Epidemiology and Outcome of Pressure Injuries in Critically Ill Patients With Chronic Obstructive Pulmonary Disease A propensity score adjusted analysis

: Background: Pressure injuries are a frequent complication in intensive care unit (ICU) patients, especially in those with comorbid conditions such as chronic obstructive pulmonary disease (COPD). Yet no epidemiological data on pressure injuries in critically ill COPD patients are available. Objective: To assess the prevalence of ICU-acquired pressure injuries in critically ill COPD patients and to investigate associations between COPD status, presence of ICU-acquired pressure injury, and in-hospital mortality. Study design and methods: This is a secondary analysis of prospectively collected data from DecubICUs , a multinational one-day point-prevalence study of pressure injuries in adult ICU patients. We generated a propensity score summarizing risk for COPD and ICU-acquired pressure injury. Propensity score-adjusted logistic regression was used to assess the relationship between COPD and ICU-acquired pressure injury. Thereafter the propensity score was used as matching criterion (1:1-ratio) to assess the proportion of ICU-acquired pressure injury attributable to COPD. The propensity score was then used in regression modelling assessing the association of COPD with risk of ICU-acquired pressure injury, and examining variables associated with mortality (Cox proportional-hazard regression). Results: Of the 13,254 patients


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Reviewer #1: The authors have addressed my queries from my earlier review.Just 1 comment: Figure 2: Survival Analysis: This figure is very difficult to read as the colors on the curves are so similar and the differences between the 4 groups in terms of the type of lines is hard to distinguish.Can this be altered to make the 4 lines different colors?
A: As requested the curves or now in four different colors.The legend of the figure is adapted accordingly.
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A: Thank you for these kind words.

Contribution of the paper
What is already known  Chronic obstructive pulmonary disease (COPD) is a condition that frequently leads to intensive care unit (ICU) admission and is characterized by multimorbidity including hormonal, metabolic and musculoskeletal derangements.
 ICU patients are at high risk of pressure injuries because of their severity of acute illness and often debilitated physical condition.
 No epidemiological data on pressure injuries in ICU patients with COPD are reported.

What this paper adds
 COPD constitutes an important risk factor for ICU-acquired pressure injuries.
 ICU patients with COPD who developed ICU-acquired pressure injuries are at an increased risk of death.

Introduction
Pressure injuries are localised lesions to the skin and/or underlying tissues caused by mechanical stress (pressure or pressure combined with shear) 1 .They usually occur at bony prominences such as the heels or sacral region but can develop anywhere on the body.
Intensive care unit (ICU) patients have a higher prevalence of pressure injury compared to other hospitalised patients. 2A systematic review and meta-analysis reported the upper and lower 95% confidence intervals (CI) of the cumulative incidence were 9.4% to 27.5% 3 in studies using skin inspection (gold standard) to identify pressure injury in the ICU.Pressure injuries occur in ICU patients due to multiple comorbidities, acute clinical conditions, and ICU treatments 4,5,6 .Pressure injury more frequently affects those with acute organ derangements such as cardiovascular instability requiring vasopressor agents and acute respiratory failure requiring invasive mechanical ventilation and sedation, analgesia, and/or neuromuscular blockade agents 7 .Critical illness also threatens skin integrity by systemic inflammation and associated catabolic processes triggering muscle wasting and weight loss.Presence of underlying chronic disease associated with immobility, tissue ischemia, and malnutrition also increases the risk of pressure injury 8 .In the context of critical illness, the occurrence rate of pressure injury is strongly associated with case-mix and particular risk profiles thereby compromising the predictive value of risk scores 9,10,11 .
Chronic obstructive pulmonary disease (COPD) is amongst the most common comorbid conditions of patients admitted to the ICU 12 with the proportion ranging from 10% to 25% depending on local case-mix 13,14 .COPD is a chronic inflammatory lung disease which is considered a systemic disease 15 .Multi-morbidity including hormonal, metabolic and musculoskeletal derangements are common [16][17][18] .In the context of critical illness, COPD represents an independent risk factor for unfavourable outcomes including increased length of ICU stay, prolonged ventilator weaning, muscle wasting and interrupted skin integrity 19 , ICU readmission, and death 14,20,21 .As such, the typical COPD patient profile is characterized by a progressively debilitated physical condition reflecting a risk for pressure injury.
For that reason, we hypothesized that critically ill patients with COPD have an increased risk for developing pressure injury and that this may be associated with an increased risk of death.
Our objectives were (i) to assess the prevalence of pressure injury in critically ill patients with COPD as a comorbidity or as a primary ICU admission diagnosis around the world, (ii) to investigate to what extent COPD constitutes an independent risk factor for pressure injury acquisition during ICU stay, (iii) to assess the proportion of pressure injury prevalence attributable to COPD, and (iv) to model relationships between COPD, ICU-acquired pressure injury, and hospital mortality.

Methods
Study design.We performed a secondary analysis of the DecubICUs study (NCT03270345), a multinational, prospective, observational one-day, point-prevalence study of pressure injury in adult ICU patients conducted in 1,117 ICUs and 90 countries 4 .Data were collected anonymously on all patients aged ≥18 years present in a participating ICU from 0:00 to 23:59 on the study day (15 May 2018); there were no exclusion criteria.Patients were followed until hospital discharge (maximum of 12 weeks) to assess survival status.A detailed description of the study protocol and data handling are reported elsewhere 4 .Ethics approval was granted by ethics committees or institutional review boards at the hospital, regional or national level 4 .

Variables and definitions
Demographic and clinical data included ICU admission type, principal ICU admission diagnosis, mechanical ventilation on admission, and presence of pressure injury at time of ICU admission.Comorbidities, including COPD defined as Global Initiative for Chronic Lung Disease (GOLD) 22 Stage ≥1, were documented from the medical record.Severity of acute illness on the point-prevalence day was assessed using physiological data including the Simplified Acute Physiology Score (SAPS) II 23 .Pressure injury risk was evaluated using the Braden scale 24 .
Pressure injury overall and by body site was determined by direct observation using the international staging definitions, i.e.Stage I to IV, Unstageable, and Suspected Deep Tissue Injury 1 .Data collectors recorded all pressure injuries.ICU-acquired pressure injuries were defined as those not present on ICU admission but present on the point prevalence day.

Statistical analysis.
We used chi-square or Mann Whitney U tests for univariate comparisons of demographic and clinical characteristics and patient outcomes.Pressure injury prevalence was calculated as the proportion (95% CI) of the study cohort who had at least one pressure injury on the point prevalence day.ICU-acquired prevalence was calculated as the proportion who had at least one pressure injury identified as ICU acquired.
Adequate correction for confounding was pursued through propensity score adjustment.A propensity score is a versatile method to control for confounding and is particularly useful when the number of potential confounders is high [25][26][27]  These covariates were selected based on their relationship with pressure injury risk based of the DecubICUs database 4 , or alternatively, based on a plausible relationship with pressure injury risk (e.g.diabetes).No feature selection was applied given the relatively conservative number of predictors and the adequate dataset size that minimised the risk of overfitting.
Patients with missing values were not included in the regression model.
Propensity score-adjustment was used in three ways.First, the propensity score was used to adjust for confounding in a logistic regression model that assessed the impact of COPD on the risk of ICU-acquired pressure injury on the total cohort.The relationship with ICU-acquired pressure injury (dependent variable) with the propensity score and COPD was reported with odds ratio (OR), 95% confidence interval (CI) and regression coefficient (B).
Second, the propensity score was used as the matching criterion in a matched cohort analysis to assess the proportion of ICU-acquired pressure injury attributable to COPD as underlying disease.In this matched cohort analysis (1:1 matching ratio) cases were designated as COPD patients and matched controls as non-COPD patients.For matching on the propensity score, a 1% deviation (± 0.01) was allowed creating matched pairs with a nearly identical risk of acquiring pressure injury during the ICU stay.In fact, concerning pressure injury risk, the only clinical difference between cases and matched controls is the presence, respectively absence, of COPD.This permitted calculation of the proportion of ICU-acquired pressure injury attributable to COPD by subtracting the crude pressure injury rate of controls from that of cases [28][29][30] .
Third, propensity score adjustment was applied in a Cox proportional-hazard regression model to assess the relationship between COPD, ICU-acquired pressure injury, and hospital mortality at 12 weeks from study day.In this model, we examined mortality in four patient groups defined according to their COPD/pressure injury status: (i) non-COPD patients without ICUacquired pressure injury (i.e.reference category); (ii) non-COPD patients with ICU-acquired pressure injury; (iii) COPD patients without ICU-acquired pressure injury; and (iv) COPD patients with ICU-acquired pressure injury.This model was executed on the total cohort (n=13,254).Results of the model were reported as hazard ratios (HR) and 95% CI.In addition, based on these Cox regression outcomes, survival curves were created according to the Kaplan Meier method.
Observational studies are susceptible for potential unmeasured or uncontrolled confounding.
For that reason, we calculated the E-value for our logistic and Cox proportional-hazard regression models using the VanderWeele & Ding approach 31 .The E-value is defined as the minimum strength of association, on the relative risk, odds ratio or hazard ratio scale, that an unmeasured confounder would need for both the independent covariate (e.g.COPD) and outcome variable (e.g.pressure injury) to fully explain away the association between risk factor and outcome.We calculated the E-value for both the observed association estimate (after adjustments for confounding) and the lower limit of the 95% CI.

Study cohort and pressure injury prevalence
The DecubICUs cohort included 13,254 patients recruited from 1,117 ICUs and 90 countries.
Of these 13,254 patients, COPD was an underlying condition in 1,663 (12.5%); 333 (20.0%) were admitted for acute COPD exacerbation.Compared to ICU patients without COPD, COPD patients were older, more commonly admitted for medical reasons, had higher severity of acute illness, and had more underlying conditions (Table 1).COPD patients had a longer ICU and hospital length of stay and increased in-hospital mortality (Table 2).
In COPD patients, the overall prevalence of pressure injury was higher than non-COPD patients ).Pressure injury prevalence of COPD patients was higher across all pressure injury severity stages (Table 2).

ICU-acquired pressure injury and body location.
In the COPD-cohort (n=1,663), 710 ICU-acquired pressure injuries were identified in 368 COPD patients with 162 (44%) patients with more than one ICU-acquired pressure injury.Figure 1 shows frequencies and proportions of ICU-acquired pressure injuries at the affected body sites in COPD and non-COPD patients.In both COPD and non-COPD patients, the most common regions for pressure injury were the sacral region and the heels.

Relationship between COPD and ICU-acquired pressure injuries
The propensity score ranged from 0.011 to 0.

Hospital mortality
Unadjusted mortality rates for COPD and non-COPD patients are shown in Table 2. Table 3 shows the propensity score-adjusted Cox regression modelling reporting on the mortality risk relative of non-COPD patients without pressure injuries.Compared with this reference group, mortality was higher among COPD patients with pressure injury.E-value calculation indicated that the observed HR of 1.35 could be explained away by an unmeasured confounder associated with both COPD plus ICU-acquired pressure injury and mortality by an HR of 2.1 (lower limit 95% CI 1.37), but weaker confounding could not do so.Compared with the reference group, mortality was not increased in non-COPD patients with pressure injury nor in COPD patients without pressure injury.Kaplan Meier survival curves are shown in Figure 2.

Discussion
We performed this secondary analysis of data from the DecubICUs study, the largest epidemiological study of pressure injury in the ICU to date, to explore relationships between COPD, pressure injury, and mortality.We found the prevalence of overall pressure injury was higher in COPD patients, as was ICU-acquired pressure injury.Prevalence was higher across all pressure injury severity stages.COPD was an independent risk factor of developing ICUacquired pressure injury with an attributable risk of 6.4%.Additionally, pressure injury in COPD patients was associated with increased risk of in-hospital mortality.
Despite pressure injury being associated with multiple other risk factors, we convincingly showed that a significant proportion of the pressure injury prevalence could be attributed to COPD.Our data indicate that COPD is more than a "lung disease" and that this chronic condition affects the body beyond respiratory function including an inherent high risk for pressure injury development in the ICU setting.Other studies identify COPD as a risk factor for pressure injury in ICU patients.Hu et al. reported COPD to be associated with an increased risk of pressure injury at the sacral region (OR 3.2, 95% CI 1.3 to 8.0) with an association stronger than the Braden score and multiorgan dysfunction syndrome 32 .Argenti et al. also reported COPD to be associated with pressure injury risk in univariate analysis (OR 2.6, 95% CI 1.8 to 3.9) but these data were not further explored in multivariable analysis 33 .
Reasons for the higher prevalence of pressure injury in COPD patients overall and ICUacquired are likely multifactorial.Well-described risk factors for pressure injury are poor mobility, impaired skin perfusion, malnutrition, and an overall higher burden of underlying conditions, all of which are well-recognized features of COPD 1 .In the COPDGene project 34 commonly occurring comorbidities included chronic heart failure, osteoporosis, stroke, peripheral vascular disease, gastroesophageal reflux disease, coronary heart disease, hypertension, and stomach ulcers.In our study, more COPD than non-COPD patients had chronic heart failure, impaired mobility, peripheral vascular disease, chronic renal failure, diabetes mellitus, and malnutrition.COPD patients received more long-term corticosteroid therapy which causes skin thinning and atrophy contributing to pressure injury risk 35 .
COPD patients in our cohort had higher severity of acute illness as evidenced by higher SAPS II scores on the day of the point-prevalence study and more organ support (mechanical ventilation and vasopressor use) than non-COPD patients.This reflects an overall high burden of illness severity predisposing pressure injury development.Critical illness is associated with a hypercatabolic state and resultant nutritional deficiency.Wenzel et al. 36 recently reported that the time to pressure injury development for patients who did not achieve nutritional goals was shorter compared to those achieving nutritional goals.These findings highlight the importance of nutritional state and pressure injury 37 The combination of chronic conditions associated with COPD and severity of acute illness contribute to a patient phenotype explaining the higher pressure injury prevalence at the time of ICU admission as well as ICUacquired pressure injury among COPD patients.
One hypothesis generating finding is that critically ill COPD patients with pressure injury had a higher mortality risk.Previously, we reported independent and gradually increasing risk of mortality with increasing severity of pressure injury. 4As such, the acquisition of pressure injury during ICU stay may reflect a debilitated condition leading to an unfavourable outcome.
The relationship between pressure injury and mortality was also demonstrated in a recently published study from Finland including over 6,000 critically ill patients 38 .In the 1980s Kennedy reported pressure injury to be predictive of impending death in intermediate care facilities with 56% of those developing a pressure injury dying within six weeks 39,40 .To the best of our knowledge, such a time-dependent relationship has not been described in the context of critical illness.Due to its point-prevalence approach also our study could not assess such an association.However, COPD is an independent risk factor for ICU mortality in critically ill patients with VAP 41 and for in-hospital mortality after ICU discharge 42 .
Our study has important strengths such as the large sample size which provides a current and worldwide epidemiology of pressure injury in critically ill COPD patients.We used robust analysis methods to assess known risk factors independently associated with pressure injury including propensity score adjustment and matching.
Study limitations are those inherent to point-prevalence studies such as the absence of exposure time for some variables such as mechanical ventilation and vasopressor use.
However, while incidence data are better suited to evaluate effectiveness of prevention measures, prevalence data support insights in resource requirements and their allocation 43 .
Data collectors recorded COPD, defined as GOLD stage ≥1, from the medical record.As such we were unable to perform sensitivity analyses according to COPD severity.The database also did not allow discriminating acute COPD exacerbations from acute exacerbation of other chronic pulmonary diseases.Because of our cross-sectional design, pressure injury prevention strategies such as patient positioning were not included in our analyses.Data were collected on a single day, therefore we could not account for any preventative strategies used prior to this.Finally, the propensity score may be suboptimal as we were unable to include known risk factors for COPD and pressure injury, such as smoking status.Smoking has previously been shown to be a risk factor for pressure injury in ICU patients, probably due to morphological changes resulting in decreased microvascular function and consequent worsening of the skin's natural defence 44 .Consequently, our study may be subject to unmeasured confounding.
However, E-values indicate that potentially unmeasured confounders would need to provide robust associations to reduce the observed relationships to non-significant proportions.
Future studies aiming to assess specific risk factors for pressure injury should use a study design that enables collection of cumulative incidence data with sufficient attention to disease-specific aspects, details on preventive measures, and other contextual influences of care delivery 9,11 .

Conclusion
In conclusion, our study demonstrates critically ill COPD patients are at higher risk than non-COPD patients for pressure injury, and when they occur, pressure injury in COPD patients is an independent risk factor for mortality.As such, pressure injury may serve as a surrogate for poor prognostic status in COPD patients and may help clinicians identify patients at high risk of death.Also, delivery of interventions to prevent pressure injury are paramount in critically ill COPD patients.Further studies should determine if early intervention in critically ill COPD patients can modify development of pressure injury and improve prognosis.

Figure 1 -
Figure 1 -Number (%) of ICU-acquired pressure injuries by body site in patients with and patients without chronic obstructive pulmonary disease (COPD)

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Other Epidemiology and Outcome of Pressure Injuries in Critically Ill PatientsWith Chronic Obstructive Pulmonary Disease A propensity score adjusted analysis ).Where your paper is based on analysis of a publically available data set or is part of a series of publications from a large cohort study (or similar) you can be selective in the references you provide and give a more general account of how this paper relates to others but it is essential that editors are able to verify the unique contribution of the paper you are submitting.If unsure about declarations we encourage you to err on the side of openness and suggest you consult Norman, I., Griffiths, P., 2008.Duplicate publication and 'salami slicing': Ethical issues and practical solutions.International Journal of Nursing Studies 45 (9), 1257-1260.information Funding 22 Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on which the present article is based 10 *Give information separately for exposed and unexposed groups.Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and published examples of transparent reporting.The STROBE checklist is best used in conjunction with this article (freely available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/,Annals of Internal Medicine at http://www.annals.org/,and Epidemiology at http://www.epidem.com/).Information on the STROBE Initiative is available at www.strobe-statement.org.Ms. Ref.No.:NS-D-21-02107R1 Title: COMMENT FROM ASSOCIATE EDITOR . The basic principle is to reduce this large number of confounding covariates to a single variable that summarizes all the relevant information about the confounders, i.e. the propensity score.We used logistic regression to generate a propensity score summarizing potential risk for COPD and risk for ICU-acquired pressure injury.The following covariates were considered for building the propensity score: country, World Bank economy status, ICU admission type, age, sex, body mass index, underlying comorbidities other than COPD (heart failure, peripheral vascular disease, renal failure, cirrhosis, malnutrition, diabetes, malignancy, and steroid therapy), Braden score, length of ICU stay before point prevalence day, and need for major organ support (i.e. mechanical ventilation at ICU admission, renal replacement therapy, and vasopressor use).
773 (very low to high-risk respectively) for pressure injury acquisition in the ICU.Due to missing values, we were unable to generate a propensity score for 221 patients, including 22 with COPD.As a summary statistic representing all potential risk factors except COPD, the propensity score itself was strongly associated with ICU-acquired pressure injury risk (OR 635, 95% CI 406 to 995; B 6.46).Notwithstanding, after propensity score-adjustment, COPD remained positively associated with risk of an ICUacquired pressure injury (OR 1.40, 95% CI 1.23 to 1.61; B 0.34).E-value calculation indicated that the observed OR of 1.40 could be explained away by an unmeasured confounder associated with both COPD and ICU-acquired pressure injury by an OR of 1.65 (lower limit 95% CI 1.46), but weaker confounding could not do so.Of the 1,663 COPD patients, we were able to match 1640 cases (23 patients not matched within a 1% deviation in propensity score).Prevalence of ICU-acquired pressure injury in cases and matched controls was 22.1% and 15.7%, respectively.As such, the proportion of ICUacquired pressure injury attributable to COPD was 6.4% (95% CI 5.2% to 7.6%).

Table 1 -Characteristics of ICU patients with or without chronic obstructive pulmonary disease (COPD).
: intensive care unit.SAPS: Simplified Acute Physiology Score.AIDS: acquired immunodeficiency syndrome Data are reported as n (%) or median (interquartile range, 1 st -3 rd quartile) *Economy: categorised according to the 2016 World Bank classification (https://data.worldbank.org/indicator/SH.XPD.CHEX.GD.ZS) ** The database did not allow discriminating between acute exacerbations of COPD and other chronic pulmonary diseases.In non-COPD patients this may include patients with acute exacerbation for asthma, cystic fibrosis, … but not COPD.In COPD patients this may include acute exacerbation of COPD or other chronic pulmonary conditions. ICU

Table 2 -Outcomes of ICU patients with or without chronic obstructive pulmonary disease (COPD).
ICU: intensive care unit *includes Stage III, Stage IV, unstageable pressure injury, and suspected deep tissue injury