Volume 90, Issue 2 , Pages 213-231, February 2009
A Systematic Review of Therapeutic Interventions for Pressure Ulcers After Spinal Cord Injury
Article Outline
- Abstract
- Methods
- Direct Versus Indirect Indicators of Prevention
- Prevention of Pressure Ulcers
- Conclusions
- Pressure Relief Practices
- Conclusions
- Wheelchair Cushion Selection
- Conclusions
- Thickness of Lumbar Support
- Conclusions
- Specialized Seating Clinics
- Conclusions
- Education
- Conclusions
- Behavioral Contingencies
- Conclusions
- Telerehabilitation and Pressure Ulcer Management
- Conclusions
- Treatment of Pressure Ulcers
- Conclusions
- Laser Treatment for Pressure Ulcer Healing
- Conclusions
- US/UVC for Pressure Ulcer Healing
- Conclusions
- Effects of Nonthermal Pulsed Electromagnetic Energy Treatment
- Conclusions
- Anabolic Steroid Agents
- Conclusions
- Effectiveness of Dressings
- Conclusions
- Maggot Therapy
- Conclusions
- Conclusions
- References
- Copyright
Abstract
Regan MA, Teasell RW, Wolfe DL, Keast D, Mortenson WB, Aubut JL, for the Spinal Cord Injury Rehabilitation Evidence Research Team. A systematic review of therapeutic interventions for pressure ulcers after spinal cord injury.
Objective
To systematically review evidence on the prevention and treatment of pressure ulcers in those with a spinal cord injury (SCI).
Data Sources
For this evidence-based review, the following data sources were used: MEDLINE/PubMed, CINAHL, EMBASE, and PsycINFO.
Study Selection
To be selected for inclusion in the current review, there had to have been an intervention, studies had to have 3 or more subjects, and 50% or more of the participating group had to have an SCI.
Data Extraction
Data extracted included study design, subject demographics, inclusion and exclusion criteria, study type, sample size, outcome measures used, and study results.
Data Synthesis
Articles selected for this review were organized into 1 of 2 categories: prevention or treatment. Within each broad category, several smaller ones were created, and articles were grouped according to the prevention (direct or indirect) or treatment intervention discussed.
Conclusions
Of the 26 articles selected for inclusion in the systematic review, 7 were randomized controlled trials (RCTs) that dealt with treatment for pressure ulcers, and there was 1 RCT on prevention. Despite the cost-effectiveness of prevention, little research exists on preventative interventions, and what does exist is mostly level 4 evidence. More research is needed for both prevention and treatment, but especially the former.
Key Words: Paraplegia, Pressure ulcer, Quadriplegia, Rehabilitation
List of Abbreviations: HD, hydrocolloid dressing, HVPC, high-voltage pulsed current, HVPGS, high-voltage pulsed galvanic stimulation, IT, ischial tuberosity, MDT, maggot debridement therapy, NAC, Needs Assessment Checklist, NMES, neuromuscular electrical stimulation, PEDro, Physiotherapy Evidence Database Scale, PUSH, Pressure Ulcer Scale for Healing, RCT, randomized controlled trial, SCI, spinal cord injury, SCIRE, Spinal Cord Injury Rehabilitation Evidence, PTCo2, transcutaneous oxygen tension, US, ultrasound, UVC, ultraviolet C radiation
PRESSURE ULCERS ARE serious, secondary complications of SCI. Although preventable in most situations, pressure ulcers may disrupt rehabilitation, prevent persons with SCI from working or attending school, interfere with community reintegration, and affect quality of life.1, 2, 3, 4 When the pressure ulcer is severe, it can lead to further disability, decreases in mobility, loss of independence, the need for surgical interventions, and fatal infections.3, 5
Pressure ulcers have been defined as a lesion on any skin surface that results from pressure or pressure in combination with shear force and/or friction.5, 6, 7, 8 The primary cause is felt to be externally applied pressure for a prolonged period over bony prominences, such as the sacrum and IT. This leads to ischemia of overlying soft tissues, which ultimately can lead to necrosis.6, 9, 10 While the ulcer may appear confined to the skin, it may take weeks before the true size and depth of the ulcer is known.11 In addition, muscle is more sensitive than skin to ischemia caused by pressure.1
Pressure ulcers are staged according to the degree of tissue damage observed. The staging system developed by the National Pressure Ulcer Advisory Panel in 198912 and recently revised in 20078 is widely used and supported.13, 14 It consists of 4 stages that range in severity from stage I (which involves intact skin) to stage IV (full-thickness tissue loss; table 1). In community-dwelling persons with SCI, 25% of pressure ulcers are classified as severe (stage III or IV).2 Another type of pressure ulcer is suspected deep tissue injury. This injury looks like a bruise on intact skin but may rapidly progress to involve deeper layers, despite treatment.8, 15
Table 1. Stages of Pressure Ulcers
| Stage | Descriptions |
|---|---|
| Suspected deep tissue injury | Purple or maroon localized area of discolored intact skin or blood-filled blister caused by damage underlying soft tissue from pressure and/or shear force. The area may be preceded by tissue that is firm, mushy, boggy, warmer, or cooler compared with adjacent tissue. |
| Stage 1 | Intact skin with nonblanchable redness of localized area, usually over a bony prominence. Darkly pigmented skin may not have visible blanching; its color may differ from the surrounding area. |
| Stage 2 | Partial thickness loss of dermis presenting as a shallow open ulcer with a red/pink wound bed, without slough. May also present as an intact or open/ruptured serum-filled blister. |
| Stage 3 | Full-thickness tissue loss. Subcutaneous fat may be visible, but bone, tendon, or muscles are not exposed. Slough may be present but does not obscure the depth of tissue loss. May include undermining and tunneling. |
| Stage 4 | Full-thickness tissue loss with exposed bone, tendon, or muscle. Slough or eschar may be present in some parts of the wound bed. Often includes undermining and tunneling. |
| Unstageable | Full-thickness tissue loss in which the base of ulcer is covered by slough (yellow, tan, gray, green, or brown) and/or eschar (tan, brown, or black) in the wound bed. |
Cost data on pressure ulcers in SCI populations are difficult to obtain.16 In a case study of a community-dwelling person with paraplegia, Allen and Houghton16 demonstrated that the cost of 3 months of accelerated wound treatment to heal a stage III ulcer was $27,632 Canadian, with approximately half the cost paid for by the person. In the United States, for persons with SCI, it has been estimated that the cost of care for pressure ulcers is about $1.2 to 1.3 billion annually, whereas prevention would cost about one tenth of this.4, 17, 18 Despite the attention given to preventative strategies by rehabilitation and public health professionals, pressure ulcers are common among persons with an SCI.19 Annual incidence rates range from 20% to 31% and prevalence rates from 10.2% to 30%.11, 17
Prevention of pressure ulcers requires the recognition of significant risk factors, which effect either the intensity and duration of pressure or the tissue tolerance for pressure.20 Identified risk factors include limitations in activity and mobility, injury completeness, moisture from bowel and/or bladder incontinence, lack of sensation, muscle atrophy, nutritional status, and being underweight.11, 17, 19
Prevention of pressure ulcers begins at the time of injury and is a lifelong commitment for those living with SCI or their caregivers.21 Typical prevention recommendations made during rehabilitation include examining skin daily to allow for early detection; minimizing moisture and incontinence, and keeping skin clean and dry; regular pressure relief every 15 to 30 minutes by performing a lateral bend, forward lean, or vertical push-up1, 9; having an individually prescribed wheelchair with a pressure redistribution cushion, and a power or manual tilt/recline feature if manual pressure relief is not possible1; ensuring that all equipment is functioning properly; decreasing or stopping smoking, and limiting alcohol consumption; and eating a well balanced, nutritionally complete diet, which includes monitoring of weight to detect undesirable trends.1, 22 Persons with SCI and their caregivers must learn the importance of following a skin care regimen, recognize potential consequences of a pressure ulcer, and begin to take responsibility for maintaining healthy skin.9, 23, 24 To promote sustainable outcomes, health care professionals must assist persons with SCI to determine which preventative strategies are realistic for them to implement, based on their life circumstances, and must help them identify ways to integrate these preventative strategies into daily schedules.25
Given the significant personal and societal consequences of pressure ulcers, it is prudent to understand the existing evidence for prevention and treatment interventions, and to identify future directions for research on pressure ulcer management. Prevention and treatment interventions for pressure ulcers post-SCI will be examined in the following review article.
Methods
A systematic review of all relevant literature published from 1980 to 2007 was conducted using multiple databases (MEDLINE/PubMed, CINAHL, EMBASE, PsycINFO) and our standardized SCIRE methodology.26 Search terms included pressure ulcers (skin sores, decubitus ulcer, ischemic ulcer, bed sores, or skin sores) paired with spinal cord injuries, tetraplegia, paraplegia, or quadriplegia. Over 17,000 titles were reviewed for version 1 of the SCIRE project (http://www.icord.org/scire). For the current review, 26 articles met inclusion criteria, consisting of English language interventional studies with a sample size of 3 or greater, and with at least half the study population having an SCI.
A quality assessment was conducted for each article, using either the PEDro27 assessment tool (for RCTs) using questions 2 through 10, or the Downs and Black28 tool for nonrandomized studies. With the PEDro tool, the higher the score, the better the quality of the study, with the following cutpoints used: 9 to 10, excellent; 6 to 8, good; 4 to 5, fair; and less than 4, poor. The Downs and Black28 tool consists of 27 questions that evaluate the level of (1) reporting, (2) external validity, and (3) internal validity (both bias and confounding). It was modified slightly because of ambiguity in the last question; thus, the highest score any reviewed article could receive was 28, with a higher score indicating higher methodologic quality.28 Five levels of evidence, based on a modified Sackett scale, were used to summarize the data29 (table 2).
Table 2. Levels of Evidence
| Levels | Evidence |
|---|---|
| Level 1 | RCTs with a PEDro score ≥6 |
| Level 2 | RCTs with a PEDro score <6, cohort and non-RCTs |
| Level 3 | Case-control studies |
| Level 4 | Pre-post or postinterventions and case series |
| Level 5 | Case reports, clinical consensus, or observational studies |
The results of the quality assessment and a brief study summary were tabulated for each study as follows: PEDro or Downs and Black28 score, study design, inclusion/exclusion criteria (when stated), a brief summary of intervention outcomes, and study results.
Direct Versus Indirect Indicators of Prevention
It should be noted that outcome assessment for pressure ulcer prevention can be measured via either direct or indirect means. That is, the effectiveness of preventative interventions can be determined by direct indicators, like pressure ulcer incidence, or by indirect indicators, like IT pressure mapping or PTCo2 levels.
Prevention of Pressure Ulcers
Electrical stimulationElectrical stimulation has been used since the 1960s to enhance the healing of various chronic wounds, including pressure ulcers in both able-bodied people and persons with an SCI.18, 30, 31 Given that the primary cause of pressure ulcers is felt to be externally applied pressure over bony prominences like the ischial tuberosities,9 investigators have studied the role of electrical stimulation for reducing ischial pressures and redistributing seating interface pressures, both of which might assist with pressure ulcer prevention32 (table 3).
Table 3. Electrical Stimulation
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Bogie and Triolo,33 2003, USA D&B=13 | Inclusion: low cervical or thoracic level SCI (C6–T12); more than 6 months postinjury; skeletal and cognitive maturity; upper motor neuron injury; ASIA impairment scale grade: for low cervical/high thoracic injuries (C6–T4): A, B, or C to mid to low thoracic injuries (T4–T12): A or B. Exclusion: cardiac arrhythmia or pacemaker-fitted; acute orthopedic problems; acute medical complications; frequent urinary tract infections; current open pressure sores; immunodeficiency; acute chronic psychologic problems or chemical dependency; seizure disorder; pregnancy. | Pre-post: recruited 7 men and 1 woman who ranged in age from 27 to 47y and had ASIA scores ranging from 56 to 113.4. All 8 patients with SCI participated in an exercise regimen that included 3 different stimulation patterns. The duration of exercise was varied over the 8-wk training period (15–30min [wk 1] up to 120 minutes [wk 7/8]) as the muscles became conditioned. | Interface pressure. | 1.Overall, with NMES, mean interface pressure showed no significant differences between baseline and postexercise levels. 2.Mean ischial region interface pressure had a uniform tendency to decrease postexercise assessment (P<.01). |
Bogie and Triolo33 studied changes in interface pressure distribution at the support/surface interface after 8 weeks of NMES delivered via an implanted neuroprosthesis for standing and transfers. The neuroprothesis consisted of bilateral epimysial electrodes, a multichannel stimulator, and bilateral gluteal electrodes. After healing associated with the implantation, subjects began 8 weeks of NMES exercise using 3 different stimulation patterns. Duration and modes (eg, unresisted vs resisted) of exercise changed from 15 to 30 minutes (week 1) up to 120 minutes (week 7 or 8) as muscles became conditioned. After 8 weeks of NMES, mean ischial regional interface pressure uniformly decreased postexercise assessment (P<.01).
Research also has shown that, with increasing interface pressures over bony prominences, regional blood flow is adversely affected.9, 30 Electrical stimulation has been shown to change blood flow to skin and muscle. It is believed that, by increasing regional blood flow, tissue viability is enhanced, thereby assisting with pressure ulcer prevention9, 18, 32, 33, 34 (table 4).
Table 4. Effects of Electrical Stimulation on Regional Blood Flow
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Bogie and Triolo,33 2003, USA D&B=13 | Inclusion: low cervical or thoracic level SCI (C6–T12); more than 6 months postinjury; skeletal and cognitive maturity; upper motor neuron injury; ASIA impairment scale grade: low cervical/high thoracic injuries (C6–T4): A, B, or C to mid to low thoracic injuries (T4–T12): A or B. Exclusion: cardiac arrhythmia or pacemaker-fitted; acute orthopedic problems; acute medical complications; frequent urinary tract infections; current open pressure sores; immunodeficiency; acute chronic psychologic problems or chemical dependency; seizure disorder; pregnancy. | Pre-post: recruited 7 men and 1 woman who ranged in age from 27 to 47y and had ASIA scores ranging from 56 to 113.4. All 8 patients with SCI were included in the following study. Electrical stimulation was delivered via an implanted neuroprosthesis, which included gluteal electrodes. Eight weeks of conditioning exercises followed. | PTCo2. | 1.Baseline mean unloaded tissue oxygen levels increased by 1% to 36% at postexercise assessment for 5 of 8 subjects. 2.Differences between baseline and postexercise tissue oxygen levels were not statistically significant. |
| Mawson et al,35 1993, USA D&B=10 | Inclusion: inclusion criteria not specified; however, those selected ranged in age from 18 to 57y. Ulcer sites were as follows: sacral (n=7), heel (n=2), other (n=1). Ulcer grade ranged from 1 to 4. Exclusion: not specified. | Case series: 29 patients with SCI lying on egg crate mattresses were included in the study. Sensor was applied to the skin at approximately the second sacral segment along the midline, using a 2-sided airtight seal. 2 electrodes and conductive sponges, measuring 4 cm in diameter, were used to administer electrical stimulation. | PTCo2. | 1.Experiment 1: subsequent experiments were performed using 75V, because no additional effect on PTCo2 was seen when 100V were used. 2.Experiment 2: compared to final baseline PTCo2 reading (mean ± SD) of 49±2mmHg, the level reached at the 30-min period of HVPGS was 66±18mmHg—35% higher (P<.001). 3.The level fell slightly after the first 15 minutes poststimulation (P<.001). 4.Experiment 3: no change in PTCo2 with simulated HVPGS. 5.Experiment 4: no significant differences were observed (P=.66 in all comparisons) when experiment 2 and 4 results were compared. |
Mawson et al35 administered HVPGS to 29 subjects lying supine. Baseline PTCo2 levels were compared with levels reached at the end of 30 minutes of HVPGS. The authors found that the PTCo2 level at the end of stimulation was 66±18mmHg or 35% higher (F=39.42, P<.001).
Bogie and Triolo33 administered 8 weeks of NMES to 8 subjects using implanted gluteal electrodes. They then assessed unloaded gluteal tissue blood flow by measuring local PTCo2. While the results did not achieve statistical significance, baseline mean unloaded PTCo2 levels increased by 1% to 36% in 5 of the 8 subjects.
Conclusions
There is limited level 4 evidence that electrical stimulation decreases ischial pressures post-SCI. There is level 4 evidence that electrical stimulation may increase blood flow at sacral and gluteal areas post-SCI.
Pressure Relief Practices
Current clinical practice regarding pressure relief education is based on the premise that the absence of regular pressure relief places the person with SCI at a higher risk for pressure ulcers.3 The techniques chosen for pressure relief depend on the physical and cognitive status of the individual. When a manual weight shift cannot be performed, 1 alternative is a mechanical reclining or power tilt wheelchair. It has been suggested that pressure relief optimally should be performed every 15 to 30 minutes for 30 to 120 seconds, depending on the technique1 (table 5).
Table 5. Pressure Relief Practices
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Coggrave and Rose,36 2003, United Kingdom D&B=14 | Inclusion: no specific inclusion criteria were documented; however, patients selected were 13 women and 33 men who ranged in age from 20 to 83y. No other details provided. Exclusion: not specified. | Case series: 46 patients with SCI in a retrospective chart review. | Effect of pressure relief on TCPo2. | 1. Mean duration of pressure relief required to raise tissue oxygen to unloaded levels was 1min 51s (range, 42s-3.5min). |
| 2. Leaning forward with elbows, or chest on knees, leaning from side to side or tilting back in wheelchair to 65° or higher all were effective for pressure relief (raising TCPo2 to unloaded levels) and were more easily sustained for most patients than a pressure lift. | ||||
| 3. Resulted in a change in practice at the seating clinic. | ||||
| Henderson et al,37 1994, USA D&B=12 | Inclusion: specific inclusion criteria not provided; however, subjects were from 22 to 67 years old, 9 were men and 1 was a woman. No further details provided. Exclusion: not specified. | Case series: 10 subjects with SCI sat upright in a wheelchair in the neutral position; tipped backward at 35° and 65°; assisted to lean forward (>45° from wheelchair backrest). Pressures were measured at IT (point pressure) and over a circumscribed area around the IT. | Pressure levels. | 1. Average pressure in the resting seated position was 189mmHg for point pressure area and 114mmHg for the circumscribed area. |
| 2. When subjects were in the 65° backward tipped position, there was a 47% reduction in maximum point pressure and a 36% reduction in circumscribed area pressure (P<.05). | ||||
| 3. In the leaning forward position, there was a 78% reduction in maximum point pressure and a 70% reduction in circumscribed area (P<.05). |
A retrospective chart review of 46 subjects with an SCI seen in a seating clinic noted that approximately 2 minutes of pressure relief was required to raise transcutaneous oxygen tension to unloaded levels for most subjects.36 The required duration of pressure relief was more easily sustained by the subjects leaning forward or side to side, or having the wheelchair tipped back by 65° or higher compared with a vertical lift for pressure relief.
Henderson et al37 pressure-mapped 10 subjects with SCI at the IT and over a circumscribed area around the IT. Subjects were placed in 4 different positions: sitting upright at rest in a neutral position, tipped back 35° from vertical, tipped back 65° from vertical, and leaning forward as far as was comfortable. When the subjects were in a forward-leaning and 65° tipped-back position, there was a statistically significant pressure reduction at the IT and over the circumscribed area (forward lean: 78% reduction at IT, 70% reduction over circumscribed area [P<.05]; 65° tipped back: 47% reduction at IT, 36% reduction over circumscribed area [P<.05]); this compared with a 27% reduction at the IT, and to a 17% reduction over the circumscribed area (P>.05) in the 35° tipped-back position. While the pressure reduction for the 65° tipped-back position was statistically significant, it was not felt by the authors to be optimal to prevent pressure ulcer development.
These findings suggest that a forward-leaning position is the most effective pressure relief technique, if sustained for an appropriate period. Leaning side to side, having the wheelchair tipped back by 65° or more, or doing a pressure relief lift for an appropriate length of time (ie, 2min) also was effective. The traditional pressure relief lift (15–30s) was ineffective at reducing tissue oxygen levels to unloaded levels.
Conclusions
There is level 4 evidence to support the forward-leaning position as the most effective method of pressure relief. There is level 4 evidence that a 15-second to 30-second vertical lift is not effective.
Wheelchair Cushion Selection
Wheelchair cushion selection is important when an individual with an SCI is prescribed a wheelchair. Bogie et al9 noted that 47% of pressure ulcers occurred over the IT and sacrum and were therefore more likely to have been initiated while the patient was seated. When optimizing wheelchair cushion selection for a person with SCI, the degree of pressure reduction and redistribution38 and temperature effects39, 40 along with individual characteristics such as level of SCI (paraplegia or tetraplegia), pressure relief abilities, transfer techniques, and lifestyle must be considered.38, 41 Seat cushioning can be made from various materials; it may be static or dynamic (typically accomplished with air bladders)38, 41; and it may be incorporated into upright, powered tilt, or reclined wheelchairs (table 6).
Table 6. Wheelchair Cushion Selection
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Burns and Betz,42 1999, USA D&B=17 | Inclusion: ASIA grade A or B tetraplegia; use of power tilt-in-space wheelchair; 18 or older. Those selected ranged in age from 24 to 65 years. All injuries were cervical (C4–C6) and all were 0.5 to 31y postinjury. Exclusion: current skin breakdown; history of surgical resection to any portion of the femur; hip flexion passive range of motion less than 90° | Non-RCT: 3 wheelchair cushions were tested: dry flotation, gel, and dynamic (ErgoDynamic). The dynamic cushion was composed of 2 air bladders, which alternated between inflation and deflation. One bladder was shaped like the letter H (H-bladder) with the longer portions under the femurs. The other bladder (IT-bladder) filled the remainder of the cushion and supported the ITs. Subjects (n=16) had their regular cushions removed and replaced with one of the test cushions. | Interface pressure at IT was assessed with Clinseat seating interface pressure sensor placed on the test cushion. | 1.IT pressure for the dry flotation cushion in a tilted position was similar to that for the IT pressure during H-bladder inflation in an upright position (74 vs 71mmHg, P=.91), whereas the gel cushion had significantly higher IT pressure in the tilted position (71 vs 86mmHg, P<.05). 2.Pressure was significantly higher in the upright position than in the tilted position for both the dry flotation and the gel cushion (P<.001) and for IT-bladder (157±45) versus H-bladder inflation (71±30, P<.001) with the dynamic cushion. 3.In upright sitting position, the dry flotation cushion showed lower pressures than the gel cushion (111 vs 128mmHg, P<.01), whereas the IT bladder (157mmHg) had greater pressure than both (P<.001). |
| Brienza and Karg,43 1998, USA D&B=14 | Inclusion: inclusion criteria not specified; however, all subjects were between the ages of 21 and 52y and had a BMI 17–32.3kg/m2. Exclusion: not specified. | Case series: 12 participants assessed on 3 different surfaces (flat foam, or initial contour and a final optimized foam contour) with the force sensing array pad between the cushion and buttocks. Compared subjects with SCI to a seniors group. | Tissue stiffness, deformation (depth), interface pressure, BMI. | 1.Depth values for the SCI group were greater for the final vs the initial contour from 37.9±6.5mm to 52.5±11.5mm (P<.001), as was the case for the elderly group (P<.001). 2.The mean max depth of the final contour was deeper for the SCI group than for seniors (P=.016). 3.Mean pressure values for initial and final cushions were significantly less than for flat cushions (P=.006, P=.003, respectively), but not for the initial versus final cushions (P=.80). 4.In general, mean and peak pressures were greater for the subjects with SCI than for elderly subjects. 5.BMI was significantly related to peak and mean pressure values. |
| Seymour and Lacefield,39 1985, USA D&B=13 | Inclusion: specific inclusion criteria not stated; however, the age range of the group was 16 to 35y; the weight of the group ranged from 40.6 to 72.5kg. No other details provided. Exclusion: not specified. | Case-control: 20 subjects (10 subjects with SCI and 10 able-bodied controls) participated in the study. Seven commercially available cushions and 1 experimental cushion were evaluated for each subject. | Temperature and pressure effects (pressure evaluation pad) were assessed for each cushion. Subjects were asked to rate each cushion for appearance, handling, and suitability for purchase. | 1.Greatest pressure was seen under the soft tissue areas of most subjects, with no significant differences between cases and controls. 2.Temperatures were lowest for gel, water, and air cushions and highest for alternating pressure and foam cushions. 3.SCI group: GP under a bony area occurred most often with the Spenco cushion (90.10±8.75); controls: corresponding GP occurred most often with the Tri-Pad (89.20±11.40), indicating that these cushions did not compare favorably to others. 4.While there was wide variability in pressure measurements in individual subjects (SD=12.21mmHg), the air-filled (Bye Bye Decubiti) had the best pressure readings. 5.Appearance (83%) and handling (73%) were related to purchase decisions. |
| Garber,38 1985, USA D&B=8 | Inclusion: inclusion criteria: (1) a history of pressure ulcers, (2) an existing ulcer, or (3) the need to correct a pressure ulcer after surgery. A total of 207 men and 44 women were included in the study. Exclusion: not specified. | Case series: 251 subjects with SCI were selected for inclusion. An assessment of pressure distribution for 7 cushions was undertaken. | Seated pressure distribution using a pressure evaluation pad. | 1.The air-filled cushion (Roho, which was 1 of 2 used) produced the greatest pressure reduction in 51% of the subjects. 2.A foam cushion (the stainless comfy hard cushion) was effective for only 18% of the subjects, even though it was the second most frequently prescribed cushion. 3.More subjects with quadriplegia received the Rohos than subjects with paraplegia (55% vs 45%), while more subjects with paraplegia were prescribed the Jay cushion—a combination of foam and flotation materials (19% vs 7%). |
| Makhsous et al,41 2007, USA D&B=18 | Inclusion: for those with paraplegia (T4 or lower): able independently to do pushups for pressure relief. For the able-bodied: no history of neuromuscular disorders. Overall, 45 men and 15 women participated. Exclusion: degenerative disorder of the spine; history of injury of or surgery to the pelvis, hip joint, or thigh; hip contractures; severe pain, spasms; or psychologic concerns preventing proper cooperation. | Case-control: 60 subjects (40 cases: 20 subjects with paraplegia, 20 subjects with tetraplegia, 20 controls) were exposed to two 1-hour protocols: alternate (sitting posture was dynamically alternated every 10min between normal and partially removed ischial support [WO-BPS] postures), normal (normal posture plus pushups), performed by subjects themselves or using a Hoyer lifti every 20 minutes. | Interface pressure at the back rest and seat, assessed using a pressure mapping device. | 1.Normal posture: the anterior portion of the seat cushion had a larger contact area for those with tetraplegia compared with those in the other 2 groups. Those with an SCI had a larger contact area in the middle portion of the seat cushion. 2.At the posterior portion of the seat where ischial tuberosities are usually positioned, average pressure was highest for subjects with paraplegia (88.9±4.2mmHg). 3.When looking at the total contact area on the seat cushion in the WO-BPS posture position, average pressure for those with tetraplegia was higher than it was for the other 2 groups (P<.001). 4.Overall, the total contact area on the posterior portion of the cushion was less for the WO-BPS posture for all groups, as was peak interface pressure and average pressure, with the greatest decrease seen in the group of subjects with tetraplegia (P<.001). 5.Average push-up time ± SE (ie, time of pressure relief) was 49.0±2.8s for those with paraplegia. |
In the study conducted by Burns and Betz,42 3 wheelchair cushions were tested: dry flotation (ROHO High Profile),a gel (Jay 2),b and dynamic (ErgoDynamic),c the last consisting of 2 air-filled bladders, the H-bladder (shaped like the letter H) and the IT-bladder. These were compared under high pressure conditions (upright sitting or IT-bladder inflated) and low pressure conditions (seat tilted back 45° or H-bladder inflated). When the pressure placed on the ischial tuberosities was analyzed, the pressure was higher during upright sitting than in the tilted back position for both the dry flotation and the gel cushion (P<.001), with the dry flotation cushion providing more pressure relief than the gel cushion during upright sitting (112 vs 128mmHg, P=.01). Mean pressure with the IT-bladder inflated cushion (157mmHg) was greater than upright pressures for either the dry flotation or gel cushions (111 and 128mmHg, respectively; P<.01). Most importantly, ischial tuberosity pressure for the dynamic cushion during H-bladder inflation in an upright position was comparable to the pressure for the dry flotation cushion in a tilted back position (71 vs 74mmHg, P=.91) and significantly less than the pressure obtained with the gel cushion (71 vs 86mmHg, P<.05).
Brienza and Karg43 had 12 subjects with SCI sit on 3 different surfaces (flat foam, initial contour, and final contour) while measuring interface pressures using a pressure-sensing pad. Subjects with SCI had greater depth values than elderly subjects without SCI (N=30), and the mean maximum depth of the final contour was deeper for the group with SCI, suggesting that pressure distributions for the subjects with SCI were more sensitive to support surface characteristics than for the elderly subjects without SCI.
Seymour and Lacefield39 evaluated 8 cushions (gel: Jobst pad,d Spencoe; water: Jobst cushiond; air-filled: Bye Bye Decubiti,f Alternating Pressureg; foam: Luxaire,h Durafoam,g Tri-Padg) for pressure, temperature effects, and subjective factors influencing cushion purchase. While data indicated a wide variability in pressure measurements in individual subjects seated on the 8 cushions, the air-filled cushion (Bye Bye Decubiti) had the best pressure readings. The alternating pressure and foam cushions had consistently higher temperature readings across both groups, which could increase tissue susceptibility to pressure ulcer formation.39, 40
Garber38 evaluated 7 cushions (air-filled: Bye Bye Decubiti, Roho; flotation: Aqua Seat, Stryker Gel; foam: Stainless Comfy Hard Foam, Temper Foam; foam/flotation combination: Jay) based on the amount of pressure reduction achieved, and noted how frequently each cushion was prescribed to subjects with quadriplegia and paraplegia. The Roho cushion produced the greatest pressure reduction in most subjects (51%) and was prescribed more often for subjects with quadriplegia than with paraplegia (55% vs 45%).
Makhsous et al,41 in a case-control study, exposed subjects to two 1-hour protocols: alternate, where sitting posture was alternated dynamically every 10 minutes between normal (sitting upright with ischial support) and sitting upright with partially removed ischial support and lumbar support, and normal (normal posture plus pushups performed every 20 minutes). These investigators found that the anterior portion of the seat cushion had a larger contact area among those with tetraplegia compared with those in the other groups. It also was determined that those with an SCI had a larger contact area in the midportion of the seat cushion. There were significant differences between the groups when looking at the average pressure over the whole seat (P<.001) and the total contact area on the seat cushion. Sitting upright with partially removed ischial support and lumbar support posture, the average pressure for the tetraplegia group was higher than it was for the other groups (P<.001). Most importantly, the total contact area on the posterior portion of the cushion was less for sitting upright with partially removed ischial support and lumbar support posture for all groups. As well, peak interface pressure was lower for all groups, with the greatest decrease from normal posture seen in the tetraplegia group. The average pressure increased on the anterior and middle portion of the cushion in all groups.
The results of these studies and the apparent interindividual variation inherent in those with an SCI (eg, paraplegia vs tetraplegia) support the practice of specialized pressure-mapping assessments to assist with individualized wheelchair cushion prescriptions. None of these studies included direct evidence of pressure ulcer prevention associated with a particular practice or cushion type. Objective findings, such as pressure mapping together with the clinical knowledge of the prescriber and the clients' subjective reports, need to be considered when prescribing a wheelchair seat cushion for an individual with an SCI, so as to minimize pressure ulcer risk factors.
Conclusions
There is level 3 evidence that various cushions or seating systems (eg, dynamic vs static) are associated with potentially beneficial reductions in seating interface pressure or pressure ulcer risk factors, like skin temperature.
Thickness of Lumbar Support
Shields and Cook44 discussed the role that spinal deformities, like kyphosis, may play a role in the formation of pressure ulcers in persons with chronic SCI. In previous research on nondisabled subjects, they had demonstrated that the addition of lumbar support reduced highest seated buttock pressure (>.915kg/cm2) and was associated with a change in pelvic tilt. If those findings were to hold true in the SCI population, the authors noted that this could lead to ways to assess postures while seated for appropriate pressure distribution44 and augment electric wheelchair backrests by adding an automated lumbar support system, potentially providing a mechanism for continuous pressure shifts.
In the Shields and Cook44 study, 18 SCI and 18 able-bodied subjects were studied to test the effects of varying lumbar support thickness (0, 2.5, 5.0, 7.5cm) on seated buttock pressures at the ischial tuberosities. Within the SCI group, a 2% decrease in mean highest seated buttock pressure (>.915kg/cm2) was seen with the 7.5-cm lumbar support compared with a 90% reduction within the able-bodied group. With the 5-cm and the 2.5-cm lumbar support, there was an increase in mean high pressure of 13% and 12%, respectively, compared with reductions in the able-bodied group of 80% and 25%, respectively. Surprisingly, the findings showed that the addition of lumbar support to wheelchairs had a minimal effect on reducing highest seated buttock pressure at the ischial tuberosities of subjects with chronic SCI of 3 years or more (table 7).
Table 7. Thickness of Lumbar Support
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Shields and Cook,44 1992, USA D&B=19 | Inclusion: 3 years or more post-SCI injury; complete motor deficit below the lesion level; controls included 7 men and 11 women, ranging in age from 21 to 52y. Cases ranged in age from 21 to 38y, with 13 men and 5 women. Exclusion: no pressure ulcers; no spinal stabilization of the lumbar spine; no severe spinal scoliosis. | Case-control: all 36 subjects with an SCI were seated onto a pressure-sensing transducer incorporated into an adjustable chair. The output was calibrated so that 8 pressure intervals were displayed. | Pressure distribution. | 1. Significantly reduced pressures were seen with greater thickness of lumbar supports (2.5–7.5cm) for controls, but not for those with SCI (P<.001). |
| 2. The highest-pressure areas were greater for SCI group (P<.05) than controls for all lumbar support conditions. | ||||
| 3. The mean area of lowest pressure for all support conditions was significantly less for SCI than controls. | ||||
| 4. SCI group had significantly lower pelvifemoral angles than controls in all lumbar support conditions (P<.05). |
Conclusions
There is level 3 evidence that adding lumbar support to the wheelchair of those with a chronic SCI has a negligible effect on reducing seated buttock pressures at the IT. As a consequence, it is unlikely to have a role in pressure ulcer prevention post-SCI.
Specialized Seating Clinics
Education regarding the prevention of pressure ulcers post-SCI includes an emphasis on taking personal responsibility for maintaining healthy skin through personal care, inspection of skin, pressure relief, and the correct use of prescribed equipment.9 The incorporation of seating clinics into both inpatient and outpatient rehabilitation programs has been shown to reduce the incidence of pressure ulcers and readmission rates as a result of pressure ulcers.45 Seating clinics not only provide education but also make recommendations for appropriate seating systems based on interface pressures, thermography, and assessments of tissue viability. Verbal and visual feedback are provided to the individual with an SCI, and active participation is encouraged36, 45, 46 (table 8).
Table 8. Specialized Seating Clinics
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Kennedy et al,46 2003, United Kingdom D&B=18 | Inclusion: all who participated had 1 or more pressure ulcers. Those who participated ranged in age from 16 to 74y; 37 were men and 13 women. Participants had either paraplegia or tetraplegia. Participants were divided into 3 groups: group 1 to 30 who attended a seating assessment before their first NAC assessment, group 2 to 11 who attended SSA between their first and second NACs, and group 3 to 9 who did not receive SSA because of their methicillin-resistant Staphylococcus aureus status. Exclusion: not specified. | Cohort: 50 subjects with an SCI participated. Postural assessment took place while the individual adopted their usual posture in the wheelchair. Physical alignment was documented and correct positioning of adjustable parts of the chair was checked. Any abnormal posture then was checked for correct alignment; set-up of the seating was adjusted, as required. | Skin management subscale of the NAC to assess skin management rehabilitation. | 1.Significant differences were identified between groups 1 and 3 for both NAC 1 (P<.05) and NAC 2 (P<.01). 2.Skin management to be achieved scores were significantly lower for patients who had attended specialized SSA before their first NAC at both time points. 3.Significant differences also were observed between the skin management to be achieved scores at the first and second NAC within all groups: group 1 (P<.001), group 2 (P<.01), and group 3 (P<.01). |
Kennedy et al46 studied 50 patients with an SCI participating in a comprehensive rehabilitation program. The participants were divided into 3 groups—group 1 (attendance at seating assessment clinic prior to NAC administered within 1 month of mobilization), group 2 (attended seating assessment clinic between their first and second NAC), and group 3 (no attendance at seating assessment clinic)—to determine whether attendance at a seating assessment clinic would improve skin management ability, as evidenced by lower to be achieved scores on the skin subscale of the NAC. The NAC was administered within 1 month of mobilization and on admission to the predischarge ward.46 Optimal timing of attendance at the seating assessment clinic also was studied. Results indicated significant differences between group 1 and group 3 both at 1 month of mobilization (P<.05) and on admission to the predischarge ward (P<.01) assessments. Skin management to be achieved scores were significantly lower among participants who attended a seating assessment clinic before their first NAC at both time points. Significant differences also were observed between to be achieved scores at first and second NAC within all groups: group 1 (P<.001), group 2 (P<.01), and group 3 (P<.01).46
Conclusions
There is level 2 evidence showing that early attendance at specialized seating assessment clinics increases the skin management abilities of persons post-SCI. Attendance at a seating assessment clinic is an adjunct to the skin management abilities learned during a comprehensive rehabilitation program.
Education
Education programs for pressure ulcer prevention designed for persons with SCI provide knowledge and emphasize specific behaviors, which, when adhered to on a regular basis, are intended to reduce the risk of pressure ulcer occurrence.9, 47, 48 Most education is delivered as part of an inpatient rehabilitation program when patients and families are adjusting to a diagnosis of SCI and also during a time of potential information overload that may compromise an appreciation of knowledge and behaviors they will need to prevent pressure ulcers over the course of their lifetimes.24, 48 With shorter lengths of stay, the time available for education is also reduced, and persons with SCI are being discharged with potentially less information and fewer opportunities for reinforcement of acquired knowledge.24 While pressure ulcer prevention education is a key part of rehabilitation, there are few data available on the specific educational needs required by persons with SCI at risk for pressure ulcer development48 (table 9).
Table 9. Education
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Garber et al,23 2002, USA PEDro=5 | Inclusion: those with an SCI, regardless of age, ethnicity, level of function, or independence. The average age of subjects was 53y, and the average time since injury was 17y. Injuries ranged from cervical to lumbar level. Exclusion: cognitive impairment (not able to understand the consent form or the educational material). | RCT: 41 subjects participated in the study; 39 had an SCI and 2 had MS. Those in the treatment group received four 1-hour sessions of structured education on the prevention and management of PU. After discharge, subjects were followed for 2 years. The control group also was followed, but no information (other than standard education) was given regarding preventative practices. | Demographic and Health Information Questionnaire; Pressure Ulcer Knowledge Test; Multidimensional Health Locus of Control Scale; Health Beliefs Questionnaire. | 1.An improvement in the pressure ulcer knowledge test was noted for both groups on discharge from hospital, but it was significantly different between the groups (P<.03). Those in the treatment group gained more knowledge about preventing PU. 2.No significant intergroup differences were noted on the Multidimensional Health Locus of Control scale or the Health Beliefs Questionnaire at discharge. 3.At 2 years posttreatment, although both groups retained the knowledge, the level of knowledge retained in the control group was substantially below that of the treatment group, 60.8% vs 68% on the Pressure Ulcer Knowledge Test. |
In an RCT conducted by Garber et al23 while still in the hospital, those in the treatment group (n=20) were provided with four 1-hour sessions of structured education on the prevention and management of pressure ulcers. Education presented at the sessions included information regarding nutrition, pressure redistribution surfaces for the bed and wheelchair, and pressure ulcer etiology. The control group (n=21) received only standard education regarding preventative practices. After discharge, the groups were followed for 2 years.
Improvement on the pressure ulcer knowledge test was noted in both groups on discharge from the hospital; however, it differed significantly between the groups (P<.03), with those in the treatment group gaining more knowledge about preventing pressure ulcers. No significant differences were noted on the multidimensional Health Locus of Control Scale and the Health Beliefs Questionnaire between the 2 groups at discharge. Two years posttreatment, it was noted that both groups had retained most of the knowledge they had been given during their hospitalization, but the level of knowledge retained by the control group was substantially below that of the treatment group: 60.8% versus 68% on the pressure ulcer knowledge test.23
Conclusions
There is level 2 evidence that providing enhanced pressure ulcer prevention education is effective at helping persons with SCI gain and retain this knowledge. However, no evidence exists regarding whether this enhanced education results in a reduction in pressure ulcer formation.
Behavioral Contingencies
Despite the knowledge available on pressure ulcers and prevention strategies, pressure ulcers continue to occur in persons with SCI.19 Little information exists about why certain individuals do not practice the health-sustaining behaviors that they are taught and that are required to optimize skin care and prevent pressure ulcers.4, 24 There is a subset of patients who experience recurrent pressure ulcers because of nonadherence to recommended prevention strategies. Patients with recurrent pressure ulcers may lack incentives to follow prevention behaviors.4 What is not known is whether rewarding positive preventative strategies reduces the severity or likelihood of a patient developing pressure ulcers.
Jones et al4 conducted 2 separate small studies. The behavioral intervention in the first study (n=6) consisted of a health plan, clinic visits, and financial rewards ($50 a visit as long as ulcer-free), all of which were implemented at the same time. In the second study (n=3), a health plan and visits were implemented in phase 1 of the study; payments were added if a patient experienced new skin problems. Results from the first study revealed that average PUSH scores were lower by 10.5 points from baseline at the end of the intervention phase. No hospitalizations were required and, ultimately, costs during the intervention phase went from $6263 (United States) to $235 (United States). In the postintervention phase, 3 subjects were able to maintain lower PUSH scores and 3 were not. In the second study, mean PUSH scores decreased from baseline by 8.3 points (visits only) and a further 3.1 points when payments were added. PUSH scores rose again in 2 out of 3 participants during the postintervention phase. The mean number of hospitalizations dropped from 1.67 (baseline) to 0.33 (intervention and postintervention; table 10).
Table 10. Behavioral Contingencies
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Jones et al,4 2003, USA D&B=11 | Inclusion: traumatic SCI; adults; history of repeated episodes of treatment for severe pressure ulcers; paraplegia. Those included had 1 or more pressure ulcer. Exclusion: not specified. | Pre-post: 2 studies were conducted. In study 1, 6 SCI patients participated; in study 2, 3 participated. Study 1 behavioral intervention: 3 primary components: health plan, clinic visits, and financial rewards. Study 2 behavioral intervention: 2 treatment components were implemented (health plan and visits) during the initial phase. Phase 2 began after the patient began to experience skin problems (included visits plus payment). | Severity of pressure ulcers was recorded at each phase; ulcer severity was classified using PUSH tool. | Study 1: |
| 1. Average PUSH decreased from baseline by an average of 10.5 points per participant (range, 5.4–19.2). | ||||
| 2. Six patients were hospitalized (not during the intervention) a total of 16 times during baseline for treatment of pressure ulcers. | ||||
| 3. No hospitalizations were noted during the intervention phase. Compared with the baseline phase, the average monthly cost of care decreased from $6262/participant to $235 (United States). | ||||
| Study 2: | ||||
| 1. Mean PUSH scores decreased from baseline by 8.3 points (visits only) and a further 3.1 points (visits plus payments phase). | ||||
| 2. Mean number of hospitalizations decreased from 1.67 (baseline) to 0.33 (intervention and postintervention phase). |
Conclusions
There is very limited level 4 evidence to suggest that the introduction of behavioral contingencies is associated with a reduction in pressure ulcer severity and decreased health care costs.
Telerehabilitation and Pressure Ulcer Management
Impaired mobility and distance to specialized SCI centers often make follow-up care difficult for persons with SCI.49, 50 Telerehabilitation has the potential to deliver medical rehabilitation, nutritional, and psychosocial elements of health care at a distance using telecommunication technology, thereby facilitating continuity of care.49 Pressure ulcer management is 1 area in which telerehabilitation currently is being used51 (table 11).
Table 11. Telerehabilitation and Pressure Ulcer Management
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Phillips et al,52 1999, USA D&B=12 | Inclusion: all who participated had 1 or more pressure ulcers. Patients ranged in age from 18 to 58y. There were 9 men and 2 women. Level of injury ranged from C5 to L12. Exclusion: not specified. | Case-control: 37 patients with SCI were asked to participate. Video conferencing was used to assist patients in treating and monitoring pressure ulcers. Patients were divided into 3 groups (telephone, video, and standard care). | Number of pressure ulcers, ED visits, hospitalizations, and doctor visits annually; employment rate. | 1.Overall, it was found that the video group reported the largest number of ulcers, followed by the standard care group and the telephone group. 2.The standard care group reported the lowest number of ED visits, hospitalizations, and health care provider visits. 3.The numbers of visits were similar for the other 2 groups. 4.Of each group, 55% had no hospitalizations during the study period. It also was noted that 26% of the subjects had returned to work by 6 months after injury. |
| Vesmarovich et al,51 1999, USA D&B=10 | Inclusion: specific inclusion criteria not recorded. Subjects were men between the ages 38 and 78y and had either a cervical or thoracic spine injury. Exclusion: not specified. | Case series: 8 subjects participated. The outpatient nurse, using the Picasso Still Image Videophone, conducted weekly telerehabilitation visits. Subjects and family members received 30min education; equipment was sent home with subjects. Interviews were conducted to determine level of satisfaction. | Development of pressure ulcers. | 1.Subjects were seen approximately 7 times (range, 1–18 visits). 2.Seven of 12 wound sites healed completely; 2 needed surgery. 3.Subjects and family were highly satisfied. |
Vesmarovich et al51 described the use of telerehabilitation delivered via a videophone system that transmitted still images and audio to treat stage III/IV ulcers. While no statistical results were reported, 7 of 12 ulcer sites healed. Phillips et al,52 using the same videophone system, divided SCI participants into 3 groups: information delivered by telephone, information delivered by video, and standard care. The video group had the highest number of identified and/or reported ulcers during the study. The annualized data for emergency department visits, hospitalizations, and health care visits were similar for the video and telephone groups, and were tracked weekly. Hospitalizations and health care visits, tracked every 8 to 12 weeks, were less in the standard care group. Fifty-five percent of each of the 3 groups had no hospitalizations. Repeat emergency department visits and hospitalizations appeared to be driven by a small number of people; no significant differences were noted between the 3 study groups.52
Conclusions
There is level 4 evidence that telerehabilitation does not make a significant difference in the prevention and treatment of pressure ulcers post-SCI.
Treatment of Pressure Ulcers
Electrical stimulation for pressure ulcer healingThe therapeutic effect of electrical stimulation for wound healing has been well documented since the 1960s, especially for wounds not responding to standard forms of treatment.18, 30, 31 Despite the use of electrical stimulation to promote wound healing, there remains a lack of clear understanding about how it works to facilitate tissue repair, although a variety of cellular actions (eg, migration and activation of key cells) have been purported as a mechanism of action.53
Some of the effects of electrical stimulation on wound healing include decreased healing time, increased collagen synthesis, increased wound tensile strength, increased rate of wound epithelialization, and enhanced bactericidal effects.30 Electrical stimulation also has been shown to improve tissue perfusion and reduce edema formation, indirectly stimulating healing by improving oxygen delivery to tissue.53 The literature shows high variability about which type of electric current and application protocol is effective for a specific patient or ulcer type18 (table 12).
Table 12. Electrical Stimulation for Pressure Ulcer Healing
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Griffin et al,54 1991, USA PEDro=7 | Inclusion: patients were men; had complete or incomplete SCI, with a pelvic pressure ulcer; classified between grades II and IV. Exclusion: severe cardiac disease, cardiac arrhythmia or uncontrolled autonomic dysreflexia, or used a pacemaker. | RCT: 20 patients with SCI with pelvic (sacral/coccygeal or gluteal/ischial) ulcers received HVPC or sham HVPC for 1 hour daily for 20 consecutive days. All patients received equivalent dressing changes. Wounds were mechanically debrided as necessary. Efforts were made to relieve pressure, but this was not described. | Pressure ulcer status. | 1. Percentage reduction in the wound surface area exhibited by the HVPC group was greater than sham treatment group at day 5 (P=.03), day 15 (P=.05), and day 20 (P=.05). |
| Adegoke and Badmos,56 2001, Nigeria PEDro=6 | Inclusion: all ulcers were grade IV, and located in the pelvic region; age from 21 to 60y; either quadriplegia or paraplegia; ulcers located in the greater trochanter or sacral region. Exclusion: nonsmokers; otherwise not specified. | RCT: 7 patients with SCI underwent stimulation with interrupted DC and nursing care or sham DC and nursing care; three 45-min treatments once weekly for 4wk. | Surface area of pressure ulcers. | 1.Surface area of grade IV pelvic pressure ulcers of DC group decreased by 22.2% vs 2.6% in sham DC group. 2.Most of the decrease in surface area occurred during the first 2 weeks of the study (DC group, 13.3±14.1, % change, 15.8; sham DC group 15.1±3.6, % change, 1.9). |
| Baker et al,31 1996, USA PEDro=4 | Inclusion: 1 or more pressure ulcers. Age 17 to 76y. SCI, 66 men and 14 women. Injuries either cervical, thoracic, or lumbar. Exclusion: not specified. | RCT: stimulation of A vs B vs MC group originally thought to incorporate stimulation below effective level became the third treatment group when some early therapeutic effect was noted. All remained on their stimulation protocols until their ulcers healed, the physician intervened, or subject withdrew from study. Controls received sham for 4 weeks, then were entered into either A or B stimulation protocol. Electrical stimulation treatment for all subjects consisted of 1.5 hours of stimulation 5d/wk. | Pressure ulcer status. | 1. No statistical differences were noted between the initial or discharge ulcer areas or in the mean healing rates among the 4 treatment groups—A, B, MC, controls. |
| 2. Comparing the descriptive data by classifying them as good or poor healing responses failed to identify any statistically significant differences between these 2 groups. | ||||
| 3. When looking at the good response group, the group A protocol was more effective than either the MC or control protocols (P<.05). No significant differences were found between protocol B and the other treatments. | ||||
| 4. Those in the control group who had wounds healed by either protocol A or B experienced a healing rate greater (43.3%±12.5% change/wk) than during the control period (9.7%±3.4% change/wk). | ||||
| Stefanovska et al,55 1993, Slovenia D&B=14 | Inclusion: no specific inclusion criteria cited; however, all who participated had SCI and 1 or more pressure ulcers. Exclusion: not specified. | Prospective controlled trial: 150 patients with SCI participated. Currents were applied across wounds by a pair of self-adhesive skin electrodes. Low density (DC) group (N=18) treated with low-density DCs (600μA) for 2 hours daily. AC group (n=82) treated with low-frequency pulsed currents for 2 hours daily. Control group (n=50) received conventional treatment (not described) for the first month. | Pressure ulcer status. | 1. The healing rate for the AC group (n=42) was significantly better than the other 2 groups: DC (n=12), control (n=34) (P=.003), after excluding those with very deep, superficial, or long-term wounds. |
Griffin et al54 showed the efficacy of direct HVCP for the healing of pelvic pressure ulcers in subjects with SCI. Compared with a placebo group, the subjects treated with HVPC experienced a greater percentage reduction in wound surface area at day 5 (P=.03), day 15 (P=.05), and day 20 (P=.05). Stefanovska et al55 showed that the healing rate for wounds treated with low-frequency pulsed current was significantly better than for groups treated with direct current or conventional treatment alone (P=.003). Baker et al31 demonstrated that, for ulcers that responded to any form of electrical simulation (good responses), asymmetric biphasic stimulation (group A) was most effective for enhanced wound healing. Wounds that already were exhibiting signs of healing in the control group, with the subsequent addition of either protocol A or B (symmetric biphasic), experienced a greater healing rate (43.3%±12.5% change/wk) versus the control period (9.7%±3.4% change/wk). Adegoke and Badmos56 found that the surface area of grade IV pelvic pressure ulcers treated with interrupted direct current and nursing care decreased by 22.2% versus 2.6% with sham treatment. While there were differences in the type and duration of electric current applied in the 4 studies, all the studies demonstrated that, when used in conjunction with standard wound management, electrical stimulation can accelerate the healing rate of pressure ulcers in patients with SCI.
Conclusions
There is level 1 evidence from 2 RCTs to support the use of electrical stimulation to accelerate the healing rate of stage III/IV pressure ulcers when combined with standard wound management.
Laser Treatment for Pressure Ulcer Healing
Lasers have been used as a therapeutic modality for wound healing since the 1970s. Laser treatments are felt to act during the proliferative phase of wound healing to promote fibroblast activity and increase granulation tissue formation in nonhealing, chronic wounds. Currently the use of lasers to promote wound closure in chronic wounds is not supported by evidence.53 The Consortium for Spinal Cord Medicine1 reviewed the literature on adjunct wound therapies, including laser treatments, and did not identify enough supporting evidence to recommend lasers for the treatment of pressure ulcers in persons with SCI. The 2 studies presented in this article support the conclusion of the consortium (table 13).
Table 13. Laser Treatment for Pressure Ulcer Healing
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Taly et al,57 2004, India PEDro=10 | Inclusion: patients with spinal cord disorders admitted to the rehabilitation ward with pressure ulcers or who developed ulcers during their stay in the ward. Pressure ulcers at stage 2, 3, or 4 were included. Ages from 8 to 65y; 27 men, 8 women. Exclusion: stage 1 ulcer: nonblanching erythema of intact skin; photosensitivity; ulcers from other causes; necrotic tissue in ulcers that would interfere with the application of laser; flask-shaped ulcers that cannot be exposed to laser; pressure ulcers with underlying osteomyelitis; pressure ulcers requiring surgical intervention at first assessment. | RCT: 35 patients with SCI with 64 ulcers. Experimental group received multiwavelength light therapy (gallium-aluminum arsenide laser source) in addition to conventional treatment. For controls, the light therapy source was held over the ulcer after switching off the beam. A total of 14 treatments were given, 1 every other day, 3 times a week. Treatments ended once the ulcer had healed or after the 14 treatment exposures. | Number of ulcers that healed. | 1.Overall, no significant differences were found between the control and treatment groups. In controls, 14 ulcers healed completely compared with 18 in the treatment group (P<.80). 2.The mean time taken to heal was 2.5±2.1wk in the treatment group and 1.8±2.1wk in controls (P<.33). 3.Multiwavelength light therapy reduced the time taken by a small subgroup (n=4) of stage 3 and 4 ulcers to reach stage 2, 2.3±0.5wk; control group (n=5) 4.3±1.5wk (t=2.62, P=.047). |
| Nussbaum et al,58 1994, Canada PEDro=6 | Inclusion: SCI with 1 or more skin ulcer. Ages: 15 to 61y. A total of 16 men and 2 women. Pressure ulcers were located in the cervical, thoracic, or lumbar regions of the body. Exclusion: not specified. | RCT: originally 20 subjects began the study, but only 16 completed it. | Pressure ulcer status. | 1.US/UVC and laser treatment with US/UVC showing greater effect on wound healing than laser or control. Mean percentage of change per week in ulcer size (±1 SD) from day 0 to complete healing for controls (32.4%), US/UVC (53.5%), and laser (23.7%). 2.Several subjects experienced deterioration, with ulcers increasing in size (laser=3, 62%–167% change; control=1, 58% change; US/UVC=1, 1% change). All ulcers healed by the end of the study; the last ulcer to heal in laser group healed by week 20 vs week 6 with US/UVC. |
Taly et al57 studied 35 subjects with an SCI (64 ulcers) using multiwavelength light therapy compared with standard wound care alone. Overall, no significant differences were found between the 2 groups with regard to the number of ulcers healed or the time required for ulcers to heal.
Nussbaum et al58 studied 16 patients with an SCI and compared standard wound care alone with standard care combined with either laser or US/UVC. In this study, laser treatment combined with standard wound care had the least effect on wound healing compared with either standard care or US/UVC. A significant difference was found between the US/UVC and the laser groups, with the US/UVC treatment producing the greater effect on wound healing.
Conclusions
There is level 1 evidence (from 2 RCTs) to suggest that laser treatment has no added benefit in pressure ulcer healing post-SCI over standard wound care alone.
US/UVC for Pressure Ulcer Healing
Houghton and Campbell53 note that both US and UVC have been used in the treatment of chronic wounds. US acts mainly during the inflammatory stage of wound healing to activate the release of chemical messengers from cells, resulting in changes to the amount and strength of scar tissue.53 The bactericidal effects of UVC suggest that it is best used for the treatment of chronic, infected wounds in which there is an excess of surface bacteria or bacteria have become resistant to antibiotic therapy. There is research to support consideration of UVC in the treatment of chronic infected wounds, but therapeutic US has no added benefits when used to treat pressure ulcers.53 The Consortium of Spinal Cord Medicine1 found minimal data specific to the use of US or UVC to treat pressure ulcers in SCI.
In 1 small RCT (N=16), Nussbaum et al58 demonstrated that, compared with standard wound care alone or laser combined with standard wound care, US/UVC plus standard wound care generated a greater effect on wound healing over a shorter period of time. However, as US and UVC were alternated over 5 days and provided in combination to a single treatment group, conclusions cannot be drawn as to the individual effects of either US or UVC (table 14).
Table 14. US/UVC for Pressure Ulcer Healing
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Nussbaum et al,58 1994, Canada PEDro=6 | Inclusion: SCI with 1 or more skin ulcer. Ages: 15 to 61y. A total of 16 men and 2 women. Pressure ulcers were located in the cervical, thoracic, or lumbar regions of the body. Exclusion: not specified. | RCT: Originally 20 subjects with SCI began the study, but only 16 completed it. | Pressure ulcer status. | 1. US/UVC and laser treatment with US/UVC exerted greater effect on wound healing than laser or control. Mean percentage of change per week in ulcer size (±1 SD) from day 0 to complete healing for controls (32.4%), US/UVC (53.5%), and laser (23.7%). |
| 2. Several subjects experienced deterioration, with ulcers increasing in size (laser=3, 62% to 167% change; control=1, 58% change; US/UVC=1, 1% change). All ulcers healed by the end of the study; the last ulcer to heal in laser group healed by week 20 vs week 6 with US/UVC. |
Conclusions
There is level 1 evidence, from 1 small RCT, to suggest that combining US/UVC with standard wound care decreases the wound healing time of pressure ulcers post-SCI, but no evidence exists to clarify whether UVC or US, used alone, exerts any beneficial effect.
Effects of Nonthermal Pulsed Electromagnetic Energy Treatment
Electromagnetic energy acts during the proliferative stage of wound healing to increase production of granulation tissue formation. Other beneficial effects include increased blood and oxygen availability to tissues and decreased tissue edema.53 Keast et al,22 while updating best practice recommendations for the prevention and treatment of pressure ulcers, recommend considering electromagnetic fields as 1 adjunct modality for stimulating closure of chronic nonhealing pressure ulcers (table 15).
Table 15. Nonthermal Pulsed Electromagnetic Energy
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Salzberg et al,59 1995, USA PEDro=8 | Inclusion: all who participated had 1 or more pressure ulcers. Ages 24–69y. Exclusion: more than 1 ulcer; recent ulcer surgery; fitted with a cardiac pacemaker; comorbid disease; active cellulitis; sepsis; terminally ill or end stage disease; total joint replacement; stage I or IV ulcers. | RCT: 30 patients with SCI were selected to participate and subclassified into stage II vs stage III ulcers. Active treatment consisted of nonthermal pulsed high frequency, high peak power, electromagnetic energy delivered through a treatment head placed in light contact with the wound site and tuned to resonance in the area of the wound. Treatment was noninvasive and delivered through wound dressings for 30min, twice daily for 12wk or until healed. The control group received 12 wk of sham treatment. | Pressure ulcer status. | 1. Stage II group: active treatment (n=10), sham n=10). After 1 week, active treatment healed a greater percentage of ulcers (84%) than sham (40%, P=.01) and the median size of ulcer also was smaller at 1 week (2.7 vs 16.5cm2, P=.015). |
| 2. Complete healing with active treatment occurred in a median of 13d vs 31.5d with sham (P<.001). | ||||
| 3. Given that there were more large ulcers (>60cm2) in the sham group, data were reanalyzed for 15 patients with ulcers less than 60cm2, with similar results. | ||||
| 4. Stage III group: with active treatment, 3 of 5 healed over an average of 43d. 0 of 5 healed with sham. Ulcer area decreased by an average of 70.6% vs 20.7%, respectively. |
Salzberg et al59 evaluated the effects of nonthermal pulsed electromagnetic energy for the healing of stage II/III ulcers in patients with SCI, assessing effects in stage II ulcers and stage III ulcers separately. In those with stage II ulcers (n=10), a greater proportion of ulcers healed (84%) after 1 week of active treatment versus a sham treatment (40%; P=.01). For complete healing, the treatment group healed in a median of 13 days versus 31.5 days among controls (P<.001). Given that there were a larger number of ulcers with size greater than 60cm2 in the sham group, the data were reanalyzed, and the results obtained were consistent with the initial findings: again, treated patients with stage II ulcers experienced a greater proportion of lesions healed at 1 week (P=.002), and the number of days to being fully healed was fewer (P=.007). In those with stage III ulcers, healing was also associated with pulsed electromagnetic energy treatment: 3 of 5 healed within an average of 43 days, while 0 of 5 healed in the sham group. Ulcer area decreased 70.6% with active treatment versus 20.7% with the sham treatment.
Conclusions
There is level 1 evidence from 1 RCT to support the efficacy of pulsed electromagnetic energy to accelerate the healing of stage II and III pressure ulcers post-SCI.
Anabolic Steroid Agents
Impaired nutritional status and decreased nutritional intake are significantly associated with the development and healing of pressure ulcers.1 The use of anabolic steroids and increased protein intake have been associated with promoting anabolism, weight gain and, in turn, wound closure in burn patients.1 An anabolic steroid agent may also promote closure of nonhealing pressure ulcers in the SCI population because pressure ulcers are associated with an increased metabolic rate and catabolism.60
In a case series of 9 subjects with stage III or IV pressure ulcers, Spungen et al60 demonstrated complete healing in 8 of 9 subjects 3 to 12 months after daily administration of 20mg oxandrolone. Given the small size of this case series, further research is needed to determine the role of anabolic steroid agents (oxandrolone) for the promotion of healing of stage III and IV pressure ulcers post-SCI (table 16).
Table 16. Anabolic Steroid Agents
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Spungen et al,60 2001, USA D&B=15 | Inclusion: 1 of the following: a self-reported or documented healing PU that had existed for more than 2mo; or a full-thickness PU that extended through fascia into muscle, tendon, or bone. Exclusion: not specified. | Case series: 9 patients with SCI with stage III/IV PU were treated with 20mg oxandrolone daily and 20g glutamine dissolved in orange juice. PU care and support services remained unchanged. | Not specified. | 1. With oxandrolone and glutamine treatment, 8 of 9 patients completely healed, the majority within 3 to 6mo. Two subjects required 12mo of treatment for complete healing. |
Conclusions
There is very limited level 4 evidence to support the use of anabolic steroid agents (oxandrolone) to promote the healing of stage III and IV pressure ulcers post-SCI.
Effectiveness of Dressings
Because of the estimated costs associated with pressure ulcers and their treatment, various dressing types used with the SCI population have been investigated, including hydrogel61 and hydrocolloid dressings.62 When HDs are placed over the wound, fluids are absorbed, causing the dressing to swell and form a gel.53, 63 The outer surface of the dressing allows for exchange of water vapor and protects the wound from outside contamination. HDs also create a moist wound environment and are believed to act by accelerating wound debridement. They are cost effective because patients can wear the dressing for 3 to 5 days, and they are available in a sheet form as well as a paste or granules that are used to fill deeper wounds such as stage II and III pressure ulcers.1, 53, 64
A hydrogel dressing creates a healing environment by retaining moisture and rehydrating tissue; autolytic debridement and filling of any dead space in the wound.64, 65 It is believed that hydrogel dressings promote faster healing, provide protection against wound contamination, are acceptable to patients, decrease pain, and have been found to be cost effective65 (table 17).
Table 17. Effectiveness of Dressings Post-SCI
| Author, Year, Country PEDro/D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Hollisaz et al,62 2004, Iran PEDro=7 | Inclusion: paraplegia caused by an SCI; all past soldiers in the Iran/Iraq war; stage I or II pressure ulcers, smooth ulcer area so an adhesive dressing could be used. Exclusion: addiction; heavy smoking (>20 cigarettes/d or >10 packs/y); concomitant chronic disease. | RCT: 83 patients (with 91 PU, 33 stage 1 and 58 stage 2) with an SCI were randomly assigned to 1 of 3 groups: (1) SD, (2) HD, or (3) adhesive with PC. Dressings were changed twice daily for SD, daily for PC, and twice weekly for HD. | Healing status of the ulcer. | 1.Overall, completion of healing (regardless of location or stage) was better with HD (74% vs 40% with PC and 27% with SD; P<.01 and <.005, respectively). 2.Complete healing of stage I ulcers also was significantly greater in the HD group than in the other 2 (P<.005). 3.For stage II ulcers, those in the HD-treated ulcers healed better than SD-treated ulcers (67% vs 16%, respectively; P<.005), but no better than PC-treated ulcers. 4.Gluteal ulcers also healed more completely with HD than with either of the other 2 dressings (P<.001). 5.Complete healing of sacral ulcers did not differ among the 3 groups. |
| Kaya et al,61 2005, Turkey PEDro=4 | Inclusion: SCI; otherwise, no specific inclusion criteria cited. A total of 24 men and 3 women; ages 16–56y. PU stages I to III. No further details provided. Exclusion: not specified. | RCT: In total, 27 subjects with 49 PUs were randomly allocated to either of the following: Active treatment group (n=15 with 25 ulcers): received an occlusive hydrogel–type dressing, changed every 4 days unless the area became contaminated. Control group (n=12 with 24 ulcers): received povidone-iodine–soaked gauze applied to the area, with dressing changed daily to avoid contamination. | Rate of healing (cm2/d). | 1.There was no difference in the healing rates between the 2 groups. 2.Those in the treatment group had more wounds (n=21) heal than those in the control group (n=13) (P<.04). |
Hollisaz et al,62 in an RCT involving 83 subjects, found that those in the HD group (n=28) seemed to have the greatest completion of healing regardless of the location and stage, compared with those in the phenytoin cream group (n=28) or simple dressing group (n=27; P<.005). When considering stage I ulcers, those in the HD group healed faster than those in the other 2 groups (P<.005). For stage II ulcers, HD-treated ulcers healed better than simple dressing–treated ulcers (P<.005) but no better than phenytoin cream–treated ulcers. When looking at the area of injury, gluteal ulcers healed more completely in the HD group than in the other 2, whereas the healing of sacral ulcers did not differ between the 3 groups.
Kaya et al61 compared the effectiveness of applying an occlusive hydrogel–type dressing to a povidone-iodine–soaked gauze dressing. Although those using the hydrogel dressing experienced a somewhat higher rate of healing, no statistically significant differences were noted between the 2 groups. The 21 subjects in the treatment group did have significantly more wounds heal than the 13 controls (P<.04).
Conclusions
There is level 1 evidence from a single RCT that completion of healing for stage I and II pressure ulcers is greater with an occlusive HD compared with phenytoin cream or simple dressing. There is level 2 evidence from another single, small RCT that occlusive hydrogel–type dressings heal more pressure ulcers than conservative treatment.
Maggot Therapy
Maggot therapy, also called MDT, is a treatment for wound healing that has been practiced for several centuries; however, with the development of various antibiotics, this therapy began to lose its popularity after World War II. More fashionably called myasis or biosurgery, MDT uses specially bred larvae of the Lucilia sericata species. L sericata larvae do not damage healthy dermis or subcutaneous tissue, but can destroy healthy epithelium; thus, epithelium protection is mandatory with MDT. Maggots assist with the debridement of wounds by secreting digestive enzymes that dissolve necrotic tissue; these enzymes also contain antibacterial substances that assist with disinfecting wounds.66, 67 Maggot therapy is associated with an increase in wound granulation tissue debridement and disinfection, and is felt to accelerate wound healing (table 18).66, 67
Table 18. Effectiveness of Maggot Therapy
| Author, Year, Country D&B Score | Eligibility Criteria | Study Design and Methods | Outcome Measures | Results |
|---|---|---|---|---|
| Sherman et al,68 1995, USA D&B=9 | Inclusion: SCI; quadriplegia or paraplegia; pressure ulcer stage III or IV. Ages ranged from 44 to 68y. Both men and women, and 7 were patients with paraplegia. Exclusion: not specified. | Non-RCT: overall, 20 patients with SCI were recruited, but only 8 patients were allocated to the treatment group. Treatment group underwent conventional therapy for 3 to 4wk followed by the placing of maggots (covered with porous sterile dressings), which were left in place for 48-h to 72-h cycles. Between cycles of maggot therapy, the group received sodium hypochlorite, normal saline or wet-to-dry gauze dressings every 8 hours. Controls received traditional treatment. | Healing of the pressure ulcer; size of wound area. | 1.Noted change in surface area during maggot therapy (ulcer surface area decreased by approximately 22% per week P<.001 during therapy). 2.No complications or infection were noted as a result of treatment. |
In 1 non-RCT conducted by Sherman et al,68 8 of 20 patients diagnosed with pressure ulcers (stage III or IV) were treated with maggot therapy. All 8 patients underwent 3 weeks of conventional treatment, followed by maggot therapy. All necrotic wounds were debrided within 1 week of maggot treatment, and wound healing was faster among the 8 who had received maggot therapy than in the 12 who had not.
Conclusions
There is level 2 evidence from 1 study to support the use of maggot therapy as an adjunctive therapy for nonhealing pressure ulcers post-SCI.
Conclusions
Numerous authors cited in this article have noted that pressure ulcers, though largely preventable, remain a common, potentially serious lifelong secondary complication of SCI. Pressure ulcers have the potential to affect overall quality of life and to disrupt rehabilitation, vocational and educational pursuits, and community reintegration.1, 2, 3, 4 Pressure ulcers lead to increased hospital readmission rates with longer lengths of stay.69 While pressure ulcer prevention is more cost effective than treatment, pressure ulcers continue to be a major issue.4, 17, 19
Many of the 15 prevention studies reviewed had very small sample sizes. There was level 2 evidence to support early attendance at seating assessment clinics and provision of enhanced pressure ulcer prevention education; level 3 evidence that various cushions and seating systems have potentially beneficial effects; and level 4 evidence to support use of electrical stimulation, forward-leaning position for pressure relief, and behavioral contingencies. There was evidence to show that telerehabilitation, the addition of lumbar support to wheelchairs, and the 15-second to 30-second vertical lift for pressure relief were not effective. More rigorous research is needed in all areas of pressure ulcer prevention post-SCI to determine effective interventions so evidence-based conclusions may guide education and practice.
Eleven articles were found that studied treatment interventions post-SCI. While there were a small number of articles and generally small sample sizes, there was level 1 evidence to support electrical stimulation, US/UVC, and pulsed electromagnetic energy as adjunctive therapies to standard wound management. There also was level 1 evidence to support the use of an occlusive HD for healing of stage I and II pressure ulcers. Interventions that are well supported by evidence need to be incorporated into treatment plans for persons with SCI who have nonhealing pressure ulcers. Nonetheless, more research needs to be done to assess treatment interventions in the SCI population.
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- a ROHO Inc, PO Box 658, Belleville, IL 62222.
- b Jay Medical, Ltd, PO Box 18665, Boulder, CO 80308.
- c ErgoAir, Inc, 131 DW Highway, #326, Nashua, NH 03060.
- d Jobst, Box 653, Toledo, OH 43694.
- e Spenco Medical Corp, PO Box 8113, Waco, TX 76710.
- f Ken McRight Suppliers, 7456 South Oswego, Tulsa, OK 74136.
- g Everest & Jennings, 1803 Pontius Ave, Los Angeles, CA 90025.
- h Sci Medics Inc, 700 N Valley St, Bldg A, Anaheim, CA 92801.
- i Sunrise Medical, 7477 East Dry Creek Parkway, Longmont, CO 80503.
Supported by the Ontario Neurotrauma Foundation (grant no. 2007-SCI-SCIRE-528) and the Rick Hansen Man in Motion Foundation (International Collaboration on Repair Discoveries (ICORD) grant no. Rick Hanson 2008-13).
No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.
PII: S0003-9993(08)01553-0
doi:10.1016/j.apmr.2008.08.212
© 2009 American Congress of Rehabilitation Medicine. Published by Elsevier Inc. All rights reserved.
Volume 90, Issue 2 , Pages 213-231, February 2009
