Fouling in ocular devices: implications for drug delivery, bioactive surface immobilization, and biomaterial design

Abstract

The last 30 years has seen a proliferation of research on protein-resistant biomaterials targeted at designing bio-inert surfaces, which are prerequisite for optimal performance of implantable devices that contact biological fluids and tissues. These efforts have only been able to yield minimal results, and hence, the ideal anti-fouling biomaterial has remained elusive. Some studies have yielded biomaterials with a reduced fouling index among which high molecular weight polyethylene glycols have remained dominant. Interestingly, the field of implantable ocular devices has not experienced an outflow of research in this area, possibly due to the assumption that biomaterials tested in other body fluids can be translated for application in the ocular space. Unfortunately, progression in the molecular understanding of many ocular conditions has brought to the fore the need for treatment options that necessitates the use of anti-fouling biomaterials. From the earliest implanted horsehair and silk seton for glaucoma drainage to the recent mini telescopes for sight recovery, this review provides a concise incursion into the gradual evolution of biomaterials for the design of implantable ocular devices as well as approaches used to overcome the challenges with fouling. The implication of fouling for drug delivery, the design of immune-responsive biomaterials, as well as advanced surface immobilization approaches to support the overall performance of implantable ocular devices are also reviewed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Adapted from Adv. Drug Deliv. Rev., vol. 128, pp. 148–157, H. Kaji, N. Nagai, M. Nishizawa, and T. Abe, “Drug delivery devices for retinal diseases,” Copyright (2018) with permission from Elsevier [40]

Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Abbreviations

MEMS:

Microelectromechanical systems

DME:

Diabetic macular edema

AMD:

Age-related macular degeneration

FBR:

Foreign body response

GDD:

Glaucoma drainage device

TF:

Tissue factor

PMN:

Polymorphonuclear leucocytes

ACAID:

Anterior chamber-associated immune deviation

ROS:

Reactive oxygen species

TLR:

Toll-like receptors

PRR:

Pattern recognition receptor

HMGB 1:

High mobility group box 1

MCP:

Monocyte chemotactic protein

MIP 1β:

Macrophage inflammatory protein 1β

DC:

Dendritic cells

CLs:

Contact lens

IPN or ipn:

Interpenetrating polymer networks

MPC:

2-Methacryloyloxyethyl phosphorylcholine

PMPC:

Poly(2-methacryloyloxyethyl) phosphorylcholine

PSiMA:

Poly(bis(trimethylsilyloxy)methylsilylpropyl glycerol methacrylate)

IOL:

Intraocular lens

ACO:

Anterior capsular opacification

PCO:

Posterior capsule opacification

FGF:

Fibroblast growth factor

LBL:

Layer by layer

ASC:

Anterior subcapsular cataract

MIGS:

Minimally invasive glaucoma surgery

TBO:

Trabeculoctomy

TBE:

Trabeculectomy

GFS:

Glaucoma filtration surgery

MMPC:

2-(Methacryloyloxy)ethyl-[N-(methacryloyloxy)ethyl phosphorylcholine

BSA:

Bovine serum albumin

FIH:

First in humans

References

  1. 1.

    Neves HP. “1 - Materials for implantable systems,” in Implantable Sensor Systems for Medical Applications. Inmann A, Hodgins D, Eds. Woodhead Publishing. 2013. pp. 3–38.

  2. 2.

    Du Toit LC, Govender T, Carmichael T, Kumar P, Choonara YE, Pillay V. Design of an Anti-inflammatory composite nanosystem and evaluation of its potential for ocular drug delivery. J Pharm Sci. 2013;102(8):2780–805. https://doi.org/10.1002/jps.23650.

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Subrizi A, del Amo EM, Korzhikov-Vlakh V, Tennikova T, Ruponen M, Urtti A. Design principles of ocular drug delivery systems: importance of drug payload, release rate, and material properties. Drug Discov Today. 2019. https://doi.org/10.1016/j.drudis.2019.02.001.

    Article  PubMed  Google Scholar 

  4. 4.

    Choonara YE, Pillay V, Danckwerts MP, Carmichael TR, du Toit LC. A review of implantable intravitreal drug delivery technologies for the treatment of posterior segment eye diseases. J Pharm Sci. 2010;99(5):2219–39. https://doi.org/10.1002/jps.21987.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Choonara YE, Pillay V, Carmichael T, Danckwerts MP. An in vitro study of the design and development of a novel doughnut-shaped minitablet for intraocular implantation. Int J Pharm. 2006;310(1–2):15–24. https://doi.org/10.1016/j.ijpharm.2005.10.019.

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Humar M, Kwok SJJ, Choi M, Yetisen AK, Cho S, Yun S-H. Toward biomaterial-based implantable photonic devices. Nanophotonics. 2016;6(2):414–34. https://doi.org/10.1515/nanoph-2016-0003.

    Article  Google Scholar 

  7. 7.

    Cullen CL. Glaucoma Drainage Devices. In: Tombran-Tink J, Barnstable CJ, Rizzo JF, editors. Visual prosthesis and ophthalmic devices: new hope in sight. Totowa, NJ: Humana Press; 2007. p. 173–90.

    Google Scholar 

  8. 8.

    Lim K et al. Glaucoma drainage devices; past, present, and future. Br J Ophthalmol. 1998;82(9):1083–1089 Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1722728/. Accessed 04 Mar 2019.

  9. 9.

    du Toit LC, Pillay V, Choonara YE, Govender T, Carmichael T. Ocular drug delivery – a look towards nanobioadhesives. Expert Opin Drug Deliv. 2011;8(1):71–94. https://doi.org/10.1517/17425247.2011.542142.

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Vassileva E. The Challenge of Non Fouling Surfaces: Polymers could be the Answer. p. 2.

  11. 11.

    Bixler Gregory D, Bhushan B. Biofouling: lessons from nature. Philos Trans R Soc Math Phys Eng Sci. 1967;2012(370):2381–417. https://doi.org/10.1098/rsta.2011.0502.

    CAS  Article  Google Scholar 

  12. 12.

    Onuki Y, Bhardwaj U, Papadimitrakopoulos F, Burgess DJ. A Review of the biocompatibility of implantable devices: current challenges to overcome foreign body response. J Diabetes Sci Technol. 2008;2(6):1003–15. https://doi.org/10.1177/193229680800200610.

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Chen S, Li L, Zhao C, Zheng J. Surface hydration: principles and applications toward low-fouling/nonfouling biomaterials. Polymer. 2010;51(23):5283–93. https://doi.org/10.1016/j.polymer.2010.08.022.

    CAS  Article  Google Scholar 

  14. 14.

    Zhang TD, Zhang X, Deng X. Applications of protein-resistant polymer and hydrogel coatings on biosensors and biomaterials. 2018. https://doi.org/10.33582/2637-4927/1006.

  15. 15.

    Chirila T, Harkin D. Biomaterials and regenerative medicine in ophthalmology. Woodhead Publishing. 2016.

  16. 16.

    Bawa P, Pillay V, Choonara YE, du Toit LC. Stimuli-responsive polymers and their applications in drug delivery. Biomed Mater Bristol Engl. 2009;4(2):022001. https://doi.org/10.1088/1748-6041/4/2/022001.

    CAS  Article  Google Scholar 

  17. 17.

    du Toit LC, Carmichael T, Govender T, Kumar P, Choonara YE, Pillay V. In vitro, in vivo, and in silico evaluation of the bioresponsive behavior of an intelligent intraocular implant. Pharm Res. 2014;31(3):607–34. https://doi.org/10.1007/s11095-013-1184-3.

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Isaacson A, Swioklo S, Connon CJ. 3D bioprinting of a corneal stroma equivalent. Exp Eye Res. 2018;173:188–93. https://doi.org/10.1016/j.exer.2018.05.010.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Xie J, Lee S, Chen X. Nanoparticle-based theranostic agents. Adv Drug Deliv Rev. 2010;62(11):1064–79. https://doi.org/10.1016/j.addr.2010.07.009.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Pop-Georgievski O, Rodriguez-Emmenegger C, de los Santos Pereira A, Proks V, Brynda E, Rypáček F. Biomimetic non-fouling surfaces: extending the concepts. J Mater Chem B. 2013;1(22):2859–2867 https://doi.org/10.1039/C3TB20346H.

  21. 21.

    Rønbeck M, Kugelberg M. Posterior capsule opacification with 3 intraocular lenses: 12-year prospective study. J Cataract Refract Surg. 2014;40(1):70–6. https://doi.org/10.1016/j.jcrs.2013.07.039.

    Article  PubMed  Google Scholar 

  22. 22.

    Jiang S, Cao Z. Ultralow-fouling, functionalizable, and hydrolyzable zwitterionic materials and their derivatives for biological applications. Adv Mater. 2010;22(9):920–32. https://doi.org/10.1002/adma.200901407.

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    McKeown PP, et al. Magnetically actuated left ventricular assist device (lvad): acute animal test results. In: Akutsu T, Koyanagi H, editors., et al., Heart Replacement: Artificial Heart 4. Tokyo: Springer Japan; 1993. p. 295–9.

    Google Scholar 

  24. 24.

    Ayyala RS, et al. Comparison of different biomaterials for glaucoma drainage devices. Arch Ophthalmol. 1999;117(2):233–6. https://doi.org/10.1001/archopht.117.2.233.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Gullapalli VK, Khodair MA, Wang H, Sugino IK, Madreperla S, Zarbin MA. Chapter 125 - transplantation frontiers. In: Ryan SJ, Sadda SR, Hinton DR, Schachat AP, Sadda SR, Wilkinson CP, Wiedemann P, Schachat AP, editors. Retina (Fifth Edition). London: W.B. Saunders; 2013. p. 2058–77.

    Google Scholar 

  26. 26.

    Hoffman AS. Non-fouling surface technologies. J Biomater Sci Polym Ed. 1999;10(10):1011–4. https://doi.org/10.1163/156856299X00658.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Ferrari M, Cirisano F, Morán MC. Mammalian Cell Behavior on Hydrophobic Substrates: Influence of Surface Properties. Colloids Interfaces. 2019;3(2):48. https://doi.org/10.3390/colloids3020048.

    CAS  Article  Google Scholar 

  28. 28.

    Franz S, Rammelt S, Scharnweber D, Simon JC. Immune responses to implants – a review of the implications for the design of immunomodulatory biomaterials. Biomaterials. 2011;32(28):6692–709. https://doi.org/10.1016/j.biomaterials.2011.05.078.

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Kohn J, Khan IJ, Iovine C, Velagaleti P, Anglade E, Gilger B. Ocular biocompatibility, toxicity, and distribution from erodible polycarbonate polymer episcleral implants (LX212) in rabbits. Invest Ophthalmol Vis Sci. 2010;51(13):5326–5326. Available: https://iovs.arvojournals.org/article.aspx?articleid=2373928. Accessed 22 Mar 2019.

  30. 30.

    Puleo DA, Bizios R. Biological interactions on materials surfaces: understanding and controlling protein, cell, and tissue responses. Springer Science & Business Media. 2009.

  31. 31.

    Mariani E, Lisignoli G, Borzì RM, Pulsatelli L. Biomaterials: foreign bodies or tuners for the immune response? Int J Mol Sci. 2019;20(3):636. https://doi.org/10.3390/ijms20030636.

    CAS  Article  PubMed Central  Google Scholar 

  32. 32.

    Masli S, Vega JL. Ocular immune privilege sites. Methods Mol Biol Clifton NJ. 2011;677:449–58. https://doi.org/10.1007/978-1-60761-869-0_28.

    CAS  Article  Google Scholar 

  33. 33.

    Keino H, Horie S, Sugita S. Immune Privilege and Eye-Derived T-Regulatory Cells. J Immunol Res 2018. https://www.hindawi.com/journals/jir/2018/1679197/. Accessed 18 Feb 2020.

  34. 34.

    Davis JL, Gilger BC, Robinson MR. Novel approaches to ocular drug delivery. Curr Opin Mol Ther. 2004;6(2):195–205.

    CAS  PubMed  Google Scholar 

  35. 35.

    “US Patent Application for compositions, systems, and methods for scar tissue modification Patent Application (Application #20190117746 issued April 25, 2019) - Justia Patents Search.” https://patents.justia.com/patent/20190117746. Accessed 27 Apr 2020.

  36. 36.

    “- Optician.” https://www.opticianonline.net/cet-archive/5915. Accessed 27 Apr 2020.

  37. 37.

    Mann A, Tighe B. Contact lens interactions with the tear film. Exp Eye Res. 2013;117:88–98. https://doi.org/10.1016/j.exer.2013.07.013.

    CAS  Article  PubMed  Google Scholar 

  38. 38.

    Willcox MD. Tear film, contact lenses and tear biomarkers. Clin Exp Optom. 2019;102(4):350–63. https://doi.org/10.1111/cxo.12918.

    Article  PubMed  Google Scholar 

  39. 39.

    Fonn D. Targeting contact lens induced dryness and discomfort: what properties will make lenses more comfortable. Optom Vis Sci. 2007;84(4):279–85. https://doi.org/10.1097/OPX.0b013e31804636af.

    Article  PubMed  Google Scholar 

  40. 40.

    Kaji H, Nagai N, Nishizawa M, Abe T. Drug delivery devices for retinal diseases. Adv Drug Deliv Rev. 2018;128:148–57. https://doi.org/10.1016/j.addr.2017.07.002.

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Jacob JT. Biocompatibility in the development of silicone-hydrogel lenses. Eye Contact Lens. 2013;39(1):13–9. https://doi.org/10.1097/ICL.0b013e31827dbb00.

    Article  PubMed  Google Scholar 

  42. 42.

    Hui A. Contact lenses for ophthalmic drug delivery. Clin Exp Optom. 2017;100(5):494–512. https://doi.org/10.1111/cxo.12592.

    Article  PubMed  Google Scholar 

  43. 43.

    Choi SW, Kim J. Therapeutic contact lenses with polymeric vehicles for ocular drug delivery: a review. Materials. 2018;11(7):1125. https://doi.org/10.3390/ma11071125.

    CAS  Article  PubMed Central  Google Scholar 

  44. 44.

    Nasr FH, Khoee S, Dehghan MM, Chaleshtori SS, Shafiee A. Preparation and evaluation of contact lenses embedded with polycaprolactone-based nanoparticles for ocular drug delivery. Biomacromol. 2016;17(2):485–95. https://doi.org/10.1021/acs.biomac.5b01387.

    CAS  Article  Google Scholar 

  45. 45.

    Lu C, Yoganathan RB, Kociolek M, Allen C. Hydrogel containing silica shell cross-linked micelles for ocular drug delivery. J Pharm Sci. 2013;102(2):627–37. https://doi.org/10.1002/jps.23390.

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Mandal A, Bisht R, Rupenthal ID, Mitra AK. Polymeric micelles for ocular drug delivery: from structural frameworks to recent preclinical studies. J Controlled Release. 2017;248:96–116. https://doi.org/10.1016/j.jconrel.2017.01.012.

    CAS  Article  Google Scholar 

  47. 47.

    Danion A, Arsenault I, Vermette P. Antibacterial activity of contact lenses bearing surfaceimmobilized layers of intact liposomes loaded with levofloxacin. J Pharm Sci. 2007;96(9):2350–63. https://doi.org/10.1002/jps.20871.

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Katzer T, Chaves P, Bernardi A, Pohlmann AR, Guterres SS, Beck RCR. Castor oil and mineral oil nanoemulsion: development and compatibility with a soft contact lens. Pharm Dev Technol. 2014;19(2):232–7. https://doi.org/10.3109/10837450.2013.769569.

    CAS  Article  PubMed  Google Scholar 

  49. 49.

    Lattimore MR, Harding TH, Williams ST. Hydrogel Contact lens water content is dependent on tearfilm pH. Mil Med. 2018;183 Suppl_1:224–30. https://doi.org/10.1093/milmed/usx233.

  50. 50.

    Lorenz KO, Kakkassery J, Boree D, Pinto D. Atomic force microscopy and scanning electron microscopy analysis of daily disposable limbal ring contact lenses. Clin Exp Optom. 2014;97(5):411–7. https://doi.org/10.1111/cxo.12148.

    Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Goda T, Matsuno R, Konno T, Takai M, Ishihara K. Protein adsorption resistance and oxygen permeability of chemically crosslinked phospholipid polymer hydrogel for ophthalmologic biomaterials. J Biomed Mater Res B Appl Biomater. 2009a;89B(1):184–90. https://doi.org/10.1002/jbm.b.31204.

    CAS  Article  Google Scholar 

  52. 52.

    Maulvi FA, et al. Design and optimization of a novel implantation technology in contact lenses for the treatment of dry eye syndrome: In vitro and in vivo evaluation. Acta Biomater. 2017;53:211–21. https://doi.org/10.1016/j.actbio.2017.01.063.

    Article  PubMed  Google Scholar 

  53. 53.

    Yuan X, et al. Ocular drug delivery nanowafer with enhanced therapeutic efficacy. ACS Nano. 2015;9(2):1749–58. https://doi.org/10.1021/nn506599f.

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Ciolino JB, et al. In vivo performance of a drug-eluting contact lens to treat glaucoma for a month. Biomaterials. 2014;35(1):432–9. https://doi.org/10.1016/j.biomaterials.2013.09.032.

    CAS  Article  PubMed  Google Scholar 

  55. 55.

    Maulvi FA, Soni TG, Shah DO. A review on therapeutic contact lenses for ocular drug delivery. Drug Deliv. 2016;23(8):3017–26. https://doi.org/10.3109/10717544.2016.1138342.

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    “Contact Lens Spectrum - CONTACT LENSES 2017,” Contact Lens Spectrum. https://www.clspectrum.com/issues/2018/january-2018/contact-lenses-2017. Accessed 23 Mar 2019.

  57. 57.

    Peng CC, Burke MT, Carbia BE, Plummer C, Chauhan A. Extended drug delivery by contact lenses for glaucoma therapy. J Control Release Off J Control Release Soc. 2012;162(1):152–8. https://doi.org/10.1016/j.jconrel.2012.06.017.

    CAS  Article  Google Scholar 

  58. 58.

    Peng C-C, Ben-Shlomo A, Mackay EO, Plummer CE, Chauhan A. Drug delivery by contact lens in spontaneously glaucomatous dogs. Curr Eye Res. 2012;37(3):204–11. https://doi.org/10.3109/02713683.2011.630154.

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Ross AE, et al. Topical sustained drug delivery to the retina with a drug-eluting contact lens. Biomaterials. 2019;217:119285. https://doi.org/10.1016/j.biomaterials.2019.119285.

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    “TECHNOLOGY,” OcuMedic. https://ocumedic.net/technology/. Accessed 23 Mar 2019.

  61. 61.

    “Sensimed Triggerfish – Sensimed S.A.” https://www.sensimed.ch/sensimed-triggerfish/. Accessed 23 Mar 2019.

  62. 62.

    Lee JH, Pidaparti RM, Atkinson GM, Moorthy RS. Design of an implantable device for ocular drug delivery. J Drug Deliv. 2012. https://www.hindawi.com/journals/jdd/2012/527516/. Accessed 06 Nov 2018.

  63. 63.

    Badugu R, Reece EA, Lakowicz JR. Glucose-sensitive silicone hydrogel contact lens toward tear glucose monitoring. J Biomed Opt. 2018;23(5):1–9. https://doi.org/10.1117/1.JBO.23.5.057005.

    Article  PubMed  Google Scholar 

  64. 64.

    Omali N, Subbaraman L, Coles-Brennan C, Fadli Z, Jones L. Biological and clinical implications of lysozyme deposition on soft contact lenses. Optom Vis Sci. 2015;92(7):750–7. https://doi.org/10.1097/OPX.0000000000000615.

    Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Peng C-C, Fajardo NP, Razunguzwa T, Radke CJ. In vitro spoilation of silicone-hydrogel soft contact lenses in a model-blink cell. Optom Vis Sci Off Publ Am Acad Optom. 2015;92(7):768–80. https://doi.org/10.1097/OPX.0000000000000625.

    Article  Google Scholar 

  66. 66.

    Krysztofiak K, Szyczewski A. Study of dehydration and water states in new and worn soft contact lens materials. Opt Appl. 2014;44(2):237–50. https://doi.org/10.5277/oa140206.

    CAS  Article  Google Scholar 

  67. 67.

    Zhang W, Li G, Lin Y, Wang L, Wu S. Preparation and characterization of protein-resistant hydrogels for soft contact lens applications via radical copolymerization involving a zwitterionic sulfobetaine comonomer. J Biomater Sci Polym Ed. 2017;28(16):1935–49. https://doi.org/10.1080/09205063.2017.1363127.

    CAS  Article  PubMed  Google Scholar 

  68. 68.

    Shimizu T, Goda T, Minoura N, Takai M, Ishihara K. Super-hydrophilic silicone hydrogels with interpenetrating poly(2-methacryloyloxyethyl phosphorylcholine) networks. Biomaterials. 2010;31(12):3274–80. https://doi.org/10.1016/j.biomaterials.2010.01.026.

    CAS  Article  PubMed  Google Scholar 

  69. 69.

    Nanu RV et al. An overview of the influence and design of biomaterial of the intraocular implant of the posterior capsule opacification. Romanian J Ophthalmol. 2018;62(3):188–193. Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6256071/. Accessed 21 Mar 2019.

  70. 70.

    Thrimawithana TR, Rupenthal ID, Räsch SS, Lim JC, Morton JD, Bunt CR. Drug delivery to the lens for the management of cataracts. Adv Drug Deliv Rev. 2018;126:185–94. https://doi.org/10.1016/j.addr.2018.03.009.

    CAS  Article  PubMed  Google Scholar 

  71. 71.

    Callahan MA. Technique of congenital cataract surgery with the kelman cavitron phacoemulsifier. Ophthalmology. 1979;86(11):1994–8. https://doi.org/10.1016/S0161-6420(79)35319-2.

    CAS  Article  PubMed  Google Scholar 

  72. 72.

    Hucknall A, Rangarajan S, Chilkoti A. In pursuit of zero: polymer brushes that resist the adsorption of proteins. Adv Mater. 2009;21(23):2441–6. https://doi.org/10.1002/adma.200900383.

    CAS  Article  Google Scholar 

  73. 73.

    Xu X, Tang JM, Han YM, Wang W, Chen H, Lin QK. Surface PEGylation of intraocular lens for PCO prevention: an in vivo evaluation. J Biomater Appl. 2016;31(1):68–76. https://doi.org/10.1177/0885328216638547.

    CAS  Article  PubMed  Google Scholar 

  74. 74.

    Kochounian HH, Kovacs SA, Sy J, Grubbs DE, Maxwell WA. Identification of intraocular lens-adsorbed proteins in mammalian in vitro and in vivo systems. Arch Ophthalmol. 1994;112(3):395–401. https://doi.org/10.1001/archopht.1994.01090150125034.

    CAS  Article  PubMed  Google Scholar 

  75. 75.

    Han Y, et al. Drug eluting intraocular lens surface modification for PCO prevention. Colloid Interface Sci Commun. 2018;24:40–4. https://doi.org/10.1016/j.colcom.2018.03.007.

    CAS  Article  Google Scholar 

  76. 76.

    Qin Y, Zhu Y, Luo F, Chen C, Chen X, Wu M. Killing two birds with one stone: dual blockade of integrin and FGF signaling through targeting syndecan-4 in postoperative capsular opacification. Cell Death Dis. 2017;8(7):e2920. https://doi.org/10.1038/cddis.2017.315.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Chen HC, Lee CY, Sun CC, Huang JY, Lin HY, Yang SF. Risk factors for the occurrence of visual-threatening posterior capsule opacification. J Transl Med. 2019;17(1):209. https://doi.org/10.1186/s12967-019-1956-6.

    Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Pérez-Vives C. Biomaterial influence on intraocular lens performance: an overview. J Ophthalmol. 2018. https://www.hindawi.com/journals/joph/2018/2687385/. Accessed 15 Feb 2020.

  79. 79.

    Liu Y-C, Wong T, Mehta J. Intraocular lens as a drug delivery reservoir. Curr Opin Ophthalmol. 2013;24(1):53–9. https://doi.org/10.1097/ICU.0b013e32835a93fc.

    Article  PubMed  Google Scholar 

  80. 80.

    Kao ECY, McCanna DJ, Jones LW. Utilization of in vitro methods to determine the biocompatibility of intraocular lens materials. Toxicol In Vitro. 2011;25(8):1906–11. https://doi.org/10.1016/j.tiv.2011.06.005.

    CAS  Article  PubMed  Google Scholar 

  81. 81.

    Auffarth GU, Golescu A, Becker KA, Völcker HE. Quantification of posterior capsule opacification with round and sharp edge intraocular lenses. Ophthalmology. 2003;110(4):772–80. https://doi.org/10.1016/S0161-6420(02)01980-2.

    Article  PubMed  Google Scholar 

  82. 82.

    Findl O, Buehl W, Menapace R, Sacu S, Georgopoulos M, Rainer G. Long-term effect of sharp optic edges of a polymethyl methacrylate intraocular lens on posterior capsule opacification: a randomized trial. Ophthalmology. 2005;112(11):2004–8. https://doi.org/10.1016/j.ophtha.2005.06.021.

    Article  PubMed  Google Scholar 

  83. 83.

    Werner L, Legeais JM, Nagel MD, Renard G. Neutral red assay of the cytotoxicity of fluorocarbon-coated polymethylmethacrylate intraocular lenses in vitro. J Biomed Mater Res. 1999;48(6):814–9.

    CAS  Article  Google Scholar 

  84. 84.

    Li DJ, Cui FZ, Gu HQ. F+ ion implantation induced cell attachment on intraocular lens. Biomaterials. 1999;20(20):1889–96. https://doi.org/10.1016/S0142-9612(99)00084-8.

    CAS  Article  PubMed  Google Scholar 

  85. 85.

    Wang J, Jiang A, Joshi M, Christoforidis J. Drug delivery implants in the treatment of vitreous inflammation. Mediators Inflamm. 2013. https://www.hindawi.com/journals/mi/2013/780634/. Accessed 01 Mar 2019.

  86. 86.

    Haldar RS, Chauhan R, Kapoor K, Niyogi UK. Development of a hydrophobic polymer composition with improved biocompatibility for making foldable intraocular lenses. Opt Mater. 2014;36(7):1165–76. https://doi.org/10.1016/j.optmat.2014.02.022.

    CAS  Article  Google Scholar 

  87. 87.

    Tan X, et al. Improvement of uveal and capsular biocompatibility of hydrophobic acrylic intraocular lens by surface grafting with 2-methacryloyloxyethyl phosphorylcholine-methacrylic acid copolymer. Sci Rep. 2017;7:40462. https://doi.org/10.1038/srep40462.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Molokhia SA, et al. The capsule drug device: novel approach for drug delivery to the eye. Vision Res. 2010;50(7):680–5. https://doi.org/10.1016/j.visres.2009.10.013.

    CAS  Article  PubMed  Google Scholar 

  89. 89.

    Pan T, Brown JD, Ziaie B. “An Artificial Nano-Drainage Implant (ANDI) for Glaucoma Treatment,” in 2006 International Conference of the IEEE Engineering in Medicine and Biology Society. Aug. 2006. pp. 3174–3177. https://doi.org/10.1109/IEMBS.2006.260147.

  90. 90.

    Natarajan JV, Ang M, Darwitan A, Chattopadhyay S, Wong TT, Venkatraman SS. Nanomedicine for glaucoma: liposomes provide sustained release of latanoprost in the eye. Int J Nanomedicine. 2012;7:123–31. https://doi.org/10.2147/IJN.S25468.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Editor Senior CK, “Managing & preventing tube shunt problems.” https://www.reviewofophthalmology.com/article/managing-preventing-tube-shunt-problems. Accessed 2018 Jul 2018.

  92. 92.

    Li T, et al. Comparative effectiveness of first-line medications for primary open angle glaucoma – a systematic review and network meta-analysis. Ophthalmology. 2016;123(1):129–40. https://doi.org/10.1016/j.ophtha.2015.09.005.

    Article  PubMed  Google Scholar 

  93. 93.

    “Trabeculectomy - EyeWiki.” https://eyewiki.aao.org/Trabeculectomy. Accessed 26 Mar 2019.

  94. 94.

    Ko F, Papadopoulos M, Khaw PT. “Chapter 9 - Primary congenital glaucoma,” in Progress in Brain Research, vol. 221. Bagetta G, Nucci C, Eds. Elsevier. 2015. pp. 177–89.

  95. 95.

    Mercieca K, Drury B, Bhargava A, Fenerty C. Trabeculectomy bleb needling and antimetabolite administration practices in the UK: a glaucoma specialist national survey. Br J Ophthalmol. 2018;102(9):1244–7. https://doi.org/10.1136/bjophthalmol-2017-310812.

    Article  PubMed  Google Scholar 

  96. 96.

    Amoozgar B, et al. A novel flexible microfluidic meshwork to reduce fibrosis in glaucoma surgery. PLoS ONE. 2017;12(3):e0172556. https://doi.org/10.1371/journal.pone.0172556.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  97. 97.

    “Enzyme Injection to Reopen Blocked Ocular Drainage Devices in Glaucoma Patients - 15872 - University of Florida Office of Technology Licensing.” https://www.technologylicensing.research.ufl.edu/technologies/15872_enzyme-injection-to-reopen-blocked-ocular-drainage-devices-in-glaucoma-patients. Accessed 04 Mar 2019.

  98. 98.

    Ayyala RS, et al. A clinical study of the Ahmed glaucoma valve implant in advanced glaucoma. Ophthalmology. 1998;105(10):1968–76. https://doi.org/10.1016/S0161-6420(98)91049-1.

    CAS  Article  PubMed  Google Scholar 

  99. 99.

    Acosta AC et al. “Ocular biocompatibility of QuatromerTM (polystyrene–polyisobutylene triblock polymers) for glaucoma implants.” Invest Ophthalmol Vis Sci. 2004;45(13):2929 Available: https://iovs.arvojournals.org/article.aspx?articleid=2408470. Accessed 16 Jul 2018.

  100. 100.

    Choritz L, Koynov K, Renieri G, Barton K, Pfeiffer N, Thieme H. Surface topographies of glaucoma drainage devices and their influence on human tenon fibroblast adhesion. Invest Ophthalmol Vis Sci. 2010;51(8):4047–53. https://doi.org/10.1167/iovs.09-4759.

    Article  PubMed  Google Scholar 

  101. 101.

    Patel S, Pasquale LR. Glaucoma drainage devices: a review of the past, present, and future. Semin Ophthalmol. 2010;25(5–6):265–70. https://doi.org/10.3109/08820538.2010.518840.

    Article  PubMed  Google Scholar 

  102. 102.

    “Investigational MIGS device could minimize fibrotic response,” American Academy of Ophthalmology. Oct. 19, 2017. https://www.aao.org/headline/investigational-migs-device-could-minimize-fibroti. Accessed 04 Mar 2019.

  103. 103.

    Chaudhary A, Salinas L, Guidotti J, Mermoud A, Mansouri K. XEN Gel Implant: a new surgical approach in glaucoma. Expert Rev Med Devices. 2018;15(1):47–59. https://doi.org/10.1080/17434440.2018.1419060.

    CAS  Article  PubMed  Google Scholar 

  104. 104.

    Buffault J, Baudouin C, Labbé A. XEN® Gel Stent for management of chronic open angle glaucoma: a review of the literature. J Fr Ophtalmol. 2019;42(2):e37–46. https://doi.org/10.1016/j.jfo.2018.12.002.

    CAS  Article  PubMed  Google Scholar 

  105. 105.

    Lewis RA. Ab interno approach to the subconjunctival space using a collagen glaucoma stent. J Cataract Refract Surg. 2014;40(8):1301–6. https://doi.org/10.1016/j.jcrs.2014.01.032.

    Article  PubMed  Google Scholar 

  106. 106.

    Chang PY, Kresch Z, Samson CM, Gentile RC. Spontaneous dissociation of fluocinolone acetonide sustained release implant (Retisert) with dislocation into the anterior chamber. Ocul Immunol Inflamm. 2015;23(6):454–7. https://doi.org/10.3109/09273948.2014.902074.

    CAS  Article  PubMed  Google Scholar 

  107. 107.

    Humayun M, et al. Implantable micropump for drug delivery in patients with diabetic macular edema. Transl Vis Sci Technol. 2014;3(6):5. https://doi.org/10.1167/tvst.3.6.5.

    Article  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Lloyd AW. Ophthalmology: biomaterials. In: Buschow KHJ, Cahn RW, Flemings MC, Ilschner B, Kramer EJ, Mahajan S, Veyssière P, editors. Encyclopedia of materials: science and technology. Oxford: Elsevier; 2001. p. 6411–5.

    Google Scholar 

  109. 109.

    Williams RL, Levis HJ, Lace R, Doherty KG, Kennedy SM, Kearns VR. Biomaterials in ophthalmology. In: Narayan R, editor. Encyclopedia of biomedical engineering. Oxford: Elsevier; 2019. p. 289–300.

    Google Scholar 

  110. 110.

    Thompson JT, Chambers WA. Good ideas gone bad: the MIRAgel saga. Ophthalmology. 2016;123(1):5–6. https://doi.org/10.1016/j.ophtha.2015.09.038.

    Article  PubMed  Google Scholar 

  111. 111.

    Song J, Woo I, Eom Y, Kim H. Five misconceptions related to punctal plugs in dry eye management. Cornea. 2018;37 https://doi.org/10.1097/ICO.0000000000001734.

  112. 112.

    “Punctal Plugs for Dry Eyes,” All About Vision. https://www.allaboutvision.com/conditions/punctal-plugs.htm. Accessed 27 Mar 2019.

  113. 113.

    Kim BM, Osmanovic SS, Edward DP. Pyogenic granulomas after silicone punctal plugs: a clinical and histopathologic study. Am J Ophthalmol. 2005;139(4):678–84. https://doi.org/10.1016/j.ajo.2004.11.059.

    Article  PubMed  Google Scholar 

  114. 114.

    March 31 and 2008, “QLT begins phase 2 trial of punctal plug drug delivery system for treating glaucoma, ocular hypertension.” https://www.healio.com/ophthalmology/glaucoma/news/online/%7ba3de4c13-da9a-4508-948e-7333145a0f8e%7d/qlt-begins-phase-2-trial-of-punctal-plug-drug-delivery-system-for-treating-glaucoma-ocular-hypertension. Accessed 27 Mar 2019.

  115. 115.

    “Ocular Therapeutix Announces DEXTENZA® (dexamethasone ophthalmic insert) Recommended for Unique J-Code by CMS,” BioSpace. https://www.biospace.com/article/ocular-therapeutix-announces-dextenza-dexamethasone-ophthalmic-insert-recommended-for-unique-j-code-by-cms/. Accessed 27 Apr 2020.

  116. 116.

    Palchesko RN, Carrasquilla SD, Feinberg AW. Natural biomaterials for corneal tissue engineering, repair, and regeneration. Adv Healthc Mater. 2018;e1701434. https://doi.org/10.1002/adhm.201701434.

  117. 117.

    Akpek EK, Alkharashi M, Hwang FS, Ng SM, Lindsley K. Artificial corneas versus donor corneas for repeat corneal transplants. Cochrane Database Syst Rev.  2014;11:CD009561. https://doi.org/10.1002/14651858.CD009561.pub2.

  118. 118.

    Baino F, Potestio I. Orbital implants: state-of-the-art review with emphasis on biomaterials and recent advances. Mater Sci Eng C. 2016;69:1410–28. https://doi.org/10.1016/j.msec.2016.08.003.

    CAS  Article  Google Scholar 

  119. 119.

    Pillay V, Choonara YE, Kumar P. Frontiers in biomaterials: unfolding the biopolymer landscape. Bentham Science Publishers. 2016.

  120. 120.

    Vermette P. Biomedical applications of polyurethanes. Landes Bioscience. 2001.

  121. 121.

    Tsay RY, Imae T. “Development of nonfouling biomaterials,” in Encyclopedia of Biocolloid and Biointerface Science 2V Set. Wiley, Ltd. 2016. pp. 145–160.

  122. 122.

    Feng W, Zhu S, Ishihara K, Brash JL. Adsorption of fibrinogen and lysozyme on silicon grafted with poly(2-methacryloyloxyethyl phosphorylcholine) via surface-initiated atom transfer radical polymerization. Langmuir ACS J Surf Colloids. 2005;21(13):5980–7. https://doi.org/10.1021/la050277i.

    CAS  Article  Google Scholar 

  123. 123.

    Senaratne W, Andruzzi L, Ober CK. Self-assembled monolayers and polymer brushes in biotechnology: current applications and future perspectives. Biomacromol. 2005;6(5):2427–48. https://doi.org/10.1021/bm050180a.

    CAS  Article  Google Scholar 

  124. 124.

    Kujawa P, Schmauch G, Viitala T, Badia A, Winnik FM. Construction of viscoelastic biocompatible films via the layer-by-layer assembly of hyaluronan and phosphorylcholine-modified chitosan. Biomacromol. 2007;8(10):3169–76. https://doi.org/10.1021/bm7006339.

    CAS  Article  Google Scholar 

  125. 125.

    Gong M, et al. Investigation on the interpenetrating polymer networks (ipns) of polyvinyl alcohol and poly(N-vinyl pyrrolidone) hydrogel and its in vitro bioassessment. J Appl Polym Sci. 2012;125(4):2799–806. https://doi.org/10.1002/app.36247.

    CAS  Article  Google Scholar 

  126. 126.

    Ngo BKD, Grunlan MA. Protein resistant polymeric biomaterials. ACS Macro Lett. 2017;6(9):992–1000. https://doi.org/10.1021/acsmacrolett.7b00448.

    CAS  Article  Google Scholar 

  127. 127.

    Roach P, Farrar D, Perry CC. Surface tailoring for controlled protein adsorption: effect of topography at the nanometer scale and chemistry. J Am Chem Soc. 2006;128(12):3939–45. https://doi.org/10.1021/ja056278e.

    CAS  Article  PubMed  Google Scholar 

  128. 128.

    Ruiz A, Rathnam KR, Masters KS. Effect of hyaluronic acid incorporation method on the stability and biological properties of polyurethane–hyaluronic acid biomaterials. J Mater Sci Mater Med. 2014;25(2):487–98. https://doi.org/10.1007/s10856-013-5092-1.

    CAS  Article  PubMed  Google Scholar 

  129. 129.

    Vishwakarma A, et al. Engineering immunomodulatory biomaterials to tune the inflammatory response. Trends Biotechnol. 2016;34(6):470–82. https://doi.org/10.1016/j.tibtech.2016.03.009.

    CAS  Article  PubMed  Google Scholar 

  130. 130.

    Homme RP et al. Remodeling of retinal architecture in diabetic retinopathy: disruption of ocular physiology and visual functions by inflammatory gene products and pyroptosis. Front Physiol. 2018;9. https://doi.org/10.3389/fphys.2018.01268.

  131. 131.

    Sivak JM, Fini ME. MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog Retin Eye Res. 2002;21(1):1–14. https://doi.org/10.1016/s1350-9462(01)00015-5.

    CAS  Article  PubMed  Google Scholar 

  132. 132.

    Zaleska-Żmijewska A, Strzemecka E, Wawrzyniak ZM, Szaflik JP. Extracellular MMP-9-based assessment of ocular surface inflammation in patients with primary open-angle glaucoma. J Ophthalmol 2019. https://www.hindawi.com/journals/joph/2019/1240537/. Accessed 06 May 2020.

  133. 133.

    Singh M, Tyagi SC. Metalloproteinases as mediators of inflammation and the eyes: molecular genetic underpinnings governing ocular pathophysiology. Int J Ophthalmol. 2017;10(8):1308–18. https://doi.org/10.18240/ijo.2017.08.20.

    Article  PubMed  PubMed Central  Google Scholar 

  134. 134.

    Weinreb RN, Robinson MR, Dibas M, Stamer WD. Matrix metalloproteinases and glaucoma treatment. J Ocul Pharmacol Ther. 2020. https://doi.org/10.1089/jop.2019.0146.

    Article  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Purcell BP et al. Injectable and bioresponsive hydrogels for on-demand matrix metalloproteinase inhibition. Nat Mater. 2014;13(6) https://doi.org/10.1038/nmat3922.

  136. 136.

    Zhang L, et al. Zwitterionic hydrogels implanted in mice resist the foreign-body reaction. Nat Biotechnol. 2013;31(6):553–6. https://doi.org/10.1038/nbt.2580.

    CAS  Article  PubMed  Google Scholar 

  137. 137.

    Jansen LE, et al. Zwitterionic PEG-PC hydrogels modulate the foreign body response in a modulus-dependent manner. Biomacromol. 2018;19(7):2880–8. https://doi.org/10.1021/acs.biomac.8b00444.

    CAS  Article  Google Scholar 

  138. 138.

    Carr LR, Xue H, Jiang S. Functionalizable and nonfouling zwitterionic carboxybetaine hydrogels with a carboxybetaine dimethacrylate crosslinker. Biomaterials. 2011;32(4):961–8. https://doi.org/10.1016/j.biomaterials.2010.09.067.

    CAS  Article  PubMed  Google Scholar 

  139. 139.

    Chou YN, Wen TC, Chang Y. Zwitterionic surface grafting of epoxylated sulfobetaine copolymers for the development of stealth biomaterial interfaces. Acta Biomater. 2016;40:78–91. https://doi.org/10.1016/j.actbio.2016.03.046.

    CAS  Article  PubMed  Google Scholar 

  140. 140.

    Sharma S, Gupta D, Mohanty S, Jassal M, Agrawal AK, Tandon R. Surface-modified electrospun poly (ε-caprolactone) scaffold with improved optical transparency and bioactivity for damaged ocular surface reconstruction. Invest Ophthalmol Vis Sci. 2014;55(2):899–907. https://doi.org/10.1167/iovs.13-12727.

    CAS  Article  PubMed  Google Scholar 

  141. 141.

    Wang JJ, Liu F. Photoinduced graft polymerization of 2-methacryloyloxyethyl phosphorylcholine on silicone hydrogels for reducing protein adsorption. J Mater Sci Mater Med. 2011;22(12):2651–7. https://doi.org/10.1007/s10856-011-4452-y.

    CAS  Article  PubMed  Google Scholar 

  142. 142.

    Lin Q, Tang J, Han Y, Xu X, Hao X, Chen H. Hydrophilic modification of intraocular lens via surface initiated reversible addition-fragmentation chain transfer polymerization for reduced posterior capsular opacification. Colloids Surf B Biointerfaces. 2017;151:271–9. https://doi.org/10.1016/j.colsurfb.2016.12.028.

    CAS  Article  PubMed  Google Scholar 

  143. 143.

    Matsushima H, Iwamoto H, Mukai K, Obara Y. Active oxygen processing for acrylic intraocular lenses to prevent posterior capsule opacification. J Cataract Refract Surg. 2006;32(6):1035–40. https://doi.org/10.1016/j.jcrs.2006.02.042.

    Article  PubMed  Google Scholar 

  144. 144.

    Amoozgar B, Morarescu D, Sheardown H. Sulfadiazine modified PDMS as a model material with the potential for the mitigation of posterior capsule opacification (PCO). Colloids Surf B Biointerfaces. 2013;111:15–23. https://doi.org/10.1016/j.colsurfb.2013.05.002.

    CAS  Article  PubMed  Google Scholar 

  145. 145.

    Silva D, Pinto LF, Bozukova D, Santos LF, Serro AP, Saramago B. Chitosan/alginate based multilayers to control drug release from ophthalmic lens. Colloids Surf B Biointerfaces. 2016;147:81–9. https://doi.org/10.1016/j.colsurfb.2016.07.047.

    CAS  Article  PubMed  Google Scholar 

  146. 146.

    Ashtiani MK, Zandi M, Shokrollahi P, Ehsani M, Baharvand H. Surface modification of poly (2-hydroxyethyl methacrylate) hydrogel for contact lens application. Polym Adv Technol. 2018;29(4):1227–33. https://doi.org/10.1002/pat.4233.

    CAS  Article  Google Scholar 

  147. 147.

    Askari F, Zandi M, Shokrolahi P, Tabatabaei MH, Hajirasoliha E. Reduction in protein absorption on ophthalmic lenses by PEGDA bulk modification of silicone acrylate-based formulation. Prog Biomater. 2019;8(3):169–83. https://doi.org/10.1007/s40204-019-00119-x.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  148. 148.

    Shimizu T, Goda T, Minoura N, Takai M, Ishihara K. Super-hydrophilic silicone hydrogels with interpenetrating poly(2-methacryloyloxyethyl phosphorylcholine) networks. Biomaterials. 2010;31(12):3274–80. https://doi.org/10.1016/j.biomaterials.2010.01.026.

    CAS  Article  PubMed  Google Scholar 

  149. 149.

    Goda T, Matsuno R, Konno T, Takai M, Ishihara K. Protein adsorption resistance and oxygen permeability of chemically crosslinked phospholipid polymer hydrogel for ophthalmologic biomaterials. J Biomed Mater Res B Appl Biomater. 2009;89(1):184–90. https://doi.org/10.1002/jbm.b.31204.

    CAS  Article  PubMed  Google Scholar 

  150. 150.

    Zhang W, Li G, Lin Y, Wang L, Wu S. Preparation and characterization of protein-resistant hydrogels for soft contact lens applications via radical copolymerization involving a zwitterionic sulfobetaine comonomer. J Biomater Sci Polym Ed. 2017;28(16):1935–49. https://doi.org/10.1080/09205063.2017.1363127.

    CAS  Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Research Foundation (NRF) of South Africa, South African Medical Research Council (SAMRC), and the University of the Witwatersrand, Johannesburg.

Author information

Affiliations

Authors

Contributions

O.J.U., P.K., V.P., and Y.E.C. planned the review; O.J.U. conducted the literature search and wrote the first draft; P.K., V.P., and Y.E.C. reviewed and revised the manuscript; all authors provided input to the reviewer comments and approved the final version.

Corresponding author

Correspondence to Yahya E. Choonara.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Uwaezuoke, O.J., Kumar, P., Pillay, V. et al. Fouling in ocular devices: implications for drug delivery, bioactive surface immobilization, and biomaterial design. Drug Deliv. and Transl. Res. (2021). https://doi.org/10.1007/s13346-020-00879-1

Download citation

Keywords

  • Biomaterials
  • Ocular
  • Fouling
  • Protein adsorption
  • Implantable device
  • Drug delivery
  • Immune responsive