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A Compressible Scaffold for Minimally Invasive Delivery
Of Large Intact Neuronal Networks
Amélie Béduer,* Thomas Braschler, Oliver Peric, Georg E. Fantner, Sébastien Mosser,
Patrick C. Fraering, Sidi Benchérif, David J. Mooney, and Philippe Renaud
DOI: 10.1002/adhm.201400250
Dr. A. Béduer, Dr. T. Braschler, Prof. P. Renaud
STI-IMT-LMIS4, Station 17, EPFL
1015, Lausanne, Switzerland
E-mail: amelie.beduer@epfl.ch
Dr. T. Braschler, Dr. S. Benchérif, Prof. D. J. Mooney
School of Engineering and Applied Sciences
Harvard University,
02138, Cambridge, MA, USA
O. Peric, Prof. G. E. Fantner
STI-IBI-LBNI, Station 17, EPFL
1015, Lausanne, Switzerland
S. Mosser, Prof. P. C. Fraering
SV-BMI-CMSN, Station 15, EPFL
1015, Lausanne, Switzerland
Millimeter to centimeter-sized injectable neural scaffolds based on macropo-
rous cryogels are presented. The polymer-scaffolds are made from alginate
and carboxymethyl-cellulose by a novel simple one-pot cryosynthesis. They
allow surgical sterility by means of autoclaving, and present native laminin as
an attachment motive for neural adhesion and neurite development. They are
designed to protect an extended, living neuronal network during compression
to a small fraction of the original volume in order to enable minimally inva-
sive delivery. The scaffolds behave as a mechanical meta-material: they are
soft at the macroscopic scale, enabling injection through narrow-bore tubing
and potentially good cellular scaffold integration in soft target tissues such
as the brain. At the same time, the scaffold material has a high local Young
modulus, allowing protection of the neuronal network during injection. Based
on macroscopic and nanomechanical characterization, the generic geometri-
cal and mechanical design rules are presented, enabling macroporous cellular
scaffold injectability.
procedures involved in implanting com-
plex and large solid grafts into the brain
are very invasive and can easily lead to
further tissue damage rather than the
desired reconstruction outcome.
[4]
A
number of minimally invasive delivery
methods have been proposed, allowing to
apply in situ gelling formulations, micro-
particulate scaffold suspensions, partially
dissociated tissue, or neural stem cell
suspensions through narrow-bore nee-
dles.
[5–15]
Unfortunately, without the guid-
ance of a large-scale organized scaffold,
the cells typically build chaotic structures
rather than repairing the native tissue
architecture as desired.
[14]
As a result, the
associated functional recovery is never
complete and data from successful human
clinical studies are extremely scarce.
[15]
We propose here to address this current
major bottleneck of neural tissue engi-
neering by the use of a smart cellular scaffold system, which
is highly and reversibly compressible, allowing for minimally
invasive implantation of large, potentially preorganized con-
structs. To achieve this goal, several requirements must be met:
The scaffold material must be highly compressible, such that
mL-scale volumes can be delivered through narrow-bore tubing
or needles, yet it should recover its original shape, volume and
organization after the injection process. It should protect dif-
ferentiated neurons with their extended neurites during the
compression associated with the delivery process, but neverthe-
less behave as a globally soft material to minimize glial scarring
reactions in the brain.
[16]
For the long-term culture necessary
to develop differentiated neuronal networks, and in light of
potential clinical translation, the scaffolds need to be reliably
sterilized, preferentially by autoclaving. Last but not least, it is
desirable to be able to provide native extracellular matrix (ECM)
proteins to guide cell adhesion and differentiation. Macropo-
rous scaffolds with shape memory amenable to injection
through narrow-bore tubing can be fabricated by different tech-
niques, such as emulsion polymerization, lyophilization, and
cryogelation.
[17–19]
We base our scaffolds on the process of cryo-
gelation, involving polymerization of a hydrogel precursor at
subzero temperature, since this has been observed to produce
particularly robust gels, and since the possibility of neuronal
tissue engineering with cryogels has been reported.
[19–21]
We
provide a novel cryogel fabrication paradigm, consisting of a
1. Introduction
It is a clinical observation that the adult human brain typically
fails to repair large-scale tissue damage.
[1]
This contrasts with
the observation that neurons are continuously generated in
the subventricular zone and dentate gyrus,
[2,3]
and it is indeed
the hope and aim of cell-based therapies to extend the brain’s
regeneration capacity to large-scale lesions. A major limitation
on the path to successful neural tissue engineering and deep
brain transplantation is the development of minimally inva-
sive surgical techniques and scaffolds. Indeed, the surgical
Adv. Healthcare Mater. 2014,
DOI: 10.1002/adhm.201400250
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