In vivo muscle stiffening under bone compression promotes deep pressure sores.

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 1/4-2 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]  Cees W J Oomens,et al.  In vitro models to study compressive strain-induced muscle cell damage. , 2003, Biorheology.

[2]  T. Husain,et al.  An experimental study of some pressure effects on tissues, with reference to the bed-sore problem. , 1953, The Journal of pathology and bacteriology.

[3]  Cwj Cees Oomens,et al.  Quantification and localisation of damage in rat muscles after controlled loading; a new approach to study the aetiology of pressure sores. , 2001, Medical engineering & physics.

[4]  A F Mak,et al.  Objective assessment of limb tissue elasticity: development of a manual indentation procedure. , 1999, Journal of rehabilitation research and development.

[5]  R. Daniel,et al.  Etiologic factors in pressure sores: an experimental model. , 1981, Archives of physical medicine and rehabilitation.

[6]  S V Fisher,et al.  Pressure and temperature patterns under the ischial tuberosities. , 1980, Bulletin of prosthetics research.

[7]  J. Mann Wind field simulation , 1998 .

[8]  Samuel A. Lippert,et al.  The degradation of the material properties of brain tissue as a function of time postmortem , 2001 .

[9]  J. Carney,et al.  An animal model and computer-controlled surface pressure delivery system for the production of pressure ulcers. , 1995, Journal of rehabilitation research and development.

[10]  R. Mayer EMBALMING: HISTORY, THEORY AND PRACTICE , 1980 .

[11]  U. Klose,et al.  Comparison of quantitative shear wave MR‐elastography with mechanical compression tests , 2003, Magnetic resonance in medicine.

[12]  A Gefen,et al.  Mechanical compression-induced pressure sores in rat hindlimb: muscle stiffness, histology, and computational models. , 2004, Journal of applied physiology.

[13]  A. Gefen,et al.  Are in vivo and in situ brain tissues mechanically similar? , 2004, Journal of biomechanics.

[14]  M. Tsokos,et al.  Pressure sores: epidemiology, medico-legal implications and forensic argumentation concerning causality , 2000, International Journal of Legal Medicine.

[15]  T A Wilson,et al.  Elastic constants of inflated lobes of dog lungs. , 1976, Journal of applied physiology.

[16]  A. Freeland,et al.  Viscoelastic response of intervertebral disks at audiofrequencies , 1971, Medical and biological engineering.

[17]  A. Gefen,et al.  Age-dependent changes in material properties of the brain and braincase of the rat. , 2003, Journal of neurotrauma.

[18]  C. Oomens,et al.  The etiology of pressure ulcers: skin deep or muscle bound? , 2003, Archives of physical medicine and rehabilitation.

[19]  Yossi Matias,et al.  Fast and Efficient Simulations among CRCW PRAMs , 1994, J. Parallel Distributed Comput..

[20]  M. Kosiak,et al.  Etiology of decubitus ulcers. , 1961, Archives of physical medicine and rehabilitation.

[21]  D S Childress,et al.  Indentor tests and finite element modeling of bulk muscular tissue in vivo. , 1996, Journal of rehabilitation research and development.

[22]  S M Peirce,et al.  Ischemia‐reperfusion injury in chronic pressure ulcer formation: A skin model in the rat , 2008, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[23]  C A Salzberg,et al.  Major risk factors for pressure ulcers in the spinal cord disabled: a literature review , 1996, Spinal Cord.

[24]  R. Allman,et al.  Pressure ulcer risk factors among hospitalized patients with activity limitation. , 1995, JAMA.

[25]  J M Huyghe,et al.  Mechanical blood-tissue interaction in contracting muscles: a model study. , 1998, Journal of biomechanics.

[26]  R. A. Shenoi,et al.  Quantification and localisation of damage in beam-like structures by using artificial neural networks with experimental validation , 2003 .

[27]  En-Jui Lee,et al.  The Contact Problem for Viscoelastic Bodies , 1960 .

[28]  W C Hayes,et al.  Flow-independent viscoelastic properties of articular cartilage matrix. , 1978, Journal of biomechanics.

[29]  Mark E Ladd,et al.  In vivo elasticity measurements of extremity skeletal muscle with MR elastography , 2004, NMR in biomedicine.

[30]  Philip Smith,et al.  Infected Pressure Ulcers in the Long-Term–Care Facility , 1999, Infection Control &#x0026; Hospital Epidemiology.

[31]  Nicholas W. Tschoegl,et al.  The Phenomenological Theory of Linear Viscoelastic Behavior: An Introduction , 1989 .

[32]  Mathias Fink,et al.  Transient elastography in anisotropic medium: application to the measurement of slow and fast shear wave speeds in muscles. , 2003, The Journal of the Acoustical Society of America.

[33]  Richard L Ehman,et al.  Evaluation of healthy and diseased muscle with magnetic resonance elastography. , 2002, Archives of physical medicine and rehabilitation.

[34]  M. Bliss,et al.  Aetiology of pressure sores , 1993 .

[35]  A. Mak,et al.  In vivo friction properties of human skin , 1999, Prosthetics and orthotics international.

[36]  D L Bader,et al.  Establishing predictive indicators for the status of loaded soft tissues. , 2001, Journal of applied physiology.

[37]  P. Rolfe,et al.  Skin surface PO2 and blood flow measurements over the ischial tuberosity. , 1982, Archives of physical medicine and rehabilitation.

[38]  G. H. Rose,et al.  Magnetic resonance elastography of skeletal muscle , 2001, Journal of magnetic resonance imaging : JMRI.

[39]  David J Margolis,et al.  Medical conditions as risk factors for pressure ulcers in an outpatient setting. , 2003, Age and ageing.

[40]  N. Tschoegl The Phenomenological Theory of Linear Viscoelastic Behavior , 1989 .

[41]  M R Drost,et al.  Passive transverse mechanical properties of skeletal muscle under in vivo compression. , 2001, Journal of biomechanics.

[42]  E. Heikkinen,et al.  Mechanical properties of fast and slow skeletal muscle with special reference to collagen and endurance training. , 1984, Journal of biomechanics.

[43]  I. Vesely,et al.  Role of Preconditioning and Recovery Time in Repeated Testing of Aortic Valve Tissues: Validation Through Quasilinear Viscoelastic Theory , 2000, Annals of Biomedical Engineering.

[44]  Richard L Lieber,et al.  Spastic muscle cells are shorter and stiffer than normal cells , 2003, Muscle & nerve.

[45]  J. W. Smith The elastic properties of the anterior cruciate ligament of the rabbit. , 1954, Journal of anatomy.

[46]  Y. Itzchak,et al.  Integration of plantar soft tissue stiffness measurements in routine MRI of the diabetic foot. , 2001, Clinical biomechanics.