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Supplementing the Braden scale for pressure ulcer risk among medical inpatients: the contribution of self-reported symptoms and standard laboratory tests. Ingrid Johansen Skogestad, MSc, RN*; Liv Martinsen, RN; Tove Elisabet Børsting, Assistant Professor, MSc, Paediatric Nurse, RN; Tove Irene Granheim; Eirin Sigurdssøn Ludvigsen MNc, CCN, RN; Caryl L. Gay, PhD, Researcher; Anners Lerdal, PhD, RN, Professor and Research Director Word count: 5504

IJS (*Corresponding author): Medical Department, Lovisenberg Diakonale Hospital, Lovisenberggata 17, N-0456 Oslo, Norway Telephone +4723226040. Fax: +4723225881 E-mail: ingridjohansen.skogestad@lds.no LM Medical Department, Lovisenberg Diakonale Hospital, Lovisenberggata 17, N-0456 Oslo, Norway Telephone +4723225870. Fax: +4723225881 E-mail: liv.martinsen@lds.no TEB Lovisenberg Diaconal University College, Lovisenberggata 15b, N-0456 Oslo, Norway Telephone 92447764. E-mail: tove.borsting@ldh.no TIG & ESL Surgical Department, Lovisenberg Diakonale Hospital, Lovisenberggata 17, N-0456 Oslo, Norway Telephone +4723226291/6353 E-mail: toveirene.granheim@lds.no & eirinsigurdsson.ludvigsen@lds.no CLG Department of Family Health Care Nursing, School of Nursing, University of California, San Francisco, USA and Department of Research and Development, Lovisenberg Diakonale Hospital, N-0456 Oslo, Norway. 2 Koret Way, Room N411Y, Box 0606, San Francisco CA, 94143-0606. Telephone: +14154764435 Fax: +14157532161 E-mail: caryl.gay@ucsf.edu AL Dept. of Nursing Science, Institute of Health and Society, Faculty of Medicine, University of Oslo, Norway and Department of Research and Development, Lovisenberg Diakonale Hospital, Lovisenberggata 17, N-0456 Oslo, Norway. Telephone: +4723225000, Fax: +4723225023, E-mail: anners.lerdal@medisin.uio.no Acknowledgements

Anne Marit Tangen, Lars Vasli, Ellen-Anne Alvin, Tove Mosvold, Magne Hustavenes, Gro Mikkelsen, Magnus Tarangen, Einar Amli, Laila Randen Stenrud, Heidi Irene Hammerstad, Andreas Grønbeck, Reidun Grimsbø, Caroline Hammer, Margrete Bjørkhaug, Nina Kristiansen, Ingrid Holter, Leif Brunsvik.

This study was funded by Lovisenberg Diakonale University College and Lovisenberg Diakonale Hospital.

Contributions

Study design: AL, TIG; data collection and analysis: IJS, LM, TEB, TIG, ESL, CG, AL; manuscript preparation: IJS, LM, TEB, TIG, ESL, CG, AL

Conflict of interest

The authors declare no financial or personal interests that could bias the work.

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Supplementing the Braden scale for pressure ulcer risk among medical inpatients:

the contribution of self-reported symptoms and standard laboratory tests.

ABSTRACT

Aims and objectives. To evaluate medical inpatients’ symptom experience and selected laboratory

blood results as indicators of their pressure ulcer risk as measured by the Braden scale.

Background. Pressure ulcers reduce quality of life and increase treatment costs. The prevalence of

pressure ulcers is 6-23% in hospital populations, but literature suggests that most pressure ulcers are

avoidable.

Design. Prosepective, cross-sectional survey.

Methods. 328 patients admitted to medical wards in an acute hospital in Oslo, Norway consented to

participate. Data were collected on 10 days between 2012 and 2014 by registered nurses and nursing

students. Pressure ulcer risk was assessed using the Braden Scale, and scores <19 indicated pressure

ulcer risk. Skin examinations were categorized as normal or stages I-IV using established definitions.

Comorbidities were collected by self-report. Self-reported symptom occurrence and distress were

measured with 15 items from the Memorial Symptom Assessment Scale, and pain was assessed using

two numeric rating scales. Admission laboratory data were collected from medical records.

Results. Prevalence of pressure ulcers was 11.9%, and 20.4% of patients were identified as being at risk

for developing pressure ulcers. Multivariable analysis showed that pressure ulcer risk was positively

associated with age ≥80 years, vomiting, severe pain at rest, urination problems, shortness of breath and

low albumin, and was negatively associated with nervousness.

Conclusion. Our study indicates that using patient-reported symptoms and standard laboratory results as

supplemental indicators of pressure ulcer risk may improve identification of vulnerable patients, but

replication of these findings in other study samples is needed.

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Relevance to clinical practice.

• Nurses play a key role in preventing pressure ulcers during hospitalization. A better

understanding of the underlying mechanisms may improve the quality of care.

• Knowledge about symptoms associated with pressure ulcer risk may contribute to a faster

clinical judgment of patients at risk.

Key words. Pressure ulcer, risk factors, risk assessment, symptoms, and laboratory results

What does this paper contribute to the wider global clinical community?

• Assessment of patient symptoms, age and albumin levels may help identify which patients are at

risk for pressure ulcers.

• The patient-reported symptoms associated with pressure ulcer risk in this sample of medical

inpatients included vomiting, severe pain at rest, urination problems, shortness of breath and

nervousness.

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INTRODUCTION

Pressure ulcers can develop within hours during hospitalization (Gefen 2008) and early

identification of patients at risk is the first step towards preventing this unnecessary complication

(Cuddigan et al. 2001, NPUAP et al. 2014). The prevalence of pressure ulcers in the general hospital

population varies between 10 and 23% (Cuddigan et al. 2001, Bours et al. 2002, Bredesen et al. 2015),

and based on systematic pressure ulcer risk screening (i.e. Braden Scale), 35-50% of hospitalized

patients are at risk of developing a pressure ulcer (Bours et al. 2002, Vanderwee et al. 2007).

Furthermore, most pressure ulcers are avoidable (Black et al. 2011, Pinkney et al. 2014).

Pressure ulcers reduce health-related quality of life and are associated with fatal septic infections

and higher mortality (Redelings et al. 2005, Gorecki et al. 2009). Patients with pressure ulcers have

prolonged hospitalization and increased hospital costs (Theisen et al. 2012). Several factors have been

associated with the development of pressure ulcers, including older age, multiple comorbidities,

immobility, nutritional status and laboratory results (Coleman et al. 2013). However, clinical features in

patients at risk of pressure ulcer development have not been fully characterized.

BACKGROUND

Pressure ulcer is defined as a “localized injury to the skin and/or underlying tissue usually over a

bony prominence, as a result of pressure, or pressure in combination with shear” (NPUAP et al. 2014, p.

12). It has been proposed that pressure ulcers result when these mechanical pressure and shear forces

interact with patient vulnerabilities, such as localized ischaemia, reperfusion injury, impaired lymphatic

drainage or cell deformation (Coleman et al. 2014). In addition, skin microclimate, including both

temperature and surface moisture, has been implicated in the aetiology of pressure ulcer, as increased

temperature can impair perfusion and excessively moist or dry skin can increase shear forces (Dealey et

al. 2015). Pressure ulcers can vary in severity from non-blanchable erythema to full thickness tissue

loss.

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Pressure ulcers are associated with a numbers of factors, but the significance of these factors

remains unclear (NPUAP et al. 2014). Older age (e.g. above 75 years) and immobility are well-known

risk factors for pressure ulcer development (Wann-Hansson et al. 2008, Gunningberg et al. 2011), but

there are contradictory findings regarding several other proposed risk factors. Most studies report no

gender difference (Eberlein-Gonska et al. 2013, Bredesen et al. 2015), although some studies have

reported men as being at higher risk than women (Scott et al. 2006). Urinary incontinence and low body

mass index (BMI) have also been considered as risk factors in some studies (Compher et al. 2007,

Gunningberg et al. 2011). There are conflicting results with respect to comorbidities as risk factors,

including diabetes, cardiovascular disease, respiratory disease, fracture, cognitive failure, neurological

diseases and cancer (Perneger et al. 1998, Nonnemacher et al. 2009, Amir et al. 2011). Furthermore,

recent studies have shown associations between pressure ulcers and low albumin, high C-reactive

protein (CRP) and low hemoglobin (Hatanaka et al. 2008), but most studies on pressure ulcers do not

include laboratory results.

The Norwegian Patient Safety Program (2014), outlined by the Norwegian Ministry of Health

and Care Services, recommends the use of a structured risk assessment scale, such as the Braden scale,

when patients are admitted to hospital or other care facilities. The Braden scale (Bergstrom et al. 1987)

was developed to facilitate the identification of patients with pressure ulcer risk and is a well tested and

widely used instrument (Vanderwee et al. 2007). Although the value of the more than 40 pressure ulcer

risk scales has been questioned in the research literature (Kottner & Balzer 2010), a systematic review

concluded that the Braden scale is the most thoroughly validated, is the best predictor of pressure ulcer

risk, and has the best balance between sensitivity and specificity compared to other scales (Pancorbo-

Hidalgo et al. 2006). International guidelines further advise that a risk assessment scale should not be

used alone, but rather should be combined with a skin assessment and clinical judgment informed by

knowledge of relevant risk factors to determine each patient’s level of risk (NPUAP et al. 2014).

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While the risk assessment guidelines recommend consideration of other relevant risk factors

such as advanced age, skin status and poor nutritional status (NPUAP et al. 2014), the research literature

is contradictory with regard to such risk factors for pressure ulcers in hospitalized patients. Thus, further

studies in this area are needed to ensure a better understanding of which patients are at risk for pressure

ulcers. The contradictions in the literature may be a result of differences in study population (e.g., ICU

patients, immobile patients, patients with fracture or spinal cord injury) or unreliable conclusions based

on small numbers. Coleman et al. (2014) has proposed a pressure ulcer risk assessment framework that

combines laboratory blood values with other potential risk factors to identify patients at risk of pressure

ulcer development, and several studies do this in an acute hospital settings (Anthony et al. 2011, Raju et

al. 2015). However, to our knowledge, no studies have explored the potential association between

pressure ulcer risk and patients’ symptoms. A better understanding of these potential relationships would

be valuable knowledge for nurses and health authorities and may improve the assessment of pressure

ulcer risk.

Thus, the aim of this study was to describe the prevalence of pressure ulcers and pressure ulcer

risk in medical patients at an acute general hospital and to examine possible risk factors, including

sociodemographic factors, comorbidities, symptom experience, and laboratory blood values. Due to the

hospital’s relatively low prevalence of pressure ulcers, the study focuses on factors related to pressure

ulcer risk (as measured by the Braden scale) rather than to actual pressure ulcers. This approach may

have the additional benefit of characterizing patients at risk before they develop pressure ulcers so that

nurses and other health care professionals can implement strategies to prevent them.

METHODS

Design and Setting

This prospective, cross-sectional study was conducted in the medical and elective surgical wards of a

general hospital in Oslo, Norway, between September 2012 and May 2014. The study is part of a larger

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research project involving the hospital’s nurses in the standardized screening of patients’ pain intensity

and risk of pressure ulcers, falls, and malnutrition. Given the relatively low risk of pressure ulcers

among elective surgery patients, this analysis focuses specifically on patients in medical wards. The

medical department treats approximately 7800 patients annually and offers free acute medical services to

a specific catchment area of Oslo. Pulmonary, cardiovascular, gastro-intestinal and infectious diseases

are the main disease groups for which patients are treated. Patients admitted to the hospital have standard

foam mattresses. Based on the nurses’ clinical judgment, patients considered at risk of developing

pressure ulcer are provided with pressure redistributing surfaces (Tempur-MED) and the few patients

considered to be at very high risk are provided with alternating pressure air mattresses (Arjohuntleigh

Alpha Response).

Study population

All adult inpatients (≥18 years) admitted to one of the hospital’s medical wards by 7 AM on 10

prescheduled days (4 during the first project year and 6 during the second) were asked to participate in

the study. Patients admitted to hospice or the intensive care unit or who were cognitively impaired or

unable to read Norwegian were not included. For patients screened on more than one screening day,

only data from the date they first consented was included in the analysis; data from their other screenings

was excluded. During the second year of the study (last 6 screening days), the hospital implemented

routine screening for pressure ulcer risk as part of standard procedures. Thus, age, gender and risk

screening scores for patients who did not participate in the research project on these dates were

compared to study participants for evaluation of possible sampling bias.

Data collection

Before the study started, the research staff (second year nursing bachelor students and a selected group of

ward nurses attending to the project) were trained on the study protocol, including informed consent,

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standardized screening and skin examination. The training consisted of a three-hour session led by the

senior author and four risk specialists (i.e., a nurse, a physiotherapist, a nutritionist and an assistant

professor in nursing). All ward nurses underwent training in skin exams and pressure ulcer classification.

Data on age and gender was collected from the patients’ medical records. Data on co-morbidity and

symptoms was collected using questionnaires on the day of screening. Each patient’s primary nurse

conducted a skin examination and pressure ulcer classification. The pressure ulcer risk screenings were

conducted by bachelor students in nursing and ward nurses specially trained for the project. Laboratory

blood results were collected from medical records.

Measurements

The dependent variable was pressure ulcer risk, defined as a Braden score <19. The independent

variables were divided into four categories: (1) socio-demographic characteristics (age and gender were

collected from the patients’ medical record), (2) clinical variables (comorbidities, length of hospital stay

and body mass index), (3) symptoms and (4) laboratory blood results.

The Braden scale (Bergstrom et al. 1987) was used to assess pressure ulcer risk. It consists of 6

items related to known risk factors for pressure ulcers: sensory perception, moisture, activity, mobility,

nutrition, and friction and shear. Each item is scored on a scale of 1 to 3 or 4, with lower scores

indicating greater risk of pressure ulcer. Item scores are summed to yield a total score ranging from 6

(highest risk) to 23 (lowest risk). Total scores below 19 are indicative of pressure ulcer risk. The Braden

Scale has demonstrated acceptable validity and reliability (Bergstrom et al. 1998, Kring 2007).

Prevalence of pressure ulcers was determined by skin examination, and the results were coded

according to the definitions established by the National Pressure Ulcer Advisory Panel (NPUAP) as

normal or stage I-IV: non-blanchable erythema (I), partial thickness skin loss (II), full thickness skin loss

(III) and full thickness tissue loss (IV) (NPUAP et al. 2014). If patients had more than one pressure ulcer,

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each ulcer was staged and all locations were registered. For analysis, patients were categorized as having

a normal or abnormal (stage I-IV) skin exam based on their most severe pressure ulcer.

Body mass index was calculated based on height and weight obtained on the day of screening or

from the medical record. Data on 13 comorbidities were obtained by self-report. Patients were asked if

they ever had one of the following diseases and if so, whether it was a current condition: cardiovascular

disease, pulmonary disease, cancer, gastro-intestinal disease, muscular-skeletal disease, fracture,

cognitive impairment, neurological disease, psychiatric disease, significant vision loss, significant

hearing loss, diabetes mellitus, other comorbid condition. Because cognitive impairment was an

exclusion criterion, patients who reported current cognitive impairment (n=9) were considered ineligible

and were excluded from the analysis, and this comorbidity was not evaluated. This analysis focused only

on current comorbidities given the improbability of past conditions impacting current pressure ulcer risk.

An abbreviated version of the Memorial Symptom Assessment Scale (MSAS) (Portenoy et al.

1994) was used to assess a variety of physical and psychological symptoms relevant to the three areas of

risk screening in the project (pressure ulcers, falls and malnutrition). Patients were given a list of 15

symptoms and were asked to indicate whether or not they had each symptom during the past week (i.e.,

occurrence). If they experienced the symptom in the past week, they were asked to rate the level of

distress it caused using a five-point Likert Scale (i.e., 0 = not at all, 1 = mild, 2 = moderate, 3 = severe, 4

= very severe). A score of 3 or 4 was indicative of severe distress related to that symptom. The list

consisted of the following symptoms: difficulty concentrating, lack of energy, feeling nervous, nausea,

feeling drowsy, numbness or tingling in hands or feet, difficulty sleeping, vomiting, problems with

urination, shortness of breath, diarrhea, itching, dizziness, swelling of arms or legs and changes in skin.

The reliability and validity of the MSAS is well established (Portenoy et al. 1994).

Pain intensity on activity and at rest were measured using two self-report items based on the

average pain item from the Brief Pain Inventory (BPI) (Cleeland 1985). The BPI has been validated in

Norwegian cancer patients (Klepstad et al. 2002) and has also been used with non-cancer patients

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(Keller et al. 2004). Patients retrospectively rated the intensity of their average pain during the last 24

hours (both on activity and at rest) using an 11-point numeric rating scale (NRS) (Williamson & Hoggart

2005), suitable for both younger and older patients (Gagliese et al. 2005). The anchor points are 0 = no

pain and 10 = worst imaginable pain. Severe pain was defined as a score of 7 or higher (McCaffery et al.

1994).

All patients admitted to the hospital had standard laboratory blood tests performed on the day of

admittance. The following blood tests have been identified as relevant to pressure ulcer risk in prior

studies and were therefore included in the current analysis: hemoglobin, hematocrit, C-reactive protein

(CRP), and albumin. Standard reference values were used to categorize the following laboratory results

as abnormal: hemoglobin<12 g/ml, hematocrit<0.35, CRP>10 mg/L, and albumin<35 g/L. Hemoglobin

and hematocrit were measured using Sysmex K4500 or Advia 2120I. CRP and albumin were measured

using Cobas 6000.

Ethics

The Regional Committee for Medical and Health Research Ethics (REC South-East) and the hospital

management approved the study (Reference # 2012/980A). All patients received verbal and written

information about the study, and all participants signed consent forms prior to completing the

questionnaires. Participants also consented to the retrieval of routinely collected clinical data from their

medical records.

Data Analysis

Completed questionnaires were scanned into a research database, and SPSS version 22.0 (IBM Corp,

Armonk, NY) was used for all statistical analyses. Descriptive statistics (frequencies and means with

standard deviations) were used to summarize sample characteristics. Independent sample t-tests were

used for group comparisons of continuous variables and chi-square tests were used for group

comparisons of categorical variables. Fisher’s Exact Test was used for group comparisons of categorical

11

variables when one or more of the expected cell frequencies was <5. Length of stay was not normally

distributed, and thus, the non-parametric Mann Whitney U Test was used for group comparisons.

Logistic regression was used to determine the unique relationships between the independent variables

and pressure ulcer risk, while controlling for the effects of other relevant factors. Age and gender were

forced into the model for face validity. Other variables significantly associated with pressure ulcer risk in

univariate analyses were considered for inclusion in the multivariate model, but were only retained if

they remained significant predictors of pressure ulcer risk. A significance level of p<.05 was used for all

analyses.

RESULTS

Sample

The total hospital population admitted to the three medical wards on the 10 screening days was 718

patients. Of these, a total of 170 patients were not eligible (e.g., unable to read Norwegian, cognitively

impaired, or under 18 years of age), 34 were unavailable at the time of screening, 40 were excluded

because the patient had already been screened at a prior date, and 1 was excluded due to a missing

pressure ulcer risk score. Of the 473 individual patients eligible and approached for inclusion, 145 (31%)

declined to participate in the study; 80 of these patients were screened in year 2 of the study as part of

standard hospital procedures, and their pressure ulcer risk screening data are available for comparison.

The remaining 328 patients were included in the analysis (see Figure 1).

The mean Braden score was 20.5 (SD 2.5), ranging from 13 to 23, and 67 (20.4%) patients were

categorized as being at risk of pressure ulcers (Braden score<19). The prevalence of pressure ulcer stage

I-IV was 11.9% (n=37). Among the 37 patients who had a pressure ulcer at the time of screening, the

most common sites were the heel (n=14) and the sacrum (n=11), and these were also the locations of the

most severe ulcers. Analysis of the relationship between Braden risk scores and the development of a

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pressure ulcer indicates that patients with scores <19 are significantly more likely to develop a pressure

ulcer (see Table 1).

Table 1. Pressure ulcer risk scores and skin examination results

A comparison of patients who did and did not consent to participate in the research project

indicated that the 328 patients included in the study were significantly less likely to be at risk of pressure

ulcers according to their Braden score (20.4% vs. 33.8%, p=.012), but were just as likely to have

abnormal skin exams (11.9% vs. 13.5%, p=.696) as the 80 who did not consent (only patients

hospitalized in year 2 of the project were screened as part of standard hospital procedures and included in

this comparison). The included patients were also slightly younger (mean age of 62.7 vs. 67.8 years,

p=.056) than patients who did not consent, but the two groups did not differ with respect to gender (52%

vs. 47% male, p=.451).

Socio-demographic and clinical factors

As shown in Table 2, patients at risk of pressure ulcers had a significantly higher mean age than patients

who were not at risk. Patients ≥80 years of age were more than 3 times as likely to be at risk for pressure

ulcers compared to patients <65, and while not statistically significant, patients 65-79 years of age were

almost twice as likely as patients <65 to be at risk of pressure ulcer. In addition, patients with BMI<20

were more likely to be at risk of pressure ulcer than patients with BMI≥20, although the risk groups did

not differ with respect to mean BMI. There was no gender difference between the at-risk and non-risk

groups.

Table 2. Sample characteristics by pressure ulcer risk.

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The mean current comorbidity count for the full sample was 1.84 (SD 1.52), with no significant

difference between the at-risk and non-risk groups (1.94 (SD 1.41) vs. 1.82 (SD 1.54), p=.582). Of the 2

comorbidities evaluated, only fracture was associated with pressure ulcer risk (see Table 2).

Symptoms and laboratory results

The mean symptom count in the total group was 7.96 (SD 3.86) with no significant difference between

the at-risk and non-risk groups (8.09 (SD 3.11) vs. 7.92 (SD 4.03), p=.752). Although the two groups

reported a similar number of symptoms, patients at-risk for pressure ulcers were significantly more likely

to report drowsiness, urination problems and swelling of arms and legs and were significantly less likely

to report nervousness (see Table 3). Pain at rest and pain on activity were both significantly related to

pressure ulcer risk (see Table 3). In regard to symptom distress, patients at risk of pressure ulcers were

significantly more likely than patients not at risk to report high distress related to vomiting, urination

problems and shortness of breath.

Table 3. Significant associations between pressure ulcer risk and patient-reported symptoms (N=328)

With regard to laboratory blood results, pressure ulcer risk was associated with lower levels of

hemoglobin and albumin and higher levels of C-reactive protein. Patients at risk for pressure ulcers also

had slightly lower hematocrit levels compared with patients not at risk, but the difference did not reach

statistical significance.

Multivariate analysis

Not surprisingly, older age was the most significant predictor of pressure ulcer risk in adjusted analyses,

with patients ≥80 years of age being more than 4 times as likely to be at risk for pressure ulcer compared

to patients <65 year of age when controlling for other relevant factors. In addition, 5 symptoms were

14

associated with pressure ulcer risk. High distress due to vomiting was the strongest symptom predictor

(OR=4.45), followed by severe pain at rest (OR=3.52). Urination problems and high distress due to

shortness of breath more than doubled the likelihood of pressure ulcer risk (OR = 2.74 and 2.60,

respectively). Interestingly, patients who reported feeling nervous were 70% less likely to be at risk for

pressure ulcers than patients without nervousness. Patients with albumin levels below 35g/L were 4

times as likely as patients with higher albumin levels to be at risk for pressure ulcers.

Table 4. Multivariate model predicting pressure ulcer risk

DISCUSSION

In this study, 11.9% of patients had pressure ulcers and 20.4% were found to be at risk for pressure

ulceration. Multivariate analyses revealed that age, 5 symptoms and albumin were significantly

associated with patients’ risk of pressure ulcers. The systematic inclusion of symptoms associated with

pressure ulcer risk in this study is a novel approach, and may represent a new area for pressure ulcer

research.

Not surprisingly, patients ≥80 years of age were found to be at significantly higher risk of

developing pressure ulcers than younger patients, which is consistent with previous findings (Wann-

Hansson et al. 2008, Gunningberg et al. 2011). The pressure ulcer prevalence rate in this study (11.9%)

is consistent with previous studies in acute general hospital settings that have reported pressure ulcer

prevalence rates of 10%-18.5% (Cuddigan et al. 2001, Gunningberg 2004). The pressure ulcer risk rate

in our study of medical patients was 20.4% based on a Braden score <19. A study from 5 European

countries with patients from general and teaching hospitals reported that 22-42% were at risk using a

Braden score <17 (Vanderwee et al. 2007). The comparability of these prevalence rates is difficult due to

the different patient populations and varying methodologies.

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Of all the comorbidities, only fracture was significantly related to pressure ulcer risk in bivariate

analysis, although it was not associated after controlling for other variables in the multivariate analysis.

This is in agreement with Perneger et al. (1998) and Nonnemacher et al. (2009) who found no

association between pressure ulcers and medical diagnoses such as diabetes mellitus, cardiovascular

disease, sepsis, inflammatory disease, cyanotic hearth disease, hearth failure, hypotension, arterial

obstructive disease or cancer. In the final multivariate regression analyses, Nonnemacher (2009) only

found the presence of a malignant tumour and arterial obstructive disease to be significantly related to

pressure ulcers. In contrast, Bry et al. (2012) found high prevalence of organ failure and co-morbid

conditions in patients with pressure ulcers, but the lack of a control group limits the validity of these

findings. Similarly, Amir et al. (2011) reported that patients with an infectious disease, diabetes mellitus,

respiratory disease, cardiovascular disease and/or cerebrovascular accident were at increased risk of

pressure ulceration, but it is not clear if these analyses are multivariate and adjusted for age and other

factors. Thus, it is possible, that such associations between comorbidities and pressure ulcer development

are due to the presence of confounding factors (e.g., age, mobility, specific symptoms) not adequately

controlled for in the analyses rather than to a direct association between the comorbidity and pressure

ulcers. Furthermore, the disease severity of each diagnosis can vary widely, and thus the experience of

symptoms and symptom distress might be more relevant than the diagnosis itself.

Five of the 15 symptoms assessed in this study were significantly associated with patients at risk

for pressure ulcers (Braden score <19). Four of the symptoms (i.e., vomiting, severe pain at rest,

urination problems and shortness of breath) can all, for various reasons and at different levels, be related

to all six items in the Braden scale (i.e. sensory perception, moisture, activity, mobility, nutrition, and

friction and shear). The applicability of these symptoms is further supported by previous research on risk

factors associated with pressure ulcers.

Immobility is a well known risk factor for pressure ulcer development and confirmed by several

recent studies (Wann-Hansson et al. 2008, Nonnemacher et al. 2009). More specifically, being bed or

16

chair fast and needing help in daily activities have been identified as important factors for developing

pressure ulcers (Wann-Hansson et al. 2008), and such immobilization is to be expected among patients

experiencing high distress from symptoms such as vomiting, severe pain at rest and shortness of breath.

Further, the presence of pain itself has been identified as a predictor for pressure ulcer development

(Nonnemacher et al. 2009), which is consistent with our findings.

Vomiting can also lead to dehydration, both in terms of direct fluid loss and reduced fluid intake.

Previous studies have reported that insufficient hydration is associated with pressure ulcers, and that this

could lead to reduced tissue tolerance for pressure (Nonnemacher et al. 2009, Bry et al. 2012). Urinary

catheter use and/or incontinence are also risk factors associated with pressure ulcer development

(Gunningberg et al. 2011), which supports our findings that urination problems were significantly related

to pressure ulcer risk. In contrast, a recent study has challenged the assumption that incontinence is a risk

factor (Nonnemacher et al. 2009), reporting that incontinence is better understood as a marker for

underlying frailty. The somewhat unexpected finding that patients reporting nervousness were less likely

to be at risk for pressure ulcers could reflect a tendency for such patients to be more mobile and restless,

thus resulting in higher Braden scores compared to patients without nervousness.

In multivariate analyses, low albumin was also related to patients’ risk of pressure ulcers, which

is consistent with several recent studies (Hatanaka et al. 2008, Bry et al. 2012). In contrast, Gumeiro et

al. (2012) found no significant associations between age, albumin and pressure ulcer development. This

could be explained by the older age of the Gumeiros sample and by the generally low levels of albumin

in patients both with and without pressure ulcers. Given that pressure ulcers are more common among

older patients with severe illness, the association with serum albumin may reflect the patient’s condition

due to the impact of the disease (Lindgren et al. 2004). Low serum albumin is correlated with an

increased risk of morbidity and mortality in hospitalized patients and is regarded as an important

prognostic indicator (Walter et al. 2001).

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Strengths and Limitations

The results of this study need to be considered in light of several strengths and limitations. First, this

study included 69% of eligible medical patients admitted to an acute general hospital on 10 different

screening days over a 2-year period. This high inclusion rate suggests that the study findings likely

represent the majority of this population. However, another strength of the study is the inclusion of a

comparison between the study sample and non-participating patients, the results of which suggest that

our sample may be slightly biased toward healthier patients, which could explain the pressure ulcer

prevalence rate being in the lower range compared to previous studies. In addition, the study sample was

relatively small and limited to medical patients without cognitive impairment, and therefore the findings

are not generalizable to other patient groups, such as those admitted to a surgical ward, intensive care

unit (ICU), palliative care unit, or nursing home. In our study, patients from the elective surgical

department were excluded due to the low rate of actual pressure ulcers. Prior studies have already

documented a high prevalence of pressure ulcers among ICU patients, those with cognitive impairment,

and others requiring high levels of care (Eberlein-Gonska et al. 2013), and thus we targeted this study

toward patients in general medical wards. Medical patients constitute a large proportion of patients in

general hospitals, and thus increasing our understanding of pressure ulcer risk in this group is likely to be

of considerable benefit.

The symptoms evaluated in this study were general so that they might be applicable to a broad

range of medical patients. However, in some cases, it may have been helpful to have more specific

symptoms to better understand their association with pressure risk. For example, it is unclear whether

patients reporting urination problems were experiencing urinary retention, urgency, incontinence or pain,

which likely have different implications for pressure ulcer risk.

Another limitation is that, due to the low prevalence of pressure ulcers in the sample, the study

focused on factors related to pressure ulcer risk (i.e., Braden Score <19) rather than actual pressure

ulcers. Although we have established the strong connection between Braden scores and the development

18

of pressure ulcers and contend that it is more valuable to characterize patients at risk before they develop

pressure ulcers in order to prevent them, additional studies are needed to determine whether the risk

factors identified in this study are also associated with the development of pressure ulcers. Furthermore,

the majority patients identified as being at risk of pressure ulcer did not have an actual pressure ulcer,

which may have been due to the successful use of prevention strategies or insufficient time for the

pressure ulcer to develop. Nonetheless, it was a strength of this study that the skin assessments were

conducted according to EPUAP’s widely-used classification for pressure ulcers, thereby increasing the

comparability of results across settings and countries. The EPUAP recommends a Braden score cut-off

value of <17 (Clark et al. 2002), but the cut-off value used in other studies varies between 16-19 (Kring

2007, Wann-Hansson et al. 2008). In a large multisite study, a cut-off score <19 was recommended for

all settings to achieve the best balance between sensitivity and specificity (Bergstrom et al. 1998). If the

cut-off is too low, the sensitivity of the Braden score decreases (Wann-Hansson et al. 2008). Thus, we

used a cut-off score of <19 in order to maximize the scale’s sensitivity.

Finally, pressure ulcer risk has been associated with a wide range of factors, but causal

relationships are difficult to determine. In this correlational study, complementary data such as present

and previous diagnoses from the medical record, medications and vital signs were not accounted for in

the analyses and it is unclear how their inclusion might have influenced the study findings. In addition to

these patient factors, environmental, organizational and staff variables can also contribute to pressure

ulcer risk. Future studies should include such factors to better understand their role in determining

pressure ulcer risk.

CONCLUSION

This study investigated the novel hypothesis that pressure ulcer risk (as measured by the Braden scale) is

associated with self-reported symptoms among hospitalized medical patients. Controlling for both age

and gender, pressure ulcer risk was positively associated with patient reports of severe distress related to

19

vomiting or shortness of breath, severe pain at rest, urination problems and low laboratory values of

albumin, and was negatively associated with self-reported nervousness. Assessing patient symptoms is

one of the most valuable tasks for nurses, and the relationship between pressure ulcer risk and symptoms

is highly relevant in the clinical context.

Relevance to Clinical Practice

Given how quickly pressure ulcers can develop, it is crucial to identify patients at risk and initiate

preventive measures at an early stage after hospital admission or in response to changes in the patient’s

condition during their hospital stay. Systematic risk screening has been implemented in a variety of

hospital settings around the world, and some studies have shown a reduction in pressure ulcer prevalence

after introduction of a pressure ulcer risk-screening tool. However, Saleh et al. (2009) question the

usefulness of standardized risk screening targeted at all patients and discuss whether it is the risk

screening itself or the raised awareness during implementation of risk screening tools that give nurses

improved clinical judgment and thus the ability to identify patients at risk of pressure ulcers. Further,

Eberlein-Gonska et al. (2013) found that screening of all patients did not lead to any direct changes in

type or level of care of the patient and propose that it is more helpful to limit decubitus screening to the

groups of patients that are most at risk of pressure ulceration. A more targeted risk screening would also

result in nursing time being freed up for other aspects of patient care (Eberlein-Gonska et al. 2013).

The widely-used guidelines developed by NPUAP et al. (2014) recommend pressure ulcer risk

screening be carried out as soon as possible after hospital admission and within a maximum of eight

hours. Sharp and White (2015) discuss this recommendation and highlight the need for fast pressure

ulcer risk screening and the lack of evidence supporting the eight hour maximum as pressure ulcers can

develop within this time. Sharp and White (2015) further claim that pressure ulcer risk screening should

be done as fast as possible, preferably within one hour of hospitalization, and that the fastest way to do

this is by rapid clinical judgment.

20

Symptom assessment is a routine for nurses and is done on a regular basis. This study shows that

patient-reported symptoms, older age and low albumin may help identify which patients are at risk for

pressure ulcers. This can be valuable knowledge for nurses in their clinical judgment of patients, and can

serve as a supplement to existing pressure ulcer risk tools, such as the Braden Scale. In a world of

increasing need for cost-effectiveness and efficiency, it is necessary to thoroughly evaluate each new

task introduced in hospital settings. In contrast to systematically screening all patients admitted to acute

general hospitals for pressure ulcer risk, a quick assessment of symptoms, age and laboratory blood

results could assist nurses in identifying which patients are most likely to be at risk, so that further risk

screening and prevention efforts could be targeted to these patients. Future studies are needed to validate

the use of symptom assessment, laboratory blood results and age as useful indicators of pressure ulcer

risk.

21

Figure 1. Flow chart of study sample.

328 medical patients included in analysis

197 patients consented and completed the self-report

study questionnaires

131 patients consented and completed the self-report

study questionnaires

146 patients not included: • 61 were not eligible • 16 were unavailable • 4 were screened before • 65 did not consent to the study

(were not screened)

YEAR 1 277 inpatients on 4 screening days (consent required for risk screening

as well as comorbidity & symptoms)

YEAR 2 441 inpatients on 6 screening days

(risk screening part of standard care; consent for comorbidity & symptoms)

718 patients hospitalized on a medical ward on one of the 10 screening days

164 patients not included: • 109 were not eligible • 18 were unavailable • 36 were screened before • 1 missing pressure ulcer risk

80 patients were screened, but did not consent to the study; their risk screening data were available for comparison

22

Table 1. Pressure ulcer risk scores and skin examination results (n=312)

Total Sample

(n=312)

Pressure Ulcer Risk Group* Statistic Non-risk

(n=249) At-risk (n=63)

Skin examination Normal Stage I Stage II-IV

275 (88.1%) 17 (5.4%) 20 (6.4%)

236 (94.8%) 9 (3.6%) 4 (1.6%)

39 (61.9%) 8 (12.7%) 16 (25.4%)

Fisher’s Exact p<.001

Note. 16 patients had missing data for the skin examination and were excluded from this analysis. Significant statistics (p<.05) are presented in bold type. * The non-risk group had Braden scores of 19-23, while the at-risk group had scores of 13-18.

23

Table 2. Sample characteristics by pressure ulcer risk

Total Sample

(N=328)

Pressure Ulcer Risk Group* Statistics Non-risk

(n=261) At-risk (n=67)

Gender Male Female

(=328) 169 (52%) 159 (48%)

135 (80%) 126 (79%)

34 (20%) 33 (21%)

X2(1)=0.02, p=.886

Age, years Mean (SD) Range Category, n (%) <65 years 65-79 years ≥80 years

(n=328) 62.7 (18.0) 20 – 100

160 (49%) 96 (29%) 72 (22%)

60.7 (19.1) 20 – 100

139 (87%) 75 (78%) 47 (65%)

70.8 (18.0)

23 – 99

21 (13%) 21 (22%) 25 (35%)

t(326)=3.91, p<.001

X2(2)=14.4, p=.001

ref OR = 1.85, p=.070 OR = 3.52, p<.001

Length of stay Mean (SD) Median Range

6.2 (4.2)

5 1 – 30

5.9 (4.1)

6 1 – 30

7.1 (4.7)

5 1 – 23

t(321)=1.95, p=.052

MWU p=.019

Body mass index Mean (SD) Range Category, n (%) <20 ≥20

(n=323) 24.9 (6.1)

13.6 – 56.6

63 (20%) 260 (80%)

25.2 (5.9)

14.0 – 56.6

45 (71%) 215 (83%)

23.9 (6.6)

13.6 – 46.9

18 (29%) 45 (17%)

t(321)=1.45, p=.149

X2(1)=4.10, p=.043

Laboratory values Hemoglobin, g/dL Mean (SD) Category, n (%) Low (<12) Normal (≥12)

(n=285) 12.23 (2.04)

171 (60%) 114 (40%)

(n=226) 12.41 (1.99)

144 (84.2%) 82 (71.9%)

(n=59) 11.55 (2.09)

27 (15.8%) 32 (28.1%)

t(283)=2.93, p=.004 X2(1)=6.28, p=.012

Hematocrit (%) Mean (SD) Category, n (%) Low (<35%) Normal (≥35%)

(=241) 38.02 (5.76)

55 (23%) 186 (77%)

(n=195) 38.36 (5.73)

40 (73%) 155 (83%)

(n=46) 36.59 (5.71)

15 (27%) 31 (17%)

t(239)=1.89, p=.060 X2(1)=3.09, p=.079

Albumin, g/L Mean (SD) Category, n (%) Low (<35) Normal (≥35)

(n=261) 39.54 (5.69)

48 (18%) 213 (82%)

(n=211) 40.11 (5.41)

30 (63%) 181 (85%)

(n=50) 37.11 (6.20)

18 (37%) 32 (15%)

t(259)=3.44, p=.001 X2(1)=12.8, p<.001

C-reactive protein, mg/L Mean (SD) Category, n (%) Normal (<10) High (≥10)

(n=283) 53.45 (83.67)

111 (39%) 172 (61%)

(n=222) 46.54 (79.74)

100 (90%) 122 (71%)

(n=61) 78.57 (93.11)

11 (10%) 50 (29%)

t(281)=2.68, p=.008 X2(1)=14.6, p<.001

Comorbidities* Current fracture No Yes

(n=306) 279 (91%) 27 (9%)

230 (82%) 18 (67%)

49 (19%) 9 (33%)

X2(1)=3.99, p=.046

24

Note. Significant statistics (p<.05) are presented in bold type. * The following 11 comorbidities were unrelated to pressure ulcer risk: cardiovascular disease, pulmonary disease, cancer, gastro-intestinal disease, muscular-skeletal disease, neurological disease, psychiatric disease, significant vision loss, significant hearing loss, diabetes mellitus, and other comorbid condition. The 9 patients reporting cognitive impairment were excluded from the analysis, and cognitive impairment was not evaluated as a comorbidity.

25

Table 3. Significant associations between pressure ulcer risk and patient-reported symptoms (N=328)

Total Sample (N=328)

Pressure Ulcer Risk Group Statistics Non-risk

(n=261) At-risk (n=67)

PAIN Pain at rest Mean (SD) Category, n (%) Low-Moderate (0-7) Severe (7-10)

(n=326) 2.97 (2.86)

283 (87%) 43 (13%)

(n=259) 2.73 (2.65)

233 (82%) 26 (60%)

(n=67) 3.87 (3.44)

50 (18%) 17 (40%)

t(87*)=2.68, p=.014 X2(1)=10.9, p=.001

Pain in activity Mean (SD) Category, n (%) Low-Moderate (0-7) Severe (7-10)

(n=324) 3.39 (3.02)

264 (81%) 60 (19%)

(n=257) 3.08 (2.88)

218 (83%) 39 (65%)

(n=67) 4.57 (3.26)

46 (17%) 21 (35%)

t(322)=3.66, p<.001 X2(1)=9.21, p=.002

OCCURRENCE OF OTHER SYMPTOMS

Nervousness No Yes

(n=322) 150 (47%) 172 (53%)

110 (73%) 146 (85%)

40 (27%) 26 (15%)

X2(1)=6.56, p=.010

Drowsy No Yes

(n=322) 76 (24%) 246 (76%)

66 (87%) 189 (77%)

10 (13%) 57 (23%)

X2(1)=3.53, p=.060

Urination problems No Yes

(n=316) 188 (59%) 128 (41%)

158 (84%) 92 (72%)

30 (16%) 36 (28%)

X2(1)=6.82, p=.009

Swelling of arms/legs No Yes

(n=321) 183 (57%) 138 (43%)

154 (84%) 102 (74%)

29 (16%) 36 (26%)

X2(1)=5.11, p=.024

DISTRESS DUE TO OTHER SYMPTOMS

Urination problems No/low distress High distress

(n=316) 280 (89%) 36 (11%)

230 (82%) 20 (56%)

50 (18%) 16(44%)

X2(1)=13.6, p<.001

Vomiting No/low distress High distress

(n=322) 303 (94%) 19 (6%)

245 (81%) 10 (53%)

58 (19%) 9 (47%)

Fisher’s Exact p=.007

Shortness of breath No/low distress High distress

(n=321) 238 (74%) 83 (26%)

197 (83%) 59 (71%)

41 (17%) 24 (29%)

X2(1)=5.21, p=.023

Note: The following 9 symptoms were unrelated to pressure risk and are not reported in this table: concentration, lack of energy, nausea, numbness/tingling in hands/feet, sleep problems, diarrhea, itching, dizziness, and skin changes. Significant statistics (p<.05) are presented in bold type. * Separate variance t-test with adjusted degrees of freedom due to unequal variances.

26

Table 4. Multivariate model predicting pressure ulcer risk Predictors Odds Ratio 95% CI p Female gender (ref: male) 1.49 0.69, 3.22 .315 Age in years (ref: <65)

65-74 ≥80

1.18 4.67

0.44, 3.14

1.86, 11.72

.001

.739

.001 Lab values

Low albumin (<35g/L) 4.06 1.79, 9.18 .001 Symptoms

Severe pain at rest (≥7) 3.52 1.29, 8.92 .008 Urination problems (ref: no) 2.74 1.24, 6.04 .013 Nervousness (ref: no) 0.30 0.13, 0.67 .003 Vomiting (ref: low distress) 4.45 1.21, 16.35 .025 Shortness of breath (ref: low distress) 2.60 1.16, 5.81 .020

Note. Overall model is significant: X2(9)=62.5, p<.001. Dependent variable = pressure ulcer risk group. The following variables were evaluated for inclusion in the model but were excluded due to non-significance: length of hospital stay, BMI, hemoglobin<12, hematocrit<35%, CRP<10, count of comorbidities, comorbid fracture, severe pain in activity, occurrence of drowsiness and swelling, and distress due to urination problems.

27

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