Organ Failure and Dermatologic Skin Area/Severity Indexes
The SCALE document clearly stated that other situations such as multiple organ failure were beyond the scope of the SCALE panel document. Multiorgan dysfunction or failure described by Irwin and Rippe42 is defined as the “presence of altered organ function in acutely ill patients such that homeostasis cannot be maintained without intervention. It usually involves two or more organ systems.” Not all patients with SCALE necessarily have multiorgan failure, but research is needed to document the severity and extent of injury that may accompany SCALE. The authors of the present article will use examples to illustrate recognized quantitative models for other organ compromise that could be used to create a model for the skin.
Kidney disease represents a purely quantitative model for organ failure. To determine renal failure, glomerular filtration rate is calculated using the serum creatinine, age, body size, and gender. This is an objective measurement to determine kidney failure based on various levels of compromise.
For governments or policy makers to accept skin failure as a framework of unavoidable skin injury at the end of life and not subject these changes to penalties for substandard healthcare, it would require diagnostic criteria that reflect area and extent of injury. Dermatologists have utilized scores for research on treatment effectiveness that combine these components. The body surface area could be calculated similarly to burn score formulas, with the hand and fingers representing approximately 1% of the total body surface, or as in the rule of nines.43
Another diagnostic option is the Psoriasis Area and Severity Index, which is often used to assess new treatments, including newer biologic agents.44 Areas of psoriasis are given a 0 to 4 score for each of three clinical criteria: erythema, thickness of the scale, and thickness of the lesions. Other more complicated scoring systems also exist; for example, scoring for atopic dermatitis45 bases 60% of the score on the intensity of the injury, 20% for the area, and 20% for symptoms (pruritus and insomnia). The potential components for a proposed preliminary skin failure score are provided in Table 5.
TROMBLEY-BRENNAN TERMINAL TISSUE INJURY
Over a decade after the KTU was first described, a different team of clinicians published data regarding skin manifestations observed in persons in the last hours/days/weeks of their life. Trombley and Brennan noticed skin alterations that spontaneously appeared on patients in their inpatient palliative care unit. A 2010 retrospective chart review of 22 patients revealed pink, purple, or maroon bruiselike butterfly-shaped skin alterations.7 These lesions do not progress to a pressure injury. This chart review was expanded to include an additional 58 patients. All of these terminal tissue injuries developed despite the staff’s prevention strategies. Researchers also identified linear striations on patient legs that often extended downward. Horizontal striations may also be observed on the thoracic or lumbar spine. These skin alterations were noted both over bony prominences and elsewhere, including on the thigh. These lesions often had a mirror-image pattern in patients at end of life. These skin alterations appeared spontaneously, evolved rapidly, and could appear in an area of little to no pressure (Figure 3). The research team cautioned that these terminal tissue injuries could be confused with a deep tissue injury (which they were not) but rather were an unavoidable occurrence related to internal organ and skin compromise for persons at the end of life. In addition, they noted in a few patients that when the center of the wound was devoid of color, death often occurred within 2 hours.7 The hospital named these terminal tissue injuries after the researchers (TB-TTI).7
A related 2012 study of 80 patients revealed that 79 had intact skin without any exudate. Researchers concluded that the 500 observed changes could not be attributed to gaps in care.8 Another retrospective chart review of an additional 86 patients corroborated earlier results. The median time from identification of the injury until death was 36 hours (M.R.B., unpublished data, December 2018). The pooled results indicated that 75% of the patients exhibiting a TB-TTI died within 72 hours of the first identification of these skin changes (M.R.B., unpublished data, December 2018). A further unpublished multisite study involving several hospitals within the health system is now in progress, and a National Institutes of Health grant has been submitted to continue this work.
Skin failure is a concept that has ignited passion and opposing opinions among healthcare professionals. One of the earliest proposals that the skin as an organ could fail was published by John La Puma10 in 1991. It was part of his remarks at a 2-day 1991 conference about the Agency for Health Care Policy and Research’s clinical guideline, Prediction, Prevention and Early Treatment of Pressure Ulcers in Adults.10 Dr La Puma remarked, “The skin is the largest organ of the body. If the heart, lungs, and kidneys are showing signs of failing, isn’t it logical that the skin would also show signs of failing? Why is a pressure ulcer considered a sign of inadequate healthcare, when symptoms of heart disease or lung disease or kidney disease are not? In the terminally ill patient, a pressure ulcer may only be a sign of physical decline and mortality.”10
In 2000, Witkowski and Parish12 also published a similar belief that “If the heart, lungs, and kidneys are failing, is it not logical that the body’s cover would also show signs of failure?” The concept of skin failure was once again brought to the forefront in presentations and publications by Langemo and Brown.14 Their expert opinion was based on a systematic review of literature published between 1984 and 2015, where seven articles were identified and explicated with clinical observation. Langemo14 defined skin failure as “an event in which the skin and underlying tissue die due to hypoperfusion that occurs concurrent with severe dysfunction or failure of other organ systems.” Three types of skin failure were described: acute, chronic, and end stage. Acute skin failure occurs concurrently with an acute illness such as septic shock or myocardial infarction; chronic skin failure occurs concurrently with a chronic condition such as multiple sclerosis or a malignancy, and end-stage skin failure occurs concurrently with end-of-life issues such as renal failure, pulmonary fibrosis, and so on.14 Other authors began to show interest in engaging with the concept of skin failure—both for and against.11–21
Levine18 built on Langemo’s definition by proposing that skin failure is “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.” This includes pressure injuries, wounds that occur at life’s end and in the setting of acute illness, and multisystem organ failure.17 Levine17 believes that skin failure is “an emerging concept that clarifies current trends in clinical practice” and “will lay the foundation for common nomenclature and open new directions for research.” Levine17,18 uses skin failure as a unifying concept that encompasses broader etiologies including pressure injury, KTU, TB-TTI, SCALE, and so on. The position of Langemo and many others in the wound care arena is to clarify that a pressure injury has pressure and/or shear as its etiology, whereas pressure is not a necessary component of skin failure. Langemo and Brown14 go on to note that skin failure and pressure injury can occur concomitantly on the same individual. Despite this research and key opinion leader commentaries, there is currently no agreed-upon definition of skin failure.
Acute Skin Failure
Empirical evidence regarding ASF is limited. One “clinical conundrum” is defining and identifying skin failure in acutely ill hospitalized patients.16 To provide some evidence to answer this question, Delmore and colleagues16 have published data from 552 ICU patients in the US to predict the development of ASF. They used Langemo’s definition and refined it slightly to state it is “the hypoperfusion state that leads to tissue death that occurs simultaneously to a critical illness.”16 This retrospective case-control study sorted the data into several categories: disease status, physical conditions, and conditions of hospitalization. Their ICU patients results revealed that peripheral arterial disease, mechanical ventilation for more than 72 hours, respiratory failure, liver failure, and severe sepsis/septic shock were statistically significant and independent predictors of ASF.16 The authors expressed concern that there is no clear-cut diagnostic criteria for ASF: “in certain populations, such as the critically ill patient, the phenomenon of ASF may be occurring and with the current level of evidence, these ulcers may be incorrectly identified as PrUs.”16
As one of the few data-based articles, this is an important contribution to ASF research and serves as a stimulus for further inquiry. Olshansky19 agreed with statements made by Delmore et al16 and gave examples of potential skin failures that appear randomly over the body, including Stevens-Johnson syndrome, necrotizing fasciitis, pemphigus, and epidermolysis bullosa. However, these diseases often occur without other organ failure. He agreed with Delmore and colleagues that ASF is not a pressure injury and called for the wound and dermatology communities to work together to create a uniform definition and diagnostic criteria for skin failure.19
TERMINAL ULCER TERMINOLOGY
Controversy exists regarding which term (KTU,1–3 TB-TTI7,8) is best to describe terminal lesions or whether these lesions, such as the lesser known Miller pressure equivalent injuries, are even terminal lesions.39 According to the KTU website,2,3 the KTU is a particular type of pressure injury seen in patients at the end of life. It states that the KTU “can start out larger than other pressure ulcers, are usually more superficial initially and develop rapidly in size, and depth and color.”2,3
Levine believes that terminal ulcer terminology, including SCALE, has limited application because of variability in late life trajectories and longer life spans in today’s healthcare environment, such as with artificial life support that can prolong the dying process.46 He believes that nomenclature associated with “end of life” is intrinsically problematic because this period is complex, often prolonged, and difficult to define and does not include breakdown in critical care settings that may share similar mechanisms. Levine’s solution is to recast these terms under the umbrella of the prognostically neutral term “skin failure” that is consistent with concepts of tissue physiology in other organ systems.
Although the literature may not always agree as to whether or not KTUs, SCALE, or TB-TTIs are pressure injuries, many clinicians and researchers believe that these skin injuries are not pressure injuries and can be unavoidable as part of the dying process. The CMS agrees with this stated belief and does provide some guidance in long-term care (LTC) settings (Supplemental Table, http://links.lww.com/NSW/A20). For example, according to the CMS, when a clinician determines that a patient has a terminal ulcer (mostly known as Kennedy ulcers), then this is no longer considered a pressure ulcer and is not coded in the pressure ulcer section of the Minimum Data Set (MDS) 3.0.27
There are no CMS statements regarding terminal skin injuries in acute care or in the Resident Assessment Instrument manual for LTC, long-term acute-care hospitals, or inpatient rehabilitation facilities. However, there are statements in the CMS’s State Operations Manual: Guidance to Surveyors for Long Term Care Facilities about pressure ulcers (F686, §483.25(b) Skin Integrity, §483.25(b)(1)).27 They became effective on November 28, 2017, and indicate that terminal ulcers can be a clinical phenomenon that are part of the dying process.27
Beyond reimbursement, other quandaries related to terminology exist. One of the controversies is how to accurately diagnose any terminal ulcer, because often they can only be retrospectively diagnosed (ie, after patient death). It is also unclear whether any terminal ulcers have healed; this is not reported in the peer-reviewed literature. Further, as alluded to in previous sections, there is controversy over whether terminal ulcers are pressure ulcers. Because these terminal lesions (as such) may be in areas exposed to pressure, pressure may be a factor in their development.
AVOIDABLE VERSUS UNAVOIDABLE PRESSURE INJURIES
Another debate central to these complex concerns is whether KTU, TB-TTI, SCALE, and skin failure are avoidable or unavoidable. By reviewing and synthesizing the literature on this topic, the authors’ intent is to summarize and introduce criteria for determining whether or not these skin phenomena, in addition to pressure injuries, are avoidable.
Early in the wound care literature, authors began to propose the idea that some or even all pressure ulcers were preventable or unavoidable. In the 19th century, Jean Martin Charcot believed that pressure ulcers were unavoidable given damage to the central nervous system, with the assumption that there were “neurotrophic fibers” that went directly from the brain and spinal cord to the skin.37 Because they could not be prevented, they were deemed unavoidable.
In November 2004, after a 3-year review of the existing literature and opportunity for public comment, the CMS revised its guidance for surveyors in LTC, using the term “unavoidable.” The intent of the CMS guidance was that residents should not develop a pressure ulcer while in LTC unless the resident’s condition was such that the ulcer could not be prevented:
Based on the comprehensive assessment of a resident, the facility must ensure that (1) a resident who enters the facility without pressure sores does not develop pressure sores unless the individual’s clinical condition demonstrates that they were unavoidable; and (2) a resident having pressure sores receives necessary treatment and services to promote healing, prevent infection and prevent new sores from developing.47[emphasis added]
This language clearly indicated that based on some residents’ clinical condition, some pressure injuries could be designated as unavoidable or not preventable. The CMS defined unavoidable as follows: “Unavoidable means that the resident developed a pressure ulcer even though the facility had evaluated the resident’s clinical condition and pressure ulcer risk factors; defined and implemented interventions that are consistent with resident needs, goals, and recognized standards of practice; monitored and evaluated the impact of the interventions; and revised the approaches as appropriate.”47 In turn, the CMS defined avoidable as follows: “‘Avoidable’ means that the resident developed a pressure ulcer and that the facility did not do one or more of the following: evaluate the resident’s clinical condition and pressure ulcer risk factors; define and implement interventions that are consistent with resident needs, resident goals, and recognized standards of practice; monitor and evaluate the impact of the interventions; or revise the interventions as appropriate.”47
Note that the four criteria listed in both definitions are the same except that in one instance the facility did all of the specified tasks (unavoidable), and in the other, the facility did not do one or more of the required care items (avoidable). Therefore, determining if a pressure injury is unavoidable is a process that includes assessment and evaluation of patient condition and risk factors, as well as a clearly defined and implemented individualized plan of care that was monitored, evaluated, and revised as appropriate.
In 2010 and 2014, the NPUAP held a series of conferences to further explore the notion that not all pressure injuries could be avoided. Soon after the NPUAP consensus conference held in 2010 at the Johns Hopkins Medical Center, the CMS definition of unavoidable pressure injury was broadened so it was applicable to all care settings.23 This was accomplished by consensus of the 24 national and international professional organizations in attendance at the conference. Stakeholders replaced the words “facility” with “provider,” and “resident” with “individual.”23 Further, there was 100% agreement among stakeholders that not all pressure injuries were avoidable,23 particularly when the ability of the body to reperfuse the tissue is limited or inadequate. There was 83% agreement that the condition called skin failure exists, and 100% indicated that skin failure was not the same as a pressure ulcer.23 Further, “the panelists recognized that no formal diagnostic criteria exist for skin failure. They supported that skin failure is a documentable condition and that skin failure is not the same as a pressure ulcer. There was no vote taken on Kennedy terminal ulcers as either a documentable pressure injury, or a low profusion association lesion.”23
The second NPUAP International Consensus Conference on avoidable versus unavoidable pressure injuries was held in 2014, again at the Johns Hopkins Medical Center.24 National and international experts from 25 stakeholder organizations as well as an audience of more than 400 individuals explored the multifaceted issue of pressure ulcer unavoidability within a systemic, scientific, organ-system framework. The attendees also considered the complexities of nonmodifiable intrinsic and extrinsic risk factors for unavoidable pressure injury and came to an 80% or greater consensus on a number of such factors. The resulting 2014 NPUAP Unavoidable Pressure Injury document was based on a review of hundreds of research articles that provided scientific evidence behind unavoidable risk factors for pressure ulcer development.24
The year 2017 saw updates to two documents regarding avoidable/unavoidable pressure injuries, one by the Wound, Ostomy and Continence Nurses Society26 and the other in a CMS State Operations Manual Appendix that updated its guidance to surveyors regarding the definition of avoidable and unavoidable pressure injuries.27 The bolded terms (emphasis added) were added to the original CMS definitions and are current as of October 1, 2018.27
“Avoidable” means that the individual developed a pressure ulcer/injury and that the facility did not do one or more of the following: evaluate the individual’s clinical condition and risk factors; define and implement interventions that are consistent with individual needs, goals, and professional standards of practice; monitor and evaluate the impact of the interventions; or revise the interventions as appropriate. “Unavoidable” means that the individual developed a pressure ulcer/injury even though the facility had evaluated the individual’s clinical condition and risk factors; defined and implemented interventions that are consistent with individual needs, goals, and professional standards of practice; monitored and evaluated the impact of the interventions; and revised the approaches as appropriate.
Given the current state of the literature, more research is needed to identify which factors in the development of pressure injuries are modifiable and which are not. There is currently no validated algorithm to determine whether a pressure ulcer is unavoidable.48 However, the concept of unavoidable pressure injury is supported by definitions from the CMS, NPUAP, and Wound, Ostomy and Continence Nurses Society, and consensus from conferences and in the literature supports the phenomenon of skin failure as distinct from pressure injuries.
Through synthesis of the literature on these concepts, it is clear that while there is agreement that skin changes at end of life are real clinical phenomena seen in practice, the pathophysiology of skin changes in dying and palliative care patients is incomplete. There is also the need to agree on definitions and terms and to begin to define diagnostic criteria for skin failure as well as skin changes at end of life. Having multiple terms to describe these phenomena can be confusing and may impede communication among clinicians, especially across disciplines. It may also be puzzling to payors and regulators.
Coming to consensus will be best accomplished in an interprofessional forum, regardless of professional licensure, specialty, or practice care setting. Terminology needs to be consistent and subject to validation in the clinical setting. This article provides a platform for further dialogue.
- The physiologic understanding of KTU, TB-TTI, SCALE, and skin failure is incomplete.
- Kennedy terminal ulcer, TB-TTI, and SCALE are considered to be unavoidable in persons at end of life.
- Skin failure is clinically distinct from pressure injury.
- There is a need to agree on definitions and terms and to begin to define diagnostic criteria for skin failure and skin changes at end of life.
1. Kennedy KL. The prevalence of pressure ulcers
in an intermediate care facility. Decubitus 1989;2(2):44–5.
4. Sibbald RG, Krasner DL, Lutz JB, et al. Skin Changes at Life’s End
): a preliminary consensus statement. WCET J 2008;28(4):15–22.
5. 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(5):225–36.
6. Krasner DL, Stewart TP. SCALE
wounds: unavoidable pressure injury. Wounds 2015;27(4):92–4.
7. Brennan MB, Trombley K. Kennedy terminal ulcers
—a palliative care unit´s experience over a 12-month period of time. WCET J 2010;30(3):20–2.
8. Trombley K, Brennan MR, Thomas L, Kline M. Prelude to death or practice failure? Trombley-Brennan terminal tissue injuries. Am J Hosp Palliat Care 2012;29(7):541–5.
9. Goode PS, Allman RM. The prevention and management of pressure ulcers
. Med Clin North Am 1989;73:1511–24.
10. La Puma J. The ethics of pressure ulcers
. Decubitus 1991;4(2):43–4.
11. Brown G. Long-term outcomes of full-thickness pressure ulcers
: healing and mortality. Ostomy Wound Manage 2003;49(10):42–50.
12. Witkowski JA, Parish LC. The decubitus ulcer: skin failure
and destructive behavior. Int J Dermatol 2000; 39(12):894–6.
13. Langemo DK, Black J; National Pressure Ulcer Advisory Panel. Pressure ulcers
in individuals receiving palliative care: a National Pressure Ulcer Advisory Panel white paper. Adv Skin Wound Care 2010;23(2):59–72.
14. Langemo DK, Brown G. Skin fails too: acute, chronic, and end stage skin failure
. Adv Skin Wound Care 2006;19(4):206–11.
15. Langemo D, Haesler E, Naylor W, Tippett A, Young T. Evidence-based guidelines for pressure ulcer management at the end of life. Int J Palliat Nurs 2015;21(5):225–32.
16. 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(11):514–24.
17. Levine JM. Skin failure
: an emerging concept. J Am Med Dir Assoc 2016;17(7):666–9.
18. Levine JM. Unavoidable pressure injuries
, terminal ulceration, and skin failure
: in search of a unifying classification system. Adv Skin Wound Care 2017;30(5):200–2.
19. Olshansky 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(4):150.
20. White-Chu EF, Langemo D. Skin failure
: identifying and managing an under recognized condition. Ann Long Term Care 2012;20(7):28–32.
21. Worley CA. Skin failure
: the permissible pressure ulcer? Dermatol Nurs 2007;19(4):384–5.
22. Alvarez O, 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. JWOCN 2016;43(5);455–63.
23. Black JM, Edsberg LE, Baharestani MM, et al. Pressure ulcers
: avoidable or unavoidable? Results of the National Pressure Ulcer Advisory Panel consensus conference. Ostomy Wound Manage 2011;57(2):24–37.
24. Edsberg LE, Langemo D, Baharestani MM, Posthauer ME, Goldberg M. Unavoidable pressure injury: state of the science and consensus outcomes. JWOCN 2014;41:313–34.
25. Wound, Ostomy and Continence Nurses Society. Position statement: avoidable versus unavoidable pressure ulcers
. JWOCN 2009;36(4):378–81.
26. Wound Ostomy and Continence Nurses Society. WOCN Society Position Paper: Avoidable Versus Unavoidable Pressure Ulcers
(Injuries). Mt Laurel, NJ: Wound Ostomy and Continence Nurses Society; 2017.
28. Bansal C, Scott R, Stewart D, Cockerell CJ. Decubitus ulcers: a review of the literature. Int J Dermatol 2005;44(10):805–10.
29. Pittman J, Beeson T, Terry C, et al. Unavoidable pressure ulcers
: development and testing of the Indiana University Health Pressure Ulcer Prevention Inventory. JWOCN 2016;43(1):32–8.
31. Edsberg LE, Langemo D, Baharestani MM, Posthauer ME, Goldberg M. Unavoidable pressure injury: state of the science and consensus outcomes. JWOCN 2014;41(4):313–34.
32. Levine JM, Humphrey S, Lebovits S, Fogel J. The unavoidable pressure ulcer: a retrospective case series. J Clin Outcomes Manage 2009;16(8):1–5.
33. McIntyre L, May R, Marks-Maran D. A strategy to reduce avoidable pressure ulcers
. Nurs Times 2012;108(29):14–7.
34. Peterson AM, Rogers B. Pressure ulcers
: is it a case of negligence? J Legal Nurs Consult 2012;23(1):32–4.
35. Woywodt A, Matteson E. Should eponyms be abandoned? Yes. BMJ 2007;335:424.
36. Whitworth JA. Should eponyms be abandoned? No. BMJ. 2007; 335:425.
37. Levine JM. Historical notes on pressure ulcers
: the decubitus ominosus of Jean-Martin Charcot. J Am Geriatr Soc 2005;53:1248–51.
38. Yastrub DJ. Pressure or pathology: distinguishing pressure ulcers
from the Kennedy terminal ulcer
. JWOCN 2010;37:249–50.
39. Miller MS. The death of the Kennedy terminal ulcer
. J Am Coll Clin Wound Spec 2017;8(1-3):44–6.
40. Schank JE. The Kennedy terminal ulcer
—alive and well. J Am Coll Clin Wound Spec 2016;8(1-3):54–5.
41. Carlsson ME, Gunningberg L. Predictors for development of pressure ulcer in end-of-life care: a national quality register study. J Palliat Med 2017;20(1):53–8.
42. Irwin RS, Rippe MJ. Irwin and Rippe’s Intensive Care Medicine. 5th ed. Philadelphia, PA: Lippincott Williams & Wilkins; 2003.
44. Fredriksson T, Pettersson U. Severe psoriasis—oral therapy with a new retinoid. Dermatologica 1978;157:238–44.
45. Severity scoring of atopic dermatitis: the SCORAD index. Consensus report of the European Task Force on Atopic Dermatitis. Dermatology 1993;186(1):23–31.
46. Cohen-Mansfield J, Cohen R, Skornick-Bouchbinder M, et al. What is the end of life period? Trajectories and characterization based on primary caregiver reports. J Gerontol Med Sci 2018;73(5):695–701.
48. Levine JM, Zulkowski KM. Secondary analysis of OIG pressure ulcer data, including incidence, avoidability, and level of harm. Adv Skin Wound Care 2015;28(9):420–8.
acute skin failure; avoidable pressure injuries; chronic skin failure; end-stage skin failure; Kennedy terminal ulcer; KTU; pressure injuries; pressure ulcers; SCALE; Skin Changes At Life’s End; skin failure; TB-TTI; terminal ulcers; Trombley-Brennan terminal tissue injury; unavoidable pressure injuries
Supplemental Digital Content
Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.