Anti-biofouling strategies for implantable biosensors of continuous glucose monitoring systems
Yan Zheng1, Dunyun Shi2, Zheng Wang1()
1. School of Pharmaceutical Science & Technology, Tianjin University, Tianjin 300072, China 2. Institute of Hematology, Shenzhen Second People’s Hospital/the First Affiliated Hospital of Shenzhen University, Shenzhen 518035, China
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.
Premature biodegradation and low mechanical strength
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Fig.7
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1
K Ogurtsova, J D da Rocha Fernandes, Y Huang, U Linnenkamp, L Guariguata, N H Cho, D Cavan, J E Shaw, L E Makaroff. IDF diabetes atlas: global estimates for the prevalence of diabetes for 2015 and 2040. Diabetes Research and Clinical Practice, 2017, 128: 40–50 https://doi.org/10.1016/j.diabres.2017.03.024
2
P Zimmet, K Alberti, J Shaw. Global and societal implications of the diabetes epidemic. Nature, 2001, 414(6865): 782–787 https://doi.org/10.1038/414782a
3
L Johnston, G Wang, K Hu, C Qian, G Liu. Advances in biosensors for continuous glucose monitoring towards wearables. Frontiers in Bioengineering and Biotechnology, 2021, 9: 733810 https://doi.org/10.3389/fbioe.2021.733810
4
D Timofte, A Mandita, A E Balcangiu-Stroescu, D Balan, L Raducu, M D Tanasescu, A Diaconescu, D Dragos, C I Cosconel, S M Stoicescu, D Ionescu. Hyperuricemia and cardiovascular diseases clinical and paraclinical correlations. Revista de Chimie, 2019, 70(3): 1045–1046 https://doi.org/10.37358/RC.19.3.7060
5
C S Fox, S H Golden, C Anderson, G A Bray, L E Burke, I H de Boer, P Deedwania, R H Eckel, A G Ershow, J Fradkin. et al.. 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 https://doi.org/10.2337/dci15-0012
6
A E B Stroescu, M D Tanasescu, A Diaconescu, L Raducu, D G Balan, A Mihai, M Tanase, I I Stanescu, D Ionescu. Diabetic nephropathy: a concise assessment of the causes, risk factors and implications in diabetic patients. Revista de Chimie, 2018, 69(11): 4018–4021
7
C Wanner, S E Inzucchi, B Zinman. Empagliflozin and progression of kidney disease in type 2 diabetes reply. New England Journal of Medicine, 2016, 375(18): 1801–1802
8
Y Cui, L Zhang, M Zhang, X Yang, L Zhang, J Kuang, G Zhang, Q Liu, H Guo, Q Meng. 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 https://doi.org/10.1038/s41598-017-11365-z
9
A Mandita, D Timofte, A E Balcangiu-Stroescu, D Balan, L Raducu, M D Tanasescu, A Diaconescu, D Dragos, C I Cosconel, S M Stoicescu, D Ionescu. Treatment of high blood pressure in patients with chronic renal disease. Revista de Chimie, 2019, 70(3): 993–995 https://doi.org/10.37358/RC.19.3.7047
10
D A Mihai, D S Stefan, D Stegaru, G E Bernea, I A Vacaroiu, T Papacocea, M O D Lupusoru, A E Nica, O Stiru, D Dragos, O Olaru. Continuous glucose monitoring devices: a brief presentation. Experimental and Therapeutic Medicine, 2021, 23(2): 174 https://doi.org/10.3892/etm.2021.11097
11
D M Nathan, D E R Grp. The diabetes control and complications trial/epidemiology of diabetes interventions and complications study at 30 years: overview. Diabetes Care, 2014, 37(1): 9–16 https://doi.org/10.2337/dc13-2112
12
O Didyuk, N Econom, A Guardia, K Livingston, U Klueh. 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 https://doi.org/10.1177/1932296819899394
13
R M Bergenstal, J E Layne, H Zisser, R A Gabbay, N A Barleen, A A Lee, A R Majithia, C G Parkin, R F Dixon. 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 https://doi.org/10.1089/dia.2020.0396
G Cappon, M Vettoretti, G Sparacino, A Facchinetti. Continuous glucose monitoring sensors for diabetes management: a review of technologies and applications. Diabetes & Metabolism Journal, 2019, 43(4): 383–397 https://doi.org/10.4093/dmj.2019.0121
16
G M Pepper. Hemoglobin A1c values and CGM response. Diabetes Technology & Therapeutics, 2012, 14(10): 972
17
N Poolsup, N Suksomboon, A M Kyaw. 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 https://doi.org/10.1186/1758-5996-5-39
18
S J Fonda, C Graham, J Munakata, J M Powers, D Price, R A Vigersky. 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 https://doi.org/10.1177/1932296816628547
19
R A Vigersky, S J Fonda, M Chellappa, M S Walker, N M Ehrhardt. Short- and long-term effects of real-time continuous glucose monitoring in patients with type 2 diabetes. Diabetes Care, 2012, 35(1): 32–38 https://doi.org/10.2337/dc11-1438
20
S E Clarke, J R Foster. 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 https://doi.org/10.1080/09674845.2012.12002443
21
P J Taylor, C H Thompson, G D Brinkworth. Effectiveness and acceptability of continuous glucose monitoring for type 2 diabetes management: a narrative review. Journal of Diabetes Investigation, 2018, 9(4): 713–725 https://doi.org/10.1111/jdi.12807
Y Zou, Z Chu, J Guo, S Liu, X Ma, J Guo. Minimally invasive electrochemical continuous glucose monitoring sensors: recent progress and perspective. Biosensors & Bioelectronics, 2023, 225: 115103 https://doi.org/10.1016/j.bios.2023.115103
24
O Moser, J Münzker, S Korsatko, C Pachler, K Smolle, W Toller, T Augustin, J Plank, T R Pieber, J K Mader. et al.. 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 https://doi.org/10.1038/s41598-018-19768-2
25
T V Brennan, K E Lunsford, P C Kuo. Innate pathways of immune activation in transplantation. Journal of Transplantation, 2010, 2010: 826240 https://doi.org/10.1155/2010/826240
26
Z Sheikh, P J Brooks, O Barzilay, N Fine, M Glogauer. Macrophages, foreign body giant cells and their response to implantable biomaterials. Materials (Basel), 2015, 8(9): 5671–5701 https://doi.org/10.3390/ma8095269
27
S Toda, A Fattah, K Asawa, N Nakamura, K N Ekdahl, B Nilsson, Y Teramura. Optimization of islet microencapsulation with thin polymer membranes for long-term stability. Micromachines, 2019, 10(11): 755 https://doi.org/10.3390/mi10110755
28
Y J Heo, S Takeuchi. Towards smart tattoos: implantable biosensors for continuous glucose monitoring. Advanced Healthcare Materials, 2013, 2(1): 43–56 https://doi.org/10.1002/adhm.201200167
M Elsherif, M U Hassan, A K Yetisen, H Butt. Glucose sensing with phenylboronic acid functionalized hydrogel-based optical diffusers. ACS Nano, 2018, 12(3): 2283–2291 https://doi.org/10.1021/acsnano.7b07082
31
J H Yuan, K Wang, X H Xia. Highly ordered platinum-nanotubule arrays for amperometric glucose sensing. Advanced Functional Materials, 2005, 15(5): 803–809 https://doi.org/10.1002/adfm.200400321
32
R Ahmad, N Tripathy, M S Ahn, K S Bhat, T Mahmoudi, Y Wang, J Y Yoo, D W Kwon, H Y Yang, Y B Hahn. Highly efficient non-enzymatic glucose sensor based on cuo modified vertically-grown ZnO nanorods on electrode. Scientific Reports, 2017, 7(1): 5715 https://doi.org/10.1038/s41598-017-06064-8
33
B N Kharbikar, G S Chendke, T A Desai. Modulating the foreign body response of implants for diabetes treatment. Advanced Drug Delivery Reviews, 2021, 174: 87–113 https://doi.org/10.1016/j.addr.2021.01.011
34
L A McKiel, K A Woodhouse, L E Fitzpatrick. The role of toll-like receptor signaling in the macrophage response to implanted materials. MRS Communications, 2020, 10(1): 55–68 https://doi.org/10.1557/mrc.2019.154
35
M T Novak, W M Reichert. Modeling the physiological factors affecting glucose sensor function in vivo. Journal of Diabetes Science and Technology, 2015, 9(5): 993–998 https://doi.org/10.1177/1932296815593094
36
P Vadgama. Monitoring with in vivo electrochemical sensors: navigating the complexities of blood and tissue reactivity. Sensors (Basel), 2020, 20(11): 3149 https://doi.org/10.3390/s20113149
37
U Klueh, J T Frailey, Y Qiao, O Antar, D L Kreutzer. Cell based metabolic barriers to glucose diffusion: macrophages and continuous glucose monitoring. Biomaterials, 2014, 35(10): 3145–3153 https://doi.org/10.1016/j.biomaterials.2014.01.001
38
C Li, C Guo, V Fitzpatrick, A Ibrahim, M J Zwierstra, P Hanna, A Lechtig, A Nazarian, S J Lin, D L Kaplan. Design of biodegradable, implantable devices towards clinical translation. Nature Reviews. Materials, 2019, 5(1): 61–81 https://doi.org/10.1038/s41578-019-0150-z
39
M Gray, J Meehan, C Ward, S P Langdon, I H Kunkler, A Murray, D Argyle. Implantable biosensors and their contribution to the future of precision medicine. Veterinary Journal (London, England), 2018, 239: 21–29 https://doi.org/10.1016/j.tvjl.2018.07.011
40
K A Jansen, P Atherton, C Ballestrem. Mechanotransduction at the cell-matrix interface. Seminars in Cell & Developmental Biology, 2017, 71: 75–83 https://doi.org/10.1016/j.semcdb.2017.07.027
41
I A Janson, A J Putnam. 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 https://doi.org/10.1002/jbm.a.35254
42
B Gu, F Papadimitrakopoulos, D J Burgess. PLGA microsphere/PVA hydrogel coatings suppress the foreign body reaction for 6 months. Journal of Controlled Release, 2018, 289: 35–43 https://doi.org/10.1016/j.jconrel.2018.09.021
43
M J Malone-Povolny, T M Bradshaw, E P Merricks, C T Long, T C Nichols, M H Schoenfisch. Combination of nitric oxide release and surface texture for mitigating the foreign body response. ACS Biomaterials Science & Engineering, 2021, 7(6): 2444–2452 https://doi.org/10.1021/acsbiomaterials.1c00022
44
A Márquez, C Jimenez-Jorquera, C Dominguez, X Munoz-Berbel. Electrodepositable alginate membranes for enzymatic sensors: an amperometric glucose biosensor for whole blood analysis. Biosensors & Bioelectronics, 2017, 97: 136–142 https://doi.org/10.1016/j.bios.2017.05.051
45
N L Walker, J E Dick. Oxidase-loaded hydrogels for versatile potentiometric metabolite sensing. Biosensors & Bioelectronics, 2021, 178: 112997 https://doi.org/10.1016/j.bios.2021.112997
46
Z Liang, J Zhang, C Wu, X Hu, Y Lu, G Wang, F Yu, X Zhang, Y Wang. Flexible and self-healing electrochemical hydrogel sensor with high efficiency toward glucose monitoring. Biosensors & Bioelectronics, 2020, 155: 112105 https://doi.org/10.1016/j.bios.2020.112105
47
T J J Williams, A S S Jeevarathinam, F Jivan, V Baldock, P Kim, M J J McShane, D L L Alge. 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 https://doi.org/10.1039/D2TB02339C
48
J Zhou, Z Ma, X Hong, H M Wu, S Y Ma, Y Li, D J Chen, H Y Yu, X J Huang. Top-down strategy of implantable biosensor using adaptable, porous hollow fibrous membrane. ACS Sensors, 2019, 4(4): 931–937 https://doi.org/10.1021/acssensors.9b00035
49
X Jin, G Li, T Xu, L Su, D Yan, X Zhang. Fully integrated flexible biosensor for wearable continuous glucose monitoring. Biosensors & Bioelectronics, 2022, 196: 113760 https://doi.org/10.1016/j.bios.2021.113760
50
C Sun, J Miao, J Yan, K Yang, C Mao, J Ju, J Shen. Applications of antibiofouling PEG-coating in electrochemical biosensors for determination of glucose in whole blood. Electrochimica Acta, 2013, 89: 549–554 https://doi.org/10.1016/j.electacta.2012.11.005
51
R Feng, Y Chu, X Wang, Q Wu, F Tang. A long-term stable and flexible glucose sensor coated with poly(ethylene glycol)-modified polyurethane. Journal of Electroanalytical Chemistry (Lausanne, Switzerland), 2021, 895: 115518 https://doi.org/10.1016/j.jelechem.2021.115518
52
Y Hu, B Liang, L Fang, G Ma, G Yang, Q Zhu, S Chen, X Ye. 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 https://doi.org/10.1021/acs.langmuir.6b03016
53
X Xie, J C Doloff, V Yesilyurt, A Sadraei, J J McGarrigle, M Omami, O Veiseh, S Farah, D Isa, S Ghani, I Joshi, A Vegas, J Li, W Wang, A Bader, H H Tam, J Tao, H Chen, B Yang, K A Williamson, J Oberholzer, R Langer, D G Anderson. 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 https://doi.org/10.1038/s41551-018-0273-3
54
K Burugapalli, S Wijesuriya, N Wang, W Song. Biomimetic electrospun coatings increase the in vivo sensitivity of implantable glucose biosensors. Journal of Biomedical Materials Research. Part A, 2018, 106(4): 1072–1081 https://doi.org/10.1002/jbm.a.36308
55
R Ravichandran, J G Martinez, E W H Jager, J Phopase, A P F Turner. Type I collagen-derived injectable conductive hydrogel scaffolds as glucose sensors. ACS Applied Materials & Interfaces, 2018, 10(19): 16244–16249 https://doi.org/10.1021/acsami.8b04091
56
B P Partlow, C W Hanna, J Rnjak-Kovacina, J E Moreau, M B Applegate, K A Burke, B Marelli, A N Mitropoulos, F G Omenetto, D L Kaplan. Highly tunable elastomeric silk biomaterials. Advanced Functional Materials, 2014, 24(29): 4615–4624 https://doi.org/10.1002/adfm.201400526
57
K N Ekdahl, J D Lambris, H Elwing, D Ricklin, P H Nilsson, Y Teramura, I A Nicholls, B Nilsson. Innate immunity activation on biomaterial surfaces: a mechanistic model and coping strategies. Advanced Drug Delivery Reviews, 2011, 63(12): 1042–1050 https://doi.org/10.1016/j.addr.2011.06.012
58
T Papacocea, E Popa, T Dana, R Papacocea. The usefulness of dexamethasone in the treatment of chronic subdural hematomas. Farmacia, 2019, 67(1): 140–145 https://doi.org/10.31925/farmacia.2019.1.19
59
N G Welch, D A Winkler, H Thissen. Antifibrotic strategies for medical devices. Advanced Drug Delivery Reviews, 2020, 167: 109–120 https://doi.org/10.1016/j.addr.2020.06.008
60
A W Bridges, A J Garcia. Anti-inflammatory polymeric coatings for implantable biomaterials and devices. Journal of Diabetes Science and Technology, 2008, 2(6): 984–994 https://doi.org/10.1177/193229680800200628
61
D P Go, J A Palmer, S L Gras, A J O’Connor. 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 https://doi.org/10.1002/jbm.a.33299
62
R D Jayant, M J McShane, R Srivastava. 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 https://doi.org/10.1016/j.ijpharm.2010.10.035
63
D Li, G Guo, R Fan, J Liang, X Deng, F Luo, Z Qian. 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 https://doi.org/10.1016/j.ijpharm.2012.11.019
64
R Srivastava, R D Jayant, A Chaudhary, M J McShane. “Smart tattoo” glucose biosensors and effect of coencapsulated anti-inflammatory agents. Journal of Diabetes Science and Technology, 2011, 5(1): 76–85 https://doi.org/10.1177/193229681100500111
65
Y Wang, F Papadimitrakopoulos, D Burgess. J. Polymeric “smart” coatings to prevent foreign body response to implantable biosensors. Journal of Controlled Release, 2013, 169(3): 341–347 https://doi.org/10.1016/j.jconrel.2012.12.028
66
N Tipnis, M Kastellorizios, A Legassey, F Papadimitrakopoulos, F Jain, D J Burgess. Sterilization of drug-loaded composite coatings for implantable glucose biosensors. Journal of Diabetes Science and Technology, 2021, 15(3): 646–654 https://doi.org/10.1177/1932296819890620
67
J Xu, H Lee. Anti-biofouling strategies for long-term continuous use of implantable biosensors. Chemosensors (Basel, Switzerland), 2020, 8(3): 66 https://doi.org/10.3390/chemosensors8030066
68
M Kastellorizios, F Papadimitrakopoulos, D J Burgess. Multiple tissue response modifiers to promote angiogenesis and prevent the foreign body reaction around subcutaneous implants. Journal of Controlled Release, 2015, 214: 103–111 https://doi.org/10.1016/j.jconrel.2015.07.021
69
C F Price, D J Burgess, M Kastellorizios. L-DOPA as a small molecule surrogate to promote angiogenesis and prevent dexamethasone-induced ischemia. Journal of Controlled Release, 2016, 235: 176–181 https://doi.org/10.1016/j.jconrel.2016.05.065
70
S G Vallejo-Heligon, B Klitzman, W M Reichert. Characterization of porous, dexamethasone-releasing polyurethane coatings for glucose sensors. Acta Biomaterialia, 2014, 10(11): 4629–4638 https://doi.org/10.1016/j.actbio.2014.07.019
71
K Jiang, J D Weaver, Y Li, X Chen, J Liang, C L Stabler. Local release of dexamethasone from macroporous scaffolds accelerates islet transplant engraftment by promotion of anti-inflammatory M2 macrophages. Biomaterials, 2017, 114: 71–81 https://doi.org/10.1016/j.biomaterials.2016.11.004
72
D Paul, S Achouri, Y Z Yoon, J Herre, C E Bryant, P Cicuta. Phagocytosis dynamics depends on target shape. Biophysical Journal, 2013, 105(5): 1143–1150 https://doi.org/10.1016/j.bpj.2013.07.036
73
R J Soto, B J Privett, M H Schoenfisch. In vivo analytical performance of nitric oxide-releasing glucose biosensors. Analytical Chemistry, 2014, 86(14): 7141–7149 https://doi.org/10.1021/ac5017425
74
K H Cha, X Wang, M E Meyerhoff. Nitric oxide release for improving performance of implantable chemical sensors—a review. Applied Materials Today, 2017, 9: 589–597 https://doi.org/10.1016/j.apmt.2017.10.002
75
R Chang, G Faleo, H A Russ, A V Parent, S K Elledge, D A Bernards, J L Allen, K Villanueva, M Hebrok, Q Tang, T A Desai. Nanoporous immunoprotective device for stem-cell-derived beta-cell replacement therapy. ACS Nano, 2017, 11(8): 7747–7757 https://doi.org/10.1021/acsnano.7b01239
76
M C Frost, M M Reynolds, M E Meyerhoff. Polymers incorporating nitric oxide releasing/generating substances for improved biocompatibility of blood-contactincy medical devices. Biomaterials, 2005, 26(14): 1685–1693 https://doi.org/10.1016/j.biomaterials.2004.06.006
77
D P Arora, S Hossain, Y Xu, E M Boon. Nitric oxide regulation of bacterial biofilms. Biochemistry, 2015, 54(24): 3717–3728 https://doi.org/10.1021/bi501476n
78
Y N Chou, Y Chang, T C Wen. Applying thermosettable zwitterionic copolymers as general fouling-resistant and thermal-tolerant biomaterial interfaces. ACS Applied Materials & Interfaces, 2015, 7(19): 10096–10107 https://doi.org/10.1021/acsami.5b01756
79
E Mariani, G Lisignoli, R M Borzi, L Pulsatelli. Biomaterials: foreign bodies or tuners for the immune response?. International Journal of Molecular Sciences, 2019, 20(3): 636 https://doi.org/10.3390/ijms20030636
80
N J Walters, E Gentleman. 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 https://doi.org/10.1016/j.actbio.2014.09.038
81
K L Helton, B D Ratner, N A Wisniewski. 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 https://doi.org/10.1177/193229681100500317
82
A U Ernst, L H Wang, M Ma. Islet encapsulation. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2018, 6(42): 6705–6722 https://doi.org/10.1039/C8TB02020E
83
Y A Mørch, I Donati, B L Strand, G Skjak-Braek. Effect of Ca2+, Ba2+, and Sr2+ on alginate microbeads. Biomacromolecules, 2006, 7(5): 1471–1480 https://doi.org/10.1021/bm060010d
84
D M Higgins, R J Basaraba, A C Hohnbaum, E J Lee, D W Grainger, M Gonzalez-Juarrero. Localized immunosuppressive environment in the foreign body response to implanted biomaterials. American Journal of Pathology, 2009, 175(1): 161–170 https://doi.org/10.2353/ajpath.2009.080962
85
M O Dellacherie, B R Seo, D J Mooney. Macroscale biomaterials strategies for local immunomodulation. Nature Reviews. Materials, 2019, 4(6): 379–397 https://doi.org/10.1038/s41578-019-0106-3
86
S N Christo, K R Diener, A Bachhuka, K Vasilev, J D Hayball. Innate immunity and biomaterials at the nexus: friends or foes. BioMed Research International, 2015, 2015: 342304 https://doi.org/10.1155/2015/342304
87
P de Candia, F Prattichizzo, S Garavelli, V De Rosa, M Galgani, F Di Rella, M I Spagnuolo, A Colamatteo, C Fusco, T Micillo, S Bruzzaniti, A Ceriello, A A Puca, G Matarese. Type 2 diabetes: how much of an autoimmune disease?. Frontiers in Endocrinology (Lausanne), 2019, 10: 451 https://doi.org/10.3389/fendo.2019.00451
88
W Chen, B C Yung, Z Qian, X Chen. Improving long-term subcutaneous drug delivery by regulating material-bioenvironment interaction. Advanced Drug Delivery Reviews, 2018, 127: 20–34 https://doi.org/10.1016/j.addr.2018.01.016
89
R A S Nascimento, M Mulato. Microelectronic sensor for continuous glucose monitoring. Applied Physics. A, Materials Science & Processing, 2019, 125(3): 175 https://doi.org/10.1007/s00339-019-2455-6
90
H Lee, Y J Hong, S Baik, T Hyeon, D H Kim. Enzyme-based glucose sensor: from invasive to wearable device. Advanced Healthcare Materials, 2018, 7(8): 1701150 https://doi.org/10.1002/adhm.201701150
91
G Marchioli, L van Gurp, P P van Krieken, D Stamatialis, M Engelse, C A van Blitterswijk, M B J Karperien, E de Koning, J Alblas, L Moroni, A A van Apeldoorn. Fabrication of three-dimensional bioplotted hydrogel scaffolds for islets of Langerhans transplantation. Biofabrication, 2015, 7(2): 025009 https://doi.org/10.1088/1758-5090/7/2/025009
92
Y Lee, N Matsushima, S Yada, S Nita, T Kodama, G Amberg, J Shiomi. Revealing how topography of surface microstructures alters capillary spreading. Scientific Reports, 2019, 9(1): 7787 https://doi.org/10.1038/s41598-019-44243-x
93
T L Hanson, C A Diaz-Botia, V Kharazia, M M Maharbiz, P N Sabes. The “sewing machine” for minimally invasive neural recording. BioRxiv, 2019, 578542 https://doi.org/10.1101/578542
94
C L Stabler, Y Li, J M Stewart, B C Keselowsky. Engineering immunomodulatory biomaterials for type 1 diabetes. Nature Reviews. Materials, 2019, 4(6): 429–450 https://doi.org/10.1038/s41578-019-0112-5
95
P T J Hwang, D K Shah, J A Garcia, C Y Bae, D J Lim, R C Huiszoon, G C Alexander, H W Jun. Progress and challenges of the bioartificial pancreas. Nano Convergence, 2016, 3(1): 28 https://doi.org/10.1186/s40580-016-0088-4
96
A J Guseman, S L Speer, G M Perez Goncalves, G J Pielak. Surface charge modulates protein-protein interactions in physiologically relevant environments. Biochemistry, 2018, 57(11): 1681–1684 https://doi.org/10.1021/acs.biochem.8b00061
97
E J Shin, S M Choi. Advances in waterborne polyurethane-based biomaterials for biomedical applications. Advances in Experimental Medicine and Biology, 2018, 1077: 251–283 https://doi.org/10.1007/978-981-13-0947-2_14
98
Y Cai, B Liang, S Chen, Q Zhu, T Tu, K Wu, Q Cao, L Fang, X Liang, X Ye. 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 https://doi.org/10.1016/j.bios.2020.112408
99
S Campuzano, M Pedrero, P Yanez-Sedeno, J M Pingarron. Antifouling (bio)materials for electrochemical (bio)sensing. International Journal of Molecular Sciences, 2019, 20(2): 423 https://doi.org/10.3390/ijms20020423
100
I Francolini, C Vuotto, A Piozzi, G Donelli. Antifouling and antimicrobial biomaterials: an overview. Acta Pathologica et Microbiologica Scandinavica. Supplement, 2017, 125(4): 392–417 https://doi.org/10.1111/apm.12675
101
M Liu, Y Xu, Y Zhao, Z Wang, D Shi. Hydroxyl radical-involved cancer therapy via Fenton reactions. Frontiers of Chemical Science and Engineering, 2022, 16(3): 345–363 https://doi.org/10.1007/s11705-021-2077-3
102
X Mu, Y Xu, Z Wang, D Shi. 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 https://doi.org/10.1007/s11705-022-2194-7
103
J Wu, W Lin, Z Wang, S Chen, Y Chang. Investigation of the hydration of nonfouling material poly(sulfobetaine methacrylate) by low-field nuclear magnetic resonance. Langmuir, 2012, 28(19): 7436–7441 https://doi.org/10.1021/la300394c
104
S Jiang, Z Cao. Ultralow-fouling, functionalizable, and hydrolyzable zwitterionic materials and their derivatives for biological applications. Advanced Materials, 2010, 22(9): 920–932 https://doi.org/10.1002/adma.200901407
105
G Cheng, G Li, H Xue, S Chen, J D Bryers, S Jiang. Zwitterionic carboxybetaine polymer surfaces and their resistance to long-term biofilm formation. Biomaterials, 2009, 30(28): 5234–5240 https://doi.org/10.1016/j.biomaterials.2009.05.058
106
Z Zhang, S Chen, Y Chang, S Jiang. Surface grafted sulfobetaine polymers via atom transfer radical polymerization as superlow fouling coatings. Journal of Physical Chemistry B, 2006, 110(22): 10799–10804 https://doi.org/10.1021/jp057266i
107
W Feng, J L Brash, S P Zhu. 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 https://doi.org/10.1016/j.biomaterials.2005.07.006
108
A B Lowe, C L McCormick. Synthesis and solution properties of zwitterionic polymers. Chemical Reviews, 2002, 102(11): 4177–4190 https://doi.org/10.1021/cr020371t
109
S Chen, L Li, C Zhao, J Zheng. Surface hydration: principles and applications toward low-fouling/nonfouling biomaterials. Polymer, 2010, 51(23): 5283–5293 https://doi.org/10.1016/j.polymer.2010.08.022
110
F Xuan, J Liu. Preparation, characterization and application of zwitterionic polymers and membranes: current developments and perspective. Polymer International, 2009, 58(12): 1350–1361 https://doi.org/10.1002/pi.2679
111
S F Chen, J Zheng, L Y Li, S Y Jiang. 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 https://doi.org/10.1021/ja054169u
112
M He, K Gao, L Zhou, Z Jiao, M Wu, J Cao, X You, Z Cai, Y Su, Z Jiang. Zwitterionic materials for antifouling membrane surface construction. Acta Biomaterialia, 2016, 40: 142–152 https://doi.org/10.1016/j.actbio.2016.03.038
113
R Jayakumar, M Prabaharan, P T Sudheesh Kumar, S V Nair, H Tamura. Biomaterials based on chitin and chitosan in wound dressing applications. Biotechnology Advances, 2011, 29(3): 322–337 https://doi.org/10.1016/j.biotechadv.2011.01.005
114
R Jayakumar, M Prabaharan, S V Nair, H Tamura. Novel chitin and chitosan nanofibers in biomedical applications. Biotechnology Advances, 2010, 28(1): 142–150 https://doi.org/10.1016/j.biotechadv.2009.11.001
115
F Robotti, S Bottan, F Fraschetti, A Mallone, G Pellegrini, N Lindenblatt, C Starck, V Falk, D Poulikakos, A Ferrari. A micron-scale surface topography design reducing cell adhesion to implanted materials. Scientific Reports, 2018, 8(1): 10887 https://doi.org/10.1038/s41598-018-29167-2
116
S Franz, S Rammelt, D Scharnweber, J C Simon. Immune responses to implants—a review of the implications for the design of immunomodulatory biomaterials. Biomaterials, 2011, 32(28): 6692–6709 https://doi.org/10.1016/j.biomaterials.2011.05.078
117
J S Lewis, K Roy, B G Keselowsky. Materials that harness and modulate the immune system. MRS Bulletin, 2014, 39(1): 25–34 https://doi.org/10.1557/mrs.2013.310
118
V B Damodaran, N S Murthy. Bio-inspired strategies for designing antifouling biomaterials. Biomaterials Research, 2016, 20(1): 18 https://doi.org/10.1186/s40824-016-0064-4
119
A Espinoza-Jiménez, A N Peon, L I Terrazas. Alternatively activated macrophages in types 1 and 2 diabetes. Mediators of Inflammation, 2012, 2012: 815593 https://doi.org/10.1155/2012/815953
