PM R XXX (2015) 1-24

www.pmrjournal.org

Analytical Review: Systematic Review

Prevention of Pressure Ulcers Among People With Spinal Cord Injury: A Systematic Review Suzanne L. Groah, MD, MSPH, Manon Schladen, MSE, Cynthia G. Pineda, MD, Ching-Hui J. Hsieh, PhD

Abstract Objectives: To evaluate the literature on the effectiveness of bed and wheelchair positioning and repositioning in the prevention of pressure ulcers (PUs) in both the spinal cord injury (SCI) and non-SCI populations. Design: Systematic review. Methods: PubMed, CINAHL, PsycINFO, and EMBASE were queried with the subject heading terms “pressure sore,” “pressure ulcer,” “position or turn in bed, wheelchair,” “pressure relief,” and “pressure release.” All study design types that assessed the effectiveness of bed and wheelchair positioning and pressure relief maneuvers in any patient group and in any setting were sought. Three independent reviewers extracted and summarized details of eligible trials using a standardized method. Two independent reviewers assessed the methodological quality of each trial using the American Academy of Neurology guidelines. When reviewers were not able to reach consensus, a third independent reviewer served as tiebreaker. Results: We identified 2820 publications, of which 49 met inclusion criteria. Of these publications, the subject population was 2834 (923 persons with SCI, 717 persons without SCI, and 1194 healthy control subjects). Among studies examining pressure related to position or repositioning in bed or sitting, procedures for measuring skin pressure and metabolism were highly variable by anatomic location, measurement technique, outcome measure, study site, participant characteristics, and description of position/turning for bed and seated interventions. Numerous factors can influence tissue interface pressures, and no prospective studies had been performed to determine a causal relationship between interface pressure and skin breakdown. Several studies suggest that skin response to pressure differs between subjects with and without SCI. Conflicting results and insufficient evidence for optimal bed and seated positioning and turning and pressure relief maneuvers to prevent PUs in both SCI and non-SCI populations were limiting factors. Conclusions: Although there is no clear optimal positioning or turning frequency in bed, the evidence suggests avoiding the 90 lateral position because of high pressures and PU risk over the trochanters. During sitting, pressures are linearly redistributed from the sitting area during recline and tilt; however, reclining carries with it an increased risk of shear forces on this skin. The evidence does not support conclusive guidelines on positioning or repositioning techniques for PU prevention in bed or during sitting. We conclude that PU risk is highly individualized, with the SCI population at a higher risk, which demands flexible PU prevention strategies for bed/seated positioning and pressure relief maneuvers. Education has and will remain our most powerful ally to thwart this pervasive public health problem.

Introduction The prevalence of pressure ulcers (PUs) in the U.S. general population is estimated at 14%-17% [1,2], and PU-related health care costs are estimated to be in excess of $3 billion annually [3], placing a significant burden on individuals and society. It is well known that people with a spinal cord injury (SCI) have a higher risk of PUs as a result of immobility, insensate skin, and varying

degrees of incontinence. During initial acute medical and rehabilitation hospitalization, 27%-40% of persons with an SCI will experience a PU [4-6]. Data from the annual report of the National SCI Statistical Center indicate that 17.7% of persons with an SCI had been rehospitalized for a PU during their first year after rehabilitation and that by year 20, that number had increased to 37.4% [7-9]. If left untreated, PUs can lead to immobility, surgery, and in extreme cases, death [10].

1934-1482/$ - see front matter ª 2015 by the American Academy of Physical Medicine and Rehabilitation http://dx.doi.org/10.1016/j.pmrj.2014.11.014

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Pressure Ulcer Prevention and SCI

PU risk is multifactorial, with in excess of 200 risk factors described in the literature [11], and thus population-based evaluation of risk factor impact and the subsequent development of effective preventive strategies are extremely challenging. A recent prospective observational cohort study of 159 people with SCI in acute rehabilitation revealed only an existing PU and a Functional Independence Measure admission transfer score of 36 (n ¼ 14) but it was not possible to explore the cause of PUs from data

SCI ¼ spinal cord injury; IP ¼ interface pressure; HOB ¼ head of bed; BW ¼ body weight; TCPO2 ¼ transcutaneous oxygen pressure; ICU ¼ intensive care unit; SBF ¼ skin blood flow; T ¼ temperature; R ¼ right; PU ¼ pressure ulcer; TCO2 ¼ total carbon dioxide.

evaluated side-lying positions and trochanteric pressure in patients with SCI (n ¼ 50) admitted to an inpatient rehabilitation program. Compared with the traditional position of hip and knee flexion across the body, a position of 30 hip flexion and 35 knee flexion (with the lower leg behind the midpoint of the body) resulted in lower contralateral trochanteric pressure. However, when sacral skin temperature was used in place of IP as a risk factor for PU risk in hospitalized patients (6 with SCI and 11 with stroke), no difference was noted in supine versus lateral side-lying positions [29]. Several studies examined differences among patient populations and/or by severity or duration of impairment. Sae-Sia et al [28] examined skin perfusion

responses in patients with acute SCI (n ¼ 20) compared with matched groups of subjects with orthopedic trauma (n ¼ 35) and healthy control subjects (n ¼ 47). Microvascular dysfunction in response to prolonged pressure loading was observed in patients with SCI as early as 1 to 4 days after injury [28]. Schubert and He ´raud [30] evaluated 30 elderly patients with stroke and Parkinson disease and divided them into 2 groups (not at risk/low risk versus high risk) based on the 5-factor Norton score (factors include physical condition, mental condition, activity, mobility, and incontinence). Similarly, when the HOB was increased from 0 to 45 , the high-risk patients were observed to have an inability to recover a satisfactory blood supply after perfusion insult was found.

Figure 2. Bed positioning schematic.

8

Pressure Ulcer Prevention and SCI

Repositioning in Bed Six articles that examined the effect of various protocols of turning in bed on PU incidence were identified (Table 2). The primary outcome measure(s) was PU incidence in 4 of the 6 articles [45-48] and IP and skin temperature in 2 studies [49,50]. Subjects in the studies were mostly elderly persons without SCI in long-term care facilities, geriatric nursing homes, or the community and patients without SCI who had mixed diagnoses in a critical care setting. Study duration was highly variable, ranging from 1 day to 21 months. One study was graded as class I [49] and 5 studies were graded as class III [45-48,50]. The laboratory-based study was a quasi-experimental study of 16 healthy elder volunteers that examined skin surface temperature and start-end IP while in varying positions (left trochanter, right trochanter, and sacrum) and with varying turning intervals (1 hour, 1.5 hours, and 2 hours). Skin surface temperature increased with a longer turning schedule (P ¼ .0004) and trochanteric positioning, but start-end IP did not differ by position or turning interval [49]. The 3 RCTs identified had variable turning protocols and study durations (2 weeks to 21 months). Smith and Malone [46] compared a 2-hour turning protocol versus 2-hour turning plus additional unscheduled shifts using a rolled hand towel in 19 subjects. No difference was found between the protocols, with a PU developing in one participant in each group during the 2-week study period [46]. Similarly, Vanderwee et al [47] found no difference in PU incidence in patients who were turned every 4 hours while supine and every 2 hours while lateral versus patients on a fixed 4-hour turning schedule. Defloor et al [45] conducted a 4-week cluster RCT of 4 turning protocols, utilizing 2 different mattresses in 262 subjects in 11 nursing homes. The control group (N ¼ 511) received “standard of care,” defined as preventive nursing care based on clinical judgment of the nursing staff and variable use of protective devices (mattresses, sheepskin, and gel cushions). The 4 intervention groups were (a) standard mattress þ a 2-hour turn schedule (N ¼ 65); (b) standard mattress þ a 3-hour turn schedule (N ¼ 65); (c) pressure reducing mattress þ a 4-hour turn schedule (N ¼ 67); and (d) a pressure-reducing mattress þ a 6-hour turn schedule (N ¼ 65). The group being turned every 4 hours on a pressure-reducing mattress had the lowest incidence of stage II or higher PUs (P ¼ .003) and the longest time to develop a PU (P ¼ .001). No difference was found between the groups in stage I PU onset. A study in a critical care setting by Kaitani et al [48] (class III) looked into risk factors, including frequent turning every 2 hours, of PU incidence among patients (N ¼ 98) over a 3-month period. A total of 14 PUs developed in 11 subjects, and 3 patients had more than one PU. The study showed no relationship between PU development and severity of disease or medications.

Multivariate analysis demonstrated that being an emergency intensive care unit patient and infrequent turning and repositioning resulted in higher incidence of PU development. Oertwich et al [50] evaluated 50 longterm care skilled nursing care residents with variable diagnoses (68% with cardiovascular diseases) to determine the effect of small shifts in body weight on IP and blood flow under a bony prominence over time in the lateral oblique (side-lying) and supine positions. The study demonstrated that small shifts in body weight can relieve IP (sacrum and trochanter) and increase blood flow (sacrum) in both positions; however, blood flow and IP did not change significantly over time. Pressures Related to Sitting Twenty-five studies examined pressures and pressure relief maneuvers during sitting (see Table 3). As with the studies on bed positioning, there was significant heterogeneity of methods and outcomes of seated positioning and pressure relief maneuvers, precluding aggregation of study results. Study designs were primarily case series [51-57], cohort [44,58-63], or crosssectional [64-72]. There was one N-of-1 study and one RCT [73,64]. Two studies [67,74], which were also the 2 studies conducted with community-dwelling subjects, were graded as evidence class IV. The remaining studies were graded as class III. No class I or II studies were identified. The one RCT [73] was graded as class III because of lack of information about blinding. Most studies (19) were conducted in a laboratory setting [44,51-63,68-72]. Six studies [64-66,73] were conducted in the clinic, and two of these studies [67,74] were with community-dwelling subjects. The total number of subjects examined across the 25 identified studies was 1148. Of these subjects, 321 were able-bodied individuals, 137 had paraplegia, 100 had tetraplegia, and the level of injury was not specified for 590 subjects with SCI. Nine studies examined seated pressures exclusively in able-bodied persons [51-57,70,71], and a like number of studies examined persons with SCI exclusively [64-69,72-74]. The remaining 7 studies examined both able-bodied persons and those with SCI [44,58-63]. The ischium was an anatomic site of interest in 17 studies [44,52,55,56,58,59,61,62,64-71,73]. The next most common sites examined were the seating interface as a whole [51,53,54,57,60,63,72,74] and the buttocks. The thighs [58,62,65] and the sacrum [57] received less focus. Pelvic rotation was the focus of 2 studies [55,56]. The principal outcome measure of interest across 19 of the 25 identified studies was average and/or maximum IP [44,51-56,58,59,61-63,65-69,71,72]. Authors of one study looked at pressure distribution [60], and authors of 3 studies reported shear forces [52,58,59] at the interface. Tissue oxygenation/perfusion was an outcome of interest in 4 studies [44,57,64,70], and skin or pressure ulcer characteristics

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Table 2 Summary of articles pertaining to turning in bed

First Author, Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Pressure Measured During Relief Maneuver Outcomes

No

No

The 4-h turn schedule with pressurereducing mattress is associated with (1) lower probability of PU (OR ¼ 0.12), and (2) a significantly lower number of PU lesions

No

No

Random order No of positioning, including left trochanter, right trochanter, and sacrum, with 3 different turning intervals: 1, 1.5, and 2 h

No

Yes

Small shifts

No

Yes

A total of 14 PUs developed in 11 subjects; 3 patients had more than 1 PU; the study showed no relationship between PU development and severity of disease or medications; multivariate analysis demonstrated that being a patient in the ICU and infrequent turning and repositioning resulted in higher incidence of PU onset Skin surface temperature increased the most in the 2-h turn interval; skin surface temperature increased the most in right and left trochanter positions; start-end interface pressure is not significantly different among different turning intervals or positions Small shifts in body weight can relieve interface pressure (sacrum and trochanter) and

Bed Turning Duration Schemes

Defloor 2005

I

4-group Clinic cluster RCT (geriatric nursing homes)

No (N ¼ 761) 4 wk

Kaitani 2010

III

Cohort, Clinic (ICU) prospective

No (N ¼ 98)

Knox 1994

III

Laboratory Quasiexperiment with Latinsquare design

No (N ¼ 16 1d elderly volunteers)

Oertwich 1995

III

Time series, withinsubject repeated measures

Clinic (long- No (N ¼ 50) term care facility)

Pressure Measured While Seated

3 mo

1d

Pressure Measured While Reclining

No 2-h turn on standard mattress; 3h turn on standard mattress; 4h turn on pressurereducing mattress; 6h turn on pressurereducing mattress; control using standard nursing care with variable protective devices Turning every No 2h

No

(continued on next page)

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Pressure Ulcer Prevention and SCI

Table 2 (continued )

First Author, Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Smith 1990 III

2-group RCT, Clinic (long- No (N ¼ 19) pretestterm care posttest facility) design

Vanderwee III 2007

2-arm RCT

Bed Turning Duration Schemes

2 wk

Clinic (elder No (N ¼ 235) 21 mo care nursing homes)

Pressure Measured While Reclining

No Treatment group was turned every 2 h plus small unscheduled shifts; control group was turned every 2h No Experiment group was repositioned alternately every 2 h in a lateral position and every 4 h in a supine position; control group was repositioned every 4 h

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

No

No

No

No

increase blood flow (sacrum) in oblique and supine positions 11.1% in treatment group and 10% in control group developed PU

16.4% in the experiment group and 21.2% in the control group developed PU; there is no statistical significance in the rate of PU onset, severity of PU, or time to develop a PU

SCI ¼ spinal cord injury; PU ¼ pressure ulcer; OR ¼ odds ratio; ICU ¼ intensive care unit; RCT ¼ randomized controlled trial.

were studied in 3 studies [63,73,74]. Four studies looked at rate [67,70,74] or duration [64,67,70,74] of pressure relief performance or postural shifts. All identified studies measured seated pressures except for one study, which examined pressure relief behavior in response to verbal feedback [74]. Twenty-two studies measured seated pressures through a range of maneuvers [44,5265,67-73], and 6 studies included pressures during full recline [51,52,54,59,63,71]. A manual wheelchair was the most commonly used seating apparatus [44,53,61,62,65,70,72,73]. The subject’s own wheelchair was used in 6 studies [64,6669,74], a power, reclining wheelchair was used in 3 studies [52,58,63], and a custom, instrumented chair was described in 5 reports [55-57,59,71]. Three studies used a plain, hard chair [60], an arm chair [54], or a geriatric chair [51] instead of a wheelchair. Eight studies considered the effects of cushions [51,52,58,61,65-67,72]. A major confounder in assessing efficacy of seated position (and pressure relief maneuvers) was the cushion material used. Although a review of pressure relief by cushion material is beyond the scope of this review, we did find generalizable differences in the effectiveness of pressure relief by seating surface, with the following results. Generally, when comparing water,

foam, gel, and air cushions, water provided the least amount of pressure relief, followed by foam [51]. Contoured foam provides some pressure relief compared with uncontoured foam; however, neither provided the degree of pressure relief of gel or air cushions [72]. Comparisons of air versus gel cushions show that whereas air cushions distribute pressure well to the thighs and buttocks, shaving down the front of a gel cushion allows levering forward of the pelvis, with reductions of pressure on the ischial tuberosities [58,72]. Generally speaking, across all conditions, air cushions were the most effective at relieving pressure [51,52,58,61,65-67,72], and persons using custom-fitted cushions experienced less skin breakdown and skin redness than did those using depot cushions (ie, off the shelf, non-custom foam cushions) [66]. The types of instrumentation used to measure IP across the identified studies most frequently fell into the general categories of pressure mats [44,51,61-63,68,70,72] and force plates/sensors [52-58]. Two studies [55,56] also incorporated an infrared camera Vicon motion capture system. The remaining studies used a heterogenous mix of pressure monitoring sensors to measure IP [59,60,65-67,69,71,73]. When tissue oxygenation and perfusion were measured, transcutaneous oxygen

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Table 3 Seated pressures and pressure relief maneuvers

First Author/ Year

Study Group (SCI Subjects?)

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

Class Study Design

Setting

Makhsous 2007

III

Cohort

Laboratory Yes (SCI ¼ 40, Investigated relief of No non-SCI ¼ 20) pressure in a sitting posture that reduces ischial support: normal sitting vs sitting upright with the back part of the seat tilted downward 20 and enhanced lumbar support

Yes

Yes

Koo 1996

III

Cohort

Laboratory Yes (SCI ¼ 6, non-SCI ¼ 8)

No

Yes

Yes

FergusonPell, 1980

III

Cross- sectional Clinic

Yes (SCI ¼ 567) Examined the relationship between IP and persistence of PUs

No

Yes

No

Coggrave 2003

III

CrossClinic sectional/ retrospective review

Yes (SCI ¼ 46)

No

Yes

Yes

Makhsous 2009

III

RCT

Yes

Yes

Makhsous 2007

III

Cohort

No Evaluated whether a cyclic pressure relief protocol accelerates PU healing in WC users; off-loading of pressure on posterior portion of WC seat customized to maintain IP lower than 15 mm Hg Laboratory Yes (SCI ¼ 40, Examined effect of No non-SCI ¼ 20) push-up pressure relief maneuvers vs automated, dynamic

Yes

Yes

Clinic

Yes (SCI ¼ 44)

Compared air vs foam cushion in 6 postures

Evaluated ischial, TCPO2 measurements

Cyclically repositioning the IP between postures resulted in a significantly lower average IP over the buttocks compared with normal sitting plus push-ups; a sitting protocol that periodically reduces ischial support helps lower sitting load on buttocks and ischial tuberosities Pressures lowest on ROHO cushion; forward-leaning posture provided the greatest pressure relief; ROHO compensated for poor sitting posture (lateral trunk bend) Positive correlation between pressure and PUs (sole article that examined this relationship); positive correlation between clinic-fitted cushion and absence of PUs Mean duration of pressure relief to return tissue O2 to unloaded levels was 1 min 51 s (range 42 s-3 min 30 s); findings suggest inadequacy of standard recommendation of 15-30 s for pressure relief; recommend side or forward leaning, tilt in chair Treatment group achieved 30% healing significantly faster than did control group; individualized cyclic pressure relief may help promote PU healing in a clinical setting Dynamic sitting protocol had significant effect on improving perfusion (continued on next page)

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Pressure Ulcer Prevention and SCI

Table 3 (continued )

First Author/ Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

pressure relief protocol: alternating between normal upright sitting, full seat support, no added lumbar support, and offloading configuration (sitting upright with the posterior seat section tilted down 20 with enhanced lumbar support); push-up protocol was defined as normal sitting with a standard WC push-up every 20 min

Tanimoto 1998

III

Cross-sectional Laboratory Yes (SCI ¼ 19)

Karatas 2008

III

Hobson 1992

III

Examined buttocks No pressure distribution on 5 kinds of WC cushions; air cushions specifically

Yes

Yes

Cohort

No Laboratory Yes (SCI ¼ 16, Evaluated center-ofnon-SCI ¼ 18) pressure displacement in persons with vs without SCI; investigated dynamic sitting stability in relation to PU

Yes

Yes

Cohort

Yes Laboratory Yes (SCI ¼ 12, Identified pressure non-SCI ¼ 10) distribution differences between SCI and non-SCI; investigate how forces change with 9 body postures

Yes

Yes

and periodic repositioning concentrated pressure from buttocks to thighs; manual push-ups relieved pressure but perfusion did not return to baseline; non-SCI control subjects demonstrated different perfusion physiology than that of persons with SCI; control subjects regain O2 and disperse CO2, faster than patients with SCI, suggesting altered physiology after SCI On air cushions, buttocks pressure is widely distributed; pressure only on lateral parts of IT in cushions with cutouts; maximum pressure highest on foam, lowest on air and silicone gel cushions; air cushion most effective at pressure redistribution; optimum air pressure a function of weight and area Subjects with SCI were less stable than subjects without SCI in forward, backward, and lateral leaning; lack of dynamic stability postulated as a factor in PU development in paraplegics SCI subjects had maximum pressures higher than non-SCI subjects in all postures; postural changes reduced maximum pressures: forward flexion to 50 , e9%; backrest recline to 120 , (continued on next page)

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Table 3 (continued )

First Author/ Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Park 1993

III

Cross-sectional Laboratory Yes (SCI ¼ 12)

Gilsdorf 1991

III

Cohort

Sprigle 2010

III

Cohort

Bed Turning Schemes/ Repositioning Protocols While Seated

Investigated the effect of forward, cross-body, and lateral reach on pressure relief

Pressure Measured While Reclining

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

No

Yes

Yes

Laboratory Yes (SCI ¼ 11, non-SCI ¼ 6)

No Compared normal and shear forces, location of center of mass, armrest force while sitting on 2 cushion types and hard surface

Yes

Yes

Laboratory Yes (SCI ¼ 10, non-SCI ¼ 6)

Compared forced Yes reduction of tilt (0 ,

Yes

Yes

e12%; full body tilt, e12%; SCI subjects had average peak pressure gradients 1.5-2.5 times greater than the non-SCI group; tangential shear force acted on body-seat interface in all postures; fullbody tilt reduced shear to almost 0; full-body tilt to 20 reduced TIS to near 0; further tilting caused a gradual increase in the opposite direction; backrest recline postures caused an increase in TIS by 7%25% Forward leaning and lateral positioning can supplement typical pressure relief; specifically, ipsilateral ischial tuberosity pressure was lower for crossbody reach during flat-plane activity Armrests reduced seat force by carrying part of body weight; variation in arm force greatest with paraplegics; ROHO cushions generally demonstrated both greater normal and shear forces than did Jay cushions; most variability among static factors among paraplegics; normal forces higher in all SCI than in non-SCI subjects; non-SCI subjects showed more anterior center of force than did paraplegics; armrests carried 8%9% of body weight for non-SCI subjects and paraplegics, 5% for tetraplegics SCI subjects: maximum seat load decreased (continued on next page)

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Pressure Ulcer Prevention and SCI

Table 3 (continued )

First Author/ Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

15 , 25 , 40 , 55 ), recline (10 , 30 , 50 , 70 , 90 ), and standing (0 , 20 , 40 , 60 , 75 ) positions

Henderson III 1994

Cross- sectional Laboratory Yes (SCI ¼ 10)

Compared 3 methods No of pressure relief in persons with SCI: forward leaning, tipped back 35 and 65

Yes

Yes

Eksteen 2006

Cross- sectional Clinic

Yes (SCI ¼ 10)

Determined IP during No normal sitting on 3 different WC cushions; compared IPs with forward leaning and diagonal forward-leaning PR; determined most effective PR techniques for the 3 cushion types Comparison of 2 types No of WCs on pressure relief during tilt

Yes

Yes

Yes

Yes

Yes

Yes

III

MacDonald III 2009

Case series

Laboratory No (N ¼ 8)

Stinson 2003

Case series

Laboratory No (N ¼ 63)

III

Investigated Yes relationship between IP and BMI, seating positions (recline 10 , 20 and 30 , foot support and foot elevation), and gender

during full standing and full recline; able-bodied subjects: maximum seat load decreased during full standing; standing relieved both seat and backrest pressure; pressure change observed to be linear 35 backwards tip of WC did not significantly relieve pressure over IT, but 65 did; forward leaning was most effective at relieving IT pressure; 65 tip may be indicated for patients who can’t/ shouldn’t lean forward During forward leaning: lowest IP under CCP (45 mm Hg) was seen for the air cushion for both IT and upper thighs; during diagonal forward leaning, there was a statistically significant reduction in IP under the IT Comparable pressure relief found between the ARC-RAD and TIS chairs; ARC-RAD: mean pressure 58.6 upright, 45.8 tilted; TIS: 55.7 upright, 47.2 tilted Average and maximum pressures were independent of gender; average pressure has significant positive correlation with BMI; significant reduction in average pressure with 30 recline; recline of 10 or 20 had no effect on average pressure; maximum pressure not significantly altered at 10 , 20 , or 30 recline; elevating feet (on (continued on next page)

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Table 3 (continued )

First Author/ Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

Defloor 1999

III

Cross- sectional Laboratory No (N ¼ 56)

Measured effect of Yes posture and cushion on peri-IT pressures in chairs

Yes

No

Reenalda 2009

III

Cross-sectional Laboratory No (N ¼ 25)

No Analyzed the pressure relief habits of able-bodied subjects and the effect of maneuvers on perfusion

Yes

Yes

Shields 1988

III

Cross-sectional Laboratory No (N ¼ 20)

Compared lumbar Yes support at 0 and 10 angle on buttock pressure

Yes

Yes

footstool) reduced average pressure to level approaching significance; supported vs unsupported feet significantly increased average pressure at 0 , 10 , 20 , and 30 recline and maximum pressure at 0 , 10 , and 30 recline Sitting pressures were greater than lying pressures; reclining backrest and placing legs on a rest yielded the lowest pressure; high pressures were associated with slouched or sliddown positions; sitting upright in an armless chair also had higher pressure; air cushions and slow-foam cushions reduced pressure more than did water cushions; air cushions were best for reducing pressure in slouched or sliddown positions Non-disabled subjects shift position on average 7.8  5.2 (SD) per h; average increase in oxygenation 2.2  2.4% with each shift; shifts 80% saggital, 20% frontal plane (coronal) were proposed as normative; changing sitting load at least every 8 min was proposed for WC users Lumbar spine support reduced pressure over the IT and in both upright (horizontal seat) and reclined (seat tilted 10 ) positions; reclining the seat (without lumbar (continued on next page)

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Pressure Ulcer Prevention and SCI

Table 3 (continued )

First Author/ Year

Class Study Design

Setting

Study Group (SCI Subjects?)

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

Van Geffen III 2008

Case series

Laboratory No (N ¼ 18)

Investigated influence No of sagittal postural adjustment on buttock load (pressure)

Yes

Yes

Van Geffen III 2009

Case series

Laboratory No (N ¼ 18)

Investigate effects of DPR on buttockseat interface load; evaluated applicability of DPR to regulate buttock load in sitting

No

Yes

Yes

Van Geffen III 2010

Case series

Laboratory No (N ¼ 15)

Examined relationship No between redistribution of external buttock load in relation to the dynamics of subtuberal blood dynamics in sitting with a dynamic TSE

Yes

Yes

spine support) did not cause a significant reduction in pressure; as pressures areas measuring >100 mm Hg decreased, the lower pressure levels showed a corresponding increase Seat inclination was most effective to regulate buttock shear force; pelvic rotation most effective to regulate center of pressure and sacral load; combination of independent pelvis rotation and seat inclination adequate to regulate net buttock shear force and sacral IP but not pressure over the IT Sagittal pelvic adjustment is most effective to regulate sacral pressure while frontal pelvis adjustment regulates tuberal pressure; with pelvis rotated up to 9 in frontal and up to 19 in sagittal, sacral relief up to 40% and tuberal relief up to 34% TSE adjustment was effective to regulate center of buttock pressure and the dispersion index under the IT; blood supply to the subtuberal buttock tissue was inversely related to the applied loads under the IT; a rapid inflow of blood in the initial stage of tuberal unloading, followed by a more gradual outflow in the rest of the movement cycle, suggested that average blood supply (continued on next page)

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Table 3 (continued )

First Author/ Year

Gilsdorf 1990

Class Study Design

III

Fisher 1983 IV

Case series

Setting

Study Group (SCI Subjects?)

Laboratory No (N ¼ 10)

Cross- sectional Clinic (out Yes (N ¼ 5) patients)

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Investigated the Yes effects of back angle and leg height on sitting forces in a WC for ROHO, Jay cushion, and hard surface

Ascertained pressure relief behavior of tetraplegics in the community on 2 different types of cushions

No

Pressure Measured While Seated

Pressure Measured During Relief Maneuver Outcomes

Yes

Yes

Yes

Yes

increased with adjustment frequency; TSE adjustment affected tissue under the sacrum and thighs, as well as buttock tissue under the IT; results suggest a potential benefit for buttock tissue viability under the entire ischial region with TSE adjustment Sitting up from reclining increased both normal and shear pressure; forces transmitted by the ROHO and Jay cushion were similar; hard surface showed less force build-up as chair back returned to vertical; leaning forward returned pressures to baseline; recommended leaning forward upon sitting up; firm material under the thighs, by levering the pelvis forward, reduced pressure on IT when legs were lowered Average pressure under IT for ROHO, 71.5; for foam, 105.4; pressure difference is statistically significant; average time between pushups >1 s on ROHO: 76 min; on foam, 60 min; average time between push-ups >5 s on ROHO: 116 min; on foam, 78 min; no statistically significant difference in number or >1 s and >5 s relief maneuvers performed on ROHO or foam cushion; no subject acquired a PU; data suggest re-examination of the (continued on next page)

18

Pressure Ulcer Prevention and SCI

Table 3 (continued )

First Author/ Year

Carr 1983

Class Study Design

IV

Setting

Study Group (SCI Subjects?)

N of 1/multiple Clinic (out Yes (N ¼ 1) baseline patients) across settings

Bed Turning Schemes/ Repositioning Protocols While Seated

Pressure Measured While Reclining

Performance of No pressure relief exercises in response to verbal feedback

Pressure Measured While Seated

Yes

Pressure Measured During Relief Maneuver Outcomes

Yes

recommendations for pressure relief in PU prevention Verbal feedback procedure increased pressure relief performance; concomitant improvement in PUs observed; no new ulcers observed at follow-up

SCI ¼ spinal cord injury; IP ¼ interface pressure; PU ¼ pressure ulcer; TCPO2 ¼ transcutaneous oxygen pressure; O2 ¼ oxygen; RCT ¼ randomized controlled trial; WC ¼ wheelchair; CO2 ¼ carbon dioxide; IT ¼ ischial tuberosity; TIS ¼ tangentially induced sheer; PR ¼ pressure relief; CCP ¼ capillary closing pressure; BMI ¼ body mass index; SD ¼ standard deviation; DPR ¼ decoupled pelvis rotation; TSE ¼ tuberal support element.

pressure/transcutaneous carbon dioxide pressure electrodes [44,64] or O2C, a combination of laser Doppler flowmetry and diffuse reflectance spectroscopy [57,70], were used. Pressure Related to Sitting Posture Twenty-four studies measured pressure during varying seated postures. Of these, 23 were appraised as class III and one study as class IV (no blinded or randomized studies were identified). A neutral erect sitting posture served as the point of departure for looking at pressure changes in other seated positions across all of the studies. Generally, the neutral erect posture was defined as positioning the chair backrest at 90 -110 and positioning the subject’s buttocks touching the back of the chair and thighs parallel to the floor with knees and ankles at right angles. Higher pressures were associated with slouching, slumping, and sliding down in the chair. Defloor and Grypdonck [51] found that a 15 lateral slouch significantly increased pressure from neutral, midline sitting, as did sliding down in the chair 45 [51]. Koo and colleagues [61] likewise found that maximum pressure was higher when the subject was slumped (with the pelvis 5 cm forward) compared with that of neutral posture. Because armrests carry 8%-9% of body weight for paraplegics and persons without SCI versus 5% of body weight for persons with tetraplegia [52,61], sitting upright in a chair with no armrests was comparable to slouching, with a large demonstrable increase in pressure over upright sitting in a chair with arms [51]. Pressure Relief Maneuvers Pressure relief maneuvers assessed include reclining, push-ups, tilt, and various combinations of leaning and

reaching [6,8,13-15,21,23]. Major findings for each maneuver are described in this section. Sprigle et al [63] compared load redistribution in 10 people with SCI and 6 able-bodied control subjects and demonstrated a linear relationship between the angle of recline and seat unloading. However, other studies suggest that less than 30 of recline changes seated pressure (perpendicular to the horizontal plane of sitting) little from that measured in a neutral, upright position [51,54,59,63,71]. Gilsdorf et al [52] demonstrated that reclining to 58 decreased average, normal force sitting pressure by 13.7-16.6 kg depending on the surface (hard surface, gel, or air cushion) compared with the upright position. However, Gilsdorf et al [52] also found that shear forces (ie, pressure parallel to the horizontal plane of sitting) during the same recline increased by 6.38-7.17 kg. Similarly, Hobson [59] found that the reduction in seated pressure during recline of greater than 30 was accompanied by an increase in shear forces that was 7% greater at 110 and 25% greater at 120 . Lower extremity position was demonstrated to have a various impact on pressure distribution during upright sitting and reclining. In a cross-sectional study of 56 able-bodied subjects, Defloor and Grypdonck [51] found that raising both the feet and lower legs (by at least 30 cm, with knees extended) reduced pressure during a 30 recline; however, this maneuver increased the pressure during neutral, upright sitting. In contrast, in another case-series study, Stinson and colleagues [54] found that supporting able-bodied subjects’ feet on blocks with the knees flexed (versus allowing their legs to dangle) caused a significant increase in maximum pressures as the subjects reclined from 0 to 30 . As with reclining, Sprigle et al [63] measured pressures during various tilt angles and found that the

S.L. Groah et al. / PM R XXX (2015) 1-24

relationship between angle of tilt and seat unloading was linear in people with SCI and, in general, tilting increases backrest load. MacDonald et al [53] reported that a tilt of 38.1 e39 reduced mean pressure by 7.912.8 mm Hg, depending on the type of wheelchair studied. In a laboratory-based study of 10 people with SCI (7 paraplegics and 3 tetraplegics), Henderson and colleagues [68] found that tilting to 65 reduced pressure more than tilting to 35 (36% versus 17%, respectively). However, tilting to 55 provided less unloading than did fully reclining (90 ), while full standing (75 angle between chair seat and vertical plane) results in the greatest reductions in seat pressure, with a 40% reduction in pressures [63]. Authors of several studies found that forward leaning was the maneuver that provided the most effective pressure relief [59,61,68]dgreater than that provided by a 65 tilt [68]dand registered the lowest maximum ischial pressures [61]. During forward leaning, pressures initially increase by 10% at 30 flexion and then decrease, such that at 50 flexion, pressures decrease by approximately 15% of those in the neutral sitting position [59]. Although leaning forward has the benefit of avoiding the additional shear pressure encountered during recline and recovery to the neutral position [58], if forward leaning is associated with large pressure gradients, shear stress subsequently increases [59]. Diagonal forward leaning also produced lower interface pressure under capillary closure pressure (45 mm Hg) than did leaning straight forward in subjects with tetraplegia, irrespective of cushion type used (gel, foam, or air) [65]. Park [69] reported that in persons with paraplegia, cross-body (ie, diagonal) reaching in the flat (horizontal) plane was the most effective reaching maneuver for pressure relief of the ipsilateral ischial trochanter. Diagonal reaching was about 18% more effective at relieving sitting pressure than were either lateral or forward reaching. Park [69] further found that, in the upright (vertical) plane, cross-body reaching reduced pressure approximately 14% over that measured during sitting without reaching. Both forward and lateral reaching in the upright plane, however, increased ischial trochanter pressure by approximately 1% and 26%, respectively [69]. Push-ups Fisher and Patterson [67] found that compliance with push-ups was poor in persons with tetraplegia, regardless of cushion type used (air or foam). Individuals performed a push-up pressure relief maneuver of greater than 1 second duration every 60-76 minutes and push-ups of greater than 5 seconds duration every 78116 minutes, with average pressures ranging between 71.5 and 105.4 mm Hg [67] (capillary closure pressure occurs at 45 mm Hg [65]). Notably, the push-up was the

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maneuver least frequently recommended (6/36) in the study of seating clinic practice by Coggrave and Rose [64]. Discussion In this review we sought to extract evidence from the literature substantiating the development of evidencebased guidelines on pressure relief and repositioning for PU prevention in people with SCI. A database search revealed 19 articles addressing repositioning for PU prevention in people with SCI; all of these articles were graded as class III or IV. Because of the dearth of quality evidence, 30 studies of subjects without SCI were included so related data could be extrapolated and evaluated. For the outcomes of interestdrepositioning in bed and pressure relief maneuvers while seated in a wheelchairdfew conclusive recommendations can be drawn because of a general lack of evidence, which is confounded by heterogeneity of outcomes, participants, and methods utilized. Trends supported by class III and IV evidence are summarized in the following sections. Extrapolation of Data from Non-SCI Populations Although not a primary outcome of interest, several studies suggest that the physiologic response of the skin to pressure and pressure-relieving maneuvers is highly individual and affected by medical comorbidities and neurologic impairment. Sae-Sia et al [28] demonstrated changes in microperfusion in people with SCI within days of injury and also differentiated the response of people with SCI from that of healthy control subjects and patients with orthopedic trauma [26,28]. Likewise, in another study of elderly persons with neurologic impairments due to stroke or Parkinson disease, it was found that those at greater risk of skin breakdown (presumably because of more severe neurologic impairment) had altered physiologic responses to pressure [28]. Although risk of skin breakdown after SCI has largely been attributed to insensate skin, sarcopenia, lack of mobility, and incontinence, it is conceivable that other effects of the SCI such as autonomic control, vascular function, immune response, and other unknowns further affect the normal physiology and repair mechanisms of this organ. Therefore, it is our recommendation that any extrapolation of data regarding skin physiology, integrity, and PUs from non-SCI populations be interpreted with great caution. Bed Positioning Generally, although the type of support surface clearly influences pressures transmitted to the skin, there was a general consensus that pressures are more widely distributed, and hence lower over any one given

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Pressure Ulcer Prevention and SCI

area, in the fully supine [25,39,40] and prone [27,32,41] positions. However, although these positions may be more favorable for pressure distribution over the skin, the prone position, especially, is used infrequently because it is often felt to be uncomfortable [39], more staff assistance is required to attain prone positioning, and in patients with neurologic impairment, it may increase aspiration and other respiratory risks [36]. Beyond fully prone or supine, there is no clear trend in sacral IP with increasing HOB elevation from supine in healthy control subjects or hospitalized subjects without SCI, although there was a suggestion of increasing sacral IP with increasing HOB in one study of persons with tetraplegia. Further, it is unclear at what angle of elevation the pressure increase becomes clinically relevant [36,41], and this may, in fact, vary by other factors, such as age, body habitus, body mass index, and medical comorbidities. The 30 semi-Fowler position with the feet elevated may reduce pressures transmitted to the heels, but the effect on the sacrum is unclear [35]. The full or 90 lateral position was associated with high pressures over the trochanters [39]. The evidence upon which these conclusions are based was related solely to pressure, so confidence in establishing a causal relationship between body position in bed and subsequent PU development is limited because of methodological differences and a lack of prospective evidence directly linking position to PU incidence. Further, it is unknown at what degree and duration of IP that damage occurs, nor are the repair mechanisms defined. Clinical application of this “best” evidence is challenging, because numerous factors influence positioning in bed. Support surface, skin temperature, moisture, IP between a bony prominence and the support surface, and turning schedule are among an array of risk factors in play at any given time. In many cases, multiple factors are thought to be interactive with one another, and thus uncovering the relative contribution of each factor is challenging. Further, when multiple medical cormorbidities or multiple risks are present and potentially interacting, evidence-based treatment and prevention guidelines may compete with one other. In the clinical setting, this situation may result in modification of or even jettisoning of accepted evidence-based prevention practices for one condition in favor of prevention or treatment guidelines for another medical condition. For example, in the acutely injured tetraplegic patient (and other patients in critical care), there is often a concern for aspiration and other pulmonary complications because of impaired swallowing and secretion clearance, the presence of enteral nutrition, mechanical ventilation, impaired cognition, and other factors. Numerous evidence-based guidelines [75-84] recommend elevation of the HOB above 30 -45 to avoid respiratory complications [78,82]. This practice is in direct opposition to guidelines established for PU

prevention by the National Pressure Ulcer Advisory Panel, Wound Ostomy and Continence Nurses Association, and Wound Healing Society to “raise the head of bed no more than 30 (and preferably less)” [15,85,86]. A recent critical care nursing review highlights the competing priorities of optimal HOB positioning in critically ill patients [87]. The authors acknowledge that increasing the HOB puts the patient at greater risk for PUs while decreasing the risk for aspiration but note that the evidence for aspiration prevention is more robust than that for PU prevention and that aspiration carries a greater risk of mortality than do PUs. This observation suggests that greater consideration be given to risk stratification of the patient and adjustment of the HOB elevation accordingly. In addition, this situation re-emphasizes the critical importance of multiple modalities in PU prevention, such as the use of pressurerelieving surfaces, because clinicians cannot always employ best practices and existing guidelines for optimal PU prevention. Bed Turning and Repositioning Insufficient evidence exists to support specific statements regarding bed-based repositioning and turning protocols for PU prevention. First, studies aiming to examine turning protocols and the effect on prevention of PUs are scarce. All participants in the studies reviewed did not have SCIs and largely were elderly. Study settings were nursing homes or long-term care facilities, and varying sample sizes make any definitive conclusions a challenge. The majority of the studies in this review compared their respective experimental turning schemes with the 2-hour turning intervaldthe clinical “gold standard” most commonly used in practice [14-16]. Taken together, the studies compared an every 2-hour turning schedule with frequencies of 2, 4, or every 6-hour turns; however, other factors such as mattress type and additional bolstering or turning were not held constant [42,43,45]. A 4-hour turning schedule combined with use of a pressurereducing mattress was associated with the lowest risk of PU occurrence across groups; however, controlling for confounders was not adequate to disentangle advantages of a specific turn schedule versus mattress type. Further, no particular weight redistribution or regular repositioning in bed schedule was associated with a lack of PU development [13]. Hence, no clinically meaningful inference about an “optimal” turning interval in bed can be concluded from the existing literature. Sitting Pressure and Pressure Relief Maneuvers Of the topical areas addressed in this review, seated pressure measurement and pressure relief maneuvers had the largest total number of participants, the majority of which involved tilting and reclining in power

S.L. Groah et al. / PM R XXX (2015) 1-24

wheelchairs, with assessment of push-ups, leaning, tilting, and reaching in manual wheelchairs to a lesser extent. In general, the greater the tilt or recline angle from neutral, the greater the pressure relief over the sitting areas. Tilting from neutral to 90 linearly decreases ischial and sacral pressures while redistributing pressure to the back. Reclining from neutral to 30 had a negligible effect on pressure, with more substantial reductions in sitting pressure beyond 30 ; however, the benefits needs to be weighed against greater generated shear forces when reclining 30 and beyond. Forward leaning (with a suggestion that diagonal forward leaning is superior) provides the greatest amount of pressure relief while avoiding the shearing associated with reclining. Although forward leaning was associated with the greatest amount of pressure relief, pressures do appear to increase during the initial part of the maneuver. Furthermore, findings from several laboratorybased studies suggest a wide range of duration of pressure relief needed to return skin perfusion to prepressure levels (1-3 minutes) [64]. This duration may also be related to the applied loads and frequency of pressure relief maneuvers, indicating a need for individualization of recommendations [57]. Likewise, crosssectional studies of patient-reported behaviors and PUs have not yielded conclusive findings as to the benefit of repositioning [88-90]. Admittedly, with the large number of PU risk factors combined with heterogeneity among patients, equipment, and support surfaces, determining a cause and effect relationship between any particular type or frequency of pressure relief would be exceedingly costly and challenging. Clinical Applications The results of this review are largely inconclusive, stemming from the wide variability in skin physiology and response to stress and pressure due to many factors, all of which contribute to an overall “paucity of evidence.” Further, these inconclusive results have significant policy implications. The National Qualify Forum (NQF) appropriately classifies PUs as “serious reportable events” that are “largely preventable and of concern to both the public and to healthcare providers” [91]. Reporting of PUs can demonstrate trends that hospitals and providers can react to, and perhaps they can subsequently implement policy change that reduces the incidence and/or severity of PUs. However, it is unfortunate that because most of NQF’s “serious reportable events” carry with them liability and negligence assumptions, the “implicit yet incorrect assumption that PU’s develop exclusively from improper care or lack of quality care” has become relatively commonplace [92]. Although PUs clearly can be the result of negligent care, they can also occur in the setting of implementation of best evidence-based practices for holistic care of the individual.

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Further, our results call into question (1) the universal classification of stage III and IV PUs as “never events,” defined by Centers for Medicare and Medicaid Services as “non-reimbursable serious hospital-acquired conditions,” and (2) the Federal Register statement that PUs can be “reasonably prevented through the application of evidence-based guidelines” [93]. A more accurate statement might be that PUs can be “reasonably prevented through the application of evidence-based guidelines when clinically appropriate.” “Never events” involve motivation to improve patient safety through nonreimbursement; however, nonreimbursement for the costs associated with development of a condition in favor of prevention of another condition with greater morbidity and mortality risk does not represent meaningful progress toward improved patient safety. The evidence and clinical experience indicate that not all “serious reportable events” and “never events” are preventable [94] at all times or indicative of obvious negligence [95]. Although PUs are clearly “serious reportable events,” the evidence is surprisingly weak and does not support the supposition that existing guidelines will prevent all PUs, nor does it support guideline applicability across all populations. Rather, the evidence suggests that different populations and individuals within given populations react very differently to pressure applied to the skin. Furthermore, the evidence base upon which our existing guidelines are based is extremely limited, and hence these guideline recommendations should be considered more accurately as an initial framework for prevention. If anything, the evidence suggests that best PU prevention should be highly individualized and reassessed often with modifications if necessary, with the SCI population at greater risk than other hospitalized populations because of the severity of neurologic impairment, and that the best prevention may be a “moving target” depending on individual characteristics, comorbidities, and equipment. Conclusions Evidence supports avoiding the 90 lateral position because of the risk of PU formation over the trochanters; however, no clear trends recommend for or against any other bed positions. During sitting, pressures are linearly redistributed from the sitting area during recline and tilt, but reclining carries with it an increased risk of shear forces on this skin. Beyond this finding, the evidence does not support conclusive guidelines on positioning or repositioning techniques for PU prevention, which includes the clinical “gold standard” recommendation of turning every 2 hours while in bed and pressure relief maneuvers ranging anywhere from every 15 minutes to hourly. Rather, the evidence suggests that PU risk is highly individualized (and risk may

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vary within an individual given a variety of circumstances), which demands flexible PU prevention strategies based on individual characteristics and response to a particular type of support surface and repositioning protocols. Consideration needs to be given to more frequent turning (adding to burden of cost), liberal use of pressure-relieving support surfaces, and/or use of rotating support surfaces. Based on the existing evidence, current “guidelines” cannot be considered evidence based, and consideration should be given to re-evaluating existing guideline-based turning intervals for this high-risk population. Despite the impressive investment in scientific synthesis, practice guideline development, and education, a dramatic decline in the incidence of PUs has yet to be realized [96-98]. Fortunately, most persons with SCI and health care professionals are keenly aware of the risks for PUs, their disruptive effects, and the resources needed to manage a new ulcer [99]. Education has and will remain our most powerful ally to thwart this pervasive public health problem. Acknowledgment We thank Katherine Schomer, who was at the U.W. Model Systems Knowledge Translation Center at the time this study was performed, for assisting with article identification and data extraction, and Brenda Tsai of MedStar National Rehabilitation Hospital for her assistance with illustrations.

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Disclosure S.L.G. MedStar National Rehabilitation Hospital, 102 Irving St., NW, Washington, DC 20010; Department of Rehabilitation Medicine, MedStar Georgetown University Hospital, Washington, DC. Address correspondence to: S.L.G.; e-mail: [email protected] Disclosure: nothing to disclose M.S. MedStar National Rehabilitation Hospital, 102 Irving St., NW, Washington, DC 20010; MedStar Health Research Institute, Hyattsville, MD; Washington, DC Veterans Affairs Medical Center, Washington, DC Disclosure: nothing to disclose C.G.P. MedStar National Rehabilitation Hospital, 102 Irving St., NW, Washington, DC 20010; Department of Rehabilitation Medicine, MedStar Georgetown University Hospital, Washington, DC; MedStar Montgomery Medical Center, Olney, MD Disclosure: nothing to disclose

C.-H.J.H. MedStar National Rehabilitation Hospital, 102 Irving St., NW, Washington, DC 20010; MedStar Health Research Institute, Hyattsville, MD Disclosure: nothing to disclose This project was funded by the Rehabilitation Research and Training Center on Secondary Conditions after Spinal Cord Injury (H133B090002) and the Model Systems Knowledge Translation Center (H133A060070) from the National Institute on Disability and Rehabilitation Research, Office of Special Education and Rehabilitative Services, U.S. Department of Education, Washington, DC. Submitted for publication July 31, 2014; accepted November 29, 2014.

Prevention of Pressure Ulcers Among People With Spinal Cord Injury: A Systematic Review.

To evaluate the literature on the effectiveness of bed and wheelchair positioning and repositioning in the prevention of pressure ulcers (PUs) in both...
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