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Minimally Invasive Intradiscal Delivery of BM-MSCs via Fibrous Microscaffold Carriers

  • Paweł Nakielski*
    Paweł Nakielski
    Department of Biosystems and Soft Matter, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
    *Email: [email protected]
  • Daniel Rybak
    Daniel Rybak
    Department of Biosystems and Soft Matter, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
    More by Daniel Rybak
  • Katarzyna Jezierska-Woźniak
    Katarzyna Jezierska-Woźniak
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
  • Chiara Rinoldi
    Chiara Rinoldi
    Department of Biosystems and Soft Matter, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
  • Emilia Sinderewicz
    Emilia Sinderewicz
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
  • Joanna Staszkiewicz-Chodor
    Joanna Staszkiewicz-Chodor
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
  • Mohammad Ali Haghighat Bayan
    Mohammad Ali Haghighat Bayan
    Department of Biosystems and Soft Matter, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
  • Wioleta Czelejewska
    Wioleta Czelejewska
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
  • Olga Urbanek
    Olga Urbanek
    Laboratory of Polymers and Biomaterials, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
    More by Olga Urbanek
  • Alicja Kosik-Kozioł
    Alicja Kosik-Kozioł
    Department of Biosystems and Soft Matter, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
  • Monika Barczewska
    Monika Barczewska
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
  • Mateusz Skomorowski
    Mateusz Skomorowski
    Neurosurgery Clinic, University Clinical Hospital in Olsztyn, Warszawska 30, Olsztyn 10-082, Poland
  • Piotr Holak
    Piotr Holak
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
    More by Piotr Holak
  • Seweryn Lipiński
    Seweryn Lipiński
    Department of Electrical Engineering, Power Engineering, Electronics and Automation, Faculty of Technical Sciences, University of Warmia and Mazury, Oczapowskiego 11, Olsztyn 10-082, Poland
  • Wojciech Maksymowicz
    Wojciech Maksymowicz
    Laboratory for Regenerative Medicine, Department of Neurosurgery, School of Medicine, University of Warmia and Mazury, Warszawska 30, Olsztyn 10-082, Poland
  • , and 
  • Filippo Pierini*
    Filippo Pierini
    Department of Biosystems and Soft Matter, Institute of Fundamental Technological Research, Polish Academy of Sciences, Pawińskiego 5B, Warsaw 02-106, Poland
    *Email: [email protected]
Cite this: ACS Appl. Mater. Interfaces 2023, 15, 50, 58103–58118
Publication Date (Web):November 29, 2023
https://doi.org/10.1021/acsami.3c11710
Copyright © 2023 American Chemical Society

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    Abstract

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    Current treatments of degenerated intervertebral discs often provide only temporary relief or address specific causes, necessitating the exploration of alternative therapies. Cell-based regenerative approaches showed promise in many clinical trials, but limitations such as cell death during injection and a harsh disk environment hinder their effectiveness. Injectable microscaffolds offer a solution by providing a supportive microenvironment for cell delivery and enhancing bioactivity. This study evaluated the safety and feasibility of electrospun nanofibrous microscaffolds modified with chitosan (CH) and chondroitin sulfate (CS) for treating degenerated NP tissue in a large animal model. The microscaffolds facilitated cell attachment and acted as an effective delivery system, preventing cell leakage under a high disc pressure. Combining microscaffolds with bone marrow-derived mesenchymal stromal cells demonstrated no cytotoxic effects and proliferation over the entire microscaffolds. The administration of cells attached to microscaffolds into the NP positively influenced the regeneration process of the intervertebral disc. Injectable poly(l-lactide-co-glycolide) and poly(l-lactide) microscaffolds enriched with CH or CS, having a fibrous structure, showed the potential to promote intervertebral disc regeneration. These features collectively address critical challenges in the fields of tissue engineering and regenerative medicine, particularly in the context of intervertebral disc degeneration.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsami.3c11710.

    • Scheme presenting an arrangement of study groups and controls; FE-SEM micrographs showing PLLA microscaffolds; FE-SEM micrograph showing nanofibers after hydrolysis; FE-SEM micrographs showing PLLA and PLGA after CH and CS modifications; CA measurements; proliferative activity of BM-MSC cultured on PLLA and PLGA microscaffolds; quantification of cell attachment and spreading; the activity of LDH released from damaged cells cultured on microscaffolds; metabolic activity (MTT) of MSCs cultured on microscaffolds; proliferative activity of MSCs cultured on PLLA and PLGA microscaffolds; MRI signal intensity of IVDs implanted with PLGA and PLGA/CS MS without cells; histological assessment of positive control; histological assessment of negative control; damage to the disc by a laser beam; histological assessment of IVDs implanted with BM-MSC on PLLA MS; histological assessment of IVDs implanted with BM-MSC on PLLA/CH MS; histological assessment of IVDs implanted with BM-MSC on PLLA/CS MS; histological assessment of IVDs implanted with BM-MSC on PLGA MS; histological assessment of IVDs implanted with BM-MSC on PLGA/CH MS; histological assessment of IVDs implanted with BM-MSC on PLGA/CS MS; histology of IVDs’ structures with microscaffolds and without BM-MSC; and PLGA microscaffolds in NP (PDF)

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