Abstract

Scaffolds play an essential role in bone healing by providing temporary structural support to the native bone tissue and by hosting bone cells. To this end, several biomaterials and manufacturing methods have been proposed. Among the biomaterials, bio-active glasses have attractive properties as a scaffold material for bone repair. Simultaneously, additive manufacturing (AM) techniques have attracted significant attention owing to their capability of fabricating complex and patient-specific scaffolds. Accordingly, borosilicate bio-active glass (BG-B30) has been used to fabricate the scaffolds using an extrusion-based AM devices in this study. Pluronic F-127 was used as an ink carrier that showed suitable shear thinning behavior for fabrication. The pure BG-B30 scaffold had a compressive strength of 23.30 MPa and was reinforced further with functionalized multiwalled carbon nanotube (MWCNT-COOH) to reduce its brittleness and enhance its compressive strength. When compared to the conventional polymer foam replication technique, the combination of MWCNT-COOH reinforcement and AM resulted in an enhancement of the compressive strength by ∼646% (1.05 MPa to 35.84 MPa). Further, structural analysis using microcomputed tomography revealed that the scaffolds fabricated using AM had better control over strut size and pore size in addition to better network connectivity. Finally, in vitro experiments demonstrated its bio-active behavior by the formation of hydroxyapatite, and the cellular studies revealed good cell viability and osteogenesis initiation. These results are promising for the fabrication of patient-specific CNT-reinforced bio-active glass porous scaffolds for bone tissue engineering applications.

References

1.
Campana
,
V.
,
Milano
,
G.
,
Pagano
,
E.
,
Barba
,
M.
,
Cicione
,
C.
,
Salonna
,
G.
,
Lattanzi
,
W.
, and
Logroscino
,
G.
,
2014
, “
Bone Substitutes in Orthopaedic Surgery: From Basic Science to Clinical Practice
,”
J. Mater. Sci. Mater. Med.
,
25
(
10
), pp.
2445
2461
.10.1007/s10856-014-5240-2
2.
Chen
,
Q. Z.
,
Thompson
,
I. D.
, and
Boccaccini
,
A. R.
,
2006
, “
45S5 Bioglass-Derived Glass-Ceramic Scaffolds for Bone Tissue Engineering
,”
Biomaterials
,
27
(
11
), pp.
2414
2425
.10.1016/j.biomaterials.2005.11.025
3.
Rezwan
,
K.
,
Chen
,
Q. Z.
,
Blaker
,
J. J.
, and
Boccaccini
,
A. R.
,
2006
, “
Biodegradable and Bioactive Porous Polymer/Inorganic Composite Scaffolds for Bone Tissue Engineering
,”
Biomaterials
,
27
(
18
), pp.
3413
3431
.10.1016/j.biomaterials.2006.01.039
4.
Thavornyutikarn
,
B.
,
Nattapon
,
C.
,
Sitthiseripratip
,
K.
,
Thouas
,
G. A.
, and
Chen
,
Q.
,
2014
, “
Bone Tissue Engineering Scaffolding: Computer-Aided Scaffolding Techniques
,”
Prog. Biomater.
,
3
(
2–4
), pp.
61
102
.10.1007/s40204-014-0026-7
5.
Fu, Q., Saiz, E., and Tomsia, A. P., 2011, “Bioinspired Strong and Highly Porous Glass Scaffolds,”
Adv. Funct. Mater.
, 21(6), pp. 1058–1063.10.1002/adfm.201002030
6.
Fu
,
Q.
,
Rahaman
,
M. N.
,
Bal
,
B. S.
,
Brown
,
R. F.
, and
Day
,
D. E.
,
2008
, “
Mechanical and In Vitro Performance of 13-93 Bioactive Glass Scaffolds Prepared by a Polymer Foam Replication Technique
,”
Acta Biomater.
,
4
(
6
), pp.
1854
64
.10.1016/j.actbio.2008.04.019
7.
Fu
,
Q.
,
Rahaman
,
M. N.
,
Fu
,
H.
, and
Liu
,
X.
,
2010
, “
Silicate, Borosilicate, and Borate Bioactive Glass Scaffolds With Controllable Degradation Rate for Bone Tissue Engineering Applications. I. Preparation and In Vitro Degradation
,”
J. Biomed. Mater. Res. - Part A
,
95A
(
1
), pp.
164
171
.10.1002/jbm.a.32824
8.
Gu
,
Y.
,
Wang
,
G.
,
Zhang
,
X.
,
Zhang
,
Y.
,
Zhang
,
C.
,
Liu
,
X.
,
Rahaman
,
M. N.
,
Huang
,
W.
, and
Pan
,
H.
,
2014
, “
Biodegradable Borosilicate Bioactive Glass Scaffolds With a Trabecular Microstructure for Bone Repair
,”
Mater. Sci. Eng. C
,
36
(
1
), pp.
294
300
.10.1016/j.msec.2013.12.023
9.
Lu
,
L.
, and
Mikos
,
A. G.
,
1996
, “
The Importance of New Processing Techniques in Tissue Engineering
,”
MRS Bull.
,
21
(
11
), pp.
28
32
.10.1557/S088376940003181X
10.
Healy
,
K. E.
,
Whang
,
K.
, and
Thomas
,
C. H.
,
1998
, “
Method of Fabricating Emulsion Freeze-Dried Scaffold Bodies and Resulting Products
,” (
19
), pp.
1
12
.
11.
Roohani-Esfahani
,
S.-I.
,
Newman
,
P.
, and
Zreiqat
,
H.
,
2016
, “
Design and Fabrication of 3D Printed Scaffolds With a Mechanical Strength Comparable to Cortical Bone to Repair Large Bone Defects
,”
Sci. Rep.
,
6
, pp.
1
8
.10.1038/srep19468
12.
Peng
,
E.
,
Wei
,
X.
,
Garbe
,
U.
,
Yu
,
D.
,
Edouard
,
B.
,
Liu
,
A.
, and
Ding
,
J.
,
2018
, “
Robocasting of Dense Yttria-Stabilized Zirconia Structures
,”
J. Mater. Sci.
,
53
(
1
), pp.
247
273
.10.1007/s10853-017-1491-x
13.
Hench
,
L. L.
,
2006
, “
The Story of Bioglass®
,”
J. Mater. Sci. Mater. Med.
,
17
(
11
), pp.
967
978
.10.1007/s10856-006-0432-z
14.
Greenspan
,
D. C.
,
2016
, “
Glass and Medicine: The Larry Hench Story
,”
Int. J. Appl. Glass Sci.
,
7
(
2
), pp.
134
138
.10.1111/ijag.12204
15.
Yao
,
A.
,
Wang
,
D.
,
Huang
,
W.
,
Fu
,
Q.
,
Rahaman
,
M. N.
, and
Day
,
D. E.
,
2007
, “
In Vitro Bioactive Characteristics of Borate-Based Glasses With Controllable Degradation Behavior
,”
J. Am. Ceram. Soc.
,
90
(
1
), pp.
303
306
.10.1111/j.1551-2916.2006.01358.x
16.
Lepry
,
W. C.
, and
Nazhat
,
S. N.
,
2020
, “
The Anomaly in Bioactive Sol–Gel Borate Glasses
,”
Mater. Adv.
,
1
(
5
), pp.
1371
1381
.10.1039/D0MA00360C
17.
Cole
,
K. A.
,
Funk
,
G. A.
,
Rahaman
,
M. N.
, and
McIff
,
T. E.
,
2020
, “
Mechanical and Degradation Properties of Poly(Methyl Methacrylate) Cement/Borate Bioactive Glass Composites
,”
J. Biomed. Mater. Res. Part B Appl. Biomater.
,
108
(
7
), pp.
2765
2775
.10.1002/jbm.b.34606
18.
Al-Rashidy
,
Z. M.
,
Omar
,
A. E.
,
El-Aziz
,
T. H. A.
, and
Farag
,
M. M.
,
2020
, “
In Vivo Bioactivity Assessment of Strontium-Containing Soda-Lime-Borate Glass Implanted in Femoral Defect of Rat
,”
J. Inorg. Organomet. Polym. Mater.
,
30
(
10
), pp.
3953
3964
.10.1007/s10904-020-01535-4
19.
Parthasarathy
,
J.
,
Starly
,
B.
,
Raman
,
S.
, and
Christensen
,
A.
,
2010
, “
Mechanical Evaluation of Porous Titanium (Ti6Al4V) Structures With Electron Beam Melting (EBM)
,”
J. Mech. Behav. Biomed. Mater.
,
3
(
3
), pp.
249
259
.10.1016/j.jmbbm.2009.10.006
20.
Yin
,
H.
,
Qi
,
H. J.
,
Fan
,
F.
,
Zhu
,
T.
,
Wang
,
B.
, and
Wei
,
Y.
,
2015
, “
Griffith Criterion for Brittle Fracture in Graphene
,”
Nano Lett.
,
15
(
3
), pp.
1918
1924
.10.1021/nl5047686
21.
Gao
,
C.
,
Feng
,
P.
,
Peng
,
S.
, and
Shuai
,
C.
,
2017
, “
Carbon Nanotube, Graphene and Boron Nitride Nanotube Reinforced Bioactive Ceramics for Bone Repair
,”
Acta Biomater.
,
61
, pp.
1
20
.10.1016/j.actbio.2017.05.020
22.
Dixit
,
K.
, and
Sinha
,
N.
,
2019
, “
Compressive Strength Enhancement of Carbon Nanotube Reinforced 13-93B1 Bioactive Glass Scaffolds
,”
J. Nanosci. Nanotechnol.
,
19
(
5
), pp.
2738
2746
.10.1166/jnn.2019.16029
23.
Dixit
,
K.
,
Gupta
,
P.
,
Kamle
,
S.
, and
Sinha
,
N.
,
2020
, “
Structural Analysis of Porous Bioactive Glass Scaffolds Using Micro-Computed Tomographic Images
,”
J. Mater. Sci.
,
55
(
27
), pp.
12705
12724
.10.1007/s10853-020-04850-w
24.
Dixit
,
K.
, and
Sinha
,
N.
,
2021
, “
Effects of Boron Oxide Concentration and Carbon Nanotubes Reinforcement on Bioactive Glass Scaffolds for Bone Tissue Engineering
,”
J. Nanosci. Nanotechnol.
,
21
(
10
), pp.
5026
5035
.10.1166/jnn.2021.19370
25.
Deliormanlı
,
A. M.
, and
Rahaman
,
M. N.
,
2012
, “
Direct-Write Assembly of Silicate and Borate Bioactive Glass Scaffolds for Bone Repair
,”
J. Eur. Ceram. Soc.
,
32
(
14
), pp.
3637
3646
.10.1016/j.jeurceramsoc.2012.05.005
26.
Nommeots-Nomm
,
A. E.
,
2015
, “
3D Printing versus Foaming of Melt-Derived Bioactive Glasses for Bone Regeneration
,”
Ph.D. dissertation
,
Imperial College London
,
London, UK
.10.25560/50295
27.
Eqtesadi
,
S.
,
Motealleh
,
A.
,
Miranda
,
P.
,
Pajares
,
A.
,
Lemos
,
A.
, and
Ferreira
,
J. M. F.
,
2014
, “
Robocasting of 45S5 Bioactive Glass Scaffolds for Bone Tissue Engineering
,”
J. Eur. Ceram. Soc.
,
34
(
1
), pp.
107
118
.10.1016/j.jeurceramsoc.2013.08.003
28.
Franco
,
J.
,
Hunger
,
P.
,
Launey
,
M. E.
,
Tomsia
,
A. P.
, and
Saiz
,
E.
,
2010
, “
Direct Write Assembly of Calcium Phosphate Scaffolds Using a Water-Based Hydrogel
,”
Acta Biomater.
,
6
(
1
), pp.
218
228
.10.1016/j.actbio.2009.06.031
29.
Kokubo
,
T.
,
Kushitani
,
H.
,
Sakka
,
S.
,
Kitsugi
,
T.
, and
Yamamuro
,
T.
,
1990
, “
Solutions Able to Reproduce In Vivo Surface-Structure Changes in Bioactive Glass-Ceramic A-W
,”
J. Biomed. Mater. Res.
,
24
(
6
), pp.
721
734
.10.1002/jbm.820240607
30.
Fabert
,
M.
,
Ojha
,
N.
,
Erasmus
,
E.
,
Hannula
,
M.
,
Hokka
,
M.
,
Hyttinen
,
J.
,
Rocherullé
,
J.
,
Sigalas
,
I.
, and
Massera
,
J.
,
2017
, “
Crystallization and Sintering of Borosilicate Bioactive Glasses for Application in Tissue Engineering
,”
J. Mater. Chem. B
,
5
(
23
), pp.
4514
4525
.10.1039/C7TB00106A
31.
Huber
,
T.
,
Misra
,
M.
, and
Mohanty
,
A. K.
,
2015
, “
The Effect of Particle Size on the Rheological Properties of Polyamide 6/Biochar Composites
,”
AIP Conf. Proc.
,
1664
(
May 2015
), pp.
6
10
.10.1063/1.4918500
32.
Herschel
,
W. H.
, and
Bulkley
,
R.
,
1926
, “
Konsistenzmessungen Von Gummi-Benzollösungen
,”
Kolloid-Z.
,
39
(
4
), pp.
291
300
.10.1007/BF01432034
33.
Fu
,
Q.
,
Saiz
,
E.
, and
Tomsia
,
A. P.
,
2011
, “
Direct Ink Writing of Highly Porous and Strong Glass Scaffolds for Load-Bearing Bone Defects Repair and Regeneration
,”
Acta Biomater.
,
7
(
10
), pp.
3547
3554
.10.1016/j.actbio.2011.06.030
34.
Lenaerts
,
V.
,
Triqueneaux
,
C.
,
Quartern
,
M.
,
Rieg-Falson
,
F.
, and
Couvreur
,
P.
,
1987
, “
Temperature-Dependent Rheological Behavior of Pluronic F-127 Aqueous Solutions
,”
Int. J. Pharm.
,
39
(
1–2
), pp.
121
127
.10.1016/0378-5173(87)90206-7
35.
Vadnere
,
M.
,
Amidon
,
G.
,
Lindenbaum
,
S.
, and
Haslam
,
J. L.
,
1984
, “
Thermodynamic Studies on the Gel-Sol Transition of Some Pluronic Polyols
,”
Int. J. Pharm.
,
22
(
2–3
), pp.
207
218
.10.1016/0378-5173(84)90022-X
36.
Nommeots-Nomm
,
A.
,
Lee
,
P. D.
, and
Jones
,
J. R.
,
2018
, “
Direct Ink Writing of Highly Bioactive Glasses
,”
J. Eur. Ceram. Soc.
,
38
(
3
), pp.
837
844
.10.1016/j.jeurceramsoc.2017.08.006
37.
Karageorgiou
,
V.
, and
Kaplan
,
D.
,
2005
, “
Porosity of 3D Biomaterial Scaffolds and Osteogenesis
,”
Biomaterials
,
26
(
27
), pp.
5474
5491
.10.1016/j.biomaterials.2005.02.002
38.
Meng
,
D.
,
Rath
,
S. N.
,
Mordan
,
N.
,
Salih
,
V.
,
Kneser
,
U.
, and
Boccaccini
,
A. R.
,
2011
, “
In Vitro Evaluation of 45S5 Bioglass-Derived Glass-Ceramic Scaffolds Coated With Carbon Nanotubes
,”
J. Biomed. Mater. Res. - Part A
,
99A
(
3
), pp.
435
444
.10.1002/jbm.a.33185
39.
Meng
,
D.
,
Ioannou
,
J.
, and
Boccaccini
,
A. R.
,
2009
, “
Bioglass Based Scaffolds With Carbon Nanotube Coating for Bone Tissue Engineering
,”
J. Mater. Sci. Mater. Med.
,
20
(
10
), pp.
2139
2144
.10.1007/s10856-009-3770-9
40.
Boccaccini
,
A. R.
,
Chicatun
,
F.
,
Cho
,
J.
,
Bretcanu
,
O.
,
Roether
,
J. A.
,
Novak
,
S.
, and
Chen
,
Q.
,
2007
, “
Carbon Nanotube Coatings on Bioglass-Based Tissue Engineering Scaffolds
,”
Adv. Funct. Mater.
,
17
(
15
), pp.
2815
2822
.10.1002/adfm.200600887
41.
Zhang
,
D.
,
Kandadai
,
M. A.
,
Cech
,
J.
,
Roth
,
S.
, and
Curran
,
S. A.
,
2006
, “
Poly(L-Lactide) (PLLA)/Multiwalled Carbon Nanotube (MWCNT) Composite: Characterization and Biocompatibility Evaluation
,”
J. Phys. Chem. B
,
110
(
26
), pp.
12910
12915
.10.1021/jp061628k
42.
Bizios
,
R.
,
Ullmann
,
K. R.
,
Supronowicz
,
P. R.
,
Ajayan
,
P. M.
,
Metzger
,
D. W.
, and
Arulanandam
,
B. P.
,
2002
, “
Novel Current-Conducting Composite Substrates for Exposing Osteoblasts to Alternating Current Stimulation
,”
J. Biomed. Mater. Res.
,
59
(
3
), pp.
499
506
.10.1002/jbm.10015
43.
ASTM F2450-18
,
2018
,
Standard Guide for Assessing Microstructure of Polymeric Scaffolds for Use in Tissue-Engineered Medical Products
,
ASTM International
,
West Conshohocken, PA
.
44.
Zhang
,
J.
,
Jia
,
C.
,
Jia
,
Z.
,
Ladegard
,
J.
,
Gu
,
Y.
, and
Nie
,
J.
,
2012
, “
Strengthening Mechanisms in Carbon Nanotube Reinforced Bioglass Composites,” Front
,”
Chem. Sci. Eng.
,
6
(
2
), pp.
126
131
.10.1007/s11705-012-1279-0
45.
Mukhopadhyay
,
A.
,
Chu
,
B. T. T.
,
Green
,
M. L. H.
, and
Todd
,
R. I.
,
2010
, “
Understanding the Mechanical Reinforcement of Uniformly Dispersed Multiwalled Carbon Nanotubes in Alumino-Borosilicate Glass Ceramic
,”
Acta Mater.
,
58
(
7
), pp.
2685
2697
.10.1016/j.actamat.2010.01.001
46.
Baino
,
F.
,
Barberi
,
J.
,
Fiume
,
E.
,
Orlygsson
,
G.
,
Massera
,
J.
, and
Vern
,
E.
,
2019
, “
Robocasting of Bioactive SiO2-P2O5-CaO-MgO-Na2O-K2O Glass Scaffolds
,”
J. Healthc. Eng.
,
2019
, pp.
1
12
.10.1155/2019/5153136
47.
Liu
,
X.
,
Rahaman
,
M. N.
,
Hilmas
,
G. E.
, and
Bal
,
B. S.
,
2013
, “
Mechanical Properties of Bioactive Glass (13-93) Scaffolds Fabricated by Robotic Deposition for Structural Bone Repair
,”
Acta Biomater
.,
9
(
6
), pp.
7025
7034
.10.1016/j.actbio.2013.02.026
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