Achilles tendon ruptures are traumatic injuries, and techniques for assessing repair outcomes rely on patient-based measures of pain and function, which do not directly assess tendon healing. Consequently, there is a need for a quantitative, in vivo measure of tendon properties. Therefore, the purpose of this study was to validate ultrasound imaging for evaluating collagen organization in tendons. In this study, we compared our novel, high-frequency ultrasound (HFUS) imaging and analysis method to a standard measure of collagen organization, crossed polarizer (CP) imaging. Eighteen mouse Achilles tendons were harvested and placed into a testing fixture where HFUS and CP imaging could be performed simultaneously in a controlled loading environment. Two experiments were conducted: (1) effect of loading on collagen alignment and (2) effect of an excisional injury on collagen alignment. As expected, it was found that both the HFUS and CP methods could reliably detect an increase in alignment with increasing load, as well as a decrease in alignment with injury. This HFUS method demonstrates that structural measures of collagen organization in tendon can be determined through ultrasound imaging. This experiment also provides a mechanistic evaluation of tissue structure that could potentially be used to develop a targeted approach to aid in rehabilitation or monitor return to activity after tendon injury.

References

References
1.
Suchak
,
A. A.
,
Bostick
,
G.
,
Reid
,
D.
,
Blitz
,
S.
, and
Jomha
,
N.
,
2005
, “
The Incidence of Achilles Tendon Ruptures in Edmonton, Canada
,”
Foot Ankle Int.
,
26
(
11
), pp.
932
936
.
2.
Houshian
,
S.
,
Tscherning
,
T.
, and
Riegels-Nielsen
,
P.
,
1998
, “
The Epidemiology of Achilles Tendon Rupture in a Danish County
,”
Injury
,
29
(
9
), pp.
651
654
.10.1016/S0020-1383(98)00147-8
3.
Moller
,
A.
,
Astron
,
M.
, and
Westlin
,
N.
,
1996
, “
Increasing Incidence of Achilles Tendon Rupture
,”
Acta Orthop. Scand.
,
67
(
5
), pp.
479
481
.10.3109/17453679608996672
4.
Lin
,
T. W.
,
Cardenas
,
L.
, and
Soslowsky
,
L. J.
,
2004
, “
Biomechanics of Tendon Injury and Repair
,”
J. Biomech.
,
37
(
6
), pp.
865
877
.10.1016/j.jbiomech.2003.11.005
5.
Saxena
,
A.
,
Ewen
,
B.
, and
Maffulli
,
N.
,
2011
, “
Rehabilitation of the Operated Achilles Tendon: Parameters for Predicting Return to Activity
,”
J. Foot Ankle Surg.
,
50
(
1
), pp.
37
40
.10.1053/j.jfas.2010.10.008
6.
Mullaney
,
M. J.
,
McHugh
,
M. P.
,
Tyler
,
T. F.
,
Nicholas
,
S. J.
, and
Lee
,
S. J.
,
2006
, “
Weakness in End-Range Plantar Flexion After Achilles Tendon Repair
,”
Am. J. Sports Med.
,
34
(
7
), pp.
1120
1125
.10.1177/0363546505284186
7.
Robinson
,
J. M.
,
Cook
,
J. L.
,
Purdam
,
C.
,
Visentini
,
P. J.
,
Ross
,
J.
,
Maffulli
,
N.
,
Taunton
,
J. E.
, and
Khan
,
K. M.
,
2001
, “
The VISA-A Questionnaire: A Valid and Reliable Index of the Clinical Severity of Achilles Tendinopathy
,”
Br. J. Sports Med.
,
35
(
5
), pp.
335
341
.10.1136/bjsm.35.5.335
8.
Silbernagel
,
K. G.
,
Nilsson-Helander
,
K.
,
Thomee
,
R.
,
Eriksson
,
B. I.
, and
Karlsson
,
J.
,
2010
, “
A New Measurement of Heel-Rise Endurance With the Ability to Detect Functional Deficits in Patients With Achilles Tendon Rupture
,”
Knee Surg. Sports Traumatol. Arthrosc.
,
18
(
2
), pp.
258
264
.10.1007/s00167-009-0889-7
9.
Chinn
,
L.
, and
Hertel
,
J.
,
2010
, “
Rehabilitation of Ankle and Foot Injuries in Athletes
,”
Clin. Sports Med.
,
29
(
1
), pp.
157
167
.10.1016/j.csm.2009.09.006
10.
Miller
,
K. S.
,
Connizzo
,
B. K.
,
Feeney
,
E.
, and
Soslowsky
,
L. J.
,
2012
, “
Characterizing Local Collagen Fiber Re-Alignment and Crimp Behavior Throughout Mechanical Testing in a Mature Mouse Supraspinatus Tendon Model
,”
J. Biomech.
,
45
(
12
), pp.
2061
2065
.10.1016/j.jbiomech.2012.06.006
11.
Miller
,
K. S.
,
Edelstein
,
L.
,
Connizzo
,
B. K.
, and
Soslowsky
,
L. J.
,
2012
, “
Effect of Preconditioning and Stress Relaxation on Local Collagen Fiber Re-alignment: Inhomogeneous Properties of Rat Supraspinatus Tendon
,”
ASME J. Biomech. Eng.
,
134
(
3
),
p
. 031007.
12.
Gimbel
,
J. A.
,
Van Kleunen
,
J. P.
,
Mehta
,
S.
,
Perry
,
S. M.
,
Williams
,
G. R.
, and
Soslowsky
,
L. J.
,
2004
, “
Supraspinatus Tendon Organizational and Mechanical Properties in a Chronic Rotator Cuff Tear Animal Model
,”
J. Biomech.
,
37
(
5
), pp.
739
749
.10.1016/j.jbiomech.2003.09.019
13.
Dourte
,
L. M.
,
Perry
,
S. M.
,
Getz
,
C. L.
, and
Soslowsky
,
L. J.
,
2010
, “
Tendon Properties Remain Altered in a Chronic Rat Rotator Cuff Model
,”
Clin. Orthop. Relat. Res.
,
468
(
6
), pp.
1485
1492
.10.1007/s11999-009-1206-y
14.
Lake
,
S. P.
,
Miller
,
K. S.
,
Elliott
,
D. M.
, and
Soslowsky
,
L. J.
,
2009
, “
Effect of Fiber Distribution and Realignment on the Nonlinear and Inhomogeneous Mechanical Properties of Human Supraspinatus Tendon Under Longitudinal Tensile Loading
,”
J. Orthop. Res.
,
27
(
12
), pp.
1596
1602
.10.1002/jor.20938
15.
Quinn
,
K. P.
, and
Winkelstein
,
B. A.
,
2008
, “
Altered Collagen Fiber Kinematics Define the Onset of Localized Ligament Damage During Loading
,”
J. Appl. Physiol.
,
105
(
6
), pp.
1881
1888
.10.1152/japplphysiol.90792.2008
16.
Quinn
,
K. P.
,
Bauman
,
J. A.
,
Crosby
,
N. D.
, and
Winkelstein
,
B. A.
,
2010
, “
Anomalous Fiber Realignment During Tensile Loading of the Rat Facet Capsular Ligament Identifies Mechanically Induced Damage and Physiological Dysfunction
,”
J. Biomech.
,
43
(
10
), pp.
1870
1875
.10.1016/j.jbiomech.2010.03.032
17.
Thomopoulos
,
S.
,
Williams
,
G. R.
,
Gimbel
,
J. A.
,
Favata
,
M.
, and
Soslowsky
,
L. J.
,
2003
, “
Variation of Biomechanical, Structural, and Compositional Properties Along the Tendon to Bone Insertion Site
,”
J. Orthop. Res.
,
21
(
3
), pp.
413
419
.10.1016/S0736-0266(03)0057-3
18.
Franchi
,
M.
,
Torricelli
,
P.
,
Giavaresi
,
G.
, and
Fini
,
M.
,
2013
, “
Role of Moderate Exercising on Achilles Tendon Collagen Crimping Patterns and Proteoglycans
,”
Connect. Tissue Res.
,
54
, pp.
267
274
.10.3109/03008207.2013.807808
19.
Lau
,
T. Y.
,
Ambekar
,
R.
, and
Toussaint
,
K. C.
,
2012
, “
Quantification of Collagen Fiber Organization Using Three-Dimensional Fourier Transform-Second-Harmonic Generation Imaging
,”
Opt. Express
,
20
(
19
), pp.
21821
21832
.10.1364/OE.20.021821
20.
Gusachenko
, I
.
,
Tran
, V
.
,
Houssen
,
Y. G.
,
Allain
,
J. M.
, and
Schanne-Klein
,
M. C.
,
2012
, “
Polarization-Resolved Second-Harmonic Generation in Tendon Upon Mechanical Stretching
,”
Biophys. J.
,
102
(
9
), pp.
2220
2229
.10.1016/j.bpj.2012.03.068
21.
Abraham
,
T.
,
Fong
,
G.
, and
Scott
,
A.
,
2011
, “
Second Harmonic Generation Analysis of Early Achilles Tendinosis in Response to in vivo Mechanical Loading
,”
BMC Musculoskelet. Disord.
,
12
,
p
. 26.
22.
Vidal Bde
,
C.
, and
Mello
,
M. L.
,
2011
, “
Collagen Type I Amide I Band Infrared Spectroscopy
,”
Micron
,
42
(
3
), pp.
283
289
.10.1016/j.micron.2010.09.010
23.
Alfredson
,
H.
,
Masci
,
L.
, and
Ohberg
,
L.
,
2011
, “
Partial Mid-portion Achilles Tendon Ruptures: New Sonographic Findings Helpful for Diagnosis
,”
Br. J. Sports Med.
,
45
(
5
), pp.
429
432
.10.1136/bjsm.2009.067298
24.
Maranho
,
D. A.
,
Nogueira-Barbosa
,
M. H.
,
Simao
,
M. N.
, and
Volpon
,
J. B.
,
2009
, “
Ultrasonographic Evaluation of Achilles Tendon Repair After Percutaneous Sectioning for the Correction of Congenital Clubfoot Residual Equinus
,”
J. Pediatr. Orthop.
,
29
(
7
), pp.
804
810
.10.1097/BPO.0b013e3181b76a5f
25.
Mangat
,
K. S.
,
Kanwar
,
R.
,
Johnson
,
K.
,
Korah
,
G.
, and
Prem
,
H.
,
2010
, “
Ultrasonographic Phases in Gap Healing Following Ponseti-Type Achilles Tenotomy
,”
J. Bone Joint Surg. Am.
,
92
(
6
), pp.
1462
1467
.10.2106/JBJS.I.00188
26.
Vadala
,
A.
,
De Carli
,
A.
,
Vulpiani
,
M. C.
,
Iorio
,
R.
,
Vetrano
,
M.
,
Scapellato
,
S.
,
Suarez
,
T.
,
Di
Salvo
,
F.
, and
Ferretti
,
A.
,
2012
, “
Clinical, Functional and Radiological Results of Achilles Tenorraphy Surgically Treated With Mini-open Technique
,”
J. Sports Med. Phys. Fitness
,
52
(
6
), pp.
616
621
.
27.
Poposka
,
A.
,
Georgieva
,
D.
, and
Dzoleva-Tolevska
,
R.
,
2012
, “
Significance of Ultrasound in the Diagnosis and Treatment of Achilles Tendon Rupture
,”
Prilozi
,
33
(
1
), pp.
209
216
.
28.
Chamberlain
,
C. S.
,
Duenwald-Kuehl
,
S. E.
,
Okotie
,
G.
,
Brounts
,
S. H.
,
Baer
,
G. S.
, and
Vanderby
,
R.
,
2013
, “
Temporal Healing in Rat Achilles Tendon: Ultrasound Correlations
,”
Ann. Biomed. Eng.
,
41
(
3
), pp.
477
487
.10.1007/s10439-012-0689-y
29.
Duenwald-Kuehl
,
S.
,
Lakes
,
R.
, and
Vanderby
,
R.
, Jr.
,
2012
, “
Strain-Induced Damage Reduces Echo Intensity Changes in Tendon During Loading
,”
J. Biomech.
,
45
(
9
), pp.
1607
1611
.10.1016/j.jbiomech.2012.04.004
30.
Bashford
,
G. R.
,
Tomsen
,
N.
,
Arya
,
S.
,
Burnfield
,
J. M.
, and
Kulig
,
K.
,
2008
, “
Tendinopathy Discrimination by Use of Spatial Frequency Parameters in Ultrasound B-Mode Images
,”
IEEE Trans. Med. Imaging
,
27
(
5
), pp.
608
615
.10.1109/TMI.2007.912389
31.
Kulig
,
K.
,
Landel
,
R.
,
Chang
,
Y. J.
,
Hannanvash
,
N.
,
Reischl
,
S. F.
,
Song
,
P.
, and
Bashford
,
G. R.
,
2013
, “
Patellar Tendon Morphology in Volleyball Athletes With and Without Patellar Tendinopathy
,”
Scand. J. Med. Sci. Sports
,
23
(
2
), pp.
e81
e88
.10.1111/sms.12021
32.
Chen
,
X. M.
,
Cui
,
L. G.
,
He
,
P.
,
Shen
,
W. W.
,
Qian
,
Y. J.
, and
Wang
,
J. R.
,
2013
, “
Shear Wave Elastographic Characterization of Normal and Torn Achilles Tendons: A Pilot Study
,”
J. Ultrasound Med.
,
32
(
3
), pp.
449
455
.
33.
Shah
,
S. A.
,
Santago
,
P.
, and
Rubin
,
B. K.
,
2005
, “
Quantification of Biopolymer Filament Structure
,”
Ultramicroscopy
,
104
(
3–4
), pp.
244
254
.10.1016/j.ultramic.2005.04.007
34.
Gimbel
,
J. A.
,
Mehta
,
S.
,
Van Kleunen
,
J. P.
,
Williams
,
G. R.
, and
Soslowsky
,
L. J.
,
2004
, “
The Tension Required at Repair to Reappose the Supraspinatus Tendon to Bone Rapidly Increases After Injury
,”
Clin. Orthop. Rela.t Res.
,
4
(
26
), pp.
258
265
.10.1097/01.blo.0000136831.17696.80
35.
Garcia
,
T.
,
Hornof
,
W. J.
, and
Insana
,
M. F.
,
2003
, “
On the Ultrasonic Properties of Tendon
,”
Ultrasound Med. Biol.
,
29
(
12
), pp.
1787
1797
.10.1016/S0301-5629(03)01069-X
36.
Khoury
, V
.
,
Guillin
,
R.
,
Dhanju
,
J.
, and
Cardinal
,
E.
,
2007
, “
Ultrasound of Ankle and Foot: Overuse and Sports Injuries
,”
Semin. Musculoskelet. Radiol.
,
11
(
2
), pp.
149
161
.10.1055/s-2007-1001880
37.
VisualSonics
,
2007
,
VisualSonics 700-Series RMV Scanhead Selector
,
VisualSonics
,
Toronto
.
38.
Hansen
,
P.
,
Haraldsson
,
B. T.
,
Aagaard
,
P.
,
Kovanen
, V
.
,
Avery
,
N. C.
,
Qvortrup
,
K.
,
Larsen
,
J. O.
,
Krogsgaard
,
M.
,
Kjaer
,
M.
, and
Peter Magnusson
,
S.
,
2010
, “
Lower Strength of the Human Posterior Patellar Tendon Seems Unrelated to Mature Collagen Cross-Linking and Fibril Morphology
,”
J. Appl. Physiol.
,
108
(
1
), pp.
47
52
.10.1152/japplphysiol.00944.2009
39.
Ros
,
S. J.
,
Andarawis-Puri
,
N.
, and
Flatow
,
E. L.
,
2013
, “
Tendon extracellular matrix damage detection and quantification using automated edge detection analysis
,”
J. Biomech.
,
46
(
16
), pp.
2844–2847
.10.1016/j.jbiomech.2013.09.002
You do not currently have access to this content.