Healing of Incisional Wounds in Rats: *

The Relationship of Tensile Strength and Morphologyto the Normal Skin Wrinkle Lines

CAPT. COSTAN W. BERARD,** MC, USA, CAPT. STEPHEN C. WOODWARD, MC, USA,CAPT. JoHN B. HERRMANN, MC, USA, COL. EDWIN J. PULASI, MC, USA

From the Walter Reed Army Institute of Research, Walter Reed Army MedicalCenter, Washington, D. C.

PRINCIPAL goals in surgical repair of skinincisions are rapid accretion of strengthand minimal ultimate deformity of thewound site. Efforts to improve results havefocused attention upon both surgical tech-nic3 and presence in the skin of a well-ordered topographic pattern, first exten-sively described by Langer.17The first description of lines of skin ten-

sion on the cadaver is credited to Dupuy-tren.7 Langer extended these observationson adynamic skin and presumed the ex-istence of minute rhomboids of connectivetissue fibers arranged in a manner similarto the geodetic lines on the earth's surface.Kocher 14 advocated the making of surgicalincisions in conformity with Langer's lines,resulting in their wide acceptance as aguide for the direction of incisions on thebody. Langer's lines continue to be repro-duced in many publications on general andplastic surgery.2 4,9 21 It has been taken forgranted that incisions parallel to these linesafford good exposure, facilitate marginalapproximation, allow rapid healing, andminimize the size of the scar."5More recently, attention has been di-

rected to the importance of wrinkle lines,which often parallel Langer's lines yet de-viate considerably at several body sites.55 16, 22, 27 Most apparent about the face,such wrinkle lines have been shown to be

oriented perpendicular to the direction ofthe subjacent muscle pUll.'15 16, 22 It hasbeen suggested that incisions parallelingwrinkle lines result in minimal scarring andinterference with muscle contraction be-neath the cicatrix.15' 16 22 In a study em-ploying x-ray diffractograms of normal skinand scars, Holmstrand et al.13 provided anultrastructural basis for making surgical in-cisions along wrinkle lines. They providedevidence that collagen at the molecularlevel is oriented in intact skin principallyin the same direction as the wrinkle lines,and that orientation of collagen in scars ispredominantly in the longitudinal axis ofthe scar. The authors concluded that inincisions made parallel to the wrinkle lines,"the new collagen will develop the sameorientation as the neighboring skin andpresent the best ultrastructural reconstruc-tion of the dermis."With the light microscope, studies relat-

ing the orientation of connective tissuefibers to Langer's lines or wrinkle lines arefew. Cox 5 found a relationship between thedirection of collagen fibers and the cleav-age lines in human skin using ordinary his-tologic methods. Shaw and Copenhaver 23 24

using similar methods suggested that themajority of fibers of connective tissue aredirected in a pattern similar to Langer'slines. We wish to report the effects of ori-entation, with reference to wrinkle lines,upon the tensile strength and morphologyof healing skin incisions in the rat.

260

* Submitted for publication February 1, 1963.** Present address: Department of Pathologic

Anatomy, N.I.H., Bethesda 14, Md.

HEALING OF INCISIONAL WOUNDS IN RATS

Methods

Three experiments were performed: oneto investigate the tensile strength of normalskin parallel and perpendicular to wrinklelines, and two to characterize healing of in-cisions performed in both directions. WalterReed strain, male, albino rats weighing350 to 550 Gm. were used. The animalswere maintained in separate cages on astock diet of rat biscuits** and tap waterad libitum for at least a month prior toand during each experiment. For each ex-periment the groups were matched forage and body weight. The principles oflaboratory animal care as promulgated bythe National Society for Medical Researchwere observed.

Experiment 1. Tensile Strength of NormalSkin. Watts 28 has shown that on the dorsal sur-face of the guinea pig the lines of skin tensionare oriented transversely, that is, perpendicularto the long axis of the animal. In the live rat it

** G. L. Baking Co., Frederick, Maryland.

elm I

is also grossly apparent that with normal postur-ing the dorsal wrinkle lines are directed trans-versely. To determine the relationship of suchwrinkle lines to the tensile strength of normal skin,20 rats were randomly assigned to two equalgroups. Animals from both groups were alter-nately sacrificed with overdose of intraperitonealpentobarbital, the dorsum of each clipped andshaven, and skin to be used excised as follows(Fig. 1): In each rat, a point in the dorsal mid-line 5 cm. caudal to the occiput was marked witha blue water-color pencil. A 5 cm. square of skinwith the original dot in the center was thenexcised from each animal by sharp dissection inthe subdermal plane.

Each square was placed in the desired orien-tation on the base-plate of a specially constructedskin cutter L8 and adjusted to its in situ dimen-sions. In one group the blocks were oriented sothat the long axis of the cut dumbbell wouldparallel the longitudinal axis of the animal, thatis, perpendicular to the wrinkle lines; this groupwill henceforth be referred to as longitudinal.In the other group, the block was oriented sothat the longitudinal axis of the cut dumbbellwould be perpendicular to the longitudinal axisof the animal, that is, parallel to the wrinldelines; this group will henceforth be referred toas transverse. The upper plate of the cutter, con-taining sharp cutting blades which fit into the

EXERIMENTS 2 AMQ3

FIG. 1. Tensile-strengthtesting of normal and in-cised skin.

TENSILE STRENGtH / tRNfERSWNORMAL SKIN W(PARALLEL TO

PERPENDICULAR W L

LONTUOINALNRMA

S tU II

'LONGITUDINA TENSILE STRENGTH(PERPENDICULAR TO LONGITUDINAL INCISION

WRINKLE LINES) (PERPENaCULAR TOWRIE LNS)

Volume 159Number 2 261

TENILE STRENGTHTRANSVERSE INCISION

TENSILE STRENGTHNORMAL SKINPARALLEL'TRA W*OS

BERARD, WOODWARD, HERRMANN AND PULASKI Annals of SurgeryFebruary 1964

TABLE 1. Tensile Strength of Normal Skin

Mean 4 S. E.

TensileBody Weight Thickness Strength

Orientation No. (Gm.) (mm.) (Gm./mm.2)

Longitudinal (perpen- 10 337 + 8 1.26 ±t 0.06 777 i 61dicular to wrinklelines)

Transverse (parallel 10 353 i 14 1.24 4 0.07 994 i 80to wrinkle lines)

P Value No difference No difference <0.05

grooves on the lower plate, was then broughtdown sharply and a dumbbell of skin cut. Eachdumbbell, containing the original blue dot at itscentral pole, was 6 mm. wide at its narrowestcentral portion, 2 cm. wide at each end, and 5cm. in length.

The cut dumbbell was next placed on a stain-less steel guide bar, adjusted to its in vivo di-mensions, and its thickness at the central sixmillimeter wide portion measured five times witha special micrometer* to the nearest ten-thou-sandth of an inch.'8 The average of these readingswas converted to millimeters and expressed asskin thickness. The product of skin thicknesstimes width of strip at its narrowest 6 mm. di-mension was calculated as cross-sectional area ofthe skin in square millimeters at its narrowestportion.

The strip was finally fixed between the jawsof a specially constructed breaking strength de-vice18 so that the 2 cm. ends of the dumbbellwere held by the jaws and the 6 mm. centralportion was equidistant between the jaws. Thelower jaw was connected via a metal arm to amotor geared to pull the jaw at 0.2 inch/min.while the upper jaw was connected via a freely-rotatable bead-chain (to prevent torsion effects)to a strain gauge.** As traction was exerted onthe skin strip, the force measured by the straingauge was recorded on a zero-to-ten millivoltstrip-chart recorder* * * calibrated in grams andthe peak value, recorded just before the stripdisrupted at its narrow 6 mm. waist, taken as thebreaking force. The breaking force, divided by thecross-sectional area at the waist, yielded tensilestrength in Gm./mm2.

Experiment 2. Tensile Strength and Morphol-ogy of Skin Incisions. For this experiment 24rats were randomly assigned to two equal groups.Under ether anesthesia and aseptic technic, eachrat, after clipping and shaving, received a 5 cm.dorsal skin incision (through only the epidermisand dermis) centered at a point 5 cm. caudal tothe occiput. In one group, designated as longi-tudinal, the incision followed the midline dorsalaxis of the animal and therefore was perpendicularto the wrinkle lines. In the other group, desig-nated as transverse, the incision was perpendicu-lar to the axis of the animal and parallel to thewrinkle lines. Each incision was closed withouttension using five evenly-spaced interruptedthrough-and-through sutures of No. 35 stainlesssteel wire. Wounds were not manipulated furtherexcept for removal of sutures at six days.

On the fourteenth postoperative day, each ani-mal was sacrificed with overdose of intraperitonealpentobarbital and the dorsum clipped and shaven.The length of the incision in situ was measured.Utilizing the same methods as in Experiment 1,a 5 cm. square of skin (bisected either longitudi-nally or transversely by the partially healed in-cision) was excised (Fig. 1). Each square wasoriented and adjusted to its in situ dimensions onthe base-plate of a skin cutter18 designed to cutthe central portion of the incision into five paral-lel strips each 6 mm. wide. The incision was ori-ented perpendicular to the blades so that thehealing wound bisected the center of each strip.This cutter is suitable for preparing strips of ahealing incision but must be replaced by thedumbbell cutter when testing normal skin to as-sure breaks at the strip-center rather than at thejaws. The middle strip was used for histologicstudy and the adjacent strips tested for thicknessand breaking strength as described in experiment1. Again the thickness in millimeters multiplied by6 mm. width yielded cross-sectional area at the

262

* B. C. Ames, Waltham, Mass.** Statham Instrument Co., Puerto Rico.*** Leeds and Northrup Co., Philadelphia,

Penna.

HEALING OF INCISIONAL WOUNDS IN RATS

incision in square millimeters, and the quotient ofbreaking strength divided by cross-sectional area

gave tensile strength in Gm./mm2.Experiment 3. This experiment was identical

to Experiment 2 except that animals were sacri-ficed on the twenty-first postoperative day.

Histologic Methods. Following neutralformalin fixation the middle 6 mm. stripfrom each incision was embedded in paraf-fin and sectioned at seven micra perpen-

dicular to both the skin surface and theline of incision. Representative specimenswere additionally sectioned either parallelto the epithelial surface at the mid-dermallevel, or perpendicular to the skin surface,but parallel to and through or immediatelyadjacent to the incision. It was technicallydifficult to orient specimens so as to obtainsections truly parallel to the incision. Hema-toxylin-eosin, Wilder's reticulum 30 andGomori's one-step trichrome stains (thelatter employing aniline-blue)10 were pre-

pared on sequential sections from eachspecimen.

Results

The results of Experiment 1 (Table 1)indicate that there is a moderate but sig-nificant difference in the tensile strengthof normal skin when tested perpendicularand parallel to the wrinkle lines. The ten-sile strength of soft tissue principally de-pends on the collagen fibers present.',12

The greater tensile strength of strips testedparallel to wrinkle lines would thus beconsistent with the histologic findings ofCox5 and of Shaw and Copenhaver,23 24

that connective tissue fibers tend to paral-lel skin lines. Additional supporting evi-dence, at approximately 1,000 times greatermagnification, is supplied by the x-ray dif-fractogram studies of Holmstrand et al.'sThey showed that although there are twosystems of collagen fibrils in the dermis,one parallel and the other perpendicularto the crease lines, "the strongest orienta-tion effect is derived from collagen fibrilsparallel to the crease lines, suggesting thatcollagen is oriented principally in the same

direction as the crease lines."The results of our Experiments 2 and 3

reveal several novel findings about dorsalskin incisions oriented perpendicular andparallel to wrinkle lines. It was apparentat surgery that incisions perpendicular tothe wrinkle lines gaped more widely, butit was possible to approximate skin edgeseasily in both groups, and none of thewounds appeared to be under marked ten-sion. No wounds disrupted in the post-operative period and at sacrifice the inci-sions were all grossly apparent as finewhitish lines, without hyperemia, elevation,or cross-hatching attributable to suture re-

tention. Assessment of the physical char-

TABLE 2. 14-Day Postoperative Dorsal Skin Incision

Mean 4± S.E.

Body Thickness Breaking TensileWeight at Incision Strength Strength

Orientation No. (Gm.) (mm.) (Gm.) (Gm./mm.2)

Longitudinal (perpen- 10* 538 4 8 1.33 0.03 625 i 44 80 i 7dicular to wrinklelines)

Transverse (parallel 12 535 4± 6 1.47 ± 0.05 329 ±t 17 38 4 2to wrinkle lines)

P Value No difference <0.05 <0.001 <0.001

* 2 animals excluded due to technical difficulty.

Volume 159Number 2 263

BERARD, WOODWARD, HERRMANN AND PULASKI Annals of SurgeryFebruary 1964

TABLE 3. 21-Day Postoperative Dorsal Skin Incisions

Mean + S.E.

Body Thickness Breaking TensileWeight at Incision Strength Strength

Orientation No. (Gm.) (mm.) (Gm.) (Gm./mm.2)

Longitudinal (perpen- 10 331 4i 3 1.37 i 0.05 1291 i 85 160 4- 14dicular to wrinklelines)

Transverse (parallel 10 332 i 4 1.69 i 0.05 872 i 41 88 4t 9to wrinkle lines)

P Value No difference <0.001 <0.001 <0.001

acteristics of the wounds revealed some

striking differences between the two groups

in Experiment 2 (Table 2) and these dif-ferences were confirmed and extended inExperiment 3 (Table 3).

It was noted at sacrifice that in neithertype of incision was there a measurableshortening from the original 5 cm. length.This is in contrast to the statement ofWatts 28 that incisions across Langer's linescontracted by about 10 per cent of theirlength while wounds parallel to Langer'slines did not contract at all. The reason

for this difference between Watts's andour findings is uncertain, but it may be

noted that Watts used flank while we useddorsal incisions and that his time of meas-

urement, although not stated, may havebeen different from ours. Our findings are

in harmony, however, with the observationof Majno and Hertig 20 that "some scars

contract, some expand-and there is a thirdgroup in between, probably the largest,consisting of those scars which just stay as

they are."Contrary to common conception is the

evidence that healing incisions parallel towrinkle lines are moderately (but signifi-cantly) thicker at 14 days (Table 2) andstrikingly so at 21 days (Table 3). Al-

FIG. 2. Margin of

healingi of 14-day longi-tudina incision revealingsmooth transition be-

tween re-existing colla-

Y lgen (leFt) and area of re-

pair (right). Tn-chrome

~ zstain, X 309.

264

HEALING OF INCISIONAL WOUNDS IN RATS 265

though an incision perpendicular to skinlines may eventually be more susceptibleto hypertrophy or even keloid formation,this tendency is not apparent at the pe-

riods examined. The findings are in factquite opposite.

Equally striking is the discovery that atboth 14 and 21 days incisions perpendicu-lar to skin lines are markedly stronger thanparallel ones. The differences in crudebreaking strength are even greater whenexpressed as tensile strength, due to thegreater thickness and, hence, increasedcross-sectional area of the weaker parallelincisions. Although parallel-oriented inci-sions may lead to better healing in termsof final cosmetic and functional result,maximal rate of accretion in strength cannotbe included in their advantages.The period during which maximal gain

in tensile strength occurs is now knownto be longer than has been supposed.6 18For the type of longitudinal incision re-

ported here in the rat, wound strength ap-proaches that of normal skin at 80 to 100days."' 19 At the end of the two- or three-week period, the gain in tensile strengthof skin has been reported as 10 to 20 percent of the total ultimate gain.6 This is con-

FIG. 3. Same specimen as

Figure 2, X 1108.

firmed by our data on longitudinal inci-sions in which tensile strengths at 14 and21 days are 8.0 and 16.1 per cent, respec-tively, of normal skin strength tested paral-lel to wrinkle lines. At the same periods,however, transverse incisions reach only 4.9and 11.3 per cent of normal skin strengthperpendicular to wrinkle lines. Whether in-cisions parallel to wrinkle lines continueto be weaker or simply gain strength at aslower rate cannot be concluded from thisstudy.

Histologic Findings. Evidence of repairin 14- and 21-day specimens is seen pri-marily in the dermis. The epithelium overthe incision is intact, and is either mini-mally acanthotic or indistinguishable fromthe surrounding epithelium. Inflammatorycells are scant within the wound and newcapillary formation near the incision site isnot striking.Moderate variation is seen among the

21-day specimens; however, there is a gen-eral pattern. Directly under the epithelium,in both transverse and longitudinal inci-sions, is located a wide area of fibrosis inwhich newly-formed, fine fibers are lo-cated parallel to the epithelium and per-pendicular to the direction of, and bridg-

Volume 159Number 2

B3ERARD, WOODWARD, HERRMANN AND PULASKI Annals of SurgeryFebruary 1964

FIG. 4. Margin of 14-day transverse incisionrevealing whorl-like junc-tional-structure, X 1108.

ing, the incision. Deeper in the dermis a

more vertical fiber-pattern occurs, althoughrandomly-oriented fibers are plentiful. Inthe deepest areas of the incision bifurca-tion of the fibrous tract is sometimes seen.

At the mid-dermal level, skin-appendagesboth partially demarcate the area of repairand are surrounded by reparative collagen.Skin appendages within and adjacent tothe incision are seen with about equal fre-quency in transverse and longitudinal spec-

imens. Scar width, somewhat variable, ap-

pears unrelated to incisional orientation.Muscle giant cells and fibrous binding be-tween panniculus carnosus and wound are

variable.The most striking morphologic difference

between transverse and longitudinal inci-sions is found at the junction of newly-forming connective tissue and pre-existingdermal collagen. The longitudinal incisionmanifests an imperceptible transition be-

~~FIG. 5. Margin of 21-

day transverse incision

containing junctional

structure, X 1152.

266

HEALING OF INCISIONAL WOUNDS IN RATS

tween the new fibrillar collagen bundlesand the surrounding large dermal fibers,which are often oriented parallel to theplane of section (Fig. 2, 3). This smoothinterdigitation is seen at all dermal levels.Contrasting sharply is the junctional area

of the transverse incision. Here, large col-lagen bundles, seen on end, are surrounded

in claw-like fashion by circumferential fi-brils (Fig. 4, 5). This whorl-like structure,albeit sometimes incomplete, demarcatesreparative processes at all dermal levels(Fig. 6), and although the pattern some-

times is seen in longitudinal incisions, itis the most common junctional pattern inthe transverse incision. Figures 2 to 6, rep-

FIG. 6. Fourteen-day transverse incision showing multiple whorl-like junctional areasdemarcating wound, X 79.

Volume 159Number 2 267

268 BERARD, WOODWARD, HERRMANN AND PULASKI

resenting trichrome stains, reveal changeswhich also are identified in both reticulumand H & E stained sections. Sections paral-lel to the incision did not reveal these dif-ferences in margins.

Fourteen-day specimens vary little fromthe previous description except that newcollagen appears more fibrillar, and junc-tional patterns are less pronounced.

DiscussionThe results here reported confirm and

extend the observations of others thatmammalian skin is not a homogeneous con-tinuum of scattered cells and random fi-bers, but has a somewhat orderly patternwith anatomic and functional implications.Tensile strength of normal skin is shownby this study to vary with orientation.Reports of tensile strength or breakingstrength of intact or wounded skin shouldinclude this important consideration. Cross-sectional area of the tissue tested is an-other important variable.'2 18 Publishedreports of breaking strength, failing to in-clude this parameter, are erroneously la-belled as "tensile strength."

It has been suggested8' 25, 29 that tensionon collagen fibers determines their direc-tion and abundance, and from this onemight conclude that longitudinal inci-sions, perpendicular to wrinkle lines, gainstrength more rapidly because of theirgreater susceptibility to natural skin ten-sion. It has already been stated that al-though such wounds gape more widely atsurgery, suture approximation is not diffi-cult, and no gross evidence of tension isapparent. More meaningful to this consid-eration is the work of Borgstrom andSandblom 3 in which paired dorsal skinincisions were performed on white rabbits.One incision was sutured without interfer-ence while the contralateral one was placedunder tension by a specially constructedbrace. The wounds with tissue tensionwere significantly weaker than those with-

Annals of SurgeryFebruary 1964

out such tension. Supportive is the x-raydiffraction work of Holmstrand et al.13 onmature and hypertrophic scars. Althoughthe majority of collagen fibers were ori-ented in the longitudinal direction of thescar, "the data obtained did not indicatea clear-cut correlation between the orien-tation of the fibrils and the direction ofmechanical forces acting on the scars."Thus, although evidence exists 28 that "ten-sions orient fibers and fibers orient cells,"the effect of tension on incisional woundsin skin is uncertain and cannot at presentbe invoked to explain the results of thisinvestigation.The histologic observations conform with

the earlier reports 5' 23, 24 that connectivetissue fibers are oriented with regard toskin lines, and suggest that fiber-orientationinfluences the character of healing inincisional wounds. The demarcation ofincisions parallel to wrinkle lines by claw-like junctions may explain the observa-tion 15' 18 that such incisions result in mini-mal scarring and are less likely to widenor contract. Longitudinal incisions, on theother hand, demonstrate multiple smoothinterdigitations with the adjacent dermalpattern. These communications may havea role in the greater tensile strength of suchwounds. It is also conceivable that thisconfiguration may be more susceptible towidening, contracture, and over-all poorcosmetic and functional result.These findings emphasize the expression

of Weiss28 that "not only must we learnto gauge macroscopic situations on themicroscopic scale of behavior, but cell be-havior must be projected downward to theultramicroscopic, macromolecular realm."He noted that the fibrous membrane ofamphibian skin is laminated and with elec-tron microscopic examination reveals anamazing regularity of collagen fibrils instrictly parallel array, but oriented at rightangles from each to the next of about 20layers. Proceeding from layer to layer, one

Volume 150 HEALING OF INCISIONAL WOUNDS IN RATS 269Number 226sees the fibers alternately in profile and incross-section. Evidence from the light mi-croscope at 50 to 400 times magnificationand from x-ray diffractograms at about400,000 times magnification suggests a pat-tern in mammalian skin similar in natureif not in detail and degree. The implica-tions of this consideration are yet to beexplored. Intriguing are statements such as"Scars that run across the lines of the skinare more readily affected than those par-allel to these lines and this probably ex-plains the keloid developing in one limbof an L-shaped incision,"' or "A nice re-finement with full-thickness skin transplan-tation is an attempt to place the skin inits new position in a similar manner withrespect to the lines it occupied in its donorsite." 1

SummaryThe relationship of wrinkle lines to the

tensile strength and morphology of normaland healing skin has been examined in therat.

In a series of three experiments, tensilestrength was related to orientation in bothnormal skin and in healing incisionalwounds at 14 and 21 days.The tensile strength of normal rat skin

is significantly greater parallel to wrinklelines than at right angles to such lines.The healing dorsal skin incision varies

physically and morphologically dependingupon its orientation. At both 14 and 21days, incisions parallel to wrinkle lines aresignificantly thicker and weaker than in-cisions oriented perpendicularly. Histologicexamination supplemented the studies onwound healing. The principal morphologicdifference between the two types of inci-sion is found at the junction of newly-forming connective tissue and pre-existingdermal collagen.Under the conditions of this study, the

incision parallel to wrinkle lines has noadvantage in thickness or strength in com-parison to a perpendicular incision.

AcknowledgmentsThe technical assistance of Messrs. John Diggs,

Ernest Sloan and Lee Lewis and PFC. CliffordRea, Wilbur Pumpaly, and George Nokes is grate-fully acknowledged. The chart and photomicro-graphs were prepared by the Medical Audio VisualDepartment, Walter Reed Army Institute of Re-search, Walter Reed Army Medical Center.

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nic and Wound Healing. Ann. Surg., 144:982, 1956.

4. Christopher, F.: A Textbook of Surgery. Phil-adelphia, Saunders, 1947.

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