Redefining Slough: A New Classification System to Improve Wound Bed Assessment and Management

In the United States, wound management is conservatively estimated to account for $28 billion in annual health care expenditure for the Medicare population.¹ Chronic wounds are complex areas of skin and subcutaneous tissue failure that arise from a variety of conditions. The surface of a chronic wound is a hostile environment where neutrophils—the friendly forces sent to clean up an injury and provide a functional surface repair—are constantly losing the fight to repetitive setbacks and unfriendly bacteria insistent on establishing undesirable communities. After neutrophils remove dead and devitalized tissue from acute wounds, redundant cells are removed by macrophages that carry out the normal cleanup process.^2,3 Macrophages in the wound bed release a number of growth factors that facilitate the rapid progression to granulation, the next stage of the normal healing process.⁴ The sustained presence of nonviable debris in the wound prolongs the inflammatory phase, and the continued presence of apoptotic neutrophils in the chronic wound results in the constant release of matrix metalloproteinases (MMPs) and inflammatory cytokines.⁵ Cellular debris observed on the wound bed surface often presents as a soft, mucinous or stringy material that is frequently colonized by multispecies bacterial biofilms and is referred to as “slough.”⁶

Common chronic wound types seen by the majority of health care professionals include diabetic, venous, arterial, and pressure ulcers. However, a more detailed list includes traumatic wounds, surgical dehiscence, failed flaps and grafts, burns, wounds caused by autoimmune disorders, and other atypical disruptions in skin function.⁷ The etiology of each wound should be identified to help guide treatment, because 2 wounds that look very similar may require quite different treatment. Chronicity, at least in diabetic foot ulcers, is established when the wound either fails to decrease in volume by 50% within 4 weeks or is not on track to close within 12 weeks.⁸ Other types of wounds have different timelines for measuring failure to heal, but all have in common the development of a wound bed composed of various percentages of nonviable tissue, healthy healing tissue, and bacterial biofilms. In a 2017 meta-analysis, Malone et al⁹ found the prevalence of biofilm in chronic skin wounds to be approximately 80%. The longer a wound remains open, the higher the risk of microbial attachment, proliferation, and the formation of a recalcitrant, virulent biofilm.

Nonviable tissue can be divided into 2 basic types: the dry, hard, leathery material called “eschar,” and the soft, yellowish material referred to as slough. Slough is a nonspecific term used to describe several different presentations of nonviable tissue within the wound bed, created by prolonged inflammation and repetitive injury.¹⁰ The definition of slough is very broad, and the appearance of slough on the wound bed is not always indicative of delayed healing; in fact, it can even mask the underlying etiology. At the 2018 Wild on Wounds 2018 National Wound Conference, held September 12 to 15, 2018, in Las Vegas, Nevada, the authors had asked the audience what term in wound care they felt was the least well defined, and the resounding favorite was slough. Various reasons were given, including the broad nature of slough itself, lack of a consistent definition, uncertainty as to the exact appearance of slough, and confusion with other nonviable tissues based on the level of hydration of the wound surface. If it is not black or red, it seems all else gets defined as slough and is treated mostly the same. This confusion has at times even led to debridement of recently applied cellular and acellular tissue-based products by untrained clinicians; these products often appear as a thin slough-like layer on the wound surface (Figure 1).

The Merriam-Webster Dictionary defines slough as “a place of deep mud or mire, a swamp or slew; an inlet or a backwater; a creek in a marsh or tide flat; a state of moral degradation or spiritual dejection.”¹¹ In the wound setting, a state of tissue degradation and dejection is a fairly accurate description of the chronic wound bed. For the authors’ purposes, herein they define slough as a well-hydrated, yellow-to-white material; loosely to firmly attached to the various tissues in the wound bed; made up of accumulated leukocytes, macrophages, fibroblasts, fibrin, angiogenic ingrowth, and apoptotic cells; infiltrated by biofilms of varying thickness and complexity; and perpetuated by the continual accumulation of tissue-destructive enzymes.

The interface between slough and granulation is best referred to as a zone of conflict, where the products of tissue construction and destruction accumulate in increasing and decreasing numbers, depending on the degree to which treatments facilitate or fail to aid in healing. Failure to address the high levels of nonviable cellular debris present in the chronic wound encourages the accumulation of slough, the development of a bacterial bioburden, and the potential for wound chronicity. Removing nonviable tissue and accumulated biofilm is the initial step in wound bed preparation.¹² Delay in the removal of nonviable material slows wound healing, and frequent debridements using a variety of means are required to maintain a healthy wound bed.¹³ The question usually is, “What tissue needs to be removed, and by what method?” In discussing debridement methods, the debridement terminology controversy of conservative sharp debridement vs surgical/excisional debridement at bedside or clinic vs selective debridement arises. The purpose of this paper is to define the nature of the material known as slough and review some of the treatment methods used to address it. The choice of debridement is the purview of the attending wound care professional and may include each of the aforementioned types. Suggestions as to the method of debridement made later in this article are not meant to limit the practitioner but to act as a guide for possible choices.  

To instruct students at the authors’ institution, Temple University School of Podiatric Medicine, Philadelphia, and to bring some clarity to communication between clinicians, the authors developed a slough classification system. Until more specific, cost-effective methods of tissue cellular typing become readily available, clinical visual and tactile observation of color, texture, handling characteristics, and odor are the best assessment tools. Complicating the decision regarding tissue type is the ever-changing wound landscape during its progression through the various stages of the healing process. Eschar initially firmly attached loosens at the margins, and the bed begins to drain. The then open wound becomes colonized, softens, and morphs at some point into a sloughy material that gives way to granulation tissue in a “2 steps forward, 1 step back” progression to closure.¹⁴ Failure to make an accurate diagnosis and manage underlying systemic and local causes is a major factor in the global cost associated with treating chronic wounds.¹⁵ Accurately assessing and classifying the various types of slough on a wound aids the clinician in choosing the correct therapy to facilitate rapid wound closure. Because of its anatomic origin, slough arising from necrotic tissue tends to be firmly attached, whereas slough produced by the inflammatory process is more loosely attached; however, both types of slough delay wound healing. Owing to the differences in appearance, composition, and formation of slough, the authors propose 4 subtypes of slough—necroslough, leukoslough, fibroslough, and bioslough—to ensure accurate assessment and guide clinicians in choosing the appropriate treatment. Each slough type has its own set of defining characteristics that help to determine the recommended treatment.

Necroslough is the most difficult of the 4 slough types to identify and requires a more detailed discussion than the other types. Eschar is previously viable tissue that has become separated from its blood supply and has essentially mummified, rendering it hard, dry, discolored, and firmly attached. The vascular injury is usually caused by pressure in anatomic areas that are poorly perfused, thin, and situated over bony prominences. This patch of necrotic tissue is densely opaque (black or brown) and hides an unknown depth of tissue damage. It may be relatively superficial or deep to the underlying bone, which is a very short distance in areas where the bone is close to the surface. The body’s response to the presence of eschar is to wall it off, revascularize tissues at its base, and slowly release it from its margins by a process of granulation, marginal epiboly, and reepithelialization. Treatment for these areas is to remove all causes of pressure, keep the area dry, and allow the process to slowly proceed to completion. Occasionally, the amount of underlying necrotic material triggers the production of an inflammatory exudate that initiates a liquefaction process. This attracts numerous neutrophils and macrophages, which subsequently produce metalloproteinases that loosen the base and margins of the patch and soften the eschar. Once deeper tissues are open to the surface of the skin, invading bacteria rapidly colonize the space and begin to form local biofilms that invite the growth of anaerobic bacteria. Usually, when the eschar begins to drain significantly, sharp surgical removal of all or part of the tissue is performed, leaving behind a layer of residual necrotic tissue that is managed using autolytic dressings or the addition of an enzymatic debriding agent. This transitional material historically referred to as eschar is the slough type the authors classify as necroslough. Other forms of necroslough can be produced by burns, infection, dressing compression, or other trauma. The resulting tough, fibrinous material has the same characteristics as those produced by the devolving eschar and must be treated in a similar manner. Sharp debridement, augmented by the addition of autolytic or enzymatic debridement, is required; often, this is performed in stages to avoid causing trauma to surrounding tissues and to allow preservation of delicate areas of new granulation. Even the best surgical (macro) debridement often leaves behind residual areas of necroslough that will require autolytic (micro) debridement using saline or gauze moistened with hypochlorous acid, surfactants, hydrogels or enzymatic agents (collagenase), and dressings that maintain a moist wound environment to loosen the remaining nonviable tissues from advancing viable wound bed cells. Surrounding muscle, fascial tissues, exposed tendon, and adipose tissue, for example, may have been affected by the initial injury and will slowly break down as the cells die. This is the most difficult slough tissue type to identify, because it lies on a continuum from eschar (surface) and necrosis (deep) to liquefaction necrosis, to necroslough (Figure 2).

Initiation of an inflammatory response in a chronic wound results in infiltration of the wound bed by white blood cells, which leads to the formation of a soft, yellowish to white layer they termed leukoslough, which is often worsened by vasculitis and colonization of the wound surface. The hallmark of leukoslough is local inflammation and a loosely attached, easily removed, soft, yellow to white gelatinous material. Treatment consists of frequent gentle selective surgical or mechanical debridement to remove accumulated inflammatory cells, cleansing with antiseptic solutions, and the use of antiseptic gels to prevent the formation of biofilms. When vasculitis is present, the inflammatory stimulus to the wound bed can be managed using short-term oral or topical steroids (Figure 3). Enzymatic agents can be used to help decrease the accumulation of leukoslough from one clinical visit to the next and aid in the healing process.

When wound chronicity has led to the repetition of inflammation and fibroblastic collagen deposition over an extended time period, the wound bed has much the same appearance as that of leukoslough; however, at this point mechanical debridement is inadequate and selective surgical debridement must be used. The authors call this type of slough fibroslough, and a more extensive macrodebridement using sharp curettage, hydrosurgical planing, or ultrasonic curettage of the material is required. Surgical macrodebridement is rarely complete unless a true excision is performed, and microdebridement using applications of enzymatic or surfactant debriding agents, or dressings that enhance the autolytic process, may be required. This type slough is not the remnants of anatomically identifiable necrotic tissue; rather, it is a newly formed, tough, firmly attached fibrous material that interferes with progression of the wound to granulation. Treatment consists of selective surgical removal of excess fibrous tissue, but not a whole-scale excision of the layer, because removing too much may remove valuable scaffolding material necessary for the newly forming granulation tissue. Regular “deep” debridement, commonly performed by many clinicians on a weekly basis, is in fact counterintuitive to the healing process. Selective removal of nonviable slough helps prevent reversion of an acute healing surface to one dominated by chronicity. Dressings for fibroslough are much the same as those used for leukoslough, preserving moist healing and preventing the establishment of bacterial colonization that can proceed to biofilms (Figure 4). 

When colonization proceeds to local infection, the wound bed develops a thick, accumulating biomass of multispecies bacteria that form biofilms over the wound surface. These areas are dark maroon, brown, or even greenish black in color, have a strong odor, and have a friable, undermining wound bed with invaginations and involutions. Biofilms encourage the development of an inflammatory state, which enhances the production of a protein-rich exudate that nourishes the biofilm and encourages the formation of a leukocyte-rich slough.¹⁶ Percival and Suleman¹⁴ suggest that slough has many of the same properties as biofilm. The entire wound, or sections of the wound, may be covered with the biofilm; the authors refer to this as bioslough. This slough is harder to remove than leukoslough because what had previously been healthy wound bed is now producing areas of new necrotic tissue. A great deal of drainage occurs with these wounds, and daily or biweekly dressing changes may be required, even with multilayer compression, to get the bioload under control and establish a clean granular base. Treatment consists of surgical excision, select surgical or mechanical debridement, regular cleansing with appropriate antiseptics (hypochlorous acid or polyhexamethylene biguanide preparations), the use of topical antibiofilm agents (iodine preparations such as cadexomer iodine, or antibiofilm topicals), and antimicrobial dressings (iodine-releasing foams, pigment base antiseptics, and silver dressings) to help eliminate bacteria on the wound bed and prevent bacterial reformation on the wound. Antimicrobial dressings that maintain close contact with the wound bed are more effective at preventing biofilm accumulation than those that allow for fluid to accumulate between the dressing and the wound bed. In venous or vasculitic ulcers, it may be necessary to use topical anesthesia prior to debridement by light curettage and mechanical removal to mitigate pain. Systemic antibiotics are reserved for patients with signs of systemic infection and should not be used as part of the treatment described herein. This protocol is often referred to as “biofilm-based wound care,” or more recently, “wound hygiene,” and has been proposed by a number of researchers and prominent clinicians (Figure 5).¹⁶

No one timeline exists against which to measure failure to heal across all chronic wounds, but all such wounds have in common the development of a wound bed composed of various percentages of nonviable tissue, healthy healing tissue, and bacterial biofilms. Failure to address the high levels of nonviable cellular debris present in the chronic wound encourages the increased accumulation of slough. The initial step in managing a wound with a high percentage of slough is to identify the origin and type or types of slough present. All slough types require debridement, but the manner in which the wound is debrided is dependent on the slough to be treated, which makes prompt and accurate categorization particularly important. Appropriate management of each type of slough will maximize preservation of viable tissue, minimize the amount of remaining devitalized tissue, and prepare the wound bed to heal in the most effective manner possible. Complex wounds have multiple tissue types within the same wound bed. Likewise, multiple types of slough may present within a single wound bed, thereby complicating treatment. Understanding the dominant slough type in a given wound allows for correct decisions regarding debridement and dressing applications (Figure 6). 

The classification system presented herein was created to help wound care clinicians better describe what they are observing within the wound bed (identification), to provide a terminology for transmitting those observations to other wound care clinicians (classification), and to aid clinicians in choosing optimal debridement and dressing choices (decision making). Reducing the chronicity of wounds results in improved patient outcomes, reduced health care costs, and ultimately, improved quality of life of affected patients. 

Authors: James McGuire, PT, DPM, LPed, FAPWHc¹; and Jacob Jamal Nasser, BS², DPM

Affiliations: ¹Department of Medicine, Temple University, Philadelphia, PA; ²Temple University School of Podiatric Medicine, Philadelphia, PA

Correspondence: James McGuire, Department of Medicine, Temple University School of Podiatric Medicine, 148 N. 8^th St. Philadelphia, PA 19107; jimnanmcguire@gmail.com 

Disclosure: The authors disclose no financial or other conflicts of interest.