ARTICLE IN PRESS

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International Journal of Nursing Studies 44 (2007) 655–663

www.elsevier.com/locate/ijnurstu

Skin alterations of intact skin and risk factors associated withpressure ulcer development in surgical patients: A cohort study

Jane Nixona,�, Gillian Crannyb, Senga Bondc

aClinical Trials Research Unit, University of Leeds, 17 Springfield Mount, Leeds LS2 9NG, UKbCentre for Reviews and Dissemination, Alcuin Block B, University of York, Heslington, York YO10 5DD, UK

cSchool of Population and Health Sciences, University of Newcastle, William Leech Building, The Medical School, Framlington Place,

Newcastle upon Tyne NE2 4HH, UK

Received 22 February 2005; received in revised form 24 January 2006; accepted 28 February 2006

Abstract

Background: The pathology literature suggests three types of pressure ulcer with six possible mechanisms leading to

tissue breakdown. A limitation of current evidence is the difficulty in replicating the clinical situation and in

determining the point at which a tissue assault becomes irreversible and results in tissue breakdown. In particular

clinical observations of alteration in darkly pigmented skin, blanching erythema, non-blanching erythema and non-

blanching erythema with other skin changes including induration, oedema, pain, warmth or discolouration have not

been assessed in relation to subsequent skin/tissue loss and their pathophysiological and aetiological importance is not

fully understood.

Objectives: To assess the validity of clinical signs of erythema as predictors of pressure ulcer development and identify

variables which independently are predictive of XGrade 2 pressure ulcer development.

Design: Prospective cohort study.

Participants: 109 general, vascular and orthopaedic hospital patients, aged over 55 years with an expected length of

stay ofX5 days were recruited. Of these 97 were pressure ulcer free at baseline and/or had complete follow-up including

59 women and 38 men with a median age of 75 years (range 55–95).

Setting: Single centre large acute UK NHS hospital.

Methods: To identify clinical signs of erythema predictive of skin loss, the odds of pressure ulcer development were

examined using logistic regression. To identify variables independently predictive of XGrade 2 pressure ulcer

development logistic regression modeling was undertaken.

Results: There was significantly increased odds of pressure ulcer development associated with non-blanching erythema

(7.98, p ¼ 0:002) and non-blanching erythema with other skin changes (9.17, p ¼ 0:035). Logistic regression modeling

identified non-blanching erythema, pre-operative albumin, weight loss, and intra-operative minimum diastolic blood

pressure, as independent predictors of GradeX2 pressure ulcer development.

Conclusions: Non-blanching erythema with or without other skin changes is distinct from normal skin/blanching

erythema and is associated with subsequent pressure ulcer development.

r 2006 Elsevier Ltd. All rights reserved.

Keywords: Pressure ulcers; Cohort study; Risk factors; Pressure ulcer classification; Skin erythema

e front matter r 2006 Elsevier Ltd. All rights reserved.

urstu.2006.02.010

ing author. Tel.: +44133 343 1488; fax: +44113 343 1471.

ess: j.e.nixon@leeds.ac.uk (J. Nixon).

ARTICLE IN PRESSJ. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663656

What is already known about the topic?

�

there are pathophysiological differences between

‘normal’ skin, blanching erythema and non-blanch-

ing erythema

�

cohort studies suggest five key risk factors associated

with pressure ulcer development—mobility, nutri-

tion, factors affecting tissue perfusion, skin condition

and age.

�

risk factors identified support the theoretical schema

of the aetiology of pressure ulcer development where

the interaction between the intensity and duration of

pressure (mobility) and the tolerance of the skin

(nutrition, perfusion and age) determines the skin

response (skin condition).

What this paper adds

�

first cohort study to explore in detail the risk factor

‘skin condition’ and the relationship between blanch-

ing erythema, non-blanching erythema and other

alterations to intact skin and pressure ulcer develop-

ment using a multi-variate risk factor analysis.

�

exploration of erythema at both the patient level and

independently by skin site.

1. Introduction

Pressure ulcers are described as ‘an area of localised

damage to the skin and underlying tissue caused by

pressure, shear, friction and or a combination of these’

(EPUAP, 1999). They vary in size and severity of tissue

layer affected, ranging from skin erythema to damage to

muscle and underlying bone (Witkowski and Parish,

1982). They are associated with increased mortality rates

and are a marker for underlying disease severity and

other comorbitities (Thomas et al., 1996).

A review of the mechanisms that protect the skin

microvasculature from ischaemic assault and restore

local tissue perfusion following occlusion illustrates

clearly that there is an interaction between the pressure

assault and the capacity of the skin to maintain and

effectively restore skin blood flow (Nixon, 2001).

A number of auto-regulatory mechanisms exist to

protect the skin from pressure assault and these

processes break down at pressure values that are highly

variable. Pressure ulcer development is multidimen-

sional and complex (Nixon, 2001; Bouten et al., 2003).

A review of the pathology of pressure ulcer develop-

ment suggests three types of pressure ulcer with possibly

six mechanisms that lead to tissue breakdown

(Bosboom, 2001; Bouten et al., 2003; Nixon, 2001).

A limitation of current research is the difficulty in

replicating the clinical situation and in determining the

point at which the tissue assault becomes irreversible

and results in tissue breakdown. There remains an

ongoing debate regarding the importance, description

and assessment of skin alterations of intact skin

including Grade/Stage 1 pressure ulcers (Bethell, 2003;

Bergstrom and Braden, 2002; NPUAP, 1998).

Clinical observations of alteration in darkly pigmen-

ted skin (NPUAP, 1998), blanching erythema, non-

blanching erythema and non-blanching erythema with

other skin changes such as, local induration, oedema,

pain, warmth or discolouration have not been assessed

in relation to skin viability (that is, subsequent skin/

tissue loss) and their pathophysiological and aetiological

importance is not fully understood. The purpose of this

clinical investigation was to explore the relationship

between alterations of intact skin and subsequent skin/

tissue loss.

Pathophysiological differences between ‘normal’ skin,

blanching erythema and non-blanching erythema are

reported. Witkowski and Parish (1982) performed post-

mortem histology and reported a spectrum of histolo-

gical changes, with transitional phases and overlap

between normal, blanching erythema and non-blanching

erythema skin. The histological changes reported ranged

from reactive hypereamia and pathological events

including endothelial dysfunction, neutrophil adhesion

and capillary plugging, consistent with reperfusion

injury. Nixon et al. (2005) assessed skin using laser

Doppler imaging and reported that both blanching and

non-blanching erythema were characterized by high

blood flow of differing intensity, suggesting that the

responses observed are not pathologically different but

reflect the capacity of the skin to increase blood flow

locally up to tenfold compared to baseline. They found

no evidence of low flow associated with reperfusion

injury. Both studies suggest that clinically assessed

blanching and non-blanching erythema are distinct from

normal skin. Other clinically observed alterations to

intact skin are not reported in the pathophysiological

literature.

A number of cohort studies have assessed the

relationship of potential risk factors to pressure ulcer

development using multi-variate modeling. Five key

variables emerge including mobility, nutrition, factors

affecting tissue perfusion, skin condition and age (Nixon

and McGough, 2001). These can be directly related to

the theoretical schema of the aetiology of pressure

ulcer development (Braden and Bergstrom, 1987)

where the interaction between the intensity and duration

of pressure (mobility) and the tolerance of the skin

(nutrition, perfusion and age) determines the skin

response (skin condition) (Nixon and McGough,

2001).

At the time of the study design the relationship of skin

condition to pressure ulcer development was explored

ARTICLE IN PRESSJ. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663 657

and reported in five cohort studies. Variables reported as

important using multi-factor modeling included ‘the

state of the skin at the site’ (Clarke and Kadhom, 1988),

‘physician diagnosed dry or scaling skin’ (Guralnik

et al., 1988), ‘skin redness’ (Marchette et al., 1991),

blanching erythema severity (Schnelle et al., 1997), and

non-blanching erythema (Allman et al., 1995).

In addition, Schnelle et al. (1997) reported that 29%

of non-blanchable erythema observed at first assessment

developed into a Stage 2 pressure ulcer in the same

location, within 60 days. Allman et al. (1995) reported a

very high odds ratio associated with non-blanching

erythema at baseline (7.52, p ¼ 0:05, 95% CI 1.00–

59.12) and that non-blanching erythema observed any

time during hospital follow up was significantly asso-

ciated with pressure ulcer development with conversion

of 11/19 (57.9%) hospital acquired non-blanching skin

areas to a pressure ulcer ðpo0:001Þ.In summary, limited evidence suggests that, blanching

and non-blanching erythema are important precursors

of pressure ulcer development. However, there is no

evidence relating to the observation of non-blanching

erythema with other skin changes including, local

induration, oedema, pain, warmth or discolouration

and the importance of these alterations to intact skin in

relation to the pathology or aetiology of pressure ulcer

development are unknown. In addition, it is not possible

to identify when alterations to intact skin are indicative

of irreversible damage and inevitable Grade 2 pressure

ulcer development.

1.1. Objectives

(a)

To assess the validity of clinical signs of erythema as

predictors of pressure ulcer development.

(b)

To identify variables which independently are

predictive of XGrade 2 pressure ulcer development.

Table 1

Reproduced with permission from Nixon et al. (1999)

Grade Description

0 No skin changes

1a Redness to skin (blanching)

1b Redness to skin (non-blanching)

1b+ Redness to skin (non-blanching) plus one or more:

Pain

Induration

Heat

Edema

Discoloration (specify)

2. Method

2.1. Design

A prospective cohort study was undertaken involving

patients admitted to St. James’s University Hospital,

Leeds between September 1998 and May 1999. Sur-

gical in-patients were recruited and written informed

consent obtained if they met the following inclusion

criteria:

2 Partial thickness wound involving epidermis/dermis

only

(a) 3 Full thickness wound involving subcutaneous tissue

4 Full thickness wound through subcutaneous tissue

Scheduled for elective major general or vascular

surgery OR acute orthopaedic, vascular and general

surgical admission.

to muscle or bone

5 Black eschar

(b) Aged 55 years or over on day of surgery.

(c)

Expected length of stay of 5 or more days.

Exclusion criteria included:

(a)

General surgery sub-specialities including liver,

urology and breast surgery.

(b)

Dark skin pigmentation which precluded reliable

identification of skin erythema.

(c)

Skin conditions over the sacrum, buttocks or heels

which precluded reliable identification of pressure

induced skin erythema.

Elective major general or vascular surgery was defined

as a planned surgical prcedure with an average surgical

time of 90min or more.

Elective general and vascular patients were recruited

pre-operatively. Acute general, vascular and orthopaedic

surgical patients were recruited up to 72h following

admission. Skin was assessed daily until discharge by the

researcher or a Clinical Research Nurse and classified as

detailed in Table 1. Other risk factors were obtained by

clinical assessment and from medical and nursing records.

2.2. Skin classification and outcome definition

The classification scale used was adapted from

international classification scales, (AHCPR (Agency for

Health Care Policy and Research) 1992; EPUAP, 1999)

in order to meet practical data collection requirements

for the purpose of research (Table 1). Specifically, Grade

0 (no skin changes) was included to clearly distinguish

skin assessment of normal skin from missing data. Grade

5 (black eschar) was included as a separate grade until

wound debridement enabled classification by tissue layer.

In addition, alterations to intact skin were classified as

blanching (1a), non-blanching (1b) and non-blanching

with other skin changes including, local induration,

oedema, pain, warmth or discolouration (1b+).

ARTICLE IN PRESSJ. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663658

The dependent outcome variable ‘pressure ulcer’ was

defined as a skin area assessed as XGrade 2 (Table 1),

that is, a superficial skin break/blister or worse.

2.3. Sample size

To assess the validity of clinical signs of erythema as

predictors of pressure ulcer development a sample of 300

patients was estimated for the comparison of the

proportions of patients classified as having Grade 0,

Grade 1a, Grade 1b and Grade 1b+ skin areas

preceding pressure ulcer development. This was based

on a Chi-squared test with 95% power at the 5%

significance level (two-sided) and was estimated using

the following proportions: Grade 0, 33%; Grade 1a,

40%; Grade 1b, 20% and; Grade 1b+, 7%. These

estimates were based upon previous prospective cohorts

(Nixon et al., 1998; Nixon et al., 1999).

Sample size for multi-factoral analyses are difficult to

estimate because parameters such as correlations be-

tween variables and effect sizes are difficult to obtain.

Therefore, to identify variables which are independently

predictive of subsequent pressure ulcer development

using regression methods an accepted ‘rule of thumb’

was applied, that is analysis would include no more than

n/10 variables, where n is the sample size (Altman, 1991).

2.4. Statistical method

A w2 test was used to compare the proportions of

patients classified as having Grade 0, Grade 1a, Grade

1b and Grade 1b+ on any skin site preceding pressure

ulcer development. Skin changes preceding pressure

ulcer development were also classified by Grade,

independently for each site, and the difference in

frequency of pressure ulcers between Grades examined

using Fisher’s exact test.

To identify which clinical signs of erythema were

predictive of skin loss, the odds of pressure ulcer

development for Grade 0, Grade 1a, 1b and 1b+ were

examined using single factor logistic regression.

To identify variables which independently are pre-

dictive of XGrade 2 pressure ulcer development, the

relationship between risk factors and pressure ulcer

development was explored using a three stage process

for patients who were pressure ulcer free at baseline. The

‘worst’ skin grade recorded at any time and on any site

during hospital stay or preceding pressure ulcer devel-

opment was used to categorise skin alteration as a risk

factor. Univariate analysis used single factor logistic

regression with a binary response of pressure ulcer or no

pressure ulcer. Variables were excluded from further

analysis if the p value was X0.2 (Altman, 1991) or

X25% of data was missing. Correlations between

variables were then examined using Pearson’s correla-

tion coefficient for continuous data or Spearmans rank

correlation for ordered categorical data. Where variables

were correlated with a correlation coefficient of 40.7

and an associated p-value of o0.01 (Fielding et al.,

1992), one was eliminated from further consideration.

The final candidate variables were entered into a

logistic regression model using forward stepwise selec-

tion. The p value determined entry (o0.25) and removal

(40.9). The variables identified by the forward stepwise

selection were then used as the basic model for further

logistic regression analysis. Correlated variables were

dropped and added systematically in order to determine

the final model in which each variable independently

predicted subsequent pressure ulcer development as

assessed by the size of the p value.

The model was determined only from patients with

complete data for all candidate variables. Therefore,

when the final set of variables was obtained the model

was refitted with only those final variables in the model

statement.

Analyses were carried out using the Stata Statistical

Software package.

3. Results

3.1. Sample

One hundred and nine patients were recruited to a

prospective cohort study, within the funding period and

follow-up was complete for 97. Incomplete follow-up

resulted from cancelled elective surgery and early

discharge (4), patient request to discontinue (4) and

presence of pressure ulcer at baseline assessment (4).

The sample comprised 59 women and 38 men

admitted for vascular (37), general (22) and orthopaedic

(38) surgery. Fifty-three patients were planned admis-

sions and 44 acute. The median age of the sample was 75

years (range 55–95 years).

A total of 26 pressure ulcers were observed on 15

patients during their hospital stay an incidence rate of

15.5%. The majority of pressure ulcers observed were

superficial ulcers, with 23 classified as Grade 2 and three

Grade 4 ulcers. Body sites affected included heels (9),

sacral areas (10) and buttock areas (7). The three severe

ulcers were observed on the heels of two patients.

Chi-squared analysis identified a statistically signifi-

cant association between Grades and subsequent pres-

sure ulcer development (Table 2). Due to the small

numbers of Grade 0 observations single factor logistic

regression was undertaken using Grade 1a as the

baseline comparison (Table 3). This procedure identified

significantly increased odds of pressure ulcer develop-

ment associated with the observation of Grade 1b (7.98,

p ¼ 0.002) and 1b+ (9.17, p ¼ 0.035). An increased

odds was also associated with Grade 0 (3.06, p ¼ 0.365)

compared to 1a but this was not statistically significant.

ARTICLE IN PRESSJ. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663 659

Skin assessment data were classified by Grade 0–1b+,

independently for each site, and the association between

Grade and pressure ulcer development was examined

using Fisher’s exact test. From a total of 485 skin areas

(five per patient), six were excluded due to the presence

of an amputated or bandaged limb. Two of the five skin

sites demonstrated a statistically significant association

between the worst skin Grade recorded (0–1b+) and

conversion to pressure ulcer (right buttock and right

heel), with high incidence rates noted for skin areas

clinically assessed as 1b and 1b+. Only 3.28% and

2.83% of skin areas assessed as normal (0) and

Table 2

Skin changes preceding pressure ulcer occurrence

Pressure

ulcer

Grade 0 Grade

1a

Grade

1b

Grade

1b+

Total

No 6 55 17 4 82

Yes 1 3 9 2 15

Total 7 58 26 6 97

Number of cases n ¼ 97.

w2 ¼ 13.02, p ¼ 0.005.

Table 3

Single factor logistic regression model of skin changes preced-

ing pressure ulcer occurrence compared to grade 1a

Odds ratio p 95% CI

Grade 0 3.06 0.365 0.27–34.19

Grade 1b 9.71 0.002 2.36–39.97

Grade 1b+ 9.17 0.035 1.17–71.71

Number of cases n ¼ 97.

Table 4

Variables explored by univariate analysis

Patient variables

Age (years)*, gender, Braden subscales (6) and total score, existing wou

albumin(g/l), pre* and post-operative* haemoglobin (g/dl), body mas

temperature (1C), pre-operative blood pressure (mmHg)

Admission variables

Type of admission (elective/acute)*, type of surgery (vascular/general

Intervention variables

Ward mattress (foam/alternating overlay/alternating replacement)

Intra-operative variables

Diastolic blood pressure—minimum*, maximum*, final (mmHg), sys

of anaesthetic (general/spinal and epidural)*, length of surgery (min)

Skin variable

Gradep1a/X1b*

*Indicates the variables with an associated p value of o0.2 when exp

blanching (1a) subsequently developed a pressure ulcer,

whilst 15.15% and 33.33% of areas assessed as non-

blanching (1b) and non-blanching plus (1b+) subse-

quently developed a pressure ulcer.

Thirty-one variables were explored by single factor

logistic regression and 13 variables had an associated p

value of o0.2 (Table 4). Single factor logistic regression

using the variable Grade was limited by the small

number of patients classified as Grade 0 and Grade 1b+

(Table 3). Analysis indicated no statistical difference

between Grades 0/1a or Grades 1b/1b+, therefore the

variable Grade was reclassified as two groups combining

0/1a and 1b/1b+ for all subsequent analysis.

Correlations of variables indicated an association

between many of the variables. However, only minimum

intra-operative diastolic blood pressure and maximum

intra-operative diastolic blood pressure had a correla-

tion coefficient of 40.7 and p-value o0.001, and there

remained a large number of variables measuring the

same physiological indicators at different points in time.

Whilst the use of a stepwise procedure in the multi-

factor modeling does not require exclusion of all

variables (Altman, 1991) a pragmatic approach was

taken to reduce the number of surgery-related variables

which did not have high correlation coefficients but were

significant at p-values of o0.05. The variable with the

lowest p-value was selected for inclusion in the pre-

liminary modeling process and resulted in the exclusion

of post-operative haemoglobin, post-operative albumin

and maximum intra-operative diastolic blood pressure

variables. Similarly type of anaesthetic and acute/

elective surgery were correlated and the variable acute/

elective surgery was excluded.

The final eight candidate variables are detailed in

Table 5. However, difficulties were encountered due

to the amount of missing data for the variables

nd (yes/no)*, diabetes (yes/no), pre* and post-operative* serum

s index, history of weight loss (yes/no)*, pre-operative

/orthopaedic)

tolic blood pressure—minimum, maximum, final (mmHg), type

lored using single factor logistic regression.

ARTICLE IN PRESS

Table 5

Final candidate variables for multi-factor examination—vari-

able parameters

Age

Median (range) 75 (55–95)

Mean (SD) 75.1 (8.95)

Pre-operative haemoglobin (g/dl)

Median (range) 12.9 (8.9–16.3)

Mean (SD) 12.6 (1.68)

Missing 10

Pre-operative albumin (g/l)

Median (range) 39 (24–48)

Mean (SD) 37.4 (5.46)

Missing 15

Diastolic BP minimum (mmHg)

Median (range) 47 (15–90)

Mean (SD) 47.7 (11.99)

Missing 6

Type of anaesthetic

General 87 (89.7%)

Epidural/Spinal 8 (8.2%)

Not applicable 2 (2.1%)

Grade

p1a 65 (67.0%)

X1b 32 (33.0%)

Weight loss

No 66 (68.0%)

Yes 18 (18.6%)

Missing 13 (13.4%)

Wounds

No 84 (86.6)

Yes 13 (13.4)

Table 6

Risk factors identified by forward stepwise logistic regression

Odds ratio p 95% CI

Pre-op albumin 0.81 0.009 0.70–0.95

GradeX1b 7.02 0.008 1.67–29.49

Weight loss 0.29 0.092 0.07–1.22

DiastolicBPmin 0.96 0.205 0.90–1.02

Number of cases n ¼ 90.

J. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663660

pre-operative albumin, pre-operative haemoglobin and

weight loss. Missing values were replaced by imputed

data. Regression models were used to ‘predict’ the value

of the missing items and the predicted values imputed.

Forward stepwise logistic regression identified Gra-

deX1b, pre-operative albumin, weight loss and intra-

operative minimum diastolic blood pressure as the risk

factors associated with pressure ulcer development

(Table 6).

The addition and substitution of the correlated

variables did not significantly alter the model. Repeating

the final model without imputed data resulted in similar

odds associated with pressure ulcer development but

reduced levels of significance and wider confidence

intervals.

4. Discussion

Whilst there was a considerable short-fall in the

sample obtained, the findings remain important and

relevant to nursing practice and assessment of patient

risk.

The overall incidence of new pressure ulcers (XGrade

2) of 15.5% is consistent with other studies of major

surgical and acute orthopaedic patients. The develop-

ment of 3 severe ulcers (XGrade 3) in two patients

(2.06%) is also consistent with studies which reports

pressure ulcer incidence by Grade for this population,

with incidence ranging from 0.19% to 9% (Kemp et al.,

1990; Marchette et al., 1991; Clark and Watts, 1994;

Gebhardt, 1992).

A limitation in establishing the predictive value of

clinical signs of erythema in relation to subsequent

pressure ulcer development was the small sample size,

and differences between Grade 0 and Grade 1a skin

could not be established, nor could differences between

Grade 1b and 1b+ skin.

The small sample was further limited by the large

denominator population of patients who were observed

to have a blanching erythema on at least one site during

their hospital stay. The results concur with Schnelle et

al. (1997) who reported high incidence rates of blanch-

able erythema (94.2%), but are not consistent with other

findings where reported incidence of erythema ranges

from 11.76% to 33.71%; (Allman et al., 1995; Papanto-

nio et al., 1994; Kemp et al., 1990). Attempts to quantify

the duration of blanching erythema was unsatisfactory

due to the small sample.

In relation to differences between non-blanching

erythema and non-blanching erythema with other skin

changes (including local induration, oedema, pain,

warmth or discolouration), crude rates suggest that

clinical observations do reflect important underlying

pathological differences between Grades 1b and 1b+. A

larger proportion (33.33%) of Grade 1b+ skin sites

subsequently developed into a pressure ulcer compared

to Grade 1b (15.15%).

Despite the limitations of sample size, exploration of

erythema at the patient level and independently by skin

site suggest that non-blanching erythema with or with-

out other skin changes are distinct from normal skin/

blanching erythema and associated with subsequent

pressure ulcer development. This was confirmed by the

risk factor analysis, which determined non-blanching

erythema as an independent risk factor.

The multi-factor analysis established variables whose

presence are independently predictive of pressure ulcer

ARTICLE IN PRESSJ. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663 661

development. Whilst the sample size did appear to be

sufficiently large using the accepted ‘rule of thumb’

(Altman, 1991), a number of problems were encountered

with the distribution of characteristics within the sample

and it is possible that the data are not representative

resulting in important effects having been missed.

Specifically, the distributions of some variable para-

meters were skewed by type of surgery. There were

insufficient data within some categorical variables to

undertake meaningful analysis and categories were

combined (for example, Grade). Also, missing data

reduced the sample available within the multi-factoral

modeling process, which requires complete data for all

candidate variables. Regression models were used to

‘predict’ the value of the missing items and these were

used in the subsequent modeling process. This assumes

that missing data is random and the calculation error is

unknown.

The eight candidate variables for multi-factoral

examination (Table 5) are consistent with findings from

other studies which have utilised multi-variate analyses

(Nixon and McGough, 2001). With the exception of

type of anaesthetic, the candidate variables including

age, skin grade, haemoglobin, albumin, weight loss,

wounds and intra-operative diastolic blood pressure are

either direct or indirect measures associated with the key

themes identified as risk factors in pressure ulcer

development including poor nutrition, factors affecting

perfusion, increased age and skin condition (Nixon and

McGough, 2001).

As reported in other studies (Barnes and Payton,

1993; Capobianco and McDonald, 1996; Halfens, 1997;

Langemo et al., 1991; Ramundo, 1995) the Braden Scale

did not discriminate well between patients who did or

did not develop pressure ulcers when analysed as a

continuous variable or categorical variable (p16, 417).

However, the patient population was homogenous, with

a majority of patients (76/97) with a Braden Score

between 13 and 18.

The relationship between type of anaesthetic (general

verses spinal/epidural) and pressure ulcer development is

likely to reflect existing co-morbidity. Spinal and

epidural anaesthesia are administered for various

purposes including induction and maintenance of a

controlled hypotension (for example, during vascular

surgery) and where general anaesthesia is considered to

pose a very high risk to an individual patient due to

associated co-morbidity. Whilst spinal/epidural anaes-

thesia is considered to increase risk by reducing both

blood pressure and mobility (Bliss and Simini, 1999),

further exploration determined that administration of

spinal/epidural anaesthesia in this cohort of patients

was limited to a very small number. Sample size and

clinical indication for administration preclude any

meaningful exploration of associations with intra-

operative hypotension and mobility and no conclusions

can be made regarding its importance as an independent

risk factor.

Despite limitations of the data, the final logistic

regression model is consistent with findings from other

studies which have utilised multi-factoral analyses

(Nixon and McGough, 2001). Non-blanching erythema

is identified as an independent predictor of pressure

ulcer development and a key prognostic factor. Whilst

the confidence interval is wide, the findings from this

study validate the research by Allman et al. (1995) and a

recently published study which also identified non-

blanchable erythema as one of 6 factors independently

associated with XStage 2 pressure ulcer development

(odds ratio 3.13 CI 2.41–4.06, p ¼o0:001) (Reed et al.,

2003).

5. Conclusions

Investigation of the relationship between clinical

observations of changes to intact skin and the develop-

ment of XGrade 2 pressure ulcers, suggests that it is the

observation of non-blanching erythema with or without

other skin changes (local induration, oedema, pain,

warmth or discolouration) which is important in the

development of pressure ulcers. When summarized on

both a patient level and independently by skin site,

blanching erythema was not found to be associated with

pressure ulcer development, but the importance of non-

blanching erythema with or without other skin changes

was confirmed.

The risk factor analysis logistic regression modeling

identified non-blanching erythema (X1b), pre-operative

albumin, weight loss preceding admission and intra-

operative minimum diastolic blood pressure as indepen-

dent predictors of pressure ulcer development.

In relation to blanching erythema, the need to include

such observations in a skin classification system and

record this information in practice requires further

debate. The skin response of patients preceding pressure

ulcer development and the high incidence of blanching

erythema in the sample, illustrate the difficulties in

translating the observation of blanching erythema into a

meaningful indicator of risk. Overall the evidence

relating to blanching erythema as a risk factor is limited.

This cohort study did not identify blanching erythema as

predictive of subsequent pressure ulcer development.

There is evidence that there are pathological differences

between normal skin and blanching erythema

(Witkowski and Parish, 1982; Nixon et al., 2005) and

one prospective cohort study has identified blanching

erythema severity as a predictor of ‘non-blanching

erythema and Grade 2 pressure ulcers’ using multi-

factoral methods. However, like many other studies, this

was limited by small sample size, outcome definition and

atypical population, that is, all patients were incontinent

ARTICLE IN PRESSJ. Nixon et al. / International Journal of Nursing Studies 44 (2007) 655–663662

(Schnelle et al., 1997). Further research is required to

determine the association between duration of blanching

erythema and pressure ulcer development, addressing

design issues such as sample size and characteristics

(such as risk profile) and statistical modeling.

Non-blanching erythema is an independent predictor

of pressure ulcer development. However, it is not

indicative of irreversible ischaemic damage and resolves

in approximately two thirds of cases. The point at which

it becomes irreversible remains unknown. A higher

conversion rate was found where non-blanching erythe-

ma and other skin changes such as localised induration,

pain, oedema and discoloration were also observed,

suggesting these clinical signs are indicative of advancing

pathological change and providing some validation for

the descriptors of a Grade 1 for darkly pigmented skin

(NPUAP, 1998). Evidence from this study and others

(Allman et al., 1996; Reed et al., 2003) emphasize the

importance of detailed skin assessment and observation

in the care of high risk patients. Where non-blanching

erythema with or without other skin changes such as

localised induration, pain, oedema and discoloration is

observed in practice, it should be recorded, prompting

nursing interventions and be reassessed to monitor the

outcome of the treatment provided.

Acknowledgements

The authors would like to acknowledge the contribu-

tion of: Jayne Upperton (Clinical Research Nurse) who

managed patient recruitment and data collection; Da-

wood Dassu who provided statistical advice and

supported the analysis; the staff of St James’s University

Hospital, Leeds, including ward, theatre and anaesthetic

recovery staff who supported the research.

Conflicts of Interest: Jane Nixon has been reimbursed

for attending conferences, has been paid speakers fees

and received research funding from Huntleigh Health-

care Ltd. Gillian Cranny and Senga Bond have no

conflicts of interest to declare.

Author Contributions: Jane Nixon was the Chief

Investigator, conceived the study, led all grant applica-

tions, protocol development, data analysis and manu-

script preparation. She was also involved in the

recruitment and follow-up of some patients. Gillian

Cranny critically appraised and revised important

intellectual content and undertook some analysis.

Senga Bond supervised the research from conception

to completion, though the design, analysis, interpreta-

tion and manuscript preparation, including revising

the manuscript critically for important intellectual

content.

Funding awards from the Tissue Viability Society

Training Fellowship (UK) and the Smith and Nephew

Foundation Nursing Research Fellowship were made to

Jane Nixon. These organizations peer reviewed the grant

application and received a report of the findings.

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