International Journal of Biological Macromolecules

30 (2002) 119– 127

www.elsevier.com/locate/ijbiomac

The viscoelastic basis for the tensile strength of elastin

M.A. Lillie *, J.M. Gosline
Department of Zoology, Uni6ersity of British Columbia, Vancou6er, Canada V6T 1Z4

Received 23 August 2001; received in revised form 15 December 2001; accepted 15 January 2002

Abstract

Purified aortic elastin displays failure behaviour characteristic of an amorphous, noncrystalizing elastomer with failure
properties showing a strong dependence on viscoelastic behaviour. Tensile breaking stresses and breaking strains measured over
a range of temperatures, hydration levels, and strain rates are reducible to single curves by the application of shift factors obtained
from dynamic mechanical tests. The breaking stress of rubbery elastin is similar to that found in other elastomers, but glassy
elastin is about an order of magnitude less strong than expected. We suggest elastin’s ability to be strengthened through viscous
dissipation of strain energy and crack tip blunting is limited by its fibrillar structure. © 2002 Elsevier Science B.V. All rights
reserved.

Keywords: Elastin; Tensile strength; Viscoelasticity

1. Introduction We undertook this study to understand the failure

Degradation of the elastic tissue in the arterial wall
occurs in several pathologies. In many cases it is the
result of enzyme-mediated biochemical processes con-
trolling tissue remodelling [1,2]. In other cases, the
degradation appears uncontrolled and associated with
the mechanical failure of the elastin. This may readily
occur in elastic tissue that has been improperly manu-
factured because of a genetic disorder involving the
elastin [3] or an elastin associated protein [4]. But
failure may also occur in normal elastin because of
chemical changes in the extracellular environment that
compromise elastin’s mechanical properties, such as
oxidative damage associated with atherosclerotic infl-
ammation [5,6] that may weaken or possibly cleave the
elastin chains [7,8]. It is also possible that physical
abrasion from the deposition of calcium weakens the
elastin as it does in heart valves [9,10]. Although, a
number of pathologies may result in mechanical degra-
dation of the elastin, it is unlikely that the failure
mechanism is the same for all.
Abbre6iations: DMSO, dimethyl sulfoxide; RH, relative humidity;
SBR, styrene butadiene rubber.
* Corresponding author. Tel.: + 1-604-822-2373; fax: + 1-604-822-
2416.
E-mail address: lillie@zoology.ubc.ca (M.A. Lillie).
properties of normal, healthy elastin. Normally, there is
very little turnover of elastin once it is laid down
[11 –13], so that it presumably survives for the lifetime
of the individual, but this is difficult to confirm me-
chanically. By measuring the failure characteristics of
normal elastin, we can estimate the likelihood that it
will fail in vivo under nonpathological conditions. We
also want to identify the molecular mechanism by
which it fails to be able to predict how various patho-
logical conditions might affect its lifetime. The data
collected from normal tissues under physiological con-
ditions can provide a baseline against which to judge
the effects of treatments to assess whether failure is
accelerated.
Elastin’s quasistatic stress –strain behaviour over
large strains and its dynamic mechanical behaviour
over small strains are compatible with theories describ-
ing the viscoelastic behaviour of noncrystalizing, amor-
phous elastomers. Elastin itself does not crystalize when
exposed to high strains [14]. In these elastomers, failure
is initiated by the formation of a microcrack whose
growth rate depends on the stress intensity and the rate
of energy dissipation at the crack tip [15,16]. The
elastomer’s capacity for energy dissipation is the great-
est single factor determining its lifetime, and other
features of network topology have little impact. If the
crosslinking density is accounted for, the breaking

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120 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127

stress becomes essentially independent of the chemical A total of 298 rings was tested, divided into four
nature or the molecular structure of the elastomer [15]. treatment groups (Table 1). Treatments were selected to
Thus a wide range of elastomers exhibit very similar provide a range of hydration levels. Group 1 rings
behaviour, and they exhibit similar failure envelopes remained in water. Group 2 rings were dehydrated
when breaking stress per chain is plotted against breaking aseptically at 37 °C through the vapour phase at a
strain [17]. If elastin’s failure processes are also domi- relative humidity (RH) of 98% [21]. The water contents
nated by a viscoelastic response, then its failure envelope of these samples measured gravimetrically averaged
should superimpose on those produced by these other 0.339 0.03 g water/g elastin. Group 3 rings were dehy-
elastomers. drated through the liquid phase by equilibration in either
The dependence of crack growth on energy dissipation 2 or 2.35 M sucrose with 0.02% sodium azide. Group 4
makes elastomer failure processes time dependent, and rings were equilibrated in 25% dimethyl sulfoxide
because they conform to the Williams Landel Ferry (DMSO, BDH Chemical Company) with 0.02% azide. At
(WLF) equation [18], failure data collected at different 24 °C, 25% DMSO slightly stiffens elastin, while at
temperatures and deformation rates can be superimposed 80 °C it reduced stiffness by substantial swelling but does
to form one master curve [19,20]. The temperature shift not appear to affect the network otherwise [23].
factor used to reduce the data, aT, is the ratio of the
friction coefficient for segmental mobility measured at
one temperature relative to the value of the coefficient 2.2. Mechanical testing
at a reference temperature [18]. Elastin’s dynamic stress–
strain behaviour has been shown to be superposable, not The rings were mounted in a custom-made frame
only for time and temperature data, but also for time and around 6.4 mm diameter steel rods. Groups 1, 3, and 4
solvent content data [21– 23]: dynamic stress–strain rings were immersed in water, sucrose or a DMSO
behaviour at various degrees of hydration or at different solution containing 0.02% azide. Group 2 rings were
degrees of swelling in solutions of certain solutes is immersed in mineral oil to prevent change in hydration.
reducible using the shift factor, ac, where the subscript The rings were held at a temperature between −16
c refers to the solvent concentration in the elastin and 80 °C. The samples were deformed in tension to
network. If elastin failure is dominated by energy dissi- failure in an Instron 1122 tensile testing machine at a
pating processes, then its failure behaviour should also cross-head rate of between 0.05 and 1000 mm/min,
be time dependent, and we should be able to use shift corresponding to strain rates from 35× 10 − 6 to 0.8/s.
factors obtained from dynamic tests to reduce its break- Five samples tested at 1000 mm/min broke in under 1 s,
ing strain or breaking stress data collected at different for which the response time of the system is considered
temperatures or concentrations to a single curve. inadequate, and their stress data were omitted. Stress, |,
was calculated as the force divided by the cross-sectional
area, with area based on the dimensions of the unde-
2. Materials and methods formed sample in water at room temperature. Strain, m,
was calculated as the change in sample length, DL,
2.1. Aortic rings divided by L0. All lengths were midwall lengths, calcu-
lated as the average of the lengths along the outer
Thoracic aortas from about 18 month old pigs were
collected from a local abattoir. The elastin was purified
Table 1
by autoclaving [24] and was stored under sterile condi-
Test conditions for samples
tions until used. Rings averaging 9 mm in width were
carefully cut using a fresh razor for each cut, ensuring Group Condition Temperature/°C na acaTb
that the edges were completely smooth. Tissues contain-
ing branches or any visible irregularities were not used. 1 Water 37 53 0
75 27 −0.9
Fully hydrated rings were compressed by the weight of
two glass histology slides for measurement of length 2 98%RH −16 19 11
(flattened length) and width with calipers. Thickness was 5 22 9
20 17 4.5
measured with calipers or with a custom-built device that 37 18 3
applied a small fixed load to the tissue. Since aortic rings
3 2 M sucrose 37 49 4
are thicker on the dorsal side, thickness was measured in
2.35 M sucrose 37 32 6
3– 5 places and averaged. The load used in the custom-
built device compressed the tissue by 229 1% relative to 4 25% DMSO 24 31 0.8
80 30 −2
the thickness of the unloaded tissue measured with
calipers. This difference in thickness due to the different a
n =number of samples.
measurement protocols was accounted for. b
acaT =shift factors.
 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127 121

and inner walls of the ring [24]. L0 was the length at

which force in the treated sample first became nonzero.
In samples tested in water at room temperature, L0 is
identical to the flattened length [24], but the lengths
differ in samples tested at another temperature or in
samples that have been dehydrated or swollen in
DMSO. Therefore, using this definition of L0 requires
making the assumption that treatment affects DL in
proportion to its effects on L0. The validity of this
assumption is supported by the data in Fig. 5 that show
the strain at break is the same for fully hydrated and
strongly dehydrated samples when compared at the
same point on the x axis, i.e. at the same reduced time
to break. Breaking stress, |b, was the greatest stress
borne by the tissue, and breaking strain, mb, was the
strain at the breaking stress. The tangential modulus, E,
was the local slope of the stress– strain curve measured
at a wall stress of 0.2 MPa. Modulus values were
Fig. 1. Stress – strain curves for eight samples tested at the following
corrected for system compliance. Shift factors ac and aT hydration condition, temperature, and crosshead rate: (1) water,
were either obtained from our published work [21,23] 75 °C, 0.2 mm/min; (2) water, 75 °C, 0.05 mm/min; (3) 2 M sucrose,
or were measured in dynamic tensile tests following the 37 °C, 500 mm/min; (4) 98%RH, 20 °C, 1000 mm/min; (5) 98%RH,
published protocols. 5 °C, 10 mm/min; (6) 98%RH, −17 °C, 10 mm/min; (7) 98%RH,
Linear regressions were performed by SigmaStat −16 °C, 10 mm/min; (8) 98%RH, 5 °C, 10 mm/min.
(Jandel.) Nonlinear curve fitting was done by Table-
Curve (Jandel). Values are reported as means9 SEM. essentially the initial modulus. With progression
through the glass transition, the effect of yield on the
post-yield modulus became more pronounced, but the
yield stress increased beyond 0.2 MPa. The stress at
3. Results which the yield occurred correlated with E (Fig. 2;
slope= 0.8, PB 0.0001, r 2 = 0.84, n=91). Moving
Elastin exhibited a range of stress– strain behaviours through the curves from the rubbery to the glassy state,
under the various regimes of time, temperature and
the strain at yield decreased from highs of between 0.4
hydration level, as illustrated by the curves in Fig. 1.
and 0.7 to lows of around 0.1 (data not shown).
The stress–strain curves for elastin in water at low
The breaking strain initially increased, from a value
strain rates and in 25% DMSO at 80 °C is illustrated
in water of just over 1, i.e. doubling in length, to a
by the lowest, right-most curves. Because the curves are
maximum of over 2 in sucrose and some of the 98%RH
compressed on the y axis, their features are difficult to
rings, but then decreased, reaching values as low as 0.05
discern, but they were essentially J-shaped, similar to
as the curves in Fig. 1 move to the extreme left. Moving
curves previously reported [25]. Dehydrating the elastin,
increasing the rate of deformation, or decreasing the through the curves from rubbery to glassy behaviour,
temperature shifted the behaviour towards or into the the breaking stress rose progressively from an average
glass transition, giving the tissue the behaviour shown low of 0.2 MPa to an average high of 2.9 MPa (Table
by the curves towards the left. The left-most curves 2).
were recorded from elastin in its glassy state, obtained The time to break, tb, was dominated by the rate of
with tissues dehydrated at 98%RH, tested at high strain cross-head movement, shown by the clear grouping of
rates and at low temperatures. The tangential modulus the breaking strain and breaking stress data when
measured at 0.2 MPa rose from a value of about 0.17 plotted against the time to break (Figs. 3 and 4). The
MPa in the rubbery, right-most curves to about 44 time to break appears to be uncorrelated with the
MPa in the glassy, left-most curves (Table 2), an in- breaking strain and breaking stress of samples because
crease of 262-fold. This value is comparable to the they were tested under different conditions and so
282-fold increase in modulus shown for ligament elastin represent elastin in different viscoelastic states. To re-
[14]. duce the elastin to corresponding states, shift factors
With the exception of the right-most curves, the obtained from dynamic mechanical tests were applied
curves exhibited a yield point. For samples near the to the time to break data (Table 1). Breaking stress was
rubber zone, the yield occurred below 0.2 MPa, but the reduced to 37 °C by multiplying by 310/T where T is
change in modulus was minimal so the value for E is the temperature in K at which data were collected.
122 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127

Table 2
Comparison of the mechanical behaviour of elastin with the behaviour of a typical amorphous noncrystalizing polymer

Elastin swollena Elastin unswollenb Typical polymer

|b (MPa) Rubberc 0.20 9 0.01 1.38 9 0.08 1

Glassd 2.990.2 21 9 1 150e
Glass/rubber 15 15 150
E (MPa) Rubber 0.17 9 0.01 1.18 90.03 1–2f
Glass 449 24 311 9170 3000e
Glass/rubber 262 262 1500–3000
|b/E Rubber 1.2 1.2 0.5–1
Glass 0.07 0.07 0.05–0.1

a
Values were based on uncorrected lengths and thicknesses.
b
Values were based on lengths and thickness corrected for interfibrillar and network water contents and fibre angle. Temperatures have been
reduced to 37 °C.
c
Values for rubbery samples are the average of all samples tested in water at 70 °C.
d
Values for glassy samples are the average of all samples tested at 98%RH at −16 °C.
e
Published data [57,58].
f
Published data [33].

In addition, a corrected breaking stress, |*, b was whether a correction factor is necessary for the fibre
obtained by applying three, straight-forward adjust- angle, we have compared our values for E for pig
ments to the breaking stresses to account for elastin’s arterial elastin in water with the reported value for a
swollen fibrous structure. The first adjustment takes single elastin fibre from bovine ligament. The modulus
into account that the elastin cross-sectional area on value for the single fibre elastin was corrected for
which stress is based is augmented by the swelling from network swelling by multiplying by w − 2
1/3
[27], and the
network hydration. At the temperature at which sample values for arterial elastin were corrected for both net-
dimensions were measured, the water content of the work swelling and interfibrillar volume. These correc-
swollen network is 0.6 g/g, [22] giving a volume fraction tions increased our sample tangential modulus for
of the elastin in the network, 62, of 0.56. To obtain the elastin in water at 37 °C to 0.86 MPa. Aaron and
stress for the unswollen network, | must be multiplied Gosline reported a value of 0.41 MPa for G, the shear
by w −
2
2/3
. elastic modulus of a single fibre at 24 °C, which, as-
The second adjustment was required because a test suming E=3G, corresponds to a value for E of 1.28
sample is composed of elastin fibres surrounded by the MPa at 37 °C [28]. Our arterial value is 33% below the
interfibrillar space, which is occupied largely by smooth value for the single fibre. Assuming pig and bovine
muscle in vivo and replaced by water or air in our elastin have the same elastic modulus, this value sug-
samples. The interfibrillar volume in these samples is 3 gests that 67% of the arterial fibres are fully load
ml water/g elastin. Therefore, the swollen network oc- bearing. We have therefore included a factor of 0.33 to
cupies a volume fraction in the sample of 0.31. The
fibres run continuously the length of a sample, so that
the proportion occupied by the water is constant along
the length of a sample. Therefore, | is divided by 0.31
to correct for the area occupied by the interfibrillar
space.
The third adjustment arises from the disposition of
the elastin as fibres, since both stiffness and stress will
be reduced by off-axis fibre orientation. Under physio-
logical (triaxial) loading, in the bulk of the media the
fibres are oriented parallel to the circumferential direc-
tion [26], which is the loading axis in our specimens.
Deviation from circumferential fibre orientation occurs
on the intimal and adventitial sides of the media, as
well as in the intima and adventitia [26]. Under a
Fig. 2. The correlation between yield stress and uncorrected modulus.
uniaxial load, lateral retraction will likely allow moder- () 98%RH, −15 °C; () 98%RH, 5– 40 °C; (
) 2.35 M sucrose,
ately off-axis fibres to reorient to an angle whose cosine 37 °C; ( ) 2 M sucrose, 37 °C; ( ) water, 37 °C. The line shows a
is insignificantly different from unity. To determine linear regression on all points but the rightmost with a slope of 0.80.
 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127 123

Fig. 5. Breaking strain against reduced time to break. () 98%RH,

−15 °C; () 98%RH, 5– 40 °C; (
) 2.35 M sucrose, 37 °C; ( ) 2
Fig. 3. Breaking strain against time to break. The numbers above
M sucrose, 37 °C; ( ) water, 37 °C; () water, 75 °C; (2) DMSO.
each data set give the test crosshead rate in mm/min. Only four
The solid line is fit to the data points (left axis). The broken line gives
samples were tested at 100 mm/min; the points for two of which
overlie each other. () 98%RH, −15 °C; () 98%RH, 5– 40 °C; the behaviour of SBR (right axis), shifted three decades to the left to
(
) 2.35 M sucrose, 37 °C; ( ) 2 M sucrose, 37 °C; ( ) water, facilitate comparison.
37 °C; () water, 75 °C; (2) DMSO.
[29]. The SBR data have been shifted three decades to
adjust stress and modulus for the variation in fibre the left along the x axis to facilitate a comparison of the
orientation. curves. The breaking stress in the SBR increased by a
The breaking strain plotted against reduced time to factor of 100 between the longest and shortest breaking
break is shown in Fig. 5, and the structurally corrected times. In contrast, the breaking stress in the elastin
breaking stress, |*,
b in Fig. 6. The dominance of the test increased by only 15-fold.
strain rate disappears, and the failure behaviour takes The time dependence of the failure behaviour can be
on the pattern characteristic of a wide range of elas- removed by plotting the breaking stress against the
tomers tested under a range of conditions. The break-
ing strain goes through a maximum, and the breaking
stress increases monotonically with decreasing time to
break. The breaking stress becomes less sensitive to
strain rate at low and high rates. The solid line in each
figure is a least squares fit to the data, and the broken
line shows the behaviour of styrene butadiene rubber
[SBR] a typical noncrystalizing amorphous elastomer

Fig. 6. Structurally corrected breaking stress against reduced time to

break. () 98%RH, −15 °C; () 98%RH, 5– 40 °C; (
) 2.35 M
sucrose, 37 °C; (
) 2 M sucrose, 37 °C, water, ( ) 37 °C, ()
Fig. 4. Breaking stress against time to break. the Crosshead rates are water, 75 °C, (2) DMSO. The solid line is fit to the data points. The
not indicated but are the same as in Fig. 3. () 98%RH, − 15 °C; broken line gives the behaviour of SBR, shifteds three decades to the
() 98%RH, 5– 40 °C; (
) 2.35 M sucrose, 37 °C; (
) 2 M sucrose, left to facilitate comparison. The dashed horizontal line gives the in
37 °C; ( ) water, 37 °C; () water, 75 °C; (2) DMSO. vivo stress.
124 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127
Fig. 7. Failure envelope for elastin (data points) and SBR (broken
line). () 98%RH, −15 °C; () 98%RH, 5–40 °C; (
) 2.35 M from its dynamic stress–strain behaviour indicates that
sucrose, 37 °C; (
) 2 M sucrose, 37 °C; ( ) water, 37 °C; () elastin’s failure mechanisms are dominated by its vis-
water, 75 °C; (2) DMSO. The solid line is generated with Eq. (1).
breaking strain (Fig. 7). True stress was calculated as
|(m+ 1) to account for the decrease in cross-sectional
area that occurs as the specimen is strained. Stress has
been divided by the crosslink density, we, calculated as
z/Mc where z is the density and Mc is the average
molecular weight of the individual chains. Elastin den-
sity is 1.31 g/ml [30] and elastin Mc was calculated as
5.5 kDa from the precursor protein structure allowing a
molecular weight of 72 kDa for tropoelastin and 13
crosslinks per molecule [31]. Values for SBR crosslink
density were taken from reference [29].
The resulting failure envelope outlines the breaking
points shown in Fig. 1, except that the stress values are
slightly altered by the conversion of stress to true stress
so that in Fig. 7 the maximum value for stress at break
occurs close to the maximum value for strain at break.
The broken line shows the envelope for SBR, and the
solid line shows the reduced true stress at equilibrium
calculated from the kinetic theory of rubber elasticity
[27]:
|u = (zRT/Mc)(u 2 − 1/u), (1)
where u = m+1, and R is the gas constant. At low
strain rates, high hydration, and high temperature, both
the elastin and the SBR breaking stresses match the
equilibrium stress. As strain rate increases or as hydra-
tion or temperature decreases, the curves peel off from
the equilibrium values towards higher stress values.
Near equilibrium, the points of the elastin failure envel-
ope centre on the theoretical line, but this matching is
in part fortuitous since the uncertainties introduced by
the reductions are on the order of 0.2 log units. The
scatter is considerably larger than is observed with
synthetic elastomers. Most of this is the unavoidable
variability of biological specimens whose dimensions
can be measured with limited precision. Additionally,
adiabatic heating, especially in the samples dehydrated
through the vapour phase, will tend to rotate individual
stress–strain curves clockwise through the envelope,
contributing to the variation. However, the deviations
appear statistical, and although greater scatter is com-
monly observed on the glassy side of mmax when super-
position fails [20,32], the scatter in our data appears to
be independent of the viscoelastic state of the samples.
4. Discussion
4.1. The strength of elastin
The ability to reduce elastin’s failure data to one
master curve (Figs. 5 and 6) using shift factors obtained
coelastic processes, and the time dependence of its
breaking stress and breaking strain follows the time
dependence of its modulus. Therefore, the molecular
basis of elastin’s strength can be understood in terms of
its viscoelasticity. Where viscous resistance to segmental
mobility is negligible, such as would be found in an
elastomer at high temperatures, the modulus observed
at low strain rates approaches that given by its confor-
mational entropy, shown by the solid line in Fig. 7. But
as the network moves towards its glass transition,
molecular friction increases, allowing individual chains
to be supported by their neighbours, evening the load
distribution. The onset of molecular friction raises the
modulus above its equilibrium value, but it also inhibits
the growth of microcracks by dissipating energy
through viscous processes. Thus, the breaking stress
increases, raising the failure envelope above the values
predicted for equilibrium.
Elastin’s behaviour at the rubbery end of the failure
envelope is typical of a noncrystalizing elastomer. Both
its modulus and its breaking stress agree with values
listed in Table 2 for rubbery elastomers, and the
stresses match the predicted stress at equilibrium calcu-
lated from the kinetic theory of rubber elasticity. How-
ever, towards the glassy portion (the top part of the
curve in Fig. 7 to the left of mmax), the developed stresses
are roughly an order of magnitude below what is
typically found. Usually, breaking stresses rise two
orders of magnitude between the rubbery and glassy
states [20,33,34]; in elastin, they rose by about one
order of magnitude (Table 2). This behaviour is not
limited to fully glassy elastin. Low breaking stress
values were also obtained at mmax, midway through the
glass transition. Values here are typically about 1.3
orders of magnitude above the equilibrium value, but
were only 0.8 orders in elastin. And the highest yield
stresses obtained in glassy elastin were about 12 MPa,
lower than the range for glassy polymers of 41–240
 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127
MPa [35]. The low failure stresses are not artefacts of
our testing methods, and significant lytic or similar
damage to the tissue during processing and handling,
including the creation of nonloadbearing fibres at the
cut edges of the rings, can be excluded since it would
reduce its rubbery strength as well as the glassy.
Elastin, therefore, appears to become unusually weak
for an elastomer within its glass transition.
The weakness may be the consequence of elastin’s
fibrous structure. The energy required to advance a
crack in an elastomer is directly proportional to the
crack tip diameter [36], and glassy elastomers are strong
despite their inherent flaws because they can form a
large crack tip. This has been demonstrated in cutting
experiments where, by preventing crack diameter from
growing, the energy of fracture at high cutting speeds is
reduced by over an order of magnitude relative to
tearing [37–39]. Crack tip diameter in bulk rubbery
elastomers can reach typically about 100 mm [40], and
can increase by up to two orders of magnitude as
temperature is reduced or strain rate is increased [38].
Such dimensions are clearly out of range for a 2-mm
diameter elastin fibre, and therefore the basic strength-
ening mechanism available to bulk elastomers cannot
operate in elastin. But by the same token, elastin can-
not contain the same flaws that weaken bulk elas-
tomers, since the critical flaw size for a bulk elastomer,
typically around 40 mm [41], cannot be reached. There-
fore, at least some of the failure processes in elastin
must operate on a smaller scale than they do in a bulk
elastomer, on a submicron scale, and so failure may be
subject to a somewhat different set of constraints.
The dissipation of strain energy occurs through a
relatively small volume of material preceding the tip
[42]. Strengthening is possible only if the volume of
material at the crack tip is of sufficient magnitude to
allow the necessary viscous self-reinforcement. If not,
tip dimensions will be constrained, reducing the ability
to dissipate energy, and hence, reducing sample
strength. To spread energy through this region, the
material at the crack tip must form a continuum capa-
ble of load transmission, and therefore it cannot con-
tain an interface. The subfibre architecture of elastin is
unclear, but there are numerous levels at which the
elastin network may not be structurally continuous.
The fibre appears to be a bundle of 100– 200 nm fibrils
[43], which are in turn bundles of primary filaments
with diameters on the order of 4 nm [44]. X-ray diffrac-
tion indicates the existence of yet smaller structures not
normally present in an elastomer [14]. If any of these
structures are separated by nonload-transmitting inter-
faces, they may interfere with failure mechanisms.
Therefore, one possibility is that elastin’s low strength
might be attributable to its small structural dimensions.
However, low adhesion interfaces could reduce
strength through a second mechanism. In the absence
125
of other factors, strength is expected to be proportional
to modulus, and a value of 0.1 is predicted for the ratio
|b/E as the theoretical strength of most solids [45]. The
presence of defects in many material reduces their
actual strength-to-modulus ratio by orders of magni-
tude [33]. The value of 0.07 for |b/E for glassy elastin
(Table 2) is close to this theoretical maximum, suggest-
ing that elastin’s strength is as high as its should be
considering its modulus, and as high as is found for
other glassy elastomers. The weakness through the
transition would then be due to the low ratio of Eglass/
Erubber shown in Table 2.
One possible cause of a lower modulus within the
glass transition is the presence of a free surface at an
interface. The mobility of the chains in proximity to the
surface could be enhanced, as is observed in ultrathin
films of elastomers [46]. Altered dynamics have been
observed in free standing films with thicknesses of 70
nm [47] and in supported films a few tens of nm thick
[48]. An enhanced mobility lowers stiffness, and the
effect should become more pronounced as the transi-
tion is traversed. On yet a lower scale, there is a second
possible cause of low modulus. The size of the smallest
structures in elastin is comparable to the 2–3 nm
domains of cooperatively rearranging regions that de-
velop in elastomers close to the glass transition [49–51].
If rearrangement amongst these domains is facilitated
by these structures, the attainment of a fully glassy
modulus may be delayed or prevented. Thus, the exis-
tence of surfaces in elastin may reduce the internal
viscous interaction near the glass. The implication is
that elastin’s low strength may be associated with a low
stiffness, rather than the dimensional limitations of the
crack tip suggested above.
4.2. The lifetime of elastin
The data presented in Fig. 6 show how the lifetime of
an elastin sample depends on the stress to which it is
subjected, and we can use these data to estimate the
lifetime of elastin in vivo. Given a modulus for the
rubbery network of 1.28 MPa, we can calculate the
mean in vivo stress of the elastin if we can identify the
strain required to restore a sample of purified elastin to
its in vivo length. The circumferential and longitudinal
dimensions of an arterial segment change upon excision
and again upon purification. Longitudinal retraction
will increase the resting diameter of the tissue, reducing
the strain required to restore the elastin to its in vivo
circumferential length. The circumferential extension
ratio falls from about 1.55 to 1.0 on excision [52,53]
and to 0.92 on purification [24], requiring a circumfer-
ential extension of 1.68 to restore in vivo length. The
longitudinal extension ratio falls from 1.3 to 1.0 on
excision [54] and to 0.95 on purification [24]. Assuming
incompressibility of both the whole artery and the
126 M.A. Lillie, J.M. Gosline / International Journal of Biological Macromolecules 30 (2002) 119–127
elastin, the longitudinal retraction will increase the
sample’s circumference by 12%, reducing the required
circumferential strain to only 0.56. To achieve this
strain, a sample must be loaded to a stress of 0.72 MPa.
This value is therefore our estimate of elastin’s mean
stress in vivo. It is shown in Fig. 6 by the dashed,
horizontal line at 5.86 on the log stress scale.
The solid line fit to the data in Fig. 6 has been
extrapolated to several decades beyond the range cov-
ered by the data. We have no way of predicting the
actual form of the curve in this region, beyond the
theoretical restriction that a zero slope asymptote is
unlikely [19], and so we have conservatively selected a
curve that predicts a relatively rapid fall in stress at
very long times to break. Despite the obvious limita-
tions on the accuracy of this prediction, we can
nonetheless draw two useful conclusions from the exer-
cise. First, the predicted average lifetime of the elastin
well exceeds the lifetime of the individual. The extrapo-
lated curve remains well above the in vivo stress line at
the abscissa value of 10 which corresponds to a lifetime
in excess of 300 years. For comparison, a human
lifespan would fall around 9.4 on the abscissa, and a
pig lifespan would fall around 8.6. A linear regression
of the last 110 data points gives a yet more conservative
model, but it still crosses the in vivo line at a value of
12. Even when we add on an additional stress to
account for the dynamic component of the loading
regime, the predicted lifetimes are still excessively long.
Assuming a total dynamic strain of 0.09 and a complex
modulus of 1.29 MPa (based on a 6° phase [21]), the
peak total stress is only 0.05 MPa above the static
mean, which does not appreciably raise the in vivo line
in Fig. 6. This result suggests that the in vivo stress is
too low to cause failure in normal, healthy arterial
elastin within the individual’s lifetime. The validity of
this conclusion is supported by the absence of measur-
able turnover of mature elastin in vivo [11– 13].
The second conclusion is that elastin operates with a
remarkably low safety factor. The lowest average fail-
ure stress measured under our test conditions is 1.38
MPa, only 1.9 times the in vivo level of 0.72 MPa. A
sample of elastin subjected to the much longer in vivo
loading times would be able to withstand lower stresses,
so the safety factor is actually lower than 1.9. Such a
low safety factor presumably represents an economy of
construction, possible because arterial elastin is pro-
tected by a parallel array of collagen fibres and there-
fore need not be particularly strong itself. The in vivo
load balance between the elastin and collagen elements
must be relatively finely tuned. Based on the behaviour
of whole pig arterial segments [55,56], we calculate the
maximum circumferential strain attained by the artery
before rupture of the collagen is only about 1, which
would also strain the elastin to about its breaking
point. The elastin in the artery wall appears able to
function as long as the collagen is intact, but will break
at about the same pressures as the rest of the arterial
wall.
In summary, elastin appears to be well designed to
fulfill its biological functions under normal conditions.
It operates in the rubbery plateau, so any strength
limitations from an inability to develop viscous interac-
tions will not incur any immediate consequences. How-
ever, its fibrillar architecture may reduce its survival
ability when faced with a pathological challenge. Rela-
tively small amounts of damage, for example cleavage
due to an oxidative attack, may result in stresses that,
while tolerable in a bulk material, may be insupportable
in a fibrous structure with a limited cross-sectional area.
The low safety factor would require only a modest
stress concentration to precipitate failure. It appears
then, that although elastin functions in many ways like
a typical amorphous elastomer, structural features that
are made possible through the fine control of biosyn-
thetic processes may endow elastin with some atypical
properties as well. If we can identify whether these
differences represent specific design features of the
elastin, then we may be better able to understand the
basis of its physiological and pathological behaviour.
Acknowledgements
This work was supported by a grant to J.M.G. from
the Heart and Stroke Association of British Columbia
and the Yukon. The authors would like to thank Sylvia
Wu, Gavin Chalmers, and Glen David for their excel-
lent technical assistance.
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