Skin Failure Clinical Characteristics and Clinical Instruments for Diagnosis in Adult Patients With Advanced or Terminal Diseases: A Scoping Review

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Prevention of skin injuries or lesions due to pressure is key to health care quality. However, despite the resources focused on this issue, it continues to be a prevalent and growing problem due to the aging population, prolonged institutionalization, unknown biological elements, and a lack of historical clinical research.¹

Advanced chronic diseases are currently described as progressive and irreversible conditions according to specific clinical criteria, which in pathologies such as cardiac, renal, neurological, hepatic, and pulmonary, among others, will determine a limited life prognosis in the absence of near or imminent death.^2,3 According to disease trajectory there could be specific risk factors for the development of skin lesions associated with organ decline, that is, organ failure and frailty characteristic of chronicity or terminality.^4,5 Such factors could lead to the provision of care focused on irreversible and unavoidable injuries⁶ considering a different etiology to pressure and shearing.⁷ In the context of organic deterioration, advanced disease or terminal illness, in this context, specific injuries have been proposed: KTU, Trombley-Brennan terminal tissue injury, SCALE, and skin failure.^8-12

In 1990, the term skin failure was used in the field of dermatology to describe severe skin conditions such as erythroderma, burns, pemphigus, Stevens-Johnson syndrome, and toxic epidermal necrolysis.^13,14 In 1991, Irvine¹⁵ defined skin failure with a focus on alterations of the skin’s functions, loss of normal temperature control, and failure to prevent percutaneous loss of fluids, electrolytes, and proteins, with consequent imbalance and failure of the mechanical barrier to penetration of foreign materials. In a 2006 report, Langemo and Brown addressed the concept of skin failure, describing lesions resulting from a state of hypoperfusion due to organ dysfunction, and establishing a correlation between skin death and underlying tissue according to disease state, acute skin failure due to critical illness, chronic skin failure due to advanced chronic disease, and terminal skin failure due to hypoperfusion at the end of life.¹⁶ In 2017, Levine¹⁷ strengthened this definition of skin failure by positing the presence of compromised tissue tolerance to such a degree that hypoxia and local mechanical stress result in altered nutrient supply and accumulation of toxic metabolic byproducts.

For the identification of skin failure, a specific description has been proposed which could differentiate this phenomenon from a pressure injury, while the latter is round and mainly reddish in appearance, the lesions associated with skin failure exhibit a butterfly or pear shape with a yellow, purple, or black coloration of accelerated progression and in a context of high mortality.¹⁸ This cutaneous injury, moreover, can occur even in the absence of pressure points or exposure to interface pressures; instead, there is an alteration of the angiosome as a functional unit of the skin with respect to states of hypoperfusion and prolonged hypoxia with a consequent cellular and vascular alteration.^19,20 

A preliminary search in PubMed identified a scoping review by Dalgleish et al,²¹ whose objective was to map the concept of “skin failure,” highlighting differences with respect to skin lesions and pressure injuries for example, and specific risk factors related to disease states, strengthening the importance of considering other etiologies for skin lesions. Likewise, Sibbald and Ayello¹⁰ published levels of agreement and consensus among health care professionals on the terminology for skin failure, terminal ulcers, and unavoidable pressure injuries. Bain et al⁷ described the pathophysiology of skin failure in contrast to pressure injuries, establishing the importance of etiological and therapeutic differentiation between the conditions, which could result in better management of resources and individualized treatment. Similar conclusions are presented in the literature review by García-Fernández et al,²⁰ who established a differentiating conceptual model for injuries associated with organic deterioration and dependence.

In 2016, the National Pressure Injury Advisory Panel (formerly the National Pressure Ulcer Advisory Panel) published revised definitions for “unstageable pressure injury” and “deep tissue pressure injury.”²² Despite the advances in skin failure definitions regarding potential etiological differences between skin failure and pressure ulcers or injuries,^7,10 important conceptual variability in definitions of skin failure still exists. There is a notable lack of scientific evidence about etiological factors and the links to disease status from a diagnostic and treatment perspective, and in terms of resource management, associated health costs, and therapeutic individualization.^7,23,24

There is no consensus for lesions that may not need curative clinical intervention. Health care professionals focus their goals of care on prevention and healing rather than on meeting the needs of patients with irreversible wounds, and they focus on therapeutic approaches that transition toward maintenance, palliation, and comfort, such as control of pain, infection, odor, bleeding, and exudate to optimize quality of life.²⁵ Consequently, little is known about the relationship between skin failure injuries and risk factors resulting from multiorgan failure or organ deterioration, appropriate specific evaluation of skin failure, and respective nursing interventions related to the phenomenon. The present scoping review aimed to evaluate the available evidence about characteristics and clinical instruments for skin failure diagnosis and evaluation in adult patients (aged 18 years or older) with advanced or end-stage disease.

Study design

This scoping review was guided by JBI methodology for scoping reviews²⁶ and is reported according to the PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and Explanation recommendations.²⁷ The scoping review methodology was chosen to map the existing literature²⁸ about skin failure. 

The guiding question of the present scoping review was: What is the available evidence regarding the characteristics and clinical instruments for skin failure diagnosis in adult patients with advanced or end-stage diseases?

Search strategy

The search strategy was carried out using a 3-step method. First, an initial limited MEDLINE (PubMed) search was performed to identify articles on the topic and refine keywords. The search strategy combined MeSH terms and uncontrolled language (relevant synonyms) and was constructed by 2 authors (M.Z.V. and V.B.P.) in collaboration with a librarian. Second, the text words contained in the titles and abstracts of the relevant articles were used to construct a comprehensive search strategy in all databases included in the review. The search strategy was adapted to each database and/or information source included. Finally, the reference lists of all included information sources were examined for additional studies. 

The search for articles was conducted between April 4 and May 18 2023. The databases searched were PubMed, CINAHL, Web of Science, LILACS, ScienceDirect, the Cochrane Database of Systematic Reviews; and grey literature was retrieved via “DART E-theses Portal” and “CAPES Thesis Portal.” An initial search was done in PubMed to refine the index terms. The definitive search was then done with combinations of MeSH terms and noncontrolled language, given that skin failure is not a health descriptor, in an effort to guarantee a wide retrieval of literature related to the subject. The Boolean operators AND, OR, and NOT were used, along with filters according to database and exclusion criteria (Table 1).

Study inclusion and exclusion criteria

This review considered qualitative and quantitative studies, without restrictions related to time or language, concerning the characteristics and clinical instruments for skin failure diagnosis in adult patients with advanced or end-stage disease. 

Editorials, consensus and opinion articles, studies on animal and pediatric populations, and studies related to dermatological diagnoses (eg, erythroderma, burns, pemphigus, Stevens-Johnson syndrome, toxic epidermal necrolysis) were excluded because their clinical expressions in terms of morphology and progression are not compatible with the definition of skin failure used in this review, which consists of a specific concept referring to a perfusion state, angiosome involvement, and expression of skin failure by means of a lesion with specific characteristics.^7,16,18,20

Study selection

After the literature search, the entire selection of articles was exported to EndNote (version 20.6), which was used for bibliographic management, and duplicates were eliminated.

Two researchers (M.Z.V. and J.D.G.) independently assessed the title and abstract of potentially relevant studies using the selection criteria. The full-text versions of articles considered eligible were examined. After selection of eligible articles, the same 2 researchers noted above read the publications in full to define the study sample. A third researcher (V.B.P.) analyzed the data only if there was disagreement.

Data extraction and synthesis

Data extraction was carried out independently by 2 researchers (M.Z.V. and J.D.G.) using a structured instrument developed by the researchers. The instrument included the following information: title, study type or design, objective, study population/context, evidence type, author, publication year, country, journal, volume, study group size, concepts associated with skin failure (eg, KTU, SCALE, Trombley-Brennan terminal tissue injury, unavoidable pressure injuries, pressure ulcer/pressure injury), elements used for clinical evaluation related to “skin failure,” type of instrument and evidence of the validity of the instrument, the objective of clinical evaluation for skin failure, limitations, and other relevant findings.

The articles were organized in relation to the characteristics of skin failure and the classifications used in this review, as well as concepts related to skin failure and clinical indicators involved in the appearance of the lesion. Quantitative analysis of the data was performed by 3 researchers (V.B.P., P.C.N., and M.Z.V.).

EndNote (version 20.6) was used for bibliographic management, and Covidence online software was used as a data extraction and review tool. 

A total of 196 articles were initially identified from searching the PubMed (n = 110 [56.1%]), CINAHL (n = 24 [12.2%]), Web of Science (n = 50 [25.5%]), LILACS (n = 4 [2.0%]), ScienceDirect (n = 5 [2.6%]), and Cochrane (n = 3 [1.5%]) databases. No documents were found in the grey literature. After removing duplicates, the titles and abstracts of 103 articles were evaluated, and 80 of these were excluded. (Excluded articles focused only on the definition of skin failure or reported on the pediatric population and on dermatologic pathologies [eg, erythroderma, burns, pemphigus, Stevens-Johnson syndrome, toxic epidermal necrolysis]). The researchers reviewed 23 full-text articles according to the inclusion and exclusion criteria. Of these, 15 articles did not fulfill the selection criteria, mainly because they only referred to theoretical definitions of skin failure and did not relate to its diagnosis or clinical evaluation in patients or patient groups. Eight articles were ultimately included for data extraction (Figure).

Characterization of studies to identify skin failure

According to the definition of skin failure used for this review as stated above in the “Study inclusion and exclusion criteria” section,^7,16,18,20 the included studies analyzed between 1 patient and 552 patients aged 50 to 99 years, mainly male, admitted to the intensive critical care unit (Table 2). It was not possible to establish averages, both because not all studies describe subjects’ demographic characteristics with adequate specificity and because of the studies’ methodological designs.

All the reviewed articles mentioned acute skin failure, with 2 articles^29,30 mentioning skin failure in a terminal illness stage. Most studies focused on patients in the critical intensive care unit, with skin failure primarily associated with physiological stress (Table 2, Table 3).

According to the studies reviewed, sepsis, hypoperfusion, use of vasopressors, respiratory failure, malnutrition or obesity, acute organ failure, mechanical ventilation, and chronic diseases were the most important aspects related to skin failure, mainly acute skin failure.^30,31 These clinical characteristics can also aid in differentiating between skin failure vs. injuries caused by pressure or friction.

This study identified an instrument—the SFCIS—whose objective is to evaluate the characteristics of skin failure. The SFCIS was developed by Hill and Petersen,³² based on variables from the literature, and allows differentiation between skin failure and pressure lesions. Their statistical analysis determined clinical characteristics associated with skin failure: a serum albumin level less than 3.5 mg/dL (P = .07), blood flow impairment (P = .05), presence of sepsis/multiorgan dysfunction syndrome (P = .001), and use of vasopressors/inotropic drugs (P < .001) and mechanical ventilation (P = .06). The SFCIS identified 83.7% of patients as having probable cutaneous failure; however, this instrument corresponds to a retrospective study in a limited population of 52 patients and does not describe evidence of current psychometric validity. 

This review mapped the available evidence on clinical characteristics of and instruments for diagnosing and/or assessing skin failure in a context of organ impairment in critical, advanced chronic, and terminal settings against the definition used as inclusion criteria,^7,16,18,20 and it demonstrates that there is limited evidence on clinical indicators for skin failure in these settings.

There is also a lack of data about incidence and prevalence of skin failure lesions. An 83.7% rate of probable acute skin failure was reported in a retrospective case-control study that included 52 patients hospitalized in different clinical services, using a tool that had not been validated.³²

The characteristics associated with skin failure were diagnosed in an acute context, and the term “skin failure” was often associated with pressure injuries, in line with the review by Dalgleish, who described an interchangeable use of definitions and a lack of etiological consensus.²¹

The articles reviewed by Langemo et al¹⁶ identified hypoperfusion as among the main factors associated with skin failure. The current scoping review found that the concept of acute skin failure was mostly used in the context of patients with ineffective tissue perfusion³⁴—specifically, in the context of those with peripheral arterial disease^21,35—and with blood pressure below 50 mm Hg to 60 mm Hg.³⁶ Two studies linked the pharmacological use of vasopressors to skin failure.^30,32 The retrospective case-control study involving 552 patients determined that patients with peripheral arterial disease were almost 4 times more likely than patients without the condition to have compromised tissue perfusion to develop a lesion secondary to skin failure, contributing empirically to its differentiation with other types of skin failure and, fundamentally, with pressure lesions.¹⁵ 

Factors that could lead to skin failure include compromised tissue tolerance due to hypoxia, local mechanical stress, malnutrition or moderate malnutrition,³⁵ hypoalbuminemia less than 3.5 mg/dL,³² body mass index greater than or equal to 30,³¹ and the accumulation of toxic metabolic product³⁷ in a context of functional and multiorgan deterioration¹⁶ with the involvement of 2 or more organs (respiratory, renal, cardiac, and/or hepatic systems^29,32,33,35). The presence of cardiac ischemia, or of hypovolemic or cardiogenic shock, could be a predictive risk factor as well.³⁵

Two additional important characteristics for skin failure reportedly are respiratory failure^29-31,33,35 and mechanical ventilation,^29,30,33,35 more specifically for 72 hours^29,35 and greater than 96 hours.³⁵ 

Sepsis^29-36 and long-duration surgeries such as orthopedic, general, and vascular surgery can have an important role in skin failure, possibly associated with patients’ critical health status.³⁵

The results of the present scoping review describe characteristics that can differentiate secondary skin insufficiency lesions from pressure lesions. This aligns with various authors’ perspectives that both conditions correspond to different clinical phenomena even when they present simultaneously. Pressure ulcer is understood as an ischemic and necrotic tissue injury that can occur even in healthy individuals; it is a marker of coexisting illness, rather than a mortality factor per se.³⁸ Skin failure thus tends to indicate organ failure.³⁹ Currently, expert consensus recognizes unavoidable pressure injury, defined them as an injury generated despite a clinical assessment of risk factors for pressure/shearing injuries and the application of standard prevention measures,⁴⁰ and resulting from clinical conditions including hemodynamic instability, impaired cardiopulmonary function, and nutritional deficit.⁴¹

Even when all the reviewed articles were framed within a context of critical patients, the term “end-of-life ulcer” is mentioned from the perspective of SCALE and KTU, exposing the lack of clinical specificity.^29,35 In 1989, Kennedy described KTU as a specific subgroup of ulcers derived from functional skin compromise at the end of life.¹¹ The term “SCALE” emerged to discuss clinical phenomena of specific skin changes at the end of life. Terminal injuries were associated with mortality, with a mortality rate varying between 55.7% during the 6 weeks after detection of a lesion in patients in an intermediate care facility,⁹ to 62% within 2 weeks prior to death in non-oncological patients, for example, those with Alzheimer’s disease.⁴² This perspective is important considering that it is still unclear whether other concepts such as SCALE, inevitable ulcer, or KTU correspond to a classification of skin failure or are skin failure itself.^8-10

Other potential specific characteristics of injuries resulting from skin failure include their shape (pear-, butterfly-, or horseshoe-shaped), their predominate localization on the coccyx or in the sacral zone, and their sudden appearance and accelerated progression.^21,30 Previous studies observed differences between skin failure and pressure ulcer based on the rapidly progressive butterfly presentation of the former, along with sacral/gluteal localization,³⁰ or the presence of a pear-shaped ulcer on the buttock with black lesions on the occiput, elbow, back, and ankle, which occurred at multiple sites simultaneously in a patient with an albumin level less than 3.0 g/dL, respiratory failure, and renal failure with septic shock.³⁶ A retrospective cohort study added the presence of irregular and fixed edges as signs of skin failure, as well as the absence of edematous or indurate periwound zones, which would correspond to characteristics of acute injuries during cases of concomitant organ failure and hemodynamic instability.³¹

Other results contribute to the characteristic of so-called atypical localization. In a case-control study, 69.2% of patients (n = 36) had atypical ulcer locations, defined as areas not exposed to pressure and/or shear forces.³² The irregular lesions reported in the retrospective cohort study of critically ill patients with COVID-19 were located in the sacrococcygeal region and the gluteal region (42% and 46%, respectively).³¹

Some tools could contribute to identifying clinical characteristics of skin failure, such as a Braden scale score of 14 or lower,²⁹ or functional capacity based on Karnofsky Performance Scale score.³² Although neither variable can be considered to be a predictive factor for or a clinical characteristic of skin failure because each lacks statistical significance, these variables may be relevant, specifically because life prognosis is not included as an important factor in current lesion assessments or clinical decisions for cutaneous therapeutic approach. This is also consistent with the theory of García-Fernández et al, who explain the main etiological mechanisms of dependence-related injuries, linking such a concept to the terminal and end-of-life scenario.²⁰ The study by Roca-Biosca et al, using the Garcia-Fernandez model, described lesions differentiated with pressure injuries, supporting the paradigm shift to other factors involved.⁴³ 

This review identified only 1 instrument specific to skin failure assessment—the SFCIS.³² Although the SFCIS does not present evidence of psychometric validity, it has aspects potentially indicative of skin failure that are not currently evaluated in the context of pressure injuries. These aspects correspond to atypical location and other factors likely to differentiate between skin failure and pressure injury, such as a serum albumin level below 3.5 mg/dL, impaired blood flow, presence of sepsis/multiorgan dysfunction syndrome, use of vasopressors/inotropes, and mechanical ventilation. In terms of validity evidence, although not all variables were independently significant due to the sample size of 52 patients, multivariate analysis determined significant results in all cases except serum albumin (P = .09).³² Such factors were mainly found in all other articles reviewed, and even when presented from the perspective of acute skin failure, it is interesting to consider the common etiological scenario of organ deterioration, stating that a skin failure could appear at any stage of the disease according to its classification: chronic, acute, and/or terminal.^16,22

The results of this review present common factors such as probable causes of and diagnostic factors for skin failure. Even in the absence of convincing evidence, at least from the perspective of primary studies, all the articles emphasize the importance of further study of skin failure in order to unify the concept and to guide diagnosis and clinical management in terms of best practice, patient quality of life, and associated health care costs. 

The results of this review complement the empirical literature related to the concept of skin failure, showing current gaps and areas that should be better explored (Table 4).

This study is limited by the absence of controlled terminology related to skin failure, which may have affected the ability to retrieve all relevant studies. The phenomenon of skin failure currently has interchangeable definitions. This review was based on a specific concept of skin failure involving perfusion status, angiosome involvement, and expression of skin failure through a lesion with specific characteristics. This may be a limitation of the study because this definition may have excluded other studies of importance. The authors took measures to minimize the effect of such limitations by analyzing different databases, including grey literature.

This exploratory review included articles that described patients with critical, advanced chronic, or terminal disease in whom a lesion developed that was compatible with the established definition of skin failure based on morphology and clinical progression. The evidence regarding skin failure is limited and is mainly based on retrospective studies and case reports. Only 1 tool for aiding in identifying skin failure was identified, which, in relation to its publication, does not describe the evidence of psychometric validity with respect to current recommendations. The included studies present potential skin failure lesions in a terminal setting but mainly in patients under physiological stress in intensive care units, which could strengthen the proposed classification. The studies related to the theoretical concept of skin failure identified sepsis, hypoperfusion, vasopressor use, respiratory failure, malnutrition or obesity, acute organ failure, mechanical ventilation, and chronic diseases as the most important aspects related to skin failure. 

These clinical features could be differentiators in relation to pressure injuries because in addition many of them are aspects that are not routinely assessed and are not dimensions of the currently used pressure injury assessment tools. The findings of this review may complement the published literature regarding the theoretical concept of skin failure and may contribute to the clinical knowledge gap regarding the phenomenon by providing support for the need for further studies. 

Authors: Melissa Zimmermann-Vildoso, Mag¹; Javier Devia-González, Mag¹; Paula Cristina Nogueira, PhD²; and Vanessa de Brito Poveda, PhD²

Affiliations: ¹School of Nursing and Midwifery, School of Nursing, Universidad de los Andes, Chile, Santiago, Chile; ²School of Nursing, University of São Paulo, São Paulo, Brazil

ORCID: Nogueira, 0000-0001-5200-1281; Zimmermann-Vildoso, 0000-0003-2432-7166

Disclosure: This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), or the Brazilian Federal Agency for Support and Evaluation of Graduate Education, finance code 001. For the language revision process, this manuscript was supported by the research assistance fund (FAI) of the University of the Andes.

Correspondence: Melissa Zimmermann-Vildoso, Mag; Universidad de los Andes, Chile, School of Nursing and Midwifery, School of Nursing, Monseñor Álvaro del Portillo 12455, Santiago, Las Condes, Región Metropolitana, Santiago, 7620060 Chile; melizimmermann@gmail.com

Manuscript Accepted: August 2, 2024