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132 InternationalJournaloTherapyandRehabilitation,March2010,Vol17,No3

Research

Stretching exercises are commonly under-

taken in sports and rehabilitation set-

tings. Among the benets o stretching

o human musculoskeletal structures are

injury prevention, and improved perormance by

regaining joint range o motion (Hortobagyi et

al, 1985; Taylor et al, 1990; Wilson et al, 1991;

Witvrouw et al, 2004). Similarly, in physical

therapy, stretching is one o the most eective

techniques used or lengthening shortened mus-cles, and improvement o joint range o motion

(Ylinen, 2008).

To determine the most eective stretching

method and optimal stretching time, an under-

standing o the response to stretching o the

muscle-tendon unit in various states is required.

The reaction o a healthy muscle-tendon unit

to stretching has been previously examined in

healthy adults (Herbert et al, 2002; Kubo et al,

2005; Morse et al, 2008). Herbert et al (2002)

measured changes in length o muscle ascicles

in relaxed human gastrocnemius muscle during

passively imposed changes in joint angle. They

Behaviourothemuscle-tendonunitduringstatic

stretchingollowingunloading

reported that in gastrocnemius, which has rela-

tively long tendons, only 27% o the total change

in muscle-tendon length was transmitted to the

muscle ascicles. Kubo et al (2005) showed that

while the muscle ascicles, tendon and apone-

urosis stretched during passive dorsifexion o

the ankle joint, the elongation o the tendon was

signicantly greater than that o the aponeuro-

sis. Morse et al (2008) reported that the muscle-

tendon unit length increased by 21.9 mm duringstretching. However, the reaction to stretching

o an unhealthy muscle-tendon unit, such as in

muscle injuries including muscle strain, muscle

tendon atrophy, or unloading, is largely unknown.

The aims o the present study were to inves-

tigate the reaction o the muscle-tendon unit to

stretching ater a period o non-weight-bearing,

compared with that o a healthy muscle-tendon

unit, and to quantiy, using ultrasonograms, the

displacement o the ascicle-deep aponeurosis

junction (DA) and the myotendinous junction

(MTJ) during stretching o the medial head o the

gastrocnemius muscle.

Aims: To determine the amount o displacement in the muscle-tendon unit o the medial head o the

human gastrocnemius muscle during static stretching, ater a period o non-weight-bearing ollowing injury.

Methods: Twenty emale patients with a unilateral lower leg injury participated in this study ( N= 13

ollowing ankle racture-dislocation; N= 7 ollowing racture o the tibiofbula). The dierence in

displacement o the junction o the ascicle and the deep aponeurosis junction (DA) at ¼ proximal

height o the lower leg and that o the myotendinous junction (MTJ) between the injured and

uninjured leg was measured using ultrasonograms and analyzed by two way analysis o variance or

repeated measures and paired t-tests.

Findings: Initially, DA displacement was larger, and MTJ displacement was smaller, in the injured

compared with the uninjured leg. Ater treatment, DA and MTJ displacements in the injured leg

approached levels o the uninjured leg. At all time points, DA and MTJ displaced distally during the

frst three minutes o stretching in both legs ( P < 0.01).

Conclusions: Following a non-weight-bearing period, ascicles and tendon may be excessively

extended. Recovery o the muscle tendon complex might be accelerated by applying exercises aimed

at attaining increased extensibility o the aponeurotic tissue.

Keywords:nmuscle-tendonunitnrehabilitationnstretchingnunloading

Submitted 7 August 2009, sent back or revisions 1 October 2009; accepted or publication ollowing double-blind peer review

3 December 2009

Hiroshi Kanazawa, Yukio Urabe, Taizan Shirakawa

Hiroshi Kanazawa

is Senior Physiotherapist,

Director o Department

o Rehabilitation,

Department o

Rehabilitation,

Matterhorn

Rehabilitation Hospital,

and Doctorate Student,

Graduate School

o Health Sciences,

Hiroshima University,

Hiroshima; Yukio

Urabeis Proessor,Graduate School

o Health Sciences,

Hiroshima University,

Hiroshima; and Taizan

Shirakawa is Senior

Orthopedic Surgeon,

President o Matterhorn

Rehabilitation

Hospital, Matterhorn

Rehabilitation Hospital,

Hiroshima, Japan

Correspondence to:

H Kanazawa

E-mail: kanah@mbe.

ocn.ne.jp



InternationalJournaloTherapyandRehabilitation,March2010,Vol17,No3 133

maximal ankle dorsifexion angle o the injured

leg. Equal distribution o load between both legs

was ensured at the beginning o stretching by

asking the patient to apply hal their body weight

to each o two independent scales. Pelvis and

trunk orientation during stretching was moni-

tored by visual observation.

During stretching, ultrasonograms were

recorded every minute using an ultrasonic appa-

ratus (Power Vision 6000 SSA-370A; ToshibaMedical Systems Co., Japan) with an 8MHz linear

scanning probe (PLM-805AT; Toshiba Medical

Systems Co.). The amount o distal displacement

o each o the markers in the recorded images was

measured using ImageJ image analysis sotware

(NIH, USA). A probe xation rame made rom

an ethylene-vinyl acetate sponge was used during

ultrasonographic measurements to help maintain

the position o the probe. A given coordinate point

was precisely reproduced by using records o our

squares o the probe xation rame. A photograph

o an representative ultrasonographic measure-

ment is shown in Figure 3.

Methods

dgThe study was an observational clinical study

design. Using an ultrasonogram, the amount o

displacement o two markers in the DA and MTJduring stretching on a stretching board was meas-

ured in both the injured and uninjured legs o

each patient. The amount o distal displacement

o each o the markers refects the reaction o the

muscle-tendon unit to stretching.

ParpaTwenty emale patients (age 52.6 ± 12.2 years;

height, 154.6 ± 6.4 cm; weight 57.3 ± 4.6 kg;

(mean±SD)) were examined. All patients were

non-weight-bearing on one leg ollowing a unilat-

eral lower leg injury. Thirteen patients were diag-

nosed with a racture-dislocation o the ankle, and

seven with tibiobular ractures. All patients had

undergone surgical repair, but none had received

direct injury to the gastrocnemius muscle or

soleus muscles, or to the Achilles tendon.

All participants provided written inormed con-

sent ollowing study approval by the Institutional

Review Board o the authors’ hospital, in accord-

ance with the principles o the Declaration o

Helsinki. Anonymity and condentiality o the

patients were assured.

PrrDetermining markers in the medial head of

the gastrocnemius muscle

Two markers were identied in the gastrocnemius

muscle by ultrasonogram perormed in a stand-

ing position. The markers were the junction o

the ascicle and the DA at ¼ proximal height o

the lower leg and at the MTJ ( Figure 1). These

markers were careully chosen and conrmed to

show clear echoes.

Ultrasonographic measurements

Ultrasonographic measurements were perormed

ater medical approval was given or the patientto begin weight-bearing o more than hal o their

body weight on the injured limb. In a standing

position, the maximal ankle dorsifexion angle o

the patients’ injured leg was quickly measured on

a stretching board, using a reely adjustable angle

and an attached incline level meter (Niigata Seiki

Co., Japan; Figure 2).

In each experimental session, the maximal

ankle dorsifexion angle was determined as the

angle o tolerable submaximal stretching pain, or

the angle just beore the patients bent their knee.

Patients then stood or 10 minutes on the stretch-

ing board, which was set to the predetermined

proximal distal proximal distal

Figure 1. Determination o the markers. Markers were determined on ultrasonogram

(arrows). The let image shows the ascicle-deep aponeurosis junction (DA). The

right image shows the myotendinous junction (MTJ). DA was determined with high

brightness and a clearly depicted point in the junction o ascicle and deep aponeurosis

at 1/4 proximal height o the lower leg.

Figure 2. The stretching board with a reely adjustable

angle, and the level metre.




Research

Ultrasonographic measurements were repeated

every week, and were concluded when there was

no statistical laterality in the amount o displace-

ment o both markers ater stretching. One physi-

cal therapist blinded to the purpose and methods

o the study measured the displacement o the

markers in the ultrasonograms.

Calf circumference

Cal circumerence was measured using a bre-

glass tape measure at the point o maximum cal girth. One physical therapist blinded to the pur-

pose and methods o the study measured the cal

circumerence.

saa aayAll statistical tests were perormed in GraphPad

Prism 5.00 (GraphPad Sotware, La Jolla, CA).

Two-way analysis o variance or repeated meas-

ures (actors: injured leg, uninjured leg and time)

was used to compare the dierence in the amount

o displacement o DA and MTJ between the

uninjured and injured legs or every 1 minute

(a= 0.05). Upon detection o a signicant main

eect, paired t -tests were perormed to compare

the dierence between the uninjured and injured

legs. Bonerroni correction or multiple com-

parisons was applied, and the level o signii-

cance was set at 0.005. Paired t -tests were used

to assess the dierence in the amount o dis-

placement o DA and MTJ or every 1 minute

a=0.0011). Paired t -tests were used to detect sig-

nicant dierences in maximal ankle dorsifexion

angle and circumerences o the cal between the

rst and nal measurements (a=0.05). Data are

presented as means ± 1SD.

Figure 3. Ultrasonographic measurement. A probe xation

rame was used to acilitate the depiction o the markers.

proximal distal proximal distal

Figure 4. A case o shit o the markers beore and ater stretching. (a) The arrow shows a DA position in the standing

position. (b) The white arrow is a DA position ater stretching or 10 minutes. (c) The arrow shows a MTJ position in the

standing position. (d) The white arrow is a MTJ position ater stretching or 10 minutes.




Results

The average postoperative period beore approval

or partial weight-bearing (50% body weight) was

6.9 ± 2.4 weeks, at which time the maximal angle

o ankle dorsifexion in the injured leg improved rom 4.8 ± 3.8° at the beginning o measurements

to 18.8 ± 4.6° at the nal measurement ( P < 0.05).

There was no signiicant change in the maxi-

mal ankle dorsifexion angle in the uninjured leg

(23.5 ± 4.1° vs 24.3 ± 3.9°; P = 0.73).

At the beginning o measurements, maximal

cal circumerence was 1.8 ± 0.6cm smaller in the

injured leg than in the uninjured leg ( P = 0.023).

At the nal measurement, cal circumerence was

1.3 ± 0.7 cm lower in the injured leg than in the

uninjured leg ( P = 0.035) indicating muscle atro-

phy (Table 1). There was a signicant main eect

between uninjured and injured legs at the DA

( P< 0.05).

Signicant dierences in the amount o dis-

placement o DA or every 1 minute between

the uninjured and injured legs were ound dur-

ing the three minutes beore the nal measure-

ment ( P < 0.01). At the MTJ, a signicant main

eect between uninjured legs and injured legs

was ound ( P < 0.05), and there was a signicant

dierence in the amount o displacement o MTJ

between uninjured legs and injured legs or every

one minute, during the three minutes prior to

the nal measurement ( P < 0.01). No signicantinteractions between actors were ound or unin-

jured and injured legs. The amount o displace-

ment o the DA and MTJ at the rst and nal

measurements is shown in Table 2.

A typical case o DA and MTJ displace-

ments measured by ultrasonogram are shown in

Figure 4a, b and Figure 4c, d , respectively. The

overall average o DA displacement is shown in

Figure 5. The distal displacement o DA on the

injured side was larger than that on the unin-

jured side in irst measurement ( Figure 5a).

Subsequently, the distal displacement o DA on

the injured side gradually decreased towards thenal measurements ( Figure 5b, c). In the nal

measurement, the distal displacement o DA

became more similar to that o the uninjured

side ( Figure 5d ). During the entire measurement

period, DA displaced signicantly until three min-

utes beore the nal measurement, on both the

injured and uninjured sides ( P< 0.01). The aver-

age MTJ displacement is shown in Figure 6 . The

distal displacement o MTJ on the injured side

was smaller than that on the uninjured side in

the rst measurement ( Figure 6a). Subsequently,

the distal displacement o MTJ on the injured

side gradually increased towards the nal meas-

urements ( Figure 6b, c). In the nal measure-

ment, the distal displacement o MTJ became

increasingly similar to that o the uninjured side

( Figure 6d ). During the entire measurement

period, MTJ displaced signicantly until three

minutes beore the nal measurement on both

the injured and uninjured sides (P < 0.01). The

amount o the displacement o DA and MTJ did

not dier signicantly ater our minutes.

discussion

Ultrasonograms o the gastrocnemius muscle inhumans with a unilateral lower leg injury were

used to examine the reaction to static stretching

in the present study. The DA and the MTJ were

identied by the deep aponeurosis-ascicle junc-

tion and the myotendinous junction, respectively.

Previous histological studies have demonstrated

a high incidence o damage to the myotendi-

nous junction in muscle strain injuries (Garrett

et al, 1987; Nikolaou et al, 1987; Taylor et al,

1993; Noonan et al, 1994). Furthermore, detailed

observations revealed a deep aponeurosis-asci-

cle junction and/or supercial aponeurosis-as-

cicle junction in injured regions (Hughes et al,1995). These regions are easily injured and are

aected by changes in the state o the muscle-

tendinous tissue. As such, the authors considered

that these regions may be particularly responsive

to muscle stretching.

Tabl 1. Chag f th circumfrc f th calf

Circumfrc f th calf (cm)

Firt maurmt Fial maurmt

Uijurd lg (a) 32.2±3.2 32.5±3.1

Ijurd lg (b) 30.4±3.2 31.2±2.8

Latralit (a)-(b) -1.8±0.6 -1.3±0.7

Note:*P<0.05:signicantdierencebetweenguresjoinedbylines

Tabl 2. Amut f diplacmt f th DA ad MTJ durig 10 miut trtchig

DA (mm) MTJ (mm)

Firt maurmt Fial maurmt Firt maurmt Fial maurmt

Uijurd 5.4±0.9 5.7±0.9 16.1±1.4 15.8±1.2

Ijurd 9.7±2.6 5.6±1.1 4.8±2.0 15.1±1.2

Note:*P<0.05:signicantdierencebetweenguresjoinedbylines

**

* *



In this study, injured DA displacement was

greater than that in uninjured legs, ollowing 10

minutes o stretching, at the time o rst measure-

ment. In contrast, injured MTJ displacement was

smaller than that in uninjured legs at this time,

showing a reversed reaction to that seen in the

uninjured leg ( Figure 7 ). Following longer periodso recovery, the reaction o the injured leg became

closer to that o the uninjured leg. These ndings

may relate to changes in the mechanical character-

istics o the muscle–tendon complex.

Mechanical properties o human muscle and

tendon reported in the literature include tendon

stiness, tendon hysteresis and Young’s modulus

(Shorten, 1987; Fukashiro et al, 2001; Bennet et

al, 1986; Hubbard and Soutas-Little, 1984; Ker,

1981; Pollock and Shadwick, 1994; Maganaris and

Paul, 2002). Unloading can aect these properties,

as shown in animal models. Suspended rat tendons

had lower values or maximal stress and tangent


Research

modulus than tendons o control rats (Almeida-

Silveira et al, 2000). In addition, decreased sti-

ness o the suspended rat soleus muscle (Canon

and Goubel, 1995) has been reported. Eliasson

et al (2007) ound that the mechanical properties

most aected by unloading in the rat were hys-

teresis and creep, and both decreased with disusecompared with the control rat. Achilles tendon

suspension resulted in smaller surace area o col-

lagen bres (Nakagawa et al, 1989) and lower con-

centration o collagen (Vailas et al, 1988).

These actors could explain the mechanical

changes in the passive part o series elasticity

(Almeida-Silveira et al, 2000) and increased ten-

don compliance, which has been observed in dis-

use and ageing (Reeves et al, 2005; Narici, 2005).

These mechanical characteristic changes would

infuence the results o this study. However, the

authors were not able to identiy a specic actor

to explain the change observed in the patients.

D i s t a l d i s p l a c e m e n t (

m m )


m m )

Stretchingtime(min) Stretchingtime(min)

**

**

** **

****

**P <0.01

**

**

** **

****

a) Post-operation 6.9 ± 2.4 weeks (rst measurement)

Ankle dorsifexion angle: 4.8 ± 3.8°

b) Post-operation 8.1 ± 2.4 weeks


Figure 5. Total average o the distal displacement o the deep aponeurosis junction (DA). a) In the rst measurement, on the

injured side, the distal displacement o the DA was larger than the uninjured side. b) In the postoperation 8.1 weeks and c)

postoperation 10.7 weeks measurements, the distal displacement o DA on the injured side were gradually decreased, to the

nal measurements, d), where the distal displacement o DA became similar to that o the uninjured side. Over the whole o

the measurement period, DA displaced signicantly ( P< 00.1) until three minutes on both the injured and uninjured sides.

D i s t a l d i s p l a c e m e n t ( m m )



**

** **

**

**

**

**** **

****

c) Post-operation 10.7 ± 1.2 weeks Ankle dorsifexion angle: 13.6 ± 4.3°

d) Post-operation 12.7 ± 2.0 weeks (nal measurement) Ankle dorsifexion angle: 18.8 ± 4.6°

**



Laterality o injured cal circumerence was

observed. Skeletal muscle atrophy due to inac-

tivity has been investigated using experimental

animal models o hind limb suspension (Morey,

1979; Winiarski et al, 1987) and plaster cast xa-

tion (Cooper, 1972; Herbison et al, 1978). Those

studies suggested that shortening o the cross-sectional area and minimization o the muscular

bre (Desplanches et al, 1987; Hauschka et al,

1987), irregularity o the muscular bre sequence

(Winiarski et al, 1987; Desplanches et al, 1990),

and decreased tensile strength during muscle

contraction (McDonald et al, 1994) occurred in

the atrophic muscle. Hind limb suspension and

plaster cast ixation resulted in 40% and 42%

weight reduction in the rat gastrocnemius and

soleus muscles, respectively (Herbison et al,

1978; Morey, 1979). In addition, Herbison et al

(1979) observed injury to muscle cells ollowing

six weeks o a plaster cast xed to the hind leg o



m m )


m m )


a rat. Thus, the laterality o cal muscle circum-

erence in this study may refect muscle atrophy,

and greater lengthening o the muscle belly in the

injured leg may have been caused by decreased

tensile strength o the muscle.

Many authors consider that a muscle electro-

myogram (EMG) level must be lower than 1% o that during maximal voluntary contraction beore

considering that muscular contraction is negli-

gible (McNair et al, 2002; Gajdosik, 2006). The

authors did not measure the EMG o the gastroc-

nemius muscle at the period o unloading in the

present study. However, the 5.6% decrease in the

circumerence o the cal in the injured leg com-

pared with that in the uninjured leg, at the time

o the rst measurements, suggests the presence

o muscle atrophy.

Ultrasonographic measurements in the present

study showed that both markers were distally dis-

placed in both legs in the spontaneous standing

**P <0.01

**

a) Post-operation 6.9 ± 2.4 weeks (rst measurement)


b) Post-operation 8.1 ± 2.4 weeks


Figure 6. Total average o the distal displacement o the myotendinous junction (MTJ). (a) In the rst measurement, on the

injured side, the distal displacement o MTJ was smaller than uninjured side. (b) In the postoperation 8.1 weeks, and (c) in the

postoperation 10.7 weeks measurements, the distal displacement o MTJ on the injured side were gradually increased, to the

nal measurements d), the distal displacement o MTJ became increasingly similar to that o the uninjured side. Over the whole

o the measurement period, MTJ displaced signicantly until three minutes ( P< 0.01) on both the injured and uninjured sides.

**

******

**

**

**

** **

****




c) Post-operation 10.7 ± 1.2 weeks Ankle dorsifexion angle: 13.6 ± 4.3°

d) Post-operation 12.7 ± 2.0 weeks (nal measurement) Ankle dorsifexion angle: 18.8 ± 4.6°

****

****

**

**

**

**

** **

****




Research

position. The distal displacement o the MTJ at

0–1 minute o standing may be caused by the

outer-tendon elongation due to movement dis-tal to the calcaneus bone at the insertion o the

Achilles tendon. Elongation o the muscle asci-

cle and supercial aponeurosis located proximal

o the DA may lead to simultaneous distal dis-

placement o the DA.

The authors have previously observed only

minor displacement o the supercial aponeurosis

during the stretching to the gastrocnemius mus-

cle in the knee extended position (Kanazawa et al,

2007). Thus, the distal displacement o the DA in

the present study may be caused by muscle ascicle

elongation. Furthermore, the distal displacement o

the MTJ observed ater one minute indicated short-ening o the outer-tendon. As distal displacement o

the DA occurred at the same time, a muscle asci-

cle may have been more extended. The authors also

observed that the outer-tendon was extended rap-

idly by stretching, and the outer-tendon length then

gradually returned and reached a plateau. Similarly,

muscle tissues were extended rapidly by stretching,

urther extended up to three minutes and then mus-

cle ascicle length reached a plateau.

Ultrasonograms have been used previously to

examine extension o the muscle-tendon unit. For

instance, Herbert et al (2002) demonstrated that the

gastrocnemius muscle ascicles lengthened one-

quarter o the lengthening o their muscle-tendon

unit during stretching. In resting muscles, much

o the increase in muscle-tendon length during

stretching occurred in the tendon, while the muscle

ascicles appeared to contribute little to the total

changes in muscle-tendon length. On the other hand, Kubo et al (2005) demonstrated that although

the muscle ascicle, tendon, and aponeurosis were

stretched by 21.8 ± 2.9 mm, 22.9 ± 3.0 mm, and

5.2 ± 2.5 mm, respectively, during passive dorsifex-

ion, there was no dierence between elongations o

the muscle ascicle and tendon.

More recently, Morse et al (2008) reported

that the muscle-tendon unit length increased by

21.9 mm during stretching, and that the muscle

ascicles changed length in a very similar man-

ner to the change in MTJ. Thus, in that study,

the increase in length o the muscle was entirely

accounted or by the change in length o the mus-

cle ascicles, and they concluded that pre-con-

ditioning o the muscle-tendon unit extension

occurs nearly equally by the tendon and muscle

ascicles. In the present study, the authors did

not measure the actual muscle length or calculate

the values or the tendon and muscle ascicles.

However, it was possible to determine internal

changes by displacement o DA and MTJ.

In the injured leg, distal displacement o the

DA was larger, and displacement o the MTJ

was smaller, than those in the uninjured leg. We

suggest that large distal displacement o the DAmainly relates to muscle ascicle elongation,

while the small distal displacement o the MTJ

relates to outer-tendon elongation. Thus, the

deep aponeurosis located between MTJ and DA

appears to stretch less in the injured leg than the

uninjured leg suggesting a change in the mechan-

ical characteristics o the deep aponeurosis.

The present study showed that the laterality o

the DA and MTJ did not resolve until 12.7 ± 2.0

weeks ater surgery. Thus, rehabilitation during

this period should be perormed careully. We

suggest that extensibility o the deep aponeuro-

sis, thermotherapy, and/or massotherapy may beeective treatments. Ater this period, the reaction

o the muscle-tendon unit to stretching returns to

normal, and as such, concentrated rehabilitation

can be perormed eectively. Future studies are

required to investigate an eective method or

treatment o damaged muscles and tendons.

conclusions

The results o the present study indicate that an

injured leg exhibits an opposite reaction to an

uninjured leg with respect to DA and MTJ dis-

placement during eight weeks o postoperative

MTJ

DA

a)

b)

c)

Figure 7. Schematic diagram showing the distal displacement o the deep aponeurosis

(DA) and o the myotendinous junction (MTJ). a) A location o DA and MTJ in the

spontaneous standing position. The bold arrow shows DA and MTJ. b) The distal

displacement o the DA and MTJ in the uninjured leg. The arrow shows an approximate

distal displacement. c) The distal displacement o the DA and the MTJ in the injured leg.




n Thereactiontostretchingoanunhealthymuscle-tendonunitislargelyunknown.

n Theaimothestudywastoinvestigatethereactionothemuscle-tendon

unittostretchingateraperiodonon-weight-bearingbyultrasonograms.

n Atalltimepoints,thejunctionotheascicleandthedeepaponeurosis

(DA)andthemyotendinousjunction(MTJ)displaceddistallyduringthefrst

threeminutesostretchinginbothlegs( P <0.01).

n InjuredDAdisplacementwasinitiallygreaterthanthatintheuninjuredleg

andinjuredMTJdisplacementwassmallerthanthatintheuninjuredleg.

n Atertreatment,DAandMTJdisplacementsintheinjuredlegapproached

levelssimilartothatotheuninjuredleg.

n Followinganinjury,asciclesandtendonmayhavebeenexcessivelyextended.

n Recoveryothemuscletendoncomplexmightbeacceleratedbyapplying

exercisesaimedatattainingincreasedextensibilityotheaponeurotictissue.

Key PoInTsrecovery rom a unilateral lower leg injury. The

large distal displacement o the DA suggests

muscle ascicle elongation, while the small dis-

tal displacement o the MTJ suggests outer-ten-

don elongation. There was less elongation o the

deep aponeurosis located between the DA and MTJ. Thereore, normalization o the muscle ten-

don complex might be accelerated by attaining

increased extensibility o the aponeurotic tissue

during the treatment period. IJTR

Conlict o interest: none Acknowledgements: The authors acknowledge the sta at the Department o Rehabilitation, Matterhorn Rehabilitation

Hospital or their help with the data collection. The authorsalso acknowledge the students at the Graduate School o

Health Sciences, Hiroshima University or their continuous support with this project.

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Canon F, Goubel F (1995) Changes in stiness induced byhind limb suspension in rat soleus muscle. Pfugers Arch429(3):332–7

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Herbert RD, Moseley AM, Butler JE, Gandevia SC (2002)Change in length o relaxed muscle ascicles and ten-

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Morse CI, Degens H, Seynnes OR, Maganaris CN, Jones DA(2008) The acute eect o stretching on the passive sti-ness o the human gastrocnemius muscle tendon unit. J

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Taylor DC, Dalton JD, Seaber AV, Gar rett WE (1990)Viscoelastic properties o muscle-tendon units. The biome-chanical eects o stretching. Am J Sports Med 18(3): 300–9

Taylor DC, Dalton JD Jr, Seaber AV, Garrett WE Jr (1993)Experimental muscle strain injury. Early unctional and structural decits and the increased risk or reinjury. Am J Sports Med 21(2): 190–4

Vailas AC, Duluna DM, Lewis LL, Curwin SL, Roy RR, Alord EK (1988) Adaptation o bone and tendon to prolonged hindlimb suspension in rats. J Appl Physiol 65(1): 373–6

Wilson GJ, Wood GA, Elliott BC (1991) The relationship between stiness o the musculature and static fexibility:an alternative explanation or the occurrence o muscular injury. Int J Sports Med 12(4): 403–7

Winiarski AM, Roy RR, Alord EK, Chiang PC, Edgerton VR (1987) Mechanical properties o rat skeletal muscle ater hind limb suspension. Exp Neurol 96(3): 650–60

Witvrouw E, Mahieu N, Danneels L, McNair P (2004)Stretching and injury prevention: an obscure relationship.

Sports Med 34(7): 443–9Ylinen J (2008) Stretching Therapy. Elsevier, Philadelphia




Research

Stretching exercises are com-

monly undertaken or sports

and rehabilitation proceduresater injury. The displacement

in the muscle-tendon unit o

the hum an gas trocne mius

muscleduringstaticstretching,

ater a period o non-weight-

bearing ollowing injury, is o

importanceinbothsportsand

and stroke injuries.In physical

therapy,stretchingisoneothe

mosteectivetechniquesused

orlengtheningshortenedmus-

cles,andimprovementojoint

rangeomotion.Inthistypeo

clinicalsetting,anunderstand-ing o optimal stretching time

isessential.

Herbertetal(2002)measured

changesinthelengthomuscle

ascicles in a relaxed human

gastrocnemius muscle during

passively imposed changes in

joint angle. Kubo et al (2005)

showed that while the muscle

ascicles,tendonandaponeuro-

sisstretchedduringpassivedor-

sifexion othe anklejoint, the

elongation o the tendon was

signicantly greater than thatotheaponeurosis.Meanwhile,

the stretching reaction o an

unhealthy muscle-tendon unit,

such as in muscle injuries,

including musclestrain, muscle

tendonatrophy,orunloading,is

o high clinical signicance but

largelyunknown.

Inthisstudy,ultrasonograph-

ic measurementso equal dis-

tributionoloadbetweenboth

legs were made, with equal

distributionatthebeginningo

stretchingensuredbyaskingthe

patienttoapplyhaltheirbody

weight to each o two inde-

pendentscales.Ultrasonograms

were recorded every minute,

usinganultrasonicimagingsys-

tem. Corresponding distal dis-

placementmeasurementswere

carried out using the image

analysissotware.

Thendings rom theultra-

sonic imaging quantitative

study included a signicant

maineectbetweenuninjured

and injured legs at the deep

aponeurosisjunction(DA),and

signicant dierences in theamountodisplacementoDA.

At the myotendinous junction

(MTJ),asignicantmaineect

between uninjured legs and

injuredlegswasalsoound.No

signicantinteractionsbetween

actors were ound or unin-

juredandinjuredlegs.

Further, the distal displace-

mentoDAontheinjuredside

gradually decreased towards

the nal measurements and

nally, the distal displacement

o DA became more similarto that o the uninjured side.

ThedistaldisplacementoMTJ

on the injured side gradually

increased towards the nal

measurements and lastly, the

distal displacement o MTJ

became increasingly similar

to that o the uninjured side.

Thus, the nal outcome ater

treatment was DA and MTJ

displacements in the injured

leg approached levels o the

uninjured leg. These ndings

may relate to changes in themechanical characteristics o

themuscle–tendoncomplex.

Earlierstudiessuggestedthat

shorteningothecross-section-

alareaandminimizationothe

muscularbre(Desplancheset

al,1987;Hauschkaetal,1987),

irregularity o the muscular

bresequence(Winiarskietal,

1987;Desplanchesetal,1990),

anddecreased tensilestrength

during m us cle contraction

(McDonaldet al,1994) occurs

in the atrophic muscle. More

recently, Morse et al (2008)

reported that the muscle-ten-

don unit length increased by

21.9mm during stretching,

and that the muscle ascicles

changedlengthinaverysimi-

lar manner to the change in

MTJ.Inthisstudy,theauthors

wereabletodetermineinternal

changesbydisplacementoDA

andMTJ.

In the injured leg, dis tal

displacement o the DA was

larger,anddisplacementothe

MTJ was smaller, than those

in the uninjured leg. It wassuggestedthatlargedistaldis-

placement o the DA mainly

relatestomuscleascicleelon-

gation, while the small distal

displacementotheMTJrelates

to outer-tendon elongation.

Thus, the deep aponeurosis

located between MTJ and DA

appears to stretch less in the

injured leg thanthe uninjured

leg, suggesting a change in

the mechanical characteristics

othedeepaponeurosis.

Hence, rehabilitation dur-ing this peri od should be

perormed very careully. The

authorssuggestextensibilityo

thedeepaponeurosis,thermo-

therapy, and/or massotherapy

as eective treatments. Ater

thisperiod,thereactionothe

muscle-tendonunit to stretch-

ing returns to normal. The

authors o this study suggest

uture studies are required to

investigateaneectivemethod

ortreatmentodamagedmus-

clesandtendons.Earlierliteraturerevealsthata

muscle electromyogram(EMG)

levelmustbelowerthan1%o

that during maximal voluntary

contractionbeore considering

that muscular contraction as

negligible(McNairetal,2002;

Gajdosik,2006).Theauthorsin

thisstudydidnotmeasurethe

EMGothemuscleattheperi-

odounloading.Itisproposed

thaturther studyshould look

attheEMGinthesemuscles,as

there may be muscle atrophy.

There is 5.6%decrease in the

circumerences o the cal in

theinjuredleg comparedwith

thatintheuninjuredlegatthe

timeotherstmeasurements

– suggesting the presence o

muscleatrophy.

The results o the present

study indicate that an injured

leg, ater postoperative recov-

ery rom a leg injury, exhib-

its an oppositereaction to an

uninjured leg with respect to

DA and MTJ displacement.

Normalization o the muscle

tendoncomplexmightacceler-atebyattainingincreasedexten-

sibilityotheaponeurotictissue

during the treatment period.

Theproceduralndingsothe

present study would help in

postoperativecareduringreha-

bilitation, something o great

importancetothepatient.

Desplanches D, Mayet MH, Sempore B,Flandrois R (1987) Structural and func-tional responses to prolonged hindlimbsuspension in rat muscle. J Appl Physiol

63(2): 558–63

Desplanches D, Kayar SR, Sempore B,Flandrois R, Hoppeler H (1990) Rat soleusmuscle ultrastructure after hindlimb sus-pension. J Appl Physiol 69(2): 504–08

Gajdosik RL (2006) Influence of a low-levelcontractile response from the soleus, gas-trocnemius and tibialis anterior muscleson viscoelastic stress-relaxation of agedhuman calf muscle-tendon units. Eur J

Appl Physiol 96(4): 379–88

Hauschka EO, Roy RR, Edgerton VR (1987)Size and metabolic properties of singlemuscle fibers in rat soleus after hind-limb suspension. J Appl Physiol 62(6):2338–47

Herbert RD, Moseley AM, Butler JE, GandeviaSC (2002) Change in length of relaxedmuscle fascicles and tendons with knee

and ankle movement in humans. J Physiol 539(Pt 2): 637–45

Kubo K, Kanehisa H, Fukunaga T (2005)Effect of clod and hot water immersionon the mechanical properties of humanmuscle and tendon in vivo. Clin Biomech 20(3): 291–300

McDonald KS, Blaser CA, Fitts RH (1994)Force-Velocity and power character-istics of rat soleus muscle fibers afterhindlimb suspension. J Appl Physiol

77(4): 1609–16

McNair PJ, Hewson DJ, Dombroski E, StanleySN (2002) Stiffness and passive peakforce changes at the ankle joint: theeffect of different joint angular velocities.Clin Biomech 17(7): 536–40

Morse CI, Degens H, Seynnes OR, Maganaris

CN, Jones DA (2008) The acute effect ofstretching on the passive stiffness of thehuman gastrocnemius muscle tendonunit. J Physiol 586(1): 97–106

Winiarski AM, Roy RR, Alford EK, Chiang PC,Edgerton VR (1987) Mechanical proper-ties of rat skeletal muscle after hind limbsuspension. Exp Neurol 96(3): 650–60

Manjunatha Mahadevappa, PhD Assistant Proessor,School o Medical Science and Technology,Indian Institute o Technology Kharagpur, [email protected]

COMMENTARIES




This article represents a unique

andinterestingstudythatexam-

ined the muscle-tendon unit’s

responses to static stretching

using an ultrasound imaging

device in the injured and uninjured legs o 20 women. The

authors should be commended

ortheireortstoinvestigatethe

pragmaticuseostaticstretching

orthepurposesorehabilitation.

The majority o research

related to stretching is most

oten ocused on perormance

and mechanistic approaches.

Much less isknown about the

applicationostretchinginreha-

bilitation settings. Thereore,

the present study supports

the hypothesis that stretchingan injured limb can improve

the range o motion to that

demonstratedby the uninjured

limb,whichurtherimpliesthat

stretchingis an important part

o the postoperative rehabilita-

tion programme. Furthermore,

the authors suggested that

the improved range o motion

mayberelatedtoanincreased

extensibilityotheaponeuroses.

Thus, stretching may infuence

the noncontractile, rather than

the contractile elements o themusculotendinousunit.

Thesendingsare consistent

with those o previous studies

(Morseetal,2008;Ryanetal,

2009)thathavesuggestedthat

theelongationothemusculo-

tendinousunitmaybeexplained

by viscoelastic changes in the

perimysium,whichisstructurally

andphysiologicallysimilartothe

aponeuroses described in the

presentstudy.

The undamental question

stillremains,however,regarding

theacuteviscoelasticchangesvs

stretch tolerance increases. For

instance, stretching has been

shown to decrease musculo-

tendinous stiness (Ryan et al,

2008; 2009) which is usually

causedbychangesinviscoelastic

propertiesothemusculotendi-

nous unit. Conversely, stretch-

ing may just cause a transient

increaseinstretchtolerance,not

necessarily muscle extensibility

(BenandHarvey,2009).

Thedierencebetweenthese

two responses may be due to

the duration o the stretch-

ing protocol. Presumably, it is

the viscoelastic alterations and

decreases in musculotendinousstinessthataredesirableeects

ostretchingsoastoelicitpro-

gressive increases in range o

motion and perhaps (although

this is debatable) decrease the

risk o injury. Nevertheless, an

increaseinstretchtolerancecan

alsobeapositiveoutcomerom

stretchingconsideringthatthere

is a plausible analgesic eect

which refects less pain dur-

ing stretching (Malliaropoulos

etal,2004).Thus,urtherstud-

iesareneededinclinicalpopu-lations to help answer these

undamentalquestions.

Acute stretching-induced

orce decits (Shrier, 2004;

Rubini et al, 2007) must also

beacknowledgedashavingthe

potential to transiently weaken

the stretched muscles – even

duringrehabilitation.Thepresent

study examined the range o

motionotheinjuredvsnonin-

jured limbs as outcome meas-

ures to assess the eectiveness

otherehabilitationstretching.However, strength assess-

m ents are also requently

conducted in order to assess

muscle imbalances and the

progress o the rehabilitation

programme. For example, a

common assessment used to

assess the risk o thigh muscle

strain injuries, track rehabilita-

tionprogress,anddecidewhen

athletescanreturntoplayisthe

hamstrings-to-quadriceps (H:Q)

ratio.Previousstudiesromour

laboratory have indicated that

anacuteboutostretchingmay

aecttheH:Qratio(Costaetal,

2009a; 2009b). We previously

suggestedthatcliniciansshould

use caution when interpreting

the H:Q ratio i this test was

perormed immediately ater

stretching (Costa et al,2009a).

Thus, attention must be given

astowhenthestretchingproto-

colisperormedduringareha-

bilitation session. Conversely,

although acute stretching has

been consistently shown to

decreasestrength(Shrier,2004;

Rubinietal,2007),thesendings

needtobeplacedinthecontext

o a comprehensive rehabilita-

tion programme. For example,Marek et al (2005) suggested

thatintheearlystagesoreha-

bilitation,when thereis a clear

benetoregainingaunctional

rangeo motion, smallstretch-

ing-induced strength decits

maynotbeclinicallyrelevant.

However, as the rehabilita-

tion programme progresses,

care must be taken and clini-

cians should beawareo these

stretching-inducedstrengthde-

cits when conducting strength

assessments immediately aterstretchingontheirpatients,par-

ticularly i the results o these

testsaretobeusedormaking

decisionsregardingrehabilitation

progressorthereturntoplayor

athletes(Mareketal,2005).

Asshowninthisstudy,dier-

encesbetweenthe injured and

non-injured side only resolved

aternearly 13weeks otreat-

ment.Thereore,weagreewith

the authors that extreme care

mustbetakenduringtheperiod

whereinjury-relatedbilateraldi-erencesarestillsignicant.

Future well-controlled stud-

iesshouldocusonthechronic

eectsostaticstretchingduring

a rehabilitation programme on

injuredlimbsinordertoprovide

urther support or the recom-

mendation o stretching during

post-injuryrehabilitation.Finally,

specic rehabilitation guidelines

concerning the type o stretch-

ing regimen, stretch volume,

duration,andrequencyhaveyet

tobeestablished,andthesemay

infuenceordeterminetheeec-

tivenessostretchingasareha-

bilitationtool(Malliaropouloset

al,2004).

Collectively,evidenceisbuild-

ing to suggest that stretching

mayindeedbeanecessaryreha-

bilitation component or recov-

eryollowingamusculoskeletal

injury, as long as precautions

are taken regarding when the

stretching protocol takes place

within a rehabilitation session,

particularlywhen strength test-

ing may also occur during the

samesession.

Furthermore , a ddit iona l

researchisneededtodelineate

thetype,duration,andintensityo stretching necessary to elicit

changes in musculotendinous

stinessandviscoelasticchang-

esasopposedtomereincreases

instretchtolerance.

Ben M, Harvey LA (2010) Regular stretchdoes not increase muscle extensibility: arandomized controlled trial. Scand J Med

Sci Sports 20(1): 136–44

Costa PB, Ryan ED, Herda TJ, Defreitas JM,Beck TW, Cramer JT (2009a) Effects ofstatic stretching on the hamstrings-to-quadriceps ratio and electromyographicamplitude in men. J Sports Med Phys

Fitness 49(4): 401–09Costa PB, Ryan ED, Herda TJ, DeFreitas JM,

Beck TW, Cramer JT (2009b) Effects ofstretching on peak torque and the H:Qratio. Int J Sports Med 30(1): 60–5

Malliaropoulos N, Papalexandris S, PapaladaA, Papacostas E (2004) The role ofstretching in rehabilitation of hamstringinjuries: 80 athletes follow-up. Med Sci

Sports Exerc 36(5): 756–59

Marek SM, Cramer JT, Fincher AL et al (2005)Acute effects of static and proprioceptiveneuromuscular facilitation stretching onmuscle strength and power output. J Athl

Train 40(2): 94–103

Morse CI, Degens H, Seynnes OR, MaganarisCN, Jones DA (2008) The acute effect of

stretching on the passive stiffness of thehuman gastrocnemius muscle tendonunit. J Physiol 586(1): 97–106

Rubini EC, Costa AL, Gomes PS (2007) Theeffects of stretching on strength perform-ance. Sports Med 37(3): 213–24

Ryan ED, Beck TW, Herda TJ et al (2008) Thetime course of musculotendinous stiffnessresponses following different durations ofpassive stretching. J Orthop Sports Phys

Ther 38: 632–9

Ryan ED, Herda TJ, Costa PB, Defreitas JM,Beck TW, Stout J, Cramer JT (2009)Determining the minimum number ofpassive stretches necessary to alter musc-ulotendinous stiffness. J Sports Sci 27(9):957–61

Shrier I (2004) Does stretching improveperformance? A systematic and criticalreview of the literature. Clin J Sport Med 14(5): 267–73

Pablo B. CostaDoctoral Research Assistant;

Joel T. Cramer Assistant Proessor,Biophysics Laboratory,Department o Health and Exercise Science,University o Oklahoma,Oklahoma, USA

[email protected]



The challenge o sot tissue

stretching to alleviate pain,

to increase range o motion,

and to decrease the stiness

and the thixotropicproperties

o the whole unit ollowing

injury,isundamentalandcen-

tralorphysiotherapypractice,

andmustbesolvedinorderto

choose the best intervention

programmeorpatients.Since

theirstroleingoodpracticeis

‘donot harm’, twoquestions

that requently come up and

we struggle with are: ‘should

we stretch by any means?’,

and‘howmuchistoomuch?’.

Eventhoughtheconclusiono

thisarticlewasconvincinglyin

support o stretching, it lacks‘scientiic humility’ and some

degreeoprudence.

Applyingstretchingisalways

controversial among praction-

ers.Onemayask:‘whybother

with stretching?’. Previous

studies have indicated that

during passive stretching o

the gastrocnemius muscle,

only a small percentage (less

th an 2 5% ) o th e ov eral l

length(i.e.,theasciclelength-

ens,andconsequentlytheten-

don) change,and these small

changes are not maintained

minutesater the intervention

ceases. On the other hand,

some believethat recovery o

the muscle tendon complex

mightbeacceleratedbyapply-

ingstretching.

Themuscletendonregionisa

complexunit,bothanatomically

and biomechanically, and one

mustalwaysabolishthepoten-

tial or urther muscle-tendon

injuriesduringastretch.

Themyotendinousunitplays

animportantroleinorcetrans-missionrom myobrilsacross

themusclecellmembrane,to

the extracellular matrix, and

thantothetendon.Themag-

nitude o the orce transmit-

ted rom muscle to tendon

is directly infuenced by the

unique, complex and ragile,

structureothisunit.

As well-described by many

investigators, during stretch-

ing, a) the quiescent/inactive

brocytes in the myo-tendon

region are replaced by acti-

vated broblasts; b) there is

anincreaseinbasementmem-

branes in the myo side; and

c)thereisenlargementothe

rough sarcoplasmic reticulum.

The basement membrane is

modied by the presence o

caveolae and vacuoles, and

at the tendon side, the col-

lagen bundles are disrupted,

resulting in the ormation o

disorientedbres.

These apparently adaptive

changes to stretching are a

non-infammatory reaction othemyo-tendonregion,charac-

terizedby intensivemembrane

renewal and recycling. Yet,

rom the mechanical point o

viewthis local response might

permanentlyweakenthemyo-

tendon resistance to stretch,

and result in intererence or

obstruction o the electrome-

chanicaldelay, in terms o the

extent o myotendon complex

loose.So,inalongrunwemay

losemorethanwegain.

As long as a denite and

explicitanswerdoesnotexist,

w he n p re sc ri bi ng s tr et ch

exercises to our patients, it

is important to use cautious

steps. These should consider

severalactors: intensity: how

intense should the stretch be

–isitpain-ree;duration:how

longshouldthestretchbeheld

(slowandprolongedupto20

seconds); and requency: how

otenshouldoneperormthe

stretch(5–6timesperweek).

Dr Eli Carmeli Proessor,Physical Therapy Department,Sackler Faculty o Medicine,Stanley Steyer School o HealthProessions,Tel Aviv University,Israel [email protected]

Karina McGann

Text takes a holistic approach to

the assessment and management of

pain and its multi-dimensional nature

Includes pharmacological and

non-pharmacological approaches

Patient-centred and evidence based

essential text on the management

of painISBN-13: 978-1-85642-292-5;

234 x 156 mm; paperback; 176 pages;

publication January 2007; £19.99

To claim your discount call

01722 716 935and quote code: QBJA Offer expires 30 April 2010

To find out more about Quay books titles visit www.quaybooks.co.uk

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