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WIREs Nanomed Nanobiotechnol
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Process hybridization schemes for multiscale engineered tissue biofabrication

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Abstract Recapitulation of multiscale structure–function properties of cells, cell‐secreted extracellular matrix, and 3D architecture of natural tissues is central to engineering biomimetic tissue substitutes. Toward achieving biomimicry, a variety of biofabrication processes have been developed, which can be broadly classified into five categories—fiber and fabric formation, additive manufacturing, surface modification, remote fields, and other notable processes—each with specific advantages and limitations. The majority of biofabrication literature has focused on using a single process at a time, which often limits the range of tissues that could be created with relevant features that span nano to macro scales. With multiscale biomimicry as the goal, development of hybrid biofabrication strategies that synergistically unite two or more processes to complement each other's strengths and limitations has been steadily increasing. This work discusses recent literature in this domain and attempts to equip the reader with the understanding of selecting appropriate processes that can harmonize toward creating engineered tissues with appropriate multiscale structure–function properties. Opportunities related to various hybridization schemes and a future outlook on scale‐up biofabrication have also been discussed. This article is categorized under: Nanotechnology Approaches to Biology > Nanoscale Systems in Biology Implantable Materials and Surgical Technologies > Nanotechnology in Tissue Repair and Replacement
Examples of hybrid biofabrication strategies with RF processes. (a) Aligned electrospun PLGA fiber mats are chopped up into microfibers and aligned within a hydrogel through an external magnetic field (Omidinia‐Anarkoli et al., 2017). (b) Label‐free bioprinting processes utilizing magnetophoresis for cell herding in intricate structures (Abdel Fattah et al., 2016); (c) Hybrid process utilizing ultrasound stimulation during SLA printing for deterministically organizing hASC in crisscross patterns within GelMA hydrogels (Chansoria & Shirwaiker, 2020). (d) Electrophoretic deposition of charged dexamethasone‐loaded mesoporous silica nanoparticles onto casted PLLA/PCL scaffold for bone tissue engineering (Qiu et al., 2016)
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Examples of hybridization strategies with SM processes. (a) Electrospun PEOT/PBT fibers produced under varying relative humidity to nano surface porosity for enhanced MSC attachment and ECM production for skeletal tissue engineering (Chen et al., 2017). (b) NaOH treatment to enhance the hydrophilicity and cell attachment of extrusion printed PCL scaffolds for bone tissue engineering (Wang et al., 2016). (c) Electrospun PLA fibers coated with nano HAp particles for bone tissue engineering (Mohammadi et al., 2018)
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Examples of hybrid biofabrication strategies involving two or more AM processes. (a) Extrusion printing of support structures (agarose) to support extrusion‐printed SMC or fibroblast spheroids, which later fuse to form vasculature (Norotte et al., 2009). (b) Extrusion printing of PLA and SLA of cell‐laden GelMA, with the entire tissue featuring various peptides to promote bone formation (Cui et al., 2016)
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Examples of hybrid FF‐AM processing strategies. (a) Multiscale fibrous scaffolds fabricated via layer‐wise extrusion printing of PCL and solution spinning of PLGA for musculoskeletal tissue constructs featuring enhanced entrapment and proliferation of seeded 3 T3 cells (Mota et al., 2010). (b) Inkjet printing of growth factors (FGF2 and BMP2) over aligned electrospun polystyrene fibers, wherein seeded myoblasts (MF20) exhibited elongation and differentiation to tenocytes and osteoblasts (Ker et al., 2011). (c) Tubular PCL scaffolds fabricated via solution spinning (inner structure of the lumen) and MEW (providing mechanical reinforcement) (Jungst et al., 2019). (d) Melt electrowritten PCL scaffolds with varying fiber sizes combined with electrospun “catching” fibers, wherein the larger fibers provided structural strength while the smaller “catching” fibers facilitated subsequent cell or spheroid seeding (Hrynevich et al., 2018)
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(a) Usage of terms “hybrid material” or “hybrid process”, and “biofabrication” or “tissue engineering” in publication titles, abstracts, and author keywords in the past two decades. (b) Relative usage of each process (Table 1), and “hybrid,” and “biofabrication” or “tissue engineering” in publication titles, abstracts, and author keywords, for the calendar year 2019. Both graphics were generated using the Web of Science Core Collection
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The five broader categories of biofabrication processes. Hybrid biofabrication strategies can be devised using these processes and appropriate biomaterials to engineer various types of functionalized tissue constructs featuring biomimetic micro/nano‐scale fibrous architectures, surface morphologies, and composite structures
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Summary of materials and process considerations for tissue biofabrication. Appropriate processes should be selected as per the optimized materials formulations and process constraints (Table 1). Automation schemes should further be investigated for reproducible and efficient scale‐up tissue biofabrication
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Examples of hybrid biofabrication strategies involving ON processes. (a) Biomimicking bone tissue constructs containing alternate layers of casted 3 T3 cell‐laden GelMA and electrospun PHB sheets (Sadat‐Shojai et al., 2016). (b) Extrusion printing of plaster, which formulates the template for casting of PCL decorated with TiO2 or bioactive glass nanoparticles for musculoskeletal tissue engineering (Tamjid et al., 2013). (c) Concomitant solution electrospinning and electrospraying of cells to achieve high cell seeding efficiency within multi‐layered electrospun PEUU scaffolds (Stankus et al., 2006). (d) Laser‐assisted printing of cells over an electrospun cardiac PEUU patch made using TIPT (Gaebel et al., 2011)
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Future outlook of an automated hybrid manufacturing system, which consists of tool heads representing different biofabrication processes configured in an indexing mechanism (turret or gantry system) or selectively handled by robots. For less versatile processes (Table 1), dedicated workstations could be used, and handling and transfer between stations performed by robots
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Implantable Materials and Surgical Technologies > Nanotechnology in Tissue Repair and Replacement
Nanotechnology Approaches to Biology > Nanoscale Systems in Biology

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