Hospital-acquired pressure injuries (HAPIs) are a dangerous and costly patient safety concern affecting more than 2.5 million patients annually in acute care settings in the United States.1 In addition to the physical, psychological, and financial impact on a patient's quality of life, the care related to HAPIs presents a major economic burden on the healthcare system.2,3 In the United States, the estimated cost of treating pressure injuries (PIs) ranges from $9.1 billion to $11.6 billion.1 A 2007 ruling by the Centers for Medicare & Medicaid Services (CMS) classified stage 3 and stage 4 HAPIs as “never events” and in 2008, stopped reimbursing hospitals for the costs related to their care.4 Per the CMS, a single stage 3 or stage 4 HAPI, as a secondary diagnosis, adds $43,180 to each hospital stay.5 Thus, early detection and prevention of PIs is critical for improving patient outcomes and reducing the economic burden on patients and the healthcare system.6
The current National Pressure Ulcer Advisory Panel (NPUAP) staging system is widely adopted internationally and classifies PIs based on anatomical features and the extent of existing tissue loss.7 Pressure injuries are staged from 1 to 4 with the additional categories of unstageable, deep tissue pressure injury (DTPI), and medical device-related PI.8 The NPUAP defines a stage 1 PI as intact skin with a localized area of nonblanchable erythema.8 Pressure-related blanchable erythema (PrBE) or alterations in sensation, temperature, or firmness often precede stage 1 pressure-related nonblanchable erythema (PrNBE).8 Because melanin is not blanchable, distinguishing PrBE from a stage 1 PI is problematic on individuals with dark skin.
A DTPI is defined as intact or nonintact skin with localized area of persistent nonblanchable deep red, maroon, purple discoloration, or epidermal separation revealing a dark wound bed or blood-filled blister.8 The injury is often preceded by a change in temperature or the presence of pain. The discoloration with stage 1 PI and DTPI may appear differently on darkly pigmented skin. Injury to deep tissue may occur despite overlying intact skin. Black and colleagues9 noted necrosis under intact skin may take 48 hours from time of injury until it can be visually detected. Additionally, 7 to 10 days may be required for a DTPI to deteriorate into a full-thickness stage 3 or stage 4 PI.9
There is increasing evidence in the literature supporting the idea that PIs are the result of DTPI, progressing outward until the damage can be seen visually.10–12 Traditionally, visual skin assessment has been the standard used by researchers and clinicians for identifying early signs of skin damage.10,13 However, visual skin inspection is difficult and unreliable, predisposing individuals, especially those with darker skin tones, to advanced skin damage before it is recognized.10,13 Thus, the ability to have a nonvisual assessment tool to identify DTPI at the time of hospital admission would have an important impact on quality of patient care.
The purpose of this systematic review was to determine whether sufficient research evidence exists to support the use of bedside technologies for early detection of PIs, which is inclusive of pressure-related erythema (PrE) and DTPI. Our review sought to answer the question: What available bedside technologies are effective for enhancing the early detection of PIs? Because blanching cannot be reliably assessed on individuals with dark skin, we included both PrBE and PrNBE in this review.
The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) protocol was used to guide our systematic review process.14 We derived our Population-Intervention-Comparison-Outcome (PICO) elements directly from the search question, and these elements served as the basis for our inclusion and exclusion criteria. Inclusion criteria were peer-reviewed, English-language publications or conference proceedings. Eligible studies also included primary quantitative studies, systematic reviews, meta-analyses, which used technologies to identify tissue injury—PrBE, PrNBE (stage 1), or DTPIs, which had not yet progressed to epidermal separation or blistering—as an outcome measure. Technologies had to be bedside accessible (ie, ultrasound, thermography, subepidermal moisture (SEM) measurement, alternative light sources, spectrophotometry, laser Doppler, etc). Exclusion criteria eliminated dissertations, case studies/series (eg, sample size < 5), qualitative studies, and studies using animal models, computer simulation, and/or healthy volunteers. We also excluded studies that used remote technologies such as telemedicine, focused on stage 2, 3 or 4 PIs, and did not differentiate between stage 1 or DTPIs. However, studies that failed to differentiate PrBE and PrNBE were not excluded, as both conditions are indicators of early PI damage.
Four databases were searched including Medline, Cumulative Index to Nursing and Allied Health Literature (CINAHL), Web of Science, and Cochrane with the assistance of a health sciences research librarian. We selected search terms, subject headings, and MeSH terms based on our PICO criteria (see Supplemental Digital Content 1, available at: http://links.lww.com/JWOCN/A53, for specific search language/strategy). Studies were abstracted from the earliest year available for each database through March 1, 2018. Using Zotero15 reference management software, the lead author (K.N.S.) imported all publications and removed duplicates (Figure). To decrease the risk of selection bias, 2 researchers (K.N.S. and M.C.N.) then each independently screened the titles and abstracts for eligibility. Full-text versions of the remaining publications were retrieved. Screening results were compared and discrepancies discussed until agreement was reached. A similar process was used to perform full-text reviews of the surviving studies, while enlisting the assistance of a third researcher, a certified Wound Ostomy Continence Nurse (L.A.), to clarify terminology and patient-related issues. An ancestry search of the bibliographies of eligible publications was conducted by K.N.S. and subjected to a similar review process. Data were extracted from each of the eligible studies and organized into Tables 1 to 4 that show abbreviated versions of the data collected. Again, to reduce risk of selection bias, we used a triple independent data extraction process with all 3 researchers (K.N.S., M.C.N., and L.A.) independently collecting the data from each of the eligible studies. Data were then compared and combined for synthesis.
During the data collection process, we each independently analyzed the quality of the eligible studies using the Johns Hopkins Nursing Evidence-Based Practice (JHNEBP) Rating Scale.20 This grading scale assesses the strength and quality of research studies. The strength of a study is based on the study's design: experimental studies are graded as I, quasi-experimental studies are graded as II, and nonexperimental studies and qualitative studies are graded as III. Quality is measured against indicators of the rigor of the study methodology, such as sampling design, sample size, instrument reliability/validity, data collection plan, analysis of the findings, and other strengths and limitations of the studies. After assessing the study against the criteria, a letter grade is assigned: A for high quality, B for good quality, and C for low quality or major flaws. The researchers discussed the grades they assigned to each of the studies until consensus was reached.
Of the 1050 articles identified across the database and ancestry searches, 850 were screened by title and abstract resulting in 128 full-text articles retrieved for review. Ultimately, 18 studies met eligibility for inclusion in our final synthesis (Figure). These studies examined technologies that were accessible for the bedside use; the most common were ultrasound (n = 5, Table 1), thermography (n = 7, Table 2), and SEM measurement (n = 5, Table 3). In addition, 1 study each examined the effectiveness of spectroscopy, laser Doppler, and spectrophotometry on early detection of PrBE, PrNBE, and DTPI (Table 4). Two of the studies used more than 1 technology.16,23 Nearly half of the studies examined the effectiveness of the technology specifically in the assessment of stage 1 PIs.12,16,18,19,27,29–31 Another 8 studies did not distinguish between PrBE and PrNBE.13,17,22–27 Deep tissue pressure injury was directly assessed in only 4 studies,5,12,19,25 while several others attempted to predict deterioration of PrE as a possible indicator of suspected underlying DTPI.16,21,24,26
The methodological rigor of the included studies varied greatly based on how they addressed our specific search question. The following JHNEBP grades were assessed: 3 As,24,26,29 11 Bs,5,13,16,17,22,23,25,27,28,30,31 and 4 Cs.12,18,19,21 All of the studies were observational in design (level 3), 14 were prospective/longitudinal, and 4 were cross-sectional. With a few exceptions, earlier research (prior to 2007) tended to be more descriptive and exploratory in nature. Seven studies had small samples sizes (n < 50) of PIs 5,12,16,19,21,30,31 of which 4 had 11 or fewer PIs.12,19,21,30 Only 4 studies conducted a power analysis as a basis for sample size determination.24,25,30,31 Sample ethnic diversity ranged from 3% to 35% African Americans or persons with dark skin across 9 studies, although half of the studies did not report those participant characteristics.5,16–19,21,24,30,31
All but 4 studies16,19,21,23 provided sufficient detail on the theoretical basis and execution of each of the technologies studied. The reliability of instruments' application and associated measurements were formally evaluated in all SEM studies13,26,28–30 but only in 1 thermography study,25 1 ultrasound study,17 and 1 spectrophotometry study.31 The selection of control or comparison skin sites also varied across thermography and SEM studies. Only 3 studies reported blinding the clinician who performed the visual assessment from the results of the technology application.12,18,21 Finally, environmental factors associated with temperature such as exposure to ambient temperature and moisture including incontinence were controlled in 8 of the 12 studies.
Study results pertaining to the systematic review question were generally clear with relevant findings presented for individual studies (Tables 1–4). However, the number of PIs or number of PIs identified using the technologies was not completely transparent in 3 studies,5,16,18 requiring access to supplemental material for one of them.12 Finally, due in large part to small sample sizes, 4 studies performed only descriptive analyses, preventing inference to a broader population.12,13,17,18
Technology for Early Detection
A description of the technology and synthesis of data for the 4 technologies used for early detection of PI identified through our systematic review include ultrasound, thermography, SEM, and light.
Since its development in the 1970s, healthcare providers have used ultrasound as a diagnostic tool for a variety of conditions.32 The technology relies on pulsed sound waves emitted from a probe to penetrate the skin's surface and determine its underlying structure based on the echo received from reflected waves. The speed by which the reflected sound returns determines the underlying structure distance and density from the probe.32,33 Using mathematical formulas, a computer converts the waves to a cross-sectional image, also known as a B-mode scan.32 In the ultrasound images, structures with a greater density appear bright indicating higher echogenicity (hyperechoic). By comparison, areas of fluid or macroscopic edema appear dark (hypoechoic). More recently, the development of high-frequency ultrasound (>10 MHz) has improved image resolution but at the expense of penetration depth, making it ideal for the evaluation of more superficial dermal structures.33 Such devices have become more portable to allow for bedside use.
Of the 5 studies identified in our review that examined the effectiveness of ultrasound for PI detection (Table 1), all reported a hypoechoic area was observed in most images taken of PrBE and PrNBE.12,16–19 Additional image findings included unclear structural layers19 and evidence of inflammation and dermal damage.18 The hypoechoic region was more frequently described as superficial in the presence of erythema.16,17 Quintavalle and colleagues17 noted detection of deep hypoechoic regions with no associated erythema, suggesting evidence of early DTPI. Sato and colleagues16 also noted similar findings among stage 1 injuries that deteriorated. Ultrasounds were performed by nurses in 3 of the 5 studies.12,16,17 Only 2 studies performed interrater analysis of the image interpretation with good results (see Table 1).17,18 None of the studies reported findings based on participant race/skin tone, with the only study by Helvig and Nichols12 providing overall sample characteristics.
Perfusion of the skin is reflected in its surface temperature. Increased perfusion from injury or inflammation from reperfusion (hyperemic response) may be associated with a localized increase in skin temperature.24,34 Alternatively, nonviable tissue associated with DTPI would lack sufficient perfusion, resulting in cooler overlying skin.25 Such differences in skin temperature can be detected through conduction by liquid crystal contact monitors placed on the skin's surface or, more commonly today, with infrared, noncontact imaging devices that capture thermal radiation.34,35 Selecting an unaffected adjacent skin site for comparison and controlling for ambient temperature acclimation are both important strategies to ensure accurate thermography results.24,25,35
Five of the 7 studies that evaluated thermography noted a difference in temperature as an indicator of PI (Table 2).16,21,22,24,25 Three of the studies noted that areas of PrE were more often warmer than adjacent skin.21,22,25 Pressure injuries that ultimately deteriorated were significantly more likely to be cooler than the surrounding skin, suggesting the possibility of underlying DTPI.16,24,25 But when assessing actual suspected DTPI, no significant difference in temperature was found in 2 studies.5,23 Sprigle and colleagues23 were unable to distinguish PrBE from PrNBE based on temperature difference. None of the studies reported interrater analysis of the technologies' application. One study examined the relationship between erythema and underlying skin tone, noting no significant association.23
Subepidermal Moisture Measurement
Inflammatory processes resulting from pressure injury-associated cell death contribute to an increase in local microvascular fluid.36 The presence of this extracellular edema within the epidermal and dermal layers can be detected through changes in the skin's SEM.29,36 In brief, SEM measurement technology captures the skin's capacitance (ability to hold an electrical charge) by determining its relative dielectric constant (eg, electrical field resistance).36 The greater the water content in the tissue, the higher the dielectric constant; actual reported SEM values are equipment dependent. Changes in SEM are determined based on delta values calculated from several measurement points taken on the skin.37
All 5 studies that examined SEM measurement as an indicator of PI noted significantly higher moisture readings for PrE compared to normal skin (Table 3). Bates-Jensen and colleagues27 found SEM measurement predicted 99% of concurrent PrE. When comparing PrBE to PrNBE, 2 studies found significantly higher SEM associated with PrNBE (stage 1).28,29 In 2 studies, measurement thresholds relative to 2 different SEM devices significantly predicted concurrent PrE or stage 1 PIs (see Table 3 for specific equipment).28,29 The study by Bates-Jensen and colleagues29 was the only one to report sensitivity (37.4%) and specificity (77.7%). The SEM measurement technology also demonstrated good interrater reliability (r = 0.63-0.92) in 4 studies.13,26,27,29 Finally, 4 of the 5 studies examined whether current SEM values could predict the future development of PIs; the measurements predicted the development of between 15% and 88% of PrE and/or stage 1 PI identified on repeated assessment conducted at least 1 week later, with darker skin tone favoring a greater likelihood of detection.26–29
Light Technology (Spectroscopy and Laser Doppler)
Hemoglobin is 1 of 2 major chromophores contributing to skin color, the other being melanin.38 The concentration of hemoglobin is associated with the skin's perfusion, which is greatly affected by the extent and degree of ischemia. Temporary occlusion of microvasculature can result in reactive hyperemia, or a temporary increase in blood flow, which is typically assessed by pressure applied to the skin to produce blanching.23,39 However, blanching is often difficult to observe, especially in individuals with darker skin tones. Blood flow or flux can be evaluated using laser Doppler, which captures the reflected light from both moving red blood cells and surrounding tissue and converts the information into an electrical signal.40 The resulting images can then be analyzed for perfusion based on intensity. Alternatively, reflectance spectrometry (spectral measurements of light reflected off matter) can provide a proximity measure of perfusion by measuring the degree of erythema, which is highly correlated with the concentration of hemoglobin.38 Using a spectrophotometer, white light is applied to the skin's surface. The reflectance of certain spectral bandwidths is measured and, using an algorithm, converted to an erythema index.
In 3 studies, researchers attempted to distinguish PrBE from PrNBE (stage 1) based on indicators of perfusion using the technologies described earlier (Table 4).23,30,31 Findings from these studies demonstrated PrNBE had significantly greater perfusion than PrBE as observed by laser Doppler30 and through higher erythema index values.23,31 Studies examining reflectance spectrometry23,31 reported good interrater and intrarater reliability along with sensitivity and specificity for the erythema algorithms used (see Table 4). Nixon and colleagues30 did not report any such analyses for their use of laser Doppler. The erythema index used in the Sprigle and colleagues23 study was able to compensate for melanin concentration, allowing it to be applied to different skin tones.
Pressure injuries remain physical, psychological, and financial burdens on patients and an economic drain on the healthcare system. Visual skin assessment is unreliable, especially in individuals with darker skin tones. Our systematic review identified 5 technologies that have been studied for their potential to provide early detection of PIs. These technologies included ultrasound, thermography, SEM measurement, reflectance spectrometry, and laser Doppler flowmetry.
Evidence from our review supports the use of SEM measurement as a potential tool for the early identification of PI, specifically blanchable erythema and nonblanchable erythema, with ultrasound and alternate light devices warranting further research. Based on our assessment using the JHNEBP Rating Scale,20 the methodological rigor was consistently higher across the SEM measurement studies compared to the other technology identified in the review. A body of research regarding SEM measures, which includes multiple, high-quality studies, increases the reliability of findings identified in our review. As such, these devices may help identify early pressure-related skin damage before clinical manifestations, potentially decreasing healthcare costs and benefitting patients of all skin tones.
Studies using ultrasound to detect early PIs found meaningful and consistent results, but the quality of the research to date precludes us from recommending its use. More rigorous studies with larger sample sizes are needed before ultrasound can be recommended as an effective technology. Two additional considerations for ultrasound include it being limited to detecting macroscopic level tissue damage and its training requirements for image interpretation.36
Thermography was the most studied technology with 7 studies identified; however, findings were inconsistent. Furthermore, thermography requires positioning of the patient to allow the temperature of exposed skin sufficient time to stabilize prior to assessment. Such additional effort may cause nurses to be reluctant to use the technology in daily clinical practice. Measuring erythema using reflectance spectrometry was found to be effective at differentiating between PrBE and PrNBE (stage 1). However, only 2 studies supported this technology, and distinguishing between PrBE and PrNBE skin damage may be of limited clinical importance. The results of a single study investigating laser Doppler flowmetry were promising, but require further research.
The 1 technology consistently able to provide early detection of PIs, supported by 5 high-quality studies, is SEM measurement. The body of evidence supports the technology's use as an effective tool for detecting stage 1 or PrBE. Though literature suggests SEM measurements may also assist in the detection of deep tissue injury,41 currently sufficient evidence is not available to support this practice.
For SEM measurements to be clinically useful, the technology must be applied using a simple, noninvasive, durable, light-weight, and easily transportable instrument that requires only minimal training to operate. Nurses must find the tool quick to use and interpret at the bedside with good inter-rater reliability. Several SEM measurement devices are on the market that appear to meet these requirements, with one used in 2 studies recently approved by the Food and Drug Administration and available in the United States.37,41 The purchase prices of many reliable SEM measurement, thermography, spectrometry, and portable ultrasound devices can range between $2000 and $10,000. The initial investment of early detection technology must be weighed against the potential savings in preventive PI care.
According to a systematic review conducted by Gunowa and colleagues,42 patients with dark skin tones are at higher risk for developing severe PIs. Although reasons for this risk disparity have not been rigorously investigated, evidence suggests that current recommended visual and tactile skin assessment practices are inadequate to meet the needs of patients with darker skin tones. Evidence from our review suggests technologies used to perform SEM measurements and spectroscopy may improve the identification of PrE in this particular population.23,28 Nurses should include assessment techniques that allow equitable care and reduce outcome disparities in high-risk populations. Thus, recognizing and adopting technology that can detect early-stage skin injury in patients with dark skin is critical.
The current state of the science related to technologies that can identify early pressure-related skin damage has implications for clinical practice, education, and research. Larger scale studies are needed to evaluate the effectiveness and feasibility of these devices in the clinical setting to facilitate preventive interventions and decrease the incidence and prevalence of PIs. Additionally, more research is needed to understand how location of the PI on the body may affect the application and interpretation of the different technologies. For example, the impact of peripheral vascular disease and greater skin thickness on the heel may alter measurements of perfusion and ultrasound image interpretation, respectively.17 In the meantime, nurses in clinical practice settings and the nurse educators who train them need to recognize the shortcoming of visual and tactile assessments for identifying early skin injury, especially for patients with dark skin tones. Skin assessments should be performed carefully and with consultation from a certified wound nurse.
Several limitations to our systematic review should be noted. First, despite performing a comprehensive review of the literature, our efforts may have missed eligible studies. A systematic search of relevant journals may have provided additional publications. Second, we included both populations with PrBE and PrNBE in our eligibility criteria. Even though the NPUAP does not include a stage for PrBE, we felt its inclusion was necessary to address the important disparity in identifying stage 1 PIs on individuals with dark skin. Data provided in Tables 1 to 4 demonstrate that much of the available research on PI detection does not distinguish between these types of injuries. Finally, the JHNEBP Rating Scale is a widely used tool to assess the quality of evidence to support clinical decision-making.20 However, its application, as with any grading scale, is subjective. We attempted to overcome this challenge by utilizing 3 raters and focusing our assessment on only those elements relevant to the search question. We did not contact the authors of the included studies, which would have helped clarify challenges identified in some of the findings.
Currently, there is promising technology for the early detection of pressure-related injury of the skin. Evidence identified in our systematic review supports several options for further development or immediate practice implementation. The technology must be readily available and easily integrated into clinical practice by the bedside nurse. Skill training for the use of the technology should begin with the certified wound nurse who has the expertise in visual skin assessment and can then progress the technology to bedside nursing.
Visual skin inspection is not highly reliable in identifying pressure-related skin injuries, especially in individuals with darker skin tones. As we learn more about the pathology of PI development and causal factors, cost-effective assistive assessment technology may play an integral role in the timely detection of PI and early implementation of optimal PI prevention measures and treatments.
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