Clinical Science (1970) 39, 223-238.
A METHOD FOR MEASURING H U M A N S K I N
ELASTICITY I N V I V O WITH OBSERVATIONS ON
THE EFFECTS OF AGE, SEX A N D PREGNANCY
R . GRAHAME*
Clinical Research Division, Kennedy Institute of Rheumatology,
West London Hospital
(Received 27 November 1969)
SUMMARY
1. A method is presented for the measurement of the elasticity of human skin
in vivo. A simple suction cup device is applied to the intact skin and the distortion
produced in response to pre-determined negative pressures recorded. By the use of
appropriate formulae stress and strain may be calculated and a stress/strain curve
drawn, the gradient of which represents the elastic modulus for intact skin.
2. The test, which is simple to perform and entirely innocuous to the patient, has
been shown to achieve acceptable standards of accuracy and reproducibility.
3. In the present study, the physiological variation in skin elasticity that occurs in
respect of age, sex and pregnancy is investigated and the implications concerning the
physiological changes that occur in skin collagen discussed.
The elastic properties of skin have interested physicians for a considerable period of time.
However, no satisfactory method has been evolved of measuring skin elasticity in the living
subject and enabling the result to be expressed in absolute terms.
A number of workers have measured the elasticity of human and animal skin in vitro using
the conventional ‘strip’ method on specimens of skin removed from the body (Rollhauser,
1950; Dirnhuber & Tregear, 1966). An alternative technique was introduced by Dick (1951).
By this method, a circle or diaphragm of skin is clamped peripherally and uniform pressure is
applied from below by raising the pressure in a water-filled chamber (Fig. 1). The distortion
produced represented by the height of the resulting dome of skin can be measured by a suitable
recording device. Tregear (1966), using the standard formulae that represent pressure changes
across spherical membranes, evolved the following formulae to express stress (T)and strain (S)
in this system in mathematical terms.
pa2(1
T=
+$)
* Present address: Guy’s Hospital, London, S.E.l.
223
R. Grahame
224
where p
=
pressure (cmHg)
a = radius of diaphragm (cm)
x = height of the dome (cm)
d = thickness of skin (cm)
When a stress/strain curve for skin is constructed (from data obtained by either the strip
or diaphragm methods) it shows the following characteristics (Tregear, 1966). Initially there is
considerable strain for relatively little stress. This represents the phase of taking up slack. After
approximately 5% strain has been achieved further strain is obtained only at the expense of
considerable stress. From this point the relationship is virtually linear, i.e. Hooke’s Law applies,
and the gradient represents the Elastic Modulus (Young’s Modulus) for skin.
P =pgh
Water
FIG.1. The in vitro diaphragm method for measuring skin elasticity (after Tregear).
METHOD
The method herein described consists of adapting the diaphragm method for measuring skin
elasticity (Dick, 1951) for clinical use, employing the formulae evolved by Tregear (1966) for
the calculation of the results. Instead of applying positive pressure from below, as in the in
vitro system, in the present method negative pressure is applied to the intact skin, from above,
by means of a simple suction cup. Providing that tethering is negligible (see below), the effect
is the same: namely, a dome of skin (of height ‘2)is raised into the cup in response to the
negative pressure.
The cup is made of glass and is bell-shaped. The circumference of the bell is flanged and the
under surface of the flange is flattened. The diameter of the inner margin of the flange, which
Skin elasticity in vivo
225
corresponds to the outer margin of the diaphragm skin, is 2 cm. At its apex the bell is in continuity with a graduated precision tube approximately 20 cm long and it is to the lumen of the
top of this tube that the negative pressure is delivered during the test.
In order to measure the distortion resulting from the negative pressure, a water-filled system
is used. Since the volume of the dome of skin sucked into the suction-cup will displace an
equal volume of water up the precision tube, the former can be calculated if the latter is measured. The bell is filled with water by injection into a side arm, which is then sealed by a 'Subaseal' cap during the test. The cap also permits adjustment of the initial level of the water
column to the zero mark on the tube, as well as the removal of any air bubbles by means of a
syringe and needle, the latter penetrating the rubber seal.
In order to obtain a water-tight join between the flange of the cup and the skin, a doubly
adhesive ring (Devices Sales Ltd.) cut to the appropriate size is applied to the rim of the cup,
and sticks it to the circle of skin immediately adjacent to the area tested. It also has the effect
of discouraging any movement of skin when the negative pressure is applied.
FIG.2. Diagrammaticrepresentationof the apparatus for measuring skin elasticity in vivo (see text).
The apparatus is shown in diagrammatic form in Fig. 2. By means of a 50 ml glass syringe
(A) air is evacuated from the pressure chamber (B). Two bicycle valves (C) prevent air from reentering the pressure chamber from the syringe and also permit air to be blown off once the
syringe is full. Having lowered the pressure below atmospheric pressure in the pressure chamber, this negative pressure is transmitted by means of pressure tubing to the top of a mercury
manometer (enabling negative pressure to be measured) and from there to the top of the graduated tube connected to the suction cup. The spring clips (E) and (F) respectively transmit and
release the negative pressure to the suction cup.
The suction cup itself is clamped to a push-pull tension gauge (H) (John Chatillon and Son)
which is itself clamped to a rack-and-pinion device, so that the suction cup can be lowered on
to the skin under test. The purpose of the tension gauge is to standardize the pressure with
which the suction cup is applied to the skin. The indicator (L) records the tension and for the
P
226
R. Grahame
tests described below the cup is applied to the skin with a force of 2 Ib. This is equivalent to
700 g cm-’.
When the cup is in position on the dorsum of the forearm, with water filling the bell up to
the zero mark on the graduated precision tube, and the tension gauge registering 2 lb, one is
ready to commence readings. A series of readings are taken at intervals of 5 cmHg down to
minus 30 cm, viz. at 5, 10, 15, 20, 25, and 30 cmHg in that order.
It is important to emphasize that in order to attempt to measure elasticity of skin, stress
must be applied for the minimum period of time required to enable the distortion to be measured. With this method, this period is about 2 s. Longer periods of stress result in viscous slip,
an irreversible extension due to the slipping of individual collagen fibrils (or bundles) relative
to one another. Furthermore, in the living state the prolonged application of sub-atmospheric
pressure may result in cutaneous oedema. Proof that extension has been completely reversible
(i.e. elastic) is forthcoming when the meniscus of the column of water ‘h’ returns to zero after
the stress is released. In practice this is not invariable but the irreversible component rarely
exceeds 1% of the strain.
By observing, at the conclusion of the test, the mark on the skin caused by the pressure of
the bell, one may verify the adequacy of the clamping effect. Where two complete concentric
circular lines are seen it is taken that the clamping has been satisfactory. Where one or both of
the circles are incomplete, this is taken to represent inadequate clamping, and implies that skin
may have travelled inside the bell from without when the negative pressure was applied. Under
these circumstances the results are discarded and the test is repeated. In practice, however, this
is a rare event, encountered chiefly in thin subjects. Careful attention to placing the bell on an
area overlying muscle belly obviates this hazard.
Calculation of results
Before being in a position to substitute into the Tregear formulae, it is necessary firstly to
calculate ‘x’, the height of the dome, from the rise in the column of water ‘h’ (the latter being
the indirect measurement of the distortion produced in response to the negative pressure) and
secondly to measure the thickness of the skin ‘d’.
To obtain ‘x’, the height of the dome, the following manoeuvre is used. It is assumed that
the geometric shape of the dome is that of a segment of a sphere, the segment having a height
of ‘x’ and a radius ‘a’.(The validity of this assumption is tested below.) Since it is the volume
of this dome which displaces an equal volume of water up the graduated precision tube, by
equating these two values and solving the equation, a value for ‘x’ may be obtained from a
value for ‘h’.
Thus, the volume of a segment of a sphere =
and the volume of a cylinder =
nr’h
where ‘r’ is the radius of the lumen of the precision tube, thus:
(%’ )
nx -+x2
=nr2h
Skin elasticity in vivo
227
The solution of the equation is as follows:
If
then
3hr2
sinh8 = a3
0
x = 2a sinh3
Using sinh 8 tables it is possible to calculate a value for ‘x’ for any given value of ‘ti’.
To measure skin thickness Harpenden calipers (Tanner & Whitehouse, 1955) are used on a
skin fold of the dorsum of the hand over the fourth metacarpal bone. This particular site was
chosen as it was shown by McConkey, Fraser, Bligh & Whitley (1963), to contain very little
subcutaneous fat. Three measurements on the same site were made and the mean was taken to
represent a double thickness of skin.
It will be apparent that the test is done on the skin of the dorsum of the forearm, but that the
thickness is measured on the dorsum of the hand. This is because, for technical reasons, to
obtain a satisfactory clamping effect an area of skin with an underlying cushion of subcutaneous fat or muscle is desirable, but for the purpose of measuring skin thickness a fat-free zone
of skin is necessary. However, a study comparing the thickness of excised skin overlying the
fourth right metacarpal bone with that of the mid-dorsal region of the right forearm in thirteen
cadavers using Harpenden calipers showed insignificant differences between these two sites,
viz: means 0.0712 cm (SEM 0-0067) and 0.0712 cm (SEM 0.0068) respectively.
Having obtained values for ‘x’ (the height of the dome) and ‘8(the skin thickness), one is
now in a position to substitute into Tregear’s formulae and obtain for every pair of ‘p’ and ‘h’
a value for T (stress) and S (strain), and thus construct a stress/strain curve.
A stress/strain curve obtained from the forearm of a healthy adult female subject aged 33
years by the above technique is shown in Fig. 3.
In order to include the lower part of the stress/strain relationship for the purposes of illustration a modification of the technique was used in which the initial tension of the cup was zero.
In practice this is superfluous since the elastic modulus is the gradient of the higher (and virtually linear) part of the curve.
The practical problems in calculating the results are considerable as a result of the complicated mathematical procedures involved. However, by suitable programming it was possible
for all these three stages of calculation to be performed by the Elliott computer at the Royal
Postgraduate Medical School of London.
Simplijkation of the formulae. It has been possible to simplify the method of calculating
the results in the following way. Values T and S were calculated accurately by using the original
formulae, and these results were equated with a simplified version of the formulae incorporating the data ‘p‘ and ‘h‘ and arbitrary constants designated K, and K, (for T and S
respectively). Both these operations were performed on the computer. Thus :
R. Grahame
228
6t
2
t
I
2l
b
3
I
i
7‘
0’
i
t’
,
/
c
‘
/‘
I
1
002
004
I
006
I
I
0.00
S
FIG.3. A stress/strain curve obtained in vivo from the skin of the forearm of a healthy female aged
33 years.
Values for K, and K, were obtained from 500 pairs of values for ‘p’ and ‘h’. The mean value
for K, was 172.4 (SEM 0.0744) while that for K, was 0.00026 (SEM 0~0000005).From this it
will be apparent that in practice the constants K1and K, vary little over the range of the data
obtained.
Using the simplified version of the formulae, rapid calculation of T and S can be achieved
from the raw data and the use of the two constants K, and K,. A stresslstrain curve can then
be drawn and the gradient of the line of best fit then represents the elastic modulus for
skin.
VeriJicationof the method
The accuracy of the method was assessed in the laboratory by testing two varieties of rubber
sheeting using the in vivo apparatus as described above, and the results were compared with
those obtained by the conventional strip method on the same materials. The two materials
used were (a) a rubber mackintosh sheet and (b) an Esmarch’s bandage. Details of the technique used the strip method and the results obtained by both methods have been recorded
elsewhere (Grahame, 1968). They have been summarized graphically in Fig. 4 which shows
that the two stress/strain curves obtained by the two methods for each material are virtually
parallel. Since the elastic modulus may be defined as the gradient of the stress/strain curve it
follows that the values for the modulus obtained by the in vivo method approximate closely
to the true value (as obtained with the strip method). It will be observed that the results in
using the suction-cup method cross the ordinate on the positive side of zero if extrapolated
backwards. This has been shown by a series of laboratory experiments (Grahame, 1968) to be
related to the initial pressure with which the suction cup is applied to the rubber.
Skin elasticity in vivo
1
//
4
229
---- Diaphragm
-Strip
I
h
0
0025
005
0075
S
FIG.4. Results obtainedtesting two specimens of rubber sheeting by the in vivo apparatus compared
with those obtained by the ‘strip’ method.
_____ --------_
FIG.5. The suction cup used for measuring skin distortion directly.
230
R. Grahame
To test the validity of the assumption that the shape of dome of distorted skin is a segment
of a sphere a direct method of recording ‘x’, the height of the dome, was used.
The device (Fig. 5) was modified by Holt (personal communication, 1968) from that used
by Potter (personal communication, 1967). By this method ‘x’ represented by the distance
from the bottom of the central column to the skin, can be pre-determined by means of a screw
micrometer gauge. Negative pressure is applied to the lumen of the column, and the pressure
at which the lumen of the column is occluded by the dome of skin represents ‘p’. Stress and
strain may be calculated for each pair of ‘x’ and ‘p’ (both recorded directly) using Tregear
formulae, and the gradient of the resultant stress/strain curve taken to represent Young’s
modulus ( Y ) . As in the case of the indirect method of measuring distortion the results were
calculated by the computer.
In four subjects the values for Y using the indirect and direct methods respectively were
1-8 and 1.6; 1.7 and 2.0; 2.2 and 3.3; and 3.0 and 3.6 dyne cm-’. lo8. From the closeness of
the results with the two methods it is concluded that the assumption that the dome is a segment of a sphere is valid.
In an attempt to assess the influence of blood flow on the results of skin elasticity estimations,
a study was undertaken in which measurements were made before, during and 10 min after the
application on the ipsilateral arm of a sphygmomanometer cuff inflated to above the arterial
blood pressure. The results for Y in the left arm were 3.0, 3.1 and 1.6 and in the right arm
2.1, 3.0 and 2.4 dyne cm-’ . 10’ respectively. Thus there was no consistent effect of arterial
occlusion on the in vivo skin elasticity results.
The overall validity of the formulae is shown in Fig. 6 where the results obtained using
suction cups of differing dimensions on the same subject are drawn. It will be seen that the
gradients of the upper parts of the stress/strain curves (i.e. values for elastic modulus) are
similar. By raising the cup pressure to 10 lb in this experiment it was possible to extend the
stress/strain curve to a point that is much higher than is possible in clinical testing where
discomfort is of necessity avoided.
Reproducibility of the method
Optimum reproducibility is achieved only by paying due attention to the following points.
Firstly, a well cushioned area of skin, e.g. mid-dorsal region of the forearm is required to
obtain an adequate clamping effect and secondly, maximal manual stretching of the skin in
two dimensions prior to the application of the cup and with standardization of the pressure
with which the cup is applied to the skin at 2 lb ensures that it is the higher part of the stress/
strain curve that is being sampled during the test.
To assess reproducibility, serial observations were made on the same subjects on 6 successive
days. The results show that a range of +20% of the mean was obtained in each case. In
subject 1 the mean value for the elastic modulus was 3-0 dyne cm-’ . lo8 (range 2.6-3.4;
SEM 0.1) and in subject 2 the mean was 2.6 dyne cm-’. 10’ (range 2.2-3.2; SEM 0.2).
RESULTS
The results obtained will be considered under the following headings : physiological variation
in adults in respect of age and sex; the results in children; and the effect of pregnancy.
231
Skin elasticity in vivo
13-
a
r
0 7 8 01
12 II-
A
10
01
0
128
01
A 159
017
I
%I
S
FIG.6. Results obtained from the right forearm of a healthy male subject using suction Cups of
different dimensions.
Physiological variation in adults in respect of age and sex
The test was performed in adults on thirty-two females and twenty-seven males. Most of
the subjects were either members of the hospital or Institute staff or other healthy volunteers.
A few, mostly from the older age groups, were in-patients at the West London Hospital
convalescing from a variety of acute conditions but were otherwise in good health.
The results (Fig. 7) show that value for the elastic modulus for intact forearm skin in
healthy adult female subjects is significantly higher than that obtained in males (P<O-OOl). If
the data are analysed into the three age groups: 20-44 years, 45-69 years and over 70 years, a
significantly higher value for females is obtained in each group viz. P<O.O1, t0.01 and <0.05
in the three age groups respectively.
There is, in addition, a tendency for the elastic modulus to rise with age in both sexes, and
a regression analysis between elastic modulus and age (Fig. 7) gives a highly significant
correlation (females r = i-0.67, P<O.ooOOl; males r = +0-60, P<0-0004).
The results of the analyses of skin thickness in the same series showed a significant difference
R. Grahame
232
0
-
Male
r=+0.60 P 0.0004
oFemale r=t0.67 PQ~OOOOI
0
W
0
0
0
2
0
x
4l
0
6t-
0
5-20
2
0
I
I
I
I
I
10
20
30
40
50
I
60
I
70
I
80
Age (years)
FIG.7. Elastic modulus of skin in vivo in fifty-nine healthy subjects.
between the sexes only in the 20 to 44 year group, the males showing the thicker skin. A significant inverse relationship between skin thickness and age was also demonstrated in both sexes
in the same series (females r = -0.51, P<0.002; males r = -0.68, P<0-00005).
Results in children
The test was performed on a small group of ten healthy children aged from 3 to 17 years.
The mean value for Young's modulus of intact skin in females was 2.5 dyne cm-2. 10'
(SEM 0.5) compared with 2.0 dyne cm-2. 10' (SEM 0.3) for males. The differences do not,
however, achieve statistical significance. There was also no significant difference in skin thickness between the two sexes.
Pregnancy
Controls
PeOO5
FIG.8. Skin thickness measurements in fourteen pregnant and matched control subjects.
Skin elasticity in vivo
233
Eflect of pregnancy
The test was performed on fourteen patients (aged 18-36) in the last trimester of pregnancy.
Six were primigravide, the remainder multigravide and the mean duration of the pregnancy
was 36 weeks, range 32 weeks to full term. The patients were all attending the Ante-natal
Clinic of the Fulham Maternity Hospital.
Each patient was matched with a control subject for age, height and race. Results obtained
in the skin thickness and elasticity measurements in pregnant patients and control subjects
Pregnancy
Controls
P >005
FIG.9. Elastic modulus of skin in vivo in fourteen pregnant and matched control subjects.
are shown graphically in Figs. 8 and 9. Although skin was just thicker in the pregnant group
(at the 4% level of significance), there was no difference in values for the modulus of elasticity
in the two groups.
DISCUSSION
Vlasblom (1967) came to the conclusion that it was not possible to measure skin elasticity in
vivo by a suction method because of the effect of tethering. The evidence is scanty and is based
on the fact that the experimental results did not coincide with predicted ones. Furthermore
it was assumed that Young's modulus for skin is constant at all ranges of strain, a view which
is at variance with most other workers in this field (Rollhauser (1950), Wenzel(1950), Tregear
(1966), and the present author).
In order to substantiate the idea that using the technique described in this paper the values
obtained for the modulus of elasticity for skin reflect changes in the properties of body collagen,
it is necessary to verify two concepts, firstly, that it is the elasticity of skin alone that is being
measured, and secondly that it is the dermal collagen in the skin that is responsible for its
elastic properties.
R. Grahame
234
Evidence that it is skin elasticity that is being measured is as follows:
(a) the values of the elastic modulus for skin in vivo obtained by this method are of a very
similar order to those obtained by other workers with skin in vitro. Thus in this series the elastic
modulus for in vivo forearm skin ranged in healthy adult subjects from 1.4 to 10.0 dynecm-' . lo8
compared with 64-1 1.47 dyne cm-' . 10' obtained by Rollhauser (1950) with in vitro skin from
the anterior abdominal wall, and 3.4-7.3 dyne cm-' . 10' on in vitro epigastrichuman skin after
formalin fixation obtained by Wenzel (1950).
(b) the calculation of the results is based on the assumption that in the in vivo test the circle
of skin behaves as a free-moving diaphragm uninhibited by underlying tissues. The assertion
that this assumption is correct is based on the findings that meaningful results are obtained
--*I
Y f
le
Adherent skin
f9
...........
*.*.:.:.:.:.:.:..
............
.....................
....................
...........
..............
....................................
.......................................
T=p
=x
S d
P-d
p- - -0- -+I
FIG. 10. Method of calculating stress ( T ) and strain
complete skin adhesion to underlying tissues.
(3under the theoretical circumstances of
in clinical testing with healthy skin, and not when free movement is interfered with either in
vivo when the skin is tethered as in scleroderma or in laboratory experiments where skin
removed a t operation was tested after it had been tethered artificially by a variety of methods
(Grahame, 1968). Where the skin is behaving as a free diaphragm it is unlikely that tissues
underlying the skin would participate in the stretching process.
Theoretically the question of tethering may be considered as follows: at one extreme is the
hypothetical situation where there is no significant tethering. In this case the skin will behave
as an unimpeded diaphragm when subjected to sub-atmospheric pressure and the formulae
applicable to the Dick diaphragm may be expected to apply. At the opposite extreme the skin
may be considered to be totally tethered. In this case the correct formulae would be as in Fig.
10.
Substituting data obtained from in vivo skin tests into the two sets of formulae gives a range
Skin elasticity in vivo
235
of values for Young’s modulus of 1.4 to 10 dyne cm-2. 10’ in the case of the ‘free-diaphragm’
formulae and 2-1-6 dyne cm-2. loJin the case of the ‘adherent skin’ formulae. Since the former
range is likely to be correct (as judged by in vitro work cited in the previous paragraphs) it is
concluded that ‘significant’ tethering does not occur.
(c) even if they could participate, other tissues which might be implicated such as fat, muscle,
etc. have by comparison with skin such a low modulus of elasticity that they would not appear
above the abscissa on the stress/strain curve, e.g. striated muscle has an elastic modulus of
5-2 dyne crn-’. lo4 (Hmcke, 1947) and elastic fibres 3 dyne cm-2. lo8 (Hass, 1942).
It could be argued that since as age advanced there is an associated rise in elastic modulus
and a fall in skin thickness (so that the highly significant inverse correlation exists between
elastic modulus and skin thickness), and since the reciprocal of skin thickness is a factor in
calculating stress, that all the test does is to measure thickness in a round-about way. This
argument can be refuted on the following grounds :
(i) Patients with the same skin thickness show widely differing values for elastic modulus,
e.g. those healthy subjects with a skin thickness of 0-1 cm showed an elastic modulus which
varied from 1.6 to 4.6 dyne cm-’. 10’.
(ii) If thickness were merely all that was being measured then if two differing varieties of
rubber of equal thickness were tested, they should give equal result for elasticity. It was not
possible to acquire two different types of rubber with identical thickness. However, in the experiment to verify the method described above, the ratio of the two thicknesses should equal the
ratio of the two elastic moduli if the test was in fact measuring thickness alone, i.e. dl/dz should
equal Y l / Y 2(where d, and d2 and Y, and Y, represent thickness and the modulus for the
rubber sheet and Esmarch’s bandage respectively).
In fact
Thus
d, = 0.09 cm
d, = 0.0635 cm
Y, = 0.94 dyne cm-’. lo8
Y2 = 0.16 dyne ern-?. 10’
d,
_ ---=0.09
1-4
d, 0.0635
Y, 0-94
_- - - - 5.9
Y, 0-16
That is, there is a four-fold difference between the ratios so that the measurements cannot be
purely an index of skin thickness.
(iii) Finally, the study reported above in pregnancy, together with other studies on the
Ehlers-Danlos syndrome and on chronic obstructive airways disease (Grahame, 1968) all
give results for skin thickness which are significantly less than controls, but there was no
significant difference in either case with regard to elasticity.
The assertion that it is the collagen in skin that is reponsible for its elastic properties is based on
the following evidence:
(a) Skin contains 75% dry-weight of collagen (Weinstein & Boucek, 1960) compared with
only 0.4% reticulum and 4% of elastin, and therefore collagen is the only fibrous protein of
R. Grahame
236
any consequence from the point of view of tensile strength, being the only structure to possess
sufficiently high tensile properties to produce the values obtained for the elastic modulus of
skin.
(b) This idea is strengthened by comparing the values for the elastic modulus of skin with
those obtained for tendon, which is almost pure collagen. Thus the elastic modulus for pig
skin is 2.6 dyne cm-’.108 (Dirnhuber & Tregear, 1966) compared with 7.0 dyne cm-’.108 for
pig Achilles tendon (Bull, 1957).
It seems likely therefore that the strength and elasticity of skin devolves on its dermal collagen. This being so, alteration in elastic properties may be expected to reflect abnormalities in
dermal collagen and possible changes in body collagen in general.
In the light of the above it is now possible to review the results obtained in the clinical studies
and re-assess them from the point of view of possible alterations in structure and function of
collagen.
Age
The results show a progressive rise in the modulus of elasticity with age in both sexes. With
increasing age as skin thickness (d) falls, Td/S rises (P<O.Ol), so that the former alone could
only partly explain the apparent rise in elastic modulus with age. Thus the results confirm
previous in vitro work (Rollhauser, 1950; Wenzel, 1950). This ‘stiffening up’ process of age
could be due to change in the molecular structure of collagen.
There is considerable evidence of an increase in intra-molecular cross-linkages in collagen
(Bjorksten, 1962). More recently it has been shown that inter-molecular cross-links occur,
which may be even more important in increasing stability of the collagen molecule with age
than the intra-molecular ones (Bailey, 1969).
It seems likely that it is these changes within and between the collagen molecules which occur
as part of the ageing process that are responsible for the increasing elastic modulus seen in this
study, and by analogy one may speculate that changes in various other conditions (see below)
may also reflect the changes at a molecular level.
Sex
A striking feature of this study has been the finding of significantly higher values of the
modulus of elasticity in females than in males. It is appreciated that skin thickness (d) is
I
greater in males than females. Since - is a factor of elasticity ( Y ) this could in part explain
d
the sex differences in Y. However, Td/S (which is tensile strength uncorrected for thickness) is
significantly higher in females P<O-001. This sex difference is evident not only in the present
series of healthy patients but also in the other studies of different pathological conditions where
the samples were smaller (Grahame, 1968).
In the healthy groups a significant difference between the elastic modulus in the two sexes
was evident in all the three adult age groups. In children the same differences were also apparent
though less marked than in adults and in the present small series did not achieve statistical
significance.
The finding of higher values for Young’s modulus in females than in males at all age groups
suggest the possibility that genetic rather than endocrine factors may be responsible, since the
Skin elasticity in vivo
237
differencesare seen both after the menopause and in children (where admittedly the differences
were not statistically significant). The implication here is that because female collagen has
different physical properties it is possible that it has different structural properties related to
the collagen molecule and the strength of the cross-linkages.
The increased modulus of elasticity in females has not been previously recorded. The previous
workers were working on in vitro skin. Rollhauser (1950) could not detect any significant
difference between the two sexes, whereas Wenzel (1950) observed a higher value for the
elastic modulus of skin in males. At the present time there is no obvious explanation for the
apparent contradiction between those results obtained by Wenzel and those seen in the present
study. However, Wenzel's results were obtained in vitro on post-mortem formalin-fixed
specimens, whereas the present results were obtained from tests performed on living intact
skin.
Pregnancy
It is known that changes occur in certain ligaments around the pelvis, notably the symphysis
pubis to facilitate parturition. Little is known about the nature of the change that occurs in
the collagen framework of these ligaments. This study was undertaken to investigate whether a
general change in body collagen took place which could be identified by measuring skin
elasticity. The elasticity results suggest no qualitative change in the collagen in this condition.
ACKNOWLEDGMENTS
I am grateful to Dr R. T. Tregear for his continued encouragement and advice; to the staff of
the workshop and the computer unit Royal Postgraduate Medical School ;to Academic Press
Inc., London, for permission to publish Fig. 1, and to Karger A.G., Basel, for permission to
publish Figs. 2, 4 and 7, and Ballibre, Tindell and Cassell for permission to publish Fig. 3.
This work formed part of a thesis for the degree of M.D. of the University of London. It
was commenced during the tenure of an appointment as Registrar to the Department of
Medicine, Royal Postgraduate Medical School and I am grateful to Professor E. G . L. Bywaters
and Dr P. J. L. Holt for their encouragement and advice.
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