risk factors for pressure ulcer development in critically ill patients: a conceptual model to guide...

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Research in Nursing & Health Risk Factors for Pressure Ulcer Development in Critically Ill Patients: A Conceptual Model to Guide Research Richard Benoit, * Lorraine Mion ** Vanderbilt University School of Nursing, 461 21st Avenue South, Nashville, TN 37240 Accepted 20 March 2012 Abstract: This paper presents a proposed conceptual model to guide research on pressure ulcer risk in critically ill patients, who are at high risk for pressure ulcer development. However, no conceptual model exists that guides risk assessment in this population. Results from a review of prospective studies were evaluated for design quality and level of statistical reporting. Multivariate findings from studies having high or medium design quality by the National Institute of Health and Clinical Excellence standards were conceptually grouped. The conceptual group- ings were integrated into Braden and Bergstrom’s (Braden and Bergstrom [1987] Rehabilitation Nursing, 12, 8–12, 16) conceptual model, retaining their original constructs and augmenting their concept of intrinsic factors for tissue tolerance. The model could enhance consistency in research on pressure ulcer risk factors.ß 2012 Wiley Periodicals, Inc. Res Nurs Health Keywords: pressure sore; skin care; critical care; nursing; conceptual model Pressure ulcers and the risk factors that con- tribute to their development have been studied for almost 50 years, yet the combination of risk factors that best predict pressure ulcer incidence is still poorly understood. Risk factors for pressure ulcer incidence vary with unique patient populations, such as those requiring care in long-term environments or those requiring short-term care in acute and critical care environments (de Laat, Schoonhoven, Pickkers, Verbeek, & van Achterberg, 2006). However, existing conceptual models to explain associa- tions between risk factors and pressure ulcer development generally do not have a specific patient population orientation. Although knowledge about pressure ulcer risk factors is plentiful, it is difficult to apply to various patient populations, leaving clinicians with a variety of risk assess- ment tools that may not be well suited for the patient populations they serve. Pressure ulcer risk factor research has been fraught with methodological and definitional inconsistencies that complicate and slow the process of translating research into clinical practice (Keller, Wille, van Ramshorst, & van der Werken, 2002). Of the populations studied, patients who are critically ill (i.e., receiving care in an intensive care unit [ICU]) are the Correspondence to Richard Benoit *PhD Candidate. **Independence Foundation Professor of Nursing. Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/nur.21481 ß 2012 Wiley Periodicals, Inc.

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Page 1: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Research in Nursing & Health

Risk Factors for PressureUlcer Development in Critically IllPatients: A Conceptual Model to

Guide Research

Richard Benoit,* Lorraine Mion**

Vanderbilt University School of Nursing, 461 21st Avenue South, Nashville, TN 37240

Accepted 20 March 2012

Abstract: This paper presents a proposed conceptual model to guideresearch on pressure ulcer risk in critically ill patients, who are at highrisk for pressure ulcer development. However, no conceptual model existsthat guides risk assessment in this population. Results from a reviewof prospective studies were evaluated for design quality and level ofstatistical reporting. Multivariate findings from studies having high ormedium design quality by the National Institute of Health and ClinicalExcellence standards were conceptually grouped. The conceptual group-ings were integrated into Braden and Bergstrom’s (Braden and Bergstrom[1987] Rehabilitation Nursing, 12, 8–12, 16) conceptual model, retainingtheir original constructs and augmenting their concept of intrinsic factorsfor tissue tolerance. The model could enhance consistency in research onpressure ulcer risk factors.� 2012 Wiley Periodicals, Inc. Res Nurs Health

Keywords: pressure sore; skin care; critical care; nursing; conceptual model

Pressure ulcers and the risk factors that con-tribute to their development have been studiedfor almost 50 years, yet the combination of riskfactors that best predict pressure ulcer incidenceis still poorly understood. Risk factors forpressure ulcer incidence vary with uniquepatient populations, such as those requiring carein long-term environments or those requiringshort-term care in acute and critical careenvironments (de Laat, Schoonhoven, Pickkers,Verbeek, & van Achterberg, 2006). However,existing conceptual models to explain associa-tions between risk factors and pressure ulcerdevelopment generally do not have a specific

patient population orientation. Although knowledgeabout pressure ulcer risk factors is plentiful, it isdifficult to apply to various patient populations,leaving clinicians with a variety of risk assess-ment tools that may not be well suited for thepatient populations they serve.Pressure ulcer risk factor research has been

fraught with methodological and definitionalinconsistencies that complicate and slow theprocess of translating research into clinicalpractice (Keller, Wille, van Ramshorst, & vander Werken, 2002). Of the populations studied,patients who are critically ill (i.e., receivingcare in an intensive care unit [ICU]) are the

Correspondence to Richard Benoit*PhD Candidate.**Independence Foundation Professor of Nursing.Published online in Wiley Online Library

(wileyonlinelibrary.com). DOI: 10.1002/nur.21481

� 2012 Wiley Periodicals, Inc.

Page 2: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

most prone to the development of pressureulcers (Bours, de Laat, Halfens, & Lubbers,2001; de Laat et al., 2006), yet few investigatorshave systematically evaluated the predictiverelationships between risk factor presence andpressure ulcer development in this population.The purposes of this discussion paper are to

� review and critique the literature on patient-specific pressure ulcer risk factors describedin prospectively designed acute and criticalcare studies;

� review existing patient-specific conceptualmodels for pressure ulcer etiology; and

� augment an existing model with significantfindings from the literature to create aconceptual model that more completelydescribes the etiology of pressure ulcers incritically ill patients.

Environmental and Patient-SpecificPressure Ulcer Risk Factors

The etiology of pressure ulcer development ismultifactorial and not well understood (Nixon,2001; Nixon & McGough, 2001). Conceptually,patient outcomes are a function of the patient’sbaseline clinical, psychosocial, and demographic(i.e., patient) characteristics influenced by thetreatments received and the setting in whichthose treatments occur (i.e., environment-specific;Kane, 2006). Thus, pressure ulcer risk factorsinclude patient-specific variables that affect theindividual and environmental variables thataffect care delivery to the patient.

Environmental influences on patient outcomescan be categorized as nurse characteristics,such as educational level, attitude, and age(Aiken, Clarke, Cheung, Sloane, & Silber,2003), and administratively mediated variables,such as nurse staffing levels, nurse skill mix,hospital structural characteristics, patient careenvironments, and equipment (Aiken, Clarke,Sloane, Lake, & Cheney, 2008). Because suchvariables are generally outside the sphere ofcontrol of nurses delivering care to patients,this review is limited to a discussion of patientpopulation variables that influence pressureulcer development. A pressure ulcer risk factorwas defined as any patient-specific characteristic,occurring alone or in combination withothers, which either actually or theoreticallyinfluences a person’s risk for pressure ulcerdevelopment.

The Need for a Pressure Ulcer RiskFactor Conceptual Model forCritically Ill Patients

A conceptual model specific to pressure ulcerrisk in critically ill patients would focus preven-tion efforts and provide adequate risk stratifica-tion, thereby enhancing the data used tocompare quality outcomes across hospitals.Evidence from both descriptive and prospectivepredictive studies conducted in hospital environ-ments indicates that patients classified ascritically ill are at the greatest risk for pressureulcer development (de Laat et al., 2006; Shahin,Dassen, & Halfens, 2008; Theaker, Mannan,Ives, & Soni, 2000). The most recent Interna-tional Pressure Ulcer Prevalence Survey(IPUPS; VanGilder, Amlung, Harrison, &Meyer, 2009), conducted in 2008 and 2009,substantiates the disproportionate prevalence ofpressure ulcers in ICUs. Pressure ulcersacquired in the ICU had a prevalence rate of8.8–12.1% in 2008 and 2009, respectively,representing approximately 8,000–11,000 USpatients annually who developed a pressureulcer while in the ICU. In 2009, 3.3% ofUS ICU patients developed a severe facility-acquired pressure ulcer defined as Stage III,Stage IV, unstageable, or deep tissue injury(VanGilder et al., 2009). Use of a conceptualmodel designed to elaborate pressure ulcer riskin a critically ill patient will assist clinicians tobetter focus their prevention efforts.Adequate risk stratification is also essential

for accurate comparisons of adverse event ratesacross hospitals (Needleman, Kurtzman, &Kizer, 2007). There is a lack of empirical datasupporting the putative link between nursingprocesses and pressure ulcer incidence (Needlemanet al., 2007). This lack of data suggests a need fora more rigorous risk adjustment methodology tocontrol for the multiplicity of pressure ulcer riskfactors that may be functioning as confoundingvariables in pressure ulcer outcome research.Use of a conceptual model that more completelydescribes pressure ulcer risk factors in thecritically ill patient population would help toalign risk stratifications, giving clinicians moremeaningful comparisons of outcome data acrosshospitals (Needleman et al., 2007). This riskalignment would assist in identifying andsharing best practice strategies toward reducingpressure ulcer incidence.Currently, there is no conceptual model to

guide research into pressure ulcer risk factorsfor critically ill patients. Existing models

2 RESEARCH IN NURSING & HEALTH

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Page 3: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

include Braden & Bergstrom’s conceptualschema for the study of the etiology of pressuresores (Braden & Bergstrom, 1987; Fig. 1) andDefloor’s conceptual model (Defloor, 1999;Fig. 2). Both include the constructs of pressure

and tissue tolerance for pressure. Shearingforces and factors affecting oxygen delivery tothe tissues, although identified by both authors,assume greater importance in Defloor’s modelbecause they are identified as unique and

FIGURE 1. Braden and Bergstrom’s conceptual schema depicting factors in the etiology of pressuresores. From Braden and Bergstrom (1987). Reprinted with permission.

FIGURE 2. Defloor’s conceptual scheme. From Defloor (1999). Reprinted with permission.

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 3

Research in Nursing & Health

Page 4: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

equally important constructs contributing topressure ulcer risk. Both models include riskfactors that are frequently substantiated in theliterature (de Laat et al., 2006). However,neither was conceptually designed to depict riskfactors for pressure ulcer development in thecritically ill patient.

The Braden Scale for Predicting PressureSore Risk� (Copyright by Braden & Bergstrom,1988; Bergstrom, Braden, Laquzza, &Holman, 1987) is derived from Braden andBergstrom’s (1987) conceptual model. To date,Defloor’s (1999) conceptual model has noassociated risk assessment scale (RAS). Thepredictive ability of the Braden Scale hasbeen evaluated extensively in the literature(Pancorbo-Hidalgo, Garcia-Fernandez, Lopez-Medina, & Alvarez-Nieto, 2006), however itspredictive ability in critically ill patient popula-tions has not been widely evaluated. Table 1summarizes four studies of the Braden Scaleand cutoff scores in ICU settings. In threestudies, cutoff scores of 16 or less yieldedspecificities ranging from 22% to 63.9%. In twoof the three studies with larger sample sizesspecificities were lower (<30%). The samecutoff score had associated positive predictivevalues (PPVs) ranging from 15.3% to 60.6%.The results of these studies indicate that aBraden Scale score of 16 or less adequatelyidentifies patients at risk that do develop apressure ulcer, but the score is not specificenough to adequately screen out patients that donot develop a pressure ulcer.

These values indicate that ICU clinicians maylack an accurate tool that accounts for uniquepressure ulcer risk factors associated withcritically ill patients, resulting in a diffuseapplication of prevention efforts to patientsincorrectly identified to be at risk. Multiple

studies of the sensitivity and specificity ofvarious RAS, including the Braden Scale,indicate that none of them adequately identifypressure ulcer risk across various patientpopulations (Anthony, Parboteeah, Saleh, &Papanikolaou, 2008), raising doubt about theefficacy of any one tool to guide treatmentdecisions in nursing homes, in acute carefacilities, and ICUs.The goal of this review was to develop a

conceptual model to identify risk factors thataffect critically ill patients and thereby toinform and guide nursing care in the preventionof pressure ulcers in critically ill patients. This,in turn, could lead to developing and testinginterventions to minimize the effects of the riskfactors identified.

Overview of the ProcessUsed to IdentifyStudy Findings That Contributed to the

Proposed Model

First Level Inclusion Screening

A search of the PubMed database was con-ducted using the search terms ‘‘risk factors’’and ‘‘pressure ulcers,’’ with the limits of alladult, humans, core clinical and nursing journals,and English, but with no date constraints. Thesearch yielded 569 articles published between1975 and 2011. To refine the search to riskfactors for pressure ulcer development incritically ill patients, the search term ‘‘intensivecare’’ was added using the same limits. Thesearch returned 57 articles published from 1975to 2011. One duplicate article was identified inthe two search strategies, yielding 625 articles.Both authors independently screened the

Table 1. Braden Scale� Psychometrics in ICU Settings

Author Cutoff Score Setting N Sensitivity Specificity

Positive

Predictive

Value

Negative

Predictive

Value

Bergstrom, Demuth,

and Braden (1987)

Braden � 16 ICU 60 83.3 63.9 60.6 85.2

Cho and Noh (2010) Braden � 16 ICU 715 91.6 22.2 15.3 94.6

Lewicki, Mion,

and Secic (2000)

Braden � 14 ICU (cardiac

surgery)

337 66.6 29.6 4.5 94.7

Seongsook, Ihnsook,

and Younghee (2004)

Braden � 16 ICU 125 97.0 26.0 37.3 95.0

Note: ICU, intensive care unit.�Braden Scale for Predicting Pressure Sore Risk� (Copyright by Braden & Bergstrom, 1988).

4 RESEARCH IN NURSING & HEALTH

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Page 5: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

resulting search results for step-wise inclusionor exclusion from the model based on the crite-ria presented below. The authors then comparedtheir decisions to include or exclude articles. Incases of disagreement, consensus was reachedafter discussion.

Articles were screened and included forfurther review if they:

� were prospective in design with the primaryaim of identifying pressure ulcer riskfactors;

� identified development of pressure ulcer asthe dependent (outcome) variable;

� described patient-specific risk factors relatedto pressure ulcer development withoutexperimental intervention that could affectpressure ulcer incidence;

� were conducted on patients in acute carehospitals or in ICUs; and

� met the study design criteria identified bythe National Institute of Health and ClinicalExcellence (NICE, 2005), which are (a)shows adequate (>70%) participation ofeligible subjects; (b) contains conceptuallyrelevant risk factors; (c) provides studymethods including demographic informationand inclusion criteria; (d) allows adequatetime to capture the phenomenon of interest;and (e) provides a detailed report of the sta-tistical findings.

Findings in acute care facilities were includedbecause they have potential to generate find-ings generalizable to the critically ill ICUpopulation.

Of the 625 articles returned in the combinedsearches, 18 met the criteria outlined above.Seven studies, published between 1994 and2008, were designed to identify risk factors inpatients receiving care in ICUs who developedpressure ulcers. Eleven studies, publishedbetween 1987 and 2005, were designed toidentify risk factors in patients receiving care inacute care settings who developed pressureulcers.

Second Level Inclusion Screening

The reference lists from the 18 identified studieswere then evaluated to ensure that all studiesthat could contribute to the conceptual modelwere included. Using the same screeningcriteria listed earlier, 7 additional studies wereidentified for a total of 25 studies meeting the

inclusion criteria. Fourteen studies of riskfactors in patients in acute care hospital settings(Table 2) and 11 studies of risk factors in ICUpatients were identified (Table 3).

Profile of the Studies MeetingInclusion Criteria

Acute Care Studies

In the 14 studies of pressure ulcer risk factors inpatients in acute care settings (Table 2), datawere obtained on 37,883 patients (range 33–34,238) and 213 non-unique pressure ulcer riskfactors were evaluated as independent variables,91 of which were statistically significant atp � .05. Four of the studies were of exclusivelysurgical patients. These studies were includedin the acute care findings because they didnot indicate a need for ICU placement post-operatively, and the surgical interventions weremixed. In the two studies conducted by,Schoonhoven, Defloor, van der Tweel, Buskens,and Grypdonck’s (2002) and Nonnemacheret al. (2008), some patients required ICU careduring their hospitalizations but the risk factorassessment period was not limited to the ICUstay, therefore these studies were included inthe acute care risk factor group.

Critical Care Studies

In the 11 studies of pressure ulcer risk factorsin critically ill patients (Table 3), data wereobtained on 5,358 patients (range 36–2,615). Inthese studies, 170 non-unique pressure ulcerrisk factors were evaluated as independentvariables, 76 of which were statistically signifi-cant at p � .05. In two of the studies, riskfactors were evaluated in patients who hadundergone cardiac surgery (Lewicki, Mion,Splane, Samstag, & Secic, 1997; Papantonio,Wallop, & Kolodner, 1994). These studies wereincluded in the ICU findings because mostpatients who have had cardiac surgery require aperiod of ICU care post-operatively.

Exclusion Screening

The 25 studies listed in Tables 2 and 3 wereranked on the quality of their design using thequality rating assessment tool developed by

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 5

Research in Nursing & Health

Page 6: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

2.Pre

ssure

UlcerRiskFactors

inPatients

inAcute

Care

:A

Sum

mary

ofPro

spectiveStudiesPublish

edFro

m19

87to

2008

(N¼

14)

Study

TypeofSetting/P

atients

(N)

Outcom

eVariable

Dependent

Variables

Evaluated

Patients

With

Pre

ssure

Ulcers

(n)

StatisticallySignificantFindings�

Allm

an,Goode,

Patrick,Burs

t,and

Bartolucci(1

995)

Patients

adm

ittedto

urb

an

teachinghosp

ital(N

¼286)

Pre

ssure

ulcer

stageII–IV

2737

aIn

cre

ase

dage;dry

sacra

lsk

in;pre

viouspre

ssure

ulcer;

non-blanchable

ery

them

a;decre

ase

d

mobility;fecalincontinence;depletedtriceps

skinfold;decre

ase

dlym

phocyte

count;

decre

ase

d

bodyweight;

bnon-blanchable

ery

them

a;decre

ase

d

lym

phocyte

count;

imm

obility;dry

sacra

lsk

in;

decre

ase

dbodyweight

Anthony,Reynolds,

andRuss

ell(2

000)

Patients

�65years

adm

ittedto

genera

ldistricthosp

ital

(N¼

773)

Pre

ssure

ulcer

gra

deI–V

(Torr

ancesc

ale)

4113

aHigherW

aterlow

score

s;decre

ase

dse

rum

album

in;

hyponatrem

ia.bHigherW

aterlow

score

s;decre

ase

d

seru

malbum

in

Berg

stro

m,Bra

den,

Kem

p,Cham

pagne,

andRuby(1

996)

Patients

adm

ittedto

various

institutionsincluding

tertiary

care

andVetera

n’s

Adm

inistrationHosp

itals

(VAH);

Tertiary

Care

(N¼

306)

;VAH

(N¼

282)

Pre

ssure

ulcer

stageI–IV

7Tertiary

Care

,

26;VAH,21

a(T

ertiary

Care

)none;

a(V

AH)lowerBra

densc

ore

Gro

us,

Reilly,andGift

(1997)

Patients

underg

oingpro

longed

surg

icalpro

cedure

sin

alarg

e

universityhosp

ital(N

¼33)

Pre

ssure

ulcer

stageI–IV

615

aUse

ofwarm

ingblanketduringsu

rgicalpro

cedure

Halfens,

Van

Achterb

erg

,andBal

(2000)

Patients

adm

ittedto

11ward

sin

thre

ehosp

itals

(N¼

320)

Pre

ssure

ulcer

stageI–IV

1147

aUrinary

incontinence;fecalincontinence;incre

ase

d

age.bLowersu

mm

ativeBra

densc

ore

;incre

ase

d

age;decre

ase

dse

nso

ryperc

eption(B

raden);

decre

ase

dfriction/shear(B

raden);

incre

ase

d

moisture

(com

binedconcept)

Kem

p,Keithley,

Sm

ith,and

Morreale

(1990)

Surg

icalpatients

inanacute

care

facility(N

¼125)

Pre

ssure

ulcer

stageI–IV

715

aIn

traopera

tiveextra-corp

ore

alcirculation.

bIn

cre

ase

dtim

ein

opera

tingro

om

;intraopera

tive

extra-corp

ore

alcirculation;incre

ase

dage

(Continued)

6 RESEARCH IN NURSING & HEALTH

Research in Nursing & Health

Page 7: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

2.(C

ontinued)

Study

TypeofSetting/P

atients

(N)

Outcom

eVariable

Dependent

Variables

Evaluated

Patients

With

Pre

ssure

Ulcers

(n)

StatisticallySignificantFindings�

Lindgre

n,Unoss

on,

Fre

drikso

n,andEk

(2004)

Patients

inm

edicalorsu

rgical

ward

sin

acounty

hosp

ital

(N¼

530)

Pre

ssure

ulcer

stageI–IV

1662

aFem

ale

gender;

incre

ase

dage;lowerRAPStotal

score

;lowerbodym

ass

index;lowerdiastolicblood

pre

ssure

;higherdura

tionofhosp

italstay;decre

ase

d

weight;

more

surg

icalinterv

entions;

lowervalueson

thefollowingRAPSsu

bsc

ore

s:physicalactivity,

mobility,foodintake,se

rum

album

in,friction/shear.

bDecre

ase

dm

obility(R

APSsu

bsc

ore

);incre

ase

d

length

ofhosp

italstay;incre

ase

dage;decre

ase

d

weight;

requiredsu

rgery

Lindgre

n,Unoss

on,

Kra

ntz,andEk

(2005)

Patients

underg

oingsu

rgery

in

acounty

hosp

ital(N

¼286)

Pre

ssure

ulcer

stageI–IV

2441

aFem

ale

gender;

incre

ase

dage;lowerweight;

lower

bodym

ass

index;lowerRAPStotalsc

ore

;use

of

epidura

l/sp

inalanalgesia;lowervaluesonthe

followingRAPSsu

bsc

ore

s:physicalactivity,

mobility,m

oisture

,se

nso

ryperc

eption;se

rum

album

in;foodintake,friction/shear.

bM

ale

gender,

gre

aterrisk

(ASA;NYHA)sc

ore

s;decre

ase

dfood

intake

Nonnem

acheretal.

(2008)

Patients

adm

ittedto

alarg

e

universityhosp

ital

(N¼

34,238)

Pre

ssure

ulcer

stageI–IV

33625

aIn

cre

ase

dage;m

ale

gender;

incre

ase

dlength

ofstay;

surg

icalpro

cedure

;re

quiredintensivecare

unitstay;

decre

ase

dm

obility.bDecre

ase

dm

obility;m

alignant

tum

or;

pain;insu

fficientnutrition;use

ofse

datives;

vasc

ulardisease

;sk

inpro

blem

sin

pre

ssure

ulcer

pro

neare

as;

genera

lsk

inpro

blem

s;friction/shear

Olsonetal.(1

996)

Medicalorsu

rgicalpatients

in

acute

care

(N¼

149)

Pre

ssure

ulcer

stageI–IV

1820

aDecre

ase

dadm

issionhem

oglobin;m

ore

hours

spentin

bedperday;fewerhours

upin

chair

perday;

bnone

Schoonhoven,Defloor,

vanderTweel,

Busk

ens,

and

Gry

pdonick(2

002)

Surg

icalpatients

inacadem

ic

hosp

ital(N

¼208)

Pre

ssure

ulcer

stageI–IV

1244

aIn

cre

ase

dlength

oftim

ein

opera

tingro

om

;

pre

-opera

tiveuse

ofanalgesics;

malnutrition;longer

continuousperiodofdiastolicbloodpre

ssure

below

60m

mHgintraopera

tively;sp

inalsu

rgery

;head/

necksu

rgery

;length

ofsu

rgery

;longerstayin

intensivecare

unit.bLength

ofsu

rgery

(Continued)

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 7

Research in Nursing & Health

Page 8: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

2.(C

ontinued)

Study

TypeofSetting/P

atients

(N)

Outcom

eVariable

Dependent

Variables

Evaluated

Patients

With

Pre

ssure

Ulcers

(n)

StatisticallySignificantFindings�

Stotts(1

987)

Secondary

analysisof

pro

spectivedata

set.

Surg

icalpatients

adm

ittedto

thecard

iovasc

ularor

neuro

surg

ery

serv

icesofa

larg

e,tertiary

care

center

(N¼

67)

Pre

ssure

ulcer

gra

deI–IV

(gra

de

definitions

pro

videdby

Stotts)

1067

None

StottsandPaul(1

988)

Secondary

analysisof

pro

spectivedata

set.

Surg

icalpatients

adm

ittedto

thecard

iovasc

ularor

neuro

surg

ery

serv

icesofa

larg

e,tertiary

care

center

(N¼

117)

Pre

ssure

ulcer

gra

deI–IV

(gra

de

definitions

pro

videdby

Stotts)

1639

aHigherlym

phocyte

count;

lowerNortonsc

ore

;longer

hosp

italtim

epriorto

surg

icalpro

cedure

;higher

estim

atedbloodloss

inopera

tingro

om

Strord

eur,

Laure

nt,

andD’H

oore

(199

8)

Patients

adm

ittedforcard

iac

surg

ery

(N¼

163)

Pre

ssure

ulcer;

StageII

orIII

2548

aIn

cre

ase

dage;incre

ase

dlength

ofstayin

hosp

italand

intensivecare

unit;decre

ase

dadm

ission

hem

oglobin;lowerNortonsc

ore

s(a

dm

issionand

post-opera

tively);

lowerBra

densc

ore

s(a

dm

ission

andpost-opera

tively);

pre

senceofpre

ssure

ulceron

adm

ission;use

ofanti-hypertensivedru

gs;

post-opera

tivecorticostero

iduse

;noso

com

ial

infections;

unplannedsu

rgicalre

-interv

ention;

re-admissionto

intensivecare

unit.bLower

post-opera

tiveBra

densc

ore

;decre

ase

dadm

ission

hem

oglobin;post-opera

tivecorticostero

iduse

Note:RAPS,RiskAss

ess

mentPre

ssure

Sore

scale;ASA,Am

ericanSociety

ofAnesthesiologists

score

;NYHA,New

York

Heart

Ass

ociationsc

ore

.aStatisticallysignificantfindingsfrom

univariate

statistics.

bStatisticallysignificantfindingfrom

regre

ssionanalysis.

� p�

.05.

8 RESEARCH IN NURSING & HEALTH

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Page 9: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

3.Pre

ssure

UlcerRiskFactors

inCriticallyIllPatients:A

Summ

ary

ofPro

spectiveStudiesPublish

edFro

m19

87to

2008

(N¼

11)

Study

TypeofSetting/

Patients

(N)

Outcom

eVariable

Dependent

Variables

Evaluated

Patients

With

Pre

ssure

Ulcers

(n)

StatisticallySignificantFindings�

Baldwin

and

Ziegler(1998)

Criticallyilltrauma

patients

(N¼

36)

Pre

ssure

ulcerany

stage

911

aIn

cre

ase

dhosp

itallength

ofstay;

bBra

denm

obilityandm

oisture

Berg

stro

m,

Dem

uth,and

Bra

den(1

987)

AdultIC

U(N

¼60

)Pre

ssure

ulcerany

stage

924

aBra

densc

ore

Carlso

n,Kem

p,

andShott

(1999)

Thre

eIC

U/Tertiary

care

settings

(N¼

136)

Pre

ssure

ulcerany

stage

836

aSum

mativeBra

densc

ore

;Bra

denSenso

ryPerc

eption

Eachem

pati,

Hydo,andBarie

(2001)

Surg

icalIC

U,Phase

I

(N¼

2615),

Phase

II

(N¼

412)

Pre

ssure

ulcer

stageII

or

deeper

Phase

11,

Phase

II¼

9

101,

33aPhase

I:incre

ase

dlength

ofstay;incre

ase

dnum

berofintensivecare

unitdaysto

developm

entofpre

ssure

ulcer.

Phase

II:incre

ase

dage;

incre

ase

dlength

ofstay;em

erg

encyadm

ission;daysin

bed;days

withoutnutrition;higherCURSrisk

score

.bEm

erg

encyadm

ission;

incre

ase

dage;daysin

bed;dayswithoutnutrition;higherCURS

risk

score

Fifeetal.(2001)

Neuro

logic

ICU

(N¼

186)

Pre

ssure

ulcer

stageII

or

deeper

1023

aLow

Bra

den(<

13);

bowelincontinence.bLow

seru

malbum

in

Lewicki,M

ion,

Splane,Sam

-

stag,andSecic

(1997)

Card

iacsu

rgery

patients

(N¼

337)

Pre

ssure

ulcerany

stage

1716

aPre

-opera

tive:higherCharlso

nco-m

orb

idityindex;decre

ase

d

seru

malbum

in;hem

oglobin

andhem

atocrit;

diabetes;

lower

Bra

densc

ore

s.aPost-opera

tive:pre

senceofintra-aortic

balloonpum

p;notturn

eddaily;ra

pid

return

topre

-opera

tivebody

tem

pera

ture

Nijsetal.(2

008)

Surg

icalIC

U

(N¼

520)

Pre

ssure

ulcer

stageII–IV

25104

aAdm

issiondiagnosis(h

epatologyorother)

;higherAPACHE

II

score

;turn

ing/turn

ingfrequency;sittingin

chair/incre

ase

dlength

oftim

ein

chair;physicalfixation(r

estra

ints);

bodytem

pera

ture

�38.58C;use

ofanalgesics;

use

ofse

datives;

edem

a;floatingheels;

lowerGCSsc

ore

s;continuousorinterm

ittentdialysis;

higherSOFA

score

;m

echanicalventilation;use

ofaltern

atingm

attre

ss;

adequate

pre

ventionm

easu

res;

lowerNortonsc

ore

;lower

hem

oglobin;use

ofdopam

ine.bDopam

ine�5

mg/kg/m

inute;

continuousorinterm

ittentdialysis;

use

ofaventilator;

history

of

vasc

ulardisease

;heelfloating;turn

ing�6

tim

esperday;adequate

pre

ventionm

easu

res;

use

ofse

datives;

sittingin

chair;body

tem

pera

ture

�38.58C

(Continued)

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 9

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Table

3.(C

ontinued)

Study

TypeofSetting/

Patients

(N)

Outcom

eVariable

Dependent

Variables

Evaluated

Patients

With

Pre

ssure

Ulcers

(n)

StatisticallySignificantFindings�

Papantonio,

Wallop,and

Kolodner(1

994)

Card

iacsu

rgery

patients

(N¼

136)

Pre

ssure

ulcer

stageII

orIII

2237

aIn

cre

ase

dage;lowerhem

atocrit;

bdiabetes;

resp

iratory

disease

;

hypertension;pre

-existingsk

incondition;ecchym

osis;

intraopera

tiveuse

ofdopam

ine

Penderand

Fra

zier(2005)

Genera

lIC

U(N

¼40

)Pre

ssure

ulcerany

stage

218

None

Theaker,

Mannan,

Ives,

andSoni

(2000)

Genera

lIC

Uandhigh

dependencyunit

(N¼

286)

Pre

ssure

ulcerany

stage

2277

aIn

cre

ase

dage;anem

ia;higherAPACHE

IIsc

ore

s;coagulopathy;

diabetes;

use

ofdopam

ineandepinephrine;fecalincontinence;

incre

ase

dlength

ofstayin

intensivecare

unit;lowerse

rum

album

in;m

oisture

/pers

piration;nore

pinephrine;edem

a;pain;

periphera

lvasc

ulardisease

;re

ducednutritionalintake;stero

id

use

;andtoounstable

toturn

.bAPACHE

IIsc

ore

�13;

fecal

incontinence;anem

ia;length

ofstay>3days

Westra

te,Hop,

Aalbers

,

Vre

eling,and

Bru

ining(1998)

Surg

icalIC

U(N

¼594)

Pre

ssure

ulcer

stageII,III,

or

IV

747

aFem

ale

gender;

incre

ase

dlength

ofstayin

intensivecare

unit;

Waterlow

score

;incre

ase

dfrequencyofpatientturn

ing;incre

ase

d

frequencyofnurs

ingpatientonaltern

ativesides;

decre

ase

d

mobilizationoutofbed

Note:CURS,Corn

ell

ulcerrisk

score

;APACHE

II,AdvancedPhysiologyandChro

nic

HealthEvaluation

II;GCS,Glasg

ow

Com

aScale;SOFA,Sepsis-re

latedOrg

anFailure

Ass

ess

mentScale.

aStatisticallysignificantfindingsfrom

univariate

statistics.

bStatisticallysignificantfindingfrom

multivariate

regre

ssionanalysis.

� p�

.05.

10 RESEARCH IN NURSING & HEALTH

Research in Nursing & Health

Page 11: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

NICE (2005). Each study was rated as high,medium, or low quality. Because NICE did notprovide guidelines on adequate sample sizesrequired for high or medium study designquality, we adopted a conservative strategy toguard against including studies that may eitherhave been under-powered for multivariateanalysis or in which an overfitted multivariatemodel was used. Table 4 summarizes the NICEquality ratings, provides rationale for theassigned ratings, indicates the presence ofmultivariate analysis, and whether or not therisk factors contributed by the study wereincluded in the conceptual model. Of the 25studies evaluated using the NICE criteria, 6were assessed as having low study quality andwere therefore excluded from inclusion in theconceptual model. The remaining 19 wereclassified as high or medium quality. However,only 8 of these provided adjusted odds ratios,thereby excluding 11 studies with high ormedium NICE criteria ranking that did notreport adjusted odds ratios. Ultimately, 8 studiescontributed findings to the conceptual model.

Categorization of Risk Factors inPressure Ulcer Development

Table 5 summarizes 42 non-unique risk factorvariables for pressure ulcer developmentidentified as statistically significant (p � .05) atthe multivariate level in the eight identifiedhigher quality studies. Five of the variablesidentified by Nijs et al. (2008) representcommon nursing interventions for the preven-tion of pressure ulcers, such as frequent turningand repositioning. Because patient-specificvariables were the focus of this analysis, theywere not included in further evaluation, leaving37 variables.

Next, we collaborated on a step-wise strategyto identify conceptual groupings and combinerelated risk factors as shown in Table 5, main-taining independent predictors identified withinstudies. Ultimately, we reached consensus onthe conceptual groups and the placement of therisk factors within those groups. There wasconsiderable conceptual overlap in individualrisk factor variables identified. Although in theirstudy on the use of serum albumin levels topredict pressure ulcer development, Anthony,Reynolds, and Russell (2000) identified thesummative score from the Waterlow PressureUlcer Prevention/Treatment Policy� (Copyrightby J. Waterlow, 1985. Revised, 2005) to be a

multivariate predictor of pressure ulcer develop-ment, Halfens, Van Achterberg, and Bal (2000)identified the summative score from the BradenScale to be a predictor.

Combination of ConceptuallyEquivalent Waterlow andBraden Components

As a next step, we compared components of theWaterlow and Braden scales and evaluated theconceptual overlap. The Braden Scale subscalesare: Moisture, Activity, Mobility, Nutrition,Sensory Perception, and Friction/Shear. TheWaterlow Scale was revised in 2005, butbecause the study identifying the Waterlowsummative score was published before therevision, the original Waterlow subscales wereused for comparison. They are: Mobility,Incontinence, Sensory Perception, Nutrition,Build and Weight Relative to Height, VisualSkin Type, Sex, Age, Anti-inflammatory orSteroid use, Smoking, and Orthopedic Surgeryor Fracture Below the Waist. The two scales arecompared in Table 6.Because it has been the most extensively test-

ed and validated in the literature (Pancorbo-Hidalgo et al., 2006), the Braden Scale waschosen as the gold standard against whichcomponents of the Waterlow RAS were com-pared. Three subscales are similar in the Bradenand Waterlow scales: Mobility, Sensory Percep-tion, and Nutrition. Waterlow’s Incontinencesubscale overlaps with the Braden Moisturesubscale, given that incontinence is includedwithin Braden’s Moisture subscale definition.Similarly, Waterlow’s Orthopedic Surgery belowthe Waist subscale can be captured in eitherthe Braden Mobility or Activity subscales. Inaddition, there is potential overlap betweenWaterlow’s Steroid, Anti-inflammatory use andthe Braden Scale’s risk factor emotional stress,as elevated serum cortisol levels have beenassociated with increased emotional stress states(Braden, 1998), and increased stress states havebeen associated with critical illness (Rothwell& Lawler, 1995). Increased cortisol and otherglucocorticoid production is a known resultof the stress response, regardless of etiology(Tsigos, Kyrou, & Chrousos, 2004). However,emotional stress was not included in the finallist of risk factors because of the feasibility ofmeasurement as well as the potential proxymeasure represented by the Waterlow Steroid/Anti-inflammatory use.

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 11

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Page 12: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

4.Quality

ofStudiesExam

iningPre

ssure

UlcerRiskFactors

inAcute

andCriticalCare

SettingsUsingNIC

EQuality

Assess

mentTool(N

¼25

)

Study

NBase

line

Participation

RiskFactor

Measu

res

Outcom

eM

easu

res

Quality

Ass

ess

ment

ofStudy

Adjusted

RiskFactor

Reportinga

Includedin

Conceptual

Model

Rationale

Allman,Goode,Patrick,

Burs

t,andBartolucci

(199

5)(A

C)

286

Yes

Yes

Yes

Medium

Som

eYes

Selectedvariableswith

multivariate

analysis

Anthony,Reynolds,

and

Russell(2

000)

(AC)

773

Yes

Yes

Yes

High

Yes

Yes

AllNIC

Ecriteriam

et

Baldwin

andZiegler(1

998)

(ICU)

36Unclear

No

Yes

Low

Yes

No

Possibly

underp

owere

d;unable

todeterm

inebase

line

participation;risk

factor

measu

resnotclearlydefined

Berg

stro

m,Bra

den,Kem

p,

Champagne,andRuby

(199

6),Tertiary

Care

FacilitiesandVAH

(AC)

Tertiary

Care

,30

6Yes

Yes

Yes

High

No

No

AllNIC

Ecriteriam

et

VAH,28

2Yes

Yes

Yes

High

No

AllNIC

Ecriteriam

et

Berg

stro

m,Dem

uth,and

Bra

den(1

987)

(ICU)

60Yes

Yes

Yes

High

No

No

AllNIC

Ecriteriam

et

Carlso

n,Kem

p,andShott

(199

9)(ICU)

136

Yes

Yes

Yes

High

No

No

AllNIC

Ecriteriam

et

Eachem

pati,Hydo,and

Barie(2

001)

,Phase

Iand

Phase

II(ICU)

Phase

I,26

15Yes

Yes

No

Low

No

No

Outcom

em

easu

resnotclearly

defined;blindedass

essm

ents

andinter-ra

terre

liabilitynot

docum

ented

Phase

II,41

2Yes

Yes

No

Low

No

Outcom

em

easu

resnotclearly

defined;blindedass

essm

ents

andinter-ra

terre

liabilitynot

docum

ented;oddsra

tiodata

poss

ibly

incorr

ect(n

oerr

atum

am

endm

entlocated)

Fifeetal.(2

001)

(ICU)

186

No

No

Yes

Low

Som

eNo

Eligible

base

lineparticipation

notdocum

ented;notallrisk

factorm

easu

resclearly

defined;re

ducedm

odelfor

multivariate

analyse

s;OR/CI

notre

ported

(Continued)

12 RESEARCH IN NURSING & HEALTH

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Page 13: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

4.(C

ontinued)

Study

NBase

line

Participation

RiskFactor

Measu

res

Outcome

Measu

res

Quality

Ass

ess

ment

ofStudy

Adjusted

RiskFactor

Reportinga

Includedin

Conceptual

Model

Rationale

Gro

us,

Reilly,andGift(1

997)

(AC)

33Yes

Yes

Yes

Medium

No

No

Possibly

underp

owere

d

Halfens,

VanAchterb

erg

,andBal(2

000)

(AC)

320

Yes

No

Yes

Medium

Yes

Yes

Notallrisk

factors

clearly

defined

Kem

p,Keithley,Sm

ith,and

Morr

eale

(199

0)(A

C)

125

Unclear

Yes

Yes

Medium

No

No

Unclear%

ofbase

line

participation;re

ducedm

odel

for

multivariate

analyse

sLewicki,M

ion,Splane,

Sam

stag,andSecic

(1997)

(ICU)

337

Yes

Yes

Yes

Medium

No

No

UnadjustedOR

reportedfor

somevariables

Lindgre

n,Unoss

on,

Fre

drikso

n,andEk(2

004)

(AC)

530

Yes

No

Yes

Medium

Som

eYes

Notallrisk

factors

clearly

defined;re

ducedm

odelfor

multivariate

analyse

sLindgre

n,Unoss

on,Kra

ntz,

andEk(2

005)

(AC)

286

Yes

No

Yes

Medium

Som

eYes

Notallrisk

factors

clearly

defined;re

ducedm

odelfor

multivariate

analyse

sNijsetal.(2

008)

(ICU)

520

Yes

Yes

Yes

High

Yes

Yes

AllNIC

Ecriteriam

et

Nonnem

acheretal.(2

008)

(AC)

34,238

Yes

Yes

Yes

High

Yes

Yes

AllNIC

Ecriteriam

et

Olsonetal.(1

996)

(AC)

149

Yes

No

No

Low

Som

eNo

Possibly

underp

owere

d;notall

risk

factorvariablesclearly

defined;m

easu

rem

ent

frequenciesnotclear;

outcom

em

easu

renotclear;

reducedm

odelfor

multivariate

analyse

sPapantonio,W

allop,and

Kolodner(1

994)

(ICU)

148

Yes

Yes

Yes

Medium

No

No

Possibly

underp

owere

d;

relativerisk

pre

sented;

inconsistencywithso

meof

risk

factors

andtheir

measu

res

(Continued)

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 13

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Page 14: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table

4.(C

ontinued)

Study

NBase

line

Participation

RiskFactor

Measu

res

Outcome

Measu

res

Quality

Ass

ess

ment

ofStudy

Adjusted

RiskFactor

Reportinga

Includedin

Conceptual

Model

Rationale

PenderandFra

zier(2

005)

(ICU)

40Unclear

Yes

Yes

Low

No

No

Unclear%

eligible

base

line

participation;nounadjusted

OR

reported

Schoonhoven,Defloor,

van

derTweel,Busk

ens,

and

Gry

pdonick(2

002)

(AC)

208

Yes

No

Yes

Medium

No

No

Notallrisk

factors

clearly

defined;logisticre

gre

ssion

mentionedbutnoadjusted

data

pre

sented

Strord

eur,

Laure

nt,and

D’H

oore

(1998)

(AC)

163

Yes

No

Yes

Medium

Som

eNo

Notallrisk

factors

clearly

defined;re

ducedm

odelfor

multivariate

analyse

s;odds

ratiosnotre

ported

Stotts(1

987)

(AC)

67Yes

Yes

Yes

Medium

No

No

Possibly

underp

owere

dStottsandPaul(1

988)

(AC)

117

No

No

Yes

Low

No

No

Possibly

underp

owere

d;unclear

%eligible

base

line

participation;notallrisk

factors

clearlydefined

Theaker,

Mannan,Iv

es,

and

Soni(2

000)

(ICU)

332

Yes

Yes

Yes

High

Yes

Yes

AllNIC

Ecriteriam

et

Westra

te,Hop,Aalbers

,Vre

eling,andBru

ining

(1998)

(ICU)

594

Yes

No

Yes

Medium

No

No

Notallrisk

factorm

easu

res

clearlydefined

Note:NIC

E,NationalIn

stitute

ofHealthandClinicalExcellence;AC,acute

care

study;IC

U,criticalcare

study;VAH,Vetera

n’s

Adm

inistrationhosp

ital.

aExclusioncriterion.

14 RESEARCH IN NURSING & HEALTH

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Page 15: Risk factors for pressure ulcer development in critically Ill patients: A conceptual model to guide research

Table 5. Summary of Multivariate Statistically Significant Pressure Ulcer Risk Factors in Studies ofHigh and Medium Quality (N ¼ 8)

Study

Multivariate Statistically

Significant Findings� OR [95% CI]

Allman, Goode, Patrick, Non-blanchable erythema 7.52 [1.00–59.12]

Burst, and Bartolucci Decreased lymphocyte count 4.86 [1.70–13.89]

(1995) Immobility 2.36 [1.14–4.85]

Dry sacral skin 2.31 [1.02–5.21]

Decreased body weight (<58 kg) 2.18 [1.05–4.52]

Anthony, Reynolds, and High Waterlowa summative score 1.18 [1.13–1.23]

Russell (2000) High serum albumin (protective

factor)

0.95 [0.90–0.99]

Halfens, Van Achterberg, Low Braden summative scoreb 2.98 [1.81–4.99]

and Bal (2000) Increased age 2.68 [1.62–4.43]

Increased moisture (fecal and

urinary incontinence, sweating)

2.35 [1.40–3.94]

Lindgren, Unosson, Fredrikson, RAPSc Mobility subscale 0.53 [0.33–0.86]

and Ek (2004), From total Increased length of hospitalization 1.03 [1.01–1.05]

sample of medical and Increased age 1.04 [1.01–1.08]

surgical patients Surgical treatment 4.8 [2.03–11.39]

Increased weight (protective factor) 0.96 [0.94–0.99]

Lindgren, Unosson, Krantz, and Female gender 0.27 [0.11–0.68]

Ek (2005), Pre-operative

findings

Poor physical status (ASAd or NYHAe

scores)

2.30 [1.21–4.38]

RAPS Food Intake subscale 0.53 [0.31–0.91]

Study

Multivariate Statistically

Significant Findings�OR [95% CI]

24 hour 48 hour

Nijs et al. (2008) at Dopamine �5 mg/kg/minute 6.05 [1.88–19.54] —

24 and/or 48 hours Continuous or intermittent dialysis 3.77 [1.03–13.86] 9.43 [3.01–29.51]

prior to pressure Ventilator use — 4.82 [1.74–13.36]

ulcer development Medical history of vascular disease 4.51 [1.99–10.24] 2.85 [1.29–6.30]

Adequate prevention 5.96 [1.91–18.64] 10.06 [3.03–33.35]

Frequency of turning (�6 times/day)

or use of alternating mattress

30.21 [12.20–74.77] 3.63 [1.09–12.05]

Turning 6.66 [2.70–16.44] —

Floating heels — 3.82 [1.66–8.78]

Up in chair 0.08 [0.02–0.27] —

Use of sedatives (protective factor) 0.30 [0.13–0.70] 0.27 [0.11–0.65]

Body temperature �38.58C(protective factor)

0.18 [0.18–0.92] —

Study

Multivariate Statistically

Significant Findings� OR [95% CI]

Nonnemacher et al. (2008) Limited mobility/activity 4.42 [3.50–5.59]

Malignant tumor 1.48 [1.20–1.83]

Pain presence 1.43 [1.16–1.75]

Insufficient nutrition 1.61 [1.20–2.17]

Sedative use 1.61 [1.23–2.12]

Obstructive vascular disease (pelvic

and abdominal arteries)

1.80 [1.05–3.08]

Skin problems in pressure prone areas 4.70 [3.61–6.12]

General skin problems 1.34 [1.06–1.70]

Friction/Shearing forces 1.72 [1.33–2.22]

(Continued)

FACTORS FOR ICU PRESSURE ULCER DEVELOPMENT/BENOIT AND MION 15

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Combination of Other Risk Factors WithBraden Scale Components

Risk factors representing similar concepts tothose of the Braden subscales included sedativeuse (Nijs et al., 2008; Nonnemacher et al.,2008), which could reflect the Braden subscalesof Activity, Mobility, or Sensory Perception,and pain (Nonnemacher et al., 2008), whichcould reflect the Activity or Mobility subscales.Although not identified as part of the Bradensubscale, Allman, Goode, Patrick, Burst, and

Bartolucci (1995) identified immobility as anindependent risk factor. It is conceptuallyidentical to the Braden subscale, so it was notincluded separately. Although Nijs et al. (2008)identified sedative use at 24 hours, p < .01,OR ¼ 0.30, 95% CI [0.13, 0.70] and 48 hours,p < .01, OR ¼ 0.27, 95% CI [0.11, 0.65] priorto pressure ulcer development as a protectivefactor, and speculated that the protective effectsof sedation use may be due to decreased muscletension, thereby enhancing cutaneous circula-tion. On the other hand, Nonnemacher et al.(2008) found sedative use to be a risk factor,p < .001, OR ¼ 1.61, 95% CI [1.23, 2.12].Therefore, sedative use was not included as adistinct risk factor in the model. In addition, theBraden Scale captures sedation’s relative effectson mobility or activity. Total lymphocyte count,identified by Allman et al. (1995), is oftenincluded as a component in a comprehensivenutritional assessment and is considered a serumindicator for nutritional status (Rosenthal et al.,1998; Thorsdottir, Gunnarsdottir, & Eriksen,2001), but because nutritional status is capturedby the Braden Scale, total lymphocyte countwas not included separately.

Conceptual Categorization of theRemaining Waterlow Subscales

Because the remaining five Waterlow subscales(Skin Type, Build/Weight, Sex, Age, andSmoking) do not have a conceptual counterpartin the Braden RAS, these components weregrouped with similar risk factors contributedfrom other studies. Waterlow’s (1985) Skin Typedescriptors include: healthy, tissue paper, dry,

Table 5. (Continued)

Study

Multivariate Statistically

Significant Findings� OR [95% CI]

Theaker, Mannan, Ives, APACHE IIf score �13 3.4 [1.4–7.92]

and Soni (2000) Fecal Incontinence 3.27 [1.32–8.3]

Anemia 2.81 [1.24–6.34]

Length of stay >3 days 2.76 [1.08–7.05]

aRisk increases with higher scores.bRisk increases with lower scores.cRisk Assessment Pressure Sore Scale—Risk increases with lower score.dAmerican Society of Anesthesiologists—Physical status declines with increased category rating (Owens, Felts, &

Spitznagel, 1978).eNew York Heart Association—Physical status declines with increased category rating (Texas Heart Institute, n.d.).fAcute Physiology and Chronic Health Evaluation—risk of mortality increases with higher scores (Knaus, Draper,

Wagner, & Zimmerman, 1985).�p � .05.

Table 6. Comparison of Subscales in the Braden,and Waterlow Risk Assessment Scales

Subscales Bradena Waterlowb

Mobility X XActivity X —Sensory perception X XNutrition X XMoisture X —Friction/shear X —Incontinence — XBuild/weight — XSkin type — XSex — XAge — XSteroid/anti-inflammatoryuse

— X

Smoking — XOrthopedic surgery — X

aBraden Scale for Predicting Pressure Sore Risk�

(Copyright by Braden & Bergstrom, 1988) Risk

increases with lower score.bWaterlow Pressure Ulcer Prevention/Treatment Poli-

cy� (Copyright by J. Waterlow, 1985. Revised, 2005)

Risk increases with higher score.

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edematous, clammy/pyrexia, discolored, andbroken/spots. Healthy skin does not carrypressure ulcer risk according to the WaterlowRAS, so it was not included. Skin describedas clammy with pyrexia is similar to the bodytemperature risk factor identified by Nijset al. (2008), so these risk factors were concep-tually grouped. The remaining skin descriptorsidentified by Waterlow (tissue paper, dry,edematous, discolored, and broken/spots) areconceptually similar to skin integrity threatsidentified by Allman et al. (1995), Halfens et al.(2000), and Nonnemacher et al. (2008), so wereconceptually grouped. Interstitial fluid flow isincluded in Braden and Bergstrom’s (1987)conceptual model discussed below, but is notcaptured in the Braden Scale. Consequently,it was retained as a separate risk factor con-tributing to the same conceptual grouping asother threats to skin integrity. Smoking is a riskfactor identified in the Waterlow scale and isalso included by Braden and Bergstrom asa theoretical risk to tissue tolerance. It wasconceptually grouped with other risk factorsidentified by Nonnemacher et al., Nijs et al.,and Theaker et al. (2000) as factors that affectperfusion and oxygenation. The remainingWaterlow risk factors (Build/Weight, Age, andSex) were considered demographic variablesand retained separately in various conceptualgroupings.

Remaining Risk Factors

Poor scores on the New York Heart Association(NYHA) functional classification (Lindgren,Unosson, Krantz, & Ek, 2005), the AmericanSociety of Anesthesiologists (ASA) assessment(Lindgren et al., 2005) and the AdvancedPhysiology and Chronic Health Evaluation(APACHE) II (Theaker et al., 2000) werecombined with other indicators of severity ofillness. Those included length of hospital stay(Lindgren, Unosson, Fredrikson, & Ek, 2004;Theaker et al., 2000) and ventilator use (Nijset al., 2008).

Dialysis (Nijs et al., 2008) was added to theconceptual category containing body tempera-ture, emotional stress, and steroid/anti-inflam-matory use as an indicator of physiologicalteration. Surgical procedure (Lindgren et al.,2005) was retained as a separate conceptualcategory. Gender (Anthony et al., 2000;Lindgren et al., 2005) was treated as a demo-graphic variable, as was body weight (Allman

et al., 1995; Anthony et al., 2000; Lindgrenet al., 2004). The results of the risk factorcombinations and their respective conceptualgroupings are shown in Table 7.

Integration of Findings Into aConceptual Model

Integration With the Braden andBergstrom Conceptual Model

The proposed conceptual model resulting fromthe integration of the study findings is presentedin Figure 3. Approximately 25% of the statisti-cally significant multivariate risk factors ana-lyzed were identical or conceptually related toone or more of the six subscales comprising theBraden Scale. To maintain the sensitivity andNPV of the Braden RAS (Table 1), we retainedthe two constructs of pressure and tissuetolerance for pressure as defined by the authors(Bergstrom, Braden, et al., 1987) and measuredby the Braden Scale. Risk factors identified inthis review that were not conceptually related toone of the six Braden Scale subscales servedto augment Bergstrom, Braden, et al.’s (1987)concept of intrinsic factors—a component oftissue tolerance.

Augmenting the Intrinsic FactorConcept

Bergstrom, Braden, et al. (1987) defined intrin-sic factors that affect the skin’s tolerance forpressure as those that ‘‘influence the architec-ture and integrity of the skin and supportingstructures . . . and diminish the ability of softtissues to absorb and tolerate mechanical load’’(Bergstrom, Braden, et al., 1987, p. 206). Bra-den and Bergstrom’s (1987) conceptual modelidentifies decreased nutrition, increased age, anddecreased arteriolar pressure as components ofintrinsic risk factors ultimately affecting thetissue’s tolerance for pressure. Additionally,Braden and Bergstrom identified four hypotheti-cal risk factors that may affect intrinsic tissuetolerance. They are interstitial fluid flow, skintemperature, smoking, and emotional stress.Braden and Bergstrom’s concept, intrinsicfactors, was augmented to include three con-cepts: metabolic supply and demand, pressuredistribution capacity, and threats to skinintegrity.

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Table 7. Combination of Statistically Significant Risk Factors Into Conceptual Groupings WithIdentified Measurement

Risk Factor and Study Measurement Conceptual Group

Dopamine use (Nijs et al., 2008) Type/amount of IV vasopressor use Perfusion/Oxygenation

Obstructive arterial disease(Nonnemacher et al., 2008)

Vascular disease of any type exceptcoronary artery and cerebralvascular disease

Peripheral vascular disease (Nijset al., 2008)

Hemoglobin/hematocrit

Anemia (Theaker et al., 2000) Nicotine useSmoking (Braden & BergstromConceptual model); Smoking—Waterlow (Anthony et al., 2000)

APACHE II Score (Theaker et al.,2000)

APACHE II Score on admission Severity of Illness

NYHA Score (Lindgren et al., 2005) ASA scoreLOS (Lindgren et al., 2004; Theakeret al., 2000)

NYHA score

Ventilator use (Nijs et al., 2008) Hospital LOSIncreased surgical risk—ASA score(Lindgren et al., 2005)

Ventilator use

Dialysis (Nijs et al., 2008) Requiring dialysis of any typeduring hospital stay

PhysiologicAlterations

Skin temperature (Braden andBergstrom Conceptual Model)

Body temperature

Clammy/Pyrexia—Waterlow(Anthony et al., 2000)

Steroid/Anti-Inflammatory use

Steroid/Anti-Inflammatory use—Waterlow (Anthony et al., 2000)

Emotional stress (Braden andBergstrom Conceptual Model)

Body temperature �38.58C (Nijset al., 2008)

Non-blanchable erythema, drysacral skin (Allman et al., 1995)

Skin problems in areas at risk forpressure ulcer development(sacrum, elbows, heels)

Current Stage I or worse pressureulcer

Threats to SkinIntegrity

Skin problems in areas at risk forpressure ulcer development(Nonnemacher et al., 2008)

General skin problems (thin,edema)

Discolored skin—Waterlow(Anthony et al., 2000)

Chemical exposure (e.g., fecalincontinence)

Broken/Spots—Waterlow (Anthonyet al., 2000)

General skin problems(Nonnemacher et al., 2008)

Tissue paper skin/edema—Waterlow (Anthony et al., 2000)

Interstitial fluid flow (Braden andBergstrom Conceptual Model)

Fecal/Urinary incontinence(Halfens et al., 2000)

(Continued)

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Five conceptual groups (see Table 7) wereidentified that represent the body’s ability tobalance metabolic supply and demand needs.Metabolic supply includes perfusion/oxygen-ation and nutrition as captured by the Bradennutrition subscale. Metabolic demand includesphysiologic alterations, severity of illness, andsurgical intervention. Gender, body habitus,age, and demographic variables identified inboth Waterlow’s (1985) and Braden andBergstrom’s (1987) models were combined asa second proposed supplement to Braden andBergstrom’s (1987) intrinsic factor conceptbecause they affect the body’s ability todistribute pressure. Each of these variablesaffects subcutaneous fat stores, which arecritical in dispersing the effects of extraneouspressure (Nixon, 2001).

Threat to skin integrity is the third conceptproposed to supplement the construct represent-ing intrinsic factors that affect tissue tolerance.We maintained threats to skin integrity as adiscrete concept because it contributes elementsof pressure ulcer risk that are not directly relat-ed to metabolic balance or the tissues’ ability todistribute pressure.

Tissue Tolerance as a ModeratingFactor

Defloor (1999) questioned the placement ofBraden and Bergstrom’s (1987) tissue toleranceconstruct within their model. Defloor arguedthat Braden and Bergstrom’s placement of thetissue tolerance concept indicated that tissue tol-erance was independently capable of producingpressure ulcers in the absence of pressure.

Defloor subsequently adjusted his model toindicate a moderating effect of tissue toleranceon pressure ulcer outcomes. However, it is clearin Braden and Bergstrom’s accompanying textthat they also view tissue tolerance as having amoderating influence on the development ofpressure ulcers.To emphasize its moderating effects on

pressure ulcer outcomes in the presence ofpressure, our proposed model, using theconvention suggested by Bennett (2000), placedBraden and Bergstrom’s augmented tissuetolerance construct between Pressure andPressure Ulcer outcome.

The Final Model

The proposed conceptual model as presented inFigure 3 posits that metabolic supply anddemand, pressure distribution capacity, andthreats to skin integrity are risk factors thataugment Braden and Bergstrom’s (1987)concept of intrinsic factors affecting tissuetolerance in critically ill patients. Metabolicsupply and demand are factors that alter physio-logic balance and include the concepts of perfu-sion/oxygenation, the Braden Scale’s nutritionsubscale, surgical treatment, severity of illness,and other physiologic alterations such asdialysis, body temperature, and steroid use.Pressure distribution capacity refers to thesubcutaneous fat store’s ability to distributepressure over the body surface; variablesinclude gender, body habitus, and age. Threatsto skin integrity refer to conditions that affectthe skin’s protective ability; variables includepreexisting pressure ulcer, dry or thin skin,

Table 7. (Continued)

Risk Factor and Study Measurement Conceptual Group

Surgery (Lindgren et al., 2004) Required surgery during hospitalstay

Surgical Intervention

Male gender (Lindgren et al., 2005) Gender GenderSex—Waterlow (Anthony et al.,

2000)

Decreased body weight (Lindgrenet al., 2004)

BMI (weight indexed with height) Body Habitus

Build/Weight—Waterlow (Anthonyet al., 2000)

Decreased body weight (Allmanet al., 1995)

Note: APACHE II, Advanced Physiology and Chronic Health Evaluation II; ASA, American Society of Anesthesiolo-

gists; NYHA, New York Heart Association functional classification; BMI, body mass index.

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edema, skin problems in pressure prone areas,and chemical exposure such as with fecalincontinence.

The model indicates that tissue tolerancefunctions as a moderating factor betweenpressure and pressure ulcer development. Theintrinsic risk factors presented in this model canguide research on pressure ulcer risk factors incritically ill patients to (a) more fully explainthe disproportionate incidence of pressure ulcersin this vulnerable patient population; and (b)target risk factors amenable to intervention.

Discussion

The purpose of this review was to identify riskfactors for pressure ulcer development in criti-cally ill patients and organize them into a

conceptual model that guides pressure ulcerresearch in this population. As patients in ICUsare prone to pressure ulcer incidence, under-standing the salient risk factors for the criticallyill will help target prevention measures. Weexpanded the etiologic understanding ofpressure ulcer genesis in critically ill patients byaugmenting the tissue tolerance construct inBraden and Bergstrom’s (1987) conceptualmodel with ICU-specific intrinsic risk factorsidentified in a review of the literature.In applying the model, the potential moderat-

ing effects of evolving technological advancesin treatment processes on pressure ulcer devel-opment should be considered. When viewedwithin the context of their effect on the sensitiv-ity and specificity of the current Braden Scale,technological innovations such as advancedmattress surfaces and improved incontinence

FIGURE 3. Conceptual model for pressure ulcer etiology in critically ill patients. Metabolic supplyincludes the concepts of perfusion/oxygenation, and the Braden Scale’s nutrition subscale. Metabolicdemand includes surgical treatment, severity of illness, and physiologic alterations. Pressure distribu-tion capacity includes gender, body habitus, and age. Threats to skin integrity include preexisting pres-sure ulcer, dry/thin skin, edema, skin problems in pressure prone areas, and chemical exposure suchas with fecal incontinence. Items identified as ‘‘Braden’’ are risk factors from The Braden Scale forPredicting Pressure Sore Risk� (Copyright by Braden & Bergstrom, 1988).

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control could arguably reduce the Braden’ssensitivity by moderating extrinsic risk factorssuch as moisture, friction/shear, and pressuredistribution contained within the Braden scale.Indeed, approximately 83% (19 out of 23 possi-ble points or 5 out of the 6 subscales) of theBraden Scale is dedicated to evaluating riskfactors that may be modifiable by technologicadvancements in patient care delivery. However,despite these innovations in patient care deliveryprocesses, the incidence of hospital acquiredpressure ulcers (HAPUs) continues to rise.HAPU rates increased by 63% between 1993and 2006 (Russo & Elixhauser, 2006), suggest-ing that elements of intrinsic risk that are notmodifiable by technological advancements havea disproportionate influence on the developmentof pressure ulcers. This review augments theremaining 17% of the Braden Scale exclusivelydedicated to evaluating intrinsic risk factors,such as metabolic supply and demand, that arenot modifiable by technological innovations. Byenhancing the definitional clarity of Braden andBergstrom’s (1987) intrinsic factor concept, theresulting theoretical reduction in the percentageof false positive screening occurrences will helpto increase the Braden Scale’s specificity andPPV in ICU settings.

Further research will be conducted to refinethe conceptual model. Finalizing the conceptualmodel for pressure ulcer risk factors in criticalcare settings has the potential to enhance consis-tency in research on pressure ulcer risk andguide targeted prevention efforts.

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