ARTICLE IN PRESS

Journal of Biomechanics 38 (2005) 377–399

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Biomechanics of cellular solids

Lorna J. Gibson
Department of Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 8-135,
Cambridge, MA 02139, USA
Accepted 29 September 2004

Abstract

Materials with a cellular structure are widespread in nature and include wood, cork, plant parenchyma and trabecular bone.
Natural cellular materials are often mechanically efficient: the honeycomb-like microstructure of wood, for instance, gives it an
exceptionally high performance index for resisting bending and buckling. Here we review the mechanics of a wide range of natural
cellular materials and examine their role in lightweight natural sandwich structures (e.g. iris leaves) and natural tubular structures
(e.g. plant stems or animal quills). We also describe two examples of engineered biomaterials with a cellular structure, designed to
replace or regenerate tissue in the body.
r 2004 Elsevier Ltd. All rights reserved.

Keywords: Cellular solids; Wood; Trabecular bone; Plant stems; Titanium foams; Scaffolds; Mechanical behavior

1. Introduction attachment, migration, proliferation and functioning of

In nature, materials with a cellular structure are
widespread. Examples of natural materials with pris-
matic, honeycomb-like cells include wood and cork (Fig.
1a,b), while those with polyhedral cells include the inner
core in plant stems and trabecular bone (Fig. 1c,d). They
also appear as the cores in natural sandwich structures:
in long, narrow plant leaves, such as the iris, and in
shell-like bones, such as the skull (Fig. 1e,f). Natural
tubular structures often have a honeycomb-like or
foam-like core supporting a denser outer cylindrical
shell, increasing the resistance of the shell to kinking or
local buckling failure (e.g. plant stems and animal quills,
Fig. 1g,h). Engineers design biomaterials with a cellular
structure to replace or regenerate tissues in the body.
For example, titanium foams are being considered as
substitute materials for trabecular bone (Fig. 2a). And
porous scaffolds used in tissue engineering are designed
to mimic the body’s extracellular matrix, allowing the
Tel.: 617 253 7107; fax: 617 258 6275.
E-mail address: ljgibson@mit.edu (L.J. Gibson).
cells (Fig. 2b).
The microstructural features of cellular solids affect-
ing their mechanical response are most easily observed
in engineering honeycombs and foams (Fig. 3). Honey-
combs, with their prismatic cells, are referred to as two-
dimensional cellular solids while foams, with their
polyhedral cells, are three-dimensional cellular solids.
The relative density is the density of the cellular solid
divided by that of the solid it is made from, and is
equivalent to the volume fraction of solid. Foams may
be either open (with solid only at the edges of the
polyhedra) or closed (with solid membranes over the
faces of the polyhedra). The properties of the foam
depend on those of the solid making up the cellular
material; in materials such as wood, the cell wall is itself
a multilayered composite material.
The stress–strain curve for a cellular solid in
compression is characterized by three regimes (Fig.
4a): a linear elastic regime, corresponding to cell edge
bending or face stretching; a stress plateau, correspond-
ing to progressive cell collapse by elastic buckling,
plastic yielding or brittle crushing, depending on the
nature of the solid from which the material is made; and

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doi:10.1016/j.jbiomech.2004.09.027
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378 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Fig. 1. Examples of cellular solids in nature: (a) balsa wood (b) cork (c) inner core of plant stem in (g) (d) trabecular bone (e) iris leaf (f) skull (g)
plant stem (h) porcupine quill. (Fig. 1a,b,d,f reproduced with permission from Gibson and Ashby, 1997; Fig. 1h reproduced with permission from
Gibson et al., 1995.)
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L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 379

Fig. 2. Examples of biomaterials with a cellular structure (a) titanium

foam (courtesy Louis-Philippe Lefebvre, National Research Council of
Canada) (b) collagen-glycosaminoglycan scaffold for tissue engineer-
ing. (Reprinted from Progress in Materials Science 46, 273–282
Freyman TM, Yannas IV and Gibson LJ Cellular materials as
scaffolds for tissue engineering, copyright 2000, with permission from
Elsevier.)

densification, corresponding to collapse of the cells

throughout the material and subsequent loading of the
cell edges and faces against one another. Many cellular
materials have low relative densities (
10–20%) so that
they can be deformed up to large strains (
70–80%)
before densification occurs. In tension, the linear elastic
response is the same as in compression, at least at small
strains (Fig. 4b). As the strain increases, the cells become
more oriented with the loading direction, increasing the
stiffness of the material until tensile failure occurs.
The mechanical response of cellular solids has been
modeled by representing the cellular structure in several
ways. Initial models performed a structural analysis of a
unit cell such as a hexagon (in two dimensions) or a
dodecahedron (a 12-faced polyhedron) or tetrakaideca-
Fig. 3. Examples of engineering cellular solids (a) aluminum
honeycomb (b) open-cell polyurethane foam (c) closed-cell polyethy-
lene foam (Reproduced with permission from Gibson and Ashby,
1997).
hedron (a 14-faced polyhedron) in three dimensions
(Fig. 5) (Ko, 1965; Patel and Finnie, 1970; Gibson and
Ashby, 1982a; Warren and Kraynik, 1997; Zhu et al.,
1997a,b). The geometry of the unit cell makes the
analysis tractable but may not give an exact representa-
tion of the real material (e.g. foams). An even simpler
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380 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Fig. 4. Schematic uniaxial stress–strain curves for (a) elastomeric foam in compression (b) elastic–plastic foam in compression (c) elastomeric foam
in tension (d) elastic–plastic foam in tension. (Reproduced with permission from Gibson and Ashby, 1997.)

approach is to use dimensional analysis to model the
mechanisms of deformation and failure observed in the
cellular material without specifying the exact cell
geometry (Gibson and Ashby, 1982b, 1997). This
approach assumes that the cell geometry is similar in
foams of different relative densities. It gives the
dependence of the properties on the relative density
and the solid properties, but requires experiments to
determine the constants related to the cell geometry. A
third approach is to use finite element analysis of either
regular or random cellular structures (Silva et al., 1995,
van der Burg et al., 1997). Finite element analysis allows
local effects, such as imperfections, to be studied (Silva
and Gibson, 1997a; Chen et al., 2001). It can also be
used in conjunction with imaging techniques such as
micro-computed tomography to model the exact geo-
metry of a particular sample (e.g. trabecular bone),
although this is computationally intensive (van Reitber-
gen, 1995).
In this review, we first summarize the results of
micromechanical models developed using dimensional
analysis and compare them to selected results from the
analysis of unit cells and finite element modeling. We
then show how the models can be applied to honey-
comb- and foam-like natural cellular solids (wood and
trabecular bone). The role that cellular materials play in
increasing the efficiency of natural sandwich structures
(e.g. iris leaves) and tubular structures (e.g. plant stems,
animal quills) is also described. Cellular materials are
increasingly used as biomaterials to replace or regener-
ate tissue in the body. Here we describe titanium foams
that are being considered for bone replacement and
porous scaffolds for the regeneration of a wide variety of
tissues, including skin, nerve, liver, bone and cartilage.
2. Micromechanical models
2.1. Two-dimensional cellular solids (honeycombs), in-
plane loading
When loaded uniaxially in the plane of the hexagonal
cells, the cell walls of a honeycomb initially deform by
bending (so long as the wall thickness, t, is small
compared with the wall length, l) (Fig. 6a,b). The
Young’s modulus, E* can be related to the relative
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L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 381

Fig. 6. Hexagonal cell (a) undeformed (b) linear elastic bending (c)
non-linear elastic buckling. (Reproduced with permission from Gibson
and Ashby, 1997.)

where Es is the Young’s modulus of the solid cell wall

Fig. 5. Unit cells (a) hexagon (b) pentagonal dodecahedron (c)
tetrakaidecahedron. (Reproduced with permission from Gibson and
Ashby, 1997.)
density, r =rs ; the modulus of the solid, Es, and the cell
geometry (h/l, y) using structural mechanics. A stress s1
acting in the x1 direction induces a load P on the end of
the inclined cell wall:
P ¼ s1 ðh þ l sin yÞb; (1)
where b is the wall thickness. The wall deflects by:
Pl 3 sin y
d¼ ; (2)
12E s I
material and I is the moment of inertia of the wall cross
section (I ¼ bt3 =12). The strain in the x1 direction is then:
d sin y s1 ðh þ l sin yÞbl 2 sin2 y
1 ¼ ¼ : (3)
l cos y 12E s I cos y
The Young’s modulus parallel to x1 is then:
E 1 t3 cos y
¼ : (4)
Es l ðh þ l sin yÞ sin2 y
The Young’s modulus for loading in the x2 direction and
the shear modulus for loading in the x1–x2 plane, can be
found in a similar way (Gibson and Ashby, 1997); they
are listed in Table 1. All depend on the Young’s modulus
of the solid from which the honeycomb is made, the cube
of the relative density (since r =rs is proportional to t/l
(Table 1)) and a factor related to the cell geometry
(through h/l and y). The Poisson’s ratios are found by
taking the negative ratio of the strains normal to and
parallel to the loading direction (Table 1). To a first
approximation, ignoring shear and axial deformations of
the cell wall, we find that they depend only on the cell
geometry.
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382 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Table 1 compress axially, so that the Young’s modulus simply

Properties of Two-Dimensional Cellular Solids
varies with the volume fraction of solid, or with the
In-plane properties Out-of-plane properties relative density:
r h=lþ2 E 3 r
rs ¼ tl 2 cos yðh=lþsin yÞ
¼ : (7)
E s rs
Elastic moduli
E 1

t 3 E 3 
If buckling is avoided, the yield strength and brittle
Es ¼ l
cos y
ðhþl sin yÞ sin2 y Es ¼ rr
s
E 2
3
t h=lþsin y
crushing strength for loading in the x3 direction also
Es ¼ l cos3 y vary directly with the relative density. The stresses
n12 ¼  2 ¼ cos2 y n31 ¼ n32 ¼ ns
1 ðh=lþsin yÞ sin y corresponding to elastic and plastic buckling are given in
n21 ¼  1 ¼
ðh=lþsin yÞ sin y n13
n23
0 Table 1 (Gibson and Ashby, 1997).
2 cos2 y
G 12

t 3 h=lþsin y G13 G t


¼ ¼ G23s ¼ 0:577 (regular
Es l
ðh=l Þ2 ð1þ2h=l Þ cos y Gs l
2.3. Three-dimensional cellular materials (foams)
hexagons)
Collapse stresses Dimensional arguments, based on the mechanisms of


s2el 2 2 t3 sel

Es ¼ n 24p 1
lh2 cos y
3

t 3 2 l=hþ2
deformation and failure in foams, can be used to
Es l 1n2s ðh=lþsin yÞ cos y
elastic buckling estimate their mechanical properties. The dimensional
   
spl spl
arguments assume that the cells in foams of different


t 2 1

5=3
sys
1
¼ l 2ðh=lþsin yÞ sin y sys
3
¼ 5:6 tl plastic relative densities are geometrically similar. While here
 
buckling; (regular hexagons) we use a cubic cell to illustrate the argument, the same
spl
result is obtained for any cell geometry, so long as the
2 t 2 1
sys ¼ l 2 cos2 y mode of deformation or failure is the same.
ðscr Þ1

sfs ¼ t 2
l
1 In the linear elastic regime, under uniaxial stress,
3ðh=lþsin yÞ sin y
ðscr Þ2

t 2 1
open-cell foams deform primarily by bending of the cell
¼
sfs l 3 cos2 y edges. The Young’s modulus, E* can be estimated as
follows (Fig. 7a,b). Under a transverse load, F, the
bending deflection, d; of a strut of length, l, and cross-
At a sufficiently high load, cells collapse, by elastic sectional area proportional to t2, is given by:
buckling, plastic yielding or brittle crushing, depending
Fl 3
on the properties of the cell wall material. The elastic d/ ;
buckling collapse stress is related to the Euler buckling E s t4
load, Pcrit, of the vertical column (Fig. 6c): where Es is the Young’s modulus of the solid. The stress
Pcrit acting on the cell is proportional to F/l2 and the strain is
sel ¼ ; (5) proportional to d/l, giving:
2lb cos y
2 2
where Pcrit ¼ n ph2E s I and n, is a factor describing the E  t4
/ : (8)
rotational stiffness of the node. We find: Es l

s2el n2 p2 t3 1 The relative density of any open-cell foam, r =rs ; is

¼ : (6) proportional to the square of the ratio of the strut
Es 24 lh2 cos y
thickness to length, t/l, so that
For h=l ¼ 1; n ¼ 0:686 and for h=l ¼ 2; n ¼ 0:806:   2
The plastic collapse stress can be calculated from the E r
¼ C1 : (9)
plastic moment to form plastic hinges in the cell walls Es rs
while the brittle crushing stress can be calculated from The analysis gives the dependence of the Young’s
the modulus of rupture required to fracture the walls modulus on the solid modulus and the relative density,
(Gibson and Ashby, 1997) (Table 1). Cell collapse and combines all of the constants of proportionality
progresses throughout the material at a roughly related to the cell geometry into a single constant, C1. By
constant load to large strains. Once all the cells have fitting Eq. (9) to data, we find that C 1
1: A structural
collapsed, and the cell walls press against one another, analysis of a tetrakaidecaheral unit cell model with cell
the stress rises sharply (densification). edges with Plateau borders finds that C 1 ¼ 0:98 (Warren
and Kraynik, 1997). Finite element analysis of random
2.2. Two-dimensional cellular materials (honeycombs), three-dimensional Voronoi foams with struts of circular
out-of-plane loading cross-section finds that C 1 ¼ 0:8 (Vajjhala et al., 2000).
All three approaches give similar results and all give the
For loading along the prism axis, in the out-of-plane same dependence of modulus on the square of the
direction, the cell walls of a honeycomb initially relative density.
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L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 383

Fig. 7. Dimensional analysis for an open-cell foam (a) undeformed cell (b) linear elastic strut bending. Cell collapse by (c) elastic buckling (d) plastic
yielding (e) brittle crushing. (Reproduced with permission from Gibson and Ashby, 1997.)

As for honeycombs, the Poisson’s ratio of foams 1/3, the shear modulus is
 
depends only on cell geometry and does not depend G  3 r 2
on relative density (assuming that bending deformations ¼ : (10)
E s 8 rs
dominate). Typical values lie around 1/3, although
there is a wide range in reported values. Re-entrant The elastic collapse stress is proportional to the Euler
foams, with negative Poisson’s ratios, have been buckling load divided by l2 (Fig. 7c):
reported with values of 0:8ono0 (see, for example, Pcrit E s t4
sel / 2 / 4 (11)
Lakes, 1987). l l
Like the Young’s modulus, the shear modulus of
or
open-cell foams is related to the bending stiffness of the   2
cell edges, and depends on the square of the relative r
sel ¼ C 2 : (12)
density. For an isotropic foam with a Poisson’s ratio of rs
 ARTICLE IN PRESS
384 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Fitting Eq. (12) to data gives C 2
0:05: Structural
analysis of a tetrakaidecahedral unit cell gives C2

0:120:18; depending on the cross section of the edges,
for loading in one direction; loading normal to the
square faces does not produce buckling (Zhu et al.,
1997b).
The plastic collapse stress, spl is found by equating the
applied moment, M, on a strut from a transverse force F
to the plastic moment, Mp, required to form plastic
hinges (Fig. 7d):
M / Fl / spl l 3 ; (13)
M p / sys t3 (14)
giving
  3=2
spl t3 r strength along the grain are much higher than those
/ ¼ C3 ; (15)
sys l rs
where sys is the yield strength of the solid cell wall
material. Fitting Eq. (15) to data gives C 3
0:3:
The brittle crushing strength is found in a similar
manner, with (Fig. 7e):
  3=2
scr r the cell walls axially while loading across the grain
¼ C4 ; (16)
sfs rs
where sfs is the modulus of rupture of the solid cell wall
material. Fitting Eq. (16) to data gives C 4
0:2:
In closed cell foams, stretching of the cell faces also
contributes to the mechanical response. In many
polymer foams, the faces are thinner than the cell edges,
as polymer is drawn away from the faces and into the
edges by surface tension forces during processing. The
contribution of the faces to the overall mechanical
response depends, then, on the fraction of the solid in
the faces and adds a linear relative density term to the
expressions already obtained for the Young’s modulus
and the collapse stresses. The derivation of the proper-
ties of closed-cell foams is given in Gibson and Ashby
(1997).
The fluid within the cells can also contribute to the
mechanical response (Gibson and Ashby, 1997). In
open-cell foams, there is the viscous dissipation of fluid
moving through the cells. This effect depends on the
fluid viscosity, the strain rate, the cell size and the
sample size. In closed-cell foams, as the volume of the
cell decreases during compression, the pressure of the
enclosed gas within the cells increases according to the
ideal gas law, contributing to the overall stress required
to deform the foam.
The modelling of honeycombs and foams are next
applied to two common natural cellular solids: wood
and trabecular bone.
3. Wood: a two-dimensional cellular solid
The structure of two species of wood, cedar and oak,
are shown in Fig. 8. In both softwoods and hardwoods,
the bulk of the cells are long prismatic cells (tracheids in
softwoods and fibres in hardwoods). The annual growth
rings are distinguished by alternating bands of thin- and
thick-walled cells, corresponding to spring and summer,
respectively. The cells making up the rays are squatter
and more box-like. Hardwoods also have vessels,
relatively large diameter channels through which fluids
are conducted.
Compressive stress–strain curves for loading several
species of wood across and along the grain, are shown in
Fig. 9 (across the grain is the tangential direction while
along the grain is the axial direction in the figure). Both
stiffness and strength depend on the density of the
wood. And wood is highly anisotropic: the stiffness and
across the grain.
To a first approximation, the cellular structure of
wood can be modeled as a honeycomb (Easterling et al.,
1982). Micrographs of specimens of balsa wood loaded
in a small vice in a scanning electron microscope
indicate that loading along the grain (analogous to the
out-of-plane direction in the honeycomb) compresses
(analogous to the in-plane direction in the honeycomb)
bends them: the mechanisms of deformation are the
same as those of a honeycomb. The honeycomb model
suggests that the Young’s modulus along the grain
varies linearly with relative density (Eq. 7) while that
across the grain varies with the cube of the relative
density (Eq. 4). (The values of the cell wall density and
modulus rs and Es are roughly constant for different
species of wood.) The value of Es, the solid cell wall
modulus, also depends on loading direction, as the cell
wall is a composite of cellulose fibres in a lignin/
hemicellulose matrix. The axial and transverse cell wall
Young’s moduli have been measured to be 35 and
10 GPa, respectively (Cave, 1968). Data for the Young’s
moduli of woods of widely varying density, along and
across the grain, are fairly well described by the simple
honeycomb model (Fig. 10a). The modulus across the
grain varies with density to a slightly lower power than
3, as predicted by the honeycomb model, probably due
to stiffening effect of the rays.
The compressive strength of wood is determined by
uniaxial yielding for loading along the grain and by the
formation of plastic hinges in bending for loading across
the grain. The strength along the grain varies linearly
with relative density while that across the grain varies
with density squared (spl1 Table 1). The value of the
strength of the cell wall depends on loading direction;
the axial and transverse yield strengths have been
measured to be 350 and 135 MPa, respectively (Cave,
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L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 385

Fig. 8. Scanning electron micrographs of wood (a) cedar, cross section (b) cedar, longitudinal section, (c) oak, cross-section (d) oak, longitudinal
section. (Reproduced with permission from Gibson and Ashby, 1997.)

1969). The trends in the data for the compressive (Ashby et al., 1995):
strengths of woods of widely varying density, along and  1=2
across the grain, are fairly well described by the simple E 1=2 E 1=2
s rs
¼ : (17)
honeycomb model (Fig. 10b). r rs r
The different density dependencies of the modulus
The performance of wood is better than that of the

1=2solid
and strength for loading along and across the grain arise
from which it is made, by a factor of rs =r ; or
from the different mechanisms of deformation and
about 2 for typical softwoods with a relative density of
failure for the two loading directions. The honeycomb
0.3. Woods perform well, even compared to modern
model explains both the strong dependence of the
engineering composites: spruce, for instance has a value
properties on density and the pronounced anisotropy
of E=r1=2 of 7.1 GPa1/2 (Mg m3)1 while a unidirec-
in wood.
tional carbon fibre composite typically has a value of
The linear dependence of modulus and strength on
about 9 GPa1/2 (Mg m3)1. A similar argument can be
density for loading along the grain gives rise to the
made for the strength of a beam in bending. The
remarkable efficiency of wood in resisting bending
performance index to be maximized is then s2=3 =r; for
and buckling loads. For a beam of a given stiffness
wood, loaded along the grain,
or a column of a given elastic buckling load, the
material that minimizes the mass of the beam or column 2=3  
s2=3 sys rs 1=3
is that which maximizes the performance index E 1=2 =r ¼ : (18)
r rs r
(assuming that the length and cross-section of
the member are fixed) (Ashby, 1999). For wood, Again, the performance of wood is better than that of
loaded along the grain, rearranging Eq. (7) then gives the solid from which it is made. The performance of
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386 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Fig. 9. Compressive stress–strain curves for wood (a) loading in the
tangential direction, across the grain (b) loading in the axial direction,
along the grain. Note the different scales for compressive stress.
(Reproduced with permission from Gibson and Ashby, 1997.)
spruce s2=3 =r ¼ 92 MPa2=3 (Mg m3)1, for instance,
is somewhat better than that of a unidirectional
carbon fiber reinforced composite s2=3 =r ¼ 75 MPa2=3
(Mg m3)1.
In trees, it is the bending and buckling performance of
wood that is critical. Bending loads are imposed on the
branches by their own weight and the wind and on the
trunk by the wind. The trunk is also loaded in axial
compression (supporting the weight of the entire tree
above any given height). Interestingly, dimensional
analysis of elastic buckling in trees indicates that the
diameter, d, should increase with the 3/2 power of the
height, h (McMahon and Bonner, 1983). The Euler
buckling load is given by:
EI
Pcr / :
h2
The weight of the tree is:
W / rgd 2 h:
Equating the weight to the Euler buckling load gives:
Ed 2
¼ C:
rgh3
Rearranging gives:
 
Crg 1=2 3=2
d¼ h ; (19)
E
where E is the Young’s modulus of the wood, I is the
moment of inertia of the tree cross-section, r is the
density of the wood, g is the acceleration from gravity,
and C is a constant. We have already seen that for
loading along the grain, the ratio of E=r is a constant
(Eq. 7), so that tree diameter should increase as the 3/2
power of the height. In practice, this gives a good
description of the data for tree height and diameter
(Fig. 11) (McMahon and Bonner, 1983). The absolute
height of the tallest trees (California redwoods, Sequoia
sempervirens) is limited by constraints on water trans-
port (Koch et al., 2004).
4. Trabecular bone: a three-dimensional cellular solid
Trabecular bone exists at the ends of the long bones,
within the vertebral body, and in the core of shell-like
bones such as the skull. It has a cellular structure, with a
relative density typically between about 0.05 and 0.3.
Bone grows in response to load, so that the density of
trabecular bone depends on the magnitude of the loads
and the orientation of the trabeculae depends on the
direction of the loading (Fig. 12). Low-density trabe-
cular bone resembles an open-cell foam. High-density
trabecular bone has a more plate-like structure, with
perforations through the plates. The orientation of the
trabeculae can vary from almost equiaxed (e.g. in some
sites in the proximal femur; Gibson and Ashby, 1997) to
a nearly rectangular grid (e.g. in the vertebral body;
Jensen et al. 1990). Because of the variation in
trabecular architecture at even one density, there is
more variation in the stiffness and strength of trabecular
bone than in many other types of cellular materials.
The Young’s modulus of trabecular bone is plotted
against relative density in Fig. 13a. The data lie roughly
on a line of slope 2, but with substantial scatter in the
data. We have already seen that for open-cell foams,
with bending-dominated linear elastic behavior, the
modulus varies with the square of the density (Eq. 9).
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L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 387

Fig. 10. (a) The Young’s modulus of wood plotted against density. One pair of axes is normalized by the cell wall Young’s modulus in the axial
direction (35 GPa) and by the cell wall density (1500 kg/m3). The other pair of axes corresponds to the raw data. (Reproduced with permission from
Gibson and Ashby, 1997.) (b) The compressive strength of wood plotted against density. One pair of axes is normalized by the axial strength of the
cell wall (350 MPa) and by the cell wall density (1500 kg/m3). The other pair corresponds to the raw data. Data from: Goodman and Bodig (1970,
1971); Bodig and Goodman (1973); Bodig and Jayne (1982); United States Forest Products Laboratory (1974); Dinwoodie (1981) and Easterling et
al. (1982) (Reproduced with permission from Gibson and Ashby, 1997).

There is evidence both from micro-computed tomogra-
phy imaging of deformed specimens and from detailed
finite element analysis of representations of trabecular
bone architecture that bending is the dominant mode of
linear elastic deformation in trabecular bone (van
Rietbergen et al., 1995; Muller et al., 1998; Nazarian
and Muller, 2004). This is not surprising for low density
trabecular bone resembling an open-cell foam. It is more
surprising for higher density trabecular bone with a
more plate-like structure. We infer that the perforations
prevent truly closed-cell plate behavior, so that the
dominant mode of deformation is bending, even in these
higher density structures. We note that the name
trabecular bone, is then particularly appropriate, given
that trabecula means ‘‘little beam’’ in Latin.
Variations in the trabecular architecture give rise to
the scatter in the data, even at one density. The
dimensional arguments used to develop Eq. (9) assume
that the cell geometry in the cellular materials of
different densities is similar, so that the constant C1 in
Eq. (9), representing the dependence of the modulus on
cell geometry, has a single value. For many engineering
cellular materials, such as polymer foams made by a
blowing process, this is, to a first approximation, a good
assumption. The architecture of trabecular bone varies
substantially from one site to another, however, so that
there is some variation in the value of C1. A framework
for incorporating the dependence of the elastic moduli
on architecture, or fabric, has been provided by Cowin
(1985) and has been applied to trabecular bone by
various groups (Turner et al., 1990; van Rietbergen
et al., 1998). Models incorporating both density and
trabecular architecture account for roughly 70–95% of
the variance in the elastic constants.
The compressive strength is plotted against relative
density in Fig. 13b. The data are again fairly well
described by a line of slope 2. Cellular solids models
suggest that this corresponds to failure by elastic
buckling (Eq. 12) rather than brittle crushing, which
depends on density raised to the 3/2 power (Eq. 16). This
is a somewhat surprising result, but there is evidence for
elastic buckling failure in trabecular bone. For instance,
recent time-lapsed micro-computed tomography ima-
ging of trabecular bone loaded in uniaxial compression
indicates that the maximum local strains were found in
rod-like elements that were aligned with the compres-
sion axis. Some of these elements bend, while others are
compressed and some of those in compression buckle
(Muller et al., 1998; Nazarian and Muller, 2004). We
expect that buckled struts become inelastic at small
strains, as microdamage, in the form of microcracks
within trabeculae, initiates at global strains of less than
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388 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Fig. 11. Diameter at breast height plotted against overall height for
576 record trees from the Social Register of Big Trees. The relationship
d / h3=2 is indicated by the dashed line. (After McMahon and Bonner,
1983, with permission.)
1% (Moore and Gibson, 2002). Interestingly, micro-
damage was often observed to occur in trabeculae
oriented parallel to the compressive loading direction,
consistent with a buckling failure mode.
The similarity in the density dependencies of the
Young’s modulus and compressive strength suggest that
the failure strain is a constant. In particular, for
specimens of trabecular bone of similar trabecular
architecture, the values of the constants relating to cell
geometry in the equations for modulus (Eq. 9) and
compressive strength (Eq. 12) will be fixed, so that the
failure strain in compression will have a constant value.
The strain at failure in trabecular bone has been found
to be independent of density (Kopperdahl and Keaveny,
1998; Keaveny et al., 1994), and to be isotropic for
particular specimen (Chang et al., 1999). Compressive
yield strains (0.2% offset) are higher than those in
tension (Kopperdahl and Keaveny, 1998; Keaveny et al.,
1994), and can vary between sites (Kopperdahl and
Keaveny, 1998; Morgan and Keaveny, 2001). Measured
values of the compressive yield strain in trabecular bone
are 0.84% for human vertebra and 1.09% for bovine
tibia.
Up until this point, the discussion has focused on
normal trabecular bone. In patients with osteoporosis,
bone mass is lost through thinning of the trabeculae,
and then, at some critical trabecular thickness, pre-
sumably related to the osteoblast or osteoclast cell size,
through resorption of trabeculae (Fig. 14). Intuitively,
one might expect that the residual stiffness and strength
are more adversely affected by resorption than by
uniform thinning (consider, for instance, the mechanical
consequences of removing a column from a steel
framework in a skyscraper compared with removing
the same mass of material uniformly from all the
members of the framework).
The relative effects of density reduction from uniform
strut thinning versus random strut removal on the
modulus and compressive strength of cellular solids
have been studied using finite element analysis (Silva
and Gibson, 1997a; Vajjhala et al., 2000; Guo and Kim,
1999, 2002). The initial study analyzed regular, hexago-
nal honeycombs as well as random Voronoi honey-
combs (Fig. 15a) while the later studies applied the same
techniques to regular tetrakaidecahedral cells and
random three-dimensional Voronoi cells. For all the
structures studied, random removal of struts led to
greater reductions in stiffness and strength than uniform
thinning of struts (for a given density reduction) (Fig.
15b). For a given structure, the residual stiffness and
strength were similar for a given density reduction by
one of the two mechanisms. The three-dimensional
structures were less sensitive to density reductions than
the two-dimensional structures. For instance, a 10%
reduction in density by strut removal decreased the
modulus of a three-dimensional structure by roughly
40% while the same density loss reduced that of a two-
dimensional structure by roughly 70% (Fig. 15c).
Similar models for the relative effect of bone density
loss through trabecular thinning and resorption have
also been applied to vertebral bone, accounting for the
more aligned trabecular architecture (Silva and Gibson,
1997b; Espinoza Ortiz et al., 2002; Rajapakse et al.,
2004). The results for the two-dimensional model are
similar to those for regular and random cellular solids
(e.g. 10% reduction in the number of trabeculae leads to
about a 70% reduction in modulus and strength). The
results for the three-dimensional model are slightly less
sensitive than those for the regular or Voronoi cellular
solids (e.g. 10% reduction in the number of trabeculae
leads to about a 30% loss in the perturbed cubic bone
model while the same reduction in strut number leads to
about a 40% loss in modulus in the three-dimensional
regular or Voronoi models).
To summarize, in normal bone, the linear elastic
deformation is bending dominated and the Young’s
modulus varies as the density squared. The variation in
trabecular architecture leads to large scatter in the data,
even at one density. Differences in trabecular architec-
ture can be accounted for by the inclusion of fabric in
models. There is evidence that the compressive strength
 ARTICLE IN PRESS
L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 389

Fig. 12. Scanning electron micrographs showing the cellular structure of trabecular bone. (a) Specimen taken from the femoral head, showing low-
density, open-cell, rod-like structure. (b) Specimen taken from the femoral head, showing a higher density, perforated plate-like structure. (c)
Specimen taken from the femoral condyle, of intermediate density, showing an oriented structure, with rods normal to parallel plates. (Fig. 12a,b,c
reprinted from Gibson, 1985 with permission of Elsevier.)

of trabecular bone is related to buckling of trabeculae
leading to a dependence on density squared. The strain
to failure in bone is a constant for a given site with
consistent trabecular architecture. In osteoporotic bone,
bone loss occurs through trabecular thinning as well as
resorption. The modulus and strength are more severely
reduced by resorption than by uniform thinning of
trabeculae.
5. Natural sandwich structures: plant leaves, skull
Engineers sometimes make use of cellular solids as the
cores of sandwich structures: components with two stiff,
strong outer faces separated by a lightweight honey-
comb or foam core. The separation of the faces by the
core increases the moment of inertia of the section with
little increase in weight, making sandwich structures
attractive for resisting bending and buckling. Examples
of engineering sandwich panels include aircraft flooring
panels and downhill skis. Sandwich structures also occur
in nature, in, for instance, the skull and the leaves of
plants such as the iris and cattail (Fig. 16). The skull has
two outer faces of dense compact bone separated by a
core of trabecular bone. Iris and cattail leaves have
outer layers that are like a fiber reinforced composite,
with ribs of dense sclerenchyma running along their
length, separated by a core of either thin-walled
parenchyma cells (in the iris) or a rib-like structure
(in the cattail). The sandwich structure allows the iris
and cattail leaves to have a large surface area for
photosynthesis while providing sufficient structural
rigidity and strength at relatively low mass to maintain
their more or less upright position in the living plant.
Mechanically, the sandwich structure acts like an
I-beam, with the faces corresponding to the flanges of
the I-beam and the core corresponding to the web. The
equivalent moment of inertia of a sandwich beam is
(Allen, 1969):
E f bt3 E c bc3 E f btðc þ tÞ2
ðEI Þeq ¼ þ þ ; (20)
6 12 2
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390 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Fig. 13. (a) The Young’s modulus of trabecular bone plotted against density. One pair of axes is normalized by the strut Young’s modulus (12 GPa)
and by the strut density (2000 kg/m3). The other pair of axes corresponds to the raw data. Data from (a) Carter and Hayes, 1977 (b) Carter et al.,
1980 (c) Bensusan et al., 1983 (d) Hvid et al., 1989 (e) Linde et al., 1991 H=human B=bovine. (Reproduced with permission from Gibson and
Ashby, 1997.) (b) The compressive strength of trabecular bone plotted against density. One pair of axes is normalized by the strut strength (136 MPa)
and by the strut density (2000 kg/m3). The other pair corresponds to the raw data. (Reproduced with permission from Gibson and Ashby, 1997.) J,
Behrens et al. (1974) Femur & Tibia; +, Carter and Hayes (1977) Bovine femoral condyle; ’, Carter and Hayes (1977) Tibial plateau; , Galante et
al. (1970) Vertebrae; &, Hayes and Carter (1976) Bovine femoral condyle; K, Weaver and Chalmers (1966) Vertebrae; W, Weaver and Chalmers
(1966) Calcaneus; m, Carter et al. (1980) Femur; E, Bensusan et al. (1983) B. Femur.

where Ef and Ec are the Young’s moduli of the face and
the core, t and c are the thicknesses of the face and the
core, and b is the width of the beam. In practice, for
efficient sandwich beams, the face material is much
stiffer than that of the core and the faces are thin relative
to the core, so that the third term is much larger than the
first two terms and
E f btc2
ðEI Þeq ¼ : (21)
2 bc
The compliant core in sandwich beams gives rise to
significant shear deflections. The shear rigidity of the
core is (for a beam with stiff, thin faces):
ðAG Þeq ¼ bcGc :
The overall deflection of a sandwich beam, under a load
P, is then:
2Pl 3 Pl
d¼ 2
þ ;
B1 E f btc B2 bcG c
where B1 and B2 are constants related to the loading
geometry (e.g. for a simply supported beam with a
central load, B1 ¼ 48 and B2 ¼ 4).
The faces carry most of the normal stress while the
core carries most of the shear stress (Allen, 1969).
Again, assuming that E f bE c and that t5c; then
MyE f M
sf ¼ ¼ (24)
ðEI Þeq btc
and the shear stress in the core is
V
tc ¼ (25)
where M and V are the bending moment and shear force
at a cross-section.
Measurements of the geometry of the iris leaf (e.g. the
thickness and relative density of the face, the thickness
(22) and relative density of the core, the diameter, spacing
and volume fraction of solid in the ribs) along with
estimates of the solid tissue Young’s modulus for the
plant cell wall allow estimates of the bending stiffness of
the iris leaf to be made, using the sandwich beam
(23) analysis (Eq. 23). The bending stiffness of iris leaves has
also been measured by hanging small weights from
cantilevered leaves and measuring the corresponding
deflections. Agreement between the measured and
calculated bending stiffness is sufficiently good to
 ARTICLE IN PRESS
L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Fig. 14. Radiographs of sections through human lumbar vertebrae
(L1) (a) normal bone (b) osteoporotic bone, showing thinning and
resorption of trabeculae. (Reproduced with permission from Vajjhala
et al., 2000, published by the American Society of Mechanical
Engineers.)
conclude that the iris leaf behaves mechanically like a
sandwich beam (Gibson et al., 1988).
6. Natural tubular structures: plant stems, animal quills
Tubular structures in nature often have a dense outer
cylindrical shell with an inner honeycomb- or foam-like
core. Examples include plant stems, animal quills and
bird feather quills (known as the rachis) (Fig. 17). In
plant stems, this is known as the ‘‘core-rind’’ structure
(Niklas, 1992). Quills from porcupines, hedgehogs,
echidnas and spiny rats all have a similar structure
(Vincent and Owers, 1986; Karam and Gibson, 1994). In
nature, these structures are loaded primarily in bending
and/or compression. In all of these instances, the core
391
acts as an elastic foundation supporting the outer shell,
increasing its resistance to buckling.
In uniaxial compression, the presence of a compliant
core induces an axisymmetric buckling mode rather than
the diamond-pattern associated with a thin walled
cylindrical tube. The buckling wavelength is reduced
and buckling stress is increased, by an amount that
depends on the Young’s modulus of the core, Ec,
relative to that of the outer shell, Es, and the ratio of the
outer shell radius to thickness, a/t (Brush and Almroth,
1962; Siede, 1962; Yao, 1962; Weingarten and Wang,
1976; Karam and Gibson, 1995a). In bending, the
presence of the compliant core resists kinking failure
(e.g. as in a bent drinking straw). The increase in
moment capacity of a tubular beam with a compliant
core again depends on Ec/Es and a/t (Yabuta, 1980;
Karam and Gibson, 1995a). In both uniaxial compres-
sion and bending, stresses within the core decay fairly
rapidly in the radial direction, into the depth of the core:
they are reduced to less than 5% of the maximum value
at a radial distance of about 3 buckling wavelengths.
Material at a greater depth does not resist any
significant load. We note that plant stems are generally
hollow in the center, consistent with this finding. Animal
quills and bird feather rachis have a completely filled
core, possibly for thermal insulation, rather than
mechanical resistance.
The analysis of Karam and Gibson (1995a) has been
compared with experimental measurements of the
buckling load and bending moment capacity of silicone
rubber cylindrical tubes with foam cores (Karam and
Gibson, 1995b). The analysis gives a good description of
the dependence of the uniaxial compressive buckling
load on a/t, and the core depth, for the single value of
Ec/Es tested (Fig. 18a). It also gives a good description
of the bending moment capacity as a function of a/t
(again, for the single value of Ec/Es tested (Fig. 18b).
The analysis confirmed that the critical uniaxial buck-
ling loads and bending moments of shells with foam
cores can be increased significantly above those of
hollow cylinders of equivalent radius and mass; in the
experiments, the bending moment capacity was in-
creased by a factor of up to 4.8. It appears that the
cellular cores of natural tubular structures increase their
buckling resistance in axial compression and bending.
7. Cellular solids as biomaterials
Cellular solids are increasingly used as biomaterials to
replace or regenerate damaged or diseased tissue. Here
we consider two examples: open-cell titanium foams for
bone implants and porous scaffolds for tissue engineer-
ing, for the regeneration of a wide range of tissues (e.g.
skin, nerve, bone, cartilage).
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392 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Fig. 15. (a) Two-dimensional random Voronoi honeycomb (Reprinted from International Journal of Mechanical Sciences 37 Silva et al. The effects
of non-periodic microstructure on the elastic properties of two-dimensional cellular solids. 1161–1177, copyright 1995 with permission from Elsevier).
(b) Young’s modulus and compressive strength of 2D Voronoi honeycombs plotted against reduction in relative density by either uniform thinning or
random removal of struts. The modulus and strength are normalized by the values for the intact honeycomb. (Reproduced with permission from
Vajjhala et al., 2000, published by the American Society of Mechanical Engineers.) (c) Comparison of normalized Young’s modulus plotted against
reduction in relative density by strut removal for a random, three-dimensional Voronoi structure, a regular tetrakaidecahedral structure, a random
two-dimensional Voronoi structure and a regular two-dimensional hexagonal structure. (Reproduced with permission from Vajjhala et al., 2000
published by the American Society of Mechanical Engineers.)

Recently, there have been a number of novel processes
developed for making metallic foams (Ashby et al.,
2000). Open-cell foams are of the most interest as
biomaterials, as the interconnectivity of the pores allows
for tissue ingrowth. Open-cell metallic foams for use in
structural and thermal applications have been made
using an open-cell polymer foam precursor. The
polymer foam is coated with a ceramic slurry which is
then dried. To avoid damage to the ceramic foam
replica, the voids are filled with a casting sand. The
ceramic is then sintered, burning off the original
polymer foam. Molten metal is then cast into the voids
left by the polymer foam and the mold materials are
removed, leaving a metallic foam replica of the original
polymer foam. Open-cell metal foams can also be made
by depositing metal onto a polymer foam template by
chemical vapor deposition (CVD), evaporation, or
electrodeposition.
For bone implant applications, open-cell titanium
foams are being developed (Fig. 19). Titanium has
excellent biocompatibility and is already widely used in
orthopaedic implants. It is well known that porous
titanium coatings on implants induces bone ingrowth
(Head et al., 1995). Titanium foams offer the possibility
of matching the stiffness of the foam with that of bone,
through control of the relative density. A number of
different processes have been developed.
In one processing route, a polymer binder charged
with metallic particles and a foaming agent is foamed by
heating to a temperature sufficient to melt the polymer,
causing it to flow around the metal particles, and to
decompose the foaming agent, generating a gas that
produces the foam. The temperature is then further
increased to decompose the polymer and sinter the metal
particles together (Gauthier et al., 2003). The relative
density of these titanium foams is about 30% and the
 ARTICLE IN PRESS
L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399 393

Fig. 16. Natural sandwich structures (a) skull (b) iris leaf (c) cattail leaf. ((a) Reproduced with permission from Gibson and Ashby, 1997 (b)
Reproduced from Gibson et al. copyright 1988 with kind permission of Springer Science and Business Media.)

pore size is roughly 450–750 mm. The mechanical
properties such as the Young’s modulus and compres-
sive strength are similar to those of trabecular bone
(E
0:6–2.1 GPa, sc
10–25 MPa). In another proces-
sing route, titanium foams are made using a fugitive
phase: titanium and ammonium hydrogen carbonate
powders are mixed, pressed and heat-treated to burn out
the fugitive phase, leaving porous titanium (Wen et al.,
2002). The relative density of these foams ranges from
0.2 to 0.65, the Young’s modulus ranges from 2.9 to
10.3 GPa and the compressive strength ranges from 25
to 478 MPa. Values at the lower densities are similar to
those for trabecular bone while the values at the higher
densities exceed them. The foaming processes described
by both Gauthier et al. (2003) and Wen et al. (2002) give
relatively random, foam-like porous materials. Porous
titanium biomaterials with a more regular structure can
be made by Direct Material Deposition (DMD), a Solid
Free-Form Fabrication technique (Maddox et al., 2003).
The porous structure is fabricated by using a laser beam
to melt titanium powder along a computer-controlled
pathway.
There is also interest in the development of tantalum
foams for bone implants, although tantalum is not yet
widely used as an orthopaedic implant material. In one
process the tantalum foam is made by chemical vapor
infiltration (CVI) of tantalum onto a commercially
available reticulated vitreous carbon foam (Zardiackas
et al., 2001). The tantalum foam is 99% tantalum and
1% vitreous carbon and replicates the carbon foam
architecture. The relative density is 15–25% and the
pore size is nominally 550 mm. The Young’s modulus
and compressive strength are roughly 1.5 GPa and
35 MPa, respectively.
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394 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Fig. 17. Natural tubular structures: (a,b) grassy stem (c,d) porcupine quill (e,f) blue jay feather rachis. (c,d reproduced with permission from Gibson
et al., 1995.)

The goal of tissue engineering is to synthesize or
regenerate tissues and organs. Today, this is done by
providing a synthetic porous scaffold, or matrix, which
mimics the body’s own extracellular matrix, onto which
cells attach, multiply, migrate and function. Matrix
materials must satisfy a number of requirements. The
solid phase must be biocompatible and promote cell
adhesion and growth. Over time, as the cells produce
their own natural extracellular matrix, the synthetic
matrix should degrade into non-toxic components that
can be eliminated from the body. Examples of materials
used in synthetic matrices include: poly L lactic acid
 ARTICLE IN PRESS
L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Fig. 18. (a) Uniaxial buckling stress of the fully filled cylinder of a
given a/t divided by the buckling stress of a hollow cylinder of the same
a/t plotted against Seide’s dimensionless core stiffening parameter,

3=2

a=t E c =E s : (b) Ratio of measured local buckling moment of
partially filled cylinders to theoretical predictions for empty cylinders
of equal weight, plotted against a/t for the partially filled cylinders.
(Fig. 18a,b, reprinted from International Journal of Solids and
Structures 32, 1285–1306 Karam GN and Gibson LJ Elastic buckling
of cylindrical shells with elastic cores II: Experiments Copyright (1995)
with permission from Elsevier.) E Weingarten and Wang (1976),
FEM predictions; W, Kachman (1959), experimental results; J,
Goree and Nash (1962), experimental results; &, Malyutin et al.
(1980), experimental results; m, Malyutin et al. (1980), theoretical
predictions; ——, Siede (1962), theoretical predictions; — –, Yao
(1962), theoretical predictions; .........., Karam and Gibson (1994),
theoretical predictions; , Karam and Gibson (1994), experimental
results.
(PLLA), polyglycolic acid (PGA) and poly DL lactic co-
glycolic acid (PLGA); all of these are currently used in
resorbable sutures. Collagen-based matrices are also
available and are widely used for skin regeneration in
burn patients. Mineralized matrices are being developed
for bone tissue engineering.
The porous structure must also be designed to satisfy
several requirements. The porosity must be intercon-
nected to allow cell migration, vascularization and
diffusion of nutrients. High porosity is needed for cell
seeding and migration (typical porosities are greater
than 90%). The pore size must be within a critical range
(usually a few hundred mm): the lower bound is
controlled by the size of the cells while the upper bound
is related to the specific surface area through the
availability of binding sites. And the material must have
395
Fig. 19. Titanium foam for bone replacement (image courtesy Louis-
Philippe Lefebvre, National Research Council of Canada).
sufficient mechanical integrity to resist handling during
implantation and in vivo loading.
Matrix materials can be made by a variety of routes:
freeze-drying (Chen et al., 1995; Yannas et al., 1989),
fiber bonding (Mikos et al., 1993; Lu and Mikos, 1996),
foaming (Mikos et al., 1994; James and Kohn, 1996),
salt leaching (Lhommeau et al., 1998) and solid free-
form fabrications methods such as three-dimensional
printing (Park et al., 1998) have all been used (Fig. 20).
As a result of the requirements for the porous structure,
many tissue engineering scaffolds resemble open-cell
foams. Their mechanical response, too, is similar to that
of an open-cell foam (Fig. 21).
The mechanical interaction between cells and the
matrix is of importance in understanding wound
contraction that occurs during wound healing. It is
believed that contraction is associated with the forma-
tion of scar tissue and that contraction and scar
formation must be inhibited for normal tissue to
regenerate (Yannas, 2001). It has been shown, in vitro,
that the contractile force developed by fibroblasts on a
collagen-GAG scaffold is associated with elongation or
spreading of the cells (Freyman et al., 2001). As the
fibroblasts spread, the focal adhesion sites are main-
tained at the periphery of the cell. Tensile forces in the
actin network within the cell induce a compressive force
in the matrix strut to which the cell is attached (via the
focal adhesion sites). As the cell spreads, and the
distance between the adhesion sites increases, the Euler
buckling load for the matrix strut decreases until
eventually the strut buckles, causing contraction of the
matrix.
8. Summary
The cellular structure of wood resembles that of an
engineering honeycomb. The stiffness and strength of
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396 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399

Fig. 20. Examples of porous scaffolds for tissue engineering made by: (a) freeze-drying (collagen-GAG, image (Reprinted from Progress in Materials
Science 46, 273–282 Freyman TM, Yannas IV and Gibson LJ Cellular materials as scaffolds for tissue engineering, copyright 2000, with permission
from Elsevier). (b) fibre bonding (PGA, image reprinted from Mikos et al., copyright 1993 with permission of John Wiley and Sons, Inc.) (c) foaming
(PLLA, image reprinted from Polymer 35, 1068–1077 Mikos AG, Thorsen AJ, Czerwonka LA, Bao Y, Winslow DN, Vacanti JP, Langer R
Preparation and characterization of poly (L-lactic acid) foams. copyright 1994, with permission of Elsevier) (d) salt leaching (tyrosine-derived
polycarbonate, SEM image of a porous scaffold prepared in the laboratory of Professor Kohn at Rutgers University, as described in Lhommeau et
al., 1998).

different species of woods depend on the density of the

Fig. 21. Compressive stress–strain curve for a collagen-GAG scaffold.
(Image courtesy of Brendan Harley.)
species and the direction of loading: woods are much
stiffer and stronger when loaded along the grain than
across it. Models based on dimensional analysis of the
mechanisms of deformation in honeycomb models
(uniaxial compression of the cell wall for loading along
the grain and bending of the cell wall for loading across
the grain) give a good description of the dependence of
the stiffness and strength of wood on relative density
and direction of loading. In particular, the linear
dependence of the stiffness and strength of wood on
the relative density for loading along the grain gives rise
to wood’s remarkable mechanical efficiency: in bending
and buckling, wood is more efficient than the solid from
which it is made. In trees, it is the bending and buckling
loads that are critical.
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L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
The architecture of trabecular bone is more complex,
as bone grows in response to the loads applied to it and
the magnitude and the direction of the loads vary from
one site to another in the body. Both micro-computed
tomography imaging of compressed specimens of
trabecular bone and detailed finite element models
suggest that the trabeculae deform to a large extent by
bending and, at sufficiently high loads, by buckling.
Cellular solid models for open-cell foams indicate that
bending and buckling lead to a squared dependence of
the Young’s modulus and compressive strength on
density. The trend in the data for the Young’s modulus
and compressive strength of trabecular bone indicate
that both vary with density squared, although there is a
large scatter in the data, as a result of variations in the
trabecular architecture, even at one density. In patients
with osteoporosis, bone is lost through trabecular
thinning and resorption. Finite element models show
that resorption of trabeculae reduces stiffness and
strength much more dramatically than uniform thinning
of trabeculae.
In nature, as in engineering, cellular solids are
sometimes combined with dense materials to form
efficient structural components. Both the skull and
plant leaves such as the iris and cattail have a sandwich
structure with two stiff strong faces separated by a
lightweight core. In the skull, the faces are dense
compact bone while the core is trabecular bone. Plant
leaves such as the iris and cattail have outer layers of
dense ribs separated by a low-density core of parench-
yma cells or inner ribs. The separation of the stiff faces
by a lightweight core increases the moment of inertia of
sandwich structures, with little increase in weight,
making them efficient for resisting bending and buckling
loads. Tubular structures in nature often have a dense
outer cylindrical shell supported by an inner core of
honeycomb- or foam-like cells. Examples include plant
stems, animal quills and bird feather rachis. The core
acts as an elastic foundation supporting the outer shell,
increasing its resistance to buckling.
Cellular solids are increasingly being used as bioma-
terials to replace or regenerate damaged or diseased
tissue. Two examples described here are open-cell
titanium foams for bone implants and porous tissue
engineering scaffolds, for the regeneration of a wide
range of tissues (e.g. skin, nerve, bone, cartilage). In
both applications, the cellular structure is critical. In
titanium foams, it allows bone ingrowth and control of
the mechanical properties of the foam to match those of
trabecular bone. In scaffolds for tissue engineering
applications the low relative density, open-cell, foam-
like structure allows cells to migrate throughout the
scaffold.
Models for the mechanical behavior of cellular solids
provide a framework for understanding the mechanics
of the natural structures described in this paper (wood,
397
trabecular bone, plant leaves, plant stems, animal quills)
as well as novel biomaterials with highly porous, cellular
structures.
Acknowledgements
I am grateful for a number of stimulating and
productive collaborations with colleagues over many
years: Prof. MF Ashby of Cambridge University
Engineering Department (cellular solids, including
wood); Prof. TA McMahon (deceased), formerly of
Harvard University Division of Applied Sciences
(trabecular bone); Prof. WC Hayes, formerly of the
Orthopaedic Biomechanics Laboratory, Beth Israel
Deaconess Medical Center, Harvard Medical School
(trabecular bone); and Prof. IV Yannas of the Depart-
ment of Mechanical Engineering, Massachusetts Insti-
tute of Technology (tissue engineering scaffolds and cell
mechanics). I would also like to acknowledge the
outstanding graduate students that I have had the great
good fortune to work with at MIT. Those who
contributed to the work described in this paper are:
Dr. Toby Freyman of Boston Scientific, Prof. Ed Guo,
Department of Biomedical Engineering, Columbia
University, Mr. Brendan Harley, of the Department of
Mechanical Engineering, MIT, Dr. Gebran Karam of
Kredo, s.a.r.l., Dr. Tara Moore of Exponent, Inc., Prof.
Matt Silva, Department of Orthopaedic Surgery,
Washington University, and Ms. Surekha Vajjhala, of
Nanostream, Inc. Financial support for our work on
cellular solids in nature and biomaterials has been
provided by the National Science Foundation, the
National Institute of Arthritis and Musculoskeletal
and Skin Diseases and the Matoula S. Salapatas
Professorship at MIT.
References
Allen, H.G., 1969. Analysis and Design of Structural Sandwich Panels.
Pergamon Press, Oxford.
Ashby, M.F., 1999. Materials Selection in Mechanical Design, second
ed. Butterworth Heinemann, Stoneham, MA.
Ashby, M.F., Gibson, L.J., Wegst, U., Olive, R., 1995. The mechanical
properties of natural materials. I Material property charts.
Proceedings of the Royal Society of London A450, 123–140.
Ashby, M.F., Evans, A., Fleck, N.A., Gibson, L.J., Hutchinson, J.W.,
Wadley, H.N.G., 2000. Metal Foams: A Design Guide. Butter-
worth Heinemann, Stoneham, MA.
Behrens, J.C., Walker, P.S., Shoji, H., 1974. Variations in strength and
structure of cancellous bone at the knee. Journal of Biomechanics
7, 201–207.
Bensusan, J.S., Davy, D.T., Heiple, K.G., Verdin, P.J., 1983. 19th
Annual Orthopaedic Research Society Meeting 8, pp. 132.
Bodig, J., Goodman, J.R., 1973. Prediction of elastic parameters of
wood. Wood Science 5, 249–264.
Bodig, J., Jayne, B.A., 1982. Mechanics of Wood and Wood
Composites. Van Nostrand Reinhold, New York.
 ARTICLE IN PRESS
398 L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Brush, D.O., Almroth, B.O., 1962. Buckling of core-stabilized
cylinders under axisymmetric external loads. Journal of Aerospace
Science 29, 1164–1170.
Carter, D.R., Hayes, W.C., 1977. The compressive behavior of bone as
a two-phase porous structure. Journal of Bone and Joint Surgery
59A, 954–962.
Carter, D.R., Schwab, G.H., Spengler, D.M., 1980. Acta Orthopae-
dica Scandinavica 51, 733.
Cave, I.D., 1968. The anisotropic elasticity of the plant cell wall. Wood
Science and Technology 2, 268–278.
Cave, I.D., 1969. The longitudinal Young’s modulus of Pinus radiata.
Wood Science and Technology 3, 40–48.
Chang, W.C.W., Christensen, T.M., Pinilla, T.P., Keaveny, T.M.,
1999. Isotropy of uniaxial yield strains for bovine trabecular bone.
Journal of Orthopaedic Research 17, 582–585.
Chen, C.S., Yannas, I.V., Spector, M., 1995. Pore strain behavior of
collagen-glycosaminoglycan analogues of extracellular matrix.
Biomaterials 16, 777–783.
Chen, C., Lu, T.J., Fleck, N.A., 2001. Effect of inclusions and holes on
the stiffness and strength of honeycombs. International Journal of
Mechanical Sciences 43, 487–504.
Cowin, S.C., 1985. The relationship between the elasticity tensor and
the fabric tensor. Mechanics and Materials 4, 137–147.
Dinwoodie, J.M., 1981. Timber: Its Nature and Behaviour. Van
Nostrand Reinhold, New York.
Easterling, K.E., Harrysson, R., Gibson, L.J., Ashby, M.F., 1982. On
the mechanics of balsa and other woods. Proceedings of the Royal
Society of London A383, 31–41.
Espinoza Ortiz, J.S., Rajapakse, C.S., Gunaratne, G.H., 2002.
Strength reduction in electrical and elastic networks. Physical
Review B66 (14) (144203), 1–8.
Freyman, T.M., Yannas, I.V., Pek, Y.S., Yokoo, R., Gibson, L.J.,
2001. Micromechanics of fibroblast contraction of a collagen-GAG
matrix. Experimental Cell Research 269, 140–153.
Galante, J., Rostoker, W., Ray, R.D., 1970. Physical properties of
trabecular bone. Calcified Tissue Research 5, 236–246.
Gauthier, M., Menini, R., Bureau, M.N., So, S.K.V., Dion, M-J.,
Lefebvre, L.P., 2003. Properties of novel titanium foams intended
for biomedical applications. American Society for Metals Materials
and Processes for Medical Devices Conference. Anaheim, CA, 8–10
September 2003.
Gibson, L.J., 1985. The mechanical behavior of cancellous bone.
Journal of Biomechanics 18, 317–328.
Gibson, L.J., Ashby, M.F., 1982a. The mechanics of two-dimensional
cellular materials. Proceedings of the Royal Society of London
A382, 25–42.
Gibson, L.J., Ashby, M.F., 1982b. The mechanics of three-dimen-
sional cellular materials. Proceedings of the Royal Society of
London A382, 43–59.
Gibson, L.J., Ashby, M.F., 1997. Cellular Solids: Structure and
Properties, second ed. Cambridge University Press, Cambridge.
Gibson, L.J., Ashby, M.F., Easterling, K.E., 1988. Structure and
mechanics of the iris leaf. Journal of Materials Science 23,
3041–3048.
Gibson, L.J., Ashby, M.F., Karam, G.N., Wegst, U., Shercliff, H.R.,
1995. The mechanical properties of natural materials II: Micro-
structures for mechanical efficiency. Proceedings of the Royal
Society of London A450, 141–162.
Goodman, J.R., Bodig, J., 1970. Orthotropic elastic properties of
wood. Journal of the Structures Division American Society of Civil
Engineers ST11, pp. 2301–2319.
Goodman, J.R., Bodig, J., 1971. Orthotropic strength of wood in
compression. Wood Science 4, 83–94.
Goree, W.S., Nash, N.W., 1962. Elastic stability of circular cylindrical
shells stabilized by a soft elastic core. Experimental Mechanics 2,
142–149.
Guo, X.E., Kim, C.H., 1999. Effects of age-related bone loss: A 3D
microstructural simulation. Proceedings of the 1999 Bioengineering
Conference American Society of Mechanical Engineers Bioengi-
neering Division, vol 42. pp. 327–328.
Guo, X.E., Kim, C.H., 2002. Mechanical consequence of trabecular
bone loss and its treatment: A three-dimensional model simulation.
Bone 30, 404–411.
Hayes, W.C., Carter, D.R., 1976. Postyield behavior of subchondral
trabecular bone. Journal of Biomedical Materials Research
Symposium 7, 537–544.
Head, W.C., Bauk, D.J., Emerson, R.H., 1995. Titanium as the
material of choice for cementless femoral components in total hip-
arthroplasty. Clinical Orthopaedics and Related Research 311,
85–90.
Hvid, I., Bentzen, S.M., Linde, F., Mosekilde, L., Pongsoipetch, B.,
1989. X-ray quantitative computed tomography: the relations to
physical properties of proximal tibial trabecular bone specimens.
Journal of Biomechanics 22, 837–844.
James, K., Kohn, J., 1996. New biomaterials for tissue engineering.
Materials Research Society Bulletin 21 (11), 22–26.
Jensen, K.S., Mosekilde, L., Mosekilde, L., 1990. A model of vertebral
trabecular bone architecture and its mechanical properties. Bone
11, 417–423.
Kachman, D.R., 1959. Test report on buckling of propellant cylinders
under compressive loads. Space Technology Labs, Inc. GM
59-7520.6.24, 30 November.
Karam, G.N., Gibson, L.J., 1994. Biomimicking of animal quills and
plant stems: natural cylindrical shells with foam cores. Materials
Science and Engineering C2, 113–132.
Karam, G.N., Gibson, L.J., 1995a. Elastic buckling of cylindrical
shells with elastic cores—I Analysis. International Journal of Solids
and Structures 32, 1259–1283.
Karam, G.N., Gibson, L.J., 1995b. Elastic buckling of cylindrical
shells with elastic cores—II Experiments. International Journal of
Solids and Structures 32, 1285–1306.
Keaveny, T.M., Wachtel, E.F., Ford, C.M., Hayes, W.C., 1994.
Differences between the tensile and compressive strengths of bovine
tibial trabecular bone depend on modulus. Journal of Biomecha-
nics 27, 1137–1146.
Ko, W.L., 1965. Deformations of foamed elastomers. Journal of
Cellular Plastics 1, 45–50.
Koch, G.W., Sillett, S.C., Jennings, G.M., Davis, S.D., 2004. The
limits to tree height. Nature 428, 851–854.
Kopperdahl, D.L., Keaveny, T.M., 1998. Yield strain behavior of
trabecular bone. Journal of Biomechanics 31, 601–608.
Lakes, R., 1987. Foam structures with a negative Poisson’s ratio.
Science 235, 1038–1040.
Lhommeau, C., Levene, H., Abramson, S., Kohn, J., 1998. Prepara-
tion of highly interconnected porous tyrosine-derived polycarbo-
nate scaffolds. Tissue Engineering 4, 468.
Linde, F., Norgaard, P., Hvid, I., Odgaard, A., Soballe, K., 1991.
Mechanical properties of trabecular bone: dependency on strain
rate. Journal of Biomechanics 24, 803–809.
Lu, L., Mikos, A.G., 1996. The importance of new processing
techniques in tissue engineering. Materials Research Society
Bulletin 21 (11), 28–31.
Maddox, R.D., Carroll, J.W., Hollister, S.J., Mazumdar, J., Krebs-
bach, P.H., 2003. Gene/cell delivery from designed titanium
scaffolds made by free-form fabrication. Society for Biomaterials
29th Annual Meeting Transactions. Reno, Nevada.
Malyutin, I.S., Pilipenko, P.B., Georgievskii, V.P., Smykov, V.I., 1980.
Experimental and theoretical study of the stability in axial
compression, of cylindrical shells reinforced with an elastic filler.
Prikladnaya Mekhanika 16, 56–60.
McMahon, T.A., Bonner, J.T., 1983. On Size and Life. Scientific
American Library.
 ARTICLE IN PRESS
L.J. Gibson / Journal of Biomechanics 38 (2005) 377–399
Mikos, A.G., Bao, Y., Cima, L.G., Ingber, D.E., Vacanti, J.P.,
Langer, R., 1993. Preparation of poly (glycolic acid) bonded fiber
structures for cell attachment and transplantation. Journal of
Biomedical Materials Research 27, 183–189.
Mikos, A.G., Thorsen, A.J., Czerwonka, L.A., Bao, Y., Winslow,
D.N., Vacanti, J.P., Langer, R., 1994. Preparation and character-
ization of poly (L-lactic acid) foams. Polymer 35, 1068–1077.
Moore, T.L.A., Gibson, L.J., 2002. Microdamage accumulation in
bovine trabecular bone in uniaxial compression. Journal of
Biomechanical Engineering 124, 63–71.
Morgan, E.F., Keaveny, T.M., 2001. Dependence of yield strain of
human trabecular bone on anatomic site. Journal of Biomechanics
34, 569–577.
Muller, R., Gerber, S.C., Hayes, W.C., 1998. Micro-compression: a
novel technique for the nondestructive assessment of local bone
failure. Technology and Health Care 6, 433–444.
Nazarian, A., Muller, R., 2004. Time-lapsed microstructural imaging
of bone failure behavior. Journal of Biomechanics 37, 55–65.
Niklas, K.J., 1992. Plant Biomechanics: An Engineering Approach to
Plant Form and Function. University of Chicago Press, Chicago.
Park, A., Wu, B., Griffith, L.G., 1998. Integration and surface
modification and 3D fabrication techniques to prepare patterned
poly (L-lactide) substrates allowing regionally selective cell adhe-
sion. Journal of Biomaterials Science Polymer Edition 9, 89–110.
Patel, M.R., Finnie, I., 1970. Structural features and mechanical
properties of rigid cellular plastics. Journal of Materials 5, 909–932.
Rajapakse, C.S., Thomsen, J.S., Espinoza Ortiz, J.S., Wimalawansa,
S.T., Ebbesen, E.N., Mosekilde, L., Gunaratne, G.H., 2004. An
expression relating breaking stress and density of trabecular bone.
Journal of Biomechanics 37, 1241–1249.
Siede, P., 1962. The stability under uniaxial compression and lateral
pressure of circular-cylindrical shells with a soft elastic core.
Journal of Aerospace Science 29, 851–862.
Silva, M.J., Gibson, L.J., 1997a. The effects of non-periodic
microstructure and defects on the compressive strength of two-
dimensional cellular solids. International Journal of Mechanical
Sciences 39, 549–563.
Silva, M.J., Gibson, L.J., 1997b. Modeling the mechanical behavior of
vertebral trabecular bone: effects of age-related changes in
microstructure. Bone 21, 191–199.
Silva, M.J., Hayes, W.C., Gibson, L.J., 1995. The effects of non-
periodic microstructure on the elastic properties of two-dimen-
sional cellular solids. International Journal of Mechanical Sciences
37, 1161–1177.
Turner, C.H., Cowin, S.C., Rho, J.Y., Ashman, R.B., Rice, J.B., 1990.
The fabric dependence of the orthotropic elastic constants of
cancellous bone. Journal of Biomechanics 23, 549–561.
United States Forest Products Laboratory 1974. Wood Handbook:
Wood as an Engineering Material. U.S. Department of Agricul-
ture, Agricultural Handbook 72.
Vajjhala, S., Kraynik, A.M., Gibson, L.J., 2000. A cellular solid model
for modulus reduction due to resorption of trabeculae in bone.
Journal of Biomechanical Engineering 122, 511–515.
399
van der Burg, M.W.D., Shulmeister, V., van der Geissen, E., Marissen,
R., 1997. On the linear elastic properties of regular and random
open-cell foam models. Journal of Cellular Plastics 33, 31–54.
van Rietbergen, B., Weinans, H., Huiskes, R., Odgaard, A., 1995. A
new method to determine trabecular bone elastic properties and
loading using micromechanical finite-element models. Journal of
Biomechanics 28, 69–81.
van Rietbergen, B., Odgaard, A., Kabel, J., Huiskes, R., 1998.
Relationships between bone morphology and bone elastic proper-
ties can be accurately quantified using high resolution computer
reconstructions. Journal of Orthopaedics Research 16, 23–28.
Vincent, J.F.V., Owers, P., 1986. Mechanical design of hedgehog
spines and porcupine quills. Journal of Zoology A210, 55–75.
Warren, W.E., Kraynik, A.M., 1997. Linear elastic behavior of a low-
density Kelvin foam with open cells. Journal of Applied Mechanics
64, 787–794.
Weaver, J.K., Chalmers, J., 1966. Cancellous bone: Its strength and
changes with aging and an evaluation of some methods of
measuring its mineral content: I Age changes in cancellous bone.
Journal of Bone and Joint Surgery 48A, 289.
Weingarten, V.I., Wang, Y.S., 1976. Stability of shells attached to
elastic core. Journal of the Engineering Mechanics Division
American Society of Civil Engineers 102, 839–870.
Wen, C.E., Yamada, Y., Shimojima, K., Chino, Y., Hosokawa, H.,
Mabuchi, M., 2002. Novel titanium foam for bone tissue
engineering. Journal of Materials Research 17, 2633–2639.
Yabuta, T., 1980. Effects of elastic supports on the buckling of circular
cylindrical shells under bending. Journal of Applied Mechanics 47,
866–870.
Yannas, I.V., 2001. Tissue and Organ Regeneration in Adults.
Springer, Berlin.
Yannas, I.V., Lee, E., Orgill, D.P., Skrabut, E.M., Murphy, G.F.,
1989. Synthesis and characterization of a model extracellular
matrix that induces partial regeneration of adult mammalian skin.
Proceedings of the National Academy of Science USA 86, 933–937.
Yao, J.C., 1962. Buckling of axially compressed long cylindrical shell
with elastic core. Journal of Applied Mechanics 29, 329–334.
Zardiackas, L.D., Parsell, D.E., Dillon, L.D., Mitchell, D.W.,
Nunnery, L.A., Poggie, R., 2001. Structure, metallurgy and
mechanical properties of a porous tantalum foam. Journal of
Biomedical Materials Research 58, 180–187.
Zhu, H.X., Knott, J.F., Mills, N.J., 1997a. Analysis of the elastic
properties of open-cell foams with tetrakaidecahedral cells. Journal
of the Mechanics and Physics of Solids 45, 319–343.
Zhu, H.X., Mills, N.J., Knott, J.F., 1997b. Analysis of the high strain
compression of open-cell foams. Journal of the Mechanics and
Physics of Solids 45, 1875–11904.
Further reading
Freyman, T.M., Yannas, I.V., Gibson, L.J., 2000. Cellular materials as
porous scaffolds for tissue engineering. Progress in Materials
Science 46, 273–282.