EVALUATION OF TISSUE HEALTH AND INTERVENTIONS FOR THE
PREVENTION OF PRESSURE ULCERS IN PERSONS WITH SPINAL CORD
INJURY
by
GARY ANTHONY AUYONG WU
Submitted in partial fulfillment of the requirements For the degree of Doctor of Philosophy
Dissertation Adviser: Kath Bogie, D.Phil.
Department of Biomedical Engineering
CASE WESTERN RESERVE UNIVERSITY
May, 2013
CASE WESTERN RESERVE UNIVERSITY
SCHOOL OF GRADUATE STUDIES
We hereby approve the thesis/dissertation of
______Gary Anthony Auyong Wu candidate for the ______degreePh.D. *.
(signed)______Kath Bogie, D.Phil. (chair of the committee)
______Horst von Recum, Ph.D.
______Dustin Tyler, Ph.D.
______Heng Wang, M.D., Ph.D.
(date) ______March 11, 2013
*We also certify that written approval has been obtained for any proprietary material contained therein. Table of Contents
Table of Contents ...... iii
List of Figures ...... vi
List of Tables ...... viii
Abstract ...... ix
Chapter 1) Introduction ...... 1-1
1a. Research motivation ...... 1-1
i. Gluteal muscle geometry and composition ...... 1-2
ii. Impact on tissue health of dynamic cushion use ...... 1-3
iii. Impact on tissue health of gluteal NMES ...... 1-4
iv. Imaging the gluteal neurovascular anatomy ...... 1-5
1b. Spinal cord injury and pressure ulcer risk ...... 1-6
i. Definition of pressure ulcers ...... 1-6
ii. Pressure ulcer staging ...... 1-7
iii. Causes of pressure ulcers ...... 1-9
iv. Spinal cord injury ...... 1-16
v. Pressures ulcers and spinal cord injury ...... 1-19
vi. Cost of pressure ulcers ...... 1-20
1c. Interventions to prevent pressure ulcers ...... 1-22
i. Cushions for prevention of pressure ulcers ...... 1-23
ii. Tissue health assessment techniques ...... 1-26
iii. Electrical stimulation for improved tissue health ...... 1-29
Chapter 2) Tissue composition and implications ...... 2-33
2a. Preface ...... 2-33
2b. Literature review ...... 2-33
iii i. Muscle atrophy ...... 2-33
ii. Measuring adipose tissue ...... 2-34
2c. Not just quantity: Gluteus maximus muscle characteristics in able-bodied and SCI individuals – implications for tissue viability ...... 2-35
2d. Addendum...... 2-50
Chapter 3) Multi-factorial tissue health assessment (THEToolBox – Methods) ...... 3-53
3a. Preface ...... 3-53
3b. A multifactorial toolbox for tissue health assessment ...... 3-53
Chapter 4) The impact on tissue health of using a dynamic cushion (RERC results) ...... 4-102
4a. Preface ...... 4-102
4b. Differences in tissue health measurements when using a standard cushion and dynamic cushion...... 4-102
4c. Chapter conclusion ...... 4-126
Chapter 5) NMES and its effects on muscle mass ...... 5-127
5a. Preface ...... 5-127
5b. Assessment of gluteus maximus muscle area with image analysis programs ...... 5-127
5c. The effects of combined trunk and gluteal neuromuscular electrical stimulation on posture and tissue health in spinal cord injury ...... 5-149
5d. Chapter conclusion ...... 5-172
Chapter 6) Imaging the gluteal neurovascular anatomy ...... 6-173
6a. Preface ...... 6-173
6b. CT to visualize neurovascular anatomy ...... 6-173
Chapter 7) Thesis conclusions ...... 7-184
7a. Assessment of gluteal muscle geometry and composition using CT ...... 7-184
7b. Multi-factorial tissue health assessment of weight shifting maneuvers ...... 7-185
7c. The impact of trunk NMES on tissue health (Trunk study) ...... 7-186
7d. Imaging the gluteal neurovascular anatomy ...... 7-187
iv Chapter 8) Future work ...... 8-189
8a. Assessment of gluteal muscle geometry and composition using CT ...... 8-189
8b. Multi-factorial tissue health assessment for personalized pressure relief regimes . 8-189
8c. Determine changes in blood perfusion for person with PU occurence ...... 8-193
8d. Adaptive tissue loading and unloading responses ...... 8-195
8e. Improved imaging of the gluteal neurovascular anatomy ...... 8-197
8f. Tissue health in chronic SCI and other degenerative neurological diseases ...... 8-198
v List of Figures
Figure 1.1: Risk factors for pressure ulcer development leading to costs of daily living ...... 1-10
Figure 1.2: Pressure intensity and duration tolerance guidelines for people with SCI ...... 1-11
Figure 2.1: Pelvic region CT with scout view indicating the location of axial slices ...... 2-40
Figure 2.2: Gluteal muscle cross-sectional area at levels of interest...... 2-44
Figure 2.3: Representative axial CT slices at the level of the ischial tuberosities showing varying muscle composition...... 2-45
Figure 2.4: Average gluteal muscle tissue composition ...... 2-46
Figure 2.5: Injury level and muscle quality of participants grouped PU History ...... 2-51
Figure 2.6: Neurological level and muscle quality/muscle cross-sectional area (CSA) grouped by weight of participant...... 2-52
Figure 3.1: Representative cross section of interface pressure values...... 3-64
Figure 3.2: CONFORMat® Tekscan Clinical Seating System ...... 3-66
Figure 3.3: Radiometer® TCM400 system ...... 3-72
Figure 3.4: LaserFlo® BPM24415 SoftFloTMprobe ...... 3-77
Figure 3.5: THEToolbox Results Panel: Effects of weight shifting on sitting posture...... 3-92
Figure 4.1: Diagram of THEToolbox Assessment for each participant in the study ...... 4-106
Figure 4.2: Dynamic cushion in different inflation patterns with left and right ROI outlined in blue box. Representative graphs of mean contact pressures (MCP) with pressure relief using dynamic cushions ...... 4-111
Figure 4.3: THEToolbox measures for when grouped by PU history ...... 4-123
Figure 4.4: THEToolbox measures when grouped by neurological level ...... 4-124
Figure 4.5: THEToolbox measures when grouped by weight ...... 4-125
Figure 4.6: THEToolbox measures when grouped by myogenic contribution ...... 4-125
Figure 5.1: CT scan image locations used for assessments...... 5-134
Figure 5.2: Histograms showing differences in repeated measurements to the mean measurement for each muscle using ImageJ and VeVMD...... 5-138
vi Figure 5.3: Bland Altman analysis for each rater between image analysis programs...... 5-139
Figure 5.4: Longitudinal study for one patientover a period of 24 months ...... 5-142
Figure 5.5: Interval plot of measurements using (A) ImageJ and (B) VeVMD...... 5-142
Figure 5.6: Tissue health evaluation results panel: The effects of trunk stimulation on sacral sitting posture. A) Interface pressure distribution. B) Maximum interface pressure gradient. C) Tissue oxgenation ...... 5-164
Figure 5.7: Tissue health evaluation results panel: The effects of trunk stimulation on ‘normal’ sitting posture...... 5-166
Figure 6.1: CT scout image and surface reconstruction of pelvic CT image ...... 6-179
vii List of Tables
Table 1.1: Pressure Ulcer Staging ...... 1-8
Table 1.2: Cost of care according to severity of SCI ...... 1-18
Table 2.1: Tissue classification based on HU value ...... 2-42
Table 2.2: Participant demographics ...... 2-43
Table 2.3: Gluteus maximus muscle characteristics ...... 2-43
Table 3.1: Tissue health assessment tool timeline for CONFORMAT concurrent with TcPO2 or LDF sensors ...... 3-86
Table 4.1: Change in mean contact pressures (MCP) and TcPO2 during IPR...... 4-108
Table 4.2: Significant differences between mean contact pressures in the ROI during quiet seating assessments ...... 4-110
Table 4.3: Change in mean contact pressures MCP and TcPO2 for PR-DAve...... 4-112
Table 4.4: Blood flow contribution during pressure relief...... 4-114
Table 5.1: Repeated measurements for each image analysis program according to rater. .... 5-139
Table 5.2: Measurement means for each image analysis program...... 5-140
Table 5.3: Test for differences in precision of image analysis programs...... 5-140
Table 5.4: Population demographics and initial sitting posture...... 5-155
Table 5.5: Tissue health assessment timeline ...... 5-158
viii Evaluation of Tissue Health and Interventions for the Prevention of Pressure
Ulcers in Persons with Spinal Cord Injury
Abstract
by
GARY ANTHONY AUYONG WU
Persons with spinal cord injury (SCI) have atrophied muscle, leading to increased risk of developing pressure ulcers (PU). Even so, some persons with
SCI are more susceptible to PUs. The thesis presents several measurements of tissue health to better understand individual differences.
The gluteus maximus muscle of persons with SCI in the current study have increased intramuscular fat and decreased lean muscle which make the soft tissue around bony prominences prone to higher stress and strains.
Furthermore, atrophy is more pronounced in the region of the ischial tuberosities. A relationship was found between PU history with the gluteal muscle quality/composition but not with muscle cross-sectional area (CSA).
Weight redistributing cushions are prescribed to address the increased risk of developing PUs around the bony prominences. The Tissue Health Evaluation
Toolbox (THEToolbox) was used to determine the impact on tissue health of independent pressure relief (IPR) on a standard cushion and weight-shifting by a
ix dynamic cushion. The overall improvements in tissue health with use of
dynamic cushion are similar though smaller in magnitude to IPR. Differences
include prolonged increase in oxygenation during the weight-shifting
intervention period and smaller increases in metabolic, neurogenic and
myogenic contributions to blood flow during pressure relief. Sustained myogenic
contributions to blood flow were observed post-intervention with use of the
dynamic cushion. This could be evidence of prolonged influences to blood flow responses and different hyperemic response compared to IPR.
Neuromuscular electrical stimulation (NMES) is an approach that could address both extrinsic need for periodic, sustained weight shifting and intrinsic need to improve muscle geometry and quality. It has been shown that, gluteal muscle mass increased in persons with SCI with continued use of gluteal NMES.
Concurrent use of trunk and gluteal stimulation improved anterior/posterior postural misalignment for sacral sitters. The postural correction improved regional tissue health. There was a small positive impact on maximum IP gradient with improved lateral postural stability.
The case for individualized care is strengthened by the increase in both intramuscular and visceral fat together with varying levels of muscle atrophy and differing physiological responses to weight shifting as observed with the
THEToolbox.
x Chapter 1) Introduction
1a. Research motivation
All persons with spinal cord injury (SCI) are at risk of developing pressure ulcers
(PUs). As there are different levels and extents of injury, these individuals also present with different susceptibility and risk of developing PUs. The question still exists in regard to these individual differences where some persons have never developed PUs, while others have recurrent bouts of PUs. This presents a major concern in healthcare as PU care and management is associated with a large financial and personnel burden. Understanding the variability of tissue in the sitting region could help elucidate reasons for these differences. The thesis looks into measures of tissue health and proposes ways to determine the risk of developing pressure ulcers. It is followed by studying interventions and how they affect tissue health measurements.
Chapter 1-1 This thesis will address the following hypotheses:
i. Gluteal muscle geometry and composition
Hypothesis: Intramuscular fat infiltration in the gluteus maximus is present in
differential levels in SCI compared to able bodied (AB).
Studies involving chronic SCI tend to focus on muscle atrophy and regaining
muscle mass to improve tissue health. Computer Tomography (CT) can be used
as an alternative to Magnetic Resonance Imaging (MRI) to differentiate
intramuscular fat from lean muscle for persons who have implants that can be
affected by strong magnetic fields. There is increased intramuscular fat in the
thigh muscles of persons with SCI compared to AB counterparts [1]. Modeling of
muscles with intramuscular fat and scarring from previous pressure ulcers show
increased internal strains and stresses in the affected tissues during seating [2].
Our pilot study showed increased intramuscular fat infiltration in individuals
with SCI who had a history of PUs. The muscle located near regions of high
pressure ulcer risk had high levels of atrophy and intramuscular fat. . In a
secondary analysis, we found relationship of PU history with the gluteal muscle
quality/composition but not muscle cross-sectional area (CSA).
Chapter 1-2 ii. Impact on tissue health of dynamic cushion use
Hypothesis: Intermittent use of a dynamic cushion will produce
improvements in tissue health measurements during the dynamic phase
compared to static sitting.
Dynamic cushions are used for persons with high risk of developing PUs. They
are also occasionally prescribed for persons who currently have a PU and are not
able to adhere to prolonged bed rest. The aim of this study was to evaluate the
impact of using a dynamic cushion on the tissue health of wheelchair users and
test whether it can be an effective tool in preventing PUs. Tissue health
measurements including interface pressure mapping, transcutaneous oxygen
partial pressures (TcPO2) and blood perfusion measurements using Laser
Doppler flowmetry (LDF) were measured during static sitting, standard pressure relief maneuvers and during use of a dynamic cushion.
Dynamic cushions have been shown to have lower interface pressures during the low inflation phase of the cushion, comparable to tilting on a gel cushion [3,4].
The benefits of cycling of high to low pressures for short periods of time may outweigh the risks of higher interface pressure during high inflation phase.
Dynamic cushions would most likely benefit persons who have a higher level of
SCI and have difficulty performing effective weight shifting, but may also be useful as a PU prevention tool for individuals at risk of developing PUs [5].
Chapter 1-3 iii. Impact on tissue health of gluteal NMES
Hypothesis: Combined trunk and gluteal neuromuscular electrical stimulation
(NMES) alters seated posture and improves pelvic region tissue health in individuals with SCI.
Regular use of NMES for functional applications on regularly stimulated
muscles exhibited significant increases in thigh blood flow and quadriceps
muscle depth, both positive changes in regional tissue health [6]. NMES system increased unloaded TcPO2 measurements for persons with SCI following an exercise regimen for several weeks [7]. Several other studies have also observed
TcPO2 in loaded and unloaded conditions. This would be the first time an implanted NMES system was evaluated for its potential to provide improvements with tissue health of a seated individual with measurements of
interface pressures and local tissue oxygenation due to postural changes induced
by NMES.
Chapter 1-4 iv. Imaging the gluteal neurovascular anatomy
Hypothesis: CT with contrast can be used to locate the gluteal motor point in
persons with SCI who have significant muscle atrophy.
CT with contrast was used to determine the gluteal neuroanatomy. Nerves such as the inferior gluteal nerve (IGN) are hard to locate and are deep in the muscle bed and sometimes have a varied course due to altered anatomy or surgery. The aim of the study was to refine the efficacy of the minimally invasive implantation technique. Visualizing the gluteal neurovasculature in sufficient detail can allow placement of the stimulating tip of an intramuscular electrode for better muscle recruitment to achieve a stronger motor response. More accurate placement could also decrease current leak to nearby sciatic nerve and its distal nerve branches. The stimulating tip placed at the branching of the nerve would recruit the majority of the nerves that innervate the gluteus maximus muscle. By stimulating the majority of the IGN, muscle recruitment is optimized for maximal contractile response. Furthermore, pre-surgical planning for the placement of the stimulating tip could decrease surgical time by decreasing probing and implantation times. CT assessments of the pelvic region in SCI subjects were carried out to determine regional vascular and nervous anatomy.
Chapter 1-5 1b. Spinal cord injury and pressure ulcer risk
An overview of pressure ulcers in people with spinal cord injury is presented together with current interventions to address the issue.
i. Definition of pressure ulcers (PUs)
A pressure ulcer is defined by the National Pressure Ulcer Advisory Panel
(NPUAP) as a localized injury to the skin and/or underlying tissue usually over a bony prominence. Often it is the result of unrelieved pressure for a prolonged period of time, or pressure in combination with shear and/or friction [8]. As such, weight bearing tissues over bony prominences, such as the sacrum and ischial tuberosities (ITs) are susceptible to pressure ulcers. The ankles and the balls of the feet are also prone to pressure ulcers in people with diabetes who have impaired circulation. PUs are also known as decubitus ulcers, ischemic ulcers, bed sores or pressure sores. In this thesis all such chronic wounds will be generally referred to as PUs.
Chapter 1-6 ii. Pressure ulcer staging
The most common indication that a PU is developing is the appearance of a red area, or erythema. Ordinarily, erythema should clear within 30 minutes after pressure is released from the area. Redness not clearing is indication that tissue damage has occurred [9]. A person with dark skin may also see a change in their skin color, though this is not easily observed [10]. Other signs that indicate the beginning of a PU is an area of skin that is warmer than normal or adjacent areas or a change in the skin's texture, harder, dry, flaky, ashy and even lighter in color than adjacent skin [11].
PUs range in severity from mild (minor skin erythema) to severe deep tissue injury (DTI) that affects even muscle and bone). PUs are staged according to the severity of the wound and the tissues involved (see Table 1.1).
Chapter 1-7 Table 1.1: Pressure Ulcer Staging (as defined by the NPUAP [8])
Stage of Pressure Definition Ulcer Suspected Deep Damage is suspected to be in the underlying soft tissue Tissue Injury due to pressure and/or shear. There is a localized area with discoloration of intact skin or blood-filled blister due to damage. The area may be preceded by tissue that is painful, firm, mushy, boggy, warmer or cooler as compared to adjacent tissue. Stage 1 Damage is limited to the epidermal and dermal layers of skin. The skin is not broken and the redness does not turn white when touched (non-blanchable erythema). This is usually found over a bony prominence. Stage 2 Damage extends beyond the epidermal and dermal layers of the skin to the adipose tissue. The skin is slightly broken. The sore appears to be an abrasion, blister or small crater. Stage 3 Damage extends through all the superficial layers of the skin, adipose tissue, down to and including the muscle. The ulcer appears as a deep crater and damage to adjacent tissue may be present. Stage 4 Damage includes destruction of soft tissue structures and involves bone or joint structures. Undermining of tissue and sinus tracts may be associated with these ulcers. Unstageable A full thickness pressure ulcer is unstageable if there is slough or eschar in the wound bed that prevent examination of the extent and depth of the ulcer.
Chapter 1-8 iii. Causes of pressure ulcers
It is understood that prolonged applied pressure and shear stress on the skin are
primary risk factors in PU development. There are several intrinsic and extrinsic
factors that impact the risk for developing pressure ulcers. Extrinsic factors that
cause pressure ulcers include shear stress, prolonged high pressures, and damp
skin that breakdown the integrity of the skin. Intrinsic factors include muscle
atrophy and change in tissue physiology, which include both muscle and soft tissue physiology. Impaired circulation and nutrition also lead to changes in
tissue health. Clinically, it is not known why one individual might develop
recurrent PUs, while given similar predisposing risk factors, another individual
does not [12].
A number of contributing or confounding factors are associated with pressure
ulcers (see Figure 1.1), but the relative significance of each of these factors is yet
to be fully elucidated [8,12].
Chapter 1-9
Figure 1.1: Risk factors for pressure ulcer development leading to costs of daily living. [13]
Risk factors for developing pressure ulcers
The following are extrinsic risk factors involved in soft tissue damage and should be addressed in order to prevent injury:
• Normal applied pressure - unrelieved pressure on the tissues can
compress blood vessels. An inadequate blood supply or circulation to a
local area due to a blockage of the blood vessels, ischemia, can result.
Ischemia would hinder the supply of nutrients and oxygen for proper
tissue function. Resumption of blood flow after ischemia (reactive
hyperemia) has been known to have deleterious effects to neural and
cardiac tissue. Furthermore, the absence of blood flow also prevents
removal of cellular wastes and leads to the eventual breakdown of cells in
Chapter 1-10 the tissue. An early indicator of irreversible tissue damage is localized
warming of the skin and erythema persistent after pressure is removed.
The amount and duration of pressure to cause damage depends on the
individual’s tissue tolerance. The key factors are intensity and duration of
pressure (See Figure 1.2).
Figure 1.2: Pressure intensity and duration tolerance guidelines for people with SCI (Reswick and Rogers 1976 [14]) and preliminary observations in canine trochanters (Kosiak, 1959 [15]). Figure courtesy of Digital resource foundation for the Orthotics and Prosthetics Community
• Shear – most often occurs as a person slides or is repositioned across the
bed or seat. Blood vessels in the tissue can stretch or bend and cause tissue
damage at lower applied loads than normal. Even slight rubbing or
friction on the skin may cause minor PUs. Shearing occurs when the
skeleton and deep fascia slide downwards with gravity or direction of
movement, whilst the skin and upper fascia remain in the original
Chapter 1-11 position. Deep tissue necrosis can occur when the shearing between two
layers of tissue leads to stretching, kinking and tearing of vessels in the
subcutaneous tissues. Shearing forces should not be considered separately
from pressure: they are an integral effect of pressure.
• Friction - occurs when two surfaces move relative to each other. It often
removes superficial layers of skin. Friction damage often occurs as a result
of poor lifting techniques [16,17,18].
• Microenvironment of the skin – urinary and fecal incontinence, wound
drainage and sweat are potential irritants to the skin and can cause
changes in the following micro-environmental conditions
o Moisture – Dry skin decreases the elasticity of epidermal and dermal
layers and leads to cracking or splitting of the upper layers of skin,
exposing a wound. Prolonged dampness of vulnerable skin, together
with pH, temperature and friction, soften the skin and make it
susceptible to breakage [19].
o pH – although the skin has tolerance to changes in pH, a change in
external pH can lead to breakdown of collagen fibrils in the skin
leading to irritation and eventual breakdown of skin.
o Temperature – heat accumulation in the tissue requires increased
nutrient consumption as metabolism is increased. The addition of
unrelieved external pressure or shear forces reduces blood flow by
obstructing blood vessels. If the tissue is deprived of oxygen and
Chapter 1-12 nutrients for an extended period it may cause cell death [20].
Furthermore prolonged application of high temperatures on the body
leads to increased sweating which changes moisture and pH, and can
be detrimental to tissue health as described above.
An individual’s potential to develop pressure ulcers may be influenced by the following intrinsic risk factors which should be considered when performing a risk assessment (adapted from NCIS 2005 [21,22]):
• Reduced mobility or immobility - a key factor in the development of
pressure ulcers is reduced mobility or immobility. A number of studies
have identified reduced mobility as an independent risk factor in pressure
ulcer development [23,24]. Immobility is a significant risk factor in
individuals who develop PUs.
• Sensory impairment – results in a reduced (or lacking) stimulus to move
to relieve pressure. For example neurological damage or disorder results
in reduced sensation and thus insensitivity to pain or discomfort. There
are certain groups of individuals that may suffer from sensory
neuropathy, for example, individuals with SCI or with diabetes.
• Level of consciousness - a reduced level of consciousness may reduce an
individual’s awareness of the need to relieve pressure. Likewise an
anesthetized person cannot reposition themselves.
• Previous history of pressure damage places individuals at a greater risk of
developing further ulcers than previously PU free individuals [25, 26, 27].
Chapter 1-13 • Tissue thickness and condition – tissue thickness covering the IT provides
padding that would help prevent ischemia and development of PUs. The
thickness of muscle, adipose tissue, and skin affects the distribution of
pressures over a bony prominence [28].
• Acute illness - clinical experience, observation and emerging research
suggests that ill individuals are vulnerable to developing pressure ulcers.
This is because of co-morbidities including heart failure, vasomotor
failure, vasoconstriction due to shock, low blood pressure, pain [29],
which prevents movement and increases oxygen demand. Furthermore,
during and after anesthesia, immobility and temperature changes can also
increase vulnerability to developing PUs [30].
• Age (less than 5 or more than 65 years of age) - neonates and very young
children are at risk of developing PUs. The national incidence of PUs in
the critically ill and injured children is reported to be at 13-27% [31]. Their
skin is still maturing and their head-to-body weight is disproportionate. It
is currently thought that the factors that place children and neonates at
risk are the same as those that place adults at risk, but the sites of greatest
risk for pressure damage and the nature of the injury may differ [32]. Skin
integrity, vascular flow, inadequate redistribution of pressure seem to be
particular risk factors in this population together with pressure or shear
due to mechanical ventilation, beds and clothing [33]. Advancing age is
associated with an increase in cardiovascular and neurological disease,
Chapter 1-14 and changes to the resilience and elasticity of the skin. Individuals over 65
years of age are at greater risk than the general population of developing
pressure ulcers [34,35,36].
• Vascular disease - reduces total blood flow and impairs micro circulation
potentially making individuals more vulnerable to pressure necrosis.
• Severe chronic or terminal illness - places individuals at greater risk
because of multi-organ failure, poor perfusion and immobility, etc.
• Nutritional status - impairment of healing occurs with mild malnutrition.
Related to this is body weight, both emaciated [23,37] and obese
individuals [38] may be more vulnerable to pressure damage [39].
Dehydration may reduce the elasticity of tissues and thus increase tissue
deformability under pressure or friction.
• Medications – several classes of medication can impact PU risk both
directly and indirectly. Sedatives and hypnotics can make an individual
excessively sleepy and reduce mobility. Analgesics may reduce normal
stimulus to relieve pressure. Inotropes cause peripheral vasoconstriction
and tissue hypoxia. Non-steroidal anti-inflammatory drugs impair
inflammatory responses to pressure injury. Though this list is not
exhaustive, it is an example of how medication can affect intrinsic
conditions leading to an increased vulnerability to develop PUs.
Practitioners should refer to pharmacists for specialist advice.
Chapter 1-15 iv. Spinal cord injury
The human spinal cord carries nerve tracts that connect the central nervous
system to peripheral nerves. The brain and spinal cord make up the central
nervous system. The brain sends and receives signals through the spinal cord to
the peripheral nervous system. When damage occurs to the spine, depending on the extent and severity, muscle control is lost and sensory impairment occurs one to two spinal cord levels below the level of injury. Likewise physiological changes happen below the level of injury.
The incidence of SCI is approximately 40 cases per million population in the US, or approximately 12,000 new cases per year (1970s). In the US, the number of people living in 2010 with SCI was approximately 265,000 individuals [40]. From
2005-2010, the average age at injury was 40.7 years. The primary cause of all traumatic spinal cord injury is vehicular motor accidents (40.4%), followed by falls (27.9%)violence which is primarily gunshot wounds (15%), sports (8%) and others unknown (8.7%)[40]. Note that the population data taken here is taken
from the SCI model system. Although extensive, only select hospitals across the
United States participate in the Model SCI System. Our studies included
participants who are involved with the SCI Model System or are veterans and
receive care from the Veteran Administration (VA). VA hospitals have a high
proportion of individuals with long-term chronic SCI and disorder [41], who
Chapter 1-16 receive life-long care in both urban and rural areas. The model SCI systems centers focus primarily on acute traumatic SCI in urban areas.
Life expectancy and lifetime costs of people with SCI
Life expectancy is 74 years for individuals who acquire or develop SCI at any age compared to 80 years for able-bodied (AB) individuals. The average age of injury is 40 years. Thus, the average life expectancy for individuals following SCI is
nearly 35 years [40].
It can be noted that the mean age of injury does not necessarily reflect the general
population as a bimodal distribution of the types of injuries that are sustained
has been observed [40]. Typically SCI is traumatic for those who are injured in
their early 20s. Those who sustain an SCI in their late 50s are due to non-
traumatic causes or falls.
A longitudinal study in the United Kingdom followed 122 individuals with SCI
for 25 years who were recruited from 1990-1993, and followed-up in 2006. The
mean age at injury was 21.8 years at initial recruitment. The study showed that
although Quality of Life (QoL) measurements were pretty stable, and there was
no statistical difference in pressure ulcer prevalence (12.6% in 1990 and 15.8% in
2006), up to 40% of participants reported having had one or more PUs in
between follow ups. The average yearly health care and living expenses and the
Chapter 1-17 estimated lifetime costs that are directly attributable to SCI vary greatly according to severity of injury.
Table 1.2: Cost of care according to severity of SCI
Severity of Injury Average Yearly Expenses Estimated Lifetime (in 2010 dollars) Costs by Age at Injury (discounted at 2%) First Year Each 25 years 50 years old Subsequent old Year High Tetraplegia (C1-C4) $985,774 $171,183 $4,373,912 $2,403,828 Low Tetraplegia (C5-C8) $712,308 $105,013 $3,195,853 $1,965,735 Paraplegia $480,431 $63,643 $2,138,824 $1,403,646 Incomplete Motor $321,720 $39,077 $1,461,255 $1,031,394 Functional at Any Level Data Source: Economic Impact of SCI [42,43]
With the high cost of care for individuals with SCI it is important to understand the health problems associated with the medical costs. The most frequently reported health problems for individuals with SCI were urinary tract infections, upper extremity pain, fatigue, pressure ulcers, constipation, and bowel accidents.
The top three primary causes of death in SCI are diseases of the respiratory system (21.2%), where seven out of ten respiratory cases were of pneumonia. The second leading cause of death was infectious and parasitic diseases (11.1%).
Nineteen of twenty cases were of septicemia, usually associated with pressure ulcers, urinary tract or respiratory infections. [44].
Chapter 1-18 v. Pressures ulcers and spinal cord injury
Individuals with SCI are most susceptible to PUs acutely following injury. PUs
can develop within a few hours of immobilization, with a high incidence of
hospital acquired(nosocomial) PU as they are brought to the Emergency
Department to be stabilized. PU prevention has become a major concern for
hospitals as Medicare no longer covers for nosocomial PUs since October 2008
[45].
Despite research and efforts in preventing PUs, development of a pressure ulcer
is still one of the most prevalent secondary complications in people with SCI [46].
After spinal cord injury, 15.2% of individuals with SCI had at least 1 PU within
the first annual follow-up evaluations [46]. Of all individuals with SCI, 80% will develop a PU over their lifetime and 30% of individuals will develop more than 1
PU [9]. People with impaired sensation, advanced age and prolonged immobility are at risk for PU. The primary reason for individuals with SCI developing
pressure ulcers is the combination of losing the neurological protective sensation
that the tissue is being harmed and prolonged immobility. The high recurrence
rate can be attributed both to healed scar tissue that is prone to damage and
impaired sensation.
Furthermore, individuals with SCI are subject to many of the intrinsic and extrinsic factors for developing pressure ulcers. Typically, individuals with SCI
Chapter 1-19 have impairments in the vascular system below the level of injury. [This will be discussed further in Chapter 3] Regional blood flow is adversely affected, due to reduced patency of the remaining vascular supply and muscle atrophy. The reduced blood flow to the tissue makes the individual susceptible to develop
PUs [47].
vi. Cost of pressure ulcers
PUs are non-healing wounds that continue to be a major secondary complication for many individuals with chronic disease [48]. They cause detriment to a person’s quality of life and further psychological distress. In addition there is a significant healthcare burden due to prolonged hospitalization and bed rest to keep pressure off the wound and increased critical care to keep a PU clean. The many negative effects of PU development drive a continued need for better prevention strategies [49].
According to the NPUAP inclusive pressure ulcers cost, for US healthcare systems are 1.3 – 11 billion USD yearly [50, 51]. In the UK the cost is 2.6 -4 billion
USD [52]. Literature on the economics of PU is scarce and some are several decades old. In 1999, it was estimated that average treatment cost per hospital stay for a PU ranges from $2,000 to $30,000 for Stages 1 to 3 and at least $70,000 to more than $129,000 for Stage 4 ulcers.[53,54] The cost of PU can be estimated based on inflation, cost of care and person hours in care.
Chapter 1-20 The occurrence of PUs in all senior citizens is 0.15% for ages 65 to 74 and 0.81% for ages 75 and older [55]. From 1993 to 2006 the number of hospitalizations for pressure ulcers as a primary diagnosis rose to 45,500 which is an increase of
27.2% [56]. A primary diagnosis of PU does not paint the whole picture as PUs
lead to grave conditions such as septicemia or infections that result in
hospitalization. When hospitalizations related to PUs is taken into account the numbers increase from 281,300 to 503,300 individuals, a rise of 80%. Out of
hospitalizations with pressure ulcers as a secondary diagnosis 1 in 8 is fatal [56].
Preventive strategies will improve quality of life and also minimize the treatment
costs of PUs. Padula et al. found that prevention was cost saving and resulted in
greater expected effectiveness when compared with the standard care approach
per hospitalization. The expected cost of prevention was $7276.35, and the
expected effectiveness was 11.241 quality-adjusted life years (QALYs). The
expected cost for standard care was $10,053.95, and the expected effectiveness
was 9.342 QALYs. Their multivariate probabilistic sensitivity analysis showed
that prevention resulted in cost savings in 99.99% of the simulations. The
threshold cost of prevention was $821.53 per day per person, whereas the cost of
prevention was estimated to be $54.66 per day per person [57].
Chapter 1-21 1c. Interventions to prevent pressure ulcers
Current techniques for prevention of pressure ulcers
The physiological changes in individuals with SCI predispose them to
developing PUs. Traditional techniques to reduce PU incidence have focused on
extrinsic risk factors, for example shifting weight every 15 minutes, repositioning
every hour, inspecting the skin at least once a day, and using cushions for seating
surfaces to improve regional pressure distribution [58]. The individual with SCI
should also consider their postural alignment, distribution of weight, balance
and stability, and pressure relief when positioning in a wheelchair.
Rehabilitation programs also provide wheelchair users and their caregivers with
education on the importance of regular pressure relief procedures.
Individuals with SCI are able to perform different regular pressure relief
typically depending on their level of injury. Individuals with SCI who have
injury levels of C4 or higher can use power tilt wheelchair or a dynamic cushion
for regular pressure relief. Individuals with injury levels of C5 or C6 are usually
able to lean forward or side-to-side. Individuals with injury levels of C7 and
below can usually perform a wheelchair push-up [9].
There remain a significant number of people who, despite the best standards of care, continue to develop major pressure ulcers. These individuals are frequently unable to maintain a regular pressure relief regime and standard pressure relief
Chapter 1-22 cushions are inadequate [59]. Several primary factors are related to the intrinsic changes in the paralyzed body leading to poor extrinsic pressure distributions.
For example, severe disuse muscle atrophy in the gluteus maximus could increase applied interface pressures over bony prominences while seating. The cushioning effect of a thick muscle and tissue that distributes the pressure over a bony protrusion is diminished, thus the seating interface pressures are concentrated to a smaller contact area.
i. Cushions for prevention of pressure ulcers
Prevention of pressure ulcers should a major objective in the rehabilitation of
individuals with SCI. The primary risk factor for pressure ulcer is prolonged
high pressures. Mattress surfaces and wheelchair cushions are frequently
prescribed to minimize pressures and thus prevent PUs. The use of pressure
relieving surfaces to reduce the risk of developing a PU in the population with
SCI [60] can result in health service efficiencies and quality of life gains for
individuals [61].
It is economically sound to use high specification foam rather than standard
hospital foam mattresses in the people at high risk of developing a PU. A study
in Ireland shows that the additional cost of using high specification surfaces is
£3,314. The cost of care for an individual who developed a PU is £64,199. Overall
Chapter 1-23 there is a cost saving of £60,885 if a high specification surface prevents the
development of a PU [62].
Different types of cushions have been employed to decrease the pressures
underneath the bony prominences during long periods of sitting. The cushions
typically in use are foam cushions, air cushions and gel cushions; dynamic
cushions were also used in our study.
1) Foam cushions are the most basic of cushions. They are lightweight, simple
and have minimal maintenance issues. Physical therapists, rehabilitation professionals, and cushion users have observed that this type of wheelchair seat cushions are among the least effective cushions with regard to sustained seat- related skin and pressure management [63].
2) Air cushions are cushions with compartmentalized bladders filled with air.
The fluidity of the air in the bladders allow for easier weight shifts and redistribution of weight on a surface [ 64]. Depending on the construction and
design, this type of cushion can also permit circulation of air on the skin surface.
3) Gel cushions exhibit excellent pressure distribution properties and typically
employ a combination of foam as a base structure and a gel-filled or fluid-filled
cell. From a pressure relief perspective, the wheelchair cushion's gel or fluid
Chapter 1-24 component may be thought of as simulating an additional layer of flesh
providing an additional layer of cushioning and redistribution of pressures from
bony prominences that are prone to high pressures [64].
4) Dynamic cushions use mechanically active or dynamic components. This type of cushion is particularly effective for individuals with acute mobility restriction as may occur from a high level spinal cord injury or from a non-injury-related
restriction such as the cockpit seat of a fighter plane. Dynamic wheelchair
cushions typically employ actively pressurized air cells to facilitate pressure
management. Dynamic cushions are the most costly and mechanically complex
of all cushion types. Unlike other cushion types, dynamic cushions are typically
powered—usually with a battery or other electrical source [64]. A dynamic cushion automatically performs temporally cycled pressure reducing actions at strategic locations across the buttocks area. The localized pressure reductions occur at the expense of pressure increases (of equal magnitude and duration) at less critical areas, providing pressure redistribution and effective pressure management. A dynamic wheelchair cushion may not be needed for a person with paraplegia or for someone who maintains some independent mobility.
However, a person whose impairment involves high-level quadriplegia may find a dynamic cushion to be an effective seating solution since their impairments deter them performing a PU prevention regimen.
Chapter 1-25 ii. Tissue health assessment techniques
Pressure ulcers primarily develop over the ischial tuberosities in wheelchair users. As such, it is important to study the tissue health of the tissue and gluteus maximus muscle which lie over the ischial tuberosities. Several techniques can be utilized to study the tissue health as presented below.
1. Interface Pressure Monitoring
Pressure mapping devices usually consist of an array of pressure sensors on a flexible fabric that is used to measure pressures in the interface of skin (usually with clothing) and the support surface. The pressures are typically color coded similar to a heat map where red corresponds to higher pressures and blue corresponds to lower pressures. As such, the interface pressure mapping gives a topographical picture of where the highest pressures are located and how pressures are distributed. Pressure mapping is a widely accepted assessment tool to evaluate and adjust cushions to improve the distribution of pressure on the support surface interface [65,66].
2. Transcutaneous Oxygen Measurement (TcPO2)
Oxygen is required in the metabolic processes of muscle and is a good indicator of tissue health. The transcutaneous oxygen tension electrode/sensor allows the measurement of oxygen tension across the surface of the skin. Transcutaneous oxygen tension measurements have been used to study oxygen tensions of
Chapter 1-26 individuals with circulatory impairments such as SCI, diabetes, and even
premature babies. The measurement is sensitive to a hemispherical space with a
1.5 millimeter radius centered at the tip of the electrode. Because of this
measurement depth, measurement is partially limited to venuoles and arterioles
close to the epithelium. To functionally estimate the oxygen tension in the
muscles overlying the IT, the electrode is heated to 42°C to open blood vessels in
the capillary bed. The oxygen tension in the perfused capillary bed gives an
estimate of the oxygen available in deeper vasculature, which supplies the
muscle bed.
3. Laser Doppler Flowmetry
Blood flow in the tissue reflects healthy circulation where blood is able to carry
oxygen and other nutrients to the tissue and also allows the diffusion and
delivery of wastes out of the tissue. The LaserFlo BPM2 system uses a low
powered laser light device to measure blood flow, blood velocity and blood
volume. The low powered laser light is directed towards the blood vessels in the
tissue. Laser Doppler flowmetry uses the refraction and time of return to
calculate the blood flow measurements.
4. Metabolic studies
Creating models for PUs have led to the development of studying metabolites
that are present in tissue that is subject to high prolonged pressures. These are
Chapter 1-27 understood to be indicators of developing PUs. Such metabolites include increased urea, lactate, chloride other acids in the tissue [67]. Assays for inflammatory cytokines are being studied [68,69] to better understand the inflammatory response to PUs for individuals with SCI.
5. Muscle geometry and composition
Muscle cross-sectional area is related to the amount of force that a contractile muscle can apply during exercise. The muscle CSA gives an idea of muscle mass and the extent of atrophy. Adipose tissue infiltration of muscle is common in neurological disease and SCI. Adipose tissue replaces muscle fibers in atrophied muscle changing its quality. Increased adipose tissue is related to glucose retention in the cells, increasing the risk of diabetes. Muscle atrophy has implications in pressure ulcer risk. The atrophied muscle reduces tissue available to absorb the pressures on bony prominences. The increase in adiposity changes the elastic and absorption characteristics of muscle tissue making it more susceptible to shear forces that may lead to even aggravated pressure ulcers such as deep tissue injuries.
[Tissue health measurements are further discussed in Chapter 3 and its analysis in Chapter 4]
Chapter 1-28 iii. Electrical stimulation for improved tissue health
Despite the regular use of cushions and different means of PU prevention, PUs
still occur in many individuals with SCI. The use of cushions and offloading only
address external risk factors. Electrical stimulation is an approach that addresses
internal risk factors such as increasing muscle mass that improve pressure
distribution and providing contractions that provide benefits such as increased
circulation. The use of electrical stimulation in the rehabilitation setting has
become more widespread in hospitals, clinics, outpatient settings and even at
home[7]. Electrical stimulation can be divided into several categories depending
on use, one such division is surface, percutaneous and implanted stimulation.
Surface electrical stimulation (SES) delivers electrical stimulation by placing
electrodes on the surface of the skin and exciting the underlying muscles to produce a contraction. It has many clinical applications, it is used to improve circulation and at low frequencies (<10Hz) is used to contract weak or unused
muscles. At higher frequencies, (>50Hz) it is used as an electroanalgesic for low
back pain, neurogenic pain, muscle pain. SES has been employed for exercise to
condition the thigh muscles of persons who showed increases in thigh blood
flow and quadriceps muscle depth [6]. Increases in muscle cross-sectional area in
individuals with SCI were also observed following a weekly regimen of lower
extremity cycling with SES [70]. Placement of SES may vary with each application and is dependent on a competent therapist, if self-administered it is
Chapter 1-29 easy to misplace, decreasing repeatability and effectiveness of the results.
Scremin et al [70] observed that increases in muscle size were directly related to
proximity of the muscle to the stimulating electrodes.
Percutaneous system electrodes have a stimulating source or control unit outside
of the body but the electrodes are fed through the skin allowing the stimulating
tip to have close contact to the muscle and nerves that are to be stimulated. Since
skin greatly increases electrical resistance, percutaneous systems improve on the
concept of surface electrodes, bypassing the skin which allows the use of smaller
electrical currents. Neuromuscular electrical stimulation (NMES) further improves effectiveness of stimulation by placing the stimulating tip at the motor point, directly stimulating the nerve and decreasing by an order of magnitude the amount of stimulation needed to elicit a contraction. The nerve is the physiological pathway whereby muscles are contracted. One nerve may be
connected to several and hundreds of muscle fibers. The stimulated nerve
delivers an electrical impulse to its innervated muscle evoking a response such as
a muscle contraction when an appropriate amount of current is delivered.
Percutaneous systems can be divided into intramuscular electrodes and nerve
electrodes. Intramuscular electrodes target the muscle and individual muscle
fibers are stimulated to produce a contraction. Typically intramuscular electrodes
are used with people who have flaccid paralysis which is due to lower motor
Chapter 1-30 neuron injury where the nerves are damaged akin to muscles denervation. Nerve
electrodes target the nerves itself which allows a smaller amount of current,
because as the nerve is stimulated the signal is passed to the muscles to contract
similar to the way our brains control muscles through nerves. Nerve stimulation
is used when an individual has upper motor neuron injury where the nerve to
the muscle of interest is intact. An implanted system carries with it the benefits of
a targeted placement of electrodes, thus minimizing contraction of unintended or opposing muscles. An implanted stimulator also obviates the need for maintaining hygiene at the site where a percutaneous electrode enters the skin, thus reducing possible infections. Implanted electrodes can also be divided by function and location such as spinal stimulators, muscular stimulators and cardiac pacemakers, brain stimulators.
Bogie et al. [71] have shown increased tissue oxygen levels and increased gluteal thickness in paralyzed gluteal muscles with regular use of NMES. Withdrawal of stimulation results in a reversal of improved tissue health and decreased gluteal thickness [72]. Continuous use of gluteal NMES is therefore indicated for
individuals at high risk of PU development. A surface stimulation system
requires daily proper placement of electrodes on the surface to produce a
suitable response. Although a percutaneous system addresses this problem, there is still a need for daily maintenance and cleaning of where the wires exit the skin.
Chapter 1-31 For increased ease and reliability of long-term use, fully implanted stimulation systems are indicated. Chapter 5 discusses NMES of gluteal muscles further.
Improving the localization of peripheral nerves has broad reaching applications surgical and imaging procedures. Nerves could be avoided during flap surgeries and soft tissue reconstruction. Likewise nerves could be properly located for more precise peripheral nerve stimulation for both sensory (nerve block of pain and anesthesia or sensory stimulation) and motor (block and/or stimulation of contractions)
One of the major challenges in implantation of stimulators is to improve the clinical accuracy of the implantation. The use of imaging for surgical planning and stereotactic devices could greatly improve mechanical accuracy, but there is a difference in mechanical accuracy between the optimal performance of a stereotactic system and clinical accuracy of locating the nerve [73]. Studies on visualizing neurovasculature will be discussed in Chapter 6.
Chapter 1-32 Chapter 2) Tissue Composition and implications
2a. Preface
A person with spinal cord injury (SCI) has a high risk of developing pressure
ulcers (PU), though it is unclear what causes pressure ulcers to actually
develop. Some individuals with SCI remain PU free while others experience a
recurring cycle of tissue breakdown. Detailed analysis of gluteal muscle
characteristics may provide insights to local tissue viability variability. The
primary study hypothesis was that not only do persons with SCI have muscle
atrophy but they have altered muscle composition compared to able-bodied
(AB) which can be observed with CT scans. Changes in muscle composition
could contribute to altered tissue oxygenation and blood flow characteristic
responses which will be discussed in later chapters.
2b. Literature review
i. Muscle atrophy
Disuse muscle atrophy is a prevalent consequence of SCI. Muscle atrophy has
substantial effects on shear and stresses that can lead to tissue breakdown,
both at surface-originating PU and DTI. The substantial muscle atrophy in SCI
produced larger interfacial pressures compared to healthy counterparts.
Though the absolute internal pressures remained similar, they were localized
in a smaller region for SCI [74]. Internal stresses and strains are higher in
paraplegics compared to their nondisabled counterparts during prolonged
Chapter 2-33 sitting [75]. Internal muscle tissue stresses and deformations in the buttocks of
patients with SCI are likely to be greater than in AB individuals because of the
reduction in muscle thickness. This endangers the integrity and viability of the
muscles in these patients [76]. Modeling of tissue thickness shows that tissue
deformation depends considerably on relative stiffness values of different
tissues. The decrease in muscle thickness and stiffness in turn led to increased
maximum shear strains and deformations [77].
ii. Measuring adipose tissue
Currently most clinical studies estimate muscle mass and body mass index
(bmi), which is an estimate of the amount of visceral fat in the body. Many of
these studies on adipose tissue do not consider intramuscular fat infiltration.
There have been a few MRI studies of the thigh muscle that show muscle
atrophy accompanied by increased intramuscular fat during the chronic phase
of SCI compared to nondisabled controls. This increase in percentage of
intramuscular fat constituting thigh muscles is 3 to 4 fold that of age-matched
controls [1,78]. Progressive amounts of intramuscular fat were correlated with
increasing percentage of muscle volume exposed to such critical strains and
stresses [2].
Chapter 2-34 2c. Not just quantity: Gluteus maximus muscle characteristics in able- bodied and SCI individuals – implications for tissue viability
Submitted Paper (in press)
Title: Not just quantity: Gluteus maximus muscle characteristics in able- bodied and SCI individuals – implications for tissue viability
Gary A Wu, M.S.1, 2, Kath M Bogie, D.Phil 1, 3
1. Advanced Platform Technology Center, Louis Stokes Cleveland Department of
Veterans Affairs Medical Center, Cleveland, OH 44106 USA.
2. Department of Biomedical Engineering, Case Western Reserve University, Cleveland,
OH, 44106 USA
3. Departments of Orthopaedics and Biomedical Engineering, Case Western Reserve
University,Cleveland, OH, 44106 USA
Chapter 2-35 ABSTRACT
Study Aim: Some individuals with spinal cord injury (SCI) remain pressure ulcer
(PU) free whilst others experience a recurring cycle of tissue breakdown.
Detailed analysis of gluteal muscle characteristics may provide insights to local tissue viability variability. The study hypothesis was that SCI individuals have altered muscle composition compared to able-bodied (AB).
Materials: Ten AB and ten SCI received a supine pelvic CT scan, with contrast.
Methods: Cross-sectional area (CSA) and overall muscle volume were derived using image analysis. Gluteal muscle tissue type was classified at the S2/S3 sacral vertebrae midpoint, the superior greater trochanters margin (GT) and the inferior ischial tuberosities margin (IT) using the linear transformation
Hounsfield Unit scale.
Results: SCI gluteal CSA was less than for AB throughout the muscle, with the greatest relative atrophy at the IT (48%). Average AB gluteal volume was nearly double SCI. Eight SCI had over 20% infiltrative adipose tissue, three with over
50%. SCI gluteal CSA and intramuscular fat infiltration were significantly negatively correlated (p<0.05). SCI IT axial slices showed less lean muscle and higher intramuscular fat infiltration than more proximally (p<0.05).
Chapter 2-36 Conclusion: SCI gluteal muscle characteristics were indicative of impaired tissue viability. SCI disuse muscle atrophy was anticipated; the analytic approach further indicated that intramuscular atrophy was not uniform. SCI muscle composition showed increased proportions of both low density muscle and adipose tissue. CT scan with contrast is effective for gluteal muscle characterization. This assessment technique may contribute to determination of personalized risk for PU development and other secondary complications.
INTRODUCTION
Pressure ulcer (PU) development remains a significant complication for many individuals following spinal cord injury (SCI). Once a PU develops, it can take several months to fully heal with a devastating impact on the quality of life due to the need for frequent hospital admissions and long periods of bedrest [79].
Susceptibility to PU development is increased for the SCI population due to many factors. Most prominent is impaired mobility following injury that leads to physiological changes in the soft tissues below the level of injury, such as muscle disuse atrophy [80], and altered vascular circulation [81] which contribute to decreased tissue health. Tissue breakdown and PU development is prevented by maintaining healthy viable tissue under applied loads. For the person with SCI who is a full-time wheelchair user, this means maintaining tissue health particularly in the pelvic region while seated. The regions at higher risk for PU development when seated are over the bony prominences of the pelvic region, i.e.
Chapter 2-37 the ischial tuberosities, sacrum and, to a lesser extent, the greater trochanters.
There are a host of known risk factors for tissue breakdown and PU development.
However the relative importance of each is not known [4, 12], making reliable
determination of personalized risk status challenging.
Approaches to PU prevention have tended to focus on external risk factors, such
as applied pressure distribution. The use of specialized cushions can decrease
surface interface pressures but it is essential that this is combined with a regular
pressure relief regime. Periodic pressure relief provides cyclic loading of the
pelvic region soft tissue with the goal of restoring local tissue oxygenation so that
tissue viability is maintained. PU prevention would also be enhanced if the
health of soft tissue under applied load could be improved. Changes in soft
tissue composition and function following SCI may provide a personalized
indication of risk status which the clinician can employ to determine an
individual’s optimal PU prevention regime.
The current study employed pelvic CT with contrast to investigate the hypothesis that individuals with SCI have altered muscle composition, indicative of impaired regional tissue health, compared to able-bodied (AB) individuals.
Chapter 2-38 MATERIAL AND METHODS
A prospective single-measure study of twenty individuals who received a single
CT with contrast assessment of the pelvic region was carried out. Two groups
were recruited; 10 AB and 10 individuals with SCI. The local Institutional Review
Board approved the study, and written informed consent was obtained from all
subjects. An initial evaluation process was carried out at recruitment in order to
determine physical, psychological and physiological suitability for CT
assessment. A comprehensive medical and physical profile was obtained
together with a renal function panel.
Pelvic CT scans with contrast were obtained using a Philips Brilliance 16 CT
system (Philips Medical Systems, Cleveland, OH) by a single qualified radiology
technologist under the supervision of expert radiologists. All scans were performed in the supine position with a cushion placed under the legs to minimize soft tissue compression in the buttocks. To limit radiation exposure, an initial anterior-posterior scout image of the pelvis was used to define the limits of
the scan from the inferior aspect of the sacroiliac joints to the inferior margins of
the femoral heads. This distance ranged from 180 to 210 mm. Slice thickness was
0.4mm, resulting in a pelvic region scan of 450 - 525 CT slices per participant.
Iodinated contrast agent was administered intravenously in two half-dose 50cc
boluses at 80 seconds and 40 seconds before the scan followed by saline. This
Chapter 2-39 procedure allowed both the arteries and the veins to display contrast. Contrast was administered at 50cc for each bolus for approximately 17 seconds.
Data Analysis
Axial images of the gluteus maximus muscle were obtained from its superior origin near the sacrum to an inferior point below the ischial tuberosities (IT). The gluteal muscle region of interest (ROI) was identified by outlining the fascia of the gluteus maximus muscle in each axial CT image slice using Amira
(Visualization Sciences Group, Burlington, MA). This ROI was defined as the muscle cross-sectional area (CSA) in each slice. Overall muscle volume was then calculated by multiplying CSA by slice thickness for all slices.
A: S2/S3 level
A B: Greater trochanter
B
C C: Ischial tuberosities Figure 2.1: Pelvic region CT with scout view indicating the location of axial slices. A: S2/S3 level, B: greater trochanters C: ischial tuberosities.
Chapter 2-40 In order to determine intramuscular fat infiltration of the gluteal muscle, axial
muscle slices were selected for further analysis using ImageJ. [82] As shown in
Figure 2.1, these cross-sections were located at level A, the midpoint of the S2/S3 sacral vertebrae level B, the superior margin of the greater trochanters (GT) and level C, the inferior margin of the ischial tuberosities (IT).
X-ray attenuation in CT scans is influenced by the density of the material being imaged. Tissues with higher density, such as lean muscle, appear brighter than lower density tissue, such as adipose regions. This attenuation is quantified using the linear transformation Hounsfield Unit (HU) scale [83], which was derived for use in soft tissue imaging. The scale is calibrated using air at the minimum of -1024 HU with distilled water as baseline at 0 HU and bone at around 400 to 1000 HU. In the current study protocol, the use of contrast increased the brightness of the vasculature such that the HU value was the same or higher than lean muscle. Tissue type for each pixel within the slice ROI was classified based on HU value as shown in Table 2.1 and overall muscle
composition determined by calculating the ratio of pixels within the specified
range for each tissue type of interest to the total pixels in the muscle CSA.
Chapter 2-41 Table 2.1: Tissue classification based on HU value
Hounsfield Unit (range) Tissue classification 100 to 200 Vascularized muscle 30 to 100 Lean Muscle 0 to 30 Low Density Muscle (LDM) -30 to 0 Fluid (other) -150 to -30 Adipose Tissue (Intramuscular fat)
Spearman’s rank-order correlation coefficient was applied to determine level of
correlation between gluteus maximus muscle CSA and proportion of
intramuscular fat infiltration. Student’s t-test was applied to examine differences between AB and SCI groups for muscle CSA, muscle volume, and relative tissue type composition. A paired t-test was applied to evaluate intrasubject left and right gluteal muscle asymmetry. All statistical analyses were performed using
VassarStats [84].
RESULTS:
Participant demographics are summarized in Table 2.2. The AB group comprised 6 males and 4 females of median age 25.5 years (range 19 – 57 years).
The SCI group comprised 8 males and 2 females of median age 43.5 years with ages (range 22 – 65).
Chapter 2-42 Table 2.2: Participant demographics
Participant Sex Age years Neurological ASIA PU History Injury Injury Level Level AB-01 M 23 N/A N/A N/A N/A AB-02 M 19 N/A N/A N/A N/A AB-03 F 24 N/A N/A N/A N/A AB-04 M 29 N/A N/A N/A N/A AB-05 F 22 N/A N/A N/A N/A AB-06 M 57 N/A N/A N/A N/A AB-07 M 24 N/A N/A N/A N/A AB-08 M 27 N/A N/A N/A N/A AB-09 F 47 N/A N/A N/A N/A AB-10 F 57 N/A N/A N/A N/A SCI-01 M 25 9 C7 C Sacral SCI-02 M 65 25 T7 A Pelvic SCI-03 M 53 7 C6 D None SCI-04 M 53 5 T5 A Sacral SCI-05 M 42 12 T12 A Left Ischial SCI-06 M 38 3 C8 A Sacral SCI-07 F 50 27 C6 incomplete None SCI-08 M 42 8 C5 B Sacral SCI-09 F 45 21 C7 A Sacral SCI-10 M 22 6 T6 A None
Gluteus maximus muscle geometry:
Average gluteal muscle volume for the AB group was nearly double the SCI group (Table 2.3).
Table 2.3: Gluteus maximus muscle characteristics
Gluteus Maximus SCI [range] AB [range] p value Volume (cm3) 379 ± 159 [154 to 582] 667 ± 114 [504 to 892] <0.05 CSA (cm2) 22 ± 8 [7 to 30] 40 ± 5 [30 to 43] <0.05 Fat (%) 29 ± 23 [3 to 84] 8 ± 9 [2 to 35] <0.05 Low Density Muscle (%) 19 ± 6 [5 to 25] 18 ± 5 [11 to 28] NSD Lean Muscle (%) 30 ± 19 [3 to 63] 59 ± 18 [29 to 81] <0.05 LDM/Total muscle (%) 45 ± 15 [23 to 74] 26 ± 11 [13 to 40] <0.05
Chapter 2-43 Ninety percent (9) of AB participants had total gluteal muscle volumes greater
than 600cm3, whereas only 10% (1) of the SCI group had total gluteal muscle
volume greater than 600cm3.
SCI group gluteal muscle CSA (CSASCI) was less than AB group gluteal muscle
CSA (CSAAB) at every level evaluated (Figure 2.2). The relative decrease in CSA was greatest inferiorly; level A CSASCI was 32% less than CSAAB while level C
CSASCI was 48% less than CSAAB.
6000 SCI group 5000 AB group
) 2 4000
3000
2000 muscle CSA (mm
1000
0 Right Left Right Left Right Left
S2/S3 level Greater trochanter Ischial tuberosities
Figure 2.2: Gluteal muscle cross-sectional area at levels of interest.
Chapter 2-44 Gluteus maximus muscle composition:
SCI AB Figure 2.3: Representative axial CT slices at the level of the ischial tuberosities
showing varying muscle composition.
Legend:
Vascularized muscle Lean Muscle Low Density Muscle
Fluid /other Intramuscular fat
Figure 2.3 shows representative gluteal muscle axial slices at level C (IT) for AB
and SCI subjects. Eight SCI subjects had greater than 20% intramuscular fat
infiltration, three of whom had very high (50% or greater) intramuscular fat
infiltration (Figure 2.4a). One SCI participant with an incomplete C6 level injury had low total intramuscular fat infiltration with a low gluteal muscle CSA. One
SCI participant with a complete C2 level injury had low total intramuscular fat infiltration with a high gluteal muscle CSA. Two AB subjects had greater than 25% intramuscular fat infiltration and a high gluteal muscle CSA (Figure 2.4b).There was a significant negative correlation between muscle CSA and intramuscular fat infiltration (p<0.05) for the SCI group, but not for the AB group.
Chapter 2-45 AB group SCI group
100% 100%
50% 50%
0% 0% AB-07 AB-02 AB-01 AB-05 AB-03 AB-06 AB-04 AB-08 AB-10 AB-09 SCI-03 SCI-10 SCI-01 SCI-05 SCI-08 SCI-04 SCI-07 SCI-09 SCI-06 SCI-02 % Tissue in Muscle CSA Muscle in Tissue % % Tissue in Muscle CSA Muscle in Tissue %
Figure 2.4: Average gluteal muscle tissue composition (normalized to muscle cross-sectional area)
Legend:
Vascularized muscle Lean Muscle Low Density Muscle
Fluid /other Intramuscular fat
Minor PU history Significant/repeated PU history
In the SCI group, level A axial slices showed a decreased proportion of lean muscle and higher intramuscular fat infiltration compared to both level B and C
(p<0.05). No differences between levels were found for the AB group. In addition to increased intramuscular fat infiltration, the SCI group had a greater proportion of low density muscle relative to lean muscle at all levels. Thus low density muscle was a greater proportion of the overall gluteal muscle tissue in the SCI group than in the AB group for the current study population.
Chapter 2-46 DISCUSSION
All individuals with SCI are at increased risk of PU development throughout their lifetime following injury. However, it is well known that some individuals appear to remain PU-free following injury whilst others suffer from a continuous
cycle of recurring PUs. Following injury, there is a rapid loss of muscle bulk,
together with decreased mobility and altered sensation. The majority of muscle
atrophy below the level of injury occurs acutely following injury. The amount of
disuse muscle atrophy that occurs in the paralyzed muscle is thought to be
affected by both level and extent of the injury. In order to maintain healthy,
viable tissue, particularly over the bony prominences, it is necessary to have
adequate soft tissue coverage and for the soft tissue to be well vascularized.
Detailed analysis of gluteal region CT images has the potential to provide insight
regarding muscle composition which may be indicative of local tissue health. The
current study found that gluteal muscle characteristics showed several
differences in the SCI group indicative of impaired tissue viability. It was not unexpected to find that overall volume and muscle CSA were reduced. Disuse
muscle atrophy is a well-established phenomenon. However, the analytic
approach employed in the current study indicates that muscle atrophy is not
uniform, even within an individual muscle. The finding that gluteal muscle atrophy is relatively greater at the level of the ischial tuberosities highlights the
need for protective measures to prevent tissue breakdown in this region.
Chapter 2-47 In addition to a reduced quantity of muscle, the SCI group was found to have an
altered quality of muscle for the majority of participants; both low density
muscle and adipose tissue occurred in higher proportions than for AB
individuals. The amount of intramuscular fat infiltration also differed by level within the muscle for most SCI participants and was greatest proximally. This
finding combined with the variable muscle atrophy, results in a negative
correlation between muscle cross sectional area and intramuscular fat infiltration for the SCI group, which was not observed for the AB group.
In the current study of individuals with chronic SCI, the amount of intramuscular fat infiltration did not appear to be directly related to the level or extent of injury. The highest levels of muscle adiposity were seen in most of the individuals with complete SCI, however low levels were also seen in one individual with a complete high cervical injury and extensive muscle atrophy.
Increased intramuscular adipose tissue in the gluteus maximus muscle has been shown in modeling studies to increase stress and strain in the deeper tissues surrounding the ischial tuberosity [2]. The SCI group was also found to have a higher proportion of LDM in the total muscle. Higher percentages of LDM and intramuscular fat infiltration have been positively correlated with increased risk of diabetes [78] and cardiovascular disease [85]. Thus the changes in muscle composition may have health indications beyond compromised tissue health and potential increased risk of PU development.
Chapter 2-48 CONCLUSION
The CT method employed was effective for characterization of the gluteal muscle, including both muscle geometry and tissue composition. Muscle atrophy decreases the cushioning of the soft tissue around bony prominences; furthermore adipose tissue is more susceptible than muscle to shear forces. The combination of muscle atrophy and deterioration in remaining muscle quality, indicative of dystrophic changes, will decrease local tissue health status and increase the risk of PU development, in particular the risk of DTI.
The use of CT scanning to quantify muscle volume, CSA, LDM to total muscle ratio and intramuscular fat infiltration has the potential to contribute to an assessment tool to determine personalized risk for PU development and other secondary complications. Characterization of tissue viability status could provide a basis for defining appropriate interventions to improve tissue health [86,87].
To minimize CT radiation, gluteal muscle characteristics may be determined from axial scans at sacral, GT and IT levels to give a ‘snapshot’ of the gluteus maximus. Variables such as muscle CSA and intramuscular fat infiltration may be indicative of regional tissue viability for persons at risk for PU development.
A baseline scan could also serve as reference to determine the effects of preventive interventions.
Chapter 2-49 2d. Addendum
Muscle atrophy and increased intramuscular adipose tissue in persons with SCI increase their susceptibility to develop PUs. The changes in muscle characteristics of persons with SCI were indicative of impaired tissue viability.
In the models developed by Oomens et.al, the decreased muscle mass resulted in decreased stiffness. The increased deformation is aggravated by ischemia leading to tissue breakdown and eventual DTI. The study also notes that there are individual variations in critical deformation threshold and period of ischemia that causes muscle damage and that these are related to intrinsic factors, such as pathological states. This suggests that regular assessments must be done individually [88]. In the succeeding chapters we assess the interface pressures, oxygenation and blood flow to better understand and determine the tissue health of persons with SCI on an individual basis.
A preliminary analysis was undertaken to look at how demographic information might be related to muscle volume, muscle CSA or the muscle composition described above.
Chapter 2-50
Figure 2.5: Injury level and muscle quality of participants grouped PU history
PU history is related to muscle composition and quality. Persons with PU
History exhibit higher intramuscular fat infiltration and less lean muscle (Figure
2.5). PU history was not related to muscle CSA or muscle volume. To our knowledge this is the first study to examine PU history and gluteal muscle composition. These early findings have implication that might be predictive of risk for pressure ulcers.
Chapter 2-51
Figure 2.6: Neurological level and muscle quality/muscle cross-sectional area (CSA) grouped by weight of participant.
When grouped by weight, those weighing less than 180 lbs have smaller muscle
CSA, higher %fat infiltration and lower %lean muscle.(Figure 2.6) This is in contrast with able bodied persons where lower weight would have higher % lean muscle and lower % fat infiltration. In this study we did not take into account activity level, though in the study population there was a mixture of active and sedentary persons with SCI.
Chapter 2-52 Chapter 3) Multi-factorial tissue health assessment (THEToolBox – Methods)
3a. Preface
The previous chapter suggests that persons with SCI have widely varying
tissue health characteristics. The modeling of these characteristics suggests
that these muscle characteristic might be integral in pressure ulcer risk. It is
possible that individual muscle characteristics are related to the different
reports of tissue oxygenation and blood flow. A standardized multi-factorial
tissue health assessment will provide systematic and regular assessments for
individuals. The quantitative nature of the assessments also aid in the
interpretation of tissue health measurements for groups across varied test
conditions.
3b. A Multifactorial Toolbox for Tissue Health Assessment
Submitted paper: (in revision)
Chapter 3-53 TITLE: A MULTIFACTORIAL TOOLBOX FOR TISSUE HEALTH ASSESSMENT
Gary A Wu, M.S.1, 2, Kath M Bogie, D.Phil 1, 3, 4
1. Department of Physical Medicine and Rehabilitation, MetroHealth Medical Center,
Cleveland OH, 44109
2. Department of Biomedical Engineering, Case Western Reserve University,
Cleveland, OH, 44106
3. Departments of Orthopaedics and Biomedical Engineering, Case Western Reserve
University, Cleveland, OH, 44106
4. Advanced Platform Technology Center, Louis Stokes Cleveland Department of
Veterans Affairs Medical Center, Cleveland, OH 44106.
FUNDING SOURCES
Mr Wu and Dr Bogie’s effort partially supported by the National Institute on
Disability and Rehabilitation Research (NIDRR), Rehabilitation Engineering
Research Center (RERC) on Spinal Cord Injury, Grant #H133E070024
Chapter 3-54 CORRESPONDING AUTHOR
Kath M Bogie, DPhil; Cleveland Advanced Platform Technology Center, Louis
Stokes Cleveland VA Medical Center, 10701 East Boulevard, Cleveland, OH
44106;
Phone 216-368-5270
Fax: 216-707-6420
Email: [email protected]
AUTHOR CONTRIBUTIONS
Study concept and design: KM Bogie
Acquisition of data: GA Wu
Analysis and interpretation of data: GA Wu, KM Bogie
Drafting of manuscript: GA Wu
Critical revision of manuscript for important intellectual content: KM Bogie
Obtained funding: KM Bogie
Study supervision: KM Bogie
Chapter 3-55 Abstract
Decreasing tissue breakdown risk is dependent on many factors, thus the effect of interventions should be assessed using multiple non-invasive, quantitative, repeatable techniques. We describe the Tissue Health Evaluation Toolbox
(THEToolbox), a clinically feasible tool using a modular group of standardized assessment methodologies to evaluate several aspects of tissue health.
Quantitative assessment methodologies in THEToolbox currently include interface pressure monitoring (IP), transcutaneous oxygen (TcPO2) and Laser
Doppler blood flow. Unloaded measurements are obtained with the person side- lying for 20 minutes to obtain steady-state measurements from the assessment region(s) of interest, followed by a loaded period where interface pressures are assessed concurrent with tissue blood flow measurements. The loaded assessment comprises three or more 5 minute phases: quiet pre-intervention, active intervention and post-intervention. Further intervention phases may be added after the first active intervention phase. Outcomes measures include; a) mean IP in the overall contact area and selected analysis regions of interest, magnitude and location of maximum IP gradient, b) TcPO2 mean and threshold to determine relative high/low TcPO2 duration, c) blood flow components derived using short-term Fourier transform. A case study of applying
THEToolbox to determine the effects of independent weight-shifting for an individual with spinal cord injury is presented.
Chapter 3-56 KEYWORDS
Blood flow, chronic wound, interface pressure mapping, pressure gradient, pressure ulcer, seating, shear, spinal cord injury, tissue health, tissue oxygenation,
CLINICAL TRIAL REGISTRATION: Not Required
ABBREVIATIONS
ASIA American Spinal Injury Association Impairment Scale
IP Interface pressure
KCl Potassium chloride
PU Pressure ulcer
RERC SCI Rehabilitation Engineering and Research Center in SCI
ROI Region of interest
SCI Spinal cord injury
STFT Short-term Fourier transform
TcPO2 Transcutaneous oxygen tension
THEToolbox Tissue health evaluation toolbox
Chapter 3-57 INTRODUCTION
CLINICAL MOTIVATION
People with prolonged or acute immobility, impaired sensation and/or advanced age are at increased risk for developing pressure ulcers (PUs). Several intrinsic and extrinsic tissue health factors have been identified as contributing to the development of PUs. The relative contributions of these confounding factors are yet to be elucidated, motivating a multifactorial assessment approach.
It is well established that while applied pressure is a significant factor in tissue health, the assessment of interface pressures at the junction between the individual and the support surface doesn’t adequately describe either tissue health or risk of tissue breakdown. Indeed, it is becoming well accepted that tissue breakdown leading to the clinical presentation of a PU may start at the skin/support interface or in the deep tissues nearer the soft tissue/bone interface
[89,90]. Tissue breakdown that starts in the deep tissues is classified as a DTI.
Several pre-clinical models have described soft tissue changes related to development of a DTI [88,91,92,93]. While some measurement techniques to monitor deep tissue health status have been evaluated in the research setting
[94,95], they have not been clinically implemented to date. In addition to the magnitude of applied pressures and local shear stresses, the duration of loading is also recognized to be a critical extrinsic risk factor [96]. Intrinsic factors include
Chapter 3-58 disuse muscle atrophy, impaired sensation, reduced vascularity and
dysfunctional circulatory regulation.
Increased risk of PU development can be summarized as being due to the
combination of prolonged immobility and loss of neurological protective
mechanisms that minimize soft tissue damage. High risk groups who exhibit
these risk factors include the elderly, the critically ill and those with chronic
neuromuscular disease and disorders such as spinal cord injury (SCI). The SCI
population exhibit reduced tissue health below the level of injury for many
reasons, including impaired vascular system function [97]. SCI disrupts spinal
vasomotor pathways, thus affecting the sympathetic nervous system, but
allowing the parasympathetic system to remain functional [98, ,99]. This
imbalance alters baseline vasodilation in denervated tissue and may impair the
normal inflammatory response to wounding. Vasodilation may also lead to
lower systolic and diastolic blood pressures in individuals with SCI compared to
non-injured controls [100 ,101]. Furthermore there is evidence of remodeling of the vascular bed and progressive loss of capillaries in the denervated tissue [102].
These contribute to impaired tissue perfusion and compromise the delivery of
nutrients, enzymes and oxygen to the tissues [103]. Impaired tissue perfusion
below the level of the lesion further increases PU risk for individuals with SCI
[47]. When a PU does occur, healing is compromised due to poor local tissue
oxygenation and essential nutrient supply resulting from the decreased blood
Chapter 3-59 supply. Oxygen is essential for several steps in building new tissues during the
wound healing cascade. Reduced transcutaneous oxygen pressure can be a
reliable indicator of local ischemia and is significantly related to failure to heal
[104 ,105].
In order to minimize the risk of PU development, a regime of regular postural
alteration and pressure relief is essential. Individuals with impaired sensation
and mobility, often find it difficult to adhere to a rigorous pressure relief regime.
Many interventions to prevent PU development in these at-risk individuals have been developed. Most are focused on extrinsic factors, such as by addressing pressure distribution at the support interface through the use of pressure relieving cushions and adjustable (tilt-in-space) wheelchairs to provide postural variation. There are many anecdotal and case studies of these interventions. A recent Cochrane review found there have been just over 50 randomized controlled trials of support surfaces [62]. It is of interest to note, that interface pressure (IP) measurement was considered to be a proxy outcome. The sole outcome measure considered by the review was clinically recorded incidence of pressure ulcers. The optimal outcome when developing interventions or determining an effective pressure relief regime is for tissue breakdown not to happen. The efficacy of any preventative approach, from smallpox inoculation to seatbelt usage, is most rigorously achieved through epidemiological studies of large populations. In clinical management or research this is most often not
Chapter 3-60 practicable. Clinical effectiveness studies have been considered as an alternative
approach to large randomized clinical trials. These studies are often designed to
determine equal efficacy rather than prevention. A more detailed philosophical
discussion on the design of preventative healthcare studies is beyond the scope
of the current paper. Suffice to say, there remains an inherent challenge in
quantifying successful prevention on a case-by-case basis. The prevention of tissue breakdown depends on many factors and while it is challenging to quantify, it is clear that proxy outcome metrics based on more than an endpoint failure, i.e. development of a PU, are needed.
There remains a critical need to investigate and quantify the effectiveness of current and new approaches to prevention. Comprehensive characterization of tissue health has the potential to provide a valid risk indicator without tissue breakdown being the primary outcome measure. We propose that THEToolbox, a non-invasive multi-factorial approach to tissue health assessment which will be invaluable in the development and assessment of approaches to PU prevention which are currently much more limited than PU treatment options [106].
TISSUE HEALTH ASSESSMENT TECHNIQUES
Interface Pressure Mapping
Background: Interface pressure (IP) mapping has been the primary tool used in
prescribing wheelchair cushions and is widely accepted as a means to evaluate
Chapter 3-61 distribution of pressure on the support surface interface [66]. The measurement
technique has also been used assess the effectiveness of pressure-relieving mattresses [107, 108] and operating tables [109,110].
A pressure mapping device consists of an array of sensors contained in a flexible mat which measure interface pressures between the user and the support surface. Pressure values and surface contact area are displayed in a color-coded image on a computer screen, which may include a numerical value at each sensor location on the image. Pressure mapping allows interface pressures over the entire loading surface to be assessed over time. IP variables such as mean and maximum pressures can be determined for the total contact area or a user-defined region of interest (ROI) for detailed analysis [111]. In the majority of seating studies these analysis ROI would the regions considered to be at highest risk for tissue breakdown, the ischial tuberosities and sacrum. In mattress or lying studies, the analysis ROI could include the ischial tuberosities, sacrum, scapulae, occiput and heels. Bench-top testing by Sprigle et al has shown that mean IP and ischial region percent force are reliable measures of IP distribution [112]. The authors also showed that maximum IP is not a reliable measure. Furthermore, it is of limited use if there is no accompanying positional information.
Chapter 3-62 In current clinical use, real-time graphical visualization provides an IP map which is easily accessible for patient education. [113] Numeric data underlying an IP map maybe overlaid in the visual presentation and/or collected as IP data.
The location of bony prominences on an IP map can be rapidly determined empirically by clinicians [65]. If concentrated areas of high pressure “hotspots” are identified, the support surface can be modified according to the user’s specific needs.
Although IP maps can provide a simple graphical and numerical interface there are limitations in interpreting the results of IP data. Tissue health is a personalized quality and there is no universal safe IP value that can ensure maintenance of tissue health. It has been shown that there is significant inter- subject variability in IP values [65,114]. Furthermore, there is no correlation between IP and PU prevalence in the general and SCI population [115]. It is clear that IP measurement alone cannot provide a comprehensive understanding of tissue health status in a specific region of interest. Not only must IP magnitude be considered but also the duration of loading together with other physiological factors that affect tissue health [116,117].
Chapter 3-63
Figure 3.1: Representative cross section of interface pressure values.
A large-area low gradient peak can be, compared to a small-area high gradient peak. The latter is the peak of interest since it is surrounded by high shear. It can be seen that maximum IP is not always the maximum IP gradient.
Ferguson, et al. and others have proposed multiple IP outcomes measures should be employed, including pressure gradient [118, 119]. Friction and shear are primary PU predictors [120]. In preclinical testing it has been shown that interface shear forces can characterized in wheelchair cushions when the sensor is applied to a flat, hard indentor surface [121]. However, these forces are difficult to measure directly in soft tissues using non-invasive techniques. The use of IP gradient derived from IP distribution maps may provide the clinician with an indicator of localized high shear forces, without requiring the use of a specialized sensor. It is important to note that, as shown in Figure 3.1, maximum
Chapter 3-64 IP is not necessarily co-located with maximum IP gradient. Maximum IP is seen at the first peak, marked by a yellow dotted circle. However, this peak has a gradual slope indicating low surrounding IP gradients. The second peak, marked by a red circle has a lower peak but has high gradient. Thus, the second peak is where the maximum IP gradient would be observed and where the soft tissue would experience high shear. The maximum IP gradient thus gives an indirect
measure of local surface shear, which is more relevant to tissue health than
maximum IP.
Methods: There are several commercially available IP mapping systems
currently available, e.g. Xsensor (XSENSOR Technology Corp, Calgary, Alberta),
FSA (Vista Medical, Winnipeg, Manitoba). In the THEToolbox protocol, the
CONFORMat Tekscan Clinical Seating System (Tekscan Inc., Boston MA) is
used to measures IP in the region of interest (Figure 3.2). The CONFORMat system employs 0.8 mm thin flexible sensors utilizing conductive and semi- conductive inks in a grid-based array. The pressure sensing mat contains 1024 sensing elements (sensels) arranged in a 32x32 array.
Chapter 3-65
Figure 3.2: CONFORMat® Tekscan Clinical Seating System (reproduced with permission from Tekscan Inc)
Before use the system must be calibrated according to the manufacturer’s
recommendations. Specifically; pressure calibration is carried out monthly using
standard known applied pressures and a force calibration based on user weight
is carried out at the start of each assessment period.
Following calibration, the measurement range is 0-250 mmHg (4.8psi/33.3kPa) with an overall accuracy of ±10% [111]. Scan rates are adjustable from 0.02Hz to
100Hz. Although the manufacturer states that data can be collected for up to 1 hour before calibration is required, in use it is found that drift occurs within 10 minutes of continuous loading due to heating of the piezoresistive ink in the sensor mat, therefore more frequent intra-assessment force calibration is
Chapter 3-66 required. In THEToolbox protocol IP distribution is recorded at a rate of 2 Hz for
assessment periods up to 5 minutes and then force calibration is repeated.
During data collection, real-time 2-D or 3-D images of pressure distribution are produced for immediate user feedback using proprietary graphical display software
Data analysis: At the end of each assessment period the CONFORMat software
creates 2D/3D IP distribution maps. These maps are easily navigable to define
region of interests and create simple graphs to see the changes in pressure over
time but have limited capacity for storage of quantitative analyses. In
THEToolbox protocol, data together with time and frame information are
exported to Excel and Matlab for further detailed analysis.
Analysis Regions of Interest: The ROI for detailed IP analysis are manually selected
within the overall pressure map. In the THEToolbox protocol, the ischial
tuberosity analysis ROI are bilateral 5x5 sensel regions (approximately
7.5x7.5cm2). The sacral analysis ROI is a 3x12 sensel region centered at the
midline at the posterior margin of the overall pressure map. Mean regional IP is
determined for the areas within the analysis ROI, specifically the left and right
ischial tuberosities and the sacral region in seating assessments.
Chapter 3-67 Maximum IP gradient is calculated by determining the highest difference between all adjacent sensels across the whole contact area; the true contact area is first delineated by segmentation of the IP map through morphological opening
(erosion and dilation) to delete small regions of noise outside the contact pressure area.
Morphological opening is a generalizable image analysis technique used to segment ‘noisy’ images to that small regions which are not part of the true region of interest can be eliminated form further analysis. Morphological opening first applies an erosion, or removal of area margins, by a fixed structural element followed a dilation, or addition to remaining area margins, by the same structural element. In the current application to IP maps, a structural element of 1 pixel is applied. The resultant segmented image is saved as a black and white mask. This mask is then applied over the original image, to delineate the main contact area.
It should be noted that this approach does have a tendency to round out sharp edges in a segmented image.
The magnitude and location of the maximum IP gradient is then determined for the true contact area. Each sensel within this area is surrounded by up to 8 neighbors. These may be linearly adjacent, i.e. in the next row or column, at a distance of one sensel, or diagonally adjacent, at a distance of √2 sensels. Each sensel is sequentially compared to its 8 nearest neighbors; the difference between
Chapter 3-68 IP values is determined and then adjusted for actual separation by dividing by
the relevant distance. This is repeated for all sensels across the true contact area
with appropriate corrections for edge effects. The location and magnitude of the
maximum IP gradient is thus determined for the total contact area by comparing
all sensels with all adjacent neighbors.
In some cases, sensels will record high out-of-range pressures. These saturation points are also potential locations of high IP gradients but the magnitude cannot be accurately determined and so these points are excluded from calculation of maximum IP gradient. The maximum IP output map therefore indicates both maximum IP gradient within range and saturation points. An output map is derived for each frame of IP data and can be viewed as a snapshot or a ‘movie’ to evaluate stability of both magnitude and location of maximum IP gradient.
Transcutaneous Oxygen Tension (TcPO2) Measurement
Background: Transcutaneous oxygen (TcPO2) monitoring, also known as
transcutaneous oximetry, is well established in clinical settings as a non-invasive continuous monitoring tool for at-risk patients, particularly in neonatal intensive care units [122, 123, 124] and adult respiratory care [125,126]. It has also been long been used as a reliable clinical diagnostic tool in wound treatment [127,128] and limb ischemia [129, 130]. In the research setting, TcPO2 measurements have
been used to study blood flow with interventions such as temperature,
Chapter 3-69 wheelchair and bed tilt and gluteal neuromuscular electrical stimulation
[131, 132, 133, 134].
Oxygenation and blood flow in the soft tissues affect local tissue hypoxia and ischemia leading to deep tissue stress [135]. Prolonged reduction in tissue oxygenation due to decreased blood flow in loaded soft tissues will cause cell damage and eventually cell death. Low levels of oxygen and accumulation of extracellular adenosine will trigger inflammation, leading to possible immune cell-mediated destruction in muscle and adipose tissue [136]. Thus tissue oxygenation is a significant factor in the development of pressure ulcers and deep tissue injury.
The transcutaneous oxygen sensor employed in THEToolbox is a platinum Clark- type oxygen sensor which allows measurement of oxygen tension through the superficial skin layers. The Clark sensor is based on the principle of quantifying oxygen on the surface of a catalytic platinum surface. In use, the sensor surface is moistened with a thin film of potassium chloride (KCl) electrolyte solution and a
Teflon membrane placed over the moistened sensor surface. The Teflon membrane preferentially filters oxygen molecules which react with the free electrons in the KCl electrolyte. The negatively charged hydroxide product alters the surface charge on the catalytic platinum sensor. This change is linearly related to the amount of oxygen available on the sensor surface and thus
Chapter 3-70 provides a direct, quantifiable measure of local tissue oxygenation. At skin
temperature, the measurement is limited to a hemispherical space of 1.5 mm
radius centered at the tip of the sensor. In order to expand the effective
measurement depth, the sensor is heated to 43oC to maximize local vasodilation
and allow blood flow through the capillary bed. The oxygen tension in the
perfused capillary bed thus gives an estimate of the oxygen tension available to
the assessment ROI from the deeper vasculature to an effective measurement
depth to 3-5 mm under the sensor. Local surface heating is dissipated by a
combination of convection and conduction to the deeper skin layers; however
sensors must be moved every 2-4 hours in order to ensure no thermal damage occurs.
Methods: In THEToolbox assessment protocol, transcutaneous oxygen tension is
measured using the Radiometer TCM400 (Radiometer USA, Westlake, OH).
The TCM400 system allows concurrent oxygen measurements at up to five
locations (Figure 3.3). Each sensor is attached within an assessment ROI on the
skin using a disposable fixation ring. The fixation ring is a 20mm diameter
adhesive ring surrounding a central 10mm plastic screw-mounting, 6 mm tall.
Overall the sensor is 15 mm in diameter and 11.3 mm tall [137]. The sensors are
calibrated to atmospheric oxygen (155-165 mmHg). System measurements range from 0 to 200 mmHg (where 160 mmHg is atmospheric O2) with an accuracy of ±
2 mmHg at a data collection rate of 5Hz. [137]
Chapter 3-71
Figure 3.3: Radiometer® TCM400 system (reproduced with permission from Radiometer USA)
When assessing TcPO2 under applied external load the external interface surface
must be compliant so that the sensor is not compressing the underlying skin.
When carrying out concurrent interface pressure measurement it is important to
check whether a peak pressure region appears to be occurring at a point
coincident with a TcPO2 sensor. When assessing advanced pressure relieving
surfaces such as wheelchair cushions this is generally not seen because these
cushions have good immersion characteristics. However, if the assessment will
include surfaces that may have reduced compliance or poor immersion
characteristics then a soft compliant ring may need to be placed around the
sensor to distribute the local pressure point [138].
Chapter 3-72 During assessment, event markers are defined at the start of each period to
facilitate synchronization of TcPO2 and assessment status in subsequent analyses.
TcPO2 data is uploaded via a USB connection for further detailed analysis.
Data analysis: In order to avoid data being influenced by any initial hyperemic
response or end-phase anticipatory movements, data from the first and last
minute of each assessment period is discarded. The tissue oxygenation response
during each assessment phase is characterized by applying a threshold to
determine the relative time the tissue under assessment is adequately or
inadequately oxygenated, i.e. healthy or at-risk. In previous studies, an upper
threshold of 30mmHg was suggested [139]. This represents a 60% reduction from
normal unloaded TcPO2. It was considered that the risk of tissue breakdown was
reduced above this threshold value. This upper threshold has also been
supported by consensus statements on the clinical use of transcutaneous
oximetry [140]. If TcPO2 is less than 10mmHg then tissue oxygenation is severely
compromised. Threshold values are thus defined as low for TcPO2 below 10
mmHg, mid for TcPO2 10-30 mmHg and high for TcPO2 values above 30 mmHg.
THEToolbox analysis of tissue oxygenation data determines the percent of time
TcPO2 values are within each range during the time period of interest. The
percentage of each assessment phase that TcPO2 is high and low is then
determined.
Chapter 3-73 Blood Flow Measurements
Background: In the normal healthy individual there is a direct correlation between tissue oxygenation and blood flow. The measurement of blood flow in soft tissue under load provides an indication of active local responses. Pressure redistribution causes a hyperemic response. During this period the blood vessels dilate and blood flow returns to the region at a rate much higher than steady state blood flow. One of the factors which may indicate compromised systemic function and local tissue health status is a mismatch between measures of vascular function, such as blood flow and hyperemic response, and load status
[141]. Impaired skeletal muscle microvascular function has been observed in some studies of at-risk individuals [142,143]. For example, in individuals with
SCI, blood metabolic activity may be altered. It has been shown that in response to passive movement, oxygenated hemoglobin levels change independent of total hemoglobin level in the paralyzed lower limb, but are not affected in able- bodied individuals [144]. Bhambhani et al found that muscle deoxygenation relative to oxygen uptake was faster in individuals with SCI than in healthy individuals [145], implying an impaired tissue oxygenation response. It has also been observed that the adaptive tissue oxygenation response under applied load is impaired in some individuals with neuromuscular disability or disease [146].
Specifically, Bader et al showed that able-bodied individuals exhibit a partial recovery of tissue oxygenation under sustained applied load and that repeated loading cycles have decreasing effects on tissue oxygenation. Conversely for
Chapter 3-74 individuals with neuromuscular disability or disease, tissue oxygenation under
sustained applied load may not show any recovery and repeated loading further
decreases tissue oxygenation. It has been suggested that vascular responses not
only vary between groups but may be muscle specific [147]. It has also been reported that microvascular dysfunction may alter the epidermal response to heating resulting in reduced TcPO2 levels even when blood flow is adequately
maintained[148]. Thus, in high risk individuals the normal correlation between
tissue oxygenation and blood flow may be absent or altered. It is therefore useful
to monitor blood flow in addition to local tissue oxygenation. Blood flow
measurements have been used in research setting to study microclimate, tilt and
changes in blood flow due to differing applied pressures [10, 65,149].
Methods: The signal from a Laser Doppler sensor can penetrate non-invasively
to an approximate subcutaneous depth of 1.0-1.5 mm, with no local tissue
heating. The LaserFlo BPM2 system (Väsamed, Eden Prairie, MN) is used in
THEToolbox protocol. The system uses a fiber optic cable to emit and receive a
low-powered (2 mW) laser light (780 nm) to measure red blood cell (RBC)
dynamics indicative of microcirculatory perfusion in the soft tissue of interest.
Laserflo probes employ a single transmitter and two receivers, which provides
two statistically independent measurements of the vascular bed using the same
transmitter, with an internal system resistance of 10 ohms. This increases the
Doppler shift signal whilst significantly reducing laser-generated signal noise
Chapter 3-75 [150]. Internal system software first applies a high pass filter at 30Hz and then employs both Doppler shift and noise content of the signal to determine absolute outputs, specifically; blood flow (ml/min/100g tissue), RBC velocity (mm/s) and
RBC volume (percentage of total blood volume in tissue sampled). Manufacturer specifications indicate that internal system processing further averages this data over 0.3 second timeframes with a data collection rate of approximately 10 Hz
[151].
The system is factory calibrated against standardized tissue phantoms. At start- up the internal software runs through a diagnostic/fault checking procedure to confirm function.
Series 4000 SoftFloTM probes have a flexible, flat profile which conforms to the body. This obviates any additional source of pressure and deformation of tissue.
The tip is made of silicon elastomer that encases the fiber optic cable. The
THEToolbox protocol employs the 4415 probe which has overall dimensions of
150mmx13mmx2.4mm (Figure 3.4).
Chapter 3-76
Figure 3.4: LaserFlo® BPM2 4415 SoftFloTM probe (reproduced with permission from Väsamed)
Analog output is communicated through a BNC connector for each variable with a voltage range of 0-5 volts proportional to each unit of measure. The output signal is optimized to measure blood flow within a range of 0-50ml/min/100g tissue with ± 10% repeatability.
Laser Doppler flowmetry (LDF) data is collected from the Laserflo BPM2 system using a data acquisition board and Labview (National Instruments Corporation,
Austin TX). A custom Labview program for data acquisition was written by our group in collaboration with the Rehabilitation Engineering and Research Center in SCI (RERC SCI) at University of Pittsburgh.
Data analysis: Taking measurements over a longer period of time makes it possible to study low frequency components of the blood flow signal from
Chapter 3-77 different underlying functions. The concept of applying wavelet analysis to a
dynamically varying signal was first described mathematically by Grossman and
Morlet [152]. The wavelet transform concept was then applied to LDF signals
initially by Stefanovska and Bracic [153]. It has since been further developed and
applied in clinical studies by others [154,155]. Spectral analysis can be applied to determine the relative contributions of metabolic, neurogenic, myogenic, respiratory, and cardiac components [156].
In THEToolbox protocol, the LDF blood flow output data is processed using STFT over the whole seating assessment (Pre-Intervention, Intervention and Post-
Intervention assessment periods including acclimatization and transition periods in between). The cardiac variability signal is related to the heartbeat at which is around 1 beat per second or 1 Hertz (Hz). Early studies on spectral analysis identified two characteristic peaks, a high frequency component for sympathetic control (between 0.15 to 0.4 Hz) and a low frequency parasympathetic control at
(0.04 to 0.15 Hz). [157] Spectral analysis of the LDF blood flow components suggests that these low frequency oscillations have different physiological control mechanisms [158]. Metabolic control of blood flow is controlled by endothelial cell according to the metabolic needs of the tissue. This control mechanism is typically mediated by oxygen demand and nitric oxide (NO) release. Local anesthetic does not block this response but addition of NO synthase inhibitor significantly diminishes the frequency characteristic at 0.008 to
Chapter 3-78 0.02Hz. This frequency range is thus considered to be governed by metabolic
processes. The use of local anesthesia to block the nerve or nerve transection
diminishes the spectral density at 0.02 to 0.05 Hz, this frequency range is
attributed to neurogenic control. The myogenic component is an ion-mediated response of the smooth muscles around the blood vessel that respond to continual changes in the transmural pressure. When the blood vessel is passively stretched due to increased pressure or flow, the smooth muscle surrounding the blood vessels constrict via a calcium-mediated response. Calcium ion channel blockers likewise diminish the myogenic response at the frequency range of 0.5 to 0.15 Hz. Thus the spectral frequency signals are separated into metabolic
(0.008-0.02 Hz), neurogenic (0.02-0.05 Hz), myogenic (0.05-0.15 Hz), respiratory
(0.15-0.4 Hz) and cardiac (0.4-2.0 Hz) [159]. The energy of the signal in each range is an indication of the relative contribution of each component to the total blood flow. The first three components are locally regulated and thus of interest in determining regional tissue health. Respiratory and cardiac components are centrally regulated and thus not a focus of this assessment approach but are kept for reference.
The Matlab program (The MathWorks, Natick, MA; v.2012a) is used to perform
LDF signal processing. The original LDF data is collected at 10Hz. The data is then digitally down-sampled to 5Hz with an anti-aliasing filter in Matlab using the decimate routine. This signal is then filtered with a 3 second moving average
Chapter 3-79 in order to reduce noise. Data points in the LDF signal beyond 2 standard
deviations are replaced by values in the moving average mask, thus keeping the
integrity and resolution of the rest of the data intact. The LDF signal is sensitive
to motion which in this assessment is signal noise due to muscle spasms and
small shifts in weight. Initial signal filtering prior to transformation thus ensures
that the LDF output signal reflects the locally mediated response to an
intervention.
Spectral density of the LDF is computed using the Matlab spectrogram function
which applies a STFT to the filtered signal for the entire loaded assessment
period, which is around 20 minutes in length. The spectrogram function allows the frequency scale F, defined by the frequency range and frequency resolution,
to be specified. The frequency range is from 0 to half the sampling frequency
(Fs/2). Typically it is a linear scale with 1024/2 frequency points. In THEToolbox
protocol the frequency range is defined with a logarithmic space in order to
increase the data points in the lower frequency components and allow for better
visualization for the lower frequency ranges of interest (metabolic, neurogenic
and myogenic). Thus, F is defined as the logarithmic space from 0.001 to 2.5Hz
with 512 frequency points. A 1024-sample Hamming window is applied to compute the spectrogram, i.e Window length (WLEN) =1024. This window is equivalent to 204.8 seconds of data, giving a frequency resolution of 1/(204.8 seconds) or 0.005Hz. The resulting STFT is then passed through a tenth-order
Chapter 3-80 Chebyshev I low-pass filter with a 2.0 Hz cut-off frequency. Normalized spectral densities are obtained by computing the spectrogram, based on the magnitude-
square of the STFT (Cohen, 1995b). Assessment phases are then separated out
after performing the STFT.
The main outcome of the LDF STFT analysis is the power spectral density (PSD)
calculated from the spectral densities at the three target frequency bands
(metabolic, neurogenic and myogenic) averaged over each assessment phase
(Pre-Intervention, Intervention and Post-Intervention). The PSD for each assessment period is calculated from the spectrogram by averaging the spectral densities over the respective duration of each assessment (Equation 1).
Equation 1: PSD is summed over each 200s phase, with approximately the first and last 10 s cut off to minimize edge effects.
1 190s a) PSD for Q1: PSD = ()T dT Q1 ∫ = QQ11 TQ1 10 TQ1 − 20
1 190s b) PSD for I1: PSD = ()T dT I1 ∫ = II11 TI 1 10 TI1 − 20
1 190s c) PSD for I2: PSD = ()T dT I2 ∫ = II22 TI 2 10 TI 2 − 20
1 190s d) PSD for Q2: PSD = ()T dT Q2 ∫ = QQ22 TQ 2 10 TQ2 − 20
Chapter 3-81 The spectrogram is then integrated over the frequency range of interest
(Equation 2) to derive the specific frequency band PSD for each assessment phase.
Equation 2: The area under the curve is determined for each frequency range of interest
a) Metabolic PSD for Q1, (frequency range 0.008 to 0.02Hz)
0.02Hz 1 190s 0.02Hz = (T ,)ωω dT d or PSD()ωω d Q1( Met ) ∫∫ω= = QQ11 ∫ω= Q1 PSD 0.008Hz − TQ1 10 s 0.008Hz TQ1 20
b) Neurogenic PSD for Q1, (frequency range 0.02 to 0.05Hz)
1 0.05Hz 190s 0.05Hz = (T ,)ωω dT d or PSD()ωω d Q1( Neuro ) ∫∫ω= = QQ11 ∫ω= Q1 PSD − 0.02Hz TQ1 10 s 0.02Hz TQ1 20
c) Myogenic PSD for Q1, (frequency range 0.05 to 0.15Hz)
1 0.15Hz 190s 0.15Hz = (T ,)ωω dT d or PSD()ωω d Q1( Myo ) ∫∫ω= = QQ11 ∫ω= Q1 PSD − 0.05Hz TQ1 10 s 0.05Hz TQ1 20
d) Respiratory PSD for Q1, (frequency range 0.15 to 0.40Hz)
1 0.4Hz 190s 0.4Hz = (T ,)ωω dT d or PSD()ωω d Q1(Re sp ) ∫∫ω= = QQ11 ω= Q1 PSD − 0.15Hz TQ1 10 s ∫ 0.15Hz TQ1 20
e) Cardiac PSD for Q1, (frequency range 0.40 to 2.00Hz)
1 2Hz 190s 2Hz = (T ,)ωω dT d or PSD()ωω d Q1( Cardio ) ∫∫ω= = QQ11 ω= Q1 PSD − 0.4Hz TQ1 10 s ∫ 0.4Hz TQ1 20
To allow comparison between assessment phases, the PSD of the each phase is normalized relative to the cumulative PSD for the whole seating assessment
Chapter 3-82 (Equation 3). This enables the varying effects of active and passive interventions
to be compared, e.g. passive changes due to induced postural change compared
to active muscle contraction.
Equation 3: Relative blood flow for each phase, and percent contribution of each blood flow component.
PSDQ1 a) Relative PSD for Q1 x100% PSDQII112+++ PSD PSD PSD Q 2
PSD b) Relative PSD for I1: I1 x100% PSDQII112+++ PSD PSD PSD Q 2
PSD c) Relative PSD for I2: I 2 x100% PSDQII112+++ PSD PSD PSD Q 2
PSDQ2 d) Relative PSD for Q2: x100% PSDQII112+++ PSD PSD PSD Q 2
Furthermore the relative contribution of the blood flow components is calculated by taking the PSD of each component’s frequency range normalized to the PSD of the whole frequency range of the signal (Equation 4).
Equation 4: Relative contribution of blood flow components
a) Relative contribution of Metabolic component in Q1 phase
1 2.5Hz 190s PSD (T ,ωω ) dT d x 100% Q1( Met ) ∫∫ω= = QQ1 1 − 0Hz TQ1 10 TQ1 20
Chapter 3-83 b) Relative contribution of Neurogenic component in Q1 phase
1 2.5Hz 190s PSD (T ,ωω ) dT d x 100% Q1( Neuro ) ∫∫ω= = QQ1 1 − 0Hz TQ1 10 TQ1 20
c) Relative contribution of Myogenic component in Q1 phase
1 2.5Hz 190s PSD (T ,ωω ) dT d x 100% Q1( Myo ) ∫∫ω= = QQ1 1 − 0Hz TQ1 10 TQ1 20
To optimize collection of LDF data, the duration of assessment periods should be
maximized however this must be balanced with clinical and practical constraints,
including reducing the overall duration of tissue health assessments and
minimizing drift of the IP measuring device. In THEToolbox protocol, the each
assessment phase has a minimum data collection period of approximately 200
seconds. For the lowest frequency range, specifically the metabolic blood flow
component, there is at least 2 to 4 cycles in this period. The STFT is calculated
with a very high degree of windowing overlap (number of overlap is WLEN-1 =
1023 points). The high overlap ensures determination of these very low frequency cycles.
Further statistical analysis using nonparametric tests can be applied to evaluate intra- and inter-subject differences, including Friedman’s test repeated-measures analysis of variance and Wilcoxon Rank-Sum tests.
Chapter 3-84 Summary
A multi-factorial assessment tool is required to evaluate interventions which impact the tissue health of a person at risk of PU development. The assessment tool should include capabilities for spatial and longitudinal analysis of interface seating pressures together with the responses of transcutaneous oxygenation and blood flow. The relative contributions of the components of blood flow can also be determined.
The current paper describes THEToolbox, a suitable multifactorial assessment tool, together with application of this tool to evaluate the effects of weight- shifting on tissue health for an individual with SCI.
Assessment Protocol
Participants are asked to wear loose fitting clothes for all assessments. Upon arrival the participant’s weight is measured in order to provide force calibration for the CONFORMat® system. The participant then transfers to the mat for pre- assessment skin review and baseline tissue health assessment. If the participant is unable to transfer independently, a Hoyer lift is used to assist in transfers. The pants and undergarments are pulled down in order to access the buttock region for tissue health testing. The skin in the buttock region is inspected thoroughly for signs of pressure ulcers, which would prevent further assessment. The skin is cleansed with a clean paper towel or moist towelette as necessary in order to
Chapter 3-85 improve sensor attachment. Room temperature over the course of each
assessment is maintained at 25±2oC.
Each procedure consists of unloaded and loaded intervention assessments (Table
3.1). The modular approach to the assessment procedure enables the duration of
intervention periods to be varied as needed and interventions to be applied
concurrently if appropriate.
Table 3.1: Tissue health assessment tool timeline for CONFORMAT concurrent with TcPO2 or LDF sensors
Side Lying Pre- Intervention Intervention Post- (Unloaded) Intervention 1 2 Intervention (Quiet) (optional) (Quiet) 20 min 5min 5 min 5 min 5 min
a) Assessment of transcutaneous oxygen tension and interface pressure: TcPO2 sensors are located over bony prominences in assessment ROI within the overall contact area. Assessment ROI for TcPO2 monitoring are selected based on the assessment goals as described in Assessment Techniques above. Tissue health response has been found to be asymmetric even in able-bodied individuals [133].
It is therefore useful to assess tissue health bilaterally wherever possible. In the case study presented in this paper, the multichannel capabilities of the TCM400 allowed two channels to be employed in order to measure TcPO2 bilaterally at the
ischial assessment ROI.
Chapter 3-86 The subject is placed in a side-lying position on a bed or plinth, with hips and
knees flexed to 90o. In this position the soft tissue over the buttock region is in the
same position relative to the bony anatomy as in sitting. This allows sensors to be
placed over the selected assessment ROI in side-lying for baseline unloaded
measurements. The bony prominence to be monitored is palpated and a fixation
ring located over the bony landmark. The central region of the ring is filled with
contact fluid and the electrode securely attached. The attachment procedure is
then repeated for the contralateral region of interest. To allow local vasodilation
to stabilize, a 20-minute equilibration period with the sensors unloaded is
completed before TcPO2 monitoring commences.
Following the equilibration period, the subject is carefully transferred to the loaded posture and the sensor location palpated to ensure it remains over the relevant bony landmark before continuing with the loaded assessment phase.
The IP mapping system is calibrated to 80% of the participant’s weight based on an estimate that approximately 20% of their weight acts through the backrest and footrests [160]. TcPO2 levels are continuously monitored throughout the loading
period concurrent with IP measurement. Event markers are activated in the TCM
system to sync IP data collection with TcPO2 measurement and assessment
periods, e.g. quiet sitting, weight-shifting. On completion of the loaded tissue health assessment, the participant then transfers to the mat for removal of TcPO2
sensors.
Chapter 3-87 b) Assessment of blood flow and interface pressure: The participant is asked to lie on their side with knees bent to allow for palpation and placement of the sensor over the selected assessment ROI. As noted above, tissue health response has been found to be asymmetric [133]. If repeated unilateral measurements are to be made, it is important that the either a left or right measurement region is selected at initial assessment and used at all assessments thereafter so that changes over time can be monitored reliably. Consistent participant positioning and bony landmark palpation prior to placement of the sensor is also essential in order to optimize repeatability. A BPM2 flat flexible sensor (model # 4415) is secured in place using medical tape. To allow for local blood flow to stabilize, a
20-minute equilibration period with the BPM2 sensor unloaded is completed before monitoring of blood flow levels commences.
Following the equilibration period, the subject is carefully transferred to the loaded posture and the sensor location palpated to ensure it remains over the relevant bony landmark before continuing with the loaded assessment phase before continuing with the seated assessment. Blood flow is continuously monitored with the subject throughout the loading period concurrent with interface pressure measurement. In order to match interface pressure data collection with blood flow measurement, events are synced manually.
Specifically, the observer presses an event marker in the Labview data
Chapter 3-88 acquisition interface for the BPM2 system concurrent with starting recording of interface pressure data and again when the recording period is completed.
Case study
The local institutional Review Board (MetroHealth Medical Center) approved the
protocol for this study.
Seated Assessment:
Current Example – Intervention: A 61 year old male with at T7 ASIA A injury for 21 years was assessed. He used a manual wheelchair with a ROHO cushion
and was able to perform push-ups and side-to-side weight shifts independently.
During the pre-intervention, the participant sat quietly for 5 minutes in a comfortable position while maintaining an upright posture. This was followed by 5 minutes intervention period of side-to-side weight-shifting. During the intervention period the participant leant from left to right at a self-selected rate.
This was then followed by a post-intervention period of 5 minutes of quiet sitting.
DATA ANALYSIS: The case study assessment produced three phases each of 5
minutes duration; pre-intervention, intervention and post-intervention. As
described above, the first and last minute of each phase was discarded from
further analysis of all variables in order to minimize transition effects. Thus, data
Chapter 3-89 sets of three minutes duration were extracted for further analysis as described in
detail above.
RESULTS:
Case Study: Tissue health outcomes measures for the case study with
independent self-regulated side-to-side weight-shifting showed there was no
change in mean IP for the total contact area over the entire assessment period
(Figure 3.5a/c). During the intervention, left ischial ROI interface pressures
increased, while right ischial ROI IP decreased. Post-intervention ischial region pressures were higher bilaterally than pre-intervention values. Sacral ROI interface pressures increased over the total assessment period, i.e. between pre- and post-intervention. Maximum IP gradient increased during intervention but decreased post-intervention (Figure 3.5b/c). The sensels that registered saturation pressure at baseline did not remain static. Saturation pressure was also measured at other sensels during the assessment indicating that there was redistribution of high pressure.
Chapter 3-90
Figure 3.5a: Interface pressure distribution: seated interface pressures under each intervention conditions are shown. All images are orientated with the back of the seating region is at the base of the image. The color map indicates high and low pressure areas.
Figure 3.5b: Maximum interface pressure gradient. All images are orientated with the back of the seating region is at the base of the image. The blue region indicates the total contact area. The location and direction of the interface pressure gradient is indicated in green. Saturation, i.e higher than range, pressures are indicated in red.
Figure 3.5c: Interface pressure summary
Chapter 3-91
Figure 3.5d: Tissue oxygenation within each assessment phase showing distribution of high, mid and low oxygenation.
Legend: Pre-L = pre-intervention left ischial ROI Pre-R = pre-intervention right ischial ROI Int-L = Intervention left ischial ROI Int-R = Intervention right ischial ROI Post-L = post-intervention left ischial ROI Post-R = post-intervention right ischial ROI Figure 3.5: THEToolbox Results Panel: Effects of weight shifting on sitting posture. a) Interface pressure distribution. b) maximum interface pressure gradient. c) interface pressure summary. d) tissue oxygenation. e) LDF Wavelet Analysis (below)
Tissue oxygenation was high (above 30mmHg) in the right ischial region
throughout the assessment (Figure 3.5d). In contrast, tissue oxygenation at the left ischial region was very low throughout the assessment period. LDF STFT wavelet analysis indicated, there was a slight decrease in the metabolic
Chapter 3-92 contribution during intervention, which decreased further post-intervention
(Figure 3.5e). The neurogenic component was unaffected during the weight- shifting intervention, and decreased post-intervention. The myogenic component increased slightly during the weight-shifting intervention and post-intervention returned to pre-intervention levels.
Figure 3.5e: LDF Wavelet Analysis
i. Log-Amplitude STFT for blood flow signal, normalized to total flow
ii. Contribution of each blood flow component in the STFT signal at each phase of the assessment, normalized to the energy of the whole signal. Legend: Met= metabolic, Neuro=neurogenic, Myo =myogenic
DISCUSSION
Despite on-going research and efforts in PU prevention, this devastating
complication continues to pose a major secondary risk factor for many
individuals including people in a hospital or hospice setting with impaired
sensation or bodily function and those with chronic disease or disorders such as
diabetes, amyotrophic lateral sclerosis and SCI [46]. THEToolbox may be used to
Chapter 3-93 study individuals who have chronically compromised circulatory or
microcirculatory systems, due to disease or disability. It can also be applied to or
those with acute immobility or similar short-term constraints, such as airplane or
space pilots.
Soft tissue materials properties have been compared by loading tissue with an
indenter or increased pressure normalized to completely unloaded tissue values.
Using the THEToolbox methodology it is possible to compare to unloaded values
and/or the differences between a quiet loaded posture and an intervention. The
magnitude of external applied loads arises from the proportion of the
individual’s weight acting on the support surface of interest. The distribution of
the applied loads is due to several inter-related factors, including local anatomy
and any pressure relief system employed. In many individuals at increased risk for PU development, changing posture may also produce a systemic physiological change for example due to postural orthostatic hypotension or autonomic dysreflexia. In most situations, the clinical and research goal is to
provide an intervention that will improve tissue health status relative to the
initial posture.
THEToolbox was developed with the goal of assessing tissue health in a
physiologically relevant posture. It can be used to assess tissue health in sitting
or lying postures. Systemic physiological conditions such as smoking,
Chapter 3-94 pharmaceutical or substance use are known to have deleterious effects on oxygen
perfusion or blood flow. THEToolbox takes into account the individual physiology and physical conditions of a person by comparing the intervention and post-intervention to pre-intervention responses. Our approach to studying tissue health thus allows multiple factors to be evaluated with the individuals in the physiologically appropriate position with an internal control for systemic effects.
The components employed in THEToolbox complement each other by evaluating
different aspects of tissue health to provide a quantitative overall assessment. IP
mapping can be an invaluable tool for biofeedback, which allows seating clinics
to provide good education and an idea of gross needs for improvements in
sitting cushions or postures. However, IP is highly individualized: not only are
two people of similar build and weight likely to have different seating interface
pressures but even the left and right seating areas of the same person are not
symmetric [133]. Moreover, IP only measures what is happening in the region
between the support surface and the user. Used alone it cannot provide an
objective measure of tissue health.
There is currently no simple direct way to measure shear which is clinically
feasible. Although implanted shear sensors have been proposed for prosthetic
applications [161], they have not been developed for soft tissue environments.
Chapter 3-95 Imaging approaches such as MRI can measure local deformation [162] but are not clinically feasible for routine use. Maximum IP Gradient measures the greatest difference in pressures over a small area, and is thus a reasonable surrogate for shear forces at the seating surface. It should be noted that the relationship between maximum IP gradient and internal shear forces is likely to be affected by local soft tissue composition. For example, force transmission in an individual with muscle atrophy will differ from that seen in an individual with a higher proportion of adipose tissue. As a general principle, high risk zones for
PU development in a seated and side-lying person include the ischial tuberosities and sacral area. Maximum IP gradient can provide an active indication of increased risk by highlighting the specific location where the greatest surface shear forces are present.
TcPO2 measurements give an indication of the health and vascularity of the soft tissue in the region of interest. Analyzing the different microvascular perfusion components through spectral analysis of blood flow provides some insight regarding the underlying physiology of the person, as in the case study presented. Concurrent application of these assessment methodologies using
THEToolbox can start to elucidate the changes that occur in response to loading and unloading.
Chapter 3-96 CASE STUDY DISCUSSION:
In the current case study, IP mapping indicated that the weight-shifting intervention appeared to effectively alter ischial and sacral region IP values, with a concurrent increase in maximum IP gradient. The intervention did not appear to impact ischial region tissue oxygenation, which was very low on the left side and high on the right side. Blood flow STFT showed increased myogenic contributions and decreased metabolic contributions.
Relative to pre-intervention tissue health variables, post-intervention tissue health status showed increased mean interface pressures for analysis ROI, with a concurrent decrease in maximum IP gradient. Ischial region tissue oxygenation had similar values to pre-intervention values. Blood flow STFT showed a general decrease in blood flow contributions compared to pre-intervention components.
In this case study, it could be seen that while IP mapping provided biofeedback that would appear to indicate that the weight-shifting intervention was effective, this intervention did not impact either tissue oxygenation or blood flow.
Clinically, this would indicate that this individual should be recommended to modify their pressure relief regime to include maneuvers or interventions that would allow recovery of adequate tissue oxygenation in the left ischial region.
Such modifications could include forward leaning, if the individual has sufficient trunk stability to recover from a forward lean. Effective interventions for an
Chapter 3-97 individual with less mobility could include the use of tilt-in-space wheelchair or a dynamic weight-shifting cushion.
THEToolbox assessment also showed that the normal inverse relationships between tissue oxygenation and blood flow and interface pressures and pressure relief maneuvers were not present. Furthermore, there did not appear to be a direct relationship between ischial region tissue oxygenation and blood flow for this individual. As described in the Background this phenomena has been observed previously in individuals with SCI and may be indicative of impaired microvascular response to applied loading. This would imply that this individual did not have a normal healthy adaptive response to applied load, providing a further indication that there was a sustained increased risk of PU development.
LIMITATIONS:
Interface Pressure mapping: Any quantitative sensor should be reliable and accurate over the range and time for which it is being used. The ideal interface pressure sensor should also be thin and flexible so that it causes minimal disruption at the interface it is measuring. These requirements have led to advances in pressure sensor design leading to increased reliability. However, the materials properties of a piezoresistive sensor mat such used in the
CONFORMat system, can limit the duration of reliable measurement. As an individual sits on the mat, the conductive and semi-conductive inks will heat up,
Chapter 3-98 causing creep in the IP measurements. This can be addressed by recalibrating the
IP sensor mat frequently. In our protocol, the IP sensor mat is calibrated at the beginning of each assessment. The total assessment period, as shown in Table
3.1, is 15-20 minutes long. Over this length of time, minimal creep and measurement drift would be experienced. However, caution should be used if extended intervention periods are assessed because creep may lead to inaccurate
IP measurement during later intervention and post-intervention periods
Tissue oxygenation monitoring: TcPO2 measurements are obtained using small rigid sensors with a height of 1 to 1.5 cm. These sensors have the potential to disrupt the local interface pressure distribution and produce an additional localized pressure in the assessment ROI. Previous work has shown that, if the subject is sitting on a conforming surface, TcPO2 measurements are minimally affected by the load induced by the sensor itself. It has also been our experience that there are no detrimental effects on the skin due to loading the sensor. The design and function of the sensor is not detrimental to the tissue health and local erythema dissipates within 30 minutes of sensor removal. As noted in the
Assessment Techniques, if the subject is being assessed on a non-conforming surface it will be necessary to place a compliant ring of material such as foam around the sensor to avoid increased local pressures.
Chapter 3-99 Blood flow analysis: The laser Doppler flowmetry system used in THEToolbox
does not use local tissue heating. Thus, blood flow assessed is derived from the
superficial tissue regions and most likely does not approximate the blood flow in
deeper arteries and veins. Doppler measurements are also dependent on the
reflected and refracted light. Though fidgeting and unconscious weight shifting
is not usually present in persons with restricted mobility, some do have frequent
spasms. Muscular spasms can temporarily alter blood flow and add spiking
noise to the LDF data. In THEToolbox analysis, this noise was minimized using a moving average filter and low pass filter with a frequency cutoff at 2.5 Hz. The duration of assessment may also minimize the number of low frequency oscillations that are measured. However this must be balanced by the need to minimize IP sensor drift and the practicality of extended assessments, particularly in the busy clinic setting.
CONCLUSIONS:
THEToolbox was developed with the overall goal of providing an approach to
tissue health assessment that can be used by the researcher in the tissue health
laboratory and the therapist in the clinical setting. The modular approach allows
the appropriate tools to be selected for quantitative characterization of tissue
health while accommodating considerations such as available time and.
THEToolbox outcomes measures can be used in conjunction with relevant clinical
information to provide a personalized approach to preventing pressure ulcers.
Chapter 3-100 For example, digital recordings of weight shifting maneuvers or sitting posture can provide a record of changes over an extended period of time.
In the case study presented, the intervention of interest was weight-shifting while seated, thus a seated assessment was performed. THEToolbox assessment indicated that the weight-shifting employed was not adequate to maintain healthy ischial region tissue oxygenation. The normal healthy adaptive response to applied load was not observed. In order to decrease this individual’s risk of
PU development, a regular pressure relief regime is essential. The provision of an
‘automated’ intervention to augment active weight-shifting should be considered. This could be achieved by addressing intrinsic tissue health in order to increase resistance to PU development using techniques such as electrical stimulation which has been shown to increase muscle bulk and vascularity [71].
The use of tilt-in-space wheelchair or a dynamic weight-shifting cushion should also be considered.
The THEToolbox assessment methodology obtains clinically relevant measurements in a physiologically relevant posture for comparison of an intervention with pre-and post-intervention periods. Frequent use of the
THEToolbox assessment methodology could enhance our understanding of periodic changes in tissue health. Significant changes could also alert the clinician that an individual’s personalized PU risk status had increased.
Chapter 3-101 Chapter 4) The impact on tissue health of using a dynamic cushion
4a. Preface
Having introduced the use of THEToolbox, we now present some cohort and
longitudinal assessments employing THEToolbox measurements.
4b. The impact on tissue health of using a dynamic cushion
Paper for submission (in preparation)
Background:
Motivation: To compare the efficacy of independent pressure relief performed
with the participant’s prescribed pressure redistributing cushion (IPR) to
pressure relief performed by an alternating pressure dynamic cushion (PR-D) for
persons with spinal cord injury (SCI) while sitting in a wheelchair.
In wheelchair seating clinics, interface pressure (IP) maps have been used to
recommend seating cushions and pressure relieving interfaces [116]. IP mapping
provides visual feedback for the patient and allows the clinician to point out high interface pressure areas that need to be addressed by cushion modification for improved pressure redistribution. Even so, some persons continue to be at risk of developing pressure ulcers. Our previous studies report that IP mapping does not always relate with concurrent transcutaneous oxygenation (TcPO2), this might be due to impaired adaptation to applied pressures in persons with SCI
Chapter 4-102 [133]. A systems-level approach can help elucidate the biomechanics of at-risk
tissue and its response to pressure redistribution. Measuring interface pressures
together with subcutaneous blood flow measurements using LDF) [163,164] can
help determine component contributions to blood flow and microcirculation of
the tissue immediately interacting with the pressures. Measurements of
underlying tissue oxygenation with transcutaneous oxygen pressures (TcPO2)
[138, 165] can reveal oxygenation in deeper tissues.
Studies regarding induced pressures and corresponding tissue measurements
typically involve the person lying prone or on their side and tested with a controlled pressure inducer. The Tissue Health Evaluation Toolbox
(THEToolbox) was developed for use in a more practical clinical setting: taking measurements while the person is seated on their cushion.
Pressure ulcer development is multifactorial [12,166], because of this it is hard to
determine the effectiveness of an intervention or cushion just by looking at one
factor. As such there is no current standardized approach to managing the individual-at-risk of developing PUs [79]. Many techniques have been employed
to minimize high pressure areas and prevent long periods of diminished
circulation; current recommendations of PU prevention include adherence to a
weight shifting regimen and use of pressure redistributing/relieving cushions
[60,167]. THEToolbox is a multi-factorial tissue health assessment protocol that
Chapter 4-103 includes key measures to assess the effects of weight shifting interventions. In
this paper we present a longitudinal repeated-measures study of 13 individuals
with SCI using a dynamic cushion.
Methodology:
Collection and analysis of data were performed according to the methodology
previously described in THEToolbox methods paper [Chapter 3].
Assessment Procedure
The study compared the effects on tissue health with independent pressure relief
performed on a prescribed cushion (IPR) and pressure relief provided by a
dynamic cushion (PR-D). The different independent pressure relief techniques
include tilt and recline with a power chair, shifting weight from side to side,
leaning forward and wheelchair push-ups. These were performed according to
the abilities of the participant. Prescribed pressure-redistributing cushions include air-filled, gel filled and foam cushions.
The Airpulse PK cushion (Aquila Corporation, Holmen, WI) was the powered alternating pressure active cushion used for PR-D assessments. A battery powered control unit inflates and deflates alternating cells in timed intervals to allow for weight redistribution. The pressure in select cells is programmed to be maintained for 3-minute intervals with a transition period between
Chapter 4-104 inflation/deflation lasting approximately 1 minute. The cushion is set to an
inflation pressure relative to the weight of the person. One (1) initial assessment
was performed using IPR and six (6) assessments performed with PR-D after use
for 2 week periods at 3 months intervals for 18 months.
Each tissue health assessment (Figure 4.1) commenced with an initial period of
20 minutes with the participant side-lying on a mat. This allowed the participant to acclimatize to the clinical environment and minimized personal differences in seating fatigue of tissue prior to assessments. The TcPO2 sensors were placed on the skin over the left and right ischial tuberosities (IT). The CONFORMat was placed on the cushion prior to the seated phase of the assessment. The intervention period for IPR assessment involved performing independent pressure relief maneuvers according to their normal regime. The intervention period for PR-D assessments involved periodic inflation and deflation of cells under the IT: Intervention 1 cushion starts with high inflation on right IT area
(pattern A) and switches to high inflation on left IT area (pattern B) halfway through the measurement, giving relief on the right side, while Intervention 2 relieves the left side. (Figure 4.2)
Chapter 4-105 The seating periods are repeated after another 20 minutes of side-lying but this time replacing the TcPO2 sensors with the LDF sensor placed on the skin proximal to the right IT.
Each Participant has independent pressure relief (IPR) and 6 dynamic cushion (PR-D) assessments Each Assessment consists of IP with TcPO2 and BPM IPR measurements
MCP+TcPO2 Each measurement has a side-lying period and 4 seating periods 6x MCP+BPM Side Lying Q1 I1 I2 Q2 PR-D
Figure 4.1: Diagram of THEToolbox Assessment for each participant in the study
Output Measurements
Tissue health measurements were described in Chapter 3. Primary tissue health
measurements were used in this study to simplify analysis. Mean contact
pressures for the left and right ischial tuberosity (IT) regions of interest (ROI)
were used for interface pressure. Mean TcPO2 was used for tissue oxygenation
and percent contributions of blood flow components for LDF.
In the current study, statistical analyses were performed using Wilcoxon Rank
Test and Friedman Test unless otherwise noted. The Wilcoxon Rank Test is a
nonparametric test for the significance of the difference between distributions of
Chapter 4-106 two non-independent samples involving repeated measures or matched pairs.
The Friedman test is also a nonparametric test for the significance of the
difference among the distributions of several correlated samples of equal size
involving repeated measures or matched sets. Nonparametric statistics was used
because with measurements including intervention periods because normal
distribution of data and equal variance cannot be assumed.
For each tissue health measurement, the mean value was taken for each seating
period (quiet and intervention periods). Measurements during IPR maneuvers
on a prescribed cushion were compared as a cohort between each seating period
(section 4.1). The changes over time for 6 PR-D pre-intervention assessments were analyzed with repeated measures ANOVA for longitudinal studies (section
4.2). The tissue health measurements for the 6 PR-D assessments did not exhibit a clear trend and were pooled together as an average measure (PR-DAve) for each
participant. The measurements for each seating period were compared to each
other (section 4.3). Finally, IPR and PR-DAve measurements were compared to
see how they affect tissue health differently (section 4.4).
Results:
4.1) Impact on tissue health with independent pressure relief
In the current study, IPR maneuvers sitting on a prescribed cushion produced
significantly decreased mean IP (p<0.05), significantly increased TcPO2 (p<0.05)
Chapter 4-107 and increase in most contributions of blood flow (except respiratory and cardiac
components) during independent pressure relief. The decrease in mean IP during intervention was sustained for the right side through post-intervention, though no significant sustained increase of TcPO2 (Table 4.1) or blood flow contributions were observed except for the cardiac component.
Table 4.1: Change in mean contact pressures (MCP) and TcPO2 during IPR (all patients, n=13).
Assessment Side MCP TcPO2 Side MCP TcPO2 Period Q1 and I1 Left Q1 > I1 * Q1 < I1 * Right Q1 > I1 * Q1 < I1 Q1 and I2 Left Q1 > I2 * Q1 < I2 * Right Q1 > I2 * Q1 < I2 Q1 and Q2 Left ------Right Q1 > Q2 * --- I1 and I2 Left ------Right I1 > I2 * --- Legend: Wilcoxon Signed-Rank Statistics: * for p<0.05
Three (3) participants employed different pressure redistribution techniques
during intervention periods (I1 and I2). Significant difference was observed in
MCP between techniques for the right side, but was not observed for TcPO2
between interventions (Table 4.1). LDF showed a trend to increase with
metabolic contribution and decrease for the other components.
Chapter 4-108 4.2) Pressure relief changes over time with dynamic cushion
Pressure relief due to dynamic cushion weight shifting produced significant
differences between intervention periods for most participants. A correlated
sample repeated measures ANOVA between seating periods for each assessment
was performed to test whether THEToolbox measurements were consistent over
a period of time,. A significant F-Ratio for 88% of the participants was observed
for MCP. The Tukey HSD test for significant differences between pairings show
non-significant differences for most pairings but first and fifth assessments
tended to be significantly different from other assessments (Table 4.2). This was
specially observed for persons with spastic paralysis. Similar results were seen
with TcPO2 longitudinal measurements where the first and fifth assessments
tended to be significantly different from the rest of the assessments.
Chapter 4-109 Table 4.2: Significant differences between mean contact pressures in the ROI during quiet seating assessments
Graphs of mean contact pressures over six PR-D Positive Tukey HSD test Assessments for each participant for significant difference in paired comparisons Representative for high MCP over time (High Cervical) cervical injury:
Pre- Int 1 Int 2 Post- Very few significant
100 difference between 80 assessments 60 40 20 0 1 2 3 4 5 6
MCP of ROI (mmHg) of ROI MCP PR-D Assessments
Representative for spastic MCP over time (Spastic) paralysis:
Pre- Int 1 Int 2 Post- Significant differences
100 between 1st and 5th with other assessments 50
0 1 2 3 4 5 6 MCP of ROI(mmHg) MCP PR-D Assessments
Representative for flaccid MCP over time (Flaccid) paralysis:
Pre- Int 1 Int 2 Post- Some significant
100 difference between assessments 50
0 1 2 3 4 5 6
MCP of ROI (mmHg) of ROI MCP PR-D Assessments
Chapter 4-110 4.3) Impact on tissue health with dynamic cushion
Inflation Pattern A Inflation Pattern B MCP of Left ROI MCP of Right ROI
150 150 100 100 50 50 0 0
MCP (mmHg)MCP Q1 I1 I2 Q2 (mmHg)MCP Q1 I1 I2 Q2
Figure 4.2: Dynamic cushion in different inflation patterns with left and right ROI outlined in blue box. Representative graphs of mean contact pressures (MCP) during pre- intervention (Q1), interventions 1 (I1-Pattern A), 2 (I2-Pattern B) and post-intervention (Q2) periods. Green = low, red = high inflation.
When the dynamic cushion is turned on during intervention it follows a periodic pattern of inflation, because of this the interpretation of MCP was more involved although consistent. The right ROI had higher inflation during Intervention
1(Inflation Pattern A) and near the end of the seating period inflation was switched to relieve the right side, this was followed by Intervention 2, where the left ROI had higher inflation (Inflation Pattern B) and at the end of the seating period inflation is switched, relieving the left side and inflating the right side
Chapter 4-111 before Q2 seating period began. (Figure 4.2) Significant decrease or increase in
MCP followed accordingly (Table 4.3).
Table 4.3: Change in mean contact pressures MCP and TcPO2 for PR-DAve (all patients, n=13).
Assessment Side MCP TcPO2 Side MCP TcPO2 Period Q1 and I1 Left Q1 > I1 * Q1 < I1 Right Q1 < I1 Q1 < I1 * Q1 and I2 Left Q1 < I2 Q1 < I2 Right Q1 > I2 * Q1 < I2 * Q1 and Q2 Left Q1 > Q2 * --- Right Q1 < Q2 * --- I1 and I2 Left I1 < I2 * --- Right I1 > I2 * --- Legend: Wilcoxon Signed-Rank Statistics: * for p<0.05
Mean TcPO2 of PR-DAve showed a significant increase in mean TcPO2 for the right ROI compared to quiet sitting (Q1) for both intervention periods (I1, I2 p<0.05). Although increases were noted on the left side, the changes were not significant for this population.
Compared to Quiet sitting, intervention caused an overall decrease in total blood perfusion power spectral density, with significantly decreased neurogenic and
increased cardiac components. The pressure relief performed between I1 and I2
produced a significant increase in total blood perfusion, matched with a trend
toward increase of component contributions except for Respiratory. There was
no significant difference in LDF between pre- and post-intervention periods.
Chapter 4-112 4.4) Comparison of independent pressure relief and pressure relief due to
dynamic cushion weight shifting
Pressure relief with dynamic cushions had similar pre- and post-intervention
MCPs with IPR. IPR produced better pressure relief with significantly lower
MCPs during intervention periods (p<0.05). Q1 and Q2 were similar for Left side but PR-DAve had higher interface pressures on the Right side at Q2. This could be
expected as the PR-D cushion is in pattern A with higher inflation in Right ROI
during Q2.
Improvements in oxygenation between the Q1 to I1 on the left ROI for IPR was
significantly larger in magnitude for IPR compared to PR-D. There was no
significant difference for the increase in TcPO2 on the right ROI between IPR and
PR-D.
Overall PR-D had significantly lower metabolic, neurogenic and myogenic
contributions than IPR during intervention periods. Post-intervention PR-D had
lower metabolic but higher neurogenic contributions than IPR (p<0.05).
Blood flow component contributions varied in the study cohort. Level of injury
(American Spinal Injury Association Impairment Scale (AIS)) may affect the
responsiveness of the average individual contributions to blood flow on a per
person basis (Table 4.4).
Chapter 4-113 Table 4.4: Table of participants arranged according to injury level with varying responses in blood flow contribution during pressure relief.
PT# Injury IPR: Q1 to I1 or I2 PR-D: I1 to I2 Level Met Neu Myo Met Neu Myo High Cervical Injury PT008 C2-A - - + - = = PT015 C2-A = - - + - - PT002 C5-C - = + = + = Spastic Paralysis PT009 C6-C + + - + = + PT000 C6-D + + - = - + PT012 C7-C + + = + + = PT016 C8-A + + + + + - PT014 T4-A + + - = + + PT001 T5-A + + - = - = PT013 T6-A - + + + = - Flaccid Paralysis PT004 T7-A + = + - = + PT011 T10-A - - + - + - PT005 T12-A = - + - + + Legend: (+) increase or (-) decrease in blood flow component during pressure relief, (=) varying changes for the repeated measures
A) Participants with very high cervical injury (c5 and above) have decreased metabolic and neurogenic components with IPR and varied changes with PR-D.
B) Participants with Spastic Paralysis – (injury of T6 and above) tend to have increased metabolic and neurogenic components during IPR intervention and increased metabolic but varied responses in neurogenic and myogenic components for PR-D
C) Participants with Flaccid Paralysis (injury below T6) have increased myogenic component during IPR intervention. With a decreased metabolic and increased neurogenic and myogenic with PR-D (Table 4.4)
Chapter 4-114 4.5 Correlations between MCP and TCPO2 or LDF
Overall both IPR and PR-DAve have negative correlation between MCP and
TcPO2. However some individual assessments have positive correlations
between MCP and mean TcPO2
Overall there was no significant correlation between MCP and LDF for either IPR
or dynamic cushion weight shifting. The LDF components did not have clear
correlations to interface pressures. The general trend for MCP and LDF is
negative correlation between metabolic and neurogenic contributions and MCP
and varying correlation between myogenic contributions and MCP.
Discussion
Independent pressure relief is effective in significantly relieving mean contact
pressures and, to a certain extent, increases TcPO2 during pressure relief.
Furthermore we see a general increase in blood perfusion in LDF contributions of
metabolic, neurogenic and myogenic components. There is an increase in cardiac
component during post-intervention not seen during IPR which could be a result
of physical movement. THEToolbox measurements for PR-D have similarities to
IPR yet distinct differences in response to interventions and pressure relief.
Chapter 4-115 Mean interface pressures and pressure relief with IPR and PR-D
Direct comparisons between IPR and PR-D should be avoided. Pressure relief with a dynamic cushion is dependent upon the inflation of the cells in the cushion. The pre-intervention seating period of the dynamic cushion is determined by the inflation condition of the cushion before the control unit is turned off. Therefore unless the cushion is calibrated for each sitting period, IP would not be evenly distributed for both left and right ROIs unlike when a person has good postural alignment on a prescribed cushion. Likewise the intervention with PR-D works by inflating the cell underneath one ROI while deflating the cell on the opposite ROI. This pressure relief is more similar to pressure redistribution by shifting their weight/posture from left to right or vice versa. We should not only consider changes from quiet periods and intervention period but also for differences between high and low pressure relief (such as pre- intervention and intervention for IPR and alternating periodic interventions for
PR-D). Taking this into account, the pressure relief period of PR-D between loading and relief produces similar changes in tissue health that are smaller in magnitude to that of IPR.
Impact of dynamic cushions on TcPO2
Interventions 1 and 2 for the dynamic cushions are at different inflation patterns and correspond to pressure relief for one side and loading for the other ROI.
Even so, the changing inflation patterns produce an increase in mean TcPO2
Chapter 4-116 (significant for the right side). This shows that even though the MCPs follow the
inflation pattern of the cushion, it was effective in increasing mean TcPO2 for
both ROIs. Interestingly, with the IPR significant increase in TcPO2was observed only with the left side. This is probably due to postural differences and small
sample size. This agrees with earlier studies that not only are IPs not symmetric
with the left and right sides but likewise the TcPO2 response to intervention is different between left and right ROIs [133]. It is unclear whether this asymmetry is due to external factors such as duration of pressure relief, cushion inflation, subject posture or asymmetric physiology.
Impact of dynamic cushion use on blood perfusion contributions
Persons with SCI have significantly lower relative amplitude of metabolic and
neurogenic components when compared to able-bodied subjects [163]. An increase in these lower frequency blood flow components show improved blood perfusion in the tissue but it could be a result of hyperemia.
Unlike TcPO2, LDF measurements seem to be more sensitive to the MCP of the
ROI as opposed to general increases in TcPO2 during intervention, the blood flow components response to relief is most evident between Intervention 1 and 2.
The pressure relief from loading to relief (I1 to I2) with PR-D results in significant increase in total power spectral density of blood flow contributions. With PR-D relief (I1 to I2) there is an increase in metabolic, neurogenic and myogenic
Chapter 4-117 components which is similarly observed with IPR. The difference in PR-D and
IPR is that during post- intervention we see that these lower components decrease contribution although myogenic contribution with PR-D is still increased. This suggests improvements in perfusion that are longer lasting.
Overall IPR and PR-D relief produce increases in blood flow contributions.
Individually, we observed different responses to intervention. Only the group with spastic paralysis had consistent and similar responses of blood flow contributions to IPR. Most participants had varying responses to IPR and PR-D.
Longitudinal considerations
The dynamic cushion was used for 2 weeks before each assessment at 3 month intervals. There was no increasing or decreasing trend for either MCP or TcPO2 over the 6 repeated PR-D assessments except for one participant with increasing
MCP. Rather some trends were seen with spastic paralysis individuals where there were significant differences among paired assessments between the 1st with other assessment and 5th with other assessments. It is possible that these are due to periodic changes such as weather or physiology as the 1st and 5th assessments are separated by one year. Clothing and cushion inflation should be considered for uniformity/consistency.
Chapter 4-118 Discussion of Correlation
Correlation data was negative for pooled participants but some assessments that
produce a consistent positive correlation. Furthermore, the correlations were not
always the same for the left and right side of the same participant. The asymmetry and individual variations in TcPO2 and blood flow contribution responses to pressure relief help us better appreciate the variation in the SCI population. There is no significant correlation with the pooled population for
MCP and LDF but trends per spastic paralysis participants suggest increased metabolic and neurogenic component contributions and varying myogenic
responses during pressure relief, suggesting varying vascular tone in the gluteal blood flow of these individuals.
In clinical practice, when recommending a cushion and pressure relief regimen one should also consider both pressure and time. Even though top of the line air- filled cushion may have better pressure redistribution characteristics, the person who is not able to or forgets to pressure relief would have these pressures over a prolonged period of time. Though, the PR-D cushion may have higher peak pressure during moments of high inflation, pressure can be redistributed periodically and prolonged high pressures can be prevented.
Chapter 4-119 Conclusions
Taken as a cohort, we observed a similar response in tissue health measurements
to pressure relief with a dynamic cushion and independent pressure relief,
though individually these responses are varied. The individual variations might
be due to differences in physiology (muscle geometry and composition observed
in Chapter 2) and level and extent of spinal cord injury. Furthermore, it is
possible that individual variations in tissue health measurements could be used a measure of for pressure ulcer risk.
Due to the variation in response to IP changes of TCM and LDF, it is recommended that persons at risk of developing pressure ulcers should not only look at their interface pressures on the seating surface but also take into consideration MCPs for regions prone to pressure ulcer and the duration of pressure in these areas. TcPO2 and LDF measure oxygenation and regional blood flow, respectively, which are essential in maintaining the tissue health of these persons at developing PUs. THEToolbox can help to develop a profile for tissue
health and possibly help in deciding specific therapies or interventions that may
improve the tissue health of persons at risk of pressure ulcers.
Chapter 4-120 Limitations and Future Work
This study had a small number of participants and a larger sample size needs to be performed to determine statistical significance.. The variations in
measurements highlight the sensitivity and multifactorial aspect of measuring
tissue health. These could be due in part to physiological changes in the
participants over the period of time. The advantages of using their own weight to
induce pressures include understanding the individual response to pressure
relief with different interventions. Limitations include imprecise duration and
magnitude of pressures depending on the individual.
There are several ways to improve repeatability with THEToolbox measurements
with PR-D. To name a few these include: 1) repeatable and accurate placement of
sensors on the ischial tuberosities, 2) alignment of posture to previous
assessments which can be aided by camera and markers, 3) setting a standard
inflation pressure for cushions based on subject weight, 4) wear uniform or
similar clothing during assessment and 5) calibration of the cushion for quiet
sitting. Taking these into account can help elucidate improvements in
physiological and blood perfusion measurements.
Future studies on comparing PR-D and IPR could focus on more similar
interventions such as a prolonged side to side weight shift of similar duration to
that of PR-D. The PR-D should also be checked for even inflation during quiet
Chapter 4-121 sitting. In that study, the person leaning side to side would be actively relieving
pressure and be in a leaning posture while PR-D would keep the posture upright and passively redistribute pressures. Although pressure relief with a dynamic cushion is passive, it affected a significant increase in cardiac component and similar responses to independent pressure relief maneuvers.
Chapter 4-122 4c. Addendum
An exploratory study on grouping participants according to muscle composition and tissue health measurements was performed to identify clustering.
Demographic data such as History of Pressure ulcers, neurological level of SCI and weight was compared to mean TcPO2 and percent contributions of blood flow components. Increased TcPO2 is observed for persons with increased lean muscle. This can be developed as a predictive model to show interface pressures, oxygenation and blood flow from demographic data.
Independent Pressure Relief Pressure Relief with Dynamic Cushion
Figure 4.3: THEToolbox measures for when grouped by PU History
PU history is related to muscle composition and quality. Persons with PU
History exhibit higher intramuscular fat infiltration and less lean muscle. PU history was not related to muscle CSA or muscle volume. In persons with history of pressure ulcers, there is increased mean TcPO2 with IPR and Respiratory
Chapter 4-123 component contribution of blood flow is different. Metabolic component contribution of blood flow is higher with PR-D. Mean TcPO2 is higher than
10mmHg with use of PR-D though no relationship was found with PU history.
Independent Pressure Relief Pressure Relief with Dynamic Cushion
Figure 4.4: THEToolbox measures when grouped by Neurological Level
Persons with flaccid paralysis (neurological level below T6) have lower respiratory and cardiac contributions with IPR compared to higher level of injury. But when using dynamic cushion have higher neurogenic and respiratory contributions and decreased Mean IP. This might be confounded by subject recruitment since in the cohort those with injury lower than C8 had complete injuries and some with higher injuries had incomplete injuries.
Chapter 4-124 Pressure Relief with Dynamic Cushion
Figure 4.5: THEToolbox measures when grouped by weight
Those weighing less than 180 lbs have smaller muscle CSA, higher %fat infiltration and lower %lean muscle and decreased %Cardiac contribution.
Independent Pressure Relief Pressure Relief with Dynamic Cushion
Figure 4.6: THEToolbox measures when grouped by myogenic contribution
Myogenic contribution vary with mean IP during quiet sitting. With PR-D, increased myogenic contribution imply vasodilation due to decrease in IP. While with IPR increased myogenic contribution might be due to decreased arterial pressures downstream from high IPs.
THEToolbox measurements can be grouped by demographic data to determine clustering. Analysis can give further implications to risk of developing PUs.
Specifically of interest would be characteristics that are present in persons with
Chapter 4-125 recurrent PU History. This could help determine a rating scale or a means to
measure the risk of developing pressure ulcers.
4d. Chapter conclusion
The general recommendation to prevent PU development is to reduce the
duration of loading by breaking up long periods of immobility weight/pressure
redistribution techniques. Even with adherence to this rigorous routine many
have shown that the pressure redistribution is not performed adequately or
maintained to relieve pressures and increase oxygenation and blood flow.
Persons with SCI who are able to, do not maintain weight shifts for an
inadequate period of time to allow for reperfusion of tissue [168].
Dynamic cushions can be used as an aid to perform periodic and maintained
weight shifts to produce positive effects in tissue health of persons with SCI. The
positive effects include significantly decreased mean contact pressures and
increased oxygenations during the intervention periods comparable to, though to
a lesser magnitude to that of independent pressure reliefs. Furthermore, we also
observed significant increases in total power spectral density of blood flow with
increased contributions of metabolic, neurogenic, myogenic and cardiac
components.
The next chapter addresses interventions that target not only the duration and
magnitude of pressure but also intrinsic physiologic changes due to SCI.
Chapter 4-126 Chapter 5) NMES and its effects on muscle mass (muscle mass changes, trunk
stimulation papers)
5a. Preface
Neuromuscular Electrical Stimulation (NMES) of the gluteus maximus provides
a means to reduce both the duration of and magnitude of pressure by cyclically
stimulating the muscles to produce side-to-side weight-shift. NMES also increases the muscle mass of atrophied muscle but this increase is only sustained with continuous use of NMES. The first paper shows muscle changes in persons
with SCI who had NMES. The second paper shows effects of Trunk NMES with
THEToolbox variant on some persons with sacral sitting and persons leaning to
one side.
5b. Assessment of gluteus maximus muscle area with different image
analysis programs
Wu GA, Bogie KM. Assessment of gluteus maximus muscle are with different
image analysis programs. Arch Phys Med Rehabil. 2009 Jun; 90(6):1048-54
Gary A. Wu, MS; Kath Bogie, DPhil
From the Department of Biomedical Engineering, Case Western Reserve
University, Cleveland OH, USA (Wu);Department of Orthopaedics, Case
Western Reserve University, Cleveland OH, USA (Bogie);Cleveland FES Center,
Louis Stokes Cleveland VA Medical Center, Cleveland OH, USA (Wu, Bogie).
Chapter 5-127 ABSTRACT
Reports of original data: Clinical implications of basic research.
Objective:
Determine the effectiveness of a percutaneous gluteal stimulation system
(GSTIM) by comparing assessments of axial CT scans for the pelvic area.
Design: Comparing the measurements of the cross-sectional area (CSA) of the gluteus maximus muscle between raters and two image analysis programs.
Setting
Retrospective axial CT scans of the pelvic area.
Participants
Nine (9) male individuals with complete (below T6) spinal cord injury (SCI) and at least 2 years post-injury participated in the study (Range: 29-75 years. Mean age: 51.8 years).
Interventions
Comparing gluteus maximus CSA before and after a period of GSTIM.
Chapter 5-128 Main Outcome Measure
Measurements made by two expert and two non-expert raters were used to compare the repeatability and reliability of measuring muscle CSA. The longitudinal study presented here are from repeated CT scans over a period of two years for one participant who received GSTIM.
Results
For repeatability: Non-expert raters measured a mean CSA of 35.2 cm2 (range 20 -
45cm2), while experts measured 21cm2 (range 10 to 35cm2). A composite of all
raters using the same program had standard deviations of 2.5-2.6cm2 for ImageJ
and 2.5-4.4cm2 for VeVMD.
For reliability: Differences between the two programs had mean differences in
standard deviation between 2.2 and 3.7 cm2.
Conclusions
The same rater and program (preferably the more reliable ImageJ) is
recommended for the course of a longitudinal study, otherwise significant error
would be introduced. Furthermore, significant increases in the CSA of gluteal
muscle compared to pre-intervention (baseline) measurements were observed for
the participant receiving GSTIM.
Chapter 5-129 Key Words
Electrical Stimulation, muscle cross-sectional area, reliability, SCI, gluteus maximus muscle.
List of Abbreviations
GSTIM – percutaneous gluteal stimulation system
CSA – cross-sectional area
CT – X-ray Computed Tomography; MRI – Magnetic Resonance Imaging
SCI – spinal cord injury
L – left; R – right
C1, C2, C3 – CT axial scan determined by anatomical landmarks approximately between the second and third sacral notch (C1), where the caudal head of the femur starts to appear (C2) and where the lateral aspect of the greater trochanter is most prominent (C3) mm2 – square millimeters; cm2 – square centimeters
2 2 2 σ – overall variance; Q – ratio of the variances (Q= σImageJ /σVeVMD )
T0, T1, T2, T3 - Time points at which successive CT scans were taken after
implantation of GSTIM. T0: immediately after implantation of the GSTIM system
serves as baseline; T1: 6 months; T2: 12 months and T3: 24 months post-
implantation.
R1, R2, R3, R4 – raters for the study. R1, R2: university students, R3, R4:
radiologists.
Chapter 5-130 INTRODUCTION
Muscle atrophy occurs due to paralysis of muscles in patients with complete spinal cord injury (SCI) due to loss of the ability to communicate command signals from the central nervous system to muscles below the level of injury.
Rapid widespread loss of muscle mass has been found to occur in the first 6 weeks following SCI [169] and continues for up to 15 months post-injury before the muscle mass eventually plateaus. Muscle atrophy leads to an average of 45-
80% reduction in muscle cross-sectional area (CSA) following SCI [170]. An estimated 20-30% of these patients develop a history of pressure ulcers at 5-10 years post-injury [171,172]. The prevalence, together with high economic and sociologic costs of pressure ulcers, demonstrate the importance of identifying risk factors, preventing pressure ulcer occurrence and developing cost-effective interventions. The finding that previous incidence of pressure ulcer is the most significant factor in predicting development of future pressure ulcers suggests that preventive methods must be made a priority [173].
The use of a percutaneous gluteal stimulation system (GSTIM) can provide a means for varying the pressure under bony prominences and minimize the loss of muscle bulk. While sitting, GSTIM can contract one side of the buttocks at a time simulating weight-shifting strategies and redistributing pressure [174,175].
Tissue viability is improved when mechanical occlusion of blood flow is alleviated increasing blood and lymph flow. Additionally, the repeated rhythmic
Chapter 5-131 muscle contractions may act as a pump increasing oxygen supply in the muscle
tissue [176,177].. Longer term studies have shown that continued use produces an
increase in weight-shifting efficacy [71].
Minimizing the loss of muscle bulk also decreases the risk of pressure ulcer development. It has been shown that electrical stimulation of paralyzed muscles affected by SCI can increase muscle bulk [178], condition the muscle and decrease fatigability [179]. Previous studies have shown an increase in gluteal lean muscle mass after six months of stimulation in patients with acute SCI [178].
CSA measurements of stimulated muscle were used as an indication of the
effectiveness of stimulation.
The primary goal of the current study was to evaluate two image analysis techniques in CSA measurements of the gluteal region anatomy. The hypothesis was that measurements from two different image analysis programs and different raters were repeatable and reliable. The secondary goal was to determine changes over time in gluteal muscle CSA with use of the GSTIM. Due to the long-term nature of the study it was also important to minimize the number of scans and confine them to the specific area of interest in order to minimize radiation exposure. CT imaging techniques met these goals and minimized the risk of compromising the GSTIM.
Chapter 5-132 METHODS & MATERIALS
Intervention and assessment
Nine (9) male individuals with complete SCI below T6 level participated in the
study. Ages range from 29 to 75 years old and mean age is 51.8. Participants were
at least 2 years post-injury. Three (3) participants received GSTIM while 6 others
served as controls.
CT imaging was used as an outcomes measure to monitor changes in the cross-
sectional area of the gluteus maximus muscle due to long-term use of GSTIM.
Two image-analysis software programs to measure the cross-sectional area were
evaluated. The goals of this evaluation study were to determine the reliability
and repeatability of measurements taken by different raters using either image
software program. Two non-expert raters did measurements for all 9 patients,
while 2 non-expert and 2 expert raters did repeated measurements for one
patient.
For participants receiving the GSTIM system, a baseline CT scan was taken
shortly after of implantation. The research participant initially underwent
conditioning stimulation for 2-3 months, in order to slowly build up the fatigue resistance of the muscles. The participants then started the dynamic stimulation phase using GSTIM daily. The frequency of weight shifting recommended for wheelchair users at risk of tissue breakdown was approximated by applying
Chapter 5-133 stimulation for a 3-minute period, with a 17-minute interstimulation interval, giving an overall 20 minute pattern. Alternating stimulation was provided to the left (L) and right (R) gluteal muscles with a duty cycle of 15 seconds on and 15 seconds off; more specifically stimulation was applied that while one muscle (L) was being stimulated the other (R) was off. The stimulation activity was then reversed (L off/R on), leading to a 50% active duty cycle for each muscle. The aforementioned stimulation protocol is further described in Bogie et al. 2006. For all participants, CT scans were taken at regular intervals during the 3 years post- implantation.
C1: Between the second C2: Caudal head of the C3: Greater trochanter is and third sacral notch femur appears most prominent Figure 5.1: CT scan image locations used for assessments. Key: outlined dotted area is the gluteus maximus. 6x6cm2 inset square on top left used as reference for VeVMD measurements.
Retrospective spiral CT scans of the pelvic area were analyzed. Scans had a resolution of 0.5-1mm in the axial x- and y-direction and 5-12mm in z-direction
(slice thickness). Baseline scans were obtained before use of GSTIM with up to three further scans obtained over a period of 2 to 36 months for each research participant. Scan locations were determined by anatomical landmarks (Figure
Chapter 5-134 5.1); between the second and third sacral notch (C1), where the caudal head of the femur starts to appear (C2) and where the lateral aspect of the greater trochanter is most prominent (C3). These three scan locations were compiled for each patient per time point. Images were de-identified and randomized prior to taking measurements.
Image Analysis Techniques
ImageJ (v1.37, National Institutes of Health, USA, http://rsb.info.nih.gov/ij/) is an image processing and analysis program written in Java for operating systems such as Linux, Windows, and Mac OSX. It is provided free of charge by the NIH.
ImageJ was used to measure muscle area by outlining the muscle on the image.
The pixel to mm2 ratio was automatically converted by ImageJ from the information stored in the image. Image editing to ease visualization of the muscle was performed when necessary. The freehand selection tool was used to outline the gluteus maximus muscle. The measure tool was then used to calculate the area within the outline. The muscle outlines were saved separately from the image for future reference. The outline could not be modified after being saved and measurements were repeated on the original image. Measurement values were saved in cm2 to a MS Excel spreadsheet.
VeVMD (v1.1.14, Verg Inc 2000) is an image analysis program primarily used for wound measurement, assessment, documentation, tracking and outcomes. The
Chapter 5-135 program calibrates wound area using a 6x6 cm2 white template placed in the field of view. In order to process CT images for measurement by VeVMD, Adobe
Photoshop CS2 (v.9.0.2 Adobe Systems Inc.) was used to create a template. This was merged onto the CT axial image to provide the VeVMD software with a reference for pixel to cm2 conversion. Adjustment of contrast and brightness was performed when necessary using other image editing software. After image preparation, measurements were taken using the outline tool. The outline was saved for future reference. VeVMD allows storage of images for the same patient in the same batch so that one can easily refer to them. It is also possible to edit the measurements after saving. Measurement values were then saved to an MS
Excel spreadsheet.
Evaluation
In order to test the repeatability (accuracy) of measurements, three repeated measurements were tested against the mean of the measurements for all raters.
The repeatability is assessed by the standard deviation from the mean. The reliability of measurements were assessed using Bland-Altman analysis which compares two outcome measures that are highly correlated and graphically represents rater bias and variance[180] by analysis of the difference of the output from the individual measures with the average output from both outcomes measures.
Chapter 5-136 The precision of each rater between image analysis programs was tested using
the methods described by Shoukri and Edge [181]. The statistic compares the
2 2 2 overall variance (σ ) to the variance of each method (σImageJ ,σVeVMD ) and
2 2 2 compares the ratio of the variances (Q= σImageJ /σVeVMD ) to σ . The statistic is similar in principle to nonparametric statistics. A value of 1 or -1 within the confidence interval Q shows comparable precision of variances.
All four raters analyzed a longitudinal series with four time points from one participant obtained over a period of two years. CT scans were obtained at T0: baseline (immediately after implantation of the GSTIM system) and T1: 6 months, T2: 12 months and T3: 24 months post-implantation. A total of four raters evaluated the scans; two experts (radiologists) and two non-experts
(university students). In order to determine intra-rater reliability, each rater repeated the analysis of all images three times for each program at intervals of 1-
2 weeks. The two non-expert raters also analyzed the remaining 8 participants following the same protocol for time periods between 3-36 months
General factorial designs were used to test the significance of the following
factors in measuring: rater, image analysis program, longitudinal measures over
time (Longitudinal), side of the body (Side), cross-sectional imaging location
(ImageLoc). Student’s t-test and Tukey’s pairwise comparisons were used to
compare the difference in measurements of significant factors, specifically to
Chapter 5-137 distinguish for separate levels of each factor, i.e. different time points in the longitudinal factor to see if the CSA of muscle changed significantly or stayed the same for each time point.
RESULTS
Histogram of ImageJ Residuals Histogram of VeVMD Residuals Normal Normal
0.15 0.15 y y t 0.10 t 0.10 i i s s n n e e D D
0.05 0.05
0.00 0.00 -15 -10 -5 0 5 10 15 -15 -10 -5 0 5 10 15 A Data B Data
Figure 5.2: Histograms showing differences in repeated measurements to the mean measurement for each muscle using (A) ImageJ and (B) VeVMD.
Legend: R1, R2, R3, R4.
The boundaries of the muscle of interest are hard to find, particularly in individuals with muscle atrophy where the fascia is not as prominent, and can lead to widely varying repeated measurements. The differences in repeated measurements as seen in the histogram (Figure 5.2) were centered about zero and had different standard deviations for each rater as seen in Table 5.1.
Measurement differences between raters showed a standard deviation of 2.5 to
2.6 cm2 with ImageJ and standard deviation of 2.5 to 4.4cm2 with VeVMD
Chapter 5-138 Table 5.1: Standard deviations of the repeated measurements for each image analysis program according to rater, N=72.
Expertise Raters ImageJ VeVMD ST Dev ST Dev Non-expert R 1 2.52 4.42 rater R 2 2.62 3.63 Expert rater R 3 2.63 2.73 R 4 2.49 2.54
10 10
5 5
0 VeVMD 0 10 20 30 40 50 10 15 20 25 30 35 40 45 50 -5
ImageJ - VeVMD -5 - ImageJ
-10 -10
-15 -15 Average of ImageJ and VeVMD Average of ImageJ and VeVMD A B y = 0.2042x - 7.9812 y = -0.3326x + 10.254
10 10
5 5
0 0 10 20 30 40 50 10 20 30 40 50 -5 -5 ImageJ - VeVMD ImageJ - VeVMD
-10 -10
-15 -15 Average of ImageJ and VeVMD Average of ImageJ and VeVMD C D y = 0.0072x - 1.626 y = 0.0226x + 0.0609
Figure 5.3: Bland Altman analysis for each rater between image analysis programs. The analysis compares the difference in measurement to the mean measurement. Y describes the trendline for each rater.
Dotted lines signify 2 standard deviations 2*SD=6.51, 7.42, 5.73, 4.21 respectively.
Legend: (A) ●R1, (B) ■ R2, (C) ♦ R3, (D)▲ R4.
The Bland Altman analysis (Figure 5.3) show that non-expert raters had inter- program measurement differences that increased with measurement size, while expert raters were not affected by measurement size with a bias of -1.6 to 0.6.
Chapter 5-139 VeVMD measurements are frequently larger than ImageJ measurements, with a trend line less than zero for all but one rater (R3). Differences between the two analysis programs were found to have standard deviations ranging from 2.2 to
3.7cm2 for all raters (Table 5.2). Measurements means are higher for non-expert raters (R1 and 2) compared to expert raters (R3 and 4). Measurement differences between programs were significant for all raters, except for one expert (R3). The
Shoukri and Edge analysis showed that precision of the two programs was comparable for expert raters but not for non-expert raters (Table 5.3).
Table 5.2: Measurement means for each image analysis program.
Expertise Rater ImageJ VeVMD ImageJ – ST Dev 95% CI p-value Mean Mean VeVMD of Mean Diff Non- R 1 31.44 32.85 -1.42 3.25 -2.79 to -0.04 P<0.05 expert R 2 37.17 39.70 -2.53 3.71 -4.09 to -0.96 P<0.05 rater Expert R 3 23.05 22.52 0.54 2.88 -0.68 to 1.75 NS rater R 4 23.07 24.64 -1.56 2.20 -2.49 to -0.63 P<0.05
Table 5.3: Shoukri and Edge analysis test for differences in precision of image analysis programs.
2 2 2 2 2 Expertise Rater σ σImageJ σVeVMD t-value Q=σImageJ /σVeVMD Non- R 1 36.31 26.51 -5.33 2.0* -4.98 expert R 2 21.77 -3.01 30.53 -2.36* -0.099 rater Expert R 3 40.79 10.14 6.27 0.24 (NS) 1.62 rater R 4 26.47 4.82 4.02 0.08 (NS) 1.199 If |t-value| < t24-2, 0.05/2 = 2.0, then the precision of measurements between the programs are equal for p<0.05.
Chapter 5-140 A General Linear Model and Tukey’s Comparison test was used to compare the
significance of these factors to the measurements. Both the main effects and
interaction plot (Figure 5.4) showed significant differences in raters (p<0.01)
except between the two expert raters.
In Figure 5.5, the muscle CSA increased compared to baseline. Non-expert raters had larger measurements compared to expert raters. Likewise, expert raters observed significant statistical differences compared to baseline using both programs (Figure 5.5A, 5.5B), while significant differences were seen in ImageJ by one of the two non-experts (Figure 5.5A). The differences in measurements between programs were statistically significant (p<0.05), with VeVMD (program
2) giving a larger measurement than ImageJ (program 1).
Longitudinal analysis for one research participant receiving GSTIM over a two- year period post-implantation showed increased muscle CSA over time (Figure
5.4, 5.5). Tukey’s comparison test showed that the difference in longitudinal measurements was significant only when compared to baseline (p<0.05).
Chapter 5-141 Main Effects Plot for Measurement Interaction Plot for Measurement Data Means Data Means
Rater Program 1 2 0.0 0.5 1.0 2.0 40 40
35 Rater 30 30
20 25 40 n a
e 1 2 3 4 1 2 Program M Longitudinal 30 40
35 20
30 Longitudinal
25 A 0.0 0.5 1.0 2.0 B
Figure 5.4: Longitudinal study for one patient. (A)Main effects and (B) interaction plot for four raters and two different programs over a period of 24 months. Legend for 4B: ●R1, ■ R2, ♦ R3, ▲ R4, ○Image J, □VeVMD.
A R1 T1 T2 T3 R2 T1 T2 T3 Interval Plot of Measurement for ImageJ 60 T0 * ** ** T0 NS NS NS T1 NS NS T1 NS NS 50 T2 NS T2 NS
t n e
m 40 e r u s a e M 30 R3 T1 T2 T3 R4 T1 T2 T3 T0 * ** ** T0 ** ** ** 20 T1 NS NS T1 NS NS Rater 1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4 Month 0 6 12 24 T2 NS T2 NS
B R1 T1 T2 T3 R2 T1 T2 T3 Interval Plot of Measurement for VeVMD
60 T0 NS NS NS T0 NS NS NS T1 NS NS T1 NS NS 50 T2 NS T2 NS
t n e 40 m e r u s a
e 30 M R3 T1 T2 T3 R4 T1 T2 T3 20 T0 * ** NS T0 ** * **
10 T1 NS NS T1 NS NS Rater 1 2 3 4 1 2 3 4 1 2 3 4 1 2 3 4 Month 0 6 12 24 T2 NS T2 NS
Figure 5.5: Interval plot of measurements using (A) ImageJ and (B) VeVMD. Interval bars represent 95% confidence interval for the mean. Measurements of gluteus maximus muscle at the slice where the caudal head of femur appears (C2) on the right side. Tables show significance of measurement differences between time points: NS= not significant, * = p <0.05 , **= p <0.01
Legend: ●R1, ■R2, ♦R3, ▲R4.
Chapter 5-142 Furthermore, in the 9 participants followed longitudinally: controls show no significant change in muscle CSA comparing baseline to the last measurement, though there was slight increases or decreases between these time periods; with the 3 participants who received GSTIM, one patient had similar results as the one presented here, while another patient showed no significant change in muscle
CSA while GSTIM was actively used but had decreased CSA when GSTIM use was stopped.
DISCUSSION
There are several significant risk factors for the development of pressure ulcers following SCI. Increased pressures over bony prominences are primary risk factors. Muscle loss leads to a reduced contact area for distribution of applied loads on the skin and soft tissues while sitting or lying, leading to increasingly high pressures. The lack of proprioception and inability to reposition in most individuals with SCI also prolongs this application of increased pressures.
Decreased blood flow further compromises the cycling of vital nutrient intake and elimination of toxins in the muscle [182]. When an individual repositions, care must be exercised to prevent soft tissue damage due to shear and friction. In addition, the skin must be checked regularly for wounds and discoloration. Skin hygiene must be maintained as incontinence and abnormal sweating adversely affect the skin health. GSTIM can be used to stimulate and condition the gluteus maximus muscle providing dynamic weight-shifting in pre-programmed
Chapter 5-143 intervals. Stimulating muscle contractions with the GSTIM may also prevent or
attenuate the muscle atrophy seen in SCI patients.
This study addresses the assessment of muscle CSA using retrospective CT scans
as a measure for the effectiveness of GSTIM to increase muscle mass. Raters used
two different image analysis programs to measure gluteus maximus CSA in
individuals with SCI, some of whom received regular GSTIM.
Resolution of CT images is in many cases comparable to MRI and the technique
does not have any contraindications for patients with implants. Furthermore, the
technique is widely available and more economical than MRI. CT produces
images by measuring the attenuation of X-rays that are sent through the body.
Different tissue types attenuate the signal differentially and thus fat-free skeletal
muscle can be assessed very effectively. Both MRI and CT give a direct
visualization of the muscle CSA and can be used to estimate the mass of skeletal
muscle [183].
Using the same rater will effectively minimize the large intra-rater differences but may limit researchers to shorter studies or to retrospective scans. The Bland-
Altman analysis showed that smaller areas tend to have greater uniformity of measurement. Expert raters were also found to obtain smaller but similar measurements, suggesting that rater training and well-defined criteria for what
Chapter 5-144 constitutes the boundaries of cross-sectional muscle area will improve repeatability. Other than training, factors that differentiate radiologists and university students may also be involved, one might want to compare
measurements done by radiologists to physicians of a different specialty or with
well-trained and minimally-trained personnel. In future studies, computer-aided
diagnosis software may be used to outline the boundaries of the specific muscle
of interest. Techniques such as increasing the high frequency content of the
image to give contrast to the boundaries of muscles, seeding and watershed
techniques to separate regions of interest may be used. Computer-aided
diagnosis may prove useful in further improving reliability and reproducibility
of muscle CSA measurements, but a human rater, preferably expert or well-
trained would need to approve of the assessment to prevent errors such as
including other muscles in the measurement.
A person with disuse muscle atrophy typically exhibits higher lipid content in
the atrophied muscles. Therefore not only does the CSA decrease over time but
also the relative percentages of fat and fat-free tissue in the muscle may change
significantly. This issue was not addressed in this current study; in the future, we
may be able to use intrinsic features in CT scans to address the issue of fat
content as fat and fat-free muscle exhibit different gray-values. The relative
percentage of fat in the muscle may be assessed by the gray-values that are
exhibited within the muscle boundary. [184]
Chapter 5-145
VeVMD is designed to take measurements of wounds and pressure ulcers and thus has a very robust and flexible data management and handling protocol.
However, VeVMD requires a square template of known size to quantify the image, presenting a potential source of error, which is not necessary with ImageJ.
ImageJ automatically reads the pixel conversion information from the CT scans and has more flexibility in image processing and analysis capabilities, such as the potential to apply a threshold based on gray-levels. This capability is of value since different tissue types have different ranges of gray-levels, and thus ImageJ can be used to segment and choose the muscle of interest via computer algorithms as described above.
CONCLUSION
This study addresses the assessment of muscle CSA using retrospective CT scans as a measure for the effectiveness of GSTIM to increase muscle mass. Raters used two different image analysis programs to measure gluteus maximus CSA in individuals with SCI, some of whom received regular GSTIM.
Either image analysis program can produce muscle measurements where inter- rater variability is minimized and measurements are similar (Table 5.1 and 5.3), but the variability in switching between different programs is significant (Table
5.2). Nevertheless, the inter-rater standard deviations are smaller for ImageJ
Chapter 5-146 (Table 5.1). These findings imply that using one program, and that ImageJ, will be more appropriate for repeatable and reliable muscle measurements.
Longitudinal studies for one research participant showed that muscle CSA changes compared to baseline were significant (Figure 5.4B). These results correspond to similar results of statistically significant decreases in ischial region pressures over time with baseline/post-intervention comparisons of sitting interface pressures for gluteal stimulation system users[116]. The error associated with using different image analysis programs and raters may mask or dramatically increase the change in measurements (Figure 5.4A). It is suggested that longitudinal studies be performed using the same program and same rater to decrease inter-rater and inter-program errors.
This paper presents development of a methodology to observe muscle CSA changes using an image analysis program. Accurately assessing the cross- sectional area of muscle has several important applications in rehabilitation, physiology, nutrition and clinical medicine. Significant increases in CSA of gluteal muscle receiving GSTIM compared to baseline measurements were observed. These findings confirm our previously observed significant changes in pressure relief in these subjects. The increase in gluteal muscle CSA provides improved pressure distribution and implies that GSTIM is an effective intervention for preventing pressure ulcers.
Chapter 5-147 ACKNOWLEDGMENTS
We thank the veterans of VA Wade Park Medical Center without which this study would not have been possible. Thanks to Dr. Ho for his professional guidance. Thanks to Xiaofeng Wang, Steven Sidik, Monique Washington for statistical expertise. Thank you to Dr. Saad, Dr. Rochon, Jonathan Olbrych as raters. Thank you to Drs. Alvarado, George and Lew and the Imaging
Department for expertise and medical images. Thank you to Jonathan Sakai,
Patricia Banks, Christine Wu, Arden Bartlett for suggestions, ideas and technical support.
This was funded by VA Rehabilitation Research and Development Service
Chapter 5-148 5c. The effects of combined trunk and gluteal neuromuscular electrical
stimulation on posture and tissue health in spinal cord injury
Submitted Paper (in press)
Title: THE EFFECTS OF COMBINED TRUNK AND GLUTEAL NEUROMUSCULAR ELECTRICAL STIMULATION ON POSTURE AND TISSUE HEALTH IN SPINAL CORD INJURY.
Authors: Gary A Wu, M.S.1, 2, Lisa Lombardo M.P.T2, Ronald J Triolo Ph.D. 2, 3,
Kath M Bogie, D.Phil 2, 3
Affiliations:
5. Department of Biomedical Engineering, Case Western Reserve University,
Cleveland, OH, 44106
6. Advanced Platform Technology Center, Louis Stokes Cleveland Department of
Veterans Affairs Medical Center, Cleveland, OH 44106.
Departments of Orthopaedics and Biomedical Engineering, Case Western
Reserve University, Cleveland, OH, 44106
Chapter 5-149 ABSTRACT
Objective: To investigate the hypothesis that combined trunk and gluteal neuromuscular electrical stimulation (NMES) alters seated posture and improves pelvic tissue health in individuals with spinal cord injury (SCI).
Design: Intervention study; case series
Setting: Research laboratory, medical center
Participants: Seven individuals with SCI and implanted lower extremity NMES
systems.
Interventions: Combined trunk and gluteal NMES in sitting. Five minutes pre-
intervention was assessed followed by 5 minutes NMES application, then 5
minutes post-intervention.
Main Outcome Measure(s): Pelvic tissue health was evaluated by concurrently
measuring transcutaneous oxygen tension (TcPO2) bilaterally over the ischia and
seating interface pressure (IP). TcPO2 data was binned into low (<10mmHg),
medium (10 - 30mmHg) and high (>30 mmHg) ranges and the percentage time
that TcPO2 was in each range calculated. Ischial and sacral regions of interest
(ROI) were defined and ROI maximum and mean IP determined, together with
Chapter 5-150 maximum IP gradient for the entire contact area. Initial seating postures varied; four individuals were initially sacral sitters. Tissue health responses to NMES were reviewed for sacral and non-sacral sitters.
Results: For sacral sitters, sacral region IP and maximum IP gradient tended to decrease during NMES, re-increasing post-intervention. Mean ischial TcPO2 increased during NMES and remained elevated post-intervention, increasing healthy TcPO2 percentage time for 50% of the sacral sitters both during and after intervention. Non-sacral sitters showed little tissue health changes due to NMES application.
Conclusion(s): Trunk and gluteal stimulation acutely corrects anterior/posterior postural misalignment improving regional tissue health for sacral sitters. This correction requires constant NMES application. The potential for positive changes in tissue health would be maximized by regular NMES use incorporating weight-shifting.
Chapter 5-151 Introduction
The ideal sitting posture is achieved when the trunk and upper body are in
equilibrium above a stable base with neutral pelvic rotation, moderate lumbar
flexion[185] and the upper body center of mass acting through the ischial region.
Following spinal cord injury (SCI), sitting biomechanics are altered causing loss
of trunk stability and muscle atrophy [186]. Motor and/or sensory deficits not
only remove the conscious ability to adjust posture but also prevent the
continuous subconscious adjustments needed to maintain postural stability. The
ideal seated posture is thus very difficult to maintain and often compromised
following SCI [187, 188, 189, 190].
The functional goal of wheelchair seating systems is to maintain a balance between stability, controlled sitting posture, and maximized independent function [191,192]. However, many wheelchair users adopt compensatory sitting strategies to increase stability and achieve functional goals. Trunk stability has been identified as one of the highest priorities for motor system recovery in individuals with SCI regardless of injury level [193,194]. Due to core muscle weakness and postural instability, the most common strategy to increase anterior/posterior stability is posterior pelvic rotation, resulting in ‘sacral sitting’
[195,119]. In this posture, the pelvic support base area is increased by posterior pelvic rotation allowing the upper body center of mass to act over a larger area.
Individuals with postural instability also frequently lean to one side. This may be
Chapter 5-152 a passive postural adjustment due to asymmetrical weakness or wheelchair users may actively lean or hook an arm over a wheelchair upright to maintain lateral stability. Indeed this strategy has been recommended as helping to keep the torso against the wheelchair back [196]. However, as the same authors noted, repeated hooking can lead to skeletal deformity, back pain and tissue breakdown. A ’hooked’ sitting posture also prevents the individual from performing any bi-manual tasks.
Poor sitting postures cause redistribution of loads acting through the pelvic region. In sacral sitting, the lumbosacral and pelvic regions experience higher loads, increasing regional interface pressures (IP). Normal sitting posture is generally assumed to be symmetrical with equal loads acting bilaterally through the ischia. However, we have recently shown that even in healthy able bodied individuals, postural symmetry cannot be assumed [133]. Compensatory leaning postures further increase asymmetrical loading.
Redistributed soft tissue loading compromises tissue health and can increase the risk of pelvic region tissue breakdown, leading to pressure ulcer (PU) development. Primary PU prevention is both challenging and important; these chronic wounds are detrimental to overall quality of life, lead to psychological distress and impose significant burdens on healthcare systems, with treatment costs estimated to be in excess of $1.3 billion annually over 10 years ago [197].
Chapter 5-153 Continued high PU incidence demonstrates that there remains a critical need to
investigate new approaches to prevention.
Neuromuscular electrical stimulation (NMES) produces a contractile response in
a paralyzed muscle which when applied to appropriate muscles of the trunk and
pelvis, has the potential to counteract poor sitting postures common after SCI.
Previous studies have shown that regular application of NMES to the gluteal
muscles using an implanted system can improve tissue health by producing
reliable contractions of the targeted muscles which redistribute applied loads
and improve measures of regional tissue health [71,198].
The goal of this pilot study was to investigate the hypothesis that combined
trunk and gluteal NMES alters seated posture and improves pelvic region tissue
health in individuals with SCI.
METHODS
Study Design: Intervention study; case series/convenience sample.
Study population:
Study participants were recruited from a population of individuals with SCI who
had received implanted lower extremity NMES systems for standing and
walking, which comprise fully implanted 8 or 16 channel stimulators providing
stimulation to the trunk, hip and lower extremity muscles [199,200]. A
convenience sample of seven individuals with SCI who had implanted NMES
Chapter 5-154 systems was evaluated. Subject demographics and initial sitting postures are
summarized in Table 5.4
Table 5.4: Population demographics and initial sitting posture.
Sub ID Age Gender Ht Wt Inj AIS Years Years Sacral 1 (cm) (kg) Level Clas Post Post sitting s Inj Implant posture TR-01 45 M 177.8 97.5 T5 B 26.5 9.6 Y TR-02 56 F 167.6 67.7 T5-6 B 6.6 2.3 Y TR-04 58 M 174 80.9 T6 A 11.8 10.6 N TR-06 40 F 167.6 57.3 C7 C 13.0 11.4 N TR-07 50 M 185.4 97.7 T6 B 7.8 6.4 Y TR-08 26 M 165.1 63.2 C6 A 6.3 4.7 Y TR-09 47 M 181.6 65.5 T10 A 5.8 0.9 N 1At time of initial enrollment and testing
Although individual muscle sets were customized for each individual, all study participants had active bilateral stimulation of the lumbar paraspinal and gluteus maximus muscles. Additional muscles included the quadratus lumborum for trunk stabilization with hip extension strengthened by the semimembranosus and posterior portion of the adductor magnus.
Intervention: Trunk and gluteal stimulation was applied concurrently at 20 Hz frequency, 20 mA pulse amplitude for 5 minutes. The system delivered charge- balanced biphasic constant-current stimulus pulses with the case of the implanted pulse generator serving as a common anode. Modulation by adjusting stimulus pulse duration (0 – 255 μsec) was based on muscle response. Pulse
Chapter 5-155 duration could be independently varied for each channel [201]. Stimulus frequency could also be adjusted independently for each channel and was nominally set at 20 Hz, which was found to minimize fatigue for the intervention period.
Sitting posture for all subjects with and without active trunk and gluteal stimulation was evaluated using a VICON 370 motion capture system with reflective markers at C7, T6, and bilateral acromion and ASIS locations. Initial pelvic tilt was assessed by computing the angle between the midpoint of the line connecting the left and right ASIS and PSIS markers with the horizontal without stimulation [201].
The Institutional Review Board of the Louis Stokes Cleveland Department of
Veterans Affairs Medical Center (LSCDVAMC) approved this study. Written informed consent was obtained from all study participants.
Materials:
Transcutaneous oxygen tension (TcPO2) was measured with a Radiometer
TCM400 monitor a. The oxygen electrode (Radiometer, model E5280-8) was calibrated using the surrounding atmospheric air. To produce maximal local vasodilation, system temperature was controlled at 43oC.
Chapter 5-156 Interface pressure distribution was recorded using the Tekscan CONFORMat®
Pressure Measurement Systemb which employs resistive sensors in a grid-based
array containing more than 1000 thin flexible sensors (sensels) arranged in a
32x32 array. The CONFORMat® sensor operates within the range 1-250mmHg
(accuracy +10%), scan rate 100Hz.
Assessment protocol:
The effects of combined trunk and gluteal stimulation on pelvic tissue health
were evaluated in sitting with and without NMES. Study participants sat quietly
in their standard wheelchair seating systems in their usual sitting postures,
followed by the new postures generated with active NMES. Tissue health was
assessed based on our standardized protocol using the Tissue Health Evaluation
Toolbox (THEToolbox). All assessments were carried out in the Skin Care
Research Laboratory at the LSCDVAMC. Room temperature over the course of
each assessment was maintained at 25+2oC.
Transcutaneous gas levels were monitored bilaterally over the ischial tuberosities.
Sensors were placed with subjects in a side-lying position on a bed or plinth,
with hips and knees flexed to 90o. In this position the soft tissue over the buttocks is in the same position relative to the bony anatomy as in sitting. This allows sensors to be placed over in side-lying for baseline unloaded measurements. The ischial tuberosities were palpated and fixation rings located over the bony
Chapter 5-157 landmarks. The central region of the ring was filled with contact fluid and each sensor securely attached. A 20 minute equilibration period with all sensors unloaded followed so that local vasodilation could stabilize before tissue health monitoring commenced. The CONFORMat® mat was placed over the subject’s support cushion in their usual wheelchair. The subject then carefully transferred to the seated posture and the sensors were palpated to ensure they remained over the ischial tuberosities before continuing with the assessment.
Table 5.5: Tissue health assessment timeline
Side Lying Q1: Intervention 1: Q2: (Unloaded) Pre-Intervention NMES activation Post-Intervention 20 min 5min 5 min 5 min
Quiet sitting Activation of trunk and gluteal stimulation
Tissue health measures of TcPO2 and IP were assessed concurrently while seated for a 15-20 minute period (Table 5.5). The CONFORMat® system was calibrated to 80% of each participant’s weight based on an estimate that approximately 20% was on their backrest and footrests [160]. TcPO2 levels were continuously monitored, with event markers activated in the TCM system to sync IP data collection with TcPO2 measurement
Chapter 5-158 Pre-intervention quiet sitting was maintained for 5 minutes (Q1). Trunk and gluteal stimulation was then applied concurrently at 20 Hz frequency, 20 mA pulse amplitude for 5 minutes (Int1). Stimulation pulse width varied between individuals based on specific muscle response. Post-intervention quiet sitting was then maintained for a further 5 minutes (Q2).
DATA ANALYSIS
The first and last minute of each assessment phase was discarded to minimize transition effects. Thus, data sets of three minutes duration were extracted for further analysis. Tissue health data were processed as described below;
Interface pressure data: CONFORMat® proprietary software created 2D/3D IP distribution maps which graphically display sensor mat data, measured at 2Hz producing a 360 frame data set for analysis. These data were exported as numerical arrays and recreated in Matlab for further analysis. Contact area was delineated by segmentation using morphological opening (erosion and dilation) to remove spurious data points outside the main contact area. Pressure data arrays were aligned and standard regions of interest (ROI) around each ischia and the sacral region identified. In the current analysis protocol, the ischial tuberosity analyses ROIs were bilateral 5x5 sensel regions (approximately
7.5x7.5cm2). The sacral analysis ROI was a 3x12 sensel region centered at the midline at the posterior margin of the overall pressure map (Figure 5.6B).
Chapter 5-159 Maximum and mean ROI interface pressures within each analysis ROI were
determined for each assessment phase. Maximum IP gradient was determined
for the entire contact area by calculating the highest difference between each
sensel and its 8 adjacent sensels, adjusted for real separation distance and edge
effects. By comparing all sensels with all adjacent neighbors, the location and
magnitude of the maximum IP gradient was determined for the total contact
area.
TCM Data: Overall mean TcPO2 for each assessment phase was determined.
Tissue oxygenation was further characterized to determine the proportion of
time that the tissue in the region under assessment was adequately oxygenated.
A threshold of 30mmHg has been suggested for adequate tissue oxygenation,
which represents a 60% decrease from the normal unloaded value [139]. This
threshold has also been supported by clinical consensus statements on the use of
transcutaneous oximetry [140]. Time-series data were analyzed and binned into
low (<10mmHg), medium (10 - 30mmHg) and high (>30 mmHg). Percentage
time that TcPO2 values were in the high and low ranges was calculated for each assessment phase.
Study data did not have normal distribution. The Wilcoxon matched pairs signed-rank test was therefore applied to compare pre-intervention, intervention and post-intervention tissue health outcomes measures.
Chapter 5-160 RESULTS
Initial seating postures were highly variable across subjects; one individual had a
‘normal upright sitting posture, one leant to the right and one exhibited marked anterior pelvic rotation. The other four individuals studied exhibited an initial sacral sitting posture. Each individual used a stimulation pattern which provided constant stimulation with a goal of keeping them seated upright, with trunk stability and postural symmetry determined using both a Biodex dynamometer and Vicon motion capture [201]. Changes in tissue health variables were reviewed for all subjects and for the sacral sitting sub-group to evaluate responses to NMES application.
Interface pressure data: All subjects exhibited a small but statistically significant increase of 5-11% (median 9%) in total IP between pre- and post-intervention
(p=0.01). This was due to total IP increasing during intervention (range 3-19%, median 11%) and remaining higher post-intervention relative to before the intervention.
Although sacral region IP also showed a statistically significant increase between pre- and post-intervention (p<0.05), this was mainly due to a post-intervention increase. For sacral sitters, sacral region IP tended to decrease during NMES application (median -6%) and to increase again post-intervention (median 13%).
Chapter 5-161 Non-sacral sitters showed little change in sacral region IP due to NMES
application.
Mean ischial region IP increased between pre- and post- intervention for all
subjects. Median increase was 12% for all subjects and slightly higher for sacral
sitters (17%). These changes were statistically significant bilaterally (p<0.01) and
were predominantly due to increased regional IP during NMES application
relative to pre-intervention which was maintained post-intervention.
Maximum IP gradient decreased slightly on NMES application for all sacral
sitters (range -2 to -12%, median -2%) and showed a variable response overall.
There was no change in magnitude between pre- and post-intervention
maximum IP gradient.
TCM Data: For all sacral sitters, mean ischial region TcPO2 increased during
stimulation for at least one ischial region and remained elevated post-
intervention. This change was sufficient to increase the percentage time TcPO2
was in the high range (<30mmHg) for two of the four individuals both during
and after intervention. Individuals who were not sacral sitters were more likely
to show decreased mean ischial region TcPO2 during stimulation. There was no
change in the percentage time TcPO2 was in the high range for any individual
who was not a sacral sitter.
Chapter 5-162 Postural groups/Case Studies:
To illustrate changes seen in tissue health variables due to NMES application
detailed results are presented for two case studies, one classified as a sacral sitter
and one with a ‘normal’ sitting posture:
Case Study #1:Tissue health outcomes measures for the sacral sitting case study
(Figure 5.6) showed high sacral region IP pre-intervention (mean 75mmHg),
which decreased by 6% on NMES application (mean 70mmHg). IP appeared to
decrease overall, however post-intervention mean sacral region IP was higher
(mean 80mmHg) (Figure 5.6A). NMES application produced some increase in
left ischial IP, which further increased post-intervention, increasing 24% relative
to pre-intervention. The right ischial region showed a similar response pattern,
increasing 37% relative to pre-intervention. Pre-intervention maximum IP gradient (147mmHg/cm) occurred in the posterior sacral region (Figure 5.6B).
On NMES application, this shifted anteriorly and decreased by 12% to
129mmHg/cm. Post-intervention, the maximum IP gradient shifted even further
anteriorly under the left ischial ROI and decreased further, decreasing 15%
relative to pre-intervention. Concurrent measurement of ischial region tissue
oxygenation showed medium TcPO2 bilaterally pre-intervention. NMES
application produced an increase in TcPO2 at the left ischial region only, to a
healthy level (>30mmHg) which was sustained post-intervention (Figure 5.6C).
Chapter 5-163 Q1: Pre-intervention Intervention 1: NMES activation Q2: Post-intervention Legend: Calibrated pressures 0 to <150mmHg A)
Q1: Pre-intervention Intervention 1: NMES Q2: Post- activation Legend Left ischial Right ischial ROI Sacral ROI Saturation pressure (>150mmHg)
Maximum IP gradient (lighter color is higher pressure)
B)
C) Figure 5.6: Tissue health evaluation results panel: The effects of trunk stimulation on sacral sitting posture. A) Interface pressure distribution. B) Maximum interface pressure gradient. C) Tissue oxgenation
Chapter 5-164 Case Study #2: Tissue health outcomes measures for the normal upright sitting
case study (Figure 5.7) showed low sacral region IP at pre-intervention (mean
22mHg). Mean sacral IP increased slightly during NMES application (mean
25mmHg) returning to pre-intervention levels post-intervention (Figure 5.7A).
NMES application produced a moderate increase in left ischial IP, which was not sustained post-intervention. Mean right ischial region IP was not affected by
NMES application but increased post-intervention. Pre-intervention maximum
IP gradient (Figure 5.7B) occurred in the left ischial ROI (mean 117mmHg). On
NMES application, maximum IP gradient did not move and increased slightly
(mean 124mmHg/cm). Post-intervention, maximum IP gradient shifted to the right ischial ROI and decreased 3% relative to pre-intervention. Regional TcPO2
was markedly asymmetric: The left ischial region had very low TcPO2 levels
(<10mmHg) while the right ischial region exhibited higher healthy TcPO2 levels
(>30mmHg) throughout the assessment (Figure 5.7C).
Chapter 5-165 Q1: Pre-intervention Intervention 1: NMES activation Q2: Post-intervention Legend: Calibrated pressures 0 to <150mmHg A)
Q1: Pre-intervention Intervention 1: NMES activation Q2: Post- Legend Left ischial ROI Right ischial ROI Sacral ROI Saturation pressure (>150mmHg) B) Maximum IP gradient (lighter color is higher pressure)
C) Figure 5.7: Tissue health evaluation Results panel: The effects of trunk stimulation on ‘normal’ sitting posture. A) Interface pressure distribution. B) Maximum interface pressure gradient. C) Tissue oxygenation
Chapter 5-166 DISCUSSION
Implanted neuroprostheses have been investigated for many functional applications from standing [119, 202] to hand function [203]. Implanted NMES systems for long-term therapeutic use have several advantages over surface stimulation. An implanted electrode can be located very close to the motor point of the nerve of interest. This not only reduces the charge required to elicit a contractile response but also ensures that the response is repeatable and predicable. Furthermore, the user does not have to replace the stimulating electrode every day so the system becomes both more reliable and simpler to use.
Recently a novel system has been developed specifically to provide trunk stability and seated postural control. A long-term usage case study has shown that regular application of gluteal NMES alone for over seven years improved tissue health and may decrease the risk of pressure ulcer development [71].
Preliminary studies showed that application of appropriate stimulation to stiffen the trunk of a paralyzed individual increased bimanual workspace [204]. Trunk stabilization may allow an individual with a high level SCI to sit safely without the need for a chest strap or similar restraint. Activation of trunk stimulation can also enable independent recovery from full forward lean or lateral bending positions [201].
Chapter 5-167 The effects of applying concurrent trunk and gluteal stimulation were evaluated in a study population of individuals with implanted NMES systems which were functionally equivalent to the trunk stability/postural control system. The standardized tissue health assessment protocol allowed the effects of applying the NMES intervention to be compared to quiet sitting in the subject’s normal wheelchair system. The objective was to determine whether activating the core trunk and hip muscles modified interface pressures and/or promoted blood flow. Study participants had a variety of initial sitting postures; several demonstrated the typical postural adjustments required to stabilize sitting posture due to trunk paralysis in SCI. For the convenience sample studied, only one sat in a ‘normal’ upright sitting posture and over 50% had an initial sacral sitting posture.
Concurrent application of trunk and gluteal stimulation appeared to impact sacral region IP for individuals who were initially sacral sitting. Specifically, sacral region IP tended to decrease on NMES application. However this change was not maintained once stimulation stopped. Both overall and ischial region IP increased during and following NMES application for all subjects. These changes imply that NMES application produced a more upright sitting posture with a greater proportion of trunk and upper body mass acting through the seating support region. Concurrent changes in maximum IP gradient indicate that
NMES application produced a more uniform IP distribution located in a more
Chapter 5-168 physiologically appropriate region of the seating contact area; for the sacral sitter
(Case Study #1), maximum IP gradient decreased and moved anteriorly to a
similar anterior/posterior location to that observed for the upright sitter.
The effect on tissue oxygenation appeared to be more sustained, although a
positive change was only seen for sacral sitters. Ischial region tissue oxygenation
for these individuals tended to increase during NMES application and to remain
higher. This was sufficient to change tissue health status to increased duration of
healthy oxygenation (above 30mmHg) for some individuals even after
stimulation stopped. For non-sacral sitters, NMES application tended to decrease ischial region oxygenation.
NMES had a positive effect for sacral sitters, most probably due to the reduction
or correction of posterior pelvic rotation during intervention. For individuals
with lateral postural instability, NMES had a small positive effect in reducing
maximum IP gradient. Concurrent application of trunk and gluteal stimulation
for a short period produces a postural correction but has less immediate impact
on pelvic region tissue health.
It has previously been shown that gluteal stimulation alone has a beneficial
impact on ischial region tissue health [71]. The current findings imply that the
Chapter 5-169 addition of concurrent trunk stimulation may not have a positive short-term
effect on the regional tissue health of non-sacral sitters.
Study Limitations
The current study was a single assessment of the short-term effects of the selected intervention on tissue health in a convenience sample of experienced
NMES users with implanted systems. This type of assessment is similar to one that would be done in a seating clinic but the effects of changes over time cannot be captured without repeated assessments. The implanted trunk and gluteal
NMES system is designed for long-term use. Regular repeated stimulation of paralyzed muscles will produce changes in muscle characteristics, such as muscle hypertrophy, that can improve local tissue health. As noted all subjects in the current study were recruited from a convenience sample of long-term NMES users. The impact of NMES on the tissue health characteristics of stimulated muscles might therefore be considered to have stabilized.
In the current study, stimulation variables were optimized for both a symmetrical contractile response and user comfort. The NMES intervention was targeted for postural correction without a lateral weight-shifting component.
Maintenance of tissue health in the individual with SCI requires both postural
correction and regular postural alteration [205]. Individuals with SCI are
recommended to perform pressure relief procedures every 15-20 minutes when
Chapter 5-170 seated [9]. Individuals with impaired sensation and mobility, at high risk for PU development, often find it very hard to adhere to such a rigorous regime, both because they do not feel pain or discomfort and also because they are unable to effectively weight-shift independently. Adjustable (tilt-in-space) wheelchairs are available to provide some postural variation. However, it has been shown that a posterior tilt to at greater 30 degrees is required to alter ischial region tissue health [149]. Moreover, no wheelchair or cushion can affect the intrinsic factors which compromise tissue health. Alternating NMES induced gluteal contractions produce weight-shifts that dynamically alter loading conditions at the seating support interface. Long-term daily use of alternating gluteal NMES positively impacts multiple indirect indicators of tissue health [50, 71,206,207,208]. To optimize for sustained improvement in tissue health in addition to postural correction, stimulation patterns need to include a regular weight-shifting component.
CONCLUSIONS
Concurrent application of trunk and gluteal stimulation has a greater acute effect on anterior/posterior postural misalignment than on lateral instability. The resultant postural correction indicated improved regional tissue health for individuals who were sacral sitters.
Chapter 5-171 NMES was applied bilaterally to the trunk and gluteal musculature, however the
resultant regional tissue health response were generally asymmetric. This confirms previous findings and illustrates the need for bilateral assessment of tissue health in study populations with restricted mobility.
5d. Chapter conclusion
Application of trunk and gluteal stimulation can counteract unhealthy
anterior/posterior adaptive sitting postures common after SCI. This correction
cannot be maintained without constant NMES application. The concurrent
application of trunk and gluteal NMES appears to have a positive short-term
impact on the tissue health of sacral sitters, but not for non-sacral sitters. The
long-term effects of regular use of NMEs were not assessed in the current study
and may impact outcomes. Regular use of NMES can minimize the atrophy seen
in persons with spinal cord injury. NMES could be a possible mechanism to
improve muscle physiology and tissue health. The trunk study paper shows the
effects of NMES and postural shifts on TcPO2 is dependent on initial posture.
NMES trunk stimulation improves interface pressure and tissue oxygenation
with initial sacral sitting. The improvements are less significant when the
participant was leaning to one side before the assessment.
Chapter 5-172 Chapter 6) Imaging the gluteal neurovascular anatomy
6a. Preface
In this chapter we explore the possibility of using current CT methods to locate
the inferior gluteal nerve and possibly aid in improving placement of an NMES
electrode to stimulate similar deep nerves.
NMES impacts tissue health by increasing muscle mass and in some cases
positively affects measures of tissue health. We have shown that stimulating
muscle may have short and long term impacts on tissue health characteristics
that can also be observed with CT after placement of an NMES device.
6b. CT to Visualize Neurovascular anatomy
Paper for submission
TITLE: CT TO VISUALIZE NEUROVASCULAR ANATOMY
Motivation:
• Tissue health & changes following SCI
• The challenge of PU prevention & the role of NMES
• Why use a fully implanted system –challenge of minimally invasive surgery
Chapter 6-173 BACKGROUND/INTRODUCTION
Neuromuscular changes after spinal cord injury
Following spinal cord injury (SCI), the loss of voluntary control and nervous input leads to drastic changes in the muscles below the level of injury.
Physiological changes include muscle disuse atrophy [80], increased adiposity [1] and altered vascular circulation [81], increasing the risk of developing pressure ulcers (PU). Deep tissue injury (DTI), a classification of PU, wherein tissue breakdown initiate in the deep layers of tissue, typically originate near the bony prominences where internal strains and stresses are exacerbated by the physiological changes after SCI.
Tissue regions over the bony prominences of the pelvic region, i.e. the ischial tuberosities, sacrum and, to a lesser extent, the greater trochanters are at particular risk for PU development in wheelchair users. Positive improvements towards PU prevention can be made if the health of soft tissue under applied load could be improved. Change in soft tissue composition and function following SCI may provide a personalized indication of risk status.
NMES for pressure ulcer prevention
Delivery of an electrical stimulus to the nerve supplying a paralyzed muscle can elicit a contractile response which over time will alter the functional capabilities of the muscle. Neuromuscular electrical stimulation (NMES) has been used to
Chapter 6-174 provide functional restoration for many aspects of SCI [209,210]. Stimulation of
the gluteal muscles has also been shown to improve tissue health by improving
circulation and muscle thickness [198]. However it also been found that regular daily use of NMES is necessary in order to maintain these changes [71]. A fully
implanted system would eliminate the need for daily maintenance associated
with surface or percutaneous stimulation systems. Some drawbacks with surface
electrode placement include the difficulty in preferentially recruiting the inferior gluteal nerve. Likewise, repeatable electrode placement in the upper buttock region is hard to achieve for independent users or their caregivers.
An implanted system has the capacity to provide a more effective, reliable
contraction of the target muscle. The stimulating tip of an implanted electrode
can be placed directly adjacent to the associated target nerve. In the specific case
of an implanted gluteal stimulation system for PU prevention, the target nerve
for the gluteus maximus is the inferior gluteal nerve (IGN). The IGN originates
from the posterior portions of fifth lumbar and first sacral nerves and the ventral
primary rami of S2 nerve roots. It branches from the sacral plexus and then
further divides into several branches before innervating the gluteus maximus
muscles. In order to maximize muscle recruitment by a stimulating electrode, it is
desirable to optimize location of the stimulating tip. In this case, the gluteus
maximus is optimally recruited by NMES, if the stimulation is applied to the IGN
proximal where it branches just prior to entering the muscle.
Chapter 6-175 Currently, the stimulating tip for a gluteal electrode is placed using bony
landmark triangulation to determine the expected location of the IGN. However
extensive probing is often required in order to elicit a sufficient contraction. This
indicates that the regional anatomy can be variable. As noted, individuals with
SCI at risk for PU development often have significant muscle atrophy. Those
with a priori history of tissue breakdown will generally have markedly altered
gluteal muscle anatomy. Furthermore, the anatomy of the IGN has been found to
show variable morphology [211]. Thus the location of the desired stimulation point can vary greatly.
Imaging to improve electrode placement
Reliable identification of the target nerve location would decrease extensive
probing of delicate gluteal tissues to locate the motor point of the target muscle.
Nerve visualization using medical imaging would thus be useful in determining
a plan for implanting stimulation electrodes and to facilitate minimally invasive
implantation procedures. Magnetic Resonance Imaging (MRI) is the highest
quality technique for visualizing nerves. Indeed, MRI neurography can be used
to visualize nerves in the whole body with high resolution [212]. However, MRI
is contraindicated for individuals who have stents, wire sutures, artificial joint
replacements and electrical stimulator implants [213,214]. Many individuals with
SCI have implants that have potential for dislodgement and arcing of electrical
fields and thus cannot have MRI.
Chapter 6-176
Computer Tomography (CT) is a non-invasive imaging technique that allows the entire pelvic anatomy to be visualized in a relatively short amount of time; less than 30 minutes from prep to post-processing for a high-resolution spiral CT.
This imaging technique can be used for individuals who have a metallic implant; although these implants produce streaks and star-shaped artifacts there are several rendering techniques that can reduce these phenomena [215, 216]. CT imaging employs planar X-rays to construct a tomographic map of the anatomy.
Several scans can be ‘stacked’ to create 3D maps to allow visualization in of several image planes. CT is very effective for visualizing bony anatomy however it has limited capability for differentiating soft tissues.
A retrospective pelvic CT scans of 50 SCI patients who had routine pelvic or colon examinations with contrast was carried out. It was found that the sciatic nerve and the neurovascular bundles could be located in some individuals, although it was not possible to differentiate the inferior gluteal nerve [9]. The pelvic CT with contrast acquisition protocol was then applied to a small group of able-bodied patients. It was found that the course of the regional vasculature and the sciatic nerve could be followed. However the locations of the inferior gluteal nerve and its insertion into the muscle bed could not be reliably determined.
These findings indicate that the altered soft tissue composition in SCI, i.e.
Chapter 6-177 decreased muscle mass and increased adipose tissue, improve the viability of
locating the neurovascular bundle.
The current study employed pelvic CT with contrast to investigate the use of
contrast to improve differentiation of filamentous structures in the pelvic region.
The hypothesis is that pelvic CT contrast with modified acquisition protocol can
be applied to visualize the regional neurovascular anatomy in individuals with
SCI and AB.
METHODOLOGY
Recruitment and CT acquisition methodology for this study is described in
Chapter 2.
Data Analysis
In addition to the data analysis described in Chapter 2, additional ROI were
identified such as bones, visceral fat, contrast enhanced vasculature, sciatic nerve
throughout the scans. In some cases, portions of the inferior gluteal nerve that branch from the sciatic nerve were also noted.
Chapter 6-178 A B
Figure 6.1: A) CT Scout image and B) Surface reconstruction of CT image, regions of interest include bone, muscle and vasculature. Lines show the location of axial slices where images were assessed for CT image quality.
Neurovascular anatomy assessment
Expert radiologists rated the CT image quality for each scan using a scale from 1 to 5 (1 = unacceptable, 3 = acceptable, 5 = superior). This was a subjective scale based on contrast and clarity of visualizing elements in the scan, signal to noise ratio. The same experts then attempted to determine the location and course of the sciatic nerve, inferior gluteal artery and inferior gluteal nerve. Accuracy of identification of each relevant structure was rated from 1 to 5 (1= cannot be located, 3 = can be approximated within a 5 mm radius, 5 = can pinpoint within
1mm)
RESULTS:
The convenience sample was taken from Chapter 2. Participant demographics are found in Table 2.2.
Chapter 6-179 Neurovascular anatomy assessment
Image quality was acceptable or better (Grade 3-5) for 9/10 AB scans and 10/10
SCI scans.
The inferior gluteal artery location could be pinpointed (score=5) for 9/10 AB scans, and 8/10 SCI scans. The sciatic nerve location could be pinpointed
(score=5) for 8/10 AB scans, and 7/10 SCI scan. The inferior gluteal nerve (IGN)
location could not be pinpointed for any scan. The IGN could be located with a 5
mm radius (grade 3) for 5/10 AB scans but could be located at all for any SCI
scan.
Discussion
Comparison of image quality of CT scans of participants with and without
spinal cord injury: For both groups, although CT images were taken at a voxel
resolution of 0.8x0.8x0.4mm, radiologists preferred the CT image reconstruction
with voxel size with 1x1x0.5mm in order to achieve adequate contrast while
minimizing image noise.
In our initial study we found that the sciatic nerve and the neurovascular
bundles could be located using CT without contrast, although it was not possible
to differentiate the inferior gluteal nerve reliably [72].
Chapter 6-180 IV contrast allowed for easy identification of vasculature in the gluteus area,
even so, some persons had very extensive delivery of contrast agent while for
some persons their main blood vessels had contrast but there was minimal
delivery of contrast to smaller vessels. This indicated that i there might be
individualized changes and responses in circulation and perfusion that might
account for the differences in oxygenation and blood flow in persons with SCI.
CT with a specialized contrast protocol to visualize the vasculature and attempt
to differentiate the nerves from vasculature. The IGN was not reliably
recognized. The IGN has a diameter of less than 1.5mm [217].The resolution of
the CT system used in the study is 0.8mm The IGN is a maximum of two voxels wide in images obtained and thus hard to separate from noise. Further development of CT technology may improve nerve visualizations..
There was physiological variability between AB and SCI individuals; the reduced muscle mass and increased adiposity observed in the SCI group could also cause decreased accuracy in locating the IGN with probing. Obtaining the optimal target for stimulation can streamline implantation procedures for transcutaneous and percutaneous systems. Reliable pre-implantation planning to locate the relevant nervous anatomy may even allow more procedures to be carried out in the community physician's office.
Chapter 6-181 CONCLUSION
An effective gluteal stimulating system also has the potential to decrease the risk of developing pressure ulcers by improving tissue health. Pre-surgical methods for locating the inferior gluteal nerve would translate to savings through reduction of operating costs and possibly transfer the implantation to the outpatient setting. A non-MRI based imaging technique for locating and differentiating nerves and blood vessels in deeper tissue has the potential be highly generalizable to clinical applications where nerves and blood vessels need to be located and/or avoided. In the current study, pelvic CT with contrast was found to be a suitable imaging modality for locating the sciatic nerve accurately but not for the smaller IGN. Ongoing development of imaging modalities may provide reliable visualization of smaller nerves in deep muscle beds.
Typically for CT and MRI, imaging is performed with the patient in supine position, but would be prone or on their side with knees bent during surgery.
The altered body position and soft tissue compliance to instrument pressure could cause displacement of nerve from its calculated position.
The technique for locating and differentiating nerves and blood vessels in deeper tissue can be highly generalizable. The proposed technique could be applicable to fields of anesthesiology, rehabilitation, surgery and fields where nerves and blood vessels need to be located and/or avoided. Though we were not able to
Chapter 6-182 locate the IGN. Ongoing development of other imaging modalities may prove that visualizing nerves in deep muscle beds may not be far in the future.
Alternatively, high-performance ultrasound [218] may be applied to image peripheral nerves found in the limbs, which are generally closer to the surface of the skin [219,220] and has been used to locate the more lateral aspects of sciatic nerve. Though this technique is currently limited by penetration depth further development in the technology may allow for deeper nerves such as the IGN to be visualized
Future studies should consider whether the expected location determined using imaging translates into the actual position of the inferior gluteal nerve.
Positioning of the body should also be taken into consideration as lying supine
(conventional CT position) compared to being prone or side lying with knees and hips bent at 90 degrees (implantation position) might be enough to alter the position of the nerve due to displacement of soft tissue.
Chapter 6-183 Chapter 7) Thesis Conclusions
7a. Assessment of gluteal muscle geometry and composition using
computed tomography
SCI muscle CSA has altered composition compared to AB individuals. There is a
substantial increase in adipose tissue infiltration and atrophy of lean muscle
tissue. Furthermore, there is an increased ratio of low-density muscle in the characterized muscle tissue. The change in muscle characteristics of persons with
SCI has been well documented in literature involving increased adiposity and with biopsies, physiological changes from predominantly type-I muscles pre- injury to predominantly type-II fast twitch muscles a few months after spinal cord injury. With the use of CT and other imaging modalities it would be possible to characterize muscle composition of persons with SCI as a baseline to understand changes post-injury and possible benefits to tissue health with use of interventions such as FES or NMES.
Our preliminary study shows that persons with SCI who have low weight (less than 180lbs) and also those who have a history of pressure ulcers have increased
% intramuscular adipose infiltration and decreased % of lean muscle in the gluteus maximus CSA. To our knowledge this is the first time that the composition of gluteus maximus muscles was assessed in relation to spinal cord
injury and in prediction of tissue health.
Chapter 7-184 7b. Multi-factorial tissue health assessment of weight shifting maneuvers
THEToolbox was used to measure interface pressure maximum gradients by calculating the difference in interface pressures between adjacent sensor cells.
This measurement approximates the definition of shear forces in the seating interface. Weight shifting with standard cushion is more effective than dynamic cushion in decreasing interface pressure maximum gradients.
Although the effects of weight shifting are clearly observed with decrease in IP
Max Gradients, this is not necessarily reflected in TcPO2 and LDF flow measurements. TcPO2 has a negative correlation with IP, and generally weight shifting produces increased mean TcPO2 levels regardless of which side has redistributed pressures. Likewise, measurements also show the ROI to have equal or increased percentage of time in high TcPO2 levels when weight shifting compared to baseline.
Furthermore LDF flow measurements seemed to produce differing results for independent weight shifting and use of the dynamic cushion. This is probably due to the different nature of weight shifting, where PR-C would more dramatically shift posture and center of gravity while PR-D is a passive redistribution of ischial area IPs. Metabolic, neurogenic and myogenic blood flow contributions generally increased during pressure relief which occurred during between Q1 and I1 for independent weight shifting and between the two
Chapter 7-185 inflation phases for use of the dynamic cushion. When comparing pre-
intervention and post-intervention all three blood flow components generally
decreased following weight shifting except for the myogenic component which
increased during use of the dynamic cushion. The myogenic component of blood
flow is typically a homeostatic response of the smooth muscle surrounding
capillaries to sudden increases in pressure and shear. The increase in myogenic
component during use of the dynamic cushion might be due to the gradual
change in interface pressures as the cushion inflates and deflates in comparison
to the more immediate change in IP with an independent weight shift. This
further shows that there might be different mechanisms at play between active
independent pressure relief maneuvers and weight shifts due to use of a
dynamic cushion.
7c. The impact of trunk NMES on tissue health (Trunk study)
The concurrent application of trunk and gluteal stimulation has greater acute
effect on anterior/posterior postural misalignment than on lateral instability.
The resultant postural changes improved regional tissue health for individuals
who were sacrally sitting prior to stimulation.
NMES was applied bilaterally to trunk and gluteal musculature, however
resulting measurements of regional TcPO2 were asymmetric. This indicates
Chapter 7-186 asymmetric muscle atrophy and neurovascular integrity but also differences in placement or proximity of the stimulating electrode to the nerve of interest.
7d. Imaging the gluteal neurovascular anatomy
The methodology we employed using CT imaging with contrast to localize deep nerves, was unable to help us determine the branching of the inferior gluteal nerve. Instead, we were able to effectively locate the inferior gluteal vasculature and trace the sacral nerve. There were some structures that could possibly be the inferior gluteal nerve but we were not able to ascertain the location of the inferior gluteal nerve. These structures can be verified by placing an electrode probe near the location to stimulate the nerve. Cadaveric studies have been performed to characterize the anatomy of the inferior gluteal nerve and how it innervates the gluteus maximus muscle. The inferior gluteal nerve originates from L5 to S2 sacral nerves, it runs together with and medial to the sciatic nerve and leaving the sacral plexus inferior to the piriformis muscle [221]. The distance between the
IGN origin and the posterior inferior iliac spine, IT and GT was 3.2, 4.8 and 5.4 cm respectively [222]. The anatomy indicates that branching of the inferior gluteal nerve occurs at the infrapiriformal recess and inserts into the gluteal musculature with superior and inferior branches [223].
Improvements in CT or other imaging modalities would have to be employed to localize the course of the inferior gluteal nerve. The CT study helped the authors
Chapter 7-187 to develop a means to measure gluteus maximus muscle cross-sectional area and
its composition such as % adipose infiltration, and ratio of low-density muscle
(high adiposity) to lean muscle. % adipose infiltration and ratio of low-density to lean muscle is a lot higher in the participants with SCI compared to AB.
Chapter 7-188 Chapter 8) Future Work
8a. Assessment of gluteal muscle geometry and composition using
computed tomography
The muscle cross-sectional analysis we used for CT required analysis of the
pixels in the region of interest. A simple threshold technique was employed to bin the pixels of varying attenuation to certain categories. This technique is prone to partial pixel errors and influence from random noise. Partial pixels error occurs when a pixel contains more than 1 or more cell types i.e fat and muscle
cell might be in the same pixel, this would result in pixel with attenuation
between fat and muscle range. More advanced algorithms used in CT tissue
determination can be employed to improve the accuracy of characterizing the
pixels and decreasing error. These image classification algorithms include fuzzy
c means methods to better classify tissue according to Hounsfield units.
8b. Multi-factorial tissue health assessment for personalized pressure relief
regimes
THEToolbox protocol could provide the basis for determining a tissue health
rating scale. Clustering of the multiple outcomes measures according to
characteristics of interest could help determine classification or even lessen the
measurements that are needed.
Chapter 8-189 We could implement the multifactorial THEToolBox assessment together with
CT study for the population at risk. Studies can be determined to create an
outcome measure or score to give the overall risk of person to pressure ulcers
and be able to give recommendations as to personalized interventions that can
decrease the risk of pressure ulcers. Currently THEToolbox has three main
noninvasive measurements, interface pressures, TcPO2 and blood perfusion
measurements. We have developed different quantitative measurements such as
IP max gradient, oxygenation threshold durations and blood flow characteristic
contributions. In the previous chapters we have suggested that individual
muscle composition might be a major component of varying tissue health
measurements across participants. If so, then it might be possible to use one
measure over another and can help us better understand the tissue health of
persons with spinal cord injury.
Subject Demographics and Groupings
There have been several demographic studies that show relevant risk factors for
PU such as increased intramuscular fat infiltration, scarring from previous PUs, spasticity. For instance spasticity was modeled and shown to have detrimental effects by Sopher et.al. While another study of 13 incomplete SCI supposes that the spasticity evident in high level of injury (C5-C7) compared to those with low level injury (T12-L2) results in lower relative intramuscular fat and increased muscle CSA.
Chapter 8-190 Thus it would be worthwhile to see if level of injury, American Spinal Injury
Assocation Impairment Scale (AIS) [224 ] or muscle composition affects the tissue health measurements in THEToolbox. If participants can be grouped by such it would help us determine approaches to each group according to clinical need and not have to individualize prevention recommendations.
Economic impact
Future studies might incorporate consideration or QALYs to provide healthcare
and economic considerations as to which interventions would provide most
benefit and would likewise be cost-efficient.
Assessment Methodology
Several suggestions can be made to the current collection of data:
CONFORMat measurements for PR-C can be taken with the same cushion as will be used for the PR-D assessment. Verify that the pre-intervention condition of
the cushion has even distribution of air pressure in the cushion for both left and
right side.
The intervention period can be uniform by either choosing to tilt chair back for a
specified amount of degrees or by leaning forward. Participant can also provide
weight redistribution similar to PR-D by leaning left and then leaning right for
the same amount of time as PR-D. We recommend a starting point of maintaining the weight redistribution for 3 to 5 minutes for each intervention.
Chapter 8-191 When leaning to one side it would also be important to minimize placing the
weight of the body on chair handle or by techniques such as hooking the arm
over the chair handles.
Specifically for the Aquila cushion, it might be of interest to time the intervention
so that the cushion will be in pattern A for the 1st intervention period and will be in pattern B for the whole of the 2nd intervention period. Doing so would help
make the measurements of loading on side and unloading the other, and allow as
proper comparison for weight shifting by leaning side to side.
We would then expect a difference in Q1, I1 and I2 to be one where Q1 has even
pressures on both sides. I1 has the right side with higher interface pressures and
I2 has the right side with lower interface pressures.
The TcPO2 and LDF are also assumed to be constant during the different seating
conditions. One (1) minute was allowed for the tissue to accommodate the change in pressures by measuring TcPO2 and LDF after weight shifting. It was not tested whether the measured values are constant; we can do validation by checking that the values are within a certain percentage of error or automated recording of TcPO2 once a certain threshold of stability has been reached.
Chapter 8-192 Because the measurements are taken over a period of time it would also be
possible to determine the time of arrival after simulated ischemic condition. Also
we can study the time it takes for TcPO2 measurements to stabilize, if at all after
start of intervention. Since TcPO2 can also be measured at 0.5 Hz we can also
sync this to the 2Hz measurements of CONFORMat, possibly even measuring at
0.5 Hz as well to do a side by comparison of IP and TcPO2 and study the delay of
response.
For cushion recommendations, a quick assessment may not be enough to choose
the right cushion, it typically takes some time for the seating interface to
acclimatize to each other and “sink in”, it might be necessary for a person to use
the cushion for an extended period of time before applying THEToolbox
methods to assess the appropriate cushion to be used [225].
8c. Determine changes in blood perfusion for person with PU occurrence
LDF measurements include several frequency oscillations in distinct frequency
bands similar to a constructed sine function. Taking the mean of the flow, red
blood cell in blood volume and velocity parameters would be a very rudimentary way of assessing the influence of interventions to blood perfusion parameters. We focused on the flow measurements and used STFT to determine the contributions of each frequency band during each seating condition.
Chapter 8-193 The data was analyzed using STFT to see the changes in frequency over time.
This is due to two assumptions: 1) frequency changes over time and 2) that duration of recording (T) is long enough to be able measure changes in frequency with a resolution of 1/T. If we assume that frequency contributions should be stable over the period of time we are recording, we could essentially do a simple
Fast-Fourier Transform but if we want to measure dynamic changes, STFT would be necessary. Furthermore, with the nature of the signal where we want fine frequency resolution and fine time resolution, further studies would have to consider other transforms that might be more suited to this type of analysis. Jan et. al. have explored other analyses such as wavelet transforms and multifractal analysis for blood flow oscillations.
Furthermore, the STFT-based spectral analysis of the blood flow is sensitive to the movements or spasms which would cause a peak in the flow measurements and would add to the energy of high frequency and low frequency signals.
Instead of low-pass filtering these peaks, it might be more effective to measure delete the short period of time with the spikes and interpolate the deleted region.
Interpolations would preserve the time signal and thus low-frequency signals of interest. Deletion of peaks would also make the spectrogram more sensitive to the more subtle changes in low frequency signals.
Chapter 8-194 In this study we determined the relative contributions of metabolic, neurogenic, myogenic, respiratory and cardiac components to the overall blood flow. Tzen characterized these components with a linear scale and thus metabolic and neurogenic components have less data points in the frequency scale.[227] Since we were more interested in the metabolic, neurogenic and myogenic frequencies we used a logarithmic scale instead placing the emphasis in taking more metabolic and neurogenic data points in the frequency scale. The energy of the frequency signal is thus composed of the energy contributions from each blood flow component per assessment. One can see how noise in the signal can greatly affect the energy of the signal per assessment. Spikes in the blood flow signal would greatly increase the energy of the signal. Filtering sudden increases in blood flow due to noise would help us be better able to characterize relative changes in metabolic, neurogenic and myogenic components for each assessment.
8d. Adaptive tissue loading and unloading responses. (ischemic and reactive hyperemia)
Static cushions and dynamic alternating pressure cushions work on very different principles. Static cushions reduce interface pressures in the seating interface with the premise that lower overall interface pressures would result in better circulation and improved tissue health. It is advised that persons with SCI who are in wheelchairs should regularly redistribute their interface pressures
Chapter 8-195 with pressure relieving techniques. Dynamic alternating pressure cushions on the other hand may not necessarily lower the overall interface pressures. The primary purpose is to prevent prolonged periods of pressure in the seating interface. There will be regions of higher interface pressures and regions of lower interface pressures. The high pressure areas are necessary to simulate off-loading or partial unloading in lower interface pressure areas.
Relieving pressures in the tissue area would allow local vasodilation resulting in an increased blood flow delivering oxygenation and flushing away toxic metabolites. Note that the hyperemia is supposed to be a normal phenomenon as opposed to the hyperemia after a period of ischemia which is very damaging to delicate oxygen-sensitive cells such as brain and cardiac muscles.[226] Muscle tissue should be less sensitive to oxygen deprivation to a certain extent as it has to deal with anaerobic processes during exercises. It is well established that shear and pressure are primary contributors to pressure ulcer formation. But it is possible that changes in muscle composition in persons with SCI make the soft tissues more susceptible to damage and cell death if tissues when deprived of oxygen for a certain period of time or possible deleterious effects of hyperemia.
TcPO2 can be used to study the hyperemic effect and the delay after pressure relief. Furthermore, LDF blood flow spectrograms can be used to measure what
Chapter 8-196 frequency bands contribute to the change in blood flow. This has been extensively studied by Brienza and Jan et al. [65,227]
8e. Improved imaging of the gluteal neurovascular anatomy
We have carried out a preliminary study of ultrasound Doppler imaging and were able to visualize arterial blood flow. The imaging technique has been shown to be able to locate sciatic nerve in more distal regions of femur where the nerve surfaces closer to proximity to the skin. At the level where the sciatic nerve exits the piriformis, we were unable to locate the sciatic nerve in the volunteer.
The level where the sciatic nerve exits the piriformis would be a location of great interest because that should be the region where the inferior gluteal nerve branches to innervate the gluteus maximus muscles. The exploratory assessment was performed on a person with substantial amounts of visceral adipose tissue and high levels of intramuscular fat and low density muscle in the gluteus maximus. The visceral adipose tissue likely impaired ultrasound imaging at the depth of interest as the adipose tissue would make the location of the nerve further from the transducer head.
A hybrid ultrasound paired with CT was also recommended as a possible imaging device. Currently a few medical imaging device companies have this available where the location of the vessels seen in US is calculated and correlated to its corresponding location and structure in the CT. The final results would be a
Chapter 8-197 real-time translation from CT to US and vice versa allowing for improved
anatomical understanding and probable validation of structures. Likewise,
during surgery, CT guided surgery could be used for placement of electrode
probe and the location of the electrode stimulator to provide an optimal
contraction. Other alternative surgical procedures might be the use of
laparoscopic techniques where the end of the scope is fitted with an electrode
probe, us probe or OCT probe to determine proximity to the peripheral nerve.
It is possible that more advanced imaging techniques might also be performed to
follow the peripheral nerve starting from its origin to its insertion into the muscle
bed. Snake algorithms and tree-root analysis over the reconstructed data might be possible ways to improve determination neurovascular anatomy.
8f. Tissue health in chronic SCI and other degenerative neurological diseases
Pressure ulcers are not only common in persons with chronic SCI but also in those with diseases such as diabetes, amyotrophic lateral sclerosis (ALS) and multiple sclerosis.
A comparison study can be made to better understand the risk of pressure ulcers as SCI and these diseases have different etiology. ALS is a degenerative disorder of the motor neurons in the central nervous system which leads to paralysis of
Chapter 8-198 voluntary muscles. Degeneration of muscle in ALS is preferential to larger motor
units [228,229]. Loss of motor control is present in both SCI and ALS, but some papers report that pressure ulcers are not as prevalent in persons with ALS
[230,231]. ALS presents with dysfunctions of cortical motor neurons and lower
motor neurons but without affecting sensory systems [232]. It is possible that the presence of sensory function allows the person to address discomfort before tissue is damaged enough to lead to pressure ulcer development. The later stages of ALS where immobility and inability to communicate the need for repositioning would increase the risk for developing pressure ulcers. Using CT to study the muscle composition, and THEToolbox for surface level vascularization can both applied to better understand the physiology of different diseases and to better understand how risk factors collectively increase the risk of PU development. Population studies can be valuable to test the incidence rates of PU for different neuromuscular diseases and risk factors they currently have and take into account different types of muscle atrophy or dystrophy.
Chapter 8-199 Bibliography
1 Gorgey, A. S., and Dudley, G. A.,Skeletal Muscle Atrophy and Increased Intramuscular Fat After Incomplete Spinal Cord Injury, Spinal Cord, 2007, 45(4), pp. 304–309.
2 Sopher R, Nixon J, Gorecki C, Gefen A. Effects of intramuscular fat infiltration, scarring, and spasticity on the risk for sitting-acquired deep tissue injury in spinal cord injury patients. J Biomech Eng. 2011 Feb; 133(2):021011. doi: 10.1115/1.4003325
3 Jan YK, Brienza DM, Boninger ML, Brenes G. Comparison of skin perfusion response with alternating and constant pressures in people with spinal cord injury. Spinal Cord. 2011 Jan;49(1):136-41
4 Burns SP, Betz KL. Seating Pressures with Conventional and Dynamic Wheelchair cushions in tetraplegia. Arch Phys Med Rehabil. 1999 May; 80(5):566- 71
5 Reenalda J, van Geffen P, Snoek G, Jannink M, Ijzerman M, Rietman H. Effects of dynamic sitting interventions on tissue oxygenation in individuals with spinal cord disorders. Spinal Cord, 2010, 48, 336-41.
6 Taylor PN, Ewins DJ, Fox B, Grundy D, Swain ID. Limb blood flow, cardiac output and quadriceps muscle bulk following spinal cord injury and the effect of training for the Odstock functional electrical stimulation standing system. Paraplegia 1993; 31: 303-310.
7 Bogie, KM Triolo RJ. The effects of regular use of neuromuscular electrical stimulation on tissue health. Journal of Rehabilitation Research and Development, 2003 40(6):469-475
8 NPUAP Updated staging system. Feb 2007. http://www.npuap.org/pr2.htm
9 Lindsey L, Klebine P, Oberheu AM. Prevention of pressure sores through skin care. In: Jackson AB, Mott P, eds. Spinal Cord Injury InfoSheets. Birmingham, AL: Spinal Cord Injury Information Network; December 2000. InfoSheet #13. Rehabilitation Research and Training Center on Secondary Conditions of SCI and Model SCI Care Center. Birmingham, AL Office of Research Service. Available at: www.spinalcord.uab.edu/show.asp?durki=21486, (cited 6/03)
10 Clark M. Skin assessment in dark pigmented skin: a challenge in pressure ulcer prevention. Nurs Times. 2010 Aug 3-9; 106(30):16-7
Chapter 8-200
11 Pressure ulcer prevention and treatment following spinal cord injury: Clinical practice guidelines for health-care professionals. August 2000. www.pva.org/pubsandproducts/pvapubs/PressUlcer.htm
12 Henzel MK, Bogie KM, Guihan M, Ho CH. Pressure ulcer management and research priorities for patients with spinal cord injury: consensus opinion from SCI QUERI expert panel on pressure ulcer research implementation. J Rehabil Res Dev. 2011; 48(3):xi-xxxii
13 Fuhrer MJ, Garber SL, Rintala DH, Clearman R, Hart KA. Pressure ulcers in community-resident persons with spinal cord injury: prevalence and risk factors. Arch Phys Med Rehabil. 1993, 74(11):1172-7
14 Reswick, J B & Rogers, J E. Experience at Rancho Los Amigos Hospital with devices and techniques to prevent pressure sores. In Bed Sore Biomechanics. Ed. R. M. Kenedi, J. M. Cowden and J. T. Scales, pp. 301–310. Macmillan, London 1996.
15 Kosiak, M. Etiology and Pathology of Ischaemic ulcers. Arch. Phys. Med. Rehab. 1959, (40), 62–69.
16 Baptiste A, Boda SV, Nelson AL, Lloyd JD, Lee WE 3rd. Friction reducing devices for lateral patient transfers: a clinical evaluation. American Assoc Occup Health Nurses J, 2006 Apr;54(4):173-180
17 Defloor T and Grypdonck MHF Sitting posture and prevention of pressure ulcers. Applied Nursing research, 1999, 12(3):136-142.
18 Lahmann NA, Kottner J. Relation between pressure, friction and pressure ulcer categories: A secondary data analysis of hospital patients using CHAID methods. Intl Journ of Nurs Studies. 2011 epub ahead of print. Doi:10.1016/j.ijnurstu.2011.07.004
19 Gray M, Black JM, Baharestani MM, Bliss DZ, Colwell JC, Goldberg M, Kennedy-Evans KL, Logan S, Ratliff CR. Moisture-associated skin damage: overview and pathophysiology. J Wound Ostomy Continence Nurs 2011 May- Jun; 38(3):233-41
20 Kokate JY, Leland KJ, Held AM, et al. Temperature-modulated pressure ulcers: a porcine model. Arch Phys Med Rehabil. 1995;76:666–673.
21 National Institute for Clinical Excellence (2005). The management of pressure ulcers in primary and secondary care. Available from www.nice.org.uk/CG029
Chapter 8-201
22 National Institute for Clinical Excellence (2005). Sources of recommendations used in the quick reference guide ‘The prevention and treatment of pressure ulcers’ (CG29). Available from http://www.nice.org.uk/nicemedia/live/10972/29884/29884.pdf. Accessed October 2011
23 Allman RM, Goode PS, Patrick MM, Burst N, Bartolucci AA. Pressure ulcer risk factors among hospitalized patients with activity limitation. J Am Med Assoc 1995;273: 865-70.
24 Baumgarten M, Margolis DJ, Localio AR, Kagan SH, Lowe RA, Kinosian B, Abbuhl SB, Kavesh W, Holmes JH, Ruffin A, Mehari T. Extrinsic risk factors for pressure ulcers early in the hospital stay: a nested case-control study. J Gerontol A. Biol Sci Med Sci. 2008 Apr; 63(4):408-13.
25 Berlowitz DR and Wilkin SVB.Risk factors for pressure sores: a comparison of cross-sectional and cohort derived data. Journal of American Geriatrics Society, 1990, 37(11),pp.1043-1050
26 Bergstrom N, Braden B and Milne D. Are dietary and serum zinc and copper factors in the development of pressure sores in institutionalized elderly. Federation Proceedings,1987,46,p:902.
27 Clark M and Watts S. The incidence of pressure sores in a National Health Service Trust hospital during 1991. Journal of Advanced Nursing,1994,20,pp.33- 36.
28 Makhsous M, Lin F, Cichowski A, Cheng l, Fasanati C, Grant T, Hendrix RW. Use of MRI images to measure tissue thickness over ischial tuberosity at different hip flexion. Clin Anat. 2011 Jul;24(5):638-45. Doi: 10.1002/ca.21119.
29 Bliss M, Simini B, When are the seeds of postoperative pressure sores sown? Often during surgery. BMJ 1999 October 2; 319(7214):863-864
30 Scott EM, The prevention of pressure ulcers through risk assessment. J Wound Care. 2000 Feb; 9(2):69-70
31 Schindler CA, Mikhailov TA, Fischer K, Lukasiewicz G, Kuhn E, Duncan L. Skin integrity in critically ill and injured children. Am J Crit Care.2007;16(6):568– 574
32 Wu SS, Ahn C, Emmons KR, Salcido RS. Pressure ulcers in pediatric patients with spinal cord injury: a review of assessment, prevention, and topical management. Adv Skin Wound Care. 2009 Jun; 22(6): 273-84; quiz 285-6.
Chapter 8-202
33 Schindler CA, Mikhailov TA, Kuhn EM, Christopher J, Conway P, Ridling D, Scott AM, Simpson VS. Protecting fragile skin: nursing interventions to decrease development of pressure ulcers in pediatric intensive care. Am J Crit Care. 2011 Jan;20(1):26-34;
34 Pham B, Teague L, Mahoney J, Goodman L, Paulden M. Poss J, Li J, Ieraci L, Carcone S, Krahn M. Early prevention of pressure ulcers among elderly patients admitted through emergency departments: A cost effective analysis. Ann Emerg Med. 2011 Nov;58(5):468-78.e3.doi:10.1016/j.annemergmed.2011.04.033
35 Bergstrom N, Braden B, Kemp M et al. Multi-site study of incidence of pressure ulcers and the relationship between risk level, demographic characteristics, diagnosis and prescription of preventive interventions. Journal of American Geriatrics Society. 1996,44,pp.22-30
36 Bergstrom N and Braden B. A prospective study of pressure sore risk among institutionalized elderly. Journal of the American Geriatrics Society. 1992,40(8),pp.747-758.
37 Shahin ES, Meijers JM, Schols JM, Tannen A, Halfen RJ, Dassen T. The relationship between malnutrition parameters and pressure ulcers in hospitals and nursing homes. Nutrition 2010 Sep; 26(9):886-9.
38 Eisner JJ, Gefen A. Is obesity a risk factor for deep tissue injury in patients with spinal cord injury? J Biomech. 2008 Dec 5; 41(16)3322-31. Epub 2008 Nov 20.
39 VanGilder C, MacFarlane G, Meyer S, Lachenbruch C. Body mass index, weight, and pressure ulcer prevalence: an analysis of the 2006-2007 International Pressure Ulcer Prevalence Surveys. J Nurs Care Qual. 2009 Apr-Jun; 24(2):127-35.
40 SCI Facts and Figures University of Alabama 2011. Can be found at https://www.nscisc.uab.edu/public_content/pdf/Facts_2011_Feb_Final.pdf
41 Smith BM, Evans CT, Kurichi JE, Weaver FM, Patel N, Burns SP. Acute respiratory tract infection visits of veterans with spinal cord injuries and disorders: Rates, trends and risk factors. J Spinal Cord Med. 2007; 30(4):355-61. [PMID:17853657]
42 DeVivo MJ, Chen Y, Mennemeyer ST, Deutsch A. Costs of care following spinal cord injury. Topics in Spinal Cord Injury Rehabilitation, 2011, 16 (4): 1-9.
43 Cao Y, Chen Y, DeVivo MJ. Lifetime direct costs after spinal cord injury. Topics in Spinal Cord Injury Rehabilitation 2011, 16 (4): 10-16
Chapter 8-203
44 National Spinal Cord Injury Statistical Center, University of Alabama at Birmingham, 2009 Annual Statistical Report:
45 van Riiswijk L, Lyder C. Pressure ulcers: were they there on admission? Am J Nurs. 2008 Nov; 108(11)27-8
46 McKinley WO, Jackson AB, Cardenas DD, DeVivo MJ. Long-term medical complications after traumatic spinal cord injury: a regional model systems analysis. Arch Phys Med Rehabil 1999;80(11):1402-10.
47 Deitrick G, Charalel J, Bauman W, Tuckman J. Reduced arterial circulation to the legs in spinal cord injury as a cause of skin breakdown lesions. Angiology (58)2, 2007:175-84
48 Beckrich K, Aronovitch S. Hospital-acquired pressure ulcers: a comparison of costs in medical vs. surgical patients. Nurs Econ. 1999, 17:263-71, 1999
49 Guihan M, Garber SL, Bombardier CH, Goldstein B, Holmes SA, Cao L. Predictors of pressure ulcer recurrence in veterans with spinal cord injury. J Spinal Cord Med. 2008;31(5):551-9.
50 Bogie KM, Reger SI, Levine SP. Therapeutic applications of electrical stimulation; Wound healing and pressure sore prevention. Assist Tech 2000; 12(1): 50-66
51 Ayello EA, Lyder CH. Protecting patients from harm: preventing pressure ulcers in hospital patients. Nursing. 2007. 2007;37(10):36-40
52 Bennett G, Dealey C, Posnett J. The cost of pressure ulcers in the UK. Age Ageing 2004; 33:230-5
53 INSITEsm Wound Management System. Hill-Rom National Prevalence 1995- 1999. Batesville, Ind: Hill-Rom Inc.
54 Brem H, Maqqi J, Nierman D, Rolnitzky L, Bell D, Rennert R, Golinko M. High Cost of stage IV pressure ulcers. AM J Surg. 200 (4), Oct 2010: 473-77
55 National Pressure Ulcer Advisory Panel (NPUAP). Pressure ulcer: incidence, economics, risk assessment. Consensus development conference statement. Decubitus 1989; 2:24-8
56 Russo CA, Steiner C, Spector W. Hospitalizations Related to Pressure Ulcers Among Adults 18 Years and Older, 2006. Agency for Healthcare Research and
Chapter 8-204
Quality (AHRQ) a part of US department of Health and Human Services. Statistical Brief #64, 2008
57 Padula WV, Mishra MK, Makic MB, Sullivan PW.Improving the quality of pressure ulcer care with prevention: a cost-effectiveness analysis. Med Care. 2011 Apr;49(4):385-92.
58 Registered Nurses Association of Ontario (RNAO). Risk assessment & prevention of pressure ulcers. Toronto (ON): Registered Nurses Association of Ontario (RNAO); 2005 Mar. p80
59 National Pressure Ulcer Advisory Panel (NPUAP). Not all Pressure Ulcers are Avoidable, direct communication. March 3, 2010
60 Garber SL. Wheelchair cushions for spinal cord-injured individuals. AM J Occup Ther. 1985 Nov;39 (11):722-5.
61 Whitehead SJ, Trueman P. To what extent can pressure relieving surfaces help reduce the costs of pressure ulcers? Nursing Times; 2010 Aug 3-9, 106: 30:10- 12.
62 McInnes E, Cullum NA, Bell-Syer SEM, Dumville JC, Jammali-Blasi A. Support surfaces for pressure ulcer prevention. Cochrane Database of Systematic Reviews 2008, Issue 4. Art. No.: CD001735. DOI:10.1002/14651858.CD001735.pub3
63 Brienza D, Kelsey S, Karg P, Allegretti A, Olson M, Schmeler M, Zanca J, Geyer MJ, Kusturiss M, Holm M. A randomized clinical trial on preventing pressure ulcers with wheelchair seat cushions.J Am Geriatr Soc. 2010 Dec;58(12):2308-14. doi: 10.1111/j.1532-5415.2010.03168.x. Epub 2010 Nov 10. PMID:21070197
64 Wheelchair Sage Educational Notes and Policies. http://www.wheelchaircushionsage.com/education-and-policies.php. Accessed Nov 2011.
65 Jan Y, Brienza DM. Technology for Pressure Ulcer Prevention. Top Spinal Cord Inj Rehabil; 2006; 11(3):30-41.
66 Stinson M, Porter A, Eakin P. Measuring interface pressure: a laboratory- based investigation into the effects of repositioning and sitting. Am J Occup Ther 2002; 56(2):185-190.
Chapter 8-205
67 Pollack A, Taylor R, Bader D. Analysis of sweat during soft tissue breakdown following pressure ischemia. Jour of Rehab Research and Development 1993, 30(2):250-9
68 Davies AL, Hayes KC, Dekaban GA. Clinical correlates of elevated serum concentrations of cytokines and autoantibodies in patients with spinal cord injury. Arch Phys Med Rehabil. 2007 Nov; 88(11):1384-93.
69 Frost F, Roach MJ, Kushner I, Schreiber P. Inflammatory C-reactive protein and cytokine levels in asymptomatic people with chronic spinal cord injury. Arch Phys Med Rehabil. 2005 Feb; 86(2):312-7
70 Scremin AM, Kurta L, Gentili A, Wiseman B, Perell K, Kunkel C, Scremin OU. Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise program. Arch Phys Med Rehabil. 1999; 80(12):1531-6.
71 Bogie, KM, Wang X, Triolo RJ. Long-term prevention of pressure ulcers in high-risk patients: a single case study of the use of gluteal neuromuscular electric stimulation. Arch Phys Med Rehabil. 2006 Apr; 87(4):585-91
72 Wu GA, Bogie KM. Assessment of gluteus maximus muscle are with different image analysis programs. Arch Phys Med Rehabil. 2009 Jun; 90(6):1048-54
73 Maciunas RJ, Galloway RL, Latimer JW. The application accuracy of stereotactic frames. Neurosurgery 1994 Oct, 35:682-95
74 Solis LR, Liggins A, Uwiera RR, Poppe, Pehowich E, Seres P, Thompson RB, Mushahwar VK. Distribution of internal pressure around bony prominences: implications to deep tissue injury and effectiveness of intermittent electrical stimulation. Ann Biomed Eng. 2012 Aug; 40(8): 1740-59. Doi: 10.1007/s10439-012- 0529-0. Epub 2012 Feb 22.
75 Linder-Ganz E, Shabsin N, Itzchak Y, Yizhar Z, Siev-Ner I, Gefen A. Strains and stresses in sub-dermal tissues of the buttocks are greater in paraplegics than in healthy during sitting. J Biomech 2008, 41: 567-580.
76 Gefen A. The biomechanics of sitting-acquired pressure ulcers in patients with spinal cord injury or lesions. Int Wound J 2007; 4:222-231.
77 Loerakker S, Solis R, Bader DL, Baaijens FP, Mushahwar VK, Oomens CW. How does muscle stiffness affect the internal deformations within the soft tissue layers of buttocks under constant loading. Comput Methods Biomech Biomed Engineering. 2012 Feb 2. PMID 22300480
Chapter 8-206
78 Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA, 2004, Intramuscular Fat and Glucose Tolerance After Spinal Cord Injury – A Cross-Sectional Study, Spinal Cord 2004; 42:711-16. Doi:10.1038/sj.sc.3101652
79 Regan MA, Teasell RW, Wolfe DL, Mortenson WB, Aubut JA. A systematic review of therapeutic interventions for pressure ulcers after spinal cord injury. Arch Phys Med Rehabil. 2009 Feb; 90(2):213-31. doi:10.1016/j.apmr.2008.08.212
80 Qin W, Bauman WA, Cardozo C. Bone and muscle loss after spinal cord injury: organ interactions: Ann N Y Acad Sci. 2010 Nov;1211:66-84. Doi.: 10.1111/j.1749- 6632.2010.05806.x.
81 De Groot P, Bleeker MW, van Kuppevelt DH, van der Woude LH, Hopman MT. Rapid and extensive arterial adaptations after spinal cord injury. Arch Phys Med Rehabil 2006;87: 688–696.
82 Rasband, W.S., ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA,http://imagej.nih.gov/ij/, 1997-2012.
83 Hounsfield GN. Computed medical imaging. Nobel lecture, December 8, 1979. J Comput Assist Tomogr. 1980 Oct;4(5):665-74.
84 http://vassarstats.net/©Richard Lowry 1998-2012
85 Bauman WA, Spungen AM. Coronary heart disease in individuals with spinal cord injury:assessment of risk factors. Spinal Cord. 2008; 46(7):466-476.
86 Galea MP. Spinal cord injury and physical activity: preservation of the body. Spinal Cord. 2012, 50, 344-351
87 Gorgey AS, Shepherd C. Skeletal muscle hypertrophy and decreased intramuscular fatafter unilateral resistance training in spinal cord injury: Case Report. J Spinal Cord Medicine 2010; 33(1):90-95
88 Loerakker S. Manders E. Strijkers GJ, Nicolay K. Baaijens FPT, Bader DL, Oomens CWJ. The effects of deformation, ischemia, and reperfusion on the development of muscle damage during prolonged loading. J Appl Physiol. 2011 Oct; 111(4):1168-77.doi:10.1152/japplphysiol.00389.2011
89 Black JM, National Pressure Ulcer Advisory Panel. Moving toward consensus on deep tissue injury and pressure ulcer staging. Advances in Skin & Wound Care. 2005. 18(8): 415-6, 418, 420-1.
Chapter 8-207
90 Bouten CV, Oomens CW, Baaijens FP, Bader DL. The etiology of pressure ulcers: skin deep or muscle bound? Arch Phys Med Rehabil. 2003,Apr;84(4):616- 9.
91 Demol J, Deun DV, Haex B, Oosterwyck HV, Sloten JV. Modelling the effect of repositioning on the evolution of skeletal muscle damage in deep tissue injury. Biomech Model Mechanobiol. 2013 Apr; 12(2):267-79.
92 Mak AF, Yu Y, Kwan LP, Sun L, Tam EW. Deformation and reperfusion damages and their accumulation in subcutaneous tissues during loading and unloading: a theoretical modeling of deep tissue injuries. J Theor Biol. 2011 Nov 21;289:65-73.
93 Makhsous M, Lim D, Hendrix R, Bankard J, Rymer WZ, Lin F. Finite element analysis for evaluation of pressure ulcer on the buttock: development and validation. IEEE Trans Neural Syst Rehabil Eng. 2007 Dec;15(4):517-25.
94 Farid KJ, Winkelman C, Rizkala A, Jones K. Using temperature of pressure- related intact discolored areas of skin to detect deep tissue injury: an observational, retrospective, correlational study. Ostomy Wound Manage. 2012 Aug;58(8):20-31.
95 Shabshin N, Zoizner G, Herman A, Ougortsin V, Gefen A. Use of weight- bearing MRI for evaluating wheelchair cushions based on internal soft-tissue deformations under ischial tuberosities. J Rehabil Res Dev. 2010;47(1):31-4
96 Sprigle S, Sonenblum S. Assessing evidence supporting redistribution of pressure for pressure ulcer prevention: a review. J Rehabil Res Dev. 2011;48(3):203-13.
97 Olive JL, McCully KK, Dudley GA. Blood flow response in individuals with incomplete spinal cord injuries. Spinal Cord. 2002 Dec;40(12):639-45.
98 Guttmann L. Spinal cord injuries: comprehensive management and research, 2nd edn. Oxford: Blackwell, 1976.
99 Claus-Walker J, Halstead LS. Metabolic and endocrine changes in spinal cord injury. Part II. Section 1. Consequences of partial decentralization of the autonomic nervous system. Arch Phys Med Rehabil 1982;63:569–75.
100 Rosner MJ, Elias Z, Coley I. New principles of resuscitation for brain and spinal injury. N C Med J 1984;45:701–8.
Chapter 8-208
101 Ramos MV, Freed MM, Kayne HL. Resting blood pressures of spinal cord injured patients. Sci Dig 1981;3:19–25
102 Borisov AB, Huang SK, Carlson BM. Remodeling of the vascular bed and progressive loss of capillaries in denervated skeletal muscle. Anat Rec. 2000: 258 (3) 292-304..
103 Hunt TK, Conolly WB, Aronson SB, Goldstein P. Anaerobic metabolism and wound healing an hypothesis for the initiation and cessation of collagen synthesis in wounds Am J Surg 1978; 135:328-32
104 Rappl LM. Physiological changes in tissues denervated by spinal cord injury tissues and possible effects on wound healing. Int Wound J 2008;5:435–444
105 Grolman RE, Wilkerson DK, Taylor J, Allinson P, Zatina MA. Transcutaneous oxygen measurements predict a beneficial response to hyperbaric oxygen therapy in patients with nonhealing wounds and critical limb ischemia. Am Surg. 2001 Nov;67(11):1072-9; discussion 1080.
106 Ho C, Bogie KM. The Prevention and Treatment of Pressure Ulcers. Physical Medicine and Rehabilitation Clinics of North America. 2007 18 (2):235-253.
107 Hardin JB, Cronin SN, Cahill K. Comparison of the effectiveness of two pressure-relieving surfaces: low-air-loss versus static fluid. Ostomy Wound Manage. 2000 Sep;46(9):50-6.
108 Bell J. The role of pressure-redistributing equipment in the prevention and management of pressure ulcers. J Wound Care. 2005 Apr;14(4):185-8.
109 Allegretti AL, Malkiewicz A, Brienza DM. Measuring interface pressure and temperature in the operating room. Adv Skin Wound Care. 2012 May;25(5):226- 30.
110 Keller BP, van Overbeeke J, van der Werken C Interface pressure measurement during surgery: a comparison of four operating table surfaces.J Wound Care. 2006 Jan;15(1):5-9.
111 CONFORMat system, software features tab. http://www.tekscan.com/conformat-seating-positioning-pressure- measurement <
112 Sprigle S, Dunlop W, Press L. Reliability of bench tests of interface pressure. Assist Technol. 2003 Summer;15(1):49-57.
Chapter 8-209
113 Stinson MD, Porter-Armstrong A, Eakin P, 2003. Pressure mapping systems: reliability of a pressure map interpretation. Clin. Rehabil. 2003, 17, 504-511.
114 Brienza DM, Karg PE, Geyer MJ, Kelsey S, Trefler E. The relationship between pressure ulcer incidence and buttock-seat cushion interface pressure in at-risk elderly wheelchair users. Arch Phys Med Rehabil 2001; 82(4):529-533.
115 Reger SI, Ranganathan VK, Sahgal V. Support surface interface pressure, microenvironment, and the prevalence of pressure ulcers: an analysis of the literature. Ostomy Wound Management. 2007 Oct; 53(1):50-8
116 Bogie KM, Wang X, Fei B, Sun J. New technique for real-time interface pressure analysis: Getting more out of large image data sets. JRRD. 2008, 45(4):523-36
117 Swain ID, Bader DL. The measurement of interface pressure and its role in soft tissue breakdown. J Tissue Viability . 2002 Oct; 12(4): 132-4, 136-7, 140-6
118 Ferguson M, Nicholson G, Bain D, Call E, Grady J, deVries J. The role of wheelchair seating standards in determining clinical practices and funding policy. Asst Technol 2005; 17:1-6
119 Drummond D, Breed AL, Narechania R. Relationship of spine deformity and pelvic obliquity on sitting pressure distributions and decubitus ulceration. J Pediatr Orthop. 1985 Jul-Aug;5(4):396-402.
120 Cox J. Predictors of pressure ulcers in adult critical care patients. Am J Crit Care. 2011 Sep; 20(5):364-75.
121 Akins JS, Karg PE, Brienza DM. Interface shear and pressure characteristics of wheelchair seat cushions. J Rehabil Res Dev. 2011;48(3):225-34.
122 Barr PA. Transcutaneous measurement of oxygen tension in infants with hyaline membrane disease. Aust Paediatr J. 1979 Mar;15(1):3-6
123 Finer NN, Stewart AR. Continuous transcutaneous oxygen monitoring in the critically ill neonate. A controlled clinical trial. Crit Care Med. 1980 Jun;8(6):319- 23.
124 Jenkins JG, Lim JH, Bell A, Savage JM. Transcutaneous blood gas monitoring during peritoneal dialysis in the neonate. Int J Pediatr Nephrol. 1986 Apr- Jun;7(2):85-6.
Chapter 8-210
125 Bauman KA, Kurili A, Schmidt SL, Rodriguez GM, Chiodo AE, Sitrin RG . Home-Based Overnight Transcutaneous Capnography/Pulse Oximetry for Diagnosing Nocturnal Hypoventilation Associated with Neuromuscular Disorders. Arch Phys Med Rehabil. 2013 Jan;94(1):46-52. Doi:10.1016.j.apmr.2012.08.215
126 Chakravarthy M, Narayan S, Govindarajan R, Jawali V. Improvement in accuracy of transcutaneous measurement of oxygen with resumption of spontaneous ventilation in mechanically ventilated patients after off pump coronary artery bypass procedure: a prospective study. J Clin Monit Comput. 2009 Dec;23(6):363-8. Epub 2009 Oct 31.
127 Stirban A, Lentrodt S, Nandrean S, Pop A, Tschoepe D, Scherbaum WA. Functional changes in microcirculation during hyperbaric and normobaric oxygen therapy. Undersea Hyperb Med. 2009 Sep-Oct;36(5):381-90.
128 Markus YM, Bell MJ, Evans AW. Ischemic scleroderma wounds successfully treated with hyperbaric oxygen therapy. J Rheumatol. 2006 Aug;33(8):1694-6.
129 Karanfilian RG, Lynch TG, Zirul VT, Padberg FT, Jamil Z, Hobson RW 2nd.The value of laser Doppler velocimetry and transcutaneous oxygen tension determination in predicting healing of ischemic forefoot ulcerations and amputations in diabetic and nondiabetic patients. J Vasc Surg. 1986 Nov;4(5):511- 6.
130 Dowd GS. Predicting stump healing following amputation for peripheral vascular disease using the transcutaneous oxygen monitor. Ann R Coll Surg Engl. 1987 Jan;69(1):31-5.
131 Tzen YT, Brienza DM, Karg P, Loughlin P. Effects of local cooling on sacral skin perfusion response to pressure: implications for pressure ulcer prevention. J Tissue Viability. 2010 Aug; 19(3):86-97
132 Knight SL, Taylor RP, Polliack AA, Bader DL. Establishing predictive indicators for the status of loaded soft tissues. J Appl Physiol. 2001 Jun; 90 (6):2231-7.
133 Kim JH, Wang X, Ho CH, Bogie KM. Physiological measurements of tissue health: implications for clinical practice. Int Wound J. 2012 Jan 30. Doi: 10.1111/j.1742-481X.2011.00935.x. PMID: 22289151
134 Colin D, Saumet JL. Influence of external pressure on transcutaneous oxygen tension and laser Doppler flowmetry on sacral skin. Clin Physiol. 1996 Jan;16(1):61-72.
Chapter 8-211
135 Gefen A, Levine J. The false premise in measuring body-support interface pressures for preventing serious pressure ulcers. J Med Eng Technol. 2007 Sep- Oct; 31(5):375-80
136 Sitkovsky MV, Lukashev D, Apasov S, Kojima H, Koshiba M, Caldwell C, Ohta A, Thiel M. Damage by hypoxia-inducible factors and adenosine a2a receptors. Annual Review of Immunology. 2004, 22: 657-682. Doi:10.1146/annurev.immunol.22.012703.104731
137 TCM400 Specifications from Radiometer America website accessed 4/10/2012
138 Makhsous M, Priebe M, Bankard J, Rowles D, Zeigler M, Chen D, Lin F. Measuring tissue perfusion during pressure relief maneuvers: insights into preventing pressure ulcers. J Spinal Cord Med. 2007; 30(5):497-507.
139 Bogie KM, Nuseibeh I, Bader DL. Transcutaneous gas tensions in the sacrum during the acute phase of spinal cord injury. Proc Inst Mech Eng H. 1992;206(1):1-6.
140 Fife CE, Smart DR, Sheffield PJ, Hopf HW, Hawkins G, Clarke D. Transcutaneous oximetry in clinical practice: consensus statements from an expert panel based on evidence. Undersea Hyperb Med. 2009 Jan-Feb;36(1):43-53.
141 Schubert V, Fagrell B. Postocclusive reactive hyperemia and thermal response in the skin microcirculation of subjects with spinal cord injury. Scand J Rehabil Med 1991; 23:33e40
142 Sperandio PA, Borghi-Silva A, Barroco A, Nery LE, Almeida DR, Neder JA. Microvascular oxygen delivery-to-utilization mismatch at the onset of heavy- intensity exercise in optimally treated patients with CHF. Am J Physiol Heart Circ Physiol. 2009 Nov;297(5):H1720-8. Epub 2009 Sep 4.
143 Neviere R, Mathieu D, Chagnon JL, Lebleu N, Millien JP, Wattel F. Skeletal muscle microvascular blood flow and oxygen transport in patients with severe sepsis. Am J Respir Crit Care Med. 1996 Jan;153(1):191-5.
144 Kawashima N, Nakazawa K, Akai M. Muscle oxygenation of the paralyzed lower limb in spinal cord-injured persons. Med Sci Sports Exerc. 2005 Jun;37(6):915-21.
Chapter 8-212
145 Bhambhani Y, Tuchak C, Burnham R, Jeon J, Maikala R. Quadriceps muscle deoxygenation during functional electrical stimulation in adults with spinal cord injury. Spinal Cord. 2000 Oct;38(10):630-8.
146 Bader DL. The recovery characteristics of soft tissues following repeated loading. J Rehabil Res Dev. 1990 Spring;27(2):141-50.
147 Sanchez OA, Copenhaver EA, Chance MA, Fowler MJ, Towse TF, Kent- Braun JA, Damon BM. Postmaximal contraction blood volume responses are blunted in obese and type 2 diabetic subjects in a muscle-specific manner. Am J Physiol Heart Circ Physiol. 2011 Aug;301(2):H418-27. Epub 2011 May 13.
148 Boyko EJ, Ahroni JH, Stensel VL. Tissue oxygenation and skin blood flow in the diabetic foot: responses to cutaneous warming. Foot Ankle Int. 2001 Sep;22(9):711-4.
149 Sonenblum SE, Sprigle SH. The impact of tilting on blood flow and localized tissue loading. Journal of Tissue Viability. 2011, 20:3-13.
150 Bernardi L, Leuzzi S. Laser Doppler Flowmetry and Photoplethysmography: basic priciples and hardware. In: Bioengineering of the Skin: Cutaneous Blood Flow and Erythema. Eds: Berardesca E, Elsner P, Maibach HI. CRC Press, 1994:32-52
151 LaserFlo BPM2 Blood Perfusion Monitor Operator Manual, 1999. Vasamedics System Software Rev 1.46 October 12, 1999
152 Grossmann A, Morlet J. Decomposition of Hardy functions into square integrable wavelets of constant shape. SIAM J Mathemat Anal. 1984;15(4):723–36
153 Stefanovska A, Bracic M, Kvernmo HD. Wavelet analysis of oscillations in the peripheral blood circulation measured by laser Doppler technique. IEEE Trans Biomed Eng. 1999;46(10):1230–39
154 Geyer MJ, Jan YK, Brienza DM, Boninger ML. Using wavelet analysis to characterize the thermoregulatory mechanisms of sacral skin blood flow. J Rehabil Res Dev. 2004 Nov-Dec; 41(a);797-806
155 Tikhonova IV, Tankanag AV, Chemeris NK. Age-related changes of skin blood flow during postocclusive reactive hyperemia in human. Skin Res Technol. 2013 Feb; 19(1):e174-81. doi: 10.1111/j.1600-0846.2012.00624.x.
Chapter 8-213
156 Kverno HD, Stefanovska A, Bracic M, Kirkeboen KA, Kvernebo K. Spectral analysis of the laser Doppler perfusion signal in human skin before and after exercise. Microvasc Res. 1998 Nov; 56(3):173-82 PMID 9828155
157 Lino S, Calcagnini G, Censi f, Congi M, De Pasquale F. Cardiovascular neuroregulation and rhythms of the autonomic nervous system: frequency domain analysis. [Article in Italian] Cardiologia, 1999 Mar 44(3):281-7
158 Stafanovska A, Bracic M, Kvernmo HD. Wavelet analysis of oscillations in the peripheral blood circulation measured by laser Doppler technique. IEEE Trans Biomed Eng. 1990 Oct; 46(10):1230-9
159 Geyer MJ, Jan YK, Brienza DM, Boninger ML. Using wavelet analysis to characterize the thermoregulatory mechanisms of sacral skin blood flow. J Rehabil Res Dev. 2004 Nov-Dec;41(6A):797-806.
160 de Leva P. Adjustments to Zatsiorsky-Seluyanov's segment inertia parameters. J Biomech. 1996 Sep;29(9):1223-30.
161 Cristofolini L, Marchetti A, Cappello A, Viceconti M. A novel transducer for the measurement of cement-prosthesis interface forces in cemented orthopaedic devices. Med Eng Phys. 2000 Sep;22(7):493-501.
162 Then C, Vogl TJ, Silber G. Method for characterizing viscoelasticity of human gluteal tissue. J Biomech. 2012 Apr 30;45(7):1252-8. Epub 2012 Feb 22.
163 Li Z, Leung JY, Tam EW, Mak AF. Wavelet analysis of skin blood oscillations in persons with spinal cord injury and able-bodied subjects. Arch Phys Med Rehabil. 2006 Sep; 87(9):1207-12
164 Stefanovska A, Sheppard LW, Stankovski T, McClintock PV. Reproducibility of LDF blood flow measurements: dynamical characterization versus averaging. Microvasc Res. 2011 Nov; 82(3):274-6. Doi: 10.1016/j.mvr.2011.08.009.
165 Gélis A, Fattal C, Dupeyron A, Pérez-Martin A, Colin D, Pelissier J. Reproducibility of transcutaneous oxygen pressure measurements in persons with spinal cord injury. Arch Phys Med Rehabil. 2009 Mar;90(3):507-11. Doi: 10.1016/j.apmr.2008.09.564.
166 Schubart JR, Hilgart M, Lyder C. Pressure ulcer prevention and management in spinal cord-injured adults: analysis of educational needs. Adv. Skin Wound Care. 2008 Jul, 27(7) 322-9.
Chapter 8-214
167 Yuen HK, Garret D. Comparison of three wheelchair cushions for effectiveness of pressure relief. AM J Occup Ther. 2001. Jul-Aug; 55(4):470-5.
168 Coggrave MJ, Rose LS. A specialist seating assessment clinic: Changing pressure relief practice. Spinal Cord. 2003; 41(12):692-95. Doi:10.1038/sj.sc.3101527
169 Burnham, R., T. Martin, R. Stein, G. Bell, I. MacLean, and R. Steadward. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35: 86–91.
170 Castro MJ, Apple Jr DF, Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physio.l 1999;80:373-378.
171 Fuhrer MJ. Rehabilitation research and training center in community- oriented services for persons with spinal cord injury: a progress report. Houston: Baylor College of Medicine, Institute for Rehabilitation and Research; 1991.
172 Johnson RL, Gerhart KA, McCray J, Menconi JC, Whiteneck GG. Secondary conditions following spinal cord injury in a population based sample. Spinal Cord. 1998;36:45-50.
173 McGlinchey-Berroth R, Morrow L, Ahlquist M, Sarkarati M, Minaker KL. Late-life spinal cord injury and aging with a long term injury: characteristics of two emerging populations. J Spinal Cord Med. 1995;18:183-93.
174 Levine SP, Kett RL, Cederna PS, Bowers LD, Brooks SV. Electrical muscle stimulation for pressure variation at the seating interface. J Rehabil Res Dev. 1989;26(4):1-8.
175 Levine SP, Kett RL, Cederna PS, Bowers LD, Brooks SV. Electrical muscle stimulation for pressure sore prevention: tissue shape variation. Arch Phys Med Rehabil. 1990;71:210-5.
176 Levine SP, Kett RL, Gross MD, Wilson BA, Cederna PS, Juni JE. Blood Flow in the Gluteus Maximus of Seated Individuals during Electrical Muscle Stimulation. Arch Phys Med Rehabil. 1990;71:682-6.
177 Liu MS, Grimm DR, Teodorescu V, Kronowitz SJ, Bauman WA. Transcutaneous oxygen tension in subjects with paraplegia with and without pressure ulcers: A preliminary report. J Rehabil Res Dev. July 1999;36(3):202-6.
Chapter 8-215
178 Baldi JC, Jackson RD, Moraille R, Mysiw WJ. Muscle atrophy is prevented in patients with acute spinal cord injury using functional electrical stimulation. Spinal Cord. 1998; 26:463-469.
179 Kern H, Rossini K, Boncompagni S, Protasi F, Hofer C, Modlin M, Carraro Ugo. Long Lasting muscle trophism in complete upper motor neuron lesion paraplegia. Basic Appl Myol. 2005;15 (5&6):191-20.
180 Warfield SK, Zou KH, Wells WM. Validation of Image Segmentation by Estimating Rater Bias and Variance. MICCAI 2006, LNCS 4191, 2006:839-847.
181 Shoukri MM, Edge VL. Statistical Methods for Health Sciences. CRC Press, Boca Raton 1996.
182 NPUAP 2001 Pressure Ulcer Prevention: A Competency-based Curriculum. Accessed May 2, 2008.
183 Mitsiopoulos N, Baumgartner RN, Heymsfield SB, Lyons W, Gallagher D, Ross R. Cadaver validation of skeletal muscle measurement by magnetic resonance image and computerized tomography. J Appl Physiol. 1998;85(1):115- 122.
184 Goodpaster BH, Kelley DE, Thaete FL, He J, Ross R, Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol. 2000, 89:104-110.
185 De Carvalho DE, Soave D, Ross K, Callaghan JP. Lumbar spine and pelvic posture between standing and sitting: a radiologic investigation including reliability and repeatability of the lumbar lordosis measure. J Manipulative Physiol Ther. 2010 Jan; 33(1): 48-55
186 Ham R, Aldersea P, Porter D et al Wheelchair users and postural seating. A clinical approach. Churchill Livingstone, Singapore: 1998
187 Cooper RA. Rehabilitation Engineering Applied to Mobility and Manipulation. Taylor & Francis, NY, 1995
188 Boninger ML, Cooper RA, Schmeler M, Cooper R. Wheelchairs. p1299. In Physical Medicine and Rehabilitation: Principles and Practice, Volume 1. Ed DeLisa JA, Gans BM, Walsh NE. Lippincott Williams & Wilkins 2005
189 Cooper RA. Wheelchair Selection and Configuration. Demos Medical Publishing1998
Chapter 8-216
190 Swain I. The measurement of interface pressure. p58. In Pressure Ulcer Research Eds Bader DL, Bouten CVC, Colin D , Oomens CWJ. Springer-Verlag,, Berlin-Heidelberg, 2005
191 Trefler E, Taylor SJ. Prescription and positioning: evaluating the physically disabled individual for wheelchair seating. Prosthet Orthot Int. 1991 Dec; 15(3): 217-24
192 Hastings JD. Seating assessment and planning. Phys Med Rehabil Clin N Am. 2000 Feb; 11(1): 183-207
193 Anderson K, Targeting recovery: Priorities of the spinal cord injured population. J Neurotrauma 2004; 21(10): 1371-1383
194 Brown-Triolo DL, Roach ML, Triolo RJ, Nelson K. Consumer perspectives on mobility: implications for neuroprosthesis design. J Rehab Res Dev 2002; 39(6): 659-669
195 Collins F, Shipperley TF. Assessing the seated patient for the risk of pressure damage. J Wound Care 1999; 8: 123–126
196 Axelson P, Minkel J, Perr A, Yamada D. The Powered Wheelchair Training Guide. PAX Press, a division of Beneficial Designs, Inc., Santa Cruz, California, 2002
197 Beckrich K, Aronovitch S. Hospital-acquired pressure ulcers: a comparison of costs in medical vs. surgical patients. Nurs Econ. 1999; 17: 263-71,
198 Creasey GH, Ho CH, Triolo RJ, Gater DR, DiMarco AF, Bogie KM, Keith MW. Clinical applications of electrical stimulation after spinal cord injury. J Spinal Cord Med. 2004;27(4):365-75.
199 Davis JA Jr, Triolo RJ, Uhlir JP, Bhadra N, Lissy DA, Nandurkar S, Marsolais EB. Surgical technique for installing an eight-channel neuroprosthesis for standing. Clin Orthop Relat Res. 2001 Apr; (385): 237-52
200 Fisher LE, Miller ME, Bailey SN, Davis JA Jr, Anderson JS, Rhode L, Tyler DJ, Triolo RJ. Standing after spinal cord injury with four-contact nerve-cuff electrodes for quadriceps stimulation. IEEE Trans Neural Syst Rehabil Eng. 2008 Oct; 16(5): 473-8
201 Triolo RJ, Boggs L, Miller ME, Nemunaitis G, Nagy J, Bailey SN. Implanted electrical stimulation of the trunk for seated postural stability and function after
Chapter 8-217
cervical spinal cord injury: a single case study. Arch Phys Med Rehabil. 2009 Feb; 90(2): 340-7
202 Triolo RJ, Bailey SN, Miller ME, Rohde LM, Anderson JS, Davis JA Jr, Abbas JJ, DiPonio LA, Forrest GP, Gater DR Jr, Yang LJ. Longitudinal performance of a surgically implanted neuroprosthesis for lower-extremity exercise, standing, and transfers after spinal cord injury. Arch Phys Med Rehabil. 2012 May; 93(5): 896- 904
203 Kilgore KL, Hoyen HA, Bryden AM, Hart RL, Keith MW, Peckham PH. An implanted upper-extremity neuroprosthesis using myoelectric control. J Hand Surg Am. 2008 Apr; 33(4): 539-50
204 Kukke SN, Triolo RJ. The effects of trunk stimulation on bimanual seated workspace. IEEE Trans Neural Syst Rehabil Eng. 2004 Jun; 12(2): 177-85
205 Kosiak M. Etiology of decubitus ulcers. Arch Phys Med Rehabil. 1961; 42: 19- 29
206 Bogie KM, Reger SI, Levine SP. Therapeutic applications of electrical stimulation; Wound healing and pressure sore prevention. Assist Tech 2000; 12(1): 50-66
207 Bogie KM, Triolo RJ. The effects of regular use of neuromuscular electrical stimulation on tissue health. J Rehabil Res Dev. 2003; 40(6): 469-475
208 Bogie K, Ho CH, Chae J, Triolo RJ. Dynamic therapeutic neuromuscular electrical stimulation for pressure relief. Am J Phys Med Rehabil. 2004; 83(3), 240
209 Doucet BM, Lam A, Griffin L, Neuromuscular Electrical Stimulation for Skeletal Muscle Function. Yale J Biol Med. 2012 June; 85(2): 201-215. PMCID: PMC3375668
210 Ragnarsson KT. Functional electrical stimulation after spinal cord injury: current use, therapeutic effects and future directions. Spinal Cord 2008. 46, 255- 274; doi: 10.1038/sj.sc.3102091;
211 Tillmann VB. Variations in the pathway of the inferior gluteal nerve. Anat Anz. 1979;145:292-302 (in German)
212 Petchprapa CN, Rosenberg ZS, Sconfienza LM, Cavalcanti Cf, Vieira RL, Zember JS. MR imaging of entrapment neuropathies of the lower extremity. Part 1. The pelvis and hip. Radiographics. 2010 Jul-Aug;30(4):983-1000.
Chapter 8-218
213 Shellock FG, Magnetic resonance safety update 2002: Implants and devices. J. Magn. Reson. Imaging 2002;16:485-496
214 Baker KB, Nyenhuis JA, Hrdlicka G, Rezai AR, Tkach JA, Shellock FG. Neurostimulation systems: assessment of magnetic field interactions associated with 1.5- and 3-Tesla MR systems. J Magn Reson Imaging. 2005 Jan; 21(1):72-7.
215 Lemmens C, Faul D, Nuyts J. Suppression of metal artifacts in CT using a reconstruction procedure that combines MAP and projection completion. IEEE Trans Med Imaging. 2009 Feb;28(2):250-60.
216 Vande Berg B, Malghem J, Maldague B, Lecouvet F. Multi-detector CT imaging in the postoperative orthopedic patient with metal hardware. Radiology 2006 Dec. 60 (3), 470-479
217 Skalak AF, McGee MF, Wu G, Bogie K. Relationship of inferior gluteal nerves and vessels: target for application of stimulation devices for the prevention of pressure ulcers in spinal cord injury. Surg Radiol Anat, 2008. 30(1):41-5.
218 Tsui BCH, Chan VWS, Finucane BT, et. al. Atlas of Ultrasound and Nerve Stimulation-Guided Regional Anesthesia. New York: Springer, 2007.
219 Rivas Ferreira E, Sala-Blanch X, Bargalló X, Sadurní M, Puente A, De Andrés J. Ultrasound-guided posterior approach to block the sciatic nerve at the popliteal fossa. Rev Esp Anestesiol Reanim. 2004 Dec;51(10):604-7.
220 Wojtkowski M, Srinivasan V, Fujimoto JG, Ko T, Schuman JS, Kowalczyk A, Duker JS. Three-dimensional retinal imaging with high-speed ultrahigh- resolution optical coherence tomography. Ophthalmology. 2005 Oct;112(10):1734-46.
221 Ling ZX, Kumar VP. The course of the inferior gluteal nerve in the posterior approach to the hip. J Bone Joint Surg[Br] 2006;88 –B:1580-3
222 Apaydin N, Bozkurt M, Loukas M, Tubbs RS, Esmer AF. The course of the inferior gluteal nerve and surgical landmarks for its localization during posterior approaches to hip. Surg Radiol Anat 2009. 31:415-418. Doi 10.1007/s00276-008- 0459-6
223 Hwang K, Nam YS, Han SH, Hwang SW. The intramuscular course of the inferior gluteal nerve in the gluteus maximus muscle and augmentation gluteoplasty. Ann Plast Surg 2009; 63:361-365.
Chapter 8-219
224 Rabadi MH, Vincent AS. Do vascular risk factors contribute to the prevalence of pressure ulcer in veterans with spinal cord injury? J Spinal Cord Med. 2011, January;34(1):46-51 doi.10.1179/107902610X12923394765652.
225 Stockton L, Rithalia S. Pressure-reducing cushions: Perceptions of comfort from the wheelchair users’ perspective using interface pressure, temperature and humidity measurements. Journal of Tissue Viability. 2009 18(2) 28-35. Doi:10.1016/j.jtv.2007.09.006
226 Stockton L. Rithalia S. Is dynamic seating a modality worth considering in the prevention of pressure ulcers? Journal of Tissu e Viability. 2007, 17:15-21
227 Tzen YT. Effectiveness of Local Cooling on Enhancing Tissue Ischemia tolerance in people with Spinal Cord Injury. Doctoral Thesis. University of Pittsburgh School of Health and Rehabilitation Science. 2010
228 Dengler R, Konstanzer A, Küther G, Hesse S, Wolf W, et al. Amyotrophic lateral sclerosis: Macro-EMG and twitch forces of single motor units. Muscle Nerve 1990; 13: 545–550.
229 Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, et al. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 2004; 185: 232–240.
230 Ono S. Skin changes in amyotrophic lateral sclerosis. Brain Nerve. 2007 Oct;59 (10):1099-107
231 Raney JP. A comparison of the prevalence of pressure sores in hospitalized ALS and MS patients. Decubitus. 1989 May;2(2):48-49
232 Wijesekera L. C., Leigh P. N. Amyotrophic lateral sclerosis. Orphanet J. Rare Dis. 2009;(4), 1–22.
Chapter 8-220