Directional variations in the extensibility of human skin

British Joumal of Plastic Surgery (1977), 30, 105-114

DIRECTIONAL By H. L.

VARIATIONS IN THE EXTENSIBILITY

OF HUMAN SKIN

STARK, B.Sc., Bh.D.STRATH., C.Eng., M.I.Mech.E., M.1.E.Aust.l

Bioengineering Unit, StmthcZyde University, Glasgow, Scotland

THE extensibility of human skin enables the body to move. Coincidentally, it allows the plastic surgeon to close skin defects by advancing directly the adjacent skin and to design a variety of rotation-advancement flaps. But extensibility is very variable: it varies from one site to another on the same body; at any one site on one body, it may be quite different from that on the same site on another body; at any one site extensibility shows directional variations; finally, at any site and in any direction it decreases with age (Gibson et al., 1969; Stark et al., 1969; Millington et al., 1971). The following paper presents the results of an investigation into skin extensibility to define the more relevant parameters of extensibility and their variation particularly at different sites and in different directions. When human skin is extended along one direction, the typical relationship between load and extension is of the form shown in Figure I. The initial extension requires relatively little load but is followed by a terminal phase of high stiffness during which the skin requires very much higher increments in load to achieve similar increments in extension. Every surgeon is aware of this behaviour; if a skin defect which can be readily approximated is slowly increased, a stage is suddenly reached where, instead of closing easily, much greater force is required. This is the basic shape of the “stress-strain” curve obtained with most soft tissues although there are extremely wide variations. The individual curve can be largely characterised by the length AB and the slope of BC: i.e. the angle CB makes with the horizontal axis. AB is a measure of the initial low-stiffness extension and is known as “limit strain”; it is expressed as a percentage of the initial length. The slope of BC, the tangent to the high stiffness phase of the relationship, is quantitatively an increment in load per unit width of specimen divided by the associated increment in extension and is named “terminal stiffness”. The more closely BC approaches the vertical the greater the stiffness. METHODANDMATERIALS In order to measure these parameters in both the living body and cadaver skin the “extensometer” shown in Figure 2 was used. It has been described in detail before (Gibson et al., 1969; Stark et al., 1969; Stark, 1970) but briefly the 2 arms which can be driven apart at a constant speed, apply a load to the skin by means of metal tabs stuck to the skin by double-sided adhesive tape. The arms incorporate strain gauges. In essence the extensometer extended in one direction at a time, a 30 mm length of skin. A die was used to print on the skin four 30 mm gauge lengths at ~5~ to each other as shown in Figure 3. Load-extension recordings were taken for 3 extension tests carried out along I direction of a given site; this was then repeated in the remaining 3 directions. 1 Present address: School of Mechanical Engineering, University of New South Wales, Sydney, Australia. 3012-A

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FIG. I. When skin is stretched it will extend a certain distance with little increase in load. Thereafter great increases in load are necessary for further extension. AB measures “limit strain”, the slope of CB “terminal stiffness”.

FIG. 2. (a) The extensometer used in the tests consists of 2 strain-gauged arms (*) which can be driven apart at a constant rate. (b) The arms are attached to the skin via metal tabs stuck on with double-sided adhesive tape.

Thus 12 values of limit strain and 12 values of terminal stiffness were recorded for each site. The directional variations in skin extensibility when a standard load was applied were also measured. A polar graph of a typical set of results for one of the parameters is shown in Figure 4, the curve drawn through the points being fitted by computer aided statistical analyses. DIRECTIONAL VARIATION IN LIMIT

15

STRAIN AND TERMINAL STIFFNIN

The results obtained for a series of tests carried out on 3 male patients aged between and 30 years and of average constitution are reported in Figures 5 and 6. They were

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0

0

3

SKIN

107

I

4

FIG. 3.

FIG. 4.

OF HUMAN

Skin markings for directional

extension tests.

Three extension tests were carried out in each direction and with the aid of a computer, polar graphs of this form were drawn for each parameter at each site.

-, SYMPnYSlS PUBIS

FIG. 5. Lit FIG. 6. Terminal

strain right anterior abdomen. stiffness right anterior abdomen.

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FIG. 7.

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Maxima and minima of the load/extension curves midway between the umbilicus and the anterior superior spine.

FIG. 8. Plotting the variations in extensibility with a standard load. The scale used for the polar graph was such that a point on the graph having the same radius as the circle would be representing an extensibility of 20 per cent. In this instance the maximum would be 30 per cent and the minimum IO per cent.

carried out within the triangle defined by the umbilicus, symphysis pubis and right anterior superior iliac spine. They indicate a very pronounced orientational relationship between limit strain and terminal stiffness; the direction having the maximum value of limit strain is the same as that of minim al terminal stif’liress. A very large variation in the magnitude of both parameters is noted; the variation is apparent between test sites and with direction within each site, the extremes of the parameters being 25 to 48 per cent for limit strain, and 27 to 290 g/mm for terminal stiffness. The load-extension relationships for the orientations of maxima and minima for the site midway between the umbilicus and the anterior superior iliac spine are given in Figure 7, having been reconstructed from the data given in Figures 5 and 6. These 2 curves give a graphical indication of how the load-extension relationship varies with direction at a given site. Langer’s cleavage lines correlate very closely with the direction of minimum limit strain and maximum terminal stifkess (Langer, 1861). A similar series of tests was carried out on the chest yielding similar conclusions, although many of the chest sites did not show a significant difference in the load extension relationship with orientation of test. Tests on cadaver skin. Ten specimens of shin were removed at random from a number of fresh cadavers. Each specimen was defatted with a dermatome and then cut into a 50 mm diameter disc having a concentric 30 mm diameter circle printed on it. The load-extension tests were repeated as in the in viva series, excepting that the specimens were tested while lying on a wet glass plate and after each test were aided manually to return to their original shape; if unassisted they failed to regain completely their initial circular shape. The orientation of the cleavage lines for each specimen was also determined by tapping a conically pointed nail through the skin bordering the specimen; this was

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FIG. g. The red circle represents 20 per cent extension, the blue/green polar graphs the actual extension in each direction for a standard load. Note the extensibility on the medial side of the thigh to accommodate abduction of the hip. FIG. IO. The maximum extensibility

in the vertical direction over the buttocks and thighs permits flexion at the hip.

repeated IO times for each specimen and the average value of the orientation of the resulting linear wound recorded. The magnitude of limit strain recorded in this series of tests varied between 16and 52 per cent with 8 of the IO specimens showing a significant difference at the 5 per cent level of the F test with test orientation. Likewise terminal stiEness fluctuated between the extremes of 105 and 332 g/mm, also with 6 of the IO specimens showing a difference with test orientation. With minor variations of no statistical significance the direction of the maxima and minima of limit strain was at right angles respectively to the minima and maxima of terminal stiffness. Of the IO specimens, 8 showed a consistent cleavage line orientation; 2 specimens which did not were also the 2 specimens not showing a significant difference in limit

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strain with orientation; it was noted that these 2 specimens, in addition to not showing a consistent cleavage puncture orientation, had a high proportion of punctures of a triangular form, instead of the more usual linear wound. When present, the cleavage lines correlated well with the direction of minimum limit strain and maximum terminal stiffness. DIRECTIONAL VARIATIONS IN EXTENSIBILITY AT CONSTANT LOAD

It is not surgically possible to extend skin beyond its limit strain since the lumen of the blood vessels becomes obliterated in the aligned collagen network and necrosis The variable of greater significance and value to the surgeon results if long continued. is therefore limit strain. An extensometer was adapted to apply a constant load of 14.2 g/mm which is sticient to achieve an extension marginally in excess of that associated with the elbow in the load extension relationship (Fig. 7). It was found on application of such a constant load intensity that the extension reached relative stability after approximately 1.5 seconds. Those areas of skin with a large enough radius of curvature to allow application of the extensometer were tested on I individual: a male aged 26 and of average constitution

FIG. II.

Anterior

chest and shoulder.

FIG. IZ. Posterior

chest and shoulder.

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III

FIG. 13. Right lateral thigh. FIG. 14. Right medial thigh. FIG. IS. Right anterior leg. FIG. 16. Right lateral leg. FIG. 17. Posterolateral

aspect of right leg.

FIG. 18. Lower medial aspect of right leg.

lying horizontally, either face down or face up, with the elbow and knee joints extended. A 30 mm diameter circle was printed on the shin after which the points of the extensometer were applied, diametrically opposite, to the outer edges of the circle; a few seconds later the extended diameter was measured and the increase in length plotted in polar graph form using the centre of the circle as the origin. This procedure was repeated for at least 8 orientations per site thus allowing a continuous polar graph to be drawn for

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each site. The scale chosen for the polar plot was such that a point on the plot having the same radius as the circle would be representing an extensibility of 20 per cent. For the specimen result shown in Figure 8 a maximum extension of 30 per cent and a miniThe results are shown in Figures g-23. mum of IO per cent are recorded. To allow comparison between individuals the back of the chest was tested in 3 other males of similar age and constitution (Fig. 24). DISCUSSION That skin is extensible depends on 3 factors which operate consecutively as the extending load is increased: (I) convolutions in the dermal collagen fibres straighten out; (2) more and more fibres become aligned parallel to each other in the direction of the load; (3) the parallel aligned fibres extend but only with great increases in load. Limit strain involves factors (I) and (2), terminal stiffness, factor (3). They operate no matter in which direction the skin is extended but the values differ in direction on most parts of the body. These directional variations are a function of the woven pattern of collagen fibres in the dermis; more fibres run in a direction closer to that of minimum extensibility than at right angles to it. Thus limit strain is least in the direction of minimum extensibility; as Langer found, when a load equal in all directions such as the

FIG. 19. Posteromedial FIG. 20. FIG.

21.

FIG. 22.

aspect of right leg.

Right side of chest: axilla on left.

Lateral aspect of right upper arm: shoulder on left. Posterior

FIG. 23.

aspect of right arm: shoulder on left.

Anterior aspect of right arm.

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FIG. 24. (a, b and c) Posterior upper chest and shoulder in 3 other volunteer young adults. with Figure IZ and note the individual variations.

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Compare

pressure of the point of a round bodied instrument is applied, the fibres in the direction of minimum extensibility are the first to become aligned and can then be “cleft” (Gibson et al., 1971). Similarly, terminal stiffness is greater in that direction as more aligned fibres resist further extension. The relationship between these directional variations in extensibility and skin tension is not so readily defined. It is apparent that the described variations with orientation and site are not produced solely by fields of tensile forces within the skin on the body. Such fields of force did not exist in the cadaver skin tests since the skin was allowed to relax fully prior to testing. It was noted, however, that on removal from the cadaver a proportion of the specimens contracted, and that that contraction frequently exhibited directional variation. Skin tension depends on 3 factors: the network of elastic fibres in the dermis, the movements of the body and variations in bulk of the tissues covered. Langer (1862) has shown that changes in skin tension can alter the pattern of the cleavage lines which bear his name. The new-born child has a pattern of lines running circumferentially around the limbs and trunk; movements of the limbs in utero are greatly restricted and the main tension exerted on skin is by the swelling volume. After birth the active movements of the child gradually impose the adult pattern of cleavage lines which are present by the time the child is 2 years old. The swelling uterus of the pregnant woman also completely changes the cleavage line pattern of her abdominal skin. Langer also found that when he made incisions at the same site but on opposite sides of the same cadaver, the incision made at right angles to the cleavage lines gaped more than that which was made parallel to them. From the illustrations it is obvious that the varying patterns of extensibility depend on the joint movements involved; where there is no movement of the skin there is very little extensibility at all as on the lower leg. At first sight it would seem a paradox that joint movements should impose not only increased extensibility in one direction but increased skin tension at right angles to it.

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However the increase in skin tension in one direction may equally be regarded as decreased skin tension at right angles to it. It would appear therefore that joint and respiratory movements impose on the body skin increased extensibility and decreased skin tension in the direction in which the mobility is required. These are reflected in the pattern of the dermal collagen fibres and this in turn is responsible for the variations which have been measured in limit strain, terminal stiflbess and extensibility. SUMMARY

When an extending load is applied to human skin in sivo or in vitro the skin stretches with small increases in load until a limit is reached (limit strain) after which much greater increases in load are required to extend it further (terminal sti&ess). At many sites there are marked directional variations, the direction of maximum limit strain being the same as that of minimum terminal stifhress and vice versa. The directional variations of extensibility at constant load on a young male body have been measured and recorded. The author wishesto thank the staff of the Plastic andOra Surgeq Unit, Canniesbm Hospital, Glasgow and of the Bioengimering Unit, University of Strathclyde, Glasgow. In particular the author owes a debt of gratitude to Professor T. Gibson, Professor R. M. Kenedi and DrJ. H. Evans. REFERENCES T., STARK,H. L. and EVANS, J. H. (1969). Directional variation in extensibility of human skin, in vivo. Journal of Biomechanics, 2, 201. GIBSON, T., STARK, H. and MI. R. M. (1971). The significance of Lanner’s lines.

GIBSON,

Tr&sa&ns

of the 5th Intemakmal

Con&ss’of

Plastic-and

Reconstruct&e

Surgery,

edited by Hueston, J. T. Australia: Buqerworth, p. 1213. LANF;~~~K. (1861). Zur _Anatomze und Phynolope der Hauc. I. Uber die Spaltbarheit der Smnmgsbenchte der Mathematlsch-natmwrssenschafthcher Classe der Kaiserlichen Akademie der Wissenschaften. Wien. AA. ro. LANGER,K. (1862). Zur Anatontie und Physiologie der kk&.~ II. Die Spannung der Cutis. Sit2ungsberichte der Mathematisch-naturwissenschaftlicher Classe der Kaiserlichen Akade&ie der Wissenschaften, Wien. 45, 133. MILLINGTON, I?. F., GIBSON, T., EVANS,J. H. and BAREIBNEL, J. C. (1971). Structural and mechamcal aspects of connective tissue, in “Advances in Biomedical Engineering”, edited by Kenedi, R. M. London and New York: Academic Press. STARK,H. L., EVANS,J. H. and GIBSON, T. (rg6g). Directional variation in extensibility of human skin, in vivo. 8th International Congress on Medical and Biological Engineering, Chicago.