Abstract

The study was conducted to define the biomechanical response of rat Achilles tendon after a single bout of exercise and a short or long duration of daily exercise. We hypothesized that a single bout or a short duration of exercise would cause a transient decrease in Achilles tendon mechanical properties and a long duration of daily exercise would improve these properties. One hundred and thirty-six Sprague-Dawley rats were divided into cage activity (CA) or exercise (EX) groups for a single bout, short-term, or long-term exercise. Animals in single bout EX groups were euthanized, 3, 12, 24, or 48 h upon completion of a single bout of exercise (10 m/min, 1 h) on a flat treadmill. Animals in short-term EX groups ran on a flat treadmill for 3 days, 1, or 2 weeks while animals in long-term EX groups ran for 8 weeks. Tendon quasi-static and viscoelastic response was evaluated for all Achilles tendons. A single bout of exercise increased tendon stiffness after 48 h of recovery. Short-term exercise up to 1 week decreased cross-sectional area, stiffness, modulus, and dynamic modulus of the Achilles tendon. In contrast, 8 weeks of daily exercise increased stiffness, modulus, and dynamic modulus of the tendon. This study highlights the response of Achilles tendons to single and sustained bouts of exercise. Adequate time intervals are important to allow for tendon adaptations when initiating a new training regimen and overall beneficial effects to the Achilles tendon.

References

1.
Rooney
,
S. I.
,
Torino
,
D. J.
,
Baskin
,
R.
,
Vafa
,
R. P.
,
Kuntz
,
A. F.
, and
Soslowsky
,
L. J.
,
2017
, “
Rat Supraspinatus Tendon Responds Acutely and Chronically to Exercise
,”
J. Appl. Physiol. (1985)
, 123(4): pp.
757
763
.10.1152/japplphysiol.00368.2017
2.
Foure
,
A.
,
Nordez
,
A.
, and
Cornu
,
C.
,
2010
, “
Plyometric Training Effects on Achilles Tendon Stiffness and Dissipative Properties
,”
J. Appl. Physiol. (1985)
,
109
(
3
), pp.
849
854
.10.1152/japplphysiol.01150.2009
3.
Heinemeier
,
K. M.
,
Skovgaard
,
D.
,
Bayer
,
M. L.
,
Qvortrup
,
K.
,
Kjaer
,
A.
,
Kjaer
,
M.
,
Magnusson
,
S. P.
, and
Kongsgaard
,
M.
,
2012
, “
Uphill Running Improves Rat Achilles Tendon Tissue Mechanical Properties and Alters Gene Expression Without Inducing Pathological Changes
,”
J. Appl. Physiol. (1985)
,
113
(
5
), pp.
827
836
.10.1152/japplphysiol.00401.2012
4.
Maffulli
,
N.
,
Khan
,
K. M.
, and
Puddu
,
G.
,
1998
, “
Overuse Tendon Conditions: Time to Change a Confusing Terminology
,”
Arthroscopy
,
14
(
8
), pp.
840
843
.10.1016/S0749-8063(98)70021-0
5.
Khan
,
K.
, and
Cook
,
J.
,
2003
, “
The Painful Nonruptured Tendon: Clinical Aspects
,”
Clin. Sports Med.
,
22
(
4
), pp.
711
725
.10.1016/S0278-5919(03)00035-8
6.
Lorimer
,
A. V.
, and
Hume
,
P. A.
,
2014
, “
Achilles Tendon Injury Risk Factors Associated With Running
,”
Sports Med.
,
44
(
10
), pp.
1459
1472
.10.1007/s40279-014-0209-3
7.
Lopes
,
A. D.
,
Hespanhol
,
L. C.
,
Yeung
,
S. S.
, and
Costa
,
L. O. P.
,
2012
, “
What Are the Main Running-Related Musculoskeletal Injuries? A Systematic Review
,”
Sports Med.
,
42
(
10
), pp.
891
905
.10.1007/BF03262301
8.
Vleck
,
V. E.
, and
Garbutt
,
G.
,
1998
, “
Injury and Training Characteristics of Male Elite, Development Squad, and Club Triathletes
,”
Int. J. Sports Med.
,
19
(
01
), pp.
38
42
.10.1055/s-2007-971877
9.
Huttunen
,
T. T.
,
Kannus
,
P.
,
Rolf
,
C.
,
Fellander-Tsai
,
L.
, and
Mattila
,
V. M.
,
2014
, “
Acute Achilles Tendon Ruptures: Incidence of Injury and Surgery in Sweden Between 2001 and 2012
,”
Am. J. Sports Med.
,
42
(
10
), pp.
2419
2423
.10.1177/0363546514540599
10.
Epro
,
G.
,
Mierau
,
A.
,
Doerner
,
J.
,
Luetkens
,
J. A.
,
Scheef
,
L.
,
Kukuk
,
G. M.
,
Boecker
,
H.
,
Maganaris
,
C. N.
,
Bruggemann
,
G. P.
, and
Karamanidis
,
K.
,
2017
, “
The Achilles Tendon is Mechanosensitive in Older Adults: Adaptations Following 14 Weeks Versus 1.5 Years of Cyclic Strain Exercise
,”
J. Exp. Biol.
,
220
(
6
), pp.
1008
1018
.10.1242/jeb.146407
11.
Beyer
,
R.
,
Kongsgaard
,
M.
,
Hougs Kjær
,
B.
,
Øhlenschlæger
,
T.
,
Kjær
,
M.
, and
Magnusson
,
S. P.
,
2015
, “
Heavy Slow Resistance Versus Eccentric Training as Treatment for Achilles Tendinopathy: A Randomized Controlled Trial
,”
Am. J. Sports Med.
,
43
(
7
), pp.
1704
1711
.10.1177/0363546515584760
12.
Obst
,
S. J.
,
Barrett
,
R. S.
, and
Newsham-West
,
R.
,
2013
, “
Immediate Effect of Exercise on Achilles Tendon Properties: Systematic Review
,”
Med. Sci. Sports Exercise
,
45
(
8
), pp.
1534
1544
.10.1249/MSS.0b013e318289d821
13.
Visnes
,
H.
,
Hoksrud
,
A.
,
Cook
,
J.
, and
Bahr
,
R.
,
2005
, “
No Effect of Eccentric Training on Jumper's Knee in Volleyball Players During the Competitive Season: A Randomized Clinical Trial
,”
Clin. J. Sport Med.
,
15
(
4
), pp.
227
234
.10.1097/01.jsm.0000168073.82121.20
14.
van der Plas
,
A.
,
de Jonge
,
S.
,
de Vos
,
R. J.
,
van der Heide
,
H. J.
,
Verhaar
,
J. A.
,
Weir
,
A.
, and
Tol
,
J. L.
,
2012
, “
A 5-Year Follow-Up Study of Alfredson's Heel-Drop Exercise Programme in Chronic Midportion Achilles Tendinopathy
,”
Br. J. Sports Med.
,
46
(
3
), pp.
214
218
.10.1136/bjsports-2011-090035
15.
Woodley
,
B. L.
,
Newsham-West
,
R. J.
,
Baxter
,
G. D.
,
Kjaer
,
M.
, and
Koehle
,
M. S.
,
2007
, “
Chronic Tendinopathy: Effectiveness of Eccentric Exercise
,”
Br. J. Sports Med.
,
41
(
4
), pp.
188
198
.10.1136/bjsm.2006.029769
16.
Heinemeier
,
K. M.
,
Olesen
,
J. L.
,
Haddad
,
F.
,
Langberg
,
H.
,
Kjaer
,
M.
,
Baldwin
,
K. M.
, and
Schjerling
,
P.
,
2007
, “
Expression of Collagen and Related Growth Factors in Rat Tendon and Skeletal Muscle in Response to Specific Contraction Types
,”
J. Physiol.
,
582
(
3
), pp.
1303
1316
.10.1113/jphysiol.2007.127639
17.
Rooney
,
S. I.
,
Baskin
,
R.
,
Torino
,
D. J.
,
Vafa
,
R. P.
,
Khandekar
,
P. S.
,
Kuntz
,
A. F.
, and
Soslowsky
,
L. J.
,
2016
, “
Ibuprofen Differentially Affects Supraspinatus Muscle and Tendon Adaptations to Exercise in a Rat Model
,”
Am. J. Sports Med.
,
44
(
9
), pp.
2237
2245
.10.1177/0363546516646377
18.
Rooney
,
S. I.
,
Loro
,
E.
,
Sarver
,
J. J.
,
Peltz
,
C. D.
,
Hast
,
M. W.
,
Tseng
,
W. J.
,
Kuntz
,
A. F.
,
Liu
,
X. S.
,
Khurana
,
T. S.
, and
Soslowsky
,
L. J.
,
2019
, “
Exercise Protocol Induces Muscle, Tendon, and Bone Adaptations in the Rat Shoulder
,”
Muscles Ligaments Tendons J.
,
04
(
04
), pp.
413
419
.10.32098/mltj.04.2014.04
19.
Favata
,
M.
,
Beredjiklian
,
P. K.
,
Zgonis
,
M. H.
,
Beason
,
D. P.
,
Crombleholme
,
T. M.
,
Jawad
,
A. F.
, and
Soslowsky
,
L. J.
,
2006
, “
Regenerative Properties of Fetal Sheep Tendon Are Not Adversely Affected by Transplantation Into an Adult Environment
,”
J. Orthop. Res.
,
24
(
11
), pp.
2124
2132
.10.1002/jor.20271
20.
Peltz
,
C. D.
,
Perry
,
S. M.
,
Getz
,
C. L.
, and
Soslowsky
,
L. J.
,
2009
, “
Mechanical Properties of the Long-Head of the Biceps Tendon Are Altered in the Presence of Rotator Cuff Tears in a Rat Model
,”
J. Orthop. Res.
,
27
(
3
), pp.
416
420
.10.1002/jor.20770
21.
Galloway
,
M. T.
,
Lalley
,
A. L.
, and
Shearn
,
J. T.
,
2013
, “
The Role of Mechanical Loading in Tendon Development, Maintenance, Injury, and Repair
,”
J. Bone Jt. Surg. Am.
,
95
(
17
), pp.
1620
1628
.10.2106/JBJS.L.01004
22.
Langberg
,
H.
,
Rosendal
,
L.
, and
Kjaer
,
M.
,
2001
, “
Training-Induced Changes in Peritendinous Type I Collagen Turnover Determined by Microdialysis in Humans
,”
J. Physiol.
,
534
(
1
), pp.
297
302
.10.1111/j.1469-7793.2001.00297.x
23.
Miller
,
B. F.
,
Olesen
,
J. L.
,
Hansen
,
M.
,
Dossing
,
S.
,
Crameri
,
R. M.
,
Welling
,
R. J.
,
Langberg
,
H.
,
Flyvbjerg
,
A.
,
Kjaer
,
M.
,
Babraj
,
J. A.
,
Smith
,
K.
, and
Rennie
,
M. J.
,
2005
, “
Coordinated Collagen and Muscle Protein Synthesis in Human Patella Tendon and Quadriceps Muscle After Exercise
,”
J. Physiol.
,
567
(
3
), pp.
1021
1033
.10.1113/jphysiol.2005.093690
24.
Muiznieks
,
L. D.
, and
Keeley
,
F. W.
,
2013
, “
Molecular Assembly and Mechanical Properties of the Extracellular Matrix: A Fibrous Protein Perspective
,”
Biochim. Biophys. Acta
,
1832
(
7
), pp.
866
875
.10.1016/j.bbadis.2012.11.022
25.
Magnusson
,
S. P.
,
Langberg
,
H.
, and
Kjaer
,
M.
,
2010
, “
The Pathogenesis of Tendinopathy: Balancing the Response to Loading
,”
Nat. Rev. Rheumatol.
,
6
(
5
), pp.
262
268
.10.1038/nrrheum.2010.43
26.
Park
,
D. Y.
,
Rubenson
,
J.
,
Carr
,
A.
,
Mattson
,
J.
,
Besier
,
T.
, and
Chou
,
L. B.
,
2011
, “
Influence of Stretching and Warm-Up on Achilles Tendon Material Properties
,”
Foot Ankle Int.
,
32
(
4
), pp.
407
413
.10.3113/FAI.2011.0407
27.
Peltonen
,
J.
,
Cronin
,
N. J.
,
Avela
,
J.
, and
Finni
,
T.
,
2010
, “
In Vivo Mechanical Response of Human Achilles Tendon to a Single Bout of Hopping Exercise
,”
J. Exp. Biol.
,
213
(
8
), pp.
1259
1265
.10.1242/jeb.033514
28.
Chiu
,
T. C.
,
Ngo
,
H. C.
,
Lau
,
L. W.
,
Leung
,
K. W.
,
Lo
,
M. H.
,
Yu
,
H. F.
, and
Ying
,
M.
,
2016
, “
An Investigation of the Immediate Effect of Static Stretching on the Morphology and Stiffness of Achilles Tendon in Dominant and Non-Dominant Legs
,”
PLoS One
,
11
(
4
), p.
e0154443
.10.1371/journal.pone.0154443
29.
Leung
,
W. K. C.
,
Chu
,
K. L.
, and
Lai
,
C.
,
2017
, “
Sonographic Evaluation of the Immediate Effects of Eccentric Heel Drop Exercise on Achilles Tendon and Gastrocnemius Muscle Stiffness Using Shear Wave Elastography
,”
PeerJ.
,
5
, p.
e3592
.10.7717/peerj.3592
30.
Arnoczky
,
S. P.
,
Lavagnino
,
M.
, and
Egerbacher
,
M.
,
2007
, “
The Mechanobiological Aetiopathogenesis of Tendinopathy: Is It the Over-Stimulation or the Under-Stimulation of Tendon Cells?
,”
Int. J. Exp. Pathol.
,
88
(
4
), pp.
217
226
.10.1111/j.1365-2613.2007.00548.x
31.
Glazebrook
,
M. A.
,
Wright
,
J. R.
, Jr.
,
Langman
,
M.
,
Stanish
,
W. D.
, and
Lee
,
J. M.
,
2008
, “
Histological Analysis of Achilles Tendons in an Overuse Rat Model
,”
J. Orthop. Res.
,
26
(
6
), pp.
840
846
.10.1002/jor.20546
32.
Soslowsky
,
L. J.
,
Thomopoulos
,
S.
,
Tun
,
S.
,
Flanagan
,
C. L.
,
Keefer
,
C. C.
,
Mastaw
,
J.
, and
Carpenter
,
J. E.
,
2000
, “
Neer Award 1999. Overuse Activity Injures the Supraspinatus Tendon in an Animal Model: A Histologic and Biomechanical Study
,”
J. Shoulder Elbow Surg.
,
9
(
2
), pp.
79
84
.10.1067/mse.2000.101962
33.
Couppe
,
C.
,
Kongsgaard
,
M.
,
Aagaard
,
P.
,
Hansen
,
P.
,
Bojsen-Moller
,
J.
,
Kjaer
,
M.
, and
Magnusson
,
S. P.
,
2008
, “
Habitual Loading Results in Tendon Hypertrophy and Increased Stiffness of the Human Patellar Tendon
,”
J. Appl. Physiol. (1985)
,
105
(
3
), pp.
805
810
.10.1152/japplphysiol.90361.2008
34.
Huang
,
T. F.
,
Perry
,
S. M.
, and
Soslowsky
,
L. J.
,
2004
, “
The Effect of Overuse Activity on Achilles Tendon in an Animal Model: A Biomechanical Study
,”
Ann. Biomed. Eng.
,
32
(
3
), pp.
336
341
.10.1023/B:ABME.0000017537.26426.76
35.
Wisloff
,
U.
,
Helgerud
,
J.
,
Kemi
,
O. J.
, and
Ellingsen
,
O.
,
2001
, “
Intensity-Controlled Treadmill Running in Rats: VO(2 Max) and Cardiac Hypertrophy
,”
Am. J. Physiol. Heart Circ. Physiol.
,
280
(
3
), pp.
H1301
H1310
.10.1152/ajpheart.2001.280.3.H1301
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