Frontiers of Chemical Science and Engineering >
Long acting carmustine loaded natural extracellular matrix hydrogel for inhibition of glioblastoma recurrence after tumor resection
Received date: 08 Feb 2021
Accepted date: 23 Apr 2021
Published date: 15 Apr 2022
Copyright
Many scientific efforts have been made to penetrate the blood-brain barrier and target glioblastoma cells, but the outcomes have been limited. More attention should be given to local inhibition of recurrence after glioblastoma resection to meet real medical needs. A biodegradable wafer containing the chemotherapeutics carmustine (1,3-bis(2-chloroethyl)-1-nitrosourea, BCNU) was the only local drug delivery system approved for clinical glioblastoma treatment, but with a prolonged survival time of only two months and frequent side effects. In this study, to improve the sustained release and prolonged therapeutic effect of drugs for inhibiting tumor recurrence after tumor resection, both free BCNU and BCNU- poly (lactic-co-glycolic acid) (the ratio of lactic acid groups to glycolic acid groups is 75/25) nanoparticles were simultaneously loaded into natural extracellular matrix hydrogel from pigskin to prepare BCNU gels. The hydrogel was injected into the resection cavity of a glioblastoma tumor immediately after tumor removal in a fully characterized resection rat model. Free drugs were released instantly to kill the residual tumor cells, while drugs in nanoparticles were continuously released to achieve a continuous and effective inhibition of the residual tumor cells for 30 days. These combined actions effectively restricted tumor growth in rats. Thus, this strategy of local drug implantation and delivery may provide a reliable method to inhibit the recurrence of glioblastoma after tumor resection in vivo.
Key words: BCNU; glioblastoma recurrence; tumor resection; nanoparticles; hydrogel
Sunhui Chen , Qiujun Qiu , Dongdong Wang , Dejun She , Bo Yin , Meihong Chai , Huining He , Dong Nyoung Heo , Jianxin Wang . Long acting carmustine loaded natural extracellular matrix hydrogel for inhibition of glioblastoma recurrence after tumor resection[J]. Frontiers of Chemical Science and Engineering, 2022 , 16(4) : 536 -545 . DOI: 10.1007/s11705-021-2067-5
1 |
Siegel R L, Miller K D, Jemal A. Cancer statistics 2019. CA: a Cancer Journal for Clinicians, 2019, 69(1): 7–34
|
2 |
Bastiancich C, Bianco J, Vanvarenberg K, Ucakar B, Joudiou N, Gallez B, Bastiat G, Lagarce F, Préat V, Danhier F. Injectable nanomedicine hydrogel for local chemotherapy of glioblastoma after surgical resection. Journal of Controlled Release, 2017, 264: 45–54
|
3 |
Stupp R, Brada M, van den Bent M J, Tonn J C, Pentheroudakis G. High-grade glioma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Annals of Oncology: Official Journal of the European Society for Medical Oncology, 2014, 25(Suppl 3): 93–101
|
4 |
Wei X L, Chen X S, Ying M, Lu W Y. Brain tumor-targeted drug delivery strategies. Acta Pharmaceutica Sinica. B, 2014, 4(3): 193–201
|
5 |
Chai Z L, Hu X F, Lu W Y. Cell membrane-coated nanoparticles for tumor-targeted drug delivery. Science China Materials, 2017, 60(6): 504–510
|
6 |
Saucier-Sawyer J K, Seo Y E, Gaudin A, Quijano E, Song E, Sawyer A J, Deng Y, Huttner A, Saltzman W M. Distribution of polymer nanoparticles by convection-enhanced delivery to brain tumors. Journal of Controlled Release, 2016, 232: 103–112
|
7 |
Strohbehn G, Coman D, Han L, Ragheb R R, Fahmy T M, Huttner A J, Hyder F, Piepmeier J M, Saltzman W M, Zhou J. Imaging the delivery of brain-penetrating PLGA nanoparticles in the brain using magnetic resonance. Journal of Neuro-Oncology, 2015, 121(3): 441–449
|
8 |
Zhang C, Mastorakos P, Sobral M, Berry S, Song E, Nance E, Eberhart C G, Hanes J, Suk J S. Strategies to enhance the distribution of nanotherapeutics in the brain. Journal of Controlled Release, 2017, 267: 232–239
|
9 |
Shapira-Furman T, Serra R, Gorelick N, Doglioli M, Tagliaferri V, Cecia A, Peters M, Kumar A, Rottenberg Y, Langer R, Brem H, Tyler B, Domb A J. Biodegradable wafers releasing Temozolomide and Carmustine for the treatment of brain cancer. Journal of Controlled Release, 2019, 295: 93–101
|
10 |
Westphal M, Hilt D C, Bortey E, Delavault P, Olivares R, Warnke P C, Whittle I R, Jaaskelainen J, Ram Z. A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro-Oncology, 2003, 5(2): 79–88
|
11 |
Attenello F J, Mukherjee D, Datoo G, McGirt M J, Bohan E, Weingart J D, Olivi A, Quinones-Hinojosa A, Brem H. Use of Gliadel (BCNU) wafer in the surgical treatment of malignant glioma: a 10-year institutional experience. Annals of Surgical Oncology, 2008, 15(10): 2887–2893
|
12 |
Subach B R, Witham T F, Kondziolka D, Lunsford D, Bozik M, Schiff D. Morbidity and survival after 1,3-bis(2-chloroethyl)-1-nitrosourea wafer implantation for recurrent glioblastoma: a retrospective case-matched cohort series. Neurosurgery, 1999, 45(1): 17–22
|
13 |
Holmes T C, de Lacalle S, Su X, Liu G S, Rich A, Zhang S G. Extensive neurite outgrowth and active synapse formation on self-assembling peptide scaffolds. Proceedings of the National Academy of Sciences of the United States of America, 2000, 97(12): 6728–6733
|
14 |
Chen Q, Wang C, Zhang X D, Chen G, Hu Q, Li H, Wang J, Wen D, Zhang Y, Lu Y, Yang G, Jiang C, Wang J, Dotti G, Gu Z. In situ sprayed bioresponsive immunotherapeutic gel for post-surgical cancer treatment. Nature Nanotechnology, 2019, 14(1): 89–97
|
15 |
Park J, Doyle P S. Multifunctional hierarchically-assembled hydrogel particles with pollen grains via pickering suspension polymerization. Langmuir, 2018, 34(48): 14643–14651
|
16 |
De Leon-Rodriguez L M, Hemar Y, Mo G, Mitra A K, Cornish J, Brimble M A. Multifunctional thermoresponsive designer peptide hydrogels. Acta Biomaterialia, 2017, 47: 40–49
|
17 |
Bastiancich C, Danhier P, Preat V, Danhier F. Anticancer drug-loaded hydrogels as drug delivery systems for the local treatment of glioblastoma. Journal of Controlled Release, 2016, 243: 29–42
|
18 |
Ghuman H, Massensini A R, Donnelly J, Kim S M, Medberry C J, Badylak S F, Modo M. ECM hydrogel for the treatment of stroke: characterization of the host cell infiltrate. Biomaterials, 2016, 91: 166–181
|
19 |
Medberry C J, Crapo P M, Siu B F, Carruthers C A, Wolf M T, Nagarkar S P, Agrawal V, Jones K E, Kelly J, Johnson S A, Velankar S S, Watkins S C, Modo M, Badylak S F. Hydrogels derived from central nervous system extracellular matrix. Biomaterials, 2013, 34(4): 1033–1040
|
20 |
Chan B P, Leong K W. Scaffolding in tissue engineering: general approaches and tissue-specific considerations. European Spine Journal, 2008, 17(S4 Suppl 4): 467–479
|
21 |
Zhu J M, Marchant R E. Design properties of hydrogel tissue-engineering scaffolds. Expert Review of Medical Devices, 2011, 8(5): 607–626
|
22 |
Sayiner O, Arisoy S, Comoglu T, Ozbay F G, Esendagli G. Development and in vitro evaluation of temozolomide-loaded PLGA nanoparticles in a thermoreversible hydrogel system for local administration in glioblastoma multiforme. Journal of Drug Delivery Science and Technology, 2020, 57: 1–10
|
23 |
Singh M, Chakrapani A, O’Hagan D. Nanoparticles and microparticles as vaccine-delivery systems. Expert Review of Vaccines, 2007, 6(5): 797–808
|
24 |
McClements D J. Encapsulation, protection, and delivery of bioactive proteins and peptides using nanoparticle and microparticle systems: a review. Advances in Colloid and Interface Science, 2018, 253: 1–22
|
25 |
Sheng J Y, Han L M, Qin J, Ru G, Li R X, Wu L H, Cui D Q, Yang P, He Y W, Wang J X. N-Trimethyl chitosan chloride-coated PLGA nanoparticles overcoming multiple barriers to oral insulin absorption. ACS Applied Materials & Interfaces, 2015, 7(28): 15430–15441
|
26 |
Yang M B, Tamargo R J, Brem H. Controlled delivery of 1,3-bis(2-chloroethyl)-1-nitrosourea from ethylene-vinyl acetate copolymer. Cancer Research, 1989, 49(18): 5103–5107
|
27 |
Badylak S F. The extracellar matrix as a scaffold for tissue reconstruction. Cell & Developmental Biology, 2002, 13(5): 377–383
|
28 |
Sheets K T, Bago J R, Paulk I L, Hingtgen S D. Image-guided resection of glioblastoma and intracranial implantation of therapeutic stem cell-seeded scaffolds. Jove-Journal of Visualized Experiments, 2018, 137(137): e57452
|
29 |
Lee P W, Pokorski J K. Poly(lactic-co-glycolic acid) devices: production and applications for sustained protein delivery. Wiley Interdisciplinary Reviews. Nanomedicine and Nanobiotechnology, 2018, 10(8): e1516
|
30 |
Parrish K E, Sarkaria J N, Elmquist W F. Improving drug delivery to primary and metastatic brain tumors: strategies to overcome the blood-brain barrier. Clinical Pharmacology and Therapeutics, 2015, 97(4): 336–346
|
31 |
Hamard L, Ratel D, Selek L, Berger F, van der Sanden B, Wion D. The brain tissue response to surgical injury and its possible contribution to glioma recurrence. Journal of Neuro-Oncology, 2016, 128(1): 1–8
|
32 |
Ding L, Wang Q, Shen M, Sun Y, Zhang X, Huang C, Chen J, Li R, Duan Y. Thermoresponsive nanocomposite gel for local drug delivery to suppress the growth of glioma by inducing autophagy. Autophagy, 2017, 13(7): 1176–1190
|
33 |
Sherman J H, Redpath G T, Redick J A, Purow B W, Laws E R, Jane J A Jr, Shaffrey M E, Hussaini I M. A novel fixative for immunofluorescence staining of CD133-positive glioblastoma stem cells. Journal of Neuroscience Methods, 2011, 198(1): 99–102
|
34 |
Taal W, Bromberg J E C, van den Bent M J. Chemotherapy in glioma. CNS Oncology, 2015, 4(3): 179–192
|
35 |
Jung J, Gilbert M R, Park E M. Isolation and propagation of glioma stem cells from acutely resected tumors. Methods in Molecular Biology (Clifton, N.J.), 2016, 1516: 361–369
|
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