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Printed in the United States of America Vol. 11, 1–6, 2017

REVIEW
Impact of Nanotechnology on 3D Bioprinting
Deepti Rana1 , T. S. Sampath Kumar2 , and Murugan Ramalingam1
3
∗
1
Centre for Stem Cell Research (CSCR), A Unit of Institute for Stem Cell Biology and Regenerative Medicine, Bengaluru;
Christian Medical College Campus, Vellore 632002, India
2
Medical Materials Laboratory, Department of Metallurgical and Materials Engineering,
Indian Institute of Technology Madras, Chennai 600036, India
3
World Premier International Advanced Institute for Materials Research, Tohoku University, Sendai 980-8577, Japan

Three-dimensional (3D) bioprinting is an additive manufacturing technique that have shown tremen-
dous potential in fabricating customized patient-specific tissue scaffolds and medical devices for
various biomedical applications, in particular, tissue engineering and regenerative medicine. Owing
to its new capabilities such as high speed, fine resolution and design specificity, this evolving tech-
nology has excited various fields of biomedical engineering as well as translational medicine. In the
recent years, the combination of nanotechnological principles and nanomaterials with 3D bioprinting
techniques has shown tremendous increase in the clinical efficacy of 3D bioprinted tissue engi-
neered scaffolds. Nanotechnological approach and nanomaterials due to their high surface area
to volume ratios and quantum confinement effects, shows unique physical, chemical and biologi-
cal properties. However, on combining nanomaterials with 3D bioprinting techniques improved 3D
bioprinted scaffolds with enhanced physicochemical as well as biological properties have been
fabricated. In this article, we discuss briefly about the impact of nanotechnology, and nanomateri-
als, on 3D bioprinted tissue engineered scaffolds for tissue engineering and regenerative medicine
applications.
Keywords: Nanotechnology, 3D Bioprinting, Biomaterials, Stem Cells, Tissue Engineering.

CONTENTS translatable tissues and organs.2 The important factors that

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2. 3D Bioprinting: An Overview . . . . . . . . . . . . . . . . . . . . . . . . . .
3. Impact of Nanotechnology on 3D Bioprinting . . . . . . . . . . . . . .
4. Application of 3D Bioprinted Nanomaterials . . . . . . . . . . . . . . .
5. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References and Notes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. INTRODUCTION
3D bioprinting is an additive manufacturing technology
that creates cell patterns in a confined space where cell
function and viability are preserved within the printed
scaffold. 3D bioprinting could fabricate 3D structures
by building up material, layer-by-layer, with guidance of
a digital design.1 Technological advancements in recent
years have enabled 3D bioprinting of biocompatible mate-
rials, cells and supporting components into complex 3D
functional living tissues. Due to its design reliability,
specificity and ability to design customized structures,
3D bioprinting have been applied to tissue engineering and
regenerative medicine to address the need for clinically
∗
Author to whom correspondence should be addressed.
1 governs the success of 3D bioprinting are choice of mate-
3 rials, crosslinking mechanism, extrusion technique, cell
4
types, growth and differentiation factors, sensitivities of
5
5 living cells and the construction of tissues.3 Each factor
5 supports a particular range of control over matrix architec-
5 ture, mechanical, degradation and biological properties.3
3D bioprinting technology has been used for the genera-
tion of various transplantable tissues such as multilayered
skin, bone, vascular grafts, tracheal splints, cardiac tissues
and cartilaginous structures.4 For instance, Lee et al. com-
bined stereolithography and electrospinning techniques to
fabricate novel 3D biomimetic neural scaffold with tun-
able porous structure and embedded aligned fibers.5 By
employing two different types of biofabrication tools, both
synthetic and natural materials with varying chemical com-
position were able to achieve enhanced biocompatibili-
ties and mechanical properties in the final scaffold. The
resultant microfibers composed of polycaprolactone (PCL)
polymer and PCL mixed with gelatin were embedded in
3D printed hydrogel scaffold showed enhanced neural stem
cells adhesion and proliferation when compared to those
without the fibers.5 Additionally, an increase in average
neurite length and directed neurite extension of primary

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 Impact of Nanotechnology on 3D Bioprinting Rana et al.

cortical neurons along the fibers was also observed.5 instance, Lee et al. reported a novel method to fabri-
The other applications of 3D bioprinted products include cate a free-standing nanowall by the precise and repetitive
developing high-throughput 3D-bioprinted tissue models deposition of electrospun polymer nanofibers.6 The elec-
for cell screening, drug screening and toxicology. For trified nanojet was stably focused onto the microline of

Deepti Rana is a Research Fellow at the Centre for Stem Cell Research, Christian Medical
REVIEW

College Campus, Vellore, India and currently pursuing her research work in the field of
Stem Cell Nanotechnology. Her current research interests include the development of multi-
scale (nano to micro to macro) biomaterials for the translational stem cell research, stem
cell nanotechnology, tissue engineering and nanomedicine. She has published her research
work in several peer-review journals, book chapters and conferences. She has received the
best paper awards for her research work. Four of her articles’ figures have been highlighted
as the journal cover page. She is a reviewer of several eminent journals such as Journal of
Biomaterials and Tissue Engineering, Journal of Nanoscience and Nanotechnology, Journal
of Bionanoscience and Global Journal of Nanomedicine. She is also an Editorial Board
Member of the Journal of Nanotechnology and Materials Science (Ommega Publishers,
USA) and Journal of Nanotechnology and Nanoscience (Kenkyu Group, India).
T. S. Sampath Kumar is Professor and Head of Medical Materials Laboratory, Department
of Metallurgical and Materials Engineering at the Indian Institute of Technology Madras. He
received his Ph.D. in materials engineering from Indian Institute of Science, Bangalore in
1986. His current research areas are nanostructured biomaterials, antimicrobial ceramics and
delivery systems, injectable bone cements and value added biomaterials from natural wastes.
He is a Fellow of the Society for Biomaterials and Artificial Organs India (SBAOI) and
of International Medical Sciences Academy (IMSA). He received 1994 University Grants
Commission Career Award, Dr. Uma and Dr. B. C. Bansal International Oration 2015 of
IMSA and his research guidance is marked by many best thesis, journal best paper and best
presentation and project awards. He has also co-authored a book “Biomaterials: A Nano
Approach” published by CRC Press He has published more than 125 papers in peer reviewed
journals with many papers having well over 100 citations, 3 book chapters and edited 4 conference proceedings in
journals. He has 3 (5 filled) Indian patents to his credit. He is the Associate Editor of Biomaterials, a Frontiers Journal
and Editorial Board Member of many biomaterial journals.
Murugan Ramalingam is Professor at the Centre for Stem Cell Research (a unit of the
Institute for Stem Cell Biology and Regenerative Medicine-Bengaluru), Christian Medical
College Campus, India. Concurrently he is Adjunct Professor at the Tohoku University,
Japan. Prior to joining the CSCR, he was Associate Professor of Biomaterials and Tissue
Engineering at the Institut National de la Santé et de la Recherche Médicale, Faculté de
Chirurgie Dentaire, Université de Strasbourg, France. He has worked at the WPI Advanced
Institute for Materials Research, Japan, as an Assistant Professor. He has also worked at the
National Institute of Standards and Technology (NIST) and the National Institutes of Health
(NIH), under the U.S. National Academies Associateship program. He received his Ph.D. in
Biomaterials from the University of Madras. He has also undergone training in Ethical and
Policy issues on Stem Cells from Harvard University, USA, and in Operations Management
from the University of Illinois-Chicago. His current research interests are focused on the development of multiphase
biomedical materials, through conventional to nanotechnology to biomimetic approaches, microfabrication, cell patterning,
stem cell differentiation, tissue engineering and drug delivery. He is the author of ∼300 publications, including peer-
reviewed journal papers, conference proceedings, book chapters, authored books, edited books, and patents relevant to
biomaterials, stem cells, and tissue engineering. His current h-index is 30 with ∼7000 citations. He has organized several
international conferences and chaired Biomaterials, Nanobiotechnology, Stem Cells and Tissue Engineering sessions.
He also serves as a board member of several international scientific and research committees in various public and
private bodies and grant reviewer of various international funding agencies. He serves on the editorial boards of multiple
biomaterials and tissue engineering-related journals, including the Editor-in-Chief of the Journal of Biomaterials and Tissue
Engineering and the Journal of Bionanoscience. He is a recipient of several prestigious fellowships and awards, including
CSIR Fellowship (India), SMF Fellowship (Singapore), NRC National Academies Fellowship (USA), Nationale Professeur
des Universités (France), Fellow of Institute of Nanotechnology (UK) and Fellow of Royal Society of Chemistry (UK).

2 J. Bionanosci. 11, 1–6, 2017

Rana et al.
Fig. 1. Schematic representation of 3D bioprinting concept using nanomaterials for tissue engineering and regenerative medicine.
a metal electrode. The proposed applications of these 3D
printed nanoscale structures include their use as bioscaf-
folds, nanofilters, nanorobots or nanoelectrodes for various
biomedical applications.6 All these experimental examples,
and others, clearly indicate the impact of 3D bioprinted
scaffolding systems on controlling cellular behavior of cul-
tured cells.
In the recent years, nanotechnology or nanomaterials
have played a key role in engineering 3D bioprinted scaf-
folds suitable for various tissue engineering applications.
3D bioprinted scaffolds made up of nanoscale bioma-
terials as bio-inks play a critical role in manipulating
the cell microenvironment for altering their growth and
development.7 Nanotechnology can be used to impart the
structural and functional properties of native microenviron-
ment within the 3D bioprinted scaffold in order to enhance
the cellular growth and function of the seeded cells (see
Fig. 1).7 For instance, Henriksson et al. reported increased
lipid accumulation and adipogenic gene expression of
adipocytes in 3D bioprinted nanocellulose scaffolds.8 The
mesenchymal stem cells suspended in nanocellulose and
hyaluronic acid based 3D bioprinted scaffolds showed 95%
cell viability after culturing for one week.8 Though this
field is still in its infancy stage, but holds great potential
for the future.
Considering the aforementioned impact of nanotechnol-
ogy in the field of 3D bioprinting, in this article, the
authors have focused their attention to concisely review
the impact of different types of nanomaterials on the 3D
bioprinted scaffolds and their interaction with the cultured
cells. For the benefit of readers, brief introductions on 3D
bioprinting technology have also been included. The arti-
cle is expected to be useful for readers to gain insights
into current trends and advances of nanotechnology on
J. Bionanosci. 11, 1–6, 2017
Impact of Nanotechnology on 3D Bioprinting
REVIEW
3D bioprinting for various biomedical applications, in par-
ticular, tissue engineering and regenerative medicine.
2. 3D BIOPRINTING: AN OVERVIEW
3D Bioprinting have emerged in recent years as a flexible
tool for creating 3D tissues and organs for a variety of
tissue engineering and regenerative medicine applications.
3D bioprinting technique not only have the potential to
create fully functional replacements for damaged tissues or
organs in patients, but also could rapidly fabricate size and
shape specific human based tissue models or organoids for
diagnostics, pathology modeling and drug development.4
It is an additive manufacturing or rapid prototyping tech-
nique that creates 3D structures by adding layer-by-layer
of biomaterials (ceramic, metal, polymeric or compos-
ite) with bioactive molecules, growth factors and/or living
cells.1 The basic steps involved in product development
using 3D bioprinting includes pre-bioprinting, bioprinting
and post-bioprinting. In pre-bioprinting step, designing a
model suitable for printing by using techniques like com-
puted topography (CT) and magnetic resonance imaging
(MRI) is practiced while in bioprinting step, the mix-
ture of cells, bioactive molecules and biomaterial are used
together as bio-ink to be placed in a printer cartridge
and printed in a layer-by-layer fashion to fabricate tissue
like 3D structure followed by maintaining them in asep-
tic conditions.9 Post-bioprinting process includes remod-
eling of tissue with the help of mechanical and chemical
signals which results into well-defined 3D scaffolds.10 By
employing this method of fabrication, rapid-fabrication,
high-precision and customized-production of tissue engi-
neered scaffolds with controlled cell patterns having
retained functionality and viability of the cells within the
printed 3D structures could be achieved. Additionally,
3
 Impact of Nanotechnology on 3D Bioprinting
3D bioprinting could enhance the ability to control pore
size distribution, pore volume and pore interconnectiv-
ity within 3D printed scaffolds that could further assist
various cellular functions such as attachment, migration,
proliferation and differentiation.11 However, 3D bioprint-
ing accredit to important advances in tissue engineering
REVIEW
field by the study of bio-inks. Bio-inks are the print-
able forms of the biomaterials (for example, hydrogels) in
combination with living cells, growth factors or bioactive
molecules that could be printed into 3D structures at room
temperature without any significant effect on the cell via-
bility and good mechanical reliability.12 To this end, vari-
ous 3D printing methods have been used to fabricate tissue
engineered scaffolds such as stereolithography (SLA), dig-
ital light processing (DLP), selective laser sintering (SLS),
fused filament fabrication (FFF) and ink-jet printing. How-
ever, the most commonly used 3D bioprinting methods are
ink-jet, microextrusion and laser-assisted printing methods
where cells, drugs or biomolecules incorporated within the
hydrogel pre-polymer solution could be directly printed.4
The important factors to be considered while selecting the
3D printing technology are surface resolution, cell viability
and the biological materials to be used. The ink-jet bio-
printer delivers controlled volumes of liquid to predefined
locations. Commonly, it uses thermal or acoustic forces
to eject drops of liquid onto a substrate, which can sup-
port or form part of the final scaffold.4 The quality of
the final printed scaffold depends on the various material
properties of the bio-ink such as printability, biocompati-
bility, degradation kinetics and byproducts, structural and
mechanical properties, material biomimicry, cell sources,
etc. A balanced combination of these important factors
could deliver functional tissue engineered 3D bioprinted
tissues or organs. For instance, Park et al. demonstrated
that the combination of low molecular weight alginate
(Low Alg) with high molecular weight alginate (High Alg)
at a ratio of 1:2 could provide better processability, struc-
tural integrity, cell viability and growth than the individual
Low Alg and High Alg.13 Therefore, it is critical to ana-
lyze both the processability of printing and the viability of
printed cells for achieving successful 3D bioprinting with
cell based bio-inks.
3. IMPACT OF NANOTECHNOLOGY ON
3D BIOPRINTING
In the recent years, nanotechnology has added a whole
new dimension in engineering biomaterials in the form
of 3D bioprinted scaffolds suitable for tissue engineering
and regenerative medicine. The 3D bioprinted scaffolds
made of nanomaterials play a critical role in accommo-
dating cells and guide them to differentiate into a specific
tissue during regenerative process. The cellular behaviors,
such as adhesion, proliferation, migration and differenti-
ation, of the cultured cells have been shown to be con-
trolled by the structural and functional properties of the
4 J. Bionanosci. 11, 1–6, 2017
Rana et al.
cell microenvironment where the seeded cells are intended
to grow. Nanotechnology offers an opportunity to modu-
late the structural and functional properties of the native
cellular microenvironment within the 3D bioprinted scaf-
folds in order to enhance the cellular growth and func-
tion. For instance, Nowicki et al. demonstrated that 3D
bioprinting and nanocrystalline hydroxyapatite could pro-
vide improved human bone marrow mesenchymal stem
cells (hBMSCs) adhesion, proliferation and osteochon-
dral differentiation.14 The software aided manipulations
on scaffold geometries were proved to be beneficial for
mechanical performance without hindering its cellular
behavior. The inclusion of nanoparticles with biochemi-
cal factors into the 3D bioprinted scaffolds further elicited
desired hBMSCs differentiation in osteogenic and chon-
drogenic lineages.14 Ensuring sufficient vascularization of
the engineered bioprinted scaffold is essential for its long-
term viability. Several studies have demonstrated genera-
tion of a branched vascular tree for bioprinted scaffolds.
For instance, Holmes et al. have combined nanomate-
rials and 3D printing technology for a highly innova-
tive complex 3D printed scaffold with both nano and
micro features.15 The authors have designed and printed
a series of novel 3D bone scaffolds with both bone for-
mation supporting structures and highly interconnected
3D microvascular mimicking channels, for efficient and
enhanced osteogenic bone regeneration as well as vas-
cular cell growth. The 3D printed polylactic acid (PLA)
based scaffolds have been chemically functionalized with
the nanohydroxyapatite to fabricate micro- and nano-
featured devices for vascularized bone growth. The results
from mechanical testing and hydrodynamic measurements
confirmed bone-like physical properties and vascular-like
flow profiles.15 The in vitro hBMSCs adhesion (at 4 hr),
proliferation (1, 3 and 5 d) and osteogenic differen-
tiation (1, 2 and 3 weeks) study results demonstrated
enhanced hBMSCs adhesion, proliferation and osteogenic
differentiation.15 Additional in vitro experiments with
human umbilical vein endothelial cells also demonstrated
improved vascular cell growth, migration and organiza-
tion on micro-nano featured scaffolds.15 Various bioma-
terials are being currently used for 3D bioprinting of
tissue engineered scaffolds such as naturally derived poly-
mers (including alginate, gelatin, collagen, chitosan, fib-
rin and hyaluronic acid), synthetically derived polymers
(including polyethylene glycol; PEG) and their compos-
ites. Recently Loo et al. have reported the synthesis of
first peptide bio-inks (lysine containing hexapeptides) that
could self-assemble into stable, nanofibrous 3D hydro-
gels with unprecedented stiffness of upto 40 kPa.16 These
3D printable biocompatible bio-inks support the 3D cul-
ture of human stem cells and differentiation of primary
cells into organotypic (gastrointestinal and skin) structures
for high-throughput screening, diagnosis and tissue engi-
neering applications.16 All the experimental examples dis-
cussed in this section, and other reported studies, clearly
Rana et al.
demonstrated that the nanotechnology has made a sig-
nificant impact on the efficiency of 3D bioprinted tissue
engineering products.
4. APPLICATION OF 3D BIOPRINTED
NANOMATERIALS
3D Bioprinted nanomaterials hold great promise as a scaf-
folding system for the culture of cell lines or human
stem cells in tissue engineering due to their unique struc-
tural and functional properties which could be tuned to
suit the mechanical and physiological demands of the
host tissue by controlling the volume fraction, morphol-
ogy and arrangement of the reinforcement materials phase.
In general, tissue engineering involves the culture of iso-
lated cells from the patient or donor into a scaffolding
system, made-up of nanomaterials that can support the
growth and function of the isolated cells into a specific
tissue, which could be transplanted back to the defective
site of the patient where tissue regeneration is required.17
The important factors that affect the final tissue engi-
neered product are cell source, scaffold, nanomaterials
based fillers, bioactive molecules and cell-material inter-
actions. The combination of 3D bioprinting and nano-
materials provide enhanced scaffold design specificity,
increased cell attachment, cell-material interactions and
subsequent tissue development. From biological perspec-
tive, cells in the human body resides in a complex mixture
of pores, ridges and various components of micro- and
nano-featured ECM environment, which plays a vital role
in facilitating cell-matrix interactions and cell–cell com-
munications upon implantation of the engineered graft.17
For instance, Gao et al. evaluated potential of bioac-
tive ceramic nanoparticles in stimulating osteogenesis of
printed hBMSCs in poly(ethylene glycol) dimethacrylate
(PEGDA) scaffold.18 The hBMSCs suspended in PEGDA
were co-printed with bioactive glass (BG) nanoparticles
and hydroxyapatite nanoparticles (HA) under simultane-
ous polymerization so that the printed substrates were
delivered with highly accurate placement in 3D loca-
tions. Among all the other groups, hBMSCs interacted
with HA showed the highest cell viability of 86.63 ±
6.02% and increased compressive modulus of 358.91 ±
48.05 kPa after 21 days in culture.18 Furthermore, bio-
chemical analysis showed the most collagen production
and highest alkaline phosphatase activity in PEGDA-HA
group than the PEGDA-BG group. These results were con-
sistent with gene expression results determined by quanti-
tative PCR. Masson’s trichrome staining also showed the
most collagen deposition in PEGDA-HA group scaffolds.18
Therefore, fabricating 3D bioprinted tissue engineered
scaffolds in combination with nanomaterials could help in
mimicking the native tissue microenvironment. Addition-
ally, this technology could further be used for screening
cell-biomaterial interaction in 3D and promoting regen-
eration of functional tissue. For instance, Ma et al.
J. Bionanosci. 11, 1–6, 2017
Impact of Nanotechnology on 3D Bioprinting
proposed a bioprinting-based approach to generate nano-
liter sized 3D cell-laden hydrogel array with gradient of
extracellular matrix (ECM) components, through control-
ling the volume ratio of two hydrogels, such as gelatin
methacrylate (GelMA) and poly(ethylene glycol) (PEG)
dimethacrylate.19 The developed cell-laden array with a
REVIEW
gradient of GelMA/PEG composition was used to screen
human periodontal ligament stem cells (PDLSCs) response
to ECM components. The cellular behavior such as via-
bility and spreading of human PDLSCs in GelMA/PEG
array were found to be depended on the volume ratios
of GelMA/PEG, with cell viability and spreading area
decreased along with increasing the ratio of PEG.19 All
these experimental examples, and other studies, clearly
indicate that the nanomaterials loaded 3D bioprinted scaf-
folding systems have great potential in regeneration of
damaged tissues for various biomedical applications, in
particular, tissue engineering and regenerative medicine.
5. CONCLUDING REMARKS
The 3D bioprinting technology is one of the attractive
biofabrication tools for manufacturing patient-specific tis-
sue engineered scaffolds for various tissue engineering
and regenerative medicine applications. Nanotechnology
has potential to develop various forms of nano-featured
materials or reinforcement materials that can manipulate
the cellular microenvironment and support the growth and
function of the cultured cells specific to each application.
Extensive studies have shown that nano-featured tissue
engineered scaffolds can regulate or control the functional
properties of the cells or stem cells in engineering tis-
sues or organs. Therefore, nanotechnology in combination
with 3D bioprinting offers the possibility to manufacture
novel scaffolds that could modulate cells or stem cells fate
and functions. Despite numerous technological advances in
3D bioprinting technology, relatively little is known about
the 3D bioprinted nanomaterial based scaffolds for tissue
engineering applications and the interaction between the
nanoscale microenvironment and cells or stem cells; which
is very essential to develop physiologically functional
engineered tissue and organs. The field of nanomaterial-
based 3D bioprinting is still in its infancy stage. Keeping
these points in mind, future research may aim converging
nanomaterials, nanotechnological principles, 3D bioprint-
ing and tissue engineering in order to mimic the physio-
logical complexity of the native tissues and organs.
Acknowledgments: This work was supported by
CSCR. The author, Deepti Rana, would like to thank
CSCR for the award of research fellowship.
References and Notes
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Received: 3 January 2017. Accepted: 22 January 2017.