In this featured review manuscript, the aim is to present a critical survey on the processes available for fabricating bioartificial organs (BAOs). The focus will be on hollow tubular organs for the transport of anabolites and catabolites, i.e., vessels, trachea, esophagus, ureter and urethra, and intestine. First, the anatomic hierarchical structures of tubular organs, as well as their principal physiological functions, will be presented, as this constitutes the mandatory requirements for effectively designing and developing physiologically relevant BAOs. Second, 3D bioprinting, solution electrospinning, and melt electrowriting will be introduced, together with their capacity to match the requirements imposed by designing scaffolds compatible with the anatomical and physiologically relevant environment. Finally, the intrinsic correlation between processes, materials, and cells will be critically discussed, and directives defining the strengths, weaknesses, and opportunities offered by each process will be proposed for assisting bioengineers in the selection of the appropriate process for the target BAO and its specific required functions.

Bioengineering is a discipline in which engineering principles are applied to biological systems and biomedical technologies. One of the main goals of bioengineering is to reproduce, repair, or recapitulate tissues and organs, or their functions. In bioengineering, geometries are directly inspired by anatomy, while properties closely follow physiological functions. From an anatomical point of view, there are 5 fundamental levels of organization in the human body, from the simplest one to the most complex: (i) the cellular level, (ii) the tissue level, (iii) the organ level, (iv) the organ-system level, and (v) the organism level [Góra et al., 2016]. Each tissue is a complex structure composed by multiple cell types immersed in multiple sets of proteins dispersed in an extracellular matrix (ECM) [Chen and Liu, 2016]. The cells in a tissue work together in an orchestrated manner to accomplish specific functions. An organ is made of various types of tissues, and intrinsically, of several types of cells. Each organ is characterized by complex structural, mechanical, and motility patterns responsible for one or more specific physiological functions [Del Gaudio et al., 2014; Mandrycky et al., 2015].

Diseases, injuries, and malfunctions of one (or more than one) of the organs affect and decrease the patient’s quality of life, and in the worst case, lead to death [Leberfinger et al., 2019]. The type of clinical treatment depends on the severity of the injury, the type of disease, and the medical history of the patient. As a first option, drug therapy and/or other noninvasive therapeutic treatments are privileged. However, when the progression of the disease advances, surgical intervention, including tissue transplantation or substitution, is unavoidable. Current transplantation and substitution techniques are based on the use of (i) autologous, or (ii) heterologous tissues, or (iii) synthetic prostheses, but these do not always represent a viable option [Hodges and Atala, 2013; Holland et al., 2018]. Substitution or transplantation of autologous tissues is not possible in case of previous harvesting and/or pathological degenerative conditions. As for heterologous tissues, the main limitation is a shortage of suitable and available tissues [Atala, 2005; Del Gaudio et al., 2014; Chen and Liu, 2016; Leberfinger et al., 2019]. In the past decades, synthetic prostheses were developed in the hope of facing the abovementioned shortcomings. However, there is an important mismatch between anatomical and mechanical requirements (MRs), and other issues can be found in the required biological properties and long-term expected patency [Holland et al., 2018]. Therefore, although organ shortage is already addressed by reparative [Stock and Vacanti, 2001; Ratner et al., 2004; Vacanti and Vacanti, 2014] (through implants, artificial organs and devices) or regenerative [Mozafari et al., 2019] (cell-containing structures or cell-based therapies) medicine, clinical complications still limit the success of the implantation. In an attempt to improve this success rate and increase the overall clinical performance, tissue engineering and regenerative medicine (TERM) aim to restore the functional and structural properties of diseased or damaged tissue, while maintaining and/or improving tissue performance [Shafiee and Atala, 2017]. Different approaches have been explored, all relying on the use of cells, scaffolds, or their combination [Furth and Atala, 2013; Hodges and Atala, 2013; Del Gaudio et al., 2014; ]. Through further process engineering, the resulting constructs are expected to mimic the structure (i.e., the internal architecture) and the complex cellular microenvironment of native tissues [Chen and Liu, 2016; Barbosa and Martins, 2018]. In particular, bioartificial organs (BAOs) constitute the expected outcome of designing and developing functional organs from regenerative medicine strategies. In order to be able to mimic the native organs to the greatest extent possible, researchers have to look in detail into the anatomical hierarchy of tissues [Nerem and Schutte, 2014] and their biological and mechanical properties [Nichol and Khademhosseini, 2010; Moffat et al., 2014; Marx, 2015; Chen and Liu, 2016].

To better understand the rich complexity (issued by millions of years of biological evolution), that can be found in various tissues and organs, Atala et al. [2012] have proposed 4 levels of classification according to a defined scale of increasing complexity: (i) flat tissue structures, (ii) tubular structures, (iii) hollow, non-tubular, viscous structures, and (iv) complex solid organs. Despite the available knowledge (both on the engineering and the biology side) and the accessible technologies (both the standard and the more advanced ones), there are still plenty of challenges in designing and developing more complex structures. Therefore, this review will point out the current situation considering these challenges, and can hopefully open up a new path for future studies. More precisely, this review will focus on the second group, namely the tubular structures. The human body is composed of several organ systems, including the respiratory, digestive, urinary, and circulatory system, each one containing tubular organs [Góra et al., 2016; Holland et al., 2018]. Their main function is to transport fluids, metabolites, and gases from, to, and through organs [Atala et al., 2012; Del Gaudio et al., 2014]. In order to engineer these tubular systems, biomaterials are processed into a tubular structure that is used as such or combined with cells and allowed to mature in vitro, before implantation. Various processing techniques to fabricate tubular constructs have already been proposed [Holland et al., 2018]. Such processing techniques can be grouped into (i) conventional and (ii) advanced techniques. Some examples of conventional laboratory techniques are gas foaming, molding, solvent casting, dip coating, and a few others. More advanced techniques, for reproducible results and adapted to clinical transfer, include three-dimensional bioprinting (3DBP), solution electrospinning (sES), and melt electrowriting (MEW) [Mandrycky et al., 2015; Dutta et al., 2017; Pedde et al., 2017; Holland et al., 2018]. Each of them has its own pros and cons – they will be discussed here below – which will influence the resulting properties of the fabricated tubular construct. Likewise, the choice of the processing technique depends on the specific requirements for which each BAO has been designed for. These biological requirements (BRs) and MRs depend, in their turn, on the anatomical hierarchical structure of the different tissues and on the physiological functions related to the anatomy of a specific organ. Consequently, there is an underlying correlation between (i) the requirements to match in order to restore the physiological functions, (ii) the various processing techniques to fabricate a tubular construct, and (iii) the obtained properties of the fabricated construct.

In this work, the development of functional tubular constructs from biomaterials and/or cells was reviewed (as depicted in the flow chart, Fig. 1). More specifically, the hierarchical anatomical structure of the 4 hollow tubular organs will be described (Part 1), together with the complex physiological functions and the MRs and BRs of each one. The state-of-the-art (SOTA) of processing techniques to develop tubular constructs (Part 2) will be reviewed as well. In the final part, the effect of processing techniques on the mechanical and biological aspects (Part 3), and thus the existing correlation between process, mechanical and biological pertinence will be discussed.

Fig. 1.

Flow chart. Part 1: Requirements dictated by anatomical and physiological concerns. Part 2: Strategies for the fabrication of tubular constructs for the regeneration of tubular organs. Part 3: Relationship between the process, cells, mechanical and biological performance.

Fig. 1.

Flow chart. Part 1: Requirements dictated by anatomical and physiological concerns. Part 2: Strategies for the fabrication of tubular constructs for the regeneration of tubular organs. Part 3: Relationship between the process, cells, mechanical and biological performance.

Close modal

As introduced above, requirements for TERM applications are defined considering the organ anatomy and physiology. The wall of all tubular organs is composed of different layers. In general, 4 layers can be distinguished including (i) mucosa, (ii) submucosa, (iii) muscularis externa, and (iv) adventitia and/or serosa layer (Fig. 2, left) [Góra et al., 2016]. A comparison between the 4 basic layers of each tubular system (i.e., trachea, esophagus, intestines, urethra and ureter, and blood vessels) is shown in Figure 2. These 4 layers consist of various cell types and ECM, which are organ specific. Each kind of cell and ECM component has a specific role to perform individually, but also as a multilayered structure in its whole, in such a way that they enable the physiological functions of the tubular organ.

Fig. 2.

Anatomical structure of tubular organs. Left: General structure of tubular organs (Image adapted from UNIFAL-MG, Histologia interatva; https://www.unifal-mg.edu.br).Right: comparison of the wall structure of the trachea, esophagus, intestines, urethra, ureter, and blood vessels.

Fig. 2.

Anatomical structure of tubular organs. Left: General structure of tubular organs (Image adapted from UNIFAL-MG, Histologia interatva; https://www.unifal-mg.edu.br).Right: comparison of the wall structure of the trachea, esophagus, intestines, urethra, ureter, and blood vessels.

Close modal

Depending on the physiological functions that each tubular organ has to fulfil, each layer of the tubular wall will have its own biological and mechanical properties, resulting in great differences in the hierarchical structure of the different tissues. Thus, it is important to look in detail into the different layers of the tubular wall and into their physiological functions, taken individually and as a whole (i.e., 4-layered wall structure). Moreover, it is important to investigate the correlations existing between the anatomy (hierarchical structure), the physiological function, and the mechanical and biological properties of a specific tubular organ. The main challenge when engineering a BAO with specific physiological functions is to meet the MRs and BRs. Table 1 gives an overview on (i) anatomical hierarchical structure, (ii) physiological functions, and (iii) MRs and BRs for each of the previously mentioned tubular organs.

Table 1.

Anatomy, physiolocial functions and requirements per system

Anatomy, physiolocial functions and requirements per system
Anatomy, physiolocial functions and requirements per system

In this section, 3 processing techniques (i.e., 3DBP, sES, and MEW) that enable the development of hollow tubular constructs will be introduced. An overview of the SOTA of each processing technique used for engineering one of the 4 tubular organs discussed above will be given. In particular, the correlations between processing, mechanical and biological performances will be discussed. Then, the potential of clinical translation of these tubular constructs will be evaluated.

Processing Techniques for the Development of Tubular Constructs to Regenerate Hollow Tubular Organs

Three-Dimensional Bioprinting

3DBP is a fabrication method that, starting from a computer-aided design model, creates a 3D construct in a layer-by-layer manner [Murphy and Atala, 2014]. As the “bio” term suggests, it involves biologically derived materials and/or cells [Moroni et al., 2018]. This technique allows the creation of constructs made of multiple materials and cell types in the same process, following a design-specific distribution. 3DBP techniques are usually classified into 3 categories, depending on the working principle of the layer-by-layer deposition process. They can be distinguished in (i) microextrusion-based, (ii) inkjet-based, and (iii) laser-assisted bioprinting (Fig. 3). For detailed information on the working principles of each bioprinter type, the authors suggest the reviews of Murphy and Atala, [2014], Holland et al. [2018], Van Hoorick et al. [2019], and Jeong et al. [2020].

Fig. 3.

3DBP process: bioprinters classification based on the working principle. a Microextrusion bioprinter, b Inkjet bioprinter, c Laser-assisted bioprinter. Image adapted from Murphy and Atala [2014].

Fig. 3.

3DBP process: bioprinters classification based on the working principle. a Microextrusion bioprinter, b Inkjet bioprinter, c Laser-assisted bioprinter. Image adapted from Murphy and Atala [2014].

Close modal

Many advantages have been reported in literature on the 3DBP technique. One of them is the precise control at the micrometric scale of the biomaterial deposition. This allows to obtain a controlled porosity, in terms of both geometry and size, and to accurately mimic the physiological structure of the native organs [Li et al., 2016]. Moreover, the possibility to combine multiple materials and cell types in the same process, with specific arrangements, allows to overcome the limitations of conventional fabrication techniques and it brings TERM closer to the complexity of native tissues. Finally, despite not yet used in clinical practice, in a future perspective, 3DBP will allow the fabrication of patient-specific BAOs, starting from the patient’s medical images (e.g., magnetic resonance imaging) [Sahai and Gogoi, 2020]. This customization would improve the SOTA of regenerative medicine.

However, the formulation of biomaterials and cell components responding to the bioprinting requirements is the main challenge of this technique, and the final construct accuracy strongly depends on it [Panwar and Tan, 2016]. Additional drawbacks are (i) the possible cellular damage due to the stress applied during the process, and (ii) the use in some cases of temperatures or light wavelengths incompatible with cell survival. Table 2 shows an overview of the SOTA on 3DBP of tubular organs.

Table 2.

3D Bioprinting as a fabrication technique

3D Bioprinting as a fabrication technique
3D Bioprinting as a fabrication technique

Solution Electrospinning

sES is a versatile processing technique that relies on the application of a high voltage electrical force to enable the production of micro- and nano-scale fibers from a polymer solution and deposit these fibers on a suitable collector. The high voltage (within a range of several kV, typically between 5 and 20 kV) generates electric charges on the polymer solution. These electric charges accumulate on the polymer surface until they eventually overcome the surface tension and form a Taylor cone. This results in an electrically charged polymer jet that is drawn from the tip of the Taylor cone and stretches in the electric field towards the oppositely charged collector such as a plate, a rotating mandrel, etc. As the polymer moves towards the collector, the solvent evaporates, and the jet solidifies, forming solid micro- and nano-scaled fibers. A schematic representation of the sES process and the different elements constituting the sES set-up are illustrated in Figure 4. A detailed description of the fundamentals of sES can be found in the book of Bosworth and Downes [2011].

Fig. 4.

sES process: different elements required and overall schematic.

Fig. 4.

sES process: different elements required and overall schematic.

Close modal

Various factors influence the sES process, including solution parameters (i.e., polymer concentration and molecular weight, solution viscosity and conductivity, surface tension, solvents), process parameters (i.e., applied voltage, flow rate, collecting electrode, needle tip-to-collector distance, diameter of the needle tip), and environmental parameters (i.e., temperature, humidity). All these factors have been described in detail by Ibrahim and Klingner [2020] in a review on electrospun polymeric nanofibers and will not be discussed further in this review.

The main advantage of using sES as a processing technique for TERM is the production of fibrous networks that resemble those of the natural ECM in terms of hierarchical organization and properties. Other advantages include the high surface-to-volume ratio of the fibers, high aspect ratio, tunable porosity, flexibility to tailor surface properties, and the possibility to produce fibers from a large variety of materials. Electrospun scaffolds are known to provide a good microenvironment for cell adhesion, proliferation, and differentiation [Mo et al., 2019; Oprea et al., 2019].

Even though the sES process has been known since the 1930s, it gained renewed interest in the last decades due to the inception of advanced electrospinning set-ups (e.g., side-by-side ES and coaxial ES). These advanced set-ups have the ability to produce scaffolds with multiple layers, made of multiple materials, with gradients, with fiber alignment, with multiphasic fibers, with core-shell fibers, with drug-loaded fibers, etc [Subbiah et al., 2005; Moghe and Gupta, 2008; Sill and von Recum, 2008; Bhardwaj and Kundu, 2010]. Therefore, it has been extensively used in the research focusing on the development of scaffolds for various TERM applications [Lelkens et al., 2008; Sell et al., 2010; Jin et al., 2012; Jiang et al., 2014; Erdem et al., 2016; Kennedy et al., 2016; Pien et al., 2021]. In Table 3, a summary of recent research studies using sES for the fabrication of tubular scaffolds for the regeneration of the 4 tubular organs described in Part 1 is given.

Table 3.

Solution electrospinning as a fabrication technique

Solution electrospinning as a fabrication technique
Solution electrospinning as a fabrication technique

Melt Electrowriting

MEW process is similar to sES, except that in MEW a polymer melt is used instead of a polymer solution [Willerth, 2017; Yang et al., 2018]. Therefore, an extra heating system to heat up the polymer is needed in the MEW set-up (Fig. 5). As in sES, an electrostatically ejected jet is drawn as a polymer jet which then cools down and solidifies either in air or on the collector. A low variation in fiber diameter can be obtained due to the high viscosity and low charge of these polymer melts. In combination with a moving collector, the MEW process enables (i) to directly write a 3D scaffold, and (ii) the rational design of scaffolds with control over pore size and pore interconnectivity [Jin et al., 2020]. More specifically, MEW allows to fabricate scaffolds with high reproducibility using a computer-controlled layer-by-layer approach (similar to fused deposition modelling technologies including 3DBP). In other words, MEW fibers can be precisely deposited to generate constructs with predefined architectures [Hochleitner et al., 2015]. Another advantage of MEW compared to sES is that it has no solvent evaporation, and thus, toxicity issues associated with solvents can be avoided [Dalton et al., 2015; Muerza-Cascante et al., 2015; Brown et al., 2016].

Fig. 5.

MEW process: different elements required and overall schematic.

Fig. 5.

MEW process: different elements required and overall schematic.

Close modal

The MEW technique and its use in TERM applications have already been extensively reviewed by Dalton et al. [2013], Muerza-Cascante et al. [2015], and Afghah et al. [2019]. The most recent literature has been summarized last year by Robinson et al. [2019] and will therefore not be described in detail in this review. In addition to the optimization of general processing parameters, research has also focused on the optimization of the MEW process with the aim to fabricate hollow tubular constructs (and thus, on the fabricating process onto a rotating mandrel). For more details on MEW onto rotating mandrels, and the MEW design parameters of tubular constructs for TERM applications in general, the authors would like to refer to the work of Jungst et al. [2015], Brown et al. [2016], McColl et al. [2018], Ibrahim et al. [2019], and Paxton et al. [2020]. The focus of this review goes to the use of MEW to fabricate tubular constructs for the regeneration of the introduced 4 hollow tubular organs (Table 4).

Table 4.

Melt electrowriting as a fabrication technique

Melt electrowriting as a fabrication technique
Melt electrowriting as a fabrication technique

Strengths, Weaknesses, Opportunities, and Threats

Each one of the presented fabrication techniques has specific advantages and limitations that should be considered when scientists want to develop a BAO. Strengths, weaknesses, opportunities, and threats (SWOT) of each technique are summarized in Figure 6 in a parallel SWOT analysis of the 3 mentioned techniques.

Fig. 6.

Strengths, weaknesses, opportunities and threats (SWOT) of the 3 advanced processing techniques discussed in this review. 3DBP, 3D bioprinting; sES, solution electrospinning; MEW, melt electrowriting.

Fig. 6.

Strengths, weaknesses, opportunities and threats (SWOT) of the 3 advanced processing techniques discussed in this review. 3DBP, 3D bioprinting; sES, solution electrospinning; MEW, melt electrowriting.

Close modal

Correlation between Processing, Mechanical and Biological Performances

As discussed above (Part 1), the anatomical hierarchical structure of healthy native tissues (Fig. 2) and their corresponding complex physiological functions result in very specific mechanical and biological design requirements when engineering a BAO (Table 1). On the one hand, the MRs and BRs for the construct design influence the process selection. It is worth noting that when looking into the SOTA of the fabrication, and more precisely into the advanced processing techniques (Part 2), a wide variety of materials and biological models have been investigated (Tables 2, 3, 4). Engineering a bioartificial tubular organ not only depends on the choice of the applied processing technique, its corresponding processing parameters and the construct design, but also on the material properties and on the biological model (i.e., cells and biological cues) selected for the fabrication. This means that a first correlation can be found within the fabrication process itself: (i) material choice, (ii) biological model, and (iii) processing technique (including process parameters and construct design). On the other hand, the selection of the fabrication process (i.e., processing, materials, cells) when engineering a BAO influences the resulting mechanical and biological properties of the developed construct. These resulting properties can now be linked back to check if the requirements have been met, and to evaluate the mechanical and biological pertinence of the processing technique. In other words, there is also a correlation between (i) the construct requirements to match (depending on anatomy and physiology) and (ii) the resulting properties obtained (depending on the fabrication process).

These intrinsic correlations are discussed based on examples from literature, in the paragraphs below, and aim at showing the advancements and limitations per technique and/or per tubular organ.

Cellularization of a BAO

As shown in Table 1, some of the physiological functions of each organ rely on the presence of the proper cell types of each layer. For this reason, the cellularization of the scaffold is an important step in engineering BAOs. Because of process-related limitations [Dalton et al., 2015; Hong et al., 2019], both MEW and sES mainly provide a tubular “skeleton”, which acts as a mechanical structural support for (i) cell seeding prior to implantation or (ii) to trigger cell migration after implantation. Lv et al. [2016] reported on a bioengineered construct produced by sES for urethral repair, in which they compared (i) a cell-based model [i.e., mesenchymal stem cells (MSCs) seeded prior to implantation] with (ii) an acellular model. Results pointed out that the cell-based models outperformed the acellular models, for urethral defect repair in rabbits. However, the long production time of a cell-based model (i.e., for cell seeding and maturation) and the vast biological expertise required for its fabrication are some of the reasons why acellular models are still widely investigated.

In contrast to MEW and sES, 3DBP has the possibility to directly incorporate cells and/or biological molecules in the construct during its fabrication. Different cell types can be printed in the same process, with the desired spatial distribution, in order to reproduce the physiological multilayered structure of tubular organs. Using this strategy, Bae et al. [2018] were able to print epithelial cells in the inner layer of their trachea construct, well separated from the layer of MSCs. After in vivo implantation in rabbits, this allowed the formation of a ciliated respiratory epithelium, thus fulfilling one of the BRs (BR1 in Table 1).

Regarding the source for the BAO cellularization, Tables 2, 3, 4 show a large use of MSCs as a cell source for the construct cellularization. These multipotent stem cells can be easily harvested from different sources, including bone marrow and adipose tissue, and many studies have demonstrated the possibility to differentiate them into different cell types through biochemical and mechanical cues [Huang and Li, 2008]. The use of MSCs is convenient from a clinical perspective, thanks to the possibility to use an autologous source in the construct fabrication. This is true both at the animal and human trial level, and it is well represented in the tables, where most of the animal in vivo studies have been conducted using autologous MSCs. However, the use of MSCs also implies that at the time of its fabrication, the construct is not able to reproduce the physiological functions shown in Table 1, and thus it does not satisfy the BRs. After a transition period for cell differentiation, the construct should be able to fulfil the BRs and thus should be able to replace the organ functions.

Finally, it is important to consider that 3DBP offers an interesting and unique opportunity to print cellular spheroids, without the support of any additional material [Murata et al., 2020]. This possibility has been further explored and developed in a technique, known as Kenzan method, to create hollow tubular structures starting from needle arrays of cellular spheroids [Moldovan et al., 2017]. The absence of structural biomaterials can be seen as a significant advantage in bioprinting where the bioink formulation is challenging. However, the absence of biomaterials also makes the resulting mechanical properties more variable and unpredictable, and the fabrication process is long and complex. This technique has been explored in almost all applications of TERM of tubular organs, as shown in Table 2. While the early focus was mainly on the biological outcomes of cellular spheroids [Itoh et al., 2015], the development of this technique over the years also allowed to improve and further investigate the mechanical properties. Recently, Takeoka et al. [2019] validated this method for the esophagus. They showed that both excellent biological properties and satisfactory mechanical properties could be achieved both in vitro and in vivo.

Impact of the Processing Technique on Material Structure and Geometry

Both MEW and sES are techniques that enable micro- and nano-scale fiber production. Working at the fiber level constitutes a significant advantage in mimicking natural ECM in terms of hierarchical organization and properties. However, the fiber deposition in sES is random (or aligned in the direction of rotation when sES is performed with a high-speed rotating mandrel) [Eslamian et al., 2019; Niu et al., 2019] and cannot be controlled in specific, complex patterns. In this direction, MEW opened a new era by enabling the precise control of fiber deposition and alignment in specific 3D patterns [Jungst et al., 2015; Brown et al., 2016; McColl et al., 2018]. These patterns can direct physiological tissue-like cell organization and differentiation. Of note, cell orientation is important to recapitulate the physiological functions of the different layers, individually and as a whole (Table 1). As an example, when bioengineering blood vessels, it is possible to guide the orientation of smooth muscle cells in order to enable vasodilation and vasoconstriction [Jungst et al., 2019]. This has been studied by Jungst et al. [2019], who guided the cell orientation in the media layer (i.e., smooth muscle cells) by varying the angle of the deposited MEW fibers. As suggested by this study and as shown in Table 4, research on MEW mainly focuses on matching the BRs, but not (yet) on the MRs.

3DBP allows to control the material deposition down to the micron level [Li et al., 2016]. Moreover, the 3DBP approach can rely on cell-mediated matrix remodeling, thanks to the possibility to incorporate cells inside the construct. Matrix rearrangement can require a variable period of initial growth and further maturation in vivo, which may take up to months, to achieve a physiologically relevant construct. Freeman et al. [2019] reported the effect of maturation of a bioprinted vascular construct over 45 days in vitro. Volumetric reduction over time was observed, and histology revealed significant matrix changes and fiber alignment. Interestingly, this correlated with the evolution of mechanical properties. At day 0, the constructs did not fulfil the MRs, such as elastic modulus, burst pressure, and ultimate tensile strength. However, maturation and remodeling allowed to withstand a burst pressure of 1,110 mm Hg, which is a promising result in the cardiovascular tissue engineering scenario.

Some researchers also exploited the possibility given by 3DBP to control the direction of the material deposition to obtain layers with different functions (i.e., permeability, cell interaction), starting from the same material. This way, they demonstrated the possibility to obtain multilayered constructs with layer-specific functions. For instance, Jang et al. [2020] alternated poly (ε-caprolactone) (PCL) and sodium alginate layers to obtain a vascular construct. Diagonal cross-striping of PCL allowed to achieve good nutrient exchange between the layers, while helix deposition ensured protection against blood leakage. A similar approach has been shown also by Bae et al. [2018], but in this case for the generation of a tracheal construct. They used PCL diagonal grid patterns with micro-pores for the exchange of growth factors between cells and the surrounding ambient and helical form without pores to keep the different cell lines separated. Like this, they were able to respect the multilayered structure shown in Table 1, in particular, the epithelial layer separated from the other layers.

Impact of the Processing Technique on Material Properties

When comparing the 3 processing techniques, only sES and 3DBP enable the processing of natural materials [Wang et al., 2020], which is not feasible using MEW because of the high thermal stability required for this technique [Muerza-Cascante et al., 2015]. However, when bioengineering one of the 4 presented tubular organs, sES and 3DBP combine natural with synthetic polymers in order to attain the required mechanical properties [Lee et al., 2008]. Since most of the biological macromolecules are also sensitive to degradation or denaturation at higher temperatures, they are widely processed by sES and 3DBP, and seldom by MEW. The synergistic advantages of combining natural and synthetic materials have been shown by Wu T. et al. [2018a]. They have fabricated a bilayered vascular scaffold by combining a synthetic and natural material, and incorporated biomolecules in them. This way, they achieved better compliance performance than the commercial expanded polytetrafluoroethylene and matched compliance with the human saphenous vein, while promoting rapid endothelialization and attaining a similar organization to the native blood vessel [Wu T. et al., 2018b].

The analysis of the SOTA revealed that PCL is the most used synthetic material for 3DBP, sES and MEW applications, thanks to its low melting point and good thermoplastic properties that make it simple to be processed. Moreover, PCL does not degrade into toxic products, and it has been approved by the Food and Drug Administration (FDA; https://www.fda.gov). The study of Pan et al. [2019] clearly shows that it is possible to tune and optimize the properties of bare PCL to obtain excellent mechanical properties. Similarly, Zhang et al. [2017] combined 2 synthetic polymers, PCL and poly (lactide-co-caprolactone), to comply with the MRs of their engineered urethra. However, in many studies dealing with the use of synthetic polymers, despite the application in animal trials, the MRs were not checked, leaving a big lack of information.

Impact of the Hierarchical Structure and Physiological Functions in the Design of BAOs

Despite the importance of the multilayered organization in tubular organs and its role in organ functions, the SOTA reveals only a few studies reproducing the different layers of native tissues. Many groups focus on a single- or double-layered approach, which clearly cannot satisfy all BRs illustrated in Table 1. It is important to consider the whole life of the tubular construct. It is worth noting that after in vitro maturation or in vivo implantation, cell infiltration and/or differentiation have an impact on the biological properties of the construct. As an example, Kim et al. [2019] obtained 80% of mucosal epithelium regeneration in their tissue-engineered esophagus 2 weeks post-implantation in rats. While at day 0, the BR1 was not satisfied, due to the presence in the construct of MSCs only, the implantation allowed to attain the desired biological characteristics in a relatively short time. However, in vivo implantation may also cause inflammation or stenosis, thus adversely affecting the properties of the construct [Kaye et al., 2019].

When designing a BAO, the complex geometry is one of the fundamental requirements. One of the important innovations brought by 3DBP (and also MEW) is the possibility to design complex geometries through computer-aided design models [Paxton et al., 2020; Sahai and Gogoi, 2020]. This is relevant in TERM, since today’s technology provides tools to convert medical image data into printable information, allowing for the fabrication of patient-specific designs. Ke et al. [2019] were able to design a trachea based on a CT scan from human patients. This combined with the use of human MSCs, which can be used as an autologous cell source, constitutes the proof-of-concept for clinical translation.

Impact of the Synergetic Combination of Multiple Processing Techniques for BAO Design

An interesting approach is the combination of 2 different techniques, in a multistep process for the final tubular construct fabrication. In this context, the sES and 3DBP techniques have been combined for optimal mechanical and biological properties. Chung et al. [2018] focused on the improvement and control of mechanical performance of their artificial esophagus. They 3D printed sequential reinforcement rings of PCL, which were then combined with a tubular electrospun PCL layer. This allowed increasing the mechanical properties, while keeping a good structure for cell infiltration. Kim et al. [2019] combined electrospun PU nanofibers in the inner layer with 3D-printed PCL strands in the outer layer. The hypothesis of the study was to provide topographical cues for the mucosal layer on the inner part and to give mechanical strength and flexibility to the external layer, thus achieving both biological and mechanical good performance. sES has also been combined with MEW. In this regard, Pennings et al. [2020] used this combination with the aim to induce and maintain multiple cell phenotypes within a biomimetic structure. The sES was used for a randomly oriented layer on the luminal side, whereas the deposition of oriented MEW fibers served as a guidance for MSCs. This way, they have succeeded in inducing layer-specific cell differentiation with a blood-vessel native-like cell organization.

In vivo Studies Involving Tubular BAOs

Several works reported in vivo testing with animal models, both on 3DBP and sES-based constructs. As a general trend, the goal of in vivo testing was to assess the biological response to the tubular construct implantation, while mechanical properties after implantation were rarely reported. The animal model was generally selected based on the tubular organ to be implanted, regardless of the used fabrication technique, i.e., rabbit for trachea.

As example, Gao et al. [2019] performed a complete biological characterization of a 3D bioprinted vessel after implantation in a rat model. In this study, all 3 BRs for bioengineered blood vessels were validated, as reported in Table 1. Ultrasonography was used to assess the non-thrombogenicity and immunohistochemistry to check the multilayer composition and the endothelium integrity. They showed a great potential of the co-axial nozzle technique for the fabrication of artificial vessels. As in this study, in general, immunohistochemistry was widely used by all research groups to assess the biological properties after explantation.

When looking at the SOTA of sES-based constructs for tubular BAO (Table 3), it can be concluded that most research was mainly focused on the study of either biological or mechanical properties. Wu et al. [2017] studied the effect of cell-seeding and pre-vascularization on their bilayered tubular construct in a rat model. Based on this in vivo evaluation, they concluded that pre-cellularized and pre-vascularized constructs resulted in higher capillary regeneration, and in lower immunogenicity, while improving tracheal tissue regeneration. However, they did not assess the mechanical performances. Nevertheless, in some recent studies, research groups have started exploring both biological and mechanical performances. Townsend et al. [2020] mainly focused on studying the BRs in depth in a rabbit model, but in addition, they also started exploring some of the mechanical properties required to design a functional BAO. The explanted tracheas were studied for the lumen volume, minimum cross-sectional area and the tracheal patency, enabling better fine-tuning of the developed tubular constructs for future studies.

As shown in Table 4, no in vivo testing has yet been reported on MEW-based tubular constructs, due to the very recent introduction of this technique. Research is currently focusing on attaining more in vitro insights, before being able to step into the animal trial phase.

In conclusion, there are important consequences considering the intrinsic correlation between (i) the construct requirements to meet, i.e., the MRs and BRs (depending on anatomy and physiology) and (ii) the resulting properties obtained (depending on the fabrication process), i.e., the mechanical and biological properties of the final construct.

Clinical Translational Potential for Tubular Constructs Processed by 3DBP, sES and MEW

As previously stated, in a scenario in which heterologous organ transplantation is burdened by the shortage of donor tissue and currently available synthetic grafts show issues in terms of biological and mechanical properties (especially on the long term), bioengineered artificial tissues certainly represent a viable solution. The development of physiologically relevant tubular tissues for regenerative medicine purposes can be used to correct defects, restore functions, or substitute damaged tissues in patients suffering from life-threatening conditions [Holland et al., 2018].

Tissue engineering-based constructs, in their journey from the lab bench to clinical use, are subjected to strict regulation. As stated by the U.S. FDA, the process of development for new medical products and devices can be divided in 5 stages: (1) discovery and concept; (2) preclinical research, comprehensive of in vitro and in vivo testing, and prototype; (3) pathway to approval; (4) FDA device review, and (5) FDA post-market device safety monitoring (U.S. FDA). sES and 3DBP to design, develop and optimize tubular organs have already been reported, while MEW, despite its novelty, is rapidly gaining attention in this field (Tables 2, 3, 4). Interestingly, contrarily to more conventional tissue engineering strategies such as decellularization [Elliott et al., 2012; Gonfiotti et al., 2014], all hereby presented studies are at the preclinical research level according to the FDA subdivision.

The current advanced TERM strategies (such as 3DBP, sES, and MEW) are still affected by some limitations that impeach their successful translation into clinic. Despite the promising results and achievements obtained in the past years, the produced devices are still hampered by a mismatch in functionality (both at the mechanical and biological level) with the native tissues they are intended to substitute [Holland et al., 2018]. Hunsberger et al. [2016] reported that major drawbacks in the clinical transfer of advanced TERM strategies are related to the precise mapping of cells in the developed tissues (their placement, organization, phenotype, and function), reliable sources for cells, immunosuppression, prosthetic tissue integration with the host and vascularization.

Finally, these new technologies evolve in a specific and precise regulatory structure allowing the scaling-up and marketing of tubular BAOs [Mason et al., 2016; Holland et al., 2018]. Although regulatory processes may appear to limit their development, which might be true in some cases, it should also be noted that this constitutes a unique moment for regenerative medicine specialists, including scientists, engineers, industrials, and clinicians, to seed the basics of future regulations.

Regulating a new BAO is a long and complex procedure, which requires time, investment, and collaborations. On the one hand, the International Standards Organization (ISO) has to be involved, mainly because quality control will require testing and evaluation of the final products. ISO is open to extend and add new standards, specific to testing and assessing the mechanical performance, the stability, and the degradability of tubular BAOs. On the other hand, contrarily to what is (sometimes) mentioned in some manuscripts, FDA does not approve biomaterials, nor processes. The FDA is responsible for protecting public health by regulating medical devices (and a panoply of other industrial products, including drugs, tobacco products, food for humans and animals, cosmetics, and radiation-emitting electronic products). Future commercialized BAOs, after having been developed and fully tested in laboratories, must be proven safe and effective to FDA’s satisfaction before companies can market them in the interstate American commerce. Future manufacturers must also prove they are able to make the product according to federal quality standards. The FDA does not develop or test products before approving them. Instead, FDA experts review the results of laboratory (in vitro), animal (in vivo), and human preclinical and clinical testing done by the manufacturers. If FDA grants an approval, it means the agency has determined that the benefits of the product outweigh the known risks for the intended use. FDA, and all other country-specific regulatory bodies, will require to be convinced that the proposed BAOs will not present risks for its population. An interesting example is constituted by the recent effort between FDA and the National Institute of Standard Technology, for the collaboration on standards development activities supporting innovation and translation of regenerative medicine products [Arcidiacono et al., 2018]. Standards development can accelerate product development cycles and broaden market opportunities in innovative fields such as regenerative medicine. Standardization provides a forum for the convergence of diverse scientific approaches; standardized approaches to address common scientific challenges can enable broader application of innovative products without stifling continuing innovation. Standardization efforts made by national standards regulatory bodies, industry, and academia can lead to international harmonization and global marketing of regenerative medicine products. Regulation and standardization, together have the potential to facilitate the development and the translation of regenerative medicine products, such as BAOs.

Despite the above considerations, the advancements achieved at the preclinical level by the above-detailed strategies, and the rapid development of processing we witnessed in the last decade, foresee that the gap separating them from the clinic will shortly be filled. In particular, we are convinced that the clinical translational potential of 3DBP of degradable scaffolds with living (including autologous) cells is unique and very high. 3DBP clinical translation would open the era of personalized medicine. For example, from medical images acquired from the patient during the preoperative diagnostic phase, a 3DBP-personalized process could be implemented for developing the required BAO to regenerate the diseased tissue or organ. If on one side this constitutes a confined application, it is on the other side important to highlight the high impact that this would have in some specific clinical cases. The clinical translation potential of sES and MEW for polymeric scaffolds (not cellularized at the time of implantation but able to attract and interact with a patient’s surrounding cells all along the implantation time) will be in high demand for local and long-term support for hollow tubular BAOs partially affected by localized diseases (i.e., cancers or inflammatory processes).

Injury, diseases, and malfunctioning of hollow tubular organs represent a unique challenge for bioengineers and clinicians. A multidisciplinary approach needs to be applied in order to successfully develop functional bioartificial organs. The main efforts in addressing the challenge are summarized in the following key points:

i.The MRs and BRs should be the dictating factors during the design phase of a BAO, being the key point to address the anatomical i. structure and physiological functions. This is true for all tissues and organs, but it is particularly challenging in the case of tubular ones, due to the complex hierarchical structure;

ii.Construct cellularization is a key point for replacing diseased or damaged tissues and organs. On the one hand, 3DBP enables the incorporation of cells directly in the construct. On the other hand, sES and MEW rely on post-processing seeding or on cell migration and infiltration after implantation. In both cases, cell integration and cell-mediated remodeling are fundamental for a successful outcome of engineered BAOs;

iii.The main advanced techniques for the fabrication of tubular BAOs are 3DBP, sES, and MEW. Although they are not all at the same level of technological maturity, they all have the potential for clinical translation. While 3DBP presents the unique advantage to process materials and cells together, this also raises the question of which cell source to use to ensure the best outcome. Autologous outsourcing of cells looks like an attractive possibility, but its clinical feasibility for personalized medicine remains low, due to possible auto-contamination issues, regulatory processes, and ethical concerns. 3DBP, sES, and MEW all present unique advantages to process materials leading to high reproducibility at the micrometric level, nano- and microfibers production mimicking the ECM, and precise spatial deposition at fiber level, respectively;

iv.In the current research on the fabrication of functional tubular BAOs, there is a missing link that focuses on the correlation between (i) the MRs and BRs of the construct design dictated by the anatomical structure and physiological functions, (ii) the fabrication process, and (iii) the resulting mechanical and biological properties of the developed tubular BOA. Even though the development of functional tubular BAOs using the presented processing techniques is still at the preclinical level, the advancements in the last decade look promising and speculate great potential for clinical translation.

The authors have no conflicts of interest to declare.

The work of N. Pien was supported by a Vanier Canada Graduate Scholarship. P. Dubruel and S. Van Vlierberghe would like to acknowledge the financial support of the Research Foundation Flanders (FWO) under the form of research grants. D. Mantovani would like to acknowledge the continuous support by the Natural Science and Engineering Research Council of Canada, and the contribution of the Fonds de Recherche du Québec sur les Natures et Technologies, and the Canada Foundation for Innovation.

Literature search and SOTA: Nele Pien, Sara Palladino, Francesco Copes. Writing – Original draft: Nele Pien, Sara Palladino, Francesco Copes, Diego Mantovani. Writing – Reviewing and editing: Nele Pien, Sara Palladino, Francesco Copes, Gabriele Candiani, Peter Dubruel, Sandra Van Vlierberghe, Diego Mantovani. Finalizing manuscript: Nele Pien, Sara Palladino, Francesco Copes, Diego Mantovani.

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