Biomechanical properties of the triceps surae muscle after limb lengthening

Biomechanical properties of the triceps surae muscle after limb lengthening

Clinical Biomechanics Vol. 10. No. 5, pp. 263-267, 1995 Copyright0 1995Elsevier ScienceLimited Printed in Great Britain. All rights reserved 0268~003...

561KB Sizes 2 Downloads 39 Views

Clinical Biomechanics Vol. 10. No. 5, pp. 263-267, 1995

Copyright0 1995Elsevier ScienceLimited Printed in Great Britain. All rights reserved 0268~0033195 $10.00+ 0.00

Biomechanical properties of the triceps surae muscle after limb lengthening J-S Sun MD’, S-M Hou C-K Cheng Pm3

MD

Pm’, K-S Lu Pm*, Y-S Hang

MD’,

T-K Liu

MD’,

‘Department of Orthopedic Surgery, National Taiwan University Hospital; ‘Department of Anatomy 3Center for Biomedical Engineering, College of Medicine, National Taiwan University, Taipei, Taiwan, ROC

Summary The hindlimb of New Zealand white rabbit was osteotomized and then slowly lengthened at a rate of 1 mm/day until a 2.0-cm gain in length was reached. The triceps surae muscletendon unit was then tested either with or without 2 months fixation for bony consolidation. After limb lengthening, the strain at peak load was decreased and the axial rigidity was increased significantly; but other biomechanical parameters such as peak load, maximal deformation at peak load, stiffness, and energy absorption before peak load did not show any significant difference. We conclude that healthy triceps surae muscle has a great potential to be lengthened despite the changes in intrinsic structural properties of the muscle. The change in the biomechanical properties occurred during the time of distraction and was not affected by the time of bony consolidation. Relevance As noted in this study, many biomechanical parameters of the triceps surae muscle were not affected after prolonged distraction. This fact suggested that the healthy muscletendon unit is not a main causative factor of joint contracture after limb lengthening. However, there were intrinsic changes in the structural properties of the triceps surae muscle. Equinus contracture after limb lengthening may be caused by the aggravated intrinsic structural changes of the injured or denervated scarred muscular tissue. Key words:

Biomechanical

Clin. Biomech.

properties,

Vol. 10 No. 5: 263-267,

limb lengthening,

skeletal

muscles

1995

Introduction The work of Ilizarov promises to revolutionize the practice of orthopaedic surgery. He used a slow, gradual distraction force (1 mm/day in his study) as a mechanical signal to stimulate tissue growth, even in mature organ systems. Spatial arrangements of the fixator components permit angular or rotatory deformities to be corrected slowly, bones to be elongated, and segmental defects to be filled. With this method, treatments of the limb-length inequality’ and chronic pseudoarthrosis with or without non-union2a3 can also be substantially improved. In recent years a series of experiments had been conducted using the Ilizarov technique to lengthen the Received: 13 April 1994 Accepted: 9 August 1994 Correspondence and reprints request to: Jui-Sheng Sun MD, Depart-

ment of Orthopedic Surgery, National Taiwan University Hospital, No. 7, Chung-Shan S. Road, Taipei, Taiwan, 100, ROC

bones4 and to investigate the mineralization sequence during distraction osteogenesis’. Although many investigators have examined the effects of immobilization and training on the skeletal muscles6-8, little is known about the long-term effects of traction on the biology of skeletal muscles. The purpose of this study was to investigate the changes in biomechanical properties of healthy skeletal muscle after limb lengthening. Methods Twenty-four mature New Zealand white rabbits of both sexes (weighting 2.0-2.5 kg) were used. The rabbits were equally divided into two groups. For the first group the biomechanical test was performed immediately after 20 mm of elongation. For the second group a modified Orthofix external fixator was maintained for 2 months for bony consolidation; then the same biomechanical test was performed.

264

Clin. Biomech.

1995; 10: No 5

The rabbits were premeditated with 0.5 mg atropine and anaesthetized with ketamine (50 mg/kg, i.m.) and rompun [2-(2,6-xylidino-)-5,6-dihydro-4H-l,3-thiazine hydrochloride] (12 mg/kg, i.m.). Under aseptic technique a modified Orthofix external fixator with lengthening apparatus was transfixed by four transverse K-wires inserted across the tibia to construct one plane with bilateral frames configuration. A transverse osteotomy at the mid-portion of the tibia1 and fibular shafts was performed by handsaw. On the third postoperative day, lengthening of the hind limb was carried out daily at a speed of 1 mm/day (average 5 mm/week; with 2 days rest in each week). The traction was completed when a total of 20 mm of lengthening was obtained. The contralateral hindlimb was a nonoperated normal control. The choice of side for operation was random. The setup of biomechanical tests was the same as previous reported’. Briefly, after general anaesthesia with intramuscular administration of ketamine (dosage, 50 mg/kg). the hindlimbs were prepared. A skin incision on the lateral aspect of each hindlimb was made. The Achilles tendon was isolated with special care to maintain its neurovascular supply and tendon insertion intact. A dial caliper (accurate to 0.05 mm) was used to measure the distance between the origin of the triceps surae at the femur and the insertion at the calcaneus when the knee and ankle joints were flexed at 90” angulation. This distance was defined as the in situ muscle-tendon unit length. The distance between tendon insertion on the calcaneus to its musculotendinous junction was defined as the tendon length, The length of muscular portion was calculated by subtracting the in situ muscle-tendon unit length with the tendon length. The anaesthetized rabbit was then placed in a frame attached to the MTS machine (MTS BionixTM 858 Test System). The hind limb was immobilized with K-wire transfixation through the proximal tibia. The knee joint was kept in 90” flexion with a transverse bar of the fixation frame. The distal tendon insertion was freed by osteotomy at the calcaneal tuberosity and clamped to the MTS load cell (MTS 458.20, Microconsole, Axial). A 3-N preload was placed on the muscle, and the muscle length was again measured to restore its in situ length (resting length, Lo). During the test the muscle was stretched at a constant rate (0.5 cmimin) until a macroscopic tear or full separation of muscle fragments occurred. A TestlinkTM system Software (PCLABTM Data Translation, Data Translation Inc. Locke Drive, Marlboro, MA, USA) was used to simultaneously record the forces and length until the muscles were torn. The muscles were kept moist at physiological temperatures using warm normal saline irrigation. Additional dosage of anaesthetics was given as needed. The choice in order of the control and experimental limbs was random. This study received prior approval of the National Taiwan University Medical College’s Animal Research Committee. The measurements of biomechanical parameters

were the same as previous reported”. Peak load was defined as the maximal force recorded during each test. The deformation at peak load was calculated by muscle length at peak load recorded by personal computer minus muscle length before distraction. Within the linear portion of the curve, slope of load-deformation curve was calculated by dividing the changes in load with changes in deformation. The slope of loaddeformation curve was defined as the stiffness of the triceps surae muscle. Total energy absorption was defined as the area under the load-deformation curve before full separation of the triceps surae muscle. The energy absorption before peak load indicated the energy absorbed by the musculotendinous unit before the point of peak load. The strain was defined as the measurements of the instantaneous deformation (AL = L - Lo) at each load divided by the resting length (L/Lo). The load-strain curve was plotted for each triceps surae muscle. Within the linear portion of the curve the slope of load-strain curve was defined as the axial rigidity of the triceps surae muscle. Axial rigidity was measured by dividing the changes of load with changes of the strain, which characterized the axial loadings to the muscle-tendon unitlO. The paired t test was used to minimize the individual variation of each rabbit. The biomechanical properties of triceps surae muscle at the end of distraction and after 2 months consolidation was measured by dividing each data of the experimental limb with that of the contralateral control limb. The difference between group I and II was evaluated by comparing the ratio of the experimental limb to that of the contralateral non-operated limb with Student’s t test. Results Quantitative analysis. After 20 mm of limb lengthening there was a significant increase in the whole length of triceps surae muscle-tendon unit. The increase in length mainly occurred at the muscular portion (Table 1). The difference in the mean length of the whole muscles (including belly and tendons) was significant between the control and experimentally lengthened limbs (P
Curve pattern. All the triceps surae muscle-tendon units under distraction exhibited a similar curve pattern (Figure 1). The load-deformation curve began with an initial increasing slope and ultimately reached the peak load. After the point of peak load there is a steep drop followed by a curve with gradual increasing and decreasing of the forces. There was no statistically significant difference between the stiffness of these two curves (Figure 1A). When the load was plotted versus the strain, the curve pattern of the control and experimental limb differed. The axial rigidity of the experimental limb was greater than that of the control limb (Figure 1B).

Sun et al. : Muscle properties Table 1. Measurements and without 2 months

of the length of triceps surae muscles bony consolidation (n = 12) Control

Millimetres Whole length Group I* Group II*

from control

and experimentally

Experimental

265

after limb lengthening lengthened

limbs with

Net Increase

% of Increase

99.5 (SD, 8.6) 101.0 (SD, 6.1)

119.9 (SD, 8.1) 118.6 (SD, 6.2)

19.5 (SD, 1.6) 17.6 (SD, 1.1)

19.6 (SD, 0.8) 17.4 (SD, 0.6)

Muscular portion Group I** Group II**

70.2 (SD, 6.1) 71.8 (SD, 4.3)

89.4 (SD, 6.1) 88.1 (SD, 4.6)

19.2 (SD, 1.6) 16.3 (SD, 1 .O)

27.5 (SD, 1.1) 22.7 (SD, 0.8)

Tendinous Group I Group II

portion 29.3 (SD, 2,5) 29.2 (SD, 1.8)

29.6 (SD, 2.0) 30.5 (SD, 1.6)

*P
**P
I, without

bony consolidation;

Biomechanical measurements. The changes in the biomechanical properties of the triceps surae muscletendon unit were mainly manifested as a decrease in the strain of the peak load and an increase in the axial rigidity (Table 2). The differences in peak load, deformation at peak load, stiffness of the loaddeformation curve, mean total energy absorption, and energy absorption before peak load were not statistically significant (Table 2). The differences of the strain at the peak load and axial rigidity of the triceps surae muscle were significant (P CO.001). Table 3 summarizes the biomechanical properties of experimental lengthened triceps surae muscle at the end of distraction and after bony consolidation. As shown, all the biomechanical parameters measured were not affected by the time of bony consolidation. The change occurred during the period of limb lengthening and was not affected by the period of 2 months fixation for bony consolidation (Table 3). Site of failure. Both the control and experimental rabbits showed a similarity of the failure site when the triceps surae muscle was stretched to rupture. The sites of failure were within 0. l-l .O mm and S-15 mm from distal musculotendinous junction for the soleus and lateral head of gastrocnemius muscle respectively. While in the medial head of gastrocnemius muscle, failure occurred within 15-30 mm from the distal musculotendinous junction.

Group

0.3 (SD, 0.02) 1.3 (SD, 0.08)

II, with 2 months

bony consolidation.

A. Load-Deformation

;

250

g g

200

j

150

1.02 (SD, 0.04) 4.45 (SD, 1.6)

Curve

100 50 0 0

10

20

30

40

Deformation

50

60

70

50

60

70

(mm1

400 350 300 $

250

D g

200

a 4

150 100 50 0

Discussion

Equality of limb length in the lower extremities is not only a cosmetic but also a functional concern. Inequality of limb length may result from many causes’‘, and a variety of methods have been attempted to stimulate growth of long bones’,“~‘“. The treatment of limb length discrepancy must be tailored to the specific conditions and needs of the individual patient. Over the past years, gradual osseous lengthening by distraction has been the procedure of choice. The most difficult complications that occur during lengthening are related to the muscle’“. Although a histological

0

10

20

30

40 srrc&l I%1

Figure 1. (A). Representative load-deformation curves of the triceps surae muscle-tendon unit of rabbit after 2 months fixation. The area under the curve depicts the relative energy absorbed to failure. The stiffness of the both limbs was not statistically significant. (B). The load-strain curves of triceps surae muscle-tendon unit of the same rabbit as (A). When the load was plotted versus the strain, the curve pattern of the control and experimental limb differed. The axial rigidity of the experimental limb was greater than that of the control limb. (p ) Experimental limb; (----) Control limb.

266

Clin.

Biumech.

1995;

10: No 5

Table 2. Biomechanical data of the peak load, deformation at peak load, strain, absorption of the composite triceps surae muscle-tendon unit (n = 12) Peak load

Group 1 Control Experimental P Group It Control Experimental P

Strain *

Stiffness

0’4

Deformation at peak load (mm1

(%)

(N/mm}

358.1 (SD, 92.2) 330.2 (SD, 101.8) 0.24

35.2 (so, 6.2) 35.7 (SD, 7.4) 0.41

35.4 (SD, 6.2) 30.0 (SD, 6.2) <0.001*

15.9 15.8

396.3 375.9

35.6 35.2

35.6 (SD, 7.8) 29.6 (SD, 7.1) <0.001*

16.8 19.3

(SD, (SD,

76.5) 65.6)

0.18

*P
I, without

(SD, (SD,

7.8) 8.2)

0.37 bony consolidation;

Axial

rigidity*

15.8 (SD, 4.9) 19.1 (SD, 4.4) <0.001*

7044.8 5835.6

18.9 (SD, 3.8) 22.8 (SD, 4.2) < 0.001*

9014.4 9699.6

4.7) 3.7)

(SD,

0.48 4.3) 3.8)

(SD, (SD,

0.40

axial

rigidity,

Total energy absorption (N-mm)

IN/%)

(SD,

Group II, with 2 months

stiffness,

Energy absorption before peak load (N-mm)

3976.2) 2517.2)

(SD, (SD,

and energy

4184.4 4059.8

0.12 (SD, (SD,

(SD, (SD,

1505.8) 1656.4)

0.39 3214.4) 4273.0)

0.29

4699.2 (SD, 1540.6) 4764.0 (So, 1455.8) 0.46

bony consolidation.

study on the long-term effects of traction on the muscle has been donei5, the changes in the biomechanical properties of the lengthened muscles were not well elucidated. In this study we analysed the changes in biomechanical properties of healthy triceps surae muscles after limb lengthening. The contributions of these changes in the formation of joint contracture were investigated. The triceps surae muscle in the experimental rabbits was lengthened statistically significantly. The difference in the mean length of the muscles (including belly and tendons) was significant between the control and experimentally lengthened limbs (P < 0.001). The increase mainly occurred in the muscular portion (Table 1). Since the tendon acts as a very stiff force transmission linkage without significantly modifying the muscle’s performancei6, we performed a tensile biomechanical test of triceps surae muscle to clarify the material properties of this lengthened muscle. After 17.4 to 19.6% lengthening of the healthy muscle, the differences in the peak load (Table l), deformation at peak load, and stiffness of the load-deformation curve within the control and experimental limbs of both groups were not significant (Table 2). This means that the extensibility of the experimental limbs did not change after limb lengthening. Woittiez et al. reported that total energy absorption before failure is proportional to the mass of that muscle”. In our preliminary research the mean net weight of triceps surae muscles examined from the control and experimentally lengthened limbs did not differ significantly15. It is expected that there will be similar energy absorption to disrupt the muscle of control and experimental groups (Table 2). These results indicated that the tolerance of

healthy triceps surae muscle to limb lengthening is quite good, and not as limited as previously thought’4,1X,‘9. Although the deformation at peak load was the same in both groups, strain at the peak load of the experimental group was less, since the length of triceps surae muscle-tendon unit was longer. A similar result was observed in the axial rigidity of the experimental lengthened triceps surae muscle (Table 2). The abovementioned facts suggest that there were intrinsic changes in the biomechanical properties of the triceps surae muscle after limb lengthening despite the good extensibility of the skeletal muscle observed in clinical medicine. The changes in the intrinsic biomechanical properties of the lengthened muscle occurred mainly during the process of distraction and were not related to the period of consolidation (Table 3). It has been suggested that the tolerance of the muscle to stretch depends on many factors: the speed and amount of lengthening, the age and the associated disease of the subject, the technique of pin insertion, and the underlying status of the soleus-gastrocnemiusAchilles tendon complex”. By vigorous physical therapy, such as posterior plaster splint or placing the heel extension, the incidence of these complications can be reduced’*. However, no amount of physiotherapy or splinting will prevent further shortening of a soleus-gastrocnemius- Achilles tendon complex already scarred and injured by trauma, infection, or previous surgery. In this study we present evidence to demonstrate that the healthy triceps surae muscle possessesa great potential to stretch despite intrinsic changes within the muscle. The healthy muscle-tendon unit is not a main causative factor of joint contracture

Table 3. Comparison between the biomechanical after 2 months of bony consolidation (n = 12)

of the triceps

Deformation 1%1

Peak load (%I Group I Group II P

92.2 94.9

(SD, (SD,

26.0) 17.5)

0.41

Data were measured consolidation; Group

101.4 98.9

(SD, (SD,

0.39

19.5) 22.3)

properties

Strain (%l 84.7 (SO, 16.1) 83.1 (SD. 19.0) 0.41

Stiffness 1%) 99.4 114.9

(SD,

Axial

26.3)

(SD, 25.8)

0.08

surae muscle

Total energy absorption l%l

rigidity 1%)

120.9

(SD,

120.6

(SD, 23.1)

>0.5

by the ratio of the experimental limb to that of the contralateral II, with 2 months bony consolidation.

at the end of distraction

32.2)

82.8 107.6

(SD, (SD,

41.8) 43.1)

Energy absorption before peak load l%J 97.0 101.4

0.08 non-operated

and

(SD, (SD,

37.2) 32.1)

0.40 limb. Group

I, without

bony

Sun et al.: Muscle properties

after limb lengthening. We suggest that the injured or denervated scarred muscular tissue may aggravate the intrinsic change of biomechanical properties, which then induces the equinus contracture during lengthening of the tibia. This suggestion is further confirmed by the fact that the incidence of equinus contracture in clinical medicine is more often observed in the limb lengthening performed for the cases of poliomyelitis or of trauma with severe soft-tissue scarring. The possible aetiology of this higher incidence is due to the decrease in muscle viability caused by lack of trophic effect of the nerve. Acknowledgements

This study was supported by National Science Council, ROC (NSC 82-0412-B002-280 and NSC 83-0420-B002220) and in parts by Academia Sinica, ROC (AS NTUH CRC 92-013). We are also indebted to Mr Victor Chian-Yu Yeh and Mr Hung-Chi Chen for their excellent technical assistance during this study.

References Paley D. Current techniques of limb lengthening. J Pediatr Orthop 1988; 8: 73-92

Fabry G, Lammens J, Van Melkebeek J et al. Treatment of congenital pseudoarthrosis with Ilizarov technique. J Pediatr Orthop 1988; 8: 67-70 Paley D. Problems, obstacles, and complications of limb lengthening by the Ilizarov technique. Clin Orthop 1990; 250: 81- 104 Aronson J, Harrison B, Boyd CM et al. Mechanical induction of osteogenesis: preliminary studies. Ann Clin Lab Sci 1988; 18: 195-203

after limb lengthening

267

5 Aronson J, Good B, Stewart C et al. Preliminary studies of mineralization during distraction osteogenesis. Clin Orthop

1990;250:43-9

6 Booth FW. Physiologic and biomechanical effects of immobilization on muscle.Clin Orthop 1987; 219: 15-20 7 MacDougall JD, Elder GC, Sale DG et al. Effects of strength training and immobilzation on human muscle fibers. Eur J Appl Physiol1980; 43: 25-34 8 Taylor NA, Wilkinson JG. Exercise-induced skeletal muscle growth: hypertrophy or hyperplasia? Sports Med 1986; 3: 190-200 9 Sun JS, Tsuang YH, Liu TK et al. Failure sites and peak tensile forces of the composite triceps surae muscle by passive extension in rabbit. Clin Biomech 1994; 9: 310- 14 10 Mow VC, Hayes WC. Basic Orthopedic Biomechanics. Raven Press, New York, 1991; 103 11 Grayhack JJ, Carroll NC. Projected limb length inequality: selecting patients for surgery. Orthop Clin North Am 1991; 22: 581-87 12 Ilizarov GA. Clinical application of the tension-stress effect for limb lengthening. Clin Orthop 1990; 250: 8-26 13 Kenwright J, Spriggins AJ, Cunningham JL. Response of the growth plate to distraction close to skeletal maturity: is fracture necessary? Clin Orthop 1990; 250: 61-72 14 Green SA. Postoperative management during limb lengthening. Orthop Clin North Am 1991; 22: 723-34 15 Sun JS, Hou SM , Liu TK, Lu KS. Analysis of neogenesis in rabbit skeletal muscles after chronic traction. Histol Histopathol (in press) 16 Baratta R, Solomonow M. The effect of tendon viscoelastic stiffness on the dynamic performance of isometric muscle. J Biomech 1991; 24: 109-16 17 Woittiez RD, Huijing PA, Boom HBK, Rozendal RH. A three-dimensional muscle model: a quantified relation between form and function of skeletal muscles. J Morph01 1984; 182: 95-113 18 Eldridge JC, Bell DF. Problems with substantial limb lengthening. Orthop Clin North Am 1991; 22: 625-31 19 Lehman WB, Grant AD, Atar D. Preventing and overcoming equinus contractures during lengthening of the tibia. Orthop Clin North Am 1991; 22: 633-41