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ARTICLE IN PRESS
0020-7489/$ - se
doi:10.1016/j.ijn
�CorrespondE-mail addr
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: [email protected] (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 associatedwith pressure ulcer development—mobility, nutri-
tion, factors affecting tissue perfusion, skin condition
and age.
�
risk factors identified support the theoretical schemaof 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 andindependently 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 aspredictors of pressure ulcer development.
(b)
To identify variables which independently arepredictive of XGrade 2 pressure ulcer development.
Table 1Reproduced 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 tissue4 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 bone5 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 reliableidentification of skin erythema.
(c)
Skin conditions over the sacrum, buttocks or heelswhich 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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