Recent publications have accelerated the discussion of skin failure and its relationship to unavoidable pressure injuries and terminal ulceration.1–3 These articles underscore the confusion in nomenclature and lack of agreement on critical points, including the definition of skin failure, the relationship of skin failure to unavoidable pressure injury, and the classification of skin injuries when patients are dying. Over the years, a variety of authorities have entertained a growing array of names for terminal ulceration, including decubitus ominosus, Kennedy Terminal Ulcer, Trombley-Brennan Terminal Tissue Injury, and Skin Changes at Life’s End (SCALE), leaving many caregivers deservedly confused when discussing these lesions.4–7 There is a need for a unified classification system that brings together these concepts in a consistent, easily understandable fashion.
Given the scarcity of research regarding skin failure, terminal ulceration, and pressure ulcer unavoidability, the wound care community relies on thought leaders to generate clinical opinion, including consensus and “white papers.” A recent review reiterates the variety of classifications related to end-of-life wounds and unavoidability of certain pressure ulcers and concludes that proper characterization of terminal and unavoidable skin injuries has not been achieved.3 This article, however, does not offer solutions to consolidate or unify overlapping concepts and definitions.3 There is an urgent need to address classification of these entities and simplify nomenclature, which will require agreement from a broad interprofessional group of wound care professionals on critical points including definition of skin failure and its relationship to unavoidable pressure injury and terminal ulceration. This commentary offers suggestions for simplification of taxonomy and directions for evidence-based research.
Multiple pathophysiologic factors are at play with unavoidable pressure injuries, including the dying process itself.8 However, the literature is unclear as to whether “terminal ulcers” are different from pressure-related injuries, even though they commonly appear over bony prominences. In addition, there are other skin changes such as blistering, mottling, and gangrene that occur concomitant to the dying process, advanced chronic illness, vascular disease, and severe physiologic stress.6 Some authorities opine that pressure injuries are a form of skin failure, whereas others claim that pressure injuries and skin failure are separate entities.9–12 The solution I propose is recognition that skin failure is the common denominator for wounds occurring close to death, unavoidable pressure injuries, and skin impairment related to tissue ischemia.13 Simplification of nomenclature will facilitate coding, solve issues related to quality measurement, and set a path on the search for common mechanisms of organ failure.
The most distinctive diagnostic criterion for a terminal ulcer is the acknowledgment that a patient is dying. However, not all practitioners possess the ability to accurately prognosticate death.14,15 According to the hospice community, there are 2 phases prior to death: the “preactive phase of dying” and the “active phase of dying.”16 On average, the preactive phase of dying may last approximately 2 weeks, whereas the active phase lasts approximately 3 days. If a pressure injury occurs during the preactive or active phase of dying, most wound care specialists would agree that this could be classified as a terminal ulcer.7 But what if a pressure injury occurs before the active or preactive phase of dying—is this still a terminal ulcer? And what if a patient develops a pressure injury, and his/her life is prolonged by medical interventions, or he/she recovers from the brink of death?
Life support technologies have evolved in sophistication, increasing survivability of patients with acute catastrophic illness, including those with advanced age living with multiple chronic, debilitating illnesses.17 In this setting, the designation of “terminal ulcer” when death is months or years away is both inaccurate and inappropriate. If death is a future event at the time of diagnosis, and the time frame toward death is vague and prolonged, the diagnosis of “terminal ulcer” serves no other purpose than a designation of unavoidability, absolving caregivers of blame for an outcome with potential regulatory, reimbursement, and risk-management implications. In addition, inaccurately labeling a patient with a terminal ulcer may cause additional confusion and emotional distress to patients and families.18 Therefore, it is my opinion that any wound classification incorporating a terminal designation should be replaced by a term with greater accuracy and less morbid implications.
It is my view that skin failure should be considered as a diagnosis not only in terminal situations, but also in advanced chronic illness and intensive care settings where physiology is acutely compromised and pressure injury is unavoidable. Many chronic illnesses worsen over time and manifest in collateral comorbidities, decreased functional status, and nutritional depletion that result in unavoidable pressure injuries.8 For example, the first patient with primary degenerative dementia described by Alois Alzheimer in 1906 died with sacral and trochanteric pressure ulcers.19 In a recent article that described terminal manifestations of dementia, pressure ulcer incidence rose precipitously in the months prior to death.20 Recognition of skin failure across the continuum will unify clinical observations and assist in adjustment of quality measurement, which is a cornerstone of our evolving healthcare system.
Pressure injuries are common in the ICU, with a reported incidence of up to 42%.21 Without modern intensive care technologies, many of these patients would die. Many conditions associated with unavoidable pressure injury are present in patients in intensive care.8 Few intensivists would accept the terminology “terminal ulceration,” even though pressure injuries are associated with increased mortality and pathophysiology that share similarities with terminal ulceration occurring outside the ICU.22 These similarities, as defined in the SCALE consensus statement, include impaired tissue tolerance and hypoperfusion.7
In the 19th century, Jean Martin Charcot recognized that some pressure ulcers precede death and named this lesion the decubitus ominosus.4 In 1989, Kennedy5 observed similar phenomena in residents of long-term-care facilities. These observations are important milestones in our knowledge of the history of pressure-related injuries. We now possess powerful technologies that prolong life, and our views on pressure injuries and their nomenclature need to evolve. This is especially true in an era of data-driven quality measures, a culture of pay-for-performance, and coding requirements that promote simplification of medical terminology for Meaningful Use and better patient outcomes.23
Skin is the largest organ of the body, and it fails like any other organ system.12 Given the large surface area it covers, it may fail regionally, as well as systemically. Thus, it is a spectrum that includes unavoidable pressure injuries and other manifestations, such as blistering, mottling, and gangrene.9 This view that skin failure can occur in discrete or regional areas is in direct contrast to Olshanksy1 and others who state that skin failure must include the entire organ.10 The spectrum of skin failure may also include conditions that promote decreased tissue tolerance. If so, then pressure or shear injuries should be classified not as a separate entity, but a manifestation of skin failure. Considering that the mechanism includes hypoperfusion, vascular ulcers should also be considered in the spectrum of skin failure.
Advancements in medical knowledge and technology have enhanced our ability to prolong life, altering the natural history of many diseases and forcing us to alter our terminology. It makes sense to look beyond any “terminal” designation for accurate nomenclature that applies to all healthcare settings across the continuum. The term “skin failure” presents a reasonable alternative, defined as the state in which tissue tolerance is so compromised that cells can no longer survive in zones of physiologic impairment such as hypoxia, local mechanical stresses, impaired delivery of nutrients, and buildup of toxic metabolic byproducts. In this schema, skin failure can occur over bony prominences where skin and underlying tissues, including muscle, are stretched and subjected to external pressure.
Once skin failure is properly defined and its manifestations recognized, the door will open for physicians to accept this as a medical diagnosis—something that has been lacking in medical education and clinical practice.24 The acknowledgment of skin failure will enable more accurate coding and reimbursement across the healthcare continuum. If skin failure is clearly established as an accepted disease state, then many pressure injuries lose their validity as a quality measure, provided that we utilize preventive interventions suggested in clinical practice guidelines including basic skin care, pressure redistribution modalities, and nutritional support where applicable. As we transition from a fee-for-service healthcare system into one where quality and patient outcomes become the currency, the classification of unavoidable pressure ulcers as a manifestion of skin failure becomes increasingly important.
The time has come to clear the field of multiple terms describing the same phenomenon and remove confusing distinctions based on inadequately characterized diagnoses that lack commonalities with other organ diseases. Skin failure is a unifying concept defined by poor tissue tolerance and other factors including hypoxia, ischemia, decreased delivery of nutrients, and decreased clearance of toxic metabolites that may share characteristics with reperfusion injury.25 The resulting damage is inclusive of the subadjacent and supra-adjacent tissues, thus leading to a lowered threshold for injury in areas of mechanical stress. Adopting the terminology of skin failure is logical from both a diagnostic and quality measurement standpoint. The challenging next step is collecting evidence from basic and clinical science that supports a unified classification system that makes sense and is clinically useful.
Many questions need to be answered to reach this goal. What is the difference in pressure ulcers that develop before death and those related to hemodynamic instability? Do we need to quantify hemodynamic instability to justify the diagnosis of skin failure? What are the underlying physiologic factors associated with skin failure? Considerations include edema, vascular hyperpermeability, vasoconstriction, hypoxia, mitochondrial disease, and concomitant multiorgan dysfunction syndrome.26,27 It is probable that destructive pathways exist that share commonalities with other organ system failures such as inflammation and fibrosis.28,29 Manifestations of these pathways may include entities other than ulceration, such as mottling and gangrene in nonpressure areas. Another promising avenue of investigation is genomic medicine, whereby genetic factors that underlie vascular responses to ischemia may lead to personalized therapies for prevention and treatment.30
To date, there are no blood tests or biomarkers diagnostic for skin failure, rendering it a clinical diagnosis based on signs and symptoms observed at the bedside. Other organ systems such as heart, liver, lung, and kidney have clearly defined parameters for determination of failure. Identification of a biomarker specific for skin failure would go a long way in identification and diagnosis.
In addition, we must not lose sight of the fact that identification of the unavoidable pressure ulcer is still elusive. This has important implications from a quality measurement, reimbursement, and risk-management standpoint. Although many factors have been associated with unavoidability, including the dying process, there are no clinical studies that enable definitive determination of which pressure injuries are unavoidable and no validated algorithms to determine unavoidability.31 The development of a reliable algorithm to determine unavoidability will be of great help in defining an unavoidable wound and more accurately defining pressure ulcers as a quality measure. There are many issues ripe for investigation, and recognition of skin failure as a common denominator for many bedside observations will engender a unified classification system and pave the way to a clearer future. Achieving this goal will require agreement and collaborative effort from the entire interprofessional wound care community.
References
1. Olshanksy K. Organ failure, hypoperfusion, and pressure ulcers are not the same as skin failure: a case for a new definition. Adv Skin Wound Care 2016;29:150.
2. Delmore B, Cox J, Rolnitzky L, Chu A, Stolfi A. Differentiating a pressure ulcer from acute skin failure in the adult critical care patient. Adv Skin Wound Care 2015;28:514-24.
3. Alvarez OM, Brindle CT, Langemo D, et al. The VCU Pressure Ulcer Summit: the search for a clearer understanding and more precise clinical definition of the unavoidable pressure injury. J Wound Ostomy Continence Nurs 2016;3(5):19.
4. Levine JM. Historical notes on pressure ulcers: the decubitus ominosus of Jean-Martin Charcot. J Am Geriatr Soc 2005;53:1248-51.
5. Kennedy KL. The prevalence of pressure ulcers in an intermediate care facility. Decubitus 1989;2(2):44-5.
6. Trombley K, Brennan MR, Thomas L, Kline M. Prelude to death or practice failure? Trombley-Brennan terminal tissue injuries. Am J Palliat Care 2012;29:541-5.
7. Sibbald RG, Krasner DL, Lutz J. SCALE: Skin Changes at Life’s End: final consensus statement: October 1, 2009. Adv Skin Wound Care 2010;23:225-36.
8. Edsberg LE, Langemo D, Baharestani MM, Posthauer ME, Goldberg M. Unavoidable pressure injury: state of the science and consensus outcomes. J Wound Ostomy Continence Nurs 2014;41:313-34.
9. Witkowski JA, Parish LC. The decubitus ulcer: skin failure and destructive behavior. Int J Dermatol 2000;39:894-6.
10. White-Chu EF, Langemo D. Skin failure: identifying and managing an underrecognized condition. Ann Long Term Care 2012;20(7):28-32.
11. Yastrub DJ. Pressure or pathology: distinguishing pressure ulcers from the Kennedy terminal ulcer. J Wound Ostomy Continence Nurs 2010;37:249-50.
12. Langemo DK, Brown G. Skin fails too: acute, chronic and end-stage skin failure. Adv Skin Wound Care 2006;19:206-11.
13. Levine JM. Skin failure: an emerging concept. J Am Med Dir Assn 2016;17:666-9.
14. Taniyama TK, Hashimoto K, Katsumata N, et al. Can oncologists predict survival for patients with progressive disease after standard chemotherapies? Curr Oncol 2014;21(2):84-90.
15. Moore NA, Brennan PM, Baillie JK. Wide variation and systematic bias in expert clinicians’ perceptions of prognosis following brain injury. Br J Neurosurg 2013;27:340-3.
16. Hospice Patients Alliance. Signs and symptoms of approaching death.
www.hospicepatients.org/hospic60.html. Last accessed February 9, 2017.
17. Vetrano DL, Foebel AD, Marengoni A, et al. Chronic diseases and geriatric syndromes: the different weight of comorbidity. Eur J Intern Med 2016;27:62-7.
18. Marcus JD, Mott FE. Difficult conversations: from diagnosis to death. Ochsner J 2014;14:712-7.
19. Maurer K, Volk S, Gerbaldo H. Auguste D and Alzheimer’s disease. Lancet 1997;349:1546-949.
20. Mitchell SL, Teno JM, Kiely DK, et al. The clinical course of advanced dementia. N Engl J Med 2009;361:1529-38.
21. Cuddigan J. Critical care. In: Pieper B, ed. Pressure Ulcers: Prevalence, Incidence and Implications for the Future. Washington, DC: NPUAP; 2013:47-56.
22. Manzano F, Pérez-Pérez AM, Martínez-Ruiz S, et al. Hospital-acquired pressure ulcers and risk of hospital mortality in intensive care patients on mechanical ventilation. J Eval Clin Pract 2014;20:362-8.
23. Centers for Disease Control and Prevention. Meaningful use.
www.cdc.gov/ehrmeaningfuluse/introduction.html. Last accessed February 10, 2017.
24. Levine JM, Ayello EA, Zulkowski KM, Fogel J. Pressure ulcer knowledge in medical residents: an opportunity for improvement. Adv Skin Wound Care 2012;25:115-7.
25. Wang WZ, Baynosa RC, Zamboni WA. Update on ischemia-reperfusion injury for the plastic surgeon: 2011. Plast Reconstr Surg 2011;128:685e-92e.
26. Oakley R, Tharakan B. Vascular hyperpermeability and aging. Aging Dis 2014;5:114-25.
27. Kleiman DA, Barie PS. Survival in fully manifest multiple organ dysfunction syndrome. Surg Infect (Larchmt) 2014;15:445-9.
28. Gentile LF, Cuenca AG, Efron PA, et al. Persistent inflammation and immunosuppression: a common syndrome and new horizon for surgical intensive care. J Trauma Acute Care Surg 2012;72:1491-1501.
29. Rockey DC, Bell PD, Hill JA. Fibrosis—a common pathway to organ injury and failure. N Engl J Med 2015;372:1138-49.
30. Baczynska D, Michalowska D, Barc P, Skora J, Karczewski M, Sadakierska-Chudy A. The expression profile of angiogenic genes in critical limb ischemia popliteal arteries. J Physiol Pharmacol 2016;67:353-62.
31. Levine JM, Zulkowski KM. Secondary analysis of OIG pressure ulcer data, including incidence, avoidability, and level of harm. Adv Skin Wound Care 2015;28:420-8.
