Sys Rev Pharm 2021; 12(8): 477-483 Review Article

A multifaceted review journal in the field of pharmacy

E-ISSN 0976-2779 P-ISSN 0975-8453

3D Bioprinting: Print the Future of Periodontics

Thamarai Chandrasekharan*, M Prem Blaisie Rajula, PL Ravi Shankar, Rajarajeswari
Department of Periodontics, SRM Dental College, Chennai, India

Article History: Submitted: 17.06.2021 Accepted: 01.07.2021 Published: 08.07.2021

ABSTRACT Every method has their own pros and cons, hence hav-
ing a detailed knowledge of the method aids in impro-
3D Bioprinting is a pioneering technology in the field
vising the techniques further. In summary, we have a
of regenerative medicine that enables the fabrication of
detailed discussion of this 3D bioprinting technology
living tissues using the living cells by the printing pro-
in this review and additionally, it throws light on using
cess. Since, periodontitis has become more prevalent
various bioprinting strategies and materials to improve
disease among the population; there is a need for in-
the field of periodontal tissue engineering further in our
creased periodontal regenerative procedures to restore
clinical practices.
normal healthy periodontium for the patients. Regener-
ative procedures require placement of tissues that are
biocompatible, bioresorbabale, promotes cell growth Keywords: Bioprinting, Bioinks, Methods, Periodonti-
and proliferation in restoring the defect. Such struc- tis, Regeneration, Tissue engineering
tures can be made from this 3D bioprinting technolo-
gy which uses several bioinks and various bioprinting
methods such as autonomous self-assembly, extru- *
Correspondence: Thamarai Chandrasekharan, Depart-
sion-based, laser bioprinting etc., to print the tissues. ment of Periodontics, SRM Dental College, Chennai, In-
dia, E-mail: [email protected]

INTRODUCTION materials such as nanocomposites, blended plastics and pow-

Technology has slowly and steadily paved its way into dentistry. dered metals.
Researchers are constantly working to integrate technology into The researchers at Wake Forest Institute for Regenerative
dentistry. Of all the latest technological innovations in dentist- Medicine [WFIRM] made a synthetic scaffold of a human
ry, the most talked-about innovation is three-dimensional (3D) bladder using the 3D bioprinting technology in the year 2000
bioprinting. 3D Bioprinting is a cutting-edge technology in the (Atala A, 2001). In the process of synthesis of the scaffold,
field of regeneration that facilitates the fabrication of multiscale, they used the recipient’s host cells to overcome the problem of
biomimetic, multi-cellular tissues with highly complex tissue mi- host rejection. After 10 years of implantation, the patient had
croenvironment, intricate cytoarchitecture, structure-function no serious complications. In 2002, again at WFIRM, a team
hierarchy, and tissue-specific compositional and mechanical het- of scientists led by Professor Anthony Atala undertook a bio-
erogenicity (Vijayavenkataraman S, et al., 2018). Since, periodon- printing project of a miniature functional kidney capable of
titis has become more prevalent disease among the population; filtering blood and producing urine in an animal model. Then
periodontal regenerative procedures are needed to restore a nor- in 2003, Thomas Boland, a scientist from University of El Paso,
mal healthy periodontium. The 3D bioprinting technology allows invented his own designed 3D bioprinter, which uses bioinks
the fabrication of such structures, which use several biomaterials to print live tissues (Mironov V, et al., 2003). In 2004, Dr. For-
and various bioprinting methods (Murphy SV and Atala A, 2014). gacs made his debut with his own bioprinter, which during his
This review article discusses about 3D bioprinting and provides uprising caused a great change in the scientific community. It
little information about the technology behind 3D printers. It also was the first device that allowed 3D direct biodegradation i.e.,
throws light on using various bioprinting strategies and materials using live cells without the need to build scaffolding (Jakab K,
most often used in 3D printed scaffolds for periodontal regener- et al., 2004).
ation. In 2006, Noble Prize winner Dr. Shinya Yamanaka discovered
LITERATURE REVIEW that mature cells acquired from cultures can be reorganized
again to a stem cell state (Takahashi K and Yamanaka S, 2006).
History of 3D bioprinting This created a revolution in the field of regenerative medicine
Bioprinting is a technique that is used to design complex bio- and also in 3D bioprinting. In 2009, one of the first commer-
logical structures using bioinks. Before gaining an insight on cial Bioprinters from Organovo-NovoGen MMX was created.
the 3D bioprinting of the periodontium, it is important to They aimed at “scaffold-free” printing process. In 2010, Orga-
understand the evolution of 3D bioprinting in the medical novo-the Bioprinting Company printed the first blood vessel
field. After the invention of Stereolithography by Hull CW in and today the revolution continues on.
1983, the concept of printing human organs was developed
(Hull CW, 1984).
Three-dimensional bioprinting
As the term bioprinting implies, that process involves the
Earlier, the machine discovered by Hull used UV lasers to en-
printing of living tissues. This is done using a 3D bioprint-
grave the layers of acrylic into shapes, which are then stacked
ers that uses a computer-aided design model. In this model
to form objects. The major drawback was that the printer uses
bioinks are layered through an additive manufacturing process
written codes to engrave the acrylic, so only simple shapes
to create tissues that mimic the natural tissues (Murphy SV
were created. Later in 1986, Hull discovered the 3D technol-
and Atala A, 2014).
ogy of printing and also designed the materials that go into the
printers (Hull CW, 1984). In the 1990s, the 3D systems were Bioprinting approaches
used to fabricate dental implants and custom prosthetics using The approaches in 3D Bioprinting are: Biomimicry, Autono-

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 Chandrasekharan T: 3D Bioprinting: Print the Future of Periodontics

mous self-assembly and Mini-tissue building blocks. Types of 3D bioprinters

Biomimicry: This is one of the prime approaches in bioprinting, where 3D bioprinters are the machines that operate through various mechan-
the structures are created similar to the natural tissues that are found isms such as Direct light processing, Fused deposition modeling, Inkjet
in humans. They are useful in making similar cellular as well as extra- printing, Extrusion based printing and Laser assisted printing were in-
cellular tissues as found in humans. It involves the synthesis of bio- vented as depicted in Figure 1 . In this review, we discuss only on the
logical tissue using the synthetic materials that mimic biological func- most widely used bioprinter technologies in current practice.
tions (Atala A and Yoo J, 2015). Inkjet-based bioprinting:This was the first attempt in bioprinting. In
Autonomous self-assembly: This is the second approach in bioprint- this method of bioprinting, the data from computer is fed to printer
ing. The basic idea of self-assembly is derived from the concept of and it reproduce onto the substrate using ink drops as a non-contact
embryogenesis and organogenesis where the cells proliferate to their technique (Murphy SV and Atala A, 2014). These printers are of three
tissues of interest based on signaling molecules, creating their own types-thermal, piezoelectric and mechanical. The cartridge is filled
extracellular matrix as a foundation for the cell replication. The main with bioink and during the process they are forced through microflu-
advantage is that it is scaffold-free. Some of the shortcomings faced by idic reservoir to an output nozzle. The initial problem involved during
scaffold-based systems are immunogenicity, maladaptation, etc (Atala the printing process was that the cells died during printing due to im-
A and Yoo J, 2015). mediate drying out of the substrate. This was overcome by encapsulat-
Mini-tissue building blocks: This is the third approach in bioprint- ing the cells in a highly hydrated polymers-hydrogels. In thermal inkjet
ing. This includes both the techniques of biomimicry and autonomous printers, the printhead is heated by an electrical heat which produces
self-assembly, where the structures are constructed from mini func- pressure to force the bioink from the nozzle (Cui X, et al., 2010). In
tional tissue components, thereby organizing them into a larger struc- piezoelectric inkjet printers, when a voltage is applied to the piezoelec-
ture of required characteristics (Thomas D and Singh D, 2019). tric material it changes shape and produces acoustic waves to force the
bioink into droplets at regular intervals (Visser J, et al., 2013). In mech-
anical inkjet printers, application of pressure forces the bioink from the
nozzle (Tekin E, et al., 2008).
Table 1: Various bioinks that are used in the 3D bioprinting process (Gopinathan J and Noh I, 2018)

Bioinks Description Advantages Disadvantages

Agarose It is a marine polysaccharide taken Due to its gel forming property has Provides limited support to cell
from seaweed. a wide range of use in biomedical growth.
field.
The disaccharides D-galactose and Has good mechanical strength. Poor cell adhesion. Non degradable.
3,6 anhydro L-galacto pyranose Biocompatible.
forms the backbone of this agaro-
biose.
Alginate It is a natural polymer derived Has a good gel forming property It has slow degradation kinetics.
from brown algae. Also known and a good flexural strength. They Poor cell adhesion.
as algin or alginic acid. Com- imbibe water and other molecules
posed of monomers such as alpha by capillary forces enabling cell
L-guluronic acid and (1-4) beta D growth.
mannuronic acid.
Chitosan It is a cationic polysaccharide which Highly biocompatible. Anti-bac- Has a slow gelation rate.
is derived from natural biomaterial terial properties. Bio degradable.
chitin found in the cells of shrimp Forms stable hydrogels with good
and other crustaceans. cell affinity, mechanical strength.
Collagen It is the main structural protein Has good biomimetic property. Has poor mechanical property,
component of the extracellular ma- Biocompatible. It allows cell remod- hence need to be crosslinked with
trix. Found in skin and connective eling. other biomaterials.
tissues.
Fibrin Fibrin is synthesized from fibrin- Good biocompatibility. Biodegrad- Has a weak mechanical property.
ogen by enzymatic action with able. Has a limited printability.
thrombin. It is a protein found in
blood.
Cellulose It is a polysachharide obtained from Has improved cell viability. Bio- Lack of shear thinning property
cellulose. CMCs are used as hy- compatible. Blending with bioglass and structural shrinkage on drying.
drogels by modifying their cellular it has good mechanical property.
properties.

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 Chandrasekharan T: 3D Bioprinting: Print the Future of Periodontics

Silk Silk fibroin is a natural biopolymer Used in digital light processing Application of high shear forces
extracted from Bombyx mori. printing method. Spider silk has a causes change in conformation
good mechanical strength. It has before the extrusion printing.
good printability and keeps mesen-
chymal stem cells viable.
Gelatin It is a protein based natural It is biocompatible. It is water sol- Poor shape fidelity. It has limited
biomaterial obtained from partial uble. It has good flowable property rigidity.
hydrolysis of collagen. when blended with other bioinks.
Graphene Graphene is an allotrope of carbon 3D graphene composed of more Susceptible to oxidative environ-
in form of single layer of atoms in a than 90% graphene is flexible, ments. Quite toxic in nature. Low
2D hexagonal lattice. conductive and a biocompatible biological relevance.
material.
Hyaluronic acid It is a natural biomaterial usually Increases the proliferation of cells. Has low mechanical strength and
found in cartilages and connective High concentration increases cell has slow gelation property.
tissue. viability and stability.
Decellularis-ed ecm Decellularised ECM is obtained It keeps the cells viable and pro- Production cost is higher as com-
from native tissues by removal of vides good functionality. pared to the other hydrogel bioinks.
cells in sequential steps leaving the
ECM intact.
Hydroxy-apatite Natural biomaterial found in teeth Provides high strength and rigidity. It offers low printability and limited
and bones. tissue specificity.
Cell aggregates Spherical cell aggregates as spher- They promote good cell prolifera- Low resolution and limitations in
oids are used as a bioink for the tion, differentiation and cell migra- tissue thickness.
3D printing process. These cell tion. They maintain cell viability.
spheroids are laid in layers to form
scaffold and they fuse by self-as-
sembling process.
PCL/PLA/ PLGA These are thermoplastic synthetic PCL-it has increased flexibility in Low cell adhesion and low cell
biomaterials. PCL-Polycaprolactone drug delivery and used as scaffold proliferation.
biodegradable polyester. They are for 3D printing.
hydrophobic and semi crystalline in
nature. PLA-Polylactic acid is ther- PLA-it is biodegradable, biocom-
moplastic which is both amorphous patible and it is easy to process.
and crystalline in nature. Easily metabolized in the body.
PLGA-being used as a effective
copolymer with PLA.

Figure 1: Methods of 3D bioprinting-a) Thermal and piezoelectric mediated inkjet printer, b) Micro-extrusion printer, c) Laser-as-
sisted printer (Malda J, et al., 2013)

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 Chandrasekharan T: 3D Bioprinting: Print the Future of Periodontics

Micro-extrusion bioprinting: In this method, the printer comprises The living cells used in 3D printing require specific aqueous en-
of a fluid dispensing system and an automatic robotic system for the vironment to maintain the cellular functions at appropriate pH, for
process of extruding the liquid and bioprinting the structure. This sys- key nutrients and oxygen diffusion, to create an extracellular matrix,
tem comprises of either a pneumatic or screw-driven or piston or a non-toxic environment and to allow printed cells to form new tissue.
solenoid-based system. The piston and the screw driven systems works Such environment is provided by the materials known as hydrogels
mechanically to exhibit pressure necessary to eject the bioink whereas (Chimene D, et al., 2020). Hydrogels are made from extracellular ma-
the pneumatic system employs a pressured air for the process (Visser J, trix components like collagen, hyaluronic acid that enables stem cell
et al., 2013). This is a promising technique to create biomimetic struc- growth. Since, hydrogels are in liquid polymer state, they are insuffi-
tures (Chang R, et al., 2008). The main advantage of this process is its cient to support successive cell layering during the printing process; to
ability to print using bioinks with high cell densities (Murphy SV and overcome these limitations, newer techniques are used to strengthen
Atala A, 2014). The drawbacks are its limited resolution; require high the hydrogels such as nanocomposites, supramolecular bioinks, inter-
pressure for extrusion of low viscous bioinks which can lead to cell penetrating networks, polymer functionalization and thermoplastic
death (Nair K, et al., 2009). reinforcement (Shafiee A and Atala A, 2016). The detailed descriptions
Laser-Assisted Bioprinting (LAB): In this method a laser is used for on various bioinks are given in Table 1.
deposition of bioink on the substrate. The laser pulses are directed Steps in 3D bioprinting
through a ‘ribbon’ containing bioink and this ribbon is supported by
Pre-bioprinting: It is the first step in the process where the structure to
titanium or gold layer which absorbs and transfers energy to ribbon
be printed is designed and modeled as a 3D structure using the Com-
(Gruene M, et al., 2011). The bioink and cells are suspended on bottom
puted Tomography (CT) and MRI scans. Every fine detail is recorded
of the ribbon and when vaporized by laser pulse, they create a high
and tomographic reconstruction done on the images so that it is print-
pressure bubble which exerts a pressure on the biomaterial thereby for-
ed in a layer by layer fashion (Williams J, 2014) as shown in Figure 2.
cing the liquid towards the substrate. The Laser Assisted Bioprinting
Later, the bioinks are prepared by isolation from living tissues and they
(LAB) is a scaffold free technique; deposits biomaterials at high reso-
are allowed to multiply.
lution. Since, it is a nozzle free method; they eliminate the drawback
of biomaterial clogging. It is well-suited for bioinks with varying range Bioprinting: It is the printing process where the designed structures
of viscosities. The main disadvantage of LAB is that the presence of has to be printed using the printers. Here the bioinks are introduced
metallic absorbing layers produces metallic residues on the structure to the printer cartridges and based on the digital model the cells are
formed; also LAB is very expensive (Murphy SV and Atala A, 2014). accumulated in a layered fashion (Ozbolat IT, 2015).
Bioinks Post-bioprinting: Post-bioprinting process involves maintaining
mechanical integrity and function of the 3D printed structure (Wil-
As bioprinting is the process that involves printing of living tissues,
liams J, 2014). They control the remodeling and the growth of tissues
the printer essentially requires a bioink to print the tissues. Therefore,
by sending signals and recently, evolution of bioreactor technologies
bioinks are materials that are required to print the living tissues. The
have caused rapid tissue maturation, vascularization of tissues and in-
important properties of bioink should be biocompatible, non-toxic,
creased the survival rate of the transplants (Obregon F, et al., 2015).
printable, able to withstand mechanical stresses, good shape memory,
Depending on the type of tissue, the bioreactors differ. The steps are
ability to get nourishment from cells and enhance the metabolic activ-
summarized in Figure 3.
ities of the cells (Gopinathan J and Noh I, 2018).The bioinks are usually
comprised of natural polymers, synthetic polymers or combination of
both.

Figure 2: Represents the layering of cells during the process of bioprinting (Yeong WY and Chua CK, 2014)

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 Chandrasekharan T: 3D Bioprinting: Print the Future of Periodontics

Figure 3: The flowchart depicts the individual processes that are involved in the bioprinting process

Applications of 3D bioprinting in periodontics bioprint the structures accurately. However, the use of additive manu-
In dentistry, there is emerging use of this 3D bioprinting technology facturing technology enables printing of structures with good mechan-
for its diverse applications and it proves to provide successful treat- ics and accurate porosities as they enable the use of line spacing, line
ment options for the patients (Patel R, et al., 2017). In this article, we thickness and resolution changing features (Rasperini G, et al., 2015).
briefly discuss on the periodontal complex regeneration in the field of In a case study done by Rasperini G, et al they used a 3D printed bio-
periodontology. resorbable scaffold in treatment of a periodontal defect and this was
In periodontology, the periodontal tissues have a complex organization the first application of a personalized 3D printed scaffold in the field
which requires multilayered biomaterial constructs to restore the struc- of periodontics (Asa’ad F, et al., 2016). But to our catastrophe, this case
tural and functional integrity at the bone-ligament interface (Vaquette was a failure at the end of 13th month, which led to surgical removal
C, et al., 2018). Periodontitis, an inflammatory disease in response to of the scaffold. This was because the researchers used only PCL which
periodontal pathogens affects the periodontium causing destruction of caused wound dehiscence due to slow tissue degradation rate and led
the tissues (Gaviria L, et al., 2017). Therefore, the need for periodontal to unsuccessful tissue regeneration due to its inferior cell affinity (Aus-
regeneration procedures is increasing. Hence, many clinical researches enda F, et al., 2019). Therefore, the scientists came to a conclusion that
are ongoing in the field of 3D bioprinting to restore the lost periodontal they should use bioinks with faster resorption rate or the PCL should
structures for the individuals suffering from periodontitis. The peri- be incorporated with long standing devices like the titanium screws
odontium structures are quite complex in morphology and they re- (Carrel JP, et al., 2016). But this is strongly believed that this study has
quire special technical knowledge in the printing process. paved the way for further research in field of oral regenerative medi-
cine for improved personalized 3D bioprinted structures.
Since the periodontal structures exhibit different porosities and
strength as shown in Figure 4 , it requires more precise technology to

Figure 4: It represents the difference in strength and porosities of the cementum, periodontal ligament, and the alveolar
bone respectively (Rasperini G, et al., 2015)

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 Chandrasekharan T: 3D Bioprinting: Print the Future of Periodontics

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