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10/10/13
1
Physiological and Mechanical Adaptations of Muscle to Tendon Rupture
Samuel R. Ward, PT, PhD
Associate Professor Muscle Physiology Lab
Departments of Radiology, Orthopaedic Surgery, and Bioengineering University of California San Diego
VA Medical Center San Diego
MuscleTech Network, Barcelona, Oct 15, 2013
Background
• Cuff injuries effect ~30% of people over 60 1 • 20-50% of repairs will fail 2 • Chronic tears
– Muscle retraction, fatty atrophy and fibrosis 3 – Nerve injury 4 – Difficult to repair 5 – High re-tear rates 2 – Insensitive to rehabilitation 6
Healthy
Severe Tear
1 Lehman et al, Bull Hosp Jt Dis, 1995 2 Harryman et al, JBJS 1991 3 Gerber et al, JBJS, 2004 4 Costouros et al, Arthroscopy, 2007 5 Peterson, et al JSES 2011 6 Gerber et al, JBJS, 2000
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2
Skeletal Muscle Hierarchy
Lieber, Skeletal Muscle Structure and Function, 2010
Structure-Function Relationships
Powell et al, J Appl Physiol, 1984
Muscle Length
Mus
cle
Forc
e
Bodine et al, J Neurophysiol , 1982
Winters et al, J Biomech, 2012
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Normal Architecture
Ward, et al Clin Orthop, 2006
Ward, et al Clin Orthop 2006 Altobelli, et al, Submitted J Biomech 2013
0.0
5.0
10.0
15.0
20.0
25.0
30.0
0.0 2.0 4.0 6.0 8.0 10.0 12.0
PCSA
(cm
2 )
Fiber Length (cm)
Deltoid
Subscapularis
Infraspinatus
Supraspinatus
teres minor
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4
Pathology
Normal Tear
Anterior
SS tendon attached to Infraspinatus and anterior capsule
Biceps tendon
30.47mm
47.72 mm
Muscle Area Changes with Tear and Age (Human)
Barry et al, JSES 2012
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5
Muscle Structural Changes After Tear (Sheep)
Gerber C, et al JBJS 2004
Muscle Fat
Tomioka et al, JSES 2009
Fibe
r Len
gth
(mm
)
Muscle Fiber Length Changes After Tear (Human)
0
10
20
30
40
50
60
70
80
1
No Tear Tear
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Architectural Adaptations to Tear and Nerve Injury
Sato, et al, In Submission JBJS
4.0"3.5"3.0"2.5"2.0"1.5"1.0"0.5"0"
20"
40"
60"
80"
100"
Sarcomere Length (µm) "
Rel
ativ
e M
uscl
e Te
nsio
n"
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7
Whole Supraspinatus Muscle Stiffness
Gerber et al, JSES, 1998- Human Safran, et al, JBJS 2005- Dog Gerber et al, JBJS 2004- Sheep
0
100
200
300
400
500
600
700
Single Fiber Fiber Bundle
Inju
red
Cuf
f Ela
stic
Mod
ulus
(kPa
)
Supraspinatus
Infraspinatus
*
Silldorff, Submitted JBJS
Human Passive Mechanics
Control
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Tissue Adaptations to Tear and Nerve Injury (rat)
Sato, et al, In Submission JBJS
Structural Change- Summary
Muscle Length
Mus
cle
Forc
e
Healthy
Tear
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C: EDII
T: EDII
10 mm
C: EDL T: EDL
10 mm
C: TA
T: TA
10 mm
Rabbit Lower Extremity Tenotomy
Muscle Length
Mus
cle
Tens
ion
&
Control Tenotomy
Active & Passive Mechanics
Muscle Architecture Length-Tension Curve
In Vivo Mechanical Testing
100 µm
Fiber Area
10/10/13
10
0
50
100
150
200
250
300
TA EDL EDII
Stre
ss A
fter R
epai
rControlTenotomy
* *
*
0
10
20
30
40
TA EDL EDII
Nor
mal
ized
Fib
er L
engt
h [m
m] Control
Tenotomy
Tenotomy Alters LT Relationship
* = p < 0.05
EDII EDL
TA *
* *
0
50
100
150
200
250
0 5 10 15 20Fiber Length [mm]
Stre
ss [k
Pa]
ControlTenotomy
0
50
100
150
200
250
0 20 40 60 80Fiber Length [mm]
Stre
ss [k
Pa]
ControlTenotomy
0
50
100
150
200
250
0 5 10 15 20 25 30Fiber Length [mm]
Stre
ss [k
Pa]
ControlTenotomy
Tentomy Alters Passive Stiffness TA
EDL EDII
0
2000
4000
6000
TA EDL EDII
Pass
ive
Stiff
ness
[kPa
] ControlTenotomy
* *
*
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50 µm 50 µm
50 µm
50 µm 50 µm
50 µm
ECM Remodeling
TA
EDL
EDII
Control Tenotomy
Winters, et al, In Progress
New Histology Methods
αSMA KI67 pCEβ
Picro-sirius Red H & E Wheat Germ Agglutinin Reticulin Trichrome
Winters, Buck et al, In Progress
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12
Human Muscle Gene Expression
Choo, McCarthy et al, In Progress JBJS
Summary
• Structural Changes – Radial and longitudinal atrophy
• Physiological Changes – After chronic tears, function does not follow structure – Evidence for ECM changes leading to muscle stiffness
• Rehabilitation – Massive tears in the shoulder don’t appear to recover
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Faculty Doug Chang, MD- UCSD Adam Engler, PhD- UCSD Don Fithian, MD – Kaiser Larry Frank, PhD- UCSD Jan Fridén, MD- Göteborg, Sweden Christian Gerber, MD- Balgrist, Switzerland Eric Hentzen, MD, PhD- UCSD John Lane, MD- Coast Surgery Center Rick Lieber, PhD- UCSD Hiro Okuno, MD- Joseph Sarver, PhD- Penn Simon Schenk, PhD- UCSD Lou Soslowsky, PhD- Penn Andrea Taylor, PhD- Duke Steve Thomopoulos, PhD- Wash U
Students Grant Altobelli, MD – Tufts Geoff Abrams, MD- Stanford Alex Choo, MD- UCSD Carolyn Eng, BS- Harvard Ki Lee, MD- Yonsei Meagan McCarthy, MD- UCSD Randy McKnight- UCSD Morgan Silldorff, MD- UCSD Gretchen Meyer, PhD- UCSD Eugene Sato, BS- UCSD Ana Rodriguez-Soto, BS- UCSD