MATERIALS SCIENCE
Multiscale engineered artificial tooth enamel
Hewei Zhao^1 †, Shaojia Liu^1 †, Yan Wei^2 †, Yonghai Yue^1 †, Mingrui Gao^1 , Yangbei Li^1 , Xiaolong Zeng^1 ,
Xuliang Deng^2 , Nicholas A. Kotov3,4, Lin Guo^1 *, Lei Jiang1,5
Tooth enamel, renowned for its high stiffness, hardness, and viscoelasticity, is an ideal model
for designing biomimetic materials, but accurate replication of complex hierarchical organization of
high-performance biomaterials in scalable abiological composites is challenging. We engineered
an enamel analog with the essential hierarchical structure at multiple scales through assembly
of amorphous intergranular phase (AIP)Ðcoated hydroxyapatite nanowires intertwined with
polyvinyl alcohol. The nanocomposite simultaneously exhibited high stiffness, hardness, strength,
viscoelasticity, and toughness, exceeding the properties of enamel and previously manufactured
bulk enamel-inspired materials. The presence of AIP, polymer confinement, and strong interfacial
adhesion are all needed for high mechanical performance. This multiscale design is suitable
for scalable production of high-performance materials.
E
ffective combination of diverse mechan-
ical properties is highly desirable for
engineering applications but is difficult
to realize ( 1 ), especially for properties that
require contradictory material design ele-
mentssuchashighstiffness,hardness,visco-
elasticity, strength, and toughness ( 2 – 4 ). Tooth
enamel—the outer shell of teeth with a thick-
ness of several millimeters (Fig. 1A)—is the
hardesttissueinthehumanbodyandexhibits
excellent resistance to deformational and vi-
brational damage ( 5 , 6 ). This unusual com-
bination of properties originates from enamel’s
hierarchical architecture, which is made up of
96 wt % hydroxyapatite (HA) nanowires inter-
connected by confined biomolecules ( 7 ). Most
crystalline segments in HA nanowires in nat-
ural enamel are interconnected by amorphous
intergranular phase (AIP, Mg-substituted amor-
phous calcium phosphate) ( 8 ), which considerably
influences the mechanical performance of
enamel ( 9 , 10 ). Efforts have been made to mimic
the parallel arrangement of nanowires in
enamel to improve the stiffness, hardness, or
viscoelasticity ( 2 , 11 – 14 ) of nanocomposites,
but physical forms are usually limited to coat-
ings with submillimeter thicknesses. It has
proven difficult to assemble analogs of enamel
that retain full structural complexity of the
biological prototype with several essential struc-
tural elements responsible for their mechanical
and biological functions (i.e., nanowire align-
ment, presence of AIP, and the confined or-
ganic matrix) as bulk machinable materials.
The hierarchical structure of tooth enamel
provides a biomimetic blueprint. Self-assembled
HA nanowires with 30- to 50-nm diameters
align with each other, forming nanocolumns
(Fig. 1B) that represent the key structural motif
of enamel. The AIP layer closely connects to
the HA nanowires and has a thickness of 3 to
10 nm (Fig. 1, C and D, and figs. S1 and S2). This
interface characterization implies that there
are strong chemical bonds between the AIP
layer and HA nanowires, which enhance the
interface connectivity and contributeto mechan-
ical improvement (Fig. 1E and fig. S3).
Our materials are made from aligned HA
nanowires coated with amorphous ZrO 2 serv-
ing as the AIP. First, HA nanowires with length
~10mm and diameter ~30 nm [Fig. 1F (left) and
fig. S4] were synthesized by the solvothermal
method ( 15 ). The HA nanowires grew along the
[001] direction with no obvious defects (fig. S5)
and were then coated with a ~3-nm amor-
phous layer of ZrO 2 (A-ZrO 2 ) through in situ
hydrolysis of Zr precursors, followed by sub-
sequent annealing to form the interfaces be-
tween the ceramics in the crystalline and
amorphous phases [Fig. 1F (middle)]. The
geometry and morphology of the HA nano-
wires were retained, and the amorphous layer
was tightly connected to the crystalline core of
HA [Fig. 1F (right)]. The amorphous state and
constituents of the coated layer were demon-
strated by high-resolution transmission electron
microscopy [Fig. 1F (right)], energy dispersive
x-ray spectroscopy (EDS) mapping (fig. S6),
and x-ray diffraction patterns (fig. S7). The
abundance of surface groups–OH and PO 43 – on
HA absorbed Zr4+, contributing to the forma-
tion of the thin, amorphous ZrO 2 layer (Fig. 1F).
ToverifytheroleoftheAIPinmechanical
performance enhancement, in situ tensile tests
were performed on HA and A-ZrO 2 -coated
HA (HA@A-ZrO 2 ) nanowires with a push-to-pull (fig. S8) platform and a Picoindenter 85
nanoindenter in an environmental scanning
electron microscope (ESEM). The fracture
strength and strain of HA@A-ZrO 2 nano-
wires are ~1.6 GPa and ~6.2%, respectively
(Fig. 1G), which are 2.5 and 1.6 times as high
as those of HA nanowires (~0.65 GPa and
~4%, respectively), surpassing the mechanical
properties of bulk HA ( 16 ). Detailed observa-
tion of the tensile process of the HA@A-ZrO 2
nanowire reveals that the nanowires can
endure tensile deformation as large as ~5.2%
before fracture (fig. S9), whereas the value of
HA is ~2.5%. The fracture surface of the HA@
A-ZrO 2 surface forms a crack deflection (fig.
S10) instead of the brittle failure usually seen
in brittle ceramics, which contributed to frac-
ture strain improvement due to the presence
of the amorphous layer.
Dual-directional freezing of HA@A-ZrO 2 nano-
wire dispersions in the presence of polyvinyl
alcohol (PVA) was used to self-assemble macro-
scale composites with parallel arrangement of
the nanowires (Fig. 1H). The polydimethylsilox-
ane (PDMS) wedge produced a bidirectional
temperature gradient, driving the ice crystal
growth in perpendicular and parallel directions
(Fig. 1H). The perpendicular growth of the ice
crystals forced the HA@A-ZrO 2 nanowires and
PVA to occupy the gaps between ice lamellae,
and the parallel growth forced them to acquire
a parallel orientation (fig. S11). After freeze-
drying (fig. S12) and mechanical compression,
dense artificial tooth enamel (ATE) was prod-
uced (Fig. 1H and fig. S13).
ATE is machinable and can be formed into
tooth-like macroscopic shapes (Fig. 1I) with
densely packed parallel columns with microscale
alignment (Fig. 1J). X-ray nanotomography of
ATE reveals that the nanowires exhibit an over-
all architecture of parallel columns for the bulk
composite (fig. S14). The AIP layers between the
HA nanowires are nearly identical to those in
enamel (Fig. 1C), as they have a thickness of
~5 nm (Fig. 1K). Higher-magnification obser-
vation shows the AIP and verifies that the HA
and AIP are closely connected (Fig. 1L). EDS
mapping and line scanning (fig. S15) of the
crystal-amorphous-crystal interface further dem-
onstrate that amorphous ZrO 2 fills the gaps
between HA nanowires. Spectroscopic charac-
terizations (figs. S16 and S17) including Raman,
Fourier transform infrared spectroscopy (FTIR),
and x-ray photoelectron spectroscopy implied
strong chemical adhesion (Fig. 1M) as a result of
coordination between Zr4+and O of PO 43 −
and–OH.ThisisincontrasttosimplephysicalSCIENCEscience.org 4 FEBRUARY 2022•VOL 375 ISSUE 6580 551
(^1) School of Chemistry, Beijing Advanced Innovation Center for Biomedical Engineering, Beihang University, Beijing 100191, China. (^2) Department of Geriatric Dentistry, NMPA Key Laboratory for
Dental Materials, National Engineering Laboratory for Digital and Material Technology of Stomatology, Beijing Laboratory of Biomedical Materials, Peking University School and Hospital of
Stomatology, Beijing 100081, China.^3 Department of Chemical Engineering, Department of Materials Science, Biointerface Institute, University of Michigan, Ann Arbor, MI 48109, USA.^4 Michigan
Institute of Translational Nanotechnology (MITRAN), Ypsilanti, MI 48198, USA.^5 CAS Key Laboratory of Bio-Inspired Materials and Interfacial Science, CAS Center for Excellence in Nanoscience,
Technical Institute of Physics and Chemistry, Chinese Academy of Sciences, Beijing 100190, China.
*Corresponding author. Email: [email protected] (L.G.); [email protected] (N.A.K.); [email protected] (X.D.)
These authors contributed equally to this work.
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