Diamond-Like Carbon Depositing on the Surface of Polylactide Membrane for Prevention of Adhesion Formation During Tendon Repair
Corresponding Author: Shen Liu
Nano-Micro Letters,
Vol. 16 (2024), Article Number: 186
Abstract
Post-traumatic peritendinous adhesion presents a significant challenge in clinical medicine. This study proposes the use of diamond-like carbon (DLC) deposited on polylactic acid (PLA) membranes as a biophysical mechanism for anti-adhesion barrier to encase ruptured tendons in tendon-injured rats. The results indicate that PLA/DLC composite membrane exhibits more efficient anti-adhesion effect than PLA membrane, with histological score decreasing from 3.12 ± 0.27 to 2.20 ± 0.22 and anti-adhesion effectiveness increasing from 21.61% to 44.72%. Mechanistically, the abundant C=O bond functional groups on the surface of DLC can reduce reactive oxygen species level effectively; thus, the phosphorylation of NF-κB and M1 polarization of macrophages are inhibited. Consequently, excessive inflammatory response augmented by M1 macrophage-originated cytokines including interleukin-6 (IL-6), interleukin-1β (IL-1β), and tumor necrosis factor-α (TNF-α) is largely reduced. For biocompatibility evaluation, PLA/DLC membrane is slowly absorbed within tissue and displays prolonged barrier effects compared to traditional PLA membranes. Further studies show the DLC depositing decelerates the release of degradation product lactic acid and its induction of macrophage M2 polarization by interfering esterase and PLA ester bonds, which further delays the fibrosis process. It was found that the PLA/DLC membrane possess an efficient biophysical mechanism for treatment of peritendinous adhesion.
Highlights:
1 The anti-adhesion effect of polylactic acid (PLA) membrane with diamond-like carbon (DLC) depositing is 44.72%, enhanced by 23.11% compared to PLA.
2 DLC deposited on PLA membranes has been shown to effectively reduce the levels of reactive oxygen species, leading to a decrease in the expression of pro-inflammatory cytokines within peritendinous adhesion tissue.
3 DLC decelerates PLA biodegradation and lactic production, which reduces the number of CD68+CD206+ macrophages within peritendinous adhesion tissue.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- M. Lu, S. Wang, H. Wang, T. Xue, C. Cai et al., Pyrrolidine dithiocarbamate-loaded electrospun membranes for peritendinous anti-adhesion through inhibition of the nuclear factor-κB pathway. Acta Biomater. 155, 333–346 (2023). https://doi.org/10.1016/j.actbio.2022.10.004
- X. Rong, Y. Tang, S. Cao, S. Xiao, H. Wang et al., An extracellular vesicle-cloaked multifaceted biocatalyst for ultrasound-augmented tendon matrix reconstruction and immune microenvironment regulation. ACS Nano 17, 16501–16516 (2023). https://doi.org/10.1021/acsnano.3c00911
- B. Kheilnezhad, A. Hadjizadeh, A review: progress in preventing tissue adhesions from a biomaterial perspective. Biomater. Sci. 9, 2850–2873 (2021). https://doi.org/10.1039/d0bm02023k
- Y. Li, C. Hu, B. Hu, J. Tian, G. Zhao et al., Sustained release of dicumarol via novel grafted polymer in electrospun nanofiber membrane for treatment of peritendinous adhesion. Adv. Healthc. Mater. 12, e2203078 (2023). https://doi.org/10.1002/adhm.202203078
- Y. Dogramaci, A. Kalac, E. Atik, E. Esen, M.E. Altuğ et al., Effects of a single application of extractum cepae on the peritendinous adhesion. Ann. Plast. Surg. 64, 338–341 (2010). https://doi.org/10.1097/sap.0b013e3181afa428
- P.S. Wiggenhauser, N. Wachtel, K.C. Koban, R.E. Giunta, A. Frick et al., Prevention of postoperative peritendinous adhesions with bioresorbable suprathel barrier membrane. Plast. Reconstr. Surg. Glob. Open 10, e4370 (2022). https://doi.org/10.1097/gox.0000000000004370
- C.J. Dy, A. Hernandez-Soria, Y. Ma, T.R. Roberts, A. Daluiski, Complications after flexor tendon repair: a systematic review and meta-analysis. J. Hand Surg. 37, 543-551.e1 (2012). https://doi.org/10.1016/j.jhsa.2011.11.006
- M.J. Fatemi, S. Shirani, R. Sobhani, A.H. Lebaschi, M.J. Gharegozlou et al., Prevention of peritendinous adhesion formation after the flexor tendon surgery in rabbits. Ann. Plast. Surg. 80, 171–175 (2018). https://doi.org/10.1097/sap.0000000000001169
- M. Tao, F. Liang, J. He, W. Ye, R. Javed et al., Decellularized tendon matrix membranes prevent post-surgical tendon adhesion and promote functional repair. Acta Biomater. 134, 160–176 (2021). https://doi.org/10.1016/j.actbio.2021.07.038
- H. Capella-Monsonís, M.A. Tilbury, J.G. Wall, D.I. Zeugolis, Porcine mesothelium matrix as a biomaterial for wound healing applications. Mater. Today Bio 7, 100057 (2020). https://doi.org/10.1016/j.mtbio.2020.100057
- S. Wang, M. Lu, Y. Cao, Z. Tao, Z. Sun et al., Degradative polylactide nanofibers promote M2 macrophage polarization via STAT6 pathway in peritendinous adhesion. Compos. Part B Eng. 253, 110520 (2023). https://doi.org/10.1016/j.compositesb.2023.110520
- L. Wang, J. Ma, T. Guo, F. Zhang, A. Dong et al., Control of surface wrinkles on shape memory PLA/PPDO micro-nanofibers and their applications in drug release and anti-scarring. Adv. Fiber Mater. 5, 632–649 (2023). https://doi.org/10.1007/s42765-022-00249-1
- B. Tyler, D. Gullotti, A. Mangraviti, T. Utsuki, H. Brem, Polylactic acid (PLA) controlled delivery carriers for biomedical applications. Adv. Drug Deliv. Rev. 107, 163–175 (2016). https://doi.org/10.1016/j.addr.2016.06.018
- A.J. Vegas, O. Veiseh, J.C. Doloff, M. Ma, H.H. Tam et al., Combinatorial hydrogel library enables identification of materials that mitigate the foreign body response in Primates. Nat. Biotechnol. 34, 345–352 (2016). https://doi.org/10.1038/nbt.3462
- O. Veiseh, J.C. Doloff, M. Ma, A.J. Vegas, H.H. Tam et al., Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human Primates. Nat. Mater. 14, 643–651 (2015). https://doi.org/10.1038/nmat4290
- N.G. Welch, D.A. Winkler, H. Thissen, Antifibrotic strategies for medical devices. Adv. Drug Deliv. Rev. 167, 109–120 (2020). https://doi.org/10.1016/j.addr.2020.06.008
- S. Wang, M. Lu, W. Wang, S. Yu, R. Yu et al., Macrophage polarization modulated by NF-κB in polylactide membranes-treated peritendinous adhesion. Small 18, e2104112 (2022). https://doi.org/10.1002/smll.202104112
- S. Liu, H. Chen, T. Wu, G. Pan, C. Fan et al., Macrophage infiltration of electrospun polyester fibers. Biomater. Sci. 5, 1579–1587 (2017). https://doi.org/10.1039/c6bm00958a
- S. Nishio, S. Takeda, K. Kosuga, M. Okada, E. Kyo et al., Decade of histological follow-up for a fully biodegradable poly-L-lactic acid coronary stent (Igaki-Tamai stent) in humans: are bioresorbable scaffolds the answer? Circulation 129, 534–535 (2014). https://doi.org/10.1161/CIRCULATIONAHA.113.003769
- Z. Hou, W. Yan, T. Li, W. Wu, Y. Cui et al., Lactic acid-mediated endothelial to mesenchymal transition through TGF-β1 contributes to in-stent stenosis in poly-L-lactic acid stent. Int. J. Biol. Macromol. 155, 1589–1598 (2020). https://doi.org/10.1016/j.ijbiomac.2019.11.136
- C.K. Sen, Human wound and its burden: updated 2020 compendium of estimates. Adv. Wound Care 10, 281–292 (2021). https://doi.org/10.1089/wound.2021.0026
- R. Yu, H. Zhang, B. Guo, Conductive biomaterials as bioactive wound dressing for wound healing and skin tissue engineering. Nano-Micro Lett. 14, 1 (2021). https://doi.org/10.1007/s40820-021-00751-y
- Q. Gao, F. Sun, Y. Li, L. Li, M. Liu et al., Biological tissue-inspired ultrasoft, ultrathin, and mechanically enhanced microfiber composite hydrogel for flexible bioelectronics. Nano-Micro Lett. 15, 139 (2023). https://doi.org/10.1007/s40820-023-01096-4
- Y. Xie, S. Xiao, L. Huang, J. Guo, M. Bai et al., Cascade and ultrafast artificial antioxidases alleviate inflammation and bone resorption in periodontitis. ACS Nano 17, 15097–15112 (2023). https://doi.org/10.1021/acsnano.3c04328
- Y. Deng, Y. Gao, T. Li, S. Xiao, M. Adeli et al., Amorphizing metal selenides-based ROS biocatalysts at surface nanolayer toward ultrafast inflammatory diabetic wound healing. ACS Nano 17, 2943–2957 (2023). https://doi.org/10.1021/acsnano.2c11448
- S. Singh, A. Young, C.-E. McNaught, The physiology of wound healing. Surg. Oxf. 35, 473–477 (2017). https://doi.org/10.1016/j.mpsur.2017.06.004
- Z. Wu, Y. Sun, S. Mu, M. Bai, Q. Li et al., Manganese-based antioxidase-inspired biocatalysts with axial Mn-N5 sites and 2D d-π-conjugated networks for rescuing stem cell fate. Angew. Chem. Int. Ed. 62, e202302329 (2023). https://doi.org/10.1002/anie.202302329
- Y. Sun, S. Mu, Z. Xing, J. Guo, Z. Wu et al., Catalase-mimetic artificial biocatalysts with Ru catalytic centers for ROS elimination and stem-cell protection. Adv. Mater. 34, e2206208 (2022). https://doi.org/10.1002/adma.202206208
- S. Cao, Z. Zhao, Y. Zheng, Z. Wu, T. Ma et al., A library of ROS-catalytic metalloenzyme mimics with atomic metal centers. Adv. Mater. 34, e2200255 (2022). https://doi.org/10.1002/adma.202200255
- J. Guo, Z. Xing, L. Liu, Y. Sun, H. Zhou et al., Antioxidase-like nanobiocatalysts with ultrafast and reversible redox-centers to secure stem cells and periodontal tissues. Adv. Funct. Mater. 33(15), 2211778 (2023). https://doi.org/10.1002/adfm.202211778
- J. Lee, H. Liao, Q. Wang, J. Han, J.H. Han et al., Exploration of nanozymes in viral diagnosis and therapy. Exploration (Beijing) 2, 20210086 (2022). https://doi.org/10.1002/EXP.20210086
- P. Gong, L. Ren, X. Gao, J. Long, W. Tian et al., A novel barrier membrane with long-term ROS scavenging function for complete prevention of postoperative adhesion. Mater. Des. 238, 112691 (2024). https://doi.org/10.1016/j.matdes.2024.112691
- J. Zhao, J.-Y. Fu, F. Jia, J. Li, B. Yu et al., Precise regulation of inflammation and oxidative stress by ROS-responsive prodrug coated balloon for preventing vascular restenosis. Adv. Funct. Mater. 33, 2213993 (2023). https://doi.org/10.1002/adfm.202213993
- I.A. Darby, T.D. Hewitson, Hypoxia in tissue repair and fibrosis. Cell Tissue Res. 365, 553–562 (2016). https://doi.org/10.1007/s00441-016-2461-3
- S. Van Linthout, K. Miteva, C. Tschöpe, Crosstalk between fibroblasts and inflammatory cells. Cardiovasc. Res. 102, 258–269 (2014). https://doi.org/10.1093/cvr/cvu062
- P. Li, H. Zhou, T. Tu, H. Lu, Dynamic exacerbation in inflammation and oxidative stress during the formation of peritendinous adhesion resulted from acute tendon injury. J. Orthop. Surg. Res. 16, 293 (2021). https://doi.org/10.1186/s13018-021-02445-y
- R. An, X. Wang, L. Yang, J. Zhang, N. Wang et al., Polystyrene microplastics cause granulosa cells apoptosis and fibrosis in ovary through oxidative stress in rats. Toxicology 449, 152665 (2021). https://doi.org/10.1016/j.tox.2020.152665
- J.C. Jha, C. Banal, B.S.M. Chow, M.E. Cooper, K. Jandeleit-Dahm, Diabetes and kidney disease: role of oxidative stress. Antioxid. Redox Signal. 25, 657–684 (2016). https://doi.org/10.1089/ars.2016.6664
- C. Estornut, J. Milara, M.A. Bayarri, N. Belhadj, J. Cortijo, Targeting oxidative stress as a therapeutic approach for idiopathic pulmonary fibrosis. Front. Pharmacol. 12, 794997 (2022). https://doi.org/10.3389/fphar.2021.794997
- Y. Liang, K. Xu, P. Zhang, J. Zhang, P. Chen et al., Quercetin reduces tendon adhesion in rat through suppression of oxidative stress. BMC Musculoskelet. Disord. 21, 608 (2020). https://doi.org/10.1186/s12891-020-03618-2
- T.-H. Kim, S.-Y. Heo, G.-W. Oh, W.S. Park, I.-W. Choi et al., A phlorotannins-loaded homogeneous acellular matrix film modulates post-implantation inflammatory responses. J. Tissue Eng. Regen. Med. 16, 51–62 (2022). https://doi.org/10.1002/term.3258
- A. Carnicer-Lombarte, S.-T. Chen, G.G. Malliaras, D.G. Barone, Foreign body reaction to implanted biomaterials and its impact in nerve neuroprosthetics. Front. Bioeng. Biotechnol. 9, 622524 (2021). https://doi.org/10.3389/fbioe.2021.622524
- A. Boruah, K. Roy, A. Thakur, S. Haldar, R. Konwar et al., Biocompatible nanodiamonds derived from coal washery rejects: antioxidant, antiviral, and phytotoxic applications. ACS Omega 8, 11151–11160 (2023). https://doi.org/10.1021/acsomega.2c07981
- Y. Zhu, J. Li, W. Li, Y. Zhang, X. Yang et al., The biocompatibility of nanodiamonds and their application in drug delivery systems. Theranostics 2, 302–312 (2012). https://doi.org/10.7150/thno.3627
- N. Gibson, O. Shenderova, T.J.M. Luo, S. Moseenkov, V. Bondar et al., Colloidal stability of modified nanodiamond ps. Diam. Relat. Mater. 18, 620–626 (2009). https://doi.org/10.1016/j.diamond.2008.10.049
- S. Chauhan, N. Jain, U. Nagaich, Nanodiamonds with powerful ability for drug delivery and biomedical applications: recent updates on invivo study and patents. J. Pharm. Anal. 10, 1–12 (2020). https://doi.org/10.1016/j.jpha.2019.09.003
- Q. Lin, R.H.J. Xu Xu, N. Yang, A.A. Karim, X.J. Loh et al., UV protection and antioxidant activity of nanodiamonds and fullerenes for sunscreen formulations. ACS Appl. Nano Mater. 2, 7604–7616 (2019). https://doi.org/10.1021/acsanm.9b01698
- D.G. Lim, K.H. Kim, E. Kang, S.H. Lim, J. Ricci et al., Comprehensive evaluation of carboxylated nanodiamond as a topical drug delivery system. Int. J. Nanomed. 11, 2381–2395 (2016). https://doi.org/10.2147/IJN.S104859
- I.V. Shugalei, A.S. Borovikova, A.P. Voznyakovskii, M.A. Ilyushin, Detonation nanodiamonds as antioxidants in various test systems. J. Superhard Mater. 39, 326–335 (2017). https://doi.org/10.3103/s1063457617050045
- M.-S. Wu, D.-S. Sun, Y.-C. Lin, C.-L. Cheng, S.-C. Hung et al., Nanodiamonds protect skin from ultraviolet B-induced damage in mice. J. Nanobiotechnol. 13, 35 (2015). https://doi.org/10.1186/s12951-015-0094-4
- V. Thomas, B.A. Halloran, N. Ambalavanan, S.A. Catledge, Y.K. Vohra, In vitro studies on the effect of p size on macrophage responses to nanodiamond wear debris. Acta Biomater. 8, 1939–1947 (2012). https://doi.org/10.1016/j.actbio.2012.01.033
- S.H. Alawdi, E.S. El-Denshary, M.M. Safar, H. Eidi, M.-O. David et al., Neuroprotective effect of nanodiamond in Alzheimer’s disease rat model: a pivotal role for modulating NF-κB and STAT3 signaling. Mol. Neurobiol. 54, 1906–1918 (2017). https://doi.org/10.1007/s12035-016-9762-0
- H. Yuan, Y. Zhang, Y. Su, N. Hu, J. Yang et al., A novel BiVO4/DLC heterojunction for efficient photoelectrochemical water splitting. Chem. Eng. J. 459, 141637 (2023). https://doi.org/10.1016/j.cej.2023.141637
- C. Zhang, R. Yan, M. Bai, Y. Sun, X. Han et al., Pt-clusters-equipped antioxidase-like biocatalysts as efficient ROS scavengers for treating periodontitis. Small (2023). https://doi.org/10.1002/smll.202306966
- X. Li, L. Wang, H. Liu, J. Fu, L. Zhen et al., C60 fullerenes suppress reactive oxygen species toxicity damage in boar sperm. Nano-Micro Lett. 11, 104 (2019). https://doi.org/10.1007/s40820-019-0334-5
- Y. Xiao, K. Li, J. Bian, Y. Zhang, J. Li et al., Urolithin A protects neuronal cells against stress damage and apoptosis by Atp2a3 inhibition. Mol. Nutr. Food Res. 67, 2300146 (2023). https://doi.org/10.1002/mnfr.202300146
- T. Kisseleva, D.A. Brenner, Mechanisms of fibrogenesis. Exp. Biol. Med. 233, 109–122 (2008). https://doi.org/10.3181/0707-mr-190
- L.-K. Hung, S.-C. Fu, Y.-W. Lee, T.-Y. Mok, K.-M. Chan, Local vitamin-C injection reduced tendon adhesion in a chicken model of flexor digitorum profundus tendon injury. J. Bone Jt. Surg. 95, e41 (2013). https://doi.org/10.2106/jbjs.k.00988
- T.M. Chen, X.M. Tian, L. Huang, J. Xiao, G.W. Yang, Nanodiamonds as pH-switchable oxidation and reduction catalysts with enzyme-like activities for immunoassay and antioxidant applications. Nanoscale 9, 15673–15684 (2017). https://doi.org/10.1039/c7nr05629j
- Y. Yang, Y. Zhang, L. Wang, Z. Miao, K. Zhou et al., Antibacterial property of oxygen-terminated carbon bonds. Adv. Funct. Mater. 32, 2200447 (2022). https://doi.org/10.1002/adfm.202200447
- D. Zhu, L. Zhang, R.E. Ruther, R.J. Hamers, Photo-illuminated diamond as a solid-state sourceof solvated electrons in water for nitrogenreduction. Nat. Mater. 12, 836–841 (2013). https://doi.org/10.1038/nmat3696
- X. Dai, Q. Xu, Y. Li, L. Yang, Y. Zhang et al., Salen-manganese complex-based nanozyme with enhanced superoxide- and catalase-like activity for wound disinfection and anti-inflammation. Chem. Engin. J. 471, 144694 (2023). https://doi.org/10.1016/j.cej.2023.144694
- V.N. Mochalin, O. Shenderova, D. Ho, Y. Gogotsi, The properties and applications of nanodiamonds. Nat. Nanotechnol. 7, 11–23 (2012). https://doi.org/10.1038/nnano.2011.209
- J. Whitlow, S. Pacelli, A. Paul, Multifunctional nanodiamonds in regenerative medicine: recent advances and future directions. J. Control. Release 261, 62–86 (2017). https://doi.org/10.1016/j.jconrel.2017.05.033
- J.K.F. Wong, Y.H. Lui, Z. Kapacee, K.E. Kadler, M.W.J. Ferguson et al., The cellular biology of flexor tendon adhesion formation. Am. J. Pathol. 175, 1938–1951 (2009). https://doi.org/10.2353/ajpath.2009.090380
- M. Hedl, J. Yan, H. Witt, C. Abraham, IRF5 is required for bacterial clearance in human M1-polarized macrophages, and IRF5 immune-mediated disease risk variants modulate this outcome. J. Immunol. 202, 920–930 (2019). https://doi.org/10.4049/jimmunol.1800226
- Y. Li, X. Wang, B. Hu, Q. Sun, M. Wan et al., Neutralization of excessive levels of active TGF-β1 reduces MSC recruitment and differentiation to mitigate peritendinous adhesion. Bone Res. 11, 24 (2023). https://doi.org/10.1038/s41413-023-00252-1
- J. Braune, U. Weyer, C. Hobusch, J. Mauer, J.C. Brüning et al., IL-6 regulates M2 polarization and local proliferation of adipose tissue macrophages in obesity. J. Immunol. 198, 2927–2934 (2017). https://doi.org/10.4049/jimmunol.1600476
- S. Oishi, R. Takano, S. Tamura, S. Tani, M. Iwaizumi et al., M2 polarization of murine peritoneal macrophages induces regulatory cytokine production and suppresses T-cell proliferation. Immunology 149, 320–328 (2016). https://doi.org/10.1111/imm.12647
- P.A. Revell, The combined role of wear ps, macrophages and lymphocytes in the loosening of total joint prostheses. J. R. Soc. Interface. 5, 1263–1278 (2008). https://doi.org/10.1098/rsif.2008.0142
- Y. Xie, J. Zhou, Q. Wei, Z.M. Yu, H. Luo et al., Improving the long-term stability of Ti6Al4V abutment screw by coating micro/nano-crystalline diamond films. J. Mech. Behav. Biomed. Mater. 63, 174–182 (2016). https://doi.org/10.1016/j.jmbbm.2016.06.018
References
M. Lu, S. Wang, H. Wang, T. Xue, C. Cai et al., Pyrrolidine dithiocarbamate-loaded electrospun membranes for peritendinous anti-adhesion through inhibition of the nuclear factor-κB pathway. Acta Biomater. 155, 333–346 (2023). https://doi.org/10.1016/j.actbio.2022.10.004
X. Rong, Y. Tang, S. Cao, S. Xiao, H. Wang et al., An extracellular vesicle-cloaked multifaceted biocatalyst for ultrasound-augmented tendon matrix reconstruction and immune microenvironment regulation. ACS Nano 17, 16501–16516 (2023). https://doi.org/10.1021/acsnano.3c00911
B. Kheilnezhad, A. Hadjizadeh, A review: progress in preventing tissue adhesions from a biomaterial perspective. Biomater. Sci. 9, 2850–2873 (2021). https://doi.org/10.1039/d0bm02023k
Y. Li, C. Hu, B. Hu, J. Tian, G. Zhao et al., Sustained release of dicumarol via novel grafted polymer in electrospun nanofiber membrane for treatment of peritendinous adhesion. Adv. Healthc. Mater. 12, e2203078 (2023). https://doi.org/10.1002/adhm.202203078
Y. Dogramaci, A. Kalac, E. Atik, E. Esen, M.E. Altuğ et al., Effects of a single application of extractum cepae on the peritendinous adhesion. Ann. Plast. Surg. 64, 338–341 (2010). https://doi.org/10.1097/sap.0b013e3181afa428
P.S. Wiggenhauser, N. Wachtel, K.C. Koban, R.E. Giunta, A. Frick et al., Prevention of postoperative peritendinous adhesions with bioresorbable suprathel barrier membrane. Plast. Reconstr. Surg. Glob. Open 10, e4370 (2022). https://doi.org/10.1097/gox.0000000000004370
C.J. Dy, A. Hernandez-Soria, Y. Ma, T.R. Roberts, A. Daluiski, Complications after flexor tendon repair: a systematic review and meta-analysis. J. Hand Surg. 37, 543-551.e1 (2012). https://doi.org/10.1016/j.jhsa.2011.11.006
M.J. Fatemi, S. Shirani, R. Sobhani, A.H. Lebaschi, M.J. Gharegozlou et al., Prevention of peritendinous adhesion formation after the flexor tendon surgery in rabbits. Ann. Plast. Surg. 80, 171–175 (2018). https://doi.org/10.1097/sap.0000000000001169
M. Tao, F. Liang, J. He, W. Ye, R. Javed et al., Decellularized tendon matrix membranes prevent post-surgical tendon adhesion and promote functional repair. Acta Biomater. 134, 160–176 (2021). https://doi.org/10.1016/j.actbio.2021.07.038
H. Capella-Monsonís, M.A. Tilbury, J.G. Wall, D.I. Zeugolis, Porcine mesothelium matrix as a biomaterial for wound healing applications. Mater. Today Bio 7, 100057 (2020). https://doi.org/10.1016/j.mtbio.2020.100057
S. Wang, M. Lu, Y. Cao, Z. Tao, Z. Sun et al., Degradative polylactide nanofibers promote M2 macrophage polarization via STAT6 pathway in peritendinous adhesion. Compos. Part B Eng. 253, 110520 (2023). https://doi.org/10.1016/j.compositesb.2023.110520
L. Wang, J. Ma, T. Guo, F. Zhang, A. Dong et al., Control of surface wrinkles on shape memory PLA/PPDO micro-nanofibers and their applications in drug release and anti-scarring. Adv. Fiber Mater. 5, 632–649 (2023). https://doi.org/10.1007/s42765-022-00249-1
B. Tyler, D. Gullotti, A. Mangraviti, T. Utsuki, H. Brem, Polylactic acid (PLA) controlled delivery carriers for biomedical applications. Adv. Drug Deliv. Rev. 107, 163–175 (2016). https://doi.org/10.1016/j.addr.2016.06.018
A.J. Vegas, O. Veiseh, J.C. Doloff, M. Ma, H.H. Tam et al., Combinatorial hydrogel library enables identification of materials that mitigate the foreign body response in Primates. Nat. Biotechnol. 34, 345–352 (2016). https://doi.org/10.1038/nbt.3462
O. Veiseh, J.C. Doloff, M. Ma, A.J. Vegas, H.H. Tam et al., Size- and shape-dependent foreign body immune response to materials implanted in rodents and non-human Primates. Nat. Mater. 14, 643–651 (2015). https://doi.org/10.1038/nmat4290
N.G. Welch, D.A. Winkler, H. Thissen, Antifibrotic strategies for medical devices. Adv. Drug Deliv. Rev. 167, 109–120 (2020). https://doi.org/10.1016/j.addr.2020.06.008
S. Wang, M. Lu, W. Wang, S. Yu, R. Yu et al., Macrophage polarization modulated by NF-κB in polylactide membranes-treated peritendinous adhesion. Small 18, e2104112 (2022). https://doi.org/10.1002/smll.202104112
S. Liu, H. Chen, T. Wu, G. Pan, C. Fan et al., Macrophage infiltration of electrospun polyester fibers. Biomater. Sci. 5, 1579–1587 (2017). https://doi.org/10.1039/c6bm00958a
S. Nishio, S. Takeda, K. Kosuga, M. Okada, E. Kyo et al., Decade of histological follow-up for a fully biodegradable poly-L-lactic acid coronary stent (Igaki-Tamai stent) in humans: are bioresorbable scaffolds the answer? Circulation 129, 534–535 (2014). https://doi.org/10.1161/CIRCULATIONAHA.113.003769
Z. Hou, W. Yan, T. Li, W. Wu, Y. Cui et al., Lactic acid-mediated endothelial to mesenchymal transition through TGF-β1 contributes to in-stent stenosis in poly-L-lactic acid stent. Int. J. Biol. Macromol. 155, 1589–1598 (2020). https://doi.org/10.1016/j.ijbiomac.2019.11.136
C.K. Sen, Human wound and its burden: updated 2020 compendium of estimates. Adv. Wound Care 10, 281–292 (2021). https://doi.org/10.1089/wound.2021.0026
R. Yu, H. Zhang, B. Guo, Conductive biomaterials as bioactive wound dressing for wound healing and skin tissue engineering. Nano-Micro Lett. 14, 1 (2021). https://doi.org/10.1007/s40820-021-00751-y
Q. Gao, F. Sun, Y. Li, L. Li, M. Liu et al., Biological tissue-inspired ultrasoft, ultrathin, and mechanically enhanced microfiber composite hydrogel for flexible bioelectronics. Nano-Micro Lett. 15, 139 (2023). https://doi.org/10.1007/s40820-023-01096-4
Y. Xie, S. Xiao, L. Huang, J. Guo, M. Bai et al., Cascade and ultrafast artificial antioxidases alleviate inflammation and bone resorption in periodontitis. ACS Nano 17, 15097–15112 (2023). https://doi.org/10.1021/acsnano.3c04328
Y. Deng, Y. Gao, T. Li, S. Xiao, M. Adeli et al., Amorphizing metal selenides-based ROS biocatalysts at surface nanolayer toward ultrafast inflammatory diabetic wound healing. ACS Nano 17, 2943–2957 (2023). https://doi.org/10.1021/acsnano.2c11448
S. Singh, A. Young, C.-E. McNaught, The physiology of wound healing. Surg. Oxf. 35, 473–477 (2017). https://doi.org/10.1016/j.mpsur.2017.06.004
Z. Wu, Y. Sun, S. Mu, M. Bai, Q. Li et al., Manganese-based antioxidase-inspired biocatalysts with axial Mn-N5 sites and 2D d-π-conjugated networks for rescuing stem cell fate. Angew. Chem. Int. Ed. 62, e202302329 (2023). https://doi.org/10.1002/anie.202302329
Y. Sun, S. Mu, Z. Xing, J. Guo, Z. Wu et al., Catalase-mimetic artificial biocatalysts with Ru catalytic centers for ROS elimination and stem-cell protection. Adv. Mater. 34, e2206208 (2022). https://doi.org/10.1002/adma.202206208
S. Cao, Z. Zhao, Y. Zheng, Z. Wu, T. Ma et al., A library of ROS-catalytic metalloenzyme mimics with atomic metal centers. Adv. Mater. 34, e2200255 (2022). https://doi.org/10.1002/adma.202200255
J. Guo, Z. Xing, L. Liu, Y. Sun, H. Zhou et al., Antioxidase-like nanobiocatalysts with ultrafast and reversible redox-centers to secure stem cells and periodontal tissues. Adv. Funct. Mater. 33(15), 2211778 (2023). https://doi.org/10.1002/adfm.202211778
J. Lee, H. Liao, Q. Wang, J. Han, J.H. Han et al., Exploration of nanozymes in viral diagnosis and therapy. Exploration (Beijing) 2, 20210086 (2022). https://doi.org/10.1002/EXP.20210086
P. Gong, L. Ren, X. Gao, J. Long, W. Tian et al., A novel barrier membrane with long-term ROS scavenging function for complete prevention of postoperative adhesion. Mater. Des. 238, 112691 (2024). https://doi.org/10.1016/j.matdes.2024.112691
J. Zhao, J.-Y. Fu, F. Jia, J. Li, B. Yu et al., Precise regulation of inflammation and oxidative stress by ROS-responsive prodrug coated balloon for preventing vascular restenosis. Adv. Funct. Mater. 33, 2213993 (2023). https://doi.org/10.1002/adfm.202213993
I.A. Darby, T.D. Hewitson, Hypoxia in tissue repair and fibrosis. Cell Tissue Res. 365, 553–562 (2016). https://doi.org/10.1007/s00441-016-2461-3
S. Van Linthout, K. Miteva, C. Tschöpe, Crosstalk between fibroblasts and inflammatory cells. Cardiovasc. Res. 102, 258–269 (2014). https://doi.org/10.1093/cvr/cvu062
P. Li, H. Zhou, T. Tu, H. Lu, Dynamic exacerbation in inflammation and oxidative stress during the formation of peritendinous adhesion resulted from acute tendon injury. J. Orthop. Surg. Res. 16, 293 (2021). https://doi.org/10.1186/s13018-021-02445-y
R. An, X. Wang, L. Yang, J. Zhang, N. Wang et al., Polystyrene microplastics cause granulosa cells apoptosis and fibrosis in ovary through oxidative stress in rats. Toxicology 449, 152665 (2021). https://doi.org/10.1016/j.tox.2020.152665
J.C. Jha, C. Banal, B.S.M. Chow, M.E. Cooper, K. Jandeleit-Dahm, Diabetes and kidney disease: role of oxidative stress. Antioxid. Redox Signal. 25, 657–684 (2016). https://doi.org/10.1089/ars.2016.6664
C. Estornut, J. Milara, M.A. Bayarri, N. Belhadj, J. Cortijo, Targeting oxidative stress as a therapeutic approach for idiopathic pulmonary fibrosis. Front. Pharmacol. 12, 794997 (2022). https://doi.org/10.3389/fphar.2021.794997
Y. Liang, K. Xu, P. Zhang, J. Zhang, P. Chen et al., Quercetin reduces tendon adhesion in rat through suppression of oxidative stress. BMC Musculoskelet. Disord. 21, 608 (2020). https://doi.org/10.1186/s12891-020-03618-2
T.-H. Kim, S.-Y. Heo, G.-W. Oh, W.S. Park, I.-W. Choi et al., A phlorotannins-loaded homogeneous acellular matrix film modulates post-implantation inflammatory responses. J. Tissue Eng. Regen. Med. 16, 51–62 (2022). https://doi.org/10.1002/term.3258
A. Carnicer-Lombarte, S.-T. Chen, G.G. Malliaras, D.G. Barone, Foreign body reaction to implanted biomaterials and its impact in nerve neuroprosthetics. Front. Bioeng. Biotechnol. 9, 622524 (2021). https://doi.org/10.3389/fbioe.2021.622524
A. Boruah, K. Roy, A. Thakur, S. Haldar, R. Konwar et al., Biocompatible nanodiamonds derived from coal washery rejects: antioxidant, antiviral, and phytotoxic applications. ACS Omega 8, 11151–11160 (2023). https://doi.org/10.1021/acsomega.2c07981
Y. Zhu, J. Li, W. Li, Y. Zhang, X. Yang et al., The biocompatibility of nanodiamonds and their application in drug delivery systems. Theranostics 2, 302–312 (2012). https://doi.org/10.7150/thno.3627
N. Gibson, O. Shenderova, T.J.M. Luo, S. Moseenkov, V. Bondar et al., Colloidal stability of modified nanodiamond ps. Diam. Relat. Mater. 18, 620–626 (2009). https://doi.org/10.1016/j.diamond.2008.10.049
S. Chauhan, N. Jain, U. Nagaich, Nanodiamonds with powerful ability for drug delivery and biomedical applications: recent updates on invivo study and patents. J. Pharm. Anal. 10, 1–12 (2020). https://doi.org/10.1016/j.jpha.2019.09.003
Q. Lin, R.H.J. Xu Xu, N. Yang, A.A. Karim, X.J. Loh et al., UV protection and antioxidant activity of nanodiamonds and fullerenes for sunscreen formulations. ACS Appl. Nano Mater. 2, 7604–7616 (2019). https://doi.org/10.1021/acsanm.9b01698
D.G. Lim, K.H. Kim, E. Kang, S.H. Lim, J. Ricci et al., Comprehensive evaluation of carboxylated nanodiamond as a topical drug delivery system. Int. J. Nanomed. 11, 2381–2395 (2016). https://doi.org/10.2147/IJN.S104859
I.V. Shugalei, A.S. Borovikova, A.P. Voznyakovskii, M.A. Ilyushin, Detonation nanodiamonds as antioxidants in various test systems. J. Superhard Mater. 39, 326–335 (2017). https://doi.org/10.3103/s1063457617050045
M.-S. Wu, D.-S. Sun, Y.-C. Lin, C.-L. Cheng, S.-C. Hung et al., Nanodiamonds protect skin from ultraviolet B-induced damage in mice. J. Nanobiotechnol. 13, 35 (2015). https://doi.org/10.1186/s12951-015-0094-4
V. Thomas, B.A. Halloran, N. Ambalavanan, S.A. Catledge, Y.K. Vohra, In vitro studies on the effect of p size on macrophage responses to nanodiamond wear debris. Acta Biomater. 8, 1939–1947 (2012). https://doi.org/10.1016/j.actbio.2012.01.033
S.H. Alawdi, E.S. El-Denshary, M.M. Safar, H. Eidi, M.-O. David et al., Neuroprotective effect of nanodiamond in Alzheimer’s disease rat model: a pivotal role for modulating NF-κB and STAT3 signaling. Mol. Neurobiol. 54, 1906–1918 (2017). https://doi.org/10.1007/s12035-016-9762-0
H. Yuan, Y. Zhang, Y. Su, N. Hu, J. Yang et al., A novel BiVO4/DLC heterojunction for efficient photoelectrochemical water splitting. Chem. Eng. J. 459, 141637 (2023). https://doi.org/10.1016/j.cej.2023.141637
C. Zhang, R. Yan, M. Bai, Y. Sun, X. Han et al., Pt-clusters-equipped antioxidase-like biocatalysts as efficient ROS scavengers for treating periodontitis. Small (2023). https://doi.org/10.1002/smll.202306966
X. Li, L. Wang, H. Liu, J. Fu, L. Zhen et al., C60 fullerenes suppress reactive oxygen species toxicity damage in boar sperm. Nano-Micro Lett. 11, 104 (2019). https://doi.org/10.1007/s40820-019-0334-5
Y. Xiao, K. Li, J. Bian, Y. Zhang, J. Li et al., Urolithin A protects neuronal cells against stress damage and apoptosis by Atp2a3 inhibition. Mol. Nutr. Food Res. 67, 2300146 (2023). https://doi.org/10.1002/mnfr.202300146
T. Kisseleva, D.A. Brenner, Mechanisms of fibrogenesis. Exp. Biol. Med. 233, 109–122 (2008). https://doi.org/10.3181/0707-mr-190
L.-K. Hung, S.-C. Fu, Y.-W. Lee, T.-Y. Mok, K.-M. Chan, Local vitamin-C injection reduced tendon adhesion in a chicken model of flexor digitorum profundus tendon injury. J. Bone Jt. Surg. 95, e41 (2013). https://doi.org/10.2106/jbjs.k.00988
T.M. Chen, X.M. Tian, L. Huang, J. Xiao, G.W. Yang, Nanodiamonds as pH-switchable oxidation and reduction catalysts with enzyme-like activities for immunoassay and antioxidant applications. Nanoscale 9, 15673–15684 (2017). https://doi.org/10.1039/c7nr05629j
Y. Yang, Y. Zhang, L. Wang, Z. Miao, K. Zhou et al., Antibacterial property of oxygen-terminated carbon bonds. Adv. Funct. Mater. 32, 2200447 (2022). https://doi.org/10.1002/adfm.202200447
D. Zhu, L. Zhang, R.E. Ruther, R.J. Hamers, Photo-illuminated diamond as a solid-state sourceof solvated electrons in water for nitrogenreduction. Nat. Mater. 12, 836–841 (2013). https://doi.org/10.1038/nmat3696
X. Dai, Q. Xu, Y. Li, L. Yang, Y. Zhang et al., Salen-manganese complex-based nanozyme with enhanced superoxide- and catalase-like activity for wound disinfection and anti-inflammation. Chem. Engin. J. 471, 144694 (2023). https://doi.org/10.1016/j.cej.2023.144694
V.N. Mochalin, O. Shenderova, D. Ho, Y. Gogotsi, The properties and applications of nanodiamonds. Nat. Nanotechnol. 7, 11–23 (2012). https://doi.org/10.1038/nnano.2011.209
J. Whitlow, S. Pacelli, A. Paul, Multifunctional nanodiamonds in regenerative medicine: recent advances and future directions. J. Control. Release 261, 62–86 (2017). https://doi.org/10.1016/j.jconrel.2017.05.033
J.K.F. Wong, Y.H. Lui, Z. Kapacee, K.E. Kadler, M.W.J. Ferguson et al., The cellular biology of flexor tendon adhesion formation. Am. J. Pathol. 175, 1938–1951 (2009). https://doi.org/10.2353/ajpath.2009.090380
M. Hedl, J. Yan, H. Witt, C. Abraham, IRF5 is required for bacterial clearance in human M1-polarized macrophages, and IRF5 immune-mediated disease risk variants modulate this outcome. J. Immunol. 202, 920–930 (2019). https://doi.org/10.4049/jimmunol.1800226
Y. Li, X. Wang, B. Hu, Q. Sun, M. Wan et al., Neutralization of excessive levels of active TGF-β1 reduces MSC recruitment and differentiation to mitigate peritendinous adhesion. Bone Res. 11, 24 (2023). https://doi.org/10.1038/s41413-023-00252-1
J. Braune, U. Weyer, C. Hobusch, J. Mauer, J.C. Brüning et al., IL-6 regulates M2 polarization and local proliferation of adipose tissue macrophages in obesity. J. Immunol. 198, 2927–2934 (2017). https://doi.org/10.4049/jimmunol.1600476
S. Oishi, R. Takano, S. Tamura, S. Tani, M. Iwaizumi et al., M2 polarization of murine peritoneal macrophages induces regulatory cytokine production and suppresses T-cell proliferation. Immunology 149, 320–328 (2016). https://doi.org/10.1111/imm.12647
P.A. Revell, The combined role of wear ps, macrophages and lymphocytes in the loosening of total joint prostheses. J. R. Soc. Interface. 5, 1263–1278 (2008). https://doi.org/10.1098/rsif.2008.0142
Y. Xie, J. Zhou, Q. Wei, Z.M. Yu, H. Luo et al., Improving the long-term stability of Ti6Al4V abutment screw by coating micro/nano-crystalline diamond films. J. Mech. Behav. Biomed. Mater. 63, 174–182 (2016). https://doi.org/10.1016/j.jmbbm.2016.06.018