Outcomes Research—Incidence and Clinical Symptoms of Hourglass and Sandwich-shaped Tissue Necrosis in Stage IV Pressure Ulcers

Deep tissue injuries (DTI) in pressure ulcers have recently drawn much attention.^1–6 Experiments exploring how shear force and pressure over a bony prominence cause DTI in pressure ulcers⁷ have shown that pressure ulcer necrosis resulting from DTI appears commonly as a column with a rectangular-shaped cross section. DTI necrosis may also be shaped like an hourglass (hourglass-shaped necrosis). Necrosis of either shape may be either continuous or have a layer of relatively healthy tissue sandwiched between a superficial and deep layers of necrotic tissue (sandwich-shaped necrosis).

In order to understand this progression, definitions and mechanisms of occurrence of hourglass-shaped necrosis and sandwich-shaped necrosis are presented below. The progressive development for each is illustrated in Figure 1 and Figure 2. Hourglass-shaped necrosis is caused when pressure and shear force applied to the body surface causes damage to the soft tissue (Figure 1). These types of mechanical stress tend to be stronger with areas of bony prominence and thus produce more severe and wider damage to tissue nearest the bony prominence. On the other hand, while the skin surface has direct contact with pressure/shear force a shallow ulcer and sometimes a deep ulcer will develop in the upper layer of the tissue. Consequently, the total damage to the soft tissue is shown as two layers of necrosis, which are connected with a narrow area of necrosis in a cross section because such damage is less in the middle layer, which is influenced by the effects of strain rather than direct stress.
The defining conditions of hourglass necrosis are application of external forces (pressure/ shear force) that are applied to the body. The skin surface receives mild to moderate damage, but the soft tissue in the deep layer around a bony prominence is extensively and severely damaged. However, the soft tissue in the middle layer is not greatly affected. Consequently, the distribution of necrosis shows an hourglass shape in the soft tissue. Hourglass-shaped necrosis progresses from initial undermining of the pressure ulcer after the discharge of liquefied necrosis, defined as the initial or discharge phase of undermining.⁷

Sandwich-shaped necrosis occurs when initial damage to tissue in the middle layer between bone and skin in hourglass-shaped necrosis is small or negligible; the tissue remains healthy (Figures 2 and 3). Thereafter, the necrotic area in both the upper layer and deep layer are completely separated by an intermediate layer of nearly intact tissue, appearing as sandwiched or sandwich shaped. Damaged shallow ulcer necrotic tissue in the upper layer is liquefied and discharged early, while the necrosis in the deep layer remains as either slough necrosis or pus. The middle layer of relatively healthy tissue may temporarily hide this DTI.
The blood circulation through the necrotic deep tissue loses integrity and ischemia occurs in the middle layer of tissue during the healing process and then necrosis develops, which eventually leads to a perforation and connects the upper and lower necrotic areas that appeared previously as intact tissue. In other words, a shallow pressure ulcer in the upper layer separates from apparently healthy intermediate tissue, which then perforates, thus connecting to an originally present deep necrotic area, to ultimately become a DTI. Clinically this process appears initially as new necrosis in the central part of the wound surface. It then grows relatively slowly with a clear circumscribed border, developing and expanding in depth and area without additional pressure and shear forces around the wound.
Those changes of necrosis start from the central portion and then extend to the periphery. Namely, the central part of necrosis changes to a black or dark brown color and thicker necrosis then progressively extends to deeper more peripheral regions of tissue. Subsequently, the shallow wounds or areas of necrosis in the upper layer become diachronically connected with the deep necrotic area, which was continually present in the soft tissue near the bone. This is a new area of necrosis in the middle layer that is influenced by the insufficient blood circulation within the deep tissue necrosis (below the middle layer) during the healing process. The following points demonstrate that this is not caused by a repetition of external pressure:

• This type of necrosis develops at the central part of wound.
• There are no findings of inflammation, ischemia, and necrosis on/in the skin (necrosis would indicate increased compression and resultant congestion).
• This type of necrosis at the center of the wound does not develop rapidly. It gradually thickens—similar to the progression of ischemia to necrosis.
• When this region makes contact with necrosis in the deep layer, such tissue is already completely liquefied and discharged as pus that was liquefied at the same time as the necrosis in the upper layer.
It is important to be aware of sandwich-shaped necrosis, because of the following clinical problems that can occur later:
• Estimation of the presence of deep layer necrosis at the early stage is difficult, therefore making explanation of the unusual prognosis to patients and family members complex.
• Patients and family members often complain that pressure ulcers worsen and deepen due to inadequate nursing care or improper treatment( s). In extreme cases such individuals may even file a lawsuit as a result of perceived poor clinical treatment and nursing care.
An area of sandwich-shaped necrosis may occur in either hourglass-shaped necrosis or more typical column-shaped DTI. Sandwich-shaped necrosis is defined as a necrotic area present in two separate layers, namely an upper layer and a deep layer, which are separated with nearly intact tissue. The deep layer necrosis near the bony prominence is affected more extensively and intensively than those of the upper layer. The surrounding necrotic tissue affects the middle layer, but initially it does not seem to be damaged. Examples of sandwich- shaped necrosis are shown in Figures 4 and 5.
Clinically, specific changes begin on the surface of an ulcer in the upper layer. These changes are revealed after the discharge of the liquefied necrosis. A new area of necrosis later appears in the central part of ulcer surface which gradually grows thicker and wider from the central area to the periphery. Finally, the ulcer progression eventually leads to the same process of hourglass-shaped necrosis.
The present study will define and clarify progressions of hourglass and sandwich patterns of necrotic tissue in Stage IV pressure ulcers, and report their incidence in a Japanese tertiary care hospital (long-term care hospital).

Case Reports
Subjects. The cases were chosen from among patients treated between June 2002 and June 2006 in a tertiary care hospital setting in Japan to satisfy the following conditions. Patients at the initial phase of onset of a pressure ulcer wound with either thick necrosis or black and dark brown colored necrosis on the skin surface, patients with histories of unconsciousness with shock or immobility for a few hours in patients who have suffered a fall.

Procedure. On patient enrollment, more than 50 qualifying pressure ulcers in the initial phase of the study were diagnosed using CT scan or ultrasonography, and standardized clinical symptom assessments.The CT scan or ultrasonography was not always taken because a definite diagnosis of hourglass-shaped/sandwich-shaped necrosis was made retrospectively in the later phase of the study. The standardized assessment included ulcer symptoms such as shallow ulcers, DTI, and undermining, clinical surface symptoms such as color/thickness of necrosis, inflammation, indurations, and personal history regarding such factors as consciousness, shock, and thetime and place of the patient’s fall.
Case 1. A 57-year-old woman presented with a more shallow pressure ulcer than the anticipated state, and peritonitis without shock (Figure 6). Initial examination revealed a dark red and purple colored, relatively thick area of necrosis on the wound surface with erythema around the wound. Seven days later, a shallow ulcer appeared, and by day 21, the wound had almost completely healed.
Case 2. A 76-year-old man presented with cerebral infarction with shock (Figure 7). At the first examination, a light black-colored thin layer of necrosis was observed on the lateral sacral bone with a wide area of erythema surrounding the area of necrosis. After 7 days the color of the necrotic tissue changed into a dark brown color with a thicker area necrosis. It could not be estimated whether or not it would develop DTI. At day 14, the thick necrotic tissue was debrided. At day 21, the presence of DTI was observed.

Case 3. A 76- year-old woman presented with cerebral infarction with shock, and had been unconscious for 4 hours (Figures 8 and 9). Two weeks after pressure ulcer onset, a dark, thick, dry, brown/black colored area of necrosis was seen on the wound. A CT-scan revealed abnormalities in the soft tissue around the bony prominence, suggesting the presence of necrotic tissue. At 3 weeks after onset, the necrotic tissue started to liquefy and discharge incompletely leaving an initial type of undermining. At 4 weeks after onset, the liquefied necrosis in the deep layer had been completely discharged. A change in the process of the hourglass-shaped necrosis was recognized based on the conventional wound healing progression and symptoms, namely, it was not specific progression.

Case 4. A 73-year-old man presented with cerebral hemorrhage with shock and had been unconscious for 48 hours (Figures 10 and 11).Two weeks after pressure ulcer onset, a thick, dry, black-brown colored area of necrosis was observed. A CT-scan showed unusual areas of necrotic tissue around a bony prominence. Three weeks later, the necrosis became liquefied, and the liquefied necrosis was discharged from the deep layer, leaving a space underneath the skin. This is the initial type of undermining and confirmed the presence of hourglass- shaped necrosis.
Incidence study. The incidence of necrotic tissue patterns in Stage IV pressure ulcers was based on NPUAP classification (Figure 12).
Three hundred twenty-six cases from the same study population as those described in the Case Reports with Stage IV pressure ulcers that were treated and cared for by the hospital’s interdisciplinary wound care team from study enrollment to pressure ulcer onset were reported. A retrospective assessment of each injury was made to categorize them as either hourglass or sandwich-shaped necrosis, or DTI (Figure 12). A patient, through the course of diagnosis and treatment who developed the initial type of the undermining (discharge of necrosis type) was categorized as having hourglass-shaped necrosis. Patients who did not develop undermining were categorized as having a DTI. Together with the help of CT scan or ultrasonography and conventional diagnosing procedures, hourglass-shaped necrosis was identified as necrosis near the bones connected to the surface necrosis. Conversely, sandwich-shaped necrosis did not have any such connection to bone.

A CT scan or an ultrasonography can indicate unusual shadows, but it is difficult to make a decision based solely on these findings. A wound may develop an hourglass shaped shaped area of necrosis depending on how wide or how deep the wound becomes, altering what is seen on a CT scan or ultrasonography.
When diagnosing hourglass-shaped necrosis and sandwich-shaped necrosis, one should consider the CT scan or ultrasonography findings and the clinical procedures of wound healing, such as superficial necrosis that becomes thicker, wider, perforates deeper, produces discharge, and any resultant undermining.

Hourglass-shaped Necrosis: Clinical Symptoms
An hourglass-shaped necrosis is caused by a combination of shear force,pressure,and a bony prominence. This combination of mechanical stress will generate a large amount of compression on/in the deep tissue near the bony prominence. As a result, the damage to that area becomes more extensive and severe than that in the middle or upper layer.
If this narrow area of the tissue between the upper and the lower layer is not affected by mechanical stresses, the remaining intact tissue and both necrotic layers will separate.
Sandwich-shaped necrosis begins as a shallow ulcer in the upper layer, which seems to heal immediately; however, it thereafter changes to a deeper ulcer due to the upper layer ulcer perforating into the deep layers. A CT scan and ultrasonography cannot make a distinct diagnosis of sandwich-shaped necrosis, but can suggest it as a possibility so that the comprehensive consideration of clinical state and procedure of wound healing over time can later confirm the diagnosis.
Procedure of wound healing will only be able to make it clear what an hourglass-shaped necrosis was existed, thereafter this type of necrosis would produce the initial type (discharged type) of the undermining in pressure ulcers after the discharge of liquefied necrosis.

Results
One hundred thirty-two cases (40%) showed hourglass- shaped necrosis, 26 of which were cases of sandwich-shaped necrosis. The remaining 194 cases (60%) showed conventional column-shaped DTI, 7 of which were cases of sandwich-shaped necrosis.The total number of sandwich-shaped necrosis cases was 33 cases or 10% of all stage IV cases, with a somewhat higher incidence of sandwiched layers of necrosis above and below mid-level healthy tissue (26/132 or 20%) among patients with hourglass-shaped DTI than column-shaped DTI (7/194 or 4%).
Lesions, which seemed to worsen over time, tended to show the same process as that observed in conventional wound healing. If affected by repeated external force, then a different systems and process occurred which demonstrated the typical symptoms of pressure ulcers.
It is not clear at this time what kind of history or color change contributes to the initial phase associated with both a sandwich-like area of necrosis and DTI at the later phase. However, the following factors may be involved:
• DTI and hourglass-shaped necrosis often occur in patients with a blood pressure < 100 mmHg (eg, during shock), and also with extended periods of unconsciousness and immobility
• DTI and hourglass-shaped necrosis often occur when patients fall onto a hard bed or floor, and are immobile for more than 3 hours with a low blood pressure. However, there is no obvious association with body type/shape presently.

Discussion
When pressure and shear force are applied to the body, the compression stress generates and enhances the compression to the soft tissue, and the effect is particularly remarkable in the tissue near a bony prominence.^8,9 The results of Ohura et al^10,11 verified these effects. Under experimental conditions, a dynamic pressure was generated demonstrating 1.3–2.4 times that of static pressure. Bennett et al¹² reported that blood flow was affected by the increasing shear force added to pressure. The findings of the present study were consistent with those of a previous study.¹¹ Furthermore, Lee et al¹³ reported that high pressure was generated around the deep soft tissue near the bone by sequentially applying pressure to the soft tissue. Gefen¹⁴ reported that a muscle around a bone tended to become stiff early in a finite element analysis with rats. Linder-Ganz et al¹⁵ demonstrated that pressure damaged deep tissue around a bone by using open MRI and finite element approach. These clinical studies demonstrate that external force promotes a simple, cylindrical, deep ulcer with hourglass-shaped necrosis and sandwich-shaped necrosis that was verified by CT scan and ultrasonography.
Many studies regarding the shearing effect have elucidated some effects of mechanical stress; however, the relationship between the degree of bony prominence, the speed of the shear force, and the weight and deterioration of a pressure ulcer have yet to be elucidated. As a result, further investigation of these phenomena is needed.

Conclusion
One hundred thirty-two of 326 cases (40%) with Stage IV pressure ulcers had hourglass-shaped necrosis. The total number of sandwich-shaped necrosis was 33 cases, thus accounting for 10% of the stage IV cases.The progression of hourglass-shaped and sandwich-shaped necrosis occurs as for wound healing in other ulcers (ie, stasis, ischemia, necrosis, liquefaction, discharge), finally leading to DTI and undermining after the discharge of the liquefied necrosis.
It is important to be aware of possible hourglass- or sandwich-shaped necrosis development during the progression of healing in pressure ulcers. The ulcers appear to gradually worsen and deepen despite application of rigorous best practices in pressure ulcer management. Families often blame the nursing staff for this worsening in condition, and in some cases, may even file a lawsuit due to perceived inadequate clinical treatment. Identifying patients who are at risk for these types of deep tissue injury, and alerting all members of the interdisciplinary wound care team to their potential for progression, may be an important aspect of proper pressure ulcer management.