Veterinary Surgery, 12, 3, 113-118, 1983

Biomechanics of Cranial Cruciate Ligament Reconstruction in the Dog

II. Mechanical Properties

DAVID L. BUTLER, PhD, DONALD A. HULSE, DipACVS, DVM, MATTHEW D. KAY, EDWARD S. GROOD, PhD, PETER K. SHIRES, DVM, ROBERT D’AMBROSIA, MD,

and HIROMU SHOJI. MD

A biomechanical analysis of the results of an over-the-top procedure for replacement of the cranial cruciate ligament (CCL) in the dog is presented. Using 15 adult mongrel dogs, the CCL in one stifle joint was reconstructed using fascia lata and the lateral one-third of the patellar ligament. The opposite CCL served as the control. Animals were sacrificed at 0, 4, 12 and 26 weeks postoperation and axial failure tests were performed. Stiffness, maximum load, and elastic modulus of the replacement increased over time, while elon- gation to maximum load continually decreased as compared to controls. Other parame- ters showed less consistent trends.

The results are encouraging given the reduction in joint laxity and the increases in tissue stiffness and strength. However, the ligament substitute was still unable to repli- cate the mechanical properties of the normal cruciate ligament. Longer studies therefore are required to determine if this replacement is capable of completely restoring joint stability and normal function.

N THE PAST, SURGICAL CONSIDERATIONS have gen- I erally governed the choice of a ligament replace- ment. However, other factors are also important, in- cluding the initial mechanical properties of a graft, how and where it is fixed to bone, the amount of axial ten- sion applied at surgery, and the morbidity associated with the procedure.

We have previously identified the concepts of an “ideal” biological and have determined the mechanical properties of eight commonly used human anterior cruciate ligament replacements at the time of surgery.**2 To our knowledge, however, no one has examined the changes in mechanical properties of a ligament graft over time. The objective of this work was to determine the structural and material properties of one canine cranial cruciate ligament replacement for up to 26 weeks following surgery. The results of eight of the most important mechanical parameters are presented.

Materials and Methods

Surgery was performed on 15 adult mongrel dogs. In one knee, the cranial cruciate ligament (CCL) was re- placed with a graft composed of fascia lata and the lateral one-third of the patellar tendon. The CCL in the opposite knee served as the control. Details of the sur- gical reconstructive procedure, postoperative exercise regimen, and in vitro stifle joint laxity measurement results can be found in two separate paper^.^,^

The limbs were dissected to isolate the CCL. On the operated side, particular attention was paid during dis- section to preserving any areas where scar tissue and adhesions (that could have been load-bearing) were attached to the graft. Each completely dissected specimen consisted of the femur, the CCL or its re- placement, and the tibia.

Prior to testing, the cross-sectional area and length of each tissue were determined. The cross-sectional

From the Department of Orthopaedic Surgery, College of Medicine, University of Cincinnati, Cincinnati, Ohio (Butler, Kay, Grood) and the Department of Veterinary Clinical Sciences, School of Veterinary Medicine (Hulse, Shires) and the Department of Orthopaedic Surgery, College of Medicine (D’ Ambrosia, Shoji), Louisiana State University, Baton Rouge, Louisiana.

This work was partially supported by NIH Grants AM27517 and AM00%5 and by LSU Grant SVM179. Reprint requests: David L. Butler, PhD, Department of Orthopaedic Surgery, College of Medicine, University of Cincinnati, Cincinnati,

OH 45267.

0161-3499/83/0700/0113/$01.10 @ American College of Veterinary Surgeons

113

114 CRUCIATE LIGAMENT RECONSTRUCTION: PART I I

area was measured using an instrumented area mi- crometer (Fig. l).",' Each specimen was first inserted into a rectangular slot (2.6, 5.0, or 8.1 millimeters wide). A matching plunger then was inserted gently into the slot and rested on the tissue. Next, a cali- brated weight was placed on the pan above the plunger to produce a constant load during the area measure- ment. The pan weights were selected so that the tissue would be subjected to a constant compressive stress averaging 0.12 Megapascals. The height of the plunger was determined from the electrical output of a linear variable differential transformer positioned under the pan (Fig. 1). The area was computed by taking the height of the plunger after a period of 10 minutes and multiplying it by the slot width. This time was selected because the amount of viscoelastic creep that occurred subsequently was small. The length of each specimen was determined by averaging four readings taken with vernier calipers. Lengths were obtained on the cranial, caudal, medial, and lateral aspects of the tissue. Each length measurement was made parallel to the long axis of the ligament or graft and from insertion site to inser- tion site. A helical twist of the fiber bundles in the control ligament was noted.

The bone ends of each specimen were secured in aluminum tubes filled with methylmethacrylate and mounted in aluminum grips fabricated to maintain a flexion angle of 45". The tibia was placed in the lower grip and oriented 90 that its long axis was perpendicu- lar to the direction of loading to simulate a straight cranial drawer test. The femur was mounted in a nor- mal anatomical position relative to the tibia. A condy- lar support bracket (Fig. 2) was attached to the upper

grip to block the end of the femur, minimizing bending deformations and axial slippage.

Each bone-ligament-bone unit was tested to failure in cranial drawer in an Instron 1321 electro-hydraulic materials testing machine. All failure tests were per- formed at a fixed displacement rate of 100% of the specimen length per second. Structural parameters that were examined included stiffness in the linear loading region, maximum load, energy to maximum load, and elongation to maximum load. Corresponding material parameters (modulus, maximum stress and energy densities, and strains to maximum load) then were computed. Modulus was calculated as the prod- uct of stiffness times the ratio of initial length to cross-sectional area, maximum stress as the ratio of maximum force to initial area, energy density to maximum as the area under the stress-strain curve to maximum load, and strain to maximum as the elonga- tion to maximum load divided by initial length. A clip gauge was attached near the tissue insertions and

Fig. 1 . Area micrometer for cross-sectional area meas- Fig. 2. Specimen grips used for securing the femur and tibia in the lnstron testing machine. Note the support bracket on the upper, femoral grip.

urements. The micrometer is connected to a linear variable dif- ferential transformer and strip chart recorder.

BUTLER, HULSE, KAY, GROOD, SHIRES, D’AMBROSIA, AND SHOJI 115

TABLE 1. Dimensions of Cranial Cruciate Ligaments and Grafts in Dogs

Postoperation Number of Length Area Volume (weeks) Animals Procedure (mm) (mm2) (cc)

0 4 Control

4 4 Control

12 4 Control

26 3 Control

Operated

Operated

Operated

Operated

Total of Controls 15

15.8 i 1.4* 35.8 f 1.6 18.6 2 1.2 37.0 f 3.6 17.5 i 0.8 34.1 -t 2.7 19.8 f 1.4 34.5 t 1.5

17.8 2 0.7

8.7 t 1.0 11.2 i 0.5 11.3 t 1.5 20.2 f 6.4 13.0 t 1.5 31.8 ? 6.2 13.6 t 0.4 33.2 t 4.3

11.5 i 0.7

0.14 f 0.03 0.40 t 0.03 0.21 2 0.05 0.79 t 0.27 0.23 2 0.04 1.1 3 f 0.28 0.27 2 0.01 1.13 t 0.12

0.21 2 0.02

Mean t one standard error of the mean

oriented along the axis of the ligament to approxi- mately measure the ligament end-to-end strain (change in lengthhnitial length) and elongation. A Modcomp I1 computer was used to drive the testing machine, as well as to store and calculate the load, actuator mo- tion, and local elongation data.

The mean values of each biomechanical parameter were averaged for all animals at a specified time pe- riod. These results then were compared between groups. For each animal, each biomechanical parame- ter on the operated side was then expressed as a per- centage of the opposite control side. These mean val- ues (plus or minus one standard error of the mean) were plotted against time following surgery, thereby displaying general trends or changes in the mechanical properties during the recovery period.

Results

Tissue Dimrnsions

Average tissue dimensions for the control and re- placement CCLs are shown in Table 1. The normal CCLs from all four time periods averaged 17.8 5 0.7 mm (X k SEM) in length; the replacement grafts were much longer, ranging from 230% of control length im- mediately following surgery to 180% of control length at 26 weeks.

Cross-sectional area results are shown in Figure 3 and Table 1 . Immediately following surgery, the area of the graft was 135% ? 21% of the control area, increasing to 255% k 53% at 12 weeks, and then declining to 234% f 48% at 26 weeks.

Stiffness und Modulus

Stiffness and corresponding modulus are shown in Tables 2 and 3 and Figure 4. Immediately following

surgery, stiffness of the graft was only 9% t 3% of the control side. Stiffness increased with time reaching 31% 2 3% at 26 weeks. The graft had a modulus of 14% 5 2% of the control value immediately following surgery, increasing to 28% k 4% by 12 weeks.

Maximum Force & Stress

Maximum force and maximum stress are shown in Tables 2 and 3 and Figure 5. Immediately following surgery, maximum graft force was 14% t 4% of the control value, and increased to 28% t 4% at 26 weeks. The maximum stress of the grafts immediately follow- ing surgery was 10% ? 2% of the control value, de- creasing slightly at both 4 and 12 weeks, and then in- creasing to 13% t 4% at 26 weeks.

3501

0 ’ ;I* 4 f a 12+ 16 20 24 ** WEEKS POST-OP

Fig. 3. Cross-sectional areas (mean values t SEM) of the canine cranial cruciate ligament grafts compared to the con- tralateral control ligament.

116 CRUCIATE LIGAMENT RECONSTRUCTION: PART II

TABLE 2. Structural Mechanical Properties of Cranial Cruciate Ligaments and Grafts in Dogs

Structural Properties

Maximum Elongation Energy to Postoperation Number of Stiffness Force to Maximum Maximum

(weeks) Animals Procedure (KN/M)* (N)' (mm)* (N-M)'

0 4 c t 259.6 2 16.2$ 1264 k 132 6.1 t 0.4 3.4 t 0.7 0 22.2 i 5.2 169 t 32 11.6 t 1.6 0.9 F 0.1

4.8 F 1.1 4 4 C 360.8 t 39.3 1777 t 295 6.4 t 0.6 0 56.8 i 18.7 309 f 109 8.7 t 2.1 1.1 2 0.4

12 4 C 417.2 t 78.4 1600 '-t 230 5.9 t 1.4 3.7 t 1.1 0 9 1 . 9 ~ 14.1 454 i 83 7.3 i 1.3 1.5 2 0.5

26 3 C 356.8 t 30.3 2091 2 149 7.4 t 0.2 5.7 k 0.7 0 109.8 2 15.4 584 t 108 8.0 t 0.9 1.9 t 0.5

Total of Controls 15 348.1 t 26.9 1656 t 125 6.4 t 0.4 4.3 i 0.5

' KN/M-kilonewtons per meter, N-newtons, rnm-millimeters. NM-newton-meters. t C-control; 0-operated. t Mean 2 one standard error of the mean.

Elongtrtion trnd Strcrin to Mruimum Loud

The elongation and strain in the tissue are shown in Tables 2 and 3 and Figure 6. Elongation of the graft compared to its control was 188% * 16% immediately following surgery, declining to 107% r 9% at 26 weeks. Corresponding maximum strains averaged 83% r 8% of the control values immediately following surgery, decreasing to 60% f 1% at 26 weeks.

Energies to Muximum Locrd

Energy and energy density to maximum load are shown in Tables 2 and 3 and Figure 7. Energy values

for the grafts were 29% * 6% of control values imme- diately following surgery and 34% 2 8% at 26 weeks. Energy density ranged from 10% k 2% of control val- ues immediately following surgery to 6% e I% at 12 weeks.

Mechanisms of Fuilure

All eight of the ligament substitutes failed by pulling out from underneath the femoral washer in the zero and 4 week specimens. At 12 weeks one of the substi- tutes slipped from beneath the washer, two exhibited interstitial failure, and one failed by tibia1 bone frac-

TABLE 3. Material Properties of Cranial Cruciate Ligaments and Grafts in Dogs

Material Properties

Energy Maximum Strain Density

Postoperation Modulus Stress to Maximum to Maximum (weeks) Procedure (MPa)' (MPa)' (W (N-M/CC)'

0 c t 478.6 2 20.2$ 148.2 t 14.1 39.8 -+ 5.1 25.6 t 4.5 0 68.4 2 11.6 15.0 2 2.5 32.0 t 3.3 2.2 t 0.3

4 C 623.3 t 115.5 159.1 F 25.7 34.5 t 2.6 22.9 t 5.6 0 107.1 c 13.5 14.0 2 3.6 22.8 t 4.8 1.3 0.4

18.0 t 6.4 12 C 557.6 T 71.5 127.7 t 20.7 33.9 F 8.3 2.6 2 0.6 0 112.8 t 30.4 16.2 2 4.6 21.0 t 2.8

26 C 513.7 t 7.9 153.3 t 6.5 38.0 t 3.0 21.3 t 2.3 2.0 t 0.6 0 137.8 t 40.8 20.7 t 6.2 22.7 & 1.5

Total of Controls 15 543.8 t 36.2 146.7 2 9.2 36.4 t 2.5 22.0 ? 2.5

" MPa = megapascals, N-M/CC = newton-meters per cubic centimeter. t C = control; 0 = operated. * Mean t one standard error of the mean.

BUTLER, HULSE, KAY, GROOD, SHIRES, D'AMBROSIA, AND SHOJI 117

200'

150.

A 0 LL i- L

9 g 100

L i Y V z Y n

50.

40 '1 'n=4

*'n=3

4 107.4

6 60.0

54.1

30.6

5 0 ~

40.

.1

.A 0

c 30.

LL 0

+ z Y

2 20. W a

A STIFFNESS m 1 27.1

Y 9.0

+n=4 "n=3

" 7- 1 . . O+ 4* i 12' 16 20 24 **

WEEKS POST-OP

Fig. 4. Stiffness and modulus (mean values ? SEM) of the canine cranial cruciate ligament grafts compared to the con- tralateral control ligament.

ture. At 26 weeks, all three substitutes failed due to interstitial tears.

Reasons for failure of the control ligaments were tibial fracture (6 specimens), tibial avulsion ( 5 speci- mens), and interstitial tear (4 specimens).

Discussion

The cranial cruciate ligament-bone unit and its graft replacement were examined in this study because of the frequency of CCL injuries seen clinically. Each structure was tested at a high strain rate for two rea- sons: first to simulate the rates exhibited during in vivo injuries, and second, to test the ligament (graft) and the bone as a functional composite unit, since bone has

I A MAXIMUM FORCE 1 0 MAXIMUM STRESS

*n=4 27.6 *ql=3

0' 4 * 8 12* 16 20 24 ** 01 f

WEEKS POST-OP

Fig. 5. Maximum force and maximum stress of the canine cranial cruciate ligament grafts compared to the contralateral control ligament.

been shown to be more rate sensitive.8 A clip gauge was attached near the tissue insertions to avoid measuring the additional bending deformation of the tibia that would be sensed by measurement of cross- head motion.

Before examining the results in detail, our method of analysis should be mentioned briefly. We chose to compare across time periods by expressing each pa- rameter as a percentage of the operated to control side. This approach minimized the effects of specimen var- iability due to differences in age, sex, and weight of the animal. While the standard error in such ratios reflects the variance in both the operated and control values, it still represented, in our view, the best way to compare time periods.

T ENERGY @ MAX FORCE 3c9

P MAX STRESS 0 ENERGY DENSITY L . 0 jn

I I 1 I I *".4

5.6 5 . 6

0' 4' 8 12* 16 20 24 ** WEEKS POST-OP

0 1 .

Fig. 7. Energy and energy density developed by the canine cranial cruciate ligament grafts compared to the contralateral control ligament.

118 CRUCIATE LIGAMENT RECONSTRUCTION: PART II

One indication of how a graft performs in vivo is its stiffness, which is the slope of the force-elongation curve in its linear region.H Stiffness can be thought of as a resistance to loading and is dependent on tissue dimensions (length, area) and a material property called modulus. Given two grafts having the same cross-sectional area and composition, the longer one has a lower stiffness. Similarly, given two replace- ments of the same length and material, the one with a larger area develops the greater stiffness. Modulus in- dicates how the stiffness of the graft tissue is changing irrespective of how large or small it may be. Immedi- ately following surgery, the stiffness and modulus of the graft are extremely low but increase progressively. The increased stiffness at 4 weeks reflects both the increase in material behavior (modulus) and in cross- sectional area due to the formation of attachments (adhesions) between the graft and surrounding struc- tures. The increase in modulus at 12 weeks occurred despite an increase in tissue cross-sectional area. This indicates that the increased size of the substitute prob- ably was composed of weaker, nonload-bearing tis- sues, such as blood vessels and unorganized collagen. At 26 weeks, the stiffness increased but the cross- sectional area (as determined from left-right compari- sons in Fig. 3) declined slightly, resulting in little or no change in modulus, possibly signifying a decrease in nonload-bearing tissues and the first significant phases of collagen remodeling.

The low value of maximum force immediately fol- lowing surgery (14% -c 4% of the control) indicates the difficulty in restraining the ligament at the bony inser- tion with a spiked washer and screw. This weak inter- face also may be true of other fixation methods. The slight increase in maximum force at 4 weeks may be due to formation of collagenous adhesions at the ligament-bone interface. However, all the grafts still failed by slippage beneath the washer, indicating the adhesions were not yet a major factor. Subsequent in- creases in graft maximum force may also be a reflec- tion of the early remodeling process. Interstitial tears were seen only in the 12 and 26 week groups. Although the maximum force at 26 weeks is only 28% of the control value, this does not necessarily indicate im- pending mechanical failure of the grafted tissue under in viva loads. It has been calculated that biological tis- sues are subjected to forces ranging from one-tenth to not more than one-fourth of their breaking loads under normal It has been shown that the me- dial collateral ligament of dogs carries a minimal load when walking and trotting as well as after falling from a 30 cm height.I2 The low mechanical forces placed on the tissues, and secondary joint restraints that develop following surgery may account for the lack of mechan- ical failures seen from the grafts during in vivo labora-

tory tests and the clinical success reported in the dog 4 , 1 R The absence of graft failures in vivo in this study supports this suggestion. The increasing strength of the graft shown in this study may indicate that it is slowly assuming more of the role as a primary restraint against cranial drawer. This was also the case when patellar tendon grafts were used for anterior cruciate ligament reconstruction in monkeys.I4 Graft strength reached 52% of the control CCL 12 months postoperatively.

The slight increase in maximum stress that was seen (from 10% at zero weeks to 13% at 26 weeks) substan- tiates the fact that the graft tissue is not like the normal CCL and that the remodeling process is slow. Only longer studies can reveal if the grafted tissue ever achieves the material properties of the normal cranial cruciate ligament.

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