In an observational, retrospective, correlational study, Farid et al19 used the forensic concept that dead tissue loses heat when compared to normal tissue that can maintain its heat.20 The authors examined patients in an acute care facility who had reddened areas that had been examined using skin temperatures of PRIDAS and temperatures of normal, surrounding skin within 2 cm of the PRIDAS. The temperature of tissues yields clues to the tissue underlying the PRIDAS regarding viability (warmer than surrounding skin) or nonviability (cooler than surrounding skin).21 A highly accurate infrared digital camera was used to measure the temperatures and clearly identify PRIDAS in surrounding skin that appeared normal to the naked eye. The study also recorded blanching versus nonblanching, as well as the number of PRIDAS that became necrotic (ie, a purple DTI) and the number of days from the day the PRIDAS was originally assessed. Per protocol, only 1 PRIDAS per patient was entered into the study and a total of 85 patients/PRIDAS were examined and followed. The resulting analysis combined “warm” PRIDAS with blanchable and nonblanchable, and “cool” PRIDAS with blanchable and nonblanchable. None (0%) of the warm/blanchable PRIDAS progressed to necrosis, as opposed to 65.38% of cool/nonblanchable PRIDAS that did progress to necrosis (P <.001) — DTIs that appeared on day 6 or 7. Combined cool and blanchable PRIDAS resulted in additional 21.8% necrosis, signifying the blanching of the cool PRIDAS most likely occurred because of lividity in the localized dead tissues, not from an intact vasculature. Temperature assessment can reflect the condition only of the tissues immediately underneath the skin and not down to the bone level unless the skin is right over the bone.
Ultrasound (US). An animal study by Moghimi et al22 employed high-frequency US (20 MHz) to assess full-thickness, experimentally created DTI on the hip bones of guinea pigs and tissue decomposition from the level of the bone as it tracked to the skin. Digital photographs also were taken of the superficial skin changes on the same days as the US images (days 3, 7, 14, and 21). An interesting finding that parallels the timing of the findings in the skin temperature study by Farid et al19 on humans was the appearance of the purple skin changes on the seventh day after the initial injury. Moghimi et al21 also documented and correlated the skin color change with the penetration of the tissue decomposition through the fascia underlying the subcutaneous layer seen on US on the seventh day.
In a prospective, observational study, Aoi et al23 used US to scan DTI on the skin surface and reported predictable underlying changes in the deep and subcutaneous tissues in humans during the process of decomposition of those tissues as they converted to unstageable PUs. DTIs on 12 participants were studied using serial US from the initial appearance of the purple ulcer to necrotic draining lesions. The patterns associated with DTI necrosis of the soft tissue consistently observed by the investigators on US were discontinuous fascia (interruptions in the normally smooth lines of the fascia) and heterogeneous hypoechoic areas (mixed translucent and dense), also characteristic of an underlying Stage 4 ulcer. This study was important because it confirmed the US changes seen in the underlying tissues were not changes by progression (changes caused by repeated trauma — ie, pressure/shearing) but by the process of decomposition of tissues already dead.
Andersen and Karlsmark24 studied 15 PUs and classified characteristics of the injuries according to shades of red to measure color, skin temperatures, and skin elasticity (ie, retraction time) versus using US scanning for predicting PI severity. Each method was compared to an adjacent area of unaffected skin 5 cm from the test area. The authors found US was the most valuable tool for measuring the amount of pressure the skin was subjected to as opposed to the actual prediction of the eventual PU severity. Although the type and sensitivity of the US technology used were not discussed in the publication, the investigators measured the amount of edema in the dermal layers seen on US as their criteria for calculating the amount of pressure.
An observational, prospective study conducted by Quintavalle et al25 compared high-resolution US images obtained from 119 long-term-care facility residents with Braden Scale scores of 18 or less with images obtained from 15 healthy volunteers. Common PU sites scanned included the heels, sacrum, and ischial tuberosity. The US device used was portable; the images did not penetrate deeper than the dermal layers of the skin and the device was sensitive enough only to characterize edema in the epidermal, dermal, and subdermal layers (edema in the latter 2 layers occurred simultaneously wherever it occurred). Documentation of the clinical assessment finding for erythema was reviewed, recorded, and compared with the high-resolution US finding for each specific site. Of the 630 US images obtained, 55.3% revealed abnormal edema in the layers when compared to US images of the same locations taken on the normal, healthy volunteers. No accompanying documentation of redness or other visible abnormalities of the skin was noted for 79.7% of the abnormal US scans. The study did not extend to follow-up outcomes regarding the appearance of PUs that correlated with the abnormal US scans.
The clinical examination conducted in a case study published by Steeds26 of a comatose 20-year-old heroin addict revealed a warm swelling on the patient’s right, lower extremity calf muscle. Urine and blood studies were consistent with a rhabdomyolysis. Steeds used hospital-grade US technology (transducers that generate a transmission frequency range of 2.5 – 12 mHz, which produces clearer images at deeper tissue penetrations) upon admission to the emergency department (ED) to examine the affected calf. The scanning revealed multiple hyperechoic foci (dense white areas on US) consistent with early rhabdomyolysis related either to diabetic muscle infarction or compression (pressure, compartment syndrome). The significance of the case study is that US can detect soft tissue changes and damage within 24 hours; the changes appear as hyperechoic (white dense areas capturing the intense muscle contraction [rigor mortis] that occurs within a few hours of the muscle dying) as opposed to the hypoechoic (translucent dark areas) changes seen later after the tissues decompose and liquify (myoglobinuria [tea-colored urine] occurs within 6 hours of muscle death, signifying the breakdown/liquification of decomposing muscle).27,28 The hypoechoic decomposition can be seen on hospital-grade US images starting at the level of the bone8 where the surrounding core temperatures of the viable tissues are warmer and advance more slowly as the surrounding viable tissue becomes cooler toward the coolest area (ie, the surface of the dead skin exposed to cool ambient temperatures).15,16,19,27
Nam et al29 utilized both US and a technique described as photoacoustic imaging (a noninvasive, painless procedure) to assess the effectiveness of an engineered tissue graft on burn wounds. These techniques facilitated quantification of the amount of granulation tissue and allowed measurement of the progress and speed of healing as compared to burns with autografts or without any graft.
Hamaluik et al30 demonstrated how the stiffness of the dying muscle resulting from DTI can provide early information on deep tissue damage using numerical characterization of quasistatic US elastography. When using elastography, US technology can detect the change in muscle tissue elasticity that occurs as the scanner is moved from normal tissue to dead or damaged tissue. This information, added to the changes seen on the scan, enables the radiologist to identify the nature of the changes noted on the scan. The importance of this mathematical calculation and finite-element model of sonographic B-mode imaging and tissue deformation is the expectation that injured tissue can be identified much earlier (before the tissue dies) in hopes of providing intervention preventing irreversible damage. This ability underscores US as an ideal technology to utilize in the search for soft tissue infarcts, injuries such as DTIs, and other shearing injuries seen in sports and vehicle accidents and muscle-wasting diseases.
Rhabdomyolysis. Animal studies by Linder-Ganz and Gefen31 using magnetic resonancy imaging (MRI) to assess experimental pressure and shear effects on the hind limb muscles in rats revealed muscle tissue is extremely sensitive to pressure, ischemia, and deformation (lateral elongation of the muscle fibers caused by shear), similar to the forces that cause DTI resulting in PUs. When a significant amount of muscle dies (rhabdomyolysis) anywhere in the body, an initial, slow release of muscle protein (myoglobins) into the surrounding intact vasculature occurs, causing the first systemic effect (ie, dark myglobinuria) within 6 hours after muscle death and then a concomitant rise in the serum creatinine phosphokinase (CK) starting within the first 12 hours. The levels then peak in the next 12 hours to 3 days, slowly returning to normal over the next few days after muscle death.32-34 The large myoglobin molecules in the urine can cause damage to the kidney tubules unless detected (a combination of a rise in blood urea nitrogen and creatinine and noted dark urine and/or urine myoglobin assays) and treated, usually with increased intravenous fluids to flush the myoglobins through the tubules into the urine. Depending on the levels of CK early in the process, the patient also may be placed on continuous renal replacement therapy or dialysis.35 For reasons not clearly understood, several clinical observations32-34 report a drop in the serum calcium (Ca++) levels frequently accompanies elevated CK levels in cases of rhabdomyolysis.
Rhabdomyolysis also can occur in pressure-related DTI. A case study by Levine36 describes a young man who lay unconscious on the floor for several hours; severe pressure muscle necrosis resulted from his wallet in his back pocket. When he reached the ED, myoglobinuria and elevated CK were noted.
The primary purpose of this study was to determine whether US performed in the ED can detect pressure-related deep tissue necrosis in subcutaneous (SC) connective tissue and in muscle overlying the bone as an early predictor of subsequent visible signs of full-thickness pressure ulceration of the skin (specifically, purple DTI) within 2 to 7 days of US detection. If this was the case, it was anticipated the radiologist could determine whether lesions were present on admission and thus not facility-acquired, should they later appear as necrotic DTIs on the skin. The study also was conducted to determine whether incidental findings of other soft tissue abnormalities that may or may not be implicated in the patients’ overall symptomology and complaints could be visualized and reported to help generate early diagnosis of serious conditions. Lastly, the study was performed to evaluate if US examination of the soft tissues on the sacral/buttock areas of the body on these patients would rule out PUs in cases of skin conditions that mimic facility-acquired PUs.