Anti-biofouling strategies for implantable biosensors of continuous glucose monitoring systems

Abstract

Continuous glucose monitoring (CGM) systems play an increasingly vital role in the glycemic control of patients with diabetes mellitus. However, the immune responses triggered by the implantation of poorly biocompatible sensors have a significant impact on the accuracy and lifetime of CGM systems. In this review, research efforts over the past few years to mitigate the immune responses by enhancing the anti-biofouling ability of sensors are summarized. This review divided these works into active immune engaging strategy and passive immune escape strategy based on their respective mechanisms. In each strategy, the various biocompatible layers on the biosensor surface, such as drug-releasing membranes, hydrogels, hydrophilic membranes, anti-biofouling membranes based on zwitterionic polymers, and bio-mimicking membranes, are described in detail. This review, therefore, provides researchers working on implantable biosensors for CGM systems with vital information, which is likely to aid in the research and development of novel CGM systems with profound anti-biofouling properties.

Graphical abstract

Keywords

implantable glucose biosensor / anti-biofouling / continuous glucose monitoring / immune responses

References

[1] Ogurtsova K, da Rocha Fernandes J D, Huang Y, Linnenkamp U, Guariguata L, Cho N H, Cavan D, Shaw J E, Makaroff L E. IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Research and Clinical Practice, 2017, 128: 40–50

[2] Zimmet P, Alberti K, Shaw J. Global and societal implications of the diabetes epidemic. Nature, 2001, 414(6865): 782–787

[3] Johnston L, Wang G, Hu K, Qian C, Liu G. Advances in biosensors for continuous glucose monitoring towards wearables. Frontiers in Bioengineering and Biotechnology, 2021, 9: 733810

[4] Timofte D, Mandita A, Balcangiu-Stroescu A E, Balan D, Raducu L, Tanasescu M D, Diaconescu A, Dragos D, Cosconel C I, Stoicescu S M, Ionescu D. Hyperuricemia and cardiovascular diseases clinical and paraclinical correlations. Revista de Chimie, 2019, 70(3): 1045–1046

[5] Fox C S, Golden S H, Anderson C, Bray G A, Burke L E, de Boer I H, Deedwania P, Eckel R H, Ershow A G, Fradkin J. . Update on prevention of cardiovascular disease in adults with type 2 diabetes mellitus in light of recent evidence: a scientific statement from the american heart association and the american diabetes association. Diabetes Care, 2015, 38(9): 1777–1803

[6] Stroescu A E B, Tanasescu M D, Diaconescu A, Raducu L, Balan D G, Mihai A, Tanase M, Stanescu I I, Ionescu D. Diabetic nephropathy: a concise assessment of the causes, risk factors and implications in diabetic patients. Revista de Chimie, 2018, 69(11): 4018–4021

[7] Wanner C, Inzucchi S E, Zinman B. Empagliflozin and progression of kidney disease in type 2 diabetes reply. New England Journal of Medicine, 2016, 375(18): 1801–1802

[8] Cui Y, Zhang L, Zhang M, Yang X, Zhang L, Kuang J, Zhang G, Liu Q, Guo H, Meng Q. Prevalence and causes of low vision and blindness in a Chinese population with type 2 diabetes: the Dongguan eye study. Scientific Reports, 2017, 7(1): 11195

[9] Mandita A, Timofte D, Balcangiu-Stroescu A E, Balan D, Raducu L, Tanasescu M D, Diaconescu A, Dragos D, Cosconel C I, Stoicescu S M, Ionescu D. Treatment of high blood pressure in patients with chronic renal disease. Revista de Chimie, 2019, 70(3): 993–995

[10] Mihai D A, Stefan D S, Stegaru D, Bernea G E, Vacaroiu I A, Papacocea T, Lupusoru M O D, Nica A E, Stiru O, Dragos D, Olaru O. Continuous glucose monitoring devices: a brief presentation. Experimental and Therapeutic Medicine, 2021, 23(2): 174

[11] Nathan D M, Grp D E R. The diabetes control and complications trial/epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care, 2014, 37(1): 9–16

[12] Didyuk O, Econom N, Guardia A, Livingston K, Klueh U. Continuous glucose monitoring devices: past, present, and future focus on the history and evolution of technological innovation. Journal of Diabetes Science and Technology, 2021, 15(3): 676–683

[13] Bergenstal R M, Layne J E, Zisser H, Gabbay R A, Barleen N A, Lee A A, Majithia A R, Parkin C G, Dixon R F. Remote application and use of real-time continuous glucose monitoring by adults with type 2 diabetes in a virtual diabetes clinic. Diabetes Technology & Therapeutics, 2021, 23(2): 128–132

[14] Mauras N, Fox L, Englert K, Beck R W. Continuous glucose monitoring in type 1 diabetes. Endocrine, 2013, 43(1): 41–50

[15] Cappon G, Vettoretti M, Sparacino G, Facchinetti A. Continuous glucose monitoring sensors for diabetes management: a review of technologies and applications. Diabetes & Metabolism Journal, 2019, 43(4): 383–397

[16] Pepper G M. Hemoglobin A1c values and CGM response. Diabetes Technology & Therapeutics, 2012, 14(10): 972

[17] Poolsup N, Suksomboon N, Kyaw A M. Systematic review and meta-analysis of the effectiveness of continuous glucose monitoring (CGM) on glucose control in diabetes. Diabetology & Metabolic Syndrome, 2013, 5(1): 39

[18] Fonda S J, Graham C, Munakata J, Powers J M, Price D, Vigersky R A. The cost-effectiveness of real-time continuous glucose monitoring (RT-CGM) in type 2 diabetes. Journal of Diabetes Science and Technology, 2016, 10(4): 898–904

[19] Vigersky R A, Fonda S J, Chellappa M, Walker M S, Ehrhardt N M. Short- and long-term effects of real-time continuous glucose monitoring in patients with type 2 diabetes. Diabetes Care, 2012, 35(1): 32–38

[20] Clarke S E, Foster J R. A history of blood glucose meters and their role in self-monitoring of diabetes mellitus. British Journal of Biomedical Science, 2012, 69(2): 83–93

[21] Taylor P J, Thompson C H, Brinkworth G D. Effectiveness and acceptability of continuous glucose monitoring for type 2 diabetes management: a narrative review. Journal of Diabetes Investigation, 2018, 9(4): 713–725

[22] Edelman S V. Regulation catches up to reality. Journal of Diabetes Science and Technology, 2017, 11(1): 160–164

[23] Zou Y, Chu Z, Guo J, Liu S, Ma X, Guo J. Minimally invasive electrochemical continuous glucose monitoring sensors: recent progress and perspective. Biosensors & Bioelectronics, 2023, 225: 115103

[24] Moser O, Münzker J, Korsatko S, Pachler C, Smolle K, Toller W, Augustin T, Plank J, Pieber T R, Mader J K. . A prolonged run-in period of standard subcutaneous microdialysis ameliorates quality of interstitial glucose signal in patients after major cardiac surgery. Scientific Reports, 2018, 8(1): 1262

[25] Brennan T V, Lunsford K E, Kuo P C. Innate pathways of immune activation in transplantation. Journal of Transplantation, 2010, 2010: 826240

[26] Sheikh Z, Brooks P J, Barzilay O, Fine N, Glogauer M. Macrophages, foreign body giant cells and their response to implantable biomaterials. Materials (Basel), 2015, 8(9): 5671–5701

[27] Toda S, Fattah A, Asawa K, Nakamura N, Ekdahl K N, Nilsson B, Teramura Y. Optimization of islet microencapsulation with thin polymer membranes for long-term stability. Micromachines, 2019, 10(11): 755

[28] Heo Y J, Takeuchi S. Towards smart tattoos: implantable biosensors for continuous glucose monitoring. Advanced Healthcare Materials, 2013, 2(1): 43–56

[29] Bobrowski T, Schuhmann W. Long-term implantable glucose biosensors. Current Opinion in Electrochemistry, 2018, 10: 112–119

[30] Elsherif M, Hassan M U, Yetisen A K, Butt H. Glucose sensing with phenylboronic acid functionalized hydrogel-based optical diffusers. ACS Nano, 2018, 12(3): 2283–2291

[31] Yuan J H, Wang K, Xia X H. Highly ordered platinum-nanotubule arrays for amperometric glucose sensing. Advanced Functional Materials, 2005, 15(5): 803–809

[32] Ahmad R, Tripathy N, Ahn M S, Bhat K S, Mahmoudi T, Wang Y, Yoo J Y, Kwon D W, Yang H Y, Hahn Y B. Highly efficient non-enzymatic glucose sensor based on cuo modified vertically-grown ZnO nanorods on electrode. Scientific Reports, 2017, 7(1): 5715

[33] Kharbikar B N, Chendke G S, Desai T A. Modulating the foreign body response of implants for diabetes treatment. Advanced Drug Delivery Reviews, 2021, 174: 87–113

[34] McKiel L A, Woodhouse K A, Fitzpatrick L E. The role of toll-like receptor signaling in the macrophage response to implanted materials. MRS Communications, 2020, 10(1): 55–68

[35] Novak M T, Reichert W M. Modeling the physiological factors affecting glucose sensor function in vivo. Journal of Diabetes Science and Technology, 2015, 9(5): 993–998

[36] Vadgama P. Monitoring with in vivo electrochemical sensors: navigating the complexities of blood and tissue reactivity. Sensors (Basel), 2020, 20(11): 3149

[37] Klueh U, Frailey J T, Qiao Y, Antar O, Kreutzer D L. Cell based metabolic barriers to glucose diffusion: macrophages and continuous glucose monitoring. Biomaterials, 2014, 35(10): 3145–3153

[38] Li C, Guo C, Fitzpatrick V, Ibrahim A, Zwierstra M J, Hanna P, Lechtig A, Nazarian A, Lin S J, Kaplan D L. Design of biodegradable, implantable devices towards clinical translation. Nature Reviews. Materials, 2019, 5(1): 61–81

[39] Gray M, Meehan J, Ward C, Langdon S P, Kunkler I H, Murray A, Argyle D. Implantable biosensors and their contribution to the future of precision medicine. Veterinary Journal (London, England), 2018, 239: 21–29

[40] Jansen K A, Atherton P, Ballestrem C. Mechanotransduction at the cell-matrix interface. Seminars in Cell & Developmental Biology, 2017, 71: 75–83

[41] Janson I A, Putnam A J. Extracellular matrix elasticity and topography: material-based cues that affect cell function via conserved mechanisms. Journal of Biomedical Materials Research. Part A, 2015, 103(3): 1246–1258

[42] Gu B, Papadimitrakopoulos F, Burgess D J. PLGA microsphere/PVA hydrogel coatings suppress the foreign body reaction for 6 months. Journal of Controlled Release, 2018, 289: 35–43

[43] Malone-Povolny M J, Bradshaw T M, Merricks E P, Long C T, Nichols T C, Schoenfisch M H. Combination of nitric oxide release and surface texture for mitigating the foreign body response. ACS Biomaterials Science & Engineering, 2021, 7(6): 2444–2452

[44] Márquez A, Jimenez-Jorquera C, Dominguez C, Munoz-Berbel X. Electrodepositable alginate membranes for enzymatic sensors: an amperometric glucose biosensor for whole blood analysis. Biosensors & Bioelectronics, 2017, 97: 136–142

[45] Walker N L, Dick J E. Oxidase-loaded hydrogels for versatile potentiometric metabolite sensing. Biosensors & Bioelectronics, 2021, 178: 112997

[46] Liang Z, Zhang J, Wu C, Hu X, Lu Y, Wang G, Yu F, Zhang X, Wang Y. Flexible and self-healing electrochemical hydrogel sensor with high efficiency toward glucose monitoring. Biosensors & Bioelectronics, 2020, 155: 112105

[47] Williams T J J, Jeevarathinam A S S, Jivan F, Baldock V, Kim P, McShane M J J, Alge D L L. Glucose biosensors based on Michael addition crosslinked poly(ethylene glycol) hydrogels with chemo-optical sensing microdomains. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2023, 11(8): 1749–1759

[48] Zhou J, Ma Z, Hong X, Wu H M, Ma S Y, Li Y, Chen D J, Yu H Y, Huang X J. Top-down strategy of implantable biosensor using adaptable, porous hollow fibrous membrane. ACS Sensors, 2019, 4(4): 931–937

[49] Jin X, Li G, Xu T, Su L, Yan D, Zhang X. Fully integrated flexible biosensor for wearable continuous glucose monitoring. Biosensors & Bioelectronics, 2022, 196: 113760

[50] Sun C, Miao J, Yan J, Yang K, Mao C, Ju J, Shen J. Applications of antibiofouling PEG-coating in electrochemical biosensors for determination of glucose in whole blood. Electrochimica Acta, 2013, 89: 549–554

[51] Feng R, Chu Y, Wang X, Wu Q, Tang F. A long-term stable and flexible glucose sensor coated with poly(ethylene glycol)-modified polyurethane. Journal of Electroanalytical Chemistry (Lausanne, Switzerland), 2021, 895: 115518

[52] Hu Y, Liang B, Fang L, Ma G, Yang G, Zhu Q, Chen S, Ye X. Antifouling zwitterionic coating via electrochemically mediated atom transfer radical polymerization on enzyme-based glucose sensors for long-time stability in 37 degrees serum. Langmuir, 2016, 32(45): 11763–11770

[53] Xie X, Doloff J C, Yesilyurt V, Sadraei A, McGarrigle J J, Omami M, Veiseh O, Farah S, Isa D, Ghani S, Joshi I, Vegas A, Li J, Wang W, Bader A, Tam H H, Tao J, Chen H, Yang B, Williamson K A, Oberholzer J, Langer R, Anderson D G. Reduction of measurement noise in a continuous glucose monitor by coating the sensor with a zwitterionic polymer. Nature Biomedical Engineering, 2018, 2(12): 894–906

[54] Burugapalli K, Wijesuriya S, Wang N, Song W. Biomimetic electrospun coatings increase the in vivo sensitivity of implantable glucose biosensors. Journal of Biomedical Materials Research. Part A, 2018, 106(4): 1072–1081

[55] Ravichandran R, Martinez J G, Jager E W H, Phopase J, Turner A P F. Type I collagen-derived injectable conductive hydrogel scaffolds as glucose sensors. ACS Applied Materials & Interfaces, 2018, 10(19): 16244–16249

[56] Partlow B P, Hanna C W, Rnjak-Kovacina J, Moreau J E, Applegate M B, Burke K A, Marelli B, Mitropoulos A N, Omenetto F G, Kaplan D L. Highly tunable elastomeric silk biomaterials. Advanced Functional Materials, 2014, 24(29): 4615–4624

[57] Ekdahl K N, Lambris J D, Elwing H, Ricklin D, Nilsson P H, Teramura Y, Nicholls I A, Nilsson B. Innate immunity activation on biomaterial surfaces: a mechanistic model and coping strategies. Advanced Drug Delivery Reviews, 2011, 63(12): 1042–1050

[58] Papacocea T, Popa E, Dana T, Papacocea R. The usefulness of dexamethasone in the treatment of chronic subdural hematomas. Farmacia, 2019, 67(1): 140–145

[59] Welch N G, Winkler D A, Thissen H. Antifibrotic strategies for medical devices. Advanced Drug Delivery Reviews, 2020, 167: 109–120

[60] Bridges A W, Garcia A J. Anti-inflammatory polymeric coatings for implantable biomaterials and devices. Journal of Diabetes Science and Technology, 2008, 2(6): 984–994

[61] Go D P, Palmer J A, Gras S L, O’Connor A J. Coating and release of an anti-inflammatory hormone from PLGA microspheres for tissue engineering. Journal of Biomedical Materials Research. Part A, 2012, 100A(2): 507–517

[62] Jayant R D, McShane M J, Srivastava R. In vitro and in vivo evaluation of anti-inflammatory agents using nanoengineered alginate carriers: towards localized implant inflammation suppression. International Journal of Pharmaceutics, 2011, 403(1–2): 268–275

[63] Li D, Guo G, Fan R, Liang J, Deng X, Luo F, Qian Z. PLA/F68/dexamethasone implants prepared by hot-melt extrusion for controlled release of anti-inflammatory drug to implantable medical devices: preparation, characterization and hydrolytic degradation study. International Journal of Pharmaceutics, 2013, 441(1–2): 365–372

[64] Srivastava R, Jayant R D, Chaudhary A, McShane M J. “Smart tattoo” glucose biosensors and effect of coencapsulated anti-inflammatory agents. Journal of Diabetes Science and Technology, 2011, 5(1): 76–85

[65] Wang Y, Papadimitrakopoulos F, Burgess D. J. Polymeric “smart” coatings to prevent foreign body response to implantable biosensors. Journal of Controlled Release, 2013, 169(3): 341–347

[66] Tipnis N, Kastellorizios M, Legassey A, Papadimitrakopoulos F, Jain F, Burgess D J. Sterilization of drug-loaded composite coatings for implantable glucose biosensors. Journal of Diabetes Science and Technology, 2021, 15(3): 646–654

[67] Xu J, Lee H. Anti-biofouling strategies for long-term continuous use of implantable biosensors. Chemosensors (Basel, Switzerland), 2020, 8(3): 66

[68] Kastellorizios M, Papadimitrakopoulos F, Burgess D J. Multiple tissue response modifiers to promote angiogenesis and prevent the foreign body reaction around subcutaneous implants. Journal of Controlled Release, 2015, 214: 103–111

[69] Price C F, Burgess D J, Kastellorizios M. L-DOPA as a small molecule surrogate to promote angiogenesis and prevent dexamethasone-induced ischemia. Journal of Controlled Release, 2016, 235: 176–181

[70] Vallejo-Heligon S G, Klitzman B, Reichert W M. Characterization of porous, dexamethasone-releasing polyurethane coatings for glucose sensors. Acta Biomaterialia, 2014, 10(11): 4629–4638

[71] Jiang K, Weaver J D, Li Y, Chen X, Liang J, Stabler C L. Local release of dexamethasone from macroporous scaffolds accelerates islet transplant engraftment by promotion of anti-inflammatory M2 macrophages. Biomaterials, 2017, 114: 71–81

[72] Paul D, Achouri S, Yoon Y Z, Herre J, Bryant C E, Cicuta P. Phagocytosis dynamics depends on target shape. Biophysical Journal, 2013, 105(5): 1143–1150

[73] Soto R J, Privett B J, Schoenfisch M H. In vivo analytical performance of nitric oxide-releasing glucose biosensors. Analytical Chemistry, 2014, 86(14): 7141–7149

[74] Cha K H, Wang X, Meyerhoff M E. Nitric oxide release for improving performance of implantable chemical sensors—a review. Applied Materials Today, 2017, 9: 589–597

[75] Chang R, Faleo G, Russ H A, Parent A V, Elledge S K, Bernards D A, Allen J L, Villanueva K, Hebrok M, Tang Q, Desai T A. Nanoporous immunoprotective device for stem-cell-derived beta-cell replacement therapy. ACS Nano, 2017, 11(8): 7747–7757

[76] Frost M C, Reynolds M M, Meyerhoff M E. Polymers incorporating nitric oxide releasing/generating substances for improved biocompatibility of blood-contactincy medical devices. Biomaterials, 2005, 26(14): 1685–1693

[77] Arora D P, Hossain S, Xu Y, Boon E M. Nitric oxide regulation of bacterial biofilms. Biochemistry, 2015, 54(24): 3717–3728

[78] Chou Y N, Chang Y, Wen T C. Applying thermosettable zwitterionic copolymers as general fouling-resistant and thermal-tolerant biomaterial interfaces. ACS Applied Materials & Interfaces, 2015, 7(19): 10096–10107

[79] Mariani E, Lisignoli G, Borzi R M, Pulsatelli L. Biomaterials: foreign bodies or tuners for the immune response?. International Journal of Molecular Sciences, 2019, 20(3): 636

[80] Walters N J, Gentleman E. Evolving insights in cell-matrix interactions: elucidating how non-soluble properties of the extracellular niche direct stem cell fate. Acta Biomaterialia, 2015, 11: 3–16

[81] Helton K L, Ratner B D, Wisniewski N A. Biomechanics of the sensor-tissue interface-effects of motion, pressure, and design on sensor performance and the foreign body response-part I: theoretical framework. Journal of Diabetes Science and Technology, 2011, 5(3): 632–646

[82] Ernst A U, Wang L H, Ma M. Islet encapsulation. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2018, 6(42): 6705–6722

[83] Mørch Y A, Donati I, Strand B L, Skjak-Braek G. Effect of Ca²⁺, Ba²⁺, and Sr²⁺ on alginate microbeads. Biomacromolecules, 2006, 7(5): 1471–1480

[84] Higgins D M, Basaraba R J, Hohnbaum A C, Lee E J, Grainger D W, Gonzalez-Juarrero M. Localized immunosuppressive environment in the foreign body response to implanted biomaterials. American Journal of Pathology, 2009, 175(1): 161–170

[85] Dellacherie M O, Seo B R, Mooney D J. Macroscale biomaterials strategies for local immunomodulation. Nature Reviews. Materials, 2019, 4(6): 379–397

[86] 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: 342304

[87] de Candia P, Prattichizzo F, Garavelli S, De Rosa V, Galgani M, Di Rella F, Spagnuolo M I, Colamatteo A, Fusco C, Micillo T, Bruzzaniti S, Ceriello A, Puca A A, Matarese G. Type 2 diabetes: how much of an autoimmune disease?. Frontiers in Endocrinology (Lausanne), 2019, 10: 451

[88] Chen W, Yung B C, Qian Z, Chen X. Improving long-term subcutaneous drug delivery by regulating material-bioenvironment interaction. Advanced Drug Delivery Reviews, 2018, 127: 20–34

[89] Nascimento R A S, Mulato M. Microelectronic sensor for continuous glucose monitoring. Applied Physics. A, Materials Science & Processing, 2019, 125(3): 175

[90] Lee H, Hong Y J, Baik S, Hyeon T, Kim D H. Enzyme-based glucose sensor: from invasive to wearable device. Advanced Healthcare Materials, 2018, 7(8): 1701150

[91] Marchioli G, van Gurp L, van Krieken P P, Stamatialis D, Engelse M, van Blitterswijk C A, Karperien M B J, de Koning E, Alblas J, Moroni L, van Apeldoorn A A. Fabrication of three-dimensional bioplotted hydrogel scaffolds for islets of Langerhans transplantation. Biofabrication, 2015, 7(2): 025009

[92] Lee Y, Matsushima N, Yada S, Nita S, Kodama T, Amberg G, Shiomi J. Revealing how topography of surface microstructures alters capillary spreading. Scientific Reports, 2019, 9(1): 7787

[93] Hanson T L, Diaz-Botia C A, Kharazia V, Maharbiz M M, Sabes P N. The “sewing machine” for minimally invasive neural recording. BioRxiv, 2019, 578542

[94] Stabler C L, Li Y, Stewart J M, Keselowsky B C. Engineering immunomodulatory biomaterials for type 1 diabetes. Nature Reviews. Materials, 2019, 4(6): 429–450

[95] Hwang P T J, Shah D K, Garcia J A, Bae C Y, Lim D J, Huiszoon R C, Alexander G C, Jun H W. Progress and challenges of the bioartificial pancreas. Nano Convergence, 2016, 3(1): 28

[96] Guseman A J, Speer S L, Perez Goncalves G M, Pielak G J. Surface charge modulates protein-protein interactions in physiologically relevant environments. Biochemistry, 2018, 57(11): 1681–1684

[97] Shin E J, Choi S M. Advances in waterborne polyurethane-based biomaterials for biomedical applications. Advances in Experimental Medicine and Biology, 2018, 1077: 251–283

[98] Cai Y, Liang B, Chen S, Zhu Q, Tu T, Wu K, Cao Q, Fang L, Liang X, Ye X. One-step modification of nano-polyaniline/glucose oxidase on double-side printed flexible electrode for continuous glucose monitoring: characterization, cytotoxicity evaluation and in vivo experiment. Biosensors & Bioelectronics, 2020, 165: 112408

[99] Campuzano S, Pedrero M, Yanez-Sedeno P, Pingarron J M. Antifouling (bio)materials for electrochemical (bio)sensing. International Journal of Molecular Sciences, 2019, 20(2): 423

[100] Francolini I, Vuotto C, Piozzi A, Donelli G. Antifouling and antimicrobial biomaterials: an overview. Acta Pathologica et Microbiologica Scandinavica. Supplement, 2017, 125(4): 392–417

[101] Liu M, Xu Y, Zhao Y, Wang Z, Shi D. Hydroxyl radical-involved cancer therapy via Fenton reactions. Frontiers of Chemical Science and Engineering, 2022, 16(3): 345–363

[102] Mu X, Xu Y, Wang Z, Shi D. Probes and nano-delivery systems targeting NAD(P)H: quinone oxidoreductase 1: a mini-review. Frontiers of Chemical Science and Engineering, 2023, 17(2): 123–138

[103] Wu J, Lin W, Wang Z, Chen S, Chang Y. Investigation of the hydration of nonfouling material poly(sulfobetaine methacrylate) by low-field nuclear magnetic resonance. Langmuir, 2012, 28(19): 7436–7441

[104] Jiang S, Cao Z. Ultralow-fouling, functionalizable, and hydrolyzable zwitterionic materials and their derivatives for biological applications. Advanced Materials, 2010, 22(9): 920–932

[105] Cheng G, Li G, Xue H, Chen S, Bryers J D, Jiang S. Zwitterionic carboxybetaine polymer surfaces and their resistance to long-term biofilm formation. Biomaterials, 2009, 30(28): 5234–5240

[106] Zhang Z, Chen S, Chang Y, Jiang S. Surface grafted sulfobetaine polymers via atom transfer radical polymerization as superlow fouling coatings. Journal of Physical Chemistry B, 2006, 110(22): 10799–10804

[107] Feng W, Brash J L, Zhu S P. Non-biofouling materials prepared by atom transfer radical polymerization grafting of 2-methacryloloxyethyl phosphorylcholine: separate effects of graft density and chain length on protein repulsion. Biomaterials, 2006, 27(6): 847–855

[108] Lowe A B, McCormick C L. Synthesis and solution properties of zwitterionic polymers. Chemical Reviews, 2002, 102(11): 4177–4190

[109] Chen S, Li L, Zhao C, Zheng J. Surface hydration: principles and applications toward low-fouling/nonfouling biomaterials. Polymer, 2010, 51(23): 5283–5293

[110] Xuan F, Liu J. Preparation, characterization and application of zwitterionic polymers and membranes: current developments and perspective. Polymer International, 2009, 58(12): 1350–1361

[111] Chen S F, Zheng J, Li L Y, Jiang S Y. Strong resistance of phosphorylcholine self-assembled monolayers to protein adsorption: insights into nonfouling properties of zwitterionic materials. Journal of the American Chemical Society, 2005, 127(41): 14473–14478

[112] He M, Gao K, Zhou L, Jiao Z, Wu M, Cao J, You X, Cai Z, Su Y, Jiang Z. Zwitterionic materials for antifouling membrane surface construction. Acta Biomaterialia, 2016, 40: 142–152

[113] Jayakumar R, Prabaharan M, Sudheesh Kumar P T, Nair S V, Tamura H. Biomaterials based on chitin and chitosan in wound dressing applications. Biotechnology Advances, 2011, 29(3): 322–337

[114] Jayakumar R, Prabaharan M, Nair S V, Tamura H. Novel chitin and chitosan nanofibers in biomedical applications. Biotechnology Advances, 2010, 28(1): 142–150

[115] Robotti F, Bottan S, Fraschetti F, Mallone A, Pellegrini G, Lindenblatt N, Starck C, Falk V, Poulikakos D, Ferrari A. A micron-scale surface topography design reducing cell adhesion to implanted materials. Scientific Reports, 2018, 8(1): 10887

[116] Franz S, Rammelt S, Scharnweber D, Simon J C. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials, 2011, 32(28): 6692–6709

[117] Lewis J S, Roy K, Keselowsky B G. Materials that harness and modulate the immune system. MRS Bulletin, 2014, 39(1): 25–34

[118] Damodaran V B, Murthy N S. Bio-inspired strategies for designing antifouling biomaterials. Biomaterials Research, 2016, 20(1): 18

[119] Espinoza-Jiménez A, Peon A N, Terrazas L I. Alternatively activated macrophages in types 1 and 2 diabetes. Mediators of Inflammation, 2012, 2012: 815593

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