Pressure sores (PS) in deep muscles are potentially fatal and are considered one of the most costly complications in spinal cord injury patients. We hypothesize that continuous compression of the longissimus and gluteus muscles by the sacral and ischial bones during wheelchair sitting increases muscle stiffness around the bone-muscle interface over time, thereby causing muscles to bear intensified stresses in relentlessly widening regions, in a positive-feedback injury spiral. In this study, we measured long-term shear moduli of muscle tissue in vivo in rats after applying compression (35 KPa or 70 KPa for 14–2 h, N=32), and evaluated tissue viability in matched groups (using phosphotungstic acid hematoxylin histology, N=10). We found significant (1.8-fold to 3.3-fold, p<0.05) stiffening of muscle tissue in vivo in muscles subjected to 35 KPa for 30 min or over, and in muscles subjected to 70 KPa for 15 min or over. By incorporating this effect into a finite element (FE) model of the buttocks of a wheelchair user we identified a mechanical stress wave which spreads from the bone-muscle interface outward through longissimus muscle tissue. After 4 h of FE simulated motionlessness, 50%–60% of the cross section of the longissimus was exposed to compressive stresses of 35 KPa or over (shown to induce cell death in rat muscle within 15 min). During these 4 h, the mean compressive stress across the transverse cross section of the longissimus increased by 30%–40%. The identification of the stiffening-stress-cell-death injury spiral developing during the initial 30 min of motionless sitting provides new mechanistic insight into deep PS formation and calls for reevaluation of the 1 h repositioning cycle recommended by the U.S. Department of Health.

1.
Husain
T.
, 1953, “
An Experimental Study of Some Pressure Effects on Tissues, With Reference to the Bedsore Problem
,”
J. Pathol. Bacteriol.
0368-3494
66
, pp.
347
358
.
2.
Daniel
,
R. K.
,
Priest
,
D. L.
, and
Wheatley
,
D. C.
, 1981, “
Etiologic Factors in Pressure Sores: An Experimental Model
,”
Arch. Phys. Med. Rehabil.
0003-9993
62
, pp.
492
498
.
3.
Knight
,
L. S.
,
Taylor
,
P. R.
,
Polliac
,
A. A.
, and
Bader
L. D.
, 2001, “
Establishing Predictive Indicators for the Status of Loaded Soft Tissues
,”
J. Appl. Physiol.
8750-7587
90
, pp.
2231
2237
.
4.
Bouten
,
C. V.
,
Breuls
,
R. G.
,
Peeters
,
E. A.
,
Oomens
,
C. W.
, and
Baaijens
,
F. P.
, 2003, “
In Vitro Models to Study Compressive Strain-Induced Muscle Cell Damage
,”
Biorheology
0006-355X
40
, pp.
383
388
.
5.
Allman
,
R. M.
,
Goode
,
P. S.
,
Patrick
,
M. M.
,
Burst
,
N.
, and
Bartolucci
,
A. A.
, 1995, “
Pressure Ulcer Risk Factors Among Hospitalized Patients With Activity Limitation
,”
JAMA, J. Am. Med. Assoc.
0098-7484
273
, pp.
865
870
.
6.
National Spinal Cord Injury Statistical Center
, 1997, “
Annual Report for the Model Spinal Cord Injury Care Systems
,”
University of Alabama
, Birmingham, AL.
7.
Byrne
D. W.
, and
Salzberg
C. A.
, 1996, “
Major Risk Factors for Pressure Ulcers in the Spinal Cord Disabled: A Literature Review
,”
Spinal Cord
1362-4393
34
, pp.
255
263
.
8.
Tsokos
,
M.
,
Heinemann
,
A.
, and
Puschel
,
K.
, 2000, “
Pressure Sores: Epidemiology, Medico-Legal Implications and Forensic Argumentation Concerning Causality
,”
Int. J. Legal Med.
0937-9827
113
, pp.
283
287
.
9.
Margolis
,
D. J.
,
Knauss
,
J.
,
Bilker
,
W.
, and
Baumgarten
,
M.
, 2003, “
Medical Conditions as Risk Factors for Pressure Ulcers in an Outpatient Setting
,”
Age Ageing
0002-0729
32
, pp.
259
264
.
10.
Bouten
,
C. V.
,
Oomens
,
C. W.
,
Baaijens
,
F. P.
, and
Bader
,
D. L.
, 2003, “
The Etiology of Pressure Ulcers: Skin Deep or Muscle Bound?
,”
Arch. Phys. Med. Rehabil.
0003-9993
84
, pp.
616
619
.
11.
Bliss
,
M. R.
, 1993, “
Aetiology of Pressure Sores
,” Rev. Clin. Gerontol.
3
, pp.
379
397
.
12.
Smith
,
P. W.
,
Black
,
J. M.
, and
Black
,
S. B.
, 1999, “
Infected Pressure Ulcers in the Long-Term-Care Facility
,”
Infect. Control Hosp. Epidemiol.
0899-823X
20
, pp.
358
361
.
13.
Smith
,
J. W.
, 1954, “
Elastic Properties of the Anterior Cruciate Ligament of the Rabbit
,”
J. Anat.
0021-8782
88
, pp.
369
380
.
14.
Fitzgerald
,
E. R.
, and
Freeland
,
A. E.
, 1970, “
Viscoelastic Response of Intervertebral Discs at Audio Frequencies
,”
Med. Biol. Eng.
0025-696X
9
, pp.
459
478
.
15.
Rang
,
E. M.
,
Lippert
,
S. A.
, and
Grimm
,
M. J.
, 2001, “
The Degradation of Material Properties of Brain Tissue as a Function of Time Postmortem
,”
Proceedings of the Summer ASME Bioengineering Conference
, Snowbird, Utah, June 27–July 1, University of Toledo, OH, pp.
887
888
.
16.
Hayes
,
W. C.
, and
Bodine
,
A. J.
, 1978, “
Flow-Independent Viscoelastic Properties of Articular Cartilage Matrix
,”
J. Biomech.
0021-9290
11
, pp.
407
419
.
17.
Goll
,
D. E.
,
Taylor
,
R. G.
,
Christiansen
,
J. A.
, and
Thompson
,
V. F.
, 1992, “
Role of Proetinases and Protein Turnover in Muscle Growth and Meat Quality
,”
Procecdings 44th Annual Recip. Meat Conference
, National Livestock and Meat Board, Chicago, IL, American Meat Science Association (AMSA), Savoy, IL, pp.
25
36
.
18.
Mayer
,
R. G.
, and
Bigelow
,
G. S.
, 1990,
Embalming: History, Theory, and Practice
,
Appleton and Lange
, East Norwalk, CT.
19.
Linder-Ganz
,
E.
, and
Gefen
,
A.
, 2004, “
Mechanical Compression-Induced Pressure Sores in Rat Hind-Limb: Muscle Stiffness, Histology and Computational Models
,”
J. Appl. Physiol.
8750-7587
96
, pp.
2034
2049
.
20.
Kovanen
,
V
,
Suominen
,
H
, and
Heikkinen
,
E.
, 1984, “
Mechanical Properties of Fast and Slow Skeletal Muscle With Special Reference to Collagen and Endurance Training
,”
J. Biomech.
0021-9290
17
, pp.
725
735
.
21.
Vankan
,
W. J.
,
Huyghe
,
J. M.
,
van Donkelaar
,
C. C.
,
Drost
,
M. R.
,
Janssen
,
J. D.
, and
Huson
,
A.
, 1998, “
Mechanical Blood-Tissue Interaction in Contracting Muscles: A Model Study
,”
J. Biomech.
0021-9290
31
, pp.
401
409
.
22.
Lai-Fook
,
S. J.
,
Wilson
,
T. A.
,
Hyatt
,
R. E.
, and
Rodarte
,
J. R.
, 1976, “
Elastic Constants of Inflated Lobes of Dog Lungs
,”
J. Appl. Physiol.
0021-8987
40
, pp.
508
513
.
23.
Vannah
,
W. M
, and
Childress
,
D. S.
, 1996, “
Indentor Tests and Finite Element Modeling of Bulk Muscular Tissue In Vivo
,”
J. Rehabil. Res. Dev.
0748-7711
33
, pp.
239
252
.
24.
Gefen
,
A.
,
Megido-Ravid
,
M.
,
Azariah
,
M.
,
Itzchak
,
Y.
, and
Arcan
,
M.
, 2001, “
Integration of Plantar Soft Tissue Stiffness Measurements in Routine MRI of the Diabetic Foot
,”
Clin. Biomech. (Los Angel. Calif.)
0191-7870
16
, pp.
921
925
.
25.
Gefen
,
A.
,
Gefen
,
N.
,
Zhu
,
Q.
,
Raghupathi
,
R.
, and
Margulies
,
S. S.
, 2003, “
Age-Dependent Changes in Material Properties of the Brain and Braincase of the Rat
,”
J. Neurotrauma
0897-7151
20
, pp.
1163
1177
.
26.
Gefen
,
A.
, and
Margulies
,
S. S.
, 2004, “
Are In Vivo and In Situ Brain Tissues Mechanically Similar?
,”
J. Biomech.
0021-9290
37
, pp.
1339
1352
.
27.
Lee
,
E. H.
, and
Radok
,
J. R. M.
, 1960, “
The Contact Problem for Viscoelastic Bodies
,”
ASME J. Appl. Mech.
0021-8936
27
, pp.
438
444
.
28.
Zheng
,
Y.
,
Mak
,
A. F.
, and
Lue
,
B.
, 1999, “
Objective Assessment of Limb Tissue Elasticity: Development of a Manual Indentation Procedure
,”
J. Rehabil. Res. Dev.
0748-7711
36
, pp.
71
85
.
29.
Newson
T. P.
, and
Rolfe
,
P.
, 1982, “
Skin Surface PO2 and Blood Flow Measurements Over the Ischial Tuberosity
,”
Arch. Phys. Med. Rehabil.
0003-9993
63
, pp.
553
556
.
30.
Patterson
,
R. P.
, and
Fisher
,
S. V.
, 1980, “
Pressure and Temperature Patterns Under the Ischial Tuberosities
,”
Bull. Prosthet. Res.
0007-506X
10-34
, pp.
5
11
.
31.
Agency for Health Care Policy and Research (AHCPR)
, 1994, “
Treatment of Pressure Ulcers
” in
Clinical Practice Guideline No. 15
,
U.S. Department of Health and Human Services
, Publication No. 95-0652, Washington, DC.
32.
Kosiak
,
M.
, 1961, “
Etiology of Decubitus Ulcers
,”
Arch. Phys. Med. Rehabil.
0003-9993
42
, pp.
19
29
.
33.
Salcido
,
R.
,
Fisher
,
S. B.
,
Donofrio
,
J. C.
,
Bieschke
,
M.
,
Knapp
,
C.
,
Liang
,
R.
,
LeGrand
,
E. K.
, and
Carney
,
J. M.
, 1995, “
An Animal Model and Computer-Controlled Surface Pressure Delivery System for the Production of Pressure Ulcers
,”
J. Rehabil. Res. Dev.
0748-7711
32
, pp.
149
161
.
34.
Peirce
,
S. M.
,
Skalak
,
T. C.
, and
Rodeheaver
,
G. T.
, 2000, “
Ischemia-Reperfusion Injury in Chronic Pressure Ulcer Formation: A Skin Model in the Rat
,”
Wound Repair Regen
1067-1927
8
, pp.
68
76
.
35.
Bosboom
,
E. M.
,
Bouten
,
C. V.
,
Oomens
,
C. W.
,
van Straaten
,
H. W.
,
Baaijens
,
F. P.
, and
Kuipers
,
H.
, 2001, “
Quantification and Localisation of Damage in Rat Muscles After Controlled Loading; A New Approach to Study the Aetiology of Pressure Sores
,”
Med. Eng. Phys.
1350-4533
23
, pp.
195
200
.
36.
Drerup
B.
,
Kraneburg
,
S.
,
Koller
,
A.
, 2001, “
Visualisation of Pressure Dose: Synopsis of Peak Pressure, Mean Pressure, Loading Time and Pressure Time-Integral
,”
Clin. Biomech. (Los Angel. Calif.)
0191-7870
16
, pp.
833
834
.
37.
Carew
,
E. O.
,
Barber
,
J. E.
, and
Vesely
,
I.
, 2000, “
Role of Preconditioning and Recovery Time in Repeated Testing of Aortic Valve Tissues: Validation Through Quasilinear Viscoelastic Theory
,”
Ann. Biomed. Eng.
0090-6964
28
, pp.
1093
1100
.
38.
Zhang
,
M.
, and
Mak
,
A. F.
, 1999, “
In Vivo Friction Properties of Human Skin
,”
Prosthet. Orthot Int.
0309-3646
23
, pp.
135
141
.
39.
Tschoegl
,
N. W.
, 1989,
The Phenomenological Theory of Linear Viscoelastic Behavior: An Introduction
,
Springer
, New York.
40.
Hamhaber
,
U.
,
Grieshaber
,
F. A.
,
Nagel
,
J. H.
, and
Klose
,
U.
, 2003, “
Comparison of Quantitative Shear Wave MR-Elastography With Mechanical Compression Tests
,”
Magn. Reson. Med.
0740-3194
49
, pp.
71
77
.
41.
Fridén
J
, and
Lieber
R. L.
, 2003, “
Spastic Muscle Cells Are Shorter and Stiffer Than Normal Cells
,”
Muscle Nerve
0148-639X
27
, pp.
157
164
.
42.
Basford
,
J. R.
,
Jenkyn
,
T. R.
,
An
,
K. N.
,
Ehman
,
R. L.
,
Heers
,
G.
, and
Kaufman
K. R.
, 2002, “
Evaluation of Healthy and Diseased Muscle With Magnetic Resonance Elastography
,”
Arch. Phys. Med. Rehabil.
0003-9993
83
, pp.
1530
1536
.
43.
Uffmann
,
K.
,
Maderwald
,
S.
,
Ajaj
,
W.
,
Galban
,
C. G.
,
Mateiescu
,
S.
,
Quick
,
H. H.
, and
Ladd
,
M. E.
, 2004, “
In Vivo Elasticity Measurements of Extremity Skeletal Muscle With MR Elastography
,”
NMR Biomed.
0952-3480
17
, pp.
181
190
.
44.
Dresner
,
M. A.
,
Rose
,
G. H.
,
Rossman
,
P. J.
,
Muthupillai
,
R.
,
Manduca
,
A.
, and
Ehman
,
R. L.
, 2001, “
Magnetic Resonance Elastography of Skeletal Muscle
,”
J. Magn. Reson Imaging
1053-1807
13
, pp.
269
276
.
45.
Gennisson
,
J.-L.
,
Catheline
,
S.
,
Chaffaï
,
S.
, and
Fink
,
M.
, 2003, “
Transient Elastography in Anisotropic Medium: Application to the Measurement of Slow and Fast Shear Wave Speeds in Muscles
,”
J. Acoust. Soc. Am.
0001-4966
114
, pp.
536
541
.
46.
Bosboom
,
E. M
,
Hesselink
,
M. K
,
Oomens
,
C. W.
,
Bouten
,
C. V.
,
Drost
,
M. R.
,
Baaijens
,
F. P.
, 2001, “
Passive Transverse Mechanical Properties of Skeletal Muscle Under In Vivo Compression
,”
J. Biomech.
0021-9290
34
, pp.
1365
1368
.
You do not currently have access to this content.