J. Soc.

CosmeticChemists20 467-477 (1969) ¸ t969 Societyof Cosmetic

Chemists
of GreatBritain

The mechanicalpropertiesof skin

R. T. TREGEAR*

Presentedat the Symposiumon "Skin", organised

by theSocietyof Cosmetic
Chemists
of GreatBritain,
at Eastbourne, Sussex, on lttth November lt168.

$3tnop$i$--Threemechanical properties of the skin are defined, their empirical study des-
cribed, and the results related to the structures causing them in terms of elementary model
systems.

Any study of a physicalproperty of a tissuefalls into three distinct

stages.First onehasto definethe propertyto be studied;this is sometimes
more difficult than might be imagined,and failure to obtain a gooddefini-
tion has made much of the earlier work in this subjectimpossibleto inter-
pret (1). Secondly,a reliablemethodof measuringthe property has to be
thought out, and reproducibleresults obtained; this may lead to con-
siderabledivergencefrom the normal state of the tissue,particularly when
accurateresultscan only be obtainedon excisedtissue,as has beenthe case
in studying extensionof skin. Thirdly, these empirical results must be
related to the behaviour of the relevant component of the tissue, in the
presentcasecollagen,or the groundsubstance in whichit lies. In orderto
quantitate this relationshipit is necessaryto formulate a mathematical
model of the system; such model building involves an idealised simpli-
fication of the situation, but is essentialin order to visualisethe principles
by which the systemoperates.
In recent years this sequenceof thought and experiment has been
carried out by severalgroupsof workersinterestedin the responseof skin
to extensionand compression, sothat the elementarymechanicalproperties
*Department of Zoology, University of Oxford.
467
468 JOURNALOF THE SOCIETYOF COSMETIC
CHEMISTS

of skin can now be related to the structurescausingthem with a reasonable

degreeof assurance. The purposeof this paperis to showhowtheserelations
between structure and function were arrived at, and to indicate how
similarmeasurements
might be clinicallyor pharmacologically
applied.

DEFINITION OF THE PROPERTY TO BE STUDIED

Three distinct mechanicalpropertiesof skin have been defined:its

immediate extensionwhen tension is applied, its subsequentcontinuous
extensionwhile tensionis maintained, and its gradual thinning under a
localcompression.Taking thesein order,the first phenomenonis immediate
and reversible and is therefore called an elastic extension. The second is
gradual and irreversibleand has thereforebeentermed variouslyviscous
extension,viscousslip, or creep.The third is also irreversiblein the sense
that removal of the force doesnot restorethe status quo ante and is not a
true compression; sincethere is no gaspresent,skin must be virtually in-
compressible. It is actuallya movementof fluid out from underthe com-
pressingforce,and has thereforebeentermedviscousflow.
It is virtually impossibleto obtain completelyreversibleelasticpheno-
mena, i.e. there is always someslip, and under high tensionsomeviscous
flow alsooccursdue to internal compression (2). Thus in practicethe three
propertiescannotbe completelyseparated,but in theory they represent
different phenomena,which can be adequatelyisolated by appropriate
experiments.

EMPIRICAL STUDY OF THE MECHANICAL PROPERTIES

Elastic extension

This propertyhasbeenwidelystudied.A largevariety of extensometers

have been employed,some designedspecificallyfor the purpose(3, 4).
These deviceswork with excisedskin cut in the form of a strip; similar
resultscan be obtained from discsof skin subjectedto a uniform pressure
(5, 6). In principleit is desirablethat the measurementshouldbe instan-
taneousin order to avoid viscousslip, but in practicemeasurementshave
usuallybeentaken somesecondsafter the extension,or duringcontinuous
extensionat a rapid rate. Although this doesallow someviscousslip (7)
most of the deformation is elastic and the results obtained by different
observersshow considerableagreement.
 THE MECHANICAL PROPERTIES OF SKIN 469

/
4 I

/ = tan 8
ß /

2 4 I e e
Slack =I
I

Strain (% rest length)

FigureI Extensionof a stripof excised

pigskin[redrawnfrom(6)].

Theprimaryobservation isthat skinmaybereadilystretched by a few

percentof its lengthat zeroextension, but thenrequires progressively
greatertensionto stretchit further(Fig. 1). It hasnot beenpossible to
fit thisgraphto a single
mathematical relationship,owingtotheverygreat
change in curvaturebetween the earlierandlater portions,althoughthe
twoportions havebeenfittedseparately to different
equations(7). Without
mathematical analysisit is possibleto extracttwo parameters directly
fromthe graph,the average slopeof the finalportion,whereit is quasi-
linear,andthe interceptof thisslopeon the extension axis(Fig. 1). The
slopesoobtainedgivesthe maximalelasticmodulus(Yn•ax) for the tissue;
the published valuesforhumanskinliewithintherange2 - 11x 103Ncm-2
of cross-sectional
area,andfor otherspecies 0.8-3 x 103Ncm-2(6). The
elasticmodulus increaseswith theageof theindividual(8)andappears to
be lowerin femalesthan in males(9).
Extrapolationof thisslopebackto the extension axisyieldsa valuefor
the regionof easyextensibilityor "slack"in the tissue.Estimatesof slack
alsovarywidelybetween observers;
valuesbetween 3 and 14%may be
derivedfromthe published
data.Thisvariationis not surprising,
for it is
verydifficultto knowexactlyat whatpointto startthegraph,astheinitial
extensionrequiressolittle force.Within any onesetofobservations
thereis
muchmoreconsistency
and it hasbeenshownthat the slackdecreases
with
470 JOURNALOF THE SOCIETYOF COSMETICCHEMISTS

age (2) and is greaterwhen the specimenis cut acrossLanger'slines (the

linesof maximumpre-existenttensionin the skin)than whenit is cut along
them (10).
Gibsonet al {2) also measuredthe lateral contractionof the skin as it
wasextended,and foundthat the changeswereapproximatelyisovolumetric
up to the regionof high tension,when fluid was extruded and the volume
fell.

Viscousslip
The sameapparatusmay be used to study viscousslip as was devised
for elasticextension;
all that is requiredis that the loadbeleft on.Ridgeand
Wright (7) showedthat therewasa very rapidstressrelaxationonextension,
lastingonly a few seconds; the data citedabovewereall obtainedafterthis
relaxation. Harknessand Harkness {3, 11) on the other hand, were con-
cernedwith the much smallerand moreprolongedslip of collagenous tissue
heldunderconstantloadfor severalhours(Fig. 2, lowerline).Thisprocess
Break

• 6o

,ø"• Normal
•Ogload

I I
0 50 100

Time, rain

trigur• œ Continuedextensionof chick skin under a constant load; "circumference"as

ordinateis equivalentto length of the tissue,owingto the methodemployed [from {12)].

may be quoted in terms of a viscousextensibility(u), the velocity of

extensionper unit force applied (for derivation see6). The processis ex-
tremely slow;for examplea 10 N cm-2 forcecauseda slip in normal rat
skin of some 0.05% min-• (u---5 x 10-5 cm2 N-• min-1). Trypsin treat-
ment, but not hyaluronidase,increasedthe viscousextensibility.Wenze!
(13) in comparableobservations,showedthat the viscousslip of human
 THE MECHANICAL PROPERTIES OF SKIN 471

skin svasgreatly increasedover a regioncontainingstriae gravidae.Viscous

slip is essentiallyan irreversibleprocess,and it has often been assumed
that it is unphysiological;however,the very presenceof thesestriaeshows
that it can occur in life.

Viscousflow

This processhas beenvery little studied, although the residualimprint

madeby any heavy pressureon the skin showsits existencein ordinary life.
In order to measure the change in thickness of the skin due to such a
pressure,either onecan ensurethat the skin is supportedby a firm backing
(e.g. the shin bone, or a supportedskinfold), in which casethe movement
of the compressingweight itself registers the deformation, or one can
measurethe movementof the weight relative to undeformedneighbouring
skin. A device of this sort was usedby Schade(14) but his resultswere
not followedup until Kirk and Kvorning (15) revived the method to assess
changesin old age. Tregear and Dirnhuber (16) showedthat both methods
B

300
xx,•
x"•x•x•
x='='x7
x
200

'øø
l
0 20 40 60

Time , min

Figure 3 A, compressionof a fold of rat skin by a constant force (910g over 2 cruZ).
B, compression of the theoretical model system (cf. Fig. 6); the parameters used were
ho-----
400 •m; •1= 1.2 min-• [from (6)_•,

gave similar results, and establishedthe time-courseof the deformation

under constantpressure(Fig. 8). This time-courseis non-exponential;the
first part of the deformationis very rapid, and a long tail of continued
depressionoccursfor many hours. The processwas greatly increasedin
speedby the action of hyaluronidase.
472 JOURNAL OF THE SOCIETY OF COSMETIC CHEMISTS

THE STRUCTURAL BASIS OF THE MECHANICAL PROPERTIES

Removal of the fat and epidermisfrom excised skin has little effect
on its elasticmodulus (Ymax).The strength therefore lies in the dermis.
The only fibrousstructurein the dermisthat couldprovide this strengthis
collagen(the elastin is far too weak) and when the observedmodulusis
divided by the collagencontent it gives figuresin the order of 104N cm-2
which is similar to the values obtained from fully orientated collagenin
hydrated tendons(6). It is thereforevirtually certain that the strengthof
the skin lies in the collagen.The nature of the deformationof the collagen
structure is not so certain; X-ray diffraction has shownthat when rat tail
tendonis extendedthe tropocollagen moleculesthemselvesare elongated,
presumablyby bendingof the covalentbonds(17),but astheseexperiments
were on dried material and required much greater stressesthan can be
appliedto skin, it is possiblethat in the physiologicalstate there is another,
weaker link betweenthe tropocollagenmoleculeswhich is extended.What-
ever the exact molecularorigin, high extensionsof skin appearsto involve
extension of the collagen itself. This causes extrusion of fluid, as in
viscousflow (2) and a pronouncedchangein the stainingreaction of the
collagen(18).
In unstressed skin it has been noted that most of the histologically-
observablecollagenfibreslie along Langer'slines, the lines of pre-existent
force(19). When the excisedskin is stressed,on the other hand, the fibres
were found to line up alongthe new linesof force (2). It followsthat the
slackin excisedskinis probablydue to lining up of the collagenfibresin the
directionof pull; this explainswhy there is more slack acrossLanger's
linesthan alongthem.
It is not easy to seehow these histologically-observable fibres, which
are bands of parallel collagensfibrils, can be rotated to resist the tension
applied.Ridge and Wright (10) and Kenediet al (2) have independently
proposedmeshworkstructures,which can be pulled out straight in either
of two directions(Fig. •t). The difficultyabout a meshof this sort is that if
it isjointed(Fig. •IA) thenin the directionsof the linesof the meshitpossess-
esno slackat all. If the wiresof the meshare free to slidepast the joints
(Fig. •IB) this difficultyis avoided,but other geometricaldifficultiesarise.
Such a model explains the occurrenceof slack, its higher values across
Langer'slines, isovolumetryunder stress,and the orientationof collagen
along lines of force,whatever their direction. If one collagenfibre has to
slip past anotherto take up positionalongthe lines of force,it would also
 THE MECHANICAL PROPERTIES OF SKIN 473

Figura 4 Models of collagenmeshworkswhich contain slack. The arrows mark direction oœ

Langer's lines.
21, meshwork with fibres free to rotate but not to slip at joints.
B, meshwork with fibresfree to rotate and to slip at joints.

explain Ridge and Wright's stress-relaxation.The simplemodel doesnot,

however,provide a resistingand restoringforce, necessaryto explain the
curvature of the stress-straingraph and its reversibility. Gibson et al {2)
did insert such a componentinto their modelin the form of a compress-
ion springwhich held the meshesopen,but it is not clear what structural
validity this concepthas; it could be a property of the elastin, or of the
local compressiveforces exerted on the ground substance during the
movement.This subjectneedsfurther study.
The slowerviscousslip seenby Harknessand Harknessis not explicable
in these terms. To accountfor it one has to supposethat at somelevel
of organisationthe aggregatesof collagenmoleculesmove past one another
irreversibly. A simplifiedconsiderationof the mechanicsof this system
[Fig. $; (t3)•;showsthat the fibreswhich are slippingpast one anothermust
be very closeto oneanotherand in a highly viscousmedium;if thiswerenot
so the slip would be very much faster. 1 cm long fibrils 100nm in diameter
and 10 nm apart would need to lie in a medium of viscosity 50 P to
allow the speedof slip seen.As theseare realisticdimensionsfor the fibrils
of collagenous fibres,and a reasonablevalue for the viscosityof the ground
substancebetweenthem, this is the most probableorigin of the slip seen.
474 JOURNALOF THE SOCIETYOF COSMETICCHEMISTS

(o)
Set
i i / -Velocity
v
Set I Set n /

(b)

Rods
ofset
i+l-•"•0• h-2r

o,
s,,, o
Figure 5 Model of slipping collagenfibres. They are assumedto move at a constant velocity
[for details see (6)].

Presumablythe histologically-observable bandsof fibresdo not slide past

one another becausethey effectivelyform a continuum from one end of the
tissue to the other, as indeed has been assumedin the explanation of
elastic extension.
Viscous flow is accounted for in terms of movement of the ground
substance,and not of the fibrousmatrix. Sectionstaken through a region
of compressed skin showthat the dermisis greatly reducedin thicknessand
the collagenfibresare closelypackedtogetherunder the pressurewhereas
in the adjacentregionthe fibresare parted and the dermisis thicker than
normal;somefluid flow has occurredbetweenthe two regions.Onceagain
simple model-building sufficesto give an adequate description of the
phenomenon.If one imaginesthat the ground substancehas to flow out
through restricted channelsin local regions, and then passeseasily to
the outsideof the compressed area (Fig. 6), the mathematicalsolutionfor
the resultant time-course of deformation qualitatively resemblesthat
actuallyseen(Fig. $), and with reasonable valuesof the parametersa good
quantitative fit can be obtained (113).The processis not strictly speaking
reversible,but massagewill causea return flow, by applying an opposing
pressuregradient.
It is to be hoped that these elementary models of the mechanical
propertiesof the skin will be further testedby experiment;as the present
data are so scanty it is extremelylikely that they will have to be modified
 THE MECHANICAL PROPERTIES OF SKIN 475

when they have beentested.Nevertheless they do sufficeto explainthe

most obviousmechanicalpropertiesof the skin in termsof its structure.

Figure 6 Model of compresseddermis. It is supposedthat the viscous ground substance

moves with difficulty from within the individual stacks of plates, and then easily out from
under the total compressedregion. The equation of motion derived is that the compression
x=ho(1 - (1+ •t)-•) where[•is a constantdependentonthe viscosityof fluid and dimensions
of the system;ho is the original thicknessof the tissue [for further details see (6)].

OUTLOOK

The big drawbackto the clinicalor pharmacologicalstudy of extension

in skin is the lack of an in vivo method. Three attempts to provide
sucha methodshouldbe noted;Dr. R. Grahameat the Kennedy Institute
of Rheumatologyhas developeda method of pulling the skin up by nega-
tive pressure,and measuringthe deformationfor a givenpressuredifference,
while both Vlasblom(20) and Prof. S. Shusterat Newcastle University
have devised methodsof measuringthe twist of the skin under a given
torsion about a vertical axis. One of these methods should make
clinicalstudy of skin extensibilitya practicalproposition.
Given that a practical method of measurementexisted,what might one
hope to extract from it? The effectof extremetensionis not, in itself,
physiological,but the elasticmodulusshouldgive a measureof the state
of the collagenin the dermisand perhapsshowearlier or lessextremecases
of elastosisthan are visible simply by pulling the skin. A measureof the
tension at which slip became appreciablemight xvell also be useful in
studyingthe effectof drugson collagenous tissue.
Deformation under compressionis readily measuredin vivo, so that
there should be no difficulty in its practical application on patients or
animals.It is primarily a measureof easeof flow of the intradermal fluid,
in itself dependenton the viscosityof the groundsubstanceand on the
476 JOURNALOF THE SOCIETYOF COSMETICCHEMISTS

separationof the fibrousmatrix (hencethe easyflow in oedema,when the

fibresare parted). It is possiblethat applicationof a simplemechanical
test might supplementthe diagnosticskill of the physician'simpressed
thumb, and also might be usefulin assessing the effectsof drugson the
skins of animals.
In sum, theseare largely unexploredtechniques.The basicessentialsof
the processes are known,so that it shouldbe possibleto make meaningful
clinical or pharmacologicalmeasurements.
(Received:œOthAugustlt?6'8)
REFERENCES

(1) Rothman, S. Physiologyand biochemistryof the skin (1954) (University Press, Chicago).
(2) Gibson,T., Kenedi, R. M. and Craik, J. E. Brit. J. Surg., õ9,764 (1965).
(3) Harkness, M. L. R. and Harkhess, R. D. J. Physiol., 148 524 (1959).
(4) Ridge, M.D. and Wright, V. Med. Biol. Engng., 4 533 (1966).
(5) Dick, J. C. J. Physiol., 119,109.(1951).
(6) Tregear, R. T. Physicalfunctionso.fskin (1966) (AcademicPress,London).
(7) Ridge, M.D. and Wright, V. Biorheology,9,67 (1965).
(8) Rollhauser, H. Gegenbauers Morph. Jb., 00 9.49 (1950).
(9) Ridge, M.D. and Wright, V. Engineering, 199 363 (1965).
(10) Ridge, M.D. and Wright, V. J. Invest. Dermatol.,415341 (1966).
(11) Harkness,M. L. R. and Harkness,R. D. Nature, 18111821 (1959).
(12) Fry, P., Harkhess,M. L. R., Harkness, R. D. and Nightingale, M. J. Physiol., 115477
(1962).
(13) Wenzel, H. G. Zentr. ,,Illgem.Pathol.Phathol.,4nat., 85 117 (1948).
(14) Schade,H. Z. Exptl. Path. Ther., II 369 (1912).
(15) Kirk, E. and Kvorning, A. S. J. Gerontol.4 273 (1949).
(16) Tregear,R. T. and Dirnhuber, P. J. Invest.Dermatol.,45 119 (1965).
(17) Cowan,P.M., North, A. C. T. and Randall, J. T. Syrup.Soc.Exptl. Biol., 9 115 (1955).
(18) Craik, J. E. New Scientist,$1 88 (1966).
(19) Cox, H. T. Brit. J. Surg., 9,9234 (1942).
(20) Vlasblom, D.C. Skin Elasticity (1967) (Doctoralthesis, Utrecht University).

DISCUSSION

PROFESSOR
F. J. EBL1NG:Nothing was said about elastic fibres. Could we have a
note about this?

T}m LECTUI•Ea:I kno•v nothing certain about the role of elastic fibres. However,
it is evident that the extension of skin is elastic, even at low degreesof extension
xvhereall the collagenfibreshave not beenpulled out taut. If one assumesa meshwork
hypothesis,then somethinghas to pull the mesh back to its original angle when the
stressis removed. This restoring force could conhefrom elastic fibres running across
the meshwork, and hence strained by a much greater percentagethan the overall
strain on the skin, or it could come from local compressionof the tissue.More work
is needed before one can decide between these suggestions.

Mi•. N.J. VAN A•eg: I shouldlike to refer to page 472, particularly the tniddle
paragraph and the first sentence, where you say that most of the histologically-
 THE MECHANICAL PROPERTIES OF SKIN 477

observable collagen fibres lie along the lines of pre-existent force. Do you not think
that in the light of what has been said about collagen, this could be put that the
strains in the collagen can dictate the pattern of histological staining? In other words,
that the collagen fibres are an artefact of histology, and if you then accept the concept
that collagenis a gel, how will this fit in with your difficulties in the next paragraph?
THE LECTURER:This is a long-standing controversy. The evidence concerneddoes
not come from my work, but, as I understand it, during stressone seesin fixed tissue,
a great many more "fibres" cut in cross-sectionacrossthe line of stressthan along it.
This is plain observation and is not, I think, controversial. The controversy is whether
or not these optically-observable fibres were produced on fixation. I would suggest
that the difference between stressed and unstressed tissue can hardly be due to
fixation, since the stresswas applied, and I believe removed, before fixation.
A further point is that the orientation of fibrils is also seen within the electron
microscope, i.e. the appearance of fibres in the optical micrographs represents a
preferred orientation of the fibrils. While the parallel aggregation of these fibrils
into discretefibres with spacesbetween them may be an artefact, it is hardly likely
that the changein preferred orientation of the fibrils under stressis one.
MR. 1NI.j. VAN ABBI•: I would have thought you could get just the sanheeffects
with the electron microscopeas with the optical microscope.
THE LECTURE•:The optical microscopecan give artefacts about things shrinking,
hence this long-standingcontroversy about gelation. The electron microscopeis,
however,not giving artefactual fibrils;they can alsobe observedin X-ray diffraction
of fresh tissue, and are aggregatesof the tropocollagenmolecules,some 50nm across.
If I can seethese orientated in oneway when unstressed,and in another when stressed,
then I feel justified in saying that they turned round.
DR. T. J. ELLIOTT: What are your opinions on the application of mechanical
forces to the skin, as conducted by the forms of vibro-massageor massagecreams?
Are theselikely to have any permanenteffect upon the area of the skin that we are
interested in?

THE LECTUre;R: I know nothing specifically about vibro-massage. In general

terms, however, a sufficiently strong vibration should set up the compressireflow of
ground substancewhich I have discussed.Tile channelsthrough which this fluid
flows, even if they only exist transi•orily, are prestonablyliable to alter if they are
ex•ensivelyused. One thereforemight supposethat vibro-massagemakesthe ground
substance flow more readily.
I[I might make a specific suggestion:the co•npressionmethod which I have
mentionedcan be readily and simply applied to a patient in vioo,and you could use
it to seewhether vibro-massagehad, in [act, increasedeaseof ttow on compressiou.