Comparing Demographics, Treatments, and Outcomes of Patients With COVID-19 Lesions Versus Hospital-Acquired Pressure Ulcers/Injuries During the First Year of COVID-19

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With the emergence of SARS-CoV-2 as the virus responsible for the coronavirus disease 2019 (COVID-19) pandemic, numerous reports have surfaced to describe skin lesions that are associated with either the virus or the treatment.^1-4 Medical personnel should be aware of these COVID-19 skin lesions, know how to distinguish COVID-19 lesions from hospital-acquired pressure ulcer/injuries (HAPU/I), and understand contributing factors and patient outcomes.

COVID-19

COVID-19–associated cutaneous manifestations are grouped into 6 main patterns or types: (1) urticarial, (2) maculopapular morbilliform rash, (3) papulovesicular, (4) chilblain-like, (5) livedo reticularus, and (6) purpuric vasculitic pattern lesions.⁵ Features of COVID-related skin lesions include microvascular injury and thrombosis⁶ in both the dermal and epidermal layers,⁷ which complicates the distinction of COVID-19 lesions from HAPU/I or deep tissue injuries in patients who are acutely ill in critical care settings.⁸ This study focuses on the purpuric vasculitic lesions and pressure ulcers/injuries (PU/I) captured and photographed in the electronic health record (EHR) for symptomatic COVID-19 admissions during the first year of the pandemic.

HAPU/I

A pressure injury is defined by the National Pressure Injury Advisory Panel as "localized damage to the skin and/or underlying tissue as a result of pressure or pressure in combination with shear."⁹ HAPU/I may appear at vulnerable anatomical locations, such as bony prominences or under medical devices.⁹ Patients in intensive care units (ICUs) are at increased risk of developing HAPU/Is due to additional factors such as immobility, hemodynamic instability, and hypoxia.⁹ As a result, critically ill adults in ICUs develop PU/Is that are often unavoidable despite the best of nursing assessments and interventions.^10,11

Purpose

The COVID-19 pandemic has stressed the capacity of already-challenged health systems. Teams have fought to continue to provide safe, high-quality care within their organizations. Systems have also endeavored to protect patients across the health care continuum and during transitions of care, which is a vulnerable time for patients.¹² The authors' team has been collecting demographic and physiological data, as well as outcomes on individuals with full-thickness HAPU/Is (stage 3, 4, and unstageable), for more than 10 years. The information has been used to evaluate progress in eliminating avoidable HAPU/Is. The authors have also tracked unavoidable HAPU/Is, which occur despite all nursing interventions performed for prevention.

Quality and safety standards require reporting of all full-thickness HAPU/Is. An organization's HAPU/I incidence rate has traditionally reflected poorly on the facility's nursing care. As a result, it is essential to distinguish wounds that may mimic pressure injuries from other wound diagnoses.⁸ Timely and accurate identification will guide patient treatment, accurate reporting, coding, and reimbursement. Accurate documentation will follow the patient throughout the hospital system and beyond when the patient is eventually discharged and/or placed in another care facility and follows up with a new health care professional.¹³

The purpose of this work is to answer the following questions: What are the contributing factors for the development of COVID-19 lesions compared with PU/I in patients with symptomatic COVID-19–related hospital admissions? What are the outcomes for patients with COVID-19 lesions compared with those who have HAPU/Is?

A retrospective chart review was conducted, and data were analyzed from March 1, 2020, through March 1, 2021. The aim was to understand the difference in patient demographics, patient skin tones, treatments, hospital length of stay (LOS), ICU LOS, death, and discharge disposition for those with COVID-19 lesions compared with those who developed HAPU/I.

Rationale for Methodology

Excluded patients consisted of those who were diagnosed with COVID-19 infection due to positive test results but were asymptomatic, since many of these patients were hospitalized for another reason and COVID-19 infection was an incidental finding. Inclusion of asymptomatic individuals would have diluted the sample incidence of skin disorders in symptomatic patients. COVID-19–positive patients were identified by a nurse with expertise in coding. When necessary, coding queries were submitted to physicians to clarify the acute sequelae of symptomatic patients with COVID-19 infection.

Ethical Compliance

The institutional review board approved this study as a retrospective chart review. The authors collaborated on collecting data for ongoing studies on HAPU/I after adding COVID-19–related data collection within the modification of a previous data collection study. This was considered a consent-exempt study.

Inclusion Criteria

The authors retrospectively collected EHR data that were entered between March 1, 2020, and March 1, 2021. The records of adults (aged ≥18 years) who were admitted to the hospital with a positive COVID-19 lab result and were symptomatic on admission were reviewed. Each medical record was reviewed by 2 wound subject matter experts and an experienced coder. Outcomes and variables of those patients with COVID-19–related lesions were compared to those of patients who developed non-COVID-19–related HAPU/Is. Data were obtained through coding on the patients who were discharged with the diagnosis codes for COVID-19 or positive COVID-19 lab tests. The following COVID-19 ICD-10-CM diagnosis codes were used to identify the relevant patients: U07.1, J12.82, M35.89, and M35.81. After identifying the cohort, standardized data were collected on patient demographics, patient skin tone, body mass index (BMI), treatments, total hospital LOS, ICU LOS, and discharge disposition.

The EHR database was further queried to identify patients in the study cohort who had received any of the following treatment modalities during their hospital stay: dialysis, extracorporeal membrane oxygenation (ECMO), vasoactive medications (vasopressors), steroids, and anticoagulants. Each wound photo was categorized by patient skin tone using the Fitzpatrick skin tone chart. Two wound and skin subject matter experts evaluated the photos and classified each patient into 1 of 3 categories: 1 for light skin (Fitzpatrick 1-2), 2 for medium skin tones (Fitzpatrick 3-4), and 3 for darkest skin tones (Fitzpatrick 5-6).¹⁴ The skin tones were evaluated by tone at the area of the wound (most often the trunk location).

Wound Identification Staging of PU/I

For lesions deemed as HAPU/Is, the HAPU/I was then staged and photographed by a certified wound nurse. Inter-rater reliability was attained with separate staging obtained by photo review by 2 subject matter experts.

Explanation of Coding of COVID-19

The coding of COVID-19 was based on the COVID DX column and was obtained from the coding department. The designation of COVID-19 "symptomatic" was collected (either having COVID-19 sepsis at the time of admission or developing it later) and those admitted with sepsis due to COVID-19 were included in this study. This distinction was to exclude the asymptomatic patients who tested positively incidentally. The coding of COVID-19 U07.1 can be the result of a positive test only. There is also no timeframe in terms of coding "history of" or "current." Coding is not time-dependent; therefore, in cases without sepsis, the investigators queried the physicians for clarification if the patient had persistent active COVID-19 infection, sequelae of COVID-19, or history of COVID-19 in the following scenarios:

• Multiple polymerase chain reaction assays in a short time span with different results (might indicate viral fragments or replication-incompetent virus)
• History of COVID-19 but past the normal infection time during this hospitalization
• Conditions such as multi-inflammatory syndrome where it is unclear whether the COVID-19 was active or sequelae
• COVID-19 was documented but the patient was not put in isolation and there was no documentation of the patient not requiring quarantine.
• There was documentation of checking with the lab for cycle threshold; decreased cycle threshold indicates an increase in viral load, possibly indicating a resurgence in an immunocompromised patient.

Circumstances of COVID-19 coding based on the COVID DX column were screened by the registered nurse coding specialist and the nurse practitioner for quality and safety.

Exclusion Criteria

Since COVID-19 can be coded for both symptomatic and asymptomatic individuals,^15-17 asymptomatic patients were excluded from the cohort, as were children under 18 years of age.

Sources of Data and Data Collection Procedures

Data were collected through the EHR for all symptomatic patients with a positive COVID-19 test who met the inclusion criteria and were admitted to the hospital. The authors aimed to describe and compare the demographics, treatment modalities, and disposition at discharge.

COVID-19 in the COVID DX column included patients admitted with a principal diagnosis of COVID-19. Other specified instances of sepsis in the COVID DX column were patients admitted with a principal diagnosis of sepsis due to COVID-19.

Other diagnoses listed in the COVID DX column underwent additional review. If COVID-19 or sequelae of COVID-19 was related to the admission but did not meet the definition of principal diagnosis, a Y was placed in the COVID-19–related admission column. Examples would be patients being treated for other infections or diseases of other body systems and who also had COVID-19, but for whom COVID-19 was not the reason for admission. If the patient had tested positive for COVID-19 but was asymptomatic, an N was placed in the COVID-related admit column.

The principal diagnosis is defined in the Uniform Hospital Discharge Data Set as "that condition established after study to be chiefly responsible for occasioning the admission of the patient to the hospital for care."^16,17

Data Analysis Procedures

Descriptive statistics are reported as number and percent for categorical variables and as median and interquartile range or mean and standard deviation for continuous variables. Associations between categorical variables and wound type were tested using chi-square or Fisher’s exact test, as appropriate. Differences between wound type for numeric variables were tested using the Kruskal-Wallis test. Data were analyzed using Stata 17 MP.

Patients who developed COVID-19 lesions were typically male, younger, and had a higher BMI than patients with no wounds and patients with HAPU/I (Table 1). The original sample had 1357 patients, with 958 patients meeting inclusion criteria. Over 90% of the study population experienced no lesions during their hospital stay. COVID-19 lesions were found in 2.3% of the population, and 7.2% of the population developed HAPU/Is. Male patients (n = 565) comprised 58.9% of the entire cohort. More men than women developed COVID-19 (60.1%), COVID-19 lesions (63.6%), and HAPU/Is (69.6%) within this study. The median age of patients with COVID-19 lesions was 60.5 years, compared with 62.5 years in patients with no skin lesions and 71.3 years in patients with HAPU/Is. The mean BMI of those with COVID-19 lesions was 30.0 kg/m², compared with 28.6 kg/m² in those with no lesions and 26.3 kg/m² in those with HAPU/Is. Fitzpatrick scale skin tone classifications were only available for those patients with COVID-19 lesions or HAPU/Is, not for those without lesions or HAPU/Is. All patients with wounds were photographed. In the COVID-19 lesion group, 36.7% had light skin tone (Fitzpatrick 1 and 2), 45% had medium skin tone (Fitzpatrick 3 and 4), and 18.3% had dark skin tone (Fitzpatrick 4 and 5). In the HAPU/I group, 43.5% had light skin tone, 40.5% had medium skin tone, and 16% had dark skin tone.

Patients who developed COVID-19 lesions were more likely to receive dialysis, ECMO, and anticoagulants compared with patients who had no wounds and patients with HAPU/Is (Table 2). When comparing treatment modalities, 65 of 867 patients (7.5%) with COVID-19 who did not develop wounds had received some form of dialysis. For patients who developed COVID-19 lesions, 9 out of 22 (41%) received dialysis; for patients who developed PU/Is, 14 out of 69 (20.3%) received dialysis (P < .0001). Eight patients were treated with ECMO: 3 out of 8 patients with no wounds (0.4%), 2 patients out of 8 with COVID-19 lesions (9.1%), and 3 patients out of 8 with HAPU/Is (4.4%) (P < .0003).

Approximately 52% percent of patients who tested positive for COVID-19 and had no wounds were treated with vasopressor infusions. For patients with COVID-19 lesions, 81.8% received vasopressors; for patients who developed PU/Is, 82.6% received vasopressors to support their end-organ perfusion (P < .0001). Steroids were used in 50.2% of patients without wounds, 68.2% of patients with COVID-19 lesions, and 69.6% of patients with HAPU/Is (P < .0025). Approximately 31% of patients who tested positive for COVID-19 and had no wounds received anticoagulants, whereas 82% of patients with COVID-19 lesions and 77% of patients with HAPU/Is were treated with anticoagulants (P < .0001).

Patients who developed COVID-19 lesions were more likely to die during admission (n = 11; 50%). For those who survived, the hospital and ICU LOS were longer, and they were more likely to be discharged to a skilled nursing facility (SNF), long-term acute care (LTAC), or to require organized home health care (n = 10, 91%) compared to patients with no wounds and patients with HAPU/I (Table 3). A final analysis of the data comparing 958 patient dispositions by wound classification (no wound, COVID-19 lesion, or HAPU/I) showed that 64.8% of patients with no wounds were discharged to home, 9.1% of patients with COVID-19 lesions were discharged to home, and 11.5% of patients with HAPU/I were discharged to home (P < .0001). For patients with no wounds, 35.2% were discharged to an SNF or LTAC facility; for patients with COVID-19 lesions, 90.9% were discharged to a care facility; for patients with HAPU/I, 88.5% were discharged to a care facility (P < .0001). Patients with no wounds had a 10.7% death rate, patients with COVID-19 lesions had a 50% death rate, and those with HAPU/I had a 24.6% death rate (P < .0001) The median length of hospital stay was 7 days (range, 1-157 days) for patients with no wounds, 25 days (range, 3-102 days) for patients with COVID-19 lesions, and 22 days (range, 2-38 days) for patients with HAPU/Is (P < .001). The median ICU LOS was 5 days (range, 2-51 days) for patients with no wounds, 25 days (range, 1-98 days) for those with COVID-19 lesions, and 20 days (range, 10-35 days) for those with HAPU/Is (P < .001).

These findings underscore the burden of patients who are admitted with symptomatic COVID-19 and go on to develop cutaneous manifestations of the illness. The data show the increased utilization of hospital resources to stabilize these individuals. Despite care team efforts, patients in this population who developed wounds still faced increased morbidity and mortality.

Skin Tones

Most organizations collect data on race, ethnicity, and language in their patient population. However, race and/or ethnicity alone do not account for the diversity of skin tones that may impact early recognition of skin changes. A literature review conducted in the United Kingdom in 2018, found that patients with darker skin tones were at higher risk of sustaining a higher stage of PU/I due to difficulty in identifying the early color changes associated with PU/I development.^18,19 With society's and health care's emphasis on diversity, equity, and inclusion, vigilance in identifying skin tones for recognition of early onset of disease and decreasing burden is essential. While the current study did not find a difference in incidence of HAPU/I and COVID-19 lesions when categorized by Fitzpatrick scale, data were only available for those patients with COVID-19 lesions or HAPU/Is that were photographed; the sample size also may have been too small to detect a difference.

COVID-19 Lesions

Acute respiratory failure and a systemic coagulopathy are considered critical characteristics of COVID-19.⁶ Ongoing reports have described hypercoagulopathy and thrombosis associated with COVID-19 infection²⁰ and the associated severe acute respiratory syndrome that accompanies this infection. Etiology of skin involvement includes the pneumocytes, immune cells, and vascular endothelial cells, causing both microvascular and macrovascular thrombosis.²¹ The cutaneous manifestation of COVID-19 involves a catastrophic microvasculature injury and may be associated with a procoagulant state⁶ that manifests in the skin as purpuric vasculitic lesions. The concept of skin failure has been described in the literature.²² In the current study, treatment markers were found for profound proinflammatory and hypercoagulable states, characteristic of COVID-19, representing extensive organ damage to include skin failure.

HAPU/I

While the literature describes nursing interventions to decrease the incidence of preventable HAPU/I,²³ and the authors' facility's compliance has long been near 100%, adherence to these methodologies did not appear to prevent COVID-19 cutaneous lesions. Differences were also seen in morbidity, length of stay and treatment needs between the patients who developed HAPU/Is and those who developed COVID-19 cutaneous lesions. These findings are not surprising given the distinctly different mechanisms of injury for HAPU/I versus COVID-19 skin lesions.

Dialysis

A previous study showed that patients receiving any form of dialysis had increased odds of developing deep tissue injuries (DTI) that evolved to stage 4 HAPU/I.¹⁰ Using a backwards regression model, Kirkland-Kyhn et al.¹⁰ demonstrated that patients on dialysis had a 4-fold greater chance of developing a DTI. In the current study, all symptomatic patients with COVID-19 who developed COVID lesions were more likely to be on dialysis (41%) than patients who developed HAPU/Is (20%).

ECMO

The use of ECMO to improve oxygenation and support vital organs has improved survival rates in patients with critical COVID-19 illness who have refractory hypoxemia.²⁴ The current study collected data from patients admitted during the early phase of the pandemic. The authors found that 9.1% of the patients who received ECMO developed COVID-19 lesions, while 4.4% of patients with COVID-19 who received ECMO developed HAPU/Is. Only 0.4% of patients with COVID-19 receiving ECMO did not exhibit HAPU/Is or COVID-19 lesions.

Patients with COVID-19 who receive ECMO may have a higher likelihood of exhibiting lesions because of the underlying pathophysiological impact of COVID-19 and the inflammatory response triggered by ECMO therapy.²⁴ Both the current study and the Yusuff study (2023) are supported by additional reports of COVID-19 lesions appearing during the acute phase of COVID-19.²⁵ The current study did not examine if the type of ECMO (ie, venovenous vs venoarterial) impacted the appearance of COVID-19 lesions, HAPU/Is, or ultimate patient outcome.

Vasopressor Use With Hypotension

Previous research found that patients with low perfusion related to hypotension and any state of shock were more likely to develop HAPU/Is.¹⁰ For every millimeter of mercury decrease in diastolic blood pressure, the odds of DTI increased by 7.5%.¹⁰ In a comprehensive literature review by Cox,²⁶ both hypotension and vasoactive medications for increasing blood pressure and perfusion also increased the incidence of HAPU/Is.

Steroids

While no studies were found to support the increase in COVID-19 related lesions or HAPU/I specifically, there is significant evidence to support that corticosteroid use impacts the skin by increasing fragility of skin.²⁷ In patients with symptomatic COVID-19 infection but no skin wounds, 50.2% were treated with systemic corticosteroids. For those with COVID-19 lesions, 68.2% were treated with systemic corticosteroids compared with 69.6% of patients with HAPU/Is. For both lesions and severe respiratory distress, systemic corticosteroids are key therapeutic options.⁵

Anticoagulants

Clinical management of COVID-19 includes anticoagulation and novel therapies to improve hypercoagulopathies²¹ that occur throughout the body. In the current study, 30.8% of patients without wounds received anticoagulation treatment compared with 81.8% of patients with COVID lesions and 76.8% of patients with HAPU/Is. This finding suggests that both microvascular and macrovascular thrombotic or bleeding events may occur due to treatment or disease process. While coumadin-induced necrosis is a well-documented phenomenon,⁸ no current studies on anticoagulant use in wound healing or the development of wounds were found to have shown positive or negative associations with outcomes. However, an article by Cole (2021) has suggested anticoagulant use may slow healing.²⁸

Hospital and ICU length of stay

Patients who developed COVID-19 lesions had significantly longer hospital and ICU LOS. They also had higher utilization of dialysis and ECMO, indicating significant resource utilization and systemic compromise despite their younger age. One study evaluating patients who developed HAPU/Is as captured by artificial intelligence demonstrated that these patients had longer LOS.²⁹

Transitions of Care

With COVID-19, the risk of venous and arterial thrombotic events in patients treated in the ICU is up to 30%, even when treated with thromboprophylaxis, and thrombotic events are associated with 5.4 times higher risk of mortality.³⁰

Limitations of this study include the single-center nature and the fact that the authors did not capture results of D-dimer tests in the cohort. In the literature, D-dimer levels have been shown to correlate with disease severity and to be a reliable prognostic marker for in-hospital mortality in patients admitted for COVID-19.³¹ Future work should be multicenter in nature and consider inclusion of D-dimer trends over the admissions encounter.

It is the authors' belief that the present study is one of the first larger-scale papers to describe characteristics, treatments, and outcomes of patients with cutaneous COVID-19 lesions and to compare those factors in patients with HAPU/Is or no skin issues during the first year of the COVID-19 pandemic. While all patients received the same nursing bundles of care, were overseen by a designated wound care team, and were treated by the same critical care intensivists, patients who developed cutaneous manifestations of COVID-19 were sicker and more prone to death.

While all patients within this study were symptomatic and had positive COVID-19 test results, patients who developed COVID-19 lesions had the longest hospital and ICU LOS and increased mortality when compared with patients who had no wounds and those with HAPU/Is. Although COVID-19 lesions are just one potential complication for these patients, clinicians must consider the impacts on inpatient and long-term care. Examination of the link between COVID-19 lesions and patient- and therapy-related variables showed a significant relationship, which could shed light on how to manage and plan the transitions of care for these patients in health systems worldwide.

Affiliations: ¹University of California Davis, Sacramento, CA; ²Stanislaus State University, Turlock, CA

Potential conflicts of interest: The authors have no financial or other conflicts of interest to disclose.

Address all correspondence to: Oleg Teleten, MS, RN, CWCN, University of California Davis, One Shields Avenue, Davis, CA 95616; osteleten@ucdavis.edu