Long-Term Prevention of Pressure Ulcers in High-Risk Patients: A Single Case Study of the Use of...

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RIEF REPORT

ong-Term Prevention of Pressure Ulcers in High-Riskatients: A Single Case Study of the Use of Glutealeuromuscular Electric Stimulation

ath M. Bogie, DPhil, Xiaofeng Wang, MS, Ronald J. Triolo, PhD

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ABSTRACT. Bogie KM, Wang X, Triolo RJ. Long-termrevention of pressure ulcers in high-risk patients: a single casetudy of the use of gluteal neuromuscular electric stimulation.rch Phys Med Rehabil 2006;87:585-91.

Objective: To evaluate the efficacy of gluteal neuromuscu-ar electric stimulation (NMES) using implanted percutaneouslectrodes to improve regional tissue health and decrease theisk of pressure ulcer development.

Design: Case study of long-term use of gluteal NMES.Setting: Community.Participant: A patient with a C4-level American Spinal

njury Association grade A spinal cord injury, 22 years postin-ury at study enrollment, and a clinical history of regular gradeI and occasional IV ischial pressure ulcers.

Intervention: Gluteal NMES using an electric stimulationystem comprising a combination of implanted percutaneouslectrodes and an external stimulator (controller).

Main Outcome Measures: Objective measurements of tis-ue health comprising evaluation of gluteal muscle thickness,nterface pressures, and regional blood flow. Subjective self-eported sitting tolerance.

Results: Increased gluteal muscle thickness and blood flowogether with reduced regional interface pressures occurred.

eight-shifting because of alternating left and right glutealMES became more effective over time as the muscles

trengthened. Sitting tolerance more than doubled.Conclusions: A gluteal NMES system has been developed that

rovides both improved regional tissue health and dynamic weighthifting while seated in the wheelchair. In the current case, regularaily use had a positive impact on multiple indirect indicators ofissue health. Continued use was indicated as the positive effectsere lost when stimulation was discontinued.Key Words: Decubitus ulcer; Electric stimulation; Rehabil-

tation; Spinal cord injuries.© 2006 by the American Congress of Rehabilitation Medi-

ine and the American Academy of Physical Medicine andehabilitation

From the Department of Orthopaedics (Bogie, Triolo) and Statistics (Wang), Caseestern Reserve University, Cleveland, OH; and Cleveland VA Medical Center,

leveland, OH (Bogie, Triolo).Presented in part to the American Spinal Injuries Association and Internationaledical Society of Paraplegia, May 3-6, 2002, Vancouver, BC, Canada.Supported by the Spinal Cord Research Foundation, Paralyzed Veterans of Amer-

ca; the Rehabilitation Research and Development Service, Department of Veteransffairs; and the MetroHealth Medical Center General Clinical Research Center,leveland, OH. Devices were provided by NeuroControl Corp, Cleveland, OH.No commercial party having a direct financial interest in the results of the research

upporting this article has or will confer a benefit upon the author(s) or upon anyrganization with which the author(s) is/are associated.The device used in this study is being evaluated under an investigational device

xemption from the U.S. Food and Drug Administration.Reprint requests to Kath M. Bogie, DPhil, Cleveland FES Center, Hamann Bldg,

m 601, MetroHealth Medical Center, 2500 MetroHealth Dr, Cleveland, OH 44109-998, e-mail: [email protected].

m0003-9993/06/8704-10405$32.00/0doi:10.1016/j.apmr.2005.11.020

EOPLE WITH DECREASED MOBILITY are at increasedrisk of tissue breakdown leading to pressure ulcer devel-

pment. In many cases, chronic loss of mobility also leads tother factors that negatively impact tissue health, such asisuse muscle atrophy. People with spinal cord injury (SCI),nd in particular complete SCI, are an example of a patientroup for whom pressure ulcers remain a significant risk at allimes after injury. Indeed, pressure ulcers represent a majorecondary complication that can require prolonged periods ofedrest and hospital admission for treatment. Pressure ulcershus often affect many activities of daily living and reduceunctional independence. In addition, further medical compli-ations can arise, including systemic infections leading to sep-icemia and death.

Although pressure ulcers are sometimes still referred to asedsores, many wheelchair users develop pelvic region pres-ure ulcers near the ischial tuberosities while sitting. Tradi-ional techniques to reduce pressure ulcer incidence have fo-used on extrinsic risk factors (eg, by providing cushions thatmprove regional pressure distribution). Rehabilitation pro-rams also provide wheelchair users and their caregivers withducation on the importance of regular pressure-relief proce-ures.However, there remains a significant number of people who,

espite the best standards of care, continue to develop majorressure ulcers. These people are frequently unable to maintainregular pressure-relief regimen, and pressure relief cushions

re inadequate. A primary factor is the intrinsic changes in thearalyzed body, which lead to poor extrinsic pressure distribu-ions. Severe disuse muscle atrophy reduces the contact areaith the support surface, thus increasing interface pressuresver bony prominences. Regional blood flow is also adverselyffected both because of loss of blood vessels and reducedatency of the remaining vascular supply.It is known anecdotally that regular use of neuromuscular

lectric stimulation (NMES) for functional applications canroduce changes in regularly stimulated muscles that mayncrease the health of the muscle and surrounding soft tissues.hese changes have rarely been reported as the primary goal

or using NMES; however, various authors have reported onmprovements in factors related to tissue health as a sideffect of using electric stimulation for functional applica-ions, such as standing or systemic exercise. For example,aylor et al1 found that subjects who received surface elec-

ric stimulation for muscle conditioning during the trainingegimen for use of the Odstock functional electric stimula-ion (FES) standing system exhibited positive changes inegional tissue health. Significant increases in thigh bloodow and quadriceps muscle depth were found after following

he 3-month training regimen. Scremin et al2 also found sig-ificant increases in muscle cross-sectional area in subjectsith SCI who followed a weekly regimen of FES-induced

ower-extremity cycling incorporating surface electrodes. Me-ium-term follow-up was reported. Scremin2 found that in-reases in muscle size were directly related to proximity of the
uscle to the stimulating electrodes.
Arch Phys Med Rehabil Vol 87, April 2006

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586 LONG-TERM PRESSURE ULCER PREVENTION WITH NMES, Bogie

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As indicated earlier, published reports on studies that haveocused on the use of electric stimulation to improve tissueealth are limited. Levine et al3 found that surface stimulationf the gluteus maximus increased regional blood flow in SCIubjects. However, there was no preassessment use of stimu-ation to provide muscle conditioning nor was long-term use oftimulation reported. The effect on the SCI subjects assessedas found to be small. In previous work, we have found that

ubjects using an implanted NMES system to provide standingnd facilitate transfers exhibit positive changes in tissueealth.4 These subjects included regular stimulation of theluteal muscles as part of their exercise and standing routinesnd showed statistically significant reductions in ischial inter-ace pressures.

The hypothesis to be established by the current study is thatxercise of paralyzed gluteal muscles using implanted elec-rodes will improve the intrinsic health of the tissue at theeating interface as determined by reductions in regional inter-ace pressures and enhanced regional blood flow, together withncreased gluteal thickness. In addition dynamic weight shift-ng produced by the gluteal NMES system would vary seatedosture and pressure distributions at the seating interface andugment the efficacy of conventional pressure relief maneu-ers.A 4-channel percutaneous gluteal NMES system was devel-

ped to investigate this hypothesis. The semi-implanted sys-em comprises implanted percutaneous electrodes togetherith an external stimulator. The short- and long-term effectsf regular use on tissue health have been evaluated. Earlyesults on the use of this system, used only for glutealtimulation, indicated positive changes in tissue health.5,6

hese findings imply that therapeutic NMES provides anique intrinsic approach to reducing the risk of pressurelcer development for people with compromised tissue pa-ency and decreased independent mobility. No long-term re-ults have been presented to date. There are currently 3 activeegular users of this system. A single case study is presented ofhe first participant recruited to this ongoing study. This subjectith chronic SCI has been using gluteal NMES on a routineaily basis for over 7 years.

METHODSThe participant, GP, was a 42-year-old man who had sus-

ained an American Spinal Injury Association grade A SCI athe level of C4 22 years before enrollment in the study. Heeported a history of regularly occurring grade II ischial pres-ure ulcers, often requiring a week or 2 of bedrest for treatment.e had also undergone surgical closure of grade IV pressurelcers twice; during the first year postinjury and then again atround 20 years postinjury. He was using a power wheelchairith tilt-in-space capabilities and had been prescribed a RoHoressure cushion. At enrollment in the study, GP reported thate was unable to sit for more than 6 hours a day and that heould regularly need to spend a week or so on bedrest becausef grade II ischial region ulcers. He was ectomorphic (bodyass index �15.0kg/m2) with marked disuse muscle atrophy in

he lower limbs and pelvic region.GP received a 4-channel percutaneous gluteal NMES system

n September 1997. Stimulating electrodes were implantedilaterally in the gluteus maximus muscle under sterile condi-ions. Local anesthesia was used to minimize the risk of anutonomic dysreflexic response. The stimulating tip of thelectrode was located in the gluteus maximus near the motoroint of the inferior gluteal nerve innervating the muscle,audal to the sitting interface. The electrode lead was then
unneled subcutaneously to an exit site on the anterior aspect of s
rch Phys Med Rehabil Vol 87, April 2006

he thigh. To achieve maximal recruitment of the muscle, 2lectrodes were implanted on each side, thus providing a-channnel stimulation system (fig 1). This approach also pro-ided some built-in redundancy in case of electrode failureecause the system could be reprogrammed to remain func-ional with less than 4 channels. The stimulation was controlledy an external pager-sized stimulator.a The entire procedureook around 4 hours and was performed on an outpatient basis.he patient was discharged to home and instructed to remainn bedrest for 7 days postprocedure.Three weeks after implantation, GP started using the system

o provide conditioning stimulation to increase gluteal muscletrength and fatigue resistance. Stimulation was delivered at0Hz concurrently to the left and right glutei with a duty cyclef 8 seconds on and 4 seconds off. Treatment time was pro-ressively increased over a period of 6 weeks to a maximum ofhours a night, applied when GP was lying in bed.After completing the conditioning protocol, GP started

sing the dynamic stimulation regimen, which enabled himo achieve weight shifting while seated in the wheelchair.lternating left and right gluteal NMES was applied at 20Hzith a duty cycle of 15 seconds on and 15 seconds off to

ach muscle. Stimulation was applied for a 3-minute period,ith a 17-minute interstimulation interval, approximating

he frequency of weight shifting recommended for wheel-hair users at risk of tissue breakdown. The dynamic stim-lation regimen could be used for up to 10 hours a day whileitting in the wheelchair.

GP used dynamic stimulation daily for 6 months. Stimula-ion was then withdrawn for 3 months, after which time he wasiven the option of retaining the system. GP elected to retainhe gluteal NMES system and has currently been using the

Fig 1. Percutaneous gluteal stimulation system.

ystem on a regular, daily basis for over 7 years.

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587LONG-TERM PRESSURE ULCER PREVENTION WITH NMES, Bogie

Tissue health assessments were performed every 3 monthsuring the first year of participation and then annually forong-term follow-up. The assessment procedure included con-urrent measurement of seated interface pressures (Advancedlinical Seating Systemb) and ischial region tissue oxygen

evelsc while seated in the wheelchair, both with and withoutynamic stimulation. This allowed both long-term musclehanges and short-term effects of stimulated muscle contrac-ions to be evaluated. Tissue oxygen levels were also evaluatedn the ischial region while unloaded to determine long-termhanges in regional tissue blood flow.

Furthermore, gluteal muscle thickness was evaluated byomputed tomography. Axial images were obtained with theubject lying supine and the buttocks suspended between pil-ows to allow measurement of unloaded tissue thickness. Im-ges were obtained at 3 levels through the muscle, includinghe inferior aspect of the sacroiliac joints. In addition to therimary outcome measures, GP gave anecdotal feedback re-arding the effect of the gluteal NMES system on his overalluality of life and skin health in particular.

RESULTS

issue Health AssessmentsInterface pressure measurements. Real time 3-dimen-

ional images of pressure distributions at the seating interfacere produced by using the graphical display software.b In the

ig 2. Unprocessed pressure dataaps for static mode seated pres-

ure distribution. Each imagehows a representative interfaceressure distribution at the cush-

on-subject interface (single framerom a 400-frame dataset). (A)aseline, (B) initial daily use (post-onditioning), (C) 6 months ofaily use, and (D) 40 months ofegular use. Images are orientateduch that the thighs are toward tohe left of the image and the righthigh toward the top. Each pixelorresponds to a calibrated inter-ace pressure value (see legend).

urrent study, pressure map datasets (movies) comprised 400 m

equential maps (frames). Raw data were displayed as a 2-di-ensional map (figs 2, 3) and can also be shown as 3-dimen-

ional “mesh.” System software can be used to determine meannd maximum pressures, both for the overall region and forbserver-selected regions of interest. However, there is noapability for objective comparison of series of pressure mapatasets obtained over time. There is also no facility for sta-istical analysis to determine the significance of any observedifferences.The Longitudinal Analysis with Self-Registration (LASR)

tatistical algorithm was developed to meet these needs.7 In theurrent study, pressure-mapping assessments were performedver a period of several years. Assessment of seating postureas carried out both during quiet sitting (static mode) anduring application of alternating gluteal NMES (dynamicode). Although care was taken to position the subject in the

ame way at each assessment, it was not feasible to ensure anxact reproduction of seating posture at each visit.

Spatial registration was required to ensure that pressureaps were aligned. It was expected that alternating gluteal

ontractions would lead to dynamically varying regional inter-ace pressures. Therefore, to assess the effects of continued usef NMES over time, it was necessary to ensure that dynamicode pressure maps were compared at the same phase of

timulation (eg, when left-side stimulation was on). Temporalegistration was therefore required for dynamic mode pressure
ap datasets to ensure synchronous comparisons.

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The multistage LASR algorithm thus includes both spatialnd temporal self-registration of pressure maps to allow intra-ubject comparison of repeated assessments over time. Theocations of significant pressure reductions can be determinedver the entire pressure map area without the need for predefi-ition of areas of interest by the observer.After registration, pixel-by-pixel (and frame-by-frame)

omparisons are made to determine absolute differencesetween datasets of interest. The P values are then calcu-ated pixel by pixel for each frame to determine the loca-ion(s) of significant differences. In any situation in whichultiple statistical tests are performed, it is necessary to

pply a correction factor to minimize the occurrence of falseositives (ie, spuriously valid statistical results). The sim-lest approach is known as the Bonferroni adjustment, andhis should be used when more than 4 or 5 statistical tests arepplied simultaneously. In the current situation, severalhousand simultaneous tests are applied. A false discoveryate (FDR) procedure was applied to adjust P values in thisesting environment. Specifically, if the P value at point X isess than the critical value derived from the FDR-controlledrocedure, then the pixel value is set to 1 – P. If P is greaterhan the critical value, then the pixel value is set to zero. Theesulting FDR-controlled P maps or movies (for multiplerames) show areas that exhibit improvements in interfaceressures, implying improved tissue health.Figures 4 and 5 show LASR output maps for repeated

ssessments of subject GP. The first (left) panels show dif-
erence maps between registered datasets of interest. The i

econd panels show FDR-controlled P maps. These give araphical representation of the location of statistically sig-ificant change, calculated simultaneously for every dataoint over the entire contact area. Each positive pointgreen) represents a point where the pre-post differences aretatistically significant.

Interface pressure distribution appeared to show somehanges over time, in particular between baseline and initialaily use. LASR analysis of static mode pressure maps showedhat statistically significant reductions in seated interface pres-ures occurred even after only 6 weeks of conditioning stimu-ation (see fig 4A). At 40-month follow-up, LASR analysisndicated few significant changes in interface pressure distri-ution relative to 6 months of daily use (see fig 4C), implyinghat initial reductions had been maintained.

LASR analysis of dynamic mode pressure maps showed thatressure variations caused by the gluteal NMES regimen in-reased significantly over time, implying a more effectiveeight-shifting effect. Figure 3 shows single-frame snapshotsf pressure data obtained when applying gluteal NMES toroduce weight shifting. Corresponding LASR analysis mapsre shown in figure 5. From the single-frame snapshots, it cane inferred that the magnitude of interface pressure variationsncreased in the gluteal region over the first 6 months of usesee fig 5A). Furthermore, this effect was maintained withontinued long-term use up to 40 months (see fig 5B). Tem-oral variations in pressure distribution characteristics are bestiewed as multiple sequential pressure maps or pressure mov-

Fig 3. Unprocessed pressure datamaps for dynamic mode seatedpressure distribution (snapshots).Each image shows a representa-tive interface pressure distributionat the cushion-subject interface(single frame from a 400-framedataset). (A) Initial daily use, (B) 6months of daily use, and (C) 40months of regular use. Images areorientated such that the thighs aretoward to the left of the image andthe right thigh toward the top.Each pixel corresponds to a cali-brated interface pressure value(see legend).

es. Similarly, more comprehensive information can be re-

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rieved from LASR analysis for dynamic mode pressure mapsy viewing LASR analysis movies, which show significantifferences frame by frame. Complete LASR movies for theongitudinal changes in response to gluteal NMES can beiewed at http://stat.case.edu/lasr/.Tissue oxygen levels were found to improve over time with

ontinued use of gluteal NMES. Concurrent with rapid positivehanges in interface pressures, the most rapid increase wasbserved during the initial conditioning phase. Increased levelsere sustained during regular use of dynamic stimulation butecreased on withdrawal (fig 6).It has previously been shown that maximum gluteal muscle

hickness showed a significant increase after the conditioningtimulation program.6 Long-term follow-up now shows thathis increased muscle thickness is maintained with regular usef gluteal NMES (fig 7).Sitting tolerance and quality of life. Since commencing

egular use of the gluteal NMES system, GP has had 1 minorncident of skin breakdown because of a poor chair-to-bedransfer. This resolved after 2 days of bedrest. GP reported thatt would previously have required about 1 week of bedrest toeal.GP also reported that his sitting tolerance had increased from

bout 6 hours a day to in excess of 12 hours a day. He has been

ig 4. LASR analysis maps for staticode seated pressure distributions

howing areas of significant changever time, adjusted for simultaneousesting at multiple locations. (A) Base-ine versus initial daily use (postcondi-ioning), (B) initial versus 6 months ofaily use, and (C) 6 months of use ver-us 40 months of use; (left) differenceap, (right) FDR P maps.

ble to maintain part-time employment for over 2 years. GP m

argely attributed this to the fact that he was no longer worriedbout recurrent skin problems requiring significant periods ofedrest.

DISCUSSION

Many wheelchair users with chronically impaired mobilitynd reduced tissue health are affected by pressure ulcers.onventional methods of prevention are not universally effec-

ive. The current case study has shown that regular daily usef therapeutic gluteal NMES can have a positive impact onultiple indirect indicators of tissue health, including in-

reased muscle thickness and blood flow together with re-uced regional interface pressures. In addition to the long-erm changes in muscle characteristics, alternating glutealMES dynamically alters conditions at the seating support

nterface because of stimulated muscular contractions facilitat-ng periodic changes in interface pressure. This dynamic effectncreases over time because the paralyzed muscles becometronger with regular use of gluteal NMES. To our knowledge,o other studies have been published that report on the long-erm effect of regular gluteal NMES usage specifically formprovement of tissue health.

Our findings imply that use of therapeutic NMES for the
aintenance of tissue health may be an effective adjunctive

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ethod of preventing pressure ulcers. Daily use of NMES isndicated to maintain hypertrophy of paralyzed muscles. Sur-ace electric stimulation has reduced efficacy in this applicationoth clinically and practically. The inferior gluteal nerve lieselatively deep to the buttock surface and close to the sciaticerve. Surface electrode placement for preferential recruitmentf the inferior gluteal nerve can be difficult for users to achieve.oreover, repeatable electrode placement in the upper buttock

egion is hard to accomplish for either independent users orheir caregivers.

Implanted NMES systems for long-term therapeutic useave dual advantages. The stimulating tip of the electrode cane located very close to the motor point of the nerve of interest,hus reducing the charge required to elicit a contractile re-

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ponse. Furthermore, the user does not have to replace thetimulating electrode every day so the system becomes bothore reliable and simpler to use.Findings from our study indicate that daily use of an im-

lanted gluteal NMES system may be well accepted by usersie, practically effective). Positive changes were observed in allutcomes measures, implying that the gluteal NMES system islso clinically effective.

CONCLUSIONSThe findings from this case study support the hypothesis that

ong-term use of gluteal NMES using implanted systems mayrovide an adjunctive method for achieving a regular pressure

Fig 5. LASR analysis maps for dynamicmode seated pressure distributionsshowing areas of significant changeover time adjusted for simultaneoustesting at multiple locations (snap-shots). (A) Initial use versus 6 monthsof daily use, and (B) 6 months of useversus 40 months of use; (left) differ-ence map, (right) FDR P maps.

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elief regimen in high-risk persons. This can reduce the risk ofressure ulcer development and allow users to participate moreully in activities of daily living, including employment andocietal interaction. Further long-term study of gluteal stimu-ation users is required to confirm that the positive effects ofegular usage of NMES are seen in other people at high risk forressure ulcer development.Because of continuing paralysis withdrawal of stimulation

esults in a reversal of improved tissue health. Continuous usef gluteal NMES is therefore indicated for individuals at highisk of pressure ulcer development. For increased ease andeliability of long-term use, fully implanted stimulation sys-ems would be indicated.

References. Taylor PN, Ewins DJ, Fox B, Grundy D, Swain ID. Limb blood

flow, cardiac output and quadriceps muscle bulk following spi-nal cord injury and the effect of training for the Odstockfunctional electrical stimulation standing system. Paraplegia1993;31:303-10.

. Scremin AM, Kurta L, Gentili A, et al. Increasing muscle massin spinal cord injured persons with a functional electrical stim-ulation exercise program. Arch Phys Med Rehabil 1999;80:1531-6.

. Levine SP, Kett RL, Gross MD, Wilson BA, Cederna PS, Juni JE.Blood flow in the gluteus maximus of seated individuals duringelectrical muscle stimulation. Arch Phys Med Rehabil 1990;71:682-6.

. Bogie KM, Triolo RJ. Effects of regular use of neuromuscularelectrical stimulation on tissue health. J Rehabil Res Dev 2003;40:469-75.

. Triolo RJ, Bogie KM. Lower extremity applications of functionalneuromuscular stimulation after spinal cord injury. Top SpinalCord Inj Rehabil 1999;5:44-65.

. Bogie KM, Reger SI, Levine SP, Sahgal V. Electrical stimulationfor pressure sore prevention and wound healing. Assist Technol2000;12:50-66.

. Bogie KM, Wang X, Sun J. LASR: a new analytical tool to increaseinformation retrieval from complex images. In: Proceedings of theJoint XXth Congress of the International Society of Biomechanicsand 29th Annual Meeting of the American Society of Biomechan-ics; 2005 July 31-Aug 5; Cleveland (OH).

Suppliers. NeuroControl Corp, 8333 Rockside Rd, Valley View, OH 44125.. Tekscan Inc, 307 W First St, South Boston, MA 02127.. TINA TCM-3; Radiometer America Inc, 810 Sharon Dr, Westlake,

OH 44145.

ig 7. Computed tomography scans of gluteal muscle thicknesshowing the transverse section through top of the head of theemur. (A) At baseline, maximum thickness of 9mm (left) and 10mmright). (B) At 1-year follow-up, maximum thickness 14mm (left) and


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