J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
4 (2011) 922–932
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/jmbbm
Review article
Applications of knitted mesh fabrication techniques to
scaffolds for tissue engineering and regenerative medicine
Xingang Wang a , Chunmao Han a,∗ , Xinlei Hu a , Huafeng Sun a , Chuangang You a ,
Changyou Gao b , Yang Haiyang a,1
a Department of Burns, Second Affiliated Hospital of Zhejiang University, College of Medicine, Hangzhou, 310009, China
b Key Laboratory of Macromolecular Synthesis and Functionalization, Ministry of Education, Department of Polymer Science and
Engineering, Zhejiang University, Hangzhou, China
A R T I C L E
I N F O
A B S T R A C T
Article history:
Knitting is an ancient and yet, a fresh technique. It has a history of no less than 1,000
Received 13 January 2011
years. The development of tissue engineering and regenerative medicine provides a new
Received in revised form
role for knitting. Several meshes knitted from synthetic or biological materials have been
7 April 2011
designed and applied, either alone, to strengthen materials for the patching of soft tissues,
Accepted 11 April 2011
or in combination with other kinds of biomaterials, such as collagen and fibroin, to
Published online 19 April 2011
repair or replace damaged tissues/organs. In the latter case, studies have demonstrated
that knitted mesh scaffolds (KMSs) possess excellent mechanical properties and can
Keywords:
promote more effective tissue repair, ligament/tendon/cartilage regeneration, pipe-like-
Knitted mesh
organ reconstruction, etc. In the process of tissue regeneration induced by scaffolds, an
Mechanical properties
important synergic relationship emerges between the three-dimensional microstructure
Microstructure
and the mechanical properties of scaffolds. This paper presents a comprehensive overview
Regeneration
of the status and future prospects of knitted meshes and its KMSs for tissue engineering
and regenerative medicine.
c 2011 Elsevier Ltd. All rights reserved.
⃝
Contents
1.
Introduction ................................................................................................................................................................................. 923
2.
Fundamentals of knitting ............................................................................................................................................................. 923
3.
Ways to fabricate knitted mesh scaffolds ..................................................................................................................................... 925
3.1.
One-step moulding ............................................................................................................................................................ 925
3.2.
Assembly ........................................................................................................................................................................... 925
4.
Properties of knitted mesh scaffolds ............................................................................................................................................ 926
5.
Clinical applications of knitted mesh scaffolds ............................................................................................................................ 926
5.1.
Patches for soft tissues ...................................................................................................................................................... 926
5.2.
Ligaments and tendons ..................................................................................................................................................... 926
∗ Corresponding author. Tel.: +86 571 87767187; fax: +86 571 87784585.
E-mail address: [email protected] (C. Han).
in Dulwich College in UK.
1 Studying
c 2011 Elsevier Ltd. All rights reserved.
1751-6161/$ - see front matter ⃝
doi:10.1016/j.jmbbm.2011.04.009
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
6.
4 (2011) 922–932
923
5.3.
Cartilage ............................................................................................................................................................................ 927
5.4.
Skin ................................................................................................................................................................................... 927
5.5.
Blood vessels ..................................................................................................................................................................... 928
Conclusion and perspectives ........................................................................................................................................................ 929
Acknowledgements ...................................................................................................................................................................... 929
References .................................................................................................................................................................................... 929
1.
Introduction
Tissue-engineered scaffolds can be the artificial equivalents
of natural extracellular matrices (ECMs) that are used to
induce tissue regeneration or replace damaged tissues/organs
(Langer and Vacanti, 1993; Griffith and Naughton, 2002).
Although the requirements of scaffolds for tissue engineering
are multifaceted and specific to the structure and function of
the tissue of interest (Yang et al., 2001), ideal scaffolds should
have good biocompatibility and biodegradability, highly
porous and interconnected microstructures, and suitable
mechanical support (Hutmacher, 2000; Yang et al., 2002; Wang
et al., 2007). Comparatively, the processing and bioactivity
of scaffolds have been paid more attention than others
(Harley et al., 2007). Naturally derived materials such as
collagen have been used extensively to prepare scaffolds
due to their good biocompatibility, hydrophilicity and cell
affinity. However, scaffolds constructed entirely of collagen
sponge or gel possess poor strength to resist mechanical
forces (Bell et al., 1979; Young et al., 1998; Awad et al.,
1999; Ng et al., 2004; Nirmalanandhan et al., 2007; Mao
et al., 2009). Nowadays, for tissue-engineered scaffolds, the
importance of three-dimensional (3D) porous structures has
been confirmed to allow in vitro cell adhesion, ingrowth
and reorganisation, and provide the necessary space for
neovascularisation in vivo (Schmidt and Baier, 2000; O’Brien
et al., 2005; Puppi et al., 2010). The role of mechanical
properties is being increasingly recognised to provide
temporary mechanical support and proper mechanical cues
(Leong et al., 2008), and to maintain space for cell ingrowth
and matrix formation (Puppi et al., 2010), and rapidly
restore tissue biomechanical function (Gloria et al., 2010).
Some researchers state that constructing a scaffold that
simultaneously possesses optimal mechanical properties, a
porous structure and a biocompatible microenvironment, is
a more intriguing orientation (Chen et al., 2002, 2008).
A knitted mesh possesses highly ordered loop structures
(Wintermantel et al., 1996) and versatile mechanical properties (Quaglini et al., 2008; Yeoman et al., 2010) that can
provide sufficient internal connective space for tissue ingrowth (Ouyang et al., 2003). As a unique method of material processing, knitting has shown the potential to provide
tissue engineering with many kinds of knitted meshes, or
participate in the construction of tissue-engineered scaffolds
(Chen et al., 2002). Nowadays, well-designed knitted meshes
manufactured from synthetic or biological materials such as
polylactide-co-glycolide (PLGA) (Ouyang et al., 2003) and silk
(Chen et al., 2008) commonly have unique mechanical properties and have been used to provide improved physical support, either alone to strengthen materials for the patching of
soft tissues Clave et al. (2010), or in combination with other
types of biomaterials, for the construction of knitted mesh
scaffolds (KMSs) (Tatekawa et al., 2010).
Given increasing reports about the applications of a
knitted mesh, this review presents a comprehensive overview
of the status and future prospects of knitted meshes and
KMSs for tissue engineering and regenerative medicine.
The knitted mesh mentioned in the different papers cited
may be associated with different names, e.g. knitted mesh,
mesh, network or fabric. Meanwhile, KMSs may also have
different terms used by the researchers, e.g. hybrid scaffold
(Munirah et al., 2008; Urita et al., 2008; Dai et al., 2010), hybrid
construct (Ananta et al., 2009), combined scaffold (Liu et al.,
2008; Fan et al., 2009), composite web scaffold (Chen et al.,
2003a), composite vascular graft (Xu et al., 2010), composite
or 3D scaffold (Pu et al., 2010), etc. The inclusion criteria are
based on the knitted structure described in detail in the cited
articles.
2.
Fundamentals of knitting
Knitting as an ancient and yet, a fresh technique, has
a history of at least 1000 years. The basics of knitting,
upon which most of this section is based, have been well
documented (Spencer, 1983; Hatch, 1993; Leong et al., 2000).
The structure of a knitted mesh is often defined as a highly
ordered arrangement of interlocking loops (Wintermantel
et al., 1996). The general categories and characteristics
of textiles according to the structures and processing are
summarised in Table 1. Knitting and weaving, herein, are
traditional techniques used for making fabrics from yarns
or threads (Spencer, 1983). The yarns in knitted fabrics
follow a meandering path to form symmetric loops, which
is different from the criss-cross structure of straight threads
in woven fabrics (Hatch, 1993). The knitting process can be
used to produce fabrics by interlooping stitches using knitting
needles. A continuous series of interlooped stitches is formed
by the needle catching the yarn and drawing it through a
previously formed loop to form a new loop Leong et al. (2000).
In the knitted structures, rows running across the width of
the knitted fabric are called courses, and columns running
along the length of the fabric are known as wales. The loops
in the courses and wales are supported by and interconnected
with one another to form the final fabric (Leong et al., 2000).
According to the direction of formed loops, knitting can be
categorised into two major classifications: weft knitting and
warp knitting. In weft knitting, the wales are perpendicular
to the course of the yarn (Fig. 1(a)), where as in warp knitting,
the wales and courses run roughly parallel (Fig. 1(b)) (Spencer,
1983). On this basis, an infinite variety of knitted structures
has been successfully manufactured in the textile industry
(Lau and Dias, 1994; Leong et al., 2000).
924
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
4 (2011) 922–932
Table 1 – Categories of textile structures.a .
Type
Woven
Knitted
Weft
Warp
Braided
Nonwoven
Source
Dimension Extension
Porosity
Yarns
Stable
Low
Low
To unravel easily at the edges when cut or trimmed
Merits and demerits
Yarns
Yarns
Yarns
Fibres
Unstable
Stable
Stable
Varying
High
Versatile
Middle
high
High
High
High
Varying
Additional yarns are utilised to interlock the loops
Having flexibility and inherent ability to resist unravelling
The yarns criss-cross each other
Determined by those of the constituent polymer or fibre and by the
bonding process
a Data collected mainly from Spencer (1983), Hatch (1993) and Wintermantel et al. (1996).
c
d
cartilage, skin
a
e
f
g
h
ligament and tendon
blood vessel, bladder, ureter,
hernia,trachea, oesophagus, etc.
b
blood vessel, skin, etc.
Fig. 1 – Schematic applications of a knitted mesh and KMSs in tissue engineering. (a, b): Schematic diagrams of the wale
and course components of a knitted mesh, the principles of warp (a) and weft (b) knitting. In warp knitting, the wales and
courses run roughly parallel (a), where as in weft knitting, the wales are perpendicular to the course of the yarn (b). (c, d):
SEM images of PLGA knitted mesh (c) with typical warp-knit structures, and PLGA/collagen hybrid scaffold (d), prepared by
forming collagen microsponges in the loops. (e, f): Gross image of knitted silk mesh (e) and SEM image of the combined
scaffold (f) showing the integration of collagen sponge with the knitted silk mesh. (g, h): SEM of the knitted silk mesh (g)
and phase-contrast image of the combined silk scaffold (h), showing web-like microporous silk sponges formed in the
openings of the knitted silk mesh.
Source: Reprinted with permission from Leong et al. (2000), Chen et al. (2005, 2008) and Liu et al. (2008).
The weft-knit structures distort and stretch more easily,
whereas the warp-knit ones are more stable and less
formable. Generally, the weft-knit structures include three
primary classifications: jersey structure and its derivatives,
rib fabric and its derivatives, and purl fabric and its
derivatives (Bruer and Smith, 2005), and the entire fabric can
be fabricated from one yarn. In contrast, in warp knitting, one
yarn is required for each wale. A typical piece of a knitted
mesh may incorporate hundreds of wales. Therefore, the
production rate of warp knitting is significantly higher than
that of weft knitting, and warp knitting is more suitable for
large-scale production (Leong et al., 2000). To obtain particular
macroscopic properties and more complicated fabrics, float
and tuck stitches are often used to modify the structure of the
knitted fabric. Nowadays, knitting has reached a high level
of mechanical automation, which has been well documented
(Spencer, 1983; Leong et al., 2000). Warp knitting is performed
by Tricot or Raschel knitting machines, and weft knitting may
be finished by circular and flat-bed knitting machines.
The development of tissue engineering and regenerative
medicine provides a new role for knitting. Fig. 1 shows the
schematic applications of warp- and weft-knit structures
in the field of tissue engineering, which are further
discussed in Sections 5 and 6 by providing more details.
The materials used for the fabrication of the knitted mesh
are commonly synthetic materials, such as poly(lactic-coglycolic acid) (PLGA), which are hydrophobic and lack the cellrecognition sites necessary for cell adhesion and function
(Gunatillake and Adhikari, 2003). Besides, naturally derived
materials with good biocompatibility are selected to fabricate
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
a
d
b
4 (2011) 922–932
925
c
e
f
Fig. 2 – Schematic illustration of various designs of hybrid scaffolds from PLGA knitted mesh and collagen-based sponge.
The position (a–c), quantity (d) and shape (e, f), and of the mesh in the KMSs can be regulated as needed. Pink: PLGA knitted
mesh; yellow: collagen-based sponge.
a knitted mesh, e.g. silk fibres, but knitted silk scaffolds
with good internal communicating spaces are unsuitable for
cell seeding (Ouyang et al., 2003). Hence, in the practical
applications, a strategy of combining the knitted mesh and
other biomaterials can be used to obtain optimised scaffolds
for tissue engineering, such as KMSs.
3.
Ways to fabricate knitted mesh scaffolds
Theoretically, a knitted mesh can be designed and knitted
into many specific shapes to suit the target tissues/organs
(Chen et al., 2003a; Dai et al., 2010). To date, many methods
have been developed to integrate a mesh into a scaffold; chief
among these are one-step moulding and assembly.
3.1.
One-step moulding
One-step moulding entails simultaneous incorporation of the
knitted mesh and fabrication of the KMSs. Lyophilisation
is one of the most common methods for preparing such
scaffolds. The quantity, shape, and position of the mesh in
the KMSs can be regulated as needed, and the thickness of
the KMSs can be adjusted by laminating or rolling the web
sheets (Fig. 2(a), (d)–(f)) (Chen et al., 2003a). Dai et al. (2010)systemically investigated the effect of PLGA mesh/collagen hybrid scaffolds on cartilage regeneration; they used lyophilisation to design three kinds of hybrid scaffolds, i.e., thin, semi, and sandwich scaffolds (Fig. 2(a)–(c)), which differed based
on the location of the PLGA knitted mesh. Besides, several
novel practical scaffolds have been developed for ligamenttissue engineering by forming a collagen microstructure in
the pores of a silk-based knitted mesh using a freeze-drying
process (Chen et al., 2008; Fan et al., 2009). Xu et al. (2010)
introduced another method to prepare a composite vascular graft reinforced by a tubular weft-knitted fabric. A tubular polyester mesh was dressed onto a glass mandrel and
then uniformly coated with polyurethane/N, N-Dimethyl formamide (PU/DMF); after soaking in distilled water to remove
the DMF, the hybrid vascular graft was obtained (Xu et al.,
2010).
Fig. 3 – Diagram showing a model of assembly for plastic
compression of hyperhydrated hybrid scaffolds. By the
faster and easier method, a multilayered scaffold can be
obtained by compressing a hyperhydrated collagen gel onto
a flat warp-knitted poly(lactic acid-co-caprolactone) (PLACL)
mesh. Green arrow indicates the direction of loading. Black
arrows indicate the direction of the expulsed liquid.
3.2.
Assembly
During assembly, the fabrication of KMSs is finished by
assembling several units, even including cell elements, with
the knitted mesh constituting one auxiliary part. Ananta et al.
(2009) introduced a faster and easier technique for preparing
a multilayered scaffold by compressing a hyperhydrated
collagen gel onto a flat warp-knitted poly(lactic acid-cocaprolactone) (PLACL) mesh (Fig. 3). Ng and Hutmacher (2006)
developed an assembly method for preparing bilayer skin
equivalents by first peeling off fibroblast sheets and folding
them over a PLGA knitted mesh to form a 3D dermal matrix
and then seeding keratinocytes to form a skin substitute
in the air–liquid culture. A specific example of assembly is
DermagraftTM , a bioengineered dermal equivalent, which is
prepared by culturing allogeneic fibroblasts in PLGA knitted
mesh for 14–17 days to obtain a mixture of cells, ECM, and
degradable polymers (Cooper et al., 1991; Bello et al., 2001;
Marston, 2004).
Some researchers have tried to fabricate more complicated scaffolds by combining one-step moulding and assembly. Tatekawa et al. (2010) utilised PLGA mesh/collagen
926
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
hybrid scaffolds, tube stents, and basic fibroblast growth
factor (bFGF)-impregnated gelatin-hydrogel sheets to repair
tracheal defects. Though the scaffold combining bFGF and
reinforcement induced incomplete regeneration of tracheal
cartilage, it represented an improved method for fabricating
better scaffolds (Tatekawa et al., 2010).
4.
Properties of knitted mesh scaffolds
Proper mechanical support has been under essential
consideration for the construction of scaffolds (Ng et al.,
2005; Leong et al., 2008). Especially for naturally derived
materials, various methods have been developed to improve
the mechanical performance of scaffolds (Ruijgrok et al.,
1994; Ulubayram et al., 2002; Powell and Boyce, 2006; Rezwan
et al., 2006; Hillberg et al., 2009). Universally, the mechanical
strength should maintain enough spaces for cell ingrowth
and functionalisation in vitro, and temporarily bear in vivo
stresses and loading (Puppi et al., 2010). Mechanical strength
seems not to be an independent contributing factor, but
a synergetic one with other characteristics of scaffolds,
such as porous structures (Ng et al., 2004). Nowadays,
many fabrication techniques have been developed to design
different scaffolds characterised by porous structures, good
biocompatibility and excellent mechanical properties, e.g.,
incorporating poly(glycolic acid) fibre into collagen sponge
(Hiraoka et al., 2003; Nagato et al., 2006), combining collagen
and poly(L-lactic acid) (PLLA) braid (Idea et al., 2001),
introducing collagen microsponges into the pores of synthetic
polymer sponges (Chen et al., 2004b) or the interstices of
knitted meshes (Chen et al., 2005), forming microporous
silk sponges in the openings of a knitted silk scaffold (Liu
et al., 2008), etc. The synthetic polymer sponge, braid, fibres
and knitted meshes serve as a “skeleton” to reinforce the
entire scaffolds, while the collagen or silk sponges provide
the scaffolds with porous structures (Chen et al., 2002).
However, porous synthetic materials prepared for engineering
applications may show excellent elasticity but low shear
resistance to suturing (Xu et al., 2010). Twisted or braided
scaffolds can possess remarkable mechanical properties that
are comparable to native tissue (Altman et al., 2002), but their
limited internal space often hinders the ingrowth of neotissue
(Chen et al., 2008). Scaffolds shaped by fibres provide a large
surface for cell attachment and a rapid diffusion of nutrients,
but a lack of structural stability (Chen et al., 2002). By contrast,
a knitted mesh possesses ordered and stable loop structures,
and internal connective spaces. By changing the geometric
parameters of the fabric (yarn spacing and thickness) or the
fibre material, the required mechanical properties can be
achieved (Quaglini et al., 2008).
Synthetic or biological meshes have been used to fabricate
KMSs (Zdrahala, 1996; Chen et al., 2004b; Cui et al., 2009;
He et al., 2010). How does the knitted mesh improve the
mechanical strength of a combined or hybrid scaffold? Weftknitted structures in which loops are formed across the width
of the fabric are inelastic but can provide high levels of
compression and support, whereas warp-knitted meshes can
offer better flexibility and elasticity due to the formation of
loops along the length of the fabric (Anand, 2003). Knitted
4 (2011) 922–932
meshes incorporated into porous scaffolds can serve as a
support structure to reinforce combined or hybrid scaffolds
(Chen et al., 2005), and afford mechanical support to resist a
physical load (Chen et al., 2008). Meanwhile, the mechanical
properties of a knitted mesh can be influenced by the addition
of a polymeric matrix that bonds the filaments in the mesh
together (Wintermantel et al., 1996). In addition, although
a knitted mesh can promote homogeneous cell distribution
and tissue formation (Ng et al., 2004), the application of a
knitted mesh has been reported rarely as a scaffold and
has occasionally been regarded as a control (Ouyang et al.,
2003; Chen et al., 2005; Liu et al., 2008). It has been used
as an auxiliary tool in the construction of scaffolds for
tissue engineering. For example, Lu et al. (2011) used a
knitted PLGA mesh as a selectively removable template to
prepare an autologous extracellular matrix (aECM) scaffold.
The preparation of an aECM scaffold by combining culture
of autologous cells in the knitted mesh, decellularisation,
and template removal is depicted in Fig. 4; the in vivo
experiment indicated that the aECM scaffold had excellent
biocompatibility.
5.
Clinical applications of knitted mesh scaffolds
5.1.
Patches for soft tissues
Various knitted meshes made from synthetic materials, commonly regarded as prosthetic materials such as polypropylene, poly(ethylene terephthalate), and polylactic acid have
been designed for the treatment of hernia (Boukerrou et al.,
2007), pelvic organ prolapse (Ganj et al., 2009), pelvic floor dysfunctions (Clave et al., 2010), body wall defects (Lamb et al.,
1983; Tyrell et al., 1989), and so on. In addition to good mechanical properties, for this kind of application, all of the materials used for the knitted mesh should also have the ability
to resist erosion and defect recurrence (Boukerrou et al., 2007).
These materials are often inert or have very slow degradation
rates, and the implanted meshes are replaced gradually by
newly formed or surrounding tissues. However, such implants
were reported to cause many complications, e.g. inflammation (Pu et al., 2010), infection (Urita et al., 2008), rejection and
recurrence (Boukerrou et al., 2007), etc. In view of the above,
some researchers considered tissue engineering as an alternative treatment strategy. For example, Urita et al. (2008) used
a PLGA knitted mesh/collagen scaffold as an alternative prosthetic material to repair a diaphragmatic hernia and observed
that the hybrid scaffold was better than a simple PLGA mesh
for promoting in situ tissue regeneration. Pu et al. (2010) developed a PLLA–collagen scaffold by forming collagen sponge
within the pores of a poly(L-lactic acid) (PLLA) knitted mesh,
and cultured dermal fibroblasts on this scaffold for 7 days by
using a flow perfusion bioreactor for abdominal wall repair.
5.2.
Ligaments and tendons
Once damaged, ligaments and tendons have no ability
to heal through a regenerative process, but instead form
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
Cell seeding in a template
Cells
4 (2011) 922–932
927
Cell-ECM-template
construct
Template
ECM
deposition
Cell culture
Decellularisation
Template removal
ECM scald
ECM-template construct
Fig. 4 – Fabrication scheme for an autologous extracellular matrix (aECM) scaffold. The aECM was prepared by combining
culture of autologous cells in a template, decellularisation and template removal. The template as an auxiliary tool
indicates a knitted PLGA mesh, which can be selectively removed. The cells can be fibroblasts, chondrocytes or
mesenchymal stem cells (MSCs) (Lu et al., 2011).
fibrotic scars (Favata et al., 2006). The development of
tissue engineering and regenerative medicine may provide
a promising method to treat ligament and tendon injuries.
Of the many biomaterial grafts fabricated as ligament and
tendon scaffolds (Torres et al., 2000; Gentleman et al., 2006;
Sahoo et al., 2006; Cooper et al., 2007; Fini et al., 2007),
knitted scaffolds have mechanical properties similar to those
of biological tissues and are therefore a good prospect
for ligament and tendon reconstruction. Chen et al. (2008)
developed a new practical ligament scaffold based on the
synergistic incorporation of a plain knitted silk structure
and a collagen matrix. This scaffold, with better mechanical
properties and a more native microstructure, induced
ligament regeneration with greater collagen deposition in
a rabbit model (Fig. 1(e), (f)), suggesting that the knitted
mesh improved not only the mechanical strength of the
scaffold but also the level of regeneration of the target
tissue (Chen et al., 2008). Liu et al. (2008) fabricated a
combined scaffold with web-like microporous silk sponges
formed in the openings of a knitted silk mesh (Fig. 1(g), (h))
and subsequently seeded with adult human bone marrowderived mesenchymal stem cells (MSCs) for in vitro ligamenttissue engineering. Compared with a simple knitted scaffold,
the combined scaffold promoted greater cell activity, with
increased expression of type I and III collagen and tenascinC genes (Liu et al., 2008). Subsequently, Fan et al. (2009)
rolled combined silk scaffold around a braided silk cord
to regenerate the anterior cruciate ligament using MSCs
in a pig model; the regenerated ligament showed obvious
ligament–bone junction formation, and the MSCs in the
regenerated ligament exhibited fibroblast-like morphology 24
weeks post the operation.
With regard to tendon tissue engineering, Ouyang et al.
(2003) used a knitted PLGA scaffold to repair a 10 mm gap
in the Achilles tendon in a rabbit model. They showed that
the knitted mesh induced tendon regeneration, and when
loaded with bone marrow stromal cells, the scaffold repaired
the tendon defects more effectively.
5.3.
Cartilage
In cartilage tissue engineering, the fundamental challenge
is to develop a suitable scaffold that provides sufficient
structural support to withstand the large forces applied to
the new tissue. Chen and colleagues have conducted many
in vitro and in vivo studies in cartilage reconstruction with
the use of knitted PLGA mesh/collagen hybrid scaffolds
(Chen et al., 2003a,b, 2004a,b; Dai et al., 2010; Kawazoe
et al., 2010). The hybrid scaffolds, taking advantage of
naturally derived and synthetic materials, were prepared
by integrating collagen sponges with the knitted PLGA
mesh, and with adjustable thickness (Chen et al., 2003a,b;
Dai et al., 2010). Herein, the polymer mesh served as a
“skeleton” and reinforced the hybrid scaffold, that facilitated
cell seeding and cell distribution (Chen et al., 2003a,b). These
studies demonstrated that the PLGA mesh/collagen scaffolds
improved chondrocyte adhesion, proliferation (Chen et al.,
2004b), facilitated the redifferentiation of the dedifferentiated
multiplied chondrocytes (Chen et al., 2003b), and promoted
chondrogenic differentiation of MSCs (Chen et al., 2004a). The
engineered tissue obtained by this approach matched the
native cartilage both histologically and mechanically (Chen
et al., 2003a). A recent study has focused on a novel leak-proof
PLGA mesh/collagen cell scaffold to transdifferentiate MSCs
for cartilage tissue (Kawazoe et al., 2010).
5.4.
Skin
Collagen-based porous sponges have been developed to
guide tissue regeneration and to provide a substrate for
epidermalisation (Ruszczak, 2003). The support of collagenbased scaffolds is compromised by their low mechanical
strength. Therefore, improved mechanical properties are
important for collagen-based scaffolds to induce skin-tissue
regeneration and reduce wound contraction. Chen et al.
(2005) developed a novel porous scaffold by hybridising a
knitted PLGA mesh and naturally derived bovine collagen
(Fig. 1(c),(d)), and the hybrid scaffold exhibited good
928
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
a
4 (2011) 922–932
b
c
Fig. 5 – SEM image of the cross section of the surface of PLGAm/CCS (a), prepared by incorporating PLGA knitted mesh into
collagen–chitosan scaffold (CCS), and histological images of PLGAm/CCS (b) and CCS (c) implanted subcutaneously for one
week. The letter S indicates the collagen–chitosan sponge side, and M indicates the mesh side. Yellow arrows indicate the
direction of tissue infiltration (unpublished data).
biocompatibility and high mechanical properties. Ananta
et al. (2009) spatially distributed neonatal fibroblasts in
a PLACL mesh/collagen gel composite that mimicked
interstitial or epithelial tissue; this multilayered tissue
substitute had homogeneous cell distribution and good
biocompatibility, and it showed no macroscopic signs of
contraction. Ng et al. (2005) developed a hybrid matrix
by lyophilising collagen within a weft-knitted PLGA mesh,
which simulated the mechanical properties of native
dermis, supported cell attachment and proliferation in
vitro, and evoked minimal host tissue response in vivo.
Ng and Hutmacher (2006) seeded dermal fibroblasts and
keratinocytes into a 3D matrix composed of a weft-knitted
PLGA mesh and collagen–hyaluronic acid (CHA) sponge to
construct a bilayer skin substitute. When transplanted in
full-thickness onto wounds in nude rats for four weeks, the
substitute inhibited wound contraction similarly to autografts
(Ng and Hutmacher, 2006).
Studies have revealed that collagen–chitosan scaffold possesses good biocompatibility and suitable porous structures
for skin tissue engineering (Ma et al., 2003a,b, 2007). However, its poor mechanical strength compromises the resistance to mechanical forces (Mao et al., 2009). In order
to develop a well-supported scaffold, we incorporated a
PLGA knitted mesh into a collagen–chitosan sponge to construct a hybrid scaffold, abbreviated as PLGAm/CCS (Fig. 5(a)).
The incorporation of PLGA mesh into CCS did little influence on the microstructure of the collagen–chitosan
sponge, yet improved the mechanical strength of the hybrid scaffold similar to that of native dermis. Furthermore, when embedded subcutaneously in rats for one
week, the hybrid scaffold promoted tissue infiltration more
rapidly than the collagen–chitosan scaffold (Fig. 5(b), (c)).
Meanwhile, in the same PLGAm/CCS, more abundant tissue formation was observed near to the mesh side than the
collagen–chitosan sponge side (Fig. 5(b)). These results indicate that mechanical properties, cooperating with 3D microstructures, play an important part in tissue regeneration.
5.5.
Blood vessels
Tissue engineering techniques have been developed to
construct vascular grafts, but the clinical use of bloodvessel alternatives remains limited. The primary obstacles
include shortage of vascular endothelium, thrombosis,
lumen collapse, low seeding-cell viability, infection risk, and
insufficient mechanical strength to afford long-term patency
(Baguneid et al., 2006; Chlupac et al., 2009; Ravi and Chaikof,
2010). For an ideal blood-vessel substitute, the fundamental
requirements with respect to mechanical properties include
sufficient burst pressure and viscoelasticity. Burst pressure,
i.e., the strength required to rupture the vessel, is a
critical characteristic of blood-vessel substitutes. For native
arteries, the burst pressure is in excess of 2000 mm
Hg; given the normal arterial pressure range of up to
several hundred mm Hg, this indicates that native blood
vessels are designed with a safety factor of approximately
ten fold (Nerem, 2000). Another important characteristic
is the viscoelasticity, which should match that of native
blood vessels. Although it is difficult to construct an
ideal substitute, incorporating a weft-knitted fabric into
a polyurethane vascular graft can improve elasticity and
strength (Xu et al., 2010). Among the polymeric materials
that provide appropriate mechanical properties for vascular
scaffolds, the knitted mesh has the potential to be used
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
in routine clinical practice (Ravi et al., 2009; Ju et al.,
2010). Sawa et al. (Iwai et al., 2005; Torikai et al., 2008;
Takahashi et al., 2009) have fabricated a tissue-engineered
patch consisting of collagen microsponges, an interior layer
of PGA knitted mesh, and an exterior layer of woven
PLA fibres for reconstructing vascular walls. The results of
animal experiments revealed that this patch enabled in situ
regeneration in venous or arterial walls, with no development
of aneurysm or thrombus within the patch area in any group.
Further, the architecture of the neotissue was similar to that
of the native tissue at 6 months after implantation in dogs.
In addition to the above applications, a knitted mesh can
also be used to construct scaffolds for the bladder, ureter,
hernia, trachea, and oesophagus (Miki et al., 1999; Sha’ban
et al., 2008; Ananta et al., 2009; Kawazoe et al., 2010; Roosa
et al., 2010; Tatekawa et al., 2010).
6.
Conclusion and perspectives
For decades, knitted meshes have been applied surgically
to reinforce frail tissues such as hernia (Boukerrou et al.,
2007; Clave et al., 2010). Initially, the biomaterials constituting
the knitted mesh were regarded as inert (Clave et al.,
2010). Gradually, the biocompatibility and tissue-inducing
regeneration of biomaterials have become recognised as
important characteristics (Silva and Mooney, 2004). The
mechanical properties of scaffolds have been shown to
significantly affect cell behaviours and scaffold bioactivity
(Grinnell et al., 1999; Freyman et al., 2001; Yeung et al., 2005;
Harley et al., 2007). Therefore, improving the mechanical
properties of scaffolds is not only a hot topic in the laboratory,
but also a great challenge in the translation to clinical
research.
Knitted fabrics with unique structures and mechanical
properties are an important element of the technical textile
field. Well-designed knitted meshes, whether weft or warp,
used alone or in combination, have been shown to be
promising for tissue engineering and regenerative medicine
(Wintermantel et al., 1996; Chen et al., 2002). A knitted
mesh serves not only as a basic method for improving the
mechanical strength of scaffolds but also as the ‘skeleton’
of grafts to maintain a porous microstructure, promote cell
alignment, and induce tissue regeneration. The use of a
knitted mesh has been examined in a variety of tissueengineering applications such as repair of ligaments (Chen
et al., 2008), tendons (Ouyang et al., 2003), cartilages (Chen
et al., 2004b; Dai et al., 2010; Kawazoe et al., 2010), skin
(Ng et al., 2004), and pipe-like organs (Tatekawa et al.,
2010; Xu et al., 2010). Some of these applications are still
in preliminary, exploratory stages. Many issues relevant to
knitted meshes and KMSs should be further investigated.
Although knitted meshes have relatively homogeneous
structures (Wintermantel et al., 1996), versatile mechanical
properties (Quaglini et al., 2008; Yeoman et al., 2010), and
controllable biological properties, the ideal knitted mesh
for tissue regeneration is unknown. A knitted mesh, as an
artificial fabric, possesses many alterable factors, e.g., knitting
materials, knitting techniques, and fabric characteristics.
With regard to the current status of mesh application
4 (2011) 922–932
929
for tissue engineering, more researches are needed to
optimise biomaterials for knitting, develop suitable knitting
methods to prepare biomimetic meshes for various target
tissues/organs, match the rates of mesh degradation and
neotissue formation. Moreover, although knitted structures
exist in various forms in the textile industry, the knitted
structures applied to tissue engineering are in the infant
period. The possible reason may be that knitted structures
have been selected to obtain better functions instead of for
their appearances.
KMSs, designed explicitly to match the mechanical
properties of the native tissue or give cells proper mechanical
cues, provide a good platform for studying the roles
of mechanical properties in tissue regeneration. Many
biomaterials such as silk, PLGA, and PLACL have been made
into knitted fabrics with various biophysical properties (Chen
et al., 2008; Ananta et al., 2009; Fan et al., 2009; Dai et al.,
2010). So, how to understand the effects and mechanisms
of KMSs on cell activity and tissue regeneration? The
sound deduction may be: (1) knitted meshes with excellent
mechanical properties change the distribution of tension and
pressure on KMSs (Xu et al., 2010) and further maintain the
3D porous structures in vitro and in vivo; (2) well-maintained
porous structures facilitate the diffusion of nutrients and the
removal of waste products, and they provide enough space
for cell migration and vascular ingrowth (Schmidt and Baier,
2000; Puppi et al., 2010); and (3) because specific surface
areas (SSAs) to which cells adhere exist around the pores
(O’Brien et al., 2005), mechanical properties can affect the
distribution of SSAs by maintaining porous structures and
can thereby regulate cell behaviours and tissue formation.
Because the 3D microstructure of scaffolds plays a vital role in
the regulation of cell activity and tissue regeneration (O’Brien
et al., 2005; Ng and Hutmacher, 2006; Powell et al., 2008; Lin
et al., 2009; Murphy et al., 2010; Murphy and O’Brien, 2010),
an important synergic relationship may exist between the
3D microstructure and the mechanical properties of scaffolds
in the process of scaffold-induced tissue regeneration (Ng
et al., 2004). Additionally, criteria for knitted meshes should
be established to assess their mechanical properties for use
in tissue engineering and routine clinical practice.
Acknowledgements
The authors sincerely acknowledge Dr. Fergal J. O’Brien,
Department of Anatomy, Royal College of Surgeons in Ireland
& Trinity Centre for Bioengineering, Trinity College Dublin,
for his constructive suggestions. This work was financially
supported by the Major State Basic Program of China
(2005CB623902) and the Major Science and Technology Project
of Zhejiang, China (2007C13040).
REFERENCES
Altman, G.H., Horan, R.L., Lu, H.H., Moreau, J., Martin, I.,
Richmond, J.C., Kaplan, D.L., 2002. Silk matrix for tissue
engineered anterior cruciate ligaments. Biomaterials 23 (20),
4131–4141.
930
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
Anand, S., 2003. Spacers-at the technical frontiers. Knit. Int. 110
(1305), 38–41.
Ananta, M., Aulin, C.E., Hilborn, J., Aibibu, D., Houis, S., Brown,
R.A., Mudera, V., 2009. A poly(lactic acid-co-caprolactone)collagen hybrid for tissue engineering applications. Tissue Eng.
Part A 15 (7), 1667–1675.
Awad, H.A., Butler, D.L., Boivin, G.P., Smith, F.N., Malaviya, P.,
Huibregtse, B., Caplan, A.I., 1999. Autologous mesenchymal
stem cell-mediated repair of tendon. Tissue Eng. 5 (3), 267–277.
Baguneid, M.S., Seifalian, A.M., Salacinski, H.J., Murray, D.,
Hamilton, G., Walker, M.G., 2006. Tissue engineering of blood
vessels. Brit. J. Surg. 93 (3), 282–290.
Bell, E., Ivarsson, B., Merrill, C., 1979. Production of a tissuelike structure by contraction of collagen lattices by human
fibroblasts of different proliferative potential in vitro. Proc.
Natl. Acad. Sci. USA 76 (3), 1274–1278.
Bello, Y.M., Falabella, A.F., Eaglstein, W.H., 2001. Tissue-engineered
skin. Current status in wound healing. Am. J. Clin. Dermatol. 2
(5), 305–313.
Boukerrou, M., Boulanger, L., Rubod, C., Lambaudie, E., Dubois,
P., Cosson, M., 2007. Study of the biomechanical properties
of synthetic mesh implanted in vivo. Eur. J. Obstet. Gynecol.
Reprod. Biol. 134 (2), 262–267.
Bruer, S.M., Smith, G., 2005. Three-dimensionally knit space
fabrics: a review of production techniques and applications.
JTATM 4 (4), 1–31.
Chen, G., Liu, D., Tadokoro, M., Hirochika, R., Ohgushi, H.,
Tanaka, J., Tateishi, T., 2004a. Chondrogenic differentiation of
human mesenchymal stem cells cultured in a cobweb-like
biodegradable scaffold. Biochem. Biophys. Res. Commun. 322
(1), 50–55.
Chen, X., Qi, Y.Y., Wang, L.L., Yin, Z., Yin, G.L., Zou, X.H.,
Ouyang, H.W., 2008. Ligament regeneration using a knitted silk
scaffold combined with collagen matrix. Biomaterials 29 (27),
3683–3692.
Chen, G., Sato, T., Ohgushi, H., Ushida, T., Tateishi, T., Tanaka,
J., 2005. Culturing of skin fibroblasts in a thin PLGA-collagen
hybrid mesh. Biomaterials 26 (15), 2559–2566.
Chen, G., Sato, T., Ushida, T., Hirochika, R., Shirasaki, Y., Ochiai,
N., Tateishi, T., 2003a. The use of a novel PLGA fiber/collagen
composite web as a scaffold for engineering of articular
cartilage tissue with adjustable thickness. J. Biomed. Mater.
Res. A 67 (4), 1170–1180.
Chen, G., Sato, T., Ushida, T., Hirochika, R., Tateishi, T., 2003b.
Redifferentiation of dedifferentiated bovine chondrocytes
when cultured in vitro in a PLGA-collagen hybrid mesh. FEBS
Lett. 542 (1), 95–99.
Chen, G., Sato, T., Ushida, T., Ochiai, N., Tateishi, T., 2004b. Tissue
engineering of cartilage using a hybrid scaffold of synthetic
polymer and collagen. Tissue Eng. 10 (3–4), 323–330.
Chen, G., Ushida, T., Tateishi, T., 2002. Scaffold design for tissue
engineering. Macromol. Biosci. 2 (2), 67–77.
Chlupac, J., Filova, E., Bacakova, L., 2009. Blood vessel replacement: 50 years of development and tissue engineering paradigms in vascular surgery. Phys. Res. 58 (Suppl. 2S),
119–139.
Clave, A., Yahi, H., Hammou, J.C., Montanari, S., Gounon, P.,
Clave, H., 2010. Polypropylene as a reinforcement in pelvic
surgery is not inert: comparative analysis of 100 explants. Int.
Urogynecol. J. Pel. 21 (3), 261–270.
Cooper, M.L., Hansbrough, J.F., Spielvogel, R.L., Cohen, R., Bartel,
R.L., Naughton, G., 1991. In vivo optimization of a living
dermal substitute employing cultured human fibroblasts
on a biodegradable polyglycolic acid or polyglactin mesh.
Biomaterials 12 (2), 243–248.
Cooper Jr, J.A., Sahota, J.S., Gorum 2nd, W.J., Carter, J., Doty, S.B.,
Laurencin, C.T., 2007. Biomimetic tissue-engineered anterior
cruciate ligament replacement. Proc. Natl. Acad. Sci. USA 104
(9), 3049–3054.
4 (2011) 922–932
Cui, L., Wu, Y., Cen, L., Zhou, H., Yin, S., Liu, G., Liu, W., Cao, Y.,
2009. Repair of articular cartilage defect in non-weight bearing
areas using adipose derived stem cells loaded polyglycolic acid
mesh. Biomaterials 30 (14), 2683–2693.
Dai, W., Kawazoe, N., Lin, X., Dong, J., Chen, G., 2010. The influence
of structural design of PLGA/collagen hybrid scaffolds in
cartilage tissue engineering. Biomaterials 31 (8), 2141–2152.
Fan, H., Liu, H., Toh, S.L., Goh, J.C., 2009. Anterior cruciate ligament
regeneration using mesenchymal stem cells and silk scaffold
in large animal model. Biomaterials 30 (28), 4967–4977.
Favata, M., Beredjiklian, P.K., Zgonis, M.H., Beason, D.P., Crombleholme, T.M., Jawad, A.F., Soslowsky, L.J., 2006. Regenerative
properties of fetal sheep tendon are not adversely affected by
transplantation into an adult environment. J. Orthop. Res. 24
(11), 2124–2132.
Fini, M., Torricelli, P., Giavaresi, G., Rotini, R., Castagna, A.,
Giardino, R., 2007. In vitro study comparing two collageneous
membranes in view of their clinical application for rotator cuff
tendon regeneration. J. Orthop. Res. 25 (1), 98–107.
Freyman, T.M., Yannas, I.V., Yokoo, R., Gibson, L.J., 2001. Fibroblast
contraction of a collagen-GAG matrix. Biomaterials 22 (21),
2883–2891.
Ganj, F.A., Ibeanu, O.A., Bedestani, A., Nolan, T.E., Chesson,
R.R., 2009. Complications of transvaginal monofilament
polypropylene mesh in pelvic organ prolapse repair. Int.
Urogynecol. J. Pel. 20 (8), 919–925.
Gentleman, E., Livesay, G.A., Dee, K.C., Nauman, E.A., 2006.
Development of ligament-like structural organization and
properties in cell-seeded collagen scaffolds in vitro. Ann.
Biomed. Eng. 34 (5), 726–736.
Gloria, A., De Santis, R., Ambrosio, L., 2010. Polymer-based
composite scaffolds for tissue engineering. J. Appl. Biomater.
Biomech. 8 (2), 57–67.
Griffith, L.G., Naughton, G., 2002. Tissue engineering-current
challenges and expanding opportunities. Science 295 (5557),
1009–1014.
Grinnell, F., Ho, C.H., Lin, Y.C., Skuta, G., 1999. Differences in the
regulation of fibroblast contraction of floating versus stressed
collagen matrices. J. Biol. Chem. 274 (2), 918–923.
Gunatillake, P.A., Adhikari, R., 2003. Biodegradable synthetic
polymers for tissue engineering. Eur. Cells Mater. 5, 1–16.
Harley, B.A., Leung, J.H., Silva, E.C., Gibson, L.J., 2007. Mechanical
characterization of collagen-glycosaminoglycan scaffolds.
Acta Biomater. 3 (4), 463–474.
Hatch, K.L., 1993. Textile Science. West Publishing Company, New
York.
He, X., Lu, H., Kawazoe, N., Tateishi, T., Chen, G., 2010. A novel
cylinder-type poly(L-lactic acid)-collagen hybrid sponge for
cartilage tissue engineering. Tissue. Eng. Part. C Methods 16
(3), 329–338.
Hillberg, A.L., Holmes, C.A., Tabrizian, M., 2009. Effect of genipin
cross-linking on the cellular adhesion properties of layer-bylayer assembled polyelectrolyte films. Biomaterials 30 (27),
4463–4470.
Hiraoka, Y., Kimura, Y., Ueda, H., Tabata, Y., 2003. Fabrication
and biocompatibility of collagen sponge reinforced with
poly(glycolic acid) fiber. Tissue Eng. 9 (6), 1101–1112.
Hutmacher, D.W., 2000. Scaffolds in tissue engineering bone and
cartilage. Biomaterials 21 (24), 2529–2543.
Idea, A., Sakane, M., Chen, G., Shimojo, H., Ushida, T., Tateishi,
T., Wadano, Y., Miyanaga, Y., 2001. Collagen hybridization with
poly(L-lactic acid) braid promotes ligament cell migration.
Mater. Sci. Eng., C 17 (1–2), 95–99.
Iwai, S., Sawa, Y., Taketani, S., Torikai, K., Hirakawa, K.,
Matsuda, H., 2005. Novel tissue-engineered biodegradable
material for reconstruction of vascular wall. Ann. Thorac. Surg.
80 (5), 1821–1827.
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
Ju, Y.M., Choi, J.S., Atala, A., Yoo, J.J., Lee, S.J., 2010. Bilayered scaffold for engineering cellularized blood vessels. Biomaterials 31
(15), 4313–4321.
Kawazoe, N., Inoue, C., Tateishi, T., Chen, G., 2010. A cell leakproof
PLGA-collagen hybrid scaffold for cartilage tissue engineering.
Biotechnol Prog. 26 (3), 819–826.
Lamb, J.P., Vitale, T., Kaminski, D.L., 1983. Comparative evaluation
of synthetic meshes used for abdominal wall replacement.
Surgery 93 (5), 643–648.
Langer, R., Vacanti, J.P., 1993. Tissue engineering. Science 260
(5110), 920–926.
Lau, K.W., Dias, T., 1994. Knittability of high-modulus yarns.
J. Text. Inst. 85 (2), 173–190.
Leong, K.F., Chua, C.K., Sudarmadji, N., Yeong, W.Y., 2008.
Engineering functionally graded tissue engineering scaffolds.
J. Mech. Behav. Biomed. Mater. 1 (2), 140–152.
Leong, K.H., Ramakrishna, S., Bibo, G.A., Huang, Z.M., 2000. The
potential of knitting for engineering composites. Composites
Part A 31 (3), 197–220.
Lin, D., Li, Q., Li, W., Swain, M., 2009. Dental implant induced bone
remodeling and associated algorithms. J. Mech. Behav. Biomed.
Mater. 2 (5), 410–432.
Liu, H., Fan, H., Wang, Y., Toh, S.L., Goh, J.C., 2008. The interaction
between a combined knitted silk scaffold and microporous
silk sponge with human mesenchymal stem cells for ligament
tissue engineering. Biomaterials 29 (6), 662–674.
Lu, H., Hoshiba, T., Kawazoe, N., Chen, G., 2011. Autologous extracellular matrix scaffolds for tissue engineering. Biomaterials
32 (10), 2489–2499.
Ma, L., Gao, C., Mao, Z., Shen, J., Hu, X., Han, C., 2003a. Thermal
dehydration treatment and glutaraldehyde cross-linking to
increase the biostability of collagen-chitosan porous scaffolds
used as dermal equivalent. J. Biomater. Sci. Polym. Ed. 14 (8),
861–874.
Ma, L., Gao, C., Mao, Z., Zhou, J., Shen, J., Hu, X., Han, C., 2003b.
Collagen/chitosan porous scaffolds with improved biostability
for skin tissue engineering. Biomaterials 24 (26), 4833–4841.
Mao, Z., Shi, H., Guo, R., Ma, L., Gao, C., Han, C., Shen, J.,
2009. Enhanced angiogenesis of porous collagen scaffolds
by incorporation of TMC/DNA complexes encoding vascular
endothelial growth factor. Acta Biomater. 5 (8), 2983–2994.
Marston, W.A., 2004. Dermagraft, a bioengineered human dermal
equivalent for the treatment of chronic nonhealing diabetic
foot ulcer. Expert. Rev. Med. Devic. 1 (1), 21–31.
Ma, L., Shi, Y., Chen, Y., Zhao, H., Gao, C., Han, C., 2007. In vitro and
in vivo biological performance of collagen-chitosan/silicone
membrane bilayer dermal equivalent. J. Mater. Sci., Mater.
Med. 18 (11), 2185–2191.
Miki, H., Ando, N., Ozawa, S., Sato, M., Hayashi, K., Kitajima, M.,
1999. An artificial esophagus constructed of cultured human
esophageal epithelial cells, fibroblasts, polyglycolic acid mesh,
and collagen. ASAIO J. 45 (5), 502–508.
Munirah, S., Kim, S.H., Ruszymah, B.H., Khang, G., 2008. The use
of fibrin and poly(lactic-co-glycolic acid) hybrid scaffold for
articular cartilage tissue engineering: an in vivo analysis. Eur.
Cells Mater. 15, 41–52.
Murphy, C.M., Haugh, M.G., O’Brien, F.J., 2010. The effect
of mean pore size on cell attachment, proliferation and
migration in collagen-glycosaminoglycan scaffolds for bone
tissue engineering. Biomaterials 31 (3), 461–466.
Murphy, C.M., O’Brien, F.J., 2010. Understanding the effect of
mean pore size on cell activity in collagen-glycosaminoglycan
scaffolds. Cell Adh. Migr. 4 (3), 377–381.
Nagato, H., Umebayashi, Y., Wako, M., Tabata, Y., Manabe,
M., 2006. Collagen-poly glycolic acid hybrid matrix with
basic fibroblast growth factor accelerated angiogenesis and
granulation tissue formation in diabetic mice. J. Dermatol. 33
(10), 670–675.
4 (2011) 922–932
931
Nerem, R.M., 2000. Tissue engineering a blood vessel substitute:
the role of biomechanics. Yonsei Med. J. 41 (6), 735–739.
Ng, K.W., Hutmacher, D.W., 2006. Reduced contraction of skin
equivalent engineered using cell sheets cultured in 3D
matrices. Biomaterials 27 (26), 4591–4598.
Ng, K.W., Khor, H.L., Hutmacher, D.W., 2004. In vitro characterization of natural and synthetic dermal matrices cultured with
human dermal fibroblasts. Biomaterials 25 (14), 2807–2818.
Ng, K.W., Louis, J., Ho, B.S.T., Achuth, H.N., Lu, J., Moochhala, S.,
Lim, T.C., Hutmacher, D.W., 2005. Characterization of a novel
bioactive poly[(lactic acid)-co-(glycolic acid)] and collagen
hybrid matrix for dermal regeneration. Polym. Int. 54 (10),
1449–1457.
Nirmalanandhan, V.S., Rao, M., Sacks, M.S., Haridas, B., Butler,
D.L., 2007. Effect of length of the engineered tendon construct
on its structure–function relationships in culture. J. Biomech.
40 (11), 2523–2529.
O’Brien, F.J., Harley, B.A., Yannas, I.V., Gibson, L.J., 2005. The
effect of pore size on cell adhesion in collagen-GAG scaffolds.
Biomaterials 26 (4), 433–441.
Ouyang, H.W., Goh, J.C., Thambyah, A., Teoh, S.H., Lee, E.H., 2003.
Knitted poly-lactide-co-glycolide scaffold loaded with bone
marrow stromal cells in repair and regeneration of rabbit
Achilles tendon. Tissue Eng. 9 (3), 431–439.
Powell, H.M., Boyce, S.T., 2006. EDC cross-linking improves
skin substitute strength and stability. Biomaterials 27 (34),
5821–5827.
Powell, H.M., Supp, D.M., Boyce, S.T., 2008. Influence of
electrospun collagen on wound contraction of engineered skin
substitutes. Biomaterials 29 (7), 834–843.
Puppi, D., Chiellini, F., Piras, A.M., Chiellini, E., 2010. Polymeric
materials for bone and cartilage repair. Prog. Polym. Sci. 35 (4),
403–440.
Pu, F., Rhodes, N.P., Bayon, Y., Chen, R., Brans, G., Benne,
R., Hunt, J.A., 2010. The use of flow perfusion culture
and subcutaneous implantation with fibroblast-seeded PLLAcollagen 3D scaffolds for abdominal wall repair. Biomaterials
31 (15), 4330–4340.
Quaglini, V., Corazza, C., Poggi, C., 2008. Experimental characterization of orthotropic technical textiles under uniaxial and biaxial loading. Composites Part A 39 (8), 1331–1342.
Ravi, S., Chaikof, E.L., 2010. Biomaterials for vascular tissue
engineering. Regen. Med. 5 (1), 107–120.
Ravi, S., Qu, Z., Chaikof, E.L., 2009. Polymeric materials for tissue
engineering of arterial substitutes. Vascular 17 (Suppl. 1S),
45–54.
Rezwan, K., Chen, Q.Z., Blaker, J.J., Boccaccini, A.R., 2006.
Biodegradable and bioactive porous polymer/inorganic composite scaffolds for bone tissue engineering. Biomaterials 27
(18), 3413–3431.
Roosa, S.M., Kemppainen, J.M., Moffitt, E.N., Krebsbach, P.H.,
Hollister, S.J., 2010. The pore size of polycaprolactone scaffolds
has limited influence on bone regeneration in an in vivo
model. J. Biomed. Mater. Res. A 92 (1), 359–368.
Ruijgrok, J.M., de Wijn, J.R., Boon, M.E., 1994. Glutaraldehyde
crosslinking of collagen: effects of time, temperature,
concentration and presoaking as measured by shrinkage
temperature. Clin. Mater. 17 (1), 23–27.
Ruszczak, Z., 2003. Effect of collagen matrices on dermal wound
healing. Adv. Drug Delivery Rev. 55 (12), 1595–1611.
Sahoo, S., Ouyang, H., Goh, J.C., Tay, T.E., Toh, S.L., 2006.
Characterization of a novel polymeric scaffold for potential
application in tendon/ligament tissue engineering. Tissue Eng.
12 (1), 91–99.
Schmidt, C.E., Baier, J.M., 2000. Acellular vascular tissues:
natural biomaterials for tissue repair and tissue engineering.
Biomaterials 21 (22), 2215–2231.
932
J O U R N A L O F T H E M E C H A N I C A L B E H AV I O R O F B I O M E D I C A L M AT E R I A L S
Sha’ban, M., Kim, S.H., Idrus, R.B., Khang, G., 2008. Fibrin and
poly(lactic-co-glycolic acid) hybrid scaffold promotes early
chondrogenesis of articular chondrocytes: an in vitro study.
J. Orthop. Res. 3 (17).
Silva, E.A., Mooney, D.J., 2004. Synthetic extracellular matrices for
tissue engineering and regeneration. Curr. Top. Dev. Biol. 64,
181–205.
Spencer, D.J., 1983. Knitting Technology. Pergamon Press, New
York.
Takahashi, H., Yokota, T., Uchimura, E., Miyagawa, S., Ota, T.,
Torikai, K., Saito, A., Hirakawa, K., Kitabayashi, K., Okada, K.,
Sawa, Y., Okita, Y., 2009. Newly developed tissue-engineered
material for reconstruction of vascular wall without cell
seeding. Ann. Thorac. Surg. 88 (4), 1269–1276.
Tatekawa, Y., Kawazoe, N., Chen, G., Shirasaki, Y., Komuro, H.,
Kaneko, M., 2010. Tracheal defect repair using a PLGA-collagen
hybrid scaffold reinforced by a copolymer stent with bFGFimpregnated gelatin hydrogel. Pediatr. Surg. Int. 26 (6), 575–580.
Torikai, K., Ichikawa, H., Hirakawa, K., Matsumiya, G., Kuratani, T.,
Iwai, S., Saito, A., Kawaguchi, N., Matsuura, N., Sawa, Y., 2008.
A self-renewing, tissue-engineered vascular graft for arterial
reconstruction. J. Thorac. Cardiov. Sur. 136 (1), 37–45.
Torres, D.S., Freyman, T.M., Yannas, I.V., Spector, M., 2000. Tendon
cell contraction of collagen-GAG matrices in vitro: effect of
cross-linking. Biomaterials 21 (15), 1607–1619.
Tyrell, J., Silberman, H., Chandrasoma, P., Niland, J., Shull, J., 1989.
Absorbable versus permanent mesh in abdominal operations.
Surg. Gynecol. Obstet. 168 (3), 227–232.
Ulubayram, K., Aksu, E., Gurhan, S.I., Serbetci, K., Hasirci, N.,
2002. Cytotoxicity evaluation of gelatin sponges prepared with
different cross-linking agents. J. Biomater. Sci. Polym. Ed. 13
(11), 1203–1219.
Urita, Y., Komuro, H., Chen, G., Shinya, M., Saihara, R.,
Kaneko, M., 2008. Evaluation of diaphragmatic hernia repair
4 (2011) 922–932
using PLGA mesh-collagen sponge hybrid scaffold: an
experimental study in a rat model. Pediatr. Surg. Int. 24 (9),
1041–1045.
Wang, H.J., Gong, S.J., Lin, Z.X., Fu, J.X., Xue, S.T., Huang, J.C., Wang,
J.Y., 2007. In vivo biocompatibility and mechanical properties
of porous zein scaffolds. Biomaterials 28 (27), 3952–3964.
Wintermantel, E., Mayer, J., Blum, J., Eckert, K.L., Luscher,
P., Mathey, M., 1996. Tissue engineering scaffolds using
superstructures. Biomaterials 17 (2), 83–91.
Xu, W., Zhou, F., Ouyang, C., Ye, W., Yao, M., Xu, B.,
2010. Mechanical properties of small-diameter polyurethane
vascular grafts reinforced by weft-knitted tubular fabric.
J. Biomed. Mater. Res. A 92 (1), 1–8.
Yang, S., Leong, K.F., Du, Z., Chua, C.K., 2001. The design of
scaffolds for use in tissue engineering. Part I. Traditional
factors. Tissue Eng. 7 (6), 679–689.
Yang, S., Leong, K.F., Du, Z., Chua, C.K., 2002. The design
of scaffolds for use in tissue engineering. Part II. Rapid
prototyping techniques. Tissue Eng. 8 (1), 1–11.
Yeoman, M.S., Reddy, D., Bowles, H.C., Bezuidenhout, D., Zilla,
P., Franz, T., 2010. A constitutive model for the warp–weft
coupled non-linear behavior of knitted biomedical textiles.
Biomaterials 31 (32), 8484–8493.
Yeung, T., Georges, P.C., Flanagan, L.A., Marg, B., Ortiz, M., Funaki,
M., Zahir, N., Ming, W., Weaver, V., Janmey, P.A., 2005. Effects of
substrate stiffness on cell morphology, cytoskeletal structure,
and adhesion. Cell Motil. Cytoskeleton. 60 (1), 24–34.
Young, R.G., Butler, D.L., Weber, W., Caplan, A.I., Gordon, S.L.,
Fink, D.J., 1998. Use of mesenchymal stem cells in a collagen
matrix for Achilles tendon repair. J. Orthop. Res. 16 (4),
406–413.
Zdrahala, R.J., 1996. Small caliber vascular grafts. Part I: state of
the art. J. Biomater. Appl. 10 (4), 309–329.