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I-1 SFVIFR

Printed in Great Britain 02684033108 $lY.lHJ +o.oo

ML: SO268-0033(97)00051-X

Yang-Hwei

Tsuang1r4, Jui-Sheng

Sun’, Ing-Huo

Chen2,

Shang-Hwa

Hsu3, King-Yaw

Tsao 3, Kuan-Yih Wei4, Yi-Shiong

Hang’

‘Department of Orthopedic Surgery, National Taiwan University Hospital, College of Medicine, National Taiwan University, Taipei, Taiwan

*Department of Orthopedic Surgery, Tzu-Chi Buddhist General Hospital, Hua-Lian, Taiwan 3Graduate Institute of Industrial Engineering, National Chiao-Tung University, Hsin-Chu, Taiwan

“Department of Orthopedic Surgery, Taiwan Provincial Tao-Yuan General Hospital, Tao-Yuan, Taiwan

Abstract

Objective. To define the threshold of muscle injury with cyclic passive stretch.

Design. The changes in the load-deformation curve of muscle-tendon unit were monitored until the failure point by an in viva rabbit model.

Background. Muscle injuries range in severity from a simple strain to complete rupture. Although strains occur more frequently than complete failures, only a few studies have investigated the phenomena of these sub-failure injuries. Monitoring of the continuum for stretch-induced injury allows us to define the threshold of stretch injury.

Methods, Thirty rabbits’ triceps surae muscle-tendon unit preparations were used. One of the pairs (control) was stretched until failure; the other (experimental) was first cyclic stretched to either 12, 20 or 25% of the initial length of the muscle-tendon unit and then stretched to failure. Comparisons were made between the load-deformation curves of the experimental and control specimens.

Resulfs. When cyclic stretched to 12 or 20%, there were no significant changes existed in the biomechanical parameters except the deformation at the peak load. In contrast, all the biomechanical parameters except the ration of the energy absorption changed significantly after 25% strain cyclic stretch.

Conclusions. A threshold for stretch-induced injury does exist. This can be reproduced at the 25% strain of the triceps surae muscle-tendon unit.

Relevance

Muscle--tendon injuries, primarily muscle strains or tears, are extremely common in profes- sional and amateur athletes. This experimental study with rabbits, give evidence that changes in the biomechanical properties after sub-failure injury does exist in the muscle tendon unit. Mare importantly, stretching before competition should not exceed 25% strain in the triceps surae muscle-tendon unit. 0 1998 Elsevier Science Ltd. All rights reserved

Key woi-ds: Cyclic stretch, sub-failure, muscle-tendon unit

C/in. Biomech Vol 13, No. 1, 48-53, 1998

Introduction amateur athletes’.2. These injuries account for almost

Muscle-tendon injuries, primarily

tears. are extrcmcly common in

muscle strains or

professional and

half of all injuries in certain sports”. The triceps surae muscle is one of the most common muscles damaged

in the lower extremities”. In the past two decades,

much literature has been devoted to the preven-

tion2.‘. understanding”, and treatment of these

injuries7.

During the activities of daily living, the musculo- skeletal system is subjected to a wide range of joint

motion. Both muscle and tendon components are

_.._ -.--- _.. -.---. .-- .-.. --.-.-.--_. ..-..- .___ __ -__- J%~C(~II CJC/- 23 Milrch ! 007; .4r~c~~/>r~ti.- 1 S August I997

(‘o~~~.\/\porrtl~,~~~[, urmll rcprinf rrrp~t.\ to: Jui-Shcng Sun, Dcpartmcnt (4 Orthopedic Surgery. Nxtional Taiwan IJniversity Hospital, i‘ollege of Medicinc, National Taiwan University, No. 7, Chung- Shari South Road. Taipei. Taiwan, 10002, ROC’. Tel: +88h 2 ?3’i7OX1)0 (ext. 5277): Fax: +880 2 -7392?12.1.

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Twang et al.: Threshold of rabbits’skeletal muscle 49

susceptible to trauma or wear and tear. It is believed that warming up before an athletic event is important

for both performance and injury prevention. In sports

medicine, stretching exercise has been recommended

to prevent injuryh,8 and to improve performance”.

Previous experimental studies in animals have shown

that passive warming increases the extensibility of the

musculo-tendinous unit and that warmed muscle has

greater deformation and less stiffness than cold

muscle, and offers support to the theory that warming

up muscles can aid in injury prevention and improve-

ment in athletic performance”‘.

However, intensive exercise training can also result in muscle damage and muscle soreness. There are a

large number of biomechanical studies of ligaments

or muscles stretched to failure, but only a few studies

were done to determine the effect of sub-failure

stretch on the elastic behavior and failure properties

of the muscle-tendon unit. Our recent experimental

studies of indirect muscle strain injury have concen- trated on the muscles injured in response to excessive

stretch alone” or stretch and activation’2. Previous

studies did not determine a threshold or minimal

force-displacement necessary to create injury.

Measuring joint range of motion is not practical

for the athlete or patient attempting to assess

improvement in flexibility, therefore stretch distance

is a more useful method of measuring flexibility. In

contrast to previous human study using joint range of

motion to determine the effects of stretching of flexi-

bility, we measured stretch distance relative to a fixed

reference point. The present study investigates a

repetitive stretch of muscle-tendon units using the

minimal strain necessary to create injury, and thus,

define a threshold for injury with cyclic passive

stretch. We chose the New Zealand white rabbit for

our investigation, because their architectural design,

including the soleus in the hindlimb, were considered

to be similar to that found in humans’“. Methods

Thirty New Zealand White rabbits (mean weight, 2.5,

SD, 0.2 kg) were divided into three groups. The

preparation was the same as previously reported”.

After subcutaneous ketamine (dosage, 50 mg/kg)

general anesthesia, an incision from the mid calf to

the plantar surface of the foot was made on the

lateral aspect of each hind limb. The Achilles tendon

was isolated taking special care to maintain the

neurovascular bundle and the tendon insertion intact.

For determining the in situ muscle-tendon unit

(MTU) length, dial calipers (accurate to 0.05 mm)

were used to measure the distance between the origin of the triceps surae at the femur and the insertion at calcaneus with the knee and the ankle at 90” angula-

tion. The anesthetized rabbit was placed in a frame

attached to a MTS machine (MTS BionixTM 858 test

system). The hind limb was immobilized with a

K-wire transfixation through the proximal tibia. The

distal tendinous insertion was freed by osteotomiza-

tion at the calcaneal tuberosity and clamped to the

MTS load cell. A 3 N preload was applied on the

muscle, and then the muscle length was again

measured’ ‘.

The muscle-tendon unit of one hind limb was

cyclically loaded for one hour at a rate of 0.5 cm/min

to any of three strain amplitudes (12, 20 and 25%~).

Once the peak stretch amplitude was reached, the

stretching was discontinued and the muscle-tendon

unit returned to its initial resting length. After cyclic

passive stretch, the muscle was stretched at a

constant rate (0.5 cm/min) until a macroscopic tear or

full division of the ruptured muscle fragments

occurred. In the other hind limb, the muscle-tendon unit was stretched at the same rate to failure of the

muscle-tendon unit. The load and deformation

required to deform the muscles were simultaneously

recorded on a PC by the TestlinkTM system Software

(PCLABTM Data Translation, Data Translation Inc.,

Locke Drive, Marlboro, USA). All muscles were kept

moist and at physiologic temperature using warm

normal saline irrigation. Additional anesthesia was

given as needed. This study received prior approval

of the National Taiwan University Medical College’s

Animal Research Committee. After completion of

the experiments, the rabbits were sacrificed at the

conclusion of the study.

For each triceps surae muscle, the load and defor-

mation of the muscle-tendon unit were recorded and

plotted directly using a PC. Deformation of the

muscle-tendon unit was measured when peak load

was evident. The deformation of the muscle-tendon

unit was calculated by muscle length at peak load

minus muscle length before distraction. The area

under the load-deformation curve before the failure

point represents the relative energy absorbed by the

muscle-tendon unit prior to failure. The difference

of the energy absorbed by the muscle-tendon unit

before the point of peak load and the point of full

separation of the ruptured fragments as well as the

differences between the two limbs were evaluated by the paired t-test. Because of the great individual

variation of the triceps surae muscle strength, only

the statistic method of the paired t-test was used to evaluate the difference between the two limbs of the rabbits in each group. The level of statistical signifi- cance was set at 5%.

Results

All of the triceps surae muscle-tendon units under

distraction had a similar curve pattern, as shown

previously”. The load-deformation curve began with

an initial increasing slope and ultimately reached the

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steep cirop followed by a curve with gradual increasing and decreasing of the forces. The slopes of thrse curves were measured a1 every linear portion of the r‘urve. The means of peak tensile force. dispiacc- mcnt at peak tensile force and slope are summarized i tI T;rhi~, j

Afrct- cyclically stretched ,tt either 12 or 20%

-train. the shape of the load-deformation curve of

triceps surac muscle-tendon unit did not show any

Ggnitjcant change [Figure I (A)]. When the muscic-

tendon unit wan cyclically stretched after 259; strain,

o statistically significant difference in the biomechan-

ical parameters of the triceps surae muscle-tendon

rmit between the control and experimentally cyclic

rtretchcd group” can be noted [Figure l(B)]. In the

Froup ol‘ i A ? and 20C;i~ cyclic stretch, ail biomechanicai

parameters between the control and experimental

cyclic stretched muscle-tendon unit showed no signi-

ficant difference except in deformation at the peak

!oad (‘I’abies I and 3). In the group of 25% cyclic

~trctch. ail biomechanicai parameters between the

control and experimental cyclic stretched muscie-

tendon unit showed a statistically significant differ-

c)ncc. except for the ratio of energy absorption

(Tables I and 2 j. After 60 min cyclic stretch to 2SC4.

the peak load decreased IO.i%. deformation at peak

load decreased iO.Y,% and slope of the ioad-defor- mation increased 27.9% (Table I ).

The energy absorption before complete separation

of the disrupted fragments ctf the muscle-tendon unit

was expressed bv the area beneath the ioad-deforma- iion curve. The means of total energy absorption,

energy absorption before peak tensile force and the

ratio of energy absorption before peak tensile force

arc shown in the Table 2. In the rabbits group after cithcr I? or 20% cyclic stretch, the means of the total

energy absorption and the energy absorption before

peak load remained constant: while after 25% cyclic

stretch. the means of the total energy absorption and

the energy absorption before peak load decreased

significantly. The differences were statistically signifi-

cant (,r = 0.0025 and 0.0017 respectively). No statis-

tically significant difference appeared between the

ratio of energy absorption in both groups (P > (LOS).

The total energy absorption before muscle-tendon

unit failure decreased 33.1%; the energy absorption before peak load decreased 35.75% (Table 2).

The sites of failure were within 0.1-1.0 mm from

the distal musculo-tendinous junction for soieus

muscle and within S-10 mm from the distal muscuio-

tendinous junction in the lateral head of gastro-

cnemius muscle. While in the medial head of

gastrocnemius muscle, failure occurred within

15-30 mm from the distal muscuio-tendinous

junction as previous reported”.

Discussion

Muscuio-tendinous strain injuries have been cited as

the most common injury in competitive athletics’.“.‘J.

Their f’rcquency and disabling effects have been

documented in many epidemiologic studies” Is.

Strains not only cause a significant loss of time from

sports, but are also a common source of pain. and

impair performance following return to competition.

Despite their common occurrence, there have been

relatively few studies investigating the effects of these

injuries. Possibly as a result of the incomplete study

of these injuries, treatment is extremely variable,

ranging from complete rest and immobilization of the

injured muscle to immediate return to athletic

competition, sometimes after local injections into the

injury site’“. Previous studies involving stretching

injury have used large total displacements (beyond

the muscle’s physiologic range of motion) to create

injury’ ‘-?“. These studies did not determine a

threshold or minimal force-displacement necessi-

tated to create injury. Muscle injuries can range in

severity from a simple strain to a complete rupture.

However, strain or sub-failure comprise 80% or more of ail muscle injuries and are much more frequent

than complete failures. Only a few studies have

investigated the phenomena of these sub-failure

injuries”. Despite this prevalence, there is a paucity

of information on the mechanics of muscle strains.

The present study has investigated a repetitive stretch

of muscle-tendon units using the minimal strain

necessary to create injury, and thus, define a

threshold for injury with passive stretch. The

hypothesis of this work was that sub-failure injury

Table 1. Biomechanical data of the slope, peak tensile load and deformation at peak tensile load of the composite triceps surae muscle-

tendon unit (N = 10)

12?/0 20% 25%

-__.

Peak lead (N) Control 482.2 (SD, 68.0) 463.5 (SD, 58.4) 447.4 (SD, 56.9)

Stud\; 485.0 (SD, 63.8) 459.7 (SD, 69.6) 401.4 (SD, 90.2)

P value 0.8290 0.8627 0.0256

Deformation at Control 42.1 (SD, 5.3) 40.1 (SD, 4.6) 43.7 (SD, 5.8)

Peak load (mmi Study 38.5 (SD, 5.7) 36.6 (SD, 4.1) 35.0 (SD, 6.7)

P value 0.0098 0.0058 0.0055

Slope (N/mm) Control 19.9 (SD, 1.6) 18.1 (SD, 2.5) 17.9 (SD, 3.7)

Study 20.1 (SD, 2.0) 19.7 (SD, 2.8) 22.9 (SD, 4.0)

P value 0.7249 0.2677 0.0010

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Twang et al.: Threshold of rabbits’skeletal muscle 51

Figure 1. Load-deformation curve of triceps surae muscle-tendon unit after 20 or 25% cyclic stretch. The area below depicts the

relative energy absorbed to failure under various conditions: (- ) control; (- - -) experimentally cyclic stretched to 20 or 25%.(A)

After cyclically stretching to 20% strain, the shape of the load-deformation curve of triceps surae muscle-tendon unit showed no

significant change. (B) When the muscle-tendon unit was cyclically stretched at 25% strain, the peak load, deformation at peak load,

total energy absorption and energy absorption before peak load all significantly decreased, while the slope of the load-deformation

increased significantly.

Table 2. Energy absorption of composite triceps surae muscle-tendon unit (N = IO)

12% 20% 25% Total energy Absorbed (N/mm) Energy absorbed Before peak Load (N/mm) Ratio of energy Absorption WI Control Study P value Control Study P value Control Study P value 13068.2 (SD, 3056.0) 12992.0 (SD, 3513.8) 0.9002 7343.3 (SD, 2138.6) 6934.3 (SD, 1670.1) 0.4730 56.0 (SD, 7.9) 54.2 (SD, 6.5) 0.5913 12245.6 (SD, 4202.0) 10494.1 (SD, 2505.8) 0.1754 6761.3 (SD, 1659.2) 5937.9 (SD, 1525.4) 0.1339 57.3 (SD, 11.4) 57.3 (SD, 10.9) 0.9945 12797.0 (SD, 2879.4) 8564.6 (SD, 3610.1) 0.0025 7102.0 (SD, 2269.5) 4566.9 (SD, 2063.3) 0.0017 55.1 (SD, 10.0) 54.1 (SD, 10.4) 0.7812

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tion curve and that the sub-failure injury initial does

not alter the load-deformation behavior above the

icvei of t hc sub-failure injury.

As shown in Table I, WC find that the deformation

at the peak toad diminished at’tcr cyclic stretching at

ail ranges of strain. Howtlver. both the I2 and 20%

~‘roupx demonstrated no biomechanical evidence of

tr

injury in muscle-tendon unit injury, whiic muscles of

the 3ii’; strain group demonstrated evidence ot

injury by diminished peak toad, total energy absorp-

ti09. and energy absorption before peak toad

(Tabicx 1 and 2). These data suggest that a threshold for injury with passive stretch does exist. The finding

rhnr xl’tcr 35”: cyclic stretching the muscle-tendon

unit ixxame more stiff than that of control muscie--

tendrrrr unit supports the possibility oi’ 25% stretched

llltlSCl~ being injured. ‘This difference in stiffness

impiic~ that, i’ctr A given increase in deformation, 25%

cyclic \tretchcd muscle deceiops more force when

cornpaled with I?.‘? or 20% stretched muscle (Figure

i j. Further cvidcncc of the muscle-tendon unit being

injurtxi is obvious by observing that the peak toad,

iota1 ~ncrgy absorption. and energy absorption before

pcah toad wcrc all diminished after 25% cyclic stretch

i’rablr~ I atxi ‘1. It assumes that a critical strain

t~ccls to IV reached before strain injury can bc initi-

aled. i3clorc cucrcise. stretching has been recom-

mcndcd tii prcvcnt injury anti to improve

p”rf(~rlI1;JIicc”.Y ” T’hc widespread clinical impressions

regarding the protective effect of passive stretch on

nlurclc@ are certainly not against these data. In fact, it I‘ vicar that iC a critical strain is not reached, ;I

cictr~mcntal cfi’~ct of cvciic stretching would not

appear

Recently. Panjabi c’t L[/.‘~ elucidated that stretching

i t:c ligament iii X0’+ of the failure subsequently

incrc;tsed deformations below X0%, but had no effect

r)!l anv mechanical propertics above 80%, including

{he peak toad and deformation. This may result in

increased joint laxity, additional toads will be applied

tli other- joint structures and to the joint. In this

ctudv. we demonstrated that when the muscle-tendon

rmit’was cyclically stretched. a statistically significant

decrease in thcb deformation at the peak load of the

1 riceps surac muscle--tendon unit was noted, even

though ail other hiomechanicai parameters showed

no significant change (Tables I and 2). The anesthetic

aed in this study was ketaminc and this drug has no

muscle-relaxant cffecP. The ncrvc function and

related muscle tone were well preservedz3. This fact

suggests that the presence of nerve function can

respond to the cyclic stretch by increasing muscle

!one and then the deformation at the peak toad is

decreased. This suggestion is further consolidated by

the fact that after 25% cyclic stretch, the slope of the

tc,~td-deformatioI1 curve in the muscle-tendon unit is

significantly increased before the peak deformation.

eters between the control and experimental cyclic

stretched muscle-tendon unit showed a statistically

significant difference except in the ratio of energy

absorption. The peak toad, deformation at peak toad,

the means of total energy absorption, energy absorp-

tion before peak toad decreased (Table I and 2).

These biomechanical parameters indicated that

disruption in the muscle-tendon unit has occurred to

some extent.

Cyclic stretching of muscle-tendon units above a

threshold would drastically alter both ioad-deforma-

tion and failure properties. Using an in IJ~VU rabbit

model, we have demonstrated that the 2Oci;

sub-failure stretch does not alter the failure point of

the muscle-tendon unit, but significantly alters the

deformation at the peak toad, possibly by the nerve

reflex. Above 25% strain, the biomechanicai param-

eters are all significantly changed. The fact that there

is significant fiber damage without gross changes in

the mechanical behavior below the sub-failure point

has some intriguing consequences. The most promi-

nent morphological changes in the injured muscle

fibers were the loss of desmin staining occurred in the

absence of contractile or metabolic protein disrup-

tion. The disruption of the cytoskeletal network and

an inflammatory response could further deteriorate

the contractile response”“. Clinically, it is well

observed that mild strains can cause significant pain

without altering muscle activity. The results of this

study arc. then, in general agreement with those

observations, assuming pain is associated with

damage. We postulate that fiber failure without

accompanying change in the gross load-deformation

behavior is a potential mechanism for stimulating the

biological maintenance and repair of the muscle-

tendon unit. This suggests that this model can be

further validated by documenting a biological/inflam-

matory response to a sub-failure injury, which would

not notably alter the load-deformation behavior.

In summary, this study shows that a threshold and

continuum for stretch-induced injury does exist. It is

possible that the muscle fiber disruption occurred

initially and connective tissue disruption occurred

only with larger muscle displacementP. More

importantly, in our model, injury can be reproduced

at 25% strain of the triceps surae muscle-tendon unit.

Acknowledgements

The authors sincerely thank the National Science

Council (ROC) for their financial support of this

research.

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數據

Table  1.  Biomechanical  data  of  the  slope,  peak  tensile  load  and  deformation  at  peak  tensile  load  of  the  composite  triceps  surae  muscle-
Table  2.  Energy  absorption  of  composite  triceps  surae  muscle-tendon  unit  (N  =  IO)

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