubMed  Google Scholar 

  46. Yokota, T., K. Kuribara, T. Tokuhara, U. Zschieschang, H. Klauk, K. Takimiya, and T. Someya. Flexible low-voltage organic transistors with high thermal stability at 250°C. Adv. Mater. 25:3639–3644, 2013.

    Article  CAS  PubMed  Google Scholar 

  47. Yokota, T., T. Sekitani, T. Tokuhara, N. Take, U. Zschieschang, H. Klauk, and T. Someya. Sheet-type flexible organic active matrix amplifier system using pseudo-CMOS circuits with floating-gate structure. Electron. Devices 59:3434–3441, 2012.

    Article  Google Scholar 

  48. Zhang, S., Y. Benmakroha, P. Rolfe, T. Shinobu, and I. Kazuhiko. Development of a haemocompatible pO2 sensor with phospholipid-based copolymer membrane. Biosens. Bioelectron. 11:1019–1029, 1996.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge Dr. Yoshinori Mitamura and Hidemoto Nakagawa for their helpful in-depth discussions on this study. This study was supported by JST ERATO. The strength test of hybrid material was supported by the cooperation program of research institutes in Tohoku University.

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Authors and Affiliations

  1. Department of Electrical Engineering and Information Systems, Graduate School of Engineering, The University of Tokyo, Tokyo, 113-8656, Japan

    Yusuke Inoue, Tomoyuki Yokota, Tsuyoshi Sekitani, Akiko Kaneko, Taeseong Woo, Takao Someya & Masaki Sekino

  2. Department of Biomedical Engineering, Graduate School of Medicine, The University of Tokyo, Tokyo, 113-0033, Japan

    Yusuke Inoue, Itsuro Saito, Takashi Isoyama & Yusuke Abe

  3. Department of Medical Engineering and Cardiology, Institute of Development, Aging and Cancer, Tohoku University, Miyagi, 980-8575, Japan

    Yusuke Inoue & Tomoyuki Yambe

  4. The Institute of Scientific and Industrial Research (ISIR), Osaka University, Osaka, 567-0047, Japan

    Tsuyoshi Sekitani

  5. Department of Applied Chemistry, Graduate School of Engineering, Kyushu University, Fukuoka, 819-0395, Japan

    Shingo Kobayashi & Masaru Tanaka

  6. Department of Biochemical Engineering, Graduate School of Science and Engineering, Yamagata University, Yonezawa, 992-8510, Japan

    Tomokazu Shibuya

  7. Institute of Fluid Science, Tohoku University, Miyagi, 980-8577, Japan

    Hiroyuki Kosukegawa

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  1. Yusuke Inoue
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  2. Tomoyuki Yokota
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Correspondence to Masaki Sekino.

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Associate Editor Thurmon E. Lockhart oversaw the review of this article.

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Inoue, Y., Yokota, T., Sekitani, T. et al. Antithrombotic Protein Filter Composed of Hybrid Tissue-Fabric Material has a Long Lifetime. Ann Biomed Eng 45, 1352–1364 (2017). https://doi.org/10.1007/s10439-016-1781-5

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