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Available online at www.sciencedirect.com

ScienceDirect

journal homepage: www.intl.elsevierhealth.com/journals/dema

The tooth: An analogue for biomimetic materials

design and processing

Van P. Thompson ∗
Kings College London, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: Objective. Overview the development of human tooth; enamel, dentoenamel junction and
Received 15 August 2019 dentin in regard to hierarchical structure property relationships and how these component
Received in revised form structures can serve as templates for the design of tough materials.
21 August 2019 Methods. The dental, engineering and ceramic literature (PubMed, Science Direct, Google
Accepted 28 August 2019 Scholar) covering the last 20 years was over viewed regarding enamel and dentin character-
Available online xxx ization, structure-property studies, as well as, publications related to bioinspired materials
with relationship to tooth structure. Relevant publications were selected for inclusion.
Keywords: Results. Enamel has been studied and modelled at 3 hierarchical levels, prism structure,
Dentin parallel prism interactions and enamel decussation effects. Missing is a 4th level where
Enamel the previous three hierarchies are combined with the 3D arrangement of these levels in
Dentoenamel junction enamel areas. Aspects of the enamel prism infrastructure and prism decussation have been
Mineralized tissues used in 3D printing of Bouligand ceramic structures. The dento-enamel junction serves to
Graded structure arrest cracks and reduce the stress in enamel as a graded elastic modulus layer, leading
Enamel prisms to development of dental ceramics with increased strength and fatigue resistance. Dentin
Decussation is a compliant structure that supports enamel mechanically and may, through providing
Bioinspired design interstitial fluid at the DEJ, allow repair of microcracks in enamel. Adequate models of dentin
properties remain to be developed as it remains highly variable in tubule lumen size and
the degree of mineral density around and between tubules.
Significance. The structure of teeth, particularly the 4 hierarchical levels of enamel, creates a
vital, hard, tough damage tolerant system for inspiring new materials.
© 2019 The Academy of Dental Materials. Published by Elsevier Inc. All rights reserved.

Contents

1. Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .00
2. Enamel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.1. Enamel development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.2. Enamel prisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.3. Enamel prism properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.4. Enamel prism structures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

∗
Correspondence to: 5 Hellyer Rd, Tenants Harbor 04860, USA.
E-mail addresses: van.thompson@nyu.edu, van.thompson@kcl.ac.uk
https://doi.org/10.1016/j.dental.2019.08.106
0109-5641/© 2019 The Academy of Dental Materials. Published by Elsevier Inc. All rights reserved.

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2.4.1. Inner enamel zone. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .00

2.4.2. Enamel decussation zone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.4.3. Enamel parallel prism zone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.5. Wear of enamel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.6. Role of decussation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.7. Recent modeling of enamel . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.8. Worn enamel physical model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.9. Ameloblast path and space filling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
2.10. Other factors in enamel performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
3. Dentoenamel junction (DEJ) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4. Dentin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.1. Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.2. Dentin structure . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.3. Dentin properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
4.4. Dentin models . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
5. The tooth as a model for biomimetic/bioinspired materials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
6. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00

1. Introduction 2. Enamel

Much is known about teeth and their structure. Teeth have 2.1. Enamel development
long been studied by paleontologists and anthropologists,
since they degrade much more slowly than bone; in fact, Tooth enamel is the hardest tissue in the body, with a hardness
teeth and particularly enamel are the source of our primary comparable to that of window glass, and is highly fatigue and
knowledge of many ancient species. Human teeth are gen- wear resistant. Human enamel is laid down by cells in a pro-
erally representative, with an epithelium-derived outer shell grammed temporal and spatial sequence to provide the overall
of enamel that is highly mineralized, hard, stiff, and wear shape of the tooth. These cells that make enamel develop
resistant. The enamel is supported both mechanically and bio- from the invagination of epithelial tissue during fetal devel-
chemically by a mesenchyme-derived dentin, which is vital, opment. In what is known, because of its shape, as the ‘bell
less mineralized, softer, and more compliant. Dentin is main- stage’ of tooth development (ca. 14th week of intrauterine
tained by the dental pulp, which is cellular and innervated and life), the epithelial cells on the inside of the bell align and
has a vascular plexus. Dentin and enamel are joined at the this leads to a concentration of mesenchyme cells in what
dentoenamel junction (DEJ) which is a biomechanical transi- appear to be a one-to-one relationship. More accurately the
tion zone between these materials. In this review we detail latter are ‘ectomesenchyme’ cells, as the first branchial arch,
each of the mineralized tissues and how they develop into whose ectodermal cells migrates into the mesenchyme in the
structural components with unique properties that can serve area of the developing jaws [3]. During this alignment along
as a basis for biomimetic/bioinspired materials design. Den- a basement membrane (BM) an extracellular collagen net-
tists understand that enamel, even when heavily worn does work is created that extends from the epithelial cells to the
not generally fracture when supported by dentin. Also, that mesenchyme cells and is comprised of Type IV, VI, VII and
teeth routinely exhibit vertical fractures in enamel, particu- XVII, fibronectin and laminin [4]. Later the BM degrades and
larly with age, but this does not lead to caries or fracture (Fig. 1). is removed during the later stages of morphogenesis leading
None the less, our understanding of the intriguing structure to the DEJ in mature teeth. The composition changes leave
of teeth and their reliability in lasting a lifetime is still incom- Type IV and VII collagen. This latter is known for anchoring of
plete. epidermal cells to dermis or mesenchymal cells and appears
In a recent comprehensive review of multiscale toughening to function in enamel near the DEJ as part of the enamel
mechanism employed by nature, tooth enamel and dentin are prism sheath as well as being seen distinctly associated with
well positioned on an Ashby plot of toughness versus elastic enamel tufts [5]. The epithelial cells begin to elongate and
modulus considering a range of natural and structural mate- transform into ameloblasts, and the mesenchyme cells trans-
rials [1]. form into odontoblasts [3]. The ameloblasts elongate as they
Please note there is a comprehensive review of the mechan- differentiate to a diameter of about 4–6 ␮m and 20–30 ␮m long.
ical properties of teeth covering the literature through 2013 Odontoblast are believed to use this elongation as a signal to
[2] consequently details of physical properties will herein be differentiate, increase in size, and begin to lay down predentin
limited. [6]. Mechanical force has been shown to induce differenti-

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Fig. 1 – Clinical observation of tooth conditions. (A) Heavily worn mandibular incisors. Note the enamel is not fractured but
smooth. Subsequent loss of the less wear resistant dentin will lead to enamel flaking. (B) Vertical cracks in incisors from an
older individual have little consequence to subsequent function.
ation into odontoblasts from human dental pulp cells [7].
Odontoblasts remain in approximately cuboidal shape with
a diameter of approximately 7–10 ␮m but elongate as they lay
down dentin while ameloblasts prior to differentiation at the
DEJ basement membrane have a similar diameter. The early
elongation and decreased diameter of the ameloblasts as com-
pared to the odontoblasts leads to pulling on the BM and the
collagen network forming between the two, creating a local
wrinkling/crimping of this structure that will become the den-
toenamel junction (DEJ) [8,9]. The basis for wrinkling is well
described in other fields [10–12]. Seen in cross-section the DEJ
appears as scalloped; but viewed in 3-D, when the enamel has
been dissolved, the circular ridges and pits of the DEJ structure
become apparent [13]. The gene expression controlling tooth
morphogenesis is not fully understood, but a large number of
genes have been identified as involved in tooth development
[14].
2.2. Enamel prisms
The ameloblasts are arranged in a close, overlapping array.
Each cell has a tail that extends between its neighbors (Fig. 2A),
so that if observed from above the DEJ, they interdigitate; this
is known as a keyhole structure seen distinctly on the outer
surface of the tooth (Fig. 2B). Once aligned with their neigh-
bors, the ameloblasts begin to mature and to lay down the
enamel structure. The maturation of ameloblasts starts from
what will become the cusp tip or the incisal edge of the tooth
(but at this stage is the inner top of the bell) and proceeds
apically. The last enamel to begin formation will be that clos-
est to the cementoenamel junction (CEJ). Upon differentiation
the ameloblast at its terminal end (nearest to the DEJ) takes
on a ‘brush border’ appearance and begins to excrete pro-
teins, in particular amelogenins through the Tomes process.
The amelogenins are the template molecules for the nucle-
ation of calcium phosphate to form, with maturation, dense
hydroxyapatite (HA) nanocrystallites. These nanocrystallites
vary in orientation with those near the center of the structure
aligned with the long axis and those peripheral more later-
ally oriented. The lateral orientation is pronounced in the tail
region (Fig. 3A). How the appearance of these nanocrystallites
changes with sectioning direction though the enamel is shown
schematically in (Fig. 3B).
There are also protein fragments remaining between
the nanocrystallites. A comprehensive discussion of how
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3
ameloblasts and their secreted amelogenins create the dif-
fering orientation of apatite fibers between the head and tail
region of prisms is presented by Habelitz (Fig. 4) [15].
Via this process each ameloblast will create one enamel
prism of approximately 5 ␮m in diameter, which is also
referred to as an ‘enamel rod’ (Fig. 2). Individual prisms have
been shown to extend from the DEJ to the enamel surface
through various paths and not change diameter [8].
Prisms are joined to their neighbors by a thin organic layer
referred to as a ‘prism sheath’. Enamel is only 1% by weight
organic matter, primally located in the prism sheath. When
bulk enamel is loaded to the point of cracking, the resultant
cracks preferentially propagate through the protein sheath,
going around and along the prisms. The tensile strength
of bulk enamel is lower when loaded perpendicular to the
prism direction (11.4 ± 6.3 MPa) than it is when loaded parallel
(24.7 ± 9.6 MPa) [16].
The role of enamel organic content on crack resistance has
been shown to be of importance [17]. Removal of the proteins
resulted in a 40% decrease in fracture toughness. This was
attributed to embrittlement of the crack bridging ligaments
that remain along the crack path and to less crack deflection.
The laying down of enamel by the ameloblasts proceeds
at a rate of about 4 ␮m per day [18]. If an ameloblast were to
migrate directly to the enamel surface, the earliest it could
reach the outer dimension of a 1.5-mm-thick enamel cusp
would be (1500/4 =) 375 days. We note that ameloblasts do not
proceed directly radially from the DEJ to the surface (as dis-
cussed below), so much more time is necessary to develop
enamel for permanent teeth. First molar enamel thickness
varies by cusp from 1.4 to 1.7 mm [19], increases from the first
molar to the third [20], and is generally slightly thicker for
females [21]. First molar enamel develops from birth through 3
years of age. The enamel thickness on the facial or incisal of a
central incisor is approximately 1.3 mm [22]. Once ameloblasts
reach the outer extent of the enamel they transform to a more
cuboidal shape and die. What signaling controls this process is
not known. The calcification of the developing enamel prism
occurs gradually and continues for some time even after the
tooth erupts into the mouth. This makes newly erupted teeth
sensitive to decalcification and caries for more than a year.
Enamel growth periods are seen via structural features in
the enamel. Ameloblasts mature in layers or fronts from the
cusp toward the DEJ, resulting in layers called ‘striae of Ret-
zius’. These appear at the external surface of the tooth as
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Fig. 2 – Etched enamel and prism appearance. (A) SEM of phosphoric acid etched (40%, 60 s) of maxillary central incisor
facial surface, note the step created by acid dissolution. (B) Higher magnification of enamel near the etched facial surface of
another incisor, exhibiting keyhole arrangement of the enamel prisms.

Fig. 3 – Enamel interprism crystallite orientations and prism arrangement neat the tooth surface. (A) Crystallite direction
changes across the prism diameter (face) as well as in the transition between the tail and the body of the rod (black arrows).
Image modified from Essentials of Oral Histology and Embryology: A Clinical Approach, 3rd Edition. C.V. Mosby, 012006. pp.
99–100. (B) Ameloblast keyhole arrangement (upper right). Each cell has a head and a tail (hat extends between its
neighbors). Observe the discontinuity of the enamel crystallites. Each arrow in the upper right denotes a sectioning plane
through the enamel. Each arrow points to the diagram depicting the microscopic view of that sectioning plane in the
enamel. Image modified from Boyde [118].

‘perikymata’, with more pronounced layers in the cervical
enamel. Between striae in humans, there are 8–9-day growth
increments designated as the ‘repeat interval’ [23]. Within the
repeat interval of enamel there are ‘rhythms’, seen as vari-
ation in the width of the daily growth increment and in the
density of calcification. These same rhythms are seen in the
lamellae of bone [23].
2.3. Enamel prism properties
The properties of enamel prisms and how these properties
change with prism orientation have been studied extensively
since the advent of nanoindentation techniques [16,24–26].
Enamel is hardest along the central axis of the enamel prism
because of the alignment of the HA crystallites in this direc-
tion. When indentation occurs along the axis of one or several
prisms the enamel appears to deform as metal [26]. Nanocrys-
tallite direction changes across the prism diameter (face) as
well as in the transition between the tail and the body of
the prism which affects local properties [27]. Nanoindentation
across an axial plane section of the enamel allows the map-
ping of hardness and elastic modulus, with enamel shown to
be both harder and of higher modulus at the outer surface of
the tooth [28]. Higher hardness and modulus are the basis for
the wear resistance of the enamel surface. The higher hard-
ness is likely related to the parallel alignment of the enamel
prisms over large areas of the outer enamel surface, an align-
ment observed when the enamel surface is etched by acid
(Fig. 2). Enamel changes with age, becoming harder at the
surface but not at the DEJ [29].

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Fig. 4 – Schematic proposed by Habelitz [15] for the mechanism or enamel rod formation by ameloblasts that allows for the
prism tail region (interrod) to be elaborated by the ameloblast [15]. The Tomes process of the ameloblast (disTP and proxTP)
secretes the matrix protein scaffolds (amelogenins-dark rectangles) on which the initial hydroxyapatite ribbons form
(vertical lines leading into the rod). These ribbons, 2–3 nm thick and 10–20 nm wide, later grow with enamel maturation to
become nanocrystallites (50–70 nm in diameter highly variable in ␮m length).

At the nanohardness level (Berkovitch indenter) the elas-
tic modulus of enamel is strain rate dependent (the strain
rates used in no way replicate the strain rates in chewing
or those found in bruxism), what is demonstrated over the
range of strain rates employed is that hardness appears to
be dominated by the interlayer shear modulus of the residual
protein matrix associated with the HA nanocrystallites [30].
Drying of enamel increases prism surface hardness but leads
to increases in nanoscratch depth indicating a change in dam-
age accommodation [31]. Using nanospherical indentation the
contact elasticity of enamel rods along their axis has recently
been delineated [32].
finite number of ameloblasts must each contribute to this pro-
cess and may act in unison to create three zones of enamel
structure.
2.4.1. Inner enamel zone
Near the DEJ there is a narrow zone where the prisms extend in
groups almost perpendicular to the DEJ. Here there are “dead”
tracks and enamel tufts extending into and often through this
zone. Dead tracks and tufts are thought to be the result of
death of one or more ameloblasts after leaving the DEJ. These
apparent defects are thought to be sites for crack initiation
with high loads applied to the tooth [33].

2.4.2. Enamel decussation zone

2.4. Enamel prism structures
Enamel has unique abilities, based upon its structure, to
withstand cracking and resist fatigue. This, in part, can be
attributed to the complex pattern made by the ameloblasts as
they lay down enamel and traverse and fill the space between
the dentin and outer surface with a mineralized structure. A
Less than one cell body length (20–30 ␮m) beyond the DEJ
groups of ameloblasts begin ‘enamel prism decussation’
(crossing of prisms or groups of prisms). Decussation leads
to Hunter–Schreger bands (HSB) seen in sections of enamel
viewed with the light microscope [34]. In humans such decus-
sation is derived from bundles of what are thought to be 50–100
prisms that follow a complex path from the DEJ to the sur-

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Fig. 5 – Aspects of human enamel decussation. (A) Diagram of changing direction of enamel rods at a decussation interface.
(B) Occlusal to gingival view depiction of the direction of successive layers of enamel prism bundles as they develop from
the DEJ. (C) Polished and lightly etched section though a mandibular 2nd molar lingual cusp view in reflected circularly
polarized light. Note the occlusal slope of the decussation band as the extent of decussation toward the tooth surface the
tooth surface. Here the parazones appear thicker than the diazones, but this may be a lighting artifact. At the cusp tip the
decussation bands do not appear to have originated from the DEJ which may be the result of the bands course through the
cusp region to fill the enamel space.

Fig. 6 – Decussation observed in reflected circularly polarized light. (A) Buccal lingual section of a mandibular 2nd molar
exhibiting extensive decussation extending well toward the tooth surface. (B) Higher magnification view of the cusp tip area
with gnarled enamel present.

face in what is known as ‘multiserial patterning’. These prism
groups may be associated with the scallop pattern of the DEJ
[35]. The decussating prism groups can be seen fanning out
from the DEJ in incremental, stacked planes proceeding api-
cally from the cusp tip or the incisal edge (Fig. 5A + B). Each
plane is oriented approximately parallel to the occlusal plane
of the tooth. In each plane the ameloblast groups grow out-
ward at roughly a 40◦ angle to the radial direction, with one
plane orienting left and the maturing plane below it oriented
right. From incisal to gingival in each plane there are several
prism groups. This thickness of the bands and the transition
zone between them can be seen in a buccal to lingual verti-
cal section of a molar cusp taken in polarized light (Figs. 5B,
6 ). In small mammals such as rodents enamel is thin but
must withstand high stresses. This evolutionarily has resulted
in uniserial decussation where individual cells cover a tortu-

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Fig. 7 – Examples of uniserial decussation found in fossilized rodent teeth. Note the changes in direction of the ameloblasts
as they proceed from the DEJ. In panel 10 the interwinding of individual ameloblast and the separation as the orient to a
parallel arrangement at the surface [119].
ous but organized path from the DEJ to the enamel surface
(Fig. 7).
The light and dark bands are referred to as parazones
and diazones in the palentology literature where the enamel
prisms are considered as light pipes. In parazones the prisms
are proposed to be oriented in a decussation plane oriented
toward the viewer, while the dark diazone has prisms in a
plane oriented away from the viewer.
Following the course of individual enamel rods outward
through the enamel for lesser apes and humans has shown an
undulating path taken by the ameloblasts is most pronounced
in humans [36]. This Macho group produced models of undu-
lating rods groups that exhibit Hunter Schreger type bands
similar to the appropriate species [36]
Note that the decussation plane also bends occlusally as it
proceeds outward. (Fig. 6A) This bending was not noted in the
above study of enamel rod coursing. Near the cusp tip or incisal
edge the decussation pattern becomes more complex as the
ameloblast fronts proceed to fill the space. When sectioned,
this complex pattern beneath the cusp tip or incisal edge is
referred to as ‘gnarled enamel’ (Fig. 6B) [18].
The packing density of Hunte–Schreger bands (HSB) in
enamel varies by tooth with a packing density maximum
of 12.7 ± 1.1/mm for central incisors to 15.5 ± 2.0/mm for
mandibular first molars [34,37]. This implies that the width of
the bands is greater in incisors than molars. This leads to the
question of whether the prism groups that form decussation
are associated with the scallops of the DEJ. Brauer et al. [13]
have measured the area and circularity of DEJ tooth scallops.
Molars have the highest area per scallop of about 1400 ␮m2
and decrease to about 600 ␮m2 for incisors. Given a DEJ con-
tact area of an ameloblast of ∼16 ␮m2 there would be 88 to 37
prisms/scallop, respectively. If this is the situation then more
groups of scallops must be contributing to the decussation
bands in incisors as compared molars based on the packing
density studies [34,37]
Habeltiz pointed out the need for a change from keyhole
enamel prism morphology to a more circular prism morphol-
ogy in the developing pits of the enamel created by the Tomes
process of the ameloblast [15]. The result is more circular
shaped prisms often seen in decussated areas of enamel. With
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7
the change to the more circular morphology the prisms can
slide past one another which he proposes is necessary for
development of decussation. Radlanski et al. describe decus-
sating enamel as having an arcade structure that changes to
keyhole arrangement at the enamel surface [38].
2.4.3. Enamel parallel prism zone
Near the outer third or less of enamel the prism bundles align
in a more parallel arrangement with a predominat keyhole
appearance when viewed in cross section. The orientation of
the prisms is inclined occlusally to the enamel surface, chang-
ing from about 10◦ near the cervical to 70◦ near the cusp tip
of a molar [8]. This parallel orientation of prisms is proposed
to provide enamel with the highest hardness and stiffness.
Models studies affirm the high stiffness with a parallel prism
arrangement and indicate that hardness is governed by inelas-
tic shearing between prisms. Increasing decussation leads to
a reduced hardness as shown in several studies [29,39] This
parallel prism structure exhibits both viscoelastic and vis-
coplastic behavior on the microscale [24].
At the enamel surface of the tooth is a layer of apris-
matic enamel of 5–20 ␮m in thickness composed of unaligned
nanofibers of apatite [3]. Whether this aprismatic zone is the
result of mastication, adsorption of salivary pellicle and recal-
cification from the saliva or is created during morphogenesis is
not well delineated. Most studies of enamel remove this layer
to study the underlying prismatic structure.
2.5. Wear of enamel
Wear of enamel is of interest to paleontologists. It has been
studied over 5 years on a sliding contact basis with and with-
out silica microparticles [40,41], and with increasing particle
concentration [42]. These studies use embedded molar teeth
with cusps then ground to create flats for study. This likely
involves gnarled enamel and not the parallel prism structure
which is not discussed. These microwear studies extend to the
effect of strain rate on impact wear of enamel [30]. However,
the Zhang et al. study had no translational component to the
impacts which were conducted at 90◦ to a flat 0.2–0.3 mm in
depth from the molar cusp occlusal surface). Images indicate
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a preparation smear layer on the prepared surface. Very light
etching using the latest technique to remove this smear layer
[43] might well provide insight in to the local mechanisms of
wear or damage near the contact zone which likely involves
the peripheral area.
2.6. Role of decussation
The incisal or occlusal plane of decussation provides enamel
the ability to resist cracking in this overall direction, as a
crack must run a very long distance to traverse the struc-
ture [44–47]. This is not the case in the incisal or occlusal
to gingival direction. Teeth often show vertical cracks in
enamel without consequence but rarely horizontal cracks,
as the latter are quite detrimental [48]. Researchers have
been investigating the ‘fracture toughness’ of enamel—that
is, the energy necessary to propagate a crack [44,49,50].
Using very small sections of enamel to make compact ten-
sion and fracture toughness coupons, they have shown that
the fracture toughness from surface inward or from the DEJ
outward increases by an order of magnitude as the crack
extends from either surface. This behavior where the energy
necessary to propagate a crack increases with crack depth
is termed an R curve response which is characteristic of
tough ceramics. Enamel R curve behavior is attributed to
enamel decussation and varies with enamel orientation (Fig.8)
[50,51]. Enamel decussation which involves layers of prisms
or reinforced sheets with differing orientation of succes-
sive layers is known in engineering as a Bouligand structure
[52,53]. Bouligand structures are known for their R curve
behavior. Decussated enamel is a complex Bouligand struc-
ture.
The role of the organic component in enamel fracture
toughness has been investigated [17]. Organic removal leads
to crack initiation at lower loads while the fracture toughness
was reduced by 40%. Organic removal resulted in crack paths
little deviated by decussation.
Intact molar teeth, when loaded at the cusp tip exhibit
high resistance to enamel cracking, with exceptional resis-
tance to fracture in the occlusal as opposed to the axial plane
[54–56]. Cracking preferentially occurs perpendicular to the
plane of decussation (Fig. 9). Which leads to vertical cracks
seen clinically (Fig. 1). The resistance to horizontal fracture is
of particular importance in the long canines of mammal car-
nivores which must grasp and tear at prey. In this group the
bands of decussation are perpendicular to the axial plane but
now undulate in the axial direction while coursing to the tooth
surface [57]. The ratio of gingival width to axial height above
the gingiva of canine teeth scales with carnivore size [57].
2.7. Recent modeling of enamel
The advent of focused ion beam (FIB) milling permits mechan-
ical testing of individual prisms or small groups of prisms.
Prism damage modeling using microcantilever beams cre-
ated with FIB has been conducted on bovine enamel [58].
These involve triangular beams comprised of either small
interprism specimens with nanofibers running axially to spec-
imens with multiple prisms. The multiprism specimens are
from outer enamel (parallel prisms) or enamel with decussa-
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tion bands oriented at right angles to the beam axis [59,60].
The beam specimen sizes and orientations are suggested to
comprise 3 levels of hierarchy. These results have been com-
bined with studies of the compression of enamel micropillars
(1.1–1.42 ␮m diameter top to bottom with a height mean of
2.1 ␮m) of HA nanocrystallites in transverse, oblique and lon-
gitudinal directions [61]. These pillars show strain hardening
with load cycling in all orientations. Strength in compression
is ascribed to mineral contacts between apatite nanocrystal-
lites.
An et al. [62] modeled their groups work on loading enamel
prism micropillars and the effect of crystallite orientation
in the enamel prism. The prism was only considered as a
columnar structure. They concluded that laterially oriented
crystallites in the prism delaminate first, dissipating energy,
while those axially oriented maintain prism stiffness.
Prior to the above microbeams studies a biomechanical
model for the enamel prism key hole structure was developed
[63]. Modelled was the interactions across numbers of prisms
in axial or lateral loading. Included was consideration of the
orientation of the HA fibers within the prism head and the
transition to more lateral orientation in the prism tail [64,65].
Variation in keyhole/tail length on outcomes was considered.
There was no reference to this keyhole modeling work in any
of the FIB enabled studies.
The above FIB enabled results by the Schneider group have
now been combined into a hierarchical damage accumulation
system using a hierarchical cracking model (Fig. 10A) ([66]:
Ozcoban, 2018 #834). The cantilever microbeam results have
been supplemented with 3-point loading of bovine enamel
macrobeams (Fig. 10B). The observations and modelling indi-
cate that cracks build to a critical density at the internal prism
structure (hierarchical level 1) before a crack initiates in the
next hierarchical level where the prisms are parallel. Once
cracks are of sufficient density in the parallel region a crack
can then extend into the decussation hierarchical level and
with increasing stress propagate to specimen fracture. The
model fits the linear load to fracture curves for the macro-
beams. This study is limited to macro-beams of the occlusal
gingival orientation which exhibit horizontal cracking (paral-
lel to decussation directions). A study with beams of mesial to
distal orientation is warranted to compare occlusal-gingival
oriented damage accumulation and fracture stress although
the change in initiation and propagation crack KIC in this direc-
tion has been published (Fig. 8) [51].
Pro and Barthelat [67] used a Discrete Element Model for
enamel prism interactions to capture the effects of prisms
in parallel or various angles of decussation when subjected
to contact to evaluate elastic modulus, hardness and frac-
ture resistance. They used a virtual fracture specimen to
model crack growth through rupture of interfaces with a crack
extending though parallel enamel into a decussation zone.
If prism fracture is avoided the resistance curves increase
greatly within the inelastic region with crack branching and
tortuosity increasing toughness substantially. Increasing the
stiffness of the prisms relative to the prism interface resulted
in higher stiffness and crack resistance. Increasing decussa-
tion angle between layers increased the size of the inelastic
region resulting in increased crack resistance. Only decussa-
tion angles up to 30◦ were modeled.
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Fig. 8 – Compact tension fracture toughness testing of enamel [51]. (A) Orientation of the cube of enamel where L indicates
crack penetration from outer to the inner surface n longitudinal/circumferential direction and T cracks with an occlusal to
gingival direction (a vertical crack/occlusal gingival direction). (B) Specimen orientations with decussation shown. The
direction of the crack opening is indicated by the heavy arrows. (C) The compact tension specimen configuration with crack
opening from a notch created in the enamel block which is embedded in resin-based composite (D) Values of KIC for
initiation of cracks. (D) KIC findings for propagation of cracks. Note the difference in Y axis scale. Enamel R curve behavior is
present in all tested orientations.

Fig. 9 – Contact fatigue testing of enamel. (A) Orientation of sections tested from cusps of molar teeth. (B) Example of contact
fatigue testing (3.18 mm radius SiC ball with load of 200 N and 10,000 cycles. Circle indicates the contact area. The long
cracks extending from the contact are preferentially orientated perpendicular the decussation planes indicating vertical
(occlusal to gingival) tooth cracks.

The Pro and Barthelat model does not address the key 0.2–0.3 mm in depth which can involve parallel, decussated
hole aspects of enamel but rather treats the prisms as a close and gnarled enamel [68]. At higher loads prism fracture was
packed structure. The same is true for studies where mod- observed in the decussated enamel while within parallel
els of contact indentation propose sliding between prisms but prism areas interface cracking was observed.
ignore the keyhole contribution in distribution of stress in the
tensile zone around the contact.
2.8. Worn enamel physical model
Missing in these hierarchical models is the 4th level which
is the change in direction of the decussation bands as they
One model to investigate load fracture patterns in enamel is a
extend occlusally on teeth such as premolars and molars
glass dome filled with epoxy [69]. A flat at the apex of the dome
(Figs. 5 and 6) or, additionally consideration of the decussated
can be ground to varying depths simulating worn enamel. It
gnarled enamel found beneath cusps.
can be shown that with a distributed load (soft or hard) the
Contact fatigue testing of the enamel on the cusp tips of
load to failure is not compromised with wear depth (Fig. 11).
intact teeth has been conducted but on polished flat surfaces
Only with a hard sphere load with its high contact stress does

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Fig. 10 – Hierarchical organization of enamel as used in modeling structure property relationships [66,120]. (A) The three
dimensionally ascending levels of structure. (B) Occlusally gingivally oriented microbeam of bovine enamel subjected to
3-point loading exhibiting longitudinal/horizontal cracking regimes [120].

Fig. 11 – Testing of model for worn tooth cusp enamel fracture [56]. (A) Loading figuration for 1.5 m thick glass dome filled
with epoxy load tested with a hard sphere (SiC–HS) or distributed loads via a hard steel flat (HF) or a low stiffness “soft
“silicone pad (SF). (B) Critical load to failure with glass surface removal depth. Note that with disturbed loads the epoxy
could be exposed on the “occlusal” surface (removal depth greater than glass dome thickness) and failure load has hardly
changed. With SF loading there was no initial crack descending from the occlusal (HS and HF) but rather a “median” crack
(denoted by M in SF) initiating and extending immediately to the occlusal surface.

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wear depth reduce the critical load. Substituting an R curve
ceramic for the glass might increase the critical load to failure
but not the overall results This work is based upon studies of
human molar tooth facture in loading [56,69,70].
2.9. Ameloblast path and space filling
How ameloblasts, laying down enamel, fill the enamel space
remains to be elucidated. Radlanski suggests that recruit-
ment of ameloblasts from the extending cervical loop leads to
upward pressure on the ameloblasts laying down enamel and
this the wavy path of the prisms occurs and fills the enamel
space [71]. This contrasts with modeling based upon cells as
automata directed by strain cues [72]. These stain cues can
lead to bundles and sheets extending into the enamel in pat-
terns resembling decussation [73].
Decussation plays a role in the space-filling problem asso-
ciated with enamel but it is not clear that this is sufficient.
Recall that one ameloblast leads to one prism which does
not change in diameter [8]. The ameloblast advancing front
begins at the cusp tip and propagates toward the cervical loop.
Given the larger surface area of the enamel, as compare to the
dentin, and that the prisms at the surface of the tooth are
aligned parallel to one another, almost twice the number of
cells is required to populate the enamel surface as compared
the number that occupied the area of the developing dentin
(from the cusp to the cementoenamel junction). Recall that
the ameloblast begins differentiation at the basement mem-
brane that becomes the DEJ and thus rods are anchored to the
DEJ. The space filling of the enamel remains to be elucidated.
2.10. Other factors in enamel performance
Unlike humans, Sea Otter teeth have the HSB extending to
the enamel surface with a density of 19.4 ± 2.5/mm [74]. An
edge chipping test found that otter enamel had a high chip-
ping strength and was 2.5 times tougher when compared to
findings for human enamel [70]. What effect this lack of sur-
face parallel prisms will have on sea otter tooth wear remains
to be determined. Strength versus wear resistance may be
influenced by species lifespan.
Although enamel is hard and wear resistant with its high
HA content (>95% by weight), it is still a hydrated tissue,
and chemicals can diffuse through the structure surprisingly
rapidly. Once through the enamel the chemical species has
rapid access to the pulp via the dentinal tubules containing
the odontoblastic process, making dentin highly permeable. In
a cat canine model Lucifer Yellow dye can penetrate from the
enamel surface to the odontoblasts in the pulp within 30 min
[75]. In extracted teeth subjected to bleaching agents, perox-
ide is present in the pulp within 30 min of external application
[76]. Given the ready permeability of enamel we can hypothe-
size that microscopic cracks on the surface and at the DEJ may
be able to heal through remineralization from saliva or from
dentin interstitial fluid, respectively. There is some evidence
this may be operational [77].
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3. Dentoenamel junction (DEJ)
That the dentin–enamel junction is a natural, multilevel
interface of mechanical importance to the stability of teeth
has been amply demonstrated. Specifically, the DEJ and
associated inner enamel are known to inhibit crack propa-
gation [78], exhibit higher fracture toughness [79], and rarely
undergo catastrophic mechanical failure despite a lifetime
of masticatory and parafunctional loading. Controlled failure
mechanisms are at play [80]. As noted earlier, the DEJ is the
interphase between enamel and dentin, initially formed with
the alignment of ameloblast and odontoblast during the bell
stage of tooth development. It is approximately 60–100 ␮m in
width and is a ‘graded structure’, in that the elastic modulus
makes a nearly linear transition from the enamel (∼70 GPa for
inner enamel) to that of dentin (∼15 GPa) [81–83]. The change
in the calcium and phosphate content from the enamel to the
dentin is thought responsible for this gradient in modulus.
A graded structure serves to lower tensile stresses substan-
tially at the interface of a brittle material with one of lower
elastic modulus, resulting in increased strength and fatigue
resistance [84,85]. The DEJ gradient moves the highest ten-
sile stresses into the bulk of the enamel during function and
reduces those at the interface by nearly 50% [86]. A graded
interphase has also been identified between cementum and
dentin [87].
The scalloping of the DEJ has been proposed and modelled
to distribute stress across a larger zone of the DEJ to prevent
delamination of the enamel from the dentin [35]. However,
only human teeth exhibit scalloping of the enamel, and many
species have teeth with decussation similar to humans [8].
Human scalloping may be an exadaptation [35].
The is no obvious pattern to DEJ scalloping that relates to
decussation. The transition in properties across the DEJ can be
attributed, in part, to the change in degree of mineralization
but also to the protein density that extends into enamel from
the DEJ (Fig. 12) [4,5].
Oral cancer radiotherapy dosage has been found to have
a significant role in breakdown of teeth related to delamina-
tion of enamel from dentin. Radiation leads to reduction in the
organic component of enamel and dentin near the DEJ leading
to local increases in hardness [88]. Radiation leads to break-
down in Type IV collagen bridging the DEJ which contributes to
this problem [4], likely by reduction in the DEJ fracture tough-
ness.
4. Dentin
4.1. Development
The ectomesenchyme cells that become odontoblasts align
with the ectodermal cap cells that become ameloblasts
[3]. While the ameloblasts are elongating, the odonto-
blasts are already beginning to produce the collagen
network that becomes the DEJ; they then transition
to elaboration of the more complex collagen and pro-
teoglycan structure of dentin. This process and the
gene expression leading to congenital defects has been
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Fig. 12 – The DEJ structure and organic component distribution in enamel. (A) Lightly etched DEJ with the extent of the
organic matric associated with the enamel tufts. (B) Same section stained with Coomassie Blue showing proteins in the
structure (Type IV and VII collagen are noted) [4,5]. (C) Section of premolar tooth near a cusp tip in polarized light extent of
enamel tufting present (Courtesy of T. Bromage, New York University).

reviewed [89]. A SlideShare review also covers the differ-
entiation and role of odontoblasts in dentin formation
(https://www.slideshare.net/shravyashivanand/odontoblast).
The elaboration of the dentin structure and its following
calcification proceed inward at an initial rate of ∼2.8 ␮m/day.
This rate slows as the odontoblasts approach what is the pulp
space and slows further with completion of root formation
and tooth eruption to 0.5 ␮/day [90]. Dentin continues to grow
inward for the life of the individual and leaves a record of
growth-altering events. This is termed ‘secondary dentin
formation’. Dentin is also dynamic in that it can respond to
insults to the enamel, such as caries or excessive wear, and
lay down additional dentin, referred to as ‘reactionary dentin’
or ‘tertiary dentin’. Wear of root surfaces can also lead to
laying down of reactionary dentin [3].
4.2. Dentin structure
Dentin has a structure with tubules that course from the DEJ
to the pulp radially inward, with a broad S shape when the
tooth is sectioned axially. Within the tubules are cellular pro-
cesses extending from the odontoblasts that line the pulp.
The tubules have smaller lateral extensions along their length
that communicate with neighboring tubules, creating a com-
munication and interstitial fluid network that maintains the
dentin.
The collagen structure of dentin is complex, with the colla-
gen oriented in helical like structures to form tubules but then
changed to a more radial orientation in the plane perpendic-
ular to the tubule direction (Fig. 13D). There are proteoglycans
aligned along collagen fibers, and these play a role in miner-
alization and physical properties [91]. Calcification of dentin
starts with nucleation in the gap space between collagen
strands and proceeds outward to expand in the direction of the
fibers, forming elongated crystals of HA that are anisotropic
ally oriented to withstand loading [92]. The dentin around
tubules is more highly mineralized and this zone of miner-
alization, approximately the thickness of the tubule diameter,
is called the ‘peritubular dentin’. Outside of this zone the min-
eral content is lower; these regions comprise the ‘intertubular
dentin’.
Bertassoni has provided an in-depth review of dentin on
the nanoscale [93]. Emphasis is on the molecular make up of
dentin and how the nanostructure elements play critical roles
in mineral content. Included is the small integrin-binding
ligand N-linked glycoprotein (SIB-LING) family which con-
sists of osteopontin (OPN), bone sialoprotein (BSP), dentin
matrix protein 1 (DMP1), dentin sialophospho-protein (DSPP)
and matrix extracellular phosphoglycoprotein (MEPE). There
is evidence these non-collageness proteins may bind collagen
fibrils together along with proteoglycans. The role of these
constituents in nanomechanical properties of dentin is pre-
sented. The hierarchical organization of dentin, enamel and
bone is proposed to serve as templates for bioinspired design
of materials and several applications are overviewed.
Near the DEJ the dentin tubules that form are widely spaced
and about 0.8–1.2 ␮m in diameter, with a distance between
tubules of nearly 10 ␮m (Fig. 13A). This gives a tubule den-
sity of 17 000–20 000 per mm2 . With the radial orientation of
the tubules, tubule density increases to ∼40 000 per mm2 near
the pulp (Fig. 13B) [94]. Inner dentin has a reduced amount of
intertubular dentin, but this does not lead to an increase in
hardness: the overall mineral content changes from the DEJ
toward pulp as the HA particle size decreases with depth [92].
Note that dentin that has been etched and then dried has a
collapsed collagen layer that appears as a gel (Fig. 13A–C). Con-

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Fig. 13 – SEM of dentin tubules and structure. (A) Etched section of dentin near the DEL with small diameter tubules (some
opening with etching). (B) Etched section near the pulp with increased tubule density and large tubule diameter (increased
by etching). (C) Fracture surface of etched dentin near the middle of the enamel. The collagen gel layer left by etching can be
seen. (D) Etched and freeze–dried dentin with collagen fibrils arranged peritubular and intertubular.

trast this with the visible collagen seen in etched freeze–dried
dentin (Fig. 13D).
4.3. Dentin properties
The properties of dentin have been studied to determine its
strength with orientation as well as its fracture toughness.
Using microtensile specimens Gianni et al. [95] have shown
that the tensile strength of dentin perpendicular to the tubule
direction is 62 GPa near the DEJ and reduces to ∼34 GPa near
the pulp. This group also related the ability to bond adhe-
sively to dentin to the area of the intertubular dentin [96] and,
inversely, to the tubule density. The hardness of dentin on a
macroscopic scale (Knoop or Vickers indentation) is isotropic
perpendicular or parallel to the tubule direction at the same
relative depth [94]. Hardness is reduced with depth in dentin
and varies from buccal to lingual [97]. Radicular intertubular
dentin is of reduced elastic modulus and hardness compared
to coronal intertubular dentin [98]. Dentin can also be consid-
ered a graded structure, given its change in properties with
location [99].
Dentin toughness has been studied to understand the
mechanisms that limit crack extension ([100]:Kinney, 2003
#929 [101]). In their review Kinney et al. [102] show that crack
bridging and the formation of daughter cracks are significant
mechanisms for the dissipation of crack energy, so that the
process leading to the toughness of dentin is like fracture
toughness in bone. The R curve behavior of dentin changes
with distance from the pulp with showing increases from
baseline Kic which are related to decreases in tubule diameter
and density toward the enamel [47,103,104].
Replacing the water in dentin with less polar solvents, such
as ethanol, increases fracture toughness [105]. Dentin frac-
ture toughness is reduced with age [105–107], which may help
explain the significant increase in cusp fracture of posterior
teeth with age, in particular those that have been restored.
Restoration often leads to large areas of dentin where the
dentin tubules have been cut and thus can no longer supply
interstitial fluid minerals to the dentin, associated DEJ, and
enamel perhaps affecting fatigue response.
4.4. Dentin models
Only a few models have been proposed for the structure prop-
erty relations of dentin [108]. Qin and Swain constructed a
micromechanics model of dentin base upon circular hollow
cylinders, each of which is surrounded by two circular cylin-
drical shells, a thin shell and a matrix phase. Each layer of
cylindrical shell is modelled as a composite comprised of
proportions of collagen fibrils, with varying degrees of hydrox-
yapatite mineralization. Each cylinder assembly is loosely
connected to its neighbors. The cylinders are filled with water
(or gas in the case of a dry dentin composite). Evaluated was
the effect of mineral content, porosity and thickness on each
cylindrical grouping. The findings were compared to nano-
indentation results and were in good agreement with the
model.
Modeling of the density of tubules, lumen size and the
degree of peritubular calcification has been investigated [104].
Using a Balshin porous materials model the fracture tough-
ness of young and old dentin was compared. The model agreed
with the finding for young dentin but the reduced tubule
lumen and high mineral content of aged (sclerotic) dentin

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Fig. 14 – Bioinpired hierarchical composite structure by 3D extrusion additive printing and processing [114]. (A) Thin
alumina plates (∼5 ␮m diameter, 0.5 ␮m thickness) and fine particles mixed into a water and surfactant slurry organized
into an order structure by shear fields when extruded through a 25 mm long 0.41 mm diameter nozzle. (B–D) Filament
arrangement of test specimens after printing, drying, sintering and then epoxy infiltrated and cured. (E–H) SEM of the
fracture surface for each above structure. (H) Double cantilever crack test configuration. (I) Photograph of test specimen at
point of loading. (J) Graph of KIC versus crack length showing R curve behavior for the Bouligand structure. Videos of crack
propagation through structures is available at: https://doi.org/10.1038/s41598-017-14236-9.

resulted in an overestimate of observed facture toughness. orientation. This group has similarly investigated the struc-
Surprisingly, no reference was made to the micromechanics ture property relationships of a range of biomimetic Bouligand
model developed by Qin and Swain [108]. structures created via 3D printing [1].
In 3D extrusion printing of ceramics and cements addi-
tives play a key role in ceramic ink rheology. As an example,
a nanoclay additive allows Portland cement to be 3D printed
5. The tooth as a model for
through a 400 ␮m nozzle to create open architecture speci-
biomimetic/bioinspired materials
mens of intricate design including Bouligand structures with
superior specific energy absorption [112]. Previously Portland
The extensive development of additive manufacturing tech-
cement Bouligand structures could only be printed with a
nique is opening avenues to biomimetic materials develop-
1.36 mm nozzle [113].
ment. Graded structures as evident in enamel, the DEJ and
The hierarchical organization of HA nanocrystallites in the
dentin have led to the ability to improve ceramic perfor-
enamel prisms and the decussation of the prisms can be seen
mance. A review of 3D printing of ceramics using powder bed
in new analogue composite structures. Alumina nanoplatelets
techniques points the way to making graded ceramics [109],
in an epoxy matrix can be oriented in a radial pattern when
while the range of additive manufacturing techniques being
extruded through a print nozzle. The printing process can
employed for fabrication of dental ceramic has recently been
produce multiple layers of these prisms to create a Bouli-
reviewed in this journal [110].
gand structure which, when cured and tested, exhibits R curve
A 3D printed analogue of the parallel rod spatial arrange-
behavior (Fig. 14) [114].
ment of prisms found in teeth (here hexagonally close packed
The 3D printing of shear aligned fiber reinforced polymers
discontinuous rods) had higher indentation hardness and
opens a range of possibilities for enamel prism based hier-
stiffness than for off axis oriented or random arrangements of
archical structures [115,116]. Multi-nozzle print heads may
similar rods [111]. Their FEA modeling predicted the observed
permit printing of complex material architectures with graded
indentation deformations and cracking in these rod assem-
or localized properties. Yet, multiple nozzle printing raises
blies with changes in rod aspect ratio, volume fraction and

Please cite this article in press as: V.P. Thompson. The tooth: An analogue for biomimetic materials design and processing. Dent Mater (2019),
https://doi.org/10.1016/j.dental.2019.08.106
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questions as to the interface between different materials that
are printed simultaneously. One solution may be a coaxial
nozzle or multiple coaxial nozzles. Using a microscale coaxial
nozzle multi-metal printing of multigrain structures has been
achieved [117]. This is accomplished by “on-the-fly” switching
and mixing of two metals from a single multichannel nozzle.
Using what they refer to as electrohydrodynamic redox print-
ing, they claim a chemical feature size <400 nm at a spatial
resolution of 250 nm at reasonable printing speeds.
Additive manufacturing offers a wealth of possibilities to
fabricate strong high toughness materials based upon natural
tissues such as enamel, dentin and the DEJ [1].
6. Conclusions
Teeth are unique biological structures that can last a lifetime
in service. Nature, using a cellular approach, has constructed a
hierarchical mineralized fatigue- and damage-resistant struc-
ture, that may be self-healing. This has been accomplished
by
1 Creating highly mineralized enamel prisms with
anisotropic properties bound together by an organic
sheath and a keyhole structure.
2 Parallel alignment of the enamel prisms at and near the
tooth surface for high hardness and wear resistance.
3 Forming extensive enamel decussation proceeding outward
from near the DEJ to function as a crack stopping structure
for surface or internally initiated cracks.
4 Laying down a graded DEJ which distributes stress into adja-
cent enamel while limiting enamel crack extension into the
dentin.
5 Elaboration of a less mineralized vital dentin structure
which provides mechanical support for the enamel while
providing paths for interstitial fluids to reach the DEJ and
the internal enamel mineral.
The structure of enamel, DEJ and dentin provides a basis for
the design of high toughness materials with a broad range of
applications. The advent of extrusion based additive manufac-
turing opens the possibilities for the realization of materials
with enhanced performance in dental applications.
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Please cite this article in press as: V.P. Thompson. The tooth: An analogue for biomimetic materials design and processing. Dent Mater (2019),
https://doi.org/10.1016/j.dental.2019.08.106